An In-Depth Comparison of Latent HIV-1 Reactivation in Multiple Cell Model Systems and Resting CD4+ T Cells from Aviremic Patients

PLoS Pathogens

Volumn 9, Issue 12, 2013, Pages 1-15

  Spina, Celsa A ^a,b   Anderson, Jenny ^c   Archin, Nancie M ^d   Bosque, Alberto ^e   Chan, Jonathan ^f   Famiglietti, Marylinda ^e,n,o   Greene, Warner C ^f,g   Kashuba, Angela ^d   Lewin, Sharon R ^c,h,i   Margolis, David M ^d,j   Mau, Matthew ^e   Ruelas, Debbie ^f   Saleh, Suha ^c   Shirakawa, Kotaro ^f   Siliciano, Robert F ^k,l   Singhania, Akul ^a,p   Soto, Paula C ^a,b   Terry, Valeri H ^a   Verdin, Eric ^f,g   Woelk, Christopher ^m,p   Wooden, Stacey ^d   Xing, Sifei ^k,l   Planelles, Vicente ^e   more..

^a VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c ALFRED HOSPITAL   (Australia)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^f GLADSTONE INSTITUTE OF VIROLOGY AND IMMUNOLOGY   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h MONASH UNIVERSITY   (Australia)

ⁱ BURNET INSTITUTE   (Australia)

^j IL   (United States)

^k JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^l HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^m UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

ⁿ SAN RAFFAELE HOSPITAL   (Italy)

^o VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^p SOUTHAMPTON GENERAL HOSPITAL   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

4 METHOXYAMPHETAMINE; BRYOSTATIN; CALCIUM IONOPHORE; CD8ALPHA ANTIGEN; GREEN FLUORESCENT PROTEIN; HEXAMETHYLENEBISACETAMIDE; HISTONE DEACETYLASE INHIBITOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 2; INTERLEUKIN 7; IONOMYCIN; LUCIFERASE; PHYTOHEMAGGLUTININ; POSITIVE TRANSCRIPTION ELONGATION FACTOR B; PROTEIN KINASE C; RNA DIRECTED DNA POLYMERASE; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; VORINOSTAT; ACETAMIDE DERIVATIVE; HYDROXAMIC ACID;

ARTICLE; CD4+ T LYMPHOCYTE; CELL TYPE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; PROTEIN PROCESSING; T LYMPHOCYTE; VIRUS LATENCY; VIRUS REACTIVATION; ADULT; BIOLOGICAL MODEL; CELL CULTURE; COMPARATIVE STUDY; DRUG EFFECT; HEK293 CELL LINE; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; JURKAT CELL LINE; PATHOLOGY; PHYSIOLOGY; VIROLOGY; VIRUS ACTIVATION;

ACETAMIDES; ADULT; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; HEK293 CELLS; HISTONE DEACETYLASE INHIBITORS; HIV INFECTIONS; HIV-1; HUMANS; HYDROXAMIC ACIDS; INTERLEUKIN-7; JURKAT CELLS; MODELS, BIOLOGICAL; VIRUS ACTIVATION; VIRUS LATENCY;

EID: 84892845657     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003834     Document Type: Article

References (88)

1. 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: 1295-1300.
2. Chun TW, Carruth L, Finzi D, Shen X, DiGiuseppe JA, et al. (1997) Quantification of latent tissue reservoirs and total body viral load in HIV-1 infection. Nature 387: 183-188.
3. 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: 1291-1295.
4. Deeks SG, (2012) HIV: Shock and kill. Nature 487: 439-440.
5. Folks TM, Clouse KA, Justement J, Rabson A, Duh E, et al. (1989) Tumor necrosis factor alpha induces expression of human immunodeficiency virus in a chronically infected T-cell clone. Proc Natl Acad Sci U S A 86: 2365-2368.
6. Pomerantz RJ, Trono D, Feinberg MB, Baltimore D, (1990) Cells nonproductively infected with HIV-1 exhibit an aberrant pattern of viral RNA expression: a molecular model for latency. Cell 61: 1271-1276.
7. Antoni BA, Rabson AB, Kinter A, Bodkin M, Poli G, (1994) NF-kappa B-dependent and-independent pathways of HIV activation in a chronically infected T cell line. Virology 202: 684-694.
8. Jordan A, Bisgrove D, Verdin E, (2003) HIV reproducibly establishes a latent infection after acute infection of T cells in vitro. Embo J 22: 1868-1877.
9. Micheva-Viteva S, Kobayashi Y, Edelstein LC, Pacchia AL, Lee HL, et al. (2011) High-throughput screening uncovers a compound that activates latent HIV-1 and acts cooperatively with a histone deacetylase (HDAC) inhibitor. The Journal of biological chemistry 286: 21083-21091.
10. 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: 3078-3093.
11. Kauder SE, Bosque A, Lindqvist A, Planelles V, Verdin E, (2009) Epigenetic regulation of HIV-1 latency by cytosine methylation. PLoS Pathog 5: e1000495.
12. Pace MJ, Agosto L, Graf EH, O'Doherty U, (2011) HIV reservoirs and latency models. Virology 411: 344-354.
13. Hakre S, Chavez L, Shirakawa K, Verdin E, (2012) HIV latency: experimental systems and molecular models. FEMS Microbiol Rev 36: 706-716.
14. Bosque A, Planelles V, (2011) Studies of HIV-1 latency in an ex vivo model that uses primary central memory T cells. Methods 53: 54-61.
15. Bosque A, Planelles V, (2009) Induction of HIV-1 latency and reactivation in primary memory CD4+ T cells. Blood 113: 58-65.
16. Marini A, Harper JM, Romerio F, (2008) An in vitro system to model the establishment and reactivation of HIV-1 latency. J Immunol 181: 7713-7720.
17. Yang HC, Xing S, Shan L, O'Connell K, Dinoso J, et al. (2009) Small-molecule screening using a human primary cell model of HIV latency identifies compounds that reverse latency without cellular activation. J Clin Invest 119 (11) (): 3473-86.
18. Tyagi M, Pearson RJ, Karn J, (2010) Establishment of HIV latency in primary CD4+ cells is due to epigenetic transcriptional silencing and P-TEFb restriction. J Virol 84: 6425-6437.
19. 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 Pathog 3: 1459-1469.
20. Swiggard WJ, Baytop C, Yu JJ, Dai J, Li C, et al. (2005) Human immunodeficiency virus type 1 can establish latent infection in resting CD4+ T cells in the absence of activating stimuli. J Virol 79: 14179-14188.
21. Saleh S, Solomon A, Wightman F, Xhilaga M, Cameron PU, et al. (2007) CCR7 ligands CCL19 and CCL21 increase permissiveness of resting memory CD4+ T cells to HIV-1 infection: a novel model of HIV-1 latency. Blood 110: 4161-4164.
22. Archin NM, Eron JJ, Palmer S, Hartmann-Duff A, Martinson JA, et al. (2008) Valproic acid without intensified antiviral therapy has limited impact on persistent HIV infection of resting CD4+ T cells. AIDS 22: 1131-1135.
23. Lassen KG, Hebbeler AM, Bhattacharyya D, Lobritz MA, Greene WC, (2012) A flexible model of HIV-1 latency permitting evaluation of many primary CD4 T-cell reservoirs. PLoS One 7: e30176.
24. Cameron PU, Saleh S, Sallmann G, Solomon A, Wightman F, et al. (2010) Establishment of HIV-1 latency in resting CD4+ T cells depends on chemokine-induced changes in the actin cytoskeleton. Proc Natl Acad Sci U S A 107: 16934-16939.
25. Messi M, Giacchetto I, Nagata K, Lanzavecchia A, Natoli G, et al. (2003) Memory and flexibility of cytokine gene expression as separable properties of human T(H)1 and T(H)2 lymphocytes. Nat Immunol 4: 78-86.
26. Spina CA, Guatelli JC, Richman DD, (1995) Establishment of a stable, inducible form of human immunodeficiency virus type 1 DNA in quiescent CD4 lymphocytes in vitro. J Virol 69: 2977-2988.
27. Spina CA, Prince HE, Richman DD, (1997) Preferential replication of HIV-1 in the CD45RO memory cell subset of primary CD4 lymphocytes in vitro. J Clin Invest 99: 1774-1785.
28. Chan JKL, Bhattacharyya D, Lassen K, Ruelas D, Greene WC, (2013) Calcium/Calcineurin Synergizes with Prostratin to Promote NF-kappa B Dependent Activation of Latent HIV. PLoS ONE 8 (10) (): e77749.
29. Blankson JN, Finzi D, Pierson TC, Sabundayo BP, Chadwick K, et al. (2000) Biphasic decay of latently infected CD4+ T cells in acute human immunodeficiency virus type 1 infection. J Infect Dis 182: 1636-1642.
30. Risueno RM, Schamel WW, Alarcon B, (2008) T cell receptor engagement triggers its CD3epsilon and CD3zeta subunits to adopt a compact, locked conformation. PLoS One 3: e1747.
31. Ledbetter JA, Imboden JB, Schieven GL, Grosmaire LS, Rabinovitch PS, et al. (1990) CD28 ligation in T-cell activation: evidence for two signal transduction pathways. Blood 75: 1531-1539.
32. Mochly-Rosen D, Das K, Grimes KV, (2012) Protein kinase C, an elusive therapeutic target? Nat Rev Drug Discov 11: 937-957.
33. 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: 3006-3015.
34. Gustafson KR, Cardellina JH 2nd, McMahon JB, Gulakowski RJ, Ishitoya J, et al. (1992) A nonpromoting phorbol from the samoan medicinal plant Homalanthus nutans inhibits cell killing by HIV-1. J Med Chem 35: 1978-1986.
35. Gulakowski RJ, McMahon JB, Buckheit RW Jr, Gustafson KR, Boyd MR, (1997) Antireplicative and anticytopathic activities of prostratin, a non-tumor-promoting phorbol ester, against human immunodeficiency virus (HIV). Antiviral Res 33: 87-97.
36. Trindade-Silva AE, Lim-Fong GE, Sharp KH, Haygood MG, (2010) Bryostatins: biological context and biotechnological prospects. Curr Opin Biotechnol 21: 834-842.
37. Mehla R, Bivalkar-Mehla S, Zhang R, Handy I, Albrecht H, et al. (2010) Bryostatin modulates latent HIV-1 infection via PKC and AMPK signaling but inhibits acute infection in a receptor independent manner. PLoS One 5: e11160.
38. DeChristopher BA, Loy BA, Marsden MD, Schrier AJ, Zack JA, et al. (2012) Designed, synthetically accessible bryostatin analogues potently induce activation of latent HIV reservoirs in vitro. Nat Chem 4: 705-710.
39. Luznik L, Kraus G, Guatelli J, Richman D, Wong-Staal F, (1995) Tat-independent replication of human immunodeficiency viruses. J Clin Invest 95: 328-332.
40. 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: 128-137.
41. Lehrman G, Ylisastigui L, Bosch RJ, Margolis DM, (2004) Interleukin-7 induces HIV type 1 outgrowth from peripheral resting CD4+ T cells. J Acquir Immune Defic Syndr 36: 1103-1104.
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: 13077-13082.
43. Bosque A, Famiglietti M, Weyrich AS, Goulston C, Planelles V, (2011) Homeostatic proliferation fails to efficiently reactivate HIV-1 latently infected central memory CD4+ T cells. PLoS Pathog 7: e1002288.
44. Seddon B, Tomlinson P, Zamoyska R, (2003) Interleukin 7 and T cell receptor signals regulate homeostasis of CD4 memory cells. Nat Immunol 4: 680-686.
45. Vandergeeten C, Fromentin R, DaFonseca S, Lawani MB, Sereti I, et al. (2013) Interleukin-7 promotes HIV persistence during antiretroviral therapy. Blood 121: 4321-4329.
46. Saleh S, Wightman F, Ramanayake S, Alexander M, Kumar N, et al. (2011) Expression and reactivation of HIV in a chemokine induced model of HIV latency in primary resting CD4+ T cells. Retrovirology 8: 80.
47. Greene WC, Robb RJ, Depper JM, Leonard WJ, Drogula C, et al. (1984) Phorbol diester induces expression of Tac antigen on human acute T lymphocytic leukemic cells. J Immunol 133: 1042-1047.
48. Richardson JH, Sodroski JG, Waldmann TA, Marasco WA, (1995) Phenotypic knockout of the high-affinity human interleukin 2 receptor by intracellular single-chain antibodies against the alpha subunit of the receptor. Proc Natl Acad Sci U S A 92: 3137-3141.
49. Kim HR, Hwang KA, Kim KC, Kang I, (2007) Down-regulation of IL-7Ralpha expression in human T cells via DNA methylation. J Immunol 178: 5473-5479.
50. Duh EJ, Maury WJ, Folks TM, Fauci AS, Rabson AB, (1989) Tumor necrosis factor alpha activates human immunodeficiency virus type 1 through induction of nuclear factor binding to the NF-kappa B sites in the long terminal repeat. Proc Natl Acad Sci U S A 86: 5974-5978.
51. Osborn L, Kunkel S, Nabel GJ, (1989) Tumor necrosis factor alpha and interleukin 1 stimulate the human immunodeficiency virus enhancer by activation of the nuclear factor kappa B. Proc Natl Acad Sci U S A 86: 2336-2340.
52. Siegel DS, Zhang X, Feinman R, Teitz T, Zelenetz A, et al. (1998) Hexamethylene bisacetamide induces programmed cell death (apoptosis) and down-regulates BCL-2 expression in human myeloma cells. Proc Natl Acad Sci U S A 95: 162-166.
53. Richon VM, Webb Y, Merger R, Sheppard T, Jursic B, et al. (1996) Second generation hybrid polar compounds are potent inducers of transformed cell differentiation. Proc Natl Acad Sci U S A 93: 5705-5708.
54. Vlach J, Pitha PM, (1993) Hexamethylene bisacetamide activates the human immunodeficiency virus type 1 provirus by an NF-kappa B-independent mechanism. J Gen Virol 74 (Pt 11) (): 2401-2408.
55. Chen R, Liu M, Li H, Xue Y, Ramey WN, et al. (2008) PP2B and PP1alpha cooperatively disrupt 7SK snRNP to release P-TEFb for transcription in response to Ca2+ signaling. Genes Dev 22: 1356-1368.
56. 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: 1162-1170.
57. Trujillo KM, Tyler RK, Ye C, Berger SL, Osley MA, (2011) A genetic and molecular toolbox for analyzing histone ubiquitylation and sumoylation in yeast. Methods 54: 296-303.
58. Gardner KE, Allis CD, Strahl BD, (2011) Operating on chromatin, a colorful language where context matters. J Mol Biol 409: 36-46.
59. Struhl K, (1998) Histone acetylation and transcriptional regulatory mechanisms. Genes Dev 12: 599-606.
60. 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: 1799-1806.
61. 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: 4749-4756.
62. Contreras X, Schweneker M, Chen CS, McCune JM, Deeks SG, et al. (2009) Suberoylanilide Hydroxamic Acid Reactivates HIV from Latently Infected Cells. J Biol Chem 284: 6782-6789.
63. Edelstein LC, Micheva-Viteva S, Phelan BD, Dougherty JP, (2009) Short communication: activation of latent HIV type 1 gene expression by suberoylanilide hydroxamic acid (SAHA), an HDAC inhibitor approved for use to treat cutaneous T cell lymphoma. AIDS Res Hum Retroviruses 25: 883-887.
64. Rasmussen TA, Schmeltz Sogaard O, Brinkmann C, Wightman F, Lewin SR, et al. (2013) Comparison of HDAC inhibitors in clinical development: Effect on HIV production in latently infected cells and T-cell activation. Hum Vaccin Immunother 99 (5) (): 993-1001.
65. 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.
66. 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 Retroviruses 25: 207-212.
67. Bouchat S, Gatot JS, Kabeya K, Cardona C, Colin L, et al. (2012) Histone methyltransferase inhibitors induce HIV-1 recovery in resting CD4(+) T cells from HIV-1-infected HAART-treated patients. AIDS 26: 1473-1482.
68. Blazkova J, Chun TW, Belay BW, Murray D, Justement JS, et al. (2012) 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 206: 765-769.
69. Archin NM, Liberty AL, Kashuba AD, Choudhary SK, Kuruc JD, et al. (2012) Administration of vorinostat disrupts HIV-1 latency in patients on antiretroviral therapy. Nature 487: 482-485.
70. Bartholomeeusen K, Fujinaga K, Xiang Y, Peterlin BM, (2013) HDAC inhibitors that release Positive Transcription Elongation Factor b (P-TEFb) from its Inhibitory Complex also activate HIV Transcription. J Biol Chem 288 (20) (): 14400-7.
71. Prins JM, Jurriaans S, van Praag RM, Blaak H, van Rij R, et al. (1999) Immuno-activation with anti-CD3 and recombinant human IL-2 in HIV-1-infected patients on potent antiretroviral therapy. AIDS 13: 2405-2410.
72. van Praag RM, Prins JM, Roos MT, Schellekens PT, Ten Berge IJ, 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: 218-226.
73. Budhiraja S, Famiglietti M, Bosque A, Planelles V, Rice AP, (2012) Cyclin T1 and CDK9 T-loop phosphorylation are downregulated during establishment of HIV-1 latency in primary resting memory CD4+ T cells. J Virol 87 (2) (): 1211-20.
74. Lenasi T, Contreras X, Peterlin BM, (2008) Transcriptional interference antagonizes proviral gene expression to promote HIV latency. Cell Host Microbe 4: 123-133.
75. Irie K, Yanagita RC, Nakagawa Y, (2010) Challenges to the development of bryostatin-type anticancer drugs based on the activation mechanism of protein kinase Cdelta. Med Res Rev 32 (3) (): 518-35.
76. Perez M, de Vinuesa AG, Sanchez-Duffhues G, Marquez N, Bellido ML, et al. (2010) Bryostatin-1 synergizes with histone deacetylase inhibitors to reactivate HIV-1 from latency. Curr HIV Res 8: 418-429.
77. Schroder AR, Shinn P, Chen H, Berry C, Ecker JR, et al. (2002) HIV-1 integration in the human genome favors active genes and local hotspots. Cell 110: 521-529.
78. Lewinski MK, Bisgrove D, Shinn P, Chen H, Hoffmann C, et al. (2005) Genome-wide analysis of chromosomal features repressing human immunodeficiency virus transcription. J Virol 79: 6610-6619.
79. 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: 134-146.
80. Shan L, Yang HC, Rabi SA, Bravo HC, Shroff NS, et al. (2011) Influence of host gene transcription level and orientation on HIV-1 latency in a primary-cell model. J Virol 85: 5384-5393.
81. Sherrill-Mix S, Lewinski MK, Famiglietti M, Bosque A, Malani N, et al. (2013) HIV latency and integration site placement in five cell-based models. Retrovirology 10: 90.
82. Pace MJ, Graf EH, Agosto LM, Mexas AM, Male F, et al. (2012) Directly infected resting CD4+T cells can produce HIV Gag without spreading infection in a model of HIV latency. PLoS Pathog 8: e1002818.
83. Lewin SR, Murray JM, Solomon A, Wightman F, Cameron PU, et al. (2008) Virologic determinants of success after structured treatment interruptions of antiretrovirals in acute HIV-1 infection. J Acquir Immune Defic Syndr 47: 140-147.
84. Koelsch KK, Liu L, Haubrich R, May S, Havlir D, et al. (2008) Dynamics of total, linear nonintegrated, and integrated HIV-1 DNA in vivo and in vitro. J Infect Dis 197: 411-419.
85. Marks PA, Breslow R, (2007) Dimethyl sulfoxide to vorinostat: development of this histone deacetylase inhibitor as an anticancer drug. Nat Biotechnol 25: 84-90.
86. de Hoon MJ, Imoto S, Nolan J, Miyano S, (2004) Open source clustering software. Bioinformatics 20: 1453-1454.
87. Saldanha AJ, (2004) Java Treeview-extensible visualization of microarray data. Bioinformatics 20: 3246-3248.
88. Suzuki R, Shimodaira H, (2006) Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22: 1540-1542.