Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1996 Jan;70(1):617–622. doi: 10.1128/jvi.70.1.617-622.1996

Vaccination protects against in vivo-grown feline immunodeficiency virus even in the absence of detectable neutralizing antibodies.

D Matteucci 1, M Pistello 1, P Mazzetti 1, S Giannecchini 1, D Del Mauro 1, L Zaccaro 1, P Bandecchi 1, F Tozzini 1, M Bendinelli 1
PMCID: PMC189855  PMID: 8523581

Abstract

So far, vaccination experiments against feline immunodeficiency virus have used in vitro-grown virus to challenge the vaccinated hosts. In this study, cats were vaccinated with fixed feline immunodeficiency virus-infected cells and challenged with plasma obtained from cats infected with the homologous virus diluted to contain 10 cat 50% infectious doses. As judged by virus culture, PCRs, and serological analyses performed over an 18-month period after the challenge, all of the vaccinated cats were clearly protected. Interestingly, prior to challenge most vaccines lacked antibodies capable of neutralizing a fresh isolate of the homologous virus.

Full Text

The Full Text of this article is available as a PDF (210.5 KB).

Selected References

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

  1. 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]
  2. Arthur L. O., Bess J. W., Jr, Sowder R. C., 2nd, Benveniste R. E., Mann D. L., Chermann J. C., Henderson L. E. Cellular proteins bound to immunodeficiency viruses: implications for pathogenesis and vaccines. Science. 1992 Dec 18;258(5090):1935–1938. doi: 10.1126/science.1470916. [DOI] [PubMed] [Google Scholar]
  3. Avrameas A., Guillet J. G., Chouchane L., Moraillon A., Sonigo P., Strosberg A. D. Localisation of three epitopes of the env protein of feline immunodeficiency virus. Mol Immunol. 1992 May;29(5):565–572. doi: 10.1016/0161-5890(92)90192-z. [DOI] [PubMed] [Google Scholar]
  4. Baldinotti F., Matteucci D., Mazzetti P., Giannelli C., Bandecchi P., Tozzini F., Bendinelli M. Serum neutralization of feline immunodeficiency virus is markedly dependent on passage history of the virus and host system. J Virol. 1994 Jul;68(7):4572–4579. doi: 10.1128/jvi.68.7.4572-4579.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Beebe A. M., Dua N., Faith T. G., Moore P. F., Pedersen N. C., Dandekar S. Primary stage of feline immunodeficiency virus infection: viral dissemination and cellular targets. J Virol. 1994 May;68(5):3080–3091. doi: 10.1128/jvi.68.5.3080-3091.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bendinelli M., Pistello M., Lombardi S., Poli A., Garzelli C., Matteucci D., Ceccherini-Nelli L., Malvaldi G., Tozzini F. Feline immunodeficiency virus: an interesting model for AIDS studies and an important cat pathogen. Clin Microbiol Rev. 1995 Jan;8(1):87–112. doi: 10.1128/cmr.8.1.87. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bergmeier L. A., Walker J., Tao L., Cranage M., Lehner T. Antibodies to human and non-human primate cellular and culture medium components in macaques vaccinated with the simian immunodeficiency virus. Immunology. 1994 Oct;83(2):213–220. [PMC free article] [PubMed] [Google Scholar]
  8. Cease K. B., Berzofsky J. A. Toward a vaccine for AIDS: the emergence of immunobiology-based vaccine development. Annu Rev Immunol. 1994;12:923–989. doi: 10.1146/annurev.iy.12.040194.004423. [DOI] [PubMed] [Google Scholar]
  9. Cohen J. Jitters jeopardize AIDS vaccine trials. Science. 1993 Nov 12;262(5136):980–981. doi: 10.1126/science.8235635. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Desrosiers R. C. Safety issues facing development of a live-attenuated, multiply deleted HIV-1 vaccine. AIDS Res Hum Retroviruses. 1994 Apr;10(4):331–332. doi: 10.1089/aid.1994.10.331. [DOI] [PubMed] [Google Scholar]
  12. English R. V., Nelson P., Johnson C. M., Nasisse M., Tompkins W. A., Tompkins M. B. Development of clinical disease in cats experimentally infected with feline immunodeficiency virus. J Infect Dis. 1994 Sep;170(3):543–552. doi: 10.1093/infdis/170.3.543. [DOI] [PubMed] [Google Scholar]
  13. Flynn J. N., Cannon C. A., Beatty J. A., Mackett M., Rigby M. A., Neil J. C., Jarrett C. Induction of feline immunodeficiency virus-specific cytotoxic T cells in vivo with carrier-free synthetic peptide. J Virol. 1994 Sep;68(9):5835–5844. doi: 10.1128/jvi.68.9.5835-5844.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gardner M. B. Simian and feline immunodeficiency viruses: animal lentivirus models for evaluation of AIDS vaccines and antiviral agents. Antiviral Res. 1991 May;15(4):267–286. doi: 10.1016/0166-3542(91)90009-g. [DOI] [PubMed] [Google Scholar]
  15. Golding H., D'Souza M. P., Bradac J., Mathieson B., Fast P. Neutralization of HIV-1. AIDS Res Hum Retroviruses. 1994 Jun;10(6):633–643. doi: 10.1089/aid.1994.10.633. [DOI] [PubMed] [Google Scholar]
  16. Haynes B. F. Scientific and social issues of human immunodeficiency virus vaccine development. Science. 1993 May 28;260(5112):1279–1286. doi: 10.1126/science.8493572. [DOI] [PubMed] [Google Scholar]
  17. Hosie M. J., Osborne R., Reid G., Neil J. C., Jarrett O. Enhancement after feline immunodeficiency virus vaccination. Vet Immunol Immunopathol. 1992 Dec;35(1-2):191–197. doi: 10.1016/0165-2427(93)90149-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hosie M. J., Osborne R., Yamamoto J. K., Neil J. C., Jarrett O. Protection against homologous but not heterologous challenge induced by inactivated feline immunodeficiency virus vaccines. J Virol. 1995 Feb;69(2):1253–1255. doi: 10.1128/jvi.69.2.1253-1255.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hosie M. J. The development of a vaccine against feline immunodeficiency virus. Br Vet J. 1994 Jan-Feb;150(1):25–39. doi: 10.1016/S0007-1935(05)80094-6. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Kabat D., Kozak S. L., Wehrly K., Chesebro B. Differences in CD4 dependence for infectivity of laboratory-adapted and primary patient isolates of human immunodeficiency virus type 1. J Virol. 1994 Apr;68(4):2570–2577. doi: 10.1128/jvi.68.4.2570-2577.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kusumi K., Conway B., Cunningham S., Berson A., Evans C., Iversen A. K., Colvin D., Gallo M. V., Coutre S., Shpaer E. G. Human immunodeficiency virus type 1 envelope gene structure and diversity in vivo and after cocultivation in vitro. J Virol. 1992 Feb;66(2):875–885. doi: 10.1128/jvi.66.2.875-885.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Langlois A. J., Weinhold K. J., Matthews T. J., Greenberg M. L., Bolognesi D. P. The ability of certain SIV vaccines to provoke reactions against normal cells. Science. 1992 Jan 17;255(5042):292–293. doi: 10.1126/science.1549775. [DOI] [PubMed] [Google Scholar]
  24. Layne S. P., Merges M. J., Dembo M., Spouge J. L., Conley S. R., Moore J. P., Raina J. L., Renz H., Gelderblom H. R., Nara P. L. Factors underlying spontaneous inactivation and susceptibility to neutralization of human immunodeficiency virus. Virology. 1992 Aug;189(2):695–714. doi: 10.1016/0042-6822(92)90593-e. [DOI] [PubMed] [Google Scholar]
  25. Lombardi S., Garzelli C., La Rosa C., Zaccaro L., Specter S., Malvaldi G., Tozzini F., Esposito F., Bendinelli M. Identification of a linear neutralization site within the third variable region of the feline immunodeficiency virus envelope. J Virol. 1993 Aug;67(8):4742–4749. doi: 10.1128/jvi.67.8.4742-4749.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lombardi S., Garzelli C., Pistello M., Massi C., Matteucci D., Baldinotti F., Cammarota G., da Prato L., Bandecchi P., Tozzini F. A neutralizing antibody-inducing peptide of the V3 domain of feline immunodeficiency virus envelope glycoprotein does not induce protective immunity. J Virol. 1994 Dec;68(12):8374–8379. doi: 10.1128/jvi.68.12.8374-8379.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lombardi S., Poli A., Massi C., Abramo F., Zaccaro L., Bazzichi A., Malvaldi G., Bendinelli M., Garzelli C. Detection of feline immunodeficiency virus p24 antigen and p24-specific antibodies by monoclonal antibody-based assays. J Virol Methods. 1994 Mar;46(3):287–301. doi: 10.1016/0166-0934(94)90001-9. [DOI] [PubMed] [Google Scholar]
  28. Lutz H., Hofmann-Lehmann R., Bauer-Pham K., Holznagel E., Tozzini F., Bendinelli M., Reubel G., Aubert A., Davis D., Cox D. FIV vaccine studies. I. Immune response to recombinant FIV env gene products and outcome after challenge infection. Vet Immunol Immunopathol. 1995 May;46(1-2):103–113. doi: 10.1016/0165-2427(94)07010-5. [DOI] [PubMed] [Google Scholar]
  29. Mascola J. R., Louwagie J., McCutchan F. E., Fischer C. L., Hegerich P. A., Wagner K. F., Fowler A. K., McNeil J. G., Burke D. S. Two antigenically distinct subtypes of human immunodeficiency virus type 1: viral genotype predicts neutralization serotype. J Infect Dis. 1994 Jan;169(1):48–54. doi: 10.1093/infdis/169.1.48. [DOI] [PubMed] [Google Scholar]
  30. Matteucci D., Baldinotti F., Mazzetti P., Pistello M., Bandecchi P., Ghilarducci R., Poli A., Tozzini F., Bendinelli M. Detection of feline immunodeficiency virus in saliva and plasma by cultivation and polymerase chain reaction. J Clin Microbiol. 1993 Mar;31(3):494–501. doi: 10.1128/jcm.31.3.494-501.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Matteucci D., Mazzetti P., Baldinotti F., Zaccaro L., Bendinelli M. The feline lymphoid cell line MBM and its use for feline immunodeficiency virus isolation and quantitation. Vet Immunol Immunopathol. 1995 May;46(1-2):71–82. doi: 10.1016/0165-2427(94)07007-t. [DOI] [PubMed] [Google Scholar]
  32. Moore J. P., Cao Y., Qing L., Sattentau Q. J., Pyati J., Koduri R., Robinson J., Barbas C. F., 3rd, Burton D. R., Ho D. D. Primary isolates of human immunodeficiency virus type 1 are relatively resistant to neutralization by monoclonal antibodies to gp120, and their neutralization is not predicted by studies with monomeric gp120. J Virol. 1995 Jan;69(1):101–109. doi: 10.1128/jvi.69.1.101-109.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Murphey-Corb M., Martin L. N., Davison-Fairburn B., Montelaro R. C., Miller M., West M., Ohkawa S., Baskin G. B., Zhang J. Y., Putney S. D. A formalin-inactivated whole SIV vaccine confers protection in macaques. Science. 1989 Dec 8;246(4935):1293–1297. doi: 10.1126/science.2555923. [DOI] [PubMed] [Google Scholar]
  34. Orentas R. J., Hildreth J. E. Association of host cell surface adhesion receptors and other membrane proteins with HIV and SIV. AIDS Res Hum Retroviruses. 1993 Nov;9(11):1157–1165. doi: 10.1089/aid.1993.9.1157. [DOI] [PubMed] [Google Scholar]
  35. Pedersen N. C., Ho E. W., Brown M. L., Yamamoto J. K. Isolation of a T-lymphotropic virus from domestic cats with an immunodeficiency-like syndrome. Science. 1987 Feb 13;235(4790):790–793. doi: 10.1126/science.3643650. [DOI] [PubMed] [Google Scholar]
  36. Pistello M., Menzo S., Giorgi M., Da Prato L., Cammarota G., Clementi M., Bendinelli M. Competitive polymerase chain reaction for quantitating feline immunodeficiency virus load in infected cat tissues. Mol Cell Probes. 1994 Jun;8(3):229–234. doi: 10.1006/mcpr.1994.1032. [DOI] [PubMed] [Google Scholar]
  37. Rigby M. A., Holmes E. C., Pistello M., Mackay A., Brown A. J., Neil J. C. Evolution of structural proteins of feline immunodeficiency virus: molecular epidemiology and evidence of selection for change. J Gen Virol. 1993 Mar;74(Pt 3):425–436. doi: 10.1099/0022-1317-74-3-425. [DOI] [PubMed] [Google Scholar]
  38. Saifuddin M., Ghassemi M., Patki C., Parker C. J., Spear G. T. Host cell components affect the sensitivity of HIV type 1 to complement-mediated virolysis. AIDS Res Hum Retroviruses. 1994 Jul;10(7):829–837. doi: 10.1089/aid.1994.10.829. [DOI] [PubMed] [Google Scholar]
  39. Sawyer L. S., Wrin M. T., Crawford-Miksza L., Potts B., Wu Y., Weber P. A., Alfonso R. D., Hanson C. V. Neutralization sensitivity of human immunodeficiency virus type 1 is determined in part by the cell in which the virus is propagated. J Virol. 1994 Mar;68(3):1342–1349. doi: 10.1128/jvi.68.3.1342-1349.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Siebelink K. H., Tijhaar E., Huisman R. C., Huisman W., de Ronde A., Darby I. H., Francis M. J., Rimmelzwaan G. F., Osterhaus A. D. Enhancement of feline immunodeficiency virus infection after immunization with envelope glycoprotein subunit vaccines. J Virol. 1995 Jun;69(6):3704–3711. doi: 10.1128/jvi.69.6.3704-3711.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Sodora D. L., Shpaer E. G., Kitchell B. E., Dow S. W., Hoover E. A., Mullins J. I. Identification of three feline immunodeficiency virus (FIV) env gene subtypes and comparison of the FIV and human immunodeficiency virus type 1 evolutionary patterns. J Virol. 1994 Apr;68(4):2230–2238. doi: 10.1128/jvi.68.4.2230-2238.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Stott E. J. Towards a vaccine against AIDS: lessons from simian immunodeficiency virus vaccines. Curr Top Microbiol Immunol. 1994;188:221–237. doi: 10.1007/978-3-642-78536-8_12. [DOI] [PubMed] [Google Scholar]
  43. Tozzini F., Matteucci D., Bandecchi P., Baldinotti F., Siebelink K., Osterhaus A., Bendinelli M. Neutralizing antibodies in cats infected with feline immunodeficiency virus. J Clin Microbiol. 1993 Jun;31(6):1626–1629. doi: 10.1128/jcm.31.6.1626-1629.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Verschoor E. J., van Vliet A. L., Egberink H. F., Hesselink W., van Alphen W. E., Joosten I., Boog C. J., Horzinek M. C., de Ronde A. Vaccination against feline immunodeficiency virus using fixed infected cells. Vet Immunol Immunopathol. 1995 May;46(1-2):139–149. doi: 10.1016/0165-2427(94)07013-w. [DOI] [PubMed] [Google Scholar]
  45. Wrin T., Loh T. P., Vennari J. C., Schuitemaker H., Nunberg J. H. Adaptation to persistent growth in the H9 cell line renders a primary isolate of human immunodeficiency virus type 1 sensitive to neutralization by vaccine sera. J Virol. 1995 Jan;69(1):39–48. doi: 10.1128/jvi.69.1.39-48.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Yamamoto J. K., Ackley C. D., Zochlinski H., Louie H., Pembroke E., Torten M., Hansen H., Munn R., Okuda T. Development of IL-2-independent feline lymphoid cell lines chronically infected with feline immunodeficiency virus: importance for diagnostic reagents and vaccines. Intervirology. 1991;32(6):361–375. doi: 10.1159/000150220. [DOI] [PubMed] [Google Scholar]
  47. Yamamoto J. K., Hohdatsu T., Olmsted R. A., Pu R., Louie H., Zochlinski H. A., Acevedo V., Johnson H. M., Soulds G. A., Gardner M. B. Experimental vaccine protection against homologous and heterologous strains of feline immunodeficiency virus. J Virol. 1993 Jan;67(1):601–605. doi: 10.1128/jvi.67.1.601-605.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Yamamoto J. K., Okuda T., Ackley C. D., Louie H., Pembroke E., Zochlinski H., Munn R. J., Gardner M. B. Experimental vaccine protection against feline immunodeficiency virus. AIDS Res Hum Retroviruses. 1991 Nov;7(11):911–922. doi: 10.1089/aid.1991.7.911. [DOI] [PubMed] [Google Scholar]

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

RESOURCES