Apoptosis-induced activation of HIV-1 in latently infected cell lines

Retrovirology

Volumn 12, Issue 1, 2015, Pages

  Khan, Sohrab Z ^a   Hand, Nicholas ^b   Zeichner, Steven L ^a,b,c  

^a CHILDREN S RESEARCH INSTITUTE   (United States)

^b GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^c GEORGE WASHINGTON UNIVERSITY   (United States)

Author keywords

Activation; Apoptosis; Caspase; HIV; Latency

Indexed keywords

CASPASE 3; CASPASE 8; DOXORUBICIN; ETOPOSIDE; FLUDARABINE PHOSPHATE; GAG PROTEIN; VINCRISTINE; VIRUS RNA; ZIDOVUDINE;

ANTIVIRAL ACTIVITY; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; G1 PHASE CELL CYCLE CHECKPOINT; HOST CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; LATENT VIRUS INFECTION; LYMPHOCYTE; LYMPHOID CELL LINE; MONOCYTE MACROPHAGE PRECURSOR CELL; NONHUMAN; PROTEIN SYNTHESIS; VIRION; VIRUS ACTIVATION; VIRUS INFECTIVITY; VIRUS REACTIVATION; VIRUS REPLICATION; CELL LINE; CELL SURVIVAL; DRUG EFFECTS; HOST PATHOGEN INTERACTION; HUMAN; PHYSIOLOGY; VIRUS LATENCY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

APOPTOSIS; CELL LINE; CELL SURVIVAL; HIV CORE PROTEIN P24; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; RNA, VIRAL; VIRUS ACTIVATION; VIRUS LATENCY;

EID: 84931265981     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/s12977-015-0169-1     Document Type: Article

References (77)

1. Chun TW, Davey Jr RT, Ostrowski M, Shawn Justement J, Engel D, Mullins JI, et al. Relationship between pre-existing viral reservoirs and the re-emergence of plasma viremia after discontinuation of highly active anti-retroviral therapy. Nat Med. 2000;6(7):757-61.
2. Davey Jr RT, Bhat N, Yoder C, Chun TW, Metcalf JA, Dewar R, et al. HIV-1 and T cell dynamics after interruption of highly active antiretroviral therapy (HAART) in patients with a history of sustained viral suppression. Proc Natl Acad Sci U S A. 1999;96(26):15109-14.
3. Finzi D, Blankson J, Siliciano JD, Margolick JB, Chadwick K, Pierson T, et al. Latent infection of CD4+ T cells provides a mechanism for lifelong persistence of HIV-1, even in patients on effective combination therapy. Nat Med. 1999;5(5):512-7.
4. 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 CD4+ T cells. Nat Med. 2003;9(6):727-8.
5. Geeraert L, Kraus G, Pomerantz RJ. Hide-and-seek: the challenge of viral persistence in HIV-1 infection. Annu Rev Med. 2008;59:487-501.
6. Marsden MD, Zack JA. Eradication of HIV: current challenges and new directions. J Antimicrob Chemother. 2009;63(1):7-10.
7. Shen L, Siliciano RF. Viral reservoirs, residual viremia, and the potential of highly active antiretroviral therapy to eradicate HIV infection. J Allergy Clin Immunol. 2008;122(1):22-8.
8. Hamer DH. Can HIV be Cured? Mechanisms of HIV persistence and strategies to combat it. Curr HIV Res. 2004;2(2):99-111.
9. Katlama C, Deeks SG, Autran B, Martinez-Picado J, van Lunzen J, Rouzioux C, et al. Barriers to a cure for HIV: new ways to target and eradicate HIV-1 reservoirs. Lancet. 2013;318(9883):2109-17.
10. Kent SJ, Reece JC, Petravic J, Martyushev A, Kramski M, De Rose R, et al. The search for an HIV cure: tackling latent infection. Lancet Infect Dis. 2013;13(7):614-21.
11. Richman DD, Margolis DM, Delaney M, Greene WC, Hazuda D, Pomerantz RJ. The challenge of finding a cure for HIV infection. Science. 2009;323(5919):1304-7.
12. Lafeuillade A, Poggi C, Chadapaud S, Hittinger G, Chouraqui M, Pisapia M, et al. Pilot study of a combination of highly active antiretroviral therapy and cytokines to induce HIV-1 remission. J Acquir Immune Defic Syndr. 2001;26(1):44-55.
13. Dybul M, Hidalgo B, Chun TW, Belson M, Migueles SA, Justement JS, et al. Pilot study of the effects of intermittent interleukin-2 on human immunodeficiency virus (HIV)-specific immune responses in patients treated during recently acquired HIV infection. J Infect Dis. 2002;185(1):61-8.
14. Prins JM, Jurriaans S, van Praag RM, Blaak H, van Rij R, Schellekens PT, et al. Immuno-activation with anti-CD3 and recombinant human IL-2 in HIV-1-infected patients on potent antiretroviral therapy. Aids. 1999;13(17):2405-10.
15. Korin YD, Brooks DG, Brown S, Korotzer A, Zack JA. Effects of prostratin on T-cell activation and human immunodeficiency virus latency. J Virol. 2002;76(16):8118-23.
16. Fernandez G, Zaikos TD, Khan SZ, Jacobi AM, Behlke MA, Zeichner SL. Targeting IkappaB proteins for HIV latency activation: the role of individual IkappaB and NF-kappaB proteins. J Virol. 2013;87(7):3966-78.
17. Schulze-Forster K, Gotz F, Wagner H, Kroger H, Simon D. Transcription of HIV1 is inhibited by DNA methylation. Biochem Biophys Res Commun. 1990;168(1):141-7.
18. Ishida T, Hamano A, Koiwa T, Watanabe T. 5' long terminal repeat (LTR)-selective methylation of latently infected HIV-1 provirus that is demethylated by reactivation signals. Retrovirology. 2006;3:69.
19. Bednarik DP, Cook JA, Pitha PM. Inactivation of the HIV LTR by DNA CpG methylation: evidence for a role in latency. Embo J. 1990;9(4):1157-64.
20. 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. 2003;22(24):6550-61.
21. Sheridan PL, Mayall TP, Verdin E, Jones KA. Histone acetyltransferases regulate HIV-1 enhancer activity in vitro. Genes Dev. 1997;11(24):3327-40.
22. 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. 1996;15(5):1112-20.
23. Laughlin M, Zeichner S, Kolson D, Alwine J, Seshamma T, Pomerantz R, et al. Sodium butryate treatment of cells latently infected with HIV-1 results in the expression of unspliced viral RNA. Virology. 1993;196:496-505.
24. 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. 2004;18(8):1101-8.
25. 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 CD4+ T cell model without inducing global T cell activation. J Virol. 2011;85(12):6060-4.
26. 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(7408):482-5.
27. 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(2):207-12.
28. 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(11):6782-9.
29. Bullen CK, Laird GM, Durand CM, Siliciano JD, Siliciano RF. New ex vivo approaches distinguish effective and ineffective single agents for reversing HIV-1 latency in vivo. Nat Med. 2014;20(4):425-9.
30. Sahu GK, Cloyd MW. Latent HIV in primary T lymphocytes is unresponsive to histone deacetylase inhibitors. Virol J. 2011;8:400.
31. Blazkova J, Chun TW, Belay BW, Murray D, Justement JS, Funk EK, et al. Effect of histone deacetylase inhibitors on HIV production in latently infected, resting CD4(+) T cells from infected individuals receiving effective antiretroviral therapy. J Infect Dis. 2012;206(5):765-9.
32. Reuse S, Calao M, Kabeya K, Guiguen A, Gatot JS, 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(6):e6093.
33. Williams SA, Chen LF, Kwon H, Fenard D, Bisgrove D, Verdin E, et al. Prostratin antagonizes HIV latency by activating NF-kappaB. J Biol Chem. 2004;279(40):42008-17.
34. Mehla R, Bivalkar-Mehla S, Zhang R, Handy I, Albrecht H, Giri S, 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(6):e11160.
35. Mackay HJ, Twelves CJ. Targeting the protein kinase C family: are we there yet? Nat Rev Cancer. 2007;7(7):554-62.
36. Margolis DM. Confronting proviral HIV infection. Curr HIV/AIDS Rep. 2007;4(2):60-4.
37. Fernandez G, Zeichner SL. Cell line-dependent variability in HIV activation employing DNMT inhibitors. Virol J. 2010;7:266.
38. Ho YC, Shan L, Hosmane NN, Wang J, Laskey SB, Rosenbloom DI, et al. Replication-competent noninduced proviruses in the latent reservoir increase barrier to HIV-1 cure. Cell. 2013;155(3):540-51.
39. Allers K, Hutter G, Hofmann J, Loddenkemper C, Rieger K, Thiel E, et al. Evidence for the cure of HIV infection by CCR5Delta32/Delta32 stem cell transplantation. Blood. 2011;117(10):2791-9.
40. Hutter G, Nowak D, Mossner M, Ganepola S, Mussig A, Allers K, et al. Long-term control of HIV by CCR5 Delta32/Delta32 stem-cell transplantation. N Engl J Med. 2009;360(7):692-8.
41. Hutter G, Thiel E. Allogeneic transplantation of CCR5-deficient progenitor cells in a patient with HIV infection: an update after 3 years and the search for patient no. 2. Aids. 2011;25(2):273-4.
42. Henrich TJ, Hu Z, Li JZ, Sciaranghella G, Busch MP, Keating SM, et al. Long-term reduction in peripheral blood HIV type 1 reservoirs following reduced-intensity conditioning allogeneic stem cell transplantation. J Infect Dis. 2013;207(11):1694-702.
43. Henrich TJ, Hanhauser E, Marty FM, Sirignano MN, Keating S, Lee TH, et al. Antiretroviral-free HIV-1 remission and viral rebound after allogeneic stem cell transplantation: report of 2 cases. Ann Intern Med. 2014;161(5):319-27.
44. Weiden PL, Flournoy N, Thomas ED, Prentice R, Fefer A, Buckner CD, et al. Antileukemic effect of graft-versus-host disease in human recipients of allogeneic-marrow grafts. N Engl J Med. 1979;300(19):1068-73.
45. Maus MV, Fraietta JA, Levine BL, Kalos M, Zhao Y, June CH. Adoptive immunotherapy for cancer or viruses. Annu Rev Immunol. 2014;32:189-225.
46. Gregory CD, Dive C, Henderson S, Smith CA, Williams GT, Gordon J, et al. Activation of Epstein-Barr virus latent genes protects human B cells from death by apoptosis. Nature. 1991;349(6310):612-4.
47. Sarid R, Sato T, Bohenzky RA, Russo JJ, Chang Y. Kaposi's sarcoma-associated herpesvirus encodes a functional bcl-2 homologue. Nat Med. 1997;3(3):293-8.
48. Wang HW, Sharp TV, Koumi A, Koentges G, Boshoff C. Characterization of an anti-apoptotic glycoprotein encoded by Kaposi's sarcoma-associated herpesvirus which resembles a spliced variant of human survivin. Embo J. 2002;21(11):2602-15.
49. Chehimi J, Papasavvas E, Tomescu C, Gekonge B, Abdulhaqq S, Raymond A, et al. Inability of plasmacytoid dendritic cells to directly lyse HIV-infected autologous CD4+ T cells despite induction of tumor necrosis factor-related apoptosis-inducing ligand. J Virol. 2010;84(6):2762-73.
50. Conti L, Rainaldi G, Matarrese P, Varano B, Rivabene R, Columba S, et al. The HIV-1 vpr protein acts as a negative regulator of apoptosis in a human lymphoblastoid T cell line: possible implications for the pathogenesis of AIDS. J Exp Med. 1998;187(3):403-13.
51. Zheng L, Yang Y, Guocai L, Pauza CD, Salvato MS. HIV Tat protein increases Bcl-2 expression in monocytes which inhibits monocyte apoptosis induced by tumor necrosis factor-alpha-related apoptosis-induced ligand. Intervirology. 2007;50(3):224-8.
52. Prasad A, Lu M, Lukac DM, Zeichner SL. An alternative Kaposi's sarcoma-associated herpesvirus replication program triggered by host cell apoptosis. J Virol. 2012;86(8):4404-19.
53. Prasad A, Remick J, Zeichner SL. Activation of human herpesvirus replication by apoptosis. J Virol. 2013;87(19):10641-50.
54. Du T, Zhou G, Roizman B. HSV-1 gene expression from reactivated ganglia is disordered and concurrent with suppression of latency-associated transcript and miRNAs. Proc Natl Acad Sci U S A. 2011;108(46):18820-4.
55. Du T, Zhou G, Roizman B. Induction of apoptosis accelerates reactivation of latent HSV-1 in ganglionic organ cultures and replication in cell cultures. Proc Natl Acad Sci U S A. 2012;109(36):14616-21.
56. Michael NL, Morrow P, Mosca J, Vahey M, Burke DS, Redfield RR. Induction of human immunodeficiency virus type 1 expression in chronically infected cells is associated primarily with a shift in RNA splicing patterns. J Virol. 1991;65(3):1291-303.
57. Pomerantz RJ, Trono D, Feinberg MB, Baltimore D. Cells nonproductively infected with HIV-1 exhibit an aberrant pattern of viral RNA expression: a molecular model for latency. Cell. 1990;61(7):1271-6.
58. Folks TM, Clouse KA, Justement J, Rabson A, Duh E, Kehrl JH, et al. Tumor necrosis factor alpha induces expression of human immunodeficiency virus in a chronically infected T-cell clone. Proc Natl Acad Sci U S A. 1989;86(7):2365-8.
59. Emiliani S, Van Lint C, Fischle W, Paras Jr P, Ott M, Brady J, et al. A point mutation in the HIV-1 Tat responsive element is associated with postintegration latency. Proc Natl Acad Sci U S A. 1996;93(13):6377-81.
60. Fernandez Larrosa PN, Croci DO, Riva DA, Bibini M, Luzzi R, Saracco M, et al. Apoptosis resistance in HIV-1 persistently-infected cells is independent of active viral replication and involves modulation of the apoptotic mitochondrial pathway. Retrovirology. 2008;5:19.
61. Pinti M, Biswas P, Troiano L, Nasi M, Ferraresi R, Mussini C, et al. Different sensitivity to apoptosis in cells of monocytic or lymphocytic origin chronically infected with human immunodeficiency virus type-1. Exp Biol Med. 2003;228(11):1346-54.
62. Aguilar-Cordova E, Chinen J, Donehower L, Lewis DE, Belmont JW. A sensitive reporter cell line for HIV-1 tat activity, HIV-1 inhibitors, and T cell activation effects. AIDS Res Hum Retroviruses. 1994;10(3):295-301.
63. Emiliani S, Fischle W, Ott M, Van Lint C, Amella CA, Verdin E. Mutations in the tat gene are responsible for human immunodeficiency virus type 1 postintegration latency in the U1 cell line. J Virol. 1998;72(2):1666-70.
64. Poli G, Orenstein JM, Kinter A, Folks TM, Fauci AS. Interferon-alpha but not AZT suppresses HIV expression in chronically infected cell lines. Science. 1989;244(4904):575-7.
65. Scheller C, Sopper S, Chen P, Flory E, Koutsilieri E, Racek T, et al. Caspase inhibition activates HIV in latently infected cells. Role of tumor necrosis factor receptor 1 and CD95. J Biol Chem. 2002;277(18):15459-64.
66. Scheller C, Sopper S, Koutsilieri E, Ludwig S, Ter Meulen V, Jassoy C. Caspase inhibitors as a supplement in immune activation therapies to achieve eradication of HIV in its latent reservoirs. Ann N Y Acad Sci. 2003;1010:209-12.
67. Kamada S, Kikkawa U, Tsujimoto Y, Hunter T. Nuclear translocation of caspase-3 is dependent on its proteolytic activation and recognition of a substrate-like protein(s). J Biol Chem. 2005;280(2):857-60.
68. Gonzalvez F, Schug ZT, Houtkooper RH, MacKenzie ED, Brooks DG, Wanders RJ, et al. Cardiolipin provides an essential activating platform for caspase-8 on mitochondria. J Cell Biol. 2008;183(4):681-96.
69. Lamkanfi M, Dixit VM. Manipulation of host cell death pathways during microbial infections. Cell Host Microbe. 2010;8(1):44-54.
70. Lum JJ, Badley AD. Resistance to apoptosis: mechanism for the development of HIV reservoirs. Curr HIV Res. 2003;1(3):261-74.
71. Munger J, Hagglund R, Roizman B. Infected cell protein No. 22 is subject to proteolytic cleavage by caspases activated by a mutant that induces apoptosis. Virology. 2003;305(2):364-70.
72. Badley AD, Sainski A, Wightman F, Lewin SR. Altering cell death pathways as an approach to cure HIV infection. Cell Death Dis. 2013;4:e718.
73. Folks TM, Justement J, Kinter A, Schnittman S, Orenstein J, Poli G, et al. Characterization of a promonocyte clone chronically infected with HIV and inducible by 13-phorbol-12-myristate acetate. J Immunol. 1988;140(4):1117-22.
74. Clouse KA, Powell D, Washington I, Poli G, Strebel K, Farrar W, et al. Monokine regulation of human immunodeficiency virus-1 expression in a chronically infected human T cell clone. J Immunol. 1989;142(2):431-8.
75. Krishnan V, Zeichner SL. Host cell gene expression during human immunodeficiency virus type 1 latency and reactivation and effects of targeting genes that are differentially expressed in viral latency. J Virol. 2004;78(17):9458-73.
76. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25(4):402-8.
77. Chesebro B, Wehrly K, Nishio J, Perryman S. Macrophage-tropic human immunodeficiency virus isolates from different patients exhibit unusual V3 envelope sequence homogeneity in comparison with T-cell-tropic isolates: definition of critical amino acids involved in cell tropism. J Virol. 1992;66(11):6547-54.