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. 1997 Nov;71(11):8141–8148. doi: 10.1128/jvi.71.11.8141-8148.1997

Live, attenuated simian immunodeficiency virus vaccines elicit potent resistance against a challenge with a human immunodeficiency virus type 1 chimeric virus.

R Shibata 1, C Siemon 1, S C Czajak 1, R C Desrosiers 1, M A Martin 1
PMCID: PMC192270  PMID: 9343164

Abstract

Three rhesus macaques, previously immunized with SIVdelta3 or SIVdelta2, each an attenuated derivative of SIVmac239, and two naive monkeys were challenged with 30,000 50% tissue culture infective doses of SHIV, an SIV/human immunodeficiency virus type 1 (HIV-1) chimeric virus bearing the dual-tropic envelope of HIV-1DH12. By several criteria, including virus isolation, serological assays, and PCR (both DNA and reverse transcriptase), SHIV levels were reduced to barely detectable levels in the circulating blood of vaccinated animals. The resistant SIV-vaccinated macaques had no preexisting neutralizing antibodies directed against SHIV, nor did they produce neutralizing antibodies at any time over a 14-month observation period following SHIV challenge. Interestingly, SIV sequences, derived from the vaccine, could be amplified from numerous tissue samples collected at the conclusion of the experiment, 60 weeks postchallenge, but SHIV-specific sequences (viz., HIV-1 env) could not. These results demonstrate that live attenuated SIV vaccines provide strong long-term protection even against challenge strains with highly divergent envelope sequences.

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Selected References

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  1. Adachi A., Gendelman H. E., Koenig S., Folks T., Willey R., Rabson A., Martin M. A. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J Virol. 1986 Aug;59(2):284–291. doi: 10.1128/jvi.59.2.284-291.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ahmad S., Lohman B., Marthas M., Giavedoni L., el-Amad Z., Haigwood N. L., Scandella C. J., Gardner M. B., Luciw P. A., Yilma T. Reduced virus load in rhesus macaques immunized with recombinant gp160 and challenged with simian immunodeficiency virus. AIDS Res Hum Retroviruses. 1994 Feb;10(2):195–204. doi: 10.1089/aid.1994.10.195. [DOI] [PubMed] [Google Scholar]
  3. Almond N., Kent K., Cranage M., Rud E., Clarke B., Stott E. J. Protection by attenuated simian immunodeficiency virus in macaques against challenge with virus-infected cells. Lancet. 1995 May 27;345(8961):1342–1344. doi: 10.1016/s0140-6736(95)92540-6. [DOI] [PubMed] [Google Scholar]
  4. Arthur L. O., Bess J. W., Jr, Waters D. J., Pyle S. W., Kelliher J. C., Nara P. L., Krohn K., Robey W. G., Langlois A. J., Gallo R. C. Challenge of chimpanzees (Pan troglodytes) immunized with human immunodeficiency virus envelope glycoprotein gp120. J Virol. 1989 Dec;63(12):5046–5053. doi: 10.1128/jvi.63.12.5046-5053.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Berman P. W., Gregory T. J., Riddle L., Nakamura G. R., Champe M. A., Porter J. P., Wurm F. M., Hershberg R. D., Cobb E. K., Eichberg J. W. Protection of chimpanzees from infection by HIV-1 after vaccination with recombinant glycoprotein gp120 but not gp160. Nature. 1990 Jun 14;345(6276):622–625. doi: 10.1038/345622a0. [DOI] [PubMed] [Google Scholar]
  6. Bogers W. M., Niphuis H., ten Haaft P., Laman J. D., Koornstra W., Heeney J. L. Protection from HIV-1 envelope-bearing chimeric simian immunodeficiency virus (SHIV) in rhesus macaques infected with attenuated SIV: consequences of challenge. AIDS. 1995 Dec;9(12):F13–F18. [PubMed] [Google Scholar]
  7. Bruck C., Thiriart C., Fabry L., Francotte M., Pala P., Van Opstal O., Culp J., Rosenberg M., De Wilde M., Heidt P. HIV-1 envelope-elicited neutralizing antibody titres correlate with protection and virus load in chimpanzees. Vaccine. 1994 Sep;12(12):1141–1148. doi: 10.1016/0264-410x(94)90185-6. [DOI] [PubMed] [Google Scholar]
  8. Clements J. E., Montelaro R. C., Zink M. C., Amedee A. M., Miller S., Trichel A. M., Jagerski B., Hauer D., Martin L. N., Bohm R. P. Cross-protective immune responses induced in rhesus macaques by immunization with attenuated macrophage-tropic simian immunodeficiency virus. J Virol. 1995 May;69(5):2737–2744. doi: 10.1128/jvi.69.5.2737-2744.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cranage M. P., Polyanskaya N., McBride B., Cook N., Ashworth L. A., Dennis M., Baskerville A., Greenaway P. J., Corcoran T., Kitchin P. Studies on the specificity of the vaccine effect elicited by inactivated simian immunodeficiency virus. AIDS Res Hum Retroviruses. 1993 Jan;9(1):13–22. doi: 10.1089/aid.1993.9.13. [DOI] [PubMed] [Google Scholar]
  10. Daniel M. D., Kirchhoff F., Czajak S. C., Sehgal P. K., Desrosiers R. C. Protective effects of a live attenuated SIV vaccine with a deletion in the nef gene. Science. 1992 Dec 18;258(5090):1938–1941. doi: 10.1126/science.1470917. [DOI] [PubMed] [Google Scholar]
  11. Daniel M. D., Mazzara G. P., Simon M. A., Sehgal P. K., Kodama T., Panicali D. L., Desrosiers R. C. High-titer immune responses elicited by recombinant vaccinia virus priming and particle boosting are ineffective in preventing virulent SIV infection. AIDS Res Hum Retroviruses. 1994 Jul;10(7):839–851. doi: 10.1089/aid.1994.10.839. [DOI] [PubMed] [Google Scholar]
  12. Desrosiers R. C. HIV with multiple gene deletions as a live attenuated vaccine for AIDS. AIDS Res Hum Retroviruses. 1992 Aug;8(8):1457–1457. doi: 10.1089/aid.1992.8.1457. [DOI] [PubMed] [Google Scholar]
  13. Fenyö E. M. Antigenic variation of primate lentiviruses in humans and experimentally infected macaques. Immunol Rev. 1994 Aug;140:131–146. doi: 10.1111/j.1600-065x.1994.tb00868.x. [DOI] [PubMed] [Google Scholar]
  14. Franchini G., Robert-Guroff M., Tartaglia J., Aggarwal A., Abimiku A., Benson J., Markham P., Limbach K., Hurteau G., Fullen J. Highly attenuated HIV type 2 recombinant poxviruses, but not HIV-2 recombinant Salmonella vaccines, induce long-lasting protection in rhesus macaques. AIDS Res Hum Retroviruses. 1995 Aug;11(8):909–920. doi: 10.1089/aid.1995.11.909. [DOI] [PubMed] [Google Scholar]
  15. Fultz P. N., Nara P., Barre-Sinoussi F., Chaput A., Greenberg M. L., Muchmore E., Kieny M. P., Girard M. Vaccine protection of chimpanzees against challenge with HIV-1-infected peripheral blood mononuclear cells. Science. 1992 Jun 19;256(5064):1687–1690. doi: 10.1126/science.256.5064.1687. [DOI] [PubMed] [Google Scholar]
  16. Fultz P. N., Srinivasan A., Greene C. R., Butler D., Swenson R. B., McClure H. M. Superinfection of a chimpanzee with a second strain of human immunodeficiency virus. J Virol. 1987 Dec;61(12):4026–4029. doi: 10.1128/jvi.61.12.4026-4029.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Galetto-Lacour A., Yerly S., Perneger T. V., Baumberger C., Hirschel B., Perrin L. Prognostic value of viremia in patients with long-standing human immunodeficiency virus infection. Swiss HIV Cohort Study Group. J Infect Dis. 1996 Jun;173(6):1388–1393. doi: 10.1093/infdis/173.6.1388. [DOI] [PubMed] [Google Scholar]
  18. Giavedoni L. D., Planelles V., Haigwood N. L., Ahmad S., Kluge J. D., Marthas M. L., Gardner M. B., Luciw P. A., Yilma T. D. Immune response of rhesus macaques to recombinant simian immunodeficiency virus gp130 does not protect from challenge infection. J Virol. 1993 Jan;67(1):577–583. doi: 10.1128/jvi.67.1.577-583.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gibbs C. J., Jr, Peters R., Gravell M., Johnson B. K., Jensen F. C., Carlo D. J., Salk J. Observations after human immunodeficiency virus immunization and challenge of human immunodeficiency virus seropositive and seronegative chimpanzees. Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3348–3352. doi: 10.1073/pnas.88.8.3348. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Girard M., Kieny M. P., Pinter A., Barre-Sinoussi F., Nara P., Kolbe H., Kusumi K., Chaput A., Reinhart T., Muchmore E. Immunization of chimpanzees confers protection against challenge with human immunodeficiency virus. Proc Natl Acad Sci U S A. 1991 Jan 15;88(2):542–546. doi: 10.1073/pnas.88.2.542. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Girard M., Meignier B., Barré-Sinoussi F., Kieny M. P., Matthews T., Muchmore E., Nara P. L., Wei Q., Rimsky L., Weinhold K. Vaccine-induced protection of chimpanzees against infection by a heterologous human immunodeficiency virus type 1. J Virol. 1995 Oct;69(10):6239–6248. doi: 10.1128/jvi.69.10.6239-6248.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Heeney J. L., van Els C., de Vries P., ten Haaft P., Otting N., Koornstra W., Boes J., Dubbes R., Niphuis H., Dings M. Major histocompatibility complex class I-associated vaccine protection from simian immunodeficiency virus-infected peripheral blood cells. J Exp Med. 1994 Aug 1;180(2):769–774. doi: 10.1084/jem.180.2.769. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hirsch V. M., Fuerst T. R., Sutter G., Carroll M. W., Yang L. C., Goldstein S., Piatak M., Jr, Elkins W. R., Alvord W. G., Montefiori D. C. Patterns of viral replication correlate with outcome in simian immunodeficiency virus (SIV)-infected macaques: effect of prior immunization with a trivalent SIV vaccine in modified vaccinia virus Ankara. J Virol. 1996 Jun;70(6):3741–3752. doi: 10.1128/jvi.70.6.3741-3752.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hirsch V. M., Goldstein S., Hynes N. A., Elkins W. R., London W. T., Zack P. M., Montefiori D., Johnson P. R. Prolonged clinical latency and survival of macaques given a whole inactivated simian immunodeficiency virus vaccine. J Infect Dis. 1994 Jul;170(1):51–59. doi: 10.1093/infdis/170.1.51. [DOI] [PubMed] [Google Scholar]
  25. Hu S. L., Abrams K., Barber G. N., Moran P., Zarling J. M., Langlois A. J., Kuller L., Morton W. R., Benveniste R. E. Protection of macaques against SIV infection by subunit vaccines of SIV envelope glycoprotein gp160. Science. 1992 Jan 24;255(5043):456–459. doi: 10.1126/science.1531159. [DOI] [PubMed] [Google Scholar]
  26. Hu S. L., Fultz P. N., McClure H. M., Eichberg J. W., Thomas E. K., Zarling J., Singhal M. C., Kosowski S. G., Swenson R. B., Anderson D. C. Effect of immunization with a vaccinia-HIV env recombinant on HIV infection of chimpanzees. Nature. 1987 Aug 20;328(6132):721–723. doi: 10.1038/328721a0. [DOI] [PubMed] [Google Scholar]
  27. Israel Z. R., Edmonson P. F., Maul D. H., O'Neil S. P., Mossman S. P., Thiriart C., Fabry L., Van Opstal O., Bruck C., Bex F. Incomplete protection, but suppression of virus burden, elicited by subunit simian immunodeficiency virus vaccines. J Virol. 1994 Mar;68(3):1843–1853. doi: 10.1128/jvi.68.3.1843-1853.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lehner T., Wang Y., Cranage M., Bergmeier L. A., Mitchell E., Tao L., Hall G., Dennis M., Cook N., Brookes R. Protective mucosal immunity elicited by targeted iliac lymph node immunization with a subunit SIV envelope and core vaccine in macaques. Nat Med. 1996 Jul;2(7):767–775. doi: 10.1038/nm0796-767. [DOI] [PubMed] [Google Scholar]
  29. Letvin N. L., Li J., Halloran M., Cranage M. P., Rud E. W., Sodroski J. Prior infection with a nonpathogenic chimeric simian-human immunodeficiency virus does not efficiently protect macaques against challenge with simian immunodeficiency virus. J Virol. 1995 Jul;69(7):4569–4571. doi: 10.1128/jvi.69.7.4569-4571.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lohman B. L., McChesney M. B., Miller C. J., McGowan E., Joye S. M., Van Rompay K. K., Reay E., Antipa L., Pedersen N. C., Marthas M. L. A partially attenuated simian immunodeficiency virus induces host immunity that correlates with resistance to pathogenic virus challenge. J Virol. 1994 Nov;68(11):7021–7029. doi: 10.1128/jvi.68.11.7021-7029.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Marthas M. L., Sutjipto S., Higgins J., Lohman B., Torten J., Luciw P. A., Marx P. A., Pedersen N. C. Immunization with a live, attenuated simian immunodeficiency virus (SIV) prevents early disease but not infection in rhesus macaques challenged with pathogenic SIV. J Virol. 1990 Aug;64(8):3694–3700. doi: 10.1128/jvi.64.8.3694-3700.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Mellors J. W., Rinaldo C. R., Jr, Gupta P., White R. M., Todd J. A., Kingsley L. A. Prognosis in HIV-1 infection predicted by the quantity of virus in plasma. Science. 1996 May 24;272(5265):1167–1170. doi: 10.1126/science.272.5265.1167. [DOI] [PubMed] [Google Scholar]
  33. Miller C. J., McChesney M. B., Lü X., Dailey P. J., Chutkowski C., Lu D., Brosio P., Roberts B., Lu Y. Rhesus macaques previously infected with simian/human immunodeficiency virus are protected from vaginal challenge with pathogenic SIVmac239. J Virol. 1997 Mar;71(3):1911–1921. doi: 10.1128/jvi.71.3.1911-1921.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Mossman S. P., Bex F., Berglund P., Arthos J., O'Neil S. P., Riley D., Maul D. H., Bruck C., Momin P., Burny A. Protection against lethal simian immunodeficiency virus SIVsmmPBj14 disease by a recombinant Semliki Forest virus gp160 vaccine and by a gp120 subunit vaccine. J Virol. 1996 Mar;70(3):1953–1960. doi: 10.1128/jvi.70.3.1953-1960.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Naidu Y. M., Kestler H. W., 3rd, Li Y., Butler C. V., Silva D. P., Schmidt D. K., Troup C. D., Sehgal P. K., Sonigo P., Daniel M. D. Characterization of infectious molecular clones of simian immunodeficiency virus (SIVmac) and human immunodeficiency virus type 2: persistent infection of rhesus monkeys with molecularly cloned SIVmac. J Virol. 1988 Dec;62(12):4691–4696. doi: 10.1128/jvi.62.12.4691-4696.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. O'Brien T. R., Blattner W. A., Waters D., Eyster E., Hilgartner M. W., Cohen A. R., Luban N., Hatzakis A., Aledort L. M., Rosenberg P. S. Serum HIV-1 RNA levels and time to development of AIDS in the Multicenter Hemophilia Cohort Study. JAMA. 1996 Jul 10;276(2):105–110. [PubMed] [Google Scholar]
  37. Ohkawa S., Wilson L. A., Larosa G., Javaherian K., Martin L. N., Murphey-Corb M. Immune responses induced by prototype vaccines for AIDS in rhesus monkeys. AIDS Res Hum Retroviruses. 1994 Jan;10(1):27–38. doi: 10.1089/aid.1994.10.27. [DOI] [PubMed] [Google Scholar]
  38. Otsyula M. G., Miller C. J., Tarantal A. F., Marthas M. L., Greene T. P., Collins J. R., van Rompay K. K., McChesney M. B. Fetal or neonatal infection with attenuated simian immunodeficiency virus results in protective immunity against oral challenge with pathogenic SIVmac251. Virology. 1996 Aug 1;222(1):275–278. doi: 10.1006/viro.1996.0420. [DOI] [PubMed] [Google Scholar]
  39. Petry H., Dittmer U., Stahl-Hennig C., Coulibaly C., Makoschey B., Fuchs D., Wachter H., Tolle T., Morys-Wortmann C., Kaup F. J. Reactivation of human immunodeficiency virus type 2 in macaques after simian immunodeficiency virus SIVmac superinfection. J Virol. 1995 Mar;69(3):1564–1574. doi: 10.1128/jvi.69.3.1564-1574.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Putkonen P., Björling E., Akerblom L., Thorstensson R., Lövgren K., Benthin L., Chiodi F., Morein B., Biberfeld G., Norrby E. Long-standing protection of macaques against cell-free HIV-2 with a HIV-2 iscom vaccine. J Acquir Immune Defic Syndr. 1994 Jun;7(6):551–559. [PubMed] [Google Scholar]
  41. Putkonen P., Nilsson C., Hild K., Benthin R., Cranage M., Aubertin A. M., Biberfeld G. Whole inactivated SIV vaccine grown on human cells fails to protect against homologous SIV grown on simian cells. J Med Primatol. 1993 Feb-May;22(2-3):100–103. [PubMed] [Google Scholar]
  42. Putkonen P., Walther L., Zhang Y. J., Li S. L., Nilsson C., Albert J., Biberfeld P., Thorstensson R., Biberfeld G. Long-term protection against SIV-induced disease in macaques vaccinated with a live attenuated HIV-2 vaccine. Nat Med. 1995 Sep;1(9):914–918. doi: 10.1038/nm0995-914. [DOI] [PubMed] [Google Scholar]
  43. Quesada-Rolander M., Mäkitalo B., Thorstensson R., Zhang Y. J., Castaños-Velez E., Biberfeld G., Putkonen P. Protection against mucosal SIVsm challenge in macaques infected with a chimeric SIV that expresses HIV type 1 envelope. AIDS Res Hum Retroviruses. 1996 Jul 20;12(11):993–999. doi: 10.1089/aid.1996.12.993. [DOI] [PubMed] [Google Scholar]
  44. Schlienger K., Montefiori D. C., Mancini M., Rivière Y., Tiollais P., Michel M. L. Vaccine-induced neutralizing antibodies directed in part to the simian immunodeficiency virus (SIV) V2 domain were unable to protect rhesus monkeys from SIV experimental challenge. J Virol. 1994 Oct;68(10):6578–6588. doi: 10.1128/jvi.68.10.6578-6588.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Shafferman A., Jahrling P. B., Benveniste R. E., Lewis M. G., Phipps T. J., Eden-McCutchan F., Sadoff J., Eddy G. A., Burke D. S. Protection of macaques with a simian immunodeficiency virus envelope peptide vaccine based on conserved human immunodeficiency virus type 1 sequences. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7126–7130. doi: 10.1073/pnas.88.16.7126. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Shibata R., Hoggan M. D., Broscius C., Englund G., Theodore T. S., Buckler-White A., Arthur L. O., Israel Z., Schultz A., Lane H. C. Isolation and characterization of a syncytium-inducing, macrophage/T-cell line-tropic human immunodeficiency virus type 1 isolate that readily infects chimpanzee cells in vitro and in vivo. J Virol. 1995 Jul;69(7):4453–4462. doi: 10.1128/jvi.69.7.4453-4462.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Shibata R., Kawamura M., Sakai H., Hayami M., Ishimoto A., Adachi A. Generation of a chimeric human and simian immunodeficiency virus infectious to monkey peripheral blood mononuclear cells. J Virol. 1991 Jul;65(7):3514–3520. doi: 10.1128/jvi.65.7.3514-3520.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Shibata R., Maldarelli F., Siemon C., Matano T., Parta M., Miller G., Fredrickson T., Martin M. A. Infection and pathogenicity of chimeric simian-human immunodeficiency viruses in macaques: determinants of high virus loads and CD4 cell killing. J Infect Dis. 1997 Aug;176(2):362–373. doi: 10.1086/514053. [DOI] [PubMed] [Google Scholar]
  49. Shibata R., Siemon C., Cho M. W., Arthur L. O., Nigida S. M., Jr, Matthews T., Sawyer L. A., Schultz A., Murthy K. K., Israel Z. Resistance of previously infected chimpanzees to successive challenges with a heterologous intraclade B strain of human immunodeficiency virus type 1. J Virol. 1996 Jul;70(7):4361–4369. doi: 10.1128/jvi.70.7.4361-4369.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Siegel F., Kurth R., Norley S. Neither whole inactivated virus immunogen nor passive immunoglobulin transfer protects against SIVagm infection in the African green monkey natural host. J Acquir Immune Defic Syndr Hum Retrovirol. 1995 Mar 1;8(3):217–226. doi: 10.1097/00042560-199503010-00001. [DOI] [PubMed] [Google Scholar]
  51. Stahl-Hennig C., Coulibaly C., Petry H., Voss G., Dittmer U., Bodemer W., Makoschey B., Jurkiewicz E., Lüke W., Hunsmann G. Immunization with virion-derived glycoprotein 130 from HIV-2 or SIV protects macaques against challenge virus grown in human or simian cells or prepared ex vivo. AIDS Res Hum Retroviruses. 1994;10 (Suppl 2):S27–S32. [PubMed] [Google Scholar]
  52. Stahl-Hennig C., Dittmer U., Nisslein T., Petry H., Jurkiewicz E., Fuchs D., Wachter H., Mätz-Rensing K., Kuhn E. M., Kaup F. J. Rapid development of vaccine protection in macaques by live-attenuated simian immunodeficiency virus. J Gen Virol. 1996 Dec;77(Pt 12):2969–2981. doi: 10.1099/0022-1317-77-12-2969. [DOI] [PubMed] [Google Scholar]
  53. Titti F., Koanga Mogtomo M. L., Borsetti A., Geraci A., Sernicola L., Panzini G., Turillazzi G. P., Baroncelli S., Giovannetti A., Zamarchi R. Immunization of Macaca fascicularis with inactivated SIV preparations: challenge with human- or monkey-derived SIV and the effects of a longer immunization schedule. J Med Primatol. 1993 Feb-May;22(2-3):110–118. [PubMed] [Google Scholar]
  54. Van Rompay K. K., Otsyula M. G., Tarara R. P., Canfield D. R., Berardi C. J., McChesney M. B., Marthas M. L. Vaccination of pregnant macaques protects newborns against mucosal simian immunodeficiency virus infection. J Infect Dis. 1996 Jun;173(6):1327–1335. doi: 10.1093/infdis/173.6.1327. [DOI] [PubMed] [Google Scholar]
  55. Wakrim L., Le Grand R., Vaslin B., Chéret A., Matheux F., Theodoro F., Roques P., Nicol-Jourdain I., Dormont D. Superinfection of HIV-2-preinfected macaques after rectal exposure to a primary isolate of SIVmac251. Virology. 1996 Jul 15;221(2):260–270. doi: 10.1006/viro.1996.0375. [DOI] [PubMed] [Google Scholar]
  56. Willey R. L., Smith D. H., Lasky L. A., Theodore T. S., Earl P. L., Moss B., Capon D. J., Martin M. A. In vitro mutagenesis identifies a region within the envelope gene of the human immunodeficiency virus that is critical for infectivity. J Virol. 1988 Jan;62(1):139–147. doi: 10.1128/jvi.62.1.139-147.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Wyand M. S., Manson K. H., Garcia-Moll M., Montefiori D., Desrosiers R. C. Vaccine protection by a triple deletion mutant of simian immunodeficiency virus. J Virol. 1996 Jun;70(6):3724–3733. doi: 10.1128/jvi.70.6.3724-3733.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. de Vries P., Heeney J. L., Boes J., Dings M. E., Hulskotte E. G., Dubbes R., Koornstra W., ten Haaft P., Akerblom L., Eriksson S. Protection of rhesus macaques from SIV infection by immunization with different experimental SIV vaccines. Vaccine. 1994 Nov;12(15):1443–1452. doi: 10.1016/0264-410x(94)90154-6. [DOI] [PubMed] [Google Scholar]

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