Gastroenterology
Volume 129, Issue 3 , Pages 969-984 , September 2005

Interleukin-22, a Member of the IL-10 Subfamily, Induces Inflammatory Responses in Colonic Subepithelial Myofibroblasts

  • Akira Andoh

      Affiliations

    • Department of Internal Medicine, Shiga University of Medical Science, Seta Tukinowa, Otsu, Japan
    • Corresponding Author InformationAddress requests for reprints to: Akira Andoh, MD, Department of Internal Medicine, Shiga University of Medical Science, Seta-Tukinowa, Otsu 520-2192, Japan.fax: (81) 77-548-2219.
    • ,
  • Zhuobin Zhang

      Affiliations

    • Department of Internal Medicine, Shiga University of Medical Science, Seta Tukinowa, Otsu, Japan
    • ,
  • Osamu Inatomi

      Affiliations

    • Department of Internal Medicine, Shiga University of Medical Science, Seta Tukinowa, Otsu, Japan
    • ,
  • Sanae Fujino

      Affiliations

    • Department of Internal Medicine, Shiga University of Medical Science, Seta Tukinowa, Otsu, Japan
    • ,
  • Yasuyuki Deguchi

      Affiliations

    • Department of Internal Medicine, Shiga University of Medical Science, Seta Tukinowa, Otsu, Japan
    • ,
  • Yoshio Araki

      Affiliations

    • Department of Internal Medicine, Shiga University of Medical Science, Seta Tukinowa, Otsu, Japan
    • ,
  • Tomoyuki Tsujikawa

      Affiliations

    • Department of Internal Medicine, Shiga University of Medical Science, Seta Tukinowa, Otsu, Japan
    • ,
  • Katsuyuki Kitoh

      Affiliations

    • Department of Internal Medicine, Shiga University of Medical Science, Seta Tukinowa, Otsu, Japan
    • ,
  • Shokei Kim–Mitsuyama

      Affiliations

    • Department of Pharmacology and Molecular Therapeutics, Kumamoto University Graduate School of Medical Sciences, Kumamoto, Japan
    • ,
  • Atsushi Takayanagi

      Affiliations

    • Department of Molecular Biology, Keio University School of Medicine, Tokyo, Japan
    • ,
  • Nobuyoshi Shimizu

      Affiliations

    • Department of Molecular Biology, Keio University School of Medicine, Tokyo, Japan
    • ,
  • Yoshihide Fujiyama

      Affiliations

    • Department of Internal Medicine, Shiga University of Medical Science, Seta Tukinowa, Otsu, Japan

Received 17 February 2005 ,Accepted 26 May 2005.

References 

  1. Podolsky DK . Inflammatory bowel disease . N Engl J Med . 2002;347:417–429
  2. Zareie M , Singh PK , Irvine EJ , Sherman PM , McKay DM , Perdue MH . Monocytes/macrophage activation by normal bacteria and bacterial products (implications for altered epithelial function in Crohn’s disease) . Am J Pathol . 2001;158;:1101–1109
  3. Boirivant M, Marini M, DiFelice G, Pronio AM, Montesani C, Tersigni R, et al. Lamina propria T cells in Crohn’s disease and other gastrointestinal inflammation show defective CD2 pathway-induced apoptosis . Gastroenterology . 1999;116:557–565
  4. Saubermann LJ, Probert CSJ, Christ AD, Chott A, Turner JR, Stevens AC, et al. Evidence of T cell receptor β-chain patterns in inflammatory and noninflammatory bowel disease states . Am J Physiol . 1999;276:G613–G621
  5. Wolk K , Kunz S , Witte E , Friedrich M , Asadullah K , Sabat R . IL-22 increases the innate immunity of tissues . Immunity . 2004;21:241–254
  6. Pestka S , Krause CD , Sarkar D , Walter MR , Shi Y , Fisher PB . Interleukin-10 and related cytokines and receptors . Annu Rev Immunol . 2004;22:929–979
  7. Conti P, Kempuraj D, Frydas S, Kandere K, Boucher W, Letourneau R, et al. IL-10 subfamily members (IL-19, IL-20, IL-22, IL-24 and IL-26) . Immunol Lett . 2003;88:171–174
  8. Wolk K , Kunz S , Asadullah K , Sabat R . Immune cells as sources and targets of the IL-10 family members? . J Immunol . 2002;168:5397–5402
  9. Gurney AL . IL-22, a Th1 cytokine that targets the pancreas and select other peripheral tissues . Int Immunopharmacol . 2004;4:669–677
  10. Kotenko SV, Izotova LS, Mirochnitchenko OV, Esterova E, Dickensheets H, Donnelly RP, et al. Identification of the functional interleukin-22 (IL-22) receptor complex (the IL-10R2 chain (IL-10Rbeta) is a common chain of both the IL-10 and IL-22 (IL-10-related T-cell-derived inducible factor, IL-TIF) receptor complexes) . J Biol Chem . 2001;276:2725–2732
  11. Aggarwal S , Xie MH , Maruoka M , Foster J , Gurney AL . Acinar cells of the pancreas are a target of interleukin-22 . J Interferon Cytokine Res . 2001;21:1047–1053
  12. Lejeune D , Dumoutier L , Constantinescu S , Kruijer W , Schuringa JJ , Renauld JC . Interleukin-22 (IL-22) activates the JAK/STAT, ERK, JNK, and p38 MAP kinase pathways in a rat hepatoma cell line. Pathways that are shared with and distinct from IL-10 . J Biol Chem . 2002;277:33676–33682
  13. Dumoutier L , Van Roost E , Colau D , Renauld JC . Human interleukin-10-related T-cell-derived inducible factor (molecular cloning and functional characterization as an hepatocyte-stimulating factor) . Proc Natl Acad Sci U S A . 2000;97:10144–10149
  14. Nagalakshmi ML , Rascle A , Zurawski S , Menon S , de Waal Malefyt R . Interleukin-22 activates STAT3 and induces IL-10 by colon epithelial cells . Int Immunopharmacol . 2004;4:679–691
  15. Rachmilewitz D . Coated mesalazine (5-aminosalicylic acid) versus sulphasalazine in the treatment of active ulcerative colitis (a randomised trial) . BMJ . 1989;298:82–86
  16. Best WR , Becktel JM , Singleton JW . Rederived values of the eight coefficients of the Crohn’s disease activity index (CDAI) . Gastroenterology . 1979;77:843–846
  17. Fujino S, Andoh A, Bamba S, Ogawa A, Hata K, Araki Y, et al. Increased expression of interleukin 17 in inflammatory bowel disease . Gut . 2003;52:65–70
  18. Middel P, Reich K, Polzien F, Blaschke V, Hemmerlein B, Herms J, et al. Interleukin 16 expression and phenotype of interleukin 16 producing cells in Crohn’s disease . Gut . 2001;49:795–803
  19. Mahida YR, Beltinger J, Marh S, Goke M, Gray T, Podolsky DK, et al. Adult human colonic subepithelial myofibroblasts express extracellular matrix proteins and cyclooxygenase-1 and -2 . Am J Physiol . 1997;273:G1341–G1348
  20. Okuno T, Andoh A, Bamba S, Araki Y, Fujiyama Y, Fujiyama M, et al. Interleukin-1β and tumor necrosis factor-α induce chemokine and matrix metalloproteinase gene expression in human colonic subepithelial myofibroblasts . Scand J Gastroenterol . 2002;37:317–324
  21. Bamba S , Andoh A , Yasui H , Makino J , Kim S , Fujiyama Y . Regulation of IL-11 expression in intestinal myofibroblasts (role of c-Jun AP-1- and MAPK-dependent pathways) . Am J Physiol Gastrointest Liver Physiol . 2003;285:G529–G538
  22. Andoh A , Fujiyama Y , Sumiyoshi K , Sakumoto H , Bamba T . Interleukin 4 acts as an inducer of decay-accelerating factor gene expression in human intestinal epithelial cells . Gastroenterology . 1996;111:911–918
  23. Strausberg RL , Feingold EA , Grouse LH , et al.   Generation and initial analysis of more than 15,000 full-length human and mouse cDNA sequences . Proc Natl Acad Sci U S A . 2002;99:16899–16903
  24. Xie MH, Aggarwal S, Ho WH, Foster J, Zhang Z, Stinson J, et al. Interleukin (IL)-22, a novel human cytokine that signals through the interferon receptor-related proteins CRF2-4 and IL-22R . J Biol Chem . 2000;275:31335–31339
  25. Moreau JF , Donaldson DD , Bennett F , Witek-Giannotti J , Clark SC , Wong GG . Leukaemia inhibitory factor is identical to the myeloid growth factor human interleukin for DA cells . Nature . 1988;336:690–692
  26. Chomczynski P , Sacchi N . Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction . Anal Biochem . 1987;162:156–159
  27. Shimada M, Andoh A, Hata K, Tasaki K, Araki Y, Fujiyama Y, et al. IL-6 secretion by human pancreatic periacinar myofibroblasts in response to inflammatory mediators . J Immunol . 2002;168:861–868
  28. Andoh A, Takaya H, Saotome T, Shimada M, Hata K, Araki Y, et al. Cytokine regulation of chemokine (IL-8, MCP-1, and RANTES) gene expression in human pancreatic periacinar myofibroblasts . Gastroenterology . 2000;119:211–219
  29. Dignam JD , Lebovitz RM , Roeder RG . Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei . Nucleic Acids Res . 1983;11:1475–1489
  30. Mukaida N , Shiroo M , Matsushima K . Genomic structure of the human monocyte-derived neutrophil chemotactic factor IL-8 . J Immunol . 1989;143:1366–1371
  31. Andoh A, Shimada M, Bamba S, Okuno T, Araki Y, Fujiyama Y, et al. Extracellular signal-regulated kinases 1 and 2 participate in interleukin-17 plus tumor necrosis factor-α-induced stabilization of interleukin-6 mRNA in human pancreatic myofibroblasts . Biochim Biophys Acta . 2002;1591:69–74
  32. Frederiksen CM, Aaboe M, Dyrskjot L, Laurberg S, Wolf H, Orntoft TF, et al. Technical evaluation of cDNA microarrays . APMIS Suppl . 2003;109:96–101
  33. Obara H, Takayanagi A, Hirahashi J, Tanaka K, Wakabayashi G, Matsumoto K, et al. Overexpression of truncated IκBα induces TNF-α-dependent apoptosis in human vascular smooth muscle cells . Arterioscler Thromb Vasc Biol . 2000;20:2198–2204
  34. Yasumoto H, Kim S, Zhan Y, Miyazaki H, Hoshiga M, Kaneda Y, et al. Dominant negative c-jun gene transfer inhibits vascular smooth muscle cell proliferation and neointimal hyperplasia in rats . Gene Ther . 2001;8:1682–1689
  35. Alessi DR , Cuenda A , Cohen P , Dudley DT , Saltiel AR . PD098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo . J Biol Chem . 1995;270:27489–27494
  36. Favata MF, Horiuchi KY, Manos EJ, Daulerio AJ, Stradley DA, Feeser WS, et al. Identification of a novel inhibitor of mitogen-activated protein kinase kinase . J Biol Chem . 1998;273:18623–18632
  37. Cuenda A, Rouse J, Doza YN, Meier R, Cohen P, Gallagher TF, et al. SB203580 is a specific inhibitor of a MAP kinase homologue, which is stimulated by cellular stresses and interleukin-1 . FEBS Lett . 1995;364:229–233
  38. Gorina R , Petegnief V , Chamorro A , Planas AM . AG490 prevents cell death after exposure of rat astrocytes to hydrogen peroxide or proinflammatory cytokines (involvement of the Jak2/STAT pathway) . J Neurochem . 2005;92:505–518
  39. Hata K, Andoh A, Shimada M, Fujino S, Bamba S, Araki Y, et al. IL-17 stimulates inflammatory responses via NF-κB and MAP kinase pathways in human colonic myofibroblasts . Am J Physiol Gastrointest Liver Physiol . 2002;282:G1035–G1044
  40. Fujino S, Andoh A, Bamba S, Ogawa A, Hata K, Araki Y, et al. Increased expression of interleukin 17 in inflammatory bowel disease . Gut . 2003;52:65–70
  41. Kuhn R , Lohler J , Rennick D , Rajewsky K , Muller W . Interleukin-10-deficient mice develop chronic enterocolitis . Cell . 1993;75:263–274
  42. Powell DW , Mifflin RC , Valentich JD , Crowe SE , Saada JI , West AB . Intestinal subepithelial myofibroblasts . Am J Physiol . 1999;277:C183–C201
  43. Li X, Massa PE, Hanidu A, Peet GW, Aro P, Savitt A, et al. IKKα, IKKβ, and NEMO/IKKγ are each required for the NF-κB-mediated inflammatory response program . J Biol Chem . 2002;277:45129–45140
  44. McKinley D , Wu Q , Yang-Feng T , Yang YC . Genomic sequence and chromosomal location of human interleukin-11 gene (IL11) . Genomics . 1992;13:814–819
  45. Yeh M, Gharavi NM, Choi J, Hsieh X, Reed E, Mouillesseaux KP, et al. Oxidized phospholipids increase interleukin 8 (IL-8) synthesis by pathway . J Biol Chem . 2004;279:30175–30181
  46. D’Isanto M , Vitiello M , Raieta K , Galdiero M , Galdiero M . Prolactin modulates IL-8 production induced by porins or LPS through different signaling mechanisms . Immunobiology . 2004;209:523–533
  47. Liao YC , Liang WG , Chen FW , Hsu JH , Yang JJ , Chang MS . IL-19 induces production of IL-6 and TNF-α and results in cell apoptosis through TNF-α . J Immunol . 2002;169:4288–4297

PII: S0016-5085(05)01359-4

doi: 10.1053/j.gastro.2005.06.071

Gastroenterology
Volume 129, Issue 3 , Pages 969-984 , September 2005

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