Logo of jvirolPermissionsJournals.ASM.orgJournalJV ArticleJournal InfoAuthorsReviewers
J Virol. Oct 1989; 63(10): 4277–4284.
PMCID: PMC251042

Genital mucosal transmission of simian immunodeficiency virus: animal model for heterosexual transmission of human immunodeficiency virus.


An animal model for the heterosexual transmission of human immunodeficiency virus (HIV) was developed by the application of simian immunodeficiency virus (SIV) onto the genital mucosas of both mature and immature, male and female rhesus macaques. Virus preparations were infused into the vaginal vaults or the urethras (males) of the animals through a soft plastic pediatric nasogastric feeding tube. The macaques that were infected by this route (six males and nine females) developed SIV-specific antibodies, and SIV was isolated from peripheral mononuclear cells of all seropositive animals. One male and one female infected by this route developed severe acquired immunodeficiency syndrome-like disease with retroviral giant-cell pneumonia. As few as two inoculations of cell-free SIV containing 50 50% tissue culture infective doses induced persistent viremia. Cell-free virus preparations were capable of producing infection by the genital route. Much higher doses of virus were required to transmit SIV by this route than are required for transmission by intravenous inoculation. Thus, it appears that the mucous membranes of the genital tract act as a barrier to SIV infection. Spermatozoa and seminal plasma were not required for the genital transmission of SIV. Rarely, SIV was recovered from mononuclear cells in semen and vaginal secretions. The SIV-rhesus macaque model is suitable for assessing the role of cofactors in heterosexual transmission of HIV and will be useful for testing the effectiveness of spermicides, pharmacologic agents, and vaccines in preventing the heterosexual transmission of HIV.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (2.0M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Images in this article

Click on the image to see a larger version.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Alexander NJ, Anderson DJ. Immunology of semen. Fertil Steril. 1987 Feb;47(2):192–205. [PubMed]
  • Alexander NJ, Tarter TH, Fulgham DL, Ducsay CA, Novy MJ. Rectal infusion of semen results in transient elevation of blood prostaglandins. Am J Reprod Immunol Microbiol. 1987 Oct;15(2):47–51. [PubMed]
  • Alter HJ, Eichberg JW, Masur H, Saxinger WC, Gallo R, Macher AM, Lane HC, Fauci AS. Transmission of HTLV-III infection from human plasma to chimpanzees: an animal model for AIDS. Science. 1984 Nov 2;226(4674):549–552. [PubMed]
  • Baskin GB. Disseminated cytomegalovirus infection in immunodeficient rhesus monkeys. Am J Pathol. 1987 Nov;129(2):345–352. [PMC free article] [PubMed]
  • Baskin GB, Murphey-Corb M, Watson EA, Martin LN. Necropsy findings in rhesus monkeys experimentally infected with cultured simian immunodeficiency virus (SIV)/delta. Vet Pathol. 1988 Nov;25(6):456–467. [PubMed]
  • Benveniste RE, Morton WR, Clark EA, Tsai CC, Ochs HD, Ward JM, Kuller L, Knott WB, Hill RW, Gale MJ, et al. Inoculation of baboons and macaques with simian immunodeficiency virus/Mne, a primate lentivirus closely related to human immunodeficiency virus type 2. J Virol. 1988 Jun;62(6):2091–2101. [PMC free article] [PubMed]
  • Chakrabarti L, Guyader M, Alizon M, Daniel MD, Desrosiers RC, Tiollais P, Sonigo P. Sequence of simian immunodeficiency virus from macaque and its relationship to other human and simian retroviruses. Nature. 1987 Aug 6;328(6130):543–547. [PubMed]
  • Chalifoux LV, Ringler DJ, King NW, Sehgal PK, Desrosiers RC, Daniel MD, Letvin NL. Lymphadenopathy in macaques experimentally infected with the simian immunodeficiency virus (SIV). Am J Pathol. 1987 Jul;128(1):104–110. [PMC free article] [PubMed]
  • Comhaire F, Verschraegen G, Vermeulen L. Diagnosis of accessory gland infection and its possible role in male infertility. Int J Androl. 1980 Feb;3(1):32–45. [PubMed]
  • Daniel MD, Letvin NL, King NW, Kannagi M, Sehgal PK, Hunt RD, Kanki PJ, Essex M, Desrosiers RC. Isolation of T-cell tropic HTLV-III-like retrovirus from macaques. Science. 1985 Jun 7;228(4704):1201–1204. [PubMed]
  • Daniel MD, Letvin NL, Sehgal PK, Hunsmann G, Schmidt DK, King NW, Desrosiers RC. Long-term persistent infection of macaque monkeys with the simian immunodeficiency virus. J Gen Virol. 1987 Dec;68(Pt 12):3183–3189. [PubMed]
  • di Marzo Veronese F, Copeland TD, DeVico AL, Rahman R, Oroszlan S, Gallo RC, Sarngadharan MG. Characterization of highly immunogenic p66/p51 as the reverse transcriptase of HTLV-III/LAV. Science. 1986 Mar 14;231(4743):1289–1291. [PubMed]
  • Franchini G, Gurgo C, Guo HG, Gallo RC, Collalti E, Fargnoli KA, Hall LF, Wong-Staal F, Reitz MS., Jr Sequence of simian immunodeficiency virus and its relationship to the human immunodeficiency viruses. Nature. 1987 Aug 6;328(6130):539–543. [PubMed]
  • Fukasawa M, Miura T, Hasegawa A, Morikawa S, Tsujimoto H, Miki K, Kitamura T, Hayami M. Sequence of simian immunodeficiency virus from African green monkey, a new member of the HIV/SIV group. Nature. 1988 Jun 2;333(6172):457–461. [PubMed]
  • Fultz PN, McClure HM, Daugharty H, Brodie A, McGrath CR, Swenson B, Francis DP. Vaginal transmission of human immunodeficiency virus (HIV) to a chimpanzee. J Infect Dis. 1986 Nov;154(5):896–900. [PubMed]
  • Fultz PN, McClure HM, Anderson DC, Swenson RB, Anand R, Srinivasan A. Isolation of a T-lymphotropic retrovirus from naturally infected sooty mangabey monkeys (Cercocebus atys). Proc Natl Acad Sci U S A. 1986 Jul;83(14):5286–5290. [PMC free article] [PubMed]
  • Gardner MB, Luciw P, Lerche N, Marx P. Nonhuman primate retrovirus isolates and AIDS. Adv Vet Sci Comp Med. 1988;32:171–226. [PubMed]
  • Goedert JJ, Eyster ME, Biggar RJ, Blattner WA. Heterosexual transmission of human immunodeficiency virus: association with severe depletion of T-helper lymphocytes in men with hemophilia. AIDS Res Hum Retroviruses. 1987;3(4):355–361. [PubMed]
  • Harrison RM. Semen parameters in Macaca mulatta: ejaculates from random and selected monkeys. J Med Primatol. 1980;9(5):265–273. [PubMed]
  • Henderson LE, Benveniste RE, Sowder R, Copeland TD, Schultz AM, Oroszlan S. Molecular characterization of gag proteins from simian immunodeficiency virus (SIVMne). J Virol. 1988 Aug;62(8):2587–2595. [PMC free article] [PubMed]
  • Hicks DR, Martin LS, Getchell JP, Heath JL, Francis DP, McDougal JS, Curran JW, Voeller B. Inactivation of HTLV-III/LAV-infected cultures of normal human lymphocytes by nonoxynol-9 in vitro. Lancet. 1985 Dec 21;2(8469-70):1422–1423. [PubMed]
  • Hirsch VM, Olmsted RA, Murphey-Corb M, Purcell RH, Johnson PR. An African primate lentivirus (SIVsm) closely related to HIV-2. Nature. 1989 Jun 1;339(6223):389–392. [PubMed]
  • Hirsch V, Riedel N, Mullins JI. The genome organization of STLV-3 is similar to that of the AIDS virus except for a truncated transmembrane protein. Cell. 1987 May 8;49(3):307–319. [PubMed]
  • Ho DD, Schooley RT, Rota TR, Kaplan JC, Flynn T, Salahuddin SZ, Gonda MA, Hirsch MS. HTLV-III in the semen and blood of a healthy homosexual man. Science. 1984 Oct 26;226(4673):451–453. [PubMed]
  • James K, Harvey J, Bradbury AW, Hargreave TB, Cullen RT. The effect of seminal plasma on macrophage function--a possible contributory factor in sexually transmitted disease. AIDS Res. 1983 1984;1(1):45–57. [PubMed]
  • Kannagi M, Kiyotaki M, Desrosiers RC, Reimann KA, King NW, Waldron LM, Letvin NL. Humoral immune responses to T cell tropic retrovirus simian T lymphotropic virus type III in monkeys with experimentally induced acquired immune deficiency-like syndrome. J Clin Invest. 1986 Nov;78(5):1229–1236. [PMC free article] [PubMed]
  • Kannagi M, Yetz JM, Letvin NL. In vitro growth characteristics of simian T-lymphotropic virus type III. Proc Natl Acad Sci U S A. 1985 Oct;82(20):7053–7057. [PMC free article] [PubMed]
  • Kim HC, Raska K, 3rd, Clemow L, Eisele J, Matts L, Saidi P, Raska K., Jr Human immunodeficiency virus infection in sexually active wives of infected hemophilic men. Am J Med. 1988 Oct;85(4):472–476. [PubMed]
  • Letvin NL, Daniel MD, Sehgal PK, Desrosiers RC, Hunt RD, Waldron LM, MacKey JJ, Schmidt DK, Chalifoux LV, King NW. Induction of AIDS-like disease in macaque monkeys with T-cell tropic retrovirus STLV-III. Science. 1985 Oct 4;230(4721):71–73. [PubMed]
  • Lowenstine LJ, Pedersen NC, Higgins J, Pallis KC, Uyeda A, Marx P, Lerche NW, Munn RJ, Gardner MB. Seroepidemiologic survey of captive Old-World primates for antibodies to human and simian retroviruses, and isolation of a lentivirus from sooty mangabeys (Cercocebus atys). Int J Cancer. 1986 Oct 15;38(4):563–574. [PubMed]
  • Morrow WJ, Wharton M, Lau D, Levy JA. Small animals are not susceptible to human immunodeficiency virus infection. J Gen Virol. 1987 Aug;68(Pt 8):2253–2257. [PubMed]
  • Murphey-Corb M, Martin LN, Rangan SR, Baskin GB, Gormus BJ, Wolf RH, Andes WA, West M, Montelaro RC. Isolation of an HTLV-III-related retrovirus from macaques with simian AIDS and its possible origin in asymptomatic mangabeys. Nature. 1986 May 22;321(6068):435–437. [PubMed]
  • Peterman TA, Curran JW. Sexual transmission of human immunodeficiency virus. JAMA. 1986 Oct 24;256(16):2222–2226. [PubMed]
  • Peterman TA, Stoneburner RL, Allen JR, Jaffe HW, Curran JW. Risk of human immunodeficiency virus transmission from heterosexual adults with transfusion-associated infections. JAMA. 1988 Jan 1;259(1):55–58. [PubMed]
  • Piot P, Kreiss JK, Ndinya-Achola JO, Ngugi EN, Simonsen JN, Cameron DW, Taelman H, Plummer FA. Heterosexual transmission of HIV. AIDS. 1987 Dec;1(4):199–206. [PubMed]
  • Portis JL, McAtee FJ, Hayes SF. Horizontal transmission of murine retroviruses. J Virol. 1987 Apr;61(4):1037–1044. [PMC free article] [PubMed]
  • Salter RD, Howell DN, Cresswell P. Genes regulating HLA class I antigen expression in T-B lymphoblast hybrids. Immunogenetics. 1985;21(3):235–246. [PubMed]
  • Schaeffer AJ, Wendel EF, Dunn JK, Grayhack JT. Prevalence and significance of prostatic inflammation. J Urol. 1981 Feb;125(2):215–219. [PubMed]
  • Stewart GJ, Tyler JP, Cunningham AL, Barr JA, Driscoll GL, Gold J, Lamont BJ. Transmission of human T-cell lymphotropic virus type III (HTLV-III) by artificial insemination by donor. Lancet. 1985 Sep 14;2(8455):581–585. [PubMed]
  • Tarter TH, Cunningham-Rundles S, Koide SS. Suppression of natural killer cell activity by human seminal plasma in vitro: identification of 19-OH-PGE as the suppressor factor. J Immunol. 1986 Apr 15;136(8):2862–2867. [PubMed]
  • Vogt MW, Witt DJ, Craven DE, Byington R, Crawford DF, Schooley RT, Hirsch MS. Isolation of HTLV-III/LAV from cervical secretions of women at risk for AIDS. Lancet. 1986 Mar 8;1(8480):525–527. [PubMed]
  • Vogt MW, Witt DJ, Craven DE, Byington R, Crawford DF, Hutchinson MS, Schooley RT, Hirsch MS. Isolation patterns of the human immunodeficiency virus from cervical secretions during the menstrual cycle of women at risk for the acquired immunodeficiency syndrome. Ann Intern Med. 1987 Mar;106(3):380–382. [PubMed]
  • Wofsy CB, Cohen JB, Hauer LB, Padian NS, Michaelis BA, Evans LA, Levy JA. Isolation of AIDS-associated retrovirus from genital secretions of women with antibodies to the virus. Lancet. 1986 Mar 8;1(8480):527–529. [PubMed]
  • Wolff H, Anderson DJ. Immunohistologic characterization and quantitation of leukocyte subpopulations in human semen. Fertil Steril. 1988 Mar;49(3):497–504. [PubMed]
  • Zagury D, Bernard J, Leibowitch J, Safai B, Groopman JE, Feldman M, Sarngadharan MG, Gallo RC. HTLV-III in cells cultured from semen of two patients with AIDS. Science. 1984 Oct 26;226(4673):449–451. [PubMed]
  • Zhang JY, Martin LN, Watson EA, Montelaro RC, West M, Epstein L, Murphey-Corb M. Simian immunodeficiency virus/delta-induced immunodeficiency disease in rhesus monkeys: relation of antibody response and antigenemia. J Infect Dis. 1988 Dec;158(6):1277–1286. [PubMed]

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


Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...


Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...