Reactivation of latent HIV by histone deacetylase inhibitors

Trends in Microbiology

Volumn 21, Issue 6, 2013, Pages 277-285

  Shirakawa, Kotaro ^a,b   Chavez, Leonard ^a,b   Hakre, Shweta ^a,b   Calvanese, Vincenzo ^a,b   Verdin, Eric ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

HDAC; HDAC inhibitors; HIV; Latency

Indexed keywords

ANTIRETROVIRUS AGENT; BRG1 PROTEIN; DISULFIRAM; ENFUVIRTIDE; ENTINOSTAT; GIVINOSTAT; HISTONE DEACETYLASE; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE INHIBITOR; HISTONE H3; HISTONE H4; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MGDC 0103; MOCETINOSTAT; PANOBINOSTAT; RALTEGRAVIR; ROMIDEPSIN; SIRTUIN; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SP1; UNCLASSIFIED DRUG; VALPROIC ACID; VORINOSTAT;

CD4+ T LYMPHOCYTE; CUTANEOUS T CELL LYMPHOMA; DNA METHYLATION; DRUG BLOOD LEVEL; DRUG STRUCTURE; GENE REPRESSION; HEMATOLOGIC MALIGNANCY; HISTONE ACETYLATION; HISTONE METHYLATION; HODGKIN DISEASE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LATENT VIRUS INFECTION; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; SOLID TUMOR; SUBCUTANEOUS T CELL LYMPHOMA; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; UNSPECIFIED SIDE EFFECT; VIRUS LATENCY; VIRUS REACTIVATION; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HIV INFECTIONS; HIV-1; HUMANS; T-LYMPHOCYTES; VIRUS ACTIVATION; VIRUS LATENCY;

EID: 84878459431     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2013.02.005     Document Type: Review

References (84)

1. Perelson A.S., et al. Decay characteristics of HIV-1-infected compartments during combination therapy. Nature 1997, 387:188-191.
2. Finzi D., et al. Identification of a reservoir for HIV-1 in patients on highly active antiretroviral therapy. Science 1997, 278:1295-1300.
3. Choudhary S.K., Margolis D.M. Curing HIV: pharmacologic approaches to target HIV-1 latency. Annu. Rev. Pharmacol. Toxicol. 2011, 51:397-418.
4. Shen L., Siliciano R.F. Viral reservoirs, residual viremia, and the potential of highly active antiretroviral therapy to eradicate HIV infection. J. Allergy Clin. Immunol. 2008, 122:22-28.
5. Tobin N.H., et al. Evidence that low-level viremias during effective highly active antiretroviral therapy result from two processes: expression of archival virus and replication of virus. J. Virol. 2005, 79:9625-9634.
6. Muesing M.A., et al. Regulation of mRNA accumulation by a human immunodeficiency virus trans-activator protein. Cell 1987, 48:691-701.
7. Chun T.W., et al. Quantification of latent tissue reservoirs and total body viral load in HIV-1 infection. Nature 1997, 387:183-188.
8. Chomont N., et al. HIV reservoir size and persistence are driven by T cell survival and homeostatic proliferation. Nat. Med. 2009, 15:893-900.
9. Jordan A., et al. HIV reproducibly establishes a latent infection after acute infection of T cells in vitro. EMBO J. 2003, 22:1868-1877.
10. Jordan A., et al. The site of HIV-1 integration in the human genome determines basal transcriptional activity and response to Tat transactivation. EMBO J. 2001, 20:1726-1738.
11. Lenasi T., et al. Transcriptional interference antagonizes proviral gene expression to promote HIV latency. Cell Host Microbe 2008, 4:123-133.
12. Adams M., et al. Cellular latency in human immunodeficiency virus-infected individuals with high CD4 levels can be detected by the presence of promoter-proximal transcripts. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:3862-3866.
13. He G., Margolis D.M. 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. 2002, 22:2965-2973.
14. Rafati H., et al. Repressive LTR nucleosome positioning by the BAF complex is required for HIV latency. PLoS Biol. 2011, 9:e1001206.
15. Verdin E., et al. Chromatin disruption in the promoter of human immunodeficiency virus type 1 during transcriptional activation. EMBO J. 1993, 12:3249-3259.
16. Van Lint C., et al. Transcriptional activation and chromatin remodeling of the HIV-1 promoter in response to histone acetylation. EMBO J. 1996, 15:1112-1120.
17. Shogren-Knaak M., et al. Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 2006, 311:844-847.
18. Mujtaba S., et al. Structure and acetyl-lysine recognition of the bromodomain. Oncogene 2007, 26:5521-5527.
19. Allis C.D., et al. New nomenclature for chromatin-modifying enzymes. Cell 2007, 131:633-636.
20. Gregoretti I.V., et al. Molecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis. J. Mol. Biol. 2004, 338:17-31.
21. Yang X.J., Seto E. The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat. Rev. Mol. Cell Biol. 2008, 9:206-218.
22. Verdin E., et al. Class II histone deacetylases: versatile regulators. Trends Genet. 2003, 19:286-293.
23. Michan S., Sinclair D. Sirtuins in mammals: insights into their biological function. Biochem. J. 2007, 404:1-13.
24. Ververis K., Karagiannis T.C. Potential non-oncological applications of histone deacetylase inhibitors. Am. J. Transl. Res. 2011, 3:454-467.
25. Kim H.J., Bae S.C. Histone deacetylase inhibitors: molecular mechanisms of action and clinical trials as anti-cancer drugs. Am. J. Transl. Res. 2011, 3:166-179.
26. Dokmanovic M., Marks P.A. Prospects: histone deacetylase inhibitors. J. Cell. Biochem. 2005, 96:293-304.
27. Choudhary C., et al. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 2009, 325:834-840.
28. Yang X.J., Seto E. Lysine acetylation: codified crosstalk with other posttranslational modifications. Mol. Cell 2008, 31:449-461.
29. 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. 1991, 65:6790-6799.
30. Margolis D.M., et al. Human transcription factor YY1 represses human immunodeficiency virus type 1 transcription and virion production. J. Virol. 1994, 68:905-910.
31. Romerio F., et al. Repression of human immunodeficiency virus type 1 through the novel cooperation of human factors YY1 and LSF. J. Virol. 1997, 71:9375-9382.
32. Marban C., et al. Recruitment of chromatin-modifying enzymes by CTIP2 promotes HIV-1 transcriptional silencing. EMBO J. 2007, 26:412-423.
33. Tyagi M., Karn J. CBF-1 promotes transcriptional silencing during the establishment of HIV-1 latency. EMBO J. 2007, 26:4985-4995.
34. Williams S.A., Greene W.C. Regulation of HIV-1 latency by T-cell activation. Cytokine 2007, 39:63-74.
35. Jiang G., et al. c-Myc and Sp1 contribute to proviral latency by recruiting histone deacetylase 1 to the human immunodeficiency virus type 1 promoter. J. Virol. 2007, 81:10914-10923.
36. Malcolm T., et al. Induction of chromosomally integrated HIV-1 LTR requires RBF-2 (USF/TFII-I) and Ras/MAPK signaling. Virus Genes 2007, 35:215-223.
37. Barton K., Margolis D. Selective targeting of the repressive transcription factors YY1 and cMyc to disrupt quiescent human immunodeficiency viruses. AIDS Res. Hum. Retroviruses 2012, 29:289-298.
38. Kauder S.E., et al. Epigenetic regulation of HIV-1 latency by cytosine methylation. PLoS Pathog. 2009, 5:e1000495.
39. Blazkova J., et al. CpG methylation controls reactivation of HIV from latency. PLoS Pathog. 2009, 5:e1000554.
40. Ahringer J. NuRD and SIN3 histone deacetylase complexes in development. Trends Genet. 2000, 16:351-356.
41. Greer E.L., Shi Y. Histone methylation: a dynamic mark in health, disease and inheritance. Nat. Rev. Genet. 2012, 13:343-357.
42. du Chene I., et al. Suv39H1 and HP1gamma are responsible for chromatin-mediated HIV-1 transcriptional silencing and post-integration latency. EMBO J. 2007, 26:424-435.
43. Imai K., et al. Involvement of histone H3 lysine 9 (H3K9) methyltransferase G9a in the maintenance of HIV-1 latency and its reactivation by BIX01294. J. Biol. Chem. 2010, 285:16538-16545.
44. Friedman J., et al. Epigenetic silencing of HIV-1 by the histone H3 lysine 27 methyltransferase enhancer of Zeste 2. J. Virol. 2011, 85:9078-9089.
45. + T cells from infected individuals receiving antiretroviral therapy. J. Virol. 2012, 86:5390-5392.
46. Henderson A., et al. Recruitment of SWI/SNF to the human immunodeficiency virus type 1 promoter. Mol. Cell. Biol. 2004, 24:389-397.
47. Gatignol A. Transcription of HIV: Tat and cellular chromatin. Adv. Pharmacol. 2007, 55:137-159.
48. Ott M., et al. Acetylation of the HIV-1 Tat protein by p300 is important for its transcriptional activity. Curr. Biol. 1999, 9:1489-1492.
49. Hang C.T., et al. Chromatin regulation by Brg1 underlies heart muscle development and disease. Nature 2010, 466:62-67.
50. Chen L.F., Greene W.C. Shaping the nuclear action of NF-kappaB. Nat. Rev. Mol. Cell Biol. 2004, 5:392-401.
51. Chen L., et al. Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science 2001, 293:1653-1657.
52. Chen L.F., et al. Acetylation of RelA at discrete sites regulates distinct nuclear functions of NF-kappaB. EMBO J. 2002, 21:6539-6548.
53. Ryu H., et al. Histone deacetylase inhibitors prevent oxidative neuronal death independent of expanded polyglutamine repeats via an Sp1-dependent pathway. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:4281-4286.
54. Ott M., et al. The control of HIV transcription: keeping RNA polymerase II on track. Cell Host Microbe 2011, 10:426-435.
55. Huo L., et al. Regulation of Tat acetylation and transactivation activity by the microtubule-associated deacetylase HDAC6. J. Biol. Chem. 2011, 286:9280-9286.
56. Mahmoudi T., et al. The SWI/SNF chromatin-remodeling complex is a cofactor for Tat transactivation of the HIV promoter. J. Biol. Chem. 2006, 281:19960-19968.
57. Pagans S., et al. SIRT1 regulates HIV transcription via Tat deacetylation. PLoS Biol. 2005, 3:e41.
58. Weinberger L.S., et al. Transient-mediated fate determination in a transcriptional circuit of HIV. Nat. Genet. 2008, 40:466-470.
59. Van Lint C., et al. The expression of a small fraction of cellular genes is changed in response to histone hyperacetylation. Gene Exp. 1996, 5:245-253.
60. Peart M.J., et al. Identification and functional significance of genes regulated by structurally different histone deacetylase inhibitors. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:3697-3702.
61. Lehrman G., et al. Depletion of latent HIV-1 infection in vivo: a proof-of-concept study. Lancet 2005, 366:549-555.
62. + T cells. AIDS 2008, 22:1131-1135.
63. Sagot-Lerolle N., et al. Prolonged valproic acid treatment does not reduce the size of latent HIV reservoir. AIDS 2008, 22:1125-1129.
64. + cell infection. PLoS ONE 2010, 5:e9390.
65. Routy J.P., et al. Valproic acid in association with highly active antiretroviral therapy for reducing systemic HIV-1 reservoirs: results from a multicentre randomized clinical study. HIV Med. 2012, 13:291-296.
66. Richon V.M., et al. A class of hybrid polar inducers of transformed cell differentiation inhibits histone deacetylases. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:3003-3007.
67. Wightman F., et al. HDAC inhibitors in HIV. Immunol. Cell Biol. 2012, 90:47-54.
68. Archin N.M., et al. Administration of vorinostat disrupts HIV-1 latency in patients on antiretroviral therapy. Nature 2012, 487:482-485.
69. Reuse S., et al. Synergistic activation of HIV-1 expression by deacetylase inhibitors and prostratin: implications for treatment of latent infection. PLoS ONE 2009, 4:e6093.
70. Archin N.M., et al. Expression of latent HIV induced by the potent HDAC inhibitor suberoylanilide hydroxamic acid. AIDS Res. Hum. Retroviruses 2009, 25:207-212.
71. Tan J., et al. Novel histone deacetylase inhibitors in clinical trials as anti-cancer agents. J. Hematol. Oncol. 2010, 3:5.
72. + T-cells and monocytes and is superior to valproic acid for latent HIV-1 expression in vitro. J. Acquir. Immune Defic. Syndr. 2010, 54:1-9.
73. Atadja P. Development of the pan-DAC inhibitor panobinostat (LBH589): successes and challenges. Cancer Lett. 2009, 280:233-241.
74. Keedy K.S., et al. A limited group of class I histone deacetylases acts to repress human immunodeficiency virus type 1 expression. J. Virol. 2009, 83:4749-4756.
75. Boumber Y., et al. Mocetinostat (MGCD0103): a review of an isotype-specific histone deacetylase inhibitor. Expert Opin. Investig. Drugs 2011, 20:823-829.
76. Furumai R., et al. FK228 (depsipeptide) as a natural prodrug that inhibits class I histone deacetylases. Cancer Res. 2002, 62:4916-4921.
77. Archin N.M., et al. Expression of latent human immunodeficiency type 1 is induced by novel and selective histone deacetylase inhibitors. AIDS 2009, 23:1799-1806.
78. Williams S.A., et al. Prostratin antagonizes HIV latency by activating NF-kappaB. J. Biol. Chem. 2004, 279:42008-42017.
79. Doyon G., et al. Disulfiram reactivates latent HIV-1 expression through depletion of the phosphatase and tensin homolog. AIDS 2013, 27:F7-F11.
80. + T cell model without inducing global T cell activation. J. Virol. 2011, 85:6060-6064.
81. Contreras X., et al. Suberoylanilide hydroxamic acid reactivates HIV from latently infected cells. J. Biol. Chem. 2009, 284:6782-6789.
82. + T cells from HIV-1-infected HAART-treated patients. AIDS 2012, 26:1473-1482.
83. Montoya-Durango D.E., et al. Epigenetic control of mammalian LINE-1 retrotransposon by retinoblastoma proteins. Mutat. Res. 2009, 665:20-28.
84. Shan L., et al. Stimulation of HIV-1-specific cytolytic T lymphocytes facilitates elimination of latent viral reservoir after virus reactivation. Immunity 2012, 36:491-501.