41
Views
32
CrossRef citations to date
0
Altmetric
Article

Epithelial Tyrosine Phosphatase SHP-2 Protects against Intestinal Inflammation in Mice

, , , , , , , & show all
Pages 2275-2284 | Received 10 Jan 2013, Accepted 20 Mar 2013, Published online: 20 Mar 2023

REFERENCES

  • Kaser A, Zeissig S, Blumberg RS. 2010. Inflammatory bowel disease. Annu. Rev. Immunol. 28:573–621.
  • Nell S, Suerbaum S, Josenhans C. 2010. The impact of the microbiota on the pathogenesis of IBD: lessons from mouse infection models. Nat. Rev. Microbiol. 8:564–577.
  • McGuckin MA, Eri R, Simms LA, Florin TH, Radford-Smith G. 2009. Intestinal barrier dysfunction in inflammatory bowel diseases. Inflamm. Bowel Dis. 15:100–113.
  • Hermiston ML, Gordon JI. 1995. Inflammatory bowel disease and adenomas in mice expressing a dominant negative N-cadherin. Science 270:1203–1207.
  • Van der Sluis M, De Koning BA, De Bruijn AC, Velcich A, Meijerink JP, Van Goudoever JB, Buller HA, Dekker J, Van Seuningen I, Renes IB, Einerhand AW. 2006. Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology 131:117–129.
  • Nenci A, Becker C, Wullaert A, Gareus R, van Loo G, Danese S, Huth M, Nikolaev A, Neufert C, Madison B, Gumucio D, Neurath MF, Pasparakis M. 2007. Epithelial NEMO links innate immunity to chronic intestinal inflammation. Nature 446:557–561.
  • Glas J, Wagner J, Seiderer J, Olszak T, Wetzke M, Beigel F, Tillack C, Stallhofer J, Friedrich M, Steib C, Goke B, Ochsenkuhn T, Karbalai N, Diegelmann J, Czamara D, Brand S. 2012. PTPN2 gene variants are associated with susceptibility to both Crohn's disease and ulcerative colitis supporting a common genetic disease background. PLoS One 7:e33682. doi:10.1371/journal.pone.0033682.
  • Hassan SW, Doody KM, Hardy S, Uetani N, Cournoyer D, Tremblay ML. 2010. Increased susceptibility to dextran sulfate sodium induced colitis in the T cell protein tyrosine phosphatase heterozygous mouse. PLoS One 5:e8868. doi:10.1371/journal.pone.0008868.
  • Narumi Y, Isomoto H, Shiota M, Sato K, Kondo S, Machida H, Yanagihara K, Mizuta Y, Kohno S, Tsukamoto K. 2009. Polymorphisms of PTPN11 coding SHP-2 as biomarkers for ulcerative colitis susceptibility in the Japanese population. J. Clin. Immunol. 29:303–310.
  • Wellcome Trust Case Control Consortium. 2007. Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 447:661–678.
  • Bard-Chapeau EA, Li S, Ding J, Zhang SS, Zhu HH, Princen F, Fang DD, Han T, Bailly-Maitre B, Poli V, Varki NM, Wang H, Feng GS. 2011. Ptpn11/Shp2 acts as a tumor suppressor in hepatocellular carcinogenesis. Cancer Cell 19:629–639.
  • Chong ZZ, Maiese K. 2007. The Src homology 2 domain tyrosine phosphatases SHP-1 and SHP-2: diversified control of cell growth, inflammation, and injury. Histol. Histopathol. 22:1251–1267.
  • Bentires-Alj M, Paez JG, David FS, Keilhack H, Halmos B, Naoki K, Maris JM, Richardson A, Bardelli A, Sugarbaker DJ, Richards WG, Du J, Girard L, Minna JD, Loh ML, Fisher DE, Velculescu VE, Vogelstein B, Meyerson M, Sellers WR, Neel BG. 2004. Activating mutations of the Noonan syndrome-associated SHP2/PTPN11 gene in human solid tumors and adult acute myelogenous leukemia. Cancer Res. 64:8816–8820.
  • Zhang EE, Chapeau E, Hagihara K, Feng GS. 2004. Neuronal Shp2 tyrosine phosphatase controls energy balance and metabolism. Proc. Natl. Acad. Sci. U. S. A. 101:16064–16069.
  • Madison BB, Dunbar L, Qiao XT, Braunstein K, Braunstein E, Gumucio DL. 2002. Cis elements of the villin gene control expression in restricted domains of the vertical (crypt) and horizontal (duodenum, cecum) axes of the intestine. J. Biol. Chem. 277:33275–33283.
  • Langlois MJ, Roy SA, Auclair BA, Jones C, Boudreau F, Carrier JC, Rivard N, Perreault N. 2009. Epithelial phosphatase and tensin homolog regulates intestinal architecture and secretory cell commitment and acts as a modifier gene in neoplasia. FASEB J. 23:1835–1844.
  • Lee CS, Perreault N, Brestelli JE, Kaestner KH. 2002. Neurogenin 3 is essential for the proper specification of gastric enteroendocrine cells and the maintenance of gastric epithelial cell identity. Genes Dev. 16:1488–1497.
  • Cooper HS, Murthy SN, Shah RS, Sedergran DJ. 1993. Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Lab. Invest. 69:238–249.
  • Boudreau F, Lussier CR, Mongrain S, Darsigny M, Drouin JL, Doyon G, Suh ER, Beaulieu JF, Rivard N, Perreault N. 2007. Loss of cathepsin L activity promotes claudin-1 overexpression and intestinal neoplasia. FASEB J. 21:3853–3865.
  • Lemieux E, Bergeron S, Durand V, Asselin C, Saucier C, Rivard N. 2009. Constitutively active MEK1 is sufficient to induce epithelial-to-mesenchymal transition in intestinal epithelial cells and to promote tumor invasion and metastasis. Int. J. Cancer 125:1575–1586.
  • Garneau H, Paquin MC, Carrier JC, Rivard N. 2009. E2F4 expression is required for cell cycle progression of normal intestinal crypt cells and colorectal cancer cells. J. Cell Physiol. 221:350–358.
  • Lemieux E, Boucher MJ, Mongrain S, Boudreau F, Asselin C, Rivard N. 2011. Constitutive activation of the MEK/ERK pathway inhibits intestinal epithelial cell differentiation. Am. J. Physiol. Gastrointest. Liver Physiol. 301:G719–G730.
  • Gao N, Kaestner KH. 2010. Cdx2 regulates endo-lysosomal function and epithelial cell polarity. Genes Dev. 24:1295–1305.
  • Dance M, Montagner A, Salles JP, Yart A, Raynal P. 2008. The molecular functions of Shp2 in the Ras/Mitogen-activated protein kinase (ERK1/2) pathway. Cell Signal. 20:453–459.
  • You M, Flick LM, Yu D, Feng GS. 2001. Modulation of the nuclear factor kappa B pathway by Shp-2 tyrosine phosphatase in mediating the induction of interleukin (IL)-6 by IL-1 or tumor necrosis factor. J. Exp. Med. 193:101–110.
  • Li D, Mrsny RJ. 2000. Oncogenic Raf-1 disrupts epithelial tight junctions via downregulation of occludin. J. Cell Biol. 148:791–800.
  • Chen Y, Lu Q, Schneeberger EE, Goodenough DA. 2000. Restoration of tight junction structure and barrier function by down-regulation of the mitogen-activated protein kinase pathway in ras-transformed Madin-Darby canine kidney cells. Mol. Biol. Cell 11:849–862.
  • Basuroy S, Seth A, Elias B, Naren AP, Rao R. 2006. MAPK interacts with occludin and mediates EGF-induced prevention of tight junction disruption by hydrogen peroxide. Biochem. J. 393:69–77.
  • Gonzalez-Mariscal L, Tapia R, Chamorro D. 2008. Crosstalk of tight junction components with signaling pathways. Biochim. Biophys. Acta 1778:729–756.
  • Petecchia L, Sabatini F, Usai C, Caci E, Varesio L, Rossi GA. 2012. Cytokines induce tight junction disassembly in airway cells via an EGFR-dependent MAPK/ERK1/2-pathway. Lab. Invest. 92:1140–1148.
  • Dai C, Zhao DH, Jiang M. 2012. VSL#3 probiotics regulate the intestinal epithelial barrier in vivo and in vitro via the p38 and ERK signaling pathways. Int. J. Mol. Med. 29:202–208.
  • Sellon RK, Tonkonogy S, Schultz M, Dieleman LA, Grenther W, Balish E, Rennick DM, Sartor RB. 1998. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect. Immun. 66:5224–5231.
  • Hall JA, Bouladoux N, Sun CM, Wohlfert EA, Blank RB, Zhu Q, Grigg ME, Berzofsky JA, Belkaid Y. 2008. Commensal DNA limits regulatory T cell conversion and is a natural adjuvant of intestinal immune responses. Immunity 29:637–649.
  • Papadakis KA, Targan SR. 2000. Role of cytokines in the pathogenesis of inflammatory bowel disease. Annu. Rev. Med. 51:289–298.
  • Dvorak AM, Dickersin GR. 1980. Crohn's disease: transmission electron microscopic studies. I. Barrier function. Possible changes related to alterations of cell coat, mucous coat, epithelial cells, and Paneth cells. Hum. Pathol. 11:561–571.
  • Tytgat KM, van der Wal JW, Einerhand AW, Buller HA, Dekker J. 1996. Quantitative analysis of MUC2 synthesis in ulcerative colitis. Biochem. Biophys. Res. Commun. 224:397–405.
  • Jass JR, Walsh MD. 2001. Altered mucin expression in the gastrointestinal tract: a review. J. Cell Mol. Med. 5:327–351.
  • Lameris AL, Huybers S, Kaukinen K, Makela TH, Bindels RJ, Hoenderop JG, Nevalainen PI. 2013. Expression profiling of claudins in the human gastrointestinal tract in health and during inflammatory bowel disease. Scand. J. Gastroenterol. 48:58–69.
  • Holmes JL, Van Itallie CM, Rasmussen JE, Anderson JM. 2006. Claudin profiling in the mouse during postnatal intestinal development and along the gastrointestinal tract reveals complex expression patterns. Gene Expr. Patterns 6:581–588.
  • Koval M. 2006. Claudins—key pieces in the tight junction puzzle. Cell Commun. Adhes. 13:127–138.
  • Shen L. 2012. Tight junctions on the move: molecular mechanisms for epithelial barrier regulation. Ann. N. Y. Acad. Sci. 1258:9–18.
  • Collares-Buzato CB, Jepson MA, Simmons NL, Hirst BH. 1998. Increased tyrosine phosphorylation causes redistribution of adherens junction and tight junction proteins and perturbs paracellular barrier function in MDCK epithelia. Eur. J. Cell Biol. 76:85–92.
  • Staddon JM, Herrenknecht K, Smales C, Rubin LL. 1995. Evidence that tyrosine phosphorylation may increase tight junction permeability. J. Cell Sci. 108:609–619.
  • Araki T, Nawa H, Neel BG. 2003. Tyrosyl phosphorylation of Shp2 is required for normal ERK activation in response to some, but not all, growth factors. J. Biol. Chem. 278:41677–41684.
  • Boucher MJ, Jean D, Vezina A, Rivard N. 2004. Dual role of MEK/ERK signaling in senescence and transformation of intestinal epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 286:G736–G746.
  • Smith JM, Johanesen PA, Wendt MK, Binion DG, Dwinell MB. 2005. CXCL12 activation of CXCR4 regulates mucosal host defense through stimulation of epithelial cell migration and promotion of intestinal barrier integrity. Am. J. Physiol. Gastrointest. Liver Physiol. 288:G316–G326.
  • Qu CK. 2002. Role of the SHP-2 tyrosine phosphatase in cytokine-induced signaling and cellular response. Biochim. Biophys. Acta 1592:297–301.
  • You M, Yu DH, Feng GS. 1999. Shp-2 tyrosine phosphatase functions as a negative regulator of the interferon-stimulated Jak/STAT pathway. Mol. Cell. Biol. 19:2416–2424.
  • Lehmann U, Schmitz J, Weissenbach M, Sobota RM, Hortner M, Friederichs K, Behrmann I, Tsiaris W, Sasaki A, Schneider-Mergener J, Yoshimura A, Neel BG, Heinrich PC, Schaper F. 2003. SHP2 and SOCS3 contribute to Tyr-759-dependent attenuation of interleukin-6 signaling through gp130. J. Biol. Chem. 278:661–671.
  • Tebbutt NC, Giraud AS, Inglese M, Jenkins B, Waring P, Clay FJ, Malki S, Alderman BM, Grail D, Hollande F, Heath JK, Ernst M. 2002. Reciprocal regulation of gastrointestinal homeostasis by SHP2 and STAT-mediated trefoil gene activation in gp130 mutant mice. Nat. Med. 8:1089–1097.
  • Grivennikov S, Karin E, Terzic J, Mucida D, Yu GY, Vallabhapurapu S, Scheller J, Rose-John S, Cheroutre H, Eckmann L, Karin M. 2009. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell 15:103–113.
  • Pickert G, Neufert C, Leppkes M, Zheng Y, Wittkopf N, Warntjen M, Lehr HA, Hirth S, Weigmann B, Wirtz S, Ouyang W, Neurath MF, Becker C. 2009. STAT3 links IL-22 signaling in intestinal epithelial cells to mucosal wound healing. J. Exp. Med. 206:1465–1472.
  • Wang K, Yuan CP, Wang W, Yang ZQ, Cui W, Mu LZ, Yue ZP, Yin XL, Hu ZM, Liu JX. 2010. Expression of interleukin 6 in brain and colon of rats with TNBS-induced colitis. World J. Gastroenterol. 16:2252–2259.
  • Suzuki A, Hanada T, Mitsuyama K, Yoshida T, Kamizono S, Hoshino T, Kubo M, Yamashita A, Okabe M, Takeda K, Akira S, Matsumoto S, Toyonaga A, Sata M, Yoshimura A. 2001. CIS3/SOCS3/SSI3 plays a negative regulatory role in STAT3 activation and intestinal inflammation. J. Exp. Med. 193:471–481.
  • Han X, Sosnowska D, Bonkowski EL, Denson LA. 2005. Growth hormone inhibits signal transducer and activator of transcription 3 activation and reduces disease activity in murine colitis. Gastroenterology 129:185–203.
  • Wullaert A, Bonnet MC, Pasparakis M. 2011. NF-kappaB in the regulation of epithelial homeostasis and inflammation. Cell Res. 21:146–158.
  • Kong XN, Yan HX, Chen L, Dong LW, Yang W, Liu Q, Yu LX, Huang DD, Liu SQ, Liu H, Wu MC, Wang HY. 2007. LPS-induced down-regulation of signal regulatory protein {alpha} contributes to innate immune activation in macrophages. J. Exp. Med. 204:2719–2731.
  • Fusunyan RD, Nanthakumar NN, Baldeon ME, Walker WA. 2001. Evidence for an innate immune response in the immature human intestine: Toll-like receptors on fetal enterocytes. Pediatr. Res. 49:589–593.
  • Sartor RB. 2008. Microbial influences in inflammatory bowel diseases. Gastroenterology 134:577–594.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.