Epithelial cell-intrinsic Notch signaling plays an essential role in the maintenance of gut immune homeostasis

Journal of Immunology

Volumn 188, Issue 5, 2012, Pages 2427-2436

  Obata, Yuuki ^a,b   Takahashi, Daisuke ^b,c   Ebisawa, Masashi ^b,c   Kakiguchi, Kisa ^d   Yonemura, Shigenobu ^d   Jinnohara, Toshi ^b,c   Kanaya, Takashi ^b   Fujimura, Yumiko ^b   Ohmae, Masumi ^b   Hase, Koji ^b,c,e   Ohno, Hiroshi ^a,b,c  

^a CHIBA UNIVERSITY   (Japan)

^b RIKEN Center for Integrative Medical Sciences   (Japan)

^c YOKOHAMA CITY UNIVERSITY   (Japan)

^d RIKEN Center for Biosystems Dynamics Research   (Japan)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYCLIN DEPENDENT KINASE INHIBITOR 1C; NOTCH RECEPTOR; RBP J PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HES 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL TRANSLOCATION; CELL CYCLE ARREST; COLITIS; COLON MUCOSA; CONTROLLED STUDY; DOWN REGULATION; GASTROINTESTINAL TRACT; GENE; GENE DELETION; HOMEOSTASIS; IMMUNOREGULATION; INTESTINE EPITHELIUM CELL; INTESTINE FLORA; INTESTINE MUCOSA PERMEABILITY; LAMINA PROPRIA; MONONUCLEAR CELL; MOUSE; NONHUMAN; PERMEABILITY BARRIER; PRIORITY JOURNAL; RBPJ GENE; TH17 CELL;

ANIMALS; BACTERIAL TRANSLOCATION; CELL DIFFERENTIATION; CHRONIC DISEASE; COLITIS; GENE DELETION; HOMEOSTASIS; HUMANS; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE-BINDING PROTEIN; INTESTINAL MUCOSA; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; TH17 CELLS;

EID: 84857467280     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101128     Document Type: Article

References (40)

1. Gersemann, M., S. Becker, I. Kübler, M. Koslowski, G. Wang, K. R. Herrlinger, J. Griger, P. Fritz, K. Fellermann, M. Schwab, et al. 2009. Differences in goblet cell differentiation between Crohn's disease and ulcerative colitis. Differentiation 77: 84-94.
2. Van der Sluis, M., B. A. De Koning, A. C. De Bruijn, A. Velcich, J. P. Meijerink, J. B. Van Goudoever, H. A. Büller, J. Dekker, I. Van Seuningen, I. B. Renes, and A. W. Einerhand. 2006. Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology 131: 117-129. (Pubitemid 44015753)
3. Bergstrom, K. S., J. A. Guttman, M. Rumi, C. Ma, S. Bouzari, M. A. Khan, D. L. Gibson, A. W. Vogl, and B. A. Vallance. 2008. Modulation of intestinal goblet cell function during infection by an attaching and effacing bacterial pathogen. Infect. Immun. 76: 796-811. (Pubitemid 351251753)
4. Luperchio, S. A., and D. B. Schauer. 2001. Molecular pathogenesis of Citrobacter rodentium and transmissible murine colonic hyperplasia. Microbes Infect. 3: 333-340. (Pubitemid 32385783)
5. Crosnier, C., D. Stamataki, and J. Lewis. 2006. Organizing cell renewal in the intestine: stem cells, signals and combinatorial control. Nat. Rev. Genet. 7: 349-359.
6. Shroyer, N. F., M. A. Helmrath, V. Y. Wang, B. Antalffy, S. J. Henning, and H. Y. Zoghbi. 2007. Intestine-specific ablation of mouse atonal homolog 1 (Math1) reveals a role in cellular homeostasis. Gastroenterology 132: 2478-2488. (Pubitemid 46890862)
7. Yang, Q., N. A. Bermingham, M. J. Finegold, and H. Y. Zoghbi. 2001. Requirement of Math1 for secretory cell lineage commitment in the mouse intestine. Science 294: 2155-2158. (Pubitemid 33150670)
8. Fre, S., M. Huyghe, P. Mourikis, S. Robine, D. Louvard, and S. Artavanis-Tsakonas. 2005. Notch signals control the fate of immature progenitor cells in the intestine. Nature 435: 964-968. (Pubitemid 40896323)
9. van Es, J. H., M. E. van Gijn, O. Riccio, M. van den Born, M. Vooijs, H. Begthel, M. Cozijnsen, S. Robine, D. J. Winton, F. Radtke, and H. Clevers. 2005. Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 435: 959-963. (Pubitemid 40896322)
10. Okamoto, R., K. Tsuchiya, Y. Nemoto, J. Akiyama, T. Nakamura, T. Kanai, and M. Watanabe. 2009. Requirement of Notch activation during regeneration of the intestinal epithelia. Am. J. Physiol. Gastrointest. Liver Physiol. 296: G23-G35.
11. Shinoda, M., M. Shin-Ya, Y. Naito, T. Kishida, R. Ito, N. Suzuki, H. Yasuda, J. Sakagami, J. Imanishi, K. Kataoka, et al. 2010. Early-stage blocking of Notch signaling inhibits the depletion of goblet cells in dextran sodium sulfate-induced colitis in mice. J. Gastroenterol. 45: 608-617.
12. Han, H., K. Tanigaki, N. Yamamoto, K. Kuroda, M. Yoshimoto, T. Nakahata, K. Ikuta, and T. Honjo. 2002. Inducible gene knockout of transcription factor recombination signal binding protein-J reveals its essential role in T versus B lineage decision. Int. Immunol. 14: 637-645. (Pubitemid 34649719)
13. Ito, T., N. Udaka, T. Yazawa, K. Okudela, H. Hayashi, T. Sudo, F. Guillemot, R. Kageyama, and H. Kitamura. 2000. Basic helix-loop-helix transcription factors regulate the neuroendocrine differentiation of fetal mouse pulmonary epithelium. Development 127: 3913-3921.
14. Weigmann, B., I. Tubbe, D. Seidel, A. Nicolaev, C. Becker, and M. F. Neurath. 2007. Isolation and subsequent analysis of murine lamina propria mononuclear cells from colonic tissue. Nat. Protoc. 2: 2307-2311.
15. Date, Y., Y. Nakanishi, S. Fukuda, T. Kato, S. Tsuneda, H. Ohno, and J. Kikuchi. 2010. New monitoring approach for metabolic dynamics in microbial ecosystems using stable-isotope-labeling technologies. J. Biosci. Bioeng. 110: 87-93.
16. Bouskra, D., C. Brézillon, M. Bérard, C. Werts, R. Varona, I. G. Boneca, and G. Eberl. 2008. Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis. Nature 456: 507-510. (Pubitemid 352759006)
17. Nenci, A., C. Becker, A. Wullaert, R. Gareus, G. van Loo, S. Danese, M. Huth, A. Nikolaev, C. Neufert, B. Madison, et al. 2007. Epithelial NEMO links innate immunity to chronic intestinal inflammation. Nature 446: 557-561. (Pubitemid 46514732)
18. Taurog, J. D., J. A. Richardson, J. T. Croft, W. A. Simmons, M. Zhou, J. L. Fernández-Sueiro, E. Balish, and R. E. Hammer. 1994. The germfree state prevents development of gut and joint inflammatory disease in HLA-B27 transgenic rats. J. Exp. Med. 180: 2359-2364. (Pubitemid 24351619)
19. Sellon, R. K., S. Tonkonogy, M. Schultz, L. A. Dieleman, W. Grenther, E. Balish, D. M. Rennick, and R. B. Sartor. 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. (Pubitemid 29044613)
20. Dijkstra, G., H. Moshage, H. M. van Dullemen, A. de Jager-Krikken, A. T. Tiebosch, J. H. Kleibeuker, P. L. Jansen, and H. van Goor. 1998. Expression of nitric oxide synthases and formation of nitrotyrosine and reactive oxygen species in inflammatory bowel disease. J. Pathol. 186: 416-421. (Pubitemid 29005462)
21. Podolsky, D. K. 2002. Inflammatory bowel disease. N. Engl. J. Med. 347: 417-429. (Pubitemid 34851835)
22. Turner, J. R. 2009. Intestinal mucosal barrier function in health and disease. Nat. Rev. Immunol. 9: 799-809.
23. Ganz, T. 2003. Defensins: antimicrobial peptides of innate immunity. Nat. Rev. Immunol. 3: 710-720. (Pubitemid 41070812)
24. Ouellette, A. J. 1997. Paneth cells and innate immunity in the crypt microenvironment. Gastroenterology 113: 1779-1784. (Pubitemid 27461268)
25. Lewin, K. 1969. The Paneth cell in health and disease. Ann. R. Coll. Surg. Engl. 44: 23-37.
26. Fahlgren, A., S. Hammarström, A. Danielsson, and M. L. Hammarström. 2003. Increased expression of antimicrobial peptides and lysozyme in colonic epithelial cells of patients with ulcerative colitis. Clin. Exp. Immunol. 131: 90-101. (Pubitemid 36098827)
27. Kim, M., H. Ashida, M. Ogawa, Y. Yoshikawa, H. Mimuro, and C. Sasakawa. 2010. Bacterial interactions with the host epithelium. Cell Host Microbe 8: 20-35.
28. Cliffe, L. J., N. E. Humphreys, T. E. Lane, C. S. Potten, C. Booth, and R. K. Grencis. 2005. Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion. Science 308: 1463-1465. (Pubitemid 40791299)
29. Iwai, H., M. Kim, Y. Yoshikawa, H. Ashida, M. Ogawa, Y. Fujita, D. Muller, T. Kirikae, P. K. Jackson, S. Kotani, and C. Sasakawa. 2007. A bacterial effector targets Mad2L2, an APC inhibitor, to modulate host cell cycling. Cell 130: 611-623. (Pubitemid 47268055)
30. Sansonetti, P. J. 2004. War and peace at mucosal surfaces. Nat. Rev. Immunol. 4: 953-964. (Pubitemid 39620070)
31. Fre, S., D. Vignjevic, M. Schoumacher, S. L. Duffy, K. P. Janssen, S. Robine, and D. Louvard. 2008. Epithelial morphogenesis and intestinal cancer: new insights in signaling mechanisms. Adv. Cancer Res. 100: 85-111. (Pubitemid 351932180)
32. Riccio, O., M. E. van Gijn, A. C. Bezdek, L. Pellegrinet, J. H. van Es, U. Zimber-Strobl, L. J. Strobl, T. Honjo, H. Clevers, and F. Radtke. 2008. Loss of intestinal crypt progenitor cells owing to inactivation of both Notch1 and Notch2 is accompanied by derepression of CDK inhibitors p27Kip1 and p57Kip2. EMBO Rep. 9: 377-383.
33. Guilmeau, S., M. Flandez, L. Bancroft, R. S. Sellers, B. Tear, P. Stanley, and L. H. Augenlicht. 2008. Intestinal deletion of Pofut1 in the mouse inactivates notch signaling and causes enterocolitis. Gastroenterology 135: 849-860, 860.e1-e6.
34. Shi, S., and P. Stanley. 2003. Protein O-fucosyltransferase 1 is an essential component of Notch signaling pathways. Proc. Natl. Acad. Sci. USA 100: 5234-5239. (Pubitemid 36542688)
35. van Den Brink, G. R., P. de Santa Barbara, and D. J. Roberts. 2001. Development. Epithelial cell differentiation - a Mather of choice. Science 294: 2115-2116.
36. Madara, J. L., and J. S. Trier. 1982. Structure and permeability of goblet cell tight junctions in rat small intestine. J. Membr. Biol. 66: 145-157. (Pubitemid 12126909)
37. Yu, Q. H., and Q. Yang. 2009. Diversity of tight junctions (TJs) between gastrointestinal epithelial cells and their function in maintaining the mucosal barrier. Cell Biol. Int. 33: 78-82.
38. McConnell, B. B., S. S. Kim, A. B. Bialkowska, K. Yu, S. V. Sitaraman, and V. W. Yang. Krüppel-like factor 5 protects against dextran sulfate sodium-induced colonic injury in mice by promoting epithelial repair. Gastroenterology 140: 540-549.e2.
39. Skipper, M., and J. Lewis. 2000. Getting to the guts of enteroendocrine differentiation. Nat. Genet. 24: 3-4. (Pubitemid 30041406)
40. Koo, B. K., H. S. Lim, H. J. Chang, M. J. Yoon, Y. Choi, M. P. Kong, C. H. Kim, J. M. Kim, J. G. Park, and Y. Y. Kong. 2009. Notch signaling promotes the generation of EphrinB1-positive intestinal epithelial cells. Gastroenterology 137: 145-155, 155.e1-e3.