HIV-1 integrates into resting CD4+ T cells even at low inoculums as demonstrated with an improved assay for HIV-1 integration

Virology

Volumn 368, Issue 1, 2007, Pages 60-72

  Agosto, Luis M ^a   Yu, Jianqing J ^c   Dai, Jihong ^c   Kaletsky, Rachel ^a   Monie, Daphne ^b   O'Doherty, Una ^c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Laboratory Medicine   (United States)

Author keywords

HIV integration; HIV latency; HIV reservoirs; Resting CD4+ T cells; Restriction factors

Indexed keywords

ALU SEQUENCE; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENOME; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; INOCULATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; VIRUS DNA CELL DNA INTERACTION; VIRUS ISOLATION; VIRUS LATENCY;

CD4-POSITIVE T-LYMPHOCYTES; CELL LINE; HIV-1; HUMANS; VIRUS INTEGRATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 35348929372     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2007.06.001     Document Type: Article

References (68)

1. Adachi A., Gendelman H.E., Koenig S., Folks T., Willey R., Rabson A., and Martin M.A. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59 2 (1986) 284-291
2. Besnier C., Takeuchi Y., and Towers G. Restriction of lentivirus in monkeys. Proc. Natl. Acad. Sci. U.S.A. 99 18 (2002) 11920-11925
3. Best S., Le Tissier P., Towers G., and Stoye J.P. Positional cloning of the mouse retrovirus restriction gene Fv1. Nature 382 (1996) 826-829
4. Blankson J.N., Persaud D., and Siliciano R.F. The challenge of viral reservoirs in HIV-1 infection. Annu. Rev. Med. 53 (2002) 557-593
5. Blumenthal R., Bali-Puri A., Walter A., Covell D., and Eidelman O. pH-dependent fusion of vesicular stomatitis virus with Vero cells. Measurement by dequenching of octadecyl rhodamine fluorescence. J. Biol. Chem. 262 28 (1987) 13614-13619
6. Briant L., Coudronniere N., Robert-Hebmann V., Benkirane M., and Devaux C. Binding of HIV-1 virions or gp120-anti-gp120 immune complexes to HIV-1-infected quiescent peripheral blood mononuclear cells reveals latent infection. J. Immunol. 156 10 (1996) 3994-4004
7. Briant L., Reynes J., Coudronniere N., Benezech J.P., and Devaux C. HIV-1 reactivation in resting peripheral blood mononuclear cells of infected adults upon in vitro CD4 cross-linking by ligands of the CDR2-loop in extracellular domain 1. J. Acquired Immune Defic. Syndr. 21 1 (1999) 9-19
8. Brussel A., and Sonigo P. Analysis of early human immunodeficiency virus type 1 DNA synthesis by use of a new sensitive assay for quantifying integrated provirus. J. Virol. 77 18 (2003) 10119-10124
9. Brussel A., Delelis O., and Sonigo P. Alu-LTR real-time nested PCR assay for quantifying integrated HIV-1 DNA. Methods Mol. Biol. 304 (2005) 139-154
10. Bukrinsky M.I., Stanwick T.L., Dempsey M.P., and Stevenson M. Quiescent T lymphocytes as an inducible virus reservoir in HIV-1 infection. Science 254 (1991) 423-427
11. Bukrinsky M.I., Sharova N., Dempsey M.P., Stanwick T.L., Bukrinskaya A.G., Haggerty S., and Stevenson M. Active nuclear import of human immunodeficiency virus type 1 preintegration complexes. Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 6580-6584
12. Butler S.L., Hansen M.S.T., and Bushman F.D. A quantitative assay for HIV DNA integration in vivo. Nat. Med. 7 (2001) 631-634
13. Chiu Y.L., Soros V.B., Kreisberg J.F., Stopak K., Yonemoto W., and Greene W.C. Cellular APOBEC3G restricts HIV-1 infection in resting CD4+ T cells. Nature 435 7038 (2005) 108-114
14. Chun T.W., Finzi D., Margolick J., Chadwick K., Schwartz D., and Siliciano R.F. In vivo fate of HIV-1-infected T cells: quantitative analysis of the transition to stable latency. Nat. Med. 1 12 (1995) 1284-1290
15. Chun T.W., Carruth L., Finzi D., Shen X., DiGiuseppe J.A., Taylor H., Hermankova M., Chadwick K., Margolick J., Quinn T.C., Kuo Y.H., Brookmeyer R., Zeiger M.A., Barditch-Crovo P., and Siliciano R.F. Quantification of latent tissue reservoirs and total body viral load in HIV-1 infection. Nature 387 (1997) 183-188
16. Chun T.W., Stuyver L., Mizell S.B., Ehler L.A., Mican J.A., Baseler M., Lloyd A.L., Nowak M.A., and Fauci A.S. Presence of an inducible HIV-1 latent reservoir during highly active antiretroviral therapy. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 13193-13197
17. De Rosa S.C., Herzenberg L.A., and Roederer M. 11-color, 13-parameter flow cytometry: identification of human naive T cells by phenotype, function, and T-cell receptor diversity. Nat. Med. 7 2 (2001) 245-248
18. Ducrey-Rundquist O., Guyader M., and Trono D. Modalities of interleukin-7-induced human immunodeficiency virus permissiveness in quiescent T lymphocytes. J. Virol. 76 18 (2002) 9103-9111
19. Eckstein D.A., Penn M.L., Korin Y.D., Scripture-Adams D.D., Zack J.A., Kreisberg J.F., Roederer M., Sherman M.P., Chin P.S., and Goldsmith M.A. HIV-1 actively replicates in naive CD4(+) T cells residing within human lymphoid tissues. Immunity 15 4 (2001) 671-682
20. Emi N., Friedmann T., and Yee J.K. Pseudotype formation of murine leukemia virus with the G protein of vesicular stomatitis virus. J. Virol. 65 3 (1991) 1202-1207
21. Fouchier R.A.M., Meyer B.E., Simon J.H.M., Fischer U., and Malim M.H. HIV-1 infection of non-dividing cells: evidence that the amino-terminal basic region of the viral matrix protein is important for Gag processing but not for post-entry nuclear import. Eur. Mol. Biol. Organ. J. 16 (1997) 4531-4539
22. Han Y., Lassen K., Monie D., Sedaghat A.R., Shimoji S., Liu X., Pierson T.C., Margolick J.B., Siliciano R.F., and Siliciano J.D. Resting CD4+ T cells from HIV-1 infected individuals carry integrated HIV-1 genomes within actively transcribed host genes. J. Virol. 78 12 (2004) 6122-6133
23. Han Y., Wind-Rotolo M., Yang H.C., Siliciano J.D., and Siliciano R.F. Experimental approaches to the study of HIV-1 latency. Nat. Rev., Microbiol. 5 2 (2007) 95-106
24. Keckesova Z., Ylinen L.M., and Towers G.J. The human and African green monkey TRIM5alpha genes encode Ref1 and Lv1 retroviral restriction factor activities. Proc. Natl. Acad. Sci. U.S.A. 101 29 (2004) 10780-10785
25. Kinter A., Moorthy A., Jackson R., and Fauci A.S. Productive HIV infection of resting CD4+ T cells: role of lymphoid tissue microenvironment and effect of immunomodulating agents. AIDS Res. Hum. Retroviruses 19 10 (2003) 847-856
26. Kinter A.L., Umscheid C.A., Arthos J., Cicala C., Lin Y., Jackson R., Donoghue E., Ehler L., Adelsberger J., Rabin R.L., and Fauci A.S. HIV envelope induces virus expression from resting CD4+ T cells isolated from HIV-infected individuals in the absence of markers of cellular activation or apoptosis. J. Immunol. 170 5 (2003) 2449-2455
27. Korin Y.D., and Zack J.A. Progression to the G1b phase of the cell cycle is required for completion of human immunodeficiency virus type 1 reverse transcription in T cells. J. Virol. 72 (1998) 3161-3168
28. Kornfeld H., Cruikshank W.W., Pyle S.W., Berman J.S., and Center D.M. Lymphocyte activation by HIV-1 envelope glycoprotein. Nature 335 6189 (1988) 445-448
29. Kumar R., Vandegraaff N., Mundy L., Burrell C.J., and Li P. Evaluation of PCR-based methods for the quantitation of integrated HIV-1 DNA. J. Virol. Methods 105 2 (2002) 233-246
30. Lassen K., Han Y., Zhou Y., Siliciano J., and Siliciano R.F. The multifactorial nature of HIV-1 latency. Trends Mol. Med. 10 11 (2004) 525-531
31. Lehrman G., Hogue I.B., Palmer S., Jennings C., Spina C.A., Wiegand A., Landay A.L., Coombs R.W., Richman D.D., Mellors J.W., Coffin J.M., Bosch R.J., and Margolis D.M. Depletion of latent HIV-1 infection in vivo: a proof-of-concept study. Lancet 366 9485 (2005) 549-555
32. Li Q., Duan L., Estes J.D., Ma Z.M., Rourke T., Wang Y., Reilly C., Carlis J., Miller C.J., and Haase A.T. Peak SIV replication in resting memory CD4+ T cells depletes gut lamina propria CD4+ T cells. Nature 434 7037 (2005) 1148-1152
33. Luban J. Cyclophilin A, TRIM5, and resistance to human immunodeficiency virus type 1 infection. J. Virol. 81 3 (2007) 1054-1061
34. Nishimura Y., Brown C.R., Mattapallil J.J., Igarashi T., Buckler-White A., Lafont B.A., Hirsch V.M., Roederer M., and Martin M.A. Resting naive CD4+ T cells are massively infected and eliminated by X4-tropic simian-human immunodeficiency viruses in macaques. Proc. Natl. Acad. Sci. U.S.A. 102 22 (2005) 8000-8005
35. O'Doherty U., Swiggard W.J., and Malim M.H. Human immunodeficiency virus type 1 spinoculation enhances infection through virus binding. J. Virol. 74 21 (2000) 10074-10080
36. O'Doherty U., Swiggard W.J., Jeyakumar D., McGain D., and Malim M.H. A sensitive, quantitative, assay for Human Immunodeficiency Virus type 1 integration. J. Virol. 76 21 (2002) 10,942-10,950
37. Ostrowski M.A., Chun T.-W., Justement S.J., Motola I., Spinelli M.A., Adelsberger J., Ehler L.A., Mizell S.B., Hallahan C.W., and Fauci A.S. Both memory and CD45RA(+)/CD62L(+) naive CD4(+) T cells are infected in human immunodeficiency type 1-infected individuals. J. Virol. 73 (1999) 6430-6435
38. Oswald-Richter K., Grill S.M., Leelawong M., and Unutmaz D. HIV infection of primary human T cells is determined by tunable thresholds of T cell activation. Eur. J. Immunol. 34 6 (2004) 1705-1714
39. Pierson T., McArthur J., and Siliciano R.F. Reservoirs for HIV-1: mechanisms for viral persistence in the presence of antiviral immune responses and antiretroviral therapy. Annu. Rev. Immunol. 18 (2000) 665-708
40. Pierson T.C., Zhou Y., Kieffer T.L., Ruff C.T., Buck C., and Siliciano R.F. Molecular characterization of preintegration latency in human immunodeficiency virus type 1 infection. J. Virol. 76 17 (2002) 8518-8531
41. Schacker T.W., Little S., Connick E., Gebhard K., Zhang Z., Krieger J., Pryor J., Havlir D., Wong J., Schooley R.T., Richman D., Corey L., and Haase A.T. Productive infection of T cells in lymphoid tissue during primary and early HIV infection. J. Infect. Dis. 183 (2001) 555-562
42. Schroder A.R., Shinn P., Chen H., Berry C., Ecker J.R., and Bushman F. HIV-1 integration in the human genome favors active genes and local hotspots. Cell 110 4 (2002) 521-529
43. Sonza S., Maerz A., Deacon N., Meanger J., Mills J., and Crowe S. Human immunodeficiency virus type 1 replication is blocked prior to reverse transcription and integration in freshly isolated peripheral blood monocytes. J. Virol. 70 (1996) 3863-3869
44. Spina C.A., Guatelli J.C., and Richman D.D. Establishment of a stable, inducible form of human immunodeficiency virus type 1 DNA in quiescent CD4 lymphocytes in vitro. J. Virol. 69 (1995) 2877-2988
45. Stefanova I., Dorfman J.R., and Germain R.N. Self-recognition promotes the foreign antigen sensitivity of naive T lymphocytes. Nature 420 6914 (2002) 429-434
46. Stevenson M. HIV-1 pathogenesis. Nat. Med. 9 7 (2003) 853-860
47. Stevenson M., Stanwick T.L., Dempsey M.P., and Lamonica C.A. HIV-1 replication is controlled at the level of T cell activation and proviral integration. Eur. Mol. Biol. Organ. J. 9 (1990) 1551-1560
48. Stremlau M., Owens C.M., Perron M.J., Kiessling M., Autissier P., and Sodroski J. The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 427 6977 (2004) 848-853
49. Sun Y., and Clark E.A. Expression of the c-myc proto-oncogene is essential for HIV-1 infection in activated T cells. J. Exp. Med. 9 (1999) 1391-1397
50. Suzuki Y., Misawa N., Sato C., Ebina H., Masuda T., Yamamoto N., and Koyanagi Y. Quantitative analysis of human immunodeficiency virus type 1 DNA dynamics by real-time PCR: integration efficiency in stimulated and unstimulated peripheral blood mononuclear cells. Virus Genes 27 2 (2003) 177-188
51. Swiggard W.J., O'Doherty U., McGain D., Jeyakumar D., and Malim M.H. Long HIV Type 1 reverse transcripts can accumulate stably within resting CD4+ T cells while short ones are degraded. AIDS Res. Hum. Retroviruses 20 3 (2004) 285-295
52. Swiggard W.J., Baytop C., Yu J.J., Dai J., Li C., Schretzenmair R., Theodosopoulos T., and 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. 79 22 (2005) 14179-14188
53. Swingler S., Brichacek B., Jacque J.M., Ulich C., Zhou J., and Stevenson M. HIV-1 Nef intersects the macrophage CD40L signalling pathway to promote resting-cell infection. Nature 424 6945 (2003) 213-219
54. Towers G., Bock M., Martin S., Takeuchi Y., Stoye J.P., and Danos O. A conserved mechanism of retrovirus restriction in mammals. Proc. Natl. Acad. Sci. U.S.A. 97 22 (2000) 12295-12299
55. Towers G., Collins M., and Takeuchi Y. Abrogation of Ref1 retrovirus restriction in human cells. J. Virol. 76 5 (2002) 2548-2550
56. Towers G.J., Hatziioannou T., Cowan S., Goff S.P., Luban J., and Bieniasz P.D. Cyclophilin A modulates the sensitivity of HIV-1 to host restriction factors. Nat. Med. 9 9 (2003) 1138-1143
57. Unutmaz D., KewalRamani V.N., Marmon S., and Littman D.R. Cytokine signals are sufficient for HIV-1 infection of resting human T lymphocytes. J. Exp. Med. 189 (1999) 1735-1746
58. Vandegraaff N., Kumar R., Burrell C.J., and Li P. Kinetics of Human Immunodeficiency Virus type 1 DNA integration in acutely infected cells as determined using a novel assay for detection of integrated HIV DNA. J. Virol. 75 (2001) 11253-11260
59. Vatakis D.N., Bristol G., Wilkinson T.A., Chow S.A., and Zack J.A. Immediate activation fails to rescue efficient human immunodeficiency virus replication in quiescent CD4+ T cells. J. Virol. 81 7 (2007) 3574-3582
60. Verhoeyen E., Dardalhon V., Ducrey-Rundquist O., Trono D., Taylor N., and Cosset F.L. IL-7 surface-engineered lentiviral vectors promote survival and efficient gene transfer in resting primary T lymphocytes. Blood 101 6 (2003) 2167-2174
61. Vogt V.M., and Simon M.N. Mass determination of rous sarcoma virus virions by scanning transmission electron microscopy. J. Virol. 73 (1999) 7050-7055
62. Yamamoto N., Tanaka C., Wu Y., Chang M.O., Inagaki Y., Saito Y., Naito T., Ogasawara H., Sekigawa I., and Hayashida Y. Analysis of human immunodeficiency virus type 1 integration by using a specific, sensitive and quantitative assay based on real-time polymerase chain reaction. Virus Genes 32 1 (2006) 105-113
63. Yamashita M., and Emerman M. Retroviral infection of non-dividing cells: old and new perspectives. Virology 344 1 (2006) 88-93
64. Zack J.A., Arrigo S.J., Weitsman S.R., Go A.S., Haislip A., and Chen I.S.Y. HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell 61 (1990) 213-222
65. Zack J.A., Haislip A.M., Krogstad P., and Chen I.S.Y. Incompletely reverse-transcribed human immunodeficiency virus type 1 genomes in quiescent cells can function as intermediates in the retroviral life cycle. J. Virol. 66 (1992) 1717-1725
66. Zhang Z.-Q., Schuler T., Zupancic M., Wietgrefe S., Staskus K.A., Reimann K.A., Reinhart T.A., Rogan M., Cavert W., Miller C.J., Veazey R.S., Notermans D., Little S., Danner S.A., Richman D.D., Havlir D., Wong J., Jordan H.L., Schacker T.W., Racz P., Tenner-Racz K., Letvin N.L., Wolinsky S., and Haase A.T. Sexual transmission and propagation of SIV and HIV in resting and activated CD4+ T cells. Science 286 (1999) 1353-1357
67. Zhang Z.Q., Wietgrefe S.W., Li Q., Shore M.D., Duan L., Reilly C., Lifson J.D., and Haase A.T. Roles of substrate availability and infection of resting and activated CD4+ T cells in transmission and acute simian immunodeficiency virus infection. Proc. Natl. Acad. Sci. U.S.A. 101 15 (2004) 5640-5645
68. Zhou Y., Zhang H., Siliciano J.D., and Siliciano R.F. Kinetics of human immunodeficiency virus type 1 decay following entry into resting CD4+ T cells. J. Virol. 79 4 (2005) 2199-2210