2,690
Views
48
CrossRef citations to date
0
Altmetric
Basic Science Research Papers

Poly-ADP-ribosylation of HMGB1 regulates TNFSF10/TRAIL resistance through autophagy

, , , , , , , , & show all
Pages 214-224 | Received 10 Mar 2014, Accepted 10 Nov 2014, Published online: 01 Apr 2015

References

  • Hengartner MO. The biochemistry of apoptosis. Nature 2000; 407:770-6; PMID:11048727; http://dx.doi.org/10.1038/35037710
  • Klionsky DJ, Emr SD. Autophagy as a regulated pathway of cellular degradation. Science 2000; 290:1717-21; PMID:11099404; http://dx.doi.org/10.1126/science.290.5497.1717
  • Yang Z, Klionsky DJ. Eaten alive: a history of macroautophagy. Nat Cell Biol 2010; 12:814-22; PMID:20811353; http://dx.doi.org/10.1038/ncb0910-814
  • Maiuri MC, Zalckvar E, Kimchi A, Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 2007; 8:741-52; PMID:17717517; http://dx.doi.org/10.1038/nrm2239
  • Amaravadi RK, Lippincott-Schwartz J, Yin XM, Weiss WA, Takebe N, Timmer W, DiPaola RS, Lotze MT, White E. Principles and current strategies for targeting autophagy for cancer treatment. Clin Cancer Res 2011; 17:654-66; PMID:21325294; http://dx.doi.org/10.1158/1078-0432.CCR-10-2634
  • Kang R, Zeh HJ, Lotze MT, Tang D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ 2011; 18:571-80; PMID:21311563; http://dx.doi.org/10.1038/cdd.2010.191
  • Wiley SR, Schooley K, Smolak PJ, Din WS, Huang CP, Nicholl JK, Sutherland GR, Smith TD, Rauch C, Smith CA, et al. Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity 1995; 3:673-82; PMID:8777713; http://dx.doi.org/10.1016/1074-7613(95)90057-8
  • Johnstone RW, Frew AJ, Smyth MJ. The TRAIL apoptotic pathway in cancer onset, progression and therapy. Nat Rev Cancer 2008; 8:782-98; PMID:18813321; http://dx.doi.org/10.1038/nrc2465
  • Ashkenazi A, Dixit VM. Death receptors: signaling and modulation. Science 1998; 281:1305-8; PMID:9721089; http://dx.doi.org/10.1126/science.281.5381.1305
  • Jin Z, McDonald ER, 3rd, Dicker DT, El-Deiry WS. Deficient tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) death receptor transport to the cell surface in human colon cancer cells selected for resistance to TRAIL-induced apoptosis. J Biol Chem 2004; 279:35829-39; PMID:15155747; http://dx.doi.org/10.1074/jbc.M405538200
  • Eggert A, Grotzer MA, Zuzak TJ, Wiewrodt BR, Ho R, Ikegaki N, Brodeur GM. Resistance to tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis in neuroblastoma cells correlates with a loss of caspase-8 expression. Cancer Res 2001; 61:1314-9; PMID:11245427
  • Hopkins-Donaldson S, Bodmer JL, Bourloud KB, Brognara CB, Tschopp J, Gross N. Loss of caspase-8 expression in highly malignant human neuroblastoma cells correlates with resistance to tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis. Cancer Res 2000; 60:4315-9; PMID:10969767
  • Wagner KW, Punnoose EA, Januario T, Lawrence DA, Pitti RM, Lancaster K, Lee D, von Goetz M, Yee SF, Totpal K, et al. Death-receptor O-glycosylation controls tumor-cell sensitivity to the proapoptotic ligand Apo2L/TRAIL. Nat Med 2007; 13:1070-7; PMID:17767167; http://dx.doi.org/10.1038/nm1627
  • Pan G, Ni J, Yu G, Wei YF, Dixit VM. TRUNDD, a new member of the TRAIL receptor family that antagonizes TRAIL signalling. FEBS Lett 1998; 424:41-5; PMID:9537512; http://dx.doi.org/10.1016/S0014-5793(98)00135-5
  • Krueger A, Baumann S, Krammer PH, Kirchhoff S. FLICE-inhibitory proteins: regulators of death receptor-mediated apoptosis. Mol Cell Biol 2001; 21:8247-54; PMID:11713262; http://dx.doi.org/10.1128/MCB.21.24.8247-8254.2001
  • Ricci MS, Kim SH, Ogi K, Plastaras JP, Ling J, Wang W, Jin Z, Liu YY, Dicker DT, Chiao PJ, et al. Reduction of TRAIL-induced Mcl-1 and cIAP2 by c-Myc or sorafenib sensitizes resistant human cancer cells to TRAIL-induced death. Cancer Cell 2007; 12:66-80; PMID:17613437; http://dx.doi.org/10.1016/j.ccr.2007.05.006
  • Gump JM, Staskiewicz L, Morgan MJ, Bamberg A, Riches DW, Thorburn A. Autophagy variation within a cell population determines cell fate through selective degradation of Fap-1. Nat Cell Biol 2014; 16:47-54; PMID:24316673; http://dx.doi.org/10.1038/ncb2886
  • Hou W, Han J, Lu C, Goldstein LA, Rabinowich H. Autophagic degradation of active caspase-8: A crosstalk mechanism between autophagy and apoptosis. Autophagy 2010; 6:891-900; PMID:20724831; http://dx.doi.org/10.4161/auto.6.7.13038
  • Han J, Hou W, Goldstein LA, Lu C, Stolz DB, Yin XM, Rabinowich H. Involvement of protective autophagy in TRAIL resistance of apoptosis-defective tumor cells. J Biol Chem 2008; 283:19665-77; PMID:18375389; http://dx.doi.org/10.1074/jbc.M710169200
  • Kang R, Chen R, Zhang Q, Hou W, Wu S, Cao L, Huang J, Yu Y, Fan XG, Yan Z, et al. HMGB1 in health and disease. Mol Aspects Med 2014; PMID:25010388
  • Tang D, Kang R, Zeh HJ, 3rd, Lotze MT. High-mobility group box 1 and cancer. Biochim Biophys Acta 2010; 1799:131-40; PMID:20123075; http://dx.doi.org/10.1016/j.bbagrm.2009.11.014
  • Tang D, Kang R, Livesey KM, Kroemer G, Billiar TR, Van Houten B, Zeh HJ, 3rd, Lotze MT. High-mobility group box 1 is essential for mitochondrial quality control. Cell Metab 2011; 13:701-11; PMID:21641551; http://dx.doi.org/10.1016/j.cmet.2011.04.008
  • Tang D, Kang R, Livesey KM, Cheh CW, Farkas A, Loughran P, Hoppe G, Bianchi ME, Tracey KJ, Zeh HJ, 3rd, Lotze MT. Endogenous HMGB1 regulates autophagy. J Cell Biol 2010; 190:881-92; PMID:20819940; http://dx.doi.org/10.1083/jcb.200911078
  • Tang D, Kang R, Cheh CW, Livesey KM, Liang X, Schapiro NE, Benschop R, Sparvero LJ, Amoscato AA, Tracey KJ, et al. HMGB1 release and redox regulates autophagy and apoptosis in cancer cells. Oncogene 2010; 29:5299-310; PMID:20622903; http://dx.doi.org/10.1038/onc.2010.261
  • Yuan K, Sun Y, Zhou T, McDonald J, Chen Y. PARP-1 regulates resistance of pancreatic cancer to TRAIL therapy. Clin Cancer Res 2013; 19:4750-9; PMID:23833311; http://dx.doi.org/10.1158/1078-0432.CCR-13-0516
  • Ulloa L, Ochani M, Yang H, Tanovic M, Halperin D, Yang R, Czura CJ, Fink MP, Tracey KJ. Ethyl pyruvate prevents lethality in mice with established lethal sepsis and systemic inflammation. Proc Natl Acad Sci U S A 2002; 99:12351-6; PMID:12209006; http://dx.doi.org/10.1073/pnas.192222999
  • Bonaldi T, Talamo F, Scaffidi P, Ferrera D, Porto A, Bachi A, Rubartelli A, Agresti A, Bianchi ME. Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. Embo J 2003; 22:5551-60; PMID:14532127; http://dx.doi.org/10.1093/emboj/cdg516
  • Youn JH, Shin JS. Nucleocytoplasmic Shuttling of HMGB1 Is Regulated by Phosphorylation That Redirects It toward Secretion. J Immunol 2006; 177:7889-97; PMID:17114460; http://dx.doi.org/10.4049/jimmunol.177.11.7889
  • Luo X, Kraus WL. On PAR with PARP: cellular stress signaling through poly(ADP-ribose) and PARP-1. Genes Dev 2012; 26:417-32; PMID:22391446; http://dx.doi.org/10.1101/gad.183509.111
  • Abhari BA, Cristofanon S, Kappler R, von Schweinitz D, Humphreys R, Fulda S. RIP1 is required for IAP inhibitor-mediated sensitization for TRAIL-induced apoptosis via a RIP1/FADD/caspase-8 cell death complex. Oncogene 2013; 32:3263-73; PMID:22890322; http://dx.doi.org/10.1038/onc.2012.337
  • Jouan-Lanhouet S, Arshad MI, Piquet-Pellorce C, Martin-Chouly C, Le Moigne-Muller G, Van Herreweghe F, Takahashi N, Sergent O, Lagadic-Gossmann D, Vandenabeele P, et al. TRAIL induces necroptosis involving RIPK1/RIPK3-dependent PARP-1 activation. Cell Death Differ 2012; 19:2003-14; PMID:22814620; http://dx.doi.org/10.1038/cdd.2012.90
  • Zhang N, Chen Y, Jiang R, Li E, Chen X, Xi Z, Guo Y, Liu X, Zhou Y, Che Y, et al. PARP and RIP 1 are required for autophagy induced by 11'-deoxyverticillin A, which precedes caspase-dependent apoptosis. Autophagy 2011; 7:598-612; PMID:21460625; http://dx.doi.org/10.4161/auto.7.6.15103
  • Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. Embo J 2000; 19:5720-8; PMID:11060023; http://dx.doi.org/10.1093/emboj/19.21.5720
  • Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8:445-544; PMID:22966490; http://dx.doi.org/10.4161/auto.19496
  • Seol DW, Li J, Seol MH, Park SY, Talanian RV, Billiar TR. Signaling events triggered by tumor necrosis factor-related apoptosis-inducing ligand (TRAIL): caspase-8 is required for TRAIL-induced apoptosis. Cancer Res 2001; 61:1138-43; PMID:11221844
  • Goodwin GH, Sanders C, Johns EW. A new group of chromatin-associated proteins with a high content of acidic and basic amino acids. Eur J Biochem 1973; 38:14-9; PMID:4774120; http://dx.doi.org/10.1111/j.1432-1033.1973.tb03026.x
  • Kang R, Zhang Q, Zeh HJ, 3rd, Lotze MT, Tang D. HMGB1 in cancer: good, bad, or both? Clin Cancer Res 2013; 19:4046-57; PMID:23723299; http://dx.doi.org/10.1158/1078-0432.CCR-13-0495
  • Liu L, Yang M, Kang R, Wang Z, Zhao Y, Yu Y, Xie M, Yin X, Livesey KM, Lotze MT, et al. HMGB1-induced autophagy promotes chemotherapy resistance in leukemia cells. Leukemia 2011; 25:23-31; PMID:20927132; http://dx.doi.org/10.1038/leu.2010.225
  • Livesey KM, Kang R, Vernon P, Buchser W, Loughran P, Watkins SC, Zhang L, Manfredi JJ, Zeh HJ, 3rd, Li L, et al. p53/HMGB1 complexes regulate autophagy and apoptosis. Cancer Res 2012; 72:1996-2005; PMID:22345153; http://dx.doi.org/10.1158/0008-5472.CAN-11-2291
  • Huang J, Ni J, Liu K, Yu Y, Xie M, Kang R, Vernon P, Cao L, Tang D. HMGB1 promotes drug resistance in osteosarcoma. Cancer Res 2012; 72:230-8; PMID:22102692; http://dx.doi.org/10.1158/0008-5472.CAN-11-2001
  • Liu K, Huang J, Xie M, Yu Y, Zhu S, Kang R, Cao L, Tang D, Duan X. MIR34A regulates autophagy and apoptosis by targeting HMGB1 in the retinoblastoma cell. Autophagy 2014 Mar; 10(3):442-52.
  • Hou W, Zhang Q, Yan Z, Chen R, Zeh Iii HJ, Kang R, Lotze MT, Tang D. Strange attractors: DAMPs and autophagy link tumor cell death and immunity. Cell Death Dis 2013; 4:e966.
  • Tanuma S, Yagi T, Johnson GS. Endogenous ADP ribosylation of high mobility group proteins 1 and 2 and histone H1 following DNA damage in intact cells. Arch Biochem Biophys 1985; 237:38-42; PMID:3970545; http://dx.doi.org/10.1016/0003-9861(85)90251-6
  • Lovric MM, Hawkins CJ. TRAIL treatment provokes mutations in surviving cells. Oncogene 2010; 29:5048-60; PMID:20639907; http://dx.doi.org/10.1038/onc.2010.242
  • Solier S, Sordet O, Kohn KW, Pommier Y. Death receptor-induced activation of the Chk2- and histone H2AX-associated DNA damage response pathways. Mol Cell Biol 2009; 29:68-82; PMID:18955500; http://dx.doi.org/10.1128/MCB.00581-08
  • Kang R, Tang D, Schapiro NE, Loux T, Livesey KM, Billiar TR, Wang H, Van Houten B, Lotze MT, Zeh HJ. The HMGB1/RAGE inflammatory pathway promotes pancreatic tumor growth by regulating mitochondrial bioenergetics. Oncogene 2014; 33:567-77; PMID:23318458; http://dx.doi.org/10.1038/onc.2012.631
  • White E. Deconvoluting the context-dependent role for autophagy in cancer. Nat Rev Cancer 2012; 12:401-10; PMID:22534666; http://dx.doi.org/10.1038/nrc3262
  • He W, Wang Q, Xu J, Xu X, Padilla MT, Ren G, Gou X, Lin Y. Attenuation of TNFSF10/TRAIL-induced apoptosis by an autophagic survival pathway involving TRAF2- and RIPK1/RIP1-mediated MAPK8/JNK activation. Autophagy 2012; 8:1811-21; PMID:23051914; http://dx.doi.org/10.4161/auto.22145
  • Herrero-Martin G, Hoyer-Hansen M, Garcia-Garcia C, Fumarola C, Farkas T, Lopez-Rivas A, Jaattela M. TAK1 activates AMPK-dependent cytoprotective autophagy in TRAIL-treated epithelial cells. Embo J 2009; 28:677-85; PMID:19197243; http://dx.doi.org/10.1038/emboj.2009.8
  • Mills KR, Reginato M, Debnath J, Queenan B, Brugge JS. Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) is required for induction of autophagy during lumen formation in vitro. Proc Natl Acad Sci U S A 2004; 101:3438-43; PMID:14993595; http://dx.doi.org/10.1073/pnas.0400443101
  • Monma H, Harashima N, Inao T, Okano S, Tajima Y, Harada M. The HSP70 and Autophagy Inhibitor Pifithrin-mu Enhances the Antitumor Effects of TRAIL on Human Pancreatic Cancer. Mol Cancer Ther 2013; 12:341-51; PMID:23371857; http://dx.doi.org/10.1158/1535-7163.MCT-12-0954
  • Munoz-Gamez JA, Rodriguez-Vargas JM, Quiles-Perez R, Aguilar-Quesada R, Martin-Oliva D, de Murcia G, Menissier de Murcia J, Almendros A, Ruiz de Almodovar M, Oliver FJ. PARP-1 is involved in autophagy induced by DNA damage. Autophagy 2009; 5:61-74; PMID:19001878; http://dx.doi.org/10.4161/auto.5.1.7272
  • Yoon JH, Ahn SG, Lee BH, Jung SH, Oh SH. Role of autophagy in chemoresistance: regulation of the ATM-mediated DNA-damage signaling pathway through activation of DNA-PKcs and PARP-1. Biochem Pharmacol 2012; 83:747-57; PMID:22226932; http://dx.doi.org/10.1016/j.bcp.2011.12.029
  • Mathieu J, Flexor M, Lanotte M, Besancon F. A PARP-1/JNK1 cascade participates in the synergistic apoptotic effect of TNFalpha and all-trans retinoic acid in APL cells. Oncogene 2008; 27:3361-70; PMID:18084321; http://dx.doi.org/10.1038/sj.onc.1210997
  • Kang R, Zhang Q, Hou W, Yan Z, Chen R, Bonaroti J, Bansal P, Billiar TR, Tsung A, Wang Q, et al. Intracellular Hmgb1 inhibits inflammatory nucleosome release and limits acute pancreatitis in mice. Gastroenterology 2014; 146:1097-107; PMID:24361123; http://dx.doi.org/10.1053/j.gastro.2013.12.015
  • Seluanov A, Vaidya A, Gorbunova V. Establishing primary adult fibroblast cultures from rodents. J Vis Exp 2010 Oct 5; (44). pii: 2033. doi: 10.3791/2033.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.