Home LiteratureArticle Details
PMID: 1548758 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Induction of interleukin-1 and tumor necrosis factor alpha in brain cultures by human immunodeficiency virus type 1.

Journal of virology ·Vol. 66 ·No. 4 ·1992-04-00 ·Pages 2217-25

Merrill JE, Koyanagi Y, Zack J, Thomas L, Martin F, Chen IS

Abstract

Cytokines such as interleukin-1 (IL-1) and tumor necrosis factor alpha (TNF alpha) are produced by leukocytes and play a role in immune responses. They also function in normal brain physiology as well as in pathological conditions within the central nervous system, where they are produced by brain macrophages (microglia) and brain astrocytes. In this study, we document the ability of human immunodeficiency virus type 1 (HIV-1) to induce TNF alpha and IL-1 in primary rat brain cultures. While productive infection did not occur in these cells, it was not required for cytokine induction. Using monocyte/macrophage-tropic (JRFL) and T-cell-tropic (IIIB) strains of HIV-1, we were able to induce cytokines in both microglia and astrocytes. In addition to whole virus, recombinant envelope proteins also induced these cytokines. The induction of IL-1 and TNF alpha could be blocked by a panel of antibodies recognizing epitopes in the gp120 and gp41 areas of the envelope. Soluble recombinant CD4 did not block TNF alpha and IL-1 production. If TNF alpha and IL-1 can be induced in brain tissue by HIV-1, they may contribute to some of the neurologic disorders associated with AIDS.

MeSH Terms
Animals Brain/immunology,microbiology Cells, Cultured HIV-1/immunology Interleukin-1/biosynthesis Kinetics Polymerase Chain Reaction Rats Tumor Necrosis Factor-alpha/biosynthesis Virus Replication
Chemicals
Interleukin-1 Tumor Necrosis Factor-alpha
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Merrill J E
Department of Neurology, Reed Neurological Research Center, UCLA School of Medicine 90024-1678.
Koyanagi Y
Zack J
Thomas L
Martin F
Chen I S
References (60)
60 references, click to expand
  1. Detection of AIDS virus in macrophages in brain tissue from AIDS patients with encephalopathy.
    Science. 1986 Sep 5;233(4768):1089-93 PMID: 3016903
  2. Generation of human monoclonal antibodies to human immunodeficiency virus.
    Proc Natl Acad Sci U S A. 1989 Mar;86(5):1624-8 PMID: 2922401
  3. Neurologic manifestations of infection with human immunodeficiency virus. Clinical features and pathogenesis.
    Ann Intern Med. 1987 Sep;107(3):383-91 PMID: 3039890
  4. The T4 gene encodes the AIDS virus receptor and is expressed in the immune system and the brain.
    Cell. 1986 Nov 7;47(3):333-48 PMID: 3094962
  5. The cellular receptor (CD4) of the human immunodeficiency virus is expressed on neurons and glial cells in human brain.
    J Exp Med. 1987 Apr 1;165(4):1230-5 PMID: 3104529
  6. Antigen presentation and tumor cytotoxicity by interferon-gamma-treated microglial cells.
    Eur J Immunol. 1987 Sep;17(9):1271-8 PMID: 3115791
  7. Tumor necrosis factor (cachectin) as an essential mediator in murine cerebral malaria.
    Science. 1987 Sep 4;237(4819):1210-2 PMID: 3306918
  8. Human immunodeficiency virus can productively infect cultured human glial cells.
    Proc Natl Acad Sci U S A. 1987 May;84(10):3526-30 PMID: 3472222
  9. Humoral immune response to the entire human immunodeficiency virus envelope glycoprotein made in insect cells.
    Proc Natl Acad Sci U S A. 1987 Oct;84(19):6924-8 PMID: 3477816
  10. Interleukin 1 of the central nervous system is produced by ameboid microglia.
    J Exp Med. 1986 Aug 1;164(2):594-604 PMID: 3487617
  11. Infection of brain-derived cells with the human immunodeficiency virus.
    J Virol. 1987 Apr;61(4):1244-7 PMID: 3644020
  12. Dual infection of the central nervous system by AIDS viruses with distinct cellular tropisms.
    Science. 1987 May 15;236(4803):819-22 PMID: 3646751
  13. T4 positive human neoplastic cell lines susceptible to and permissive for HTLV-III.
    Lancet. 1984 Dec 22;2(8417-8418):1472-3 PMID: 6151082
  14. A rapid biologic assay for the detection of interleukin 1.
    J Immunol. 1983 Sep;131(3):1280-2 PMID: 6411811
  15. T cell growth factor: parameters of production and a quantitative microassay for activity.
    J Immunol. 1978 Jun;120(6):2027-32 PMID: 307029
  16. Human microglial cells: characterization in cerebral tissue and in primary culture, and study of their susceptibility to HIV-1 infection.
    Ann Neurol. 1991 Feb;29(2):152-61 PMID: 1707249
  17. Natural and induced cytotoxicity of oligodendrocytes by microglia is inhibitable by TGF beta.
    Glia. 1991;4(3):327-31 PMID: 1832660
  18. Macrophage and T cell-line tropisms of HIV-1 are determined by specific regions of the envelope gp120 gene.
    Nature. 1991 Jan 10;349(6305):167-9 PMID: 1986308
  19. AIDS pathogenesis: HIV envelope and its interaction with cell proteins.
    Immunol Today. 1990 Nov;11(11):418-25 PMID: 2078296
  20. Interleukin 6 induces human immunodeficiency virus expression in infected monocytic cells alone and in synergy with tumor necrosis factor alpha by transcriptional and post-transcriptional mechanisms.
    J Exp Med. 1990 Jul 1;172(1):151-8 PMID: 2193094
  21. Failure of human immunodeficiency virus entry and infection in CD4-positive human brain and skin cells.
    J Virol. 1990 Jan;64(1):215-21 PMID: 2293663
  22. HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure.
    Cell. 1990 Apr 20;61(2):213-22 PMID: 2331748
  23. Modulation of CD4 antigen on macrophages and microglia in rat brain.
    J Exp Med. 1987 Oct 1;166(4):1138-43 PMID: 2443599
  24. Characteristics of a neutralizing monoclonal antibody to the HIV envelope glycoprotein.
    AIDS Res Hum Retroviruses. 1988 Jun;4(3):187-97 PMID: 2456088
  25. Production of tumor necrosis factor and other cytokines by astrocytes stimulated with lipopolysaccharide or a neurotropic virus.
    Proc Natl Acad Sci U S A. 1989 Aug;86(16):6348-52 PMID: 2474832
  26. Tumor necrosis factor-alpha enhances interferon-gamma-mediated class II antigen expression on astrocytes.
    J Neuroimmunol. 1989 Dec;25(2-3):209-19 PMID: 2555395
  27. Nucleotide sequence and expression of an AIDS-associated retrovirus (ARV-2).
    Science. 1985 Feb 1;227(4686):484-92 PMID: 2578227
  28. Interleukin-1 stimulates the secretion of hypothalamic corticotropin-releasing factor.
    Science. 1987 Oct 23;238(4826):522-4 PMID: 2821621
  29. Characterization of murine monoclonal antibodies to HIV-1 induced by synthetic peptides.
    AIDS Res Hum Retroviruses. 1988 Oct;4(5):331-42 PMID: 2848556
  30. Visualization and characterization of interleukin 1 receptors in brain.
    J Immunol. 1987 Jul 15;139(2):459-63 PMID: 2955042
  31. HTLV-III infection of EBV-genome-positive B-lymphoid cells with or without detectable T4 antigens.
    Int J Cancer. 1987 Feb 15;39(2):198-202 PMID: 3026971
  32. Immunoregulatory molecules and IL 2 receptors identified in multiple sclerosis brain.
    J Immunol. 1986 May 1;136(9):3239-45 PMID: 3082983
  33. Peptide and nucleotide sequences of rat CD4 (W3/25) antigen: evidence for derivation from a structure with four immunoglobulin-related domains.
    Proc Natl Acad Sci U S A. 1987 Mar;84(6):1649-53 PMID: 3104900
  34. IL-1 and IFN-gamma increase vascular permeability.
    Immunology. 1988 Jun;64(2):301-5 PMID: 3134297
  35. Interleukin-1 regulates synthesis of nerve growth factor in non-neuronal cells of rat sciatic nerve.
    Nature. 1987 Dec 17-23;330(6149):658-9 PMID: 3317065
  36. Tumor necrosis factor (cachectin) is an endogenous pyrogen and induces production of interleukin 1.
    J Exp Med. 1986 Jun 1;163(6):1433-50 PMID: 3486936
  37. Interleukin 1 and interleukin 2 enhance proopiomelanocortin gene expression in pituitary cells.
    J Immunol. 1987 Nov 15;139(10):3181-3 PMID: 3500206
  38. Human tumor necrosis factor. Production, purification, and characterization.
    J Biol Chem. 1985 Feb 25;260(4):2345-54 PMID: 3871770
  39. Isolation of lymphocytopathic retroviruses from San Francisco patients with AIDS.
    Science. 1984 Aug 24;225(4664):840-2 PMID: 6206563
  40. Proliferation of astroglia and oligodendroglia in response to human T cell-derived factors.
    Science. 1984 Jun 29;224(4656):1428-30 PMID: 6610212
  41. LFA-3, CD44, and CD45: physiologic triggers of human monocyte TNF and IL-1 release.
    Science. 1990 Sep 14;249(4974):1295-7 PMID: 1697984
  42. Effects of interleukin-1 and tumor necrosis factor-alpha on astrocytes, microglia, oligodendrocytes, and glial precursors in vitro.
    Dev Neurosci. 1991;13(3):130-7 PMID: 1752215
  43. Inhibition of entry of HIV-1 in neural cell lines by antibodies against galactosyl ceramide.
    Science. 1991 Jul 19;253(5017):320-3 PMID: 1857969
  44. Identification of the envelope V3 loop as the primary determinant of cell tropism in HIV-1.
    Science. 1991 Jul 5;253(5015):71-4 PMID: 1905842
  45. Identification of a determinant within the human immunodeficiency virus 1 surface envelope glycoprotein critical for productive infection of primary monocytes.
    Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3097-101 PMID: 2014229
  46. HIV-1 tropism for mononuclear phagocytes can be determined by regions of gp120 outside the CD4-binding domain.
    Nature. 1990 Nov 1;348(6296):69-73 PMID: 2172833
  47. Specific tropism of HIV-1 for microglial cells in primary human brain cultures.
    Science. 1990 Aug 3;249(4968):549-53 PMID: 2200125
  48. Dissociation of gp120 from HIV-1 virions induced by soluble CD4.
    Science. 1990 Nov 23;250(4984):1139-42 PMID: 2251501
  49. HIV-1 coat protein neurotoxicity prevented by calcium channel antagonists.
    Science. 1990 Apr 20;248(4953):364-7 PMID: 2326646
  50. Conserved sequence and structural elements in the HIV-1 principal neutralizing determinant.
    Science. 1990 Aug 24;249(4971):932-5 PMID: 2392685
  51. Monoclonal antibodies to gp110 and gp41 of human immunodeficiency virus.
    J Clin Microbiol. 1987 May;25(5):845-8 PMID: 2438302
  52. Characterization of a human immunodeficiency virus neutralizing monoclonal antibody and mapping of the neutralizing epitope.
    J Virol. 1988 Jun;62(6):2107-14 PMID: 2452899
  53. Interleukin-1 injected into mammalian brain stimulates astrogliosis and neovascularization.
    J Neurosci. 1988 Jul;8(7):2485-90 PMID: 2470873
  54. Soluble CD4 blocks the infectivity of diverse strains of HIV and SIV for T cells and monocytes but not for brain and muscle cells.
    Nature. 1989 Jan 26;337(6205):368-70 PMID: 2536142
  55. In vitro study of mediators of inflammation in multiple sclerosis.
    J Clin Immunol. 1989 Mar;9(2):84-96 PMID: 2541163
  56. Tumor necrosis factor stimulates transcription of HIV-1 in human T lymphocytes, independently and synergistically with mitogens.
    J Immunol. 1989 Dec 15;143(12):3956-60 PMID: 2574206
  57. Complete nucleotide sequence of the AIDS virus, HTLV-III.
    Nature. 1985 Jan 24-30;313(6000):277-84 PMID: 2578615
  58. 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):4404-8 PMID: 2789293
  59. Neuronal cell killing by the envelope protein of HIV and its prevention by vasoactive intestinal peptide.
    Nature. 1988 Oct 13;335(6191):639-42 PMID: 2845276
  60. Cellular localization of human immunodeficiency virus infection within the brains of acquired immune deficiency syndrome patients.
    Proc Natl Acad Sci U S A. 1986 Sep;83(18):7089-93 PMID: 3018755
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1992-04-00
Pages
2217-25
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC289014
Subset
IM
Grants
NIAID NIH HHS · AI 30898 · United States
NINDS NIH HHS · NS 25508 · United States
NINDS NIH HHS · R0-1 NS26983 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com