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. 1992 Dec;66(12):7159–7167. doi: 10.1128/jvi.66.12.7159-7167.1992

Effects of the human immunodeficiency virus type 1 Tat protein on the expression of inflammatory cytokines.

L Buonaguro 1, G Barillari 1, H K Chang 1, C A Bohan 1, V Kao 1, R Morgan 1, R C Gallo 1, B Ensoli 1
PMCID: PMC240407  PMID: 1279199

Abstract

Increased levels of inflammatory cytokines, including tumor necrosis factor (TNF), interleukin-1 (IL-1), and IL-6, have been detected in specimens from human immunodeficiency virus type 1 (HIV-1)-infected individuals. Here we demonstrate that HIV-1 activates the expression of TNF but not of IL-1 and IL-6 in acutely and chronically infected T cells. The increase in TNF gene expression is due to activation of the TNF promoter by the viral gene product Tat. Transactivation of TNF gene expression requires the product of the first exon of the tat gene and is cell type independent. T cells chronically infected with pol-defective HIV-1 provirus constitutively express both Tat and TNF at levels significantly higher (fivefold) than those seen in control cells, and treatment with phorbol myristate acetate greatly enhances Tat expression and TNF production. As TNF can increase the production of IL-1 and IL-6 and these inflammatory cytokines all enhance HIV-1 gene expression and affect the immune, vascular, and central nervous systems, the activation of TNF by Tat may be part of a complex pathway in which HIV-1 uses viral products and host factors to increase its own expression and infectivity and to induce disease.

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Selected References

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  1. Aboulafia D., Miles S. A., Saks S. R., Mitsuyasu R. T. Intravenous recombinant tumor necrosis factor in the treatment of AIDS-related Kaposi's sarcoma. J Acquir Immune Defic Syndr. 1989;2(1):54–58. [PubMed] [Google Scholar]
  2. Arya S. K., Guo C., Josephs S. F., Wong-Staal F. Trans-activator gene of human T-lymphotropic virus type III (HTLV-III). Science. 1985 Jul 5;229(4708):69–73. doi: 10.1126/science.2990040. [DOI] [PubMed] [Google Scholar]
  3. Berkhout B., Gatignol A., Rabson A. B., Jeang K. T. TAR-independent activation of the HIV-1 LTR: evidence that tat requires specific regions of the promoter. Cell. 1990 Aug 24;62(4):757–767. doi: 10.1016/0092-8674(90)90120-4. [DOI] [PubMed] [Google Scholar]
  4. Boulerice F., Bour S., Geleziunas R., Lvovich A., Wainberg M. A. High frequency of isolation of defective human immunodeficiency virus type 1 and heterogeneity of viral gene expression in clones of infected U-937 cells. J Virol. 1990 Apr;64(4):1745–1755. doi: 10.1128/jvi.64.4.1745-1755.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Boulter C. A., Wagner E. F. A universal retroviral vector for efficient constitutive expression of exogenous genes. Nucleic Acids Res. 1987 Sep 11;15(17):7194–7194. doi: 10.1093/nar/15.17.7194. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Breen E. C., Rezai A. R., Nakajima K., Beall G. N., Mitsuyasu R. T., Hirano T., Kishimoto T., Martinez-Maza O. Infection with HIV is associated with elevated IL-6 levels and production. J Immunol. 1990 Jan 15;144(2):480–484. [PubMed] [Google Scholar]
  7. Cicco N. A., Lübbert M., Oster W., Lindemann A., Mertelsmann R. Cytokines in the pathogenesis and management of non-Hodgkin's lymphomas. Hematol Oncol Clin North Am. 1991 Oct;5(5):1053–1066. [PubMed] [Google Scholar]
  8. Clouse K. A., Powell D., Washington I., Poli G., Strebel K., Farrar W., Barstad P., Kovacs J., Fauci A. S., Folks T. M. Monokine regulation of human immunodeficiency virus-1 expression in a chronically infected human T cell clone. J Immunol. 1989 Jan 15;142(2):431–438. [PubMed] [Google Scholar]
  9. Clouse K. A., Robbins P. B., Fernie B., Ostrove J. M., Fauci A. S. Viral antigen stimulation of the production of human monokines capable of regulating HIV1 expression. J Immunol. 1989 Jul 15;143(2):470–475. [PubMed] [Google Scholar]
  10. Cross S. L., Feinberg M. B., Wolf J. B., Holbrook N. J., Wong-Staal F., Leonard W. J. Regulation of the human interleukin-2 receptor alpha chain promoter: activation of a nonfunctional promoter by the transactivator gene of HTLV-I. Cell. 1987 Apr 10;49(1):47–56. doi: 10.1016/0092-8674(87)90754-9. [DOI] [PubMed] [Google Scholar]
  11. Dayton A. I., Sodroski J. G., Rosen C. A., Goh W. C., Haseltine W. A. The trans-activator gene of the human T cell lymphotropic virus type III is required for replication. Cell. 1986 Mar 28;44(6):941–947. doi: 10.1016/0092-8674(86)90017-6. [DOI] [PubMed] [Google Scholar]
  12. Dinarello C. A., Savage N. Interleukin-1 and its receptor. Crit Rev Immunol. 1989;9(1):1–20. [PubMed] [Google Scholar]
  13. Ensoli B., Barillari G., Gallo R. C. Pathogenesis of AIDS-associated Kaposi's sarcoma. Hematol Oncol Clin North Am. 1991 Apr;5(2):281–295. [PubMed] [Google Scholar]
  14. Ensoli B., Barillari G., Salahuddin S. Z., Gallo R. C., Wong-Staal F. Tat protein of HIV-1 stimulates growth of cells derived from Kaposi's sarcoma lesions of AIDS patients. Nature. 1990 May 3;345(6270):84–86. doi: 10.1038/345084a0. [DOI] [PubMed] [Google Scholar]
  15. Ensoli B., Lusso P., Schachter F., Josephs S. F., Rappaport J., Negro F., Gallo R. C., Wong-Staal F. Human herpes virus-6 increases HIV-1 expression in co-infected T cells via nuclear factors binding to the HIV-1 enhancer. EMBO J. 1989 Oct;8(10):3019–3027. doi: 10.1002/j.1460-2075.1989.tb08452.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ensoli B., Nakamura S., Salahuddin S. Z., Biberfeld P., Larsson L., Beaver B., Wong-Staal F., Gallo R. C. AIDS-Kaposi's sarcoma-derived cells express cytokines with autocrine and paracrine growth effects. Science. 1989 Jan 13;243(4888):223–226. doi: 10.1126/science.2643161. [DOI] [PubMed] [Google Scholar]
  17. Fauci A. S. The human immunodeficiency virus: infectivity and mechanisms of pathogenesis. Science. 1988 Feb 5;239(4840):617–622. doi: 10.1126/science.3277274. [DOI] [PubMed] [Google Scholar]
  18. Felber B. K., Paskalis H., Kleinman-Ewing C., Wong-Staal F., Pavlakis G. N. The pX protein of HTLV-I is a transcriptional activator of its long terminal repeats. Science. 1985 Aug 16;229(4714):675–679. doi: 10.1126/science.2992082. [DOI] [PubMed] [Google Scholar]
  19. Feng S., Holland E. C. HIV-1 tat trans-activation requires the loop sequence within tar. Nature. 1988 Jul 14;334(6178):165–167. doi: 10.1038/334165a0. [DOI] [PubMed] [Google Scholar]
  20. Fisher A. G., Feinberg M. B., Josephs S. F., Harper M. E., Marselle L. M., Reyes G., Gonda M. A., Aldovini A., Debouk C., Gallo R. C. The trans-activator gene of HTLV-III is essential for virus replication. 1986 Mar 27-Apr 2Nature. 320(6060):367–371. doi: 10.1038/320367a0. [DOI] [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. Folks T. M., Powell D., Lightfoote M., Koenig S., Fauci A. S., Benn S., Rabson A., Daugherty D., Gendelman H. E., Hoggan M. D. Biological and biochemical characterization of a cloned Leu-3- cell surviving infection with the acquired immune deficiency syndrome retrovirus. J Exp Med. 1986 Jul 1;164(1):280–290. doi: 10.1084/jem.164.1.280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Frankel A. D., Pabo C. O. Cellular uptake of the tat protein from human immunodeficiency virus. Cell. 1988 Dec 23;55(6):1189–1193. doi: 10.1016/0092-8674(88)90263-2. [DOI] [PubMed] [Google Scholar]
  24. Garcia J. A., Harrich D., Soultanakis E., Wu F., Mitsuyasu R., Gaynor R. B. Human immunodeficiency virus type 1 LTR TATA and TAR region sequences required for transcriptional regulation. EMBO J. 1989 Mar;8(3):765–778. doi: 10.1002/j.1460-2075.1989.tb03437.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Gorman C. M., Moffat L. F., Howard B. H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. doi: 10.1128/mcb.2.9.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Griffin G. E., Leung K., Folks T. M., Kunkel S., Nabel G. J. Activation of HIV gene expression during monocyte differentiation by induction of NF-kappa B. Nature. 1989 May 4;339(6219):70–73. doi: 10.1038/339070a0. [DOI] [PubMed] [Google Scholar]
  27. Gruters R. A., Otto S. A., Al B. J., Verhoeven A. J., Verweij C. L., Van Lier R. A., Miedema F. Non-mitogenic T cell activation signals are sufficient for induction of human immunodeficiency virus transcription. Eur J Immunol. 1991 Jan;21(1):167–172. doi: 10.1002/eji.1830210125. [DOI] [PubMed] [Google Scholar]
  28. Inoue J., Seiki M., Taniguchi T., Tsuru S., Yoshida M. Induction of interleukin 2 receptor gene expression by p40x encoded by human T-cell leukemia virus type 1. EMBO J. 1986 Nov;5(11):2883–2888. doi: 10.1002/j.1460-2075.1986.tb04583.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Jeang K. T., Shank P. R., Kumar A. Transcriptional activation of homologous viral long terminal repeats by the human immunodeficiency virus type 1 or the human T-cell leukemia virus type I tat proteins occurs in the absence of de novo protein synthesis. Proc Natl Acad Sci U S A. 1988 Nov;85(21):8291–8295. doi: 10.1073/pnas.85.21.8291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Johnson R. T., McArthur J. C., Narayan O. The neurobiology of human immunodeficiency virus infections. FASEB J. 1988 Nov;2(14):2970–2981. doi: 10.1096/fasebj.2.14.2846395. [DOI] [PubMed] [Google Scholar]
  31. Jones K. A., Kadonaga J. T., Luciw P. A., Tjian R. Activation of the AIDS retrovirus promoter by the cellular transcription factor, Sp1. Science. 1986 May 9;232(4751):755–759. doi: 10.1126/science.3008338. [DOI] [PubMed] [Google Scholar]
  32. Kao S. Y., Calman A. F., Luciw P. A., Peterlin B. M. Anti-termination of transcription within the long terminal repeat of HIV-1 by tat gene product. Nature. 1987 Dec 3;330(6147):489–493. doi: 10.1038/330489a0. [DOI] [PubMed] [Google Scholar]
  33. Kehrl J. H., Alvarez-Mon M., Delsing G. A., Fauci A. S. Lymphotoxin is an important T cell-derived growth factor for human B cells. Science. 1987 Nov 20;238(4830):1144–1146. doi: 10.1126/science.3500512. [DOI] [PubMed] [Google Scholar]
  34. Kim S. J., Kehrl J. H., Burton J., Tendler C. L., Jeang K. T., Danielpour D., Thevenin C., Kim K. Y., Sporn M. B., Roberts A. B. Transactivation of the transforming growth factor beta 1 (TGF-beta 1) gene by human T lymphotropic virus type 1 tax: a potential mechanism for the increased production of TGF-beta 1 in adult T cell leukemia. J Exp Med. 1990 Jul 1;172(1):121–129. doi: 10.1084/jem.172.1.121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Kishimoto T., Hirano T. Molecular regulation of B lymphocyte response. Annu Rev Immunol. 1988;6:485–512. doi: 10.1146/annurev.iy.06.040188.002413. [DOI] [PubMed] [Google Scholar]
  36. Knight D. M., Flomerfelt F. A., Ghrayeb J. Expression of the art/trs protein of HIV and study of its role in viral envelope synthesis. Science. 1987 May 15;236(4803):837–840. doi: 10.1126/science.3033827. [DOI] [PubMed] [Google Scholar]
  37. Leonard J., Parrott C., Buckler-White A. J., Turner W., Ross E. K., Martin M. A., Rabson A. B. The NF-kappa B binding sites in the human immunodeficiency virus type 1 long terminal repeat are not required for virus infectivity. J Virol. 1989 Nov;63(11):4919–4924. doi: 10.1128/jvi.63.11.4919-4924.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Lepe-Zuniga J. L., Mansell P. W., Hersh E. M. Idiopathic production of interleukin-1 in acquired immune deficiency syndrome. J Clin Microbiol. 1987 Sep;25(9):1695–1700. doi: 10.1128/jcm.25.9.1695-1700.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Lifson A. R., Rutherford G. W., Jaffe H. W. The natural history of human immunodeficiency virus infection. J Infect Dis. 1988 Dec;158(6):1360–1367. doi: 10.1093/infdis/158.6.1360. [DOI] [PubMed] [Google Scholar]
  40. Lindholm P. F., Reid R. L., Brady J. N. Extracellular Tax1 protein stimulates tumor necrosis factor-beta and immunoglobulin kappa light chain expression in lymphoid cells. J Virol. 1992 Mar;66(3):1294–1302. doi: 10.1128/jvi.66.3.1294-1302.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Locksley R. M., Heinzel F. P., Shepard H. M., Agosti J., Eessalu T. E., Aggarwal B. B., Harlan J. M. Tumor necrosis factors alpha and beta differ in their capacities to generate interleukin 1 release from human endothelial cells. J Immunol. 1987 Sep 15;139(6):1891–1895. [PubMed] [Google Scholar]
  42. Merrill J. E., Koyanagi Y., Chen I. S. Interleukin-1 and tumor necrosis factor alpha can be induced from mononuclear phagocytes by human immunodeficiency virus type 1 binding to the CD4 receptor. J Virol. 1989 Oct;63(10):4404–4408. doi: 10.1128/jvi.63.10.4404-4408.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Meyerhans A., Cheynier R., Albert J., Seth M., Kwok S., Sninsky J., Morfeldt-Månson L., Asjö B., Wain-Hobson S. Temporal fluctuations in HIV quasispecies in vivo are not reflected by sequential HIV isolations. Cell. 1989 Sep 8;58(5):901–910. doi: 10.1016/0092-8674(89)90942-2. [DOI] [PubMed] [Google Scholar]
  44. Miles S. A., Rezai A. R., Salazar-González J. F., Vander Meyden M., Stevens R. H., Logan D. M., Mitsuyasu R. T., Taga T., Hirano T., Kishimoto T. AIDS Kaposi sarcoma-derived cells produce and respond to interleukin 6. Proc Natl Acad Sci U S A. 1990 Jun;87(11):4068–4072. doi: 10.1073/pnas.87.11.4068. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Miller A. D., Rosman G. J. Improved retroviral vectors for gene transfer and expression. Biotechniques. 1989 Oct;7(9):980-2, 984-6, 989-90. [PMC free article] [PubMed] [Google Scholar]
  46. Nabel G., Baltimore D. An inducible transcription factor activates expression of human immunodeficiency virus in T cells. Nature. 1987 Apr 16;326(6114):711–713. doi: 10.1038/326711a0. [DOI] [PubMed] [Google Scholar]
  47. Nedwin G. E., Naylor S. L., Sakaguchi A. Y., Smith D., Jarrett-Nedwin J., Pennica D., Goeddel D. V., Gray P. W. Human lymphotoxin and tumor necrosis factor genes: structure, homology and chromosomal localization. Nucleic Acids Res. 1985 Sep 11;13(17):6361–6373. doi: 10.1093/nar/13.17.6361. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Parrott C., Seidner T., Duh E., Leonard J., Theodore T. S., Buckler-White A., Martin M. A., Rabson A. B. Variable role of the long terminal repeat Sp1-binding sites in human immunodeficiency virus replication in T lymphocytes. J Virol. 1991 Mar;65(3):1414–1419. doi: 10.1128/jvi.65.3.1414-1419.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Paul N. L., Ruddle N. H. Lymphotoxin. Annu Rev Immunol. 1988;6:407–438. doi: 10.1146/annurev.iy.06.040188.002203. [DOI] [PubMed] [Google Scholar]
  50. Poli G., Kinter A., Justement J. S., Kehrl J. H., Bressler P., Stanley S., Fauci A. S. Tumor necrosis factor alpha functions in an autocrine manner in the induction of human immunodeficiency virus expression. Proc Natl Acad Sci U S A. 1990 Jan;87(2):782–785. doi: 10.1073/pnas.87.2.782. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Quinnan G. V., Jr, Rook A. H., Frederick W. R., Manischewitz J. F., Epstein J. S., Siegel J., Masur H., Macher A. M., Mitchell C., Armstrong G. Prevalence, clinical manifestations, and immunology of herpesvirus infections in the acquired immunodeficiency syndrome. Ann N Y Acad Sci. 1984;437:200–206. doi: 10.1111/j.1749-6632.1984.tb37138.x. [DOI] [PubMed] [Google Scholar]
  52. Ratner L., Polmar S. H., Paul N., Ruddle N. Cytotoxic factors secreted by cells infected by human immunodeficiency virus type I. AIDS Res Hum Retroviruses. 1987 Summer;3(2):147–155. doi: 10.1089/aid.1987.3.147. [DOI] [PubMed] [Google Scholar]
  53. Remenick J., Radonovich M. F., Brady J. N. Human immunodeficiency virus Tat transactivation: induction of a tissue-specific enhancer in a nonpermissive cell line. J Virol. 1991 Oct;65(10):5641–5646. doi: 10.1128/jvi.65.10.5641-5646.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Rice A. P., Mathews M. B. Transcriptional but not translational regulation of HIV-1 by the tat gene product. Nature. 1988 Apr 7;332(6164):551–553. doi: 10.1038/332551a0. [DOI] [PubMed] [Google Scholar]
  55. Rieckmann P., Poli G., Fox C. H., Kehrl J. H., Fauci A. S. Recombinant gp120 specifically enhances tumor necrosis factor-alpha production and Ig secretion in B lymphocytes from HIV-infected individuals but not from seronegative donors. J Immunol. 1991 Nov 1;147(9):2922–2927. [PubMed] [Google Scholar]
  56. Rosen C. A., Sodroski J. G., Haseltine W. A. The location of cis-acting regulatory sequences in the human T cell lymphotropic virus type III (HTLV-III/LAV) long terminal repeat. Cell. 1985 Jul;41(3):813–823. doi: 10.1016/s0092-8674(85)80062-3. [DOI] [PubMed] [Google Scholar]
  57. Ruddle N. H., Bergman C. M., McGrath K. M., Lingenheld E. G., Grunnet M. L., Padula S. J., Clark R. B. An antibody to lymphotoxin and tumor necrosis factor prevents transfer of experimental allergic encephalomyelitis. J Exp Med. 1990 Oct 1;172(4):1193–1200. doi: 10.1084/jem.172.4.1193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Sadaie M. R., Tschachler E., Valerie K., Rosenberg M., Felber B. K., Pavlakis G. N., Klotman M. E., Wong-Staal F. Activation of tat-defective human immunodeficiency virus by ultraviolet light. New Biol. 1990 May;2(5):479–486. [PubMed] [Google Scholar]
  59. Saiki R. K., Scharf S., Faloona F., Mullis K. B., Horn G. T., Erlich H. A., Arnheim N. Enzymatic amplification of beta-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science. 1985 Dec 20;230(4732):1350–1354. doi: 10.1126/science.2999980. [DOI] [PubMed] [Google Scholar]
  60. Salahuddin S. Z., Markham P. D., Wong-Staal F., Franchini G., Kalyanaraman V. S., Gallo R. C. Restricted expression of human T-cell leukemia--lymphoma virus (HTLV) in transformed human umbilical cord blood lymphocytes. Virology. 1983 Aug;129(1):51–64. doi: 10.1016/0042-6822(83)90395-1. [DOI] [PubMed] [Google Scholar]
  61. Sanceau J., Wijdenes J., Revel M., Wietzerbin J. IL-6 and IL-6 receptor modulation by IFN-gamma and tumor necrosis factor-alpha in human monocytic cell line (THP-1). Priming effect of IFN-gamma. J Immunol. 1991 Oct 15;147(8):2630–2637. [PubMed] [Google Scholar]
  62. Sastry K. J., Reddy H. R., Pandita R., Totpal K., Aggarwal B. B. HIV-1 tat gene induces tumor necrosis factor-beta (lymphotoxin) in a human B-lymphoblastoid cell line. J Biol Chem. 1990 Nov 25;265(33):20091–20093. [PubMed] [Google Scholar]
  63. Seigel L. J., Ratner L., Josephs S. F., Derse D., Feinberg M. B., Reyes G. R., O'Brien S. J., Wong-Staal F. Transactivation induced by human T-lymphotropic virus type III (HTLV III) maps to a viral sequence encoding 58 amino acids and lacks tissue specificity. Virology. 1986 Jan 15;148(1):226–231. doi: 10.1016/0042-6822(86)90419-8. [DOI] [PubMed] [Google Scholar]
  64. Shearer G. M., Levy R. B. Noninfectious cofactors in susceptibility to AIDS: possible contributions of semen, HLA alloantigens, and lack of natural resistance. Ann N Y Acad Sci. 1984;437:49–57. doi: 10.1111/j.1749-6632.1984.tb37121.x. [DOI] [PubMed] [Google Scholar]
  65. Siekevitz M., Josephs S. F., Dukovich M., Peffer N., Wong-Staal F., Greene W. C. Activation of the HIV-1 LTR by T cell mitogens and the trans-activator protein of HTLV-I. Science. 1987 Dec 11;238(4833):1575–1578. doi: 10.1126/science.2825351. [DOI] [PubMed] [Google Scholar]
  66. Sodroski J., Patarca R., Rosen C., Wong-Staal F., Haseltine W. Location of the trans-activating region on the genome of human T-cell lymphotropic virus type III. Science. 1985 Jul 5;229(4708):74–77. doi: 10.1126/science.2990041. [DOI] [PubMed] [Google Scholar]
  67. Tada H., Rappaport J., Lashgari M., Amini S., Wong-Staal F., Khalili K. Trans-activation of the JC virus late promoter by the tat protein of type 1 human immunodeficiency virus in glial cells. Proc Natl Acad Sci U S A. 1990 May;87(9):3479–3483. doi: 10.1073/pnas.87.9.3479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Tong-Starksen S. E., Luciw P. A., Peterlin B. M. Human immunodeficiency virus long terminal repeat responds to T-cell activation signals. Proc Natl Acad Sci U S A. 1987 Oct;84(19):6845–6849. doi: 10.1073/pnas.84.19.6845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Tschachler E., Robert-Guroff M., Gallo R. C., Reitz M. S., Jr Human T-lymphotropic virus I-infected T cells constitutively express lymphotoxin in vitro. Blood. 1989 Jan;73(1):194–201. [PubMed] [Google Scholar]
  70. Wahl L. M., Corcoran M. L., Pyle S. W., Arthur L. O., Harel-Bellan A., Farrar W. L. Human immunodeficiency virus glycoprotein (gp120) induction of monocyte arachidonic acid metabolites and interleukin 1. Proc Natl Acad Sci U S A. 1989 Jan;86(2):621–625. doi: 10.1073/pnas.86.2.621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Wano Y., Feinberg M., Hosking J. B., Bogerd H., Greene W. C. Stable expression of the tax gene of type I human T-cell leukemia virus in human T cells activates specific cellular genes involved in growth. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9733–9737. doi: 10.1073/pnas.85.24.9733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Zagury D., Bernard J., Leonard R., Cheynier R., Feldman M., Sarin P. S., Gallo R. C. Long-term cultures of HTLV-III--infected T cells: a model of cytopathology of T-cell depletion in AIDS. Science. 1986 Feb 21;231(4740):850–853. doi: 10.1126/science.2418502. [DOI] [PubMed] [Google Scholar]

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