Molecular Basis for Oligomeric-DNA Binding and Episome Maintenance by KSHV LANA

PLoS Pathogens

Volumn 9, Issue 10, 2013, Pages

  Domsic, John F ^a   Chen, Horng Shen ^a   Lu, Fang ^a   Marmorstein, Ronen ^a   Lieberman, Paul M ^a  

^a WISTAR INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BROMODOMAIN CONTAINING PROTEIN 2; BROMODOMAIN CONTAINING PROTEIN 4; LATENCY ASSOCIATED NUCLEAR ANTIGEN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANTIGEN EXPRESSION; ANTIGEN PURIFICATION; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; DNA BINDING; DNA EXTRACTION; DNA REPLICATION; EPISOME; FLUORESCENCE POLARIZATION; GEL MOBILITY SHIFT ASSAY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; IMMUNOBLOTTING; IMMUNOPRECIPITATION; NONHUMAN; OLIGOMERIZATION; PROTEIN ANALYSIS; PROTEIN CROSS LINKING; SOUTHERN BLOTTING; VIRUS REPLICATION;

ANTIGENS, VIRAL; CELL LINE, TUMOR; DNA REPLICATION; DNA, VIRAL; HERPESVIRUS 8, HUMAN; HUMANS; NUCLEAR PROTEINS; PLASMIDS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84887279018     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003672     Document Type: Article

References (65)

1. 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. The New England Journal of Medicine 332: 1186-1191.
2. 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 (New York, NY) 266: 1865-1869.
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. Ballestas ME, Chatis PA, Kaye KM, (1999) Efficient persistence of extrachromosomal KSHV DNA mediated by latency-associated nuclear antigen. Science 284: 641-644.
5. 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 [In Process Citation]. Virology 264: 254-264.
6. Lieberman PM, Hu J, Renne R, (2007) Maintenance and replication during latency. Human Herpesviruses:Biology, Therapy, and Immunoprophylaxis Ch. 24: 379-402.
7. 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.
8. Collins CM, Medveczky PG, (2002) Genetic requirements for the episomal maintenance of oncogenic herpesvirus genomes. Advances in Cancer Research 84: 155-174.
9. Grundhoff A, Ganem D, (2003) The latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesesvirus permits replication of terminal repeat-containing plasmids. Journal of Virology 77: 2779-2783.
10. Garber AC, Hu J, Renne R, (2002) Latency-associated Nuclear Antigen (LANA) Cooperatively Binds to Two Sites within the Terminal Repeat, and Both Sites Contribute to the Ability of LANA to Suppress Transcription and to Facilitate DNA Replication. J Biol Chem 277: 27401-27411.
11. Hu J, Garber AC, Renne R, (2002) Analysis of cis-and trans-requirements of LANA-dependent DNA replication in dividing cells,. J Virol 76: 11677-11668.
12. 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.
13. 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.
14. Sarid R, Flore O, Bohenzky RA, Chang Y, Moore PS, (1998) Transcription mapping of the Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) genome in a body cavity-based lymphoma cell line (BC-1). J Virol 72: 1005-1012.
15. 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.
16. 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. Journal of Virology 75: 3250-3258.
17. 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.
18. 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.
19. 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.
20. Verma SC, Lan K, Robertson E, (2007) Structure and function of latency-associated nuclear antigen. Curr Top Microbiol Immunol 312: 101-136.
21. Lan K, Kuppers DA, Verma SC, Robertson ES, (2004) Kaposi's Sarcoma-Associated Herpesvirus-Encoded Latency-Associated Nuclear Antigen Inhibits Lytic Replication by Targeting Rta: a Potential Mechanism for Virus-Mediated Control of Latency. J Virol 78: 6585-6594.
22. 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.
23. 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.
24. 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.
25. Platt GM, Simpson GR, Mittnacht S, Schulz TF, (1999) Latent nuclear antigen of Kaposi's sarcoma-associated herpesvirus interacts with RING3, a homolog of the drosophila female sterile homeotic (fsh) gene [In Process Citation]. J Virol 73: 9789-9795.
26. 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.
27. Krithivas A, Fujimuro M, Weidner M, Young DB, Hayward SD, (2002) Protein interactions targeting the latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus to cell chromosomes. J Virol 76: 11596-11604.
28. Mattsson K, Kiss C, Platt GM, Simpson GR, Kashuba E, et al. (2002) Latent nuclear antigen of Kaposi's sarcoma herpesvirus/human herpesvirus-8 induces and relocates RING3 to nuclear heterochromatin regions. Journal of General Virology 83: 179-188.
29. Barbera AJ, Chodaparambil JV, Kelley-Clarke B, Joukov V, Walter JC, et al. (2006) The nucleosomal surface as a docking station for Kaposi's sarcoma herpesvirus LANA. Science 311: 856-861.
30. Matsumura S, Persson LM, Wong L, Wilson AC, (2009) The latency-associated nuclear antigen interacts with MeCP2 and nucleosomes through separate domains. J Virol 84: 2318-2330.
31. Sarek G, Jarviluoma A, Moore HM, Tojkander S, Vartia S, et al. (2010) Nucleophosmin phosphorylation by v-cyclin-CDK6 controls KSHV latency. PLoS Pathog 6: e1000818.
32. Xiao B, Verma SC, Cai Q, Kaul R, Lu J, 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.
33. Jager W, Santag S, Weidner-Glunde M, Gellermann E, Kati S, et al. (2012) The ubiquitin-specific protease USP7 modulates the replication of Kaposi's sarcoma-associated herpesvirus latent episomal DNA. J Virol 86: 6745-6757.
34. Cotter MA 2nd, Subramanian C, Robertson ES, (2001) The Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen binds to specific sequences at the left end of the viral genome through its carboxy-terminus. Virology 291: 241-259.
35. 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.
36. Fejer G, Medveczky MM, Horvath E, Lane B, Chang Y, et al. (2003) The latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus interacts preferentially with the terminal repeats of the genome in vivo and this complex is sufficient for episomal DNA replication. Journal of General Virology 84: 1451-1462.
37. 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.
38. Hu J, Renne R, (2005) Characterization of the minimal replicator of Kaposi's sarcoma-associated herpesvirus latent origin. J Virol 79: 2637-2642.
39. Hegde RS, Grossman SR, Laimins LA, Sigler PB, (1992) Crystal structure at 1.7 A of the bovine papillomavirus-1 E2 DNA-binding domain bound to its DNA target. Nature 359: 505-512.
40. Kelley-Clarke B, Ballestas ME, Srinivasan V, Barbera AJ, Komatsu T, et al. (2007) Determination of Kaposi's Sarcoma-Associated Herpesvirus C-Terminal Latency-Associated Nuclear Antigen Residues Mediating Chromosome Association and DNA Binding. Journal of Virology 81: 4348-4356.
41. Androphy EJ, Lowy DR, Schiller JT, (1987) Bovine papillomavirus E2 trans-activating gene product binds to specific sites in papillomavirus DNA. Nature 325: 70-73.
42. Garber AC, Hu J, Renne R, (2002) Latency-associated Nuclear Antigen (LANA) Cooperatively Binds to Two Sites within the Terminal Repeat, and Both Sites Contribute to the Ability of LANA to Suppress Transcription and to Facilitate DNA Replication. Journal of Biological Chemistry 277: 27401-27411.
43. Rawlins DR, Milman G, Hayward SD, Hayward GS, (1985) Sequence-specific DNA binding of the Epstein-Barr virus nuclear antigen (EBNA-1) to clustered sites in the plasmid maintenance region. Cell 42: 859-868.
44. Srinivasan V, Komatsu T, Ballestas ME, Kaye KM, (2004) Definition of sequence requirements for latency-associated nuclear antigen 1 binding to Kaposi's sarcoma-associated herpesvirus DNA. J Virol 78: 14033-14038.
45. Lagunoff M, Ganem D, (1997) The structure and coding organization of the genomic termini of Kaposi's sarcoma-associated herpesvirus. Virology 236: 147-154.
46. Barbera AJ, Chodaparambil JV, Kelley-Clarke B, Joukov V, Walter JC, et al. (2006) The nucleosomal surface as a docking station for Kaposi's sarcoma herpesvirus LANA. Science (New York, NY) 311: 856-861.
47. Piolot T, Tramier M, Coppey M, Nicolas J-C, Marechal V, (2001) Close but Distinct Regions of Human Herpesvirus 8 Latency-Associated Nuclear Antigen 1 Are Responsible for Nuclear Targeting and Binding to Human Mitotic Chromosomes. Journal of Virology 75: 3948-3959.
48. Shamay M, Liu J, Li R, Liao G, Shen L, et al. (2012) A Protein Array Screen for KSHV LANA Interactors Links LANA to TIP60, PP2A activity and Telomere Shortening. J Virol doi:10.1128/JVI.00169-12.
49. Woodard C, Shamay M, Liao G, Zhu J, Ng AN, et al. (2012) Phosphorylation of the Chromatin Binding Domain of KSHV LANA. PLoS Pathog 8: e1002972.
50. 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.
51. Wu SY, Chiang CM, (2007) The double bromodomain-containing chromatin adaptor Brd4 and transcriptional regulation. J Biol Chem 282: 13141-13145.
52. Sanchez R, Zhou MM, (2009) The role of human bromodomains in chromatin biology and gene transcription. Curr Opin Drug Discov Devel 12: 659-665.
53. 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. Journal of Virology 80: 10772-10786.
54. Viejo-Borbolla A, Ottinger M, Brüning E, Bürger A, König R, et al. (2005) Brd2/RING3 interacts with a chromatin-binding domain in the Kaposi's Sarcoma-associated herpesvirus latency-associated nuclear antigen 1 (LANA-1) that is required for multiple functions of LANA-1. Journal of Virology 79: 13618-13629.
55. Bochkarev A, Barwell JA, Pfuetzner RA, Furey W Jr, Edwards AM, et al. (1995) Crystal structure of the DNA-binding domain of the Epstein-Barr virus origin-binding protein EBNA 1. Cell 83: 39-46.
56. Han S-J, Hu J, Pierce B, Weng Z, Renne R, (2010) Mutational analysis of the latency-associated nuclear antigen DNA-binding domain of Kaposi's sarcoma-associated herpesvirus reveals structural conservation among gammaherpesvirus origin-binding proteins. Journal of General Virology 91: 2203-2215.
57. Summers H, Barwell JA, Pfuetzner RA, Edwards AM, Frappier L, (1996) Cooperative assembly of EBNA1 on the Epstein-Barr virus latent origin of replication. J Virol 70: 1228-1231.
58. Bashaw JM, Yates JL, (2001) Replication from oriP of Epstein-Barr virus requires exact spacing of two bound dimers of EBNA1 which bend DNA. J Virol 75: 10603-10611.
59. Bochkarev A, Bochkareva E, Frappier L, Edwards AM, (1998) The 2.2 Å structure of a permanganate-sensitive DNA site bound by the epstein-barr virus origin binding protein, EBNA1. Journal of Molecular Biology 284: 1273-1278.
60. Wong L-Y, Wilson AC, (2005) Kaposi's Sarcoma-Associated Herpesvirus Latency-Associated Nuclear Antigen Induces a Strong Bend on Binding to Terminal Repeat DNA. Journal of Virology 79: 13829-13836.
61. Frappier L, Goldsmith K, Bendell L, (1994) Stabilization of the EBNA1 protein on the Epstein-Barr virus latent origin of DNA replication by a DNA looping mechanism. J Biol Chem 269: 1057-1062.
62. Gai D, Zhao R, Li D, Finkielstein CV, Chen XS, (2004) Mechanisms of conformational change for a replicative hexameric helicase of SV40 large tumor antigen. Cell 119: 47-60.
63. Schuck S, Stenlund A, (2005) Assembly of a double hexameric helicase. Mol Cell 20: 377-389.
64. Ou HD, Kwiatkowski W, Deerinck TJ, Noske A, Blain KY, et al. (2012) A structural basis for the assembly and functions of a viral polymer that inactivates multiple tumor suppressors. Cell 151: 304-319.
65. Lu F, Tsai K, Chen H-S, Wikramasinghe P, Davuluri RV, et al. (2012) Identification of Host-Chromosome Binding Sites and Candidate Gene Targets for Kaposi's Sarcoma-Associated Herpesvirus LANA. Journal of Virology 86: 5752-5762.