Latent HIV-1 infection occurs in multiple subsets of hematopoietic progenitor cells and is reversed by NF-κB activation

Journal of Virology

Volumn 86, Issue 17, 2012, Pages 9337-9350

  McNamara, Lucy A ^a,b   Ganesh, Janani A ^a   Collins, Kathleen L ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; ALKALINE PHOSPHATASE PLACENTA ISOENZYME; CD133 ANTIGEN; CD34 ANTIGEN; CD38 ANTIGEN; CD45RA ANTIGEN; CYCLIN DEPENDENT KINASE 9; CYCLIN T1; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HEXAMETHYLENEBISACETAMIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; POSITIVE TRANSCRIPTION ELONGATION FACTOR B; PROSTRATIN; PROTEIN KINASE C ACTIVATOR; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR FOSB; TRANSCRIPTION FACTOR JUNB; TRANSCRIPTION FACTOR REL; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR RELB; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VORINOSTAT;

ANTIGEN EXPRESSION; ARTICLE; B NK PROGENITOR CELL; BONE MARROW; CELL ISOLATION; CELL STIMULATION; CELL TYPE; COMMON MYELOID PROGENITOR CELL; CONTROLLED STUDY; DISEASE CARRIER; DISEASE MODEL; ENVELOPE GENE; GENE DELETION; GENE EXPRESSION; GRANULOCYTE MONOCYTE ERYTHROID PROGENITOR CELL; HEMATOPOIETIC STEM CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 GENE; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMATURE CELL; IN VITRO STUDY; LATENT VIRUS INFECTION; MEGAKARYOCYTE ERYTHROID PROGENITOR CELL; MEMORY T LYMPHOCYTE; MOLECULAR DYNAMICS; MULTILYMPHOID PROGENITOR CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RESTING MEMORY T LYMPHOCYTE; UMBILICAL CORD BLOOD; VIRUS GENE; VIRUS REACTIVATION; VIRUS REPLICATION;

CD4-POSITIVE T-LYMPHOCYTES; CELL LINE; CELLS, CULTURED; HEMATOPOIETIC STEM CELLS; HIV INFECTIONS; HIV-1; HUMANS; NF-KAPPA B; VIRUS LATENCY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84866145816     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00895-12     Document Type: Article

References (86)

1. Abbate I, et al. 2011. Detection of quasispecies variants predicted to use CXCR4 by ultra-deep pyrosequencing during early HIV infection. AIDS 25:611-617.
2. Aggarwal BB. 2000. Tumour necrosis factors receptor associated signalling molecules and their role in activation of apoptosis, JNK and NF-κB. Ann. Rheum. Dis. 59(Suppl. 1):i6 -i16.
3. + T cells. J. Virol. 80:6441-6457.
4. Barboric M, et al. 2007. Tat competes with HEXIM1 to increase the active pool of P-TEFb for HIV-1 transcription. Nucleic Acids Res. 35:2003-2012.
5. Baxter A, et al. 2004. Hit-to-lead studies: the discovery of potent, orally active, thiophenecarboxamide IKK-2 inhibitors. Bioorg. Med. Chem. Lett. 14:2817-2822.
6. Blazkova J, et al. 2009. CpG methylation controls reactivation of HIV from latency. PLoS Pathog. 5:e1000554. doi:10.1371/journal.ppat. 1000554.
7. + T cells. PLoS Pathog. 7:e1002288. doi:10.1371/journal.ppat.1002288.
8. + T cells. Blood 113:58-65.
9. + T cells reveals a novel source of residual viremia in patients on antiretroviral therapy. J. Virol. 83:8470-8481.
10. Burkly L, et al. 1995. Expression of relB is required for the development of thymic medulla and dendritic cells. Nature 373:531-536.
11. Canonne-Hergaux F, Aunis D, Schaeffer E. 1995. Interactions of the transcription factor AP-1 with the long terminal repeat of different human immunodeficiency virus type 1 strains in Jurkat, glial, and neuronal cells. J. Virol. 69:6634-6642.
12. Carter CC, et al. 2011. HIV-1 utilizes the CXCR4 chemokine receptor to infect multipotent hematopoietic stem and progenitor cells. Cell Host Microbe 9:223-234.
13. Carter CC, et al. 2010. HIV-1 infects multipotent progenitor cells causing cell death and establishing latent cellular reservoirs. Nat. Med. 16:446-451.
14. Chalmet K, et al. 2012. Presence of CXCR4-using HIV-1 in patients with recently diagnosed infection: correlates and evidence for transmission. J. Infect. Dis. 205:174-184.
15. Chen BK, Gandhi RT, Baltimore D. 1996. CD4 down-modulation during infection of human T cells with human immunodeficiency virus type 1 involves independent activities of vpu, env, and nef. J. Virol. 70:6044-6053.
16. Chen G, Goeddel DV. 2002. TNF-R1 signaling: a beautiful pathway. Science 296:1634-1635.
17. Chomont N, et al. 2009. HIV reservoir size and persistence are driven by T cell survival and homeostatic proliferation. Nat. Med. 15:893-900.
18. 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:e146. doi:10.1371/journal.ppat.0030146.
19. Contreras X, et al. 2009. Suberoylanilide hydroxamic acid reactivates HIV from latently infected cells. J. Biol. Chem. 284:6782-6789.
20. Doulatov S, Notta F, Eppert K, Nguyen L. 2010. Revised map of the human progenitor hierarchy shows the origin of macrophages and dendritic cells in early lymphoid development. Nat. Immunol. 11:585-593.
21. + hematopoietic progenitor cells in most patients on antiretroviral therapy. J. Infect. Dis. 205:1014-1018.
22. Duverger A, et al. 2009. Determinants of the establishment of human immunodeficiency virus type 1 latency. J. Virol. 83:3078-3093.
23. Ea C-K, Deng L, Xia Z-P, Pineda G, Chen ZJ. 2006. Activation of IKK by TNFα requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO. Mol. Cell 22:245-257.
24. Edelstein LC, Micheva-Viteva S, Phelan BD, Dougherty JP. 2009. 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.
25. + T cells provides a mechanism for lifelong persistence of HIV-1, even in patients on effective combination therapy. Nat. Med. 5:512-517.
26. Folks TM, Justement J, Kinter A, Dinarello CA, Fauci AS. 1987. Cytokine-induced expression of HIV-1 in a chronically infected promonocyte cell line. Science 238:800-802.
27. Gaide O, et al. 2002. CARMA1 is a critical lipid raft-associated regulator of TCR-induced NF-κB activation. Nat. Immunol. 3:836-843.
28. Gasmi M, et al. 1999. Requirements for efficient production and transduction of human immunodeficiency virus type 1-based vectors. J. Virol. 73:1828-1834.
29. Geeraert L, Kraus G, Pomerantz RJ. 2008. Hide-and-seek: the challenge of viral persistence in HIV-1 infection. Annu. Rev. Med. 59:487-501.
30. Gulick RM, et al. 1997. Treatment with indinavir, zidovudine, and lamivudine in adults with human immunodeficiency virus infection and prior antiretroviral therapy. N. Engl. J. Med. 337:734-739.
31. Hammer SM, et al. 1997. A controlled trial of two nucleoside analogues plus indinavir in persons with human immunodeficiency virus infection and CD4 cell counts of 200 per cubic millimeter or less. AIDS Clinical Trials Group 320 Study Team. N. Engl. J. Med. 337:725-733.
32. Hara H, et al. 2003. The MAGUK family protein CARD11 is essential for lymphocyte activation. Immunity 18:763-775.
33. Herrmann CH, Carroll RG, Wei P, Jones KA, Rice AP. 1998. Tatassociated kinase, TAK, activity is regulated by distinct mechanisms in peripheral blood lymphocytes and promonocytic cell lines. J. Virol. 72:9881-9888.
34. Hsu H, Shu HB, Pan MG, Goeddel DV. 1996. TRADD-TRAF2 and TRADD-FADD interactions define two distinct TNF receptor 1 signal transduction pathways. Cell 84:299-308.
35. 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.
36. Josefsson L, et al. 2012. Hematopoietic precursor cells isolated from patients on long term suppressive HIV therapy did not contain HIV-1 DNA. J. Infect. Dis. 206:28-34.
37. Kauder S, Boque A, Lindqvist A, Planelles V, Verdin E. 2009. Epigenetic regulation of HIV-1 latency by cytosine methylation. PLoS Pathog. 5:e1000495. doi:10.1371/journal.ppat.1000495.
38. Kim YK, Mbonye U, Hokello J, Karn J. 2011. T-cell receptor signaling enhances transcriptional elongation from latent HIV proviruses by activating P-TEFb through an ERK-dependent pathway. J. Mol. Biol. 410:896-916.
39. Kohno T, et al. 2002. A new improved method for the concentration of HIV-1 infective particles. J. Virol. Methods 106:167-173.
40. Korin Y, Brooks D, Brown S, Korotzer A, Zack JA. 2002. Effects of prostratin on T-cell activation and human immunodeficiency virus latency. J. Virol. 76:8118-8123.
41. 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. doi:10.1371/journal.pone.0030176.
42. Li SW, et al. 1999. The IKKβ subunit of IκB kinase (IKK) is essential for nuclear factor κB activation and prevention of apoptosis. J. Exp. Med. 189:1839-1845.
43. Lucas PC, et al. 2001. Bcl10 and MALT1, independent targets of chromosomal translocation in MALT lymphoma, cooperate in a novel NF-κB signaling pathway. J. Biol. Chem. 276:19012-19019.
44. McAllister-Lucas LM, et al. 2001. Bimp1, a MAGUK family member linking protein kinase C activation to Bcl10-mediated-NF-κB induction. J. Biol. Chem. 276:30589-30597.
45. McNamara LA, Collins KL. 2011. Hematopoietic stem/precursor cells as HIV reservoirs. Curr. Opin. HIV AIDS 6:43-48.
46. Micheau O, Tschopp J. 2003. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114:181-190.
47. Nabel G, Baltimore D. 1987. An inducible transcription factor activates expression of human immunodeficiency virus in T cells. Nature 326:711-713.
48. Nguyen VT, Kiss T, Michels AA, Bensaude O. 2001. 7SK small nuclear RNA binds to and inhibits the activity of CDK9/cyclin T complexes. Nature 414:322-325.
49. Notta F, et al. 2011. Isolation of single human hematopoietic stem cells capable of long-term multilineage engraftment. Science 333:218-221.
50. Palmer S, 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. 105:3879-3884.
51. Pereira LA, Bentley K, Peeters A, Churchill MJ, Deacon NJ. 2000. A compilation of cellular transcription factor interactions with the HIV-1 LTR promoter. Nucleic Acids Res. 28:663-668.
52. Pobezinskaya YL, et al. 2008. The function of TRADD in signaling through tumor necrosis factor receptor 1 and TRIF-dependent Toll-like receptors. Nat. Immunol. 9:1047-1054.
53. + T lymphocytes. J. Leukoc. Biol. 86:1345-1350.
54. Redd AD, Avalos A, Essex M. 2007. Infection of hematopoietic progenitor cells by HIV-1 subtype C, and its association with anemia in southern Africa. Blood 110:3143-3149.
55. Richman DD, Bozzette SA. 1994. The impact of the syncytium-inducing phenotype of human immunodeficiency virus on disease progression. J. Infect. Dis. 169:968-974.
56. Rieder P, et al. 2011. Characterization of human immunodeficiency virus type 1 (HIV-1) diversity and tropism in 145 patients with primary HIV-1 infection. Clin. Infect. Dis. 53:1271-1279.
57. Roebuck KA, Brenner DA, Kagnoff MF. 1993. Identification of c-fosresponsive elements downstream of TAR in the long terminal repeat of human immunodeficiency virus type-1. J. Clin. Invest. 92:1336-1348.
58. Roebuck KA, Gu DS, Kagnoff MF. 1996. Activating protein-1 cooperates with phorbol ester activation signals to increase HIV-1 expression. AIDS 10:819-826.
59. Ruefli-Brasse AA, French DM, Dixit VM. 2003. Regulation of NF-κBdependent lymphocyte activation and development by paracaspase. Science 302:1581-1584.
60. Ruland J, et al. 2001. Bcl10 is a positive regulator of antigen receptorinduced activation of NF-κB and neural tube closure. Cell 104:33-42.
61. Sahu GK, et al. 2009. Low-level plasma HIVs in patients on prolonged suppressive highly active antiretroviral therapy are produced mostly by cells other than CD4 T-cells. J. Med. Virol. 81:9-15.
62. + T cells to HIV-1 infection: a novel model of HIV-1 latency. Blood 110:4161-4164.
63. Salerno D, et al. 2007. Direct inhibition of CDK9 blocks HIV-1 replication without preventing T-cell activation in primary human peripheral blood lymphocytes. Gene 405:65-78.
64. Sedore SC, et al. 2007. Manipulation of P-TEFb control machinery by HIV: recruitment of P-TEFb from the large form by Tat and binding of HEXIM1 to TAR. Nucleic Acids Res. 35:4347-4358.
65. Shan L, et al. 2012. Stimulation of HIV-1-specific cytolytic T lymphocytes facilitates elimination of latent viral reservoir after virus reactivation. Immunity 36:491-501.
66. Shankarappa F, et al. 1999. Consistent viral evolutionary changes associated with the progression of human immunodeficiency virus type 1 infection. J. Virol. 73:10489-10502.
67. + bone marrow cells are infected with HIV in a subset of seropositive individuals. J. Immunol. 149:689-697.
68. Ting AT, Pimentel-Muiños FX, Seed B. 1996. RIP mediates tumor necrosis factor receptor 1 activation of NF-κB but not Fas/APO-1-initiated apoptosis. EMBO J. 15:6189-6196.
69. Trono D, et al. 2010. HIV persistence and the prospect of long-term drug-free remissions for HIV-infected individuals. Science 329:174-180.
70. + cells is due to epigenetic transcriptional silencing and P-TEFb restriction. J. Virol. 84:6425-6437.
71. Vallabhapurapu S, Karin M. 2009. Regulation and function of NF-κB transcription factors in the immune system. Annu. Rev. Immunol. 27:693-733.
72. Van Lint C, et al. 1997. Transcription factor binding sites downstream of the human immunodeficiency virus type 1 transcription start site are important for virus infectivity. J. Virol. 71:6113-6127.
73. Van Lint C, Emiliani S, Ott M, Verdin E. 1996. Transcriptional activation and chromatin remodeling of the HIV-1 promoter in response to histone acetylation. EMBO J. 15:1112-1120.
74. van't Wout AB, et al. 1994. Macrophage-tropic variants initiate human immunodeficiency virus type 1 infection after sexual, parenteral, and vertical transmission. J. Clin. Invest. 94:2060-2067.
75. Wang D, et al. 2002. A requirement for CARMA1 in TCR-induced NF-κB activation. Nat. Immunol. 3:830-835.
76. Wei P, Garber ME, Fang SM, Fischer WH, Jones KA. 1998. A novel CDK9-associated C-type cyclin interacts directly with HIV-1 Tat and mediates its high-affinity, loop-specific binding to TAR RNA. Cell 92:451-462.
77. Williams SA, et al. 2004. Prostratin antagonizes HIV latency by activating NF-κB. J. Biol. Chem. 279:42008-42017.
78. Wu C-J, Conze DB, Li T, Srinivasula SM, Ashwell JD. 2006. NEMO is a sensor of Lys 63-linked polyubiquitination and functions in NF-κB activation. Nat. Cell Biol. 8:398-406.
79. Yang H-C, 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.
80. Yang Z, Zhu Q, Luo K, Zhou Q. 2001. The 7SK small nuclear RNA inhibits the CDK9/cyclin T1 kinase to control transcription. Nature 414:317-322.
81. Yik JHN, et al. 2003. Inhibition of P-TEFb (CDK9/cyclin T) kinase and RNA polymerase II transcription by the coordinated actions of HEXIM1 and 7SK snRNA. Mol. Cell 12:971-982.
82. Ylisastigui L, Archin NM, Lehrman G, Bosch RJ, Margolis DM. 2004. Coaxing HIV-1 from resting CD4 T cells: histone deacetylase inhibition allows latent viral expression. AIDS 18:1101-1108.
83. Zhang H, et al. 2004. Novel single-cell-level phenotypic assay for residual drug susceptibility and reduced replication capacity of drug-resistant human immunodeficiency virus type 1. J. Virol. 78:1718-1729.
84. Zhang L, et al. 1999. Quantifying residual HIV-1 replication in patients receiving combination antiretroviral therapy. N. Engl. J. Med. 340:1605-1613.
85. Zhang M-Y, Sun S-C, Bell L, Miller BA. 1998. NF-κB transcription factors are involved in normal erythropoiesis. Blood 91:4136-4144.
86. Zhu T, et al. 1993. Genotypic and phenotypic characterization of HIV-1 patients with primary infection. Science 261:1179-1181.