Gastroenterology
Volume 139, Issue 2 , Pages 530-541 , August 2010

Paired Immunoglobulin-Like Receptor B (PIR-B) Negatively Regulates Macrophage Activation in Experimental Colitis

  • Ariel Munitz

      Affiliations

    • Division of Allergy and Immunology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio
    • Department of Microbiology and Clinical Immunology, Sackler Faculty of Medicine, Tel Aviv University, Ramat Aviv, Israel
  • ,
  • Eric T. Cole

      Affiliations

    • Division of Allergy and Immunology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio
  • ,
  • Amanda Beichler

      Affiliations

    • Division of Allergy and Immunology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio
  • ,
  • Katherine Groschwitz

      Affiliations

    • Division of Allergy and Immunology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio
  • ,
  • Richard Ahrens

      Affiliations

    • Division of Allergy and Immunology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio
  • ,
  • Kris Steinbrecher

      Affiliations

    • Division of Gastroenterology, Hepatology, and Nutrition, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio
  • ,
  • Tara Willson

      Affiliations

    • Division of Gastroenterology, Hepatology, and Nutrition, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio
  • ,
  • Xiaonan Han

      Affiliations

    • Division of Gastroenterology, Hepatology, and Nutrition, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio
  • ,
  • Lee Denson

      Affiliations

    • Division of Gastroenterology, Hepatology, and Nutrition, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio
  • ,
  • Marc E. Rothenberg

      Affiliations

    • Division of Allergy and Immunology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio
  • ,
  • Simon P. Hogan

      Affiliations

    • Division of Allergy and Immunology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio
    • Corresponding Author InformationReprint requests Address requests for reprints to: Simon P. Hogan, PhD, Division of Allergy and Immunology, Cincinnati Children's Hospital Medical Center, 3333 Burnet Avenue, MLC 7028, Cincinnati, Ohio 45229. fax: (513) 636-3310

Received 11 June 2009 ,Accepted 7 April 2010.

References 

  1. Bonen DK, Cho JH. The genetics of inflammatory bowel disease. Gastroenterology. 2003;124:521–536
  2. Marks DJ, Segal AW. Innate immunity in inflammatory bowel disease: a disease hypothesis. J Pathol. 2008;214:260–266
  3. Mahida YR, Wu KC, Jewell DP. Respiratory burst activity of intestinal macrophages in normal and inflammatory bowel disease. Gut. 1989;30:1362–1370
  4. Mahida YR, Patel S, Gionchetti P, et al. Macrophage subpopulations in lamina propria of normal and inflamed colon and terminal ileum. Gut. 1989;30:826–834
  5. Murch SH, Braegger CP, Walker-Smith JA, et al. Location of tumour necrosis factor alpha by immunohistochemistry in chronic inflammatory bowel disease. Gut. 1993;34:1705–1709
  6. Watanabe N, Ikuta K, Okazaki K, et al. Elimination of local macrophages in intestine prevents chronic colitis in interleukin-10-deficient mice. Dig Dis Sci. 2003;48:408–414
  7. Marshall D, Cameron J, Lightwood D, et al. Blockade of colony stimulating factor-1 (CSF-I) leads to inhibition of DSS-induced colitis. Inflamm Bowel Dis. 2007;13:219–224
  8. Ghia JE, Galeazzi F, Ford DC, et al. Role of M-CSF-dependent macrophages in colitis is driven by the nature of the inflammatory stimulus. Am J Physiol Gastrointest Liver Physiol. 2008;294:G770–G777
  9. Takai T. A novel recognition system for MHC class I molecules constituted by PIR. Adv Immunol. 2005;88:161–192
  10. Kubagawa H, Chen CC, Ho LH, et al. Biochemical nature and cellular distribution of the paired immunoglobulin-like receptors, PIR-A and PIR-B. J Exp Med. 1999;189:309–318
  11. Kubagawa H, Burrows PD, Cooper MD. A novel pair of immunoglobulin-like receptors expressed by B cells and myeloid cells. Proc Natl Acad Sci U S A. 1997;94:5261–5266
  12. Blery M, Kubagawa H, Chen CC, et al. The paired Ig-like receptor PIR-B is an inhibitory receptor that recruits the protein-tyrosine phosphatase SHP-1. Proc Natl Acad Sci U S A. 1998;95:2446–2451
  13. Torii I, Oka S, Hotomi M, et al. PIR-B-deficient mice are susceptible to Salmonella infection. J Immunol. 2008;181:4229–4239
  14. Nakayama M, Underhill DM, Petersen TW, et al. Paired Ig-like receptors bind to bacteria and shape TLR-mediated cytokine production. J Immunol. 2007;178:4250–4259
  15. Ujike A, Takeda K, Nakamura A, et al. Impaired dendritic cell maturation and increased T(H)2 responses in PIR-B(−/−) mice. Nat Immunol. 2002;3:542–548
  16. Ahrens R, Waddell A, Seidu L, et al. Intestinal macrophage/epithelial cell-derived CCL11/eotaxin-1 mediates eosinophil recruitment and function in pediatric ulcerative colitis. J Immunol. 2008;181:7390–7399
  17. Munitz A, Waddell A, Seidu L, et al. Resistin-like molecule alpha enhances myeloid cell activation and promotes colitis. J Allergy Clin Immunol. 2008;122:1200–1207e1
  18. Krutzik PO, Nolan GP. Intracellular phospho-protein staining techniques for flow cytometry: monitoring single cell signaling events. Cytometry A. 2003;55:61–70
  19. Munitz A, McBride ML, Bernstein JS, et al. A dual activation and inhibition role for the paired immunoglobulin-like receptor B in eosinophils. Blood. 2008;111:5694–5703
  20. Strober W, Fuss IJ, Blumberg RS. The immunology of mucosal models of inflammation. Annu Rev Immunol. 2002;20:495–549
  21. O'Neill LA. When signaling pathways collide: positive and negative regulation of Toll-like receptor signal transduction. Immunity. 2008;29:12–20
  22. Gao M, Labuda T, Xia Y, et al. Jun turnover is controlled through JNK-dependent phosphorylation of the E3 ligase Itch. Science. 2004;306:271–275
  23. Maeda A, Kurosaki M, Ono M, et al. Requirement of SH2-containing protein tyrosine phosphatases SHP-1 and SHP-2 for paired immunoglobulin-like receptor B (PIR-B)-mediated inhibitory signal. J Exp Med. 1998;187:1355–1360
  24. Ho LH, Uehara T, Chen CC, et al. Constitutive tyrosine phosphorylation of the inhibitory paired Ig-like receptor PIR-B. Proc Natl Acad Sci U S A. 1999;96:15086–15090
  25. Naftalin R. Alterations in colonic barrier function caused by a low sodium diet or ionizing radiation. J Environ Pathol Toxicol Oncol. 2004;23:79–97
  26. Takai T, Ono M. Activating and inhibitory nature of the murine paired immunoglobulin-like receptor family. Immunol Rev. 2001;181:215–222
  27. Takai T. Paired immunoglobulin-like receptors and their MHC class I recognition. Immunology. 2005;115:433–440
  28. Hayami K, Fukuta D, Nishikawa Y, et al. Molecular cloning of a novel murine cell-surface glycoprotein homologous to killer cell inhibitory receptors. J Biol Chem. 1997;272:7320–7327
  29. Pereira S, Zhang H, Takai T, et al. The inhibitory receptor PIR-B negatively regulates neutrophil and macrophage integrin signaling. J Immunol. 2004;173:5757–5765
  30. Morohoshi Y, Matsuoka K, Chinen H, et al. Inhibition of neutrophil elastase prevents the development of murine dextran sulfate sodium-induced colitis. J Gastroenterol. 2006;41:318–324
  31. Krieglstein CF, Cerwinka WH, Laroux FS, et al. Regulation of murine intestinal inflammation by reactive metabolites of oxygen and nitrogen: divergent roles of superoxide and nitric oxide. J Exp Med. 2001;194:1207–1218
  32. Takeda K, Clausen BE, Kaisho T, et al. Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of STAT3 in macrophages and neutrophils. Immunity. 1999;10:39–49
  33. Strober W, Fuss I, Mannon P. The fundamental basis of inflammatory bowel disease. J Clin Invest. 2007;117:514–521
  34. Waetzig GH, Seegert D, Rosenstiel P, et al. p38 mitogen-activated protein kinase is activated and linked with TNF-alpha signaling in inflammatory bowel disease. J Immunol. 2002;168:5342–5351
  35. Hollenbach E, Neumann M, Vieth M, et al. Inhibition of p38 MAP kinase- and RICK/NF-kappaB-signaling suppresses inflammatory bowel disease. FASEB J. 2004;18:1550–1552
  36. Rui Y, Liu X, Li N, et al. PECAM-1 ligation negatively regulates TLR4 signaling in macrophages. J Immunol. 2007;179:7344–7351
  37. Chong ZZ, Maiese K. The Src homology 2 domain tyrosine phosphatases SHP-1 and SHP-2: diversified control of cell growth, inflammation and injury. Histol Histopathol. 2007;22:1251–1267
  38. Palen DI, Belmadani S, Lucchesi PA, et al. Role of SHP-1, Kv.1.2, and cGMP in nitric oxide-induced ERK1/2 MAP kinase dephosphorylation in rat vascular smooth muscle cells. Cardiovasc Res. 2005;68:268–277
  39. Cai J, Jiang WG, Ahmed A, et al. Vascular endothelial growth factor-induced endothelial cell proliferation is regulated by interaction between VEGFR-2, SH-PTP1 and eNOS. Microvasc Res. 2006;71:20–31
  40. Kong XN, Yan HX, Chen L, et al. LPS-induced down-regulation of signal regulatory protein α contributes to innate immune activation in macrophages. J Exp Med. 2007;204:2719–2731
  41. Huynh OA, Hampartzoumian T, Arm JP, et al. Down-regulation of leucocyte immunoglobulin-like receptor expression in the synovium of rheumatoid arthritis patients after treatment with disease-modifying anti-rheumatic drugs. Rheumatology (Oxford). 2007;46:742–751
  42. Tedla N, Gibson K, McNeil HP, et al. The co-expression of activating and inhibitory leukocyte immunoglobulin-like receptors in rheumatoid synovium. Am J Pathol. 2002;160:425–431

 Conflicts of interest The authors disclose no conflicts.

 Funding Supported by an American Heart Association research fellowship (to A.M.), National Institutes of Health grants P01 HL-076383 and R01 AI057803 (to M.E.R.), the CURED and Buckeye Foundations (to M.E.R.), the Food Allergy Project (to M.E.R.), the Crohn's and Colitis Foundation of America Career Development Award (to S.P.H.), and National Institutes of Health grant R01 AI073553-01 (to S.P.H.).

PII: S0016-5085(10)00552-4

doi: 10.1053/j.gastro.2010.04.006

Gastroenterology
Volume 139, Issue 2 , Pages 530-541 , August 2010