EBNA3C regulates p53 through induction of Aurora kinase B

Oncotarget

Volumn 6, Issue 8, 2015, Pages 5788-5803

  Jha, Hem C ^a   Yang, Karren ^a   El Naccache, Darine W ^a   Sun, Zhiguo ^a   Robertson, Erle S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Aurora Kinase B; EBV; Oncogenesis; P53; Phosphorylation

Indexed keywords

AURORA B KINASE; EPSTEIN BARR VIRUS ANTIGEN 3C; PROTEIN P53; PROTEIN P73; SERINE; TRANSCRIPTION FACTOR ETS 1; UNCLASSIFIED DRUG; VIRUS ANTIGEN; AURKB PROTEIN, HUMAN; DNA BINDING PROTEIN; EBNA-3C, EPSTEIN-BARR VIRUS; EPSTEIN BARR VIRUS ANTIGEN; LYMPHOCRYPTOVIRUS NUCLEAR ANTIGEN 3C; NUCLEAR PROTEIN; P73 PROTEIN, HUMAN; TP53 PROTEIN, HUMAN; TUMOR PROTEIN P73; TUMOR SUPPRESSOR PROTEIN; VIRAL PROTEIN;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; BINDING SITE; CELL TRANSFORMATION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME INDUCTION; EPSTEIN BARR VIRUS; GENE MUTATION; GENE SILENCING; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION; UPREGULATION; WILD TYPE; BIOSYNTHESIS; CELL LINE; CELL PROLIFERATION; GENE INACTIVATION; GENETIC TRANSFECTION; GENETICS; HEK293 CELL LINE; METABOLISM; MONONUCLEAR CELL; PHOSPHORYLATION; PHYSIOLOGY; VIROLOGY;

ANTIGENS, VIRAL; AURORA KINASE B; CELL LINE; CELL PROLIFERATION; DNA-BINDING PROTEINS; ENZYME INDUCTION; EPSTEIN-BARR VIRUS NUCLEAR ANTIGENS; GENE KNOCKOUT TECHNIQUES; HEK293 CELLS; HUMANS; LEUKOCYTES, MONONUCLEAR; NUCLEAR PROTEINS; PHOSPHORYLATION; TRANSFECTION; TUMOR PROTEIN P73; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS; VIRAL PROTEINS;

EID: 84925607736     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3310     Document Type: Article

References (57)

1. Niedobitek G, Meru N and Delecluse HJ. Epstein-Barr virus infection and human malignancies. Int J Exp Pathol. 2001; 82(3):149-170.
2. Thompson MP and Kurzrock R. Epstein-Barr virus and cancer. Clin Cancer Res. 2004; 10(3):803-821.
3. Young L, Alfieri C, Hennessy K, Evans H, O'Hara C, Anderson KC, Ritz J, Shapiro RS, Rickinson A, Kieff E and et al. Expression of Epstein-Barr virus transformation-associated genes in tissues of patients with EBV lymphoproliferative disease. N Engl J Med. 1989; 321(16):1080-1085.
4. Saha A, Halder S, Upadhyay SK, Lu J, Kumar P, Murakami M, Cai Q and Robertson ES. Epstein-Barr virus nuclear antigen 3C facilitates G1-S transition by stabilizing and enhancing the function of cyclin D1. PLoS Pathog. 2011; 7(2):e1001275.
5. Saha A, Lu J, Morizur L, Upadhyay SK, Aj MP and Robertson ES. E2F1 mediated apoptosis induced by the DNA damage response is blocked by EBV nuclear antigen 3C in lymphoblastoid cells. PLoS Pathog. 2012; 8(3):e1002573.
6. Leao M, Anderton E, Wade M, Meekings K and Allday MJ. Epstein-barr virus-induced resistance to drugs that activate the mitotic spindle assembly checkpoint in Burkitt's lymphoma cells. J Virol. 2007; 81(1):248-260.
7. Parker GA, Touitou R and Allday MJ. Epstein-Barr virus EBNA3C can disrupt multiple cell cycle checkpoints and induce nuclear division divorced from cytokinesis. Oncogene. 2000; 19(5):700-709.
8. Robertson ES, Lin J and Kieff E. The amino-terminal domains of Epstein-Barr virus nuclear proteins 3A, 3B, and 3C interact with RBPJ(kappa). J Virol. 1996; 70(5):3068-3074.
9. Kaul R, Murakami M, Lan K, Choudhuri T and Robertson ES. EBNA3C can modulate the activities of the transcription factor Necdin in association with metastasis suppressor protein Nm23-H1. J Virol. 2009; 83(10):4871-4883.
10. Maruo S, Wu Y, Ishikawa S, Kanda T, Iwakiri D and Takada K. Epstein-Barr virus nuclear protein EBNA3C is required for cell cycle progression and growth maintenance of lymphoblastoid cells. Proc Natl Acad Sci USA. 2006; 103(51):19500-19505.
11. Maruo S, Wu Y, Ito T, Kanda T, Kieff ED and Takada K. Epstein-Barr virus nuclear protein EBNA3C residues critical for maintaining lymphoblastoid cell growth. Proc Natl Acad Sci USA. 2009; 106(11):4419-4424.
12. Paschos K, Smith P, Anderton E, Middeldorp JM, White RE and Allday MJ. Epstein-barr virus latency in B cells leads to epigenetic repression and CpG methylation of the tumour suppressor gene Bim. PLoS Pathog. 2009; 5(6):e1000492.
13. Wang F, Gregory C, Sample C, Rowe M, Liebowitz D, Murray R, Rickinson A and Kieff E. Epstein-Barr virus latent membrane protein (LMP1) and nuclear proteins 2 and 3C are effectors of phenotypic changes in B lymphocytes: EBNA-2 and LMP1 cooperatively induce CD23. J Virol. 1990; 64(5):2309-2318.
14. Banerjee S, Lu J, Cai Q, Saha A, Jha HC, Dzeng RK and Robertson ES. The EBV Latent Antigen 3C Inhibits Apoptosis through Targeted Regulation of Interferon Regulatory Factors 4 and 8. PLoS Pathog. 2013; 9(5):e1003314.
15. Jha HC, Lu J, Saha A, Cai Q, Banerjee S, Prasad MA and Robertson ES. EBNA3C-mediated regulation of Aurora Kinase B contributes to EBV-induced B-cell proliferation through modulation of the activities of Rb and apoptotic Caspases. J Virol. 2013; 87(22): 12121-12138.
16. Jha HC, Middeldorp JM, Saha A, Banerjee S, Lu J and Robertson ES. Epstein-Barr virus essential antigen EBNA3C attenuates H2AX expression. J Virol. 2014; 88(7):3776-3788.
17. Marshall D and Sample C. Epstein-Barr virus nuclear antigen 3C is a transcriptional regulator. J Virol. 1995; 69(6):3624-3630.
18. Knight JS, Lan K, Subramanian C and Robertson ES. Epstein-Barr virus nuclear antigen 3C recruits histone deacetylase activity and associates with the corepressors mSin3A and NCoR in human B-cell lines. J Virol. 2003; 77(7):4261-4272.
19. Radkov SA, Touitou R, Brehm A, Rowe M, West M, Kouzarides T and Allday MJ. Epstein-Barr virus nuclear antigen 3C interacts with histone deacetylase to repress transcription. J Virol. 1999; 73(7):5688-5697.
20. Subramanian C and Robertson ES. The metastatic suppressor Nm23-H1 interacts with EBNA3C at sequences located between the glutamine-and proline-rich domains and can cooperate in activation of transcription. J Virol. 2002; 76(17):8702-8709.
21. Liu Y and Kulesz-Martin M. p53 protein at the hub of cellular DNA damage response pathways through sequence-specific and non-sequence-specific DNA binding. Carcinogenesis. 2001; 22(6):851-860.
22. Hollstein M, Sidransky D, Vogelstein B and Harris CC. p53 mutations in human cancers. Science. 1991; 253(5015):49-53.
23. Levine AJ. p53, the cellular gatekeeper for growth and division. Cell. 1997; 88(3):323-331.
24. Yi F, Saha A, Murakami M, Kumar P, Knight JS, Cai Q, Choudhuri T and Robertson ES. Epstein-Barr virus nuclear antigen 3C targets p53 and modulates its transcriptional and apoptotic activities. Virology. 2009; 388(2):236-247.
25. Chan YW, Jeyaprakash AA, Nigg EA and Santamaria A. Aurora B controls kinetochore-microtubule attachments by inhibiting Ska complex-KMN network interaction. J Cell Biol. 2012; 196(5):563-571.
26. Ditchfield C, Johnson VL, Tighe A, Ellston R, Haworth C, Johnson T, Mortlock A, Keen N and Taylor SS. Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J Cell Biol. 2003; 161(2):267-280.
27. Nguyen HG, Makitalo M, Yang D, Chinnappan D, St Hilaire C and Ravid K. Deregulated Aurora-B induced tetraploidy promotes tumorigenesis. FASEB J. 2009; 23(8):2741-2748.
28. Gully CP, Velazquez-Torres G, Shin JH, Fuentes-Mattei E, Wang E, Carlock C, Chen J, Rothenberg D, Adams HP, Choi HH, Guma S, Phan L, Chou PC, Su CH, Zhang F, Chen JS, et al. Aurora B kinase phosphorylates and instigates degradation of p53. Proc Natl Acad Sci USA. 2012; 109(24):E1513-1522.
29. Cai Q, Xiao B, Si H, Cervini A, Gao J, Lu J, Upadhyay SK, Verma SC and Robertson ES. Kaposi's sarcoma herpesvirus upregulates Aurora A expression to promote p53 phosphorylation and ubiquitylation. PLoS Pathog. 2012; 8(3):e1002566.
30. Katayama H, Sasai K, Kawai H, Yuan ZM, Bondaruk J, Suzuki F, Fujii S, Arlinghaus RB, Czerniak BA and Sen S. Phosphorylation by aurora kinase A induces Mdm2-mediated destabilization and inhibition of p53. Nat Genet. 2004; 36(1):55-62.
31. Maunders MJ, Petti L and Rowe M. Precipitation of the Epstein-Barr virus protein EBNA 2 by an EBNA 3c-specific monoclonal antibody. J Gen Virol. 1994; 75 ( Pt 4):769-778.
32. Wakahara K, Ohno T, Kimura M, Masuda T, Nozawa S, Dohjima T, Yamamoto T, Nagano A, Kawai G, Matsuhashi A, Saitoh M, Takigami I, Okano Y and Shimizu K. EWS-Fli1 up-regulates expression of the Aurora A and Aurora B kinases. Mol Cancer Res. 2008; 6(12):1937-1945.
33. Gostissa M, Morelli M, Mantovani F, Guida E, Piazza S, Collavin L, Brancolini C, Schneider C and Del Sal G. The transcriptional repressor hDaxx potentiates p53-dependent apoptosis. J Biol Chem. 2004; 279(46):48013-48023.
34. Nguyen HG, Chinnappan D, Urano T and Ravid K. Mechanism of Aurora-B degradation and its dependency on intact KEN and A-boxes: identification of an aneuploidy-promoting property. Mol Cell Biol. 2005; 25(12):4977-4992.
35. Carvajal RD, Tse A and Schwartz GK. Aurora kinases: new targets for cancer therapy. Clin Cancer Res. 2006; 12(23):6869-6875.
36. Evans RP, Naber C, Steffler T, Checkland T, Maxwell CA, Keats JJ, Belch AR, Pilarski LM, Lai R and Reiman T. The selective Aurora B kinase inhibitor AZD1152 is a potential new treatment for multiple myeloma. Br J Haematol. 2008; 140(3):295-302.
37. Keen N and Taylor S. Aurora-kinase inhibitors as anticancer agents. Nat Rev Cancer. 2004; 4(12):927-936.
38. Wilkinson RW, Odedra R, Heaton SP, Wedge SR, Keen NJ, Crafter C, Foster JR, Brady MC, Bigley A, Brown E, Byth KF, Barrass NC, Mundt KE, Foote KM, Heron NM, Jung FH, et al. AZD1152, a selective inhibitor of Aurora B kinase, inhibits human tumor xenograft growth by inducing apoptosis. Clin Cancer Res. 2007; 13(12):3682-3688.
39. Yang J, Ikezoe T, Nishioka C, Tasaka T, Taniguchi A, Kuwayama Y, Komatsu N, Bandobashi K, Togitani K, Koeffler HP, Taguchi H and Yokoyama A. AZD1152, a novel and selective aurora B kinase inhibitor, induces growth arrest, apoptosis, and sensitization for tubulin depolymerizing agent or topoisomerase II inhibitor in human acute leukemia cells in vitro and in vivo. Blood. 2007; 110(6):2034-2040.
40. Rivlin N, Brosh R, Oren M and Rotter V. Mutations in the p53 Tumor Suppressor Gene: Important Milestones at the Various Steps of Tumorigenesis. Genes Cancer. 2011; 2(4):466-474.
41. Cai Q, Guo Y, Xiao B, Banerjee S, Saha A, Lu J, Glisovic T and Robertson ES. Epstein-Barr virus nuclear antigen 3C stabilizes Gemin3 to block p53-mediated apoptosis. PLoS Pathog. 2011; 7(12):e1002418.
42. Forte E and Luftig MA. MDM2-dependent inhibition of p53 is required for Epstein-Barr virus B-cell growth transformation and infected-cell survival. J Virol. 2009; 83(6):2491-2499.
43. Gruhne B, Sompallae R and Masucci MG. Three Epstein-Barr virus latency proteins independently promote genomic instability by inducing DNA damage, inhibiting DNA repair and inactivating cell cycle checkpoints. Oncogene. 2009; 28(45):3997-4008.
44. Sharma N, Knight JS and Robertson ES. Conserved cell cycle regulatory properties within the amino terminal domain of the Epstein-Barr virus nuclear antigen 3C. Virology. 2006; 346(2):379-384.
45. Saha A, Murakami M, Kumar P, Bajaj B, Sims K and Robertson ES. Epstein-Barr virus nuclear antigen 3C augments Mdm2-mediated p53 ubiquitination and degradation by deubiquitinating Mdm2. J Virol. 2009; 83(9):4652-4669.
46. Nikitin PA, Yan CM, Forte E, Bocedi A, Tourigny JP, White RE, Allday MJ, Patel A, Dave SS, Kim W, Hu K, Guo J, Tainter D, Rusyn E and Luftig MA. An ATM/Chk2-mediated DNA damage-responsive signaling pathway suppresses Epstein-Barr virus transformation of primary human B cells. Cell Host Microbe. 2010; 8(6):510-522.
47. Lin ZZ, Jeng YM, Hu FC, Pan HW, Tsao HW, Lai PL, Lee PH, Cheng AL and Hsu HC. Significance of Aurora B overexpression in hepatocellular carcinoma. Aurora B Overexpression in HCC. BMC Cancer. 2010; 10:461.
48. Yang D, Liu H, Goga A, Kim S, Yuneva M and Bishop JM. Therapeutic potential of a synthetic lethal interaction between the MYC proto-oncogene and inhibition of aurora-B kinase. Proc Natl Acad Sci USA. 2010; 107(31):13836-13841.
49. Donaldson LW, Petersen JM, Graves BJ and McIntosh LP. Solution structure of the ETS domain from murine Ets-1: a winged helix-turn-helix DNA binding motif. EMBO J. 1996; 15(1):125-134.
50. Leong WF, Chau JF and Li B. p53 Deficiency leads to compensatory up-regulation of p16INK4a. Mol Cancer Res. 2009; 7(3):354-360.
51. Cao B and Mao X. The ubiquitin-proteasomal system is critical for multiple myeloma: implications in drug discovery. Am J Blood Res. 2011; 1(1):46-56.
52. Knight JS and Robertson ES. Epstein-Barr virus nuclear antigen 3C regulates cyclin A/p27 complexes and enhances cyclin A-dependent kinase activity. J Virol. 2004; 78(4):1981-1991.
53. Saha A, Halder S, Upadhyay SK, Lu J, Kumar P, Murakami M, Cai Q and Robertson ES. Epstein-Barr virus nuclear antigen 3C facilitates G1-S transition by stabilizing and enhancing the function of cyclin D1. PLoS Pathog. 7(2):e1001275.
54. Honda R, Korner R and Nigg EA. Exploring the functional interactions between Aurora B, INCENP, and survivin in mitosis. Mol Biol Cell. 2003; 14(8):3325-3341.
55. Gao J, Cai Q, Lu J, Jha HC and Robertson ES. Upregulation of cellular Bcl-2 by the KSHV encoded RTA promotes virion production. PLoS One. 2011; 6(8):e23892.
56. Bai Y, Srinivasan L, Perkins L and Atchison ML. Protein acetylation regulates both PU.1 transactivation and Ig kappa 3' enhancer activity. J Immunol. 2005; 175(8):5160-5169.
57. Jha HC, Upadhyay SK, Prasad M, Lu J, Cai Q, Saha A and Robertson ES. H2AX phosphorylation is important for LANA-mediated Kaposi's sarcoma-associated herpesvirus episome persistence. Journal of virology. 2013; 87(9):5255-5269.