NEMO Prevents RIP Kinase 1-Mediated Epithelial Cell Death and Chronic Intestinal Inflammation by NF-κB-Dependent and -Independent Functions

Immunity

Volumn 44, Issue 3, 2016, Pages 553-567

  Vlantis, Katerina ^a   Wullaert, Andy ^a,f   Polykratis, Apostolos ^a   Kondylis, Vangelis ^a   Dannappel, Marius ^a   Schwarzer, Robin ^a   Welz, Patrick ^a,g   Corona, Teresa ^a   Walczak, Henning ^b   Weih, Falk ^c   Klein, Ulf ^d   Kelliher, Michelle ^e   Pasparakis, Manolis ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c FRITZ LIPMANN INSTITUTE   (Germany)

^d Och Spine at New York Presbyterian Hospitals   (United States)

^e UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^f GHENT UNIVERSITY   (Belgium)

^g INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

FAS ASSOCIATED DEATH DOMAIN PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN ESSENTIAL MODULATOR; PROTEIN KINASE; RECEPTOR INTERACTING PROTEIN KINASE 1; UNCLASSIFIED DRUG; FADD PROTEIN, MOUSE; NEMO PROTEIN, MOUSE; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE; RELA PROTEIN, MOUSE; RELB PROTEIN, MOUSE; RIPK1 PROTEIN, MOUSE; SIGNAL PEPTIDE; TRANSCRIPTION FACTOR REL; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR RELB;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DEATH; CELL LOSS; CHRONIC DISEASE; COLITIS; CONTROLLED STUDY; DISEASE COURSE; ENTERITIS; ENZYME ACTIVITY; ENZYME INHIBITION; EPITHELIUM CELL; GENE MUTATION; MOUSE; NONHUMAN; PANETH CELL; PRIORITY JOURNAL; ANIMAL; APOPTOSIS; C57BL MOUSE; CELL CULTURE; GENETICS; HUMAN; IMMUNOLOGY; INFLAMMATORY BOWEL DISEASE; INTESTINE MUCOSA; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ANIMALS; APOPTOSIS; CELLS, CULTURED; FAS-ASSOCIATED DEATH DOMAIN PROTEIN; HUMANS; INFLAMMATORY BOWEL DISEASES; INTESTINAL MUCOSA; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-KAPPA B; PANETH CELLS; PROTO-ONCOGENE PROTEINS C-REL; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR RELB;

EID: 84960363656     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2016.02.020     Document Type: Article

References (38)

1. Alcamo E., Mizgerd J.P., Horwitz B.H., Bronson R., Beg A.A., Scott M., Doerschuk C.M., Hynes R.O., Baltimore D. Targeted mutation of TNF receptor I rescues the RelA-deficient mouse and reveals a critical role for NF-kappa B in leukocyte recruitment. J. Immunol. 2001, 167:1592-1600.
2. Blumberg R., Powrie F. Microbiota, disease, and back to health: a metastable journey. Sci. Transl. Med. 2012, 4:137rv7.
3. Dannappel M., Vlantis K., Kumari S., Polykratis A., Kim C., Wachsmuth L., Eftychi C., Lin J., Corona T., Hermance N., et al. RIPK1 maintains epithelial homeostasis by inhibiting apoptosis and necroptosis. Nature 2014, 513:90-94.
4. Dillon C.P., Weinlich R., Rodriguez D.A., Cripps J.G., Quarato G., Gurung P., Verbist K.C., Brewer T.L., Llambi F., Gong Y.N., et al. RIPK1 blocks early postnatal lethality mediated by caspase-8 and RIPK3. Cell 2014, 157:1189-1202.
5. Dondelinger Y., Jouan-Lanhouet S., Divert T., Theatre E., Bertin J., Gough P.J., Giansanti P., Heck A.J., Dejardin E., Vandenabeele P., Bertrand M.J. NF-κB-Independent Role of IKKα/IKKβ in Preventing RIPK1 Kinase-Dependent Apoptotic and Necroptotic Cell Death during TNF Signaling. Mol. Cell 2015, 60:63-76.
6. Eckmann L., Nebelsiek T., Fingerle A.A., Dann S.M., Mages J., Lang R., Robine S., Kagnoff M.F., Schmid R.M., Karin M., et al. Opposing functions of IKKbeta during acute and chronic intestinal inflammation. Proc. Natl. Acad. Sci. USA 2008, 105:15058-15063.
7. Fish J.D., Duerst R.E., Gelfand E.W., Orange J.S., Bunin N. Challenges in the use of allogeneic hematopoietic SCT for ectodermal dysplasia with immune deficiency. Bone Marrow Transplant. 2009, 43:217-221.
8. Hanson E.P., Monaco-Shawver L., Solt L.A., Madge L.A., Banerjee P.P., May M.J., Orange J.S. Hypomorphic nuclear factor-kappaB essential modulator mutation database and reconstitution system identifies phenotypic and immunologic diversity. J Allergy Clin Immunol 2008, 122:1169-1177.e1116.
9. Hooper L.V., Littman D.R., Macpherson A.J. Interactions between the microbiota and the immune system. Science 2012, 336:1268-1273.
10. Ireland H., Houghton C., Howard L., Winton D.J. Cellular inheritance of a Cre-activated reporter gene to determine Paneth cell longevity in the murine small intestine. Dev. Dyn. 2005, 233:1332-1336.
11. Kang T.B., Yang S.H., Toth B., Kovalenko A., Wallach D. Caspase-8 blocks kinase RIPK3-mediated activation of the NLRP3 inflammasome. Immunity 2013, 38:27-40.
12. Karin M., Greten F.R. NF-kappaB: linking inflammation and immunity to cancer development and progression. Nat. Rev. Immunol. 2005, 5:749-759.
13. Kaser A., Zeissig S., Blumberg R.S. Inflammatory bowel disease. Annu. Rev. Immunol. 2010, 28:573-621.
14. Kawai T., Nishikomori R., Heike T. Diagnosis and treatment in anhidrotic ectodermal dysplasia with immunodeficiency. Allergol. Int. 2012, 61:207-217.
15. Lawlor K.E., Khan N., Mildenhall A., Gerlic M., Croker B.A., D'Cruz A.A., Hall C., Kaur Spall S., Anderton H., Masters S.L., et al. RIPK3 promotes cell death and NLRP3 inflammasome activation in the absence of MLKL. Nat. Commun. 2015, 6:6282.
16. Legarda-Addison D., Hase H., O'Donnell M.A., Ting A.T. NEMO/IKKgamma regulates an early NF-kappaB-independent cell-death checkpoint during TNF signaling. Cell Death Differ. 2009, 16:1279-1288.
17. Mizukami T., Obara M., Nishikomori R., Kawai T., Tahara Y., Sameshima N., Marutsuka K., Nakase H., Kimura N., Heike T., Nunoi H. Successful treatment with infliximab for inflammatory colitis in a patient with X-linked anhidrotic ectodermal dysplasia with immunodeficiency. J. Clin. Immunol. 2012, 32:39-49.
18. Moriwaki K., Balaji S., McQuade T., Malhotra N., Kang J., Chan F.K. The necroptosis adaptor RIPK3 promotes injury-induced cytokine expression and tissue repair. Immunity 2014, 41:567-578.
19. Nenci A., Becker C., Wullaert A., Gareus R., van Loo G., Danese S., Huth M., Nikolaev A., Neufert C., Madison B., et al. Epithelial NEMO links innate immunity to chronic intestinal inflammation. Nature 2007, 446:557-561.
20. O'Donnell M.A., Hase H., Legarda D., Ting A.T. NEMO inhibits programmed necrosis in an NFκB-independent manner by restraining RIP1. PLoS ONE 2012, 7:e41238.
21. Oeckinghaus A., Ghosh S. The NF-kappaB family of transcription factors and its regulation. Cold Spring Harb. Perspect. Biol. 2009, 1:a000034.
22. Ouellette A.J. Paneth cells and innate mucosal immunity. Curr. Opin. Gastroenterol. 2010, 26:547-553.
23. Pai S.Y., Levy O., Jabara H.H., Glickman J.N., Stoler-Barak L., Sachs J., Nurko S., Orange J.S., Geha R.S. Allogeneic transplantation successfully corrects immune defects, but not susceptibility to colitis, in a patient with nuclear factor-kappaB essential modulator deficiency. J Allergy Clin Immunol 2008, 122:1113-1118.e1111.
24. Pasparakis M. Regulation of tissue homeostasis by NF-kappaB signalling: implications for inflammatory diseases. Nat. Rev. Immunol. 2009, 9:778-788.
25. Pasparakis M., Vandenabeele P. Necroptosis and its role in inflammation. Nature 2015, 517:311-320.
26. Permaul P., Narla A., Hornick J.L., Pai S.Y. Allogeneic hematopoietic stem cell transplantation for X-linked ectodermal dysplasia and immunodeficiency: case report and review of outcomes. Immunol. Res. 2009, 44:89-98.
27. Peyrin-Biroulet L. Anti-TNF therapy in inflammatory bowel diseases: a huge review. Minerva Gastroenterol. Dietol. 2010, 56:233-243.
28. Polykratis A., Hermance N., Zelic M., Roderick J., Kim C., Van T.M., Lee T.H., Chan F.K., Pasparakis M., Kelliher M.A. Cutting edge: RIPK1 Kinase inactive mice are viable and protected from TNF-induced necroptosis in vivo. J. Immunol. 2014, 193:1539-1543.
29. Rickard J.A., O'Donnell J.A., Evans J.M., Lalaoui N., Poh A.R., Rogers T., Vince J.E., Lawlor K.E., Ninnis R.L., Anderton H., et al. RIPK1 regulates RIPK3-MLKL-driven systemic inflammation and emergency hematopoiesis. Cell 2014, 157:1175-1188.
30. Seidelin J.B., Nielsen O.H. Epithelial apoptosis: cause or consequence of ulcerative colitis?. Scand. J. Gastroenterol. 2009, 44:1429-1434.
31. Souza H.S., Tortori C.J., Castelo-Branco M.T., Carvalho A.T., Margallo V.S., Delgado C.F., Dines I., Elia C.C. Apoptosis in the intestinal mucosa of patients with inflammatory bowel disease: evidence of altered expression of FasL and perforin cytotoxic pathways. Int. J. Colorectal Dis. 2005, 20:277-286.
32. 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.
33. Takahashi N., Vereecke L., Bertrand M.J., Duprez L., Berger S.B., Divert T., Gonçalves A., Sze M., Gilbert B., Kourula S., et al. RIPK1 ensures intestinal homeostasis by protecting the epithelium against apoptosis. Nature 2014, 513:95-99.
34. Van Hauwermeiren F., Armaka M., Karagianni N., Kranidioti K., Vandenbroucke R.E., Loges S., Van Roy M., Staelens J., Puimège L., Palagani A., et al. Safe TNF-based antitumor therapy following p55TNFR reduction in intestinal epithelium. J. Clin. Invest. 2013, 123:2590-2603.
35. Wang X., Jiang W., Yan Y., Gong T., Han J., Tian Z., Zhou R. RNA viruses promote activation of the NLRP3 inflammasome through a RIP1-RIP3-DRP1 signaling pathway. Nat. Immunol. 2014, 15:1126-1133.
36. Welz P.S., Wullaert A., Vlantis K., Kondylis V., Fernández-Majada V., Ermolaeva M., Kirsch P., Sterner-Kock A., van Loo G., Pasparakis M. FADD prevents RIP3-mediated epithelial cell necrosis and chronic intestinal inflammation. Nature 2011, 477:330-334.
37. Zaph C., Troy A.E., Taylor B.C., Berman-Booty L.D., Guild K.J., Du Y., Yost E.A., Gruber A.D., May M.J., Greten F.R., et al. Epithelial-cell-intrinsic IKK-beta expression regulates intestinal immune homeostasis. Nature 2007, 446:552-556.
38. Zeissig S., Bojarski C., Buergel N., Mankertz J., Zeitz M., Fromm M., Schulzke J.D. Downregulation of epithelial apoptosis and barrier repair in active Crohn's disease by tumour necrosis factor alpha antibody treatment. Gut 2004, 53:1295-1302.