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. 1987 Sep;25(9):1695–1700. doi: 10.1128/jcm.25.9.1695-1700.1987

Idiopathic production of interleukin-1 in acquired immune deficiency syndrome.

J L Lepe-Zuniga 1, P W Mansell 1, E M Hersh 1
PMCID: PMC269310  PMID: 3498739

Abstract

We determined the capacity of peripheral blood monocytes from 19 patients with acquired immune deficiency syndrome (AIDS) or related conditions (1 with lymphadenopathy, 8 with AIDS-related complex, and 10 with AIDS) to produce intracellular and extracellular interleukin-1 (IL-1) spontaneously and upon stimulation with bacterial endotoxin. All patients were anti-human T-cell lymphotropic virus type III antibody positive. Results were compared with those obtained with 10 normal controls of similar age. A subset of patients who spontaneously produced high amounts of intracellular and extracellular IL-1 was identified. Total production of IL-1 in this subset was an average of 2.9 times that of controls. It is suggested that spontaneous production of IL-1 in this group represents an in vivo phenomenon since it was associated with more than 3 g of globulins per deciliter of serum, more than 2,300 mg of immunoglobulins per deciliter of serum, higher IgA values, higher titers of anti-Epstein-Barr virus antibodies, and lower neutrophil counts in peripheral blood. The role of Epstein-Barr virus, human immunodeficiency virus itself, or other infectious agents in spontaneous IL-1 production by these patients remains to be determined. Stimulation with endotoxin induced intracellular and extracellular IL-1 production to similar levels in patients and controls. These results show that AIDS patients are able to produce and release IL-1. High idiopathic production of IL-1 identified in some patients can help to explain the hypergammaglobulinemia seen in AIDS patients and might also be related to progression and severity of the disease.

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Selected References

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

  1. Alcocer-Varela J., Alarcon-Segovia D., Abud-Mendoza C. Immunoregulatory circuits in the acquired immune deficiency syndrome and related complex. Production of and response to interleukins 1 and 2, NK function and its enhancement by interleukin-2 and kinetics of the autologous mixed lymphocyte reaction. Clin Exp Immunol. 1985 Apr;60(1):31–38. [PMC free article] [PubMed] [Google Scholar]
  2. Auron P. E., Webb A. C., Rosenwasser L. J., Mucci S. F., Rich A., Wolff S. M., Dinarello C. A. Nucleotide sequence of human monocyte interleukin 1 precursor cDNA. Proc Natl Acad Sci U S A. 1984 Dec;81(24):7907–7911. doi: 10.1073/pnas.81.24.7907. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Belsito D. V., Sanchez M. R., Baer R. L., Valentine F., Thorbecke G. J. Reduced Langerhans' cell Ia antigen and ATPase activity in patients with the acquired immunodeficiency syndrome. N Engl J Med. 1984 May 17;310(20):1279–1282. doi: 10.1056/NEJM198405173102002. [DOI] [PubMed] [Google Scholar]
  4. Conlon P. J., Henney C. S., Gillis S. Cytokine-dependent thymocyte responses: characterization of IL 1 and IL 2 target subpopulations and mechanism of action. J Immunol. 1982 Feb;128(2):797–801. [PubMed] [Google Scholar]
  5. Dinarello C. A. An update on human interleukin-1: from molecular biology to clinical relevance. J Clin Immunol. 1985 Sep;5(5):287–297. doi: 10.1007/BF00918247. [DOI] [PubMed] [Google Scholar]
  6. Enk C., Gerstoft J., Møller S., Remvig L. Interleukin 1 activity in the acquired immunodeficiency syndrome. Scand J Immunol. 1986 Apr;23(4):491–497. doi: 10.1111/j.1365-3083.1986.tb03081.x. [DOI] [PubMed] [Google Scholar]
  7. Erb P., Feldmann M. The role of macrophages in the generation of T-helper cells. I. The requirement for macrophages in helper cell induction and characteristics of the macrophage-T cell interaction. Cell Immunol. 1975 Oct;19(2):356–367. doi: 10.1016/0008-8749(75)90217-8. [DOI] [PubMed] [Google Scholar]
  8. Falkoff R. J., Muraguchi A., Hong J. X., Butler J. L., Dinarello C. A., Fauci A. S. The effects of interleukin 1 on human B cell activation and proliferation. J Immunol. 1983 Aug;131(2):801–805. [PubMed] [Google Scholar]
  9. Gallo R. C., Salahuddin S. Z., Popovic M., Shearer G. M., Kaplan M., Haynes B. F., Palker T. J., Redfield R., Oleske J., Safai B. Frequent detection and isolation of cytopathic retroviruses (HTLV-III) from patients with AIDS and at risk for AIDS. Science. 1984 May 4;224(4648):500–503. doi: 10.1126/science.6200936. [DOI] [PubMed] [Google Scholar]
  10. Gascón P., Zoumbos N. C., Young N. S. Immunologic abnormalities in patients receiving multiple blood transfusions. Ann Intern Med. 1984 Feb;100(2):173–177. doi: 10.7326/0003-4819-100-2-173. [DOI] [PubMed] [Google Scholar]
  11. Gupta S., Gillis S., Thornton M., Goldberg M. Autologous mixed lymphocyte reaction in man. XIV. Deficiency of the autologous mixed lymphocyte reaction in acquired immune deficiency syndrome (AIDS) and AIDS related complex (ARC). In vitro effect of purified interleukin-1 and interleukin-2. Clin Exp Immunol. 1984 Nov;58(2):395–401. [PMC free article] [PubMed] [Google Scholar]
  12. Hersh E. M., Gutterman J. U., Spector S., Friedman H., Greenberg S. B., Reuben J. M., LaPushin R., Matza M., Mansell P. W. Impaired in vitro interferon, blastogenic, and natural killer cell responses to viral stimulation in acquired immune deficiency syndrome. Cancer Res. 1985 Jan;45(1):406–410. [PubMed] [Google Scholar]
  13. Hersh E. M., Mansell P. W., Reuben J. M., Rios A., Newell G. R. Immunological characterizations of patients with acquired immune deficiency syndrome, acquired immune deficiency syndrome-related symptom complex, and a related life-style. Cancer Res. 1984 Dec;44(12 Pt 1):5894–5901. [PubMed] [Google Scholar]
  14. Kaye J., Gillis S., Mizel S. B., Shevach E. M., Malek T. R., Dinarello C. A., Lachman L. B., Janeway C. A., Jr Growth of a cloned helper T cell line induced by a monoclonal antibody specific for the antigen receptor: interleukin 1 is required for the expression of receptors for interleukin 2. J Immunol. 1984 Sep;133(3):1339–1345. [PubMed] [Google Scholar]
  15. Kurt-Jones E. A., Virgin H. W., 4th, Unanue E. R. Relationship of macrophage Ia and membrane IL 1 expression to antigen presentation. J Immunol. 1985 Dec;135(6):3652–3654. [PubMed] [Google Scholar]
  16. Lane H. C., Masur H., Edgar L. C., Whalen G., Rook A. H., Fauci A. S. Abnormalities of B-cell activation and immunoregulation in patients with the acquired immunodeficiency syndrome. N Engl J Med. 1983 Aug 25;309(8):453–458. doi: 10.1056/NEJM198308253090803. [DOI] [PubMed] [Google Scholar]
  17. Lepe-Zuniga J. L., Gery I. Production of intra- and extracellular interleukin-1 (IL-1) by human monocytes. Clin Immunol Immunopathol. 1984 May;31(2):222–230. doi: 10.1016/0090-1229(84)90242-3. [DOI] [PubMed] [Google Scholar]
  18. Lepe-Zuniga J. L., Zigler J. S., Jr, Zimmerman M. L., Gery I. Differences between intra- and extracellular interleukin-1. Mol Immunol. 1985 Dec;22(12):1387–1392. doi: 10.1016/0161-5890(85)90061-6. [DOI] [PubMed] [Google Scholar]
  19. Lipsky P. E., Thompson P. A., Rosenwasser L. J., Dinarello C. A. The role of interleukin 1 in human B cell activation: inhibition of B cell proliferation and the generation of immunoglobulin-secreting cells by an antibody against human leukocytic pyrogen. J Immunol. 1983 Jun;130(6):2708–2714. [PubMed] [Google Scholar]
  20. March C. J., Mosley B., Larsen A., Cerretti D. P., Braedt G., Price V., Gillis S., Henney C. S., Kronheim S. R., Grabstein K. Cloning, sequence and expression of two distinct human interleukin-1 complementary DNAs. Nature. 1985 Jun 20;315(6021):641–647. doi: 10.1038/315641a0. [DOI] [PubMed] [Google Scholar]
  21. Mavligit G. M., Talpaz M., Hsia F. T., Wong W., Lichtiger B., Mansell P. W., Mumford D. M. Chronic immune stimulation by sperm alloantigens. Support for the hypothesis that spermatozoa induce immune dysregulation in homosexual males. JAMA. 1984 Jan 13;251(2):237–241. doi: 10.1001/jama.251.2.237. [DOI] [PubMed] [Google Scholar]
  22. Mitchell W. M., Forti R. L., Vogler L. B., Lawton A. R., Gregg C. R. Spontaneous and interferon resistant natural killer cell anergy in AIDS. AIDS Res. 1983 1984;1(3):221–229. doi: 10.1089/aid.1.1983.1.221. [DOI] [PubMed] [Google Scholar]
  23. Mizel S. B. Interleukin 1 and T cell activation. Immunol Rev. 1982;63:51–72. doi: 10.1111/j.1600-065x.1982.tb00411.x. [DOI] [PubMed] [Google Scholar]
  24. Murray H. W., Rubin B. Y., Masur H., Roberts R. B. Impaired production of lymphokines and immune (gamma) interferon in the acquired immunodeficiency syndrome. N Engl J Med. 1984 Apr 5;310(14):883–889. doi: 10.1056/NEJM198404053101404. [DOI] [PubMed] [Google Scholar]
  25. Nakagawara A., Nathan C. F. A simple method for counting adherent cells: application to cultured human monocytes, macrophages and multinucleated giant cells. J Immunol Methods. 1983 Jan 28;56(2):261–268. doi: 10.1016/0022-1759(83)90418-0. [DOI] [PubMed] [Google Scholar]
  26. Rocklin R. E., Bendtzen K., Greineder D. Mediators of immunity: lymphokines and monokines. Adv Immunol. 1980;29:55–136. doi: 10.1016/s0065-2776(08)60043-7. [DOI] [PubMed] [Google Scholar]
  27. Rosén A., Gergely P., Jondal M., Klein G., Britton S. Polyclonal Ig production after Epstein-Barr virus infection of human lymphocytes in vitro. Nature. 1977 May 5;267(5606):52–54. doi: 10.1038/267052a0. [DOI] [PubMed] [Google Scholar]
  28. Scala G., Oppenheim J. J. Antigen presentation by human monocytes: evidence for stimulant processing and requirement for interleukin 1. J Immunol. 1983 Sep;131(3):1160–1166. [PubMed] [Google Scholar]
  29. Schmidt J. A., Oliver C. N., Lepe-Zuniga J. L., Green I., Gery I. Silica-stimulated monocytes release fibroblast proliferation factors identical to interleukin 1. A potential role for interleukin 1 in the pathogenesis of silicosis. J Clin Invest. 1984 May;73(5):1462–1472. doi: 10.1172/JCI111350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Seligmann M., Chess L., Fahey J. L., Fauci A. S., Lachmann P. J., L'Age-Stehr J., Ngu J., Pinching A. J., Rosen F. S., Spira T. J. AIDS--an immunologic reevaluation. N Engl J Med. 1984 Nov 15;311(20):1286–1292. doi: 10.1056/NEJM198411153112005. [DOI] [PubMed] [Google Scholar]
  31. Sheridan J. F., Aurelian L., Donnenberg A. D., Quinn T. C. Cell-mediated immunity to cytomegalovirus (CMV) and herpes simplex virus (HSV) antigens in the acquired immune deficiency syndrome: interleukin-1 and interleukin-2 modify in vitro responses. J Clin Immunol. 1984 Jul;4(4):304–311. doi: 10.1007/BF00915298. [DOI] [PubMed] [Google Scholar]
  32. Siegal F. P. Immune function and dysfunction in AIDS. Semin Oncol. 1984 Mar;11(1):29–39. [PubMed] [Google Scholar]
  33. Smith K. A., Lachman L. B., Oppenheim J. J., Favata M. F. The functional relationship of the interleukins. J Exp Med. 1980 Jun 1;151(6):1551–1556. doi: 10.1084/jem.151.6.1551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Smith P. D., Ohura K., Masur H., Lane H. C., Fauci A. S., Wahl S. M. Monocyte function in the acquired immune deficiency syndrome. Defective chemotaxis. J Clin Invest. 1984 Dec;74(6):2121–2128. doi: 10.1172/JCI111637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Spivak J. L., Bender B. S., Quinn T. C. Hematologic abnormalities in the acquired immune deficiency syndrome. Am J Med. 1984 Aug;77(2):224–228. doi: 10.1016/0002-9343(84)90695-8. [DOI] [PubMed] [Google Scholar]
  36. Unanue E. R. Cooperation between mononuclear phagocytes and lymphocytes in immunity. N Engl J Med. 1980 Oct 23;303(17):977–985. doi: 10.1056/NEJM198010233031706. [DOI] [PubMed] [Google Scholar]

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