Regulation and pathophysiological role of epithelial turnover in the gut

Seminars in Cell and Developmental Biology

Volumn 35, Issue , 2014, Pages 40-50

  Günther, Claudia ^a   Buchen, Barbara ^a   Neurath, Markus F ^a   Becker, Christoph ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Inflammation; Necroptosis; Ripoptosome

Indexed keywords

CASPASE 8; DEATH RECEPTOR; INTERFERON; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4;

CELL DEATH; CELL SURVIVAL; DEATH; ENTERITIS; EPITHELIUM CELL; HOMEOSTASIS; HUMAN; INFLAMMATORY BOWEL DISEASE; INTESTINE CANCER; INTESTINE EPITHELIUM; NECROPTOSIS; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; APOPTOSIS; BIOLOGICAL MODEL; INFLAMMATION; INTESTINE MUCOSA; METABOLISM; NECROSIS; PHYSIOLOGY;

APOPTOSIS; CASPASE 8; HOMEOSTASIS; HUMANS; INFLAMMATION; INFLAMMATORY BOWEL DISEASES; INTESTINAL MUCOSA; MODELS, BIOLOGICAL; NECROSIS; SIGNAL TRANSDUCTION;

EID: 84908897476     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2014.06.004     Document Type: Review

References (135)

1. O'Hara A.M., Shanahn F. The gut flora as a forgotten organ. EMBO Rep 2006, 7:688-693.
2. Kamada N., Seo S.U., Chen G.Y., Nunez G. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol 2013, 13:321-335.
3. van der Flier L.G., Clevers H. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol 2009, 71:241-260.
4. Specian R.D., Oliver M.G. Functional biology of intestinal goblet cells. Am J Physiol 1991, 260:C183-C193.
5. Bevins C.L., Salzman N.H. Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis. Nat Rev Microbiol 2011, 9:356-368.
6. 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.
7. Gunther C., Neumann H., Neurath M.F., Becker C. Apoptosis, necrosis and necroptosis: cell death regulation in the intestinal epithelium. Gut 2013, 62:1062-1071.
8. Mallat Z., Tedgui A. Apoptosis in the vasculature: mechanisms and functional importance. Br J Pharmacol 2000, 130:947-962.
9. Bullen T.F., Forrest S., Campbell F., Dodson A.R., Hershman M.J., Pritchard D.M., et al. Characterization of epithelial cell shedding from human small intestine. Lab Invest 2006, 86:1052-1063.
10. Maloy K.J., Powrie F. Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature 2011, 474:298-306.
11. Edelblum K.L., Yan F., Yamaoka T., Polk D.B. Regulation of apoptosis during homeostasis and disease in the intestinal epithelium. Inflamm Bowel Dis 2006, 12:413-424.
12. Mehlen P., Puisieux A. Metastasis: a question of life or death. Nat Rev Cancer 2006, 6:449-458.
13. Meddings J. The significance of the gut barrier in disease. Gut 2008, 57:438-440.
14. Grivennikov S.I., Greten F.R., Karin M. Immunity, inflammation, and cancer. Cell 2010, 140:883-899.
15. Vandenabeele P., Galluzzi L., Vanden Berghe T., Kroemer G. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat Rev Mol Cell Biol 2010, 11:700-714.
16. Taylor R.C., Cullen S.P., Martin S.J. Apoptosis: controlled demolition at the cellular level. Nat Rev Mol Cell Biol 2008, 9:231-241.
17. Fuchs Y., Steller H. Programmed cell death in animal development and disease. Cell 2011, 147:742-758.
18. Watson A.J., Duckworth C.A., Guan Y., Montrose M.H. Mechanisms of epithelial cell shedding in the Mammalian intestine and maintenance of barrier function. Ann N Y Acad Sci 2009, 1165:135-142.
19. Yuan J., Kroemer G. Alternative cell death mechanisms in development and beyond. Genes Dev 2010, 24:2592-2602.
20. Becker C., Watson A.J., Neurath M.F. Complex roles of caspases in the pathogenesis of inflammatory bowel disease. Gastroenterology 2013, 144:283-293.
21. Potten C.S., Loeffler M. Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 1990, 110:1001-1020.
22. Eisenhoffer G.T., Loftus P.D., Yoshigi M., Otsuna H., Chien C.B., Morcos P.A., et al. Crowding induces live cell extrusion to maintain homeostatic cell numbers in epithelia. Nature 2012, 484:546-549.
23. Gunther C., Martini E., Wittkopf N., Amann K., Weigmann B., Neumann H., et al. Caspase-8 regulates TNF-alpha-induced epithelial necroptosis and terminal ileitis. Nature 2011, 477:335-339.
24. Duprez L., Takahashi N., Van Hauwermeiren F., Vandendriessche B., Goossens V., Vanden Berghe T., et al. RIP kinase-dependent necrosis drives lethal systemic inflammatory response syndrome. Immunity 2011, 35:908-918.
25. Brinkman B.M., Hildebrand F., Kubica M., Goosens D., Del Favero J., Declercq W., et al. Caspase deficiency alters the murine gut microbiome. Cell Death Dis 2011, 2:e220.
26. Colussi P.A., Kumar S. Targeted disruption of caspase genes in mice: what they tell us about the functions of individual caspases in apoptosis. Immunol Cell Biol 1999, 77:58-63.
27. Watson A.J., Pritchard D.M. Lessons from genetically engineered animal models. VII. Apoptosis in intestinal epithelium: lessons from transgenic and knockout mice. Am J Physiol Gastrointest Liver Physiol 2000, 278:G1-G5.
28. Nakayama K., Negishi I., Kuida K., Sawa H., Loh D.Y. Targeted disruption of Bcl-2 alpha beta in mice: occurrence of gray hair, polycystic kidney disease, and lymphocytopenia. Proc Natl Acad Sci USA 1994, 91:3700-3704.
29. Nakayama K., Negishi I., Kuida K., Shinkai Y., Louie M.C., Fields L.E., et al. Disappearance of the lymphoid system in Bcl-2 homozygous mutant chimeric mice. Science 1993, 261:1584-1588.
30. Knudson C.M., Tung K.S., Tourtellotte W.G., Brown G.A., Korsmeyer S.J. Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 1995, 270:96-99.
31. Nenci A., Becker C., Wullaert A., Gareus R., van Loo G., Danese S., et al. Epithelial NEMO links innate immunity to chronic intestinal inflammation. Nature 2007, 446:557-561.
32. Kajino-Sakamoto R., Inagaki M., Lippert E., Akira S., Robine S., Matsumoto K., et al. Enterocyte-derived TAK1 signaling prevents epithelium apoptosis and the development of ileitis and colitis. J Immunol 2008, 181:1143-1152.
33. Wittkopf N., Gunther C., Martini E., He G., Amann K., He Y.W., et al. Cellular FLICE-like inhibitory protein secures intestinal epithelial cell survival and immune homeostasis by regulating caspase-8. Gastroenterology 2013.
34. Steinbrecher K.A., Harmel-Laws E., Sitcheran R., Baldwin A.S. Loss of epithelial RelA results in deregulated intestinal proliferative/apoptotic homeostasis and susceptibility to inflammation. J Immunol 2008, 180:2588-2599.
35. Eckmann L., Nebelsiek T., Fingerle A.A., Dann S.M., Mages J., Lang R., et al. Opposing functions of IKKbeta during acute and chronic intestinal inflammation. Proc Natl Acad Sci USA 2008, 105:15058-15063.
36. Greten F.R., Eckmann L., Greten T.F., Park J.M., Li Z.W., Egan L.J., et al. IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 2004, 118:285-296.
37. Mukhopadhyay S., Panda P.K., Sinha N., Das D.N., Bhutia S.K. Autophagy and apoptosis: where do they meet?. Apoptosis 2014.
38. Barrett J.C., Hansoul S., Nicolae D.L., Cho J.H., Duerr R.H., Rioux J.D., et al. Genome-wide association defines more than 30 distinct susceptibility loci for Crohn's disease. Nat Genet 2008, 40:955-962.
39. Cadwell K., Patel K.K., Komatsu M., Virgin H.W., Stappenbeck T.S. A common role for Atg16L1, Atg5 and Atg7 in small intestinal Paneth cells and Crohn disease. Autophagy 2009, 5:250-252.
40. Rioux J.D., Xavier R.J., Taylor K.D., Silverberg M.S., Goyette P., Huett A., et al. Genome-wide association study identifies new susceptibility loci for Crohn disease and implicates autophagy in disease pathogenesis. Nat Genet 2007, 39:596-604.
41. Saitoh T., Fujita N., Jang M.H., Uematsu S., Yang B.G., Satoh T., et al. Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature 2008, 456:264-268.
42. Nguyen H.T., Dalmasso G., Muller S., Carriere J., Seibold F., Darfeuille-Michaud A. Crohn's disease-associated adherent invasive Escherichia coli modulate levels of microRNAs in intestinal epithelial cells to reduce autophagy. Gastroenterology 2014, 146:508-519.
43. Benjamin J.L., Sumpter R., Levine B., Hooper L.V. Intestinal epithelial autophagy is essential for host defense against invasive bacteria. Cell Host Microbe 2013, 13:723-734.
44. Wittkopf N., Gunther C., Martini E., Waldner M., Amann K.U., Neurath M.F., et al. Lack of intestinal epithelial atg7 affects paneth cell granule formation but does not compromise immune homeostasis in the gut. Clin Dev Immunol 2012, 2012:278059.
45. Proskuryakov S.Y., Konoplyannikov A.G., Gabai V.L. Necrosis: a specific form of programmed cell death?. Exp Cell Res 2003, 283:1-16.
46. Zheng Y., Gardner S.E., Clarke M.C. Cell death, damage-associated molecular patterns, and sterile inflammation in cardiovascular disease. Arterioscler Thromb Vasc Biol 2011, 31:2781-2786.
47. Welz P.S., Wullaert A., Vlantis K., Kondylis V., Fernandez-Majada V., Ermolaeva M., et al. FADD prevents RIP3-mediated epithelial cell necrosis and chronic intestinal inflammation. Nature 2011, 477:330-334.
48. Bonnet M.C., Preukschat D., Welz P.S., van Loo G., Ermolaeva M.A., Bloch W., et al. The adaptor protein FADD protects epidermal keratinocytes from necroptosis in vivo and prevents skin inflammation. Immunity 2011, 35:572-582.
49. Vanlangenakker N., Vanden Berghe T., Vandenabeele P. Many stimuli pull the necrotic trigger: an overview. Cell Death Differ 2012, 19:75-86.
50. Chan F.K., Shisler J., Bixby J.G., Felices M., Zheng L., Appel M., et al. A role for tumor necrosis factor receptor-2 and receptor-interacting protein in programmed necrosis and antiviral responses. J Biol Chem 2003, 278:51613-51621.
51. Vanlangenakker N., Vanden Berghe T., Krysko D.V., Festjens N., Vandenabeele P. Molecular mechanisms and pathophysiology of necrotic cell death. Curr Mol Med 2008, 8:207-220.
52. Laster S.M., Wood J.G., Gooding L.R. Tumor necrosis factor can induce both apoptic and necrotic forms of cell lysis. J Immunol 1988, 141:2629-2634.
53. Pierdomenico M., Negroni A., Stronati L., Vitali R., Prete E., Bertin J., et al. Necroptosis is active in children with inflammatory bowel disease and contributes to heighten intestinal inflammation. Am J Gastroenterol 2014, 109:279-287.
54. Hacker H., Karin M. Regulation and function of IKK and IKK-related kinases. Sci STKE 2006, 2006:re13.
55. Wilson N.S., Dixit V., Ashkenazi A. Death receptor signal transducers: nodes of coordination in immune signaling networks. Nat Immunol 2009, 10:348-355.
56. Declercq W., Vanden Berghe T., Vandenabeele P. RIP kinases at the crossroads of cell death and survival. Cell 2009, 138:229-232.
57. Zhang J., Zhang H., Li J., Rosenberg S., Zhang E.C., Zhou X., et al. RIP1-mediated regulation of lymphocyte survival and death responses. Immunol Res 2011, 51:227-236.
58. Ofengeim D., Yuan J. Regulation of RIP1 kinase signalling at the crossroads of inflammation and cell death. Nat Rev Mol Cell Biol 2013, 14:727-736.
59. Mahoney D.J., Cheung H.H., Mrad R.L., Plenchette S., Simard C., Enwere E., et al. Both cIAP1 and cIAP2 regulate TNFalpha-mediated NF-kappaB activation. Proc Natl Acad Sci USA 2008, 105:11778-11783.
60. Varfolomeev E., Goncharov T., Fedorova A.V., Dynek J.N., Zobel K., Deshayes K., et al. c-IAP1 and c-IAP2 are critical mediators of tumor necrosis factor alpha (TNFalpha)-induced NF-kappaB activation. J Biol Chem 2008, 283:24295-24299.
61. Meylan E., Burns K., Hofmann K., Blancheteau V., Martinon F., Kelliher M., et al. RIP1 is an essential mediator of Toll-like receptor 3-induced NF-kappa B activation. Nat Immunol 2004, 5:503-507.
62. Wright A., Reiley W.W., Chang M., Jin W., Lee A.J., Zhang M., et al. Regulation of early wave of germ cell apoptosis and spermatogenesis by deubiquitinating enzyme CYLD. Dev Cell 2007, 13:705-716.
63. He S., Wang L., Miao L., Wang T., Du F., Zhao L., et al. Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell 2009, 137:1100-1111.
64. Zhang D.W., Shao J., Lin J., Zhang N., Lu B.J., Lin S.C., et al. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 2009, 325:332-336.
65. Cho Y.S., Challa S., Moquin D., Genga R., Ray T.D., Guildford M., et al. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 2009, 137:1112-1123.
66. Muzio M., Chinnaiyan A.M., Kischkel F.C., O'Rourke K., Shevchenko A., Ni J., et al. FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex. Cell 1996, 85:817-827.
67. Bagnoli M., Canevari S., Mezzanzanica D. Cellular FLICE-inhibitory protein (c-FLIP) signalling: a key regulator of receptor-mediated apoptosis in physiologic context and in cancer. Int J Biochem Cell Biol 2010, 42:210-213.
68. Ozturk S., Schleich K., Lavrik I.N. Cellular FLICE-like inhibitory proteins (c-FLIPs): fine-tuners of life and death decisions. Exp Cell Res 2012, 318:1324-1331.
69. Budd R.C., Yeh W.C., Tschopp J. cFLIP regulation of lymphocyte activation and development. Nat Rev Immunol 2006, 6:196-204.
70. Chang D.W., Xing Z., Pan Y., Algeciras-Schimnich A., Barnhart B.C., Yaish-Ohad S., et al. c-FLIP(L) is a dual function regulator for caspase-8 activation and CD95-mediated apoptosis. EMBO J 2002, 21:3704-3714.
71. Micheau O., Thome M., Schneider P., Holler N., Tschopp J., Nicholson D.W., et al. The long form of FLIP is an activator of caspase-8 at the Fas death-inducing signaling complex. J Biol Chem 2002, 277:45162-45171.
72. Boatright K.M., Deis C., Denault J.B., Sutherlin D.P., Salvesen G.S. Activation of caspases-8 and -10 by FLIP(L). Biochem J 2004, 382:651-657.
73. Oberst A., Dillon C.P., Weinlich R., McCormick L.L., Fitzgerald P., Pop C., et al. Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis. Nature 2011, 471:363-367.
74. Lavrik I., Golks A., Krammer P.H. Death receptor signaling. J Cell Sci 2005, 118:265-267.
75. Hao Z., Mak T.W. Type I and type II pathways of Fas-mediated apoptosis are differentially controlled by XIAP. J Mol Cell Biol 2010, 2:63-64.
76. Remijsen Q., Goossens V., Grootjans S., Van den Haute C., Vanlangenakker N., Dondelinger Y., et al. Depletion of RIPK3 or MLKL blocks TNF-driven necroptosis and switches towards a delayed RIPK1 kinase-dependent apoptosis. Cell Death Dis 2014, 5:e1004.
77. Cai Z., Jitkaew S., Zhao J., Chiang H.C., Choksi S., Liu J., et al. Plasma membrane translocation of trimerized MLKL protein is required for TNF-induced necroptosis. Nat Cell Biol 2014, 16:55-65.
78. Kaiser W.J., Sridharan H., Huang C., Mandal P., Upton J.W., Gough P.J., et al. Toll-like receptor 3-mediated necrosis via TRIF, RIP3, and MLKL. J Biol Chem 2013, 288:31268-31279.
79. Murphy J.M., Czabotar P.E., Hildebrand J.M., Lucet I.S., Zhang J.G., Alvarez-Diaz S., et al. The pseudokinase MLKL mediates necroptosis via a molecular switch mechanism. Immunity 2013, 39:443-453.
80. Wu J., Huang Z., Ren J., Zhang Z., He P., Li Y., et al. Mlkl knockout mice demonstrate the indispensable role of Mlkl in necroptosis. Cell Res 2013, 23:994-1006.
81. Zhao J., Jitkaew S., Cai Z., Choksi S., Li Q., Luo J., et al. Mixed lineage kinase domain-like is a key receptor interacting protein 3 downstream component of TNF-induced necrosis. Proc Natl Acad Sci USA 2012, 109:5322-5327.
82. Sun L., Wang H., Wang Z., He S., Chen S., Liao D., et al. Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 2012, 148:213-227.
83. Wang Z., Jiang H., Chen S., Du F., Wang X. The mitochondrial phosphatase PGAM5 functions at the convergence point of multiple necrotic death pathways. Cell 2012, 148:228-243.
84. Chan F.K., Baehrecke E.H. RIP3 finds partners in crime. Cell 2012, 148:17-18.
85. Kanamaru Y., Sekine S., Ichijo H., Takeda K. The phosphorylation-dependent regulation of mitochondrial proteins in stress responses. J Signal Transduct 2012, 2012:931215.
86. Suen D.F., Norris K.L., Youle R.J. Mitochondrial dynamics and apoptosis. Genes Dev 2008, 22:1577-1590.
87. Braegger C.P., Nicholls S., Murch S.H., Stephens S., MacDonald T.T. Tumour necrosis factor alpha in stool as a marker of intestinal inflammation. Lancet 1992, 339:89-91.
88. Breese E.J., Michie C.A., Nicholls S.W., Murch S.H., Williams C.B., Domizio P., et al. Tumor necrosis factor alpha-producing cells in the intestinal mucosa of children with inflammatory bowel disease. Gastroenterology 1994, 106:1455-1466.
89. Komatsu M., Kobayashi D., Saito K., Furuya D., Yagihashi A., Araake H., et al. Tumor necrosis factor-alpha in serum of patients with inflammatory bowel disease as measured by a highly sensitive immuno-PCR. Clin Chem 2001, 47:1297-1301.
90. MacDonald T.T., Hutchings P., Choy M.Y., Murch S., Cooke A. Tumour necrosis factor-alpha and interferon-gamma production measured at the single cell level in normal and inflamed human intestine. Clin Exp Immunol 1990, 81:301-305.
91. Hampe J., Shaw S.H., Saiz R., Leysens N., Lantermann A., Mascheretti S., et al. Linkage of inflammatory bowel disease to human chromosome 6p. Am J Hum Genet 1999, 65:1647-1655.
92. Dechairo B., Dimon C., van Heel D., Mackay I., Edwards M., Scambler P., et al. Replication and extension studies of inflammatory bowel disease susceptibility regions confirm linkage to chromosome 6p (IBD3). Eur J Hum Genet 2001, 9:627-633.
93. Rioux J.D., Silverberg M.S., Daly M.J., Steinhart A.H., McLeod R.S., Griffiths A.M., et al. Genomewide search in Canadian families with inflammatory bowel disease reveals two novel susceptibility loci. Am J Hum Genet 2000, 66:1863-1870.
94. Danese S., Colombel J.F., Peyrin-Biroulet L., Rutgeerts P., Reinisch W. Review article: the role of anti-TNF in the management of ulcerative colitis-past, present and future. Aliment Pharmacol Ther 2013, 37:855-866.
95. Hanauer S.B., Sandborn W.J., Rutgeerts P., Fedorak R.N., Lukas M., MacIntosh D., et al. Human anti-tumor necrosis factor monoclonal antibody (adalimumab) in Crohn's disease: the CLASSIC-I trial. Gastroenterology 2006, 130:323-333. quiz 591.
96. Neurath M.F. New targets for mucosal healing and therapy in inflammatory bowel diseases. Mucosal Immunol 2014, 7:6-19.
97. Sandborn W.J., Hanauer S.B. Antitumor necrosis factor therapy for inflammatory bowel disease: a review of agents, pharmacology, clinical results, and safety. Inflamm Bowel Dis 1999, 5:119-133.
98. Van den Brande J.M., Koehler T.C., Zelinkova Z., Bennink R.J., te Velde A.A., ten Cate F.J., et al. Prediction of antitumour necrosis factor clinical efficacy by real-time visualisation of apoptosis in patients with Crohn's disease. Gut 2007, 56:509-517.
99. Su L., Nalle S.C., Shen L., Turner E.S., Singh G., Breskin L.A., et al. TNFR2 activates MLCK-dependent tight junction dysregulation to cause apoptosis-mediated barrier loss and experimental colitis. Gastroenterology 2013, 145:407-415.
100. Laukoetter M.G., Nava P., Nusrat A. Role of the intestinal barrier in inflammatory bowel disease. World J Gastroenterol 2008, 14:401-407.
101. Hering N.A., Fromm M., Schulzke J.D. Determinants of colonic barrier function in inflammatory bowel disease and potential therapeutics. J Physiol 2012, 590:1035-1044.
102. McGuckin M.A., Eri R., Simms L.A., Florin T.H., Radford-Smith G. Intestinal barrier dysfunction in inflammatory bowel diseases. Inflamm Bowel Dis 2009, 15:100-113.
103. Williams J.M., Duckworth C.A., Watson A.J., Frey M.R., Miguel J.C., Burkitt M.D., et al. A mouse model of pathological small intestinal epithelial cell apoptosis and shedding induced by systemic administration of lipopolysaccharide. Dis Model Mech 2013, 6:1388-1399.
104. Marchiando A.M., Shen L., Graham W.V., Edelblum K.L., Duckworth C.A., Guan Y., et al. The epithelial barrier is maintained by in vivo tight junction expansion during pathologic intestinal epithelial shedding. Gastroenterology 2011, 140. 1208-18.e1-2.
105. McAllister C.S., Lakhdari O., Pineton de Chambrun G., Gareau M.G., Broquet A., Lee G.H., et al. TLR3, TRIF, and caspase 8 determine double-stranded RNA-induced epithelial cell death and survival in vivo. J Immunol 2013, 190:418-427.
106. Wang C.Y., Mayo M.W., Korneluk R.G., Goeddel D.V., Baldwin A.S. NF-kappaB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 1998, 281:1680-1683.
107. Williams J.M., Duckworth C.A., Watson A.J., Frey M.R., Miguel J.C., Burkitt M.D., et al. A mouse model of pathological small intestinal epithelial cell apoptosis and shedding induced by systemic administration of lipopolysaccharide. Dis Model Mech 2013.
108. Fukushima H., Matsumoto A., Inuzuka H., Zhai B., Lau A.W., Wan L., et al. SCF(Fbw7) modulates the NFkB signaling pathway by targeting NFkB2 for ubiquitination and destruction. Cell Rep 2012, 1:434-443.
109. Basak S., Kim H., Kearns J.D., Tergaonkar V., O'Dea E., Werner S.L., et al. A fourth IkappaB protein within the NF-kappaB signaling module. Cell 2007, 128:369-381.
110. Fukata M., Abreu M.T. TLR4 signalling in the intestine in health and disease. Biochem Soc Trans 2007, 35:1473-1478.
111. Cario E. Toll-like receptors in inflammatory bowel diseases: a decade later. Inflamm Bowel Dis 2010, 16:1583-1597.
112. Frolova L., Drastich P., Rossmann P., Klimesova K., Tlaskalova-Hogenova H. Expression of Toll-like receptor 2 (TLR2), TLR4, and CD14 in biopsy samples of patients with inflammatory bowel diseases: upregulated expression of TLR2 in terminal ileum of patients with ulcerative colitis. J Histochem Cytochem 2008, 56:267-274.
113. Lavelle E.C., Murphy C., O'Neill L.A., Creagh E.M. The role of TLRs, NLRs, and RLRs in mucosal innate immunity and homeostasis. Mucosal Immunol 2010, 3:17-28.
114. Cario E. Microbiota and innate immunity in intestinal inflammation and neoplasia. Curr Opin Gastroenterol 2013, 29:85-91.
115. Abreu M.T., Vora P., Faure E., Thomas L.S., Arnold E.T., Arditi M. Decreased expression of Toll-like receptor-4 and MD-2 correlates with intestinal epithelial cell protection against dysregulated proinflammatory gene expression in response to bacterial lipopolysaccharide. J Immunol 2001, 167:1609-1616.
116. Hausmann M., Kiessling S., Mestermann S., Webb G., Spottl T., Andus T., et al. Toll-like receptors 2 and 4 are up-regulated during intestinal inflammation. Gastroenterology 2002, 122:1987-2000.
117. Cario E., Podolsky D.K. Differential alteration in intestinal epithelial cell expression of toll-like receptor 3 (TLR3) and TLR4 in inflammatory bowel disease. Infect Immun 2000, 68:7010-7017.
118. Meijssen M.A., Brandwein S.L., Reinecker H.C., Bhan A.K., Podolsky D.K. Alteration of gene expression by intestinal epithelial cells precedes colitis in interleukin-2-deficient mice. Am J Physiol 1998, 274:G472-G479.
119. Cario E., Golenbock D.T., Visintin A., Runzi M., Gerken G., Podolsky D.K. Trypsin-sensitive modulation of intestinal epithelial MD-2 as mechanism of lipopolysaccharide tolerance. J Immunol 2006, 176:4258-4266.
120. Leaphart C.L., Cavallo J., Gribar S.C., Cetin S., Li J., Branca M.F., et al. A critical role for TLR4 in the pathogenesis of necrotizing enterocolitis by modulating intestinal injury and repair. J Immunol 2007, 179:4808-4820.
121. Sodhi C.P., Shi X.H., Richardson W.M., Grant Z.S., Shapiro R.A., Prindle T., et al. Toll-like receptor-4 inhibits enterocyte proliferation via impaired beta-catenin signaling in necrotizing enterocolitis. Gastroenterology 2010, 138:185-196.
122. Hackam D.J., Afrazi A., Good M., Sodhi C.P. Innate immune signaling in the pathogenesis of necrotizing enterocolitis. Clin Dev Immunol 2013, 2013:475415.
123. Young J.A., He T.H., Reizis B., Winoto A. Commensal microbiota are required for systemic inflammation triggered by necrotic dendritic cells. Cell Rep 2013, 3:1932-1944.
124. Ma Y., Temkin V., Liu H., Pope R.M. NF-kappaB protects macrophages from lipopolysaccharide-induced cell death: the role of caspase 8 and receptor-interacting protein. J Biol Chem 2005, 280:41827-41834.
125. Hornef M.W., Frisan T., Vandewalle A., Normark S., Richter-Dahlfors A. Toll-like receptor 4 resides in the Golgi apparatus and colocalizes with internalized lipopolysaccharide in intestinal epithelial cells. J Exp Med 2002, 195:559-570.
126. Pott J., Stockinger S., Torow N., Smoczek A., Lindner C., McInerney G., et al. Age-dependent TLR3 expression of the intestinal epithelium contributes to rotavirus susceptibility. PLoS Pathog 2012, 8:e1002670.
127. Vijay-Kumar M., Wu H., Aitken J., Kolachala V.L., Neish A.S., Sitaraman S.V., et al. Activation of toll-like receptor 3 protects against DSS-induced acute colitis. Inflamm Bowel Dis 2007, 13:856-864.
128. Ioannidis I., Ye F., McNally B., Willette M., Flano E. Toll-like receptor expression and induction of type I and type III interferons in primary airway epithelial cells. J Virol 2013, 87:3261-3270.
129. Noppert S.J., Fitzgerald K.A., Hertzog P.J. The role of type I interferons in TLR responses. Immunol Cell Biol 2007, 85:446-457.
130. Yamamoto M., Sato S., Mori K., Hoshino K., Takeuchi O., Takeda K., et al. Cutting edge: a novel Toll/IL-1 receptor domain-containing adapter that preferentially activates the IFN-beta promoter in the Toll-like receptor signaling. J Immunol 2002, 169:6668-6672.
131. Oshiumi H., Matsumoto M., Funami K., Akazawa T., Seya T. TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-beta induction. Nat Immunol 2003, 4:161-167.
132. Feoktistova M., Geserick P., Kellert B., Dimitrova D.P., Langlais C., Hupe M., et al. cIAPs block Ripoptosome formation, a RIP1/caspase-8 containing intracellular cell death complex differentially regulated by cFLIP isoforms. Mol Cell 2011, 43:449-463.
133. Robinson N., McComb S., Mulligan R., Dudani R., Krishnan L., Sad S. Type I interferon induces necroptosis in macrophages during infection with Salmonella enterica serovar typhimurium. Nat Immunol 2012, 13:954-962.
134. Swider A., Siegel R., Eskdale J., Gallagher G. Regulation of interferon lambda-1 (IFNL1/IFN-lambda1/IL-29) expression in human colon epithelial cells. Cytokine 2014, 65:17-23.
135. Thapa R.J., Nogusa S., Chen P., Maki J.L., Lerro A., Andrake M., et al. Interferon-induced RIP1/RIP3-mediated necrosis requires PKR and is licensed by FADD and caspases. Proc Natl Acad Sci USA 2013, 110:E3109-E3118.