Preclinical shock strategies to reactivate latent HIV-1: An update

Current Opinion in HIV and AIDS

Volumn 11, Issue 4, 2016, Pages 388-393

  Darcis, Gilles ^a,b   Van Driessche, Benoît ^a   Van Lint, Carine ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

HIV 1 latency; latency reversing agents; shock strategy; transcriptional regulation

Indexed keywords

HISTONE DEACETYLASE INHIBITOR; POSITIVE TRANSCRIPTION ELONGATION FACTOR B; PROTEIN KINASE C; ANTIVIRUS AGENT;

DNA METHYLATION; EPIGENETICS; HETEROCHROMATIN; HISTONE MODIFICATION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IN VITRO STUDY; NONHUMAN; PRIMARY CELL; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; SHOCK; T LYMPHOCYTE ACTIVATION; T WAVE; VIRUS TRANSCRIPTION; COMBINATION DRUG THERAPY; DRUG EFFECTS; GENETIC TRANSCRIPTION; HIV INFECTIONS; PHYSIOLOGY; PROCEDURES; VIROLOGY; VIRUS ACTIVATION; VIRUS LATENCY;

ANTIVIRAL AGENTS; DRUG THERAPY, COMBINATION; HIV INFECTIONS; HIV-1; HUMANS; TRANSCRIPTION, GENETIC; VIRUS ACTIVATION; VIRUS LATENCY;

EID: 84973129753     PISSN: 1746630X     EISSN: 17466318     Source Type: Journal    
DOI: 10.1097/COH.0000000000000288     Document Type: Review

References (62)

1. Deeks SG. HIV: shock and kill. Nature 2012; 487:439-440.
2. Van Lint C, Bouchat S, Marcello A. HIV-1 transcription and latency: an update. Retrovirology 2013; 10:67.
3. Saayman S, Roberts TC, Morris KV, Weinberg MS. HIV latency and the noncoding RNA therapeutic landscape. Adv Exp Med Biol 2015; 848:169-189.
4. Cary DC, Fujinaga K, Peterlin BM. Molecular mechanisms of HIV latency. J Clin Invest 2016; 126:448-454.
5. Mbonye U, Karn J. Transcriptional control of HIV latency: cellular signaling pathways, epigenetics, happenstance and the hope for a cure. Virology 2014; 454-455; 328-39.
6. Yang G, Thompson MA, Brandt SJ, Hiebert SW. Histone deacetylase inhibitors induce the degradation of the t(8;21) fusion oncoprotein. Oncogene 2007; 26:91-101.
7. Colin L, Van Lint C. Molecular control of HIV-1 postintegration latency: implications for the development of new therapeutic strategies. Retrovirology 2009; 6:111.
8. Archin NM, Espeseth A, Parker D, et al. Expression of latent HIV induced by the potent HDAC inhibitor suberoylanilide hydroxamic acid. AIDS Res Hum Retroviruses 2009; 25:207-212.
9. Matalon S, Palmer BE, Nold MF, et al. The histone deacetylase inhibitor ITF2357 decreases surface CXCR4 and CCR5 expression on CD4+ 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.
10. Contreras X, Schweneker M, Chen CS, et al. Suberoylanilide hydroxamic acid reactivates HIVfromlatently infected cells. J BiolChem2009;284:6782-6789.
11. 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 2009; 4:e6093.
12. Quivy V, Adam E, Collette Y, et al. Synergistic activation of human immunodeficiency virus type 1 promoter activity by NF-kappaB and inhibitors of deacetylases: potential perspectives for the development of therapeutic strategies. J Virol 2002; 76:11091-11103.
13. Mates JM, de Silva S, Lustberg M, et al. A novel histone deacetylase inhibitor, AR-42, reactivates HIV-1 from chronically and latently infected CD4 T-cells. Retrovirology (Auckl) 2015; 7:1-5.
14. Wei DG, Chiang V, Fyne E, et al. Histone deacetylase inhibitor romidepsin induces HIV expression in CD4 T cells from patients on suppressive antiretroviral therapy at concentrations achieved by clinical dosing. PLoS Pathog 2014; 10:e1004071.
15. Bouchat S, Delacourt N, Kula A, et al. Sequential treatment with 5-aza-2'- deoxycytidine and deacetylase inhibitors reactivates HIV-1. EMBO Mol Med 2015; 8:117-138
16. Bullen CK, Laird GM, Durand CM, et al. New ex vivo approaches distinguish effective and ineffective single agents for reversing HIV-1 latency in vivo. Nat Med 2014; 20:425-429.
17. Cillo AR, Sobolewski MD, Bosch RJ, et al. Quantification of HIV-1 latency reversal in resting CD4+ T cells from patients on suppressive antiretroviral therapy. Proc Natl Acad Sci U S A 2014; 111:7078-7083.
18. Bartholomeeusen K, Fujinaga K, Xiang Y, Peterlin BM. Histone deacetylase inhibitors (HDACis) that release the positive transcription elongation factor b (P-TEFb) from its inhibitory complex also activate HIV transcription. J Biol Chem 2013; 288:14400-14407.
19. Jamaluddin MS, Hu PW, Jan Y, et al. Short communication: the broadspectrum histone deacetylase inhibitors vorinostat and panobinostat activate latent HIV in CD4+ T cells in part through phosphorylation of the T-loop of the CDK9 subunit of P-TEFb. AIDS Res Hum Retroviruses 2016; 32:169-173.
20. Marban C, Suzanne S, Dequiedt F, et al. Recruitment of chromatin-modifying enzymes by CTIP2 promotes HIV-1 transcriptional silencing. EMBO J 2007; 26:412-423.
21. Bouchat S, Gatot JS, Kabeya K, et al. Histone methyltransferase inhibitors induce HIV-1 recovery in resting CD4+ T cells from HIV-1-infected HAARTtreated patients. AIDS 2012; 26:1473-1482.
22. Imai K, Togami H, Okamoto T. 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.
23. Bernhard W, Barreto K, Saunders A, et al. The Suv39H1 methyltransferase inhibitor chaetocin causes induction of integrated HIV-1 without producing a T cell response. FEBS Lett 2011; 585:3549-3554.
24. Kauder SE, Bosque A, Lindqvist A, et al. Epigenetic regulation of HIV-1 latency by cytosine methylation. PLoS Pathog 2009; 5:e1000495.
25. Blazkova J, Trejbalova K, Gondois-Rey F, et al. CpG methylation controls reactivation of HIV from latency. PLoS Pathog 2009; 5:e1000554.
26. Blazkova J, Murray D, Justement JS, et al. Paucity of HIV DNA methylation in latently infected, resting CD4+ T cells from infected individuals receiving antiretroviral therapy. J Virol 2012; 86:5390-5392.
27. Palacios JA, Perez-Pinar T, Toro C, et al. Long-term nonprogressor and elite controller patients who control viremia have a higher percentage of methylation in their HIV-1 proviral promoters than aviremic patients receiving highly active antiretroviral therapy. J Virol 2012; 86:13081-13084.
28. Fujinaga K, Luo Z, Schaufele F, Peterlin BM. Visualization of positive transcription elongation factor b (P-TEFb) activation in living cells. J Biol Chem 2015; 290:1829-1836
29. Trushin SA, Bren GD, Asin S, et al. Human immunodeficiency virus reactivation by phorbol esters or T-cell receptor ligation requires both PKCalpha and PKCtheta. J Virol 2005; 79:9821-9830.
30. Fujinaga K, Barboric M, Li Q, et al. PKC phosphorylates HEXIM1 and regulates P-TEFb activity. Nucleic Acids Res 2012; 40:9160-9170.
31. Sung TL, Rice AP. Effects of prostratin on Cyclin T1/P-TEFb function and the gene expression profile in primary resting CD4+ T cells. Retrovirology 2006; 3:66.
32. Pandelo Jose D, Bartholomeeusen K, da Cunha RD, et al. Reactivation of latent HIV-1 by new semi-synthetic ingenol esters. Virology 2014; 462-463; 328-39.
33. Barboric M, Nissen RM, Kanazawa S, et al. NF-kappaB binds P-TEFb to stimulate transcriptional elongation by RNA polymerase II. Mol Cell 2001; 8:327-337.
34. Mehla R, Bivalkar-Mehla S, Zhang R, et al. Bryostatin modulates latent HIV-1 infection via PKC and AMPK signaling but inhibits acute infection in a receptor independent manner. PloS One 2010; 5:e11160.
35. Darcis G, Kula A, Bouchat S, et al. An in-depth comparison of latencyreversing agent combinations in various in vitro and ex vivo HIV-1 latency models identified bryostatin-1+JQ1 and ingenol-B+JQ1 to potently reactivate viral gene expression. PLoS Pathog 2015; 11:e1005063.
36. Diaz L, Martinez-Bonet M, Sanchez J, et al. Bryostatin activates HIV-1 latent expression in human astrocytes through a PKC and NF-kB-dependent mechanism. Sci Rep 2015; 5:12442.
37. Bocklandt S, Blumberg PM, Hamer DH. Activation of latent HIV-1 expression by the potent antitumor promoter 12-deoxyphorbol 13-phenylacetate. Antiviral Res 2003; 59:89-98.
38. Biancotto A, Grivel JC, Gondois-Rey F, et al. Dual role of prostratin in inhibition of infection and reactivation of human immunodeficiency virus from latency in primary blood lymphocytes and lymphoid tissue. J Virol 2004; 78:10507-10515.
39. Kulkosky J, Culnan DM, Roman J, et al. Prostratin: activation of latent HIV-1 expression suggests a potential inductive adjuvant therapy for HAART. Blood 2001; 98:3006-3015.
40. Korin YD, Brooks DG, Brown S, et al. Effects of prostratin on T-cell activation and human immunodeficiency virus latency. J Virol 2002; 76:8118-8123.
41. Williams SA, Chen LF, Kwon H, et al. Prostratin antagonizes HIV latency by activating NF-kappaB. J Biol Chem 2004; 279:42008-42017.
42. Abreu CM, Price SL, Shirk EN, et al. Dual role of novel ingenol derivatives from Euphorbia tirucalli in HIV replication: inhibition of de novo infection and activation of viral LTR. PloS One 2014; 9:e97257.
43. Jiang G, Mendes EA, Kaiser P, et al. Reactivation of HIV latency by a newly modified ingenol derivative via protein kinase Cdelta-NF-kappaB signaling. AIDS 2014; 28:1555-1566.
44. Jiang G, Mendes EA, Kaiser P, et al. Synergistic reactivation of latent HIV expression by ingenol-3-angelate, PEP005, targeted NF-kB signaling in combination with JQ1 induced p-TEFb activation. PLoS Pathog 2015; 11:e1005066
45. Jiang G, Dandekar S. Targeting NF-kappaB signaling with protein kinase C agonists as an emerging strategy for combating HIV latency. AIDS Res Hum Retroviruses 2015; 31:4-12.
46. Peterlin BM, Price DH. Controlling the elongation phase of transcription with P-TEFb. Mol Cell 2006; 23:297-305.
47. Budhiraja S, Famiglietti M, Bosque A, et al. Cyclin T1 and CDK9 T-loop phosphorylation are downregulated during establishment of HIV-1 latency in primary resting memory CD4+ T cells. J Virol 2013; 87:1211-1220.
48. Chiang K, Rice AP. MicroRNA-mediated restriction of HIV-1 in resting CD4+ T cells and monocytes. Viruses 2012; 4:1390-1409.
49. Chiang K, Sung TL, Rice AP. Regulation of cyclin T1 and HIV-1 Replication by microRNAs in resting CD4+ T lymphocytes. J Virol 2012; 86:3244-3252.
50. Hoque M, Shamanna RA, Guan D, et al. HIV-1 replication and latency are regulated by translational control of cyclin T1. J Mol Biol 2011; 410:917-932.
51. Bartholomeeusen K, Xiang Y, Fujinaga K, Peterlin BM. Bromodomain and extra-terminal (BET) bromodomain inhibition activate transcription via transient release of positive transcription elongation factor b (P-TEFb) from 7SK small nuclear ribonucleoprotein. J Biol Chem 2012; 287:36609-36616.
52. Banerjee C, Archin N, Michaels D, et al. BET bromodomain inhibition as a novel strategy for reactivation of HIV-1. J Leukoc Biol 2012; 92:1147-1154.
53. Boehm D, Calvanese V, Dar RD, et al. BET bromodomain-targeting compounds reactivate HIV from latency via a Tat-independent mechanism. Cell Cycle 2013; 12:452-462.
54. Zhu J, Gaiha GD, John SP, et al. Reactivation of latent HIV-1 by inhibition of BRD4. Cell Rep 2012; 2:807-816.
55. Li Z, Guo J, Wu Y, Zhou Q. The BET bromodomain inhibitor JQ1 activates HIV latency through antagonizing Brd4 inhibition of Tat-transactivation. Nucleic Acids Res 2013; 41:277-287.
56. Budhiraja S, Rice AP. Reactivation of latent HIV: do all roads go through PTEFb? Future Virol 2013; 8:649-659.
57. Derek D, Sloan Alivelu I, Angela T, et al. TLR7 agonist GS-9620 activates HIV- 1 in PBMCS from HIV-infected patients on cART. CROI 2015, Abstract 417 2015.
58. James B, Whitney. So-Yon Lim, et al. Treatment with a TLR7 agonist induces transient viremia in SIV-infected ART-suppressed monkeys. CROI 2015, Abstract 108 2015.
59. Spina CA, Anderson J, Archin NM, et al. An in-depth comparison of latent HIV- 1 reactivation in multiple cell model systems and resting CD4+ T cells from aviremic patients. PLoS Pathog 2013; 9:e1003834.
60. Bui JK, Mellors JW, Cillo AR. HIV-1 virion production from single inducible proviruses following T-cell activation ex vivo. J Virol 2015; 90:1673-1676
61. Laird GM, Bullen CK, Rosenbloom DI, et al. Ex vivo analysis identifies effective HIV-1 latency-reversing drug combinations. J Clin Invest 2015; 125:1901-1912
62. Jones RB, O'Connor R, Mueller S, et al. Histone deacetylase inhibitors impair the elimination of HIV-infected cells by cytotoxic T-lymphocytes. PLoS Pathog 2014; 10:e1004287