Kaposi sarcoma herpes virus latency associated nuclear antigen protein release the G2/M cell cycle blocks by modulating ATM/ATR mediated checkpoint pathway

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Kumar, Amit ^a   Sahu, Sushil Kumar ^a   Mohanty, Suchitra ^a   Chakrabarti, Sudipta ^a   Maji, Santanu ^a   Reddy, R Rajendra ^a   Jha, Asutosh K ^e   Goswami, Chandan ^e   Kundu, Chanakya N ^c   Rajasubramaniam, Shanmugam ^f   Verma, Subhash C ^d   Choudhuri, Tathagata ^a,b  

^a INSTITUTE OF LIFE SCIENCES   (India)

^b VISVA BHARATI UNIVERSITY   (India)

^c KIIT UNIVERSITY   (India)

^d UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

^e NATIONAL INSTITUTE OF SCIENCE EDUCATION AND RESEARCH   (India)

^f Regional Medical Research Centre for Tribals   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ATR PROTEIN; CAFFEINE; CHECKPOINT KINASE 2; CYCLIN DEPENDENT KINASE 1; LATENCY ASSOCIATED NUCLEAR ANTIGEN; NOCODAZOLE; ANTINEOPLASTIC AGENT; ATM PROTEIN; CDK1 PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE; LATENCY-ASSOCIATED NUCLEAR ANTIGEN; NUCLEAR PROTEIN; PROTEIN BINDING; SMALL INTERFERING RNA; VIRUS ANTIGEN;

AMINO TERMINAL SEQUENCE; ANTIGEN BINDING; ARTICLE; B LYMPHOCYTE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME PHOSPHORYLATION; G2 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; CELL CYCLE CHECKPOINT; CELL LINE; CHEMISTRY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HERPES VIRUS INFECTION; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN DOMAIN; PROTEIN TRANSPORT; RNA INTERFERENCE;

ANTIGENS, VIRAL; ANTINEOPLASTIC AGENTS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; B-LYMPHOCYTES; CELL CYCLE CHECKPOINTS; CELL LINE; CYCLIN-DEPENDENT KINASES; GENE EXPRESSION REGULATION; HERPESVIRIDAE INFECTIONS; HERPESVIRUS 8, HUMAN; HUMANS; NOCODAZOLE; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN TRANSPORT; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84903519667     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0100228     Document Type: Article

References (57)

1. Chang Y, Cesarman E, Pessin MS, Lee F, Culpepper J, et al. (1994) Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 266: 1865-1869.
2. Cesarman E, Chang Y, Moore PS, Said JW, Knowles DM (1995) Kaposi's sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas. N Engl J Med 332: 1186-1191.
3. Soulier J, Grollet L, Oksenhendler E, Cacoub P, Cazals-Hatem D, et al. (1995) Kaposi's sarcoma-associated herpesvirus-like DNA sequences in multicentric Castleman's disease. Blood 86: 1276-1280.
4. Bechtel JT, Liang Y, Hvidding J, Ganem D (2003) Host range of Kaposi's sarcoma-associated herpesvirus in cultured cells. J Virol 77: 6474-6481. (Pubitemid 36588417)
5. Zhong W, Wang H, Herndier B, Ganem D (1996) Restricted expression of Kaposi sarcoma-associated herpesvirus (human herpesvirus 8) genes in Kaposi sarcoma. Proc Natl Acad Sci U S A 93: 6641-6646. (Pubitemid 26230362)
6. Chen L, Lagunoff M (2005) Establishment and maintenance of Kaposi's sarcoma-associated herpesvirus latency in B cells. J Virol 79: 14383-14391. (Pubitemid 41552735)
7. Godfrey A, Anderson J, Papanastasiou A, Takeuchi Y, Boshoff C (2005) Inhibiting primary effusion lymphoma by lentiviral vectors encoding short hairpin RNA. Blood 105: 2510-2518. (Pubitemid 40387053)
8. Rainbow L, Platt GM, Simpson GR, Sarid R, Gao SJ, et al. (1997) The 222- to 234-kilodalton latent nuclear protein (LNA) of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) is encoded by orf73 and is a component of the latency-associated nuclear antigen. J Virol 71: 5915-5921. (Pubitemid 27304928)
9. Dupin N, Fisher C, Kellam P, Ariad S, Tulliez M, et al. (1999) Distribution of human herpesvirus-8 latently infected cells in Kaposi's sarcoma, multicentric Castleman's disease, and primary effusion lymphoma. Proc Natl Acad Sci U S A 96: 4546-4551. (Pubitemid 29190373)
10. Parravicini C, Chandran B, Corbellino M, Berti E, Paulli M, et al. (2000) Differential viral protein expression in Kaposi's sarcoma-associated herpesvirus-infected diseases: Kaposi's sarcoma, primary effusion lymphoma, and multicentric Castleman's disease. Am J Pathol 156: 743-749. (Pubitemid 30626930)
11. Lu F, Tsai K, Chen HS, Wikramasinghe P, Davuluri RV, et al. (2012) Identification of host-chromosome binding sites and candidate gene targets for Kaposi's sarcoma-associated herpesvirus LANA. J Virol 86: 5752-5762.
12. Friborg J, Jr., Kong W, Hottiger MO, Nabel GJ (1999) p53 inhibition by the LANA protein of KSHV protects against cell death. Nature 402: 889-894.
13. Kaul R, Verma SC, Robertson ES (2007) Protein complexes associated with the Kaposi's sarcoma-associated herpesvirus-encoded LANA. Virology 364: 317-329. (Pubitemid 46876687)
14. Cotter MA, 2nd, Robertson ES (1999) The latency-associated nuclear antigen tethers the Kaposi's sarcoma-associated herpesvirus genome to host chromosomes in body cavity-based lymphoma cells. Virology 264: 254-264.
15. De Leon Vazquez E, Kaye KM (2011) The internal Kaposi's sarcoma-associated herpesvirus LANA regions exert a critical role on episome persistence. J Virol 85: 7622-7633.
16. Barbera AJ, Chodaparambil JV, Kelley-Clarke B, Luger K, Kaye KM (2006) Kaposi's sarcoma-associated herpesvirus LANA hitches a ride on the chromosome. Cell Cycle 5: 1048-1052. (Pubitemid 43765297)
17. Lan K, Kuppers DA, Robertson ES (2005) Kaposi's sarcoma-associated herpesvirus reactivation is regulated by interaction of latency-associated nuclear antigen with recombination signal sequence-binding protein Jkappa, the major downstream effector of the Notch signaling pathway. J Virol 79: 3468-3478. (Pubitemid 40327935)
18. Lim C, Sohn H, Gwack Y, Choe J (2000) Latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus (human herpesvirus-8) binds ATF4/CREB2 and inhibits its transcriptional activation activity. J Gen Virol 81: 2645-2652.
19. Murakami Y, Yamagoe S, Noguchi K, Takebe Y, Takahashi N, et al. (2006) Ets-1-dependent expression of vascular endothelial growth factor receptors is activated by latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus through interaction with Daxx. J Biol Chem 281: 28113-28121. (Pubitemid 44414525)
20. Radkov SA, Kellam P, Boshoff C (2000) The latent nuclear antigen of Kaposi sarcoma-associated herpesvirus targets the retinoblastoma-E2F pathway and with the oncogene Hras transforms primary rat cells. Nat Med 6: 1121-1127.
21. Tang J, Gordon GM, Muller MG, Dahiya M, Foreman KE (2003) Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen induces expression of the helix-loop-helix protein Id-1 in human endothelial cells. J Virol 77: 5975-5984. (Pubitemid 36538988)
22. Verma SC, Borah S, Robertson ES (2004) Latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus up-regulates transcription of human telomerase reverse transcriptase promoter through interaction with transcription factor Sp1. J Virol 78: 10348-10359. (Pubitemid 39258360)
23. Fujimuro M, Hayward SD (2003) The latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus manipulates the activity of glycogen synthase kinase-3beta. J Virol 77: 8019-8030. (Pubitemid 36792798)
24. Krithivas A, Young DB, Liao G, Greene D, Hayward SD (2000) Human herpesvirus 8 LANA interacts with proteins of the mSin3 corepressor complex and negatively regulates Epstein-Barr virus gene expression in dually infected PEL cells. J Virol 74: 9637-9645.
25. Lim C, Gwack Y, Hwang S, Kim S, Choe J (2001) The transcriptional activity of cAMP response element-binding protein-binding protein is modulated by the latency associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus. J Biol Chem 276: 31016-31022.
26. Morgan DO (1995) Principles of CDK regulation. Nature 374: 131-134.
27. Elledge SJ (1996) Cell cycle checkpoints: preventing an identity crisis. Science 274: 1664-1672.
28. Hartwell LH, Kastan MB (1994) Cell cycle control and cancer. Science 266: 1821-1828.
29. Saha A, Kaul R, Murakami M, Robertson ES (2010) Tumor viruses and cancer biology: Modulating signaling pathways for therapeutic intervention. Cancer Biol Ther 10: 961-978.
30. Howe AK, Gaillard S, Bennett JS, Rundell K (1998) Cell cycle progression in monkey cells expressing simian virus 40 small t antigen from adenovirus vectors. J Virol 72: 9637-9644. (Pubitemid 28520827)
31. Lavia P, Mileo AM, Giordano A, Paggi MG (2003) Emerging roles of DNA tumor viruses in cell proliferation: new insights into genomic instability. Oncogene 22: 6508-6516. (Pubitemid 37372330)
32. Ben-Israel H, Kleinberger T (2002) Adenovirus and cell cycle control. Front Biosci 7: d1369-1395.
33. Southern SA, Herrington CS (2000) Disruption of cell cycle control by human papillomaviruses with special reference to cervical carcinoma. Int J Gynecol Cancer 10: 263-274.
34. Krauer KG, Burgess A, Buck M, Flanagan J, Sculley TB, et al. (2004) The EBNA-3 gene family proteins disrupt the G2/M checkpoint. Oncogene 23: 1342-1353. (Pubitemid 38406830)
35. 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. (Pubitemid 46878076)
36. Lapenna S, Giordano A (2009) Cell cycle kinases as therapeutic targets for cancer. Nat Rev Drug Discov 8: 547-566.
37. Gabrielli B, Brooks K, Pavey S (2012) Defective cell cycle checkpoints as targets for anti-cancer therapies. Front Pharmacol 3: 9.
38. Scholler A, Hong NJ, Bischer P, Reiners JJ, Jr. (1994) Short and long term effects of cytoskeleton-disrupting drugs on cytochrome P450 Cyp1a-1 induction in murine hepatoma 1c1c7 cells: suppression by the microtubule inhibitor nocodazole. Mol Pharmacol 45: 944-954. (Pubitemid 24155785)
39. Warrener R, Beamish H, Burgess A, Waterhouse NJ, Giles N, et al. (2003) Tumor cell-selective cytotoxicity by targeting cell cycle checkpoints. FASEB J 17: 1550-1552.
40. Verschuren EW, Jones N, Evan GI (2004) The cell cycle and how it is steered by Kaposi's sarcoma-associated herpesvirus cyclin. J Gen Virol 85: 1347-1361. (Pubitemid 38807731)
41. Liu L, Eby MT, Rathore N, Sinha SK, Kumar A, et al. (2002) The human herpes virus 8-encoded viral FLICE inhibitory protein physically associates with and persistently activates the Ikappa B kinase complex. J Biol Chem 277: 13745-13751. (Pubitemid 34967977)
42. Guttridge DC, Albanese C, Reuther JY, Pestell RG, Baldwin AS, Jr. (1999) NF-kappaB controls cell growth and differentiation through transcriptional regulation of cyclin D1. Mol Cell Biol 19: 5785-5799. (Pubitemid 29339933)
43. Ottinger M, Christalla T, Nathan K, Brinkmann MM, Viejo-Borbolla A, et al. (2006) Kaposi's sarcoma-associated herpesvirus LANA-1 interacts with the short variant of BRD4 and releases cells from a BRD4- and BRD2/RING3-induced G1 cell cycle arrest. J Virol 80: 10772-10786. (Pubitemid 44628923)
44. An FQ, Compitello N, Horwitz E, Sramkoski M, Knudsen ES, et al. (2005) The latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus modulates cellular gene expression and protects lymphoid cells from p16 INK4A-induced cell cycle arrest. J Biol Chem 280: 3862-3874. (Pubitemid 40223856)
45. Liu J, Martin HJ, Liao G, Hayward SD (2007) The Kaposi's sarcoma-associated herpesvirus LANA protein stabilizes and activates c-Myc. J Virol 81: 10451-10459. (Pubitemid 47463318)
46. Chen W, Hilton IB, Staudt MR, Burd CE, Dittmer DP (2010) Distinct p53, p53:LANA, and LANA complexes in Kaposi's Sarcoma-associated Herpesvirus Lymphomas. J Virol 84: 3898-3908.
47. Vahteristo P, Tamminen A, Karvinen P, Eerola H, Eklund C, et al. (2001) p53, CHK2, and CHK1 genes in Finnish families with Li-Fraumeni syndrome: further evidence of CHK2 in inherited cancer predisposition. Cancer Res 61: 5718-5722. (Pubitemid 32769084)
48. Spiller OB, Robinson M, O'Donnell E, Milligan S, Morgan BP, et al. (2003) Complement regulation by Kaposi's sarcoma-associated herpesvirus ORF4 protein. J Virol 77: 592-599. (Pubitemid 36004997)
49. Knight JS, Cotter MA, 2nd, Robertson ES (2001) The latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus transactivates the telomerase reverse transcriptase promoter. J Biol Chem 276: 22971-22978.
50. Enoch T, Nurse P (1990) Mutation of fission yeast cell cycle control genes abolishes dependence of mitosis on DNA replication. Cell 60: 665-673.
51. Kumagai A, Dunphy WG (1991) The cdc25 protein controls tyrosine dephosphorylation of the cdc2 protein in a cell-free system. Cell 64: 903-914. (Pubitemid 121001178)
52. Borgne A, Meijer L (1996) Sequential dephosphorylation of p34(cdc2) on Thr-14 and Tyr-15 at the prophase/metaphase transition. J Biol Chem 271: 27847-27854. (Pubitemid 26367361)
53. Agarwal C, Tyagi A, Agarwal R (2006) Gallic acid causes inactivating phosphorylation of cdc25A/cdc25C-cdc2 via ATM-Chk2 activation, leading to cell cycle arrest, and induces apoptosis in human prostate carcinoma DU145 cells. Mol Cancer Ther 5: 3294-3302. (Pubitemid 46092073)
54. Qiu L, Burgess A, Fairlie DP, Leonard H, Parsons PG, et al. (2000) Histone deacetylase inhibitors trigger a G2 checkpoint in normal cells that is defective in tumor cells. Mol Biol Cell 11: 2069-2083. (Pubitemid 30408065)
55. Darbon JM, Penary M, Escalas N, Casagrande F, Goubin-Gramatica F, et al. (2000) Distinct Chk2 activation pathways are triggered by genistein and DNA-damaging agents in human melanoma cells. J Biol Chem 275: 15363-15369. (Pubitemid 30337265)
56. Hirao A, Kong YY, Matsuoka S, Wakeham A, Ruland J, et al. (2000) DNA damage-induced activation of p53 by the checkpoint kinase Chk2. Science 287: 1824-1827.
57. Villa LL (1997) Human papillomaviruses and cervical cancer. Adv Cancer Res 71: 321-341.