Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1997 Oct;71(10):7488–7497. doi: 10.1128/jvi.71.10.7488-7497.1997

Caprine arthritis encephalitis virus dysregulates the expression of cytokines in macrophages.

F Lechner 1, J Machado 1, G Bertoni 1, H F Seow 1, D A Dobbelaere 1, E Peterhans 1
PMCID: PMC192095  PMID: 9311828

Abstract

Caprine arthritis encephalitis virus (CAEV) is a lentivirus of goats that leads to chronic mononuclear infiltration of various tissues, in particular, the radiocarpal joints. Cells of the monocyte/macrophage lineage are the major host cells of CAEV in vivo. We have shown that infection of cultured goat macrophages with CAEV results in an alteration of cytokine expression in vitro. Constitutive expression of interleukin 8 (IL-8) and monocyte chemoattractant protein 1 (MCP-1) was increased in infected macrophages, whereas transforming growth factor beta1 (TGF-beta1) mRNA was down-regulated. When macrophages were infected with a CAEV clone lacking the trans-acting nuclear regulatory gene tat, IL-8 and MCP-1 were also increased. No significant differences from cells infected with the wild-type clone were observed, suggesting that Tat is not required for the increased expression of IL-8 and MCP-1 in infected macrophages. Furthermore, infection with CAEV led to an altered pattern of cytokine expression in response to lipopolysaccharide (LPS), heat-killed Listeria monocytogenes plus gamma interferon, or fixed cells of Staphylococcus aureus Cowan I. In infected macrophages, tumor necrosis factor alpha, IL-1beta, IL-6, and IL-12 p40 mRNA expression was reduced in response to all stimuli tested whereas changes in expression of granulocyte-macrophage colony-stimulating factor depended on the stimulating agent. Electrophoretic mobility shift assays demonstrated that, in contrast to effects of human immunodeficiency virus infection of macrophages, CAEV infection had no effect on the level of constitutive nuclear factor-kappaB (NF-kappaB) activity or on the level of LPS-stimulated NF-kappaB activity, suggesting that NF-kappaB is not involved in altered regulation of cytokine expression in CAEV-infected cells. In contrast, activator protein 1 (AP-1) binding activity was decreased in infected macrophages. These data show that CAEV infection may result in a dysregulation of expression of cytokines in macrophages. This finding suggests that CAEV may modulate the accessory functions of infected macrophages and the antiviral immune response in vivo.

Full Text

The Full Text of this article is available as a PDF (719.1 KB).

Selected References

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

  1. Adams D. S., Crawford T. B., Klevjer-Anderson P. A pathogenetic study of the early connective tissue lesions of viral caprine arthritis-encephalitis. Am J Pathol. 1980 May;99(2):257–278. [PMC free article] [PubMed] [Google Scholar]
  2. Adams D. S., Klevjer-Anderson P., Carlson J. L., McGuire T. C., Gorham J. R. Transmission and control of caprine arthritis-encephalitis virus. Am J Vet Res. 1983 Sep;44(9):1670–1675. [PubMed] [Google Scholar]
  3. Adams D. S., Oliver R. E., Ameghino E., DeMartini J. C., Verwoerd D. W., Houwers D. J., Waghela S., Gorham J. R., Hyllseth B., Dawson M. Global survey of serological evidence of caprine arthritis-encephalitis virus infection. Vet Rec. 1984 Nov 10;115(19):493–495. doi: 10.1136/vr.115.19.493. [DOI] [PubMed] [Google Scholar]
  4. Anderson L. W., Klevjer-Anderson P., Liggitt H. D. Susceptibility of blood-derived monocytes and macrophages to caprine arthritis-encephalitis virus. Infect Immun. 1983 Aug;41(2):837–840. doi: 10.1128/iai.41.2.837-840.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Baba M., Imai T., Yoshida T., Yoshie O. Constitutive expression of various chemokine genes in human T-cell lines infected with human T-cell leukemia virus type 1: role of the viral transactivator Tax. Int J Cancer. 1996 Mar 28;66(1):124–129. doi: 10.1002/(SICI)1097-0215(19960328)66:1<124::AID-IJC21>3.0.CO;2-C. [DOI] [PubMed] [Google Scholar]
  6. Baggiolini M., Dewald B., Moser B. Interleukin-8 and related chemotactic cytokines--CXC and CC chemokines. Adv Immunol. 1994;55:97–179. [PubMed] [Google Scholar]
  7. Biswas D. K., Salas T. R., Wang F., Ahlers C. M., Dezube B. J., Pardee A. B. A Tat-induced auto-up-regulatory loop for superactivation of the human immunodeficiency virus type 1 promoter. J Virol. 1995 Dec;69(12):7437–7444. doi: 10.1128/jvi.69.12.7437-7444.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brennan F. M., Feldmann M. Cytokines in autoimmunity. Curr Opin Immunol. 1996 Dec;8(6):872–877. doi: 10.1016/s0952-7915(96)80018-5. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Campbell I. K., Piccoli D. S., Roberts M. J., Muirden K. D., Hamilton J. A. Effects of tumor necrosis factor alpha and beta on resorption of human articular cartilage and production of plasminogen activator by human articular chondrocytes. Arthritis Rheum. 1990 Apr;33(4):542–552. doi: 10.1002/art.1780330412. [DOI] [PubMed] [Google Scholar]
  11. Carr M. W., Roth S. J., Luther E., Rose S. S., Springer T. A. Monocyte chemoattractant protein 1 acts as a T-lymphocyte chemoattractant. Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3652–3656. doi: 10.1073/pnas.91.9.3652. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Carruth L. M., Morse B. A., Clements J. E. The leucine domain of the visna virus Tat protein mediates targeting to an AP-1 site in the viral long terminal repeat. J Virol. 1996 Jul;70(7):4338–4344. doi: 10.1128/jvi.70.7.4338-4344.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cheevers W. P., McGuire T. C. The lentiviruses: maedi/visna, caprine arthritis-encephalitis, and equine infectious anemia. Adv Virus Res. 1988;34:189–215. doi: 10.1016/s0065-3527(08)60518-7. [DOI] [PubMed] [Google Scholar]
  14. Chehimi J., Starr S. E., Frank I., D'Andrea A., Ma X., MacGregor R. R., Sennelier J., Trinchieri G. Impaired interleukin 12 production in human immunodeficiency virus-infected patients. J Exp Med. 1994 Apr 1;179(4):1361–1366. doi: 10.1084/jem.179.4.1361. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Chensue S. W., Warmington K. S., Ruth J. H., Sanghi P. S., Lincoln P., Kunkel S. L. Role of monocyte chemoattractant protein-1 (MCP-1) in Th1 (mycobacterial) and Th2 (schistosomal) antigen-induced granuloma formation: relationship to local inflammation, Th cell expression, and IL-12 production. J Immunol. 1996 Nov 15;157(10):4602–4608. [PubMed] [Google Scholar]
  16. Chougnet C., Wynn T. A., Clerici M., Landay A. L., Kessler H. A., Rusnak J., Melcher G. P., Sher A., Shearer G. M. Molecular analysis of decreased interleukin-12 production in persons infected with human immunodeficiency virus. J Infect Dis. 1996 Jul;174(1):46–53. doi: 10.1093/infdis/174.1.46. [DOI] [PubMed] [Google Scholar]
  17. Clerici M., Lucey D. R., Berzofsky J. A., Pinto L. A., Wynn T. A., Blatt S. P., Dolan M. J., Hendrix C. W., Wolf S. F., Shearer G. M. Restoration of HIV-specific cell-mediated immune responses by interleukin-12 in vitro. Science. 1993 Dec 10;262(5140):1721–1724. doi: 10.1126/science.7903123. [DOI] [PubMed] [Google Scholar]
  18. Conant K., Ma M., Nath A., Major E. O. Extracellular human immunodeficiency virus type 1 Tat protein is associated with an increase in both NF-kappa B binding and protein kinase C activity in primary human astrocytes. J Virol. 1996 Mar;70(3):1384–1389. doi: 10.1128/jvi.70.3.1384-1389.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Cork L. C., Hadlow W. J., Crawford T. B., Gorham J. R., Piper R. C. Infectious leukoencephalomyelitis of young goats. J Infect Dis. 1974 Feb;129(2):134–141. doi: 10.1093/infdis/129.2.134. [DOI] [PubMed] [Google Scholar]
  20. Cork L. C., Narayan O. The pathogenesis of viral leukoencephalomyelitis-arthritis of goats. I. Persistent viral infection with progressive pathologic changes. Lab Invest. 1980 Jun;42(6):596–602. [PubMed] [Google Scholar]
  21. Crawford T. B., Adams D. S. Caprine arthritis-encephalitis: clinical features and presence of antibody in selected goat populations. J Am Vet Med Assoc. 1981 Apr 1;178(7):713–719. [PubMed] [Google Scholar]
  22. Crawford T. B., Adams D. S., Cheevers W. P., Cork L. C. Chronic arthritis in goats caused by a retrovirus. Science. 1980 Feb 29;207(4434):997–999. doi: 10.1126/science.6153243. [DOI] [PubMed] [Google Scholar]
  23. Crawford T. B., Adams D. S., Sande R. D., Gorham J. R., Henson J. B. The connective tissue component of the caprine arthritis-encephalitis syndrome. Am J Pathol. 1980 Aug;100(2):443–454. [PMC free article] [PubMed] [Google Scholar]
  24. Demarchi F., d'Adda di Fagagna F., Falaschi A., Giacca M. Activation of transcription factor NF-kappaB by the Tat protein of human immunodeficiency virus type 1. J Virol. 1996 Jul;70(7):4427–4437. doi: 10.1128/jvi.70.7.4427-4437.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Elliott M. J., Maini R. N., Feldmann M., Kalden J. R., Antoni C., Smolen J. S., Leeb B., Breedveld F. C., Macfarlane J. D., Bijl H. Randomised double-blind comparison of chimeric monoclonal antibody to tumour necrosis factor alpha (cA2) versus placebo in rheumatoid arthritis. Lancet. 1994 Oct 22;344(8930):1105–1110. doi: 10.1016/s0140-6736(94)90628-9. [DOI] [PubMed] [Google Scholar]
  26. Esser R., Glienke W., von Briesen H., Rübsamen-Waigmann H., Andreesen R. Differential regulation of proinflammatory and hematopoietic cytokines in human macrophages after infection with human immunodeficiency virus. Blood. 1996 Nov 1;88(9):3474–3481. [PubMed] [Google Scholar]
  27. Feldmann M., Brennan F. M., Maini R. N. Role of cytokines in rheumatoid arthritis. Annu Rev Immunol. 1996;14:397–440. doi: 10.1146/annurev.immunol.14.1.397. [DOI] [PubMed] [Google Scholar]
  28. Gdovin S. L., Clements J. E. Molecular mechanisms of visna virus Tat: identification of the targets for transcriptional activation and evidence for a post-transcriptional effect. Virology. 1992 Jun;188(2):438–450. doi: 10.1016/0042-6822(92)90497-d. [DOI] [PubMed] [Google Scholar]
  29. Gendelman H. E., Narayan O., Kennedy-Stoskopf S., Kennedy P. G., Ghotbi Z., Clements J. E., Stanley J., Pezeshkpour G. Tropism of sheep lentiviruses for monocytes: susceptibility to infection and virus gene expression increase during maturation of monocytes to macrophages. J Virol. 1986 Apr;58(1):67–74. doi: 10.1128/jvi.58.1.67-74.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Gesser B., Lund M., Lohse N., Vestergaad C., Matsushima K., Sindet-Pedersen S., Jensen S. L., Thestrup-Pedersen K., Larsen C. G. IL-8 induces T cell chemotaxis, suppresses IL-4, and up-regulates IL-8 production by CD4+ T cells. J Leukoc Biol. 1996 Mar;59(3):407–411. doi: 10.1002/jlb.59.3.407. [DOI] [PubMed] [Google Scholar]
  31. Graber H. U., Meyer R. K., Fatzer R., Vandevelde M., Zurbriggen A. In situ hybridization and immunohistochemistry for prion protein (PrP) in bovine spongiform encephalopathy (BSE). Zentralbl Veterinarmed A. 1995 Sep;42(7):453–459. doi: 10.1111/j.1439-0442.1995.tb00399.x. [DOI] [PubMed] [Google Scholar]
  32. Haase A. T., Stowring L., Harris J. D., Traynor B., Ventura P., Peluso R., Brahic M. Visna DNA synthesis and the tempo of infection in vitro. Virology. 1982 Jun;119(2):399–410. doi: 10.1016/0042-6822(82)90099-x. [DOI] [PubMed] [Google Scholar]
  33. Harmache A., Vitu C., Russo P., Bouyac M., Hieblot C., Peveri P., Vigne R., Suzan M. The caprine arthritis encephalitis virus tat gene is dispensable for efficient viral replication in vitro and in vivo. J Virol. 1995 Sep;69(9):5445–5454. doi: 10.1128/jvi.69.9.5445-5454.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Jiang Y., Beller D. I., Frendl G., Graves D. T. Monocyte chemoattractant protein-1 regulates adhesion molecule expression and cytokine production in human monocytes. J Immunol. 1992 Apr 15;148(8):2423–2428. [PubMed] [Google Scholar]
  35. Johnson G. C., Adams D. S., McGuire T. C. Pronounced production of polyclonal immunoglobulin G1 in the synovial fluid of goats with caprine arthritis-encephalitis virus infection. Infect Immun. 1983 Aug;41(2):805–815. doi: 10.1128/iai.41.2.805-815.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Kalden J. R., Gay S. Retroviruses and autoimmune rheumatic diseases. Clin Exp Immunol. 1994 Oct;98(1):1–5. doi: 10.1111/j.1365-2249.1994.tb06597.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Knowles D., Jr, Cheevers W., McGuire T., Stem T., Gorham J. Severity of arthritis is predicted by antibody response to gp135 in chronic infection with caprine arthritis-encephalitis virus. J Virol. 1990 May;64(5):2396–2398. doi: 10.1128/jvi.64.5.2396-2398.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Lawrence D. A. Transforming growth factor-beta: a general review. Eur Cytokine Netw. 1996 Sep;7(3):363–374. [PubMed] [Google Scholar]
  39. Lechner F., Vogt H. R., Seow H. F., von Bodungen U., Bertoni G., Zurbriggen A., Peterhans E. Expression of TNF alpha in arthritis caused by caprine arthritis encephalitis virus. Vet Immunol Immunopathol. 1996 Nov;54(1-4):281–289. doi: 10.1016/s0165-2427(96)05701-7. [DOI] [PubMed] [Google Scholar]
  40. Legastelois I., Cordier G., Cozon G., Cadoré J. L., Guiguen F., Greenland T., Mornex J. F. Visna-maedi virus-induced expression of interleukin-8 gene in sheep alveolar cells following experimental in vitro and in vivo infection. Res Virol. 1996 Mar-Jun;147(2-3):191–197. doi: 10.1016/0923-2516(96)80234-2. [DOI] [PubMed] [Google Scholar]
  41. Lotz M., Clark-Lewis I., Ganu V. HIV-1 transactivator protein Tat induces proliferation and TGF beta expression in human articular chondrocytes. J Cell Biol. 1994 Feb;124(3):365–371. doi: 10.1083/jcb.124.3.365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Mager W. H., De Kruijff A. J. Stress-induced transcriptional activation. Microbiol Rev. 1995 Sep;59(3):506–531. doi: 10.1128/mr.59.3.506-531.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Mahé Y., Mukaida N., Kuno K., Akiyama M., Ikeda N., Matsushima K., Murakami S. Hepatitis B virus X protein transactivates human interleukin-8 gene through acting on nuclear factor kB and CCAAT/enhancer-binding protein-like cis-elements. J Biol Chem. 1991 Jul 25;266(21):13759–13763. [PubMed] [Google Scholar]
  44. Mastronarde J. G., He B., Monick M. M., Mukaida N., Matsushima K., Hunninghake G. W. Induction of interleukin (IL)-8 gene expression by respiratory syncytial virus involves activation of nuclear factor (NF)-kappa B and NF-IL-6. J Infect Dis. 1996 Aug;174(2):262–267. doi: 10.1093/infdis/174.2.262. [DOI] [PubMed] [Google Scholar]
  45. McElhinny J. A., MacMorran W. S., Bren G. D., Ten R. M., Israel A., Paya C. V. Regulation of I kappa B alpha and p105 in monocytes and macrophages persistently infected with human immunodeficiency virus. J Virol. 1995 Mar;69(3):1500–1509. doi: 10.1128/jvi.69.3.1500-1509.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Moreland L. W., Koopman W. J. Infection as a cause of arthritis. Curr Opin Rheumatol. 1991 Aug;3(4):639–649. doi: 10.1097/00002281-199108000-00015. [DOI] [PubMed] [Google Scholar]
  47. Mori N., Murakami S., Oda S., Prager D., Eto S. Production of interleukin 8 in adult T-cell leukemia cells: possible transactivation of the interleukin 8 gene by human T-cell leukemia virus type I tax. Cancer Res. 1995 Aug 15;55(16):3592–3597. [PubMed] [Google Scholar]
  48. Narayan O., Clements J. E. Biology and pathogenesis of lentiviruses. J Gen Virol. 1989 Jul;70(Pt 7):1617–1639. doi: 10.1099/0022-1317-70-7-1617. [DOI] [PubMed] [Google Scholar]
  49. Narayan O., Wolinsky J. S., Clements J. E., Strandberg J. D., Griffin D. E., Cork L. C. Slow virus replication: the role of macrophages in the persistence and expression of visna viruses of sheep and goats. J Gen Virol. 1982 Apr;59(Pt 2):345–356. doi: 10.1099/0022-1317-59-2-345. [DOI] [PubMed] [Google Scholar]
  50. Neuveut C., Vigne R., Clements J. E., Sire J. The visna transcriptional activator Tat: effects on the viral LTR and on cellular genes. Virology. 1993 Nov;197(1):236–244. doi: 10.1006/viro.1993.1584. [DOI] [PubMed] [Google Scholar]
  51. Nishiura H., Tanaka J., Takeya M., Tsukano M., Kambara T., Imamura T. IL-8/NAP-1 is the major T-cell chemoattractant in synovial tissues of rheumatoid arthritis. Clin Immunol Immunopathol. 1996 Aug;80(2):179–184. doi: 10.1006/clin.1996.0112. [DOI] [PubMed] [Google Scholar]
  52. Noah T. L., Becker S. Respiratory syncytial virus-induced cytokine production by a human bronchial epithelial cell line. Am J Physiol. 1993 Nov;265(5 Pt 1):L472–L478. doi: 10.1152/ajplung.1993.265.5.L472. [DOI] [PubMed] [Google Scholar]
  53. O'Brien P. M., Rothel J. S., Seow H. F., Wood P. R. Cloning and sequencing of the cDNA for ovine granulocyte-macrophage colony-stimulating factor (GM-CSF). Immunol Cell Biol. 1991 Feb;69(Pt 1):51–55. doi: 10.1038/icb.1991.8. [DOI] [PubMed] [Google Scholar]
  54. Paya C. V., Ten R. M., Bessia C., Alcami J., Hay R. T., Virelizier J. L. NF-kappa B-dependent induction of the NF-kappa B p50 subunit gene promoter underlies self-perpetuation of human immunodeficiency virus transcription in monocytic cells. Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7826–7830. doi: 10.1073/pnas.89.16.7826. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Perry L. L., Wilkerson M. J., Hullinger G. A., Cheevers W. P. Depressed CD4+ T lymphocyte proliferative response and enhanced antibody response to viral antigen in chronic lentivirus-induced arthritis. J Infect Dis. 1995 Feb;171(2):328–334. doi: 10.1093/infdis/171.2.328. [DOI] [PubMed] [Google Scholar]
  56. Rautonen J., Rautonen N., Martin N. L., Wara D. W. HIV type 1 Tat protein induces immunoglobulin and interleukin 6 synthesis by uninfected peripheral blood mononuclear cells. AIDS Res Hum Retroviruses. 1994 Jul;10(7):781–785. doi: 10.1089/aid.1994.10.781. [DOI] [PubMed] [Google Scholar]
  57. Rollins B. J., Walz A., Baggiolini M. Recombinant human MCP-1/JE induces chemotaxis, calcium flux, and the respiratory burst in human monocytes. Blood. 1991 Aug 15;78(4):1112–1116. [PubMed] [Google Scholar]
  58. Saltarelli M. J., Schoborg R., Gdovin S. L., Clements J. E. The CAEV tat gene trans-activates the viral LTR and is necessary for efficient viral replication. Virology. 1993 Nov;197(1):35–44. doi: 10.1006/viro.1993.1564. [DOI] [PubMed] [Google Scholar]
  59. Saltarelli M., Querat G., Konings D. A., Vigne R., Clements J. E. Nucleotide sequence and transcriptional analysis of molecular clones of CAEV which generate infectious virus. Virology. 1990 Nov;179(1):347–364. doi: 10.1016/0042-6822(90)90303-9. [DOI] [PubMed] [Google Scholar]
  60. Santamaria Babi L. F., Moser B., Perez Soler M. T., Moser R., Loetscher P., Villiger B., Blaser K., Hauser C. The interleukin-8 receptor B and CXC chemokines can mediate transendothelial migration of human skin homing T cells. Eur J Immunol. 1996 Sep;26(9):2056–2061. doi: 10.1002/eji.1830260914. [DOI] [PubMed] [Google Scholar]
  61. 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]
  62. Seow H. F., Rothel J. S., David M. J., Wood P. R. Nucleotide sequence of ovine macrophage interleukin-1 beta cDNA. DNA Seq. 1991;1(6):423–426. doi: 10.3109/10425179109020802. [DOI] [PubMed] [Google Scholar]
  63. Seow H. F., Yoshimura T., Wood P. R., Colditz I. G. Cloning, sequencing, expression and inflammatory activity in skin of ovine interleukin-8. Immunol Cell Biol. 1994 Oct;72(5):398–405. doi: 10.1038/icb.1994.59. [DOI] [PubMed] [Google Scholar]
  64. Shaw G. M., Hahn B. H., Arya S. K., Groopman J. E., Gallo R. C., Wong-Staal F. Molecular characterization of human T-cell leukemia (lymphotropic) virus type III in the acquired immune deficiency syndrome. Science. 1984 Dec 7;226(4679):1165–1171. doi: 10.1126/science.6095449. [DOI] [PubMed] [Google Scholar]
  65. Stein B., Rahmsdorf H. J., Steffen A., Litfin M., Herrlich P. UV-induced DNA damage is an intermediate step in UV-induced expression of human immunodeficiency virus type 1, collagenase, c-fos, and metallothionein. Mol Cell Biol. 1989 Nov;9(11):5169–5181. doi: 10.1128/mcb.9.11.5169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Tsai W. P., Hirose K., Nara P. L., Kuang Y. D., Conley S., Li B. Q., Kung H. F., Matsushima K. Decrease in cytokine production by HIV-infected macrophages in response to LPS-mediated activation. Lymphokine Cytokine Res. 1991 Dec;10(6):421–429. [PubMed] [Google Scholar]
  67. Verheij M., Bose R., Lin X. H., Yao B., Jarvis W. D., Grant S., Birrer M. J., Szabo E., Zon L. I., Kyriakis J. M. Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature. 1996 Mar 7;380(6569):75–79. doi: 10.1038/380075a0. [DOI] [PubMed] [Google Scholar]
  68. Wang C. Y., Mayo M. W., Baldwin A. S., Jr TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NF-kappaB. Science. 1996 Nov 1;274(5288):784–787. doi: 10.1126/science.274.5288.784. [DOI] [PubMed] [Google Scholar]
  69. 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]
  70. Wilder R. L. Hypothesis for retroviral causation of rheumatoid arthritis. Curr Opin Rheumatol. 1994 May;6(3):295–299. doi: 10.1097/00002281-199405000-00009. [DOI] [PubMed] [Google Scholar]
  71. Wilkerson M. J., Davis W. C., Baszler T. V., Cheevers W. P. Immunopathology of chronic lentivirus-induced arthritis. Am J Pathol. 1995 Jun;146(6):1433–1443. [PMC free article] [PubMed] [Google Scholar]
  72. Wilkinson P. C., Newman I. Identification of IL-8 as a locomotor attractant for activated human lymphocytes in mononuclear cell cultures with anti-CD3 or purified protein derivative of Mycobacterium tuberculosis. J Immunol. 1992 Oct 15;149(8):2689–2694. [PubMed] [Google Scholar]
  73. Woodall C. J., McLaren L. J., Watt N. J. Sequence and chromosomal localisation of the gene encoding ovine latent transforming growth factor-beta 1. Gene. 1994 Dec 15;150(2):371–373. doi: 10.1016/0378-1119(94)90455-3. [DOI] [PubMed] [Google Scholar]
  74. Woodgett J. R., Avruch J., Kyriakis J. M. Regulation of nuclear transcription factors by stress signals. Clin Exp Pharmacol Physiol. 1995 Apr;22(4):281–283. doi: 10.1111/j.1440-1681.1995.tb01995.x. [DOI] [PubMed] [Google Scholar]
  75. Yoo J., Chen H., Kraus T., Hirsch D., Polyak S., George I., Sperber K. Altered cytokine production and accessory cell function after HIV-1 infection. J Immunol. 1996 Aug 1;157(3):1313–1320. [PubMed] [Google Scholar]
  76. Zauli G., Davis B. R., Re M. C., Visani G., Furlini G., La Placa M. tat protein stimulates production of transforming growth factor-beta 1 by marrow macrophages: a potential mechanism for human immunodeficiency virus-1-induced hematopoietic suppression. Blood. 1992 Dec 15;80(12):3036–3043. [PubMed] [Google Scholar]
  77. Zink M. C., Johnson L. K. Pathobiology of lentivirus infections of sheep and goats. Virus Res. 1994 May;32(2):139–154. doi: 10.1016/0168-1702(94)90039-6. [DOI] [PubMed] [Google Scholar]

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

RESOURCES