Molecular Basis for Viral Selective Replication in Cancer Cells: Activation of CDK2 by Adenovirus-Induced Cyclin E

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Cheng, Pei Hsin ^a   Rao, Xiao Mei ^a   McMasters, Kelly M ^a   Zhou, Heshan Sam ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; CYCLIN DEPENDENT KINASE 2; CYCLIN E; E1B PROTEIN; RETINOBLASTOMA PROTEIN; ROSCOVITINE; SMALL INTERFERING RNA;

ADENOVIRUS; ADENOVIRUS INFECTION; ARTICLE; CANCER CELL; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME REPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; VIRUS REPLICATION;

ADENOVIRIDAE; CELL LINE, TUMOR; CYCLIN E; CYCLIN-DEPENDENT KINASE 2; FIBROBLASTS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; ONCOGENE PROTEINS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PURINES; RETINOBLASTOMA PROTEIN; RNA, SMALL INTERFERING; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84874228083     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0057340     Document Type: Article

References (93)

1. Ben-Israel H, Kleinberger T, (2002) Adenovirus and cell cycle control. Front Biosci 7: d1369-1395.
2. Shenk T (2001) Adenoviridae: the viruses and their replication. In: Knipe DM, Howley PM, editors. Fields Virology. 4 ed. Philadelphia, PA: Lippincott Williams & Wilkins. pp. 2265-2300.
3. Avvakumov N, Sahbegovic M, Zhang Z, Shuen M, Mymryk JS, (2002) Analysis of DNA binding by the adenovirus type 5 E1A oncoprotein. J Gen Virol 83: 517-524.
4. Dyson N, Harlow E, (1992) Adenovirus E1A targets key regulators of cell proliferation. Cancer Surv 12: 161-195.
5. Ludlow JW, Skuse GR, (1995) Viral oncoprotein binding to pRB, p107, p130, and p300. Virus Res 35: 113-121.
6. Whyte P, Buchkovich KJ, Horowitz JM, Friend SH, Raybuck M, et al. (1988) Association between an oncogene and an anti-oncogene: the adenovirus E1A proteins bind to the retinoblastoma gene product. Nature 334: 124-129.
7. Liu Y, Costantino ME, Montoya-Durango D, Higashi Y, Darling DS, et al. (2007) The zinc finger transcription factor ZFHX1A is linked to cell proliferation by Rb-E2F1. Biochem J 408: 79-85.
8. Rowland BD, Denissov SG, Douma S, Stunnenberg HG, Bernards R, et al. (2002) E2F transcriptional repressor complexes are critical downstream targets of p19(ARF)/p53-induced proliferative arrest. Cancer Cell 2: 55-65.
9. Zhang HS, Postigo AA, Dean DC, (1999) Active transcriptional repression by the Rb-E2F complex mediates G1 arrest triggered by p16INK4a, TGFbeta, and contact inhibition. Cell 97: 53-61.
10. Pelka P, Miller MS, Cecchini M, Yousef AF, Bowdish DM, et al. (2011) Adenovirus E1A directly targets the E2F/DP-1 complex. J Virol 85: 8841-8851.
11. Debbas M, White E, (1993) Wild-type p53 mediates apoptosis by E1A, which is inhibited by E1B. Genes Dev 7: 546-554.
12. Braithwaite A, Nelson C, Skulimowski A, McGovern J, Pigott D, et al. (1990) Transactivation of the p53 oncogene by E1a gene products. Virology 177: 595-605.
13. Pomerantz J, Schreiber-Agus N, Liegeois NJ, Silverman A, Alland L, et al. (1998) The Ink4a tumor suppressor gene product, p19Arf, interacts with MDM2 and neutralizes MDM2's inhibition of p53. Cell 92: 713-723.
14. Lowe SW, Ruley HE, (1993) Stabilization of the p53 tumor suppressor is induced by adenovirus 5 E1A and accompanies apoptosis. Genes Dev 7: 535-545.
15. Querido E, Marcellus RC, Lai A, Charbonneau R, Teodoro JG, et al. (1997) Regulation of p53 levels by the E1B 55-kilodalton protein and E4orf6 in adenovirus-infected cells. J Virol 71: 3788-3798.
16. Kao CC, Yew PR, Berk AJ, (1990) Domains required for in vitro association between the cellular p53 and the adenovirus 2 E1B 55K proteins. Virology 179: 806-814.
17. Martin ME, Berk AJ, (1998) Adenovirus E1B 55K represses p53 activation in vitro. J Virol 72: 3146-3154.
18. Yew PR, Berk AJ, (1992) Inhibition of p53 transactivation required for transformation by adenovirus early 1B protein. Nature 357: 82-85.
19. Nevels M, Rubenwolf S, Spruss T, Wolf H, Dobner T, (1997) The adenovirus E4orf6 protein can promote E1A/E1B-induced focus formation by interfering with p53 tumor suppressor function. Proc Natl Acad Sci U S A 94: 1206-1211.
20. Querido E, Blanchette P, Yan Q, Kamura T, Morrison M, et al. (2001) Degradation of p53 by adenovirus E4orf6 and E1B55K proteins occurs via a novel mechanism involving a Cullin-containing complex. Genes Dev 15: 3104-3117.
21. Wienzek S, Roth J, Dobbelstein M, (2000) E1B 55-kilodalton oncoproteins of adenovirus types 5 and 12 inactivate and relocalize p53, but not p51 or p73, and cooperate with E4orf6 proteins to destabilize p53. J Virol 74: 193-202.
22. Pennella MA, Liu Y, Woo JL, Kim CA, Berk AJ, (2010) Adenovirus E1B 55-kilodalton protein is a p53-SUMO1 E3 ligase that represses p53 and stimulates its nuclear export through interactions with promyelocytic leukemia nuclear bodies. J Virol 84: 12210-12225.
23. Barker DD, Berk AJ, (1987) Adenovirus proteins from both E1B reading frames are required for transformation of rodent cells by viral infection and DNA transfection. Virology 156: 107-121.
24. Bischoff JR, Kirn DH, Williams A, Heise C, Horn S, et al. (1996) An adenovirus mutant that replicates selectively in p53-deficient human tumor cells. Science 274: 373-376.
25. Rogulski KR, Freytag SO, Zhang K, Gilbert JD, Paielli DL, et al. (2000) In vivo antitumor activity of ONYX-015 is influenced by p53 status and is augmented by radiotherapy. Cancer Res 60: 1193-1196.
26. Yu W, Fang H, (2007) Clinical trials with oncolytic adenovirus in China. Curr Cancer Drug Targets 7: 141-148.
27. Dix BR, Edwards SJ, Braithwaite AW, (2001) Does the antitumor adenovirus ONYX-015/dl1520 selectively target cells defective in the p53 pathway? J Virol 75: 5443-5447.
28. Goodrum FD, Ornelles DA, (1998) p53 status does not determine outcome of E1B 55-kilodalton mutant adenovirus lytic infection. J Virol 72: 9479-9490.
29. Geoerger B, Grill J, Opolon P, Morizet J, Aubert G, et al. (2002) Oncolytic activity of the E1B-55 kDa-deleted adenovirus ONYX-015 is independent of cellular p53 status in human malignant glioma xenografts. Cancer Res 62: 764-772.
30. Rothmann T, Hengstermann A, Whitaker NJ, Scheffner M, zur Hausen H, (1998) Replication of ONYX-015, a potential anticancer adenovirus, is independent of p53 status in tumor cells. J Virol 72: 9470-9478.
31. Hobom U, Dobbelstein M, (2004) E1B-55-kilodalton protein is not required to block p53-induced transcription during adenovirus infection. J Virol 78: 7685-7697.
32. O'Shea CC, Johnson L, Bagus B, Choi S, Nicholas C, et al. (2004) Late viral RNA export, rather than p53 inactivation, determines ONYX-015 tumor selectivity. Cancer Cell 6: 611-623.
33. Rao XM, Zheng X, Waigel S, Zacharias W, McMasters KM, et al. (2006) Gene expression profiles of normal human lung cells affected by adenoviral E1B. Virology 350: 418-428.
34. Zheng X, Rao XM, Gomez-Gutierrez JG, Hao H, McMasters KM, et al. (2008) Adenovirus E1B55K region is required to enhance cyclin E expression for efficient viral DNA replication. J Virol 82: 3415-3427.
35. Ohtsubo M, Theodoras AM, Schumacher J, Roberts JM, Pagano M, (1995) Human cyclin E, a nuclear protein essential for the G1-to-S phase transition. Mol Cell Biol 15: 2612-2624.
36. Coverley D, Laman H, Laskey RA, (2002) Distinct roles for cyclins E and A during DNA replication complex assembly and activation. Nat Cell Biol 4: 523-528.
37. Furstenthal L, Kaiser BK, Swanson C, Jackson PK, (2001) Cyclin E uses Cdc6 as a chromatin-associated receptor required for DNA replication. J Cell Biol 152: 1267-1278.
38. Hinchcliffe EH, Li C, Thompson EA, Maller JL, Sluder G, (1999) Requirement of Cdk2-cyclin E activity for repeated centrosome reproduction in Xenopus egg extracts. Science 283: 851-854.
39. Matsumoto Y, Hayashi K, Nishida E, (1999) Cyclin-dependent kinase 2 (Cdk2) is required for centrosome duplication in mammalian cells. Curr Biol 9: 429-432.
40. Le Cam L, Polanowska J, Fabbrizio E, Olivier M, Philips A, et al. (1999) Timing of cyclin E gene expression depends on the regulated association of a bipartite repressor element with a novel E2F complex. EMBO J 18: 1878-1890.
41. Marone M, Scambia G, Giannitelli C, Ferrandina G, Masciullo V, et al. (1998) Analysis of cyclin E and CDK2 in ovarian cancer: gene amplification and RNA overexpression. Int J Cancer 75: 34-39.
42. Sawasaki T, Shigemasa K, Shiroyama Y, Kusuda T, Fujii T, et al. (2001) Cyclin E mRNA overexpression in epithelial ovarian cancers: inverse correlation with p53 protein accumulation. J Soc Gynecol Investig 8: 179-185.
43. Donnellan R, Chetty R, (1999) Cyclin E in human cancers. FASEB J 13: 773-780.
44. Strohmaier H, Spruck CH, Kaiser P, Won KA, Sangfelt O, et al. (2001) Human F-box protein hCdc4 targets cyclin E for proteolysis and is mutated in a breast cancer cell line. Nature 413: 316-322.
45. Akli S, Zheng PJ, Multani AS, Wingate HF, Pathak S, et al. (2004) Tumor-specific low molecular weight forms of cyclin E induce genomic instability and resistance to p21, p27, and antiestrogens in breast cancer. Cancer Res 64: 3198-3208.
46. Keyomarsi K, Tucker SL, Buchholz TA, Callister M, Ding Y, et al. (2002) Cyclin E and survival in patients with breast cancer. N Engl J Med 347: 1566-1575.
47. Wingate H, Puskas A, Duong M, Bui T, Richardson D, et al. (2009) Low molecular weight cyclin E is specific in breast cancer and is associated with mechanisms of tumor progression. Cell Cycle 8: 1062-1068.
48. Spruck CH, Won KA, Reed SI, (1999) Deregulated cyclin E induces chromosome instability. Nature 401: 297-300.
49. Minella AC, Swanger J, Bryant E, Welcker M, Hwang H, et al. (2002) p53 and p21 form an inducible barrier that protects cells against cyclin E-cdk2 deregulation. Curr Biol 12: 1817-1827.
50. Bortner DM, Rosenberg MP, (1997) Induction of mammary gland hyperplasia and carcinomas in transgenic mice expressing human cyclin E. Mol Cell Biol. 17: 453-459.
51. Loeb KR, Kostner H, Firpo E, Norwood T, K DT, et al. (2005) A mouse model for cyclin E-dependent genetic instability and tumorigenesis. Cancer Cell 8: 35-47.
52. Freemantle SJ, Dmitrovsky E, (2010) Cyclin E transgenic mice: discovery tools for lung cancer biology, therapy, and prevention. Cancer Prev Res (Phila) 3: 1513-1518.
53. Moroy T, Geisen C, (2004) Int J Biochem Cell Biol. 36: 1424-1439.
54. Geng Y, Lee YM, Welcker M, Swanger J, Zagozdzon A, et al. (2007) Kinase-independent function of cyclin E. Mol Cell. 25: 127-139.
55. Geisen C, Moroy T, (2002) The oncogenic activity of cyclin E is not confined to Cdk2 activation alone but relies on several other, distinct functions of the protein. J Biol Chem 277: 39909-39918.
56. Ortega S, Prieto I, Odajima J, Martin A, Dubus P, et al. (2003) Cyclin-dependent kinase 2 is essential for meiosis but not for mitotic cell division in mice. Nat Genet 35: 25-31.
57. Berthet C, Aleem E, Coppola V, Tessarollo L, Kaldis P, (2003) Cdk2 knockout mice are viable. Curr Biol 13: 1775-1785.
58. Geng Y, Yu Q, Sicinska E, Das M, Schneider JE, et al. (2003) Cyclin E ablation in the mouse. Cell 114: 431-443.
59. Matsumoto Y, Maller JL, (2004) A centrosomal localization signal in cyclin E required for Cdk2-independent S phase entry. Science 306: 885-888.
60. Rao XM, Tseng MT, Zheng X, Dong Y, Jamshidi-Parsian A, et al. (2004) E1A-induced apoptosis does not prevent replication of adenoviruses with deletion of E1b in majority of infected cancer cells. Cancer Gene Ther 11: 585-593.
61. Sandig V, Youil R, Bett AJ, Franlin LL, Oshima M, et al. (2000) Optimization of the helper-dependent adenovirus system for production and potency in vivo. Proc Natl Acad Sci U S A 97: 1002-1007.
62. Zhao T, Rao XM, Xie X, Li L, Thompson TC, et al. (2003) Adenovirus with insertion-mutated E1A selectively propagates in liver cancer cells and destroys tumors in vivo. Cancer Res 63: 3073-3078.
63. Bett AJ, Haddara W, Prevec L, Graham FL, (1994) An efficient and flexible system for construction of adenovirus vectors with insertions or deletions in early regions 1 and 3. Proc Natl Acad Sci U S A 91: 8802-8806.
64. Zheng X, Rao XM, Snodgrass CL, McMasters KM, Zhou HS, (2006) Selective replication of E1B55K-deleted adenoviruses depends on enhanced E1A expression in cancer cells. Cancer Gene Ther 13: 572-583.
65. Chou MM, Masuda-Robens JM, Gupta ML, (2003) Cdc42 promotes G1 progression through p70 S6 kinase-mediated induction of cyclin E expression. J Biol Chem 278: 35241-35247.
66. Gu Y, Rosenblatt J, Morgan DO, (1992) Cell cycle regulation of CDK2 activity by phosphorylation of Thr160 and Tyr15. EMBO J 11: 3995-4005.
67. Hunter T, Pines J, (1994) Cyclins and cancer. II: Cyclin D and CDK inhibitors come of age. Cell 79: 573-582.
68. Sherr CJ, (1995) D-type cyclins. Trends Biochem Sci 20: 187-190.
69. Moldovan GL, Pfander B, Jentsch S, (2007) PCNA, the maestro of the replication fork. Cell 129: 665-679.
70. Zhang H, Xiong Y, Beach D, (1993) Proliferating cell nuclear antigen and p21 are components of multiple cell cycle kinase complexes. Mol Biol Cell 4: 897-906.
71. Zarkowska T, Mittnacht S, (1997) Differential phosphorylation of the retinoblastoma protein by G1/S cyclin-dependent kinases. J Biol Chem 272: 12738-12746.
72. Schmitz NM, Leibundgut K, Hirt A, (2005) CDK2 catalytic activity and loss of nuclear tethering of retinoblastoma protein in childhood acute lymphoblastic leukemia. Leukemia 19: 1783-1787.
73. Hsieh WS, Soo R, Peh BK, Loh T, Dong D, et al. (2009) Pharmacodynamic effects of seliciclib, an orally administered cell cycle modulator, in undifferentiated nasopharyngeal cancer. Clin Cancer Res 15: 1435-1442.
74. Connell-Crowley L, Harper JW, Goodrich DW, (1997) Cyclin D1/Cdk4 regulates retinoblastoma protein-mediated cell cycle arrest by site-specific phosphorylation. Mol Biol Cell 8: 287-301.
75. Sherr CJ, Roberts JM, (1995) Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev 9: 1149-1163.
76. De Azevedo WF, Leclerc S, Meijer L, Havlicek L, Strnad M, et al. (1997) Inhibition of cyclin-dependent kinases by purine analogues: crystal structure of human cdk2 complexed with roscovitine. Eur J Biochem 243: 518-526.
77. Raynaud FI, Whittaker SR, Fischer PM, McClue S, Walton MI, et al. (2005) In vitro and in vivo pharmacokinetic-pharmacodynamic relationships for the trisubstituted aminopurine cyclin-dependent kinase inhibitors olomoucine, bohemine and CYC202. Clin Cancer Res 11: 4875-4887.
78. Akli S, Bui T, Wingate H, Biernacka A, Moulder S, et al. (2010) Low-molecular-weight cyclin E can bypass letrozole-induced G1 arrest in human breast cancer cells and tumors. Clin Cancer Res 16: 1179-1190.
79. Meijer L, Borgne A, Mulner O, Chong JP, Blow JJ, et al. (1997) Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2 and cdk5. Eur J Biochem 243: 527-536.
80. Hayflick L, Plotkin SA, Norton TW, Koprowski H, (1962) Preparation of poliovirus vaccines in a human fetal diploid cell strain. Am J Hyg 75: 240-258.
81. Keyomarsi K, O'Leary N, Molnar G, Lees E, Fingert HJ, et al. (1994) Cyclin E, a potential prognostic marker for breast cancer. Cancer Res 54: 380-385.
82. Porter DC, Zhang N, Danes C, McGahren MJ, Harwell RM, et al. (2001) Tumor-specific proteolytic processing of cyclin E generates hyperactive lower-molecular-weight forms. Mol Cell Biol 21: 6254-6269.
83. Koff A, Giordano A, Desai D, Yamashita K, Harper JW, et al. (1992) Formation and activation of a cyclin E-cdk2 complex during the G1 phase of the human cell cycle. Science 257: 1689-1694.
84. Harwell RM, Mull BB, Porter DC, Keyomarsi K, (2004) Activation of cyclin-dependent kinase 2 by full length and low molecular weight forms of cyclin E in breast cancer cells. J Biol Chem 279: 12695-12705.
85. Weinberg RA, (1995) The retinoblastoma protein and cell cycle control. Cell 81: 323-330.
86. Giacinti C, Giordano A, (2006) RB and cell cycle progression. Oncogene 25: 5220-5227.
87. Ohtani K, DeGregori J, Nevins JR, (1995) Regulation of the cyclin E gene by transcription factor E2F1. Proc Natl Acad Sci U S A 92: 12146-12150.
88. Duronio RJ, O'Farrell PH, (1995) Developmental control of the G1 to S transition in Drosophila: cyclin Eis a limiting downstream target of E2F. Genes Dev 9: 1456-1468.
89. Sheaff RJ, Groudine M, Gordon M, Roberts JM, Clurman BE, (1997) Cyclin E-CDK2 is a regulator of p27Kip1. Genes Dev 11: 1464-1478.
90. Zhu H, Nie L, Maki CG, (2005) Cdk2-dependent Inhibition of p21 stability via a C-terminal cyclin-binding motif. J Biol Chem 280: 29282-29288.
91. Vlach J, Hennecke S, Amati B, (1997) Phosphorylation-dependent degradation of the cyclin-dependent kinase inhibitor p27. EMBO J 16: 5334-5344.
92. Montagnoli A, Fiore F, Eytan E, Carrano AC, Draetta GF, et al. (1999) Ubiquitination of p27 is regulated by Cdk-dependent phosphorylation and trimeric complex formation. Genes Dev 13: 1181-1189.
93. Bornstein G, Bloom J, Sitry-Shevah D, Nakayama K, Pagano M, et al. (2003) Role of the SCFSkp2 ubiquitin ligase in the degradation of p21Cip1 in S phase. J Biol Chem 278: 25752-25757.