Skip to main content
PMC home page
Journal of Virology logoLink to Journal of Virology
. 1997 May;71(5):3776–3787. doi: 10.1128/jvi.71.5.3776-3787.1997

Human immunodeficiency virus type 1 Nef does not alter T-cell sensitivity to antigen-specific stimulation.

K A Page 1, W C van Schooten 1, M B Feinberg 1
PMCID: PMC191528  PMID: 9094653

Abstract

We have developed an in vitro model to study the influence that human immunodeficiency virus type 1 (HIV-1) may have on the ability of T cells to respond to antigenic challenge. We have examined consequences of HIV-1 gene expression on T-cell activation in antigen-dependent T cells that have stably integrated copies of replication-defective proviral HIV-1. Virus production by HIV-infected, antigen-dependent T cells was induced in response to antigenic stimulation and then decreased as infected cells returned to a state of quiescence. Contrary to the predictions of models proposing that Nef alters signal transduction pathways in T lymphocytes and thereby alters cellular activation, Nef expression in antigen-dependent T-cell clones did not influence their proliferative responses to low or intermediate concentrations of antigen and did not affect other measures of T-cell activation, such as induction of interleukin 2 receptor alpha-chain expression and cytokine production. In addition, we found no evidence for alteration of T-cell responsiveness to antigen by the gag, pol, vif, tat, or rev gene of HIV-1.

Full Text

The Full Text of this article is available as a PDF (507.7 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aiken C., Konner J., Landau N. R., Lenburg M. E., Trono D. Nef induces CD4 endocytosis: requirement for a critical dileucine motif in the membrane-proximal CD4 cytoplasmic domain. Cell. 1994 Mar 11;76(5):853–864. doi: 10.1016/0092-8674(94)90360-3. [DOI] [PubMed] [Google Scholar]
  2. Aiken C., Trono D. Nef stimulates human immunodeficiency virus type 1 proviral DNA synthesis. J Virol. 1995 Aug;69(8):5048–5056. doi: 10.1128/jvi.69.8.5048-5056.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Anderson S., Shugars D. C., Swanstrom R., Garcia J. V. Nef from primary isolates of human immunodeficiency virus type 1 suppresses surface CD4 expression in human and mouse T cells. J Virol. 1993 Aug;67(8):4923–4931. doi: 10.1128/jvi.67.8.4923-4931.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baur A. S., Sawai E. T., Dazin P., Fantl W. J., Cheng-Mayer C., Peterlin B. M. HIV-1 Nef leads to inhibition or activation of T cells depending on its intracellular localization. Immunity. 1994 Aug;1(5):373–384. doi: 10.1016/1074-7613(94)90068-x. [DOI] [PubMed] [Google Scholar]
  5. Bednarik D. P., Folks T. M. Mechanisms of HIV-1 latency. AIDS. 1992 Jan;6(1):3–16. doi: 10.1097/00002030-199201000-00001. [DOI] [PubMed] [Google Scholar]
  6. Buelow R., Paborsky L. R., van Schooten W. C., Kummerehl T. J., Schreifels R., Marshall K., Mayer J., Rothbard J. B. Comparison of three different forms of HLA-DR4Dw4 proteins. Eur J Immunol. 1993 Jan;23(1):69–76. doi: 10.1002/eji.1830230112. [DOI] [PubMed] [Google Scholar]
  7. Bukrinsky M. I., Stanwick T. L., Dempsey M. P., Stevenson M. Quiescent T lymphocytes as an inducible virus reservoir in HIV-1 infection. Science. 1991 Oct 18;254(5030):423–427. doi: 10.1126/science.1925601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Buonaguro L., Barillari G., Chang H. K., Bohan C. A., Kao V., Morgan R., Gallo R. C., Ensoli B. Effects of the human immunodeficiency virus type 1 Tat protein on the expression of inflammatory cytokines. J Virol. 1992 Dec;66(12):7159–7167. doi: 10.1128/jvi.66.12.7159-7167.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Carreer R., Groux H., Ameisen J. C., Capron A. Role of HIV-1 Nef expression in activation pathways in CD4+ T cells. AIDS Res Hum Retroviruses. 1994 May;10(5):523–527. doi: 10.1089/aid.1994.10.523. [DOI] [PubMed] [Google Scholar]
  10. Chirmule N., Than S., Khan S. A., Pahwa S. Human immunodeficiency virus Tat induces functional unresponsiveness in T cells. J Virol. 1995 Jan;69(1):492–498. doi: 10.1128/jvi.69.1.492-498.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chowers M. Y., Spina C. A., Kwoh T. J., Fitch N. J., Richman D. D., Guatelli J. C. Optimal infectivity in vitro of human immunodeficiency virus type 1 requires an intact nef gene. J Virol. 1994 May;68(5):2906–2914. doi: 10.1128/jvi.68.5.2906-2914.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chun T. W., Finzi D., Margolick J., Chadwick K., Schwartz D., Siliciano R. F. In vivo fate of HIV-1-infected T cells: quantitative analysis of the transition to stable latency. Nat Med. 1995 Dec;1(12):1284–1290. doi: 10.1038/nm1295-1284. [DOI] [PubMed] [Google Scholar]
  13. Collette Y., Chang H. L., Cerdan C., Chambost H., Algarte M., Mawas C., Imbert J., Burny A., Olive D. Specific Th1 cytokine down-regulation associated with primary clinically derived human immunodeficiency virus type 1 Nef gene-induced expression. J Immunol. 1996 Jan 1;156(1):360–370. [PubMed] [Google Scholar]
  14. Deacon N. J., Tsykin A., Solomon A., Smith K., Ludford-Menting M., Hooker D. J., McPhee D. A., Greenway A. L., Ellett A., Chatfield C. Genomic structure of an attenuated quasi species of HIV-1 from a blood transfusion donor and recipients. Science. 1995 Nov 10;270(5238):988–991. doi: 10.1126/science.270.5238.988. [DOI] [PubMed] [Google Scholar]
  15. Du Z., Lang S. M., Sasseville V. G., Lackner A. A., Ilyinskii P. O., Daniel M. D., Jung J. U., Desrosiers R. C. Identification of a nef allele that causes lymphocyte activation and acute disease in macaque monkeys. Cell. 1995 Aug 25;82(4):665–674. doi: 10.1016/0092-8674(95)90038-1. [DOI] [PubMed] [Google Scholar]
  16. Duh E. J., Maury W. J., Folks T. M., Fauci A. S., Rabson A. B. 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. 1989 Aug;86(15):5974–5978. doi: 10.1073/pnas.86.15.5974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Embretson J., Zupancic M., Ribas J. L., Burke A., Racz P., Tenner-Racz K., Haase A. T. Massive covert infection of helper T lymphocytes and macrophages by HIV during the incubation period of AIDS. Nature. 1993 Mar 25;362(6418):359–362. doi: 10.1038/362359a0. [DOI] [PubMed] [Google Scholar]
  18. Fauci A. S. Multifactorial nature of human immunodeficiency virus disease: implications for therapy. Science. 1993 Nov 12;262(5136):1011–1018. doi: 10.1126/science.8235617. [DOI] [PubMed] [Google Scholar]
  19. Feinberg M. B., Jarrett R. F., Aldovini A., Gallo R. C., Wong-Staal F. HTLV-III expression and production involve complex regulation at the levels of splicing and translation of viral RNA. Cell. 1986 Sep 12;46(6):807–817. doi: 10.1016/0092-8674(86)90062-0. [DOI] [PubMed] [Google Scholar]
  20. Folks T. M., Clouse K. A., Justement J., Rabson A., Duh E., Kehrl J. H., Fauci A. S. Tumor necrosis factor alpha induces expression of human immunodeficiency virus in a chronically infected T-cell clone. Proc Natl Acad Sci U S A. 1989 Apr;86(7):2365–2368. doi: 10.1073/pnas.86.7.2365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Folks T. M., Justement J., Kinter A., Dinarello C. A., Fauci A. S. Cytokine-induced expression of HIV-1 in a chronically infected promonocyte cell line. Science. 1987 Nov 6;238(4828):800–802. doi: 10.1126/science.3313729. [DOI] [PubMed] [Google Scholar]
  22. Garcia J. V., Miller A. D. Serine phosphorylation-independent downregulation of cell-surface CD4 by nef. Nature. 1991 Apr 11;350(6318):508–511. doi: 10.1038/350508a0. [DOI] [PubMed] [Google Scholar]
  23. Goldsmith M. A., Warmerdam M. T., Atchison R. E., Miller M. D., Greene W. C. Dissociation of the CD4 downregulation and viral infectivity enhancement functions of human immunodeficiency virus type 1 Nef. J Virol. 1995 Jul;69(7):4112–4121. doi: 10.1128/jvi.69.7.4112-4121.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Greenway A., Azad A., McPhee D. Human immunodeficiency virus type 1 Nef protein inhibits activation pathways in peripheral blood mononuclear cells and T-cell lines. J Virol. 1995 Mar;69(3):1842–1850. doi: 10.1128/jvi.69.3.1842-1850.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Haanen J. B., Ottenhoff T. H., Voordouw A., Elferink B. G., Klatser P. R., Spits H., De Vries R. R. HLA class-II-restricted Mycobacterium leprae-reactive T-cell clones from leprosy patients established with a minimal requirement for autologous mononuclear cells. Scand J Immunol. 1986 Jan;23(1):101–108. doi: 10.1111/j.1365-3083.1986.tb01947.x. [DOI] [PubMed] [Google Scholar]
  26. Hazan U., Thomas D., Alcami J., Bachelerie F., Israel N., Yssel H., Virelizier J. L., Arenzana-Seisdedos F. Stimulation of a human T-cell clone with anti-CD3 or tumor necrosis factor induces NF-kappa B translocation but not human immunodeficiency virus 1 enhancer-dependent transcription. Proc Natl Acad Sci U S A. 1990 Oct;87(20):7861–7865. doi: 10.1073/pnas.87.20.7861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ho D. D., Neumann A. U., Perelson A. S., Chen W., Leonard J. M., Markowitz M. Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature. 1995 Jan 12;373(6510):123–126. doi: 10.1038/373123a0. [DOI] [PubMed] [Google Scholar]
  28. Howcroft T. K., Strebel K., Martin M. A., Singer D. S. Repression of MHC class I gene promoter activity by two-exon Tat of HIV. Science. 1993 May 28;260(5112):1320–1322. doi: 10.1126/science.8493575. [DOI] [PubMed] [Google Scholar]
  29. Kestler H. W., 3rd, Ringler D. J., Mori K., Panicali D. L., Sehgal P. K., Daniel M. D., Desrosiers R. C. Importance of the nef gene for maintenance of high virus loads and for development of AIDS. Cell. 1991 May 17;65(4):651–662. doi: 10.1016/0092-8674(91)90097-i. [DOI] [PubMed] [Google Scholar]
  30. Kirchhoff F., Greenough T. C., Brettler D. B., Sullivan J. L., Desrosiers R. C. Brief report: absence of intact nef sequences in a long-term survivor with nonprogressive HIV-1 infection. N Engl J Med. 1995 Jan 26;332(4):228–232. doi: 10.1056/NEJM199501263320405. [DOI] [PubMed] [Google Scholar]
  31. Li C. J., Friedman D. J., Wang C., Metelev V., Pardee A. B. Induction of apoptosis in uninfected lymphocytes by HIV-1 Tat protein. Science. 1995 Apr 21;268(5209):429–431. doi: 10.1126/science.7716549. [DOI] [PubMed] [Google Scholar]
  32. Luo T., Garcia J. V. The association of Nef with a cellular serine/threonine kinase and its enhancement of infectivity are viral isolate dependent. J Virol. 1996 Sep;70(9):6493–6496. doi: 10.1128/jvi.70.9.6493-6496.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Luria S., Chambers I., Berg P. 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 U S A. 1991 Jun 15;88(12):5326–5330. doi: 10.1073/pnas.88.12.5326. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. McCune J. M. Viral latency in HIV disease. Cell. 1995 Jul 28;82(2):183–188. doi: 10.1016/0092-8674(95)90305-4. [DOI] [PubMed] [Google Scholar]
  35. Merrill J. E., Koyanagi Y., Zack J., Thomas L., Martin F., Chen I. S. Induction of interleukin-1 and tumor necrosis factor alpha in brain cultures by human immunodeficiency virus type 1. J Virol. 1992 Apr;66(4):2217–2225. doi: 10.1128/jvi.66.4.2217-2225.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Miller M. D., Feinberg M. B., Greene W. C. The HIV-1 nef gene acts as a positive viral infectivity factor. Trends Microbiol. 1994 Aug;2(8):294–298. doi: 10.1016/0966-842x(94)90007-8. [DOI] [PubMed] [Google Scholar]
  37. Miller M. D., Warmerdam M. T., Gaston I., Greene W. C., Feinberg M. B. The human immunodeficiency virus-1 nef gene product: a positive factor for viral infection and replication in primary lymphocytes and macrophages. J Exp Med. 1994 Jan 1;179(1):101–113. doi: 10.1084/jem.179.1.101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Miller M. D., Warmerdam M. T., Page K. A., Feinberg M. B., Greene W. C. Expression of the human immunodeficiency virus type 1 (HIV-1) nef gene during HIV-1 production increases progeny particle infectivity independently of gp160 or viral entry. J Virol. 1995 Jan;69(1):579–584. doi: 10.1128/jvi.69.1.579-584.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Mustafa F., Robinson H. L. Context-dependent role of human immunodeficiency virus type 1 auxiliary genes in the establishment of chronic virus producers. J Virol. 1993 Nov;67(11):6909–6915. doi: 10.1128/jvi.67.11.6909-6915.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Niederman T. M., Garcia J. V., Hastings W. R., Luria S., Ratner L. Human immunodeficiency virus type 1 Nef protein inhibits NF-kappa B induction in human T cells. J Virol. 1992 Oct;66(10):6213–6219. doi: 10.1128/jvi.66.10.6213-6219.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Niederman T. M., Hastings W. R., Luria S., Bandres J. C., Ratner L. HIV-1 Nef protein inhibits the recruitment of AP-1 DNA-binding activity in human T-cells. Virology. 1993 May;194(1):338–344. doi: 10.1006/viro.1993.1264. [DOI] [PubMed] [Google Scholar]
  42. Nunn M. F., Marsh J. W. Human immunodeficiency virus type 1 Nef associates with a member of the p21-activated kinase family. J Virol. 1996 Sep;70(9):6157–6161. doi: 10.1128/jvi.70.9.6157-6161.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Osborn L., Kunkel S., Nabel G. J. Tumor necrosis factor alpha and interleukin 1 stimulate the human immunodeficiency virus enhancer by activation of the nuclear factor kappa B. Proc Natl Acad Sci U S A. 1989 Apr;86(7):2336–2340. doi: 10.1073/pnas.86.7.2336. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Page K. A., Landau N. R., Littman D. R. Construction and use of a human immunodeficiency virus vector for analysis of virus infectivity. J Virol. 1990 Nov;64(11):5270–5276. doi: 10.1128/jvi.64.11.5270-5276.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Perelson A. S., Neumann A. U., Markowitz M., Leonard J. M., Ho D. D. HIV-1 dynamics in vivo: virion clearance rate, infected cell life-span, and viral generation time. Science. 1996 Mar 15;271(5255):1582–1586. doi: 10.1126/science.271.5255.1582. [DOI] [PubMed] [Google Scholar]
  46. Perno C. F., Yarchoan R., Cooney D. A., Hartman N. R., Webb D. S., Hao Z., Mitsuya H., Johns D. G., Broder S. Replication of human immunodeficiency virus in monocytes. Granulocyte/macrophage colony-stimulating factor (GM-CSF) potentiates viral production yet enhances the antiviral effect mediated by 3'-azido-2'3'-dideoxythymidine (AZT) and other dideoxynucleoside congeners of thymidine. J Exp Med. 1989 Mar 1;169(3):933–951. doi: 10.1084/jem.169.3.933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Purvis S. F., Georges D. L., Williams T. M., Lederman M. M. Suppression of interleukin-2 and interleukin-2 receptor expression in Jurkat cells stably expressing the human immunodeficiency virus Tat protein. Cell Immunol. 1992 Oct 1;144(1):32–42. doi: 10.1016/0008-8749(92)90223-c. [DOI] [PubMed] [Google Scholar]
  48. Rhee S. S., Marsh J. W. HIV-1 Nef activity in murine T cells. CD4 modulation and positive enhancement. J Immunol. 1994 May 15;152(10):5128–5134. [PubMed] [Google Scholar]
  49. Rogel M. E., Wu L. I., Emerman M. The human immunodeficiency virus type 1 vpr gene prevents cell proliferation during chronic infection. J Virol. 1995 Feb;69(2):882–888. doi: 10.1128/jvi.69.2.882-888.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Saksela K., Cheng G., Baltimore D. Proline-rich (PxxP) motifs in HIV-1 Nef bind to SH3 domains of a subset of Src kinases and are required for the enhanced growth of Nef+ viruses but not for down-regulation of CD4. EMBO J. 1995 Feb 1;14(3):484–491. doi: 10.1002/j.1460-2075.1995.tb07024.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Sawai E. T., Baur A. S., Peterlin B. M., Levy J. A., Cheng-Mayer C. A conserved domain and membrane targeting of Nef from HIV and SIV are required for association with a cellular serine kinase activity. J Biol Chem. 1995 Jun 23;270(25):15307–15314. doi: 10.1074/jbc.270.25.15307. [DOI] [PubMed] [Google Scholar]
  52. Sawai E. T., Baur A., Struble H., Peterlin B. M., Levy J. A., Cheng-Mayer C. Human immunodeficiency virus type 1 Nef associates with a cellular serine kinase in T lymphocytes. Proc Natl Acad Sci U S A. 1994 Feb 15;91(4):1539–1543. doi: 10.1073/pnas.91.4.1539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Scala G., Ruocco M. R., Ambrosino C., Mallardo M., Giordano V., Baldassarre F., Dragonetti E., Quinto I., Venuta S. The expression of the interleukin 6 gene is induced by the human immunodeficiency virus 1 TAT protein. J Exp Med. 1994 Mar 1;179(3):961–971. doi: 10.1084/jem.179.3.961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Schnittman S. M., Psallidopoulos M. C., Lane H. C., Thompson L., Baseler M., Massari F., Fox C. H., Salzman N. P., Fauci A. S. The reservoir for HIV-1 in human peripheral blood is a T cell that maintains expression of CD4. Science. 1989 Jul 21;245(4915):305–308. doi: 10.1126/science.2665081. [DOI] [PubMed] [Google Scholar]
  55. Schwartz O., Arenzana-Seisdedos F., Heard J. M., Danos O. Activation pathways and human immunodeficiency virus type 1 replication are not altered in CD4+ T cells expressing the nef protein. AIDS Res Hum Retroviruses. 1992 May;8(5):545–551. doi: 10.1089/aid.1992.8.545. [DOI] [PubMed] [Google Scholar]
  56. Skowronski J., Parks D., Mariani R. Altered T cell activation and development in transgenic mice expressing the HIV-1 nef gene. EMBO J. 1993 Feb;12(2):703–713. doi: 10.1002/j.1460-2075.1993.tb05704.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Spina C. A., Kwoh T. J., Chowers M. Y., Guatelli J. C., Richman D. D. The importance of nef in the induction of human immunodeficiency virus type 1 replication from primary quiescent CD4 lymphocytes. J Exp Med. 1994 Jan 1;179(1):115–123. doi: 10.1084/jem.179.1.115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Staprans S. I., Hamilton B. L., Follansbee S. E., Elbeik T., Barbosa P., Grant R. M., Feinberg M. B. Activation of virus replication after vaccination of HIV-1-infected individuals. J Exp Med. 1995 Dec 1;182(6):1727–1737. doi: 10.1084/jem.182.6.1727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Stevenson M., Stanwick T. L., Dempsey M. P., Lamonica C. A. HIV-1 replication is controlled at the level of T cell activation and proviral integration. EMBO J. 1990 May;9(5):1551–1560. doi: 10.1002/j.1460-2075.1990.tb08274.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Trono D. HIV accessory proteins: leading roles for the supporting cast. Cell. 1995 Jul 28;82(2):189–192. doi: 10.1016/0092-8674(95)90306-2. [DOI] [PubMed] [Google Scholar]
  61. Viscidi R. P., Mayur K., Lederman H. M., Frankel A. D. Inhibition of antigen-induced lymphocyte proliferation by Tat protein from HIV-1. Science. 1989 Dec 22;246(4937):1606–1608. doi: 10.1126/science.2556795. [DOI] [PubMed] [Google Scholar]
  62. Wei X., Ghosh S. K., Taylor M. E., Johnson V. A., Emini E. A., Deutsch P., Lifson J. D., Bonhoeffer S., Nowak M. A., Hahn B. H. Viral dynamics in human immunodeficiency virus type 1 infection. Nature. 1995 Jan 12;373(6510):117–122. doi: 10.1038/373117a0. [DOI] [PubMed] [Google Scholar]
  63. Westendorp M. O., Frank R., Ochsenbauer C., Stricker K., Dhein J., Walczak H., Debatin K. M., Krammer P. H. Sensitization of T cells to CD95-mediated apoptosis by HIV-1 Tat and gp120. Nature. 1995 Jun 8;375(6531):497–500. doi: 10.1038/375497a0. [DOI] [PubMed] [Google Scholar]
  64. Westendorp M. O., Li-Weber M., Frank R. W., Krammer P. H. Human immunodeficiency virus type 1 Tat upregulates interleukin-2 secretion in activated T cells. J Virol. 1994 Jul;68(7):4177–4185. doi: 10.1128/jvi.68.7.4177-4185.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Westendorp M. O., Shatrov V. A., Schulze-Osthoff K., Frank R., Kraft M., Los M., Krammer P. H., Dröge W., Lehmann V. HIV-1 Tat potentiates TNF-induced NF-kappa B activation and cytotoxicity by altering the cellular redox state. EMBO J. 1995 Feb 1;14(3):546–554. doi: 10.1002/j.1460-2075.1995.tb07030.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Zack J. A., Arrigo S. J., Weitsman S. R., Go A. S., Haislip A., Chen I. S. HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell. 1990 Apr 20;61(2):213–222. doi: 10.1016/0092-8674(90)90802-l. [DOI] [PubMed] [Google Scholar]
  67. van Schooten W. C., Ko J. L., van der Stoep N., Haanen J. B., Pickering L., de Vries R. R., van den Elsen P. T-cell receptor beta-chain gene usage in the T-cell recognition of Mycobacterium leprae antigens in one tuberculoid leprosy patient. Proc Natl Acad Sci U S A. 1992 Dec 1;89(23):11244–11248. doi: 10.1073/pnas.89.23.11244. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES