Intracellular nicotinamide adenine dinucleotide promotes TNF-induced necroptosis in a sirtuin-dependent manner

Cell Death and Differentiation

Volumn 23, Issue 1, 2016, Pages 29-40

  Preyat, N ^a   Rossi, M ^a   Kers, J ^b   Chen, L ^c   Bertin, J ^d   Gough, P J ^d   Le Moine, A ^a   Rongvaux, A ^e   Van Gool, F ^f   Leo, O ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c UNIVERSITY OF MINNESOTA   (United States)

^d GLAXOSMITHKLINE   (United States)

^e YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 8; NICOTINAMIDE ADENINE DINUCLEOTIDE; SHORT HAIRPIN RNA; SIRTUIN; SIRTUIN 2; SIRTUIN 5; TUMOR NECROSIS FACTOR; FAS LIGAND; FASLG PROTEIN, HUMAN; LIGAND; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE; RIPK3 PROTEIN, HUMAN; SIRT2 PROTEIN, HUMAN; SIRT5 PROTEIN, HUMAN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; KIDNEY ISCHEMIA; L929 CELL LINE; MOUSE; NECROPTOSIS; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY; CELL LINE; CYTOPLASM; GENETICS; METABOLISM; NECROSIS;

APOPTOSIS; CELL LINE; CYTOPLASM; FAS LIGAND PROTEIN; HUMANS; LIGANDS; NAD; NECROSIS; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; SIRTUIN 2; SIRTUINS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84949533872     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2015.60     Document Type: Article

References (68)

1. Imai S, Guarente L. Ten years of NAD-Dependent SIR2 family deacetylases: implications for metabolic diseases. Trends Pharmacol Sci 2010; 31: 212-220.
2. Houtkooper RH, Canto C, Wanders RJ, Auwerx J. The secret life of NAD+: an old metabolite controlling new metabolic signaling pathways. Endocr Rev 2010; 31: 194-223.
3. Chiarugi A, Dölle C, Felici R, Ziegler M. The NAD metabolome-A key determinant of cancer cell biology. Nat Rev Cancer 2012; 12: 741-752.
4. Feldman JL, Baeza J, Denu JM. Activation of the protein deacetylase SIRT6 by long-chain fatty acids and widespread deacylation by mammalian sirtuins. J Biol Chem 2013; 288: 31350-31356.
5. Verdin E. The many faces of sirtuins: Coupling of NAD metabolism, sirtuins and lifespan. Nat Med 2014; 20: 25-27.
6. Kolthur-Seetharam U, Dantzer F, McBurney MW, de Murcia G, Sassone-Corsi P. Control of AIF-mediated cell death by the functional interplay of SIRT1 and PARP-1 in response to DNA damage. Cell Cycle 2006; 5: 873-877.
7. Alano CC, Garnier P, Ying W, Higashi Y, Kauppinen TM, Swanson RA. NAD+ depletion is necessary and sufficient for poly(ADP-ribose) polymerase-1-mediated neuronal death. J Neurosci 2010; 30: 2967-2978.
8. Yu S-W, Wang H, Poitras MF, Coombs C, Bowers WJ, Federoff HJ., et al. Mediation of poly (ADP-ribose) polymerase-1-Dependent cell death by apoptosis-inducing factor. Science 2002; 297: 259-263.
9. Andrabi Sa, Kim NS, Yu S-W, Wang H, Koh DW, Sasaki M., et al. Poly(ADP-ribose) (PAR) polymer is a death signal. Proc Natl Acad Sci USA 2006; 103: 18308-18313.
10. Yu S-W, Andrabi Sa, Wang H, Kim NS, Poirier GG, Dawson TM., et al. Apoptosis-inducing factor mediates poly(ADP-ribose) (PAR) polymer-induced cell death. Proc Natl Acad Sci USA 2006; 103: 18314-18319.
11. Artus C, Boujrad H, Bouharrour A, Brunelle M-N, Hoos S, Yuste VJ., et al. AIF promotes chromatinolysis and caspase-independent programmed necrosis by interacting with histone H2AX. EMBO J 2010; 29: 1585-1599.
12. Welsby I, Hutin D, Leo O. Complex roles of members of the ADP-ribosyl transferase super family in immune defences: looking beyond PARP1. Biochem Pharmacol 2012; 84: 11-20.
13. Ying W, Garnier P, Swanson RA. NAD+ repletion prevents PARP-1-induced glycolytic blockade and cell death in cultured mouse astrocytes. Biochem Biophys Res Commun 2003; 308: 809-813.
14. Pillai JB, Isbatan A, Imai S, Gupta MP. Poly(ADP-ribose) polymerase-1-Dependent cardiac myocyte cell death during heart failure is mediated by NAD+ depletion and reduced Sir2alpha deacetylase activity. J Biol Chem 2005; 280: 43121-43130.
15. Zhu K, Swanson RA, Ying W. NADH can enter into astrocytes and block poly(ADP-ribose) polymerase-1-mediated astrocyte death. Neuroreport 2005; 16: 1209-1212.
16. Yang H, Yang T, Baur Ja, Perez E, Matsui T, Carmona JJ., et al. Nutrient-sensitive mitochondrial NAD+ levels dictate cell survival. Cell 2007; 130: 1095-1107.
17. Van der Veer E, Ho C, O?Neil C, Barbosa N, Scott R, Cregan SP., et al. Extension of human cell lifespan by nicotinamide phosphoribosyltransferase. J Biol Chem 2007; 282: 10841-10845.
18. Rongvaux A, Galli M, Denanglaire S, Van Gool F, Drèze PL, Szpirer C., et al. Nicotinamide phosphoribosyl transferase/pre-B cell colony-Enhancing factor/visfatin is required for lymphocyte development and cellular resistance to genotoxic stress. J Immunol 2008; 181: 4685-4695.
19. Rongvaux A, Shea RJ, Mulks MH, Gigot D, Urbain J, Leo O., et al. Pre-B-cell colonyenhancing factor, whose expression is up-regulated in activated lymphocytes, is a nicotinamide phosphoribosyltransferase, a cytosolic enzyme involved in NAD biosynthesis. Eur J Immunol 2002; 32: 3225-3234.
20. Revollo JR, Körner A, Mills KF, Satoh A, Wang T, Garten A., et al. Nampt/PBEF/Visfatin regulates insulin secretion in beta cells as a systemic NAD biosynthetic enzyme. Cell Metab 2007; 6: 363-375.
21. Holler N, Zaru R, Micheau O, Thome M, Attinger A, Valitutti S., et al. Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat Immunol 2000; 1: 489-495.
22. Degterev A, Huang Z, Boyce M, Li Y, Jagtap P, Mizushima N., et al. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol 2005; 1: 112-119.
23. Vercammen D, Vandenabeele P, Beyaert R, Declercq W, Fiers W. Tumour necrosis factorinduced necrosis versus anti-Fas-induced apoptosis in L929 cells. Cytokine 1997; 9: 801-808.
24. Van Horssen R, Willemse M, Haeger A, Attanasio F, Güneri T, Schwab A., et al. Intracellular NAD(H) levels control motility and invasion of glioma cells. Cell Mol Life Sci 2013; 70: 2175-2190.
25. McClure JM, Wierman MB, Maqani N, Smith JS. Isonicotinamide enhances Sir2 proteinmediated silencing and longevity in yeast by raising intracellular NAD+ concentration. J Biol Chem 2012; 287: 20957-20966.
26. Degterev A, Maki JL, Yuan J. Activity and specificity of necrostatin-1, small-molecule inhibitor of RIP1 kinase. Cell Death Differ 2013; 20: 366.
27. Li J-X, Feng J-M, Wang Y, Li X-H, Chen X-X, Su Y., et al. The B-Raf(V600E) inhibitor dabrafenib selectively inhibits RIP3 and alleviates acetaminophen-induced liver injury. Cell Death Dis 2014; 5: e1278.
28. Wang Z, Jiang H, Chen S, Du F, Wang X. The mitochondrial phosphatase PGAM5 functions at the covergence point of multiple necrotic death pathways. Cell 2012; 148: 228-243.
29. Tait SWG, Oberst A, Quarato G, Milasta S, Haller M, Wang R., et al. Widespread mitochondrial depletion via mitophagy does not compromise necroptosis. Cell Rep 2013; 5: 878-885.
30. Cai Z, Jitkaew S, Zhao J, Chiang H-C, 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.
31. Chen X, Li W, Ren J, Huang D, He W-T, 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.
32. Mouchiroud L, Houtkooper RH, Auwerx J. NAD+ metabolism: a therapeutic target for agerelated metabolic disease. Crit Rev Biochem Mol Biol 2013; 48: 397-408.
33. Narayan N, Lee IH, Borenstein R, Sun J, Wong R, Tong G., et al. The NAD-Dependent deacetylase SIRT2 is required for programmed necrosis. Nature 2012; 492: 199-204.
34. Solomon JM, Pasupuleti R, Xu L, McDonagh T, Curtis R, DiStefano PS., et al. Inhibition of SIRT1 catalytic activity increases p53 acetylation but does not alter cell survival following DNA damage. Mol Cell Biol 2006; 26: 28-38.
35. Cui H, Kamal Z, Ai T, Xu Y, More SS, Wilson DJ., et al. Discovery of potent and selective sirtuin 2 (SIRT2) inhibitors using a fragment-based approach. J Med Chem 2014; 57: 8340-8357.
36. Heltweg B, Gatbonton T, Schuler AD, Posakony J, Li H, Goehle S., et al. Antitumor activity of a small-molecule inhibitor of human silent information regulator 2 enzymes. Cancer Res 2006; 66: 4368-4377.
37. Legarda-Addison D, Hase H, O?Donnell Ma, Ting aT. NEMO/IKKgamma regulates an early NF-kappaB-independent cell-Death checkpoint during TNF signaling. Cell Death Differ 2009; 16: 1279-1288.
38. 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.
39. 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.
40. 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.
41. Pop C, Oberst A, Drag M, Van Raam BJ, Riedl SJ, Green DR., et al. FLIP(L) induces caspase 8 activity in the absence of interdomain caspase 8 cleavage and alters substrate specificity. Biochem J 2011; 433: 447-457.
42. Lovric MM, Hawkins CJ. TRAIL treatment provokes mutations in surviving cells. Oncogene 2010; 29: 5048-5060.
43. O?Donnell MA, Perez-Jimenez E, Oberst A, Ng A, Massoumi R, Xavier R., et al. Caspase 8 inhibits programmed necrosis by processing CYLD. Nat Cell Biol 2011; 13: 1437-1442.
44. Rosenbaum DM, Degterev A, David J, Rosenbaum PS, Roth S, Grotta JC., et al. Necroptosis, a novel form of caspase-independent cell death, contributes to neuronal damage in a retinal ischemia-reperfusion injury model. J Neurosci Res 2010; 88: 1569-1576.
45. Linkermann A, Brasen JH, Himmerkus N, Liu S, Huber TB, Kunzendorf U., et al. Rip1 (receptor-interacting protein kinase 1) mediates necroptosis and contributes to renal ischemia/reperfusion injury. Kidney Int 2012; 81: 751-761.
46. Linkermann A, Brasen JH, Darding M, Jin MK, Sanz AB, Heller J-O., et al. Two independent pathways of regulated necrosis mediate ischemia-reperfusion injury. Proc Natl Acad Sci USA 2013; 110: 12024-12029.
47. Lugrin J, Ciarlo E, Santos A, Grandmaison G, dos Santos I, Le Roy D., et al. The sirtuin inhibitor cambinol impairs MAPK signaling, inhibits inflammatory and innate immune responses and protects from septic shock. Biochim Biophys Acta 2013; 1833: 1498-1510.
48. Maurer B, Rumpf T, Scharfe M, Stolfa Da, Schmitt ML, He W., et al. Inhibitors of the NAD (+)-Dependent protein desuccinylase and demalonylase Sirt5. ACS Med Chem Lett 2012; 3: 1050-1053.
49. Preyat N, Leo O. Sirtuin deacylases: a molecular link between metabolism and immunity. J Leukoc Biol 2013; 93: 669-680.
50. Newton K, Hildebrand JM, Shen Z, Rodriguez D, Alvarez-Diaz S, Petersen S., et al. Is SIRT2 required for necroptosis? Nature 2014; 506: E4-E6.
51. Temkin V, Huang Q, Liu H, Osada H, Pope RM. Inhibition of ADP/ATP exchange in receptorinteracting protein-mediated necrosis. Mol Cell Biol 2006; 26: 2215-2225.
52. Wu Y-T, Tan H-L, Huang Q, Sun X-J, Zhu X, Shen H-M. zVAD-induced necroptosis in L929 cells depends on autocrine production of TNFa mediated by the PKC-MAPKs-AP-1 pathway. Cell Death Differ 2011; 18: 26-37.
53. Kearney CJ, Cullen SP, Tynan Ga, Henry CM, Clancy D, Lavelle EC., et al. Necroptosis suppresses inflammation via termination of TNF-or LPS-induced cytokine and chemokine production. Cell Death Differ 2015; 22: 1313-1327.
54. Rongvaux A, Jackson R, Harman CCD, Li T, West AP, de Zoete MR., et al. Apoptotic caspases prevent the induction of type I interferons by mitochondrial DNA. Cell 2014; 159: 1563-1577.
55. White MJ, McArthur K, Metcalf D, Lane RM, Cambier JC, Herold MJ., et al. Apoptotic caspases supress mtDNA-induced STING-mediated type I IFN production. Cell 2014; 159: 1549-1562.
56. 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.
57. 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.
58. G?nther C, Buchen B, He G-W, Hornef M, Torow N, Neumann H., et al. Caspase-8 controls the gut response to microbial challenges by Tnf-A-Dependent and independent pathways. Gut 2014; 64: 601-610.
59. Hsu C-P, Oka S, Shao D, Hariharan N, Sadoshima J. Nicotinamide phosphoribosyltransferase regulates cell survival through NAD+ synthesis in cardiac myocytes. Circ Res 2009; 105: 481-491.
60. Cea M, Cagnetta A, Fulciniti M, Tai Y-T, Hideshima T, Chauhan D., et al. Targeting NAD+salvage pathway induces autophagy in multiple myeloma cells via mTORC1 and extracellular signal-regulated kinase (ERK1/2) inhibition. Blood 2012; 120: 3519-3529.
61. Cagnetta A, Cea M, Calimeri T, Acharya C, Fulciniti M, Tai Y-T., et al. Intracellular NAD+ depletion enhances bortezomib-induced anti-myeloma activity. Blood 2013; 122: 1243-1255.
62. Billington RA, Genazzani AA, Travelli C, Condorelli F. NAD depletion by FK866 induces autophagy. Autophagy 2008; 4: 385-387.
63. Gomes AP, Price NL, Ling AJY, Moslehi JJ, Montgomery MK, Rajman L., et al. Declining NAD (+) induces a pseudohypoxic state disrupting nuclear-mitochondrial communication during aging. Cell 2013; 155: 1624-1638.
64. Zerez CR, Lee SJ, Tanaka KR. Spectrophotometric determination of oxidized and reduced pyridine nucleotides in erythrocytes using a single extraction procedure. Anal Biochem 1987; 164: 367-373.
65. Wagner TC, Scott MD. Single extraction method for the spectrophotometric quantification of oxidized and reduced pyridine nucleotides in erythrocytes. Anal Biochem 1994; 222: 417-426.
66. Plaisance S, Vanden Berghe W, Boone E, Fiers W, Haegeman G. Recombination signal sequence binding protein Jkappa is constitutively bound to the NF-kappaB site of the interleukin-6 promoter and acts as a negative regulatory factor. Mol Cell Biol 1997; 17: 3733-3743.
67. Liu X, Constantinescu SN, Sun Y, Bogan JS, Hirsch D, Weinberg RA., et al. Generation of mammalian cells stably expressing multiple genes at predetermined levels. Anal Biochem 2000; 280: 20-28.
68. Ran FA, Hsu PD, Wright J, Agarwala V, Scott Da, Zhang F. Genome engineering using the CRISPR-Cas9 system. Nat Protoc 2013; 8: 2281-2308.