Induction of necroptotic cell death by viral activation of the RIG-I or STING pathway

Cell Death and Differentiation

Volumn 24, Issue 4, 2017, Pages 615-625

  Schock, Suruchi N ^a   Chandra, Neha V ^a   Sun, Yuefang ^a   Irie, Takashi ^b   Kitagawa, Yoshinori ^c   Gotoh, Bin ^c   Coscoy, Laurent ^a   Winoto, Astar ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HIROSHIMA UNIVERSITY   (Japan)

^c SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

RETINOIC ACID INDUCIBLE PROTEIN I; RNA; BENZYLOXYCARBONYL-VALYL-ASPARTIC ACID FLUOROMETHYL KETONE; CYLD PROTEIN, MOUSE; CYSTEINE PROTEINASE; DDX58 PROTEIN, MOUSE; MEMBRANE PROTEIN; MPYS PROTEIN, MOUSE; PEPTIDE CHLOROMETHYL KETONE; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE; RIPK3 PROTEIN, MOUSE; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR; VIRAL PROTEIN;

ANIMAL CELL; ARTICLE; CELL DEATH; CONTROLLED STUDY; FIBROSARCOMA; GENE SILENCING; L929 CELL LINE; MOUSE; NECROPTOSIS; NONHUMAN; PRIORITY JOURNAL; SENDAI VIRUS; SENDAI VIRUS INFECTION; UBIQUITINATION; VIRUS ACTIVATION; WILD TYPE; ANIMAL; ANTAGONISTS AND INHIBITORS; APOPTOSIS; C57BL MOUSE; CELL LINE; CHEMISTRY; DRUG EFFECTS; GAMMAHERPESVIRINAE; GENETICS; KNOCKOUT MOUSE; LUNG; METABOLISM; NECROSIS; PATHOLOGY; PHYSIOLOGY; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

AMINO ACID CHLOROMETHYL KETONES; ANIMALS; APOPTOSIS; CELL LINE; CYSTEINE ENDOPEPTIDASES; DEAD BOX PROTEIN 58; GAMMAHERPESVIRINAE; LUNG; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NECROSIS; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; RNA INTERFERENCE; RNA, SMALL INTERFERING; SENDAI VIRUS; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA; UBIQUITINATION; VIRAL PROTEINS; VIRUS ACTIVATION;

EID: 85008323003     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2016.153     Document Type: Article

References (57)

1. Blander JM. A long-awaited merger of the pathways mediating host defence and programmed cell death. Nat Rev Immunol 2014; 14: 601-618.
2. Chan FK, Luz NF, Moriwaki K. Programmed necrosis in the cross talk of cell death and inflammation. Annu Rev Immunol 2015; 33: 79-106.
3. Wallach D, Kang TB, Dillon CP, Green DR. Programmed necrosis in inflammation: toward identification of the effector molecules. Science 2016; 352: aaf2154.
4. Christofferson DE, Yuan J. Necroptosis as an alternative form of programmed cell death. Curr Opin Cell Biol 2010; 22: 263-268.
5. Vanlangenakker N, Vanden Berghe T, Vandenabeele P. Many stimuli pull the necrotic trigger, an overview. Cell Death Differ 2012; 19: 75-86.
6. Degterev A, Hitomi J, Germscheid M, Ch'en IL, Korkina O, Teng X et al. Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat Chem Biol 2008; 4: 313-321.
7. 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.
8. Cho YS, Challa S, Moquin D, Genga R, Ray TD, Guildford M et al. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 2009; 137: 1112-1123.
9. Zhang DW, Shao J, Lin J, Zhang N, Lu BJ, Lin SC et al. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 2009; 325: 332-336.
10. Kaiser WJ, Upton JW, Mocarski ES. Viral modulation of programmed necrosis. Curr Opin Virol 2013; 3: 296-306.
11. Li M, Beg AA. Induction of necrotic-like cell death by tumor necrosis factor alpha and caspase inhibitors: novel mechanism for killing virus-infected cells. J Virol 2000; 74: 7470-7477.
12. Rodrigue-Gervais IG, Labbe K, Dagenais M, Dupaul-Chicoine J, Champagne C, Morizot A et al. Cellular inhibitor of apoptosis protein cIAP2 protects against pulmonary tissue necrosis during influenza virus infection to promote host survival. Cell Host & Microbe 2014; 15: 23-35.
13. Upton JW, Kaiser WJ, Mocarski ES. DAI/ZBP1/DLM-1 complexes with RIP3 to mediate virus-induced programmed necrosis that is targeted by murine cytomegalovirus vIRA. Cell Host & Microbe 2012; 11: 290-297.
14. Wang X, Li Y, Liu S, Yu X, Li L, Shi C et al. Direct activation of RIP3/MLKL-dependent necrosis by herpes simplex virus 1 (HSV-1) protein ICP6 triggers host antiviral defense. Proc Natl Acad Sci USA 2014; 111: 15438-15443.
15. Huang Z, Wu SQ, Liang Y, Zhou X, Chen W, Li L et al. RIP1/RIP3 binding to HSV-1 ICP6 initiates necroptosis to restrict virus propagation in mice. Cell Host & Microbe 2015; 17: 229-242.
16. Guo H, Omoto S, Harris PA, Finger JN, Bertin J, Gough PJ et al. Herpes simplex virus suppresses necroptosis in human cells. Cell Host & Microbe 2015; 17: 243-251.
17. Wu YT, Tan HL, Huang Q, Sun XJ, Zhu X, Shen HM. zVAD-induced necroptosis in L929 cells depends on autocrine production of TNFalpha mediated by the PKC-MAPKs-AP-1 pathway. Cell Death Differ 2011; 18: 26-37.
18. Stoner GD, Kikkawa Y, Kniazeff AJ, Miyai K, Wagner RM. Clonal isolation of epithelial cells from mouse lung adenoma. Cancer Res 1975; 35: 2177-2185.
19. Rosenberger CM, Podyminogin RL, Askovich PS, Navarro G, Kaiser SM, Sanders CJ et al. Characterization of innate responses to influenza virus infection in a novel lung type I epithelial cell model. J Gen Virol 2014; 95: 350-362.
20. 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.
21. Mocarski ES, Guo H, Kaiser WJ. Necroptosis: the Trojan horse in cell autonomous antiviral host defense. Virology 2015; 479-480: 160-166.
22. Michaud F, Coulombe F, Gaudreault E, Kriz J, Gosselin J. Involvement of TLR2 in recognition of acute gammaherpesvirus-68 infection. PloS One 2010; 5: e13742.
23. Guggemoos S, Hangel D, Hamm S, Heit A, Bauer S, Adler H. TLR9 contributes to antiviral immunity during gammaherpesvirus infection. J Immunol 2008; 180: 438-443.
24. Gaajetaan GR, Geelen TH, Grauls GE, Bruggeman CA, Stassen FR. CpG and poly(I:C) stimulation of dendritic cells and fibroblasts limits herpes simplex virus type 1 infection in an IFNbeta-dependent and-independent way. Antiviral Res 2012; 93: 39-47.
25. Shcheblyakov DV, Logunov DY, Rakovskaya IV, Shmarov MM, Naroditsky BS, Ginzburg AL. Triggering of toll-like receptor-2 in mouse myelomonocytic leukaemia cells WEHI-3B leads to the suppression of apoptosis and promotes tumor progression in vivo. Acta Naturae 2011; 3: 83-93.
26. Rehwinkel J, Tan CP, Goubau D, Schulz O, Pichlmair A, Bier K et al. RIG-I detects viral genomic RNA during negative-strand RNA virus infection. Cell 2010; 140: 397-408.
27. Ishikawa H, Barber GN. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 2008; 455: 674-678.
28. Collins SE, Noyce RS, Mossman KL. Innate cellular response to virus particle entry requires IRF3 but not virus replication. J Virol 2004; 78: 1706-1717.
29. Takeuchi K, Komatsu T, Kitagawa Y, Sada K, Gotoh B. Sendai virus C protein plays a role in restricting PKR activation by limiting the generation of intracellular double-stranded RNA. J Virol 2008; 82: 10102-10110.
30. Faisca P, Desmecht D. Sendai virus, the mouse parainfluenza type 1: a longstanding pathogen that remains up-to-date. Res Vet Sci 2007; 82: 115-125.
31. Irie T, Nagata N, Yoshida T, Sakaguchi T. Paramyxovirus Sendai virus C proteins are essential for maintenance of negative-sense RNA genome in virus particles. Virology 2008; 374: 495-505.
32. Irie T, Kiyotani K, Igarashi T, Yoshida A, Sakaguchi T. Inhibition of interferon regulatory factor 3 activation by paramyxovirus V protein. J Virol 2012; 86: 7136-7145.
33. Kato A, Kiyotani K, Sakai Y, Yoshida T, Nagai Y. The paramyxovirus, Sendai virus, V protein encodes a luxury function required for viral pathogenesis. EMBO J 1997; 16: 578-587.
34. Hitomi J, Christofferson DE, Ng A, Yao J, Degterev A, Xavier RJ et al. Identification of a molecular signaling network that regulates a cellular necrotic cell death pathway. Cell 2008; 135: 1311-1323.
35. Moquin DM, McQuade T, Chan FK. CYLD deubiquitinates RIP1 in the TNFalpha-induced necrosome to facilitate kinase activation and programmed necrosis. PloS One 2013; 8: e76841.
36. Bertrand MJ, Milutinovic S, Dickson KM, Ho WC, Boudreault A, Durkin J et al. cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol Cell 2008; 30: 689-700.
37. Mahoney DJ, Cheung HH, Mrad RL, 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.
38. Varfolomeev E, Goncharov T, Fedorova AV, Dynek JN, 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.
39. Friedman CS, O'Donnell MA, Legarda-Addison D, Ng A, Cardenas WB, Yount JS et al. The tumour suppressor CYLD is a negative regulator of RIG-I-mediated antiviral response. EMBO Rep 2008; 9: 930-936.
40. Mao AP, Li S, Zhong B, Li Y, Yan J, Li Q et al. Virus-triggered ubiquitination of TRAF3/6 by cIAP1/2 is essential for induction of interferon-beta (IFN-beta) and cellular antiviral response. J Biol Chem 2010; 285: 9470-9476.
41. Skiadopoulos MH, Surman SR, Riggs JM, Elkins WR, St Claire M, Nishio M et al. Sendai virus, a murine parainfluenza virus type 1, replicates to a level similar to human PIV1 in the upper and lower respiratory tract of African green monkeys and chimpanzees. Virology 2002; 297: 153-160.
42. Parker JC, Whiteman MD, Richter CB. Susceptibility of inbred and outbred mouse strains to Sendai virus and prevalence of infection in laboratory rodents. Infect Immun 1978; 19: 123-130.
43. Koyama AH, Irie H, Kato A, Nagai Y, Adachi A. Virus multiplication and induction of apoptosis by Sendai virus: role of the C proteins. Microbes Infect 2003; 5: 373-378.
44. Garcin D, Latorre P, Kolakofsky D. Sendai virus C proteins counteract the interferonmediated induction of an antiviral state. J Virol 1999; 73: 6559-6565.
45. Wu H, Tschopp J, Lin SC. Smac mimetics and TNFalpha: a dangerous liaison? Cell 2007; 131: 655-658.
46. Rajput A, Kovalenko A, Bogdanov K, Yang SH, Kang TB, Kim JC et al. RIG-I RNA helicase activation of IRF3 transcription factor is negatively regulated by caspase-8-mediated cleavage of the RIP1 protein. Immunity 2011; 34: 340-351.
47. Sakamaki K, Tsukumo S, Yonehara S. Molecular cloning and characterization of mouse caspase-8. Eur J Biochem 1998; 253: 399-405.
48. Nogusa S, Thapa RJ, Dillon CP, Liedmann S, Oguin TH 3rd, Ingram JP et al. RIPK3 activates parallel pathways of MLKL-driven necroptosis and FADD-mediated apoptosis to protect against Influenza A virus. Cell Host & Microbe 2016; 20: 13-24.
49. Moriwaki K, Bertin J, Gough PJ, Chan FK. A RIPK3-caspase 8 complex mediates atypical pro-IL-1beta processing. J Immunol 2015; 194: 1938-1944.
50. Alvarez-Diaz S, Dillon CP, Lalaoui N, Tanzer MC, Rodriguez DA, Lin A et al. The pseudokinase MLKL and the kinase RIPK3 have distinct roles in autoimmune disease caused by loss of death-receptor-induced apoptosis. Immunity 2016; 45: 513-526.
51. Zhang X, Fan C, Zhang H, Zhao Q, Liu Y, Xu C et al. MLKL and FADD are critical for suppressing progressive lymphoproliferative disease and activating the NLRP3 inflammasome. Cell Rep 2016; 16: 3247-3259.
52. Li L, Thomas RM, Suzuki H, De Brabander JK, Wang X, Harran PG. A small molecule Smac mimic potentiates TRAIL-and TNFalpha-mediated cell death. Science 2004; 305: 1471-1474.
53. Lindquester GJ, Greer KA, Stewart JP, Sample JT. Epstein-Barr virus IL-10 gene expression by a recombinant murine gammaherpesvirus in vivo enhances acute pathogenicity but does not affect latency or reactivation. Herpesviridae 2014; 5: 1.
54. Gaudreault E, Fiola S, Olivier M, Gosselin J. Epstein-Barr virus induces MCP-1 secretion by human monocytes via TLR2. J Virol 2007; 81: 8016-8024.
55. Monroe KM, McWhirter SM, Vance RE. Identification of host cytosolic sensors and bacterial factors regulating the type I interferon response to Legionella pneumophila. PLoS Pathog 2009; 5: e1000665.
56. Tanaka Y, Chen ZJ. STING specifies IRF3 phosphorylation by TBK1 in the cytosolic DNA signaling pathway. Sci Signal 2012; 5: ra20.
57. Bergsbaken T, Fink SL, Cookson BT. Pyroptosis: host cell death and inflammation. Nat Rev Microbiol 2009; 7: 99-109.