Preferential replication of HIV-1 in the CD45RO memory cell subset of primary CD4 lymphocytes in vitro

Journal of Clinical Investigation

Volumn 99, Issue 7, 1997, Pages 1774-1785

  Spina, Celsa A ^a,b,c   Prince, Harry E ^d,e   Richman, Douglas D ^a,b,c  

^a VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d AMERICAN RED CROSS BLOOD SERVICES   (United States)

^e Microbiology Reference Laboratory   (United States)

Author keywords

activation; differentiation; pathogenesis; T cell immunity; vital growth

Indexed keywords

CD4 ANTIGEN;

ARTICLE; CELL DIFFERENTIATION; CELL MEDIATED CYTOTOXICITY; CROSS LINKING; DNA BINDING; GENE DELETION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; LYMPHOCYTE ACTIVATION; MEMORY CELL; PRIORITY JOURNAL; REGULATOR GENE; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION; VIROGENESIS; VIRUS GENE; VIRUS REPLICATION;

EID: 0030968495     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119342     Document Type: Article

References (73)

1. Fauci, A.S. 1991. Immunopathogenic mechanisms in human immunodeficiency virus (HIV) infection. Ann. Intern. Med. 114:678-693.
2. Oyaizu, N., T.W. McCloskey, M. Coronesi, N. Chirmule, V.S. Kalyanaraman, and S. Pahwa. 1993. Accelerated apoptosis in peripheral blood mononuclear cells (PBMCs) from human immunodeficiency virus type-1 infected patients and in CD4 cross-linked PBMCs from normal individuals. Blood. 82: 3392-3400.
3. Dalgleish, A.G. 1993. Immunobiological aspects of HIV treatment. Curr. Opin. Immunol. 5:608-614.
4. Mosmann, T.R. 1994. Cytokine patterns during the progression to AIDS. Science (Wash. DC). 265:193-194.
5. Stevenson, M., T.L. Stanwick, M.P. Dempsey, and C.A. Lamonica. 1990. HIV-1 replication is controlled at the level of T cell activation and proviral integration. EMBO (Eur. Mol. Biol. Organ.) J. 9:1551-1560.
6. Zack, J.A., A. Haislip, P. Krongstad, and I.S.Y. Chen. 1992. Incompletely reverse-transcribed human immunodeficiency virus type 1 genomes in quiescent cells can function as intermediates in the retroviral life cycle. J. Virol. 66: 1717-1725.
7. Bukrinsky, M.I., S. Haggerty, P. Dempsey, N. Sharova, A. Adzhubel, L. Spitz, P. Lewis, D. Goldfarb, M. Emerman, and M. Stevenson. 1993. A nuclear localization signal within HIV-1 matrix protein that governs infection of non-dividing cells. Nature (Lond.). 365:666-669.
8. von Schwedler, U., R.S. Kornbluth, and D. Trono. 1994. The nuclear localization signal of the matrix protein of HIV-1 allows the establishment of infection in macrophages and quiescent T lymphocytes. Prof. Natl. Acad. Sci. USA. 91:6992-6996.
9. Feinberg, M.B., R.F. Jarrett, A. Aldavini, R.C. Gallo, and F. Wong-Staal. 1986. HTLV-III expression and production involve complex regulation at the levels of splicing and translation of viral mRNA. Cell. 46:807-817.
10. Kim, S.-Y., R. Byrn, J. Groopman, and D. Baltimore. 1989. Temporal aspects of DNA and RNA synthesis during human immunodeficiency virus infection: evidence for differential gene expression. J. Virol. 63:3708-3713.
11. Pavlakis, G.N., and B.K. Felber. 1990. Regulation of expression of human immunodeficiency virus. New Biol. 2:20-31.
12. Feinberg, M.B., and W.C. Greene. 1992. Molecular insights into human immunodeficiency virus type 1 pathogenesis. Curr. Opin. Immunol. 4:466-474.
13. Cullen, B.R. 1994. The role of Nef in the replication cycle of the human and simian immunodeficiency virus. Virology. 205:1-6.
14. Tong-Starksen, S.E., P.A. Luciw, and B.M. Peterlin. 1989. Signaling through T lymphocyte surface proteins, TCR/CD3 and CD28, activates the HIV-1 long terminal repeat. J. Immunol. 142:702-707.
15. Schmidt, A., L. Henninghausen, and U. Siebenlist. 1990. Inducible nuclear factor binding to the kB elements of the human immunodeficiency virus enhancer in T cells can be blocked by cyclosporin A in a signal-dependent manner. J. Virol. 64:4037-4041.
16. Dasgupta, P., P. Saikmar, C.D. Reddy, and E.P. Reddy. 1990. Myb protein binds to human immunodeficiency virus 1 long terminal repeat (LTR) sequences and transactivates LTR-mediated transcription. Proc. Natl. Acad. Sci. USA. 87:8090-8094.
17. McDougal, J.S., A. Mawle, S.P. Cort, J.K.A. Nicholson, G.D. Cross, I.A. Scheppler-Campbell, D.R. Hicks, and J.M. Sligh. 1985. Cellular tropism of the human retrovirus HTLV-III/LAV. Role of T cell activation and expression of the T4 antigen. J. Immunol. 135:3151-3162.
18. Zagury, D., J. Bernard, R. Leonard, R. Cheynier, M. Feldman, P.S. Satin, and R.C. Gallo. 1986. Long-term cultures of HTLV-III infected T cells: a model of cytopathology of T-cell depletion in AIDS. Science (Wash. DC). 231: 850-853.
19. Margolick, J.B., S.J. Volkman, T.M. Folks, and A.S. Fauci. 1987. Amplification of HTLV-III/LAV infection by antigen-induced activation of T cells and direct suppression by virus of lymphocyte blastogenic responses. J. Immunol. 138:1719-1723.
20. Smith, S.H., M.H. Brown, D. Rowe, R.E. Callard, and P.C.L. Beverley. 1986. Functional subsets of human helper-inducer cells defined by a new monoclonal antibody, UCHL-1. Immunology. 58:63-70.
21. + helper inducer T lymphocytes defined by anti-CD45R antibodies derive sequentially from a differentiation pathway that is regulated by activation-dependent post-thymic differentiation. J. Immunol. 141:1464-1470.
22. Akbar, A.N., L. Terry, A. Timms, P.C.L. Beverley, and G. Janossy. 1988. Loss of CD45R and gain of UCHL1 reactivity is a feature of primed T cells. J. Immunol. 140:2171-2178.
23. Merkenschlager, M., L. Terry, R. Edwards, and P.C.L. Beverley. 1988. Limiting dilution analysis of proliferative responses in human lymphocyte populations defined by the monoclonal anti-body UCHL1: implications for differential CD45 expression in T-cell memory formation. Eur. J. Immunol. 18:1653-1661.
24. Sanders, M.E., M.W. Makgoba, S.O. Sharrow, D. Stephany, T.A. Springer, H.A. Young, and S. Shaw. 1988. Human memory T lymphocytes express increased levels of three cell adhesion molecules (LFA-3, CD2, and LFA-1) and three other molecules (UCHLI, CDw29, and PGP-1) and have enhanced IFN-gamma production. J. Immunol. 140:1401-1407.
25. + T cell subsets. Cell. Immunol. 141:10-20.
26. Michie, C.A., A. McLean, C. Alcock, and P.C.L. Beverley. 1992. Lifespan of human lymphocyte subsets defined by CD45R isoforms. Nature (Lond.). 360:264-265.
27. Tough, D.F., and J. Sprent. 1994. Turnover of naive- and memory-phenotype T cells. J. Exp. Med. 179:1127-1135.
28. Miedema, F. 1992. Immunological abnormalities in the natural history of HIV infection: mechanisms and clinical relevance. Immunodeficiency Rev. 3: 173-193.
29. + cells are not selectively decreased in chronic HIV disease. J. Acquired Immune Defic. Syndr. 7:665-675.
30. + T cell function in the course of human immunodeficiency virus infection. Gradual decline of both naive and memory alloreactive T cells. J. Clin. Invest. 94:1947-1952.
31. + cells is associated with previous severe primary HIV infection. J. Acquired Immune Defic. Syndr. Hum. Retrovirol. 10:107-114.
32. Schellekens, P.T., M.T. Roos, F. De Wolf, J.M. Lange, and F. Miedema. 1990. Low T-cell responsiveness to activation via CD3/TCR is a prognostic marker for AIDS in HIV-infected men. J. Clin. Immunol. 10:121-127.
33. Cayota, A., F. Vuillier, D. Scott-Algara, V. Feuillie, and G. Dighiero. 1992. Impaired proliferative capacity and abnormal cytokine profile of naive and memory CD4 T cells from HIV-seropositive patients. Clin. Exp. Immunol. 88:478-483.
34. + cells of the CD4 and CD8 lineages. AIDS (Phlia.). 7:613-624.
35. + individuals to various mitogenic stimuli in vitro. Clin. Exp. Immunol. 97:266-272.
36. + memory T cells by human immunodeficiency virus type 1: evidence for a role in the selective T-cell functional defects observed in infected individuals. Immunology. 87:6058-6062.
37. Spina, C.A., T.J. Kwoh, M.Y. Chowers, J.C. Guatelli, and D.D. Richman. 1994. The importance of nef in the induction of human immunodeficiency virus type 1 replication from primary quiescent CD4 lymphocytes. J. Exp. Med. 179:115-123.
38. Adachi, A., H.E. Gendelman, S. Koenig, T. Folks, R. Willey, A. Rabson, and M.A. Martin. 1986. Production of acquired immunodeficiency syndrome-associated retrovirus in human and non-human cells transfected with an infectious molecular clone. J. Virol. 59:284-291.
39. Folks, T.M., S. Benn, A. Rabson, T. Theodore, M.D. Hoggan, M. Martin, M. Lightfoote, and K. Sell. 1985. Characterization of a continuous T-cell line susceptible to the cytopathic effects of the AIDS retrovirus. Proc. Natl. Acad. Sci. USA. 82:4539-4543.
40. Feigner, P.L., T.R. Gader, M. Holm, R. Roman, H.W. Chan, M. Wenz, J.P. Northrop, G.M. Ringold, and M. Danielson. 1987. Lipofectin: a highly efficient, lipid-mediated DNA-transfection procedure. Proc. Natl. Acad. Sci. USA. 84:7413-7417.
41. Haertle, T., C.J. Carrera, J.S. McDougal, L.C. Sowers, D.D. Richman, and D.A. Carson. 1988. Metabolism and anti-HIV activity of 2′-halo-2′,3′-dideoxyadenosine derivatives. J. Biol. Chem. 263:5870-5875.
42. Spina, C.A., J.C. Guatelli, and D.D. Richman. 1995. Establishment of a stable, inducible form of human immunodeficiency virus type 1 DNA in quiescent CD4 lymphocytes in vitro. J. Virol. 69:2977-2988.
43. Baroja, M.L., K. Lorre, F. Van Vaeck, and J.L. Ceuppens. 1989. The anti-T cell monoclonal antibody 9.3 (anti-CD28) provides a helper signal and by-passes the need for accessory cells in T cell activation with immobilized anti-CD3 and mitogen. Cell. Immunol. 120:205-217.
44. Guatelli, J.C., T.R. Gingeras, and D.D. Richman. 1990. Alternative splice acceptor utilization during HIV-1 infection of cultured cells. J. Virol. 64: 4093-4098.
45. Maniatis, T., E.F. Fritsch, and J. Sambrook. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. p. 5.
46. Zack, J.A., S.J. Arrigo, S.R. Weitsman, A.S. Go, A. Haislip, and I.S.Y. Chen. 1990. HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell. 61:213-222.
47. Davis, G.R., K. Blumeyer, L. DiMichele, K. Whitfield, H. Chappelle, N. Riggs, S. Gosh, P. Kao, E. Fahey, J. Guatelli, et al. 1990. Detection of HIV-1 in AIDS patients using amplification-mediated hybridization analysis: reproducibility and quantitative limitations. J. Infect. Dis. 162:13-20.
48. Liu, Y., and P.S. Linsley. 1992. Costimulation of T-cell growth. Curr. Opin. Immunol. 4:265-270.
49. Jenkins, M.K., P.S. Taylor, S.D. Norton, and K.B. Urdhl. 1991. CD28 delivers a costimulatory signal involved in antigen-specific IL-2 production by human T cells. J. Immunol. 147:2461-2466.
50. Schwartz, R.H. 1992. Costimulation of T lymphocytes: the role of CD28, CTLA-4, and B7/BB1 in interleukin-2 production and immunotherapy. Cell. 71: 1065-1068.
51. + T cell proliferation in HIV-positive patients as a result of CD28 costimulation. Science (Wash. DC). 272:1939-1943.
52. Dragic, T., V. Litwin, G.P. Allaway, S.R. Martin, Y. Huang, K.A. Nagashima, C. Cayanan, P.J. Maddon, R.A. Koup, J.P. Moore, and W.A. Paxton. 1996. HIV-1 entry into CD4+ cells is mediated by the chemokine receptor C-C CKR-5. Nature (Lond.). 381:667-673.
53. Hazan, U., D. Thomas, J. Alcami, F. Bachelerie, N. Israel, H. Yssel, J.L. Virelizier, and F. Arenzana-Seisdedos. 1990. Stimulation of a human T-cell clone with anti-CD3 or tumor necrosis factor induces NF-kB translocation but not human immunodeficiency virus 1 enhancer-dependent transcription. Proc. Natl. Acad. Sci. USA. 87:7861-7865.
54. Moran, P.A., M.L. Diegel, J.C. Sias, J.A. Ledbetter, and J.M. Zarling. 1993. Regulation of HIV production by blood mononuclear cells from HIV-infected donors: lack of correlation between HIV-1 production and T cell activation. J. Acquired Immune Defic. Syndr. Hum. Retrovirol. 9:455-464.
55. Asjo, B., D. Cefai, P. Debre, Y. Dudoit, and B. Autran. 1993. A novel mode of human immunodeficiency virus type 1 (HIV-1) activation: ligation of CD28 alone induces HIV-1 replication in naturally infected lymphocytes. J. Virol. 67:4395-1398.
56. Helbert, M.R., J. L'age-Stehr, and N.A. Mitchison. 1993. Antigen presentation, loss of immunological memory and AIDS. Immunol. Today. 14:340-344.
57. Cayota, A., F. Vuillier, D. Scott-Algara, V. Feuillie, and G. Dighiero. 1993. Differential requirements for HIV-1 replication in naive and memory CD4 T cells from asymptomatic HIV-1 seropositive carriers and AIDS patients. Clin. Exp. Immunol. 91:241-248.
58. - T cell subsets express CD4-p56lck complexes, CD4-associated lipid kinases, TCR/CD3-p59fyn complexes, and share similar tyrosine kinase substrates. Int. Immunol. 4:409-118.
59. Janeway, C.A., and K. Bottomly. 1994. Signals and signs for lymphocyte responses. Cell. 76:275-285.
60. Woods, T.C., S.T. Butera, and T.M. Folks. 1997. HIV preferentially infects CD4, CD45RO lymphocyte populations in vitro. Blood 89:1635-1642.
61. Baur, A.S., E.T. Sawai, P. Dazin, W.J. Fantl, C. Cheng-Mayer, and B.M. Peterlin. 1994. HIV-1 Nef leads to inhibition or activation of T cells depending on its intracellular location. Immunity. 1:373-384.
62. Sawai, E.T., A. Baur, H. Struble, B.M. Peterlin, J.A. Levy, and C. Chen-Mayer. 1994. HIV-1 Nef associates with a cellular serine kinase in T lymphocytes. Proc. Natl. Acad. Sci. USA. 91:1539-1543.
63. Bodeus, M., A. Marie-Cardine, C. Bougeret, F. Ramos-Morales, and R. Benarous. 1995. In vitro binding and phosphorylation of human immunodeficiency virus type 1 Nef protein by serine/threonine protein kinase. J. Gen. Virol. 76:1337-1344.
64. Collette, Y., H. Dutartre, A. Benziane, F. Ramos-Morales, R. Benarous, M. Harris, and D. Olive. 1996. Physical and functional interaction of nef with lck. J. Biol. Chem. 271:6333-6341.
65. Guy, B., M.P. Kieny, Y. Riviere, C. LePeuch, K. Dott, M. Girard, L. Montagnier, and J.P. Lecocq. 1987. HIV F/3′ orf encodes a phosphorylated GTP-binding protein resembling an oncogene product. Nature (Lond.). 330: 266-269.
66. Garcia, J.V., and A.D. Miller. 1991. Serine phosphorylation-independent downregulation of cell-surface CD4 by nef. Nature (Lond.). 350:508-511.
67. Luria, S., I. Chambers, and P. Berg. 1991. Expression of the type 1 human immunodeficiency virus nef protein in T cells prevents antigen receptor-mediated induction of interleukin-2 mRNA. Proc. Natl. Acad. Sci. USA. 88: 5326-5330.
68. Niederman, T.M.J., J.V. Garcia, W.R. Hastings, S. Luria, and L. Ratner. 1992. Human immunodeficiency virus type 1 nef protein inhibits NF-kB induction in human T cells. J. Virol. 66:6213-6219.
69. Niederman, T.M.J., W.R. Hastings, S. Luria, J.C. Bandres, and L. Ratner. 1993. HIV-1 nef protein inhibits the recruitment of AP-1 DNA-binding activity in human T-cells. Virology. 194:338-344.
70. Koyanagi, Y., S. Miles, R.T. Mitsuyasu, J.E. Merrill, H.V. Vinters, and I.S.Y. Chen. 1987. Dual infection of the central nervous system by AIDS viruses with distinct cellular tropisms. Science (Wash. DC). 236:819-882.
71. Seshamma, T., O. Bagasra, D. Trono, D. Baltimore, and R.J. Pomerantz. 1992. Blocked early-stage latency in the peripheral blood cells of certain individuals infected with human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. USA. 89:10663-10667.
72. Roederer, M., J.G. Dubs, M.T. Anderson, P.A. Raju, and L.A. Herzenberg. 1995. CD8 naive T cell counts decease progressively in HIV-infected adults. J. Clin. Invest. 95:2061-2066.
73. Tassinari, P., L. Deibis, I. Blanca, N.E. Bianco, and E.G. de Perez. 1995. Decreased T-cell proliferative response to common environmental antigens could be an indicator of early human immunodeficiency virus-mediated lymphocyte lesions. Clin. Diagn. Lab. Immunol. 2:404-407.