The Pseudokinase MLKL and the Kinase RIPK3 Have Distinct Roles in Autoimmune Disease Caused by Loss of Death-Receptor-Induced Apoptosis

Immunity

Volumn 45, Issue 3, 2016, Pages 513-526

  Alvarez Diaz, Silvia ^a,b   Dillon, Christopher P ^c   Lalaoui, Najoua ^a,b   Tanzer, Maria C ^a,b   Rodriguez, Diego A ^c   Lin, Ann ^a   Lebois, Marion ^a   Hakem, Razq ^d   Josefsson, Emma C ^a,b   O'Reilly, Lorraine A ^a,b   Silke, John ^a,b   Alexander, Warren S ^a,b   Green, Douglas R ^c   Strasser, Andreas ^a,b  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^d UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 8; CHEMOKINE; CYTOKINE; DEATH RECEPTOR; FAS ASSOCIATED DEATH DOMAIN PROTEIN; MIXED LINEAGE KINASE DOMAIN LIKE PROTEIN; PROTEIN KINASE; PROTEIN RIPK1; PROTEIN RIPK3; UNCLASSIFIED DRUG; MLKL PROTEIN, MOUSE; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE; RIPK3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOIMMUNE DISEASE; CELL DEATH; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; EMBRYO; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LYMPHADENOPATHY; MOUSE; NECROPTOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; THROMBOCYTOPENIA; ANIMAL; C57BL MOUSE; METABOLISM; NECROSIS; PHYSIOLOGY;

ANIMALS; APOPTOSIS; AUTOIMMUNE DISEASES; CASPASE 8; CELL DEATH; FAS-ASSOCIATED DEATH DOMAIN PROTEIN; MICE; MICE, INBRED C57BL; NECROSIS; PROTEIN KINASES; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES;

EID: 84981736924     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2016.07.016     Document Type: Article

References (63)

1. Allam, R., Lawlor, K.E., Yu, E.C., Mildenhall, A.L., Moujalled, D.M., Lewis, R.S., Ke, F., Mason, K.D., White, M.J., Stacey, K.J., et al. Mitochondrial apoptosis is dispensable for NLRP3 inflammasome activation but non-apoptotic caspase-8 is required for inflammasome priming. EMBO Rep. 15 (2014), 982–990.
2. Bossen, C., Ingold, K., Tardivel, A., Bodmer, J.L., Gaide, O., Hertig, S., Ambrose, C., Tschopp, J., Schneider, P., Interactions of tumor necrosis factor (TNF) and TNF receptor family members in the mouse and human. J. Biol. Chem. 281 (2006), 13964–13971.
3. Cai, Z., Jitkaew, S., Zhao, J., Chiang, H.C., Choksi, S., Liu, J., Ward, Y., Wu, L.G., Liu, Z.G., Plasma membrane translocation of trimerized MLKL protein is required for TNF-induced necroptosis. Nat. Cell Biol. 16 (2014), 55–65.
4. Ch'en, I.L., Beisner, D.R., Degterev, A., Lynch, C., Yuan, J., Hoffmann, A., Hedrick, S.M., Antigen-mediated T cell expansion regulated by parallel pathways of death. Proc. Natl. Acad. Sci. USA 105 (2008), 17463–17468.
5. Chan, F.K., Luz, N.F., Moriwaki, K., Programmed necrosis in the cross talk of cell death and inflammation. Annu. Rev. Immunol. 33 (2014), 79–106.
6. Chen, X., Li, W., Ren, J., Huang, D., He, W.T., Song, Y., Yang, C., Li, W., Zheng, X., Chen, P., Han, J., Translocation of mixed lineage kinase domain-like protein to plasma membrane leads to necrotic cell death. Cell Res. 24 (2014), 105–121.
7. Cho, Y.S., Challa, S., Moquin, D., Genga, R., Ray, T.D., Guildford, M., Chan, F.K., Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 137 (2009), 1112–1123.
8. Cook, W.D., Moujalled, D.M., Ralph, T.J., Lock, P., Young, S.N., Murphy, J.M., Vaux, D.L., RIPK1- and RIPK3-induced cell death mode is determined by target availability. Cell Death Differ. 21 (2014), 1600–1612.
9. Dillon, C.P., Oberst, A., Weinlich, R., Janke, L.J., Kang, T.B., Ben-Moshe, T., Mak, T.W., Wallach, D., Green, D.R., Survival function of the FADD-CASPASE-8-cFLIP(L) complex. Cell Rep. 1 (2012), 401–407.
10. 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 157 (2014), 1189–1202.
11. Dondelinger, Y., Declercq, W., Montessuit, S., Roelandt, R., Goncalves, A., Bruggeman, I., Hulpiau, P., Weber, K., Sehon, C.A., Marquis, R.W., et al. MLKL compromises plasma membrane integrity by binding to phosphatidylinositol phosphates. Cell Rep. 7 (2014), 971–981.
12. He, S., Wang, L., Miao, L., Wang, T., Du, F., Zhao, L., Wang, X., Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell 137 (2009), 1100–1111.
13. He, S., Liang, Y., Shao, F., Wang, X., Toll-like receptors activate programmed necrosis in macrophages through a receptor-interacting kinase-3-mediated pathway. Proc. Natl. Acad. Sci. USA 108 (2011), 20054–20059.
14. Hildebrand, J.M., Tanzer, M.C., Lucet, I.S., Young, S.N., Spall, S.K., Sharma, P., Pierotti, C., Garnier, J.M., Dobson, R.C., Webb, A.I., 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 111 (2014), 15072–15077.
15. Holler, N., Zaru, R., Micheau, O., Thome, M., Attinger, A., Valitutti, S., Bodmer, J.L., Schneider, P., Seed, B., Tschopp, J., Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat. Immunol. 1 (2000), 489–495.
16. Josefsson, E.C., White, M.J., Dowling, M.R., Kile, B.T., Platelet life span and apoptosis. Methods Mol. Biol. 788 (2012), 59–71.
17. Kaiser, W.J., Upton, J.W., Long, A.B., Livingston-Rosanoff, D., Daley-Bauer, L.P., Hakem, R., Caspary, T., Mocarski, E.S., RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature 471 (2011), 368–372.
18. Kaiser, W.J., Sridharan, H., Huang, C., Mandal, P., Upton, J.W., Gough, P.J., Sehon, C.A., Marquis, R.W., Bertin, J., Mocarski, E.S., Toll-like receptor 3-mediated necrosis via TRIF, RIP3, and MLKL. J. Biol. Chem. 288 (2013), 31268–31279.
19. Kaiser, W.J., Daley-Bauer, L.P., Thapa, R.J., Mandal, P., Berger, S.B., Huang, C., Sundararajan, A., Guo, H., Roback, L., Speck, S.H., et al. RIP1 suppresses innate immune necrotic as well as apoptotic cell death during mammalian parturition. Proc. Natl. Acad. Sci. USA 111 (2014), 7753–7758.
20. Kang, T.B., Yang, S.H., Toth, B., Kovalenko, A., Wallach, D., Caspase-8 blocks kinase RIPK3-mediated activation of the NLRP3 inflammasome. Immunity 38 (2013), 27–40.
21. Kearney, C.J., Sheridan, C., Cullen, S.P., Tynan, G.A., Logue, S.E., Afonina, I.S., Vucic, D., Lavelle, E.C., Martin, S.J., Inhibitor of apoptosis proteins (IAPs) and their antagonists regulate spontaneous and tumor necrosis factor (TNF)-induced proinflammatory cytokine and chemokine production. J. Biol. Chem. 288 (2013), 4878–4890.
22. 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., 6, 2015, 6282.
23. Mandal, P., Berger, S.B., Pillay, S., Moriwaki, K., Huang, C., Guo, H., Lich, J.D., Finger, J., Kasparcova, V., Votta, B., et al. RIP3 induces apoptosis independent of pronecrotic kinase activity. Mol. Cell 56 (2014), 481–495.
24. Moujalled, D.M., Cook, W.D., Okamoto, T., Murphy, J., Lawlor, K.E., Vince, J.E., Vaux, D.L., TNF can activate RIPK3 and cause programmed necrosis in the absence of RIPK1. Cell Death Dis., 4, 2013, e465.
25. Murphy, J.M., Czabotar, P.E., Hildebrand, J.M., Lucet, I.S., Zhang, J.G., Alvarez-Diaz, S., Lewis, R., Lalaoui, N., Metcalf, D., Webb, A.I., et al. The pseudokinase MLKL mediates necroptosis via a molecular switch mechanism. Immunity 39 (2013), 443–453.
26. Newton, K., Sun, X., Dixit, V.M., 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. 24 (2004), 1464–1469.
27. Newton, K., Dugger, D.L., Wickliffe, K.E., Kapoor, N., de Almagro, M.C., Vucic, D., Komuves, L., Ferrando, R.E., French, D.M., Webster, J., et al. Activity of protein kinase RIPK3 determines whether cells die by necroptosis or apoptosis. Science 343 (2014), 1357–1360.
28. O'Reilly, L.A., Tai, L., Lee, L., Kruse, E.A., Grabow, S., Fairlie, W.D., Haynes, N.M., Tarlinton, D.M., Zhang, J.G., Belz, G.T., et al. Membrane-bound Fas ligand only is essential for Fas-induced apoptosis. Nature 461 (2009), 659–663.
29. O'Reilly, L.A., Divisekera, U., Newton, K., Scalzo, K., Kataoka, T., Puthalakath, H., Ito, M., Huang, D.C., Strasser, A., Modifications and intracellular trafficking of FADD/MORT1 and caspase-8 after stimulation of T lymphocytes. Cell Death Differ. 11 (2004), 724–736.
30. Oberst, A., Dillon, C.P., Weinlich, R., McCormick, L.L., Fitzgerald, P., Pop, C., Hakem, R., Salvesen, G.S., Green, D.R., Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis. Nature 471 (2011), 363–367.
31. Oliveira, J.B., Bleesing, J.J., Dianzani, U., Fleisher, T.A., Jaffe, E.S., Lenardo, M.J., Rieux-Laucat, F., Siegel, R.M., Su, H.C., Teachey, D.T., Rao, V.K., Revised diagnostic criteria and classification for the autoimmune lymphoproliferative syndrome (ALPS): report from the 2009 NIH International Workshop. Blood 116 (2010), e35–e40.
32. Orozco, S., Yatim, N., Werner, M.R., Tran, H., Gunja, S.Y., Tait, S.W., Albert, M.L., Green, D.R., Oberst, A., RIPK1 both positively and negatively regulates RIPK3 oligomerization and necroptosis. Cell Death Differ. 21 (2014), 1511–1521.
33. Pasparakis, M., Vandenabeele, P., Necroptosis and its role in inflammation. Nature 517 (2015), 311–320.
34. Pattison, J.M., Nelson, P.J., Huie, P., Sibley, R.K., Krensky, A.M., RANTES chemokine expression in transplant-associated accelerated atherosclerosis. J. Heart Lung Transplant. 15 (1996), 1194–1199.
35. Philip, N.H., Dillon, C.P., Snyder, A.G., Fitzgerald, P., Wynosky-Dolfi, M.A., Zwack, E.E., Hu, B., Fitzgerald, L., Mauldin, E.A., Copenhaver, A.M., et al. Caspase-8 mediates caspase-1 processing and innate immune defense in response to bacterial blockade of NF-κB and MAPK signaling. Proc. Natl. Acad. Sci. USA 111 (2014), 7385–7390.
36. Powell, N., Humbert, M., Durham, S.R., Assoufi, B., Kay, A.B., Corrigan, C.J., Increased expression of mRNA encoding RANTES and MCP-3 in the bronchial mucosa in atopic asthma. Eur. Respir. J. 9 (1996), 2454–2460.
37. Rathanaswami, P., Hachicha, M., Sadick, M., Schall, T.J., McColl, S.R., Expression of the cytokine RANTES in human rheumatoid synovial fibroblasts. Differential regulation of RANTES and interleukin-8 genes by inflammatory cytokines. J. Biol. Chem. 268 (1993), 5834–5839.
38. 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 157 (2014), 1175–1188.
39. Rieux-Laucat, F., Le Deist, F., Hivroz, C., Roberts, I.A., Debatin, K.M., Fischer, A., de Villartay, J.P., Mutations in Fas associated with human lymphoproliferative syndrome and autoimmunity. Science 268 (1995), 1347–1349.
40. Rot, A., Krieger, M., Brunner, T., Bischoff, S.C., Schall, T.J., Dahinden, C.A., RANTES and macrophage inflammatory protein 1 alpha induce the migration and activation of normal human eosinophil granulocytes. J. Exp. Med. 176 (1992), 1489–1495.
41. Salmena, L., Lemmers, B., Hakem, A., Matysiak-Zablocki, E., Murakami, K., Au, P.Y., Berry, D.M., Tamblyn, L., Shehabeldin, A., Migon, E., et al. Essential role for caspase 8 in T-cell homeostasis and T-cell-mediated immunity. Genes Dev. 17 (2003), 883–895.
42. Schall, T.J., Bacon, K., Toy, K.J., Goeddel, D.V., Selective attraction of monocytes and T lymphocytes of the memory phenotype by cytokine RANTES. Nature 347 (1990), 669–671.
43. Siegel, R.M., Chan, F.K., Chun, H.J., Lenardo, M.J., The multifaceted role of Fas signaling in immune cell homeostasis and autoimmunity. Nat. Immunol. 1 (2000), 469–474.
44. Su, L., Quade, B., Wang, H., Sun, L., Wang, X., Rizo, J., A plug release mechanism for membrane permeation by MLKL. Structure 22 (2014), 1489–1500.
45. Sun, L., Wang, H., Wang, Z., He, S., Chen, S., Liao, D., Wang, L., Yan, J., Liu, W., Lei, X., Wang, X., Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 148 (2012), 213–227.
46. Tanzer, M.C., Tripaydonis, A., Webb, A.I., Young, S.N., Varghese, L.N., Hall, C., Alexander, W.S., Hildebrand, J.M., Silke, J., Murphy, J.M., Necroptosis signalling is tuned by phosphorylation of MLKL residues outside the pseudokinase domain activation loop. Biochem. J. 471 (2015), 255–265.
47. Teachey, D.T., Manno, C.S., Axsom, K.M., Andrews, T., Choi, J.K., Greenbaum, B.H., McMann, J.M., Sullivan, K.E., Travis, S.F., Grupp, S.A., Unmasking Evans syndrome: T-cell phenotype and apoptotic response reveal autoimmune lymphoproliferative syndrome (ALPS). Blood 105 (2005), 2443–2448.
48. Vandenabeele, P., Declercq, W., Van Herreweghe, F., Vanden Berghe, T., The role of the kinases RIP1 and RIP3 in TNF-induced necrosis. Sci. Signal., 3, 2010, re4.
49. Varfolomeev, E.E., Schuchmann, M., Luria, V., Chiannilkulchai, N., Beckmann, J.S., Mett, I.L., Rebrikov, D., Brodianski, V.M., Kemper, O.C., Kollet, O., et al. Targeted disruption of the mouse Caspase 8 gene ablates cell death induction by the TNF receptors, Fas/Apo1, and DR3 and is lethal prenatally. Immunity 9 (1998), 267–276.
50. Vince, J.E., Wong, W.W., Khan, N., Feltham, R., Chau, D., Ahmed, A.U., Benetatos, C.A., Chunduru, S.K., Condon, S.M., McKinlay, M., et al. IAP antagonists target cIAP1 to induce TNFalpha-dependent apoptosis. Cell 131 (2007), 682–693.
51. Vince, J.E., Wong, W.W., Gentle, I., Lawlor, K.E., Allam, R., O'Reilly, L., Mason, K., Gross, O., Ma, S., Guarda, G., et al. Inhibitor of apoptosis proteins limit RIP3 kinase-dependent interleukin-1 activation. Immunity 36 (2012), 215–227.
52. Wang, H., Sun, L., Su, L., Rizo, J., Liu, L., Wang, L.F., Wang, F.S., Wang, X., Mixed lineage kinase domain-like protein MLKL causes necrotic membrane disruption upon phosphorylation by RIP3. Mol. Cell 54 (2014), 133–146.
53. Watanabe, D., Suda, T., Hashimoto, H., Nagata, S., Constitutive activation of the Fas ligand gene in mouse lymphoproliferative disorders. EMBO J. 14 (1995), 12–18.
54. Watanabe-Fukunaga, R., Brannan, C.I., Copeland, N.G., Jenkins, N.A., Nagata, S., Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature 356 (1992), 314–317.
55. Wong, W.W., Vince, J.E., Lalaoui, N., Lawlor, K.E., Chau, D., Bankovacki, A., Anderton, H., Metcalf, D., O'Reilly, L., Jost, P.J., et al. cIAPs and XIAP regulate myelopoiesis through cytokine production in an RIPK1- and RIPK3-dependent manner. Blood 123 (2014), 2562–2572.
56. Wu, J., Huang, Z., Ren, J., Zhang, Z., He, P., Li, Y., Ma, J., Chen, W., Zhang, Y., Zhou, X., et al. Mlkl knockout mice demonstrate the indispensable role of Mlkl in necroptosis. Cell Res. 23 (2013), 994–1006.
57. Wu, X.N., Yang, Z.H., Wang, X.K., Zhang, Y., Wan, H., Song, Y., Chen, X., Shao, J., Han, J., Distinct roles of RIP1-RIP3 hetero- and RIP3-RIP3 homo-interaction in mediating necroptosis. Cell Death Differ. 21 (2014), 1709–1720.
58. Yeh, W.C., de la Pompa, J.L., McCurrach, M.E., Shu, H.B., Elia, A.J., Shahinian, A., Ng, M., Wakeham, A., Khoo, W., Mitchell, K., et al. FADD: essential for embryo development and signaling from some, but not all, inducers of apoptosis. Science 279 (1998), 1954–1958.
59. Yeh, W.C., Itie, A., Elia, A.J., Ng, M., Shu, H.B., Wakeham, A., Mirtsos, C., Suzuki, N., Bonnard, M., Goeddel, D.V., Mak, T.W., Requirement for Casper (c-FLIP) in regulation of death receptor-induced apoptosis and embryonic development. Immunity 12 (2000), 633–642.
60. Young, D.A., Hegen, M., Ma, H.L., Whitters, M.J., Albert, L.M., Lowe, L., Senices, M., Wu, P.W., Sibley, B., Leathurby, Y., et al. Blockade of the interleukin-21/interleukin-21 receptor pathway ameliorates disease in animal models of rheumatoid arthritis. Arthritis Rheum. 56 (2007), 1152–1163.
61. Zhang, D.W., Shao, J., Lin, J., Zhang, N., Lu, B.J., Lin, S.C., Dong, M.Q., Han, J., RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 325 (2009), 332–336.
62. Zhang, H., Zhou, X., McQuade, T., Li, J., Chan, F.K., Zhang, J., Functional complementation between FADD and RIP1 in embryos and lymphocytes. Nature 471 (2011), 373–376.
63. Zhao, J., Jitkaew, S., Cai, Z., Choksi, S., Li, Q., Luo, J., Liu, Z.G., Mixed lineage kinase domain-like is a key receptor interacting protein 3 downstream component of TNF-induced necrosis. Proc. Natl. Acad. Sci. USA 109 (2012), 5322–5327.