Skip to main content
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1987 Aug;80(2):316–324. doi: 10.1172/JCI113075

Antibody response to human immunodeficiency virus in homosexual men. Relation of antibody specificity, titer, and isotype to clinical status, severity of immunodeficiency, and disease progression.

J S McDougal, M S Kennedy, J K Nicholson, T J Spira, H W Jaffe, J E Kaplan, D B Fishbein, P O'Malley, C H Aloisio, C M Black, et al.
PMCID: PMC442240  PMID: 3497176

Abstract

The titers and isotypes of antibodies to specific proteins of the human immunodeficiency virus were determined by Western blot analysis of sera from 107 homosexual men. Antibody titers were generally lower in sera from patients with the acquired immunodeficiency syndrome (AIDS) and in sera from men whose condition subsequently progressed to AIDS than in sera from men who had not progressed to AIDS. We found no evidence of isotypic prominence or restriction of the antibody response. In multivariate analysis, lower levels of CD4 helper cells were most highly associated with progression to AIDS. Lower antibody titers to the envelope protein gp110, the core protein p24, and the reverse transcriptase enzyme p51/65 were also predictive of progression to AIDS independent of their association with CD4 cell levels. These data suggest that differences in antibody levels are not simply a consequence of severe immunodeficiency but may be markers for control of infection.

Full text

PDF
319

Images in this article

Selected References

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

  1. Aiuti F., Rossi P., Sirianni M. C., Carbonari M., Popovic M., Sarngadharan M. G., Contu L., Moroni M., Romagnani S., Gallo R. C. IgM and IgG antibodies to human T cell lymphotropic retrovirus (HTLV-III) in lymphadenopathy syndrome and subjects at risk for AIDS in Italy. Br Med J (Clin Res Ed) 1985 Jul 20;291(6489):165–166. doi: 10.1136/bmj.291.6489.165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aldovini A., Debouck C., Feinberg M. B., Rosenberg M., Arya S. K., Wong-Staal F. Synthesis of the complete trans-activation gene product of human T-lymphotropic virus type III in Escherichia coli: demonstration of immunogenicity in vivo and expression in vitro. Proc Natl Acad Sci U S A. 1986 Sep;83(18):6672–6676. doi: 10.1073/pnas.83.18.6672. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Allan J. S., Coligan J. E., Barin F., McLane M. F., Sodroski J. G., Rosen C. A., Haseltine W. A., Lee T. H., Essex M. Major glycoprotein antigens that induce antibodies in AIDS patients are encoded by HTLV-III. Science. 1985 May 31;228(4703):1091–1094. doi: 10.1126/science.2986290. [DOI] [PubMed] [Google Scholar]
  4. Ammann A. J., Abrams D., Conant M., Chudwin D., Cowan M., Volberding P., Lewis B., Casavant C. Acquired immune dysfunction in homosexual men: immunologic profiles. Clin Immunol Immunopathol. 1983 Jun;27(3):315–325. doi: 10.1016/0090-1229(83)90084-3. [DOI] [PubMed] [Google Scholar]
  5. Ammann A. J., Schiffman G., Abrams D., Volberding P., Ziegler J., Conant M. B-cell immunodeficiency in acquired immune deficiency syndrome. JAMA. 1984 Mar 16;251(11):1447–1449. [PubMed] [Google Scholar]
  6. Barin F., McLane M. F., Allan J. S., Lee T. H., Groopman J. E., Essex M. Virus envelope protein of HTLV-III represents major target antigen for antibodies in AIDS patients. Science. 1985 May 31;228(4703):1094–1096. doi: 10.1126/science.2986291. [DOI] [PubMed] [Google Scholar]
  7. Bedarida G., Cambiè G., D'Agostino F., Ronsivalle M. G., Berto E., Grisi M. E. HIV IgM antibodies in risk groups who are seronegative on ELISA testing. Lancet. 1986 Sep 6;2(8506):570–571. doi: 10.1016/s0140-6736(86)90133-9. [DOI] [PubMed] [Google Scholar]
  8. Biggar R. J., Melbye M., Ebbesen P., Alexander S., Nielsen J. O., Sarin P., Faber V. Variation in human T lymphotropic virus III (HTLV-III) antibodies in homosexual men: decline before onset of illness related to acquired immune deficiency syndrome (AIDS). Br Med J (Clin Res Ed) 1985 Oct 12;291(6501):997–998. doi: 10.1136/bmj.291.6501.997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Eyster M. E., Goedert J. J., Sarngadharan M. G., Weiss S. H., Gallo R. C., Blattner W. A. Development and early natural history of HTLV-III antibodies in persons with hemophilia. JAMA. 1985 Apr 19;253(15):2219–2223. [PubMed] [Google Scholar]
  10. Fishbein D. B., Kaplan J. E., Spira T. J., Miller B., Schonberger L. B., Pinsky P. F., Getchell J. P., Kalyanaraman V. S., Braude J. S. Unexplained lymphadenopathy in homosexual men. A longitudinal study. JAMA. 1985 Aug 16;254(7):930–935. [PubMed] [Google Scholar]
  11. Goedert J. J., Sarngadharan M. G., Biggar R. J., Weiss S. H., Winn D. M., Grossman R. J., Greene M. H., Bodner A. J., Mann D. L., Strong D. M. Determinants of retrovirus (HTLV-III) antibody and immunodeficiency conditions in homosexual men. Lancet. 1984 Sep 29;2(8405):711–716. doi: 10.1016/s0140-6736(84)92624-2. [DOI] [PubMed] [Google Scholar]
  12. Groopman J. E., Chen F. W., Hope J. A., Andrews J. M., Swift R. L., Benton C. V., Sullivan J. L., Volberding P. A., Sites D. P., Landesman S. Serological characterization of HTLV-III infection in AIDS and related disorders. J Infect Dis. 1986 Apr;153(4):736–742. doi: 10.1093/infdis/153.4.736. [DOI] [PubMed] [Google Scholar]
  13. Jaffe H. W., Feorino P. M., Darrow W. W., O'Malley P. M., Getchell J. P., Warfield D. T., Jones B. M., Echenberg D. F., Francis D. P., Curran J. W. Persistent infection with human T-lymphotropic virus type III/lymphadenopathy-associated virus in apparently healthy homosexual men. Ann Intern Med. 1985 May;102(5):627–628. doi: 10.7326/0003-4819-102-5-627. [DOI] [PubMed] [Google Scholar]
  14. Kaminsky L. S., McHugh T., Stites D., Volberding P., Henle G., Henle W., Levy J. A. High prevalence of antibodies to acquired immune deficiency syndrome (AIDS)-associated retrovirus (ARV) in AIDS and related conditions but not in other disease states. Proc Natl Acad Sci U S A. 1985 Aug;82(16):5535–5539. doi: 10.1073/pnas.82.16.5535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Klatzmann D., Barré-Sinoussi F., Nugeyre M. T., Danquet C., Vilmer E., Griscelli C., Brun-Veziret F., Rouzioux C., Gluckman J. C., Chermann J. C. Selective tropism of lymphadenopathy associated virus (LAV) for helper-inducer T lymphocytes. Science. 1984 Jul 6;225(4657):59–63. doi: 10.1126/science.6328660. [DOI] [PubMed] [Google Scholar]
  16. Lane H. C., Masur H., Gelmann E. P., Longo D. L., Steis R. G., Chused T., Whalen G., Edgar L. C., Fauci A. S. Correlation between immunologic function and clinical subpopulations of patients with the acquired immune deficiency syndrome. Am J Med. 1985 Mar;78(3):417–422. doi: 10.1016/0002-9343(85)90332-8. [DOI] [PubMed] [Google Scholar]
  17. Lange J. M., Coutinho R. A., Krone W. J., Verdonck L. F., Danner S. A., van der Noordaa J., Goudsmit J. Distinct IgG recognition patterns during progression of subclinical and clinical infection with lymphadenopathy associated virus/human T lymphotropic virus. Br Med J (Clin Res Ed) 1986 Jan 25;292(6515):228–230. doi: 10.1136/bmj.292.6515.228. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lasky L. A., Groopman J. E., Fennie C. W., Benz P. M., Capon D. J., Dowbenko D. J., Nakamura G. R., Nunes W. M., Renz M. E., Berman P. W. Neutralization of the AIDS retrovirus by antibodies to a recombinant envelope glycoprotein. Science. 1986 Jul 11;233(4760):209–212. doi: 10.1126/science.3014647. [DOI] [PubMed] [Google Scholar]
  19. Laurence J., Brun-Vezinet F., Schutzer S. E., Rouzioux C., Klatzmann D., Barré-Sinoussi F., Chermann J. C., Montagnier L. Lymphadenopathy-associated viral antibody in AIDS. Immune correlations and definition of a carrier state. N Engl J Med. 1984 Nov 15;311(20):1269–1273. doi: 10.1056/NEJM198411153112001. [DOI] [PubMed] [Google Scholar]
  20. Mathur-Wagh U., Enlow R. W., Spigland I., Winchester R. J., Sacks H. S., Rorat E., Yancovitz S. R., Klein M. J., William D. C., Mildvan D. Longitudinal study of persistent generalised lymphadenopathy in homosexual men: relation to acquired immunodeficiency syndrome. Lancet. 1984 May 12;1(8385):1033–1038. doi: 10.1016/s0140-6736(84)91449-1. [DOI] [PubMed] [Google Scholar]
  21. McDougal J. S., Cort S. P., Kennedy M. S., Cabridilla C. D., Feorino P. M., Francis D. P., Hicks D., Kalyanaraman V. S., Martin L. S. Immunoassay for the detection and quantitation of infectious human retrovirus, lymphadenopathy-associated virus (LAV). J Immunol Methods. 1985 Jan 21;76(1):171–183. doi: 10.1016/0022-1759(85)90489-2. [DOI] [PubMed] [Google Scholar]
  22. McDougal J. S., Kennedy M. S., Sligh J. M., Cort S. P., Mawle A., Nicholson J. K. Binding of HTLV-III/LAV to T4+ T cells by a complex of the 110K viral protein and the T4 molecule. Science. 1986 Jan 24;231(4736):382–385. doi: 10.1126/science.3001934. [DOI] [PubMed] [Google Scholar]
  23. Melbye M., Biggar R. J., Ebbesen P., Neuland C., Goedert J. J., Faber V., Lorenzen I., Skinhøj P., Gallo R. C., Blattner W. A. Long-term seropositivity for human T-lymphotropic virus type III in homosexual men without the acquired immunodeficiency syndrome: development of immunologic and clinical abnormalities. A longitudinal study. Ann Intern Med. 1986 Apr;104(4):496–500. doi: 10.7326/0003-4819-104-4-496. [DOI] [PubMed] [Google Scholar]
  24. Metroka C. E., Cunningham-Rundles S., Pollack M. S., Sonnabend J. A., Davis J. M., Gordon B., Fernandez R. D., Mouradian J. Generalized lymphadenopathy in homosexual men. Ann Intern Med. 1983 Nov;99(5):585–591. doi: 10.7326/0003-4819-99-5-585. [DOI] [PubMed] [Google Scholar]
  25. Montagnier L., Clavel F., Krust B., Chamaret S., Rey F., Barré-Sinoussi F., Chermann J. C. Identification and antigenicity of the major envelope glycoprotein of lymphadenopathy-associated virus. Virology. 1985 Jul 15;144(1):283–289. doi: 10.1016/0042-6822(85)90326-5. [DOI] [PubMed] [Google Scholar]
  26. Nicholson J. K., McDougal J. S., Jaffe H. W., Spira T. J., Kennedy M. S., Jones B. M., Darrow W. W., Morgan M., Hubbard M. Exposure to human T-lymphotropic virus type III/lymphadenopathy-associated virus and immunologic abnormalities in asymptomatic homosexual men. Ann Intern Med. 1985 Jul;103(1):37–42. doi: 10.7326/0003-4819-103-1-37. [DOI] [PubMed] [Google Scholar]
  27. Nicholson J. K., McDougal J. S., Spira T. J., Cross G. D., Jones B. M., Reinherz E. L. Immunoregulatory subsets of the T helper and T suppressor cell populations in homosexual men with chronic unexplained lymphadenopathy. J Clin Invest. 1984 Jan;73(1):191–201. doi: 10.1172/JCI111190. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Parry J. V., Mortimer P. P. Place of IgM antibody testing in HIV serology. Lancet. 1986 Oct 25;2(8513):979–980. doi: 10.1016/s0140-6736(86)90632-x. [DOI] [PubMed] [Google Scholar]
  29. Reimer C. B., Phillips D. J., Aloisio C. H., Moore D. D., Galland G. G., Wells T. W., Black C. M., McDougal J. S. Evaluation of thirty-one mouse monoclonal antibodies to human IgG epitopes. Hybridoma. 1984 Fall;3(3):263–275. doi: 10.1089/hyb.1984.3.263. [DOI] [PubMed] [Google Scholar]
  30. Reinherz E. L., Schlossman S. F. The differentiation and function of human T lymphocytes. Cell. 1980 Apr;19(4):821–827. doi: 10.1016/0092-8674(80)90072-0. [DOI] [PubMed] [Google Scholar]
  31. Robert-Guroff M., Brown M., Gallo R. C. HTLV-III-neutralizing antibodies in patients with AIDS and AIDS-related complex. Nature. 1985 Jul 4;316(6023):72–74. doi: 10.1038/316072a0. [DOI] [PubMed] [Google Scholar]
  32. Robey W. G., Safai B., Oroszlan S., Arthur L. O., Gonda M. A., Gallo R. C., Fischinger P. J. Characterization of envelope and core structural gene products of HTLV-III with sera from AIDS patients. Science. 1985 May 3;228(4699):593–595. doi: 10.1126/science.2984774. [DOI] [PubMed] [Google Scholar]
  33. Safai B., Sarngadharan M. G., Groopman J. E., Arnett K., Popovic M., Sliski A., Schüpbach J., Gallo R. C. Seroepidemiological studies of human T-lymphotropic retrovirus type III in acquired immunodeficiency syndrome. Lancet. 1984 Jun 30;1(8392):1438–1440. doi: 10.1016/s0140-6736(84)91933-0. [DOI] [PubMed] [Google Scholar]
  34. Sarngadharan M. G., diMarzo Veronese F., Lee S., Gallo R. C. Immunological properties of HTLV-III antigens recognized by sera of patients with AIDS and AIDS-related complex and of asymptomatic carriers of HTLV-III infection. Cancer Res. 1985 Sep;45(9 Suppl):4574s–4577s. [PubMed] [Google Scholar]
  35. Schroff R. W., Gottlieb M. S., Prince H. E., Chai L. L., Fahey J. L. Immunological studies of homosexual men with immunodeficiency and Kaposi's sarcoma. Clin Immunol Immunopathol. 1983 Jun;27(3):300–314. doi: 10.1016/0090-1229(83)90083-1. [DOI] [PubMed] [Google Scholar]
  36. Schwartz K., Visscher B. R., Detels R., Taylor J., Nishanian P., Fahey J. L. Immunological changes in lymphadenopathy virus positive and negative symptomless male homosexuals: two years of observation. Lancet. 1985 Oct 12;2(8459):831–832. doi: 10.1016/s0140-6736(85)90816-5. [DOI] [PubMed] [Google Scholar]
  37. Schüpbach J., Haller O., Vogt M., Lüthy R., Joller H., Oelz O., Popovic M., Sarngadharan M. G., Gallo R. C. Antibodies to HTLV-III in Swiss patients with AIDS and pre-AIDS and in groups at risk for AIDS. N Engl J Med. 1985 Jan 31;312(5):265–270. doi: 10.1056/NEJM198501313120502. [DOI] [PubMed] [Google Scholar]
  38. Schüpbach J., Popovic M., Gilden R. V., Gonda M. A., Sarngadharan M. G., Gallo R. C. Serological analysis of a subgroup of human T-lymphotropic retroviruses (HTLV-III) associated with AIDS. Science. 1984 May 4;224(4648):503–505. doi: 10.1126/science.6200937. [DOI] [PubMed] [Google Scholar]
  39. Steimer K. S., Higgins K. W., Powers M. A., Stephans J. C., Gyenes A., George-Nascimento C., Luciw P. A., Barr P. J., Hallewell R. A., Sanchez-Pescador R. Recombinant polypeptide from the endonuclease region of the acquired immune deficiency syndrome retrovirus polymerase (pol) gene detects serum antibodies in most infected individuals. J Virol. 1986 Apr;58(1):9–16. doi: 10.1128/jvi.58.1.9-16.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Steimer K. S., Puma J. P., Power M. D., Powers M. A., George-Nascimento C., Stephans J. C., Levy J. A., Sanchez-Pescador R., Luciw P. A., Barr P. J. Differential antibody responses of individuals infected with AIDS-associated retroviruses surveyed using the viral core antigen p25gag expressed in bacteria. Virology. 1986 Apr 15;150(1):283–290. doi: 10.1016/0042-6822(86)90289-8. [DOI] [PubMed] [Google Scholar]
  41. Sundqvist V. A., Linde A., Kurth R., Werner A., Helm E. B., Popovic M., Gallo R. C., Wahren B. Restricted IgG subclass responses to HTLV-III/LAV and to cytomegalovirus in patients with AIDS and lymphadenopathy syndrome. J Infect Dis. 1986 May;153(5):970–973. doi: 10.1093/infdis/153.5.970. [DOI] [PubMed] [Google Scholar]
  42. Tsang V. C., Peralta J. M., Simons A. R. Enzyme-linked immunoelectrotransfer blot techniques (EITB) for studying the specificities of antigens and antibodies separated by gel electrophoresis. Methods Enzymol. 1983;92:377–391. doi: 10.1016/0076-6879(83)92032-3. [DOI] [PubMed] [Google Scholar]
  43. Veronese F. D., DeVico A. L., Copeland T. D., Oroszlan S., Gallo R. C., Sarngadharan M. G. Characterization of gp41 as the transmembrane protein coded by the HTLV-III/LAV envelope gene. Science. 1985 Sep 27;229(4720):1402–1405. doi: 10.1126/science.2994223. [DOI] [PubMed] [Google Scholar]
  44. Weiss R. A., Clapham P. R., Cheingsong-Popov R., Dalgleish A. G., Carne C. A., Weller I. V., Tedder R. S. Neutralization of human T-lymphotropic virus type III by sera of AIDS and AIDS-risk patients. Nature. 1985 Jul 4;316(6023):69–72. doi: 10.1038/316069a0. [DOI] [PubMed] [Google Scholar]
  45. di Marzo Veronese F., Copeland T. D., DeVico A. L., Rahman R., Oroszlan S., Gallo R. C., Sarngadharan M. G. Characterization of highly immunogenic p66/p51 as the reverse transcriptase of HTLV-III/LAV. Science. 1986 Mar 14;231(4743):1289–1291. doi: 10.1126/science.2418504. [DOI] [PubMed] [Google Scholar]

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

RESOURCES