Abstract
Genetic characterization of a large number of human immunodeficiency virus type 1 (HIV-1) isolates indicates that at least 10% of all strains have mosaic genomes generated by recombination between viruses of the same or different subtypes or clades. What is not known, however, is the time between infection with the first and second HIV-1 strains as well as the time between infection with the second strain and the recombinational event. After 32 months of infection with HIV-1(LAI(IIIB)), a chimpanzee was inoculated intravenously and became infected with a subtype E strain, HIV-1(90CR402). With PCR amplification, DNA heteroduplex analysis, and DNA sequencing, both parental strains and two distinct recombinant proviruses were found in genomic DNA from lymph node tissue obtained 24 weeks after exposure to HIV-1(90CR402). These results show (i) that antiviral immune responses established by long-term infection with an HIV-1 subtype B strain did not prevent infection by a subtype E strain and (ii) that both strains actively replicated and produced sufficient quantities of virus to coinfect the same cell(s), resulting in recombinant viruses.
Full Text
The Full Text of this article is available as a PDF (271.6 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Artenstein A. W., VanCott T. C., Mascola J. R., Carr J. K., Hegerich P. A., Gaywee J., Sanders-Buell E., Robb M. L., Dayhoff D. E., Thitivichianlert S. Dual infection with human immunodeficiency virus type 1 of distinct envelope subtypes in humans. J Infect Dis. 1995 Apr;171(4):805–810. doi: 10.1093/infdis/171.4.805. [DOI] [PubMed] [Google Scholar]
- Carr J. K., Salminen M. O., Koch C., Gotte D., Artenstein A. W., Hegerich P. A., St Louis D., Burke D. S., McCutchan F. E. Full-length sequence and mosaic structure of a human immunodeficiency virus type 1 isolate from Thailand. J Virol. 1996 Sep;70(9):5935–5943. doi: 10.1128/jvi.70.9.5935-5943.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Choi D. J., Dube S., Spicer T. P., Slade H. B., Jensen F. C., Poiesz B. J. HIV type 1 isolate Z321, the strain used to make a therapeutic HIV type 1 immunogen, is intersubtype recombinant. AIDS Res Hum Retroviruses. 1997 Mar 1;13(4):357–361. doi: 10.1089/aid.1997.13.357. [DOI] [PubMed] [Google Scholar]
- Cornelissen M., Kampinga G., Zorgdrager F., Goudsmit J. Human immunodeficiency virus type 1 subtypes defined by env show high frequency of recombinant gag genes. The UNAIDS Network for HIV Isolation and Characterization. J Virol. 1996 Nov;70(11):8209–8212. doi: 10.1128/jvi.70.11.8209-8212.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Delwart E. L., Herring B., Rodrigo A. G., Mullins J. I. Genetic subtyping of human immunodeficiency virus using a heteroduplex mobility assay. PCR Methods Appl. 1995 Apr;4(5):S202–S216. doi: 10.1101/gr.4.5.s202. [DOI] [PubMed] [Google Scholar]
- Diaz R. S., Sabino E. C., Mayer A., Mosley J. W., Busch M. P. Dual human immunodeficiency virus type 1 infection and recombination in a dually exposed transfusion recipient. The Transfusion Safety Study Group. J Virol. 1995 Jun;69(6):3273–3281. doi: 10.1128/jvi.69.6.3273-3281.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Gao F., Morrison S. G., Robertson D. L., Thornton C. L., Craig S., Karlsson G., Sodroski J., Morgado M., Galvao-Castro B., von Briesen H. Molecular cloning and analysis of functional envelope genes from human immunodeficiency virus type 1 sequence subtypes A through G. The WHO and NIAID Networks for HIV Isolation and Characterization. J Virol. 1996 Mar;70(3):1651–1667. doi: 10.1128/jvi.70.3.1651-1667.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gao F., Robertson D. L., Morrison S. G., Hui H., Craig S., Decker J., Fultz P. N., Girard M., Shaw G. M., Hahn B. H. The heterosexual human immunodeficiency virus type 1 epidemic in Thailand is caused by an intersubtype (A/E) recombinant of African origin. J Virol. 1996 Oct;70(10):7013–7029. doi: 10.1128/jvi.70.10.7013-7029.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grez M., Dietrich U., Balfe P., von Briesen H., Maniar J. K., Mahambre G., Delwart E. L., Mullins J. I., Rübsamen-Waigmann H. Genetic analysis of human immunodeficiency virus type 1 and 2 (HIV-1 and HIV-2) mixed infections in India reveals a recent spread of HIV-1 and HIV-2 from a single ancestor for each of these viruses. J Virol. 1994 Apr;68(4):2161–2168. doi: 10.1128/jvi.68.4.2161-2168.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ho D. D., Neumann A. U., Perelson A. S., Chen W., Leonard J. M., Markowitz M. Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature. 1995 Jan 12;373(6510):123–126. doi: 10.1038/373123a0. [DOI] [PubMed] [Google Scholar]
- Kampinga G. A., Simonon A., Van de Perre P., Karita E., Msellati P., Goudsmit J. Primary infections with HIV-1 of women and their offspring in Rwanda: findings of heterogeneity at seroconversion, coinfection, and recombinants of HIV-1 subtypes A and C. Virology. 1997 Jan 6;227(1):63–76. doi: 10.1006/viro.1996.8318. [DOI] [PubMed] [Google Scholar]
- Kostrikis L. G., Cao Y., Ngai H., Moore J. P., Ho D. D. Quantitative analysis of serum neutralization of human immunodeficiency virus type 1 from subtypes A, B, C, D, E, F, and I: lack of direct correlation between neutralization serotypes and genetic subtypes and evidence for prevalent serum-dependent infectivity enhancement. J Virol. 1996 Jan;70(1):445–458. doi: 10.1128/jvi.70.1.445-458.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Leitner T., Escanilla D., Marquina S., Wahlberg J., Broström C., Hansson H. B., Uhlén M., Albert J. Biological and molecular characterization of subtype D, G, and A/D recombinant HIV-1 transmissions in Sweden. Virology. 1995 May 10;209(1):136–146. doi: 10.1006/viro.1995.1237. [DOI] [PubMed] [Google Scholar]
- Louwagie J., McCutchan F. E., Peeters M., Brennan T. P., Sanders-Buell E., Eddy G. A., van der Groen G., Fransen K., Gershy-Damet G. M., Deleys R. Phylogenetic analysis of gag genes from 70 international HIV-1 isolates provides evidence for multiple genotypes. AIDS. 1993 Jun;7(6):769–780. doi: 10.1097/00002030-199306000-00003. [DOI] [PubMed] [Google Scholar]
- Marquina S., Leitner T., Rabinovich R. D., Benetucci J., Libonatti O., Albert J. Coexistence of subtypes B, F, and as B/F env recombinant of HIV type 1 in Buenos Aires Argentina. AIDS Res Hum Retroviruses. 1996 Nov 20;12(17):1651–1654. doi: 10.1089/aid.1996.12.1651. [DOI] [PubMed] [Google Scholar]
- Moore J. P., Cao Y., Leu J., Qin L., Korber B., Ho D. D. Inter- and intraclade neutralization of human immunodeficiency virus type 1: genetic clades do not correspond to neutralization serotypes but partially correspond to gp120 antigenic serotypes. J Virol. 1996 Jan;70(1):427–444. doi: 10.1128/jvi.70.1.427-444.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moutouh L., Corbeil J., Richman D. D. Recombination leads to the rapid emergence of HIV-1 dually resistant mutants under selective drug pressure. Proc Natl Acad Sci U S A. 1996 Jun 11;93(12):6106–6111. doi: 10.1073/pnas.93.12.6106. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Murphy E., Korber B., Georges-Courbot M. C., You B., Pinter A., Cook D., Kieny M. P., Georges A., Mathiot C., Barré-Sinoussi F. Diversity of V3 region sequences of human immunodeficiency viruses type 1 from the central African Republic. AIDS Res Hum Retroviruses. 1993 Oct;9(10):997–1006. doi: 10.1089/aid.1993.9.997. [DOI] [PubMed] [Google Scholar]
- Perelson A. S., Neumann A. U., Markowitz M., Leonard J. M., Ho D. D. HIV-1 dynamics in vivo: virion clearance rate, infected cell life-span, and viral generation time. Science. 1996 Mar 15;271(5255):1582–1586. doi: 10.1126/science.271.5255.1582. [DOI] [PubMed] [Google Scholar]
- Ranganathan P. N., Srinivasan A. Recombination between human immunodeficiency viruses (HIV) type 1 and 2 results in generation of defective hybrid viruses. Biochem Biophys Res Commun. 1993 May 28;193(1):311–317. doi: 10.1006/bbrc.1993.1625. [DOI] [PubMed] [Google Scholar]
- Robertson D. L., Hahn B. H., Sharp P. M. Recombination in AIDS viruses. J Mol Evol. 1995 Mar;40(3):249–259. doi: 10.1007/BF00163230. [DOI] [PubMed] [Google Scholar]
- Robertson D. L., Sharp P. M., McCutchan F. E., Hahn B. H. Recombination in HIV-1. Nature. 1995 Mar 9;374(6518):124–126. doi: 10.1038/374124b0. [DOI] [PubMed] [Google Scholar]
- Sabino E. C., Shpaer E. G., Morgado M. G., Korber B. T., Diaz R. S., Bongertz V., Cavalcante S., Galvão-Castro B., Mullins J. I., Mayer A. Identification of human immunodeficiency virus type 1 envelope genes recombinant between subtypes B and F in two epidemiologically linked individuals from Brazil. J Virol. 1994 Oct;68(10):6340–6346. doi: 10.1128/jvi.68.10.6340-6346.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sala M., Zambruno G., Vartanian J. P., Marconi A., Bertazzoni U., Wain-Hobson S. Spatial discontinuities in human immunodeficiency virus type 1 quasispecies derived from epidermal Langerhans cells of a patient with AIDS and evidence for double infection. J Virol. 1994 Aug;68(8):5280–5283. doi: 10.1128/jvi.68.8.5280-5283.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Salminen M. O., Carr J. K., Robertson D. L., Hegerich P., Gotte D., Koch C., Sanders-Buell E., Gao F., Sharp P. M., Hahn B. H. Evolution and probable transmission of intersubtype recombinant human immunodeficiency virus type 1 in a Zambian couple. J Virol. 1997 Apr;71(4):2647–2655. doi: 10.1128/jvi.71.4.2647-2655.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schnittman S. M., Greenhouse J. J., Lane H. C., Pierce P. F., Fauci A. S. Frequent detection of HIV-1-specific mRNAs in infected individuals suggests ongoing active viral expression in all stages of disease. AIDS Res Hum Retroviruses. 1991 Apr;7(4):361–367. doi: 10.1089/aid.1991.7.361. [DOI] [PubMed] [Google Scholar]
- Wei X., Ghosh S. K., Taylor M. E., Johnson V. A., Emini E. A., Deutsch P., Lifson J. D., Bonhoeffer S., Nowak M. A., Hahn B. H. Viral dynamics in human immunodeficiency virus type 1 infection. Nature. 1995 Jan 12;373(6510):117–122. doi: 10.1038/373117a0. [DOI] [PubMed] [Google Scholar]
- Zhu T., Wang N., Carr A., Wolinsky S., Ho D. D. Evidence for coinfection by multiple strains of human immunodeficiency virus type 1 subtype B in an acute seroconvertor. J Virol. 1995 Feb;69(2):1324–1327. doi: 10.1128/jvi.69.2.1324-1327.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
