1887

Abstract

The intrinsic recombination rate of human immunodeficiency virus (HIV) exceeds the point mutation rate by a factor of 10. As the majority of infected cells harbour multiple proviruses, the stage is set for rampant recombination. Therefore, it may be presumed that phylogenic relationships and mutation frequencies will probably be affected by recombination. However, the proportion of homoplasies arising from recombination and mutation is not known. By studying the evolution of the hypervariable regions of the simian immunodeficiency virus envelope gene among four macaques, it is shown that homoplasies arise more from recombination than from point mutation. When recombination is accounted for, the minimum number of substitutions in a sequence set may be reduced by as much as 45 %. In fact, the true number of point mutations in a set of HIV sequences tends to the number of discrete substitutions. Hence, lineages are younger than anticipated previously, although not in proportion to the ratio of the intrinsic recombination/point mutation rate. Recombination also inflates codon polymorphisms.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.18894-0
2003-04-01
2020-06-01
Loading full text...

Full text loading...

/deliver/fulltext/jgv/84/4/vir840885.html?itemId=/content/journal/jgv/10.1099/vir.0.18894-0&mimeType=html&fmt=ahah

References

  1. Alber D., Oberkötter M., Suerbaum S., Claus H., Frosch M., Vogel U.. 2001; Genetic diversity of Neisseria lactamica strains from epidemiologically defined carriers. J Clin Microbiol39:1710–1715
    [Google Scholar]
  2. Bandelt H. J., Dress A. W.. 1992; Split decomposition: a new and useful approach to phylogenetic analysis of distance data. Mol Phylogenet Evol1:242–252
    [Google Scholar]
  3. Barbrook A. C., Howe C. J., Blake N., Robinson P.. 1998; The phylogeny of The Canterbury Tales . Nature394:839
    [Google Scholar]
  4. Blancou P., Chenciner N., Cumont M. C., Wain-Hobson S., Hurtrel B., Cheynier R.. 2001; The infiltration kinetics of simian immunodeficiency virus-specific T cells drawn to sites of high antigenic stimulation determines local in vivo viral escape. Proc Natl Acad Sci U S A98:13237–13242
    [Google Scholar]
  5. Carr J. K., Salminen M. O., Albert J., Sanders-Buell E., Gotte D., Birx D. L., McCutchan F. E.. 1998; Full genome sequences of human immunodeficiency virus type 1 subtypes G and A/G intersubtype recombinants. Virology247:22–31
    [Google Scholar]
  6. Cheynier R., Henrichwark S., Hadida F., Pelletier E., Oksenhendler E., Autran B., Wain-Hobson S.. 1994; HIV and T cell expansion in splenic white pulps is accompanied by infiltration of HIV-specific cytotoxic T lymphocytes. Cell78:373–387
    [Google Scholar]
  7. Cheynier R., Gratton S., Halloran M., Stahmer I., Letvin N. L., Wain-Hobson S.. 1998; Antigenic stimulation by BCG as an in vivo driving force for SIV replication and dissemination. Nat Med4:421–427
    [Google Scholar]
  8. Cheynier R., Kils-Hutten L., Meyerhans A., Wain-Hobson S.. 2001; Insertion/deletion frequencies match those of point mutations in the hypervariable regions of the simian immunodeficiency virus surface envelope gene. J Gen Virol82:1613–1619
    [Google Scholar]
  9. Coffin J. M.. 1979; Structure, replication, and recombination of retrovirus genomes: some unifying hypotheses. J Gen Virol42:1–26
    [Google Scholar]
  10. Eigen M., Nieselt-Struwe K.. 1990; How old is the immunodeficiency virus?. AIDS4 (Suppl. 1):S85–S93
    [Google Scholar]
  11. Evans D. T., O'Connor D. H., Jing P.. 14 other authors 1999; Virus-specific cytotoxic T-lymphocyte responses select for amino-acid variation in simian immunodeficiency virus Env and Nef. Nat Med5:1270–1276
    [Google Scholar]
  12. Feil E. J., Spratt B. G.. 2001; Recombination and the population structures of bacterial pathogens. Annu Rev Microbiol55:561–590
    [Google Scholar]
  13. Feil E. J., Maiden M. C. J., Achtman M., Spratt B. G.. 1999; The relative contributions of recombination and mutation to the divergence of clones of Neisseria meningitidis . Mol Biol Evol16:1496–1502
    [Google Scholar]
  14. Feil E. J., Smith J. M., Enright M. C., Spratt B. G.. 2000; Estimating recombinational parameters in Streptococcus pneumoniae from multilocus sequence typing data. Genetics154:1439–1450
    [Google Scholar]
  15. Feil E. J., Holmes E. C., Bessen D. E.. 9 other authors 2001; Recombination within natural populations of pathogenic bacteria: short-term empirical estimates and long-term phylogenetic consequences. Proc Natl Acad Sci U S A98:182–187
    [Google Scholar]
  16. Gratton S., Cheynier R., Dumaurier M. J., Oksenhendler E., Wain-Hobson S.. 2000; Highly restricted spread of HIV-1 and multiply infected cells within splenic germinal centers. Proc Natl Acad Sci U S A97:14566–14571
    [Google Scholar]
  17. Ho D. D., Neumann A. U., Perelson A. S., Chen W., Leonard J. M., Markowitz M.. 1995; Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature373:123–126
    [Google Scholar]
  18. Hoelscher M., Kim B., Maboko L., Mhalu F., von Sonnenburg F., Birx D. L., McCutchan F. E.. 2001; High proportion of unrelated HIV-1 intersubtype recombinants in the Mbeya region of southwest Tanzania. AIDS15:1461–1470
    [Google Scholar]
  19. Holmes E. C., Urwin R., Maiden M. C. J.. 1999a; The influence of recombination on the population structure and evolution of the human pathogen Neisseria meningitidis . Mol Biol Evol16:741–749
    [Google Scholar]
  20. Holmes E. C., Worobey M., Rambaut A.. 1999b; Phylogenetic evidence for recombination in dengue virus. Mol Biol Evol16:405–409
    [Google Scholar]
  21. Hu W. S., Temin H. M.. 1990; Genetic consequences of packaging two RNA genomes in one retroviral particle: pseudodiploidy and high rate of genetic recombination. Proc Natl Acad Sci U S A87:1556–1560
    [Google Scholar]
  22. Huson D. H.. 1998; SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics14:68–73
    [Google Scholar]
  23. Jetzt A. E., Yu H., Klarmann G. J., Ron Y., Preston B. D., Dougherty J. P.. 2000; High rate of recombination throughout the human immunodeficiency virus type 1 genome. J Virol74:1234–1240
    [Google Scholar]
  24. Jung A., Maier R., Vartanian J. P., Bocharov G., Jung V., Fischer U., Meese E., Wain-Hobson S., Meyerhans A.. 2002; Multiply infected spleen cells in HIV patients. Nature418:144
    [Google Scholar]
  25. Kawai S., Hanafusa H.. 1972; Genetic recombination with avian tumor virus. Virology49:37–44
    [Google Scholar]
  26. Kils-Hütten L., Cheynier R., Wain-Hobson S., Meyerhans A.. 2001; Phylogenetic reconstruction of intrapatient evolution of human immunodeficiency virus type 1: predominance of drift and purifying selection. J Gen Virol82:1621–1627
    [Google Scholar]
  27. Mansky L. M., Temin H. M.. 1995; Lower in vivo mutation rate of human immunodeficiency virus type 1 than that predicted from the fidelity of purified reverse transcriptase. J Virol69:5087–5094
    [Google Scholar]
  28. Martinez M. A., Vartanian J. P., Wain-Hobson S.. 1994; Hypermutagenesis of RNA using human immunodeficiency virus type 1 reverse transcriptase and biased dNTP concentrations. Proc Natl Acad Sci U S A91:11787–11791
    [Google Scholar]
  29. McCutchan F. E.. 2000; Understanding the genetic diversity of HIV-1. AIDS14 (Suppl. 3):S31–S44
    [Google Scholar]
  30. Nielsen R., Yang Z.. 1998; Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics148:929–936
    [Google Scholar]
  31. Pathak V. K., Temin H. M.. 1990; Broad spectrum of in vitro forward mutations, hypermutations, and mutational hotspots in a retroviral shuttle vector after a single replication cycle: substitutions, frameshifts, and hypermutations. Proc Natl Acad Sci U S A87:6019–6023
    [Google Scholar]
  32. Peeters M., Liegeois F., Torimiro N., Bourgeois A., Mpoudi E., Vergne L., Saman E., Delaporte E., Saragosti S.. 1999; Characterization of a highly replicative intergroup M/O human immunodeficiency virus type 1 recombinant isolated from a Cameroonian patient. J Virol73:7368–7375
    [Google Scholar]
  33. Pelletier E., Saurin W., Cheynier R., Letvin N. L., Wain-Hobson S.. 1995; The tempo and mode of SIV quasispecies development in vivo calls for massive viral replication and clearance. Virology208:644–652
    [Google Scholar]
  34. Plikat U., Nieselt-Struwe K., Meyerhans A.. 1997; Genetic drift can dominate short-term human immunodeficiency virus type 1 nef quasispecies evolution in vivo . J Virol71:4233–4240
    [Google Scholar]
  35. Plyusnin A., Kukkonen S. K. J., Plyusnina A., Vapalahti O., Vaheri A.. 2002; Transfection-mediated generation of functionally competent Tula hantavirus with recombinant S RNA segment. EMBO J21:1497–1503
    [Google Scholar]
  36. Price D. A., Goulder P. J. R., Klenerman P., Sewell A. K., Easterbrook P. J., Troop M., Bangham C. R. M., Phillips R. E.. 1997; Positive selection of HIV-1 cytotoxic T lymphocyte escape variants during primary infection. Proc Natl Acad Sci U S A94:1890–1895
    [Google Scholar]
  37. Ricchetti M., Buc H.. 1990; Reverse transciptases and genomic variability: the accuracy of DNA replication is enzyme specific and sequence dependent. EMBO J9:1583–1593
    [Google Scholar]
  38. Schierup M. H., Hein J.. 2000; Consequences of recombination on traditional phylogenetic analysis. Genetics156:879–891
    [Google Scholar]
  39. Sibold C., Meisel H., Krüger D. H., Labuda M., Lysy J., Kozuch O., Pejcoch M., Vaheri A., Plyusnin A.. 1999; Recombination in Tula hantavirus evolution: analysis of genetic lineages from Slovakia. J Virol73:667–675
    [Google Scholar]
  40. Smith N. H., Holmes E. C., Donovan G. M., Carpenter G. A., Spratt B. G.. 1999; Networks and groups within the genus Neisseria : analysis of argF , recA , rho and 16S rRNA sequences from human Neisseria species. Mol Biol Evol16:773–783
    [Google Scholar]
  41. Takehisa J., Zekeng L., Ido E., Yamaguchi-Kabata Y., Mboudjeka I., Harada Y., Miura T., Kaptu L., Hayami M.. 1999; Human immunodeficiency virus type 1 intergroup (M/O) recombination in Cameroon. J Virol73:6810–6820
    [Google Scholar]
  42. Thompson J. D., Higgins D. G., Gibson T. J.. 1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res22:4673–4680
    [Google Scholar]
  43. Vartanian J. P., Meyerhans A., Asjo B., Wain-Hobson S.. 1991; Selection, recombination, and G→A hypermutation of human immunodeficiency virus type 1 genomes. J Virol65:1779–1788
    [Google Scholar]
  44. Vartanian J. P., Plikat U., Mahieux R., Guillemot L., Meyerhans A., Wain-Hobson S.. 1997; HIV genetic variability is directed and restricted by DNA precursor availability. J Mol Biol270:139–151
    [Google Scholar]
  45. Vartanian J. P., Henry M., Wain-Hobson S.. 2002; Sustained G→A hypermutation during reverse transcription of an entire human immunodeficiency type 1 strain Vau group O genome. J Gen Virol83:801–805
    [Google Scholar]
  46. Vogt P. K.. 1971; Genetically stable reassortment of markers during mixed infection with avian tumor viruses. Virology46:947–952
    [Google Scholar]
  47. Wain-Hobson S.. 1993; Viral burden in AIDS. Nature366:22
    [Google Scholar]
  48. Wei X., Ghosh S. K., Taylor M. E.. 9 other authors 1995; Viral dynamics in human immunodeficiency virus type 1 infection. Nature373:117–122
    [Google Scholar]
  49. Weiss R. A., Mason W. S., Vogt P. K.. 1973; Genetic recombinants and heterozygotes derived from endogenous and exogenous avian RNA tumor viruses. Virology52:535–552
    [Google Scholar]
  50. Wooley D. P., Smith R. A., Czajak S., Desrosiers R. C.. 1997; Direct demonstration of retroviral recombination in a rhesus monkey. J Virol71:9650–9653
    [Google Scholar]
  51. Yamaguchi-Kabata Y., Gojobori T.. 2000; Reevaluation of amino acid variability of the human immunodeficiency virus type 1 gp120 envelope glycoprotein and prediction of new discontinuous epitopes. J Virol74:4335–4350
    [Google Scholar]
  52. Yang Z., Nielsen R., Goldman N., Pedersen A. M.. 2000; Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics155:431–449
    [Google Scholar]
  53. Yu H., Jetzt A. E., Ron Y., Preston B. D., Dougherty J. P.. 1998; The nature of human immunodeficiency virus type 1 strand transfers. J Biol Chem273:28384–28391
    [Google Scholar]
  54. Zanotto P. M., Kallas E. G., de Souza R. F., Holmes E. C.. 1999; Genealogical evidence for positive selection in the nef gene of HIV-1. Genetics153:1077–1089
    [Google Scholar]
  55. Zhang J., Temin H. M.. 1993; Rate and mechanism of nonhomologous recombination during a single cycle of retroviral replication. Science259:234–238
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.18894-0
Loading
/content/journal/jgv/10.1099/vir.0.18894-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error