Epstein-Barr virus nuclear antigen 3c facilitates G1-S transition by stabilizing and enhancing the function of Cyclin D1

PLoS Pathogens

Volumn 7, Issue 2, 2011, Pages

  Saha, Abhik ^a   Halder, Sabyasachi ^a   Upadhyay, Santosh K ^a   Lu, Jie ^a   Kumar, Pankaj ^a   Murakami, Masanao ^a,b   Cai, Qiliang ^a   Robertson, Erle S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b KOCHI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; CYCLIN DEPENDENT KINASE 6; EPSTEIN BARR VIRUS ANTIGEN; EPSTEIN BARR VIRUS ANTIGEN 3C; GLYCOGEN SYNTHASE KINASE 3BETA; PROTEASOME; RETINOBLASTOMA PROTEIN; SHORT HAIRPIN RNA; UBIQUITIN; UNCLASSIFIED DRUG; CCND1 PROTEIN, HUMAN; EBNA 3C, EPSTEIN BARR VIRUS; EBNA-3C, EPSTEIN-BARR VIRUS; VIRUS ANTIGEN;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL GROWTH; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; LYMPHOBLASTOID CELL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; UBIQUITINATION; CELL CULTURE; CHEMISTRY; EPSTEIN BARR VIRUS; EPSTEIN BARR VIRUS INFECTION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN PROCESSING; PROTEIN TERTIARY STRUCTURE; UPREGULATION; VIRUS CELL TRANSFORMATION;

HUMAN HERPESVIRUS 4;

ANTIGENS, VIRAL; CELL TRANSFORMATION, VIRAL; CELLS, CULTURED; CYCLIN D1; EPSTEIN-BARR VIRUS INFECTIONS; G1 PHASE; GENE EXPRESSION REGULATION; HERPESVIRUS 4, HUMAN; HUMANS; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; S PHASE; UBIQUITINATION; UP-REGULATION;

EID: 79952209417     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001275     Document Type: Article

References (60)

1. Robertson ES, (2010) Epstein-Barr virus: latency and transformation. Norwich, United Kingdom Caister Academic Press.
2. Kieff E, Rickinson AB, (2002) Epstein-Barr virus and its replication. In: Knipe D, Howley P, editors. Fields virology, 4th ed Philadelphia Lippincott Williams & Wilkins pp. 2511-2573.
3. O'Nions J, Allday MJ, (2004) Deregulation of the cell cycle by the Epstein-Barr virus. Adv Cancer Res 92: 119-186.
4. Bajaj BG, Murakami M, Cai Q, Verma SC, Lan K, et al. (2008) Epstein-Barr virus nuclear antigen 3C interacts with and enhances the stability of the c-Myc oncoprotein. J Virol 82: 4082-4090.
5. Bain M, Watson RJ, Farrell PJ, Allday MJ, (1996) Epstein-Barr virus nuclear antigen 3C is a powerful repressor of transcription when tethered to DNA. J Virol 70: 2481-2489.
6. Rosendorff A, Illanes D, David G, Lin J, Kieff E, et al. (2004) EBNA3C coactivation with EBNA2 requires a SUMO homology domain. J Virol 78: 367-377.
7. Cotter MA 2nd, Robertson ES, (2000) Modulation of histone acetyltransferase activity through interaction of epstein-barr nuclear antigen 3C with prothymosin alpha. Mol Cell Biol 20: 5722-5735.
8. Knight JS, Lan K, Subramanian C, Robertson ES, (2003) 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 77: 4261-4272.
9. Touitou R, Hickabottom M, Parker G, Crook T, Allday MJ, (2001) Physical and functional interactions between the corepressor CtBP and the Epstein-Barr virus nuclear antigen EBNA3C. J Virol 75: 7749-7755.
10. Subramanian C, Cotter MA 2nd, Robertson ES, (2001) Epstein-Barr virus nuclear protein EBNA-3C interacts with the human metastatic suppressor Nm23-H1: a molecular link to cancer metastasis. Nat Med 7: 350-355.
11. Yan X, Mouillet JF, Ou Q, Sadovsky Y, (2003) A novel domain within the DEAD-box protein DP103 is essential for transcriptional repression and helicase activity. Mol Cell Biol 23: 414-423.
12. Knight JS, Sharma N, Robertson ES, (2005) SCFSkp2 complex targeted by Epstein-Barr virus essential nuclear antigen. Mol Cell Biol 25: 1749-1763.
13. Subramanian C, Hasan S, Rowe M, Hottiger M, Orre R, et al. (2002) Epstein-Barr virus nuclear antigen 3C and prothymosin alpha interact with the p300 transcriptional coactivator at the CH1 and CH3/HAT domains and cooperate in regulation of transcription and histone acetylation. J Virol 76: 4699-4708.
14. Yi F, Saha A, Murakami M, Kumar P, Knight JS, et al. (2009) Epstein-Barr virus nuclear antigen 3C targets p53 and modulates its transcriptional and apoptotic activities. Virology 388: 236-247.
15. Knight JS, Robertson ES, (2004) Epstein-Barr virus nuclear antigen 3C regulates cyclin A/p27 complexes and enhances cyclin A-dependent kinase activity. J Virol 78: 1981-1991.
16. Knight JS, Sharma N, Kalman DE, Robertson ES, (2004) A cyclin-binding motif within the amino-terminal homology domain of EBNA3C binds cyclin A and modulates cyclin A-dependent kinase activity in Epstein-Barr virus-infected cells. J Virol 78: 12857-12867.
17. Knight JS, Sharma N, Robertson ES, (2005) Epstein-Barr virus latent antigen 3C can mediate the degradation of the retinoblastoma protein through an SCF cellular ubiquitin ligase. Proc Natl Acad Sci U S A 102: 18562-18566.
18. Saha A, Murakami M, Kumar P, Bajaj B, Sims K, et al. (2009) Epstein-Barr virus nuclear antigen 3C augments Mdm2-mediated p53 ubiquitination and degradation by deubiquitinating Mdm2. J Virol 83: 4652-4669.
19. Choudhuri T, Verma SC, Lan K, Murakami M, Robertson ES, (2007) The ATM/ATR signaling effector Chk2 is targeted by Epstein-Barr virus nuclear antigen 3C to release the G2/M cell cycle block. J Virol 81: 6718-6730.
20. Parker GA, Crook T, Bain M, Sara EA, Farrell PJ, et al. (1996) Epstein-Barr virus nuclear antigen (EBNA)3C is an immortalizing oncoprotein with similar properties to adenovirus E1A and papillomavirus E7. Oncogene 13: 2541-2549.
21. Parker GA, Touitou R, Allday MJ, (2000) Epstein-Barr virus EBNA3C can disrupt multiple cell cycle checkpoints and induce nuclear division divorced from cytokinesis. Oncogene 19: 700-709.
22. Bloom J, Cross FR, (2007) Multiple levels of cyclin specificity in cell-cycle control. Nat Rev Mol Cell Biol 8: 149-160.
23. Baldin V, Lukas J, Marcote MJ, Pagano M, Draetta G, (1993) Cyclin D1 is a nuclear protein required for cell cycle progression in G1. Genes Dev 7: 812-821.
24. Benzeno S, Lu F, Guo M, Barbash O, Zhang F, et al. (2006) Identification of mutations that disrupt phosphorylation-dependent nuclear export of cyclin D1. Oncogene 25: 6291-6303.
25. Gansauge S, Gansauge F, Ramadani M, Stobbe H, Rau B, et al. (1997) Overexpression of cyclin D1 in human pancreatic carcinoma is associated with poor prognosis. Cancer Res 57: 1634-1637.
26. Lin DI, Barbash O, Kumar KG, Weber JD, Harper JW, et al. (2006) Phosphorylation-dependent ubiquitination of cyclin D1 by the SCF(FBX4-alphaB crystallin) complex. Mol Cell 24: 355-366.
27. Diehl JA, Cheng M, Roussel MF, Sherr CJ, (1998) Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev 12: 3499-3511.
28. Campo E, Raffeld M, Jaffe ES, (1999) Mantle-cell lymphoma. Semin Hematol 36: 115-127.
29. Yatabe Y, Nakamura S, Seto M, Kuroda H, Kagami Y, et al. (1996) Clinicopathologic study of PRAD1/cyclin D1 overexpressing lymphoma with special reference to mantle cell lymphoma. A distinct molecular pathologic entity. Am J Surg Pathol 20: 1110-1122.
30. Nakagawa H, Wang TC, Zukerberg L, Odze R, Togawa K, et al. (1997) The targeting of the cyclin D1 oncogene by an Epstein-Barr virus promoter in transgenic mice causes dysplasia in the tongue, esophagus and forestomach. Oncogene 14: 1185-1190.
31. Kim JK, Diehl JA, (2009) Nuclear cyclin D1: an oncogenic driver in human cancer. J Cell Physiol 220: 292-296.
32. Palmero I, Holder A, Sinclair AJ, Dickson C, Peters G, (1993) Cyclins D1 and D2 are differentially expressed in human B-lymphoid cell lines. Oncogene 8: 1049-1054.
33. Meyyappan M, Wong H, Hull C, Riabowol KT, (1998) Increased expression of cyclin D2 during multiple states of growth arrest in primary and established cells. Mol Cell Biol 18: 3163-3172.
34. Sinclair AJ, Palmero I, Peters G, Farrell PJ, (1994) EBNA-2 and EBNA-LP cooperate to cause G0 to G1 transition during immortalization of resting human B lymphocytes by Epstein-Barr virus. EMBO J 13: 3321-3328.
35. Kim HR, Jeong JA, Park CH, Lee SK, Lee WK, et al. (2002) A role for cell cycle proteins in the serum-starvation resistance of Epstein-Barr virus immortalized B lymphocytes. Biochem Cell Biol 80: 407-413.
36. Park CH, Kim HR, Kim J, Jang SH, Lee KY, et al. (2004) Latent membrane protein 1 of Epstein-Barr virus plays an important role in the serum starvation resistance of Epstein-Barr virus-immortalized B lymphocytes. J Cell Biochem 91: 777-785.
37. Murai Y, Dobashi Y, Okada E, Ishizawa S, Shiota M, et al. (2001) Study on the role of G1 cyclins in Epstein-Barr virus-associated human lymphomas maintained in severe combined immune deficiency (SCID) mice. Int J Cancer 92: 232-239.
38. Lu J, Verma SC, Murakami M, Cai Q, Kumar P, et al. (2009) Latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus (KSHV) upregulates survivin expression in KSHV-Associated B-lymphoma cells and contributes to their proliferation. J Virol 83: 7129-7141.
39. Ponten J, Saksela E, (1967) Two established in vitro cell lines from human mesenchymal tumours. Int J Cancer 2: 434-447.
40. Halder S, Murakami M, Verma SC, Kumar P, Yi F, et al. (2009) Early events associated with infection of Epstein-Barr virus infection of primary B-cells. PLoS One 4: e7214.
41. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
42. Klier M, Anastasov N, Hermann A, Meindl T, Angermeier D, et al. (2008) Specific lentiviral shRNA-mediated knockdown of cyclin D1 in mantle cell lymphoma has minimal effects on cell survival and reveals a regulatory circuit with cyclin D2. Leukemia 22: 2097-2105.
43. O'Nions J, Allday MJ, (2003) Epstein-Barr virus can inhibit genotoxin-induced G1 arrest downstream of p53 by preventing the inactivation of CDK2. Oncogene 22: 7181-7191.
44. Maruo S, Wu Y, Ishikawa S, Kanda T, Iwakiri D, et al. (2006) Epstein-Barr virus nuclear protein EBNA3C is required for cell cycle progression and growth maintenance of lymphoblastoid cells. Proc Natl Acad Sci U S A 103: 19500-19505.
45. Arvanitakis L, Yaseen N, Sharma S, (1995) Latent membrane protein-1 induces cyclin D2 expression, pRb hyperphosphorylation, and loss of TGF-beta 1-mediated growth inhibition in EBV-positive B cells. J Immunol 155: 1047-1056.
46. Siegert JL, Rushton JJ, Sellers WR, Kaelin WG Jr, Robbins PD, (2000) Cyclin D1 suppresses retinoblastoma protein-mediated inhibition of TAFII250 kinase activity. Oncogene 19: 5703-5711.
47. Zwicker J, Brusselbach S, Jooss KU, Sewing A, Behn M, et al. (1999) Functional domains in cyclin D1: pRb-kinase activity is not essential for transformation. Oncogene 18: 19-25.
48. Zhou Y, Li J, Xu K, Hu SX, Benedict WF, et al. (1994) Further characterization of retinoblastoma gene-mediated cell growth and tumor suppression in human cancer cells. Proc Natl Acad Sci U S A 91: 4165-4169.
49. Maruo S, Wu Y, Ito T, Kanda T, Kieff ED, et al. (2009) Epstein-Barr virus nuclear protein EBNA3C residues critical for maintaining lymphoblastoid cell growth. Proc Natl Acad Sci U S A 106: 4419-4424.
50. Jares P, Fernandez PL, Campo E, Nadal A, Bosch F, et al. (1994) PRAD-1/cyclin D1 gene amplification correlates with messenger RNA overexpression and tumor progression in human laryngeal carcinomas. Cancer Res 54: 4813-4817.
51. Bartkova J, Lukas J, Muller H, Strauss M, Gusterson B, et al. (1995) Abnormal patterns of D-type cyclin expression and G1 regulation in human head and neck cancer. Cancer Res 55: 949-956.
52. Buckley MF, Sweeney KJ, Hamilton JA, Sini RL, Manning DL, et al. (1993) Expression and amplification of cyclin genes in human breast cancer. Oncogene 8: 2127-2133.
53. Williams ME, Swerdlow SH, Rosenberg CL, Arnold A, (1992) Characterization of chromosome 11 translocation breakpoints at the bcl-1 and PRAD1 loci in centrocytic lymphoma. Cancer Res 52: 5541s-5544s.
54. Motokura T, Bloom T, Kim HG, Juppner H, Ruderman JV, et al. (1991) A novel cyclin encoded by a bcl1-linked candidate oncogene. Nature 350: 512-515.
55. Lovec H, Sewing A, Lucibello FC, Muller R, Moroy T, (1994) Oncogenic activity of cyclin D1 revealed through cooperation with Ha-ras: link between cell cycle control and malignant transformation. Oncogene 9: 323-326.
56. Ganiatsas S, Dow R, Thompson A, Schulman B, Germain D, (2001) A splice variant of Skp2 is retained in the cytoplasm and fails to direct cyclin D1 ubiquitination in the uterine cancer cell line SK-UT. Oncogene 20: 3641-3650.
57. Yu ZK, Gervais JL, Zhang H, (1998) Human CUL-1 associates with the SKP1/SKP2 complex and regulates p21(CIP1/WAF1) and cyclin D proteins. Proc Natl Acad Sci U S A 95: 11324-11329.
58. Alao JP, Lam EW, Ali S, Buluwela L, Bordogna W, et al. (2004) Histone deacetylase inhibitor trichostatin A represses estrogen receptor alpha-dependent transcription and promotes proteasomal degradation of cyclin D1 in human breast carcinoma cell lines. Clin Cancer Res 10: 8094-8104.
59. Pontano LL, Diehl JA, (2008) Speeding through cell cycle roadblocks: Nuclear cyclin D1-dependent kinase and neoplastic transformation. Cell Div 3: 12.
60. Sherr CJ, (1996) Cancer cell cycles. Science 274: 1672-1677.