Toll-like receptor 3-mediated necrosis via TRIF, RIP3, and MLKL

Journal of Biological Chemistry

Volumn 288, Issue 43, 2013, Pages 31268-31279

  Kaiser, William J ^a   Sridharan, Haripriya ^b   Huang, Chunzi ^a   Mandal, Pratyusha ^a   Upton, Jason W ^b   Gough, Peter J ^c   Sehon, Clark A ^c   Marquis, Robert W ^c   Bertin, John ^c   Mocarski, Edward S ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c GLAXOSMITHKLINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL FATE DECISION; KINASE ACTIVITY; KINASE INHIBITORS; PATHOGEN-ASSOCIATED MOLECULAR PATTERNS; PROGRAMMED CELL DEATHS; RECEPTOR-INTERACTING PROTEINS; SMALL MOLECULES; TOLL-LIKE RECEPTORS;

ASSOCIATION REACTIONS; CELL CULTURE; CELL DEATH; CHEMICAL ACTIVATION; ENZYMES; INTERFERONS; SIGNAL TRANSDUCTION; SIGNALING;

CELL SIGNALING;

CASPASE 8; MIXED LINEAGE KINASE DOMAIN LIKE PROTEIN; PROTEIN KINASE; PROTEIN KINASE INHIBITOR; RECEPTOR INTERACTING PROTEIN 3; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL DEATH; CELL FATE; CELL SURVIVAL; CELL VIABILITY; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENETIC TRANSFECTION; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MACROPHAGE; MOUSE; NONHUMAN; PLASMID; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

APOPTOSIS; CASPASE; NECROSIS (NECROTIC DEATH); RIPK3; SERINE/THREONINE PROTEIN KINASE; TOLL-LIKE RECEPTORS (TLR);

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; GLYCOPROTEINS; MICE; MICE, KNOCKOUT; MULTIPROTEIN COMPLEXES; NECROSIS; NIH 3T3 CELLS; PROTEIN KINASE INHIBITORS; PROTEIN KINASES; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 3;

EID: 84886656964     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.462341     Document Type: Article

References (60)

1. Lamkanfi, M., and Dixit, V. M. (2010) Manipulation of host cell death pathways during microbial infections. Cell Host Microbe 8, 44-54
2. Everett, H., and McFadden, G. (1999) Apoptosis: an innate immune response to virus infection. Trends Microbiol. 7, 160-165
3. Kumar, H., Kawai, T., and Akira, S. (2011) Pathogen recognition by the innate immune system. Int. Rev. Immunol. 30, 16-34
4. Kaiser, W. J., and Offermann, M. K. (2005) Apoptosis induced by the toll-like receptor adapter TRIF is dependent on its receptor interacting protein homotypic interaction motif. J. Immunol. 174, 4942-4952
5. He, S., Liang, Y., Shao, F., and Wang, X. (2011) Toll-like receptors activate programmed necrosis in macrophages through a receptor-interacting kinase-3-mediated pathway. Proc. Natl. Acad. Sci. U. S. A. 108, 20054-20059
6. He, S., Wang, L., Miao, L., Wang, T., Du, F., Zhao, L., and Wang, X. (2009) Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-α. Cell 137, 1100-1111
7. Zhang, D. W., Shao, J., Lin, J., Zhang, N., Lu, B. J., Lin, S. C., Dong, M. Q., and Han, J. (2009) RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 325, 332-336
8. Cho, Y. S., Challa, S., Moquin, D., Genga, R., Ray, T. D., Guildford, M., and Chan, F. K. (2009) Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 137, 1112-1123
9. Upton, J. W., Kaiser, W. J., and Mocarski, E. S. (2010) Virus inhibition of RIP3-dependent necrosis. Cell Host Microbe 7, 302-313
10. Mocarski, E. S., Upton, J. W., and Kaiser, W. J. (2012) Viral infection and the evolution of caspase 8-regulated apoptotic and necrotic death pathways. Nat. Rev. Immunol. 12, 79-88
11. Upton, J. W., Kaiser, W. J., and Mocarski, E. S. (2012) DAI/ZBP1/DLM-1 complexes with RIP3 to mediate virus-induced programmed necrosis that is targeted by murine cytomegalovirus vIRA. Cell Host Microbe 11, 290-297
12. Hengartner, M. O. (2000) The biochemistry of apoptosis. Nature 407, 770-776
13. Strasser, A., O'Connor, L., and Dixit, V. M. (2000) Apoptosis signaling. Annu. Rev. Biochem. 69, 217-245
14. Vandenabeele, P., Galluzzi, L., Vanden Berghe, T., and Kroemer, G. (2010) Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat. Rev. Mol. Cell Biol. 11, 700-714
15. Holler, N., Zaru, R., Micheau, O., Thome, M., Attinger, A., Valitutti, S., Bodmer, J. L., Schneider, P., Seed, B., and Tschopp, J. (2000) Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat. Immunol. 1, 489-495
16. Wang, Z., Jiang, H., Chen, S., Du, F., and Wang, X. (2012) The mitochondrial phosphatase PGAM5 functions at the convergence point of multiple necrotic death pathways. Cell 148, 228-243
17. Sun, L., Wang, H., Wang, Z., He, S., Chen, S., Liao, D., Wang, L., Yan, J., Liu, W., Lei, X., and Wang, X. (2012) Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 148, 213-227
18. Zhao, J., Jitkaew, S., Cai, Z., Choksi, S., Li, Q., Luo, J., and Liu, Z. G. (2012) Mixed lineage kinase domain-like is a key receptor interacting protein 3 downstream component of TNF-induced necrosis. Proc. Natl. Acad. Sci. U. S. A. 109, 5322-5327
19. Feoktistova, M., Geserick, P., Kellert, B., Dimitrova, D. P., Langlais, C., Hupe, M., Cain, K., MacFarlane, M., Häcker, G., and Leverkus, M. (2011) cIAPs block ripoptosome formation, a RIP1/caspase-8 containing intracellular cell death complex differentially regulated by cFLIP isoforms. Mol. Cell 43, 449-463
20. Estornes, Y., Toscano, F., Virard, F., Jacquemin, G., Pierrot, A., Vanbervliet, B., Bonnin, M., Lalaoui, N., Mercier-Gouy, P., Pachéco, Y., Salaun, B., Renno, T., Micheau, O., and Lebecque, S. (2012) dsRNA induces apoptosis through an atypical death complex associating TLR3 to caspase-8. Cell Death Differ. 19, 1482-1494
21. Kaiser, W. J., Upton, J. W., Long, A. B., Livingston-Rosanoff, D., Daley-Bauer, L. P., Hakem, R., Caspary, T., and Mocarski, E. S. (2011) RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature 471, 368-372
22. Oberst, A., Dillon, C. P., Weinlich, R., McCormick, L. L., Fitzgerald, P., Pop, C., Hakem, R., Salvesen, G. S., and Green, D. R. (2011) Catalytic activity of the caspase-8-FLIP (L) complex inhibits RIPK3-dependent necrosis. Nature 471, 363-367
23. Feng, S., Yang, Y., Mei, Y., Ma, L., Zhu, D. E., Hoti, N., Castanares, M., and Wu, M. (2007) Cleavage of RIP3 inactivates its caspase-independent apoptosis pathway by removal of kinase domain. Cell. Signal. 19, 2056-2067
24. Lin, Y., Devin, A., Rodriguez, Y., and Liu, Z. G. (1999) Cleavage of the death domain kinase RIP by caspase-8 prompts TNF-induced apoptosis. Genes Dev. 13, 2514-2526
25. Lu, J. V., Weist, B. M., van Raam, B. J., Marro, B. S., Nguyen, L. V., Srinivas, P., Bell, B. D., Luhrs, K. A., Lane, T. E., Salvesen, G. S., and Walsh, C. M. (2011) Complementary roles of FADD and RIPK3 in T cell homeostasis and antiviral immunity. Proc. Natl. Acad. Sci. U. S. A. 108, 15312-15317
26. Chan, F. K., Shisler, J., Bixby, J. G., Felices, M., Zheng, L., Appel, M., Orenstein, J., Moss, B., and Lenardo, M. J. (2003) A role for tumor necrosis factor receptor-2 and receptor-interacting protein in programmed necrosis and antiviral responses. J. Biol. Chem. 278, 51613-51621
27. Thome, M., and Tschopp, J. (2001) Regulation of lymphocyte proliferation and death by FLIP. Nat. Rev. Immunol. 1, 50-58
28. Dillon, C. P., Oberst, A., Weinlich, R., Janke, L. J., Kang, T. B., Ben-Moshe, T., Mak, T. W., Wallach, D., and Green, D. R. (2012) Survival function of the FADD-CASPASE-8-cFLIP (L) complex. Cell Rep. 1, 401-407
29. Meylan, E., Burns, K., Hofmann, K., Blancheteau, V., Martinon, F., Kelliher, M., and Tschopp, J. (2004) RIP1 is an essential mediator of Toll-like receptor 3-induced NF-κB activation. Nat. Immunol. 5, 503-507
30. Vivarelli, M. S., McDonald, D., Miller, M., Cusson, N., Kelliher, M., and Geha, R. S. (2004) RIP links TLR4 to Akt and is essential for cell survival in response to LPS stimulation. J. Exp. Med. 200, 399-404
31. Kalai, M., Van Loo, G., Vanden Berghe, T., Meeus, A., Burm, W., Saelens, X., and Vandenabeele, P. (2002) Tipping the balance between necrosis and apoptosis in human and murine cells treated with interferon and dsRNA. Cell Death Differ. 9, 981-994
32. Upton, J. W., Kaiser, W. J., and Mocarski, E. S. (2008) Cytomegalovirus M45 cell death suppression requires receptor-interacting protein (RIP) homotypic interaction motif (RHIM)-dependent interaction with RIP1. J. Biol. Chem. 283, 16966-16970
33. Rebsamen, M., Heinz, L. X., Meylan, E., Michallet, M. C., Schroder, K., Hofmann, K., Vazquez, J., Benedict, C. A., and Tschopp, J. (2009) DAI/ZBP1 recruits RIP1 and RIP3 through RIP homotypic interaction motifs to activate NF-κB. EMBO Rep. 10, 916-922
34. Brune, W., Ménard, C., Heesemann, J., and Koszinowski, U. H. (2001) A ribonucleotide reductase homolog of cytomegalovirus and endothelial cell tropism. Science 291, 303-305
35. Mack, C., Sickmann, A., Lembo, D., and Brune, W. (2008) Inhibition of proinflammatory and innate immune signaling pathways by a cytomegalovirus RIP1-interacting protein. Proc. Natl. Acad. Sci. U. S. A. 105, 3094-3099
36. Fliss, P. M., Jowers, T. P., Brinkmann, M. M., Holstermann, B., Mack, C., Dickinson, P., Hohenberg, H., Ghazal, P., and Brune, W. (2012) Viral mediated redirection of NEMO/IKKα to autophagosomes curtails the inflammatory cascade. PLoS Pathog. 8, e1002517
37. Hoebe, K., Du, X., Georgel, P., Janssen, E., Tabeta, K., Kim, S. O., Goode, J., Lin, P., Mann, N., Mudd, S., Crozat, K., Sovath, S., Han, J., and Beutler, B. (2003) Identification of Lps2 as a key transducer of MyD88-independent TIR signalling. Nature 424, 743-748
38. Newton, K., Sun, X., and Dixit, V. M. (2004) Kinase RIP3 is dispensable for normal NF-κBs, signaling by the B-cell and T-cell receptors, tumor necrosis factor receptor 1, and Toll-like receptors 2 and 4. Mol. Cell. Biol. 24, 1464-1469
39. Kelliher, M. A., Grimm, S., Ishida, Y., Kuo, F., Stanger, B. Z., and Leder, P. (1998) The death domain kinase RIP mediates the TNF-induced NF-κB signal. Immunity 8, 297-303
40. Kuprash, D. V., Alimzhanov, M. B., Tumanov, A. V., Grivennikov, S. I., Shakhov, A. N., Drutskaya, L. N., Marino, M. W., Turetskaya, R. L., Anderson, A. O., Rajewsky, K., Pfeffer, K., and Nedospasov, S. A. (2002) Redundancy in tumor necrosis factor (TNF) and lymphotoxin (LT) signaling in vivo: mice with inactivation of the entire TNF/LT locus versus singleknockout mice. Mol. Cell. Biol. 22, 8626-8634
41. Salmena, L., Lemmers, B., Hakem, A., Matysiak-Zablocki, E., Murakami, K., Au, P. Y., Berry, D. M., Tamblyn, L., Shehabeldin, A., Migon, E., Wakeham, A., Bouchard, D., Yeh, W. C., McGlade, J. C., Ohashi, P. S., and Hakem, R. (2003) Essential role for caspase 8 in T-cell homeostasis and T-cell-mediated immunity. Genes Dev. 17, 883-895
42. Kaiser, W. J., Upton, J. W., and Mocarski, E. S. (2008) Receptor-interacting protein homotypic interaction motif-dependent control of NF-κB activation via the DNA-dependent activator of IFN regulatory factors. J. Immunol. 181, 6427-6434
43. Yamamoto, M., Sato, S., Hemmi, H., Hoshino, K., Kaisho, T., Sanjo, H., Takeuchi, O., Sugiyama, M., Okabe, M., Takeda, K., and Akira, S. (2003) Role of adapter TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 301, 640-643
44. Robinson, N., McComb, S., Mulligan, R., Dudani, R., Krishnan, L., and Sad, S. (2012) Type I interferon induces necroptosis in macrophages during infection with Salmonella enterica serovar Typhimurium. Nat. Immunol. 13, 954-962
45. Hitomi, J., Christofferson, D. E., Ng, A., Yao, J., Degterev, A., Xavier, R. J., and Yuan, J. (2008) Identification of a molecular signaling network that regulates a cellular necrotic cell death pathway. Cell 135, 1311-1323
46. Yamamoto, M., Sato, S., Mori, K., Hoshino, K., Takeuchi, O., Takeda, K., and Akira, S. (2002) Cutting edge: a novel Toll/IL-1 receptor domaincontaining adapter that preferentially activates the IFN-βpromoter in the Toll-like receptor signaling. J. Immunol. 169, 6668-6672
47. Kawai, T., and Akira, S. (2011) Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34, 637-650
48. Rebsamen, M., Meylan, E., Curran, J., and Tschopp, J. (2008) The antiviral adapter proteins Cardif and Trif are processed and inactivated by caspases. Cell Death Differ. 15, 1804-1811
49. Van Antwerp, D. J., Martin, S. J., Kafri, T., Green, D. R., and Verma, I. M. (1996) Suppression of TNF-β-induced apoptosis by NF-κB. Science 274, 787-789
50. Li, J., McQuade, T., Siemer, A. B., Napetschnig, J., Moriwaki, K., Hsiao, Y. S., Damko, E., Moquin, D., Walz, T., McDermott, A., Chan, F. K., and Wu, H. (2012) The RIP1/RIP3 necrosome forms a functional amyloid signaling complex required for programmed necrosis. Cell 150, 339-350
51. Yu, L., Alva, A., Su, H., Dutt, P., Freundt, E., Welsh, S., Baehrecke, E. H., and Lenardo, M. J. (2004) Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8. Science 304, 1500-1502
52. Zhang, H., Zhou, X., McQuade, T., Li, J., Chan, F. K., and Zhang, J. (2011) Functional complementation between FADD and RIP1 in embryos and lymphocytes. Nature 471, 373-376
53. Medzhitov, R. (2010) Innate immunity: quo vadis? Nat. Immunol. 11, 551-553
54. Kaiser, W. J., Upton, J. W., and Mocarski, E. S. (2013) Viral modulation of programmed necrosis. Curr. Opin. Virol. 3, 296-306
55. Vercammen, D., Beyaert, R., Denecker, G., Goossens, V., Van Loo, G., Declercq, W., Grooten, J., Fiers, W., and Vandenabeele, P. (1998) Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor. J. Exp. Med. 187, 1477-1485
56. O'Donnell, M. A., Perez-Jimenez, E., Oberst, A., Ng, A., Massoumi, R., Xavier, R., Green, D. R., and Ting, A. T. (2011) Caspase 8 inhibits programmed necrosis by processing CYLD. Nat. Cell Biol. 13, 1437-1442
57. Vandenabeele, P., Declercq, W., Van Herreweghe, F., and Vanden Berghe, T. (2010) The role of the kinases RIP1 and RIP3 in TNF-induced necrosis. Sci. Signal. 3, re4
58. Tabeta, K., Georgel, P., Janssen, E., Du, X., Hoebe, K., Crozat, K., Mudd, S., Shamel, L., Sovath, S., Goode, J., Alexopoulou, L., Flavell, R. A., and Beutler, B. (2004) Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection. Proc. Natl. Acad. Sci. U. S. A. 101, 3516-3521
59. Brune, W. (2011) Inhibition of programmed cell death by cytomegaloviruses. Virus Res. 157, 144-150
60. Skaletskaya, A., Bartle, L. M., Chittenden, T., McCormick, A. L., Mocarski, E. S., and Goldmacher, V. S. (2001) A cytomegalovirus-encoded inhibitor of apoptosis that suppresses caspase-8 activation. Proc. Natl. Acad. Sci. U. S. A. 98, 7829-7834