Identification of cellular proteins that maintain retroviral epigenetic silencing: Evidence for an antiviral response

Journal of Virology

Volumn 82, Issue 5, 2008, Pages 2313-2323

  Poleshko, Andrey ^a   Palagin, Ivan ^a,b   Zhang, Rugang ^a   Boimel, Pamela ^a,c   Castagna, Carolyn ^a,d   Adams, Peter D ^a   Skalka, Anna Marie ^a   Katz, Richard A ^a  

^a FOX CHASE CANCER CENTER   (United States)

^b SMOLENSK STATE MEDICAL UNIVERSITY   (Russian Federation)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^d TEMPLE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DAXX PROTEIN; GREEN FLUORESCENT PROTEIN; HETEROCHROMATIN PROTEIN 1; HISTONE DEACETYLASE; HISTONE DEACETYLASE 1; NUCLEIC ACID BINDING PROTEIN; SMALL INTERFERING RNA;

ANTIVIRAL SUSCEPTIBILITY; ARTICLE; CELL CLONE; EPIGENETICS; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; LABORATORY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REPORTER GENE; RETROVIRUS; VIRUS GENE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; BASE SEQUENCE; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA PRIMERS; EPIGENESIS, GENETIC; GENE SILENCING; HELA CELLS; HISTONE DEACETYLASES; HUMANS; NUCLEAR PROTEINS; PROMOTER REGIONS (GENETICS); PROTEINS; RETROVIRIDAE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING;

AVIAN SARCOMA VIRUS;

EID: 39749187576     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01882-07     Document Type: Article

References (60)

1. Barsov, E. V., and S. H. Hughes. 1996. Gene transfer into mammalian cells by a Rous sarcoma virus-based retroviral vector with the host range of the amphotropic murine leukemia virus. J. Virol. 70:3922-3929.
2. Berger, S. L. 2007. The complex language of chromatin regulation during transcription. Nature 447:407-412.
3. Bernstein, B. E., A. Meissner, and E. S. Lander. 2007. The mammalian epigenome. Cell 128:669-681.
4. Birmingham, A., E. M. Anderson, A. Reynolds, D. Ilsley-Tyree, D. Leake, Y. Fedorov, S. Baskerville, E. Maksimova, K. Robinson, J. Karpilow, W. S. Marshall, and A. Khvorova. 2006. 3′ UTR seed matches, but not overall identity, are associated with RNAi off-targets. Nat. Methods 3:199-204.
5. Boggio, R., R. Colombo, R. T. Hay, G. F. Draetta, and S. Chiocca. 2004. A mechanism for inhibiting the SUMO pathway. Mol. Cell 16:549-561.
6. Bolden, J. E., M. J. Peart, and R. W. Johnstone. 2006. Anticancer activities of histone deacetylase inhibitors. Nat. Rev. Drug Discov. 5:769-784.
7. Cantrell, S. R., and W. A. Bresnahan. 2006. Human cytomegalovirus (HCMV) UL82 gene product (pp71) relieves hDaxx-mediated repression of HCMV replication. J. Virol. 80:6188-6191.
8. Chen, W. Y., and T. M. Townes. 2000. Molecular mechanism for silencing virally transduced genes involves histone deacetylation and chromatin condensation. Proc. Natl. Acad. Sci. USA 97:377-382.
9. Chiocca, S., V. Kurtev, R. Colombo, R. Boggio, M. T. Sciurpi, G. Brosch, C. Seiser, G. F. Draetta, and M. Cotten. 2002. Histone deacetylase 1 inactivation by an adenovirus early gene product. Curr. Biol. 12:594-598.
10. Coull, J. J., F. Romerio, J. M. Sun, J. L. Volker, K. M. Galvin, J. R. Davie, Y. Shi, U. Hansen, and D. M. Margolis. 2000. The human factors YY1 and LSF repress the human immunodeficiency virus type 1 long terminal repeat via recruitment of histone deacetylase 1. J. Virol. 74:6790-6799.
11. Cullen, B. R. 2006. Enhancing and confirming the specificity of RNAi experiments. Nat. Methods 3:677-681.
12. Dalle, B., J. E. Rubin, O. Alkan, T. Sukonnik, P. Pasceri, S. Yao, R. Pawliuk, P. Leboulch, and J. Ellis. 2005. eGFP reporter genes silence LCRbeta-globin transgene expression via CpG dinucleotides. Mol. Ther. 11:591-599.
13. de Ruijter, A. J., A. H. van Gennip, H. N. Caron, S. Kemp, and A. B. van Kuilenburg. 2003. Histone deacerylases (HDACs): characterization of the classical HDAC family. Biochem. J. 370:737-749.
14. Du, T., and P. D. Zamore. 2005. microPrimer: the biogenesis and function of microRNA. Development 132:4645-4652.
15. du Chene, I., E. Basyuk, Y. L. Lin, R. Triboulet, A. Knezevich, C. Chable-Bessia, C. Mettling, V. Baillat, J. Reynes, P. Corbeau, E. Bertrand, A. Marcello, S. Emiliani, R. Kiernan, and M. Benkirane. 2007. Suv39H1 and HPlgamma are responsible for chromatin-mediated HIV-1 transcriptional silencing and post-integration latency. EMBO J. 26:424-435.
16. Ellis, J. 2005. Silencing and variegation of gammaretrovirus and lentivirus vectors. Hum. Gene Ther. 16:1241-1246.
17. Ellis, J., and S. Yao. 2005. Retrovirus silencing and vector design: relevance to normal and cancer stem cells? Curr. Gene Ther. 5:367-373.
18. Fukagawa, T., M. Nogami, M. Yoshikawa, M. Ikeno, T. Okazaki, Y. Takami, T. Nakayama, and M. Oshimura. 2004. Dicer is essential for formation of the heterochromatin structure in vertebrate cells. Nat. Cell Biol. 6:784-791.
19. Glozak, M. A., N. Sengupta, X. Zhang, and E. Seto. 2005. Acetylation and deacetylation of non-histone proteins. Gene 363:15-23.
20. Greger, J. G., R. A. Katz, A. M. Ishov, G. G. Maul, and A. M. Skalka. 2005. The cellular protein Daxx interacts with avian sarcoma virus integrase and viral DNA to repress viral transcription. J. Virol. 79:4610-4618.
21. Grewal, S. I., and S. Jia. 2007. Heterochromatin revisited. Nat. Rev. Genet. 8:35-46.
22. Han, Y., M. Wind-Rotolo, H. C. Yang, J. D. Siliciano, and R. F. Siliciano. 2007. Experimental approaches to the study of HIV-1 latency. Nat. Rev. Microbiol. 5:95-106.
23. He, G., and D. M. Margolis. 2002. Counterregulation of chromatin deacetylation and histone deacetylase occupancy at the integrated promoter of human immunodeficiency virus type 1 (HIV-1) by the HIV-1 repressor YY1 and HIV-1 activator Tat. Mol. Cell. Biol. 22:2965-2973.
24. Hofmann, H., H. Sindre, and T. Stamminger. 2002. Functional interaction between the pp71 protein of human cytomegalovirus and the PML-interacting protein human Daxx. J. Virol. 76:5769-5783.
25. Hollenbach, A. D., C. J. McPherson, E. J. Mientjes, R. Iyengar, and G. Grosveld. 2002. Daxx and histone deacetylase II associate with chromatin through an interaction with core histones and the chromatin-associated protein Dek. J. Cell Sci. 115:3319-3330.
26. Jaenisch, R., and A. Bird. 2003. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet. 33(Suppl.):245-254.
27. Kanellopoulou, C., S. A. Muljo, A. L. Kung, S. Ganesan, R. Drapkin, T. Jenuwein, D. M. Livingston, and K. Rajewsky. 2005. Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev. 19:489-501.
28. Katz, R. A., E. Jack-Scott, A. Narezkina, I. Palagin, P. Boimel, J. Kulkosky, E. Nicolas, J. G. Greger, and A. M. Skalka. 2007. High-frequency epigenetic repression and silencing of retroviruses can be antagonized by histone deacetylase inhibitors and transcriptional activators, but uniform reactivation in cell clones is restricted by additional mechanisms. J. Virol. 81:2592-2604.
29. Kim, J. H., H. Li, and M. R. Stallcup. 2003. CoCoA, a nuclear receptor coactivator which acts through an N-terminal activation domain of p160 coactivators. Mol. Cell 12:1537-1549.
30. Kouzarides, T. 2007. Chromatin modifications and their function. Cell 128: 693-705.
31. Lehrman, G., I. B. Hogue, S. Palmer, C. Jennings, C. A. Spina, A. Wiegand, A. L. Landay, R. W. Coombs, D. D. Richman, J. W. Mellors, J. M. Coffin, R. J. Bosch, and D. M. Margolis. 2005. Depletion of latent HIV-1 infection in vivo: a proof-of-concept study. Lancet 366:549-555.
32. Lewinski, M. K., D. Bisgrove, P. Shinn, H. Chen, C. Hoffmann, S. Hannenhalli, E. Verdin, C. C. Berry, J. R. Ecker, and F. D. Bushman. 2005. Genomewide analysis of chromosomal features repressing human immunodeficiency virus transcription. J. Virol. 79:6610-6619.
33. Lieberman, P. M. 2006. Chromatin regulation of virus infection. Trends Microbiol. 14:132-140.
34. Lomberk, G., D. Bensi, M. E. Fernandez-Zapico, and R. Urrutia. 2006. Evidence for the existence of an HP1-mediated subcode within the histone code. Nat. Cell Biol. 8:407-415.
35. Marban, C., S. Suzanne, F. Dequiedt, S. de Walque, L. Redel, C. Van Lint, D. Aunis, and O. Rohr. 2007. Recruitment of chromatin-modifying enzymes by CTIP2 promotes HIV-1 transcriptional silencing. EMBO J. 26:412-423.
36. Marks, P. A. 2007. Discovery and development of SAHA as an anticancer agent. Oncogene 26:1351-1356.
37. Marks, P. A., and R. Breslow. 2007. Dimethyl sulfoxide to vorinostat: development of this histone deacetylase inhibitor as an anticancer drug. Nat. Biotechnol. 25:84-90.
38. Merezak, C., M. Reichert, C. Van Lint, P. Kerkhofs, D. Portetelle, L. Willems, and R. Kettmann. 2002. Inhibition of histone deacetylases induces bovine leukemia virus expression in vitro and in vivo. J. Virol. 76:5034-5042.
39. Mine, E., J. C. Courvalin, and B. Buendia. 2000. HP1gamma associates with euchromatin and heterochromatin in mammalian nuclei and chromosomes. Cytogenet. Cell Genet. 90:279-284.
40. Mizutani, T., T. Ito, M. Nishina, N. Yamamichi, A. Watanabe, and H. Iba. 2002. Maintenance of integrated proviral gene expression requires Brm, a catalytic subunit of SWI/SNF complex. J. Biol. Chem. 277:15859-15864.
41. Mok, H. P., and A. M. Lever. 2007. Chromatin, gene silencing and HIV latency. Genome Biol. 8:228.
42. Murphy, J. C., W. Fischle, E. Verdin, and J. H. Sinclair. 2002. Control of cytomegalovirus lytic gene expression by histone acetylation. EMBO J. 21: 1112-1120.
43. Narezkina, A., K. D. Taganov, S. Litwin, R. Stoyanova, J. Hayashi, C. Seeger, A. M. Skalka, and R. A. Katz. 2004. Genome-wide analyses of avian sarcoma virus integration sites. J. Virol. 78:11656-11663.
44. Nevels, M., C. Paulus, and T. Shenk. 2004. Human cytomegalovirus immediate-early 1 protein facilitates viral replication by antagonizing histone deacetylation. Proc. Natl. Acad. Sci. USA 101:17234-17239.
45. Nielsen, S. J., R. Schneider, U. M. Bauer, A. J. Bannister, A. Morrison, D. O'Carroll, R. Firestein, M. Cleary, T. Jenuwein, R. E. Herrera, and T. Kouzarides. 2001. Rb targets histone H3 methylation and HP1 to promoters. Nature 412:561-565.
46. Preston, C. M., and M. J. Nicholl. 2006. Role of the cellular protein hDaxx in human cytomegalovirus immediate-early gene expression. J. Gen. Virol. 87:1113-1121.
47. Quivy, V., S. De Walque, and C. Van Lint. 2007. Chromatin-associated regulation of HIV-1 transcription: implications for the development of therapeutic strategies. Subcell. Biochem. 41:371-396.
48. Ruthenburg, A. J., C. D. Allis, and J. Wysocka. 2007. Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark. Mol. Cell 25:15-30.
49. Saffert, R. T., and R. F. Kalejta. 2006. Inactivating a cellular intrinsic immune defense mediated by Daxx is the mechanism through which the human cytomegalovirus pp71 protein stimulates viral immediate-early gene expression. J. Virol. 80:3863-3871.
50. Shi, Y., and J. R. Whetstine. 2007. Dynamic regulation of histone lysine methylation by demethylases. Mol. Cell 25:1-14.
51. Svoboda, J., J. Hejnar, J. Geryk, D. Elleder, and Z. Vernerova. 2000. Retroviruses in foreign species and the problem of provirus silencing. Gene 261:181-188.
52. Swindle, C. S., and C. A. Klug. 2002. Mechanisms that regulate silencing of gene expression from retroviral vectors. J. Hematother. Stem Cell Res. 11:449-456.
53. Taddei, A., D. Roche, W. A. Bickmore, and G. Almouzni. 2005. The effects of histone deacetylase inhibitors on heterochromatin: implications for anticancer therapy? EMBO Rep. 6:520-524.
54. Van Lint, C., V. Quivy, D. Demonte, A. Chariot, C. Vanhulle, S. de Walque, G. Gaudray, E. Veithen, V. Bours, J. Piette, and A. Burny. 2004. Molecular mechanisms involved in HIV-1 transcriptional latency and reactivation: implications for the development of therapeutic strategies. Bull. Mem. Acad. R. Med. Belg. 159:176-189.
55. Williams, S. A., L. F. Chen, H. Kwon, C. M. Ruiz-Jarabo, E. Verdin, and W. C. Greene. 2006. NF-kappaB p50 promotes HIV latency through HDAC recruitment and repression of transcriptional initiation. EMBO J. 25:139-149.
56. Wolf, D., and S. P. Goff. 2007. TRIM28 mediates primer binding site-targeted silencing of murine leukemia virus in embryonic cells. Cell 131:46-57.
57. Yao, S., T. Sukonnik, T. Kean, R. R. Bharadwaj, P. Pasceri, and J. Ellis. 2004. Retrovirus silencing, variegation, extinction, and memory are controlled by a dynamic interplay of multiple epigenetic modifications. Mol. Ther. 10:27-36.
58. Ylisastigui, L., N. M. Archin, G. Lehrman, R. J. Bosch, and D. M. Margolis. 2004. Coaxing HIV-1 from resting CD4 T cells: histone deacetylase inhibition allows latent viral expression. AIDS 18:1101-1108.
59. Yoder, J. A., C. P. Walsh, and T. H. Bester. 1997. Cytosine methylation and the ecology of intragenomic parasites. Trends Genet. 13:335-340.
60. Zhang, R., S. T. Liu, W. Chen, M. Bonner, J. Pehrson, T. J. Yen, and P. D. Adams. 2007. HP1 proteins are essential for a dynamic nuclear response that rescues the function of perturbed heterochromatin in primary human cells. Mol. Cell. Biol. 27:949-962.