Constitutive autophagy contributes to resistance to TP53-mediated apoptosis in epstein-barr viruspositive latency III B-cell lymphoproliferations

Autophagy

Volumn 11, Issue 12, 2015, Pages 2275-2287

  Pujals, Anaïs ^a,c   Favre, Loëtitia ^a   Pioche Durieu, Catherine ^a   Robert, Aude ^a   Meurice, Guillaume ^b   Gentil, Marion Le ^b   Chelouah, Sonia ^a   Martin Garcia, Nadine ^c   Cam, Eric Le ^a   Guettier, Catherine ^d   Raphaël, Martine ^a   Vassilev, Lyubomir T ^e   Gaulard, Philippe ^c   Codogno, Patrice ^f   Lipinski, Marc ^a   Wiels, Joëlle ^a  

^a UMR 8126   (France)

^b INSTITUT GUSTAVE ROUSSY   (France)

^c UNIVERSITÉ PARIS EST CRÉTEIL   (France)

^d BICÊTRE HOSPITAL   (France)

^e HOFFMANN LA ROCHE INC   (United States)

^f INSERM   (France)

Author keywords

Autophagy; BECN1; Burkitt lymphoma; EBV; Nulin 3; TP53

Indexed keywords

BECLIN 1; CHLOROQUINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; NUTLIN 3; PROTEIN P53; SESTRIN 1; UNCLASSIFIED DRUG; VIRAL PROTEIN LMP1; VIRUS PROTEIN; IMIDAZOLE DERIVATIVE; PIPERAZINE DERIVATIVE; TP53 PROTEIN, HUMAN;

ANTIVIRAL RESISTANCE; APOPTOSIS; ARTICLE; AUTOPHAGY; B LYMPHOCYTE; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; EPSTEIN BARR VIRUS INFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; UPREGULATION; VIRUS ONCOGENE; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; EPSTEIN BARR VIRUS; GENE EXPRESSION; LYMPHOMA; METABOLISM; PATHOLOGY; TUMOR CELL LINE; VIROLOGY;

APOPTOSIS; AUTOPHAGY; B-LYMPHOCYTES; CELL LINE, TUMOR; CELL PROLIFERATION; GENE EXPRESSION; HERPESVIRUS 4, HUMAN; HUMANS; IMIDAZOLES; LYMPHOMA; PIPERAZINES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84964240155     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.1080/15548627.2015.1115939     Document Type: Article

References (51)

1. Levine AJ. p53, the cellular gatekeeper for growth and division. Cell 1997; 88: 323-31; PMID: 9039259; http://dx.doi.org/10.1016/S0092-8674(00)81871-1
2. Vousden KH, Lu X. Live or let die: the cell’s response to p53. Nat Rev Cancer 2002; 2: 594-604; PMID: 12154352; http://dx.doi.org/10.1038/nrc864
3. Mizushima N. Autophagy: process and function. Genes Dev 2007; 21: 2861-73; PMID: 18006683; http://dx. doi.org/10.1101/gad.1599207
4. 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
5. Budanov AV, Karin M. p53 target genes sestrin1 and sestrin2 connect genotoxic stress and mTOR signaling. Cell 2008; 134: 451-60; PMID: 18692468; http://dx. doi.org/10.1016/j.cell.2008.06.028
6. Liu EY, Ryan KM. Autophagy and cancer-issues we need to digest. J Cell Sci 2012; 125: 2349-58; PMID: 22641689; http://dx.doi.org/10.1242/ jcs.093708
7. Tasdemir E, Chiara Maiuri M, Morselli E, Criollo A, D’Amelio M, Djavaheri-Mergny M, Cecconi F, Tavernarakis N, Kroemer G. A dual role of p53 in the control of autophagy. Autophagy 2008; 4: 810-4; PMID: 18604159; http://dx.doi.org/10.4161/ auto.6486
8. Dickens MP, Fitzgerald R, Fischer PM. Small-molecule inhibitors of MDM2 as new anticancer therapeutics. Semin Cancer Biol 2010; 20: 10-8; PMID: 19897042; http://dx.doi.org/10.1016/j.semcancer.2009.10.003
9. Vu BT, Vassilev L. Small-molecule inhibitors of the p53-MDM2 interaction. Curr Top Microbiol Immunol 2011; 348: 151-72; PMID: 21046355
10. Vassilev LT, Vu BT,Graves B, Carvajal D, Podlaski F, Filipovic Z, Kong N,Kammlott U, Lukacs C,Klein C, et al. In vivo activation of the p53 pathway by smallmolecule antagonists of MDM2. Science 2004; 303: 844-8; PMID: 14704432; http://dx.doi.org/10.1126/science.1092472
11. Stuhmer T, Chatterjee M, Hildebrandt M, Herrmann P, Gollasch H, Gerecke C, Theurich S, Cigliano L, Manz RA, Daniel PT, et al. Nongenotoxic activation of the p53 pathway as a therapeutic strategy for multiple myeloma. Blood 2005; 106: 3609-17; PMID: 16081689; http://dx.doi.org/10.1182/blood-2005-04-1489
12. Sarek G, Kurki S, Enback J, Iotzova G, Haas J, Laakkonen P, Laiho M, Ojala PM. Reactivation of the p53 pathway as a treatment modality for KSHV-induced lymphomas. J Clin Invest 2007; 117: 1019-28; PMID: 17364023; http://dx.doi.org/10.1172/ JCI30945
13. Secchiero P, Barbarotto E, Tiribelli M, Zerbinati C, di Iasio MG, Gonelli A, Cavazzini F, Campioni D, Fanin R, Cuneo A, et al. Functional integrity of the p53- mediated apoptotic pathway induced by the nongenotoxic agent nutlin-3 in B-cell chronic lymphocytic leukemia (B-CLL). Blood 2006; 107: 4122-9; PMID: 16439677; http://dx.doi.org/10.1182/blood-2005-11-4465
14. Vassilev LT. MDM2 inhibitors for cancer therapy. Trends Mol Med 2007; 13: 23-31; PMID: 17126603; http://dx.doi.org/10.1016/j.molmed.2006.11.002
15. Khoo KH, Verma CS, Lane DP. Drugging the p53 pathway: understanding the route to clinical efficacy. Nat Rev Drug Discov 2014; 13: 217-36; PMID: 24577402; http://dx.doi.org/10.1038/nrd4288
16. Renouf B, Hollville E, Pujals A, Tetaud C, Garibal J, Wiels J. Activation of p53 by MDM2 antagonists has differential apoptotic effects on Epstein-Barr virus (EBV)-positive and EBV-negative Burkitt’s lymphoma cells. Leukemia 2009; 23: 1557-63; PMID: 19421231; http://dx.doi.org/10.1038/leu.2009.92
17. Pujals A, Renouf B, Robert A, Chelouah S, Hollville E, Wiels J. Treatment with a BH3 mimetic overcomes the resistance of latency III EBV (C) cells to p53-mediated apoptosis. Cell Death Dis 2011; 2: e184; PMID: 21796156; http://dx.doi.org/10.1038/ cddis.2011.67
18. Cavignac Y, Esclatine A. Herpesviruses and autophagy: catch me if you can! Viruses 2010; 2: 314-33; PMID: 21994613; http://dx.doi.org/10.3390/v2010314
19. 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
20. Huen DS, Henderson SA, Croom-Carter D, Rowe M. The Epstein-Barr virus latent membrane protein-1 (LMP1) mediates activation of NF-kappa B and cell surface phenotype via two effector regions in its carboxy- terminal cytoplasmic domain. Oncogene 1995; 10: 549-60; PMID: 7845680
21. Laherty CD, Hu HM, Opipari AW, Wang F, Dixit VM. The Epstein-Barr virus LMP1 gene product induces A20 zinc finger protein expression by activating nuclear factor kappa B. J Biol Chem 1992; 267: 24157-60; PMID: 1332946
22. Nivon M, Richet E, Codogno P, Arrigo AP, Kretz-Remy C. Autophagy activation by NFkappaB is essential for cell survival after heat shock. Autophagy 2009; 5: 766-83; PMID: 19502777; http://dx.doi.org/10.4161/auto.8788
23. Ryu HJ, Kim JE, Yeo SI, Kang TC. p65/RelA-Ser529 NF-kappaB subunit phosphorylation induces autophagic astroglial death (Clasmatodendrosis) following status epilepticus. Cell Mol Neurobiol 2011; 31: 1071-8; PMID: 21598036; http://dx.doi.org/10.1007/s10571-011-9706-1
24. Copetti T, Demarchi F, Schneider C. p65/RelA binds and activates the beclin 1 promoter. Autophagy 2009; 5: 858-9; PMID: 19458474; http://dx.doi.org/10.4161/ auto.8822
25. Crighton D, Wilkinson S, O’Prey J, Syed N, Smith P, Harrison PR, Gasco M, Garrone O, Crook T, Ryan KM. DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell 2006; 126: 121-34; PMID: 16839881; http://dx.doi.org/10.1016/j. cell.2006.05.034
26. Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell 2010; 140: 313-26; PMID: 20144757; http://dx.doi.org/10.1016/j. cell.2010.01.028
27. Isotani S, Hara K, Tokunaga C, Inoue H, Avruch J, Yonezawa K. Immunopurified mammalian target of rapamycin phosphorylates and activates p70 S6 kinase alpha in vitro. J Biol Chem 1999; 274: 34493-8; PMID: 10567431; http://dx.doi.org/10.1074/ jbc.274.48.34493
28. Glaumann H, Ahlberg J. Comparison of different autophagic vacuoles with regard to ultrastructure, enzymatic composition, and degradation capacity-formation of crinosomes. Exp Mol Pathol 1987; 47: 346-62; PMID: 3678466; http://dx.doi.org/10.1016/0014-4800(87)90018-9
29. Rosenfeldt MT, Nixon C, Liu E, Mah LY, Ryan KM. Analysis of macroautophagy by immunohistochemistry. Autophagy 2012; 8: 963-9; PMID: 22562096; http://dx.doi.org/10.4161/auto.20186
30. Lee DY, Sugden B. The latent membrane protein 1 oncogene modifies B-cell physiology by regulating autophagy. Oncogene 2008; 27: 2833-42; PMID: 18037963; http://dx.doi.org/10.1038/sj. onc.1210946
31. Pratt ZL, Zhang J, Sugden B. The latent membrane protein 1 (LMP1) oncogene of Epstein-Barr virus can simultaneously induce and inhibit apoptosis in B-cells. J Virol 2012; 86: 4380-93; PMID: 22318153
32. Sommermann TG, O’Neill K, Plas DR, Cahir-McFarland E. IKKbeta and NF-kappaB transcription govern lymphoma cell survival through AKT-induced plasma membrane trafficking of GLUT1. Cancer Res 2011; 71: 7291-300; PMID: 21987722; http://dx.doi.org/10.1158/0008-5472.CAN-11-1715
33. Jackson WT. Viruses and the autophagy pathway. Virology 2015; 479-480: 450-6; PMID: 25858140; http://dx.doi.org/10.1016/j.virol.2015.03.042
34. Paludan C, Schmid D, Landthaler M, Vockerodt M, Kube D, Tuschl T, Munz C. Endogenous MHC class II processing of a viral nuclear antigen after autophagy. Science 2005; 307: 593-6; PMID: 15591165; http://dx. doi.org/10.1126/science.1104904
35. Leung CS, Haigh TA, Mackay LK, Rickinson AB, Taylor GS. Nuclear location of an endogenously expressed antigen, EBNA1, restricts access to macroautophagy and the range of CD4 epitope display. Proc Natl Acad Sci U S A 2010; 107: 2165-70; PMID: 20133861; http://dx.doi.org/10.1073/pnas.0909448107
36. Kirkegaard K. Subversion of the cellular autophagy pathway by viruses. Curr Top Microbiol Immunol 2009; 335: 323-33; PMID: 19802573
37. Klein G, Klein E, Kashuba E. Interaction of Epstein-Barr virus (EBV) with human B-lymphocytes. Biochem Biophys Res Commun 2010; 396: 67-73; PMID: 20494113; http://dx.doi.org/10.1016/j. bbrc.2010.02.146
38. Wei Y, Sinha S, Levine B. Dual role of JNK1-mediated phosphorylation of Bcl-2 in autophagy and apoptosis regulation. Autophagy 2008; 4: 949-51; PMID: 18769111; http://dx.doi.org/10.4161/ auto.6788
39. Chaumorcel M, Lussignol M, Mouna L, Cavignac Y, Fahie K, Cotte-Laffitte J, Geballe A, Brune W, Beau I, Codogno P, et al. The human cytomegalovirus protein TRS1 inhibits autophagy via its interaction with Beclin 1. J Virol 2012; 86: 2571-84; PMID: 22205736; http:// dx.doi.org/10.1128/JVI.05746-11
40. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005; 122: 927-39; PMID: 16179260; http://dx.doi.org/10.1016/j.cell.2005.07.002
41. Feng Z, Zhang H, Levine AJ, Jin S. The coordinate regulation of the p53 and mTOR pathways in cells. Proc Natl Acad Sci U S A 2005; 102: 8204-9; PMID: 15928081; http://dx.doi.org/10.1073/ pnas.0502857102
42. Morselli E, Shen S, Ruckenstuhl C, Bauer MA, Marino G, Galluzzi L, Criollo A, Michaud M, Maiuri MC, Chano T, et al. p53 inhibits autophagy by interacting with the human ortholog of yeast Atg17, RB1CC1/ FIP200. Cell Cycle 2011; 10: 2763-9; PMID: 21775823; http://dx.doi.org/10.4161/ cc.10.16.16868
43. Eskelinen EL. The dual role of autophagy in cancer. Curr Opin Pharmacol 2011; 11: 294-300; PMID: 21498118; http://dx.doi.org/10.1016/j. coph.2011.03.009
44. Rosenfeldt MT, Ryan KM. The multiple roles of autophagy in cancer. Carcinogenesis 2011; 32: 955-63; PMID: 21317301; http://dx.doi.org/10.1093/carcin/ bgr031
45. Guo XL, Li D, Hu F, Song JR, Zhang SS, Deng WJ, Sun K, Zhao QD, Xie XQ, Song YJ, et al. Targeting autophagy potentiates chemotherapy-induced apoptosis and proliferation inhibition in hepatocarcinoma cells. Cancer Lett 2012; 320: 171-9.
46. Sasaki K, Tsuno NH, Sunami E, Tsurita G, Kawai K, Okaji Y, Nishikawa T, Shuno Y, Hongo K, Hiyoshi M, et al. Chloroquine potentiates the anti-cancer effect of 5-fluorouracil on colon cancer cells. BMC Cancer 2010; 10: 370; PMID: 20630104; http://dx.doi.org/10.1186/1471-2407-10-370
47. Yang ZJ, Chee CE, Huang S, Sinicrope FA. The role of autophagy in cancer: therapeutic implications. Mol Cancer Ther 2011; 10: 1533-41; PMID: 21878654; http://dx.doi.org/10.1158/1535-7163.MCT-11-0047
48. Maes H, Rubio N, Garg AD, Agostinis P. Autophagy: shaping the tumor microenvironment and therapeutic response. Trends Mol Med 2013; 19: 428-46; PMID: 23714574; http://dx.doi.org/10.1016/j. molmed.2013.04.005
49. Amaravadi RK, Yu D, Lum JJ, Bui T, Christophorou MA, Evan GI, Thomas-Tikhonenko A, Thompson CB. Autophagy inhibition enhances therapy-induced apoptosis in a Myc-induced model of lymphoma. J Clin Invest 2007; 117: 326-36; PMID: 17235397; http://dx.doi.org/10.1172/JCI28833
50. Maclean KH, Dorsey FC, Cleveland JL, Kastan MB. Targeting lysosomal degradation induces p53-dependent cell death and prevents cancer in mouse models of lymphomagenesis. J Clin Invest 2008; 118: 79-88; PMID: 18097482; http://dx.doi.org/10.1172/ JCI33700
51. Floettmann JE, Ward K, Rickinson AB, Rowe M. Cytostatic effect of Epstein-Barr virus latent membrane protein-1 analyzed using tetracycline-regulated expression in B cell lines. Virology 1996; 223: 29-40; PMID: 8806537; http://dx.doi.org/10.1006/ viro.1996.0452