Skip to main content
PMC home page
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1984 Aug;74(2):496–506. doi: 10.1172/JCI111447

Functional T lymphocyte immune deficiency in a population of homosexual men who do not exhibit symptoms of acquired immune deficiency syndrome.

G M Shearer, S M Payne, L J Joseph, W E Biddison
PMCID: PMC370502  PMID: 6611354

Abstract

To determine whether healthy homosexual men are immunologically impaired, peripheral blood leukocytes (PBL) from 20 male homosexuals were compared prospectively with PBL from 14 age-matched male heterosexual donors with respect to: (a) the capacity of their PBL to generate functional T cell immune responses in vitro; and (b) the content of total T cells and T cell subsets in their peripheral blood. The homosexual donors studied indicated moderate sexual life styles in that all but one of the donors had less than five current sexual partners. The percentages of OKT3+, OKT4+, and OKT8+ T cells were similar to those of heterosexual controls. T cell function was assessed by measuring cytotoxic T cell responses to influenza virus and to allogeneic cells. Approximately one-third of the homosexual donors consistently exhibited weak cytotoxic T lymphocyte (CTL) responses to influenza virus, whereas all of the heterosexual donors generated strong CTL responses to influenza. There was no correlation between the strength of CTL responsiveness to influenza virus and the strength of CTL responses to allogeneic cells. These results suggest that the influenza-specific CTL response may be a sensitive indicator of immunologic defects in asymptomatic homosexuals. If acquired immune deficiency syndrome results from an infectious agent, it remains to be seen if such immunosuppression predisposes to the infection, or if it reflects early consequences of infection.

Full text

PDF
500

Selected References

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

  1. Ammann A. J., Cowan M. J., Wara D. W., Weintrub P., Dritz S., Goldman H., Perkins H. A. Acquired immunodeficiency in an infant: possible transmission by means of blood products. Lancet. 1983 Apr 30;1(8331):956–958. doi: 10.1016/s0140-6736(83)92082-2. [DOI] [PubMed] [Google Scholar]
  2. Andreani T., Modigliani R., le Charpentier Y., Galian A., Brouet J. C., Liance M., Lachance J. R., Messing B., Vernisse B. Acquired immunodeficiency with intestinal cryptosporidiosis: possible transmission by Haitian whole blood. Lancet. 1983 May 28;1(8335):1187–1191. doi: 10.1016/s0140-6736(83)92466-2. [DOI] [PubMed] [Google Scholar]
  3. Barré-Sinoussi F., Chermann J. C., Rey F., Nugeyre M. T., Chamaret S., Gruest J., Dauguet C., Axler-Blin C., Vézinet-Brun F., Rouzioux C. Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS). Science. 1983 May 20;220(4599):868–871. doi: 10.1126/science.6189183. [DOI] [PubMed] [Google Scholar]
  4. Biddison W. E., Payne S. M., Shearer G. M., Shaw S. Human cytotoxic T cell responses to trinitrophenyl hapten and influenza virus. Diversity of restriction antigens and specificity of HLA-linked genetic regulation. J Exp Med. 1980 Aug 1;152(2 Pt 2):204s–217s. [PubMed] [Google Scholar]
  5. Biddison W. E., Sharrow S. O., Shearer G. M. T cell subpopulations required for the human cytotoxic T lymphocyte response to influenza virus: evidence for T cell help. J Immunol. 1981 Aug;127(2):487–491. [PubMed] [Google Scholar]
  6. Biddison W. E., Shaw S., Nelson D. L. Virus specificity of human influenza virus-immune cytotoxic T cells. J Immunol. 1979 Feb;122(2):660–664. [PubMed] [Google Scholar]
  7. Biddison W. E. The role of the human major histocompatibility complex in cytotoxic T-cell responses to virus-infected cells. J Clin Immunol. 1982 Jan;2(1):1–9. doi: 10.1007/BF00915971. [DOI] [PubMed] [Google Scholar]
  8. Davis K. C., Horsburgh C. R., Jr, Hasiba U., Schocket A. L., Kirkpatrick C. H. Acquired immunodeficiency syndrome in a patient with hemophilia. Ann Intern Med. 1983 Mar;98(3):284–286. doi: 10.7326/0003-4819-98-3-284. [DOI] [PubMed] [Google Scholar]
  9. Detels R., Fahey J. L., Schwartz K., Greene R. S., Visscher B. R., Gottlieb M. S. Relation between sexual practices and T-cell subsets in homosexually active men. Lancet. 1983 Mar 19;1(8325):609–611. doi: 10.1016/s0140-6736(83)91792-0. [DOI] [PubMed] [Google Scholar]
  10. Elliott J. L., Hoppes W. L., Platt M. S., Thomas J. G., Patel I. P., Gansar A. The acquired immunodeficiency syndrome and Mycobacterium avium-intracellulare bacteremia in a patient with hemophilia. Ann Intern Med. 1983 Mar;98(3):290–293. doi: 10.7326/0003-4819-98-3-290. [DOI] [PubMed] [Google Scholar]
  11. Essex M., McLane M. F., Lee T. H., Falk L., Howe C. W., Mullins J. I., Cabradilla C., Francis D. P. Antibodies to cell membrane antigens associated with human T-cell leukemia virus in patients with AIDS. Science. 1983 May 20;220(4599):859–862. doi: 10.1126/science.6342136. [DOI] [PubMed] [Google Scholar]
  12. Fahey J. L., Detels R., Gottlieb M. Immune-cell augmentation (with altered T-subset ratio) is common in healthy homosexual men. N Engl J Med. 1983 Apr 7;308(14):842–843. doi: 10.1056/NEJM198304073081414. [DOI] [PubMed] [Google Scholar]
  13. Follansbee S. E., Busch D. F., Wofsy C. B., Coleman D. L., Gullet J., Aurigemma G. P., Ross T., Hadley W. K., Drew W. L. An outbreak of Pneumocystis carinii pneumonia in homosexual men. Ann Intern Med. 1982 Jun;96(6 Pt 1):705–713. doi: 10.7326/0003-4819-96-6-705. [DOI] [PubMed] [Google Scholar]
  14. Friedman-Kien A. E., Laubenstein L. J., Rubinstein P., Buimovici-Klein E., Marmor M., Stahl R., Spigland I., Kim K. S., Zolla-Pazner S. Disseminated Kaposi's sarcoma in homosexual men. Ann Intern Med. 1982 Jun;96(6 Pt 1):693–700. doi: 10.7326/0003-4819-96-6-693. [DOI] [PubMed] [Google Scholar]
  15. Gallo R. C., Sarin P. S., Gelmann E. P., Robert-Guroff M., Richardson E., Kalyanaraman V. S., Mann D., Sidhu G. D., Stahl R. E., Zolla-Pazner S. Isolation of human T-cell leukemia virus in acquired immune deficiency syndrome (AIDS). Science. 1983 May 20;220(4599):865–867. doi: 10.1126/science.6601823. [DOI] [PubMed] [Google Scholar]
  16. Gelmann E. P., Popovic M., Blayney D., Masur H., Sidhu G., Stahl R. E., Gallo R. C. Proviral DNA of a retrovirus, human T-cell leukemia virus, in two patients with AIDS. Science. 1983 May 20;220(4599):862–865. doi: 10.1126/science.6601822. [DOI] [PubMed] [Google Scholar]
  17. Gottlieb M. S., Schroff R., Schanker H. M., Weisman J. D., Fan P. T., Wolf R. A., Saxon A. Pneumocystis carinii pneumonia and mucosal candidiasis in previously healthy homosexual men: evidence of a new acquired cellular immunodeficiency. N Engl J Med. 1981 Dec 10;305(24):1425–1431. doi: 10.1056/NEJM198112103052401. [DOI] [PubMed] [Google Scholar]
  18. Groopman J. E., Gottlieb M. S. Kaposi's sarcoma: an oncologic looking glass. Nature. 1982 Sep 9;299(5879):103–104. doi: 10.1038/299103a0. [DOI] [PubMed] [Google Scholar]
  19. Henle W., Henle G. E., Horwitz C. A. Epstein-Barr virus specific diagnostic tests in infectious mononucleosis. Hum Pathol. 1974 Sep;5(5):551–565. doi: 10.1016/s0046-8177(74)80006-7. [DOI] [PubMed] [Google Scholar]
  20. Jaffe H. W., Choi K., Thomas P. A., Haverkos H. W., Auerbach D. M., Guinan M. E., Rogers M. F., Spira T. J., Darrow W. W., Kramer M. A. National case-control study of Kaposi's sarcoma and Pneumocystis carinii pneumonia in homosexual men: Part 1. Epidemiologic results. Ann Intern Med. 1983 Aug;99(2):145–151. doi: 10.7326/0003-4819-99-2-145. [DOI] [PubMed] [Google Scholar]
  21. Kornfeld H., Vande Stouwe R. A., Lange M., Reddy M. M., Grieco M. H. T-lymphocyte subpopulations in homosexual men. N Engl J Med. 1982 Sep 16;307(12):729–731. doi: 10.1056/NEJM198209163071206. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Lederman M. M., Ratnoff O. D., Scillian J. J., Jones P. K., Schacter B. Impaired cell-mediated immunity in patients with classic hemophilia. N Engl J Med. 1983 Jan 13;308(2):79–83. doi: 10.1056/NEJM198301133080205. [DOI] [PubMed] [Google Scholar]
  24. Levy J. A., Ziegler J. L. Acquired immunodeficiency syndrome is an opportunistic infection and Kaposi's sarcoma results from secondary immune stimulation. Lancet. 1983 Jul 9;2(8341):78–81. doi: 10.1016/s0140-6736(83)90062-4. [DOI] [PubMed] [Google Scholar]
  25. Masur H., Michelis M. A., Wormser G. P., Lewin S., Gold J., Tapper M. L., Giron J., Lerner C. W., Armstrong D., Setia U. Opportunistic infection in previously healthy women. Initial manifestations of a community-acquired cellular immunodeficiency. Ann Intern Med. 1982 Oct;97(4):533–539. doi: 10.7326/0003-4819-97-4-533. [DOI] [PubMed] [Google Scholar]
  26. Menitove J. E., Aster R. H., Casper J. T., Lauer S. J., Gottschall J. L., Williams J. E., Gill J. C., Wheeler D. V., Piaskowski V., Kirchner P. T-lymphocyte subpopulations in patients with classic hemophilia treated with cryoprecipitate and lyophilized concentrates. N Engl J Med. 1983 Jan 13;308(2):83–86. doi: 10.1056/NEJM198301133080206. [DOI] [PubMed] [Google Scholar]
  27. Mildvan D., Mathur U., Enlow R. W., Romain P. L., Winchester R. J., Colp C., Singman H., Adelsberg B. R., Spigland I. Opportunistic infections and immune deficiency in homosexual men. Ann Intern Med. 1982 Jun;96(6 Pt 1):700–704. doi: 10.7326/0003-4819-96-6-700. [DOI] [PubMed] [Google Scholar]
  28. Oleske J., Minnefor A., Cooper R., Jr, Thomas K., dela Cruz A., Ahdieh H., Guerrero I., Joshi V. V., Desposito F. Immune deficiency syndrome in children. JAMA. 1983 May 6;249(17):2345–2349. [PubMed] [Google Scholar]
  29. Pinching A. J., McManus T. J., Jeffries D. J., Moshtael O., Donaghy M., Parkin J. M., Munday P. E., Harris J. R. Studies of cellular immunity in male homosexuals in London. Lancet. 1983 Jul 16;2(8342):126–130. doi: 10.1016/s0140-6736(83)90115-0. [DOI] [PubMed] [Google Scholar]
  30. Pitchenik A. E., Fischl M. A., Dickinson G. M., Becker D. M., Fournier A. M., O'Connell M. T., Colton R. M., Spira T. J. Opportunistic infections and Kaposi's sarcoma among Haitians: evidence of a new acquired immunodeficiency state. Ann Intern Med. 1983 Mar;98(3):277–284. doi: 10.7326/0003-4819-98-3-277. [DOI] [PubMed] [Google Scholar]
  31. Poon M. C., Landay A., Prasthofer E. F., Stagno S. Acquired immunodeficiency syndrome with Pneumocystis carinii pneumonia and Mycobacterium avium-intracellulare infection in a previously healthy patient with classic hemophilia. Clinical, immunologic, and virologic findings. Ann Intern Med. 1983 Mar;98(3):287–290. doi: 10.7326/0003-4819-98-3-287. [DOI] [PubMed] [Google Scholar]
  32. Rubinstein A., Sicklick M., Gupta A., Bernstein L., Klein N., Rubinstein E., Spigland I., Fruchter L., Litman N., Lee H. Acquired immunodeficiency with reversed T4/T8 ratios in infants born to promiscuous and drug-addicted mothers. JAMA. 1983 May 6;249(17):2350–2356. [PubMed] [Google Scholar]
  33. Shaw S., Biddison W. E. HLA-linked genetic control of the specicity of human cytotoxic T-cell responses to influenza virus. J Exp Med. 1979 Mar 1;149(3):565–575. doi: 10.1084/jem.149.3.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Shearer G. M. Allogeneic leukocytes as a possible factor in induction of aids in homosexual men. N Engl J Med. 1983 Jan 27;308(4):223–224. doi: 10.1056/NEJM198301273080415. [DOI] [PubMed] [Google Scholar]
  35. Shearer G. M., Levy R. B. Graft-vs.-host-associated immune suppression is activated by recognition of allogeneic murine I-A antigens. J Exp Med. 1983 Mar 1;157(3):936–946. doi: 10.1084/jem.157.3.936. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Siegal F. P., Lopez C., Hammer G. S., Brown A. E., Kornfeld S. J., Gold J., Hassett J., Hirschman S. Z., Cunningham-Rundles C., Adelsberg B. R. Severe acquired immunodeficiency in male homosexuals, manifested by chronic perianal ulcerative herpes simplex lesions. N Engl J Med. 1981 Dec 10;305(24):1439–1444. doi: 10.1056/NEJM198112103052403. [DOI] [PubMed] [Google Scholar]
  37. Sonnabend J., Witkin S. S., Purtilo D. T. Acquired immunodeficiency syndrome, opportunistic infections, and malignancies in male homosexuals. A hypothesis of etiologic factors in pathogenesis. JAMA. 1983 May 6;249(17):2370–2374. [PubMed] [Google Scholar]
  38. Stahl R. E., Friedman-Kien A., Dubin R., Marmor M., Zolla-Pazner S. Immunologic abnormalities in homosexual men. Relationship to Kaposi's sarcoma. Am J Med. 1982 Aug;73(2):171–178. doi: 10.1016/0002-9343(82)90174-7. [DOI] [PubMed] [Google Scholar]
  39. Vieira J., Frank E., Spira T. J., Landesman S. H. Acquired immune deficiency in Haitians: opportunistic infections in previously healthy Haitian immigrants. N Engl J Med. 1983 Jan 20;308(3):125–129. doi: 10.1056/NEJM198301203080303. [DOI] [PubMed] [Google Scholar]
  40. WELLER T. H., COONS A. H. Fluorescent antibody studies with agents of varicella and herpes zoster propagated in vitro. Proc Soc Exp Biol Med. 1954 Aug-Sep;86(4):789–794. doi: 10.3181/00379727-86-21235. [DOI] [PubMed] [Google Scholar]
  41. Wormser G. P., Krupp L. B., Hanrahan J. P., Gavis G., Spira T. J., Cunningham-Rundles S. Acquired immunodeficiency syndrome in male prisoners. New insights into an emerging syndrome. Ann Intern Med. 1983 Mar;98(3):297–303. doi: 10.7326/0003-4819-98-3-297. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Clinical Investigation are provided here courtesy of American Society for Clinical Investigation

RESOURCES