Interferon-γ Regulates Intestinal Epithelial Homeostasis through Converging β-Catenin Signaling Pathways

Immunity

Volumn 32, Issue 3, 2010, Pages 392-402

  Nava, Porfirio ^a   Koch, Stefan ^a   Laukoetter, Mike G ^a,b   Lee, Winston Y ^a   Kolegraff, Keli ^a   Capaldo, Christopher T ^a   Beeman, Neal ^a   Addis, Caroline ^a   Gerner Smidt, Kirsten ^a   Neumaier, Irmgard ^c   Skerra, Arne ^c   Li, Linheng ^d   Parkos, Charles A ^a   Nusrat, Asma ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

CELLIMMUNO; MOLIMMUNO

Indexed keywords

BETA CATENIN; CYTOKINE; DICKKOPF 1 PROTEIN; GAMMA INTERFERON; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 6; TUMOR NECROSIS FACTOR ALPHA; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; EPITHELIUM CELL; HOMEOSTASIS; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANIMALS; APOPTOSIS; BETA CATENIN; CELL LINE; CELL PROLIFERATION; COLITIS; EPITHELIAL CELLS; HOMEOSTASIS; INTERFERON-GAMMA; INTESTINES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 77949937466     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2010.03.001     Document Type: Article

References (56)

1. Barker N., Ridgway R.A., van Es J.H., van de Wetering M., Begthel H., van den Born M., Danenberg E., Clarke A.R., Sansom O.J., Clevers H. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 2009, 457:608-611.
2. Bruewer M., Samarin S., Nusrat A. Inflammatory bowel disease and the apical junctional complex. Ann. N Y Acad. Sci. 2006, 1072:242-252.
3. Byrne C., Tainsky M., Fuchs E. Programming gene expression in developing epidermis. Development 1994, 120:2369-2383.
4. Capaldo C.T., Nusrat A. Cytokine regulation of tight junctions. Biochim. Biophys. Acta 2009, 1788:864-871.
5. Chan C.W., Crafton E., Fan H.N., Flook J., Yoshimura K., Skarica M., Brockstedt D., Dubensky T.W., Stins M.F., Lanier L.L., et al. Interferon-producing killer dendritic cells provide a link between innate and adaptive immunity. Nat. Med. 2006, 12:207-213.
6. Cooper H.S., Murthy S.N., Shah R.S., Sedergran D.J. Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Lab. Invest. 1993, 69:238-249.
7. Crosnier C., Stamataki D., Lewis J. Organizing cell renewal in the intestine: Stem cells, signals and combinatorial control. Nat. Rev. Genet. 2006, 7:349-359.
8. de Lau W., Barker N., Clevers H. WNT signaling in the normal intestine and colorectal cancer. Front. Biosci. 2007, 12:471-491.
9. Diarra D., Stolina M., Polzer K., Zwerina J., Ominsky M.S., Dwyer D., Korb A., Smolen J., Hoffmann M., Scheinecker C., et al. Dickkopf-1 is a master regulator of joint remodeling. Nat. Med. 2007, 13:156-163.
10. Dieleman L.A., Palmen M.J., Akol H., Bloemena E., Peña A.S., Meuwissen S.G., Van Rees E.P. Chronic experimental colitis induced by dextran sulphate sodium (DSS) is characterized by Th1 and Th2 cytokines. Clin. Exp. Immunol. 1998, 114:385-391.
11. Feagins L.A., Souza R.F., Spechler S.J. Carcinogenesis in IBD: Potential targets for the prevention of colorectal cancer. Nat Rev Gastroenterol Hepatol 2009, 6:297-305.
12. Fish S.M., Proujansky R., Reenstra W.W. Synergistic effects of interferon gamma and tumour necrosis factor alpha on T84 cell function. Gut 1999, 45:191-198.
13. Ganster R.W., Guo Z., Shao L., Geller D.A. Differential effects of TNF-alpha and IFN-gamma on gene transcription mediated by NF-kappaB-Stat1 interactions. J. Interferon Cytokine Res. 2005, 25:707-719.
14. Gollob J.A., Sciambi C.J., Huang Z., Dressman H.K. Gene expression changes and signaling events associated with the direct antimelanoma effect of IFN-gamma. Cancer Res. 2005, 65:8869-8877.
15. Grivennikov S., Karin E., Terzic J., Mucida D., Yu G.Y., Vallabhapurapu S., Scheller J., Rose-John S., Cheroutre H., Eckmann L., Karin M. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell 2009, 15:103-113.
16. Günzel D., Florian P., Richter J.F., Troeger H., Schulzke J.D., Fromm M., Gitter A.H. Restitution of single-cell defects in the mouse colon epithelium differs from that of cultured cells. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006, 290:R1496-R1507.
17. He X.C., Yin T., Grindley J.C., Tian Q., Sato T., Tao W.A., Dirisina R., Porter-Westpfahl K.S., Hembree M., Johnson T., et al. PTEN-deficient intestinal stem cells initiate intestinal polyposis. Nat. Genet. 2007, 39:189-198.
18. Ito R., Shin-Ya M., Kishida T., Urano A., Takada R., Sakagami J., Imanishi J., Kita M., Ueda Y., Iwakura Y., et al. Interferon-gamma is causatively involved in experimental inflammatory bowel disease in mice. Clin. Exp. Immunol. 2006, 146:330-338.
19. Kaiser G.C., Polk D.B. Tumor necrosis factor alpha regulates proliferation in a mouse intestinal cell line. Gastroenterology 1997, 112:1231-1240.
20. Kaiser G.C., Yan F., Polk D.B. Conversion of TNF alpha from antiproliferative to proliferative ligand in mouse intestinal epithelial cells by regulating mitogen-activated protein kinase. Exp. Cell Res. 1999, 249:349-358.
21. Kaur S., Sassano A., Dolniak B., Joshi S., Majchrzak-Kita B., Baker D.P., Hay N., Fish E.N., Platanias L.C. Role of the Akt pathway in mRNA translation of interferon-stimulated genes. Proc. Natl. Acad. Sci. USA 2008, 105:4808-4813.
22. Kaur S., Sassano A., Joseph A.M., Majchrzak-Kita B., Eklund E.A., Verma A., Brachmann S.M., Fish E.N., Platanias L.C. Dual regulatory roles of phosphatidylinositol 3-kinase in IFN signaling. J. Immunol. 2008, 181:7316-7323.
23. Koch S., Capaldo C.T., Samarin S., Nava P., Neumaier I., Skerra A., Sacks D.B., Parkos C.A., Nusrat A. Dkk-1 inhibits intestinal epithelial cell migration by attenuating directional polarization of leading edge cells. Mol. Biol. Cell 2009, 20:4816-4825.
24. Kuhnert F., Davis C.R., Wang H.T., Chu P., Lee M., Yuan J., Nusse R., Kuo C.J. Essential requirement for Wnt signaling in proliferation of adult small intestine and colon revealed by adenoviral expression of Dickkopf-1. Proc. Natl. Acad. Sci. USA 2004, 101:266-271.
25. Lekmine F., Sassano A., Uddin S., Smith J., Majchrzak B., Brachmann S.M., Hay N., Fish E.N., Platanias L.C. Interferon-gamma engages the p70 S6 kinase to regulate phosphorylation of the 40S S6 ribosomal protein. Exp. Cell Res. 2004, 295:173-182.
26. Logan C.Y., Nusse R. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 2004, 20:781-810.
27. MacDonald B.T., Adamska M., Meisler M.H. Hypomorphic expression of Dkk1 in the doubleridge mouse: Dose dependence and compensatory interactions with Lrp6. Development 2004, 131:2543-2552.
28. Mao B., Wu W., Davidson G., Marhold J., Li M., Mechler B.M., Delius H., Hoppe D., Stannek P., Walter C., et al. Kremen proteins are Dickkopf receptors that regulate Wnt/beta-catenin signalling. Nature 2002, 417:664-667.
29. Maretto S., Cordenonsi M., Dupont S., Braghetta P., Broccoli V., Hassan A.B., Volpin D., Bressan G.M., Piccolo S. Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors. Proc. Natl. Acad. Sci. USA 2003, 100:3299-3304.
30. Mi K., Johnson G.V. Regulated proteolytic processing of LRP6 results in release of its intracellular domain. J. Neurochem. 2007, 101:517-529.
31. Nakamura M., Saito H., Kasanuki J., Tamura Y., Yoshida S. Cytokine production in patients with inflammatory bowel disease. Gut 1992, 33:933-937.
32. Nakanishi Y., Lu B., Gerard C., Iwasaki A. CD8(+) T lymphocyte mobilization to virus-infected tissue requires CD4(+) T-cell help. Nature 2009, 462:510-513.
33. Nguyen H., Ramana C.V., Bayes J., Stark G.R. Roles of phosphatidylinositol 3-kinase in interferon-gamma-dependent phosphorylation of STAT1 on serine 727 and activation of gene expression. J. Biol. Chem. 2001, 276:33361-33368.
34. Niehrs C. Function and biological roles of the Dickkopf family of Wnt modulators. Oncogene 2006, 25:7469-7481.
35. Niida A., Hiroko T., Kasai M., Furukawa Y., Nakamura Y., Suzuki Y., Sugano S., Akiyama T. DKK1, a negative regulator of Wnt signaling, is a target of the beta-catenin/TCF pathway. Oncogene 2004, 23:8520-8526.
36. Pickert G., Neufert C., Leppkes M., Zheng Y., Wittkopf N., Warntjen M., Lehr H.A., Hirth S., Weigmann B., Wirtz S., et al. STAT3 links IL-22 signaling in intestinal epithelial cells to mucosal wound healing. J. Exp. Med. 2009, 206:1465-1472.
37. Pimentel-Muiños F.X., Seed B. Regulated commitment of TNF receptor signaling: A molecular switch for death or activation. Immunity 1999, 11:783-793.
38. Pinto D., Clevers H. Wnt control of stem cells and differentiation in the intestinal epithelium. Exp. Cell Res. 2005, 306:357-363.
39. Pinto D., Gregorieff A., Begthel H., Clevers H. Canonical Wnt signals are essential for homeostasis of the intestinal epithelium. Genes Dev. 2003, 17:1709-1713.
40. Renes I.B., Verburg M., Van Nispen D.J., Taminiau J.A., Büller H.A., Dekker J., Einerhand A.W. Epithelial proliferation, cell death, and gene expression in experimental colitis: Alterations in carbonic anhydrase I, mucin MUC2, and trefoil factor 3 expression. Int. J. Colorectal Dis. 2002, 17:317-326.
41. Robinson C.M., Shirey K.A., Carlin J.M. Synergistic transcriptional activation of indoleamine dioxygenase by IFN-gamma and tumor necrosis factor-alpha. J. Interferon Cytokine Res. 2003, 23:413-421.
42. Ruemmele F.M., Gurbindo C., Mansour A.M., Marchand R., Levy E., Seidman E.G. Effects of interferon gamma on growth, apoptosis, and MHC class II expression of immature rat intestinal crypt (IEC-6) cells. J. Cell. Physiol. 1998, 176:120-126.
43. Schmidt T.G., Skerra A. The Strep-tag system for one-step purification and high-affinity detection or capturing of proteins. Nat. Protoc. 2007, 2:1528-1535.
44. Schmitz H., Fromm M., Bentzel C.J., Scholz P., Detjen K., Mankertz J., Bode H., Epple H.J., Riecken E.O., Schulzke J.D. Tumor necrosis factor-alpha (TNFalpha) regulates the epithelial barrier in the human intestinal cell line HT-29/B6. J. Cell Sci. 1999, 112:137-146.
45. Scoville D.H., Sato T., He X.C., Li L. Current view: Intestinal stem cells and signaling. Gastroenterology 2008, 134:849-864.
46. Seidelin J.B., Jäättelä M., Nielsen O.H. Continuous interferon-gamma or tumor necrosis factor-alpha exposure of enterocytes attenuates cell death responses. Cytokine 2004, 27:113-119.
47. Seno H., Miyoshi H., Brown S.L., Geske M.J., Colonna M., Stappenbeck T.S. Efficient colonic mucosal wound repair requires Trem2 signaling. Proc. Natl. Acad. Sci. USA 2009, 106:256-261.
48. Serafini E.P., Kirk A.P., Chambers T.J. Rate and pattern of epithelial cell proliferation in ulcerative colitis. Gut 1981, 22:648-652.
49. Tamai K., Zeng X., Liu C., Zhang X., Harada Y., Chang Z., He X. A mechanism for Wnt coreceptor activation. Mol. Cell 2004, 13:149-156.
50. Tong Q., Vassilieva E.V., Ivanov A.I., Wang Z., Brown G.T., Parkos C.A., Nusrat A. Interferon-gamma inhibits T84 epithelial cell migration by redirecting transcytosis of beta1 integrin from the migrating leading edge. J. Immunol. 2005, 175:4030-4038.
51. Turner J.R. Molecular basis of epithelial barrier regulation: From basic mechanisms to clinical application. Am. J. Pathol. 2006, 169:1901-1909.
52. Utech M., Ivanov A.I., Samarin S.N., Bruewer M., Turner J.R., Mrsny R.J., Parkos C.A., Nusrat A. Mechanism of IFN-gamma-induced endocytosis of tight junction proteins: Myosin II-dependent vacuolarization of the apical plasma membrane. Mol. Biol. Cell 2005, 16:5040-5052.
53. Voorzanger-Rousselot N., Goehrig D., Facon T., Clézardin P., Garnero P. Platelet is a major contributor to circulating levels of Dickkopf-1: Clinical implications in patients with multiple myeloma. Br. J. Haematol. 2009, 145:264-266.
54. Wang F., Graham W.V., Wang Y., Witkowski E.D., Schwarz B.T., Turner J.R. Interferon-gamma and tumor necrosis factor-alpha synergize to induce intestinal epithelial barrier dysfunction by up-regulating myosin light chain kinase expression. Am. J. Pathol. 2005, 166:409-419.
55. Yin J., Ferguson T.A. Identification of an IFN-gamma-producing neutrophil early in the response to Listeria monocytogenes. J. Immunol. 2009, 182:7069-7073.
56. Zhao J., de Vera J., Narushima S., Beck E.X., Palencia S., Shinkawa P., Kim K.A., Liu Y., Levy M.D., Berg D.J., et al. R-spondin1, a novel intestinotrophic mitogen, ameliorates experimental colitis in mice. Gastroenterology 2007, 132:1331-1343.