Kaposi's sarcoma-associated herpesvirus-encoded LANA recruits topoisomerase IIβ for latent DNA replication of the terminal repeats

Journal of Virology

Volumn 86, Issue 18, 2012, Pages 9983-9994

  Purushothaman, Pravinkumar ^a   McDowell, Maria E ^a   McGuinness, James ^a   Salas, Ruth ^a   Rumjahn, Sharif M ^a   Verma, Subhash C ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

DNA TOPOISOMERASE (ATP HYDROLYSING); LATENCY ASSOCIATED NUCLEAR ANTIGEN; TOPOISOMERASE IIBETA; UNCLASSIFIED DRUG; VIRUS DNA;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; COMPLEX FORMATION; CONTROLLED STUDY; DNA REPLICATION; DNA STRAND BREAKAGE; EMBRYO; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; MOUSE; NONHUMAN; NUCLEOTIDE REPEAT; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; VIRUS LATENCY;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, VIRAL; BASE SEQUENCE; CELL LINE; CELL NUCLEUS; DNA REPLICATION; DNA TOPOISOMERASES, TYPE II; DNA, VIRAL; DNA-BINDING PROTEINS; ELLIPTICINES; HEK293 CELLS; HERPESVIRUS 8, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; MICE; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PROTEIN INTERACTION DOMAINS AND MOTIFS; TERMINAL REPEAT SEQUENCES; TOPOISOMERASE II INHIBITORS; VIRUS LATENCY;

HUMAN HERPESVIRUS 8;

EID: 84866176487     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00839-12     Document Type: Article

References (69)

1. An FQ, 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.
2. Ballestas ME, Chatis PA, Kaye KM. 1999. Efficient persistence of extra-chromosomal KSHV DNA mediated by latency-associated nuclear antigen. Science 284:641-644.
3. Ballestas ME, Kaye KM. 2001. Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen 1 mediates episome persistence through cis-acting terminal repeat (TR) sequence and specifically binds TR DNA. J. Virol. 75:3250-3258.
4. Ballestas ME, Kaye KM. 2011. The latency-associated nuclear antigen, a multifunctional protein central to Kaposi's sarcoma-associated herpesvirus latency. Future Microbiol. 6:1399-1413.
5. Barbera AJ, Ballestas ME, Kaye KM. 2004. The Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen 1 N terminus is essential for chromosome association,DNAreplication, and episome persistence. J. Virol. 78:294-301.
6. Barbera AJ, et al. 2006. The nucleosomal surface as a docking station for Kaposi's sarcoma herpesvirus LANA. Science 311:856-861.
7. Cai Q, Verma SC, Choi JY, Ma M, Robertson ES. 2010. Kaposi's sarcoma-associated herpesvirus inhibits interleukin-4-mediated STAT6 phosphorylation to regulate apoptosis and maintain latency. J. Virol. 84:11134-11144.
8. Cai Q, Verma SC, Lu J, Robertson ES. 2010. Molecular biology of Kaposi's sarcoma-associated herpesvirus and related oncogenesis. Adv. Virus Res. 78:87-142.
9. Cai Q, et al. 2012. Kaposi's sarcoma herpesvirus upregulates aurora A expression to promote p53 phosphorylation and ubiquitylation. PLoS Pathog. 8:e1002566. doi:10.1371/journal.ppat.1002566.
10. Cannon JS, et al. 2000. A new primary effusion lymphoma-derived cell line yields a highly infectious Kaposi's sarcoma herpesvirus-containing supernatant. J. Virol. 74:10187-10193.
11. 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.
12. Chang Y, et al. 1994. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 266:1865-1869.
13. Chen W, Hilton IB, Staudt MR, Burd CE, Dittmer DP. 2010. Distinct p53, p53:LANA, and LANA complexes in Kaposi's s-associated herpesvirus lymphomas. J. Virol. 84:3898-3908.
14. Cotter MA, II, 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. Cowell IG, Papageorgiou N, Padget K, Watters GP, Austin CA. 2011. Histone deacetylase inhibition redistributes topoisomerase IIbeta from heterochromatin to euchromatin. Nucleus 2:61-71.
16. Fakhari FD, Dittmer DP. 2002. Charting latency transcripts in Kaposi's sarcoma-associated herpesvirus by whole-genome real-time quantitative PCR. J. Virol. 76:6213-6223.
17. 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.
18. Garber AC, Shu MA, Hu J, Renne R. 2001. DNA binding and modulation of gene expression by the latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus. J. Virol. 75:7882-7892.
19. Gonzalez-Molleda L, Wang Y, Yuan Y. 2012. Potent antiviral activity of topoisomerase I and II inhibitors against Kaposi's sarcoma-associated herpesvirus. Antimicrob. Agents Chemother. 56:893-902.
20. Grundhoff A, Ganem D. 2004. Inefficient establishment of KSHV latency suggests an additional role for continued lytic replication in Kaposi sarcoma pathogenesis. J. Clin. Invest. 113:124-136.
21. Hirt B. 1967. Selective extraction of polyoma DNA from infected mouse cell cultures. J. Mol. Biol. 26:365-369.
22. Hu J, Garber AC, Renne R. 2002. The latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus supports latent DNA replication in dividing cells. J. Virol. 76:11677-11687.
23. Hu J, Renne R. 2005. Characterization of the minimal replicator of Kaposi's sarcoma-associated herpesvirus latent origin. J. Virol. 79:2637-2642.
24. Jenner RG, Alba MM, Boshoff C, Kellam P. 2001. Kaposi's sarcoma-associated herpesvirus latent and lytic gene expression as revealed by DNA arrays. J. Virol. 75:891-902.
25. Ju BG, et al. 2006. A topoisomerase IIbeta-mediated dsDNA break required for regulated transcription. Science 312:1798-1802.
26. Kaul R, Verma SC, Robertson ES. 2007. Protein complexes associated with the Kaposi's sarcoma-associated herpesvirus-encoded LANA. Virology 364:317-329.
27. Komatsu T, Ballestas ME, Barbera AJ, Kelley-Clarke B, Kaye KM. 2004. KSHV LANA1 binds DNA as an oligomer and residues N-terminal to the oligomerization domain are essential for DNA binding, replication, and episome persistence. Virology 319:225-236.
28. Lan K, et al. 2005. Induction of Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen by the lytic transactivator RTA: a novel mechanism for establishment of latency. J. Virol. 79:7453-7465.
29. Lee HR, Lee S, Chaudhary PM, Gill P, Jung JU. 2010. Immune evasion by Kaposi's sarcoma-associated herpesvirus. Future Microbiol. 5:1349-1365.
30. 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.
31. Lim C, Sohn H, Lee D, Gwack Y, Choe J. 2002. Functional dissection of latency-associated nuclear antigen 1 of Kaposi's sarcoma-associated herpesvirus involved in latent DNA replication and transcription of terminal repeats of the viral genome. J. Virol. 76:10320-10331.
32. Lu F, Day L, Gao SJ, Lieberman PM. 2006. Acetylation of the latency-associated nuclear antigen regulates repression of Kaposi's sarcoma-associated herpesvirus lytic transcription. J. Virol. 80:5273-5282.
33. Lu F, 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.
34. Lu J, et al. 2012. The RBP-Jkappa binding sites within the RTA promoter regulate KSHV latent infection and cell proliferation. PLoS Pathog. 8:e1002479. doi:10.1371/journal.ppat.1002479.
35. Lu J, 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.
36. Lyu YL, et al. 2007. Topoisomerase IIbeta mediated DNA double-strand breaks: implications in doxorubicin cardiotoxicity and prevention by dexrazoxane. Cancer Res. 67:8839-8846.
37. Matsumura S, Persson LM, Wong L, Wilson AC. 2010. The latency-associated nuclear antigen interacts with MeCP2 and nucleosomes through separate domains. J. Virol. 84:2318-2330.
38. Mesri EA, Cesarman E, Boshoff C. 2010. Kaposi's sarcoma and its associated herpesvirus. Nat. Rev. Cancer 10:707-719.
39. Mirski SE, et al. 2007. Topoisomerase II binds importin alpha isoforms and exportin/CRM1 but does not shuttle between the nucleus and cytoplasm in proliferating cells. Exp. Cell Res. 313:627-637.
40. Moore PS, Chang Y. 2010. Why do viruses cause cancer? Highlights of the first century of human tumour virology. Nat. Rev. Cancer 10:878-889.
41. Moore PS, Chang Y. 2003. Kaposi's sarcoma-associated herpesvirus immunoevasion and tumorigenesis: two sides of the same coin? Annu. Rev. Microbiol. 57:609-639.
42. Ohsaki E, Ueda K. 2012. Kaposi's sarcoma-associated herpesvirus genome replication, partitioning, and maintenance in latency. Front. Microbiol. 3:7. doi:10.3389/fmicb.2012.00007.
43. 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.
44. Rainbow L, 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.
45. Renne R, et al. 2001. Modulation of cellular and viral gene expression by the latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus. J. Virol. 75:458-468.
46. Renne R, et al. 1996. Lytic growth of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) in culture. Nat. Med. 2:342-346.
47. Riccardi C, Nicoletti I. 2006. Analysis of apoptosis by propidium iodide staining and flow cytometry. Nat. Protoc. 1:1458-1461.
48. Rossetto C, Yamboliev I, Pari GS. 2009. Kaposi's sarcoma-associated herpesvirus/human herpesvirus 8 K-bZIP modulates latency-associated nuclear protein-mediated suppression of lytic origin-dependent DNA synthesis. J. Virol. 83:8492-8501.
49. 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.
50. Sakakibara S, et al. 2004. Accumulation of heterochromatin components on the terminal repeat sequence of Kaposi's sarcoma-associated herpesvirus mediated by the latency-associated nuclear antigen. J. Virol. 78:7299-7310.
51. Schwam DR, Luciano RL, Mahajan SS, Wong L, Wilson AC. 2000. Carboxy terminus of human herpesvirus 8 latency-associated nuclear antigen mediates dimerization, transcriptional repression, and targeting to nuclear bodies. J. Virol. 74:8532-8540.
52. Si H, Robertson ES. 2006. Kaposi's sarcoma-associated herpesvirusencoded latency-associated nuclear antigen induces chromosomal instability through inhibition of p53 function. J. Virol. 80:697-709.
53. Si H, Verma SC, Robertson ES. 2006. Proteomic analysis of the Kaposi's sarcoma-associated herpesvirus terminal repeat element binding proteins. J. Virol. 80:9017-9030.
54. Skalsky RL, Hu J, Renne R. 2007. Analysis of viral cis elements conferring Kaposi's sarcoma-associated herpesvirus episome partitioning and maintenance. J. Virol. 81:9825-9837.
55. Stedman W, Deng Z, Lu F, Lieberman PM. 2004. ORC, MCM, and histone hyperacetylation at the Kaposi's sarcoma-associated herpesvirus latent replication origin. J. Virol. 78:12566-12575.
56. Tsutsui K, Sano K, Kikuchi A, Tokunaga A. 2001. Involvement of DNA topoisomerase IIbeta in neuronal differentiation. J. Biol. Chem. 276:5769-5778.
57. Ueda K, Sakakibara S, Ohsaki E, Yada K. 2006. Lack of a mechanism for faithful partition and maintenance of the KSHV genome. Virus Res. 122:85-94.
58. Verma SC, et al. 2006. Latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus recruits uracil DNA glycosylase 2 at the terminal repeats and is important for latent persistence of the virus. J. Virol. 80:11178-11190.
59. Verma SC, Choudhuri T, Kaul R, Robertson ES. 2006. Latency-associated nuclear antigen (LANA) of Kaposi's sarcoma-associated herpesvirus interacts with origin recognition complexes at the LANA binding sequence within the terminal repeats. J. Virol. 80:2243-2256.
60. Verma SC, Choudhuri T, Robertson ES. 2007. The minimal replicator element of the Kaposi's sarcoma-associated herpesvirus terminal repeat supports replication in a semiconservative and cell-cycle-dependent manner. J. Virol. 81:3402-3413.
61. Verma SC, Lan K, Choudhuri T, Cotter MA, Robertson ES. 2007. An autonomous replicating element within the KSHV genome. Cell Host Microbe 2:106-118.
62. Verma SC, Lan K, Choudhuri T, Robertson ES. 2006. Kaposi's sarcoma-associated herpesvirus-encoded latency-associated nuclear antigen modulates K1 expression through its cis-acting elements within the terminal repeats. J. Virol. 80:3445-3458.
63. Verma SC, Lan K, Robertson E. 2007. Structure and function of latency-associated nuclear antigen. Curr. Top. Microbiol. Immunol. 312:101-136.
64. Verma SC, Robertson ES. 2003. Molecular biology and pathogenesis of Kaposi sarcoma-associated herpesvirus. FEMS Microbiol. Lett. 222:155-163.
65. Viejo-Borbolla A, et al. 2005. Brd2/RING3 interacts with a chromatinbinding domain in the Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen 1 (LANA-1) that is required for multiple functions of LANA-1. J. Virol. 79:13618-13629.
66. Wang CY, Sugden B. 2004. New viruses shake old paradigms. J. Clin. Invest. 113:21-23.
67. Wang Y, Li H, Tang Q, Maul GG, Yuan Y. 2008. Kaposi's sarcoma-associated herpesvirus ori-Lyt-dependent DNA replication: involvement of host cellular factors. J. Virol. 82:2867-2882.
68. Xiao B, et al. 2010. Bub1 and CENP-F can contribute to Kaposi's sarcoma-associated herpesvirus genome persistence by targeting LANA to kinetochores. J. Virol. 84:9718-9732.
69. 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.