Cellular and molecular mechanisms involved in the establishment of HIV-1 latency

Retrovirology

Volumn 10, Issue 1, 2013, Pages

  Donahue, Daniel A ^a,b   Wainberg, Mark A ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

CD4 T cell; Chromatin; Epigenetics; Establishment; Latency; Reservoir; Transcriptional interference

Indexed keywords

ANTIRETROVIRUS AGENT; ELONGATION FACTOR; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR;

CD4+ T LYMPHOCYTE; CHROMATIN; EPIGENETICS; GENE EXPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; LATENT VIRUS INFECTION; NONHUMAN; PATHOPHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION; SIMIAN IMMUNODEFICIENCY VIRUS; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; VIRUS DNA CELL DNA INTERACTION; VIRUS LATENCY;

CD4-POSITIVE T-LYMPHOCYTES; EPIGENESIS, GENETIC; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; MODELS, BIOLOGICAL; TRANSCRIPTION, GENETIC; VIRUS LATENCY;

ANIMALIA; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84873032782     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-10-11     Document Type: Review

References (132)

1. Eisele E, Siliciano RF. Redefining the viral reservoirs that prevent HIV-1 eradication. Immunity 2012, 37:377-388. 10.1016/j.immuni.2012.08.010, 22999944.
2. Lassen KG, Ramyar KX, Bailey JR, Zhou Y, Siliciano RF. Nuclear retention of multiply spliced HIV-1 RNA in resting CD4+ T cells. PLoS Pathog 2006, 2:e68. 10.1371/journal.ppat.0020068, 1487174, 16839202.
3. Saleh S, Wightman F, Ramanayake S, Alexander M, Kumar N, Khoury G, Pereira C, Purcell D, Cameron PU, Lewin SR. Expression and reactivation of HIV in a chemokine induced model of HIV latency in primary resting CD4+ T cells. Retrovirology 2011, 8:80. 10.1186/1742-4690-8-80, 3215964, 21992606.
4. Pace MJ, Graf EH, Agosto LM, Mexas AM, Male F, Brady T, Bushman FD, O'Doherty U. Directly infected resting CD4+T cells can produce HIV gag without spreading infection in a model of HIV latency. PLoS Pathog 2012, 8:e1002818. 10.1371/journal.ppat.1002818, 3406090, 22911005.
5. Fischer M, Joos B, Niederöst B, Kaiser P, Hafner R, Wyl von V, Ackermann M, Weber R, Günthard HF. Biphasic decay kinetics suggest progressive slowing in turnover of latently HIV-1 infected cells during antiretroviral therapy. Retrovirology 2008, 5:107. 10.1186/1742-4690-5-107, 2630982, 19036147.
6. Chun TW, Engel D, Berrey MM, Shea T, Corey L, Fauci AS. Early establishment of a pool of latently infected, resting CD4(+) T cells during primary HIV-1 infection. Proc Natl Acad Sci USA 1998, 95:8869-8873. 10.1073/pnas.95.15.8869, 21169, 9671771.
7. Archin NM, Vaidya NK, Kuruc JD, Liberty AL, Wiegand A, Kearney MF, Cohen MS, Coffin JM, Bosch RJ, Gay CL, Eron JJ, Margolis DM, Perelson AS. Immediate antiviral therapy appears to restrict resting CD4+ cell HIV-1 infection without accelerating the decay of latent infection. Proc Natl Acad Sci USA 2012, 109:9523-9528. 10.1073/pnas.1120248109, 3386138, 22645358.
8. Joos B, Fischer M, Kuster H, Pillai SK, Wong JK, Böni J, Hirschel B, Weber R, Trkola A, Günthard HF, . HIV Swiss Cohort Study HIV rebounds from latently infected cells, rather than from continuing low-level replication. Proc Natl Acad Sci USA 2008, 105:16725-16730. 10.1073/pnas.0804192105, 2575487, 18936487, HIV Swiss Cohort Study.
9. Zhang L, Chung C, Hu BS, He T, Guo Y, Kim AJ, Skulsky E, Jin X, Hurley A, Ramratnam B, Markowitz M, Ho DD. Genetic characterization of rebounding HIV-1 after cessation of highly active antiretroviral therapy. J Clin Invest 2000, 106:839-845. 10.1172/JCI10565, 517816, 11018071.
10. Maldarelli F, Palmer S, King MS, Wiegand A, Polis MA, Mican J, Kovacs JA, Davey RT, Rock-Kress D, Dewar R, Liu S, Metcalf JA, Rehm C, Brun SC, Hanna GJ, Kempf DJ, Coffin JM, Mellors JW. ART suppresses plasma HIV-1 RNA to a stable set point predicted by pretherapy viremia. PLoS Pathog 2007, 3:e46. 10.1371/journal.ppat.0030046, 1847689, 17411338.
11. Palmer S, Maldarelli F, Wiegand A, Bernstein B, Hanna GJ, Brun SC, Kempf DJ, Mellors JW, Coffin JM, King MS. Low-level viremia persists for at least 7 years in patients on suppressive antiretroviral therapy. Proc Natl Acad Sci USA 2008, 105:3879-3884. 10.1073/pnas.0800050105, 2268833, 18332425.
12. 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. 10.1146/annurev.med.59.062806.123001, 17845138.
13. Chun T-W, Fauci AS. HIV reservoirs: pathogenesis and obstacles to viral eradication and cure. AIDS 2012, 26:1261-1268. 10.1097/QAD.0b013e328353f3f1, 22472858.
14. Shan L, Deng K, Shroff NS, Durand CM, Rabi SA, Yang H-C, Zhang H, Margolick JB, Blankson JN, Siliciano RF. Stimulation of HIV-1-specific cytolytic T lymphocytes facilitates elimination of latent viral reservoir after virus reactivation. Immunity 2012, 36:491-501. 10.1016/j.immuni.2012.01.014, 3501645, 22406268.
15. Berger EA. Targeted cytotoxic therapy: adapting a rapidly progressing anticancer paradigm for depletion of persistent HIV-infected cell reservoirs. Curr Opin HIV AIDS 2011, 6:80-85. 10.1097/COH.0b013e3283412515, 3388845, 21242898.
16. Chun T-W, Nickle DC, Justement JS, Large D, Semerjian A, Curlin ME, O'Shea MA, Hallahan CW, Daucher M, Ward DJ, Moir S, Mullins JI, Kovacs C, Fauci AS. HIV-infected individuals receiving effective antiviral therapy for extended periods of time continually replenish their viral reservoir. J Clin Invest 2005, 115:3250-3255. 10.1172/JCI26197, 1265878, 16276421.
17. Rong L, Perelson AS. Modeling latently infected cell activation: viral and latent reservoir persistence, and viral blips in HIV-infected patients on potent therapy. PLoS Comput Biol 2009, 5:e1000533. 10.1371/journal.pcbi.1000533, 2752194, 19834532.
18. Redel L, Le Douce V, Cherrier T, Marban C, Janossy A, Aunis D, Van Lint C, Rohr O, Schwartz C. HIV-1 regulation of latency in the monocyte-macrophage lineage and in CD4+ T lymphocytes. J Leukoc Biol 2010, 87:575-588. 10.1189/jlb.0409264, 19801499.
19. Coleman CM, Wu L. HIV interactions with monocytes and dendritic cells: viral latency and reservoirs. Retrovirology 2009, 6:51. 10.1186/1742-4690-6-51, 2697150, 19486514.
20. Le Douce V, Herbein G, Rohr O, Schwartz C. Molecular mechanisms of HIV-1 persistence in the monocyte-macrophage lineage. Retrovirology 2010, 7:32. 10.1186/1742-4690-7-32, 2873506, 20380694.
21. Murphy KM, Stockinger B. Effector T cell plasticity: flexibility in the face of changing circumstances. Nat Immunol 2010, 11:674-680. 3249647, 20644573.
22. van Leeuwen EMM, Sprent J, Surh CD. Generation and maintenance of memory CD4(+) T Cells. Curr Opin Immunol 2009, 21:167-172. 10.1016/j.coi.2009.02.005, 2676210, 19282163.
23. Fritsch RD, Shen X, Sims GP, Hathcock KS, Hodes RJ, Lipsky PE. Stepwise differentiation of CD4 memory T cells defined by expression of CCR7 and CD27. J Immunol 2005, 175:6489-6497.
24. Riou C, Yassine-Diab B, Van grevenynghe J, Somogyi R, Greller LD, Gagnon D, Gimmig S, Wilkinson P, Shi Y, Cameron MJ, Campos-Gonzalez R, Balderas RS, Kelvin D, Sékaly R-P, Haddad EK. Convergence of TCR and cytokine signaling leads to FOXO3a phosphorylation and drives the survival of CD4+ central memory T cells. J Exp Med 2007, 204:79-91. 10.1084/jem.20061681, 2118424, 17190839.
25. Sallusto F, Geginat J, Lanzavecchia A. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu Rev Immunol 2004, 22:745-763. 10.1146/annurev.immunol.22.012703.104702, 15032595.
26. Rivino L, Messi M, Jarrossay D, Lanzavecchia A, Sallusto F, Geginat J. Chemokine receptor expression identifies Pre-T helper (Th)1, Pre-Th2, and nonpolarized cells among human CD4+ central memory T cells. J Exp Med 2004, 200:725-735. 10.1084/jem.20040774, 2211963, 15381728.
27. Vatakis DN, Nixon CC, Zack JA. Quiescent T cells and HIV: an unresolved relationship. Immunol Res 2010, 48:110-121. 10.1007/s12026-010-8171-0, 20725862.
28. Bleul CC, Wu L, Hoxie JA, Springer TA, Mackay CR. The HIV coreceptors CXCR4 and CCR5 are differentially expressed and regulated on human T lymphocytes. Proc Natl Acad Sci USA 1997, 94:1925-1930. 10.1073/pnas.94.5.1925, 20019, 9050881.
29. Spear M, Guo J, Wu Y. The trinity of the cortical actin in the initiation of HIV-1 infection. Retrovirology 2012, 9:45. 10.1186/1742-4690-9-45, 3416652, 22640593.
30. Zack JA, Arrigo SJ, Weitsman SR, Go AS, Haislip A, Chen IS. HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell 1990, 61:213-222. 10.1016/0092-8674(90)90802-L, 2331748.
31. Meyerhans A, Vartanian JP, Hultgren C, Plikat U, Karlsson A, Wang L, Eriksson S, Wain-Hobson S. Restriction and enhancement of human immunodeficiency virus type 1 replication by modulation of intracellular deoxynucleoside triphosphate pools. J Virol 1994, 68:535-540. 236318, 8254768.
32. Descours B, Cribier A, Chable-Bessia C, Ayinde D, Rice G, Crow Y, Yatim A, Schawartz O, Laguette N, Benkirane M. SAMHD1 restricts HIV-1 reverse transcription in quiescent CD4+ T-cells. Retrovirology 2012, 9:87. 10.1186/1742-4690-9-87, 3494655, 23092122.
33. Baldauf H-M, Pan X, Erikson E, Schmidt S, Daddacha W, Burggraf M, Schenkova K, Ambiel I, Wabnitz G, Gramberg T, Panitz S, Flory E, Landau NR, Sertel S, Rutsch F, Lasitschka F, Kim B, König R, Fackler OT, Keppler OT. SAMHD1 restricts HIV-1 infection in resting CD4(+) T cells. Nat Med 2012, 18(11):1682-1687. 10.1038/nm.2964, 22972397.
34. Stevenson M, Stanwick TL, Dempsey MP, Lamonica CA. HIV-1 replication is controlled at the level of T cell activation and proviral integration. EMBO J 1990, 9:1551-1560. 551849, 2184033.
35. Schnittman SM, Lane HC, Greenhouse J, Justement JS, Baseler M, Fauci AS. Preferential infection of CD4+ memory T cells by human immunodeficiency virus type 1: evidence for a role in the selective T-cell functional defects observed in infected individuals. Proc Natl Acad Sci USA 1990, 87:6058-6062. 10.1073/pnas.87.16.6058, 54471, 2385584.
36. Woods TC, Roberts BD, Butera ST, Folks TM. Loss of inducible virus in CD45RA naive cells after human immunodeficiency virus-1 entry accounts for preferential viral replication in CD45RO memory cells. Blood 1997, 89:1635-1641.
37. Mo H, Monard S, Pollack H, Ip J, Rochford G, Wu L, Hoxie J, Borkowsky W, Ho DD, Moore JP. Expression patterns of the HIV type 1 coreceptors CCR5 and CXCR4 on CD4+ T cells and monocytes from cord and adult blood. AIDS Res Hum Retroviruses 1998, 14:607-617. 10.1089/aid.1998.14.607, 9591715.
38. Pierson T, Hoffman TL, Blankson J, Finzi D, Chadwick K, Margolick JB, Buck C, Siliciano JD, Doms RW, Siliciano RF. Characterization of chemokine receptor utilization of viruses in the latent reservoir for human immunodeficiency virus type 1. J Virol 2000, 74:7824-7833. 10.1128/JVI.74.17.7824-7833.2000, 112312, 10933689.
39. Dai J, Agosto LM, Baytop C, Yu JJ, Pace MJ, Liszewski MK, O'Doherty U. Human immunodeficiency virus integrates directly into naive resting CD4+ T cells but enters naive cells less efficiently than memory cells. J Virol 2009, 83:4528-4537. 10.1128/JVI.01910-08, 2668451, 19211752.
40. Wang W, Guo J, Yu D, Vorster PJ, Chen W, Wu Y. A dichotomy in cortical actin and chemotactic actin activity between human memory and naive T cells contributes to their differential susceptibility to HIV-1 infection. J Biol Chem 2012, 287(42):35455-35469. 10.1074/jbc.M112.362400, 22879601.
41. Chun TW, Carruth L, Finzi D, Shen X, DiGiuseppe JA, Taylor H, Hermankova M, Chadwick K, Margolick J, Quinn TC, Kuo YH, Brookmeyer R, Zeiger MA, Barditch-Crovo P, Siliciano RF. Quantification of latent tissue reservoirs and total body viral load in HIV-1 infection. Nature 1997, 387:183-188. 10.1038/387183a0, 9144289.
42. Delobel P, Sandres-Sauné K, Cazabat M, L'Faqihi F-E, Aquilina C, Obadia M, Pasquier C, Marchou B, Massip P, Izopet J. Persistence of distinct HIV-1 populations in blood monocytes and naive and memory CD4 T cells during prolonged suppressive HAART. AIDS 2005, 19:1739-1750. 10.1097/01.aids.0000183125.93958.26, 16227781.
43. Ostrowski MA, Chun TW, Justement SJ, Motola I, Spinelli MA, Adelsberger J, Ehler LA, Mizell SB, Hallahan CW, Fauci AS. Both memory and CD45RA+/CD62L+ naive CD4(+) T cells are infected in human immunodeficiency virus type 1-infected individuals. J Virol 1999, 73:6430-6435. 112723, 10400736.
44. Brenchley JM, Hill BJ, Ambrozak DR, Price DA, Guenaga FJ, Casazza JP, Kuruppu J, Yazdani J, Migueles SA, Connors M, Roederer M, Douek DC, Koup RA. T-cell subsets that harbor human immunodeficiency virus (HIV) in vivo: implications for HIV pathogenesis. J Virol 2004, 78:1160-1168. 10.1128/JVI.78.3.1160-1168.2004, 321406, 14722271.
45. Chomont N, El-Far M, Ancuta P, Trautmann L, Procopio FA, Yassine-Diab B, Boucher G, Boulassel M-R, Ghattas G, Brenchley JM, Schacker TW, Hill BJ, Douek DC, Routy J-P, Haddad EK, Sékaly R-P. HIV reservoir size and persistence are driven by T cell survival and homeostatic proliferation. Nat Med 2009, 15:893-900. 10.1038/nm.1972, 2859814, 19543283.
46. Wightman F, Solomon A, Khoury G, Green JA, Gray L, Gorry PR, Ho YS, Saksena NK, Hoy J, Crowe SM, Cameron PU, Lewin SR. Both CD31(+) and CD31- naive CD4(+) T cells are persistent HIV type 1-infected reservoirs in individuals receiving antiretroviral therapy. J Infect Dis 2010, 202:1738-1748. 10.1086/656721, 20979453.
47. Li Q, Duan L, Estes JD, Ma Z-M, Rourke T, Wang Y, Reilly C, Carlis J, Miller CJ, Haase AT. Peak SIV replication in resting memory CD4+ T cells depletes gut lamina propria CD4+ T cells. Nature 2005, 434:1148-1152.
48. Unutmaz D, KewalRamani VN, Marmon S, Littman DR. Cytokine signals are sufficient for HIV-1 infection of resting human T lymphocytes. J Exp Med 1999, 189:1735-1746. 10.1084/jem.189.11.1735, 2193071, 10359577.
49. Kinter A, Moorthy A, Jackson R, Fauci AS. Productive HIV infection of resting CD4+ T cells: role of lymphoid tissue microenvironment and effect of immunomodulating agents. AIDS Res Hum Retroviruses 2003, 19:847-856. 10.1089/088922203322493012, 14585216.
50. Eckstein DA, Penn ML, Korin YD, Scripture-Adams DD, Zack JA, Kreisberg JF, Roederer M, Sherman MP, Chin PS, Goldsmith MA. HIV-1 actively replicates in naive CD4(+) T cells residing within human lymphoid tissues. Immunity 2001, 15:671-682. 10.1016/S1074-7613(01)00217-5, 11672548.
51. Weissman D, Daucher J, Barker T, Adelsberger J, Baseler M, Fauci AS. Cytokine regulation of HIV replication induced by dendritic cell-CD4-positive T cell interactions. AIDS Res Hum Retroviruses 1996, 12:759-767. 10.1089/aid.1996.12.759, 8738427.
52. Saleh S, Solomon A, Wightman F, Xhilaga M, Cameron PU, Lewin SR. 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 2007, 110:4161-4164. 10.1182/blood-2007-06-097907, 17881634.
53. Cameron PU, Saleh S, Sallmann G, Solomon A, Wightman F, Evans VA, Boucher G, Haddad EK, Sékaly R-P, Harman AN, Anderson JL, Jones KL, Mak J, Cunningham AL, Jaworowski A, Lewin SR. Establishment of HIV-1 latency in resting CD4+ T cells depends on chemokine-induced changes in the actin cytoskeleton. Proc Natl Acad Sci USA 2010, 107:16934-16939. 10.1073/pnas.1002894107, 2947912, 20837531.
54. Deere JD, Schinazi RF, North TW. Simian immunodeficiency virus macaque models of HIV latency. Curr Opin HIV AIDS 2011, 6:57-61. 10.1097/COH.0b013e32834086ce, 21242894.
55. Brooks DG, Kitchen SG, Kitchen CM, Scripture-Adams DD, Zack JA. Generation of HIV latency during thymopoiesis. Nat Med 2001, 7:459-464. 10.1038/86531, 11283673.
56. Marsden MD, Kovochich M, Suree N, Shimizu S, Mehta R, Cortado R, Bristol G, An DS, Zack JA. HIV latency in the humanized BLT mouse. J Virol 2012, 86:339-347. 10.1128/JVI.06366-11, 3255908, 22072769.
57. Denton PW, Olesen R, Choudhary SK, Archin NM, Wahl A, Swanson MD, Chateau M, Nochi T, Krisko JF, Spagnuolo RA, Margolis DM, Garcia JV. Generation of HIV latency in humanized BLT mice. J Virol 2012, 86:630-634. 10.1128/JVI.06120-11, 3255928, 22013053.
58. Choudhary SK, Archin NM, Cheema M, Dahl NP, Garcia JV, Margolis DM. Latent HIV-1 infection of resting CD4+ T cells in the humanized Rag2-/- γc-/- mouse. J Virol 2012, 86:114-120. 10.1128/JVI.05590-11, 3255863, 22013038.
59. Tyagi M, Romerio F. Models of HIV-1 persistence in the CD4+ T cell compartment: past, present and future. Curr HIV Res 2011, 9:579-587. 10.2174/157016211798998754, 22211662.
60. Planelles V, Wolschendorf F, Kutsch O. Facts and fiction: cellular models for high throughput screening for HIV-1 reactivating drugs. Curr HIV Res 2011, 9:568-578. 10.2174/157016211798998826, 22211661.
61. Pace MJ, Agosto L, Graf EH, O'Doherty U. HIV reservoirs and latency models. Virology 2011, 411:344-354. 10.1016/j.virol.2010.12.041, 21284992.
62. Yang H-C. Primary cell models of HIV latency. Curr Opin HIV AIDS 2011, 6:62-67. 10.1097/COH.0b013e3283412568, 21242895.
63. Hakre S, Chávez L, Shirakawa K, Verdin E. HIV latency: experimental systems and molecular models. FEMS Microbiol Rev 2012, 36:706-716. 10.1111/j.1574-6976.2012.00335.x, 22372374.
64. Sahu GK, Lee K, Ji J, Braciale V, Baron S, Cloyd MW. A novel in vitro system to generate and study latently HIV-infected long-lived normal CD4+ T-lymphocytes. Virology 2006, 355:127-137. 10.1016/j.virol.2006.07.020, 16919704.
65. Marini A, Harper JM, Romerio F. An in vitro system to model the establishment and reactivation of HIV-1 latency. J Immunol 2008, 181:7713-7720.
66. Bosque A, Planelles V. Induction of HIV-1 latency and reactivation in primary memory CD4+ T cells. Blood 2009, 113:58-65. 10.1182/blood-2008-07-168393, 2614643, 18849485.
67. Yang H-C, Xing S, Shan L, O'Connell K, Dinoso J, Shen A, Zhou Y, Shrum CK, Han Y, Liu JO, Zhang H, Margolick JB, Siliciano RF. Small-molecule screening using a human primary cell model of HIV latency identifies compounds that reverse latency without cellular activation. J Clin Invest 2009, 119:3473-3486. 2769176, 19805909.
68. Burnett JC, Lim K-I, Calafi A, Rossi JJ, Schaffer DV, Arkin AP. Combinatorial latency reactivation for HIV-1 subtypes and variants. J Virol 2010, 84:5958-5974. 10.1128/JVI.00161-10, 2876650, 20357084.
69. Tyagi M, Pearson RJ, Karn J. Establishment of HIV latency in primary CD4+ cells is due to epigenetic transcriptional silencing and P-TEFb restriction. J Virol 2010, 84:6425-6437. 10.1128/JVI.01519-09, 2903277, 20410271.
70. Swiggard WJ, Baytop C, Yu JJ, Dai J, Li C, Schretzenmair R, Theodosopoulos T, O'Doherty U. Human immunodeficiency virus type 1 can establish latent infection in resting CD4+ T cells in the absence of activating stimuli. J Virol 2005, 79:14179-14188. 10.1128/JVI.79.22.14179-14188.2005, 1280214, 16254353.
71. Lassen KG, Hebbeler AM, Bhattacharyya D, Lobritz MA, Greene WC. A flexible model of HIV-1 latency permitting evaluation of many primary CD4 T-cell reservoirs. PLoS One 2012, 7:e30176. 10.1371/journal.pone.0030176, 3265466, 22291913.
72. Burke B, Brown HJ, Marsden MD, Bristol G, Vatakis DN, Zack JA. Primary cell model for activation-inducible human immunodeficiency virus. J Virol 2007, 81:7424-7434. 10.1128/JVI.02838-06, 1933352, 17475639.
73. McNamara LA, Ganesh JA, Collins KL. Latent HIV-1 infection occurs in multiple subsets of hematopoietic progenitor cells and is reversed by NF-κB activation. J Virol 2012, 86:9337-9350. 10.1128/JVI.00895-12, 22718820.
74. Redd AD, Avalos A, Essex M. Infection of hematopoietic progenitor cells by HIV-1 subtype C, and its association with anemia in southern Africa. Blood 2007, 110:3143-3149. 10.1182/blood-2007-04-086314, 2200905, 17693583.
75. Carter CC, Onafuwa-Nuga A, McNamara LA, Riddell J, Bixby D, Savona MR, Collins KL. HIV-1 infects multipotent progenitor cells causing cell death and establishing latent cellular reservoirs. Nat Med 2010, 16:446-451. 10.1038/nm.2109, 2892382, 20208541.
76. Durand CM, Ghiaur G, Siliciano JD, Rabi SA, Eisele EE, Salgado M, Shan L, Lai JF, Zhang H, Margolick J, Jones RJ, Gallant JE, Ambinder RF, Siliciano RF. HIV-1 DNA is detected in bone marrow populations containing CD4+ T cells but is not found in purified CD34+ hematopoietic progenitor cells in most patients on antiretroviral therapy. J Infect Dis 2012, 205:1014-1018. 10.1093/infdis/jir884, 22275402.
77. Josefsson L, Eriksson S, Sinclair E, Ho T, Killian M, Epling L, Shao W, Lewis B, Bacchetti P, Loeb L, Custer J, Poole L, Hecht FM, Palmer S. Hematopoietic precursor cells isolated from patients on long-term suppressive HIV therapy did not contain HIV-1 DNA. J Infect Dis 2012, 206:28-34. 10.1093/infdis/jis301, 22536001.
78. McNamara LA, Collins KL. Hematopoietic stem/precursor cells as HIV reservoirs. Curr Opin HIV AIDS 2011, 6:43-48. 10.1097/COH.0b013e32834086b3, 3045752, 21242893.
79. 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. 10.1093/emboj/cdg188, 154479, 12682019.
80. Kim YK, Bourgeois CF, Pearson R, Tyagi M, West MJ, Wong J, Wu S-Y, Chiang C-M, Karn J. Recruitment of TFIIH to the HIV LTR is a rate-limiting step in the emergence of HIV from latency. EMBO J 2006, 25:3596-3604. 10.1038/sj.emboj.7601248, 1538560, 16874302.
81. Duverger A, Jones J, May J, Bibollet-Ruche F, Wagner FA, Cron RQ, Kutsch O. Determinants of the establishment of human immunodeficiency virus type 1 latency. J Virol 2009, 83:3078-3093. 10.1128/JVI.02058-08, 2655589, 19144703.
82. Donahue DA, Kuhl BD, Sloan RD, Wainberg MA. The viral protein Tat can inhibit the establishment of HIV-1 latency. J Virol 2012, 86:3253-3263. 10.1128/JVI.06648-11, 3302319, 22238306.
83. Weinberger LS, Burnett JC, Toettcher JE, Arkin AP, Schaffer DV. Stochastic gene expression in a lentiviral positive-feedback loop: HIV-1 Tat fluctuations drive phenotypic diversity. Cell 2005, 122:169-182. 10.1016/j.cell.2005.06.006, 16051143.
84. Burnett JC, Miller-Jensen K, Shah PS, Arkin AP, Schaffer DV. Control of stochastic gene expression by host factors at the HIV promoter. PLoS Pathog 2009, 5:e1000260. 10.1371/journal.ppat.1000260, 2607019, 19132086.
85. Micheva-Viteva S, Pacchia AL, Ron Y, Peltz SW, Dougherty JP. Human immunodeficiency virus type 1 latency model for high-throughput screening. Antimicrob Agents Chemother 2005, 49:5185-5188. 10.1128/AAC.49.12.5185-5188.2005, 1315948, 16304201.
86. Jeeninga RE, Westerhout EM, van Gerven ML, Berkhout B. HIV-1 latency in actively dividing human T cell lines. Retrovirology 2008, 5:37. 10.1186/1742-4690-5-37, 2387167, 18439275.
87. Perelson AS, Neumann AU, Markowitz M, Leonard JM, Ho DD. HIV-1 dynamics in vivo: virion clearance rate, infected cell life-span, and viral generation time. Science 1996, 271:1582-1586. 10.1126/science.271.5255.1582, 8599114.
88. Coiras M, López-Huertas MR, Pérez-Olmeda M, Alcamí J. Understanding HIV-1 latency provides clues for the eradication of long-term reservoirs. Nat Rev Microbiol 2009, 7:798-812. 10.1038/nrmicro2223, 19834480.
89. Siliciano RF, Greene WC. HIV Latency. Cold Spring Harb Perspect Med 2011, 1:a007096. 3234450, 22229121.
90. Mbonye U, Karn J. Control of HIV latency by epigenetic and non-epigenetic mechanisms. Curr HIV Res 2011, 9:554-567. 10.2174/157016211798998736, 3319922, 22211660.
91. Margolis DM. Mechanisms of HIV latency: an emerging picture of complexity. Curr HIV/AIDS Rep 2010, 7:37-43. 10.1007/s11904-009-0033-9, 20425056.
92. Chomont N, DaFonseca S, Vandergeeten C, Ancuta P, Sékaly R-P. Maintenance of CD4+ T-cell memory and HIV persistence: keeping memory, keeping HIV. Curr Opin HIV AIDS 2011, 6:30-36. 10.1097/COH.0b013e3283413775, 21242891.
93. Schröder ARW, Shinn P, Chen H, Berry C, Ecker JR, Bushman F. HIV-1 integration in the human genome favors active genes and local hotspots. Cell 2002, 110:521-529. 10.1016/S0092-8674(02)00864-4, 12202041.
94. Wang GP, Ciuffi A, Leipzig J, Berry CC, Bushman FD. HIV integration site selection: analysis by massively parallel pyrosequencing reveals association with epigenetic modifications. Genome Res 2007, 17:1186-1194. 10.1101/gr.6286907, 1933515, 17545577.
95. Vatakis DN, Kim S, Kim N, Chow SA, Zack JA. Human immunodeficiency virus integration efficiency and site selection in quiescent CD4+ T cells. J Virol 2009, 83:6222-6233. 10.1128/JVI.00356-09, 2687367, 19369341.
96. Brady T, Agosto LM, Malani N, Berry CC, O'Doherty U, Bushman F. HIV integration site distributions in resting and activated CD4+ T cells infected in culture. AIDS 2009, 23:1461-1471. 10.1097/QAD.0b013e32832caf28, 2862484, 19550285.
97. Shan L, Yang H-C, Rabi SA, Bravo HC, Shroff NS, Irizarry RA, Zhang H, Margolick JB, Siliciano JD, Siliciano RF. Influence of host gene transcription level and orientation on HIV-1 latency in a primary-cell model. J Virol 2011, 85:5384-5393. 10.1128/JVI.02536-10, 3094997, 21430059.
98. Lewinski MK, Bisgrove D, Shinn P, Chen H, Hoffmann C, Hannenhalli S, Verdin E, Berry CC, Ecker JR, Bushman FD. Genome-wide analysis of chromosomal features repressing human immunodeficiency virus transcription. J Virol 2005, 79:6610-6619. 10.1128/JVI.79.11.6610-6619.2005, 1112149, 15890899.
99. Han Y, Lassen K, Monie D, Sedaghat AR, Shimoji S, Liu X, Pierson TC, Margolick JB, Siliciano RF, Siliciano JD. Resting CD4+ T cells from human immunodeficiency virus type 1 (HIV-1)-infected individuals carry integrated HIV-1 genomes within actively transcribed host genes. J Virol 2004, 78:6122-6133. 10.1128/JVI.78.12.6122-6133.2004, 416493, 15163705.
100. Shearwin KE, Callen BP, Egan JB. Transcriptional interference-a crash course. Trends Genet 2005, 21:339-345. 10.1016/j.tig.2005.04.009, 2941638, 15922833.
101. Mazo A, Hodgson JW, Petruk S, Sedkov Y, Brock HW. Transcriptional interference: an unexpected layer of complexity in gene regulation. J Cell Sci 2007, 120:2755-2761. 10.1242/jcs.007633, 17690303.
102. Han Y, Lin YB, An W, Xu J, Yang H-C, O'Connell K, Dordai D, Boeke JD, Siliciano JD, Siliciano RF. Orientation-dependent regulation of integrated HIV-1 expression by host gene transcriptional readthrough. Cell Host Microbe 2008, 4:134-146. 10.1016/j.chom.2008.06.008, 2604135, 18692773.
103. Lenasi T, Contreras X, Peterlin BM. Transcriptional interference antagonizes proviral gene expression to promote HIV latency. Cell Host Microbe 2008, 4:123-133. 10.1016/j.chom.2008.05.016, 18692772.
104. Gallastegui E, Millán-Zambrano G, Terme J-M, Chávez S, Jordan A. Chromatin reassembly factors are involved in transcriptional interference promoting HIV latency. J Virol 2011, 85:3187-3202. 10.1128/JVI.01920-10, 3067836, 21270164.
105. Ganesh L, Burstein E, Guha-Niyogi A, Louder MK, Mascola JR, Klomp LWJ, Wijmenga C, Duckett CS, Nabel GJ. The gene product Murr1 restricts HIV-1 replication in resting CD4+ lymphocytes. Nature 2003, 426:853-857. 10.1038/nature02171, 14685242.
106. Duverger A, Wolschendorf F, Zhang M, Wagner F, Hatcher B, Jones J, Cron RQ, van der Sluis RM, Jeeninga RE, Berkhout B, Kutsch O. An AP-1 binding site in the enhancer/core element of the HIV-1 promoter controls the ability of HIV-1 to establish latent infection. J Virol 2012, [Epub ahead of print].
107. Vandergeeten C, Fromentin R, Chomont N. The role of cytokines in the establishment, persistence and eradication of the HIV reservoir. Cytokine Growth Factor Rev 2012, 23:143-149. 10.1016/j.cytogfr.2012.05.001, 22743037.
108. Zhou Q, Yik JHN. The Yin and Yang of P-TEFb regulation: implications for human immunodeficiency virus gene expression and global control of cell growth and differentiation. Microbiol Mol Biol Rev 2006, 70:646-659. 10.1128/MMBR.00011-06, 1594588, 16959964.
109. Budhiraja S, Famiglietti M, Bosque A, Planelles V, Rice AP. Cyclin T1 and CDK9 T-loop phosphorylation are downregulated during establishment of HIV-1 latency in primary resting memory CD4+ T cells. J Virol 2012, 87(2):1211-1220.
110. Jenuwein T, Allis CD. Translating the histone code. Science 2001, 293:1074-1080. 10.1126/science.1063127, 11498575.
111. du Chéné I, Basyuk E, Lin Y-L, Triboulet R, Knezevich A, Chable-Bessia C, Mettling C, Baillat V, Reynes J, Corbeau P, Bertrand E, Marcello A, Emiliani S, Kiernan R, Benkirane M. Suv39H1 and HP1gamma are responsible for chromatin-mediated HIV-1 transcriptional silencing and post-integration latency. EMBO J 2007, 26:424-435. 10.1038/sj.emboj.7601517, 1783455, 17245432.
112. Marban C, Suzanne S, Dequiedt F, de Walque S, Redel L, Van Lint C, Aunis D, Rohr O. Recruitment of chromatin-modifying enzymes by CTIP2 promotes HIV-1 transcriptional silencing. EMBO J 2007, 26:412-423. 10.1038/sj.emboj.7601516, 1783449, 17245431.
113. Tyagi M, Karn J. CBF-1 promotes transcriptional silencing during the establishment of HIV-1 latency. EMBO J 2007, 26:4985-4995. 10.1038/sj.emboj.7601928, 2140115, 18007589.
114. Pearson R, Kim YK, Hokello J, Lassen K, Friedman J, Tyagi M, Karn J. Epigenetic silencing of human immunodeficiency virus (HIV) transcription by formation of restrictive chromatin structures at the viral long terminal repeat drives the progressive entry of HIV into latency. J Virol 2008, 82:12291-12303. 10.1128/JVI.01383-08, 2593349, 18829756.
115. Friedman J, Cho W-K, Chu CK, Keedy KS, Archin NM, Margolis DM, Karn J. Epigenetic silencing of HIV-1 by the histone H3 lysine 27 methyltransferase enhancer of Zeste 2. J Virol 2011, 85:9078-9089. 10.1128/JVI.00836-11, 3165831, 21715480.
116. Kauder SE, Bosque A, Lindqvist A, Planelles V, Verdin E. Epigenetic regulation of HIV-1 latency by cytosine methylation. PLoS Pathog 2009, 5:e1000495. 10.1371/journal.ppat.1000495, 2695767, 19557157.
117. Rafati H, Parra M, Hakre S, Moshkin Y, Verdin E, Mahmoudi T. Repressive LTR nucleosome positioning by the BAF complex is required for HIV latency. PLoS Biol 2011, 9:e1001206. 10.1371/journal.pbio.1001206, 3226458, 22140357.
118. Sobhian B, Laguette N, Yatim A, Nakamura M, Levy Y, Kiernan R, Benkirane M. HIV-1 Tat assembles a multifunctional transcription elongation complex and stably associates with the 7SK snRNP. Mol Cell 2010, 38:439-451. 10.1016/j.molcel.2010.04.012, 20471949.
119. He N, Liu M, Hsu J, Xue Y, Chou S, Burlingame A, Krogan NJ, Alber T, Zhou Q. HIV-1 Tat and host AFF4 recruit two transcription elongation factors into a bifunctional complex for coordinated activation of HIV-1 transcription. Mol Cell 2010, 38:428-438. 10.1016/j.molcel.2010.04.013, 3085314, 20471948.
120. Yukl S, Pillai S, Li P, Chang K, Pasutti W, Ahlgren C, Havlir D, Strain M, Günthard H, Richman D, Rice AP, Daar E, Little S, Wong JK. Latently-infected CD4+ T cells are enriched for HIV-1 Tat variants with impaired transactivation activity. Virology 2009, 387:98-108. 10.1016/j.virol.2009.01.013, 19268337.
121. Weinberger LS, Dar RD, Simpson ML. Transient-mediated fate determination in a transcriptional circuit of HIV. Nat Genet 2008, 40:466-470. 10.1038/ng.116, 18344999.
122. Huang J, Wang F, Argyris E, Chen K, Liang Z, Tian H, Huang W, Squires K, Verlinghieri G, Zhang H. Cellular microRNAs contribute to HIV-1 latency in resting primary CD4+ T lymphocytes. Nat Med 2007, 13:1241-1247. 10.1038/nm1639, 17906637.
123. Chable-Bessia C, Meziane O, Latreille D, Triboulet R, Zamborlini A, Wagschal A, Jacquet J-M, Reynes J, Levy Y, Saib A, Bennasser Y, Benkirane M. Suppression of HIV-1 replication by microRNA effectors. Retrovirology 2009, 6:26. 10.1186/1742-4690-6-26, 2657893, 19272132.
124. Chiang K, Rice AP. MicroRNA-Mediated Restriction of HIV-1 in Resting CD4(+) T Cells and Monocytes. Viruses 2012, 4:1390-1409. 10.3390/v4091390, 3499811, 23170164.
125. Li XD, Moore B, Cloyd MW. Gradual shutdown of virus production resulting in latency is the norm during the chronic phase of human immunodeficiency virus replication and differential rates and mechanisms of shutdown are determined by viral sequences. Virology 1996, 225:196-212. 10.1006/viro.1996.0588, 8918547.
126. van der Sluis RM, Pollakis G, van Gerven ML, Berkhout B, Jeeninga RE. Latency profiles of full length HIV-1 molecular clone variants with a subtype specific promoter. Retrovirology 2011, 8:73. 10.1186/1742-4690-8-73, 3182984, 21923919.
127. Trono D, Van Lint C, Rouzioux C, Verdin E, Barré-Sinoussi F, Chun T-W, Chomont N. HIV persistence and the prospect of long-term drug-free remissions for HIV-infected individuals. Science 2010, 329:174-180. 10.1126/science.1191047, 20616270.
128. Evans VA, Khoury G, Saleh S, Cameron PU, Lewin SR. HIV persistence: Chemokines and their signalling pathways. Cytokine Growth Factor Rev 2012, 23:151-157. 10.1016/j.cytogfr.2012.05.002, 22749173.
129. Strain MC, Little SJ, Daar ES, Havlir DV, Günthard HF, Lam RY, Daly OA, Nguyen J, Ignacio CC, Spina CA, Richman DD, Wong JK. Effect of treatment, during primary infection, on establishment and clearance of cellular reservoirs of HIV-1. In J Infect Dis 2005, 191:1410-1418.
130. Ananworanich J, Schuetz A, Vandergeeten C, Sereti I, de Souza M, Rerknimitr R, Dewar R, Marovich M, van Griensven F, Sekaly R, Pinyakorn S, Phanuphak N, Trichavaroj R, Rutvisuttinunt W, Chomchey N, Paris R, Peel S, Valcour V, Maldarelli F, Chomont N, Michael N, Phanuphak P, Kim JH, . RV254/SEARCH 010 Study Group Impact of multi-targeted antiretroviral treatment on gut T cell depletion and HIV reservoir seeding during acute HIV infection. PLoS One 2012, 7:e33948. 10.1371/journal.pone.0033948, 3316511, 22479485, RV254/SEARCH 010 Study Group.
131. Chun T-W, Justement JS, Moir S, Hallahan CW, Maenza J, Mullins JI, Collier AC, Corey L, Fauci AS. Decay of the HIV reservoir in patients receiving antiretroviral therapy for extended periods: implications for eradication of virus. J Infect Dis 2007, 195:1762-1764. 10.1086/518250, 17492591.
132. Gianella S, Wyl von V, Fischer M, Niederoest B, Battegay M, Bernasconi E, Cavassini M, Rauch A, Hirschel B, Vernazza P, Weber R, Joos B, Günthard HF, . Swiss HIV Cohort Study Effect of early antiretroviral therapy during primary HIV-1 infection on cell-associated HIV-1 DNA and plasma HIV-1 RNA. Antivir Ther (Lond) 2011, 16:535-545. Swiss HIV Cohort Study.