Abstract
The relative infectiousness of laboratory and primary human immunodeficiency virus type 1 (HIV-1) variants was evaluated in in vitro cell cultures of peripheral blood mononuclear cells or MT-2 cells and in Hu-PBL-SCID mice. HIV(MN) and syncytium-inducing primary isolates were preferentially transmitted to cells in tissue culture. HIV(Ba-L) and non-syncytium-inducing (NSI) primary isolates were more infectious in Hu-PBL-SCID mice. Phylogenetic analysis of env sequences derived from the primary isolates, from the cell cultures, and from five Hu-PBL-SCID mice was performed by using methods designed for resolving differences among closely related sequence pairs. This analysis demonstrated preferential transmission of an evolutionarily related subset of NSI variants to Hu-PBL-SCID mice. The pattern of selective transmission of a restricted range of NSI variants that is observed in the clinical setting is maintained in Hu-PBL-SCID mice and not in tissue culture systems. The Hu-PBL-SCID mouse model system, when used with appropriate phylogenetic analysis methodologies, will be useful for identifying and characterizing the more infectious HIV-1 variants that should be targeted for vaccine development.
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- Bukrinsky M. I., Sharova N., Dempsey M. P., Stanwick T. L., Bukrinskaya A. G., Haggerty S., Stevenson M. Active nuclear import of human immunodeficiency virus type 1 preintegration complexes. Proc Natl Acad Sci U S A. 1992 Jul 15;89(14):6580–6584. doi: 10.1073/pnas.89.14.6580. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bukrinsky M. I., Stanwick T. L., Dempsey M. P., Stevenson M. Quiescent T lymphocytes as an inducible virus reservoir in HIV-1 infection. Science. 1991 Oct 18;254(5030):423–427. doi: 10.1126/science.1925601. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Crandall K. A. Intraspecific phylogenetics: support for dental transmission of human immunodeficiency virus. J Virol. 1995 Apr;69(4):2351–2356. doi: 10.1128/jvi.69.4.2351-2356.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DeBry R. W., Abele L. G., Weiss S. H., Hill M. D., Bouzas M., Lorenzo E., Graebnitz F., Resnick L. Dental HIV transmission? Nature. 1993 Feb 25;361(6414):691–691. doi: 10.1038/361691a0. [DOI] [PubMed] [Google Scholar]
- Delwart E. L., Sheppard H. W., Walker B. D., Goudsmit J., Mullins J. I. Human immunodeficiency virus type 1 evolution in vivo tracked by DNA heteroduplex mobility assays. J Virol. 1994 Oct;68(10):6672–6683. doi: 10.1128/jvi.68.10.6672-6683.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Evans R. L., Faldetta T. J., Humphreys R. E., Pratt D. M., Yunis E. J., Schlossman S. F. Peripheral human T cells sensitized in mixed leukocyte culture synthesize and express Ia-like antigens. J Exp Med. 1978 Nov 1;148(5):1440–1445. doi: 10.1084/jem.148.5.1440. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hercend T., Ritz J., Schlossman S. F., Reinherz E. L. Comparative expression of T9, T10, and Ia antigens on activated human T cell subsets. Hum Immunol. 1981 Nov;3(3):247–259. doi: 10.1016/0198-8859(81)90021-5. [DOI] [PubMed] [Google Scholar]
- Holmes E. C., Zhang L. Q., Robertson P., Cleland A., Harvey E., Simmonds P., Leigh Brown A. J. The molecular epidemiology of human immunodeficiency virus type 1 in Edinburgh. J Infect Dis. 1995 Jan;171(1):45–53. doi: 10.1093/infdis/171.1.45. [DOI] [PubMed] [Google Scholar]
- Koot M., Keet I. P., Vos A. H., de Goede R. E., Roos M. T., Coutinho R. A., Miedema F., Schellekens P. T., Tersmette M. Prognostic value of HIV-1 syncytium-inducing phenotype for rate of CD4+ cell depletion and progression to AIDS. Ann Intern Med. 1993 May 1;118(9):681–688. doi: 10.7326/0003-4819-118-9-199305010-00004. [DOI] [PubMed] [Google Scholar]
- Korber B., Wolinsky S., Haynes B., Kunstman K., Levy R., Furtado M., Otto P., Myers G. HIV-1 intrapatient sequence diversity in the immunogenic V3 region. AIDS Res Hum Retroviruses. 1992 Aug;8(8):1461–1465. doi: 10.1089/aid.1992.8.1461. [DOI] [PubMed] [Google Scholar]
- Lukashov V. V., Kuiken C. L., Goudsmit J. Intrahost human immunodeficiency virus type 1 evolution is related to length of the immunocompetent period. J Virol. 1995 Nov;69(11):6911–6916. doi: 10.1128/jvi.69.11.6911-6916.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mahalingam M., Peakman M., Davies E. T., Pozniak A., McManus T. J., Vergani D. T cell activation and disease severity in HIV infection. Clin Exp Immunol. 1993 Sep;93(3):337–343. doi: 10.1111/j.1365-2249.1993.tb08182.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Markham R. B., Yu X., Farzadegan H., Ray S. C., Vlahov D. Human immunodeficiency virus type 1 env and p17gag sequence variation in polymerase chain reaction-positive, seronegative injection drug users. J Infect Dis. 1995 Apr;171(4):797–804. doi: 10.1093/infdis/171.4.797. [DOI] [PubMed] [Google Scholar]
- McNearney T., Hornickova Z., Kloster B., Birdwell A., Storch G. A., Polmar S. H., Arens M., Ratner L. Evolution of sequence divergence among human immunodeficiency virus type 1 isolates derived from a blood donor and a recipient. Pediatr Res. 1993 Jan;33(1):36–42. doi: 10.1203/00006450-199301000-00008. [DOI] [PubMed] [Google Scholar]
- Mosier D. E., Gulizia R. J., Baird S. M., Wilson D. B., Spector D. H., Spector S. A. Human immunodeficiency virus infection of human-PBL-SCID mice. Science. 1991 Feb 15;251(4995):791–794. doi: 10.1126/science.1990441. [DOI] [PubMed] [Google Scholar]
- Mosier D. E., Gulizia R. J., Baird S. M., Wilson D. B. Transfer of a functional human immune system to mice with severe combined immunodeficiency. Nature. 1988 Sep 15;335(6187):256–259. doi: 10.1038/335256a0. [DOI] [PubMed] [Google Scholar]
- Mosier D. E., Gulizia R. J., MacIsaac P. D., Torbett B. E., Levy J. A. Rapid loss of CD4+ T cells in human-PBL-SCID mice by noncytopathic HIV isolates. Science. 1993 Apr 30;260(5108):689–692. doi: 10.1126/science.8097595. [DOI] [PubMed] [Google Scholar]
- Nielsen C., Pedersen C., Lundgren J. D., Gerstoft J. Biological properties of HIV isolates in primary HIV infection: consequences for the subsequent course of infection. AIDS. 1993 Aug;7(8):1035–1040. doi: 10.1097/00002030-199308000-00002. [DOI] [PubMed] [Google Scholar]
- Ou C. Y., Ciesielski C. A., Myers G., Bandea C. I., Luo C. C., Korber B. T., Mullins J. I., Schochetman G., Berkelman R. L., Economou A. N. Molecular epidemiology of HIV transmission in a dental practice. Science. 1992 May 22;256(5060):1165–1171. doi: 10.1126/science.256.5060.1165. [DOI] [PubMed] [Google Scholar]
- Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tary-Lehmann M., Lehmann P. V., Schols D., Roncarolo M. G., Saxon A. Anti-SCID mouse reactivity shapes the human CD4+ T cell repertoire in hu-PBL-SCID chimeras. J Exp Med. 1994 Nov 1;180(5):1817–1827. doi: 10.1084/jem.180.5.1817. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tary-Lehmann M., Saxon A. Human mature T cells that are anergic in vivo prevail in SCID mice reconstituted with human peripheral blood. J Exp Med. 1992 Feb 1;175(2):503–516. doi: 10.1084/jem.175.2.503. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Templeton A. R., Boerwinkle E., Sing C. F. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. I. Basic theory and an analysis of alcohol dehydrogenase activity in Drosophila. Genetics. 1987 Oct;117(2):343–351. doi: 10.1093/genetics/117.2.343. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Templeton A. R., Crandall K. A., Sing C. F. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics. 1992 Oct;132(2):619–633. doi: 10.1093/genetics/132.2.619. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Templeton A. R., Sing C. F. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. IV. Nested analyses with cladogram uncertainty and recombination. Genetics. 1993 Jun;134(2):659–669. doi: 10.1093/genetics/134.2.659. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wysocki L. J., Sato V. L. "Panning" for lymphocytes: a method for cell selection. Proc Natl Acad Sci U S A. 1978 Jun;75(6):2844–2848. doi: 10.1073/pnas.75.6.2844. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zack J. A., Arrigo S. J., Weitsman S. R., Go A. S., Haislip A., Chen I. S. HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell. 1990 Apr 20;61(2):213–222. doi: 10.1016/0092-8674(90)90802-l. [DOI] [PubMed] [Google Scholar]
- Zhang L. Q., MacKenzie P., Cleland A., Holmes E. C., Brown A. J., Simmonds P. Selection for specific sequences in the external envelope protein of human immunodeficiency virus type 1 upon primary infection. J Virol. 1993 Jun;67(6):3345–3356. doi: 10.1128/jvi.67.6.3345-3356.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhu T., Mo H., Wang N., Nam D. S., Cao Y., Koup R. A., Ho D. D. Genotypic and phenotypic characterization of HIV-1 patients with primary infection. Science. 1993 Aug 27;261(5125):1179–1181. doi: 10.1126/science.8356453. [DOI] [PubMed] [Google Scholar]