Epigenetic regulation of HIV-1 transcription

Epigenomics

Volumn 3, Issue 4, 2011, Pages 487-502

  Tripathy, Manoj Kumar ^a   Abbas, Wasim ^a   Herbein, Georges ^a  

^a UNIVERSITÉ DE FRANCHE COMTÉ   (France)

Author keywords

HIV; latency; transcription

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; CYCLIN DEPENDENT KINASE 9; DNA; HISTONE ACETYLTRANSFERASE; HISTONE ACETYLTRANSFERASE GCN5; HISTONE ACETYLTRANSFERASE PCAF; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE 4; HISTONE DEACETYLASE 5; HISTONE DEACETYLASE 6; HISTONE DEACETYLASE 7; HISTONE DEACETYLASE 8; HISTONE H3; HISTONE H4; HISTONE METHYLTRANSFERASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE; PROTEIN P300; RNA; RNA POLYMERASE II; SIRTUIN 1; SIRTUIN 2; SIRTUIN 3; SIRTUIN 4; SIRTUIN 5; SIRTUIN 6; SIRTUIN 7; UNINDEXED DRUG;

DNA METHYLATION; ENZYME ACTIVATION; EPIGENETICS; GENE EXPRESSION; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE PHOSPHORYLATION; HISTONE UBIQUITINATION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; REVIEW; TRANSCRIPTION INITIATION; VIRUS TRANSCRIPTION;

AZEPINES; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, VIRAL; HISTONE ACETYLTRANSFERASES; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HIV INFECTIONS; HIV-1; HUMANS; NUCLEOSOMES; PHORBOL ESTERS; PIPERAZINES; QUINAZOLINES; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TRANSCRIPTION, GENETIC; VIRUS INTEGRATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 80051968545     PISSN: 17501911     EISSN: 1750192X     Source Type: Journal    
DOI: 10.2217/epi.11.61     Document Type: Review

References (143)

1. Miska EA, Karlsson C, Langley E, Nielsen SJ, Pines J, Kouzarides T. HDAC4 deacetylase associates with and represses the MEF2 transcription factor. EMBO J. 18, 5099-5107 (1999).
2. Rayman JB, Takahashi Y, Indjeian VB et al. E2F mediates cell cycle-dependent transcriptional repression in vivo by recruitment of an HDAC1/mSin3B corepressor complex. Genes Dev. 16, 933-947 (2002).
3. Ng HH, Bird A. Histone deacetylases: silencers for hire. Trends Biochem. Sci. 25, 121-126 (2000).
4. Cress WD, Seto E. Histone deacetylases, transcriptional control, and cancer. J. Cell Physiol. 184, 1-16 (2000).
5. Mahlknecht U, Will J, Varin A, Hoelzer D, Herbein G. Histone deacetylase 3, a class I histone deacetylase, suppresses MAPK11- mediated activating transcription factor-2 activation and represses TNF gene expression. J. Immunol. 173, 3979-3990 (2004).
6. Fuks F, Burgers WA, Godin N, Kasai M, Kouzarides T. Dnmt3a binds deacetylases and is recruited by a sequence-specific repressor to silence transcription. EMBO J. 20, 2536-2544 (2001).
7. Burgers WA, Fuks F, Kouzarides T. DNA methyltransferases get connected to chromatin. Trends Genet. 18, 275-277 (2002).
8. Czermin B, Schotta G, Hulsmann BB et al. Physical and functional association of SU(VAR)3-9 and HDAC1 in Drosophila. EMBO Rep. 2, 915-919 (2001).
9. Tsai SC, Valkov N, Yang WM, Gump J, Sullivan D, Seto E. Histone deacetylase interacts directly with DNA topoisomerase II. Nat. Genet. 26, 349-353 (2000).
10. Zhang X, Wharton W, Yuan Z, Tsai SC, Olashaw N, Seto E. Activation of the growth-differentiation factor 11 gene by the histone deacetylase (HDAC) inhibitor trichostatin A and repression by HDAC3. Mol. Cell. Biol. 24, 5106-5118 (2004).
11. Marzio G, Wagener C, Gutierrez MI, Cartwright P, Helin K, Giacca M. E2F family members are differentially regulated by reversible acetylation. J. Biol. Chem. 275, 10887-10892 (2000).
12. Braun H, Koop R, Ertmer A, Nacht S, Suske G. Transcription factor Sp3 is regulated by acetylation. Nucleic Acids Res. 29, 4994-5000 (2001).
13. Ammanamanchi S, Freeman JW, Brattain MG. Acetylated sp3 is a transcriptional activator. J. Biol. Chem. 278, 35775-35780 (2003).
14. Gu W, Roeder RG. Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 90, 595-606 (1997).
15. Boyes J, Byfield P, Nakatani Y, Ogryzko V. Regulation of activity of the transcription factor GATA-1 by acetylation. Nature 396, 594-598 (1998).
16. Imhof A, Yang XJ, Ogryzko VV, Nakatani Y, Wolffe AP, Ge H. Acetylation of general transcription factors by histone acetyltransferases. Curr. Biol. 7, 689-692 (1997).
17. Ito A, Kawaguchi Y, Lai CH et al. MDM2-HDAC1-mediated deacetylation of p53 is required for its degradation. EMBO J. 21, 6236-6245 (2002).
18. Ito K, Yamamura S, Essilfie-Quaye S et al. Histone deacetylase 2-mediated deacetylation of the glucocorticoid receptor enables NF-kB suppression. J. Exp. Med. 203, 7-13 (2006).
19. Gregoire S, Xiao L, Nie J et al. Histone deacetylase 3 interacts with and deacetylates myocyte enhancer factor 2. Mol. Cell Biol. 27, 1280-1295 (2007).
20. Hubbert C, Guardiola A, Shao R et al. HDAC6 is a microtubule-associated deacetylase. Nature 417, 455-458 (2002).
21. Kovacs JJ, Murphy PJ, Gaillard S et al. HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Mol. Cell. 18, 601-607 (2005).
22. Roth SY, Denu JM, Allis CD. Histone acetyltransferases. Ann. Rev. Biochem. 70, 81-120 (2001).
23. Hodawadekar SC, Marmorstein R. Chemistry of acetyl transfer by histone modifying enzymes: structure, mechanism and implications for effector design. Oncogene 26, 5528-5540 (2007).
24. Sterner DE, Berger SL. Acetylation of histones and transcription-related factors. Microbiol. Mol. Biol. Rev. 64, 435-459 (2000).
25. Allis CD, Berger SL, Cote J et al. New nomenclature for chromatin-modifying enzymes. Cell. 131, 633-636 (2007).
26. Fu M, Wang C, Zhang X, Pestell RG. Acetylation of nuclear receptors in cellular growth and apoptosis. Biochem. Pharmacol. 68, 1199-1208 (2004).
27. Yang XJ, Gregoire S. Metabolism, cytoskeleton and cellular signalling in the grip of protein Ne- and O-acetylation. EMBO Rep. 8, 556-562 (2007).
28. Baker SP, Grant PA. The SAGA continues: expanding the cellular role of a transcriptional co-activator complex. Oncogene 26, 5329-5340 (2007).
29. Nagy Z, Tora L. Distinct GCN5/PCAF-containing complexes function as co-activators and are involved in transcription factor and global histone acetylation. Oncogene 26, 5341-5357 (2007).
30. Chan HM, La Thangue NB. p300/CBP proteins: HATs for transcriptional bridges and scaffolds. J. Cell. Sci. 114, 2363-2373 (2001).
31. Liu X, Wang L, Zhao K et al. The structural basis of protein acetylation by the p300/CBP transcriptional coactivator. Nature 451, 846-850 (2008).
32. Martens JH, O'Sullivan RJ, Braunschweig U et al. The profile of repeat-associated histone lysine methylation states in the mouse epigenome. EMBO J. 24, 800-812 (2005).
33. Klose RJ, Kallin EM, Zhang Y. JmjC-domain-containing proteins and histone demethylation. Nat. Rev. Genet. 7, 715-727 (2006).
34. Shi Y. Histone lysine demethylases: emerging roles in development, physiology and disease. Nat. Rev. Genet. 8, 829-833 (2007).
35. Bannister AJ, Zegerman P, Partridge JF et al. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410, 120-124 (2001).
36. Lachner M, O'Carroll D, Rea S, Mechtler K, Jenuwein T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410, 116-120 (2001).
37. Martin C, Zhang Y. The diverse functions of histone lysine methylation. Nat. Rev. Mol. Cell. Biol. 6, 838-849 (2005).
38. Rea S, Eisenhaber F, O'Carroll D et al. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406, 593-599 (2000).
39. Jenuwein T. The epigenetic magic of histone lysine methylation. FEBS J. 273, 3121-3135 (2006).
40. Grewal SI, Jia S. Heterochromatin revisited. Nat. Rev. Genet. 8, 35-46 (2007).
41. Tachibana M, Sugimoto K, Nozaki M et al. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev. 16, 1779-1791 (2002).
42. Tachibana M, Ueda J, Fukuda M et al. Histone methyltransferases G9a and GLP form heteromeric complexes and are both crucial for methylation of euchromatin at H3-K9. Genes Dev. 19, 815-826 (2005).
43. Shi Y, Lan F, Matson C et al. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell. 119, 941-953 (2004).
44. Huang J, Sengupta R, Espejo AB et al. p53 is regulated by the lysine demethylase LSD1. Nature 449, 105-108 (2007).
45. Karytinos A, Forneris F, Profumo A et al. A novel mammalian flavin-dependent histone demethylase. J. Biol. Chem. 284, 17775-17782 (2009).
46. Shi YJ, Matson C, Lan F, Iwase S, Baba T, Shi Y. Regulation of LSD1 histone demethylase activity by its associated factors. Mol. Cell. 19, 857-864 (2005).
47. Lee MG, Wynder C, Cooch N, Shiekhattar R. An essential role for CoREST in nucleosomal histone 3 lysine 4 demethylation. Nature 437, 432-435 (2005).
48. Tsukada Y, Fang J, Erdjument-Bromage H et al. Histone demethylation by a family of JmjC domain-containing proteins. Nature 439, 811-816 (2006).
49. Falnes PO, Johansen RF, Seeberg E. AlkB-mediated oxidative demethylation reverses DNA damage in Escherichia coli. Nature 419, 178-182 (2002).
50. Trewick SC, Henshaw TF, Hausinger RP, Lindahl T, Sedgwick B. Oxidative demethylation by Escherichia coli AlkB directly reverts DNA base damage. Nature 419, 174-178 (2002).
51. Dann CE 3rd, Bruick RK. Dioxygenases as O2-dependent regulators of the hypoxic response pathway. Biochem. Biophys. Res. Commun. 338, 639-647 (2005).
52. Tahiliani M, Koh KP, Shen Y et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324, 930-935 (2009).
53. Hoffart LM, Barr EW, Guyer RB, Bollinger JM Jr, Krebs C. Direct spectroscopic detection of a C-H-cleaving high-spin Fe(IV) complex in a prolyl-4- hydroxylase. Proc. Natl Acad. Sci. USA 103, 14738-14743 (2006).
54. Ozer A, Bruick RK. Non-heme dioxygenases: cellular sensors and regulators jelly rolled into one? Nat. Chem. Biol. 3, 144-153 (2007).
55. Gao WY, Cara A, Gallo RC, Lori F. Low levels of deoxynucleotides in peripheral blood lymphocytes: a strategy to inhibit human immunodeficiency virus type 1 replication. Proc. Natl Acad. Sci. USA 90, 8925-8928 (1993).
56. Malim MH. APOBEC proteins and intrinsic resistance to HIV-1 infection. Phil. Trans. R. Soc. Lond. B. Biol. Sci. 364, 675-687 (2009).
57. Goila-Gaur R, Khan MA, Miyagi E, Strebel K. Differential sensitivity of 'old' versus 'new' APOBEC3G to human immunodeficiency virus type 1 vif. J. Virol. 83, 1156-1160 (2009).
58. Chiu YL, Soros VB, Kreisberg JF, Stopak K, Yonemoto W, Greene WC. Cellular APOBEC3G restricts HIV-1 infection in resting CD4+ T cells. Nature 435, 108-114 (2005).
59. Goila-Gaur R, Strebel K. HIV-1 Vif, APOBEC, and intrinsic immunity. Retrovirology 5, 51 (2008).
60. Lin TY, Emerman M. Determinants of cyclophilin A-dependent TRIM5a restriction against HIV-1. Virology 379, 335-341 (2008).
61. Sebastian S, Luban J. The retroviral restriction factor TRIM5a. Curr. Infect. Dis. Rep. 9, 167-173 (2007).
62. Towers GJ. The control of viral infection by tripartite motif proteins and cyclophilin A. Retrovirology 4, 40 (2007).
63. Bukrinsky MI, Stanwick TL, Dempsey MP, Stevenson M. Quiescent T lymphocytes as an inducible virus reservoir in HIV-1 infection. Science 254, 423-427 (1991).
64. Williams SA, Greene WC. Regulation of HIV-1 latency by T-cell activation. Cytokine 39, 63-74 (2007).
65. Zhou Y, Zhang H, Siliciano JD, Siliciano RF. Kinetics of human immunodeficiency virus type 1 decay following entry into resting CD4+ T cells. J. Virol. 79, 2199-2210 (2005).
66. Pierson TC, Zhou Y, Kieffer TL, Ruff CT, Buck C, Siliciano RF. Molecular characterization of preintegration latency in human immunodeficiency virus type 1 infection. J. Virol. 76, 8518-8531 (2002).
67. Lewinski MK, Yamashita M, Emerman M et al. Retroviral DNA integration: viral and cellular determinants of target-site selection. PLoS Pathog. 2, e60 (2006).
68. Meehan AM, Saenz DT, Morrison JH et al. LEDGF/p75 proteins with alternative chromatin tethers are functional HIV-1 cofactors. PLoS Pathog. 5, e1000522 (2009).
69. Schroder AR, Shinn P, Chen H, Berry C, Ecker JR, Bushman F. HIV-1 integration in the human genome favors active genes and local hotspots. Cell 110, 521-529 (2002).
70. Lenasi T, Contreras X, Peterlin BM. Transcriptional interference antagonizes proviral gene expression to promote HIV latency. Cell. Host Microbe 4, 123-133 (2008).
71. Verdin E. DNase I-hypersensitive sites are associated with both long terminal repeats and with the intragenic enhancer of integrated human immunodeficiency virus type 1. J. Virol. 65, 6790-6799 (1991).
72. Verdin E, Paras P Jr, Van Lint C. Chromatin disruption in the promoter of human immunodeficiency virus type 1 during transcriptional activation. EMBO J. 12, 3249-3259 (1993).
73. Van Lint C, Emiliani S, Ott M, Verdin E. Transcriptional activation and chromatin remodeling of the HIV-1 promoter in response to histone acetylation. EMBO J. 15, 1112-1120 (1996).
74. Yu W, Wang Y, Shaw CA, Qin XF, Rice AP. Induction of the HIV-1 Tat co-factor cyclin T1 during monocyte differentiation is required for the regulated expression of a large portion of cellular mRNAs. Retrovirology 3, 32 (2006).
75. Liou LY, Herrmann CH, Rice AP. Human immunodeficiency virus type 1 infection induces cyclin t1 expression in macrophages. J. Virol. 78, 8114-8119 (2004).
76. Voinnet O. Induction and suppression of RNA silencing: insights from viral infections. Nat. Rev. Genet. 6, 206-220 (2005).
77. Huang J, Wang F, Argyris E et al. Cellular microRNAs contribute to HIV-1 latency in resting primary CD4+ T lymphocytes. Nat. Med. 13, 1241-1247 (2007).
78. Ahluwalia JK, Khan SZ, Soni K et al. Human cellular microRNA hsa-miR-29a interferes with viral nef protein expression and HIV-1 replication. Retrovirology 5, 117 (2008).
79. Sung TL, Rice AP. miR-198 inhibits HIV-1 gene expression and replication in monocytes and its mechanism of action appears to involve repression of cyclin T1. PLoS Pathog. 5, e1000263 (2009).
80. Grewal SI, Moazed D. Heterochromatin and epigenetic control of gene expression. Science 301, 798-802 (2003).
81. Avram D, Fields A, Pretty On Top K, Nevrivy DJ, Ishmael JE, Leid M. Isolation of a novel family of C(2)H(2) zinc finger proteins implicated in transcriptional repression mediated by chicken ovalbumin upstream promoter transcription factor (COUP-TF) orphan nuclear receptors. J. Biol. Chem. 275, 10315-10322 (2000).
82. Leid M, Ishmael JE, Avram D, Shepherd D, Fraulob V, Dolle P. CTIP1 and CTIP2 are differentially expressed during mouse embryogenesis. Gene Expr. Patterns 4, 733-739 (2004).
83. Arlotta P, Molyneaux BJ, Chen J, Inoue J, Kominami R, Macklis JD. Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 45, 207-221 (2005).
84. Rohr O, Lecestre D, Chasserot-Golaz S et al. Recruitment of Tat to heterochromatin protein HP1 via interaction with CTIP2 inhibits human immunodeficiency virus type 1 replication in microglial cells. J. Virol. 77, 5415-5427 (2003).
85. Marban C, Redel L, Suzanne S et al. COUP-TF interacting protein 2 represses the initial phase of HIV-1 gene transcription in human microglial cells. Nucleic Acids Res. 33, 2318-2331 (2005).
86. Marban C, Suzanne S, Dequiedt F et al. Recruitment of chromatin-modifying enzymes by CTIP2 promotes HIV-1 transcriptional silencing. EMBO J. 26, 412-423 (2007).
87. Marcello A. Latency: the hidden HIV-1 challenge. Retrovirology 3, 7 (2006).
88. Maison C, Almouzni G. HP1 and the dynamics of heterochromatin maintenance. Nat. Rev. Mol. Cell Biol. 5, 296-304 (2004).
89. Koiwa T, Hamano-Usami A, Ishida T et al. 5́-long terminal repeat-selective CpG methylation of latent human T-cell leukemia virus type 1 provirus in vitro and in vivo. J. Virol. 76, 9389-9397 (2002).
90. Taniguchi Y, Nosaka K, Yasunaga J et al. Silencing of human T-cell leukemia virus type I gene transcription by epigenetic mechanisms. Retrovirology 2, 64 (2005).
91. Kauder SE, Bosque A, Lindqvist A, Planelles V, Verdin E. Epigenetic regulation of HIV-1 latency by cytosine methylation. PLoS Pathog. 5, e1000495 (2009).
92. Sune C, Garcia-Blanco MA. Sp1 transcription factor is required for in vitro basal and Tat-activated transcription from the human immunodeficiency virus type 1 long terminal repeat. J. Virol. 69, 6572-6576 (1995).
93. Perkins ND, Edwards NL, Duckett CS, Agranoff AB, Schmid RM, Nabel GJ. A cooperative interaction between NF-k B and Sp1 is required for HIV-1 enhancer activation. EMBO J. 12, 3551-3558 (1993).
94. Williams SA, Chen LF, Kwon H, Ruiz-Jarabo CM, Verdin E, Greene WC. NF-kB p50 promotes HIV latency through HDAC recruitment and repression of transcriptional initiation. EMBO J. 25, 139-149 (2006).
95. Gerritsen ME, Williams AJ, Neish AS, Moore S, Shi Y, Collins T. CREB-binding protein/p300 are transcriptional coactivators of p65. Proc. Natl Acad. Sci. USA 94, 2927-2932 (1997).
96. Zhong H, May MJ, Jimi E, Ghosh S. The phosphorylation status of nuclear NF-kB determines its association with CBP/p300 or HDAC-1. Mol. Cell 9, 625-636 (2002).
97. Lusic M, Marcello A, Cereseto A, Giacca M. Regulation of HIV-1 gene expression by histone acetylation and factor recruitment at the LTR promoter. EMBO J. 22, 6550-6561 (2003).
98. Thierry S, Marechal V, Rosenzwajg M et al. Cell cycle arrest in G2 induces human immunodeficiency virus type 1 transcriptional activation through histone acetylation and recruitment of CBP, NF-kB, and c-Jun to the long terminal repeat promoter. J. Virol. 78, 12198-12206 (2004).
99. Calao M, Burny A, Quivy V, Dekoninck A, Van Lint C. A pervasive role of histone acetyltransferases and deacetylases in an NF-kB-signaling code. Trends Biochem. Sci. 33, 339-349 (2008).
100. Kim YK, Bourgeois CF, Pearson R et al. Recruitment of TFIIH to the HIV LTR is a rate-limiting step in the emergence of HIV from latency. EMBO J. 25, 3596-3604 (2006).
101. Barboric M, Nissen RM, Kanazawa S, Jabrane-Ferrat N, Peterlin BM. NF-kB binds P-TEFb to stimulate transcriptional elongation by RNA polymerase II. Mol. Cell 8, 327-337 (2001).
102. Garcia-Rodriguez C, Rao A. Nuclear factor of activated T cells (NFAT)-dependent transactivation regulated by the coactivators p300/CREB-binding protein (CBP).J. Exp. Med. 187, 2031-2036 (1998).
103. He G, Margolis DM. 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 (2002).
104. Romerio F, Gabriel MN, Margolis DM. Repression of human immunodeficiency virus type 1 through the novel cooperation of human factors YY1 and LSF. J. Virol. 71, 9375-9382 (1997).
105. Imai K, Okamoto T. Transcriptional repression of human immunodeficiency virus type 1 by AP-4. J. Biol. Chem. 281, 12495-12505 (2006).
106. Jiang G, Espeseth A, Hazuda DJ, Margolis DM. c-Myc and Sp1 contribute to proviral latency by recruiting histone deacetylase 1 to the human immunodeficiency virus type 1 promoter. J. Virol. 81, 10914-10923 (2007).
107. Sorin M, Cano J, Das S et al. Recruitment of a SAP18- HDAC1 complex into HIV-1 virions and its requirement for viral replication. PLoS Pathog. 5, e1000463 (2009).
108. Lusic M, Marcello A, Cereseto A, Giacca M. Regulation of HIV-1 gene expression by histone acetylation and factor recruitment at the LTR promoter. EMBO J. 22, 6550-6561 (2003).
109. Benkirane M, Chun RF, Xiao H et al. Activation of integrated provirus requires histone acetyltransferase. p300 and P/CAF are coactivators for HIV-1 Tat. J. Biol. Chem. 273, 24898-24905 (1998).
110. Ping YH, Rana TM. DSIF and NELF interact with RNA polymerase II elongation complex and HIV-1 Tat stimulates P-TEFb-mediated phosphorylation of RNA polymerase II and DSIF during transcription elongation. J. Biol. Chem. 276, 12951-12958 (2001).
111. Yamaguchi Y, Takagi T, Wada T et al. NELF, a multisubunit complex containing RD, cooperates with DSIF to repress RNA polymerase II elongation. Cell 97, 41-51 (1999).
112. Kao SY, Calman AF, Luciw PA, Peterlin BM. Anti-termination of transcription within the long terminal repeat of HIV-1 by tat gene product. Nature 330, 489-493 (1987).
113. Coull JJ, Romerio F, Sun JM et al. 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 (2000).
114. Kiernan RE, Vanhulle C, Schiltz L et al. HIV-1 tat transcriptional activity is regulated by acetylation. EMBO J. 18, 6106-6118 (1999).
115. Barboric M, Peterlin BM. A new paradigm in eukaryotic biology: HIV Tat and the control of transcriptional elongation. PLoS Biol. 3, e76 (2005).
116. Parada CA, Roeder RG. Enhanced processivity of RNA polymerase II triggered by Tat-induced phosphorylation of its carboxy-terminal domain. Nature 384, 375-378 (1996).
117. Zhou M, Halanski MA, Radonovich MF et al. Tat modifies the activity of CDK9 to phosphorylate serine 5 of the RNA polymerase II carboxyl-terminal domain during human immunodeficiency virus type 1 transcription. Mol. Cell. Biol. 20, 5077-5086 (2000).
118. Fujinaga K, Irwin D, Huang Y, Taube R, Kurosu T, Peterlin BM. Dynamics of human immunodeficiency virus transcription. P-TEFb phosphorylates RD and dissociates negative effectors from the transactivation response element. Mol. Cell. Biol. 24, 787-795 (2004).
119. Kaehlcke K, Dorr A, Hetzer-Egger C et al. Acetylation of Tat defines a cyclinT1- independent step in HIV transactivation. Mol. Cell 12, 167-176 (2003).
120. Bres V, Kiernan R, Emiliani S, Benkirane M. Tat acetyl- acceptor lysines are important for human immunodeficiency virus type-1 replication. J. Biol. Chem. 277, 22215-22221 (2002).
121. Ott M, Dorr A, Hetzer-Egger C et al. Tat acetylation: a regulatory switch between early and late phases in HIV transcription elongation. Novartis Found. Symp. 259, 182-193; discussion 193-186, 223-185 (2004).
122. Mahmoudi T, Parra M, Vries RG et al. The SWI/SNF chromatin-remodeling complex is a cofactor for Tat transactivation of the HIV promoter. J. Biol. Chem. 281, 19960-19968 (2006).
123. Pagans S, Pedal A, North BJ et al. SIRT1 regulates HIV transcription via Tat deacetylation. PLoS Biol. 3, e41 (2005).
124. Zhang HS, Wu MR. SIRT1 regulates Tat-induced HIV-1 transactivation through activating AMP-activated protein kinase. Virus Res. 146, 51-57 (2009).
125. Blazek D, Peterlin BM. Tat-SIRT1 tango. Mol. Cell 29, 539-540 (2008).
126. Kwon HS, Brent MM, Getachew R et al. Human immunodeficiency virus type 1 Tat protein inhibits the SIRT1 deacetylase and induces T cell hyperactivation. Cell. Host Microbe 3, 158-167 (2008).
127. Trono D, Van Lint C, Rouzioux C et al. HIV persistence and the prospect of long-term drug-free remissions for HIV-infected individuals. Science 329, 174-180 (2010).
128. Rong L, Perelson AS. Modeling HIV persistence, the latent reservoir, and viral blips. J. Theor. Biol. 260, 308-331 (2009).
129. Ylisastigui L, Archin NM, Lehrman G, Bosch RJ, Margolis DM. Coaxing HIV-1 from resting CD4 T cells: histone deacetylase inhibition allows latent viral expression. AIDS 18, 1101-1108 (2004).
130. Quivy V, De Walque S, Van Lint C. Chromatin-associated regulation of HIV-1 transcription: implications for the development of therapeutic strategies. Subcell. Biochem. 41, 371-396 (2007).
131. Archin NM, Espeseth A, Parker D, Cheema M, Hazuda D, Margolis DM. Expression of latent HIV induced by the potent HDAC inhibitor suberoylanilide hydroxamic acid. AIDS Res. Hum. Retroviruses 25, 207-212 (2009).
132. Edelstein LC, Micheva-Viteva S, Phelan BD, Dougherty JP. Short communication: activation of latent HIV type 1 gene expression by suberoylanilide hydroxamic acid (SAHA), an HDAC inhibitor approved for use to treat cutaneous T cell lymphoma. AIDS Res. Hum. Retroviruses 25, 883-887 (2009).
133. Contreras X, Schweneker M, Chen CS et al. Suberoylanilide hydroxamic acid reactivates HIV from latently infected cells. J. Biol. Chem. 284, 6782-6789 (2009).
134. Ylisastigui L, Coull JJ, Rucker VC et al. Polyamides reveal a role for repression in latency within resting T cells of HIV-infected donors. J. Infect. Dis. 190, 1429-1437 (2004).
135. Archin NM, Keedy KS, Espeseth A, Dang H, Hazuda DJ, Margolis DM. Expression of latent human immunodeficiency type 1 is induced by novel and selective histone deacetylase inhibitors. AIDS 23, 1799-1806 (2009).
136. Keedy KS, Archin NM, Gates AT, Espeseth A, Hazuda DJ, Margolis DM. A limited group of class I histone deacetylases acts to repress human immunodeficiency virus type 1 expression. J. Virol. 83, 4749-4756 (2009).
137. Korin YD, Brooks DG, Brown S, Korotzer A, Zack JA. Effects of prostratin on T-cell activation and human immunodeficiency virus latency. J. Virol. 76, 8118-8123 (2002).
138. Brooks DG, Hamer DH, Arlen PA et al. Molecular characterization, reactivation, and depletion of latent HIV. Immunity 19, 413-423 (2003).
139. Reuse S, Calao M, Kabeya K et al. Synergistic activation of HIV-1 expression by deacetylase inhibitors and prostratin: implications for treatment of latent infection. PLoS ONE 4, e6093 (2009).
140. Zhang HS, Zhou Y, Wu MR, Zhou HS, Xu F. Resveratrol inhibited Tat-induced HIV-1 LTR transactivation via NAD+-dependent SIRT1 activity. Life Sci. 85, 484-489 (2009).
141. Greiner D, Bonaldi T, Eskeland R, Roemer E, Imhof A. Identification of a specific inhibitor of the histone methyltransferase SU(VAR)3-9. Nat. Chem. Biol. 1, 143-145 (2005).
142. Miranda TB, Cortez CC, Yoo CB et al. DZNep is a global histone methylation inhibitor that reactivates developmental genes not silenced by DNA methylation. Mol. Cancer Ther. 8, 1579-1588 (2009).
143. Chang Y, Zhang X, Horton JR et al. Structural basis for G9a-like protein lysine methyltransferase inhibition by BIX-01294. Nat. Struct. Mol. Biol. 16, 312-317 (2009).