Entinostat is a histone deacetylase inhibitor selective for class 1 histone deacetylases and activates HIV production from latently infected primary T cells

AIDS

Volumn 27, Issue 18, 2013, Pages 2853-2862

  Wightman, Fiona ^a   Lu, Hao K ^a   Solomon, Ajantha E ^a   Saleh, Suha ^a   Harman, Andrew N ^b   Cunningham, Anthony L ^b   Gray, Lachlan ^a   Churchill, Melissa ^a   Cameron, Paul U ^a,c   Dear, Anthony E ^a   Lewin, Sharon R ^a,c  

^a MONASH UNIVERSITY   (Australia)

^b WESTMEAD HOSPITAL   (Australia)

^c ALFRED HOSPITAL   (Australia)

Author keywords

Histone deacetylase; HIV; Primary model of latency; Viral latency

Indexed keywords

CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR4; ENTINOSTAT; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE 3; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; PANOBINOSTAT; VORINOSTAT; BENZAMIDE DERIVATIVE; HISTONE DEACETYLASE INHIBITOR; PYRIDINE DERIVATIVE;

ARTICLE; CD4+ T LYMPHOCYTE; CELL LINE; CELL VIABILITY; CHROMATIN IMMUNOPRECIPITATION; CYTOTOXICITY; DRUG MECHANISM; DRUG POTENCY; DRUG SELECTIVITY; HUMAN IMMUNODEFICIENCY VIRUS; IN VITRO STUDY; LONG TERMINAL REPEAT; NONHUMAN; PRIMARY INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; T LYMPHOCYTE ACTIVATION; VIRUS LATENCY; VIRUS REPLICATION; CELL CULTURE; DRUG EFFECTS; HUMAN; PHYSIOLOGY; POLYMERASE CHAIN REACTION; VIROLOGY; WESTERN BLOTTING;

BENZAMIDES; BLOTTING, WESTERN; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; HISTONE DEACETYLASE INHIBITORS; HIV; HUMANS; POLYMERASE CHAIN REACTION; PYRIDINES; VIRUS LATENCY; VIRUS REPLICATION;

EID: 84888293183     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0000000000000067     Document Type: Article

References (44)

1. Siliciano JD, Kajdas J, Finzi D, Quinn TC, Chadwick K, Margolick JB, et al. Long-term follow-up studies confirm the stability of the latent reservoir for HIV-1 in resting CD4R T cells. Nat Med 2003; 9:727-728.
2. Chomont N, El-Far M, Ancuta P, Trautmann L, Procopio FA, Yassine-Diab B, et al. HIV reservoir size and persistence are driven by T cell survival and homeostatic proliferation. Nat Med 2009; 15:893-900.
3. Smith MZ, Wightman F, Lewin S.R. HIV reservoirs and strategies for eradication. Curr HIV/AIDS Rep 2012; 9:5-15.
4. Archin NM, Liberty AL, Kashuba AD, Choudhary SK, Kuruc JD, Crooks AM, et al. Administration of vorinostat disrupts HIV-1 latency in patients on antiretroviral therapy. Nature 2012; 487:482-485.
5. Bowman MC, Archin NM, Margolis DM. Pharmaceutical approaches to eradication of persistent HIV infection. Expert Rev Mol Med 2009; 11:e6.
6. Wightman F, Ellenberg P, Churchill M, Lewin S.R. HDAC inhibitors in HIV. Immunol Cell Biol 2012; 90:47-54.
7. Bolden JE, Peart MJ, Johnstone RW. Anticancer activities of histone deacetylase inhibitors. Nat Rev Drug Discov 2006; 5:769-784.
8. 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 2009; 23:1799-1806.
9. Huber K, Doyon G, Plaks J, Fyne E, Mellors JW, Sluis-Cremer N. Inhibitors of histone deacetylases: correlation between isoform specificity and reactivation of HIV type 1 (HIV-1) from latently infected cells. J Biol Chem 2011; 286:22211-22218.
10. 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 2009; 83:4749-4756.
11. Khan N, Jeffers M, Kumar S, Hackett C, Boldog F, Khramtsov N, et al. Determination of the class and isoform selectivity of small-molecule histone deacetylase inhibitors. Biochem J 2008; 409:581-589.
12. Tatamiya T, Saito A, Sugawara T, Nakanishi O. Isozymeselective activity of the HDAC inhibitor MS-275. Proceedings of the 95th Annual Meeting of the American Association for Cancer Research; March 27-31, 2004 Orlando, FL.
13. Pharma BS. Safety Data Sheet 91/155/EEC MS-275. Berlin, Germany.: Bayer Schering Pharma; 2007.
14. Pili R, Salumbides B, Zhao M, Altiok S, Qian D, Zwiebel J, et al. Phase I study of the histone deacetylase inhibitor entinostat in combination with 13-cis retinoic acid in patients with solid tumours. Br J Cancer 2012; 106:77-84.
15. Witta SE, Jotte RM, Konduri K, Neubauer MA, Spira AI, Ruxer RL, et al. Randomized phase II trial of erlotinib with and without entinostat in patients with advanced non-small-cell lung cancer who progressed on prior chemotherapy. J Clin Oncol 2012; 30:2248-2255.
16. Shen L, Ciesielski M, Ramakrishnan S, Miles KM, Ellis L, Sotomayor P, et al. Class I histone deacetylase inhibitor entinostat suppresses regulatory T cells and enhances immunotherapies in renal and prostate cancer models. PLoS One 2012; 7:e30815.
17. Deeks SG. HIV: shock and kill. Nature 2012; 487:439-440.
18. Cameron PU, Saleh S, Sallmann G, Solomon A, Wightman F, Evans VA, et al. Establishment of HIV-1 latency in resting CD4R T cells depends on chemokine-induced changes in the actin cytoskeleton. Proc Natl Acad Sci U S A 2010; 107: 16934-16939.
19. Saleh S, Solomon A, Wightman F, Xhilaga M, Cameron PU, Lewin S.R. CCR7 ligands CCL19 and CCL21 increase permissiveness of resting memory CD4R T cells to HIV-1 infection: A novel model of HIV-1 latency. Blood 2007; 110:4161-4164.
20. Lassen KG, Ramyar KX, Bailey JR, Zhou Y, Siliciano RF. Nuclear retention of multiply spliced HIV-1 RNA in resting CD4R T cells. PLoS Pathog 2006; 2:e68.
21. Saleh S, Wightman F, Ramanayake S, Alexander M, Kumar N, Khoury G, et al. Expression and reactivation of HIV in a chemokine induced model of HIV latency in primary resting CD4R T cells. Retrovirology 2011; 8:80.
22. Yang Z, Engel JD. Human T cell transcription factor GATA-3 stimulates HIV-1 expression. Nucleic Acids Res 1993; 21: 2831-2836.
23. Folks TM, Justement J, Kinter A, Dinarello CA, Fauci AS. Cytokine-induced expression of HIV-1 in a chronically infected promonocyte cell line. Science 1987; 238:800-802.
24. Jordan A, Bisgrove D, Verdin E. HIV reproducibly establishes a latent infection after acute infection of T cells in vitro. EMBO J 2003; 22:1868-1877.
25. Ouaissi M, Cabral S, Tavares J, da Silva AC, Mathieu Daude F, Mas E, et al. Histone deacetylase (HDAC) encoding gene expression in pancreatic cancer cell lines and cell sensitivity to HDAC inhibitors. Cancer Biol Ther 2008; 7:523-531.
26. Aung HT, Schroder K, Himes SR, Brion K, van Zuylen W, Trieu A, et al. LPS regulates proinflammatory gene expression in macrophages by altering histone deacetylase expression. FASEB J 2006; 20:1315-1327.
27. Garcia-Manero G, Yang H, Bueso-Ramos C, Ferrajoli A, Cortes J, Wierda WG, et al. Phase 1 study of the histone deacetylase inhibitor vorinostat (suberoylanilide hydroxamic acid [SAHA]) in patients with advanced leukemias and myelodysplastic syndromes. Blood 2008; 111:1060-1066.
28. Gore L, Rothenberg ML, OBryant CL, Schultz MK, Sandler AB, Coffin D, et al. A phase I and pharmacokinetic study of the oral histone deacetylase inhibitor, MS-275, in patients with refractory solid tumors and lymphomas. Clin Cancer Res 2008; 14: 4517-4525.
29. Giles F, Fischer T, Cortes J, Garcia-Manero G, Beck J, Ravandi F, et al. A phase I study of intravenous LBH589, a novel cinnamic hydroxamic acid analogue histone deacetylase inhibitor, in patients with refractory hematologic malignancies. Clin Cancer Res 2006; 12:4628-4635.
30. Wang FX, Xu Y, Sullivan J, Souder E, Argyris EG, Acheampong EA, et al. 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 2005; 115:128-137.
31. Paroni G, Cernotta N, Dello Russo C, Gallinari P, Pallaoro M, Foti C, et al. PP2A regulates HDAC4 nuclear import. Mol Biol Cell 2008; 19:655-667.
32. Ungerstedt JS, Sowa Y, Xu WS, Shao Y, Dokmanovic M, Perez G, et al. Role of thioredoxin in the response of normal and transformed cells to histone deacetylase inhibitors. Proc Natl Acad Sci U S A 2005; 102:673-678.
33. Purrucker JC, Mahlknecht U. Targeting the epigenome: effects of epigenetic treatment strategies on genomic stability in healthy human cells. Clin Epigenetics 2010; 1:45-54.
34. Palmisano I, Della Chiara G, DAmbrosio RL, Huichalaf C, Brambilla P, Corbetta S, et al. Amino acid starvation induces reactivation of silenced transgenes and latent HIV-1 provirus via down-regulation of histone deacetylase 4 (HDAC4). Proc Natl Acad Sci U S A 2012; 109:E2284-E2293.
35. Savarino A, Mai A, Norelli S, El Daker S, Valente S, Rotili D, et al. 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 2009; 6:52.
36. Reuse S, Calao M, Kabeya K, Guiguen A, Gatot J-Sp, Quivy V, et al. Synergistic activation of HIV-1 expression by deacetylase inhibitors and prostratin: Implications for treatment of latent infection. PLoS One 2009; 4:e6093.
37. Dickinson M, Johnstone RW, Prince HM. Histone deacetylase inhibitors: potential targets responsible for their anticancer effect. Invest New Drugs 2010; 28 (Suppl 1):S3-S20.
38. Molife LR, de Bono JS. Belinostat: clinical applications in solid tumors and lymphoma. Expert Opin Investig Drugs 2011; 20: 1723-1732.
39. Matalon S, Palmer BE, Nold MF, Furlan A, Kassu A, Fossati G, et al. The histone deacetylase inhibitor ITF2357 decreases surface CXCR4 and CCR5 expression on CD4(R) 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.
40. Burnett JC, Lim KI, Calafi A, Rossi JJ, Schaffer DV, Arkin AP. Combinatorial latency reactivation for HIV-1 subtypes and variants. J Virol 2010; 84:5958-5974.
41. Xing S, Bullen CK, Shroff NS, Shan L, Yang HC, Manucci JL, et al. Disulfiram reactivates latent HIV-1 in a Bcl-2-transduced primary CD4R T cell model without inducing global T cell activation. J Virol 2011; 85:6060-6064.
42. Ying H, Zhang Y, Lin S, Han Y, Zhu HZ. Histone deacetylase inhibitor Scriptaid reactivates latent HIV-1 promoter by inducing histone modification in in vitro latency cell lines. Int J Mol Med 2010; 26:265-272.
43. 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 2009; 25:207-212.
44. Contreras X, Schweneker M, Chen CS, McCune JM, Deeks SG, Martin J, et al. Suberoylanilide hydroxamic acid reactivates HIV from latently infected cells. J Biol Chem 2009; 284:6782-6789.