Enterocyte-derived TAK1 signaling prevents epithelium apoptosis and the development of ileitis and colitis

Journal of Immunology

Volumn 181, Issue 2, 2008, Pages 1143-1152

  Kajino Sakamoto, Rie ^a   Inagaki, Maiko ^a   Lippert, Elisabeth ^b   Akira, Shizuo ^c   Robine, Sylvie ^d   Matsumoto, Kunihiro ^e,f   Jobin, Christian ^b   Ninomiya Tsuji, Jun ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c OSAKA UNIVERSITY   (Japan)

^d CNRS   (France)

^e NAGOYA UNIVERSITY   (Japan)

^f JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1BETA; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 2; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR 1; MAP KINASE KINASE KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIRTH; COLITIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; EMBRYO; GENE DELETION; HISTOPATHOLOGY; ILEITIS; IMMUNOPATHOGENESIS; INNATE IMMUNITY; INTESTINE CELL; INTESTINE EPITHELIUM; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; ANIMAL; CYTOLOGY; IMMUNOLOGY; INTESTINE MUCOSA; METABOLISM; MOUSE MUTANT;

ANIMALS; APOPTOSIS; COLITIS; ENTEROCYTES; ILEITIS; INTESTINAL MUCOSA; MAP KINASE KINASE KINASES; MICE; MICE, KNOCKOUT; MICE, MUTANT STRAINS; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 49049095991     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.2.1143     Document Type: Article

References (37)

1. Akira, S., S. Uematsu, and O. Takeuchi. 2006. Pathogen recognition and innate immunity. Cell 124: 783-801.
2. Raz, E. 2007. Organ-specific regulation of innate immunity. Nat. Immunol. 8: 3-4.
3. Macpherson, A. J., and N. L. Harris. 2004. Interactions between commensal intestinal bacteria and the immune system. Nat. Rev. Immunol. 4: 478-485. (Pubitemid 38745559)
4. O'Hara, A. M., and F. Shanahan. 2006. The gut flora as a forgotten organ. EMBO Rep. 7: 688-693.
5. Bouma, G., and W. Strober. 2003. The immunological and genetic basis of in- flammatory bowel disease. Nat. Rev. Immunol. 3: 521-533. (Pubitemid 37328672)
6. Xavier, R. J., and D. K. Podolsky. 2007. Unravelling the pathogenesis of inflammatory bowel disease. Nature 448: 427-434. (Pubitemid 47123518)
7. Ninomiya-Tsuji, J., K. Kishimoto, A. Hiyama, J. Inoue, Z. Cao, and K. Matsumoto. 1999. The kinase TAK1 can activate the NIK-I κB as well as the MAP kinase cascade in the IL-1 signalling pathway. Nature 398: 252-256. (Pubitemid 29142861)
8. Sato, S., H. Sanjo, T. Tsujimura, J. Ninomiya-Tsuji, M. Yamamoto, T. Kawai, O. Takeuchi, and S. Akira. 2006. TAK1 is indispensable for development of T cells and prevention of colitis by the generation of regulatory T cells. Int. Immunol. 18: 1405-1411. (Pubitemid 44446818)
9. Shim, J. H., C. Xiao, A. E. Paschal, S. T. Bailey, P. Rao, M. S. Hayden, K. Y. Lee, C. Bussey, M. Steckel, N. Tanaka, et al. 2005. TAK1, but not TAB1 or TAB2, plays an essential role in multiple signaling pathways in vivo. Genes Dev. 19: 2668-2681.
10. Kim, J. Y., E. Omori, K. Matsumoto, G. Nunez, and J. Ninomiya-Tsuji. 2007. TAK1 is a central mediator of NOD2 signaling in epidermal cells. J. Biol. Chem. 283: 137-144.
11. Omori, E., K. Matsumoto, H. Sanjo, S. Sato, S. Akira, R. C. Smart, and J. Ninomiya-Tsuji. 2006. TAK1 is a master regulator of epidermal homeostasis involving skin inflammation and apoptosis. J. Biol. Chem. 281: 19610-19617. (Pubitemid 44035464)
12. Aggarwal, B. B. 2003. Signalling pathways of the TNF superfamily: a doubleedged sword. Nat. Rev. Immunol. 3: 745-756. (Pubitemid 41070815)
13. Marini, M., G. Bamias, J. Rivera-Nieves, C. A. Moskaluk, S. B. Hoang, W. G. Ross, T. T. Pizarro, and F. Cominelli. 2003. TNF-α neutralization ameliorates the severity of murine Crohn's-like ileitis by abrogation of intestinal epithelial cell apoptosis. Proc. Natl. Acad. Sci. USA 100: 8366-8371. (Pubitemid 36842551)
14. Karin, M., and A. Lin. 2002. NF-κB at the crossroads of life and death. Nat. Immunol. 3: 221-227.
15. Feldmann, M., and R. N. Maini. 2001. Anti-TNFα: therapy of rheumatoid arthritis: what have we learned? Annu. Rev. Immunol. 19: 163-196. (Pubitemid 32368033)
16. Yan, F., S. K. John, G. Wilson, D. S. Jones, M. K. Washington, and D. B. Polk. 2004. Kinase suppressor of Ras-1 protects intestinal epithelium from cytokinemediated apoptosis during inflammation. J. Clin. Invest. 114: 1272-1280. (Pubitemid 40385298)
17. Sato, S., H. Sanjo, K. Takeda, J. Ninomiya-Tsuji, M. Yamamoto, T. Kawai, K. Matsumoto, O. Takeuchi, and S. Akira. 2005. Essential function for the kinase TAK1 in innate and adaptive immune responses. Nat. Immunol. 6: 1087-1095. (Pubitemid 41541786)
18. Madison, B. B., L. Dunbar, X. T. Qiao, K. Braunstein, E. Braunstein, and D. L. Gumucio. 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.
19. El Marjou, F., K. P. Janssen, B. H. Chang, M. Li, V. Hindie, L. Chan, D. Louvard, P. Chambon, D. Metzger, and S. Robine. 2004. Tissue-specific and inducible Cre-mediated recombination in the gut epithelium. Genesis 39: 186-193. (Pubitemid 39079517)
20. Pfeffer, K., T. Matsuyama, T. M. Kundig, A. Wakeham, K. Kishihara, A. Shahinian, K. Wiegmann, P. S. Ohashi, M. Kronke, and T. W. Mak. 1993. Mice deficient for the 55 kd tumor necrosis factor receptor are resistant to endotoxic shock, yet succumb to L. monocytogenes infection. Cell 73: 457-467. (Pubitemid 23143346)
21. 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.
22. Athman, R., J. Niewohner, D. Louvard, and S. Robine. 2002. Epithelial cells: establishment of primary cultures and immortalization. In Molecular Cellular Microbiology. P. Sansonetti and A. Zychlinksy, eds. Academic Press, New York, pp. 93-113.
23. 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)
24. Jadrich, J. L., M. B. O'Connor, and E. Coucouvanis. 2006. The TGFβ activated kinase TAK1 regulates vascular development in vivo. Development 133: 1529-1541.
25. Liu, H. H., M. Xie, M. D. Schneider, and Z. J. Chen. 2006. Essential role of TAK1 in thymocyte development and activation. Proc. Natl. Acad. Sci. USA 103: 11677-11682. (Pubitemid 44182510)
26. Wan, Y. Y., H. Chi, M. Xie, M. D. Schneider, and R. A. Flavell. 2006. The kinase TAK1 integrates antigen and cytokine receptor signaling for T cell development, survival and function. Nat. Immunol. 7: 851-858.
27. Papa, S., C. Bubici, F. Zazzeroni, C. G. Pham, C. Kuntzen, J. R. Knabb, K. Dean, and G. Franzoso. 2006. The NF-κB-mediated control of the JNK cascade in the antagonism of programmed cell death in health and disease. Cell Death Differ. 13: 712-729.
28. Li, Z. W., W. Chu, Y. Hu, M. Delhase, T. Deerinck, M. Ellisman, R. Johnson, and M. Karin. 1999. The IKKβ subunit of IκB kinase (IKK) is essential for nuclear factor κB activation and prevention of apoptosis. J. Exp. Med. 189: 1839-1845.
29. Li, Q., D. Van Antwerp, F. Mercurio, K. F. Lee, and I. M. Verma. 1999. Severe liver degeneration in mice lacking the IκB kinase 2 gene. Science 284: 321-325. (Pubitemid 129523450)
30. Rudolph, D., W. C. Yeh, A. Wakeham, B. Rudolph, D. Nallainathan, J. Potter, A. J. Elia, and T. W. Mak. 2000. Severe liver degeneration and lack of NF-κB activation in NEMO/IKKγ-deficient mice. Genes Dev. 14: 854-862. (Pubitemid 30215004)
31. Nenci, A., M. Huth, A. Funteh, M. Schmidt-Supprian, W. Bloch, D. Metzger, P. Chambon, K. Rajewsky, T. Krieg, I. Haase, and M. Pasparakis. 2006. Skin lesion development in a mouse model of incontinentia pigmenti is triggered by NEMO deficiency in epidermal keratinocytes and requires TNF signaling. Hum. Mol. Genet. 15: 531-542. (Pubitemid 43205419)
32. Ashkenazi, A. 2002. Targeting death and decoy receptors of the tumour-necrosis factor superfamily. Nat. Rev. Cancer 2: 420-430. (Pubitemid 37328939)
33. Rakoff-Nahoum, S., J. Paglino, F. Eslami-Varzaneh, S. Edberg, and R. Medzhitov. 2004. Recognition of commensal microflora by Toll-like receptors is required for intestinal homeostasis. Cell 118: 229-241. (Pubitemid 38962578)
34. Hanafusa, H., J. Ninomiya-Tsuji, N. Masuyama, M. Nishita, J.-i. Fujisawa, H. Shibuya, K. Matsumoto, and E. Nishida. 1999. Involvement of the p38 mitogen- activated protein kinase pathway in transforming growth factor-β-induced gene expression. J. Biol. Chem. 274: 27161-27167.
35. + pathway to antagonize Wnt/β-catenin signaling. Mol. Cell. Biol. 23: 131-139.
36. Ishitani, T., J. Ninomiya-Tsuji, S. Nagai, M. Nishita, M. Meneghini, N. Barker, M. Waterman, B. Bowerman, H. Clevers, H. Shibuya, and K. Matsumoto. 1999. The TAK1-NLK-MAPK-related pathway antagonizes signalling between β-catenin and transcription factor TCF. Nature 399: 798-802. (Pubitemid 29293177)
37. Kajino, T., E. Omori, S. Ishii, K. Matsumoto, and J. Ninomiya-Tsuji. 2007. TAK1 MAPK kinase kinase mediates transforming growth factor-β signaling by targeting SnoN oncoprotein for degradation. J. Biol. Chem. 282: 9475-9481.