Mechanisms of RIPK3-induced inflammation

Immunology and Cell Biology

Volumn 95, Issue 2, 2017, Pages 166-172

  Shlomovitz, Inbar ^a   Zargrian, Sefi ^a   Gerlic, Motti ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

MOLECULAR SCAFFOLD; RECEPTOR INTERACTING PROTEIN KINASE 3; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE;

APOPTOSIS; CELL DEATH; GENE EXPRESSION; GENETIC REGULATION; HERPES SIMPLEX VIRUS 1; HUMAN; INFLAMMATION; INFLUENZA A VIRUS; NECROPTOSIS; NONHUMAN; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN STRUCTURE; PYROPTOSIS; REVIEW; SIGNAL TRANSDUCTION; VACCINIA VIRUS; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; DISEASES; ENZYMOLOGY; METABOLISM; PATHOLOGY;

ANIMALS; APOPTOSIS; DISEASE; HUMANS; INFLAMMATION; MODELS, BIOLOGICAL; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION;

EID: 85008395330     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2016.124     Document Type: Review

References (82)

1. Sun X, Lee J, Navas T, Baldwin DT, Stewart TA, Dixit VM. RIP3, a novel apoptosisinducing kinase. J Biol Chem 1999; 274: 16871-16875.
2. Yu PW, Huang BC, Shen M, Quast J, Chan E, Xu X, et al. Identification of RIP3, a RIPlike kinase that activates apoptosis and NFkappaB. Curr Biol 1999; 9: 539-542.
3. Pazdernik NJ, Donner DB, Goebl MG, Harrington MA. Mouse receptor interacting protein 3 does not contain a caspase-recruiting or a death domain but induces apoptosis and activates NF-kappaB. Mol Cell Biol 1999; 19: 6500-6508.
4. 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.
5. 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.
6. McQuade T, Cho Y, Chan FK. Positive and negative phosphorylation regulates RIP1-and RIP3-induced programmed necrosis. Biochem J 2013; 456: 409-415.
7. Chen W, Zhou Z, Li L, Zhong CQ, Zheng X, Wu X, et al. Diverse sequence determinants control human and mouse receptor interacting protein 3 (RIP3) and mixed lineage kinase domain-like (MLKL) interaction in necroptotic signaling. J Biol Chem 2013; 288: 16247-16261.
8. 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.
9. Sun X, Yin J, Starovasnik MA, Fairbrother WJ, Dixit VM. Identification of a novel homotypic interaction motif required for the phosphorylation of receptor-interacting protein (RIP) by RIP3. J Biol Chem 2002; 277: 9505-9511.
10. Feng S, Yang Y, Mei Y, Ma L, Zhu DE, Hoti N, et al. Cleavage of RIP3 inactivates its caspase-independent apoptosis pathway by removal of kinase domain. Cell Signal 2007; 19: 2056-2067.
11. Newton K, Dugger DL, Wickliffe KE, Kapoor N, de Almagro MC, Vucic D, et al. Activity of protein kinase RIPK3 determines whether cells die by necroptosis or apoptosis. Science 2014; 343: 1357-1360.
12. 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.
13. Newton K, Sun X, Dixit VM. Kinase RIP3 is dispensable for normal NF-kappa Bs, signaling by the B-cell and T-cell receptors, tumor necrosis factor receptor 1, and Toll-like receptors 2 and 4. Mol Cell Biol 2004; 24: 1464-1469.
14. Moriwaki K, Balaji S, McQuade T, Malhotra N, Kang J, Chan FK. The necroptosis adaptor RIPK3 promotes injury-induced cytokine expression and tissue repair. Immunity 2014; 41: 567-578.
15. Silke J, Rickard JA, Gerlic M. The diverse role of RIP kinases in necroptosis and inflammation. Nat Immunol 2015; 16: 689-697.
16. Dillon CP, Weinlich R, Rodriguez DA, Cripps JG, Quarato G, Gurung P, et al. RIPK1 blocks early postnatal lethality mediated by caspase-8 and RIPK3. Cell 2014; 157: 1189-1202.
17. Kaiser WJ, Daley-Bauer LP, Thapa RJ, Mandal P, Berger SB, Huang C, et al. RIP1 suppresses innate immune necrotic as well as apoptotic cell death during mammalian parturition. Proc Natl Acad Sci USA 2014; 111: 7753-7758.
18. Rickard JA, O'Donnell JA, Evans JM, Lalaoui N, Poh AR, Rogers T, et al. RIPK1 regulates RIPK3-MLKL-driven systemic inflammation and emergency hematopoiesis. Cell 2014; 157: 1175-1188.
19. Dowling JP, Nair A, Zhang J. A novel function of RIP1 in postnatal development and immune homeostasis by protecting against RIP3-dependent necroptosis and FADDmediated apoptosis. Front Cell Dev Biol 2015; 3: 12.
20. Kaiser WJ, Upton JW, Long AB, Livingston-Rosanoff D, Daley-Bauer LP, Hakem R, et al. RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature 2011; 471: 368-372.
21. Oberst A, Dillon CP, Weinlich R, McCormick LL, Fitzgerald P, Pop C, et al. Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis. Nature 2011; 471: 363-367.
22. Chen X, Li W, Ren J, Huang D, He WT, Song Y, et al. Translocation of mixed lineage kinase domain-like protein to plasma membrane leads to necrotic cell death. Cell Res 2014; 24: 105-121.
23. Cai Z, Jitkaew S, Zhao J, Chiang HC, 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.
24. Dondelinger Y, Declercq W, Montessuit S, Roelandt R, Goncalves A, Bruggeman I, et al. MLKL compromises plasma membrane integrity by binding to phosphatidylinositol phosphates. Cell Rep 2014; 7: 971-981.
25. Hildebrand JM, Tanzer MC, Lucet IS, Young SN, Spall SK, Sharma P, et al. Activation of the pseudokinase MLKL unleashes the four-helix bundle domain to induce membrane localization and necroptotic cell death. Proc Natl Acad Sci USA 2014; 111: 15072-15077.
26. Pasparakis M, Vandenabeele P. Necroptosis and its role in inflammation. Nature 2015; 517: 311-320.
27. Mandal P, Berger SB, Pillay S, Moriwaki K, Huang C, Guo H, et al. RIP3 induces apoptosis independent of pronecrotic kinase activity. Mol Cell 2014; 56: 481-495.
28. Croker BA, O'Donnell JA, Gerlic M. Pyroptotic death storms and cytopenia. Curr Opin Immunol 2014; 26: 128-137.
29. Vince JE, Wong WW, Gentle I, Lawlor KE, Allam R, O'Reilly L, et al. Inhibitor of apoptosis proteins limit RIP3 kinase-dependent interleukin-1 activation. Immunity 2012; 36: 215-227.
30. Lawlor KE, Khan N, Mildenhall A, Gerlic M, Croker BA, D'Cruz AA, et al. RIPK3 promotes cell death and NLRP3 inflammasome activation in the absence of MLKL. Nat Commun 2015; 6: 6282.
31. Yabal M, Muller N, Adler H, Knies N, Gross CJ, Damgaard RB, et al. XIAP restricts TNFand RIP3-dependent cell death and inflammasome activation. Cell Rep 2014; 7: 1796-1808.
32. Hockendorf U, Yabal M, Jost PJ. RIPK3-dependent cell death and inflammasome activation in FLT3-ITD expressing LICs. Oncotarget (e-pub ahead of print, 10 August 2016, doi:10.18632/oncotarget.11195).
33. Kang TB, Yang SH, Toth B, Kovalenko A, Wallach D. Caspase-8 blocks kinase RIPK3-mediated activation of the NLRP3 inflammasome. Immunity 2013; 38: 27-40.
34. Antonopoulos C, El Sanadi C, Kaiser WJ, Mocarski ES, Dubyak GR. Proapoptotic chemotherapeutic drugs induce noncanonical processing and release of IL-1beta via caspase-8 in dendritic cells. J Immunol 2013; 191: 4789-4803.
35. Bossaller L, Chiang PI, Schmidt-Lauber C, Ganesan S, Kaiser WJ, Rathinam VA, et al. Cutting edge: FAS (CD95) mediates noncanonical IL-1beta and IL-18 maturation via caspase-8 in an RIP3-independent manner. J Immunol 2012; 189: 5508-5512.
36. Gaidt MM, Ebert TS, Chauhan D, Schmidt T, Schmid-Burgk JL, Rapino F, et al. Human monocytes engage an alternative inflammasome pathway. Immunity 2016; 44: 833-846.
37. Weng D, Marty-Roix R, Ganesan S, Proulx MK, Vladimer GI, Kaiser WJ, et al. Caspase-8 and RIP kinases regulate bacteria-induced innate immune responses and cell death. Proc Natl Acad Sci USA 2014; 111: 7391-7396.
38. Duong BH, Onizawa M, Oses-Prieto JA, Advincula R, Burlingame A, Malynn BA, et al. A20 restricts ubiquitination of pro-interleukin-1beta protein complexes and suppresses NLRP3 inflammasome activity. Immunity 2015; 42: 55-67.
39. Guo H, Kaiser WJ, Mocarski ES. Manipulation of apoptosis and necroptosis signaling by herpesviruses. Med Microbiol Immunol 2015; 204: 439-448.
40. Silke J, Vaux DL. IAP gene deletion and conditional knockout models. Semin Cell Dev Biol 2015; 39: 97-105.
41. Dobbelstein M, Shenk T. Protection against apoptosis by the vaccinia virus SPI-2 (B13R) gene product. J Virol 1996; 70: 6479-6485.
42. Yu E, Zhai D, Jin C, Gerlic M, Reed JC, Liddington R. Structural determinants of caspase-9 inhibition by the vaccinia virus protein, F1L. J Biol Chem 2011; 286: 30748-30758.
43. Wasilenko ST, Stewart TL, Meyers AF, Barry M. Vaccinia virus encodes a previously uncharacterized mitochondrial-associated inhibitor of apoptosis. Proc Natl Acad Sci USA 2003; 100: 14345-14350.
44. Aoyagi M, Zhai D, Jin C, Aleshin AE, Stec B, Reed JC, et al. Vaccinia virus N1L protein resembles a B cell lymphoma-2 (Bcl-2) family protein. Protein Sci 2007; 16: 118-124.
45. Gerlic M, Faustin B, Postigo A, Yu EC, Proell M, Gombosuren N, et al. Vaccinia virus F1L protein promotes virulence by inhibiting inflammasome activation. Proc Natl Acad Sci USA 2013; 110: 7808-7813.
46. Chan FK, Shisler J, Bixby JG, 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.
47. Cho YS, Challa S, Moquin D, Genga R, Ray TD, Guildford M, et al. Phosphorylationdriven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virusinduced inflammation. Cell 2009; 137: 1112-1123.
48. Upton JW, Kaiser WJ, Mocarski ES. Cytomegalovirus M45 cell death suppression requires receptor-interacting protein (RIP) homotypic interaction motif (RHIM)-dependent interaction with RIP1. J Biol Chem 2008; 283: 16966-16970.
49. 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.
50. Omoto S, Guo H, Talekar GR, Roback L, Kaiser WJ, Mocarski ES. Suppression of RIP3-dependent necroptosis by human cytomegalovirus. J Biol Chem 2015; 290: 11635-11648.
51. 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.
52. 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.
53. 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.
54. 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.
55. 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.
56. Roca FJ, Ramakrishnan L. TNF dually mediates resistance and susceptibility to mycobacteria via mitochondrial reactive oxygen species. Cell 2013; 153: 521-534.
57. 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.
58. Kitur K, Parker D, Nieto P, Ahn DS, Cohen TS, Chung S, et al. Toxin-induced necroptosis is a major mechanism of Staphylococcus aureus lung damage. PLoS Pathog 2015; 11: e1004820.
59. Kitur K, Wachtel S, Brown A, Wickersham M, Paulino F, Penaloza HF, et al. Necroptosis promotes staphylococcus aureus clearance by inhibiting excessive inflammatory signaling. Cell Rep 2016; 16: 2219-2230.
60. Ofengeim D, Ito Y, Najafov A, Zhang Y, Shan B, DeWitt JP, et al. Activation of necroptosis in multiple sclerosis. Cell Rep 2015; 10: 1836-1849.
61. Linkermann A, Brasen JH, Darding M, Jin MK, Sanz AB, Heller JO, et al. Two independent pathways of regulated necrosis mediate ischemia-reperfusion injury. Proc Natl Acad Sci USA 2013; 110: 12024-12029.
62. Lin J, Li H, Yang M, Ren J, Huang Z, Han F, et al. A role of RIP3-mediated macrophage necrosis in atherosclerosis development. Cell Rep 2013; 3: 200-210.
63. Murakami Y, Matsumoto H, Roh M, Suzuki J, Hisatomi T, Ikeda Y, et al. Receptor interacting protein kinase mediates necrotic cone but not rod cell death in a mouse model of inherited degeneration. Proc Natl Acad Sci USA 2012; 109: 14598-14603.
64. Murakami Y, Matsumoto H, Roh M, Giani A, Kataoka K, Morizane Y, et al. Programmed necrosis, not apoptosis, is a key mediator of cell loss and DAMPmediated inflammation in dsRNA-induced retinal degeneration. Cell Death Differ 2014; 21: 270-277.
65. Sato K, Li S, Gordon WC, He J, Liou GI, Hill JM, et al. Receptor interacting protein kinase-mediated necrosis contributes to cone and rod photoreceptor degeneration in the retina lacking interphotoreceptor retinoid-binding protein. J Neurosci 2013; 33: 17458-17468.
66. Weinlich R, Oberst A, Dillon CP, Janke LJ, Milasta S, Lukens JR, et al. Protective roles for caspase-8 and cFLIP in adult homeostasis. Cell Rep 2013; 5: 340-348.
67. Bonnet MC, Preukschat D, Welz PS, van Loo G, Ermolaeva MA, Bloch W, et al. The adaptor protein FADD protects epidermal keratinocytes from necroptosis in vivo and prevents skin inflammation. Immunity 2011; 35: 572-582.
68. Dannappel M, Vlantis K, Kumari S, Polykratis A, Kim C, Wachsmuth L, et al. RIPK1 maintains epithelial homeostasis by inhibiting apoptosis and necroptosis. Nature 2014; 513: 90-94.
69. Welz PS, 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.
70. Roderick JE, Hermance N, Zelic M, Simmons MJ, Polykratis A, Pasparakis M, et al. Hematopoietic RIPK1 deficiency results in bone marrow failure caused by apoptosis and RIPK3-mediated necroptosis. Proc Natl Acad Sci USA 2014; 111: 14436-14441.
71. Roychowdhury S, McMullen MR, Pisano SG, Liu X, Nagy LE. Absence of receptor interacting protein kinase 3 prevents ethanol-induced liver injury. Hepatology 2013; 57: 1773-1783.
72. Ramachandran A, McGill MR, Xie Y, Ni HM, Ding WX, Jaeschke H. Receptor interacting protein kinase 3 is a critical early mediator of acetaminophen-induced hepatocyte necrosis in mice. Hepatology 2013; 58: 2099-2108.
73. Afonso MB, Rodrigues PM, Carvalho T, Caridade M, Borralho P, Cortez-Pinto H, et al. Necroptosis is a key pathogenic event in human and experimental murine models of non-alcoholic steatohepatitis. Clin Sci (Lond) 2015; 129: 721-739.
74. Dhib-Jalbut S, Kalvakolanu DV. Microglia and necroptosis: The culprits of neuronal cell death in multiple sclerosis. Cytokine 2015; 76: 583-584.
75. Kim SK, Kim WJ, Yoon JH, Ji JH, Morgan MJ, Cho H, et al. Upregulated RIP3 expression potentiates MLKL phosphorylation-mediated programmed necrosis in toxic epidermal necrolysis. J Invest Dermatol 2015; 135: 2021-2030.
76. Zhu Y, Cui H, Xia Y, Gan H. RIPK3-mediated necroptosis and apoptosis contributes to renal tubular cell progressive loss and chronic kidney disease progression in rats. PloS ONE 2016; 11: e0156729.
77. Gautheron J, Vucur M, Schneider AT, Severi I, Roderburg C, Roy S, et al. The necroptosis-inducing kinase RIPK3 dampens adipose tissue inflammation and glucose intolerance. Nat Commun 2016; 7: 11869.
78. Vucur M, Reisinger F, Gautheron J, Janssen J, Roderburg C, Cardenas DV, et al. RIP3 inhibits inflammatory hepatocarcinogenesis but promotes cholestasis by controlling caspase-8-and JNK-dependent compensatory cell proliferation. Cell Rep 2013; 4: 776-790.
79. Ito Y, Ofengeim D, Najafov A, Das S, Saberi S, Li Y, et al. RIPK1 mediates axonal degeneration by promoting inflammation and necroptosis in ALS. Science 2016; 353: 603-608.
80. Zhang T, Zhang Y, Cui M, Jin L, Wang Y, Lv F, et al. CaMKII is a RIP3 substrate mediating ischemia-and oxidative stress-induced myocardial necroptosis. Nat Med 2016; 22: 175-182.
81. Newton K, Dugger DL, Maltzman A, Greve JM, Hedehus M, Martin-McNulty B, et al. RIPK3 deficiency or catalytically inactive RIPK1 provides greater benefit than MLKL deficiency in mouse models of inflammation and tissue injury. Cell Death Differ 2016; 23: 1565-1576.
82. Kashlov JK, Donev IS, Doneva JG, Valkov VD, Kirkorova AD, Ghenev PI, et al. Serum levels of RIPK3 and troponin I as potential biomarkers for predicting impaired left ventricular function in patients with myocardial infarction with ST segment elevation and normal troponin I levels prior percutaneous coronary intervention. Biosci Trends 2016; 10: 294-299.