Europe PMC

This website requires cookies, and the limited processing of your personal data in order to function. By using the site you are agreeing to this as outlined in our privacy notice and cookie policy.

Evolution and probable transmission of intersubtype recombinant human immunodeficiency virus type 1 in a Zambian couple.

Author information

Affiliations

  • 1. Henry M. Jackson Foundation and Division of Retrovirology, Walter Reed Army Institute of Research, Rockville, Maryland 20850, USA.
      Authors
    • Salminen MO 1
    (1 author)

Journal of Virology, 01 Apr 1997, 71(4):2647-2655
https://doi.org/10.1128/jvi.71.4.2647-2655.1997 PMID: 9060617 PMCID: PMC191386

Free full text in Europe PMC

Abstract 

The extraordinary genetic diversity of human immunodeficiency virus type 1 (HIV-1) results from the introduction of mutations by an error-prone reverse transcriptase and from recombination of the two RNA genomes packaged in the virion during the synthesis of proviral DNA. The occurrence of multiple, genetically distant HIV-1 subtypes and their geographic intermixing set up conditions for dramatic, rather than gradual, changes in genotype whenever genomes from different subtypes are copackaged in virions. Here we describe, for the first time, the sequential generation of multiple different, but related, intersubtype HIV-1 recombinants within an infected individual. Full-length gag and env genes were recovered directly from peripheral blood mononuclear cells or from primary virus cultures, using serial blood samples from a Zambian woman and a sample from her spouse. DNA sequencing and phylogenetic analysis established that two different A/C recombinant forms of HIV-1 predominated at two time points in the woman. A related but distinct recombinant HIV-1 was recovered from her spouse. Intersubtype recombination apparently played a central role in the evolution of HIV-1 in this couple and may contribute substantially to the rapid emergence of HIV-1 variants whenever mixed-subtype HIV-1 infections occur.

Free full text 

Logo of jvirolLink to Publisher's site
PMCID: PMC191386
PMID: 9060617

Evolution and probable transmission of intersubtype recombinant human immunodeficiency virus type 1 in a Zambian couple.

M O Salminen, J K Carr, D L Robertson, P Hegerich, D Gotte, C Koch, E Sanders-Buell, F Gao, P M Sharp, B H Hahn, D S Burke, and F E McCutchan
Author information Copyright and License information Disclaimer

Abstract

The extraordinary genetic diversity of human immunodeficiency virus type 1 (HIV-1) results from the introduction of mutations by an error-prone reverse transcriptase and from recombination of the two RNA genomes packaged in the virion during the synthesis of proviral DNA. The occurrence of multiple, genetically distant HIV-1 subtypes and their geographic intermixing set up conditions for dramatic, rather than gradual, changes in genotype whenever genomes from different subtypes are copackaged in virions. Here we describe, for the first time, the sequential generation of multiple different, but related, intersubtype HIV-1 recombinants within an infected individual. Full-length gag and env genes were recovered directly from peripheral blood mononuclear cells or from primary virus cultures, using serial blood samples from a Zambian woman and a sample from her spouse. DNA sequencing and phylogenetic analysis established that two different A/C recombinant forms of HIV-1 predominated at two time points in the woman. A related but distinct recombinant HIV-1 was recovered from her spouse. Intersubtype recombination apparently played a central role in the evolution of HIV-1 in this couple and may contribute substantially to the rapid emergence of HIV-1 variants whenever mixed-subtype HIV-1 infections occur.

Full Text

The Full Text of this article is available as a PDF (236K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Brodine SK, Mascola JR, Weiss PJ, Ito SI, Porter KR, Artenstein AW, Garland FC, McCutchan FE, Burke DS. Detection of diverse HIV-1 genetic subtypes in the USA. Lancet. 1995 Nov 4;346(8984):1198–1199. [Abstract] [Google Scholar]
  • Burke DS, Redfield RR, Bjornson DC, Fowler AK, Oster CN. Frequent isolation of HIV-1 from the blood of patients receiving zidovudine (AZT) therapy. N Engl J Med. 1989 Dec 14;321(24):1682–1682. [Abstract] [Google Scholar]
  • Campodonico M, Janssens W, Heyndrickx L, Fransen K, Leonaers A, Fay FF, Taborda M, Van der Groen G, Fay OH. HIV type 1 subtypes in Argentina and genetic heterogeneity of the V3 region. AIDS Res Hum Retroviruses. 1996 Jan 1;12(1):79–81. [Abstract] [Google Scholar]
  • Carr JK, Salminen MO, Koch C, Gotte D, Artenstein AW, Hegerich PA, St Louis D, Burke DS, McCutchan FE. Full-length sequence and mosaic structure of a human immunodeficiency virus type 1 isolate from Thailand. J Virol. 1996 Sep;70(9):5935–5943. [Europe PMC free article] [Abstract] [Google Scholar]
  • Clewley JP, Arnold C, Barlow KL, Grant PR, Parry JV. Diverse HIV-1 genetic subtypes in UK. Lancet. 1996 May 25;347(9013):1487–1487. [Abstract] [Google Scholar]
  • Coffin JM. Structure, replication, and recombination of retrovirus genomes: some unifying hypotheses. J Gen Virol. 1979 Jan;42(1):1–26. [Abstract] [Google Scholar]
  • Diaz RS, Sabino EC, Mayer A, Mosley JW, Busch MP. 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. [Europe PMC free article] [Abstract] [Google Scholar]
  • Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol. 1981;17(6):368–376. [Abstract] [Google Scholar]
  • Felsenstein J. Phylogenies from molecular sequences: inference and reliability. Annu Rev Genet. 1988;22:521–565. [Abstract] [Google Scholar]
  • Fransen K, Buvé A, Nkengasong JN, Laga M, van der Groen G. Longstanding presence in Belgians of multiple non-B HIV-1 subtypes. Lancet. 1996 May 18;347(9012):1403–1403. [Abstract] [Google Scholar]
  • Gao F, Robertson DL, Morrison SG, Hui H, Craig S, Decker J, Fultz PN, Girard M, Shaw GM, Hahn BH, et al. 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. [Europe PMC free article] [Abstract] [Google Scholar]
  • Gao F, Morrison SG, Robertson DL, Thornton CL, Craig S, Karlsson G, Sodroski J, Morgado M, Galvao-Castro B, von Briesen H, et al. 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. [Europe PMC free article] [Abstract] [Google Scholar]
  • Golovkina TV, Jaffe AB, Ross SR. Coexpression of exogenous and endogenous mouse mammary tumor virus RNA in vivo results in viral recombination and broadens the virus host range. J Virol. 1994 Aug;68(8):5019–5026. [Europe PMC free article] [Abstract] [Google Scholar]
  • Goodrich DW, Duesberg PH. Retroviral recombination during reverse transcription. Proc Natl Acad Sci U S A. 1990 Mar;87(6):2052–2056. [Europe PMC free article] [Abstract] [Google Scholar]
  • Gürtler LG, Hauser PH, Eberle J, von Brunn A, Knapp S, Zekeng L, Tsague JM, Kaptue L. A new subtype of human immunodeficiency virus type 1 (MVP-5180) from Cameroon. J Virol. 1994 Mar;68(3):1581–1585. [Europe PMC free article] [Abstract] [Google Scholar]
  • Hampl H, Sawitzky D, Stöffler-Meilicke M, Groh A, Schmitt M, Eberle J, Gürtler L. First case of HIV-1 subtype 0 infection in Germany. Infection. 1995 Nov-Dec;23(6):369–370. [Abstract] [Google Scholar]
  • Hu WS, Temin HM. Retroviral recombination and reverse transcription. Science. 1990 Nov 30;250(4985):1227–1233. [Abstract] [Google Scholar]
  • Janssens W, Heyndrickx L, Fransen K, Temmerman M, Leonaers A, Ivens T, Motte J, Piot P, Van der Groen G. Genetic variability of HIV type 1 in Kenya. AIDS Res Hum Retroviruses. 1994 Nov;10(11):1577–1579. [Abstract] [Google Scholar]
  • Katz RA, Skalka AM. Generation of diversity in retroviruses. Annu Rev Genet. 1990;24:409–445. [Abstract] [Google Scholar]
  • Kellam P, Larder BA. Retroviral recombination can lead to linkage of reverse transcriptase mutations that confer increased zidovudine resistance. J Virol. 1995 Feb;69(2):669–674. [Europe PMC free article] [Abstract] [Google Scholar]
  • Kostrikis LG, Bagdades E, Cao Y, Zhang L, Dimitriou D, Ho DD. Genetic analysis of human immunodeficiency virus type 1 strains from patients in Cyprus: identification of a new subtype designated subtype I. J Virol. 1995 Oct;69(10):6122–6130. [Europe PMC free article] [Abstract] [Google Scholar]
  • Leitner T, Escanilla D, Marquina S, Wahlberg J, Broström C, Hansson HB, 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. [Abstract] [Google Scholar]
  • Li H, Schmidt L, Wei MH, Hustad T, Lerman MI, Zbar B, Tory K. Three tetranucleotide polymorphisms for loci: D3S1352; D3S1358; D3S1359. Hum Mol Genet. 1993 Aug;2(8):1327–1327. [Abstract] [Google Scholar]
  • Louwagie J, Janssens W, Mascola J, Heyndrickx L, Hegerich P, van der Groen G, McCutchan FE, Burke DS. Genetic diversity of the envelope glycoprotein from human immunodeficiency virus type 1 isolates of African origin. J Virol. 1995 Jan;69(1):263–271. [Europe PMC free article] [Abstract] [Google Scholar]
  • Louwagie J, McCutchan FE, Peeters M, Brennan TP, Sanders-Buell E, Eddy GA, van der Groen G, Fransen K, Gershy-Damet GM, Deleys R, et al. Phylogenetic analysis of gag genes from 70 international HIV-1 isolates provides evidence for multiple genotypes. AIDS. 1993 Jun;7(6):769–780. [Abstract] [Google Scholar]
  • Lukashov VV, Cornelissen MT, Goudsmit J, Papuashvilli MN, Rytik PG, Khaitov RM, Karamov EV, de Wolf F. Simultaneous introduction of distinct HIV-1 subtypes into different risk groups in Russia, Byelorussia and Lithuania. AIDS. 1995 May;9(5):435–439. [Abstract] [Google Scholar]
  • Mansky LM, Temin HM. Lower in vivo mutation rate of human immunodeficiency virus type 1 than that predicted from the fidelity of purified reverse transcriptase. J Virol. 1995 Aug;69(8):5087–5094. [Europe PMC free article] [Abstract] [Google Scholar]
  • Möller A, Meyer E, Brinkmann B. Different types of structural variation in STRs: HumFES/FPS, HumVWA and HumD21S11. Int J Legal Med. 1994;106(6):319–323. [Abstract] [Google Scholar]
  • Olsen GJ, Matsuda H, Hagstrom R, Overbeek R. fastDNAmL: a tool for construction of phylogenetic trees of DNA sequences using maximum likelihood. Comput Appl Biosci. 1994 Feb;10(1):41–48. [Abstract] [Google Scholar]
  • Preston BD, Poiesz BJ, Loeb LA. Fidelity of HIV-1 reverse transcriptase. Science. 1988 Nov 25;242(4882):1168–1171. [Abstract] [Google Scholar]
  • Puers C, Hammond HA, Jin L, Caskey CT, Schumm JW. Identification of repeat sequence heterogeneity at the polymorphic short tandem repeat locus HUMTH01[AATG]n and reassignment of alleles in population analysis by using a locus-specific allelic ladder. Am J Hum Genet. 1993 Oct;53(4):953–958. [Europe PMC free article] [Abstract] [Google Scholar]
  • Robertson DL, Hahn BH, Sharp PM. Recombination in AIDS viruses. J Mol Evol. 1995 Mar;40(3):249–259. [Abstract] [Google Scholar]
  • Robertson DL, Sharp PM, McCutchan FE, Hahn BH. Recombination in HIV-1. Nature. 1995 Mar 9;374(6518):124–126. [Abstract] [Google Scholar]
  • Sabino EC, Shpaer EG, Morgado MG, Korber BT, Diaz RS, Bongertz V, Cavalcante S, Galvão-Castro B, Mullins JI, 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. [Europe PMC free article] [Abstract] [Google Scholar]
  • Salminen M, Nykänen A, Brummer-Korvenkontio H, Kantanen ML, Liitsola K, Leinikki P. Molecular epidemiology of HIV-1 based on phylogenetic analysis of in vivo gag p7/p9 direct sequences. Virology. 1993 Jul;195(1):185–194. [Abstract] [Google Scholar]
  • Salminen MO, Carr JK, Burke DS, McCutchan FE. Identification of breakpoints in intergenotypic recombinants of HIV type 1 by bootscanning. AIDS Res Hum Retroviruses. 1995 Nov;11(11):1423–1425. [Abstract] [Google Scholar]
  • Salminen MO, Johansson B, Sönnerborg A, Ayehunie S, Gotte D, Leinikki P, Burke DS, McCutchan FE. Full-length sequence of an ethiopian human immunodeficiency virus type 1 (HIV-1) isolate of genetic subtype C. AIDS Res Hum Retroviruses. 1996 Sep 20;12(14):1329–1339. [Abstract] [Google Scholar]
  • Salminen MO, Koch C, Sanders-Buell E, Ehrenberg PK, Michael NL, Carr JK, Burke DS, McCutchan FE. Recovery of virtually full-length HIV-1 provirus of diverse subtypes from primary virus cultures using the polymerase chain reaction. Virology. 1995 Oct 20;213(1):80–86. [Abstract] [Google Scholar]
  • Stuhlmann H, Berg P. Homologous recombination of copackaged retrovirus RNAs during reverse transcription. J Virol. 1992 Apr;66(4):2378–2388. [Europe PMC free article] [Abstract] [Google Scholar]
  • Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 Nov 11;22(22):4673–4680. [Europe PMC free article] [Abstract] [Google Scholar]
  • Tumas KM, Poszgay JM, Avidan N, Ksiazek SJ, Overmoyer B, Blank KJ, Prystowsky MB. Loss of antigenic epitopes as the result of env gene recombination in retrovirus-induced leukemia in immunocompetent mice. Virology. 1993 Feb;192(2):587–595. [Abstract] [Google Scholar]
  • Vanden Haesevelde M, Decourt JL, De Leys RJ, Vanderborght B, van der Groen G, van Heuverswijn H, Saman E. Genomic cloning and complete sequence analysis of a highly divergent African human immunodeficiency virus isolate. J Virol. 1994 Mar;68(3):1586–1596. [Europe PMC free article] [Abstract] [Google Scholar]
  • Voevodin A, Crandall KA, Seth P, al Mufti S. HIV type 1 subtypes B and C from new regions of India and Indian and Ethiopian expatriates in Kuwait. AIDS Res Hum Retroviruses. 1996 May 1;12(7):641–643. [Abstract] [Google Scholar]
  • Yang YL, Wang G, Dorman K, Kaplan AH. Long polymerase chain reaction amplification of heterogeneous HIV type 1 templates produces recombination at a relatively high frequency. AIDS Res Hum Retroviruses. 1996 Mar 1;12(4):303–306. [Abstract] [Google Scholar]
  • Zhu T, Wang N, Carr A, Wolinsky S, Ho DD. 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. [Europe PMC free article] [Abstract] [Google Scholar]
Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

Full text links 

Read article at publisher's site: https://doi.org/10.1128/jvi.71.4.2647-2655.1997

Read article for free, from open access legal sources, via Unpaywall: https://jvi.asm.org/content/jvi/71/4/2647.full.pdfUnpaywall

Free after 4 months at jvi.asm.org
http://jvi.asm.org/cgi/reprint/71/4/2647

Free to read at jvi.asm.org
http://jvi.asm.org/cgi/content/abstract/71/4/2647

Citations & impact 

Impact metrics

77
Citations
Jump to Citations
20
Data citations
Jump to Data

Citations of article over time

Smart citations by scite.ai
Smart citations by scite.ai include citation statements extracted from the full text of the citing article. The number of the statements may be higher than the number of citations provided by EuropePMC if one paper cites another multiple times or lower if scite has not yet processed some of the citing articles.
Explore citation contexts and check if this article has been supported or disputed.
https://scite.ai/reports/10.1128/jvi.71.4.2647-2655.1997

Supporting
Mentioning
Contrasting
0
28
0

Article citations

Go to all (77) article citations

Data 

Data behind the article

This data has been text mined from the article, or deposited into data resources.

BioStudies: supplemental material and supporting data

Similar Articles 

To arrive at the top five similar articles we use a word-weighted algorithm to compare words from the Title and Abstract of each citation.

Funding 

Funders who supported this work.

NIAID NIH HHS (2)