Kaposi's sarcoma-Associated herpesvirus (KSHV) latency-Associated nuclear antigen regulates the KSHV epigenome by association with the histone demethylase KDM3A

Journal of Virology

Volumn 87, Issue 12, 2013, Pages 6782-6793

  Kim, Kevin Y ^a   Huerta, Steve B ^a   Izumiya, Chie ^b   Wang, Don Hong ^a   Martinez, Anthony ^b   Shevchenko, Bogdan ^a   Kung, Hsing Jien ^a,b   Campbell, Mel ^a   Izumiya, Yoshihiro ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEMETHYLASE; HISTONE H3; LATENCY ASSOCIATED NUCLEAR ANTIGEN; PROTEIN KDM3A; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO; EPIGENETICS; GENE CONTROL; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; HISTONE METHYLATION; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; VIRUS GENE; VIRUS GENOME; VIRUS LATENCY; VIRUS REACTIVATION; VIRUS REPLICATION;

ANTIGENS, VIRAL; CHROMATIN IMMUNOPRECIPITATION; DNA REPLICATION; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, VIRAL; GENOME, VIRAL; HEK293 CELLS; HELA CELLS; HERPESVIRUS 8, HUMAN; HISTONES; HOST-PATHOGEN INTERACTIONS; HUMANS; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; NUCLEAR PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; VIRUS LATENCY;

HUMAN HERPESVIRUS 8;

EID: 84878175808     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00011-13     Document Type: Article

References (66)

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. N. Engl. J. Med. 332:1186-1191.
2. Dupin N, Fisher C, Kellam P, Ariad S, Tulliez M, Franck N, van Marck E, Salmon D, Gorin I, Escande JP, Weiss RA, Alitalo K, Boshoff C. 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.
3. 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.
4. Kelley-Clarke B, De Leon-Vazquez E, Slain K, Barbera AJ, Kaye KM. 2009. Role of Kaposi's sarcoma-associated herpesvirus C-terminal LANA chromosome binding in episome persistence. J. Virol. 83:4326-4337.
5. Kelley-Clarke B, Ballestas ME, Komatsu T, Kaye KM. 2007. Kaposi's sarcoma herpesvirus C-terminal LANA concentrates at pericentromeric and peri-telomeric regions of a subset of mitotic chromosomes. Virology 357:149-157.
6. 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.
7. Ye FC, Zhou FC, Yoo SM, Xie JP, Browning PJ, Gao SJ. 2004. Disruption of Kaposi's sarcoma-associated herpesvirus latent nuclear antigen leads to abortive episome persistence. J. Virol. 78:11121-11129.
8. Ganem D. 2010. KSHV and the pathogenesis of Kaposi sarcoma: listening to human biology and medicine. J. Clin. Invest. 120:939-949.
9. Mesri EA, Cesarman E, Boshoff C. 2010. Kaposi's sarcoma and its associated herpesvirus. Nat. Rev. Cancer 10:707-719.
10. Verma SC, Lan K, Robertson E. 2007. Structure and function of latencyassociated nuclear antigen. Curr. Top. Microbiol. Immunol. 312:101-136.
11. Schulz TF. 2001. KSHV/HHV8-associated lymphoproliferations in the AIDS setting. Eur. J. Cancer 37:1217-1226.
12. Kedes DH, Lagunoff M, Renne R, Ganem D. 1997. Identification of the gene encoding the major latency-associated nuclear antigen of the Kaposi's sarcoma-associated herpesvirus. J. Clin. Invest. 100:2606-2610.
13. Renne R, Barry C, Dittmer D, Compitello N, Brown PO, Ganem D. 2001. Modulation of cellular and viral gene expression by the latencyassociated nuclear antigen of Kaposi's sarcoma-associated herpesvirus. J. Virol. 75:458-468.
14. An FQ, Compitello N, Horwitz E, Sramkoski M, Knudsen ES, Renne R. 2005. The latency-associated nuclear antigen of Kaposi's sarcomaassociated herpesvirus modulates cellular gene expression and protects lymphoid cells from p16 INK4A-induced cell cycle arrest. J. Biol. Chem. 280:3862-3874.
15. Jeong JH, Orvis J, Kim JW, McMurtrey CP, Renne R, Dittmer DP. 2004. Regulation and autoregulation of the promoter for the latencyassociated nuclear antigen of Kaposi's sarcoma-associated herpesvirus. J. Biol. Chem. 279:16822-16831.
16. 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.
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. 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.
19. Murakami Y, Yamagoe S, Noguchi K, Takebe Y, Takahashi N, Uehara Y, Fukazawa H. 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.
20. 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. J. Virol. 73:9789-9795.
21. 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 sarcomaassociated herpesvirus. J. Biol. Chem. 276:31016-31022.
22. 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.
23. Lu F, Day L, Gao SJ, Lieberman PM. 2006. Acetylation of the latencyassociated nuclear antigen regulates repression of Kaposi's sarcomaassociated herpesvirus lytic transcription. J. Virol. 80:5273-5282.
24. Lan K, Kuppers DA, Verma SC, Robertson ES. 2004. Kaposi's sarcomaassociated herpesvirus-encoded latency-associated nuclear antigen inhibits lytic replication by targeting Rta: a potential mechanism for virusmediated control of latency. J. Virol. 78:6585-6594.
25. 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.
26. Ottinger M, Christalla T, Nathan K, Brinkmann MM, Viejo-Borbolla A, Schulz TF. 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.
27. Sakakibara S, Ueda K, Nishimura K, Do E, Ohsaki E, Okuno T, Yamanishi K. 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.
28. Ellison TJ, Izumiya Y, Izumiya C, Luciw PA, Kung HJ. 2009. A comprehensive analysis of recruitment and transactivation potential of K-Rta and K-bZIP during reactivation of Kaposi's sarcoma-associated herpesvirus. Virology 387:76-88.
29. Gunther T, Grundhoff A. 2010. The epigenetic landscape of latent Kaposi sarcoma-associated herpesvirus genomes. PLoS Pathog. 6:e1000935. doi: 10.1371/journal.ppat.1000935.
30. Toth Z, Maglinte DT, Lee SH, Lee HR, Wong LY, Brulois KF, Lee S, Buckley JD, Laird PW, Marquez VE, Jung JU. 2010. Epigenetic analysis of KSHV latent and lytic genomes. PLoS Pathog. 6:e1001013. doi:10.1371 /journal.ppat.1001013.
31. Pedersen MT, Helin K. 2010. Histone demethylases in development and disease. Trends Cell Biol. 20:662-671.
32. Yamane K, Toumazou C, Tsukada Y, Erdjument-Bromage H, Tempst P, Wong J, Zhang Y. 2006. JHDM2A, a JmjC-containing H3K9 demethylase, facilitates transcription activation by androgen receptor. Cell 125: 483-495.
33. Shi Y, Whetstine JR. 2007. Dynamic regulation of histone lysine methylation by demethylases. Mol. Cell 25:1-14.
34. Krieg AJ, Rankin EB, Chan D, Razorenova O, Fernandez S, Giaccia AJ. 2010. Regulation of the histone demethylase JMJD1A by hypoxiainducible factor 1 alpha enhances hypoxic gene expression and tumor growth. Mol. Cell. Biol. 30:344-353.
35. Shakya A, Kang J, Chumley J, Williams MA, Tantin D. 2011. Oct1 is a switchable, bipotential stabilizer of repressed and inducible transcriptional states. J. Biol. Chem. 286:450-459.
36. Liang Y, Vogel JL, Narayanan A, Peng H, Kristie TM. 2009. Inhibition of the histone demethylase LSD1 blocks alpha-herpesvirus lytic replication and reactivation from latency. Nat. Med. 15:1312-1317.
37. Anderton JA, Bose S, Vockerodt M, Vrzalikova K, Wei W, Kuo M, Helin K, Christensen J, Rowe M, Murray PG, Woodman CB. 2011. The H3K27me3 demethylase, KDM6B, is induced by Epstein-Barr virus and over-expressed in Hodgkin's lymphoma. Oncogene 30:2037-2043.
38. Chang PC, Fitzgerald LD, Hsia DA, Izumiya Y, Wu CY, Hsieh WP, Lin SF, Campbell M, Lam KS, Luciw PA, Tepper CG, Kung HJ. 2011. Histone demethylase JMJD2A regulates Kaposi's sarcoma-associated herpesvirus replication and is targeted by a viral transcriptional factor. J. Virol. 85:3283-3293.
39. Nakamura H, Lu M, Gwack Y, Souvlis J, Zeichner SL, Jung JU. 2003. Global changes in Kaposi's sarcoma-associated virus gene expression patterns following expression of a tetracycline-inducible Rta transactivator. J. Virol. 77:4205-4220.
40. Vieira J, O'Hearn PM. 2004. Use of the red fluorescent protein as a marker of Kaposi's sarcoma-associated herpesvirus lytic gene expression. Virology 325:225-240.
41. Izumiya Y, Ellison TJ, Yeh ET, Jung JU, Luciw PA, Kung HJ. 2005. Kaposi's sarcoma-associated herpesvirus K-bZIP represses gene transcription via SUMO modification. J. Virol. 79:9912-9925.
42. Izumiya Y, Izumiya C, Hsia D, Ellison TJ, Luciw PA, Kung HJ. 2009. NF-kappaB serves as a cellular sensor of Kaposi's sarcoma-associated herpesvirus latency and negatively regulates K-Rta by antagonizing the RBPJkappa coactivator. J. Virol. 83:4435-4446.
43. Campbell M, Chang PC, Huerta S, Izumiya C, Davis R, Tepper CG, Kim KY, Shevchenko B, Wang DH, Jung JU, Luciw PA, Kung HJ, Izumiya Y. 2012. Protein arginine methyltransferase 1-directed methylation of Kaposi sarcoma-associated herpesvirus latency-associated nuclear antigen. J. Biol. Chem. 287:5806-5818.
44. Izumiya Y, Izumiya C, Van Geelen A, Wang DH, Lam KS, Luciw PA, Kung HJ. 2007. Kaposi's sarcoma-associated herpesvirus-encoded protein kinase and its interaction with K-bZIP. J. Virol. 81:1072-1082.
45. 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.
46. Xu X, Hoang S, Mayo MW, Bekiranov S. 2010. Application of machine learning methods to histone methylation ChIP-Seq data reveals H4R3me2 globally represses gene expression. BMC Bioinformatics 11:396. doi:10 .1186/1471-2105-11-396.
47. Antonysamy S, Bonday Z, Campbell RM, Doyle B, Druzina Z, Gheyi T, Han B, Jungheim LN, Qian Y, Rauch C, Russell M, Sauder JM, Wasserman SR, Weichert K, Willard FS, Zhang A, Emtage S. 2012. Crystal structure of the human PRMT5:MEP50 complex. Proc. Natl. Acad. Sci. U. S. A. 109:17960-17965.
48. Stewart MD, Li J, Wong J. 2005. Relationship between histone H3 lysine 9 methylation, transcription repression, and heterochromatin protein 1 recruitment. Mol. Cell. Biol. 25:2525-2538.
49. Collins RE, Northrop JP, Horton JR, Lee DY, Zhang X, Stallcup MR, Cheng X. 2008. The ankyrin repeats of G9a and GLP histone methyltransferases are mono-and dimethyllysine binding modules. Nat. Struct. Mol. Biol. 15:245-250.
50. Stuber G, Mattsson K, Flaberg E, Kati E, Markasz L, Sheldon JA, Klein G, Schulz TF, Szekely L. 2007. HHV-8 encoded LANA-1 alters the higher organization of the cell nucleus. Mol. Cancer 6:28. doi:10.1186/1476-4598-6-28.
51. Campbell M, Izumiya Y. 2012. Post-translational modifications of Kaposi's sarcoma-associated herpesvirus regulatory proteins-SUMO and KSHV. Front. Microbiol. 3:31. doi:10.3389/fmicb.2012.00031.
52. Lu F, Tsai K, Chen HS, Wikramasinghe P, Davuluri RV, Showe L, Domsic J, Marmorstein R, Lieberman PM. 2012. Identification of hostchromosome binding sites and candidate gene targets for Kaposi's sarcoma-associated herpesvirus LANA. J. Virol. 86:5752-5762.
53. Wen KW, Dittmer DP, Damania B. 2009. Disruption of LANA in rhesus rhadinovirus generates a highly lytic recombinant virus. J. Virol. 83:9786-9802.
54. Li Q, Zhou F, Ye F, Gao SJ. 2008. Genetic disruption of KSHV major latent nuclear antigen LANA enhances viral lytic transcriptional program. Virology 379:234-244.
55. Chen W, Dittmer DP. 2011. Ribosomal protein S6 interacts with the latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus. J. Virol. 85:9495-9505.
56. Barbera AJ, Chodaparambil JV, Kelley-Clarke B, Joukov V, Walter JC, Luger K, Kaye KM. 2006. The nucleosomal surface as a docking station for Kaposi's sarcoma herpesvirus LANA. Science 311:856-861.
57. Wissmann M, Yin N, Muller JM, Greschik H, Fodor BD, Jenuwein T, Vogler C, Schneider R, Gunther T, Buettner R, Metzger E, Schule R. 2007. Cooperative demethylation by JMJD2C and LSD1 promotes androgen receptor-dependent gene expression. Nat. Cell Biol. 9:347-353.
58. Davis DA, Rinderknecht AS, Zoeteweij JP, Aoki Y, Read-Connole EL, Tosato G, Blauvelt A, Yarchoan R. 2001. Hypoxia induces lytic replication of Kaposi sarcoma-associated herpesvirus. Blood 97:3244-3250.
59. Shin YC, Joo CH, Gack MU, Lee HR, Jung JU. 2008. Kaposi's sarcomaassociated herpesvirus viral IFN regulatory factor 3 stabilizes hypoxiainducible factor-1 alpha to induce vascular endothelial growth factor expression. Cancer Res. 68:1751-1759.
60. Carroll PA, Kenerson HL, Yeung RS, Lagunoff M. 2006. Latent Kaposi's sarcoma-associated herpesvirus infection of endothelial cells activates hypoxia-induced factors. J. Virol. 80:10802-10812.
61. Cai Q, Murakami M, Si H, Robertson ES. 2007. A potential alpha-helix motif in the amino terminus of LANA encoded by Kaposi's sarcomaassociated herpesvirus is critical for nuclear accumulation of HIF-1alpha in normoxia. J. Virol. 81:10413-10423.
62. Mimura I, Nangaku M, Kanki Y, Tsutsumi S, Inoue T, Kohro T, Yamamoto S, Fujita T, Shimamura T, Suehiro J, Taguchi A, Kobayashi M, Tanimura K, Inagaki T, Tanaka T, Hamakubo T, Sakai J, Aburatani H, Kodama T, Wada Y. 2012. Dynamic change of chromatin conformation in response to hypoxia enhances the expression of GLUT3 (SLC2A3) by cooperative interaction of hypoxia-inducible factor 1 and KDM3A. Mol. Cell. Biol. 32:3018-3032.
63. Veeranna RP, Haque M, Davis DA, Yang M, Yarchoan R. 2012. Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen induction by hypoxia and hypoxia-inducible factors. J. Virol. 86:1097-1108.
64. Cho HS, Toyokawa G, Daigo Y, Hayami S, Masuda K, Ikawa N, Yamane Y, Maejima K, Tsunoda T, Field HI, Kelly JD, Neal DE, Ponder BA, Maehara Y, Nakamura Y, Hamamoto R. 2012. The JmjC domaincontaining histone demethylase KDM3A is a positive regulator of the G(1)/S transition in cancer cells via transcriptional regulation of the HOXA1 gene. Int. J. Cancer 131:E179-E189. doi:10.1002/ijc.26501.
65. Guo X, Shi M, Sun L, Wang Y, Gui Y, Cai Z, Duan X. 2011. The expression of histone demethylase JMJD1A in renal cell carcinoma. Neoplasma 58:153-157.
66. Bjorkman M, Ostling P, Harma V, Virtanen J, Mpindi JP, Rantala J, Mirtti T, Vesterinen T, Lundin M, Sankila A, Rannikko A, Kaivanto E, Kohonen P, Kallioniemi O, Nees M. 2012. Systematic knockdown of epigenetic enzymes identifies a novel histone demethylase PHF8 overexpressed in prostate cancer with an impact on cell proliferation, migration and invasion. Oncogene 31:3444-3456.