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. 1996 Nov;70(11):7388–7397. doi: 10.1128/jvi.70.11.7388-7397.1996

Tumor necrosis factor alpha inhibits entry of human immunodeficiency virus type 1 into primary human macrophages: a selective role for the 75-kilodalton receptor.

G Herbein 1, L J Montaner 1, S Gordon 1
PMCID: PMC190806  PMID: 8892857

Abstract

The proinflammatory cytokine tumor necrosis factor alpha (TNFalpha) is readily detected after human immunodeficiency virus type 1 (HIV-1) infection of primary macrophages in vitro and is present in plasma and tissues of patients with AIDS. Previous studies have shown that human recombinant TNFalpha (hrTNFalpha) enhances HIV replication in both chronically infected promonocytic and T-lymphoid cell lines in vitro. We report here that in contrast to untreated tissue culture-differentiated macrophages (TCDM), in which the proviral long terminal repeat (LTR) could be detected as soon as 8 h postinfection by a PCR assay, TCDM pretreatment for 3 days by hrTNFalpha markedly delayed its appearance until 72 h after infection with the HIV-1 Ada monocytotropic strain. Moreover the inhibition of formation of the proviral LTR in HIV-1-infected TCDM was directly proportional to the concentration of hrTNFalpha used. To determine if the inhibition of LTR formation results from blockade of viral entry, we performed a reverse transcription PCR assay to detect intracellular genomic viral RNA as early as 2 h after infection. Pretreatment of primary TCDM by hrTNFalpha for 3 days and even for only 2 h inhibits 75% of the viral entry into the cells. The inhibition of viral entry by hrTNFalpha was totally abolished by the use of anti-human TNFalpha monoclonal antibody. By using TNFalpha mutants specific for each human TNFalpha receptor, we showed that the inhibition of HIV-1 entry into TCDM was mediated not through the 55-kDa TNF receptor but through the 75-kDa TNF receptor. Although prolonged (1 to 5 days) TNFalpha treatment can downregulate CD4 expression in primary human TCDM, surface CD4 levels were not reduced by 2 h of treatment and was therefore not a limiting step for HIV-1 entry. In contrast to the inhibition of viral entry into primary TCDM, pretreatment with hrTNFalpha did not modify HIV-1 entry into phytohemagglutinin A-activated peripheral blood lymphocytes. TNFalpha-pretreatment inhibited HIV-1 replication in primary TCDM but not in phytohemagglutinin A-activated peripheral blood lymphocytes as assessed by decreased reverse transcriptase activity in culture supernatants. These results demonstrate that TNFalpha is able to enhance host cellular resistance to HIV-1 infection and that selective inhibition of HIV-1 entry into primary TCDM by TNFalpha involves the 75-kDa TNF receptor but not the 55-kDa TNF receptor.

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Selected References

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  1. Ameglio F., Capobianchi M. R., Castilletti C., Cordiali Fei P., Fais S., Trento E., Dianzani F. Recombinant gp120 induces IL-10 in resting peripheral blood mononuclear cells; correlation with the induction of other cytokines. Clin Exp Immunol. 1994 Mar;95(3):455–458. doi: 10.1111/j.1365-2249.1994.tb07018.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Asjö B., Ivhed I., Gidlund M., Fuerstenberg S., Fenyö E. M., Nilsson K., Wigzell H. Susceptibility to infection by the human immunodeficiency virus (HIV) correlates with T4 expression in a parental monocytoid cell line and its subclones. Virology. 1987 Apr;157(2):359–365. doi: 10.1016/0042-6822(87)90278-9. [DOI] [PubMed] [Google Scholar]
  3. Biswas P., Poli G., Kinter A. L., Justement J. S., Stanley S. K., Maury W. J., Bressler P., Orenstein J. M., Fauci A. S. Interferon gamma induces the expression of human immunodeficiency virus in persistently infected promonocytic cells (U1) and redirects the production of virions to intracytoplasmic vacuoles in phorbol myristate acetate-differentiated U1 cells. J Exp Med. 1992 Sep 1;176(3):739–750. doi: 10.1084/jem.176.3.739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Butera S. T., Roberts B. D., Leung K., Nabel G. J., Folks T. M. Tumor necrosis factor receptor expression and signal transduction in HIV-1-infected cells. AIDS. 1993 Jul;7(7):911–918. doi: 10.1097/00002030-199307000-00002. [DOI] [PubMed] [Google Scholar]
  5. Clerici M., Shearer G. M. A TH1-->TH2 switch is a critical step in the etiology of HIV infection. Immunol Today. 1993 Mar;14(3):107–111. doi: 10.1016/0167-5699(93)90208-3. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Collin M., Gordon S. The kinetics of human immunodeficiency virus reverse transcription are slower in primary human macrophages than in a lymphoid cell line. Virology. 1994 Apr;200(1):114–120. doi: 10.1006/viro.1994.1169. [DOI] [PubMed] [Google Scholar]
  8. Collin M., Herbein G., Montaner L., Gordon S. PCR analysis of HIV1 infection of macrophages: virus entry is CD4-dependent. Res Virol. 1993 Jan-Feb;144(1):13–19. doi: 10.1016/s0923-2516(06)80006-3. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Engelmann H., Holtmann H., Brakebusch C., Avni Y. S., Sarov I., Nophar Y., Hadas E., Leitner O., Wallach D. Antibodies to a soluble form of a tumor necrosis factor (TNF) receptor have TNF-like activity. J Biol Chem. 1990 Aug 25;265(24):14497–14504. [PubMed] [Google Scholar]
  11. Espevik T., Brockhaus M., Loetscher H., Nonstad U., Shalaby R. Characterization of binding and biological effects of monoclonal antibodies against a human tumor necrosis factor receptor. J Exp Med. 1990 Feb 1;171(2):415–426. doi: 10.1084/jem.171.2.415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Feng Y., Broder C. C., Kennedy P. E., Berger E. A. HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science. 1996 May 10;272(5263):872–877. doi: 10.1126/science.272.5263.872. [DOI] [PubMed] [Google Scholar]
  14. Francis M. L., Meltzer M. S. Induction of IFN-alpha by HIV-1 in monocyte-enriched PBMC requires gp120-CD4 interaction but not virus replication. J Immunol. 1993 Aug 15;151(4):2208–2216. [PubMed] [Google Scholar]
  15. Gehr G., Gentz R., Brockhaus M., Loetscher H., Lesslauer W. Both tumor necrosis factor receptor types mediate proliferative signals in human mononuclear cell activation. J Immunol. 1992 Aug 1;149(3):911–917. [PubMed] [Google Scholar]
  16. Gessani S., Puddu P., Varano B., Borghi P., Conti L., Fantuzzi L., Belardelli F. Induction of beta interferon by human immunodeficiency virus type 1 and its gp120 protein in human monocytes-macrophages: role of beta interferon in restriction of virus replication. J Virol. 1994 Mar;68(3):1983–1986. doi: 10.1128/jvi.68.3.1983-1986.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Havell E. A. Evidence that tumor necrosis factor has an important role in antibacterial resistance. J Immunol. 1989 Nov 1;143(9):2894–2899. [PubMed] [Google Scholar]
  18. Herbein G., Doyle A. G., Montaner L. J., Gordon S. Lipopolysaccharide (LPS) down-regulates CD4 expression in primary human macrophages through induction of endogenous tumour necrosis factor (TNF) and IL-1 beta. Clin Exp Immunol. 1995 Nov;102(2):430–437. doi: 10.1111/j.1365-2249.1995.tb03801.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Herbein G., Keshav S., Collin M., Montaner L. J., Gordon S. HIV-1 induces tumour necrosis factor and IL-1 gene expression in primary human macrophages independent of productive infection. Clin Exp Immunol. 1994 Mar;95(3):442–449. doi: 10.1111/j.1365-2249.1994.tb07016.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Ivey-Hoyle M., Culp J. S., Chaikin M. A., Hellmig B. D., Matthews T. J., Sweet R. W., Rosenberg M. Envelope glycoproteins from biologically diverse isolates of immunodeficiency viruses have widely different affinities for CD4. Proc Natl Acad Sci U S A. 1991 Jan 15;88(2):512–516. doi: 10.1073/pnas.88.2.512. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Jacobsen F. W., Rothe M., Rusten L., Goeddel D. V., Smeland E. B., Veiby O. P., Slørdal L., Jacobsen S. E. Role of the 75-kDa tumor necrosis factor receptor: inhibition of early hematopoiesis. Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10695–10699. doi: 10.1073/pnas.91.22.10695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Karsten V., Gordon S., Kirn A., Herbein G. HIV-1 envelope glycoprotein gp120 down-regulates CD4 expression in primary human macrophages through induction of endogenous tumour necrosis factor-alpha. Immunology. 1996 May;88(1):55–60. doi: 10.1046/j.1365-2567.1996.d01-648.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kikukawa R., Koyanagi Y., Harada S., Kobayashi N., Hatanaka M., Yamamoto N. Differential susceptibility to the acquired immunodeficiency syndrome retrovirus in cloned cells of human leukemic T-cell line Molt-4. J Virol. 1986 Mar;57(3):1159–1162. doi: 10.1128/jvi.57.3.1159-1162.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kornbluth R. S., Oh P. S., Munis J. R., Cleveland P. H., Richman D. D. Interferons and bacterial lipopolysaccharide protect macrophages from productive infection by human immunodeficiency virus in vitro. J Exp Med. 1989 Mar 1;169(3):1137–1151. doi: 10.1084/jem.169.3.1137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kruppa G., Thoma B., Machleidt T., Wiegmann K., Krönke M. Inhibition of tumor necrosis factor (TNF)-mediated NF-kappa B activation by selective blockade of the human 55-kDa TNF receptor. J Immunol. 1992 May 15;148(10):3152–3157. [PubMed] [Google Scholar]
  26. Lathey J. L., Kanangat S., Rouse B. T. Differential expression of tumor necrosis factor alpha and interleukin 1 beta compared with interleukin 6 in monocytes from human immunodeficiency virus-positive individuals measured by polymerase chain reaction. J Acquir Immune Defic Syndr. 1994 Feb;7(2):109–115. [PubMed] [Google Scholar]
  27. Loetscher H., Pan Y. C., Lahm H. W., Gentz R., Brockhaus M., Tabuchi H., Lesslauer W. Molecular cloning and expression of the human 55 kd tumor necrosis factor receptor. Cell. 1990 Apr 20;61(2):351–359. doi: 10.1016/0092-8674(90)90815-v. [DOI] [PubMed] [Google Scholar]
  28. Loetscher H., Stueber D., Banner D., Mackay F., Lesslauer W. Human tumor necrosis factor alpha (TNF alpha) mutants with exclusive specificity for the 55-kDa or 75-kDa TNF receptors. J Biol Chem. 1993 Dec 15;268(35):26350–26357. [PubMed] [Google Scholar]
  29. Lähdevirta J., Maury C. P., Teppo A. M., Repo H. Elevated levels of circulating cachectin/tumor necrosis factor in patients with acquired immunodeficiency syndrome. Am J Med. 1988 Sep;85(3):289–291. doi: 10.1016/0002-9343(88)90576-1. [DOI] [PubMed] [Google Scholar]
  30. Macchia D., Almerigogna F., Parronchi P., Ravina A., Maggi E., Romagnani S. Membrane tumour necrosis factor-alpha is involved in the polyclonal B-cell activation induced by HIV-infected human T cells. Nature. 1993 Jun 3;363(6428):464–466. doi: 10.1038/363464a0. [DOI] [PubMed] [Google Scholar]
  31. Mackay F., Loetscher H., Stueber D., Gehr G., Lesslauer W. Tumor necrosis factor alpha (TNF-alpha)-induced cell adhesion to human endothelial cells is under dominant control of one TNF receptor type, TNF-R55. J Exp Med. 1993 May 1;177(5):1277–1286. doi: 10.1084/jem.177.5.1277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Mellors J. W., Griffith B. P., Ortiz M. A., Landry M. L., Ryan J. L. Tumor necrosis factor-alpha/cachectin enhances human immunodeficiency virus type 1 replication in primary macrophages. J Infect Dis. 1991 Jan;163(1):78–82. doi: 10.1093/infdis/163.1.78. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. Mestan J., Digel W., Mittnacht S., Hillen H., Blohm D., Möller A., Jacobsen H., Kirchner H. Antiviral effects of recombinant tumour necrosis factor in vitro. 1986 Oct 30-Nov 5Nature. 323(6091):816–819. doi: 10.1038/323816a0. [DOI] [PubMed] [Google Scholar]
  35. Meylan P. R., Guatelli J. C., Munis J. R., Richman D. D., Kornbluth R. S. Mechanisms for the inhibition of HIV replication by interferons-alpha, -beta, and -gamma in primary human macrophages. Virology. 1993 Mar;193(1):138–148. doi: 10.1006/viro.1993.1110. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. Montaner L. J., Griffin P., Gordon S. Interleukin-10 inhibits initial reverse transcription of human immunodeficiency virus type 1 and mediates a virostatic latent state in primary blood-derived human macrophages in vitro. J Gen Virol. 1994 Dec;75(Pt 12):3393–3400. doi: 10.1099/0022-1317-75-12-3393. [DOI] [PubMed] [Google Scholar]
  38. O'Brien W. A., Namazi A., Kalhor H., Mao S. H., Zack J. A., Chen I. S. Kinetics of human immunodeficiency virus type 1 reverse transcription in blood mononuclear phagocytes are slowed by limitations of nucleotide precursors. J Virol. 1994 Feb;68(2):1258–1263. doi: 10.1128/jvi.68.2.1258-1263.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. 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]
  40. Pauwels R., Balzarini J., Baba M., Snoeck R., Schols D., Herdewijn P., Desmyter J., De Clercq E. Rapid and automated tetrazolium-based colorimetric assay for the detection of anti-HIV compounds. J Virol Methods. 1988 Aug;20(4):309–321. doi: 10.1016/0166-0934(88)90134-6. [DOI] [PubMed] [Google Scholar]
  41. Pavić I., Polić B., Crnković I., Lucin P., Jonjić S., Koszinowski U. H. Participation of endogenous tumour necrosis factor alpha in host resistance to cytomegalovirus infection. J Gen Virol. 1993 Oct;74(Pt 10):2215–2223. doi: 10.1099/0022-1317-74-10-2215. [DOI] [PubMed] [Google Scholar]
  42. Poli G., Fauci A. S. The role of monocyte/macrophages and cytokines in the pathogenesis of HIV infection. Pathobiology. 1992;60(4):246–251. doi: 10.1159/000163729. [DOI] [PubMed] [Google Scholar]
  43. Poli G., Kinter A. L., Fauci A. S. Interleukin 1 induces expression of the human immunodeficiency virus alone and in synergy with interleukin 6 in chronically infected U1 cells: inhibition of inductive effects by the interleukin 1 receptor antagonist. Proc Natl Acad Sci U S A. 1994 Jan 4;91(1):108–112. doi: 10.1073/pnas.91.1.108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. 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]
  45. Rimaniol A. C., Boussin F., Herbelin A., De Groote D., Dormont D., Bach J. F., Descamps-Latscha B., Zavala F. Induction of soluble tumor necrosis factor receptor (sTNF-R75) release by HIV adsorption on cultured human monocytes. Eur J Immunol. 1994 Sep;24(9):2055–2060. doi: 10.1002/eji.1830240918. [DOI] [PubMed] [Google Scholar]
  46. Rossol-Voth R., Rossol S., Schütt K. H., Corridori S., de Cian W., Falke D. In vivo protective effect of tumour necrosis factor alpha against experimental infection with herpes simplex virus type 1. J Gen Virol. 1991 Jan;72(Pt 1):143–147. doi: 10.1099/0022-1317-72-1-143. [DOI] [PubMed] [Google Scholar]
  47. Rothe J., Lesslauer W., Lötscher H., Lang Y., Koebel P., Köntgen F., Althage A., Zinkernagel R., Steinmetz M., Bluethmann H. Mice lacking the tumour necrosis factor receptor 1 are resistant to TNF-mediated toxicity but highly susceptible to infection by Listeria monocytogenes. Nature. 1993 Aug 26;364(6440):798–802. doi: 10.1038/364798a0. [DOI] [PubMed] [Google Scholar]
  48. Rothe J., Mackay F., Bluethmann H., Zinkernagel R., Lesslauer W. Phenotypic analysis of TNFR1-deficient mice and characterization of TNFR1-deficient fibroblasts in vitro. Circ Shock. 1994 Oct;44(2):51–56. [PubMed] [Google Scholar]
  49. Rothe M., Wong S. C., Henzel W. J., Goeddel D. V. A novel family of putative signal transducers associated with the cytoplasmic domain of the 75 kDa tumor necrosis factor receptor. Cell. 1994 Aug 26;78(4):681–692. doi: 10.1016/0092-8674(94)90532-0. [DOI] [PubMed] [Google Scholar]
  50. Sambhi S. K., Kohonen-Corish M. R., Ramshaw I. A. Local production of tumor necrosis factor encoded by recombinant vaccinia virus is effective in controlling viral replication in vivo. Proc Natl Acad Sci U S A. 1991 May 1;88(9):4025–4029. doi: 10.1073/pnas.88.9.4025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Shalaby M. R., Sundan A., Loetscher H., Brockhaus M., Lesslauer W., Espevik T. Binding and regulation of cellular functions by monoclonal antibodies against human tumor necrosis factor receptors. J Exp Med. 1990 Nov 1;172(5):1517–1520. doi: 10.1084/jem.172.5.1517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Siegel S. A., Shealy D. J., Nakada M. T., Le J., Woulfe D. S., Probert L., Kollias G., Ghrayeb J., Vilcek J., Daddona P. E. The mouse/human chimeric monoclonal antibody cA2 neutralizes TNF in vitro and protects transgenic mice from cachexia and TNF lethality in vivo. Cytokine. 1995 Jan;7(1):15–25. doi: 10.1006/cyto.1995.1003. [DOI] [PubMed] [Google Scholar]
  53. Simmonds P., Balfe P., Peutherer J. F., Ludlam C. A., Bishop J. O., Brown A. J. Human immunodeficiency virus-infected individuals contain provirus in small numbers of peripheral mononuclear cells and at low copy numbers. J Virol. 1990 Feb;64(2):864–872. doi: 10.1128/jvi.64.2.864-872.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Srivastava K. K., Fernandez-Larsson R., Zinkus D. M., Robinson H. L. Human immunodeficiency virus type 1 NL4-3 replication in four T-cell lines: rate and efficiency of entry, a major determinant of permissiveness. J Virol. 1991 Jul;65(7):3900–3902. doi: 10.1128/jvi.65.7.3900-3902.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Tartaglia L. A., Goeddel D. V., Reynolds C., Figari I. S., Weber R. F., Fendly B. M., Palladino M. A., Jr Stimulation of human T-cell proliferation by specific activation of the 75-kDa tumor necrosis factor receptor. J Immunol. 1993 Nov 1;151(9):4637–4641. [PubMed] [Google Scholar]
  56. Tartaglia L. A., Goeddel D. V. Two TNF receptors. Immunol Today. 1992 May;13(5):151–153. doi: 10.1016/0167-5699(92)90116-O. [DOI] [PubMed] [Google Scholar]
  57. Tartaglia L. A., Weber R. F., Figari I. S., Reynolds C., Palladino M. A., Jr, Goeddel D. V. The two different receptors for tumor necrosis factor mediate distinct cellular responses. Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):9292–9296. doi: 10.1073/pnas.88.20.9292. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Titus R. G., Sherry B., Cerami A. Tumor necrosis factor plays a protective role in experimental murine cutaneous leishmaniasis. J Exp Med. 1989 Dec 1;170(6):2097–2104. doi: 10.1084/jem.170.6.2097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Vandenabeele P., Declercq W., Vercammen D., Van de Craen M., Grooten J., Loetscher H., Brockhaus M., Lesslauer W., Fiers W. Functional characterization of the human tumor necrosis factor receptor p75 in a transfected rat/mouse T cell hybridoma. J Exp Med. 1992 Oct 1;176(4):1015–1024. doi: 10.1084/jem.176.4.1015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Vieillard V., Lauret E., Rousseau V., De Maeyer E. Blocking of retroviral infection at a step prior to reverse transcription in cells transformed to constitutively express interferon beta. Proc Natl Acad Sci U S A. 1994 Mar 29;91(7):2689–2693. doi: 10.1073/pnas.91.7.2689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Wong G. H., Goeddel D. V. Tumour necrosis factors alpha and beta inhibit virus replication and synergize with interferons. 1986 Oct 30-Nov 5Nature. 323(6091):819–822. doi: 10.1038/323819a0. [DOI] [PubMed] [Google Scholar]
  62. Wong G. H., Krowka J. F., Stites D. P., Goeddel D. V. In vitro anti-human immunodeficiency virus activities of tumor necrosis factor-alpha and interferon-gamma. J Immunol. 1988 Jan 1;140(1):120–124. [PubMed] [Google Scholar]
  63. Wong G. H., Tartaglia L. A., Lee M. S., Goeddel D. V. Antiviral activity of tumor necrosis factor is signaled through the 55-kDa type I TNF receptor [corrected]. J Immunol. 1992 Nov 15;149(10):3350–3353. [PubMed] [Google Scholar]

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