Dendritic Cell-induced Activation of Latent HIV-1 Provirus in Actively Proliferating Primary T Lymphocytes

PLoS Pathogens

Volumn 9, Issue 3, 2013, Pages

  van der Sluis, Renée M ^a   van Montfort, Thijs ^a   Pollakis, Georgios ^a   Sanders, Rogier W ^a,b   Speijer, Dave ^a   Berkhout, Ben ^a   Jeeninga, Rienk E ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUTYRIC ACID; CD14 ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; CD45RO ANTIGEN; CD69 ANTIGEN; CHEMOKINE RECEPTOR CCR7; GAG PROTEIN; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 7 RECEPTOR; IONOMYCIN; NEF PROTEIN; PHOSPHATIDYLSERINE; PHYTOHEMAGGLUTININ; PROTEIN KINASE C; RALTEGRAVIR; TIFUVIRTIDE; TRANSCRIPTION FACTOR NFAT; TRICHOSTATIN A; TUMOR NECROSIS FACTOR ALPHA;

APOPTOSIS; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DENDRITIC CELL; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PHENOTYPE; PROVIRUS; REAL TIME POLYMERASE CHAIN REACTION; T LYMPHOCYTE; VIRUS LATENCY; VIRUS LOAD; VIRUS TRANSCRIPTION;

CELL PROLIFERATION; COCULTURE TECHNIQUES; DENDRITIC CELLS; HEK293 CELLS; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; PROVIRUSES; T-LYMPHOCYTES; VIRUS ACTIVATION; VIRUS LATENCY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84875989411     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003259     Document Type: Article

References (66)

1. Chun TW, Davey RT Jr, Engel D, Lane HC, Fauci AS, (1999) Re-emergence of HIV after stopping therapy. Nature 401: 874-875.
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. Chun TW, Stuyver L, Mizell SB, Ehler LA, Mican JA, et al. (1997) Presence of an inducible HIV-1 latent reservoir during highly active antiretroviral therapy. Proc Natl Acad Sci U S A 94: 13193-13197.
4. 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.
5. Shen L, Siliciano RF, (2008) Viral reservoirs, residual viremia, and the potential of highly active antiretroviral therapy to eradicate HIV infection. J Allergy Clin Immunol 122: 22-28.
6. Chun TW, Engel D, Berrey MM, Shea T, Corey L, et al. (1998) Early establishment of a pool of latently infected, resting CD4(+) T cells during primary HIV-1 infection. Proc Natl Acad Sci U S A 95: 8869-8873.
7. Dinoso JB, Rabi SA, Blankson JN, Gama L, Mankowski JL, et al. (2009) A simian immunodeficiency virus-infected macaque model to study viral reservoirs that persist during highly active antiretroviral therapy. J Virol 83: 9247-9257.
8. Imamichi H, Degray G, Asmuth DM, Fischl MA, Landay AL, et al. (2011) HIV-1 viruses detected during episodic blips following interleukin-7 administration are similar to the viruses present before and after interleukin-7 therapy. AIDS 25: 159-164.
9. 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.
10. 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.
11. Schmid A, Gianella S, Von Wyl V, Metzner KJ, Scherrer AU, et al. (2010) Profound depletion of HIV-1 transcription in patients initiating antiretroviral therapy during acute infection. PLoS One 5: e13310.
12. 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.
13. 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.
14. Chun TW, Davey RT Jr, Ostrowski M, Shawn JJ, Engel D, et al. (2000) Relationship between pre-existing viral reservoirs and the re-emergence of plasma viremia after discontinuation of highly active anti-retroviral therapy. Nat Med 6: 757-761.
15. Zhu T, Muthui D, Holte S, Nickle D, Feng F, et al. (2002) Evidence for human immunodeficiency virus type 1 replication in vivo in CD14(+) monocytes and its potential role as a source of virus in patients on highly active antiretroviral therapy. J Virol 76: 707-716.
16. Coleman CM, Wu L, (2009) HIV interactions with monocytes and dendritic cells: viral latency and reservoirs. Retrovirology 6: 51.
17. Zhang Z, Schuler T, Zupancic M, Wietgrefe S, Staskus KA, et al. (1999) Sexual transmission and propagation of SIV and HIV in resting and activated CD4+ T cells. Science 286: 1353-1357.
18. Zhou Y, Zhang H, Siliciano JD, Siliciano RF, (2005) Kinetics of human immunodeficiency virus type 1 decay following entry into resting CD4+ T cells. J Virol 79: 2199-2210.
19. 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.
20. 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.
21. 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.
22. Unutmaz D, KewalRamani VN, Marmon S, Littman DR, (1999) Cytokine signals are sufficient for HIV-1 infection of resting human T lymphocytes. J Exp Med 189: 1735-1746.
23. Arlen PA, Brooks DG, Gao LY, Vatakis D, Brown HJ, et al. (2006) Rapid expression of human immunodeficiency virus following activation of latently infected cells. J Virol 80: 1599-1603.
24. 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.
25. Blankson JN, Persaud D, Siliciano RF, (2002) The challenge of viral reservoirs in HIV-1 infection. Annu Rev Med 53: 557-593.
26. Pierson T, McArthur J, Siliciano RF, (2000) Reservoirs for HIV-1: mechanisms for viral persistence in the presence of antiviral immune responses and antiretroviral therapy. Annu Rev Immunol 18: 665-708.
27. Yang HC, (2011) Primary cell models of HIV latency. Curr Opin HIV AIDS 6: 62-67.
28. Jeeninga RE, Westerhout EM, Van Gerven ML, Berkhout B, (2008) HIV-1 latency in actively dividing human T cell lines. Retrovirology 5: 37.
29. 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.
30. Poli G, Orenstein JM, Kinter A, Folks TM, Fauci AS, (1989) Interferon-alpha but not AZT suppresses HIV expression in chronically infected cell lines. Science 244: 575-577.
31. 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.
32. 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.
33. 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.
34. 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.
35. Van der Sluis RM, Pollakis G, Van Gerven ML, Berkhout B, Jeeninga RE, (2011) Latency profiles of full length HIV-1 molecular clone variants with a subtype specific promoter. Retrovirology 8: 73.
36. 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.
37. 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.
38. Wolschendorf F, Bosque A, Shishido T, Duverger A, Jones J, et al. (2012) Kinase control prevents HIV-1 reactivation in spite of high levels of induced NF-kappaB activity. J Virol 86: 4548-4558.
39. 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.
40. Quivy V, Adam E, Collette Y, Demonte D, Chariot A, et al. (2002) 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 76: 11091-11103.
41. 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.
42. Banchereau J, Steinman RM, (1998) Dendritic cells and the control of immunity. Nature 392: 245-252.
43. Sallusto F, Lanzavecchia A, (2000) Understanding dendritic cell and T-lymphocyte traffic through the analysis of chemokine receptor expression. Immunol Rev 177: 134-140.
44. Garcia JV, Miller AD, (1991) Serine phosphorylation-independent downregulation of cell-surface CD4 by nef. Nature 350: 508-511.
45. Bosque A, Planelles V, (2009) Induction of HIV-1 latency and reactivation in primary memory CD4+ T cells. Blood 113: 58-65.
46. 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.
47. 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.
48. Geijtenbeek TB, Kwon DS, Torensma R, Van Vliet SJ, Van Duijnhoven GC, et al. (2000) DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100: 587-597.
49. Van Montfort T, Nabatov AA, Geijtenbeek TB, Pollakis G, Paxton WA, (2007) Efficient capture of antibody neutralized HIV-1 by cells expressing DC-SIGN and transfer to CD4+ T lymphocytes. J Immunol 178: 3177-3185.
50. Gringhuis SI, Van der Vlist M, Van den Berg LM, Den Dunnen J, Litjens M, et al. (2010) HIV-1 exploits innate signaling by TLR8 and DC-SIGN for productive infection of dendritic cells. Nat Immunol 11: 419-426.
51. Butera ST, Perez VL, Wu BY, Nabel GJ, Folks TM, (1991) Oscillation of the human immunodeficiency virus surface receptor is regulated by the state of viral activation in a CD4+ cell model of chronic infection. J Virol 65: 4645-4653.
52. Clouse KA, Powell D, Washington I, Poli G, Strebel K, et al. (1989) Monokine regulation of human immunodeficiency virus-1 expression in a chronically infected human T cell clone. J Immunol 142: 431-438.
53. Dustin ML, Springer TA, (1989) T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1. Nature 341: 619-624.
54. Van Kooyk Y, Kemenade Van de Wiel-van, Weder P, Kuijpers TW, Figdor CG, (1989) Enhancement of LFA-1-mediated cell adhesion by triggering through CD2 or CD3 on T lymphocytes. Nature 342: 811-813.
55. Dustin ML, Depoil D, (2011) New insights into the T cell synapse from single molecule techniques. Nat Rev Immunol 11: 672-684.
56. Groot F, Kuijpers TW, Berkhout B, De Jong EC, (2006) Dendritic cell-mediated HIV-1 transmission to T cells of LAD-1 patients is impaired due to the defect in LFA-1. Retrovirology 3: 75.
57. Sanders RW, De Jong EC, Baldwin CE, Schuitemaker JH, Kapsenberg ML, et al. (2002) Differential transmission of human immunodeficiency virus type 1 by distinct subsets of effector dendritic cells. J Virol 76: 7812-7821.
58. Wang JH, Kwas C, Wu L, (2009) Intercellular adhesion molecule 1 (ICAM-1), but not ICAM-2 and-3, is important for dendritic cell-mediated human immunodeficiency virus type 1 transmission. J Virol 83: 4195-4204.
59. Evans VA, Saleh S, Haddad EK, Cameron PU, Sekaly RP, et al. (2010) Myeloid dendritic cells induce HIV-1 latency in non-proliferating CD4+ T cells. Journal of the international AIDS Society Suppl 3: O7.
60. 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.
61. Deeks SG, (2012) HIV: Shock and kill. Nature 487: 439-440.
62. Van Montfort T, Thomas AA, Pollakis G, Paxton WA, (2008) Dendritic cells preferentially transfer CXCR4-using human immunodeficiency virus type 1 variants to CD4+ T lymphocytes in trans. J Virol 82: 7886-7896.
63. Peden K, Sheng L, Omeir R, Yacobucci M, Klutch M, et al. (2008) Recovery of strains of the polyomavirus SV40 from rhesus monkey kidney cells dating from the 1950s to the early 1960s. Virology 370: 63-76.
64. Das AT, Klaver B, Berkhout B, (1999) A hairpin structure in the R region of the human immunodeficiency virus type 1 RNA genome is instrumental in polyadenylation site selection. J Virol 73: 81-91.
65. Liszewski MK, Yu JJ, O'Doherty U, (2009) Detecting HIV-1 integration by repetitive-sampling Alu-gag PCR. Methods 47: 254-260.
66. Van der Sluis RM, Van Montfort T, Centlivre M, Schopman NC, Cornelissen M, et al. (2012) Quantitation of HIV-1 DNA with a sensitive TaqMan assay that has broad subtype specificity. J Virol Methods 187: 94-102.