Reciprocal regulation of gastrointestinal homeostasis by SHP2 and STAT-mediated trefoil gene activation in gp130 mutant mice

Nature Medicine

Volumn 8, Issue 10, 2002, Pages 1089-1097

  Tebbutt, Niall C ^a   Giraud, Andrew S ^b   Inglese, Melissa ^a   Jenkins, Brendan ^a   Waring, Paul ^c   Clay, Fiona J ^a   Malki, Sina ^b   Alderman, Barbara M ^b   Grail, Dianne ^a   Hollande, Frédéric ^d   Heath, Joan K ^a   Ernst, Matthias ^a  

^a ROYAL MELBOURNE HOSPITAL   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c PETER MACCALLUM CANCER CENTRE   (Australia)

^d UNIV MONTPELLIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN GP 130; INTERLEUKIN 6; PHOSPHATASE; SRC HOMOLOGY TYROSINE PHOSPHATASE 2; STAT PROTEIN; STAT1 PROTEIN; STAT3 PROTEIN; TREFOIL PEPTIDE; UNCLASSIFIED DRUG;

ADENOMA; ADOLESCENT; ANIMAL TISSUE; ARTICLE; COLON MUCOSA; CONTROLLED STUDY; GASTROINTESTINAL TRACT; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HYPERPLASIA; MOUSE; MOUSE MUTANT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STOMACH TUMOR; WOUND HEALING IMPAIRMENT;

ADENOMA; ANIMALS; ANTIGENS, CD; CELL LINE; COLON; CYTOKINE RECEPTOR GP130; DIGESTIVE PHYSIOLOGY; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; GROWTH SUBSTANCES; HOMEOSTASIS; INTERLEUKIN-11; INTERLEUKIN-6; INTESTINAL MUCOSA; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE GLYCOPROTEINS; MICE; MICE, TRANSGENIC; MITOGEN-ACTIVATED PROTEIN KINASES; MUCINS; MUSCLE PROTEINS; NEUROPEPTIDES; PEPTIDES; PROTEIN-TYROSINE-PHOSPHATASE; PROTEINS; SIGNAL TRANSDUCTION; SPLEEN; STAT1 TRANSCRIPTION FACTOR; STOMACH; STOMACH NEOPLASMS; TRANS-ACTIVATORS; WOUND HEALING;

ANIMALIA; LOTUS;

EID: 0036796060     PISSN: 10788956     EISSN: None     Source Type: Journal    
DOI: 10.1038/nm763     Document Type: Article

References (43)

1. Nicola, N.A. Cytokine pleiotropy and redundancy: A view from the receptor. Stem Cells 12, Suppl. 1, 3-12; discussion 12-14 (1994).
2. Pawson, T. Protein modules and signaling networks. Nature 373, S73-S80 (199S).
3. Heinrich, P.C., Behrmann, I., Muller-Newen, G., Schaper, F. & Graeve, L. Interleukin-6-type cytokine signaling through the gp130/Jak/STAT pathway. Biochem. J. 334, 297-314 (1998).
4. Taga, T. & Kishimoto, T. Gp130 and the interleukin-6 family of cytokines. Annu. Rev. Immunol. 15, 797-819 (1997).
5. Stahl, N. et al. Choice of STATs and other substrates specified by modular tyrosine-based motifs in cytokine receptors. Science 267, 1349-1353 (1995).
6. Ohtani, T. et al. Dissection of signal cascades through gp130 in vivo: Reciprocal roles for STAT3 and SHP2-mediated signals in immune responses. Immunity 12, 95-105 (2000).
7. Giraud, A.W. Lessons from genetically engineered animal models. Trefoil peptides and EGF receptor/ligand transgenic mice. Am. J. Gastrointest. Liver Physiol. 278, G501-G506 (2000).
8. Taupin, D.R., Kinoshita, K. & Podolsky, D.K. Intestinal trefoil factor confers colonic epithelial resistance to apoptosis. Proc. Natl. Acad. Sci. USA 97, 799-804 (2000).
9. Podolsky, D.K. Mechanisms of regulatory peptide action in the gastrointestinal tract: Trefoil peptides. J. Gestroenterol. 35, Suppl. 12, 69-74 (2000).
10. Ramsay, A.J. et al. The role of interleukin-6 in mucosal IgA antibody responses in vivo. Science 264, 561-563 (1994).
11. Du, X. & Williams, D.A. Interleukin-11: Review of molecular, cell biology, and clinical use. Blood 89, 3897-3908 (1997).
12. Ernst, M. et al. Defective gp130-mediated STAT signaling results in degenerative joint disease, gastrointestinal ulceration and failure of uterine implantation. J. Exp. Med. 194, 189-203 (2001).
13. Lefebvre, O. et al. Gastric mucosa abnormalities and tumorigenesis in mice lacking the pS2 trefoil protein. Science 274, 259-262 (1996).
14. Mashimo, H., Wu, D.C., Podolsky, D.K. & Fishman, M.C. Impaired defense of intestinal mucosa in mice lacking intestinal trefoil factor. Science 274, 262-265 (1996).
15. Baumann, H., Gearing, D. & Ziegler, S.F. Signaling by the cytoplasmic domain of hematopoietin receptors involves two distinguishable mechanisms in hepatic cells. J. Biol. Chem. 269, 16297-16304 (1994).
16. Kopf, M. et al. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 368, 339-342 (1994).
17. Robb, L. at al. Infertility in female mice lacking the receptor for interleukin 11 is due to a defective uterine response to implantation. Nature Med. 4, 303-308 (1998).
18. Yoshida, K. et al. Targeted disruption of gp130, a common signal transducer for the interleukin 6 family of cytokines, leads to myocardial and hematological disorders. Proc. Natl. Acad. Sci. USA 93, 407-411 (1996).
19. Cooper, H.S., Murthy, S.N., Shah, R.S. & Sedergran, D.J. Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Lab. Invest. 69, 238-249 (1993).
20. Egger, B. et al. Keratinocyte growth factor ameliorates dextran sodium sulfate colitis in mice. Dig. Dis. Sci. 44, 836-844 (1999).
21. Sano, S. et al. Keratinocyte-specific ablation of Stat3 exhibits impaired skin remodeling, but does not affect skin morphogenesis. EMBO J. 18, 4657-4668 (1998).
22. Hollande, F. et al. HGF regulates tight junctions in a new nontumorigenic gastric epithelial cell line. Am. J. Physiol. Gestrointest. Liver Physiol. 280, G910-G918 (2001).
23. Atreya, R. et al. Blockade of interleukin 6 trans signaling suppresses T-cell resistance against apoptosis in chronic intestinal inflammation: Evidence in Crohn's disease and experimental colitis in vivo. Nature Med. 6, 583-588 (2000).
24. Taupin, D. et al. The trefoil gene family are coordinately expressed immediateearly genes: EGF receptor- and MAP kinase-dependent interregulation. J. Clin. Invest. 103, R31-R38 (1999).
25. Terada, T., Sakagami, R., Tabuchi, I. & Maeda, M. Characterization of the mouse TFF1 (pS2) gene promoter region. Biol. Pharm. Bull. 24, 135-139 (2001).
26. Ehret, G.M. et al. DNA binding specificity of different STAT proteins. Comparison of in vitro specificity with natural target sites. J. Biol. Chem. 276, 6675-6688 (2001).
27. Sands, B.E. et al. Molecular cloning of the rat intestinal trefoil factor gene: Characterization of an intestinal goblet cell-associated promoter. J. Biol. Chem. 270, 9353-9361 (1995).
28. Betz, U.A.K. et al. Postnatally induced inactivation of gp130 in mice results in neurological, cardiac, hematopoietic, immunological, hepatic, and pulmonary defects. J. Exp. Med. 188, 1955-1965 (1998).
29. Peters, M. et al. Extramedullary expression of hemopoietic progenitor cells in interleukin(IL-)-6-s-L-6R double transgenic mice. J. Exp. Med. 185, 755-766 (1997).
30. Hirota, H., Yoshida, K., Kishimoto, T. & Taga, T. Continuous activation of gp130, a signal-transducing receptor component for interleukin 6-related cytokines, causes myocardial hypertrophy in mice. Proc. Natl. Acad. Sci. USA 92, 4862-4866 (1995).
31. Suzuki, A. et al. CIS3/SOCS3/SSI3 plays a negative regulatory role in STAT3 activation and intestinal inflammation. J. Exp. Med. 193, 471-482 (2001).
32. Bossenmeyer-Pourie, C. et al. The trefoil factor 1 participates in gastrointestinal cell differentiation by delaying G1-S phase transition and reducing apoptosis. J. Cell Biol. 157, 761-770 (2002).
33. Park, W.S. et al. Somatic mutations of the trefoil factor family 1 gene in gastric cancer. Gastroenterology 119, 691-698 (2000).
34. Takagi, H., Jhappan, C., Sharp, R. & Merlino, G. Hypertrophic gastropathy resempling Menetrier's disease in transgenic mice overexpressing transforming growth factor alpha in the stomach. J Clin Invest 90, 1161-1167 (1992).
35. Boivin, P.G., Molina, J.R., Ormsby, I., Stemmermann, G. & Doetschman, T. Gastric lesions in transforming growth factor β-1 heterozygous mice. Lab. Invest. 74, 513-518 (1996).
36. Kamizono, S. et al. The SOCS box of SOCS-1 accelerates ubiquitin-dependent proteolysis of TEL-JAK2. J. Biol. Chem. 276, 9353-9361 (2001).
37. Schmitz, J., Weissenbach, M., Haan, S., Heinrich, P.C. & Schaper, F. SOCS3 exerts its inhibitory function on interleukin-6 signal transduction through the SHP2 recruitment site of gp130. J. Biol. Chem. 275, 12848-12856 (2000).
38. Nicholson, S.E. et al. Suppressor of cytokine signaling-3 preferentially binds to the SHP-2-binding site on the shared cytokine receptor subunit gp130. Proc. Natl. Acad. Sci. USA 97, 6493-6498 (2000).
39. Kim, H. & Baumann, H. Dual signaling role of the protein tyrosine phosphatase SHP-2 in regulating expression of acute-phase plasma proteins by interleukin-6 cytokine receptors in hepatic cells. Mol. Cell. Biol. 19, 5326-5338 (1999).
40. Srivatsa, G. et al. Biliary epithelial trefoil peptide expression is increased in biliary diseases. Histopathology 40, 261-268 (2002).
41. Ulaganathan, M., Familari, M., Yeomans, N.D., Giraud, A.S. & Cook, G.A. The spatio-temporal expression of TFF1 following severe gastric ulceration implicates it in the late stage repair process. J. Gastroenterol. Hepatol. 16, 506-512 (2001).
42. Taupin, D., Pang, K.C., Green, S.P. & Giraud, A.S. The trefoil peptides spasmolytic polypeptide and intestinal trefoil factor are major secretary products of the rat gut. Peptides 16, 1001-1005 (1995).
43. Ernst, M., Novak, U., Nicholson, S.E., Layton, J.E. & Dunn, A.R. The carboxyl-terminal domains of gp130-related cytokine receptors are necessary for suppressing embryonic stem cell differentiation: Involvement of STAT3. J. Biol. Chem. 274, 9729-9737 (1999).