E1a promotes c-Myc-dependent replicative stress: Implications in glioblastoma radiosensitization

Cell Cycle

Volumn 13, Issue 1, 2014, Pages 52-61

  Valero, María Llanos ^a   Cimas, Francisco Jose ^a   Arias, Laura ^a   Melgar Rojas, Pedro ^a   García, Elena ^a   Callejas Valera, Juan Luis ^a   García Cano, Jesús ^a   Serrano Oviedo, Leticia ^a   De La Cruz Morcillo, Miguel Ángel ^a   Sánchez Pérez, Isabel ^b   Sánchez Prieto, Ricardo ^a  

^a University of Castilla La Mancha   (Spain)

^b CSIC   (Spain)

Author keywords

C Myc; Chk1; E1a; Glioblastoma; Radiosensitivity; Replicative stress

Indexed keywords

CHECKPOINT KINASE 1; E1A PROTEIN; HISTONE H2AX; MYC PROTEIN;

APOPTOSIS; ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA DAMAGE; GENE OVEREXPRESSION; GENE REPLICATION; GLIOBLASTOMA; HUMAN; HUMAN CELL; IONIZING RADIATION; LENTIVIRINAE; LENTIVIRUS INFECTION; ONCOGENE C MYC; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RADIOSENSITIVITY; RADIOSENSITIZATION; STRESS; UPREGULATION;

C-MYC; CHK1; E1A; GLIOBLASTOMA; RADIOSENSITIVITY; REPLICATIVE STRESS;

ADENOVIRUS E1A PROTEINS; CELL LINE, TUMOR; DNA REPLICATION; GLIOBLASTOMA; HUMANS; LENTIVIRUS; PROTO-ONCOGENE PROTEINS C-MYC; RADIATION TOLERANCE; STRESS, PHYSIOLOGICAL;

EID: 84892603183     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.26754     Document Type: Article

References (57)

1. Frisch SM, Mymryk JS. Adenovirus-5 E1A: paradox and paradigm. Nat Rev Mol Cell Biol 2002; 3:441-52; PMID:12042766; http://dx.doi.org/10.1038/nrm827 (Pubitemid 34685701)
2. Zerler B, Moran B, Maruyama K, Moomaw J, Grodzicker T, Ruley HE. Adenovirus E1A coding sequences that enable ras and pmt oncogenes to transform cultured primary cells. Mol Cell Biol 1986; 6: 887-99; PMID:3022137 (Pubitemid 16135953)
3. Ragozzino MM, Kuo A, DeGregori J, Kohl N, Ruley HE. Mechanisms of oncogene cooperation: activation and inactivation of a growth antagonist. Environ Health Perspect 1991; 93: 97-103; PMID:1837777; http://dx.doi.org/10. 1289/ehp.919397
4. Ferbeyre G, de Stanchina E, Querido E, Baptiste N, Prives C, Lowe SW. PML is induced by oncogenic ras and promotes premature senescence. Genes Dev 2000; 14: 2015-27; PMID:10950866 (Pubitemid 30637352)
5. Callejas-Valera JL, Guinea-Viniegra J, Ramírez-Castillejo C, Recio JA, Galan-Moya E, Martinez N, Rojas JM, Ramóny Cajal S, Sánchez-Prieto R. E1a gene expression blocks the ERK1/2 signaling pathway by promoting nuclear localization and MKP up-regulation: implication in v-H-Ras-induced senescence. J Biol Chem 2008; 283: 13450-8; PMID:18316372; http://dx.doi.org/10.1074/jbc.M709230200
6. Lowe SW, Ruley HE. Stabilization of the p53 tumor suppressor is induced by adenovirus 5 E1A and accompanies apoptosis. Genes Dev 1993; 7:535-45; PMID:8384579; http://dx.doi.org/10.1101/gad.7.4.535 (Pubitemid 23125255)
7. Fuchs M, Gerber J, Drapkin R, Sif S, Ikura T, Ogryzko V, Lane WS, Nakatani Y, Livingston DM. The p400 complex is an essential E1A transformation target. Cell 2001; 106: 297-307; PMID:11509179; http://dx.doi.org/10.1016/S0092- 8674(01)00450-0 (Pubitemid 32772614)
8. Chan HM, Narita M, Lowe SW, Livingston DM. The p400 E1A-associated protein is a novel component of the p53 - > p21 senescence pathway. Genes Dev 2005; 19: 196-201; PMID:15655109; http://dx.doi.org/10.1101/gad.1280205 (Pubitemid 40111114)
9. Flinterman M, Gäken J, Farzaneh F, Tavassoli M. E1A-mediated suppression of EGFR expression and induction of apoptosis in head and neck squamous carcinoma cell lines. Oncogene 2003; 22:1965-77; PMID:12673202; http://dx.doi.org/10.1038/sj.onc.1206190 (Pubitemid 36523634)
10. Yu D, Suen TC, Yan DH, Chang LS, Hung MC. Transcriptional repression of the neu protooncogene by the adenovirus 5 E1A gene products. Proc Natl Acad Sci U S A 1990; 87: 4499-503; PMID:1972274; http://dx.doi.org/10.1073/pnas.87.12. 4499 (Pubitemid 20204129)
11. Su JL, Chen PB, Chen YH, Chen SC, Chang YW, Jan YH, Cheng X, Hsiao M, Hung MC. Downregulation of microRNA miR-520h by E1A contributes to anticancer activity. Cancer Res 2010; 70: 5096-108; PMID:20501832; http://dx.doi.org/10. 1158/0008-5472.CAN-09-4148
12. Zhou Z, Zhou RR, Guan H, Bucana CD, Kleinerman ES. E1A gene therapy inhibits angiogenesis in a Ewing's sarcoma animal model. Mol Cancer Ther 2003; 2: 1313-9; PMID:14707272
13. Liao Y, Yu D, Hung MC. Novel approaches for chemosensitization of breast cancer cells: the E1A story. Adv Exp Med Biol 2007; 608: 144-69; PMID:17993239; http://dx.doi.org/10.1007/978-0-387-74039-3-11
14. Sánchez-Prieto R, Quintanilla M, Cano A, Leonart ML, Martin P, Anaya A, Ramóny Cajal S. Carcinoma cell lines become sensitive to DNA-damaging agents by the expression of the adenovirus E1A gene. Oncogene 1996; 13: 1083-92; PMID:8806698
15. Yamaguchi H, Chen CT, Chou CK, Pal A, Bornmann W, Hortobagyi GN, Hung MC. Adenovirus 5 E1A enhances histone deacetylase inhibitors-induced apoptosis through Egr-1-mediated Bim upregulation. Oncogene 2010; 29: 5619-29; PMID:20676141; http://dx.doi.org/10.1038/onc.2010.295
16. Stiewe T, Parssanedjad K, Esche H, Opalka B, Pützer BM. E1A overcomes the apoptosis block in BCRABL+ leukemia cells and renders cells susceptible to induction of apoptosis by chemotherapeutic agents. Cancer Res 2000; 60: 3957-64; PMID:10919674 (Pubitemid 32204592)
17. Marchetti E, Romero J, Sanchez R, Vargas J, Dominguez C, Lacal J, Cajal S. Oncogenes and cellular-sensitivity to radiotherapy -a study on murine keratinocytes transformed by v-h-ras, v-myc, v-Neu, adenovirus e1a and mutant p53. Int J Oncol 1994; 5: 611-8; PMID:21559621 (Pubitemid 24269887)
18. Shao R, Tsai EM, Wei K, von Lindern R, Chen YH, Makino K, Hung MC. E1A inhibition of radiationinduced NF-κB activity through suppression of IKK activity and IkappaB degradation, independent of Akt activation. Cancer Res 2001; 61: 7413-6; PMID:11606372 (Pubitemid 32995026)
19. Su JL, Cheng X, Yamaguchi H, Chang YW, Hou CF, Lee DF, Ko HW, Hua KT, Wang YN, Hsiao M, et al. FOXO3a-Dependent Mechanism of E1A-Induced Chemosensitization. Cancer Res 2011; 71: 6878-87; PMID:21911455; http://dx.doi.org/10.1158/0008-5472.CAN-11-0295
20. Samuelson AV, Lowe SW. Selective induction of p53 and chemosensitivity in RB-deficient cells by E1A mutants unable to bind the RB-related proteins. Proc Natl Acad Sci U S A 1997; 94:12094-9; PMID:9342368; http://dx.doi.org/10.1073/ pnas.94.22.12094 (Pubitemid 27467848)
21. Samuelson AV, Narita M, Chan HM, Jin J, de Stanchina E, McCurrach ME, Narita M, Fuchs M, Livingston DM, Lowe SW. p400 is required for E1A to promote apoptosis. J Biol Chem 2005; 280:21915-23; PMID:15741165; http://dx.doi.org/10. 1074/jbc.M414564200 (Pubitemid 40827843)
22. Van Meir EG, Hadjipanayis CG, Norden AD, Shu HK, Wen PY, Olson JJ. Exciting new advances in neuro-oncology: the avenue to a cure for malignant glioma. CA Cancer J Clin 2010; 60: 166-93; PMID:20445000; http://dx.doi.org/10. 3322/caac.20069
23. Noda SE, El-Jawahri A, Patel D, Lautenschlaeger T, Siedow M, Chakravarti A. Molecular advances of brain tumors in radiation oncology. Semin Radiat Oncol 2009; 19: 171-8; PMID:19464632; http://dx.doi.org/10.1016/j.semradonc.2009.02. 005
24. Shen LF, Chen J, Zeng S, Zhou RR, Zhu H, Zhong MZ, Yao RJ, Shen H. The superparamagnetic nanoparticles carrying the E1A gene enhance the radiosensitivity of human cervical carcinoma in nude mice. Mol Cancer Ther 2010; 9: 2123-30; PMID:20587666; http://dx.doi.org/10.1158/1535-7163.MCT-09-1150
25. Pawlik TM, Keyomarsi K. Role of cell cycle in mediating sensitivity to radiotherapy. Int J Radiat Oncol Biol Phys 2004; 59: 928-42; PMID:15234026; http://dx.doi.org/10.1016/j.ijrobp.2004.03.005 (Pubitemid 38834285)
26. Xu B, Kim ST, Lim DS, Kastan MB. Two molecularly distinct G(2)/M checkpoints are induced by ionizing irradiation. Mol Cell Biol 2002; 22:1049-59; PMID:11809797; http://dx.doi.org/10.1128/MCB.22.4.1049-1059.2002 (Pubitemid 34094842)
27. Yarden RI, Pardo-Reoyo S, Sgagias M, Cowan KH, Brody LC. BRCA1 regulates the G2/M checkpoint by activating Chk1 kinase upon DNA damage. Nat Genet 2002; 30: 285-9; PMID:11836499; http://dx.doi.org/10.1038/ng837
28. Kaneko YS, Watanabe N, Morisaki H, Akita H, Fujimoto A, Tominaga K, Terasawa M, Tachibana A, Ikeda K, Nakanishi M. Cell-cycle-dependent and ATM-independent expression of human Chk1 kinase. Oncogene 1999; 18: 3673-81; PMID:10391675; http://dx.doi.org/10.1038/sj.onc.1202706 (Pubitemid 29338500)
29. Höglund A, Nilsson LM, Muralidharan SV, Hasvold LA, Merta P, Rudelius M, Nikolova V, Keller U, Nilsson JA. Therapeutic implications for the induced levels of Chk1 in Myc-expressing cancer cells. Clin Cancer Res 2011; 17: 7067-79; PMID:21933891; http://dx.doi.org/10.1158/1078-0432.CCR-11-1198
30. Chakraborty AA, Tansey WP. Adenoviral E1A function through Myc. Cancer Res 2009; 69: 6-9; PMID:19117980; http://dx.doi.org/10.1158/0008-5472.CAN-08- 3026
31. Tworkowski KA, Chakraborty AA, Samuelson AV, Seger YR, Narita M, Hannon GJ, Lowe SW, Tansey WP. Adenovirus E1A targets p400 to induce the cellular oncoprotein Myc. Proc Natl Acad Sci U S A 2008; 105: 6103-8; PMID:18413597; http://dx.doi.org/10.1073/pnas.0802095105 (Pubitemid 351758406)
32. Murga M, Campaner S, Lopez-Contreras AJ, Toledo LI, Soria R, Montaña MF, D'Artista L, Schleker T, Guerra C, Garcia E, et al. Exploiting oncogeneinduced replicative stress for the selective killing of Myc-driven tumors. Nat Struct Mol Biol 2011; 18: 1331-5; PMID:22120667; http://dx.doi.org/10.1038/nsmb.2189
33. Sankar N, Kadeppagari RK, Thimmapaya B. c-Mycinduced aberrant DNA synthesis and activation of DNA damage response in p300 knockdown cells. J Biol Chem 2009; 284: 15193-205; PMID:19332536; http://dx.doi.org/10.1074/jbc. M900776200
34. Murga M, Bunting S, Montaña MF, Soria R, Mulero F, Cañamero M, Lee Y, McKinnon PJ, Nussenzweig A, Fernandez-Capetillo O. A mouse model of ATR-Seckel shows embryonic replicative stress and accelerated aging. Nat Genet 2009; 41: 891-8; PMID:19620979; http://dx.doi.org/10.1038/ng.420
35. Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M, Bonner WM. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol 2000; 10:886-95; PMID:10959836; http://dx.doi.org/10.1016/S0960-9822(00)00610-2 (Pubitemid 30647617)
36. Gutiérrez-González A, Belda-Iniesta C, Bargiela- Iparraguirre J, Dominguez G, García Alfonso P, Perona R, Sanchez-Perez I. Targeting Chk2 improves gastric cancer chemotherapy by impairing DNA damage repair. Apoptosis 2013; 18: 347-60; PMID:23271172
37. Hong S, Paulson QX, Johnson DG. E2F1 and E2F3 activate ATM through distinct mechanisms to promote E1A-induced apoptosis. Cell Cycle 2008; 7:391-400; PMID:18235226; http://dx.doi.org/10.4161/cc.7.3.5286 (Pubitemid 351366503)
38. Brooks K, Oakes V, Edwards B, Ranall M, Leo P, Pavey S, Pinder A, Beamish H, Mukhopadhyay P, Lambie D, et al. A potent Chk1 inhibitor is selectively cytotoxic in melanomas with high levels of replicative stress. Oncogene 2013; 32: 788-96; PMID:22391562; http://dx.doi.org/10.1038/onc.2012.72
39. Tse AN, Rendahl KG, Sheikh T, Cheema H, Aardalen K, Embry M, Ma S, Moler EJ, Ni ZJ, Lopes de Menezes DE, et al. CHIR-124, a novel potent inhibitor of Chk1, potentiates the cytotoxicity of topoisomerase I poisons in vitro and in vivo. Clin Cancer Res 2007; 13: 591-602; PMID:17255282; http://dx.doi.org/10. 1158/1078-0432.CCR-06-1424 (Pubitemid 46225366)
40. Hung MC, Hortobagyi GN, Ueno NT. Development of clinical trial of E1A gene therapy targeting HER-2/neu-overexpressing breast and ovarian cancer. Adv Exp Med Biol 2000; 465: 171-80; PMID:10810625; http://dx.doi.org/10.1007/0-306- 46817-4-16 (Pubitemid 32193333)
41. Hung MC, Yan DH, Zhang S. E1A-Mediated Gene Therapy. Methods Mol Med 2001; 39: 775-82; PMID:21340839
42. Touchefeu Y, Vassaux G, Harrington KJ. Oncolytic viruses in radiation oncology. Radiother Oncol 2011; 99: 262-70; PMID:21704402; http://dx.doi.org/10. 1016/j.radonc.2011.05.078
43. Heise C, Sampson-Johannes A, Williams A, McCormick F, Von Hoff DD, Kirn DH. ONYX-015, an E1B gene-attenuated adenovirus, causes tumorspecific cytolysis and antitumoral efficacy that can be augmented by standard chemotherapeutic agents. Nat Med 1997; 3: 639-45; PMID:9176490; http://dx.doi.org/10.1038/nm0697- 639 (Pubitemid 27264973)
44. Busse PM, Bose SK, Jones RW, Tolmach LJ. The action of caffeine on X-irradiated HeLa cells. III. Enhancement of X-ray-induced killing during G2 arrest. Radiat Res 1978; 76: 292-307; PMID:156382; http://dx.doi.org/10.2307/ 3574780 (Pubitemid 9037669)
45. Ganem NJ, Pellman D. Linking abnormal mitosis to the acquisition of DNA damage. J Cell Biol 2012; 199: 871-81; PMID:23229895; http://dx.doi.org/10.1083/ jcb.201210040
46. Zhao H, Piwnica-Worms H. ATR-mediated checkpoint pathways regulate phosphorylation and activation of human Chk1. Mol Cell Biol 2001; 21: 4129-39; PMID:11390642; http://dx.doi.org/10.1128/MCB.21.13.4129-4139.2001 (Pubitemid 32565295)
47. Liu Q, Guntuku S, Cui XS, Matsuoka S, Cortez D, Tamai K, Luo G, Carattini-Rivera S, DeMayo F, Bradley A, et al. Chk1 is an essential kinase that is regulated by Atr and required for the G(2)/M DNA damage checkpoint. Genes Dev 2000; 14: 1448-59; PMID:10859164 (Pubitemid 30421838)
48. Baluchamy S, Sankar N, Navaraj A, Moran E, Thimmapaya B. Relationship between E1A binding to cellular proteins, c-myc activation and S-phase induction. Oncogene 2007; 26: 781-7; PMID:16862175; http://dx.doi.org/10.1038/ sj.onc.1209825 (Pubitemid 46204257)
49. Kadeppagari RK, Sankar N, Thimmapaya B. Adenovirus transforming protein E1A induces c-Myc in quiescent cells by a novel mechanism. J Virol 2009; 83: 4810-22; PMID:19279113; http://dx.doi.org/10.1128/JVI.02145-08
50. Connell CM, Shibata A, Tookman LA, Archibald KM, Flak MB, Pirlo KJ, Lockley M, Wheatley SP, McNeish IA. Genomic DNA damage and ATRChk1 signaling determine oncolytic adenoviral efficacy in human ovarian cancer cells. J Clin Invest 2011; 121: 1283-97; PMID:21383502; http://dx.doi.org/10.1172/JCI43976
51. Zhangand Y, Hunter T. Roles of Chk1 in cell biology and cancer therapy. Int J Cancer 2013; Ahead of Print
52. Wang WJ, Wu SP, Liu JB, Shi YS, Huang X, Zhang QB, Yao KT. MYC regulation of CHK1 and CHK2 promotes radioresistance in a stem cell-like population of nasopharyngeal carcinoma cells. Cancer Res 2013; 73: 1219-31; PMID:23269272; http://dx.doi.org/10.1158/0008-5472.CAN-12-1408
53. Gagou ME, Zuazua-Villar P, Meuth M. Enhanced H2AX phosphorylation, DNA replication fork arrest, and cell death in the absence of Chk1. Mol Biol Cell 2010; 21: 739-52; PMID:20053681; http://dx.doi.org/10.1091/mbc.E09-07-0618
54. López-Contreras AJ, Gutierrez-Martinez P, Specks J, Rodrigo-Perez S, Fernandez-Capetillo O. An extra allele of Chk1 limits oncogene-induced replicative stress and promotes transformation. J Exp Med 2012; 209: 455-61; PMID:22370720; http://dx.doi.org/10.1084/jem.20112147
55. Unsal-Kaçmaz K, Chastain PD, Qu PP, Minoo P, Cordeiro-Stone M, Sancar A, Kaufmann WK. The human Tim/Tipin complex coordinates an Intra-S checkpoint response to UV that slows replication fork displacement. Mol Cell Biol 2007; 27:3131-42; PMID:17296725; http://dx.doi.org/10.1128/MCB.02190-06 (Pubitemid 46581324)
56. Galan-Moya EM, de la Cruz-Morcillo MA, Llanos Valero M, Callejas-Valera JL, Melgar-Rojas P, Hernadez Losa J, Salcedo M, Fernández-Aramburo A, Ramon y Cajal S, Sánchez-Prieto R. Balance between MKK6 and MKK3 mediates p38 MAPK associated resistance to cisplatin in NSCLC. PLoS One 2011; 6:e28406; PMID:22164285; http://dx.doi.org/10.1371/journal.pone.0028406
57. de la Cruz-Morcillo MA, Valero ML, Callejas-Valera JL, Arias-González L, Melgar-Rojas P, Galán-Moya EM, García-Gil E, García-Cano J, Sánchez-Prieto R. P38MAPK is a major determinant of the balance between apoptosis and autophagy triggered by 5-fluorouracil: implication in resistance. Oncogene 2012; 31: 1073-85; PMID:21841826; http://dx.doi.org/10.1038/onc.2011.321