Selective Histonedeacetylase Inhibitor M344 Intervenes in HIV-1 Latency through Increasing Histone Acetylation and Activation of NF-kappaB

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Ying, Hao ^a   Zhang, Yuhao ^a   Zhou, Xin ^a   Qu, Xiying ^a   Wang, Pengfei ^a   Liu, Sijie ^a   Lu, Daru ^a   Zhu, Huanzhang ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

4 DIMETHYLAMINO N (6 HYDROXYCARBAMOYL HEXYL)BENZAMIDE; ANTIVIRUS AGENT; HISTONE DEACETYLASE INHIBITOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; M 344; PROSTRATIN; UNCLASSIFIED DRUG;

ACETYLATION; ANIMAL CELL; ARTICLE; CD4+ T LYMPHOCYTE; CELL VIABILITY; CONTROLLED STUDY; DNA BINDING; DRUG POTENCY; DRUG POTENTIATION; ENZYME ACTIVATION; FLUORESCENCE MICROSCOPY; GENE TRANSLOCATION; HISTONE ACETYLATION; HISTONE MODIFICATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOPRECIPITATION; LATENT PERIOD; LONG TERMINAL REPEAT; NONHUMAN; NUCLEOSOME; PROMOTER REGION; VIRUS REACTIVATION;

ACETYLATION; ACTIVE TRANSPORT, CELL NUCLEUS; BLOTTING, WESTERN; CHROMATIN IMMUNOPRECIPITATION; DNA PRIMERS; DRUG SYNERGISM; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, VIRAL; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HISTONE DEACETYLASE INHIBITORS; HISTONES; HIV LONG TERMINAL REPEAT; HIV-1; HUMANS; HYDROXAMIC ACIDS; IMMUNOHISTOCHEMISTRY; JURKAT CELLS; MICROSCOPY, FLUORESCENCE; NF-KAPPA B; PHORBOL ESTERS; PROPIDIUM; VIRUS LATENCY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84869221336     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0048832     Document Type: Article

References (94)

1. Davey RT, Bhat N, Yoder C, Chun TW, Metcalf JA, et al. (1999) HIV-1 and T cell dynamics after interruption of highly active antiretroviral therapy (HAART) in patients with a history of sustained viral suppression. Proceedings of the National Academy of Sciences 96: 15109-14.
2. Persaud D, Zhou Y, Siliciano JM, Siliciano RF, (2003) Latency in human immunodeficiency virus type 1 infection: no easy answers. J Virol 77: 1659-65.
3. Chun TW, Stuyver L, Mizell SB, Ehler LA, Mican JAM, et al. (1997) Presence of an inducible HIV-1 latent reservoir during highly active antiretroviral therapy. Proceedings of the National Academy of Sciences 94: 13193-7.
4. Finzi D, Hermankova M, Pierson T, Carruth LM, Buck C, et al. (1997) Identification of a reservoir for HIV-1 in patients on highly active antiretroviral therapy. Science 278: 1295-300.
5. Wong JK, Hezareh M, Gunthard HF, Havlir DV, Ignacio CC, et al. (1997) Recovery of replication-competent HIV despite prolonged suppression of plasma viremia. Science 278: 1291-5.
6. Finzi D, Blankson J, Siliciano JD, Margolick JB, Chadwick K, et al. (1999) Latent infection of CD4+ T cells provides a mechanism for lifelong persistence of HIV-1, even in patients on effective combination therapy. Nat Med 5: 512-7.
7. Zhang L, Ramratnam B, Tenner-Racz K, He Y, Vesanen M, et al. (1999) Quantifying residual HIV-1 replication in patients receiving combination antiretroviral therapy. New Engl J Med 340: 1605-13.
8. Ramratnam B, Mittler JE, Zhang L, Boden D, Hurley A, et al. (2000) The decay of the latent reservoir of replication-competent HIV-1 is inversely correlated with the extent of residual viral replication during prolonged anti-retroviral therapy. Nat Med 6: 82-5.
9. Siliciano JD, Kajdas J, Finzi D, Quinn TC, Chadwick K, et al. (2003) Long-term follow-up studies confirm the stability of the latent reservoir for HIV-1 in resting CD4+ T cells. Nat Med 9: 727-8.
10. Strain MC, Gunthard HF, Havlir DV, Ignacio CC, Smith DM, et al. (2003) Heterogeneous clearance rates of long-lived lymphocytes infected with HIV: intrinsic stability predicts lifelong persistence. Proceedings of the National Academy of Sciences 100: 4819-24.
11. Lassen K, Han Y, Zhou Y, Siliciano J, Siliciano RF, (2004) The multifactorial nature of HIV-1 latency. Trends Mol Med 10: 525-31.
12. Trono D, Van Lint C, Rouzioux C, Verdin E, Barré-Sinoussi F, et al. (2010) HIV persistence and the prospect of long-term drug-free remissions for HIV-infected individuals. Science 329: 174-80.
13. Coiras M, Lopez-Huertas MR, Pérez-Olmeda M, Alcamí J, (2009) Understanding HIV-1 latency provides clues for the eradication of long-term reservoirs. Nature Reviews Microbiology 7: 798-812.
14. Winslow BJ, Pomerantz RJ, Bagasra O, Trono D, (1993) HIV-1 latency due to the site of proviral integration. Virology 196: 849-54.
15. Han Y, Lin YB, An W, Xu J, Yang HC, et al. (2008) Orientation-dependent regulation of integrated HIV-1 expression by host gene transcriptional readthrough. Cell host & microbe 4: 134-46.
16. Wang GP, Ciuffi A, Leipzig J, Berry CC, Bushman FD, (2007) HIV integration site selection: analysis by massively parallel pyrosequencing reveals association with epigenetic modifications. Genome Res 17: 1186-94.
17. du Chéné I, Basyuk E, Lin YL, Triboulet R, Knezevich A, et al. (2007) Suv39H1 and HP1γ are responsible for chromatin-mediated HIV-1 transcriptional silencing and post-integration latency. The EMBO journal 26: 424-35.
18. Lusic M, Marcello A, Cereseto A, Giacca M, (2003) Regulation of HIV-1 gene expression by histone acetylation and factor recruitment at the LTR promoter. The EMBO Journal 22: 6550-61.
19. Coull JJ, Romerio F, Sun JM, Volker JL, Galvin KM, et al. (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: 6790-9.
20. Ylisastigui L, Coull JJ, Rucker VC, Melander C, Bosch RJ, et al. (2004) Polyamides reveal a role for repression in latency within resting T cells of HIV-infected donors. J Infect Dis 190: 1429-37.
21. Williams SA, Chen LF, Kwon H, Ruiz-Jarabo CM, Verdin E, et al. (2005) NF-κB p50 promotes HIV latency through HDAC recruitment and repression of transcriptional initiation. The EMBO journal 25: 139-49.
22. Tyagi M, Karn J, (2007) CBF-1 promotes transcriptional silencing during the establishment of HIV-1 latency. The EMBO Journal 26: 4985-95.
23. Triboulet R, Mari B, Lin YL, Chable-Bessia C, Bennasser Y, et al. (2007) Suppression of microRNA-silencing pathway by HIV-1 during virus replication. Science 315: 1579-82.
24. Huang J, Wang F, Argyris E, Chen K, Liang Z, et al. (2007) Cellular microRNAs contribute to HIV-1 latency in resting primary CD4+ T lymphocytes. Nat Med 13: 1241-7.
25. Han Y, Siliciano RF, (2007) Keeping quiet. microRNAs in HIV-1 latency. Nat Med 13: 1138-40.
26. Pagans S, Pedal A, North BJ, Kaehlcke K, Marshall BL, et al. (2005) SIRT1 regulates HIV transcription via Tat deacetylation. PLoS biology 3: e41.
27. Sabo A, Lusic M, Cereseto A, Giacca M, (2008) Acetylation of conserved lysines in the catalytic core of cyclin-dependent kinase 9 inhibits kinase activity and regulates transcription. Mol Cell Biol 28: 2201-12.
28. Boulanger MC, Liang C, Russell RS, Lin R, Bedford MT, et al. (2005) Methylation of Tat by PRMT6 regulates human immunodeficiency virus type 1 gene expression. J Virol 79: 124-31.
29. Xie B, Invernizzi CF, Richard S, Wainberg MA, (2007) Arginine methylation of the human immunodeficiency virus type 1 Tat protein by PRMT6 negatively affects Tat interactions with both cyclin T1 and the Tat transactivation region. J Virol 81: 4226-34.
30. Chun TW, Engel D, Mizell SB, Ehler LA, Fauci AS, (1998) Induction of HIV-1 replication in latently infected CD4+ T cells using a combination of cytokines. The Journal of experimental medicine 188: 83-91.
31. Marsden MD, Zack JA, (2009) Eradication of HIV: current challenges and new directions. J Antimicrob Chemoth 63: 7-10.
32. Colin L, Van Lint C, (2009) Molecular control of HIV-1 postintegration latency: implications for the development of new therapeutic strategies. Retrovirology 6: 111.
33. Richman DD, Margolis DM, Delaney M, Greene WC, Hazuda D, et al. (2009) The challenge of finding a cure for HIV infection. Science 323: 1304-7.
34. Stellbrink HJ, van Lunzen J, Westby M, O'Sullivan E, Schneider C, et al. (2002) Effects of interleukin-2 plus highly active antiretroviral therapy on HIV-1 replication and proviral DNA (COSMIC trial). AIDS 16: 1479-87.
35. Van Praag RME, Prins JM, Roos MTL, Schellekens PTA, Ten Berge IJM, et al. (2001) OKT3 and IL-2 treatment for purging of the latent HIV-1 reservoir in vivo results in selective long-lasting CD4+ T cell depletion. J Clin Immunol 21: 218-26.
36. Klichko V, Archin N, Kaur R, Lehrman G, Margolis D, (2006) Hexamethylbisacetamide remodels the human immunodeficiency virus type 1 (HIV-1) promoter and induces Tat-independent HIV-1 expression but blunts cell activation. J Virol 80: 4570-9.
37. Kutsch O, Benveniste EN, Shaw GM, Levy DN, (2002) Direct and quantitative single-cell analysis of human immunodeficiency virus type 1 reactivation from latency. J Virol 76: 8776-86.
38. Van Lint C, Emiliani S, Ott M, Verdin E, (1996) Transcriptional activation and chromatin remodeling of the HIV-1 promoter in response to histone acetylation. The EMBO journal 15: 1112-20.
39. Quivy V, Adam E, Collette Y, Demonte D, Chariot A, et al. (2002) Synergistic activation of human immunodeficiency virus type 1 promoter activity by NF-κB and inhibitors of deacetylases: potential perspectives for the development of therapeutic strategies. J Virol 76: 11091-103.
40. Adam E, Quivy V, Bex F, Chariot A, Collette Y, et al. (2003) Potentiation of tumor necrosis factor-induced NF-κB activation by deacetylase inhibitors is associated with a delayed cytoplasmic reappearance of IκBκ. Mol Cell Biol 23: 6200-9.
41. Nunnari G, Pomerantz RJ, (2005) IL-7 as a potential therapy for HIV-1-infected individuals. Expert Opin. Biol. Ther 5: 1421-6.
42. Scripture-Adams DD, Brooks DG, Korin YD, Zack JA, (2002) Interleukin-7 induces expression of latent human immunodeficiency virus type 1 with minimal effects on T-cell phenotype. J Virol 76: 13077-82.
43. Wang FX, Xu Y, Sullivan J, Souder E, Argyris EG, et al. (2005) IL-7 is a potent and proviral strain-specific inducer of latent HIV-1 cellular reservoirs of infected individuals on virally suppressive HAART. J Clin Invest 115: 128-37.
44. Williams SA, Chen LF, Kwon H, Fenard D, Bisgrove D, et al. (2004) Prostratin antagonizes HIV latency by activating NF-κB. J Biol Chem 279: 42008-17.
45. Korin YD, Brooks DG, Brown S, Korotzer A, Zack JA, (2002) Effects of prostratin on T-cell activation and human immunodeficiency virus latency. J Virol 76: 8118-23.
46. Kulkosky J, Culnan DM, Roman J, Dornadula G, Schnell M, et al. (2001) Prostratin: activation of latent HIV-1 expression suggests a potential inductive adjuvant therapy for HAART. Blood 98: 3006-15.
47. Lehrman G, Hogue IB, Palmer S, Jennings C, Spina CA, et al. (2005) Depletion of latent HIV-1 infection in vivo: a proof-of-concept study. The Lancet 366: 549-55.
48. Ylisastigui L, Archin NM, Lehrman G, Bosch RJ, Margolis DM, (2004) Coaxing HIV-1 from resting CD4 T cells: histone deacetylase inhibition allows latent viral expression. Aids 18: 1101-8.
49. Archin NM, Espeseth A, Parker D, Cheema M, Hazuda D, et al. (2009) Expression of latent HIV induced by the potent HDAC inhibitor suberoylanilide hydroxamic acid. Aids Res Hum Retrov 25: 207-12.
50. Archin NM, Keedy KS, Espeseth A, Dang H, Hazuda DJ, et al. (2009) Expression of latent human immunodeficiency type 1 is induced by novel and selective histone deacetylase inhibitors. Aids 23: 1799-806.
51. Shehu-Xhilaga M, Rhodes D, Wightman F, Liu HB, Solomon A, et al. (2009) The novel histone deacetylase inhibitors metacept-1 and metacept-3 potently increase HIV-1 transcription in latently infected cells. Aids 23: 2047-50.
52. Savarino A, Mai A, Norelli S, El Daker S, Valente S, et al. (2009) "Shock and kill" effects of class I-selective histone deacetylase inhibitors in combination with the glutathione synthesis inhibitor buthionine sulfoximine in cell line models for HIV-1 quiescence. Retrovirology 6: 1-10.
53. Choudhary SK, Archin NM, Margolis DM, (2008) Hexamethylbisacetamide and disruption of human immunodeficiency virus type 1 latency in CD4+ T cells. J Infect Dis 197: 1162-70.
54. Contreras X, Barboric M, Lenasi T, Peterlin BM, (2007) HMBA releases P-TEFb from HEXIM1 and 7SK snRNA via PI3K/Akt and activates HIV transcription. PLoS pathogens 3: e146.
55. Heltweg B, Dequiedt F, Marshall BL, Brauch C, Yoshida M, et al. (2004) Subtype selective substrates for histone deacetylases. J Med Chem 47: 5235-43.
56. Takai N, Ueda T, Nishida M, Nasu K, Narahara H, (2006) M344 is a novel synthesized histone deacetylase inhibitor that induces growth inhibition, cell cycle arrest, and apoptosis in human endometrial cancer and ovarian cancer cells. Gynecol Oncol 101: 108-13.
57. Furchert SE, Lanvers-Kaminsky C, Juürgens H, Jung M, et al. (2007) Inhibitors of histone deacetylases as potential therapeutic tools for high-risk embryonal tumors of the nervous system of childhood. Int J Cancer 120: 1787-94.
58. Palijan A, Fernandes I, Bastien Y, Tang L, Verway M, et al. (2009) Function of histone deacetylase 6 as a cofactor of nuclear receptor coregulator LCoR. J Biol Chem 284: 30264-74.
59. Li X, Chen BD, (2009) Histone deacetylase inhibitor M344 inhibits cell proliferation and induces apoptosis in human THP-1 leukemia cells. American journal of biomedical sciences 1: 352-63.
60. Kutuk O, Basaga H, (2004) Aspirin inhibits TNFalpha- and IL-1-induced NF-kappaB activation and sensitizes HeLa cells to apoptosis. Cytokine. 25: 229-37.
61. Zhu G, Cai J, Zhang J, Zhao Y, Xu B, (2007) Abnormal nuclear factor (NF)-kappaB signal pathway and aspirin inhibits tumor necrosis factor alpha-induced NF-kappaB activation in keloid fibroblasts. Dermatol Surg. 33: 697-708.
62. Emiliani S, Fischle W, Ott M, Van Lint C, Amella CA, et al. (1998) Mutations in the tat gene are responsible for human immunodeficiency virus type 1 postintegration latency in the U1 cell line. J Virol 72: 1666-70.
63. Emiliani S, Van Lint C, Fischle W, Paras P, Ott M, et al. (1996) A point mutation in the HIV-1 Tat responsive element is associated with postintegration latency. Proceedings of the National Academy of Sciences 93: 6377-81.
64. Jordan A, Bisgrove D, Verdin E, (2003) HIV reproducibly establishes a latent infection after acute infection of T cells in vitro. The EMBO journal 22: 1868-77.
65. Jordan A, Defechereux P, Verdin E, (2001) The site of HIV-1 integration in the human genome determines basal transcriptional activity and response to Tat transactivation. The EMBO journal 20: 1726-38.
66. Sheridan PL, Mayall TP, Verdin E, Jones KA, (1997) Histone acetyltransferases regulate HIV-1 enhancer activity in vitro. Gene Dev 11: 3327-40.
67. Duverger A, Jones J, May J, Bibollet-Ruche F, Wagner FA, et al. (2009) Determinants of the establishment of human immunodeficiency virus type 1 latency. J Virol 83: 3078-93.
68. Dokmanovic M, Clarke C, Marks PA, (2007) Histone deacetylase inhibitors: overview and perspectives. Molecular cancer research 5: 981-9.
69. Bolden JE, Peart MJ, Johnstone RW, (2006) Anticancer activities of histone deacetylase inhibitors. Nat Rev Drug Discov 5: 769-84.
70. De Ruijter AJM, Van Gennip AH, Caron HN, Kemp S, Van Kuilenburg ABP, (2003) Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem J 370: 737-49.
71. Verdin E, Dequiedt F, Kasler HG, (2003) Class II histone deacetylases: versatile regulators. Trends Genet 19: 286-93.
72. Mai A, (2007) The therapeutic uses of chromatin-modifying agents. Expert Opin. Ther. Targets 11: 835-51.
73. Huber K, Doyon G, Plaks J, Fyne E, Mellors JW, et al. (2011) Inhibitors of histone deacetylases: correlation between isoform specificity and reactivation of HIV type 1 (HIV-1) from latently infected cells. J Biol Chem 286: 22211-8.
74. Greene, W. C. Peterlin BM, (2002) Charting HIV's remarkable voyage through the cell: basic science as a passport to future therapy. Nat Med 8: 673-80.
75. Verdin E, Paras Jr P, Van Lint C, (1993) Chromatin disruption in the promoter of human immunodeficiency virus type 1 during transcriptional activation. The EMBO journal 12: 3249-59.
76. Henderson A, Holloway A, Reeves R, Tremethick DJ, (2004) Recruitment of SWI/SNF to the human immunodeficiency virus type 1 promoter. Mol Cell Biol 24: 389-97.
77. Tréand C, Du Chéné I, Brès V, Kiernan R, Benarous R, et al. (2006) Requirement for SWI/SNF chromatin-remodeling complex in Tat-mediated activation of the HIV-1 promoter. The EMBO journal 25: 1690-9.
78. Mahmoudi T, Parra M, Vries RGJ, Kauder SE, Verrijzer CP, et al. (2006) The SWI/SNF chromatin-remodeling complex is a cofactor for Tat transactivation of the HIV promoter. J Biol Chem 281: 19960-8.
79. He G, Margolis DM, (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: 2965-73.
80. Imai K, Okamoto T, (2006) Transcriptional repression of human immunodeficiency virus type 1 by AP-4. J Biol Chem 281: 12495-505.
81. Marban C, Suzanne S, Dequiedt F, De Walque S, Redel L, et al. (2007) Recruitment of chromatin-modifying enzymes by CTIP2 promotes HIV-1 transcriptional silencing. The EMBO journal 26: 412-23.
82. Jiang G, Espeseth A, Hazuda DJ, Margolis DM, (2007) c-Myc and Sp1 contribute to proviral latency by recruiting histone deacetylase 1 to the human immunodeficiency virus type 1 promoter. J Virol 81: 10914-23.
83. Malcolm T, Chen J, Chang C, Sadowski I, (2007) Induction of chromosomally integrated HIV-1 LTR requires RBF-2 (USF/TFII-I) and RAS/MAPK signaling. Virus Genes 35: 215-23.
84. Keedy KS, Archin NM, Gates AT, Espeseth A, Hazuda DJ, et al. (2009) A limited group of class I histone deacetylases acts to repress human immunodeficiency virus type 1 expression. J Virol 83: 4749-56.
85. Zhang W, Kone BC, (2002) NF-kappaB inhibits transcription of the H(+)-K(+)-ATPase alpha(2)-subunit gene: role of histone deacetylases. Am J Physiol Renal Physiol 283: 904-11.
86. Girdwood D, Bumpass D, Vaughan OA, Thain A, Anderson LA, et al. (2003) P300 transcriptional repression is mediated by SUMO modification. Mol Cell 11: 1043-54.
87. Sune C, Garcia-Blanco MA, (1995) 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: 6572-6.
88. Perkins ND, Edwards NL, Duckett CS, Agranoff AB, Schmid RM, et al. (1993) A cooperative interaction between NF-κB and Sp1 is required for HIV-1 enhancer activation. The EMBO journal 12: 3551-8.
89. Brummelkamp TR, Nijman SM, Dirac AM, Bernards R, (2003) Loss of the cylindromatosis tumour suppressor inhibits apoptosis by activating NF-kappaB. Nature. 424: 797-801.
90. Pande V, Ramos MJ, (2003) Nuclear factor kappa B: a potential target for anti-HIV chemotherapy.Curr Med Chem. 10: 1603-15.
91. Reuse S, Calao M, Kabeya K, Guiguen A, Gatot JS, et al. (2009) Synergistic activation of HIV-1 expression by deacetylase inhibitors and prostratin: implications for treatment of latent infection. PLoS One 4: e6093.
92. Burnett JC, Lim K, Calafi A, Rossi JJ, Schaffer DV, et al. (2010) Combinatorial latency reactivation for HIV-1 subtypes and variants. J Virol 84: 5958-74.
93. Bren GD, Whitman J, Cummins N, Shepard B, Rizza SA, et al. (2008) Infected cell killing by HIV-1 protease promotes NF-κB dependent HIV-1 replication. PloS One 3: e2112.
94. Kiefer HLB, Hanley TM, Marcello JE, Karthik AG, Viglianti GA, (2004) Retinoic acid inhibition of chromatin remodeling at the human immunodeficiency virus type 1 promoter. J Biol Chem 279: 43604-13.