Direct non-productive HIV-1 infection in a T-cell line is driven by cellular activation state and NFκB

Retrovirology

Volumn 11, Issue 1, 2014, Pages

  Dahabieh, Matthew S ^a   Ooms, Marcel ^b   Brumme, Chanson ^c   Taylor, Jeremy ^c   Harrigan, P Richard ^c   Simon, Viviana ^b   Sadowski, Ivan ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c BRITISH COLUMBIA CENTRE FOR EXCELLENCE IN HIV AIDS   (Canada)

Author keywords

CMV; Double label; eGFP; HIV 1; Latency; LTR; mCherry; NF B; Promoter; Silent infection

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; EMBRYO; EPIGENETICS; GENE MAPPING; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; LATENT VIRUS INFECTION; LEUKEMIA CELL LINE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROVIRUS; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TIME; VIRAL CLEARANCE; VIRUS DNA CELL DNA INTERACTION; VIRUS GENE; VIRUS LATENCY; VIRUS REACTIVATION; CELL LEVEL; GENE FUNCTION; GENE IDENTIFICATION; GENOME ANALYSIS; HUMAN IMMUNODEFICIENCY VIRUS 1; LYMPHOCYTE ACTIVATION; MOLECULAR DYNAMICS; PROTEIN DETERMINATION; VIRUS GENOME; VIRUS IDENTIFICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

HIV-1; HUMANS; JURKAT CELLS; NF-KAPPA B; T-LYMPHOCYTES; VIRUS INTEGRATION; VIRUS LATENCY; VIRUS REPLICATION;

EID: 84893688711     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-11-17     Document Type: Article

References (54)

1. Donahue DA, Wainberg MA. Cellular and molecular mechanisms involved in the establishment of HIV-1 latency. Retrovirology 2013, 10:11. 10.1186/1742-4690-10-11, 3571915, 23375003.
2. Siliciano RF, Greene WC. HIV latency. Cold Spring Harb Perspect Biol 2011, 1:a007096.
3. Karn J, Stoltzfus CM. Transcriptional and posttranscriptional regulation of HIV-1 gene expression. Cold Spring Harb Perspect Biol 2012, 2:a006916.
4. Finzi D, Hermankova M, Pierson T, Carruth LM, Buck C, Chaisson RE, Quinn TC, Chadwick K, Margolick J, Brookmeyer R, Gallant J, Markowitz M, Ho DD, Richman DD, Siliciano RF. Identification of a reservoir for HIV-1 in patients on highly active antiretroviral therapy. Science 1997, 278:1295-1300. 10.1126/science.278.5341.1295, 9360927.
5. Dahabieh MS, Ooms M, Simon V, Sadowski I. A doubly fluorescent HIV-1 reporter shows that the majority of integrated HIV-1 is latent shortly after infection. J Virol 2013, 87:4716-4727. 10.1128/JVI.03478-12, 3624398, 23408629.
6. Calvanese V, Chavez L, Laurent T, Ding S, Verdin E. Dual-color HIV reporters trace a population of latently infected cells and enable their purification. Virology 2013, 446:283-292. 10.1016/j.virol.2013.07.037, 24074592.
7. 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.
8. van der Sluis RM, van Montfort T, Pollakis G, Sanders RW, Speijer D, Berkhout B, Jeeninga RE. Dendritic cell-induced activation of latent HIV-1 provirus in actively proliferating primary T lymphocytes. PLoS Pathog 2013, 9:e1003259. 10.1371/journal.ppat.1003259, 3605277, 23555263.
9. 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.
10. 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.
11. 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.
12. 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.
13. Sherrill-Mix S, Lewinski MK, Famiglietti M, Bosque A, Malani N, Ocwieja KE, Berry CC, Looney D, Shan L, Agosto LM, Pace MJ, Siliciano RF, O'Doherty U, Guatelli J, Planelles V, Bushman FD. HIV latency and integration site placement in five cell-based models. Retrovirology 2013, 10:90. 10.1186/1742-4690-10-90, 3765678, 23953889.
14. Ciuffi A, Barr SD. Identification of HIV integration sites in infected host genomic DNA. Methods 2011, 53:39-46. 10.1016/j.ymeth.2010.04.004, 20385239.
15. Berry C, Hannenhalli S, Leipzig J, Bushman FD. Selection of target sites for mobile DNA integration in the human genome. PLoS Comput Biol 2006, 2:e157. 10.1371/journal.pcbi.0020157, 1664696, 17166054.
16. Su AI, Cooke MP, Ching KA, Hakak Y, Walker JR, Wiltshire T, Orth AP, Vega RG, Sapinoso LM, Moqrich A, Patapoutian A, Hampton GM, Schultz PG, Hogenesch JB. Large-scale analysis of the human and mouse transcriptomes. Proc Natl Acad Sci 2002, 99:4465-4470. 10.1073/pnas.012025199, 123671, 11904358.
17. Wang Z, Zang C, Rosenfeld JA, Schones DE, Barski A, Cuddapah S, Cui K, Roh T-Y, Peng W, Zhang MQ, Zhao K. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 2008, 40:897-903. 10.1038/ng.154, 2769248, 18552846.
18. Schones DE, Cui K, Cuddapah S, Roh T-Y, Barski A, Wang Z, Wei G, Zhao K. Dynamic regulation of nucleosome positioning in the human genome. Cell 2008, 132:887-898. 10.1016/j.cell.2008.02.022, 18329373.
19. Jothi R, Cuddapah S, Barski A, Cui K, Zhao K. Genome-wide identification of in vivo protein-DNA binding sites from ChIP-Seq data. Nucleic Acids Res 2008, 36:5221-5231. 10.1093/nar/gkn488, 2532738, 18684996.
20. Robertson AG, Bilenky M, Tam A, Zhao Y, Zeng T, Thiessen N, Cezard T, Fejes AP, Wederell ED, Cullum R, Euskirchen G, Krzywinski M, Birol I, Snyder M, Hoodless PA, Hirst M, Marra MA, Jones SJM. Genome-wide relationship between histone H3 lysine 4 mono- and tri-methylation and transcription factor binding. Genome Res 2008, 18:1906-1917. 10.1101/gr.078519.108, 2593584, 18787082.
21. Wang Z, Zang C, Cui K, Schones DE, Barski A, Peng W, Zhao K. Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 2009, 138:1019-1031. 10.1016/j.cell.2009.06.049, 2750862, 19698979.
22. Cui K, Zang C, Roh T-Y, Schones DE, Childs RW, Peng W, Zhao K. Chromatin signatures in multipotent human hematopoietic stem cells indicatethe fate of bivalent genes during differentiation. Stem Cell 2009, 4:80-93.
23. Meylan S, Groner AC, Ambrosini G, Malani N, Quenneville S, Zangger N, Kapopoulou A, Kauzlaric A, Rougemont J, Ciuffi A, Bushman FD, Bucher P, Trono D. A gene-rich, transcriptionally active environment and the pre-deposition of repressive marks are predictive of susceptibility to KRAB/KAP1- mediated silencing. BMC Genomics 2011, 12:378. 10.1186/1471-2164-12-378, 3199781, 21791101.
24. Koh Y, Wu X, Ferris AL, Matreyek KA, Smith SJ, Lee K, Kewalramani VN, Hughes SH, Engelman A. Differential effects of human immunodeficiency virus type 1 capsid and cellular factors nucleoporin 153 and LEDGF/p75 on the efficiency and specificity of viral DNA integration. J Virol 2013, 87:648-658. 10.1128/JVI.01148-12, 3536403, 23097450.
25. Schaller T, Ocwieja KE, Rasaiyaah J, Price AJ, Brady TL, Roth SL, SEP HE, Fletcher AJ, Lee K, Kewalramani VN, Noursadeghi M, Jenner RG, James LC, Bushman FD, Towers G. HIV-1 capsid-cyclophilin interactions determine nuclear import pathway. Integration targeting and replication efficiency. PLoS Pathog 2011, 7:e1002439. 10.1371/journal.ppat.1002439, 3234246, 22174692.
26. Ocwieja KE, Brady TL, Ronen K, Huegel A, Roth SL, Schaller T, James LC, Towers GJ, Young JAT, Chanda SK, Konig R, Malani N, Berry CC, Bushman FD. HIV integration targeting: a pathway involving Transportin-3 and the nuclear pore protein RanBP2. PLoS Pathog 2011, 7:e1001313. 10.1371/journal.ppat.1001313, 3053352, 21423673.
27. Han Y, Lin YB, An W, Xu J, Yang H-CC, 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.
28. 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.
29. Shan L, Yang HC, 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.
30. Chan JKL, Greene WC. NF-κB/Rel: agonist and antagonist roles in HIV-1 latency. Curr Opin HIV AIDS 2011, 6:12-18. 10.1097/COH.0b013e32834124fd, 3493179, 21242888.
31. Lopez-Cabrera M, Munoz E, MV BZ, Ursa MA, Santis AG, Sanchez-Madrid F. Transcriptional regulation of the gene encoding the human C-type lectin leukocyte receptor AIM/CD69 and functional characterization of its tumor necrosis factor-alpha-responsive elements. J Biol Chem 1995, 270:21545-21551. 10.1074/jbc.270.37.21545, 7665567.
32. Archin NM, Espeseth A, Parker D, Cheema M, Hazuda D, Margolis DM. Expression of latent HIV induced by the potent HDAC inhibitor suberoylanilide hydroxamic acid. AIDS Res Hum Retrovir 2009, 25:207-212. 10.1089/aid.2008.0191, 2853863, 19239360.
33. Archin NM, Liberty AL, Kashuba AD, Choudhary SK, Kuruc JD, Crooks AM, Parker DC, Anderson EM, Kearney MF, Strain MC, Richman DD, Hudgens MG, Bosch RJ, Coffin JM, Eron JJ, Hazuda DJ, Margolis DM. Administration of vorinostat disrupts HIV-1 latency in patients on antiretroviral therapy. Nature 2012, 487:482-485. 10.1038/nature11286, 3704185, 22837004.
34. Van Lint C, Emiliani S, Verdin E. The expression of a small fraction of cellular genes is changed in response to histone hyperacetylation. Gene Expr 1996, 5:245-253.
35. Chen G, Goeddel DV. TNF-R1 signaling: a beautiful pathway. Science 2002, 296:1634-1635. 10.1126/science.1071924, 12040173.
36. Kwon H, Pelletier N, DeLuca C, Genin P, Cisternas S, Lin R, Wainberg MA, Hiscott J. Inducible expression of IκBα repressor mutants interferes with NF-κB activity and HIV-1 replication in Jurkat T cells. J Biol Chem 1998, 273:7431-7440. 10.1074/jbc.273.13.7431, 9516441.
37. Jordan A, Defechereux P, Verdin E. The site of HIV-1 integration in the human genome determines basal transcriptional activity and response to Tat transactivation. EMBO J 2001, 20:1726-1738. 10.1093/emboj/20.7.1726, 145503, 11285236.
38. 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.
39. Wang GP, Levine BL, Binder GK, Berry CC, Malani N, McGarrity G, Tebas P, June CH, Bushman FD. Analysis of lentiviral vector integration in HIV + study subjects receiving autologous infusions of gene modified CD4+ T cells. Mol Ther 2009, 17:844-850. 10.1038/mt.2009.16, 2835137, 19259065.
40. Raj A, van Oudenaarden A. Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 2008, 135:216-226. 10.1016/j.cell.2008.09.050, 3118044, 18957198.
41. Raser JM, O'Shea EK. Noise in gene expression: origins, consequences, and control. Science 2005, 309:2010-2013. 10.1126/science.1105891, 1360161, 16179466.
42. 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.
43. Nelson DE, Ihekwaba AEC, Elliott M, Johnson JR, Gibney CA, Foreman BE, Nelson G, See V, Horton CA, Spiller DG, Edwards SW, McDowell HP, Unitt JF, Sullivan E, Grimley R, Benson N, Broomhead D, Kell DB, White MRH. Oscillations in NF-κB signaling control the dynamics of gene expression. Science 2004, 306:704-708. 10.1126/science.1099962, 15499023.
44. Coiras M, Lopez-Huertas MR, Rullas JIN, Mittelbrunn M, Alcami J, Lopez-Huertas MIAR, Rullas JIN, Mittelbrunn M, Alcami JE. Basal shuttle of NFκB/IκBα alpha in resting T lymphocytes regulates HIV-1 LTR dependent expression. Retrovirology 2007, 4:56. 10.1186/1742-4690-4-56, 1988826, 17686171.
45. Arenzana-Seisdedos F, Turpin P, Rodriguez M, Thomas D, Hay RT, Virelizier JL, Dargemont C. Nuclear localization of IκBα promotes active transport of NF-κB from the nucleus to the cytoplasm. J Cell Sci 1997, 3:369-378.
46. 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 2013, 87:2264-2277. 10.1128/JVI.01594-12, 3571467, 23236059.
47. Wolschendorf F, Bosque A, Shishido T, Duverger A, Jones J, Planelles V, Kutsch O. Kinase control prevents HIV-1 reactivation in spite of high levels of induced NF-κB activity. J Virol 2012, 86:4548-4558. 10.1128/JVI.06726-11, 3318643, 22345467.
48. Duverger A, Wolschendorf F, Anderson JC, Wagner F, Bosque A, Shishido T, Jones J, Planelles V, Willey C, Cron RQ, Kutsch O. Kinase control of Latent HIV-1 Infection: PIM-1 Kinase as a Major Contributor to HIV-1 Reactivation. J Virol 2014, 88:364-376. 10.1128/JVI.02682-13, 24155393.
49. Weiss A, Wiskocil RL, Stobo JD. The role of T3 surface molecules in the activation of human T cells: a two-stimulus requirement for IL 2 production reflects events occurring at a pre-translational level. J Immunol 1984, 133:123-128.
50. Chang LJ, Urlacher V, Iwakuma T, Cui Y, Zucali J. Efficacy and safety analyses of a recombinant human immunodeficiency virus type 1 derived vector system. Gene Ther 1999, 6:715-728. 10.1038/sj.gt.3300895, 10505094.
51. Bernhard W, Barreto K, Saunders A, Dahabieh MS, Johnson P, Sadowski I. The Suv39H1 methyltransferase inhibitor chaetocin causes induction of integrated HIV-1 without producing a T cell response. FEBS Lett 2011, 585:3549-3554. 10.1016/j.febslet.2011.10.018, 22020221.
52. Grupillo M, Lakomy R, Geng X, Styche A, Rudert WA, Trucco M, Fan Y. An improved intracellular staining protocol for efficient detection of nuclear proteins in YFP-expressing cells. Biotechniques 2011, 51:417-420.
53. Marks PA, Breslow R. Dimethyl sulfoxide to vorinostat: development of this histone deacetylase inhibitor as an anticancer drug. Nat Biotechnol 2007, 25:84-90. 10.1038/nbt1272, 17211407.
54. Krzywinski MI, Schein JE, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA. Circos: An information aesthetic for comparative genomics. Genome Res 2009, 19:1639-1645. 10.1101/gr.092759.109, 2752132, 19541911.