Advertisement

Helicobacter pylori and MALT Lymphoma

  • Pedro Farinha
    Affiliations
    Department of Pathology and Laboratory Medicine, British Columbia Cancer Agency and the University of British Columbia, Vancouver, British Columbia, Canada
    Search for articles by this author
  • Randy D. Gascoyne
    Correspondence
    Address requests for reprints to: Randy D. Gascoyne, MD, Department of Pathology, British Columbia Cancer Agency, 600 West 10th Avenue, Vancouver, British Columbia V5Z 4E6, Canada. fax: (604) 877-6178.
    Affiliations
    Department of Pathology and Laboratory Medicine, British Columbia Cancer Agency and the University of British Columbia, Vancouver, British Columbia, Canada
    Search for articles by this author
      Helicobacter pylori are gram-negative spiral microaerophilic organisms that belong to the Campylobacterales order, Helicobacteracea family. They are capable of colonizing the harsh environment of the human stomach. Over 50% of the world’s population carries this infection.
      • Parsonnet J.
      Helicobacter pylori the size of the problem.
      H pylori have colonized the human stomach since time immemorial.
      • Falush D.
      • Stephens M.
      • Pritchard J.K.
      Inference of population structure using multilocus genotype data linked loci and correlated allele frequencies.
      In virtually all infected individuals, H pylori causes inflammation in the form of chronic active gastritis, which progresses in 10%–20% of affected persons to peptic ulcer disease, gastric adenocarcinoma, and/or mucosa-associated lymphoid tissue (MALT) lymphoma. However, only a very small minority (1%–2%) of infected individuals will develop a malignant disease.
      • Suerbaum S.
      • Michetti P.
      Helicobacter pylori infection.
      One of the most distinctive features of H pylori is the genetic diversity it displays between clinical isolates.
      • Marshall D.G.
      • Coleman D.C.
      • Sullivan D.J.
      • Xia H.
      • O’Morain C.A.
      • Smyth C.J.
      Genomic DNA fingerprinting of clinical isolates of Helicobacter pylori using short oligonucleotide probes containing repetitive sequences.
      H pylori isolates are highly diverse, with evidence of a constantly changing genome, primarily caused by point mutations, substitutions, insertions, and/or deletions.
      • Tomb J.F.
      • White O.
      • Kerlavage A.R.
      • Clayton R.A.
      • Sutton G.G.
      • Fleischmann R.D.
      • Ketchum K.A.
      • Klenk H.P.
      • Gill S.
      • Dougherty B.A.
      • Nelson K.
      • Quackenbush J.
      • Zhou L.
      • Kirkness E.F.
      • Peterson S.
      • Loftus B.
      • Richardson D.
      • Dodson R.
      • Khalak H.G.
      • Glodek A.
      • McKenney K.
      • Fitzegerald L.M.
      • Lee N.
      • Adams M.D.
      • Venter J.C.
      • et al.
      The complete genome sequence of the gastric pathogen Helicobacter pylori.
      • Alm R.A.
      • Ling L.S.
      • Moir D.T.
      • King B.L.
      • Brown E.D.
      • Doig P.C.
      • Smith D.R.
      • Noonan B.
      • Guild B.C.
      • deJonge B.L.
      • Carmel G.
      • Tummino P.J.
      • Caruso A.
      • Uria-Nickelsen M.
      • Mills D.M.
      • Ives C.
      • Gibson R.
      • Merberg D.
      • Mills S.D.
      • Jiang Q.
      • Taylor D.E.
      • Vovis G.F.
      • Trust T.J.
      Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori.
      Moreover, mixed infections are frequent and may lead to exchange of DNA fragments between H pylori strains in a single host. This suggests co-evolution of H pylori with its human host and that disease may be caused both by strain-specific properties that increase virulence and by host susceptibility. Such strains possibly evolve through exercising significant flexibility in gene content and gene regulation. Among many of the host-pathogen interactions that potentially could occur, some could prove beneficial in which the co-evolved bacteria and the host reach an almost symbiotic relationship. H pylori may not be just a bad bug in all instances.

      Abbreviations used in this paper:

      CagA (cytotoxin-associated antigen A), CARD4 (caspase recruitment domain), CIMP (CpG island methylator phenotype), DC-SIGN (dendritic cell-specific intercellular adhesion molecule-3-grabbing nonintegrin), DLBCL (diffuse large B-cell lymphoma), DSB (double-strand DNA breaks), FOXP1 (Forkhead box protein P1), GST (glutathione S-transferase), IAP (inhibitors of apoptosis), IFN (interferon), IGH (immunoglobulin heavy chain), IL (interleukin), LEL (lymphoepithelial lesion), MALT (mucosa-associated lymphoid tissue), MHC (major histocompatability complex), NF-κB (nuclear factor κB), nTx (neonatal thymectomized), PAI (pathogenicity island), PCR (polymerase chain reaction), ROS (reactive oxygen species), SS (Sjögren’s syndrome), Th1 (helper1 T cells), Th2 (helper2 T cells), TRAF (tumor necrosis factor-associated factor), Treg (regulatory T cells), TNF-α (tumor necrosis factor-α)
      To read this article in full you will need to make a payment
      AGA Member Login
      Login with your AGA username and password.
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Parsonnet J.
        Helicobacter pylori.
        Gut. 1998; 43: S6-S9
        • Falush D.
        • Stephens M.
        • Pritchard J.K.
        Inference of population structure using multilocus genotype data.
        Genetics. 2003; 164: 1567-1587
        • Suerbaum S.
        • Michetti P.
        Helicobacter pylori infection.
        N Engl J Med. 2002; 347: 1175-1186
        • Marshall D.G.
        • Coleman D.C.
        • Sullivan D.J.
        • Xia H.
        • O’Morain C.A.
        • Smyth C.J.
        Genomic DNA fingerprinting of clinical isolates of Helicobacter pylori using short oligonucleotide probes containing repetitive sequences.
        J Appl Bacteriol. 1996; 81: 509-517
        • Tomb J.F.
        • White O.
        • Kerlavage A.R.
        • Clayton R.A.
        • Sutton G.G.
        • Fleischmann R.D.
        • Ketchum K.A.
        • Klenk H.P.
        • Gill S.
        • Dougherty B.A.
        • Nelson K.
        • Quackenbush J.
        • Zhou L.
        • Kirkness E.F.
        • Peterson S.
        • Loftus B.
        • Richardson D.
        • Dodson R.
        • Khalak H.G.
        • Glodek A.
        • McKenney K.
        • Fitzegerald L.M.
        • Lee N.
        • Adams M.D.
        • Venter J.C.
        • et al.
        The complete genome sequence of the gastric pathogen Helicobacter pylori.
        Nature. 1997; 388: 539-547
        • Alm R.A.
        • Ling L.S.
        • Moir D.T.
        • King B.L.
        • Brown E.D.
        • Doig P.C.
        • Smith D.R.
        • Noonan B.
        • Guild B.C.
        • deJonge B.L.
        • Carmel G.
        • Tummino P.J.
        • Caruso A.
        • Uria-Nickelsen M.
        • Mills D.M.
        • Ives C.
        • Gibson R.
        • Merberg D.
        • Mills S.D.
        • Jiang Q.
        • Taylor D.E.
        • Vovis G.F.
        • Trust T.J.
        Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori.
        Nature. 1999; 397: 176-180
        • Marshall B.J.
        • Warren J.R.
        Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration.
        Lancet. 1984; 1: 1311-1315
        • Isaacson P.
        • Wright D.H.
        Malignant lymphoma of mucosa-associated lymphoid tissue. A distinctive type of B-cell lymphoma.
        Cancer. 1983; 52: 1410-1416
        • Malaty H.M.
        • Graham D.Y.
        Importance of childhood socioeconomic status on the current prevalence of Helicobacter pylori infection.
        Gut. 1994; 35: 742-745
        • Parsonnet J.
        • Shmuely H.
        • Haggerty T.
        Fecal and oral shedding of Helicobacter pylori from healthy infected adults.
        JAMA. 1999; 282: 2240-2245
        • Rowland M.
        • Kumar D.
        • Daly L.
        • O’Connor P.
        • Vaughan D.
        • Drumm B.
        Low rates of Helicobacter pylori reinfection in children.
        Gastroenterology. 1999; 117: 336-341
        • Covacci A.
        • Telford J.L.
        • Del Giudice G.
        • Parsonnet J.
        • Rappuoli R.
        Helicobacter pylori virulence and genetic geography.
        Science. 1999; 284: 1328-1333
        • Tindberg Y.
        • Blennow M.
        • Granstrom M.
        Clinical symptoms and social factors in a cohort of children spontaneously clearing Helicobacter pylori infection.
        Acta Paediatr. 1999; 88: 631-635
        • Dore M.P.
        • Sepulveda A.R.
        • El-Zimaity H.
        • Yamaoka Y.
        • Osato M.S.
        • Mototsugu K.
        • Nieddu A.M.
        • Realdi G.
        • Graham D.Y.
        Isolation of Helicobacter pylori from sheep-implications for transmission to humans.
        Am J Gastroenterol. 2001; 96: 1396-1401
        • Ullrich A.
        • Fischbach W.
        • Blettner M.
        Incidence of gastric B-cell lymphomas.
        Ann Oncol. 2002; 13: 1120-1127
        • Doglioni C.
        • Wotherspoon A.C.
        • Moschini A.
        • de Boni M.
        • Isaacson P.G.
        High incidence of primary gastric lymphoma in northeastern Italy.
        Lancet. 1992; 339: 834-835
        • Ben-Khelifa H.
        Gastric lymphoma.
        Gastrointest Endosc. 2002; 56: 955
        • Morgner A.
        • Lehn N.
        • Andersen L.P.
        • Thiede C.
        • Bennedsen M.
        • Trebesius K.
        • Neubauer B.
        • Neubauer A.
        • Stolte M.
        • Bayerdorffer E.
        Helicobacter heilmannii-associated primary gastric low-grade MALT lymphoma.
        Gastroenterology. 2000; 118: 821-828
        • Wotherspoon A.C.
        • Ortiz-Hidalgo C.
        • Falzon M.R.
        • Isaacson P.G.
        Helicobacter pylori-associated gastritis and primary B-cell gastric lymphoma.
        Lancet. 1991; 338: 1175-1176
        • Parsonnet J.
        • Hansen S.
        • Rodriguez L.
        • Gelb A.B.
        • Warnke R.A.
        • Jellum E.
        • Orentreich N.
        • Vogelman J.H.
        • Friedman G.D.
        Helicobacter pylori infection and gastric lymphoma.
        N Engl J Med. 1994; 330: 1267-1271
        • Hussell T.
        • Isaacson P.G.
        • Crabtree J.E.
        • Spencer J.
        The response of cells from low-grade B-cell gastric lymphomas of mucosa-associated lymphoid tissue to Helicobacter pylori.
        Lancet. 1993; 342: 571-574
        • Wotherspoon A.C.
        • Doglioni C.
        • Diss T.C.
        • Pan L.
        • Moschini A.
        • de Boni M.
        • Isaacson P.G.
        Regression of primary low-grade B-cell gastric lymphoma of mucosa-associated lymphoid tissue type after eradication of Helicobacter pylori.
        Lancet. 1993; 342: 575-577
        • Isaacson P.G.
        • Diss T.C.
        • Wotherspoon A.C.
        • Barbazza R.
        • De Boni M.
        • Doglioni C.
        Long-term follow-up of gastric MALT lymphoma treated by eradication of H. pylori with antibodies.
        Gastroenterology. 1999; 117: 750-751
        • Ferea T.L.
        • Brown P.O.
        Observing the living genome.
        Curr Opin Genet Dev. 1999; 9: 715-722
        • Janssen P.J.
        • Audit B.
        • Ouzounis C.A.
        Strain-specific genes of Helicobacter pylori.
        Nucleic Acids Res. 2001; 29: 4395-4404
        • Bjorkholm B.
        • Sjolund M.
        • Falk P.G.
        • Berg O.G.
        • Engstrand L.
        • Andersson D.I.
        Mutation frequency and biological cost of antibiotic resistance in Helicobacter pylori.
        Proc Natl Acad Sci U S A. 2001; 98: 14607-14612
        • Israel D.A.
        • Salama N.
        • Krishna U.
        • Rieger U.M.
        • Atherton J.C.
        • Falkow S.
        • Peek Jr, R.M.
        Helicobacter pylori genetic diversity within the gastric niche of a single human host.
        Proc Natl Acad Sci U S A. 2001; 98: 14625-14630
        • Falush D.
        • Kraft C.
        • Taylor N.S.
        • Correa P.
        • Fox J.G.
        • Achtman M.
        • Suerbaum S.
        Recombination and mutation during long-term gastric colonization by Helicobacter pylori: estimates of clock rates, recombination size, and minimal age.
        Proc Natl Acad Sci U S A. 2001; 98: 15056-15061
        • Blaser M.J.
        Helicobacters are indigenous to the human stomach.
        Gut. 1998; 43: 721-727
        • Linden S.
        • Nordman H.
        • Hedenbro J.
        • Hurtig M.
        • Boren T.
        • Carlstedt I.
        Strain- and blood group-dependent binding of Helicobacter pylori to human gastric MUC5AC glycoforms.
        Gastroenterology. 2002; 123: 1923-1930
        • Covacci A.
        • Censini S.
        • Bugnoli M.
        • Petracca R.
        • Burroni D.
        • Macchia G.
        • Massone A.
        • Papini E.
        • Xiang Z.
        • Figura N.
        • et al.
        Molecular characterization of the 128-kDa immunodominant antigen of Helicobacter pylori associated with cytotoxicity and duodenal ulcer.
        Proc Natl Acad Sci U S A. 1993; 90: 5791-5795
        • Odenbreit S.
        • Puls J.
        • Sedlmaier B.
        • Gerland E.
        • Fischer W.
        • Haas R.
        Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion.
        Science. 2000; 287: 1497-1500
        • Hatakeyama M.
        Oncogenic mechanisms of the Helicobacter pylori CagA protein.
        Nat Rev Cancer. 2004; 4: 688-694
        • Umehara S.
        • Higashi H.
        • Ohnishi N.
        • Asaka M.
        • Hatakeyama M.
        Effects of Helicobacter pylori CagA protein on the growth and survival of B lymphocytes, the origin of MALT lymphoma.
        Oncogene. 2003; 22: 8337-8342
        • Blaser M.J.
        • Berg D.E.
        Helicobacter pylori genetic diversity and risk of human disease.
        J Clin Invest. 2001; 107: 767-773
        • Hofreuter D.
        • Odenbreit S.
        • Henke G.
        • Haas R.
        Natural competence for DNA transformation in Helicobacter pylori: identification and genetic characterization of the comB locus.
        Mol Microbiol. 1998; 28: 1027-1038
        • Hofreuter D.
        • Karnholz A.
        • Haas R.
        Topology and membrane interaction of Helicobacter pylori ComB proteins involved in natural transformation competence.
        Int J Med Microbiol. 2003; 293: 153-165
        • Kersulyte D.
        • Velapatino B.
        • Mukhopadhyay A.K.
        • Cahuayme L.
        • Bussalleu A.
        • Combe J.
        • Gilman R.H.
        • Berg D.E.
        Cluster of type IV secretion genes in Helicobacter pylori’s plasticity zone.
        J Bacteriol. 2003; 185: 3764-3772
        • Szabo I.
        • Brutsche S.
        • Tombola F.
        • Moschioni M.
        • Satin B.
        • Telford J.L.
        • Rappuoli R.
        • Montecucco C.
        • Papini E.
        • Zoratti M.
        Formation of anion-selective channels in the cell plasma membrane by the toxin VacA of Helicobacter pylori is required for its biological activity.
        EMBO J. 1999; 18: 5517-5527
        • Galmiche A.
        • Rassow J.
        • Doye A.
        • Cagnol S.
        • Chambard J.C.
        • Contamin S.
        • de Thillot V.
        • Just I.
        • Ricci V.
        • Solcia E.
        • Van Obberghen E.
        • Boquet P.
        The N-terminal 34 kDa fragment of Helicobacter pylori vacuolating cytotoxin targets mitochondria and induces cytochrome c release.
        EMBO J. 2000; 19: 6361-6370
        • Peek Jr, R.M.
        • Blaser M.J.
        Helicobacter pylori and gastrointestinal tract adenocarcinomas.
        Nat Rev Cancer. 2002; 2: 28-37
        • Guruge J.L.
        • Falk P.G.
        • Lorenz R.G.
        • Dans M.
        • Wirth H.P.
        • Blaser M.J.
        • Berg D.E.
        • Gordon J.I.
        Epithelial attachment alters the outcome of Helicobacter pylori infection.
        Proc Natl Acad Sci U S A. 1998; 95: 3925-3930
        • Israel D.A.
        • Peek R.M.
        pathogenesis of Helicobacter pylori-induced gastric inflammation.
        Aliment Pharmacol Ther. 2001; 15: 1271-1290
        • Zambon C.F.
        • Navaglia F.
        • Basso D.
        • Rugge M.
        • Plebani M.
        Helicobacter pylori babA2, cagA, and s1 vacA genes work synergistically in causing intestinal metaplasia.
        J Clin Pathol. 2003; 56: 287-291
        • Mizushima T.
        • Sugiyama T.
        • Komatsu Y.
        • Ishizuka J.
        • Kato M.
        • Asaka M.
        Clinical relevance of the babA2 genotype of Helicobacter pylori in Japanese clinical isolates.
        J Clin Microbiol. 2001; 39: 2463-2465
        • Eck M.
        • Schmausser B.
        • Haas R.
        • Greiner A.
        • Czub S.
        • Muller-Hermelink H.K.
        MALT-type lymphoma of the stomach is associated with Helicobacter pylori strains expressing the CagA protein.
        Gastroenterology. 1997; 112: 1482-1486
        • Crabtree J.E.
        • Spencer J.
        Immunologic aspects of Helicobacter pylori infection and malignant transformation of B cells.
        Semin Gastrointest Dis. 1996; 7: 30-40
        • de Jong D.
        • van der Hulst R.W.
        • Pals G.
        • van Dijk W.C.
        • van der Ende A.
        • Tytgat G.N.
        • Taal B.G.
        • Boot H.
        Gastric non-Hodgkin lymphomas of mucosa-associated lymphoid tissue are not associated with more aggressive Helicobacter pylori strains as identified by CagA.
        Am J Clin Pathol. 1996; 106: 670-675
        • Peng H.
        • Ranaldi R.
        • Diss T.C.
        • Isaacson P.G.
        • Bearzi I.
        • Pan L.
        High frequency of CagA+ Helicobacter pylori infection in high-grade gastric MALT B-cell lymphomas.
        J Pathol. 1998; 185: 409-412
        • Delchier J.C.
        • Lamarque D.
        • Levy M.
        • Tkoub E.M.
        • Copie-Bergman C.
        • Deforges L.
        • Chaumette M.T.
        • Haioun C.
        Helicobacter pylori and gastric lymphoma.
        Am J Gastroenterol. 2001; 96: 2324-2328
        • Ye H.
        • Liu H.
        • Attygalle A.
        • Wotherspoon A.C.
        • Nicholson A.G.
        • Charlotte F.
        • Leblond V.
        • Speight P.
        • Goodlad J.
        • Lavergne-Slove A.
        • Martin-Subero J.I.
        • Siebert R.
        • Dogan A.
        • Isaacson P.G.
        • Du M.-Q.
        Variable frequencies of t(11;18)(q21;q21) in MALT lymphomas of different sites.
        Blood. 2003; 102: 1012-1018
        • Lehours P.
        • Menard A.
        • Dupouy S.
        • Bergey B.
        • Richy F.
        • Zerbib F.
        • Ruskone-Fourmestraux A.
        • Delchier J.C.
        • Megraud F.
        Evaluation of the association of nine Helicobacter pylori virulence factors with strains involved in low-grade gastric mucosa-associated lymphoid tissue lymphoma.
        Infect Immun. 2004; 72: 880-888
        • Occhialini A.
        • Marais A.
        • Urdaci M.
        • Sierra R.
        • Munoz N.
        • Covacci A.
        • Megraud F.
        Composition and gene expression of the cag pathogenicity island in Helicobacter pylori strains isolated from gastric carcinoma and gastritis patients in Costa Rica.
        Infect Immun. 2001; 69: 1902-1908
        • Lehours P.
        • Dupouy S.
        • Bergey B.
        • Ruskone-Foumestraux A.
        • Delchier J.C.
        • Rad R.
        • Richy F.
        • Tankovic J.
        • Zerbib F.
        • Megraud F.
        • Menard A.
        Identification of a genetic marker of Helicobacter pylori strains involved in gastric extranodal marginal zone B cell lymphoma of the MALT-type.
        Gut. 2004; 53: 931-937
        • Chang C.S.
        • Chen L.T.
        • Yang J.C.
        • Lin J.T.
        • Chang K.C.
        • Wang J.T.
        Isolation of a Helicobacter pylori protein, FldA, associated with mucosa-associated lymphoid tissue lymphoma of the stomach.
        Gastroenterology. 1999; 117: 82-88
        • Ishii E.
        • Yokota K.
        • Sugiyama T.
        • Fujinaga Y.
        • Ayada K.
        • Hokari I.
        • Hayashi S.
        • Hirai Y.
        • Asaka M.
        • Oguma K.
        Immunoglobulin G1 antibody response to Helicobacter pylori heat shock protein 60 is closely associated with low-grade gastric mucosa-associated lymphoid tissue lymphoma.
        Clin Diagn Lab Immunol. 2001; 8: 1056-1059
        • Yang H.B.
        • Sheu B.S.
        • Wang J.T.
        • Lin S.T.
        • Wu J.J.
        Serological responses of FldA and small-molecular-weight proteins of Helicobacter pylori: correlation with the presence of the gastric MALT tissue.
        Helicobacter. 2004; 9: 81-86
        • Putsep K.
        • Branden C.I.
        • Boman H.G.
        • Normark S.
        Antibacterial peptide from H. pylori.
        Nature. 1999; 398: 671-672
        • Rothenbacher D.
        • Blaser M.J.
        • Bode G.
        • Brenner H.
        Inverse relationship between gastric colonization of Helicobacter pylori and diarrheal illnesses in children.
        J Infect Dis. 2000; 182: 1446-1449
        • Dooley C.P.
        • Cohen H.
        • Fitzgibbons P.L.
        • Bauer M.
        • Appleman M.D.
        • Perez-Perez G.I.
        • Blaser M.J.
        Prevalence of Helicobacter pylori infection and histologic gastritis in asymptomatic persons.
        N Engl J Med. 1989; 321: 1562-1566
        • Goodwin C.S.
        • Armstrong J.A.
        • Marshall B.J.
        Campylobacter pyloridis, gastritis, and peptic ulceration.
        J Clin Pathol. 1986; 39: 353-365
        • Covacci A.
        • Rappuoli R.
        Helicobacter pylori: molecular evolution of a bacterial quasi-species.
        Curr Opin Microbiol. 1998; 1: 96-102
        • Fischer W.
        • Puls J.
        • Buhrdorf R.
        • Gebert B.
        • Odenbreit S.
        • Haas R.
        Systematic mutagenesis of the Helicobacter pylori cag pathogenicity island.
        Mol Microbiol. 2001; 42: 1337-1348
        • Viala J.
        • Chaput C.
        • Boneca I.G.
        • Cardona A.
        • Girardin S.E.
        • Moran A.P.
        • Athman R.
        • Memet S.
        • Huerre M.R.
        • Coyle A.J.
        • DiStefano P.S.
        • Sansonetti P.J.
        • Labigne A.
        • Bertin J.
        • Philpott D.J.
        • Ferrero R.L.
        Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island.
        Nat Immunol. 2004; 5: 1166-1174
        • Gobert A.P.
        • Bambou J.C.
        • Werts C.
        • Balloy V.
        • Chignard M.
        • Moran A.P.
        • Ferrero R.L.
        Helicobacter pylori heat shock protein 60 mediates interleukin-6 production by macrophages via a toll-like receptor (TLR)-2-, TLR-4-, and myeloid differentiation factor 88-independent mechanism.
        J Biol Chem. 2004; 279: 245-250
        • Chamaillard M.
        • Hashimoto M.
        • Horie Y.
        • Masumoto J.
        • Qiu S.
        • Saab L.
        • Ogura Y.
        • Kawasaki A.
        • Fukase K.
        • Kusumoto S.
        • Valvano M.A.
        • Foster S.J.
        • Mak T.W.
        • Nunez G.
        • Inohara N.
        An essential role for NOD1 in host recognition of bacterial peptidoglycan containing diaminopimelic acid.
        Nat Immunol. 2003; 4: 702-707
        • Fan X.
        • Gunasena H.
        • Cheng Z.
        • Espejo R.
        • Crowe S.E.
        • Ernst P.B.
        • Reyes V.E.
        Helicobacter pylori urease binds to class II MHC on gastric epithelial cells and induces their apoptosis.
        J Immunol. 2000; 165: 1918-1924
        • Bergman M.P.
        • Engering A.
        • Smits H.H.
        • van Vliet S.J.
        • van Bodegraven A.A.
        • Wirth H.P.
        • Kapsenberg M.L.
        • Vandenbroucke-Grauls C.M.
        • van Kooyk Y.
        • Appelmelk B.J.
        Helicobacter pylori modulates the T helper cell 1/T helper cell 2 balance through phase-variable interaction between lipopolysaccharide and DC-SIGN.
        J Exp Med. 2004; 200: 979-990
        • Engering A.
        • Geijtenbeek T.B.
        • van Vliet S.J.
        • Wijers M.
        • van Liempt E.
        • Demaurex N.
        • Lanzavecchia A.
        • Fransen J.
        • Figdor C.G.
        • Piguet V.
        • van Kooyk Y.
        The dendritic cell-specific adhesion receptor DC-SIGN internalizes antigen for presentation to T cells.
        J Immunol. 2002; 168: 2118-2126
        • D’Elios M.M.
        • Amedei A.
        • Del Prete G.
        Helicobacter pylori antigen-specific T-cell responses at gastric level in chronic gastritis, peptic ulcer, gastric cancer and low-grade mucosa-associated lymphoid tissue (MALT) lymphoma.
        Microbes Infect. 2003; 5: 723-730
        • Innocenti M.
        • Thoreson A.C.
        • Ferrero R.L.
        • Stromberg E.
        • Bolin I.
        • Eriksson L.
        • Svennerholm A.M.
        • Quiding-Jarbrink M.
        Helicobacter pylori-induced activation of human endothelial cells.
        Infect Immun. 2002; 70: 4581-4590
        • Zhang Q.B.
        • Nakashabendi I.M.
        • Mokhashi M.S.
        • Dawodu J.B.
        • Gemmell C.G.
        • Russell R.I.
        Association of cytotoxin production and neutrophil activation by strains of Helicobacter pylori isolated from patients with peptic ulceration and chronic gastritis.
        Gut. 1996; 38: 841-845
        • Molinari M.
        • Salio M.
        • Galli C.
        • Norais N.
        • Rappuoli R.
        • Lanzavecchia A.
        • Montecucco C.
        Selective inhibition of Ii-dependent antigen presentation by Helicobacter pylori toxin VacA.
        J Exp Med. 1998; 187: 135-140
        • Negrini R.
        • Savio A.
        • Appelmelk B.J.
        Autoantibodies to gastric mucosa in Helicobacter pylori infection.
        Helicobacter. 1997; 2: S13-S16
        • Harris A.W.
        • Misiewicz J.J.
        Antibiotic treatment for low-grade gastric MALT lymphoma.
        Lancet. 1994; 343: 1503
        • O’Garra A.
        • Vieira P.
        Regulatory T cells and mechanisms of immune system control.
        Nat Med. 2004; 10: 801-805
        • Harris P.R.
        • Smythies L.E.
        • Smith P.D.
        • Dubois A.
        Inflammatory cytokine mRNA expression during early and persistent Helicobacter pylori infection in nonhuman primates.
        J Infect Dis. 2000; 181: 783-786
        • Smythies L.E.
        • Waites K.B.
        • Lindsey J.R.
        • Harris P.R.
        • Ghiara P.
        • Smith P.D.
        Helicobacter pylori-induced mucosal inflammation is Th1 mediated and exacerbated in IL-4, but not IFN-gamma, gene-deficient mice.
        J Immunol. 2000; 165: 1022-1029
        • Tomita T.
        • Jackson A.M.
        • Hida N.
        • Hayat M.
        • Dixon M.F.
        • Shimoyama T.
        • Axon A.T.
        • Robinson P.A.
        • Crabtree J.E.
        Expression of interleukin-18, a Th1 cytokine, in human gastric mucosa is increased in Helicobacter pylori infection.
        J Infect Dis. 2001; 183: 620-627
        • Wang J.
        • Brooks E.G.
        • Bamford K.B.
        • Denning T.L.
        • Pappo J.
        • Ernst P.B.
        Negative selection of T cells by Helicobacter pylori as a model for bacterial strain selection by immune evasion.
        J Immunol. 2001; 167: 926-934
        • Panthel K.
        • Faller G.
        • Haas R.
        Colonization of C57BL/6J and BALB/c wild-type and knockout mice with Helicobacter pylori: effect of vaccination and implications for innate and acquired immunity.
        Infect Immun. 2003; 71: 794-800
        • Raghavan S.
        • Fredriksson M.
        • Svennerholm A.M.
        • Holmgren J.
        • Suri-Payer E.
        Absence of CD4+CD25+ regulatory T cells is associated with a loss of regulation leading to increased pathology in Helicobacter pylori-infected mice.
        Clin Exp Immunol. 2003; 132: 393-400
        • Kaser A.
        • Kaser S.
        • Kaneider N.C.
        • Enrich B.
        • Wiedermann C.J.
        • Tilg H.
        Interleukin-18 attracts plasmacytoid dendritic cells (DC2s) and promotes Th1 induction by DC2s through IL-18 receptor expression.
        Blood. 2004; 103: 648-655
        • Wakkach A.
        • Fournier N.
        • Brun V.
        • Breittmayer J.P.
        • Cottrez F.
        • Groux H.
        Characterization of dendritic cells that induce tolerance and T regulatory 1 cell differentiation in vivo.
        Immunity. 2003; 18: 605-617
        • Gobert A.P.
        • McGee D.J.
        • Akhtar M.
        • Mendz G.L.
        • Newton J.C.
        • Cheng Y.
        • Mobley H.L.
        • Wilson K.T.
        Helicobacter pylori arginase inhibits nitric oxide production by eukaryotic cells.
        Proc Natl Acad Sci U S A. 2001; 98: 13844-13849
        • Gobert A.P.
        • Cheng Y.
        • Wang J.Y.
        • Boucher J.L.
        • Iyer R.K.
        • Cederbaum S.D.
        • Casero Jr, R.A.
        • Newton J.C.
        • Wilson K.T.
        Helicobacter pylori induces macrophage apoptosis by activation of arginase II.
        J Immunol. 2002; 168: 4692-4700
        • Mantovani A.
        • Sozzani S.
        • Locati M.
        • Allavena P.
        • Sica A.
        Macrophage polarization.
        Trends Immunol. 2002; 23: 549-555
        • Mazzoni A.
        • Bronte V.
        • Visintin A.
        • Spitzer J.H.
        • Apolloni E.
        • Serafini P.
        • Zanovello P.
        • Segal D.M.
        Myeloid suppressor lines inhibit T cell responses by an NO-dependent mechanism.
        J Immunol. 2002; 168: 689-695
        • Zheng P.Y.
        • Jones N.L.
        Helicobacter pylori strains expressing the vacuolating cytotoxin interrupt phagosome maturation in macrophages by recruiting and retaining TACO (coronin 1) protein.
        Cell Microbiol. 2003; 5: 25-40
        • Kalia N.
        • Bardhan K.D.
        • Atherton J.C.
        • Brown N.J.
        Toxigenic Helicobacter pylori induces changes in the gastric mucosal microcirculation in rats.
        Gut. 2002; 51: 641-647
        • Magnusson P.K.E.
        • Enroth H.
        • Eriksson I.
        • Held M.
        • Nyren O.
        • Engstrand L.
        • Hansson L.E.
        • Gyllensten U.B.
        Gastric cancer and human leukocyte antigen.
        Cancer Res. 2001; 61: 2684-2689
        • Rad R.
        • Dossumbekova A.
        • Neu B.
        • Lang R.
        • Bauer S.
        • Saur D.
        • Gerhard M.
        • Prinz C.
        Cytokine gene polymorphisms influence mucosal cytokine expression, gastric inflammation, and host specific colonisation during Helicobacter pylori infection.
        Gut. 2004; 53: 1082-1089
        • Machado J.C.
        • Pharoah P.
        • Sousa S.
        • Carvalho R.
        • Oliveira C.
        • Figueiredo C.
        • Amorim A.
        • Seruca R.
        • Caldas C.
        • Carneiro F.
        • Sobrinho-Simoes M.
        Interleukin 1B and interleukin 1RN polymorphisms are associated with increased risk of gastric carcinoma.
        Gastroenterology. 2001; 121: 823-829
        • Dinarello C.A.
        Biologic basis for interleukin-1 in disease.
        Blood. 1996; 87: 2095-2147
        • El-Omar E.M.
        • Carrington M.
        • Chow W.H.
        • McColl K.E.
        • Bream J.H.
        • Young H.A.
        • Herrera J.
        • Lissowska J.
        • Yuan C.C.
        • Rothman N.
        • Lanyon G.
        • Martin M.
        • Fraumeni Jr, J.F.
        • Rabkin C.S.
        The role of interleukin-1 polymorphisms in the pathogenesis of gastric cancer.
        Nature. 2001; 412: 99
        • El-Omar E.M.
        • Carrington M.
        • Chow W.H.
        • McColl K.E.
        • Bream J.H.
        • Young H.A.
        • Herrera J.
        • Lissowska J.
        • Yuan C.C.
        • Rothman N.
        • Lanyon G.
        • Martin M.
        • Fraumeni Jr, J.F.
        • Rabkin C.S.
        Interleukin-1 polymorphisms associated with increased risk of gastric cancer.
        Nature. 2000; 404: 398-402
        • Rollinson S.
        • Levene A.P.
        • Mensah F.K.
        • Roddam P.L.
        • Allan J.M.
        • Diss T.C.
        • Roman E.
        • Jack A.
        • MacLennan K.
        • Dixon M.F.
        • Morgan G.J.
        Gastric marginal zone lymphoma is associated with polymorphisms in genes involved in inflammatory response and antioxidative capacity.
        Blood. 2003; 102: 1007-1011
        • McGuire W.
        • Hill A.V.
        • Allsopp C.E.
        • Greenwood B.M.
        • Kwiatkowski D.
        Variation in the TNF-alpha promoter region associated with susceptibility to cerebral malaria.
        Nature. 1994; 371: 508-510
        • Tsukasaki K.
        • Miller C.W.
        • Kubota T.
        • Takeuchi S.
        • Fujimoto T.
        • Ikeda S.
        • Tomonaga M.
        • Koeffler H.P.
        Tumor necrosis factor alpha polymorphism associated with increased susceptibility to development of adult T-cell leukemia/lymphoma in human T-lymphotropic virus type 1 carriers.
        Cancer Res. 2001; 61: 3770-3774
        • Locksley R.M.
        • Killeen N.
        • Lenardo M.J.
        The TNF and TNF receptor superfamilies.
        Cell. 2001; 104: 487-501
        • Kunstmann E.
        • Epplen C.
        • Elitok E.
        • Harder M.
        • Suerbaum S.
        • Peitz U.
        • Schmiegel W.
        • Epplen J.T.
        Helicobacter pylori infection and polymorphisms in the tumor necrosis factor region.
        Electrophoresis. 1999; 20: 1756-1761
        • Wu M.S.
        • Huang S.P.
        • Chang Y.T.
        • Shun C.T.
        • Chang M.C.
        • Lin M.T.
        • Wang H.P.
        • Lin J.T.
        Tumor necrosis factor-alpha and interleukin-10 promoter polymorphisms in Epstein-Barr virus-associated gastric carcinoma.
        J Infect Dis. 2002; 185: 106-109
        • Wu M.S.
        • Chen L.T.
        • Shun C.T.
        • Huang S.P.
        • Chiu H.M.
        • Wang H.P.
        • Lin M.T.
        • Cheng A.L.
        • Lin J.T.
        Promoter polymorphisms of tumor necrosis factor-alpha are associated with risk of gastric mucosa-associated lymphoid tissue lymphoma.
        Int J Cancer. 2004; 110: 695-700
        • van Heel D.A.
        • Udalova I.A.
        • De Silva A.P.
        • McGovern D.P.
        • Kinouchi Y.
        • Hull J.
        • Lench N.J.
        • Cardon L.R.
        • Carey A.H.
        • Jewell D.P.
        • Kwiatkowski D.
        Inflammatory bowel disease is associated with a TNF polymorphism that affects an interaction between the OCT1 and NF(-kappa)B transcription factors.
        Hum Mol Genet. 2002; 11: 1281-1289
        • Lee J.
        • O’Morain C.
        Who should be treated for Helicobacter pylori infection? A review of consensus conferences and guidelines.
        Gastroenterology. 1997; 113: S99-S106
        • Seeberger H.
        • Starostik P.
        • Schwarz S.
        • Knorr C.
        • Kalla J.
        • Ott G.
        • Muller-Hermelink H.K.
        • Greiner A.
        Loss of Fas (CD95/APO-1) regulatory function is an important step in early MALT-type lymphoma development.
        Lab Invest. 2001; 81: 977-986
        • Howell W.M.
        • Leung S.T.
        • Jones D.B.
        • Nakshabendi I.
        • Hall M.A.
        • Lanchbury J.S.
        • Ciclitira P.J.
        • Wright D.H.
        HLA-DRB, -DQA, and -DQB polymorphism in celiac disease and enteropathy-associated T-cell lymphoma. Common features and additional risk factors for malignancy.
        Hum Immunol. 1995; 43: 29-37
        • Reimer P.
        • Fischbach W.
        • Goebeler M.E.
        • Kraus M.R.
        • Goldmann S.
        • Muller C.
        • Wilhelm M.
        Decreased frequency of HLA-B35 in patients with gastric MALT lymphoma.
        Ann Hematol. 2004; 83: 232-236
        • Seidegard J.
        • Vorachek W.R.
        • Pero R.W.
        • Pearson W.R.
        Hereditary differences in the expression of the human glutathione transferase active on trans-stilbene oxide are due to a gene deletion.
        Proc Natl Acad Sci U S A. 1988; 85: 7293-7297
        • Rollinson S.
        • Roddam P.
        • Kane E.
        • Roman E.
        • Cartwright R.
        • Jack A.
        • Morgan G.J.
        Polymorphic variation within the glutathione S-transferase genes and risk of adult acute leukaemia.
        Carcinogenesis. 2000; 21: 43-47
        • Du M.
        • Diss T.C.
        • Xu C.
        • Peng H.
        • Isaacson P.G.
        • Pan L.
        Ongoing mutation in MALT lymphoma immunoglobulin gene suggests that antigen stimulation plays a role in the clonal expansion.
        Leukemia. 1996; 10: 1190-1197
        • Hussell T.
        • Isaacson P.G.
        • Spencer J.
        Proliferation and differentiation of tumour cells from B-cell lymphoma of mucosa-associated lymphoid tissue in vitro.
        J Pathol. 1993; 169: 221-227
        • Hussell T.
        • Isaacson P.G.
        • Crabtree J.E.
        • Spencer J.
        Helicobacter pylori-specific tumour-infiltrating T cells provide contact dependent help for the growth of malignant B cells in low-grade gastric lymphoma of mucosa-associated lymphoid tissue.
        J Pathol. 1996; 178: 122-127
        • Hussell T.
        • Isaacson P.G.
        • Crabtree J.E.
        • Dogan A.
        • Spencer J.
        Immunoglobulin specificity of low grade B cell gastrointestinal lymphoma of mucosa-associated lymphoid tissue (MALT) type.
        Am J Pathol. 1993; 142: 285-292
        • D’Elios M.M.
        • Manghetti M.
        • Almerigogna F.
        • Amedei A.
        • Costa F.
        • Burroni D.
        • Baldari C.T.
        • Romagnani S.
        • Telford J.L.
        • Del Prete G.
        Different cytokine profile and antigen-specificity repertoire in Helicobacter pylori-specific T cell clones from the antrum of chronic gastritis patients with or without peptic ulcer.
        Eur J Immunol. 1997; 27: 1751-1755
        • D’Elios M.M.
        • Amedei A.
        • Manghetti M.
        • Costa F.
        • Baldari C.T.
        • Quazi A.S.
        • Telford J.L.
        • Romagnani S.
        • Del Prete G.
        Impaired T-cell regulation of B-cell growth in Helicobacter pylori-related gastric low-grade MALT lymphoma.
        Gastroenterology. 1999; 117: 1105-1112
        • Holzelova E.
        • Vonarbourg C.
        • Stolzenberg M.C.
        • Arkwright P.D.
        • Selz F.
        • Prieur A.M.
        • Blanche S.
        • Bartunkova J.
        • Vilmer E.
        • Fischer A.
        • Le Deist F.
        • Rieux-Laucat F.
        Autoimmune lymphoproliferative syndrome with somatic Fas mutations.
        N Engl J Med. 2004; 351: 1409-1418
        • Bertoni F.
        • Conconi A.
        • Luminari S.
        • Realini C.
        • Roggero E.
        • Baldini L.
        • Carobbio S.
        • Cavalli F.
        • Neri A.
        • Zucca E.
        Lack of CD95/FAS gene somatic mutations in extranodal, nodal and splenic marginal zone B cell lymphomas.
        Leukemia. 2000; 14: 446-448
        • Riedel S.
        • Kraft M.
        • Kucharzik T.
        • Pauels H.G.
        • Tiemann M.
        • Steinbuchel A.
        • Domschke W.
        • Lugering N.
        CD4+ Th1-cells predominate in low-grade B-cell lymphoma of gastric mucosa-associated lymphoid tissue (MALT type).
        Scand J Gastroenterol. 2001; 36: 1198-1203
        • Hauer A.C.
        • Finn T.M.
        • MacDonald T.T.
        • Spencer J.
        • Isaacson P.G.
        Analysis of TH1 and TH2 cytokine production in low grade B cell gastric MALT-type lymphomas stimulated in vitro with Helicobacter pylori.
        J Clin Pathol. 1997; 50: 957-959
        • Dunn G.P.
        • Old L.J.
        • Schreiber R.D.
        The immunobiology of cancer immunosurveillance and immunoediting.
        Immunity. 2004; 21: 137-148
        • Stromberg E.
        • Lundgren A.
        • Edebo A.
        • Lundin S.
        • Svennerholm A.M.
        • Lindholm C.
        Increased frequency of activated T-cells in the Helicobacter pylori-infected antrum and duodenum.
        FEMS Immunol Med Microbiol. 2003; 36: 159-168
        • Golgher D.
        • Jones E.
        • Powrie F.
        • Elliott T.
        • Gallimore A.
        Depletion of CD25+ regulatory cells uncovers immune responses to shared murine tumor rejection antigens.
        Eur J Immunol. 2002; 32: 3267-3275
        • Curiel T.J.
        • Coukos G.
        • Zou L.
        • Alvarez X.
        • Cheng P.
        • Mottram P.
        • Evdemon-Hogan M.
        • Conejo-Garcia J.R.
        • Zhang L.
        • Burow M.
        • Zhu Y.
        • Wei S.
        • Kryczek I.
        • Daniel B.
        • Gordon A.
        • Myers L.
        • Lackner A.
        • Disis M.L.
        • Knutson K.L.
        • Chen L.
        • Zou W.
        Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival.
        Nat Med. 2004; 10: 942-949
        • Sutton P.
        • O’Rourke J.
        • Wilson J.
        • Dixon M.F.
        • Lee A.
        Immunisation against Helicobacter felis infection protects against the development of gastric MALT Lymphoma.
        Vaccine. 2004; 22: 2541-2546
        • Fukui T.
        • Okazaki K.
        • Tamaki H.
        • Kawasaki K.
        • Matsuura M.
        • Asada M.
        • Nishi T.
        • Uchida K.
        • Iwano M.
        • Ohana M.
        • Hiai H.
        • Chiba T.
        Immunogenetic analysis of gastric MALT lymphoma-like lesions induced by Helicobacter pylori infection in neonatally thymectomized mice.
        Lab Invest. 2004; 84: 485-492
        • Mueller A.
        • O’Rourke J.
        • Grimm J.
        • Guillemin K.
        • Dixon M.F.
        • Lee A.
        • Falkow S.
        Distinct gene expression profiles characterize the histopathological stages of disease in Helicobacter-induced mucosa-associated lymphoid tissue lymphoma.
        Proc Natl Acad Sci U S A. 2003; 100: 1292-1297
        • Du M.Q.
        • Isaccson P.G.
        Gastric MALT lymphoma.
        Lancet Oncol. 2002; 3: 97-104
        • Hessian P.A.
        • Fisher L.
        The heterodimeric complex of MRP-8 (S100A8) and MRP-14 (S100A9). Antibody recognition, epitope definition and the implications for structure.
        Eur J Biochem. 2001; 268: 353-363
        • Vakkila J.
        • Lotze M.T.
        Inflammation and necrosis promote tumour growth.
        Nat Rev Immunol. 2004; 4: 641-648
        • Wotherspoon A.C.
        • Doglioni C.
        • Isaacson P.G.
        Low-grade gastric B-cell lymphoma of mucosa-associated lymphoid tissue (MALT).
        Histopathology. 1992; 20: 29-34
        • Isaacson P.G.
        • Spencer J.
        Malignant lymphoma of mucosa-associated lymphoid tissue.
        Histopathology. 1987; 11: 445-462
        • Isaacson P.G.
        • Wotherspoon A.C.
        • Diss T.
        • Pan L.X.
        Follicular colonization in B-cell lymphoma of mucosa-associated lymphoid tissue.
        Am J Surg Pathol. 1991; 15: 819-828
        • Spencer J.
        • Finn T.
        • Pulford K.A.
        • Mason D.Y.
        • Isaacson P.G.
        The human gut contains a novel population of B lymphocytes which resemble marginal zone cells.
        Clin Exp Immunol. 1985; 62: 607-612
        • Rajewsky K.
        Clonal selection and learning in the antibody system.
        Nature. 1996; 381: 751-758
        • Qin Y.
        • Greiner A.
        • Trunk M.J.
        • Schmausser B.
        • Ott M.M.
        • Muller-Hermelink H.K.
        Somatic hypermutation in low-grade mucosa-associated lymphoid tissue-type B-cell lymphoma.
        Blood. 1995; 86: 3528-3534
        • Contos M.J.
        • Kornstein M.J.
        • Innes D.J.
        • Ben-Ezra J.
        The utility of CD20 and CD43 in subclassification of low-grade B-cell lymphoma on paraffin sections.
        Mod Pathol. 1992; 5: 631-633
        • Ashton-Key M.
        • Diss T.C.
        • Isaacson P.G.
        Detection of Helicobacter pylori in gastric biopsy and resection specimens.
        J Clin Pathol. 1996; 49: 107-111
        • Diss T.C.
        • Pan L.
        Polymerase chain reaction in the assessment of lymphomas.
        Cancer Surv. 1997; 30: 21-44
        • Thiede C.
        • Wundisch T.
        • Neubauer B.
        • Alpen B.
        • Morgner A.
        • Ritter M.
        • Ehninger G.
        • Stolte M.
        • Bayerdorffer E.
        • Neubauer A.
        Eradication of Helicobacter pylori and stability of remissions in low-grade gastric B-cell lymphomas of the mucosa-associated lymphoid tissue.
        Recent Results Cancer Res. 2000; 156: 125-133
        • Miyamoto M.
        • Haruma K.
        • Hiyama T.
        • Kamada T.
        • Masuda H.
        • Shimamoto F.
        • Inoue K.
        • Chayama K.
        High incidence of B-cell monoclonality in follicular gastritis.
        Virchows Arch. 2002; 440: 376-380
        • Hiyama T.
        • Haruma K.
        • Kitadai Y.
        • Miyamoto M.
        • Tanaka S.
        • Yoshihara M.
        • Sumii K.
        • Shimamoto F.
        • Kajiyama G.
        B-cell monoclonality in Helicobacter pylori-associated chronic atrophic gastritis.
        Virchows Arch. 2001; 438: 232-237
        • Hsi E.D.
        • Greenson J.K.
        • Singleton T.P.
        • Siddiqui J.
        • Schnitzer B.
        • Ross C.W.
        Detection of immunoglobulin heavy chain gene rearrangement by polymerase chain reaction in chronic active gastritis associated with Helicobacter pylori.
        Hum Pathol. 1996; 27: 290-296
        • Hoeve M.A.
        • Krol A.D.
        • Philippo K.
        • Derksen P.W.
        • Veenendaal R.A.
        • Schuuring E.
        • Kluin P.M.
        • van Krieken J.H.
        Limitations of clonality analysis of B cell proliferations using CDR3 polymerase chain reaction.
        Mol Pathol. 2000; 53: 194-200
        • Attygalle A.D.
        • Liu H.
        • Shirali S.
        • Diss T.C.
        • Loddenkemper C.
        • Stein H.
        • Dogan A.
        • Du M.Q.
        • Isaacson P.G.
        Atypical marginal zone hyperplasia of mucosa-associated lymphoid tissue.
        Blood. 2004; 104: 3343-3348
        • Du M.Q.
        • Diss T.C.
        • Dogan A.
        • Ye H.T.
        • Aiello A.
        • Wotherspoon A.C.
        • Pan L.X.
        • Isaacson P.G.
        Clone-specific PCR reveals wide dissemination of gastric MALT lymphoma to the gastric mucosa.
        J Pathol. 2000; 192: 488-493
        • Dogan A.
        • Du M.
        • Koulis A.
        • Briskin M.J.
        • Isaacson P.G.
        Expression of lymphocyte homing receptors and vascular addressins in low-grade gastric B-cell lymphomas of mucosa-associated lymphoid tissue.
        Am J Pathol. 1997; 151: 1361-1369
        • Chan J.K.
        • Ng C.S.
        • Isaacson P.G.
        Relationship between high-grade lymphoma and low-grade B-cell mucosa-associated lymphoid tissue lymphoma (MALToma) of the stomach.
        Am J Pathol. 1990; 136: 1153-1164
        • de Jong D.
        • Boot H.
        • van Heerde P.
        • Hart G.A.
        • Taal B.G.
        Histological grading in gastric lymphoma.
        Gastroenterology. 1997; 112: 1466-1474
        • Peng H.
        • Du M.
        • Diss T.C.
        • Isaacson P.G.
        • Pan L.
        Genetic evidence for a clonal link between low and high-grade components in gastric MALT B-cell lymphoma.
        Histopathology. 1997; 30: 425-429
        • Jaffe E.S.
        • Harris N.L.
        • Stein H.
        • Vardiman J.W.
        World Health Organization classification of tumours.
        Pathology and genetics of tumors of haematopoietic and lymphoid tissues. IARC Press, 2001
        • Du M.
        • Peng H.
        • Singh N.
        • Isaacson P.G.
        • Pan L.
        The accumulation of p53 abnormalities is associated with progression of mucosa-associated lymphoid tissue lymphoma.
        Blood. 1995; 86: 4587-4593
        • Martinez-Delgado B.
        • Fernandez-Piqueras J.
        • Garcia M.J.
        • Arranz E.
        • Gallego J.
        • Rivas C.
        • Robledo M.
        • Benitez J.
        Hypermethylation of a 5′ CpG island of p16 is a frequent event in non-Hodgkin’s lymphoma.
        Leukemia. 1997; 11: 425-428
        • Martinez-Delgado B.
        • Robledo M.
        • Arranz E.
        • Osorio A.
        • Garcia M.J.
        • Echezarreta G.
        • Rivas C.
        • Benitez J.
        Hypermethylation of p15/ink4b/MTS2 gene is differentially implicated among non-Hodgkin’s lymphomas.
        Leukemia. 1998; 12: 937-941
        • Neumeister P.
        • Hoefler G.
        • Beham-Schmid C.
        • Schmidt H.
        • Apfelbeck U.
        • Schaider H.
        • Linkesch W.
        • Sill H.
        Deletion analysis of the p16 tumor suppressor gene in gastrointestinal mucosa-associated lymphoid tissue lymphomas.
        Gastroenterology. 1997; 112: 1871-1875
        • Blackburn E.H.
        Structure and function of telomeres.
        Nature. 1991; 350: 569-573
        • Kim N.W.
        • Piatyszek M.A.
        • Prowse K.R.
        • Harley C.B.
        • West M.D.
        • Ho P.L.
        • Coviello G.M.
        • Wright W.E.
        • Weinrich S.L.
        • Shay J.W.
        Specific association of human telomerase activity with immortal cells and cancer.
        Science. 1994; 266: 2011-2015
        • Hiyama E.
        • Yokoyama T.
        • Tatsumoto N.
        • Hiyama K.
        • Imamura Y.
        • Murakami Y.
        • Kodama T.
        • Piatyszek M.A.
        • Shay J.W.
        • Matsuura Y.
        Telomerase activity in gastric cancer.
        Cancer Res. 1995; 55: 3258-3262
        • Trentin L.
        • Ballon G.
        • Ometto L.
        • Perin A.
        • Basso U.
        • Chieco-Bianchi L.
        • Semenzato G.
        • De Rossi A.
        Telomerase activity in chronic lymphoproliferative disorders of B-cell lineage.
        Br J Haematol. 1999; 106: 662-668
        • Kodera Y.
        • Nakamura T.
        • Suzuki T.
        • Yamamura Y.
        • Nakamura S.
        Clinical relevance of telomerase activity in primary gastric lymphoma.
        Gastric Cancer. 2000; 3: 57-62
        • Barth T.F.
        • Bentz M.
        • Leithauser F.
        • Stilgenbauer S.
        • Siebert R.
        • Schlotter M.
        • Schlenk R.F.
        • Dohner H.
        • Moller P.
        Molecular-cytogenetic comparison of mucosa-associated marginal zone B-cell lymphoma and large B-cell lymphoma arising in the gastro-intestinal tract.
        Genes Chromosomes Cancer. 2001; 31: 316-325
        • Starostik P.
        • Patzner J.
        • Greiner A.
        • Schwarz S.
        • Kalla J.
        • Ott G.
        • Muller-Hermelink H.K.
        Gastric marginal zone B-cell lymphomas of MALT type develop along 2 distinct pathogenetic pathways.
        Blood. 2002; 99: 3-9
        • Zhou Y.
        • Ye H.
        • Hamoudi R.A.
        • Lu Y.-J.
        • Wang R.
        • Shipley J.
        • Isaacson P.
        • Dogan A.
        • Du M.
        Distinct CGH profiles between gastric MALT lymphomas with and without t(11;18)(q21;q21).
        Blood. 2003; 102 (abstr): 3291
        • Kaneko Y.
        • Sakurai S.
        • Hironaka M.
        • Sato S.
        • Oguni S.
        • Sakuma Y.
        • Sato K.
        • Sugano K.
        • Saito K.
        Distinct methylated profiles in Helicobacter pylori dependent and independent gastric MALT lymphomas.
        Gut. 2003; 52: 641-646
        • Toyota M.
        • Ahuja N.
        • Ohe-Toyota M.
        • Herman J.G.
        • Baylin S.B.
        • Issa J.P.
        CpG island methylator phenotype in colorectal cancer.
        Proc Natl Acad Sci U S A. 1999; 96: 8681-8686
        • Chuang S.S.
        • Lee C.
        • Hamoudi R.A.
        • Liu H.
        • Lee P.S.
        • Ye H.
        • Diss T.C.
        • Dogan A.
        • Isaacson P.G.
        • Du M.Q.
        High frequency of t(11;18) in gastric mucosa-associated lymphoid tissue lymphomas in Taiwan, including one patient with high-grade transformation.
        Br J Haematol. 2003; 120: 97-100
        • Remstein E.D.
        • Kurtin P.J.
        • James C.D.
        • Wang X.Y.
        • Meyer R.G.
        • Dewald G.W.
        Mucosa-associated lymphoid tissue lymphomas with t(11;18)(q21;q21) and mucosa-associated lymphoid tissue lymphomas with aneuploidy develop along different pathogenetic pathways.
        Am J Pathol. 2002; 161: 63-71
        • Takada S.
        • Yoshino T.
        • Taniwaki M.
        • Nakamura N.
        • Nakamine H.
        • Oshima K.
        • Sadahira Y.
        • Inagaki H.
        • Tadaatsu A.
        Involvement of the chromosomal translocation t(11;18) in some mucosa-associated lymphoid tissue lymphomas and diffuse large B-cell lymphomas of the ocular adnexa.
        Mod Pathol. 2003; 16: 445-452
        • Du M.Q.
        • Xu C.F.
        • Diss T.C.
        • Peng H.Z.
        • Wotherspoon A.C.
        • Isaacson P.G.
        • Pan L.X.
        Intestinal dissemination of gastric mucosa-associated lymphoid tissue lymphoma.
        Blood. 1996; 88: 4445-4451
        • Gascoyne R.D.
        Molecular pathogenesis of mucosal-associated lymphoid tissue (MALT) lymphoma.
        Leuk Lymphoma. 2003; 44: S13-S20
        • Streubel B.
        • Vinatzer U.
        • Lamprecht A.
        • Raderer M.
        • Chott A.
        T(3;14)(p14.1;q32) involving IGH and FOXP1 is a novel recurrent chromosomal aberration in MALT lymphoma.
        Leukemia. 2005; 19: 652-658
        • Levine E.G.
        • Arthur D.C.
        • Machnicki J.
        • Frizzera G.
        • Hurd D.
        • Peterson B.
        • Gajl-Peczalska K.J.
        • Bloomfield C.D.
        Four new recurring translocations in non-Hodgkin lymphoma.
        Blood. 1989; 74: 1796-1800
        • Horsman D.
        • Gascoyne R.
        • Klasa R.
        • Coupland R.
        t(11;18)(q21;q21.1).
        Genes Chromosomes Cancer. 1992; 4: 183-187
        • Ott G.
        • Katzenberger T.
        • Greiner A.
        • Kalla J.
        • Rosenwald A.
        • Heinrich U.
        • Ott M.M.
        • Muller-Hermelink H.K.
        The t(11;18)(q21;q21) chromosome translocation is a frequent and specific aberration in low-grade but not high-grade malignant non-Hodgkin’s lymphomas of the mucosa-associated lymphoid tissue (MALT-) type.
        Cancer Res. 1997; 57: 3944-3948
        • Auer I.A.
        • Gascoyne R.D.
        • Connors J.M.
        • Cotter F.E.
        • Greiner T.C.
        • Sanger W.G.
        • Horsman D.E.
        t(11;18)(q21;q21) is the most common translocation in MALT lymphomas.
        Ann Oncol. 1997; 8: 979-985
        • Streubel B.
        • Lamprecht A.
        • Dierlamm J.
        • Cerroni L.
        • Stolte M.
        • Ott G.
        • Raderer M.
        • Chott A.
        T(14;18)(q32;q21) involving IGH and MALT1 is a frequent chromosomal aberration in MALT lymphoma.
        Blood. 2003; 101: 2335-2339
        • Remstein E.D.
        • James C.D.
        • Kurtin P.J.
        Incidence and subtype specificity of API2-MALT1 fusion translocations in extranodal, nodal, and splenic marginal zone lymphomas.
        Am J Pathol. 2000; 156: 1183-1188
        • Liu H.
        • Ye H.
        • Dogan A.
        • Ranaldi R.
        • Hamoudi R.A.
        • Bearzi I.
        • Isaacson P.G.
        • Du M.Q.
        T(11;18)(q21;q21) is associated with advanced mucosa-associated lymphoid tissue lymphoma that expresses nuclear BCL10.
        Blood. 2001; 98: 1182-1187
        • Baens M.
        • Maes B.
        • Steyls A.
        • Geboes K.
        • Marynen P.
        • De Wolf-Peeters C.
        The product of the t(11;18), an API2-MLT fusion, marks nearly half of gastric MALT type lymphomas without large cell proliferation.
        Am J Pathol. 2000; 156: 1433-1439
        • Dierlamm J.
        • Baens M.
        • Wlodarska I.
        • Stefanova-Ouzounova M.
        • Hernandez J.M.
        • Hossfeld D.K.
        • De Wolf-Peeters C.
        • Hagemeijer A.
        • Van den Berghe H.
        • Marynen P.
        The apoptosis inhibitor gene API2 and a novel 18q gene, MLT, are recurrently rearranged in the t(11;18)(q21;q21) associated with mucosa-associated lymphoid tissue lymphomas.
        Blood. 1999; 93: 3601-3609
        • Akagi T.
        • Motegi M.
        • Tamura A.
        • Suzuki R.
        • Hosokawa Y.
        • Suzuki H.
        • Ota H.
        • Nakamura S.
        • Morishima Y.
        • Taniwaki M.
        • Seto M.
        A novel gene, MALT1 at 18q21, is involved in t(11;18) (q21;q21) found in low-grade B-cell lymphoma of mucosa-associated lymphoid tissue.
        Oncogene. 1999; 18: 5785-5794
        • Morgan J.A.
        • Yin Y.
        • Borowsky A.D.
        • Kuo F.
        • Nourmand N.
        • Koontz J.I.
        • Reynolds C.
        • Soreng L.
        • Griffin C.A.
        • Graeme-Cook F.
        • Harris N.L.
        • Weisenburger D.
        • Pinkus G.S.
        • Fletcher J.A.
        • Sklar J.
        Breakpoints of the t(11;18)(q21;q21) in mucosa-associated lymphoid tissue (MALT) lymphoma lie within or near the previously undescribed gene MALT1 in chromosome 18.
        Cancer Res. 1999; 59: 6205-6213
        • Liu H.
        • Ruskon-Fourmestraux A.
        • Lavergne-Slove A.
        • Ye H.
        • Molina T.
        • Bouhnik Y.
        • Hamoudi R.A.
        • Diss T.C.
        • Dogan A.
        • Megraud F.
        • Rambaud J.C.
        • Du M.Q.
        • Isaacson P.G.
        Resistance of t(11;18) positive gastric mucosa-associated lymphoid tissue lymphoma to Helicobacter pylori eradication therapy.
        Lancet. 2001; 357: 39-40
        • Rothe M.
        • Pan M.G.
        • Henzel W.J.
        • Ayres T.M.
        • Goeddel D.V.
        The TNFR2-TRAF signaling complex contains two novel proteins related to baculoviral inhibitor of apoptosis proteins.
        Cell. 1995; 83: 1243-1252
        • Roy N.
        • Deveraux Q.L.
        • Takahashi R.
        • Salvesen G.S.
        • Reed J.C.
        The c-IAP-1 and c-IAP-2 proteins are direct inhibitors of specific caspases.
        EMBO J. 1997; 16: 6914-6925
        • Uren A.G.
        • O’Rourke K.
        • Aravind L.A.
        • Pisabarro M.T.
        • Seshagiri S.
        • Koonin E.V.
        • Dixit V.M.
        Identification of paracaspases and metacaspases.
        Mol Cell. 2000; 6: 961-967
        • Liu H.
        • Hamoudi R.A.
        • Ye H.
        • Ruskone-Fourmestraux A.
        • Dogan A.
        • Isaacson P.G.
        • Du M.Q.
        t(11;18)(q21;q21) of mucosa-associated lymphoid tissue lymphoma results from illegitimate non-homologous end joining following double strand breaks.
        Br J Haematol. 2004; 125: 318-329
        • Baens M.
        • Steyls A.
        • Dierlamm J.
        • De Wolf-Peeters C.
        • Marynen P.
        Structure of the MLT gene and molecular characterization of the genomic breakpoint junctions in the t(11;18)(q21;q21) of marginal zone B-cell lymphomas of MALT type.
        Genes Chromosomes Cancer. 2000; 29: 281-291
        • Roix J.J.
        • McQueen P.G.
        • Munson P.J.
        • Parada L.A.
        • Misteli T.
        Spatial proximity of translocation-prone gene loci in human lymphomas.
        Nat Genet. 2003; 34: 287-291
        • Barkett M.
        • Gilmore T.D.
        Control of apoptosis by Rel/NF-kappaB transcription factors.
        Oncogene. 1999; 18: 6910-6924
        • Willis T.G.
        • Dyer M.J.
        The role of immunoglobulin translocations in the pathogenesis of B-cell malignancies.
        Blood. 2000; 96: 808-822
        • Kuppers R.
        • Dalla-Favera R.
        Mechanisms of chromosomal translocations in B cell lymphomas.
        Oncogene. 2001; 20: 5580-5594
        • Super H.G.
        • Strissel P.L.
        • Sobulo O.M.
        • Burian D.
        • Reshmi S.C.
        • Roe B.
        • Zeleznik-Le N.J.
        • Diaz M.O.
        • Rowley J.D.
        Identification of complex genomic breakpoint junctions in the t(9;11) MLL-AF9 fusion gene in acute leukemia.
        Genes Chromosomes Cancer. 1997; 20: 185-195
        • Jasin M.
        Homologous repair of DNA damage and tumorigenesis.
        Oncogene. 2002; 21: 8981-8993
        • Streubel B.
        • Simonitsch-Klupp I.
        • Mullauer L.
        • Lamprecht A.
        • Huber D.
        • Siebert R.
        • Stolte M.
        • Trautinger F.
        • Lukas J.
        • Puspok A.
        • Formanek M.
        • Assanasen T.
        • Muller-Hermelink H.K.
        • Cerroni L.
        • Raderer M.
        • Chott A.
        Variable frequencies of MALT lymphoma-associated genetic aberrations in MALT lymphomas of different sites.
        Leukemia. 2004; 18: 1722-1726
        • Aman P.
        Fusion genes in solid tumors.
        Semin Cancer Biol. 1999; 9: 303-318
        • Ferguson D.O.
        • Alt F.W.
        DNA double strand break repair and chromosomal translocation.
        Oncogene. 2001; 20: 5572-5579
        • Wotherspoon A.C.
        • Soosay G.N.
        • Diss T.C.
        • Isaacson P.G.
        Low-grade primary B-cell lymphoma of the lung. An immunohistochemical, molecular, and cytogenetic study of a single case.
        Am J Clin Pathol. 1990; 94: 655-660
        • Achuthan R.
        • Bell S.M.
        • Leek J.P.
        • Roberts P.
        • Horgan K.
        • Markham A.F.
        • Selby P.J.
        • MacLennan K.A.
        Novel translocation of the BCL10 gene in a case of mucosa associated lymphoid tissue lymphoma.
        Genes Chromosomes Cancer. 2000; 29: 347-349
        • Ye H.
        • Gong L.
        • Liu H.
        • Hamoudi R.A.
        • Shirali S.
        • Ho L.
        • Chott A.
        • Streubel B.
        • Siebert R.
        • Gesk S.
        • Martin-Subero J.I.
        • Radford J.A.
        • Banerjee S.
        • Nicholson A.G.
        • Ranaldi R.
        • Remstein E.D.
        • Gao Z.
        • Zheng J.
        • Isaacson P.G.
        • Dogan A.
        • Du M.Q.
        MALT lymphoma with t(14;18)(q32;q21)/IGH-MALT1 is characterized by strong cytoplasmic MALT1 and BCL10 expression.
        J Pathol. 2005; 205: 293-301
        • Ye H.
        • Dogan A.
        • Karran L.
        • Willis T.G.
        • Chen L.
        • Wlodarska I.
        • Dyer M.J.
        • Isaacson P.G.
        • Du M.Q.
        BCL10 expression in normal and neoplastic lymphoid tissue. Nuclear localization in MALT lymphoma.
        Am J Pathol. 2000; 157: 1147-1154
        • Willis T.G.
        • Jadayel D.M.
        • Du M.Q.
        • Peng H.
        • Perry A.R.
        • Abdul-Rauf M.
        • Price H.
        • Karran L.
        • Majekodunmi O.
        • Wlodarska I.
        • Pan L.
        • Crook T.
        • Hamoudi R.
        • Isaacson P.G.
        • Dyer M.J.
        Bcl10 is involved in t(1;14)(p22;q32) of MALT B cell lymphoma and mutated in multiple tumor types.
        Cell. 1999; 96: 35-45
        • Zhang Q.
        • Siebert R.
        • Yan M.
        • Hinzmann B.
        • Cui X.
        • Xue L.
        • Rakestraw K.M.
        • Naeve C.W.
        • Beckmann G.
        • Weisenburger D.D.
        • Sanger W.G.
        • Nowotny H.
        • Vesely M.
        • Callet-Bauchu E.
        • Salles G.
        • Dixit V.M.
        • Rosenthal A.
        • Schlegelberger B.
        • Morris S.W.
        Inactivating mutations and overexpression of BCL10, a caspase recruitment domain-containing gene, in MALT lymphoma with t(1;14)(p22;q32).
        Nat Genet. 1999; 22: 63-68
        • Ruland J.
        • Duncan G.S.
        • Elia A.
        • del Barco Barrantes I.
        • Nguyen L.
        • Plyte S.
        • Millar D.G.
        • Bouchard D.
        • Wakeham A.
        • Ohashi P.S.
        • Mak T.W.
        Bcl10 is a positive regulator of antigen receptor-induced activation of NF-kappaB and neural tube closure.
        Cell. 2001; 104: 33-42
        • Xue L.
        • Morris S.W.
        • Orihuela C.
        • Tuomanen E.
        • Cui X.
        • Wen R.
        • Wang D.
        Defective development and function of Bcl10-deficient follicular, marginal zone and B1 B cells.
        Nat Immunol. 2003; 4: 857-865
        • Zhang Q.
        • Cui X.
        • Sangster M.
        • et al.
        Selective hyperexpansion of marginal zone B cells in Eu-BCL10 mice.
        Blood. 2000; 96: 822a
        • Sanchez-Izquierdo D.
        • Buchonnet G.
        • Siebert R.
        • Gascoyne R.D.
        • Climent J.
        • Karran L.
        • Marin M.
        • Blesa D.
        • Horsman D.
        • Rosenwald A.
        • Staudt L.M.
        • Albertson D.G.
        • Du M.Q.
        • Ye H.
        • Marynen P.
        • Garcia-Conde J.
        • Pinkel D.
        • Dyer M.J.
        • Martinez-Climent J.A.
        MALT1 is deregulated by both chromosomal translocation and amplification in B-cell non-Hodgkin lymphoma.
        Blood. 2003; 101: 4539-4546
        • Remstein E.D.
        • Kurtin P.J.
        • Einerson R.R.
        • Paternoster S.F.
        • Dewald G.W.
        Primary pulmonary MALT lymphomas show frequent and heterogeneous cytogenetic abnormalities, including aneuploidy and translocations involving API2 and MALT1 and IGH and MALT1.
        Leukemia. 2004; 18: 156-160
        • Li S.
        • Weidenfeld J.
        • Morrisey E.E.
        Transcriptional and DNA binding activity of the Foxp1/2/4 family is modulated by heterotypic and homotypic protein interactions.
        Mol Cell Biol. 2004; 24: 809-822
        • Shaffer A.L.
        • Rosenwald A.
        • Staudt L.M.
        Lymphoid malignancies.
        Nat Rev Immunol. 2002; 2: 920-932
        • Banham A.H.
        • Beasley N.
        • Campo E.
        • Fernandez P.L.
        • Fidler C.
        • Gatter K.
        • Jones M.
        • Mason D.Y.
        • Prime J.E.
        • Trougouboff P.
        • Wood K.
        • Cordell J.L.
        The FOXP1 winged helix transcription factor is a novel candidate tumor suppressor gene on chromosome 3p.
        Cancer Res. 2001; 61: 8820-8829
        • Banham A.H.
        • Connors J.M.
        • Brown P.J.
        • Cordell J.L.
        • Ott G.
        • Sreenivasan G.
        • Farinha P.
        • Horsman D.E.
        • Gascoyne R.D.
        Expression of the FOXP1 transcription factor is strongly associated with inferior survival in patients with diffuse large B-cell lymphoma.
        Clin Cancer Res. 2005; 11: 1065-1072
        • Hans C.P.
        • Weisenburger D.D.
        • Greiner T.C.
        • Gascoyne R.D.
        • Delabie J.
        • Ott G.
        • Muller-Hermelink H.K.
        • Campo E.
        • Braziel R.M.
        • Jaffe E.S.
        • Pan Z.
        • Farinha P.
        • Smith L.M.
        • Falini B.
        • Banham A.H.
        • Rosenwald A.
        • Staudt L.M.
        • Connors J.M.
        • Armitage J.O.
        • Chan W.C.
        Confirmation of the molecular classification of diffuse large B-cell lymphoma by immunohistochemistry using a tissue microarray.
        Blood. 2004; 103: 275-282
        • Wlodarska I.
        • Vandenberghe P.
        • Nooien P.
        • Hagemeijer A.
        • Marynen P.
        • De Wolf-Peeters C.
        FOXP1, a highly expressed gene in a subset of DLBCL, is targeted by a recurrent t(3;14)(p13;q32).
        Blood. 2004; 104 (abstr): 2891
        • Ruland J.
        • Mak T.W.
        Transducing signals from antigen receptors to nuclear factor kappaB.
        Immunol Rev. 2003; 193: 93-100
        • Liu H.
        • Ye H.
        • Shirali S.
        • Gong L.
        • Chott A.
        • Streubel B.
        • Siebert R.
        • Gesk S.
        • Radford J.
        • Banerjee S.
        • Isaacson P.
        • Dogan A.
        • Du M.
        MALT Lymphoma with t(14;18)(q32;q21) is characterized by strong cytoplasmic MALT1 and BCL10 expression.
        Mod Pathol. 2004; 17 (abstr).: 1082
        • Gaide O.
        • Martinon F.
        • Micheau O.
        • Bonnet D.
        • Thome M.
        • Tschopp J.
        Carma1, a CARD-containing binding partner of Bcl10, induces Bcl10 phosphorylation and NF-kappaB activation.
        FEBS Lett. 2001; 496: 121-127
        • Bertin J.
        • Wang L.
        • Guo Y.
        • Jacobson M.D.
        • Poyet J.L.
        • Srinivasula S.M.
        • Merriam S.
        • DiStefano P.S.
        • Alnemri E.S.
        CARD11 and CARD14 are novel caspase recruitment domain (CARD)/membrane-associated guanylate kinase (MAGUK) family members that interact with BCL10 and activate NF-kappa B.
        J Biol Chem. 2001; 276: 11877-11882
        • Lucas P.C.
        • Yonezumi M.
        • Inohara N.
        • McAllister-Lucas L.M.
        • Abazeed M.E.
        • Chen F.F.
        • Yamaoka S.
        • Seto M.
        • Nunez G.
        Bcl10 and MALT1, independent targets of chromosomal translocation in malt lymphoma, cooperate in a novel NF-kappa B signaling pathway.
        J Biol Chem. 2001; 276: 19012-19019
        • Gaide O.
        • Favier B.
        • Legler D.F.
        • Bonnet D.
        • Brissoni B.
        • Valitutti S.
        • Bron C.
        • Tschopp J.
        • Thome M.
        CARMA1 is a critical lipid raft-associated regulator of TCR-induced NF-kappa B activation.
        Nat Immunol. 2002; 3: 836-843
        • Wang D.
        • You Y.
        • Case S.M.
        • McAllister-Lucas L.M.
        • Wang L.
        • DiStefano P.S.
        • Nunez G.
        • Bertin J.
        • Lin X.
        A requirement for CARMA1 in TCR-induced NF-kappa B activation.
        Nat Immunol. 2002; 3: 830-835
        • Sun Z.
        • Arendt C.W.
        • Ellmeier W.
        • Schaeffer E.M.
        • Sunshine M.J.
        • Gandhi L.
        • Annes J.
        • Petrzilka D.
        • Kupfer A.
        • Schwartzberg P.L.
        • Littman D.R.
        PKC-theta is required for TCR-induced NF-kappaB activation in mature but not immature T lymphocytes.
        Nature. 2000; 404: 402-407
        • Saijo K.
        • Mecklenbrauker I.
        • Santana A.
        • Leitger M.
        • Schmedt C.
        • Tarakhovsky A.
        Protein kinase C beta controls nuclear factor kappaB activation in B cells through selective regulation of the IkappaB kinase alpha.
        J Exp Med. 2002; 195: 1647-1652
        • Su T.T.
        • Guo B.
        • Kawakami Y.
        • Sommer K.
        • Chae K.
        • Humphries L.A.
        • Kato R.M.
        • Kang S.
        • Patrone L.
        • Wall R.
        • Teitell M.
        • Leitges M.
        • Kawakami T.
        • Rawlings D.J.
        PKC-beta controls I kappa B kinase lipid raft recruitment and activation in response to BCR signaling.
        Nat Immunol. 2002; 3: 780-786
        • Zhou H.
        • Wertz I.
        • O’Rourke K.
        • Ultsch M.
        • Seshagiri S.
        • Eby M.
        • Xiao W.
        • Dixit V.M.
        Bcl10 activates the NF-kappaB pathway through ubiquitination of NEMO.
        Nature. 2004; 427: 167-171
        • Sun L.
        • Deng L.
        • Ea C.K.
        • Xia Z.P.
        • Chen Z.J.
        The TRAF6 ubiquitin ligase and TAK1 kinase mediate IKK activation by BCL10 and MALT1 in T lymphocytes.
        Mol Cell. 2004; 14: 289-301
        • Chung J.Y.
        • Park Y.C.
        • Ye H.
        • Wu H.
        All TRAFs are not created equal.
        J Cell Sci. 2002; 115: 679-688
        • Hostager B.S.
        • Catlett I.M.
        • Bishop G.A.
        Recruitment of CD40 and tumor necrosis factor receptor-associated factors 2 and 3 to membrane microdomains during CD40 signaling.
        J Biol Chem. 2000; 275: 15392-15398
        • Haxhinasto S.A.
        • Bishop G.A.
        Synergistic B cell activation by CD40 and the B cell antigen receptor.
        J Biol Chem. 2004; 279: 2575-2582
        • Bishop G.A.
        The multifaceted roles of TRAFs in the regulation of B-cell function.
        Nat Rev Immunol. 2004; 4: 775-786
        • Thome M.
        CARMA1, BCL-10 and MALT1 in lymphocyte development and activation.
        Nat Rev Immunol. 2004; 4: 348-359
        • Isaacson P.G.
        • Du M.Q.
        MALT lymphoma.
        Nat Rev Cancer. 2004; 4: 644-653
        • Ea C.K.
        • Sun L.
        • Inoue J.
        • Chen Z.J.
        TIFA activates IkappaB kinase (IKK) by promoting oligomerization and ubiquitination of TRAF6.
        Proc Natl Acad Sci U S A. 2004; 101: 15318-15323
        • Hosokawa Y.
        • Suzuki H.
        • Suzuki Y.
        • Takahashi R.
        • Seto M.
        Antiapoptotic function of apoptosis inhibitor 2-MALT1 fusion protein involved in t(11;18)(q21;q21) mucosa-associated lymphoid tissue lymphoma.
        Cancer Res. 2004; 64: 3452-3457
        • Stoffel A.
        • Chaurushiya M.
        • Singh B.
        • Levine A.J.
        Activation of NF-kappaB and inhibition of p53-mediated apoptosis by API2/mucosa-associated lymphoid tissue 1 fusions promote oncogenesis.
        Proc Natl Acad Sci U S A. 2004; 101: 9079-9084
        • Hamajima N.
        • Matuo K.
        • Watanabe Y.
        • Suzuki T.
        • Nakamura T.
        • Matsuura A.
        • Yamao K.
        • Ohashi K.
        • Tominaga S.
        A pilot study to evaluate stomach cancer risk reduction by Helicobacter pylori eradication.
        Am J Gastroenterol. 2002; 97: 764-765
        • Megraud F.
        How should Helicobacter pylori infection be diagnosed?.
        Gastroenterology. 1997; 113: S93-S98
        • Nakamura S.
        • Yao T.
        • Aoyagi K.
        • Iida M.
        • Fujishima M.
        • Tsuneyoshi M.
        Helicobacter pylori and primary gastric lymphoma. A histopathologic and immunohistochemical analysis of 237 patients.
        Cancer. 1997; 79: 3-11
        • Everhart J.E.
        • Kruszon-Moran D.
        • Perez-Perez G.
        Reliability of Helicobacter pylori and CagA serological assays.
        Clin Diagn Lab Immunol. 2002; 9: 412-416
        • Fox J.G.
        The non-H pylori helicobacters.
        Gut. 2002; 50: 273-283
        • Catassi C.
        • Fabiani E.
        • Coppa G.V.
        • Gabrielli A.
        • Centurioni R.
        • Leoni P.
        • Barbato M.
        • Viola F.
        • Martelli M.
        • De Renzo A.
        • Rotoli B.
        • Bertolani P.
        • Federico M.
        • Carroccio A.
        • Iannitto E.
        • Baldassarre M.
        • Guarini A.
        • Guariso G.
        • Favaretto G.
        • Caramaschi P.
        • Ambrosetti A.
        [High prevalence of hepatitis C virus infection in patients with non-Hodgkin’s lymphoma at the onset. Preliminary results of an Italian multicenter study].
        Recenti Prog Med. 1998; 89: 63-67
        • De Vita S.
        • De Re V.
        • Sansonno D.
        • Sorrentino D.
        • Corte R.L.
        • Pivetta B.
        • Gasparotto D.
        • Racanelli V.
        • Marzotto A.
        • Labombarda A.
        • Gloghini A.
        • Ferraccioli G.
        • Monteverde A.
        • Carbone A.
        • Dammacco F.
        • Boiocchi M.
        Gastric mucosa as an additional extrahepatic localization of hepatitis C virus.
        Hepatology. 2000; 31: 182-189
        • Luppi M.
        • Longo G.
        • Ferrari M.G.
        • Ferrara L.
        • Marasca R.
        • Barozzi P.
        • Morselli M.
        • Emilia G.
        • Torelli G.
        Additional neoplasms and HCV infection in low-grade lymphoma of MALT type.
        Br J Haematol. 1996; 94: 373-375
        • Tkoub E.M.
        • Haioun C.
        • Pawlotsky J.M.
        • Dhumeaux D.
        • Delchier J.C.
        Chronic hepatitis C virus and gastric MALT lymphoma.
        Blood. 1998; 91: 360
        • Tursi A.
        • Brandimante G.
        • Chiarelli F.
        • Spagnoli A.
        • Torello M.
        Detection of HCV RNA in gastric mucosa-associated lymphoid tissue by in situ hybridization.
        Am J Gastroenterol. 2002; 97: 1802-1806
        • Tursi A.
        • Brandimarte G.
        • Torello M.
        Disappearance of gastric mucosa-associated lymphoid tissue in hepatitis C virus-positive patients after anti-hepatitis C virus therapy.
        J Clin Gastroenterol. 2004; 38: 360-363
        • Ye H.
        • Liu H.
        • Raderer M.
        • Chott A.
        • Ruskone-Fourmestraux A.
        • Wotherspoon A.
        • Dyer M.J.
        • Chuang S.S.
        • Dogan A.
        • Isaacson P.G.
        • Du M.Q.
        High incidence of t(11;18)(q21;q21) in Helicobacter pylori-negative gastric MALT lymphoma.
        Blood. 2003; 101: 2547-2550
        • Leandro M.J.
        • Isenberg D.A.
        Rheumatic diseases and malignancy—is there an association?.
        Scand J Rheumatol. 2001; 30: 185-188
        • Streubel B.
        • Huber D.
        • Wohrer S.
        • Chott A.
        • Raderer M.
        Frequency of chromosomal aberrations involving MALT1 in mucosa-associated lymphoid tissue lymphoma in patients with Sjogren’s syndrome.
        Clin Cancer Res. 2004; 10: 476-480
        • Raderer M.
        • Osterreicher C.
        • Machold K.
        • Formanek M.
        • Fiebiger W.
        • Penz M.
        • Dragosics B.
        • Chott A.
        Impaired response of gastric MALT-lymphoma to Helicobacter pylori eradication in patients with autoimmune disease.
        Ann Oncol. 2001; 12: 937-939
        • Nakamura T.
        • Nakamura S.
        • Yonezumi M.
        • Seto M.
        • Yokoi T.
        The t(11; 18)(q21; q21) translocation in H. pylori-negative low-grade gastric MALT lymphoma.
        Am J Gastroenterol. 2000; 95: 3314-3315
        • O’Rourke J.L.
        • Dixon M.F.
        • Jack A.
        • Enno A.
        • Lee A.
        Gastric B-cell mucosa-associated lymphoid tissue (MALT) lymphoma in an animal model of ’Helicobacter heilmannii’ infection.
        J Pathol. 2004; 203: 896-903