A flexible model of HIV-1 latency permitting evaluation of many primary CD4 T-cell reservoirs

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Lassen, Kara G ^a   Hebbeler, Andrew M ^a   Bhattacharyya, Darshana ^a   Lobritz, Michael A ^c,d   Greene, Warner C ^a,b  

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

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d STANFORD UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; T LYMPHOCYTE RECEPTOR; LUCIFERASE; VIRUS DNA;

ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; MEMORY T LYMPHOCYTE; MOLECULAR MODEL; PROVIRUS; QUANTITATIVE ANALYSIS; SENSITIVITY ANALYSIS; VIRUS LATENCY; VIRUS REACTIVATION; VIRUS REPLICATION; BIOLOGICAL MODEL; CD4 LYMPHOCYTE COUNT; CELL CULTURE; EVALUATION; GENETIC TRANSFECTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; METABOLISM; PATHOLOGY; PHYSIOLOGY; PRIMARY CELL CULTURE; THEORETICAL MODEL; VALIDATION STUDY; VIROLOGY; VIRUS DNA CELL DNA INTERACTION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

CD4 LYMPHOCYTE COUNT; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; DNA, VIRAL; HIV INFECTIONS; HIV-1; HUMANS; IMMUNOLOGIC MEMORY; LUCIFERASES; MODELS, BIOLOGICAL; MODELS, THEORETICAL; PRIMARY CELL CULTURE; TRANSFECTION; VIRUS INTEGRATION; VIRUS LATENCY;

EID: 84856190985     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030176     Document Type: Article

References (55)

1. 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.
2. 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.
3. Carter CC, Onafuwa-Nuga A, McNamara LA, Riddell Jt, Bixby D, et al. (2010) HIV-1 infects multipotent progenitor cells causing cell death and establishing latent cellular reservoirs. Nat Med 16: 446-451.
4. 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: 512-517.
5. 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: 727-728.
6. Richman DD, Margolis DM, Delaney M, Greene WC, Hazuda D, et al. (2009) The challenge of finding a cure for HIV infection. Science 323: 1304-1307.
7. Han Y, Wind-Rotolo M, Yang HC, Siliciano JD, Siliciano RF, (2007) Experimental approaches to the study of HIV-1 latency. Nat Rev Microbiol 5: 95-106.
8. 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: 6790-6799.
9. 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.
10. 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: 2965-2973.
11. 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.
12. Williams SA, Chen LF, Kwon H, Ruiz-Jarabo CM, Verdin E, et al. (2006) NF-kappaB p50 promotes HIV latency through HDAC recruitment and repression of transcriptional initiation. Embo J 25: 139-149.
13. Zack JA, Arrigo SJ, Weitsman SR, Go AS, Haislip A, et al. (1990) HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell 61: 213-222.
14. Stevenson M, Stanwick TL, Dempsey MP, Lamonica CA, (1990) HIV-1 replication is controlled at the level of T cell activation and proviral integration. Embo J 9: 1551-1560.
15. Bosque A, Planelles V, (2009) Induction of HIV-1 latency and reactivation in primary memory CD4+ T cells. Blood 113: 58-65.
16. Burke B, Brown HJ, Marsden MD, Bristol G, Vatakis DN, et al. (2007) Primary cell model for activation-inducible human immunodeficiency virus. J Virol 81: 7424-7434.
17. Sahu GK, Lee K, Ji J, Braciale V, Baron S, et al. (2006) A novel in vitro system to generate and study latently HIV-infected long-lived normal CD4+ T-lymphocytes. Virology 355: 127-137.
18. 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: 3473-3486.
19. 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.
20. Pace MJ, Agosto L, Graf EH, O'Doherty U, (2011) HIV reservoirs and latency models. Virology 411: 344-354.
21. Yang HC, (2011) Primary cell models of HIV latency. Curr Opin HIV AIDS 6: 62-67.
22. Palmer S, Maldarelli F, Wiegand A, Bernstein B, Hanna GJ, et al. (2008) Low-level viremia persists for at least 7 years in patients on suppressive antiretroviral therapy. Proc Natl Acad Sci U S A 105: 3879-3784.
23. Chomont N, El-Far M, Ancuta P, Trautmann L, Procopio FA, et al. (2009) HIV reservoir size and persistence are driven by T cell survival and homeostatic proliferation. Nat Med 15: 893-900.
24. 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.
25. Agosto LM, Yu JJ, Dai J, Kaletsky R, Monie D, et al. (2007) HIV-1 integrates into resting CD4+ T cells even at low inoculums as demonstrated with an improved assay for HIV-1 integration. Virology 368: 60-72.
26. Dai J, Agosto LM, Baytop C, Yu JJ, Pace MJ, et al. (2009) Human immunodeficiency virus integrates directly into naive resting CD4+ T cells but enters naive cells less efficiently than memory cells. J Virol 83: 4528-4537.
27. Vatakis DN, Bristol G, Wilkinson TA, Chow SA, Zack JA, (2007) Immediate activation fails to rescue efficient human immunodeficiency virus replication in quiescent CD4+ T cells. J Virol 81: 3574-3582.
28. Chen BK, Saksela K, Andino R, Baltimore D, (1994) Distinct modes of human immunodeficiency virus type 1 proviral latency revealed by superinfection of nonproductively infected cell lines with recombinant luciferase-encoding viruses. J Virol 68: 654-660.
29. Connor RI, Chen BK, Choe S, Landau NR, (1995) Vpr is required for efficient replication of human immunodeficiency virus type-1 in mononuclear phagocytes. Virology 206: 935-944.
30. Szymczak AL, Workman CJ, Wang Y, Vignali KM, Dilioglou S, et al. (2004) Correction of multi-gene deficiency in vivo using a single 'self-cleaving' 2A peptide-based retroviral vector. Nat Biotechnol 22: 589-594.
31. Donnelly ML, Luke G, Mehrotra A, Li X, Hughes LE, et al. (2001) Analysis of the aphthovirus 2A/2B polyprotein 'cleavage' mechanism indicates not a proteolytic reaction, but a novel translational effect: a putative ribosomal 'skip'. J Gen Virol 82: 1013-1025.
32. Liszewski MK, Yu JJ, O'Doherty U, (2009) Detecting HIV-1 integration by repetitive-sampling Alu-gag PCR. Methods 47: 254-260.
33. 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: 8776-8786.
34. Doitsh G, Cavrois M, Lassen KG, Zepeda O, Yang Z, et al. (2010) Abortive HIV infection mediates CD4 T cell depletion and inflammation in human lymphoid tissue. Cell 143: 789-801.
35. Pierson TC, Zhou Y, Kieffer TL, Ruff CT, Buck C, et al. (2002) Molecular characterization of preintegration latency in human immunodeficiency virus type 1 infection. J Virol 76: 8518-8531.
36. Hazuda DJ, Felock P, Witmer M, Wolfe A, Stillmock K, et al. (2000) Inhibitors of strand transfer that prevent integration and inhibit HIV-1 replication in cells. Science 287: 646-650.
37. Wu Y, Marsh JW, (2001) Selective transcription and modulation of resting T cell activity by preintegrated HIV DNA. Science 293: 1503-1506.
38. Brooks DG, Arlen PA, Gao L, Kitchen CM, Zack JA, (2003) Identification of T cell-signaling pathways that stimulate latent HIV in primary cells. Proc Natl Acad Sci U S A 100: 12955-12960.
39. 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. J Exp Med 188: 83-91.
40. Kulkosky J, Sullivan J, Xu Y, Souder E, Hamer DH, et al. (2004) Expression of latent HAART-persistent HIV type 1 induced by novel cellular activating agents. AIDS Res Hum Retroviruses 20: 497-505.
41. Church LD, Hessler G, Goodall JE, Rider DA, Workman CJ, et al. (2005) TNFR1-induced sphingomyelinase activation modulates TCR signaling by impairing store-operated Ca2+ influx. J Leukoc Biol 78: 266-278.
42. Rossol M, Meusch U, Pierer M, Kaltenhauser S, Hantzschel H, et al. (2007) Interaction between transmembrane TNF and TNFR1/2 mediates the activation of monocytes by contact with T cells. J Immunol 179: 4239-4248.
43. 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: 8118-8123.
44. Blazkova J, Trejbalova K, Gondois-Rey F, Halfon P, Philibert P, et al. (2009) CpG methylation controls reactivation of HIV from latency. PLoS Pathog 5: e1000554.
45. Burnett JC, Lim KI, Calafi A, Rossi JJ, Schaffer DV, et al. (2010) Combinatorial latency reactivation for HIV-1 subtypes and variants. J Virol 84: 5958-5974.
46. 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.
47. 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.
48. Williams SA, Chen LF, Kwon H, Fenard D, Bisgrove D, et al. (2004) Prostratin antagonizes HIV latency by activating NF-kappaB. J Biol Chem 279: 42008-42017.
49. Williams SA, Kwon H, Chen LF, Greene WC, (2007) Sustained induction of NF-kappa B is required for efficient expression of latent human immunodeficiency virus type 1. J Virol 81: 6043-6056.
50. Imamichi H, Crandall KA, Natarajan V, Jiang MK, Dewar RL, et al. (2001) Human immunodeficiency virus type 1 quasi species that rebound after discontinuation of highly active antiretroviral therapy are similar to the viral quasi species present before initiation of therapy. J Infect Dis 183: 36-50.
51. Joos B, Fischer M, Kuster H, Pillai SK, Wong JK, et al. (2008) HIV rebounds from latently infected cells, rather than from continuing low-level replication. Proc Natl Acad Sci U S A 105: 16725-16730.
52. Bailey JR, Sedaghat AR, Kieffer T, Brennan T, Lee PK, et al. (2006) Residual human immunodeficiency virus type 1 viremia in some patients on antiretroviral therapy is dominated by a small number of invariant clones rarely found in circulating CD4+ T cells. J Virol 80: 6441-6457.
53. 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.
54. Lenasi T, Contreras X, Peterlin BM, (2008) Transcriptional interference antagonizes proviral gene expression to promote HIV latency. Cell Host Microbe 4: 123-133.
55. 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.