Identification of host-chromosome binding sites and candidate gene targets for Kaposi's sarcoma-associated herpesvirus LANA

Journal of Virology

Volumn 86, Issue 10, 2012, Pages 5752-5762

  Lu, Fang ^a   Tsai, Kevin ^a   Chen, Horng Shen ^a   Wikramasinghe, Priyankara ^a   Davuluri, Ramana V ^a   Showe, Louise ^a   Domsic, John ^a   Marmorstein, Ronen ^a   Lieberman, Paul M ^a  

^a WISTAR INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; LATENCY ASSOCIATED NUCLEAR ANTIGEN; PROTEIN P53; STAT1 PROTEIN; TAP1 PEPTIDE TRANSPORTER; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 1; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANTIBODY COMBINING SITE; ANTIGEN BINDING; ANTIGEN PRESENTATION; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENE CONTROL; GENE REGULATORY NETWORK; GENE TARGETING; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; IN VITRO STUDY; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PURIFICATION; QUANTITATIVE STUDY; TRANSCRIPTION INITIATION SITE; VIRUS GENOME;

ANTIGENS, VIRAL; BASE SEQUENCE; BINDING SITES; CELL LINE; CHROMOSOMES, HUMAN; GENE EXPRESSION REGULATION; GENE TARGETING; HERPESVIRUS 8, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PROTEIN BINDING; SARCOMA, KAPOSI;

HUMAN HERPESVIRUS 8;

EID: 84861321766     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.07216-11     Document Type: Article

References (63)

1. Alkharsah KR, et al. 2011. Deletion of Kaposi's sarcoma-associated herpesvirus FLICE inhibitory protein, vFLIP, from the viral genome compro-mises the activation of STAT1-responsive cellular genes and spindle cell formation in endothelial cells. J. Virol. 85:10375-10388.
2. 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.
3. Bailey TL, Williams N, Misleh C, Li WW. 2006. MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res. 34: W369-W373.
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. 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.
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. Chau CM, Lieberman PM. 2004. Dynamic chromatin boundaries delineate a latency control region of Epstein-Barr virus. J. Virol. 78:12308- 12319.
9. 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.
10. Cloutier N, Flamand L. 2010. Kaposi sarcoma-associated herpesvirus latency-associated nuclear antigen inhibits interferon (IFN) beta expression by competing with IFN regulatory factor-3 for binding to IFNB promoter. J. Biol. Chem. 285:7208 -7221.
11. Coscoy L, Ganem D. 2000. Kaposi's sarcoma-associated herpesvirus encodes two proteins that block cell surface display ofMHCclass I chains by enhancing their endocytosis. Proc. Natl. Acad. Sci. U. S. A. 97:8051- 8056.
12. 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.
13. Crooks GE, Hon G, Chandonia JM, Brenner SE. 2004. WebLogo: a sequence logo generator. Genome Res. 14:1188 -1190.
14. Fakhari FD, Jeong JH, Kanan Y, Dittmer DP. 2006. The latencyassociated nuclear antigen of Kaposi sarcoma-associated herpesvirus induces B cell hyperplasia and lymphoma. J. Clin. Invest. 116:735-742.
15. 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.
16. Gaczynska M, Goldberg AL, Tanaka K, Hendil KB, Rock KL. 1996. Proteasome subunits X and Y alter peptidase activities in opposite ways to the interferon-gamma-induced subunits LMP2 and LMP7. J. Biol. Chem. 271:17275-17280.
17. Ganem D. 2006. KSHV infection and the pathogenesis of Kaposi's sarcoma. Annu. Rev. Pathol. 1:273-296.
18. 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.
19. 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.
20. Gwack Y, et al. 2002. Kaposi's Sarcoma-associated herpesvirus open reading frame 50 stimulates the transcriptional activity of STAT3. J. Biol. Chem. 277:6438-6442.
21. Han SJ, 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. J. Gen. Virol. 91:2203-2215.
22. Hu J, Renne R. 2005. Characterization of the minimal replicator of Kaposi's sarcoma-associated herpesvirus latent origin. J. Virol. 79:2637- 2642.
23. Hu X, Ivashkiv LB. 2009. Cross-regulation of signaling pathways by interferon-gamma: implications for immune responses and autoimmune diseases. Immunity 31:539 -550.
24. 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.
25. Komatsu T, Ballestas ME, Barbera AJ, Kaye KM. 2002. The KSHV latency-associated nuclear antigen: a multifunctional protein. Front. Biosci. 7:d726-d730.
26. 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.
27. Lagos D, et al. 2007. Kaposi sarcoma herpesvirus-encoded vFLIP and vIRF1 regulate antigen presentation in lymphatic endothelial cells. Blood 109:1550 -1558.
28. 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 Jκ, the major downstream effector of the Notch signaling pathway. J. Virol. 79:3468 -3478.
29. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R25.
30. Lim C, Lee D, Seo T, Choi C, Choe J. 2003. Latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus functionally interacts with heterochromatin protein 1. J. Biol. Chem. 278:7397-7405.
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 latencyassociated nuclear antigen regulates repression of Kaposi's sarcomaassociated herpesvirus lytic transcription. J. Virol. 80:5273-5282.
33. Lu F, et al. 2010. Genome-wide analysis of host-chromosome binding sites for Epstein-Barr virus nuclear antigen 1 (EBNA1). Virol. J 7:262.
34. Ma W, Lehner PJ, Cresswell P, Pober JS, Johnson DR. 1997. Interferongamma rapidly increases peptide transporter (TAP) subunit expression and peptide transport capacity in endothelial cells. J. Biol. Chem. 272: 16585-16590.
35. Mahony S, Benos PV. 2007. STAMP: a web tool for exploring DNAbinding motif similarities. Nucleic Acids Res. 35:W253-W258.
36. Mesri EA, Cesarman E, Boshoff C. 2010. Kaposi's sarcoma and its associated herpesvirus. Nat. Rev. Cancer 10:707-719.
37. Moore PS, Boshoff C, Weiss RA, Chang Y. 1996. Molecular mimicry of human cytokine and cytokine response pathway genes by KSHV. Science 274:1739 -1744.
38. Nicholas J, et al. 1997. Kaposi's sarcoma-associated human herpesvirus-8 encodes homologues of macrophage inflammatory protein-1 and interleukin-6. Nat. Med. 3:287-292.
39. Ohsaki E, et al. 2004. Poly(ADP-ribose) polymerase 1 binds to Kaposi's sarcoma-associated herpesvirus (KSHV) terminal repeat sequence and modulates KSHV replication in latency. J. Virol. 78:9936 -9946.
40. Ottinger M, 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.
41. Pal S, et al. 2011. Alternative transcription exceeds alternative splicing in generating the transcriptome diversity of cerebellar development. Genome Res. 21:1260 -1272.
42. Piolot T, Tramier M, Coppey M, Nicolas JC, 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. J. Virol. 75:3948 -3959.
43. Raghavan M, Del Cid N, Rizvi SM, Peters LR. 2008. MHC class I assembly: out and about. Trends Immunol. 29:436-443.
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. Robek MD, Garcia ML, Boyd BS, Chisari FV. 2007. Role of immunoproteasome catalytic subunits in the immune response to hepatitis B virus. J. Virol. 81:483- 491.
46. Robertson G, et al. 2007. Genome-wide profiles of STAT1 DNA association using chromatin immunoprecipitation and massively parallel sequencing. Nat. Methods 4:651- 657.
47. Rock KL, et al. 1994. Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 78:761-771.
48. Rouyez MC, et al. 2005. IFN regulatory factor-2 cooperates with STAT1 to regulate transporter associated with antigen processing-1 promoter activity. J. Immunol. 174:3948 -3958.
49. Schulz TF. 2006. The pleiotropic effects of Kaposi's sarcoma herpesvirus. J. Pathol. 208:187-198.
50. Shamay M, Krithivas A, Zhang J, Hayward SD. 2006. Recruitment of the de novo DNA methyltransferase Dnmt3a by Kaposi's sarcoma-associated herpesvirus LANA. Proc. Natl. Acad. Sci. U. S. A. 103:14554 -14559.
51. 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.
52. Skellam JG. 1946. The frequency distribution of the difference between two Poisson variates belonging to different populations. J. Royal Stat. Soc. Ser. A 109:296.
53. 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.
54. Sun H, et al. 2011. Genome-wide mapping of RNA Pol-II promoter usage in mouse tissues by ChIP-Seq. Nucleic Acids Res. 39:190 -201.
55. van Boxel-Dezaire AH, Stark GR. 2007. Cell type-specific signaling in response to interferon-gamma. Curr. Top. Microbiol. Immunol. 316: 119-154.
56. Verma SC, Lan K, Robertson E. 2007. Structure and function of latencyassociated nuclear antigen. Curr. Top. Microbiol. Immunol. 312:101-136.
57. Viejo-Borbolla A, et al. 2003. A Domain in the C-terminal region of latency-associated nuclear antigen 1 of Kaposi's sarcoma-associated Herpesvirus affects transcriptional activation and binding to nuclear heterochromatin. J. Virol. 77:7093-7100.
58. Viejo-Borbolla A, et al. 2005. Brd2/RING3 interacts with a chromatinbinding domain in the Kaposi's sarcoma-associated herpesvirus latencyassociated nuclear antigen 1 (LANA-1) that is required for multiple functions of LANA-1. J. Virol. 79:13618 -13629.
59. Wood VH, et al. 2007. Epstein-Barr virus-encoded EBNA1 regulates cellular gene transcription and modulates the STAT1 and TGFβ signaling pathways. Oncogene 26:4135- 4147.
60. Ye FC, et al. 2004. Disruption of Kaposi's sarcoma-associated herpesvirus latent nuclear antigen leads to abortive episome persistence. J. Virol. 78: 11121-11129.
61. You J, et al. 2006. Kaposi's sarcoma-associated herpesvirus latencyassociated nuclear antigen interacts with bromodomain protein Brd4 on host mitotic chromosomes. J. Virol. 80:8909-8919.
62. Yu H, Pardoll D, Jove R. 2009. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat. Rev. Cancer 9:798-809.
63. Zhang ZD, Rozowsky J, Snyder M, Chang J, Gerstein M. 2008. Modeling ChIP sequencing in silico with applications. PLoS Comput. Biol. 4:e1000158.