MLKL, the Protein that Mediates Necroptosis, Also Regulates Endosomal Trafficking and Extracellular Vesicle Generation

Immunity

Volumn 47, Issue 1, 2017, Pages 51-65.e7

  Yoon, Seongmin ^a   Kovalenko, Andrew ^a   Bogdanov, Konstantin ^a   Wallach, David ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

EGF; endosomes; exosomes; extracellular vesicles; inflammation; intraluminal vesicles; MLKL; multivesicular bodies; necroptosis; RIPK3; TNF

Indexed keywords

ENZYME; ESCRT PROTEIN; FLOTILLIN; INTERLEUKIN 18; INTERLEUKIN 1BETA; MEMBRANE PROTEIN; MIXED LINEAGE KINASE DOMIAN LIKE PROTEIN; PROTEIN KINASE; RECEPTOR INTERACTING PROTEIN KINASE 3; UNCLASSIFIED DRUG; MLKL PROTEIN, HUMAN; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE; RIPK3 PROTEIN, HUMAN; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; ENZYME PHOSPHORYLATION; EXOSOME; FEMALE; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; MOUSE; NECROPTOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN TRANSPORT; APOPTOSIS; CELL LINE; GENETICS; IMMUNOLOGY; METABOLISM; MUTATION; NECROSIS; PHOSPHORYLATION; PROTEIN ENGINEERING; PROTEOMICS; SIGNAL TRANSDUCTION;

APOPTOSIS; CELL LINE; ENDOSOMES; EXTRACELLULAR VESICLES; HUMANS; MUTATION; NECROSIS; PHOSPHORYLATION; PROTEIN ENGINEERING; PROTEIN KINASES; PROTEIN TRANSPORT; PROTEOMICS; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 85021771054     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2017.06.001     Document Type: Article

References (62)

1. Babst, M., Odorizzi, G., Estepa, E.J., Emr, S.D., Mammalian tumor susceptibility gene 101 (TSG101) and the yeast homologue, Vps23p, both function in late endosomal trafficking. Traffic 1 (2000), 248–258.
2. Bissig, C., Gruenberg, J., Lipid sorting and multivesicular endosome biogenesis. Cold Spring Harb. Perspect. Biol., 5, 2013, a016816.
3. Bonnet, M.C., Preukschat, D., Welz, P.S., van Loo, G., Ermolaeva, M.A., Bloch, W., Haase, I., Pasparakis, M., The adaptor protein FADD protects epidermal keratinocytes from necroptosis in vivo and prevents skin inflammation. Immunity 35 (2011), 572–582.
4. Budihardjo, I., Oliver, H., Lutter, M., Luo, X., Wang, X., Biochemical pathways of caspase activation during apoptosis. Annu. Rev. Cell Dev. Biol. 15 (1999), 269–290.
5. Caton, M.L., Smith-Raska, M.R., Reizis, B., Notch-RBP-J signaling controls the homeostasis of CD8- dendritic cells in the spleen. J. Exp. Med. 204 (2007), 1653–1664.
6. Chairoungdua, A., Smith, D.L., Pochard, P., Hull, M., Caplan, M.J., Exosome release of β-catenin: a novel mechanism that antagonizes Wnt signaling. J. Cell Biol. 190 (2010), 1079–1091.
7. 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.
8. Chiou, N.-T., Ansel, K.M., Improved exosome isolation by sucrose gradient fractionation of ultracentrifuged crude exosome pellets. Protoc. Exch., 2016, 10.1038/protex.2016.057 Published online August 23, 2016.
9. 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.
10. Christofferson, D.E., Li, Y., Yuan, J., Control of life-or-death decisions by RIP1 kinase. Annu. Rev. Physiol. 76 (2014), 129–150.
11. Colombo, M., Raposo, G., Théry, C., Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu. Rev. Cell Dev. Biol. 30 (2014), 255–289.
12. Conos, S.A., Chen, K.W., De Nardo, D., Hara, H., Whitehead, L., Núñez, G., Masters, S.L., Murphy, J.M., Schroder, K., Vaux, D.L., et al. Active MLKL triggers the NLRP3 inflammasome in a cell-intrinsic manner. Proc. Natl. Acad. Sci. USA 114 (2017), E961–E969.
13. Degterev, A., Hitomi, J., Germscheid, M., Ch'en, I.L., Korkina, O., Teng, X., Abbott, D., Cuny, G.D., Yuan, C., Wagner, G., et al. Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat. Chem. Biol. 4 (2008), 313–321.
14. 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.
15. Dunning, C.J., McKenzie, M., Sugiana, C., Lazarou, M., Silke, J., Connelly, A., Fletcher, J.M., Kirby, D.M., Thorburn, D.R., Ryan, M.T., Human CIA30 is involved in the early assembly of mitochondrial complex I and mutations in its gene cause disease. EMBO J. 26 (2007), 3227–3237.
16. Duprez, L., Takahashi, N., Van Hauwermeiren, F., Vandendriessche, B., Goossens, V., Vanden Berghe, T., Declercq, W., Libert, C., Cauwels, A., Vandenabeele, P., RIP kinase-dependent necrosis drives lethal systemic inflammatory response syndrome. Immunity 35 (2011), 908–918.
17. Eder, C., Mechanisms of interleukin-1beta release. Immunobiology 214 (2009), 543–553.
18. Gloeckner, C.J., Boldt, K., Schumacher, A., Roepman, R., Ueffing, M., A novel tandem affinity purification strategy for the efficient isolation and characterisation of native protein complexes. Proteomics 7 (2007), 4228–4234.
19. Gong, Y.N., Guy, C., Olauson, H., Becker, J.U., Yang, M., Fitzgerald, P., Linkermann, A., Green, D.R., ESCRT-III acts downstream of MLKL to regulate necroptotic cell death and its consequences. Cell 169 (2017), 286–300.e16.
20. Gur, G., Zwang, Y., and Yarden, Y. (2006). Endocytosis of Receptor Tyrosine Kinases: Implications for Signal Transduction by Growth Factors. https://www.ncbi.nlm.nih.gov/books/NBK6589/.
21. Han-Min, S., Vandenabeele, P., (eds.) Necrotic Cell Death, 2014, Humana Press, New York.
22. 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.
23. 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.
24. 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.
25. 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.
26. Jimenez, A.J., Maiuri, P., Lafaurie-Janvore, J., Divoux, S., Piel, M., Perez, F., ESCRT machinery is required for plasma membrane repair. Science, 343, 2014, 1247136.
27. Kang, T.B., Ben-Moshe, T., Varfolomeev, E.E., Pewzner-Jung, Y., Yogev, N., Jurewicz, A., Waisman, A., Brenner, O., Haffner, R., Gustafsson, E., et al. Caspase-8 serves both apoptotic and nonapoptotic roles. J. Immunol. 173 (2004), 2976–2984.
28. 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.
29. Katzmann, D.J., Odorizzi, G., Emr, S.D., Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3 (2002), 893–905.
30. Keller, A., Nesvizhskii, A.I., Kolker, E., Aebersold, R., Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 74 (2002), 5383–5392.
31. Kelliher, M.A., Grimm, S., Ishida, Y., Kuo, F., Stanger, B.Z., Leder, P., The death domain kinase RIP mediates the TNF-induced NF-kappaB signal. Immunity 8 (1998), 297–303.
32. Kovalenko, A., Kim, J.C., Kang, T.B., Rajput, A., Bogdanov, K., Dittrich-Breiholz, O., Kracht, M., Brenner, O., Wallach, D., Caspase-8 deficiency in epidermal keratinocytes triggers an inflammatory skin disease. J. Exp. Med. 206 (2009), 2161–2177.
33. Krelin, Y., Zhang, L., Kang, T.B., Appel, E., Kovalenko, A., Wallach, D., Caspase-8 deficiency facilitates cellular transformation in vitro. Cell Death Differ. 15 (2008), 1350–1355.
34. Lopez-Castejon, G., Brough, D., Understanding the mechanism of IL-1β secretion. Cytokine Growth Factor Rev. 22 (2011), 189–195.
35. Mamińska, A., Bartosik, A., Banach-Orłowska, M., Pilecka, I., Jastrzębski, K., Zdżalik-Bielecka, D., Castanon, I., Poulain, M., Neyen, C., Wolińska-Nizioł, L., et al. ESCRT proteins restrict constitutive NF-κB signaling by trafficking cytokine receptors. Sci. Signal., 9, 2016, ra8.
36. Meister, M., Tikkanen, R., Endocytic trafficking of membrane-bound cargo: a flotillin point of view. Membranes (Basel) 4 (2014), 356–371.
37. Morgenstern, J.P., Land, H., Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18 (1990), 3587–3596.
38. 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.
39. 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.
40. Newton, K., Dugger, D.L., Maltzman, A., Greve, J.M., Hedehus, M., Martin-McNulty, B., Carano, R.A., Cao, T.C., van Bruggen, N., Bernstein, L., 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. 23 (2016), 1565–1576.
41. 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.
42. Ostrowski, M., Carmo, N.B., Krumeich, S., Fanget, I., Raposo, G., Savina, A., Moita, C.F., Schauer, K., Hume, A.N., Freitas, R.P., et al. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat. Cell Biol. 12 (2010), 19–30 1–13.
43. Pasparakis, M., Vandenabeele, P., Necroptosis and its role in inflammation. Nature 517 (2015), 311–320.
44. Quarato, G., Guy, C.S., Grace, C.R., Llambi, F., Nourse, A., Rodriguez, D.A., Wakefield, R., Frase, S., Moldoveanu, T., Green, D.R., Sequential engagement of distinct MLKL phosphatidylinositol-binding sites executes necroptosis. Mol. Cell 61 (2016), 589–601.
45. Shalit, T., Elinger, D., Savidor, A., Gabashvili, A., Levin, Y., MS1-based label-free proteomics using a quadrupole orbitrap mass spectrometer. J. Proteome Res. 14 (2015), 1979–1986.
46. 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.
47. 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.
48. Thery, C., Amigorena, S., Raposo, G., Clayton, A., Isolation and characterization of exosomes from cell culture supernatants and biological fluids, Chapter 3, 2006, Curr. Protoc. Cell Biol, 22.
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. Varfolomeev, E., Blankenship, J.W., Wayson, S.M., Fedorova, A.V., Kayagaki, N., Garg, P., Zobel, K., Dynek, J.N., Elliott, L.O., Wallweber, H.J., et al. IAP antagonists induce autoubiquitination of c-IAPs, NF-kappaB activation, and TNFalpha-dependent apoptosis. Cell 131 (2007), 669–681.
51. Vercammen, D., Beyaert, R., Denecker, G., Goossens, V., Van Loo, G., Declercq, W., Grooten, J., Fiers, W., Vandenabeele, P., Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor. J. Exp. Med. 187 (1998), 1477–1485.
52. Verweij, F.J., van Eijndhoven, M.A., Hopmans, E.S., Vendrig, T., Wurdinger, T., Cahir-McFarland, E., Kieff, E., Geerts, D., van der Kant, R., Neefjes, J., et al. LMP1 association with CD63 in endosomes and secretion via exosomes limits constitutive NF-κB activation. EMBO J. 30 (2011), 2115–2129.
53. Vieira, A.V., Lamaze, C., Schmid, S.L., Control of EGF receptor signaling by clathrin-mediated endocytosis. Science 274 (1996), 2086–2089.
54. Wallach, D., Kang, T.-B., Kovalenko, A., The extrinsic cell death pathway and the élan mortel. Cell Death Differ. 15 (2008), 1533–1541.
55. Wallach, D., Kovalenko, A., Kang, T.B., ‘Necrosome’-induced inflammation: must cells die for it?. Trends Immunol. 32 (2011), 505–509.
56. Wallach, D., Kang, T.B., Yang, S.H., Kovalenko, A., The in vivo significance of necroptosis: lessons from exploration of caspase-8 function. Cytokine Growth Factor Rev. 25 (2014), 157–165.
57. 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.
58. Williams, R.L., Urbé, S., The emerging shape of the ESCRT machinery. Nat. Rev. Mol. Cell Biol. 8 (2007), 355–368.
59. Yoon, S., Bogdanov, K., Kovalenko, A., Wallach, D., Necroptosis is preceded by nuclear translocation of the signaling proteins that induce it. Cell Death Differ. 23 (2016), 253–260.
60. 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.
61. 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.
62. Zhao, H., Jaffer, T., Eguchi, S., Wang, Z., Linkermann, A., Ma, D., Role of necroptosis in the pathogenesis of solid organ injury. Cell Death Dis., 6, 2015, e1975.