Intestinal epithelial-derived TAK1 signaling is essential for cytoprotection against chemical-induced colitis

PLoS ONE

Volumn 4, Issue 2, 2009, Pages

  Kim, Jae Young ^a   Kajino Sakamoto, Rie ^a   Omori, Emily ^a   Jobin, Christian ^b   Ninomiya Tsuji, Jun ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOOXYGENASE 2; INTERLEUKIN 1; INTERLEUKIN 6; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL PROTECTION; CHEMICALLY INDUCED DISORDER; COLITIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; HYPERSENSITIVITY REACTION; INTESTINE EPITHELIUM; INTESTINE INJURY; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TISSUE REPAIR; WEIGHT REDUCTION;

BACTERIA (MICROORGANISMS); MUS;

EID: 84887212416     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0004561     Document Type: Article

References (38)

1. Ley RE, Peterson DA, Gordon JI (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124: 837-848.
2. Radtke F, Clevers H (2005) Self-renewal and cancer of the gut: two sides of a coin. Science 307: 1904-1909.
3. Bouma G, Strober W (2003) The immunological and genetic basis of inflammatory bowel disease. Nat Rev Immunol 3: 521-533.
4. Xavier RJ, Podolsky DK (2007) Unravelling the pathogenesis of inflammatory bowel disease. Nature 448: 427-434.
5. Hall PA, Coates PJ, Ansari B, Hopwood D (1994) Regulation of cell number in the mammalian gastrointestinal tract: the importance of apoptosis. J Cell Sci 107: 3569-3577.
6. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R (2004) Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118: 229-241.
7. Medzhitov R (2007) Recognition of microorganisms and activation of the immune response. Nature 449: 819-826.
8. Lotz M, Gutle D, Walther S, Menard S, Bogdan C, et al. (2006) Postnatal acquisition of endotoxin tolerance in intestinal epithelial cells. J Exp Med 203: 973-984.
9. Ninomiya-Tsuji J, Kishimoto K, Hiyama A, Inoue J, Cao Z, et al. (1999) The kinase TAK1 can activate the NIK-I kappaB as well as the MAP kinase cascade in the IL-1 signalling pathway. Nature 398: 252-256.
10. Sato S, Sanjo H, Takeda K, Ninomiya-Tsuji J, Yamamoto M, et al. (2005) Essential function for the kinase TAK1 in innate and adaptive immune responses. Nat Immunol 6: 1087-1095.
11. Shim JH, Xiao C, Paschal AE, Bailey ST, Rao P, et al. (2005) TAK1, but not TAB1 or TAB2, plays an essential role in multiple signaling pathways in vivo. Genes Dev 19: 2668-2681.
12. da Silva Correia J, Miranda Y, Leonard N, Hsu J, Ulevitch RJ (2007) Regulation of Nod1-mediated signaling pathways. Cell Death Differ 14: 830-839.
13. Hasegawa M, Fujimoto Y, Lucas PC, Nakano H, Fukase K, et al. (2008) A critical role of RICK/RIP2 polyubiquitination in Nod-induced NF-κB activation. Embo J 27: 373-383.
14. Kim JY, Omori E, Matsumoto K, Nunez G, Ninomiya-Tsuji J (2008) TAK1 is a central mediator of NOD2 signaling in epidermal cells. J Biol Chem 283: 137-144.
15. Liu HH, Xie M, Schneider MD, Chen ZJ (2006) Essential role of TAK1 in thymocyte development and activation. Proc Natl Acad Sci U S A 103: 11677-11682.
16. Sato S, Sanjo H, Tsujimura T, Ninomiya-Tsuji J, Yamamoto M, et al. (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.
17. Wan YY, Chi H, Xie M, Schneider MD, Flavell RA (2006) The kinase TAK1 integrates antigen and cytokine receptor signaling for T cell development, survival and function. Nat Immunol 7: 851-858.
18. Kajino-Sakamoto R, Inagaki M, Lippert E, Akira S, Robine S, et al. (2008) Enterocyte-derived TAK1 signaling prevents epithelium apoptosis and the development of ileitis and colitis. J Immunol 181: 1143-1152.
19. Omori E, Matsumoto K, Sanjo H, Sato S, Akira S, et al. (2006) TAK1 is a master regulator of epidermal homeostasis involving skin inflammation and apoptosis. J Biol Chem 281: 19610-19617.
20. Menard S, Forster V, Lotz M, Gutle D, Duerr CU, et al. (2008) Developmental switch of intestinal antimicrobial peptide expression. J Exp Med 205: 183-193.
21. Yan SR, Joseph RR, Rosen K, Reginato MJ, Jackson A, et al. (2005) Activation of NF-κB following detachment delays apoptosis in intestinal epithelial cells. Oncogene 24: 6482-6491.
22. Fukata M, Chen A, Klepper A, Krishnareddy S, Vamadevan AS, et al. (2006) Cox-2 is regulated by Toll-like receptor-4 (TLR4) signaling: Role in proliferation and apoptosis in the intestine. Gastroenterology 131: 862-877.
23. Karrasch T, Kim JS, Jang BI, Jobin C (2007) The flavonoid luteolin worsens chemical-induced colitis in NF-κB(EGFP) transgenic mice through blockade of NF-kappaB-dependent protective molecules. PLoS ONE 2: e596.
24. Morteau O, Morham SG, Sellon R, Dieleman LA, Langenbach R, et al. (2000) Impaired mucosal defense to acute colonic injury in mice lacking cyclooxygenase-1 or cyclooxygenase-2. J Clin Invest 105: 469-478.
25. Tebbutt NC, Giraud AS, Inglese M, Jenkins B, Waring P, et al. (2002) Reciprocal regulation of gastrointestinal homeostasis by SHP2 and STAT-mediated trefoil gene activation in gp130 mutant mice. Nat Med 8: 1089-1097.
26. Jobin C, Sartor RB (2000) The I κB/NF-κB system: a key determinant of mucosalinflammation and protection. Am J Physiol Cell Physiol 278: C451-462.
27. Nenci A, Becker C, Wullaert A, Gareus R, van Loo G, et al. (2007) Epithelial NEMO links innate immunity to chronic intestinal inflammation. Nature 446: 557-561.
28. Giles RH, van Es JH, Clevers H (2003) Caught up in a Wnt storm: Wnt signaling in cancer. Biochim Biophys Acta 1653: 1-24.
29. Korinek V, Barker N, Moerer P, van Donselaar E, Huls G, et al. (1998) Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat Genet 19: 379-383.
30. Siegel PM, Massague J (2003) Cytostatic and apoptotic actions of TGF-beta in homeostasis and cancer. Nat Rev Cancer 3: 807-821.
31. Hanafusa H, Ninomiya-Tsuji J, Masuyama N, Nishita M, Fujisawa J-i, et al. (1999) Involvement of the p38 Mitogen-activated Protein Kinase Pathway in Transforming Growth Factor-beta -induced Gene Expression. J Biol Chem 274: 27161-27167.
32. Ishitani T, Ninomiya-Tsuji J, Nagai S, Nishita M, Meneghini M, et al. (1999) The TAK1-NLK-MAPK-related pathway antagonizes signalling between beta-catenin and transcription factor TCF. Nature 399: 798-802.
33. Kajino T, Omori E, Ishii S, Matsumoto K, Ninomiya-Tsuji J (2007) TAK1 MAPK kinase kinase mediates transforming growth factor-beta signaling by targeting SnoN oncoprotein for degradation. J Biol Chem 282: 9475-9481.
34. Kanei-Ishii C, Ninomiya-Tsuji J, Tanikawa J, Nomura T, Ishitani T, et al. (2004) Wnt-1 signal induces phosphorylation and degradation of c-Myb protein via TAK1, HIPK2, and NLK. Genes Dev 18: 816-829.
35. Inan MS, Tolmacheva V, Wang QS, Rosenberg DW, Giardina C (2000) Transcription factor NF-κB participates in regulation of epithelial cell turnover in the colon. Am J Physiol Gastrointest Liver Physiol 279: G1282-1291.
36. Seitz CS, Deng H, Hinata K, Lin Q, Khavari PA (2000) Nuclear factor κB subunits induce epithelial cell growth arrest. Cancer Res 60: 4085-4092.
37. Kawai T, Akira S (2007) Signaling to NF-κB by Toll-like receptors. Trends Mol Med 13: 460-469.
38. Sellon RK, Tonkonogy S, Schultz M, Dieleman LA, Grenther W, et al. (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.