TLR3, TRIF, and caspase 8 determine double-stranded RNA-induced epithelial cell death and survival in vivo

Journal of Immunology

Volumn 190, Issue 1, 2013, Pages 418-427

  McAllister, Christopher S ^a   Lakhdari, Omar ^a   De Chambrun, Guillaume Pineton ^a   Gareau, Mélanie G ^a   Broquet, Alexis ^a,b   Lee, Gin Hyug ^a,c   Shenouda, Steven ^a   Eckmann, Lars ^a   Kagnoff, Martin F ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITÉ DE NANTES   (France)

^c University of Ulsan College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 8; DOUBLE STRANDED RNA; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON RECEPTOR; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 1; INTERLEUKIN 15; INTERLEUKIN 6; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TUMOR NECROSIS FACTOR;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CELL PROTECTION; CELL SPECIFICITY; CELL SURVIVAL; CONTROLLED STUDY; DENDRITIC CELL; DIARRHEA; ENZYME ACTIVATION; EPITHELIUM CELL; HEMATOPOIETIC CELL; IN VIVO STUDY; INTESTINE EPITHELIUM CELL; INTESTINE FUNCTION; INTESTINE VILLUS; MOUSE; MUCOSAL IMMUNITY; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SMALL INTESTINE MUCOSA;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; CASPASE 8; CELL DEATH; CELL SURVIVAL; INTESTINAL MUCOSA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; POLY I-C; RNA, VIRAL; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 3;

EID: 84871822317     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202756     Document Type: Article

References (67)

1. Abreu, M. T. 2010. Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat. Rev. Immunol. 10: 131-144.
2. Kawai, T., and S. Akira. 2008. Toll-like receptor and RIG-I-like receptor signaling. Ann. N. Y. Acad. Sci. 1143: 1-20.
3. Thompson, A. J. V., and S. A. Locarnini. 2007. Toll-like receptors, RIG-I-like RNA helicases and the antiviral innate immune response. Immunol. Cell Biol. 85: 435-445. (Pubitemid 47367510)
4. Zhou, R., H. Wei, R. Sun, and Z. Tian. 2007. Recognition of double-stranded RNA by TLR3 induces severe small intestinal injury in mice. J. Immunol. 178: 4548-4556. (Pubitemid 46492407)
5. Clarke, P., and K. L. Tyler. 2009. Apoptosis in animal models of virus-induced disease. Nat. Rev. Microbiol. 7: 144-155.
6. Chattopadhyay, S., J. T. Marques, M. Yamashita, K. L. Peters, K. Smith, A. Desai, B. R. Williams, and G. C. Sen. 2010. Viral apoptosis is induced by IRF-3-mediated activation of Bax. EMBO J. 29: 1762-1773.
7. Kalai, M., G. Van Loo, T. Vanden Berghe, A. Meeus, W. Burm, X. Saelens, and P. Vandenabeele. 2002. Tipping the balance between necrosis and apoptosis in human and murine cells treated with interferon and dsRNA. Cell Death Differ. 9: 981-994. (Pubitemid 35023613)
8. Kaiser, W. J., and M. K. Offermann. 2005. Apoptosis induced by the Toll-like receptor adaptor TRIF is dependent on its receptor interacting protein homotypic interaction motif. J. Immunol. 174: 4942-4952. (Pubitemid 40514460)
9. Feoktistova, M., P. Geserick, B. Kellert, D. P. Dimitrova, C. Langlais, M. Hupe, K. Cain, M. MacFarlane, G. Häcker, and M. Leverkus. 2011. cIAPs block Ripoptosome formation, a RIP1/caspase-8 containing intracellular cell death complex differentially regulated by cFLIP isoforms. Mol. Cell 43: 449-463.
10. Estornes, Y., F. Toscano, F. Virard, G. Jacquemin, A. Pierrot, B. Vanbervliet, M. Bonnin, N. Lalaoui, P. Mercier-Gouy, Y. Pacheco, et al. 2012. dsRNA induces apoptosis through an atypical death complex associating TLR3 to caspase-8. Cell Death Differ. 19: 1482-1494.
11. Van Herreweghe, F., N. Festjens, W. Declercq, and P. Vandenabeele. 2010. Tumor necrosis factor-mediated cell death: to break or to burst, that's the question. Cell. Mol. Life Sci. 67: 1567-1579.
12. Piguet, P. F., C. Vesin, J. Guo, Y. Donati, and C. Barazzone. 1998. TNF-induced enterocyte apoptosis in mice is mediated by the TNF receptor 1 and does not require p53. Eur. J. Immunol. 28: 3499-3505.
13. Lau, K. S., A. M. Juchheim, K. R. Cavaliere, S. R. Philips, D. A. Lauffenburger, and K. M. Haigis. 2011. In vivo systems analysis identifies spatial and temporal aspects of the modulation of TNF-α-induced apoptosis and proliferation by MAPKs. Sci. Signal. 4: ra16.
14. Beisner, D. R., I. L. Ch'en, R. V. Kolla, A. Hoffmann, and S. M. Hedrick. 2005. Cutting edge: innate immunity conferred by B cells is regulated by caspase-8. J. Immunol. 175: 3469-3473. (Pubitemid 41292003)
15. 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. (Pubitemid 34984848)
16. Günther, C., E. Martini, N. Wittkopf, K. Amann, B. Weigmann, H. Neumann, M. J. Waldner, S. M. Hedrick, S. Tenzer, M. F. Neurath, and C. Becker. 2011. Caspase-8 regulates TNF-α-induced epithelial necroptosis and terminal ileitis. Nature 477: 335-339.
17. Hoebe, K., X. Du, P. Georgel, E. Janssen, K. Tabeta, S. O. Kim, J. Goode, P. Lin, N. Mann, S. Mudd, et al. 2003. Identification of Lps2 as a key transducer of MyD88-independent TIR signalling. Nature 424: 743-748. (Pubitemid 37021696)
18. Knudson, C. M., K. S. Tung, W. G. Tourtellotte, G. A. Brown, and S. J. Korsmeyer. 1995. Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270: 96-99.
19. Mombaerts, P., J. Iacomini, R. S. Johnson, K. Herrup, S. Tonegawa, and V. E. Papaioannou. 1992. RAG-1-deficient mice have no mature B and T lymphocytes. Cell 68: 869-877.
20. Kopf, M., H. Baumann, G. Freer, M. Freudenberg, M. Lamers, T. Kishimoto, R. Zinkernagel, H. Bluethmann, and G. Köhler. 1994. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 368: 339-342. (Pubitemid 24104268)
21. Glaccum, M. B., K. L. Stocking, K. Charrier, J. L. Smith, C. R. Willis, C. Maliszewski, D. J. Livingston, J. J. Peschon, and P. J. Morrissey. 1997. Phenotypic and functional characterization of mice that lack the type I receptor for IL-1. J. Immunol. 159: 3364-3371. (Pubitemid 127482095)
22. Kennedy, M. K., M. Glaccum, S. N. Brown, E. A. Butz, J. L. Viney, M. Embers, N. Matsuki, K. Charrier, L. Sedger, C. R. Willis, et al. 2000. Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J. Exp. Med. 191: 771-780.
23. Van Uden, J. H., C. H. Tran, D. A. Carson, and E. Raz. 2001. Type I interferon is required to mount an adaptive response to immunostimulatory DNA. Eur. J. Immunol. 31: 3281-3290.
24. Yang, Y. L., L. F. Reis, J. Pavlovic, A. Aguzzi, R. Schäfer, A. Kumar, B. R. Williams, M. Aguet, and C. Weissmann. 1995. Deficient signaling in mice devoid of double-stranded RNA-dependent protein kinase. EMBO J. 14: 6095-6106. (Pubitemid 26007297)
25. Honda, K., S. Sakaguchi, C. Nakajima, A. Watanabe, H. Yanai, M. Matsumoto, T. Ohteki, T. Kaisho, A. Takaoka, S. Akira, et al. 2003. Selective contribution of IFN-α/β signaling to the maturation of dendritic cells induced by double-stranded RNA or viral infection. Proc. Natl. Acad. Sci. USA 100: 10872-10877. (Pubitemid 37140120)
26. Abe, K., K. P. Nguyen, S. D. Fine, J.-H. Mo, C. Shen, S. Shenouda, M. Corr, S. Jung, J. Lee, L. Eckmann, and E. Raz. 2007. Conventional dendritic cells regulate the outcome of colonic inflammation independently of T cells. Proc. Natl. Acad. Sci. USA 104: 17022-17027. (Pubitemid 350210984)
27. Eckmann, L., T. Nebelsiek, A. A. Fingerle, S. M. Dann, J. Mages, R. Lang, S. Robine, M. F. Kagnoff, R. M. Schmid, M. Karin, et al. 2008. Opposing functions of IKKβ during acute and chronic intestinal inflammation. Proc. Natl. Acad. Sci. USA 105: 15058-15063.
28. 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)
29. Hoshino, K., O. Takeuchi, T. Kawai, H. Sanjo, T. Ogawa, Y. Takeda, K. Takeda, and S. Akira. 1999. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide - evidence for TLR4 as the Lps gene product. J. Immunol. 162: 3749-3752. (Pubitemid 29314747)
30. Sato, M., H. Suemori, N. Hata, M. Asagiri, K. Ogasawara, K. Nakao, T. Nakaya, M. Katsuki, S. Noguchi, N. Tanaka, and T. Taniguchi. 2000. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-α/β gene induction. Immunity 13: 539-548.
31. Sun, Q., L. Sun, H. H. Liu, X. Chen, R. B. Seth, J. Forman, and Z. J. Chen. 2006. The specific and essential role of MAVS in antiviral innate immune responses. Immunity 24: 633-642. (Pubitemid 43728147)
32. Maaser, C., M. P. Housley, M. Iimura, J. R. Smith, B. A. Vallance, B. B. Finlay, J. R. Schreiber, N. M. Varki, M. F. Kagnoff, and L. Eckmann. 2004. Clearance of Citrobacter rodentium requires B cells but not secretory immunoglobulin A (IgA) or IgM antibodies. Infect. Immun. 72: 3315-3324. (Pubitemid 38697754)
33. Gareau, M. G., J. Jury, G. MacQueen, P. M. Sherman, and M. H. Perdue. 2007. Probiotic treatment of rat pups normalises corticosterone release and ameliorates colonic dysfunction induced by maternal separation. Gut 56: 1522-1528. (Pubitemid 350033189)
34. Fan, Y., and A. Bergmann. 2010. The cleaved-caspase-3 antibody is a marker of caspase-9-like DRONC activity in Drosophila. Cell Death Differ. 17: 534-539.
35. Scheuner, D., R. Patel, F. Wang, K. Lee, K. Kumar, J. Wu, A. Nilsson, M. Karin, and R. J. Kaufman. 2006. Double-stranded RNA-dependent protein kinase phosphorylation of the α-subunit of eukaryotic translation initiation factor 2 mediates apoptosis. J. Biol. Chem. 281: 21458-21468. (Pubitemid 44115484)
36. Balachandran, S., P. C. Roberts, T. Kipperman, K. N. Bhalla, R. W. Compans, D. R. Archer, and G. N. Barber. 2000. α/β Interferons potentiate virus-induced apoptosis through activation of the FADD/caspase-8 death signaling pathway. J. Virol. 74: 1513-1523. (Pubitemid 30044102)
37. Jiang, Z., T. W. Mak, G. Sen, and X. Li. 2004. Toll-like receptor 3-mediated activation of NF-κB and IRF3 diverges at Toll-IL-1 receptor domain-containing adapter inducing IFN-β. Proc. Natl. Acad. Sci. USA 101: 3533-3538. (Pubitemid 38338230)
38. Egan, L. J., L. Eckmann, F. R. Greten, S. Chae, Z. W. Li, G. M. Myhre, S. Robine, M. Karin, and M. F. Kagnoff. 2004. IκB-kinase β-dependent NF-κB activation provides radioprotection to the intestinal epithelium. Proc. Natl. Acad. Sci. USA 101: 2452-2457. (Pubitemid 38269332)
39. Page, S. T., N. S. van Oers, R. M. Perlmutter, A. Weiss, and A. M. Pullen. 1997. Differential contribution of Lck and Fyn protein tyrosine kinases to intraepithelial lymphocyte development. Eur. J. Immunol. 27: 554-562. (Pubitemid 27085263)
40. Mocarski, E. S., J. W. Upton, and W. J. Kaiser. 2012. Viral infection and the evolution of caspase 8-regulated apoptotic and necrotic death pathways. Nat. Rev. Immunol. 12: 79-88.
41. Broquet, A. H., Y. Hirata, C. S. McAllister, and M. F. Kagnoff. 2011. RIG-I/MDA5/MAVS are required to signal a protective IFN response in rotavirus-infected intestinal epithelium. J. Immunol. 186: 1618-1626.
42. Hirata, Y., A. H. Broquet, L. Menchén, and M. F. Kagnoff. 2007. Activation of innate immune defense mechanisms by signaling through RIG-I/IPS-1 in intestinal epithelial cells. J. Immunol. 179: 5425-5432.
43. Linkermann, A., J. H. Brasen, F. De Zen, R. Weinlich, R. A. Schwendener, D. R. Green, U. Kunzendorf, and S. Krautwald. 2012. Dichotomy between RIP1- and RIP3-mediated necroptosis in tumor necrosis factor α-induced shock. Mol. Med. 18: 577-586.
44. Elewaut, D., J. A. DiDonato, J. M. Kim, F. Truong, L. Eckmann, and M. F. Kagnoff. 1999. NF-κB is a central regulator of the intestinal epithelial cell innate immune response induced by infection with enteroinvasive bacteria. J. Immunol. 163: 1457-1466. (Pubitemid 29352767)
45. Chae, S., L. Eckmann, Y. Miyamoto, C. Pothoulakis, M. Karin, and M. F. Kagnoff. 2006. Epithelial cell IκB-kinase β has an important protective role in Clostridium difficile toxin A-induced mucosal injury. J. Immunol. 177: 1214-1220. (Pubitemid 44036626)
46. Leist, M., F. Gantner, I. Bohlinger, G. Tiegs, P. G. Germann, and A. Wendel. 1995. Tumor necrosis factor-induced hepatocyte apoptosis precedes liver failure in experimental murine shock models. Am. J. Pathol. 146: 1220-1234.
47. Jiang, Q., H. Wei, and Z. Tian. 2008. Poly I:C enhances cycloheximide-induced apoptosis of tumor cells through TLR3 pathway. BMC Cancer 8: 12.
48. Plümpe, J., N. P. Malek, C. T. Bock, T. Rakemann, M. P. Manns, and C. Trautwein. 2000. NF-κB determines between apoptosis and proliferation in hepatocytes during liver regeneration. Am. J. Physiol. Gastrointest. Liver Physiol. 278: G173-G183. (Pubitemid 30108082)
49. Inan, M. S., V. Tolmacheva, Q. S. Wang, D. W. Rosenberg, and C. Giardina. 2000. Transcription factor NF-κB participates in regulation of epithelial cell turnover in the colon. Am. J. Physiol. Gastrointest. Liver Physiol. 279: G1282-G1291.
50. Tong, X., L. Yin, R. Washington, D. W. Rosenberg, and C. Giardina. 2004. The p50-p50 NF-κB complex as a stimulus-specific repressor of gene activation. Mol. Cell. Biochem. 265: 171-183. (Pubitemid 41461877)
51. Toruner, M., M. Fernandez-Zapico, J. J. Sha, L. Pham, R. Urrutia, and L. J. Egan. 2006. Antianoikis effect of nuclear factor-κB through up-regulated expression of osteoprotegerin, BCL-2, and IAP-1. J. Biol. Chem. 281: 8686-8696. (Pubitemid 43847973)
52. Davidson, G. P., and G. L. Barnes. 1979. Structural and functional abnormalities of the small intestine in infants and young children with rotavirus enteritis. Acta Paediatr. Scand. 68: 181-186. (Pubitemid 9098648)
53. Salim, A. F., A. D. Phillips, J. A. Walker-Smith, and M. J. Farthing. 1995. Sequential changes in small intestinal structure and function during rotavirus infection in neonatal rats. Gut 36: 231-238.
54. Otto, P. H., I. N. Clarke, P. R. Lambden, O. Salim, J. Reetz, and E. M. Liebler-Tenorio. 2011. Infection of calves with bovine norovirus GIII.1 strain Jena virus: an experimental model to study the pathogenesis of norovirus infection. J. Virol. 85: 12013-12021.
55. Ahlquist, P. 2006. Parallels among positive-strand RNA viruses, reverse-transcribing viruses and double-stranded RNA viruses. Nat. Rev. Microbiol. 4: 371-382. (Pubitemid 43771855)
56. McCartney, S. A., L. B. Thackray, L. Gitlin, S. Gilfillan, H. W. Virgin, and M. Colonna. 2008. MDA-5 recognition of a murine norovirus. PLoS Pathog. 4: e1000108.
57. Blutt, S. E., M. Fenaux, K. L. Warfield, H. B. Greenberg, and M. E. Conner. 2006. Active viremia in rotavirus-infected mice. J. Virol. 80: 6702-6705. (Pubitemid 43927474)
58. Chiappini, E., C. Azzari, M. Moriondo, L. Galli, and M. de Martino. 2005. Viraemia is a common finding in immunocompetent children with rotavirus infection. J. Med. Virol. 76: 265-267. (Pubitemid 40594013)
59. Crawford, S. E., D. G. Patel, E. Cheng, Z. Berkova, J. M. Hyser, M. Ciarlet, M. J. Finegold, M. E. Conner, and M. K. Estes. 2006. Rotavirus viremia and extraintestinal viral infection in the neonatal rat model. J. Virol. 80: 4820-4832.
60. Moon, S., Y. Wang, P. Dennehy, K. A. Simonsen, J. Zhang, and B. Jiang. 2012. Antigenemia, RNAemia, and innate immunity in children with acute rotavirus diarrhea. FEMS Immunol. Med. Microbiol. 64: 382-391.
61. Pott, J., S. Stockinger, N. Torow, A. Smoczek, C. Lindner, G. McInerney, F. Bäckhed, U. Baumann, O. Pabst, A. Bleich, and M. W. Hornef. 2012. Age-dependent TLR3 expression of the intestinal epithelium contributes to rotavirus susceptibility. PLoS Pathog. 8: e1002670.
62. Zhou, R., H. Wei, R. Sun, J. Zhang, and Z. Tian. 2007. NKG2D recognition mediates Toll-like receptor 3 signaling-induced breakdown of epithelial homeostasis in the small intestines of mice. Proc. Natl. Acad. Sci. USA 104: 7512-7515. (Pubitemid 47185937)
63. Lodolce, J. P., P. R. Burkett, D. L. Boone, M. Chien, and A. Ma. 2001. T cell-independent interleukin 15Rα signals are required for bystander proliferation. J. Exp. Med. 194: 1187-1194.
64. Karikó, K., H. Ni, J. Capodici, M. Lamphier, and D. Weissman. 2004. mRNA is an endogenous ligand for Toll-like receptor 3. J. Biol. Chem. 279: 12542-12550. (Pubitemid 38445825)
65. Brentano, F., O. Schorr, R. E. Gay, S. Gay, and D. Kyburz. 2005. RNA released from necrotic synovial fluid cells activates rheumatoid arthritis synovial fibroblasts via Toll-like receptor 3. Arthritis Rheum. 52: 2656-2665. (Pubitemid 41369093)
66. Murray, L. A., D. A. Knight, L. McAlonan, R. Argentieri, A. Joshi, F. Shaheen, M. Cunningham, L. Alexopolou, R. A. Flavell, R. T. Sarisky, and C. M. Hogaboam. 2008. Deleterious role of TLR3 during hyperoxia-induced acute lung injury. Am. J. Respir. Crit. Care Med. 178: 1227-1237.
67. Cavassani, K. A., M. Ishii, H. Wen, M. A. Schaller, P. M. Lincoln, N. W. Lukacs, C. M. Hogaboam, and S. L. Kunkel. 2008. TLR3 is an endogenous sensor of tissue necrosis during acute inflammatory events. J. Exp. Med. 205: 2609-2621.