Cited by 223Evolution and Genetic DynamicsHIV Research and TreatmentGenomics and Phylogenetic Studies

Adaptation to different human populations by HIV-1 revealed by codon-based analyses

Open access
Kosakovsky Pond, Sergei L, Frost, Simon D. W, Grossman, Zehava, Gravenor, Michael B, Richman, Douglas D, Brown, Andrew J. Leigh·2006·PLoS Computational Biology

Abstract

Several codon-based methods are available for detecting adaptive evolution in protein-coding sequences, but to date none specifically identify sites that are selected differentially in two populations, although such comparisons between populations have been historically useful in identifying the action of natural selection. We have developed two fixed effects maximum likelihood methods: one for identifying codon positions showing selection patterns that persist in a population and another for detecting whether selection is operating differentially on individual codons of a gene sampled from two different populations. Applying these methods to two HIV populations infecting genetically distinct human hosts, we have found that few of the positively selected amino acid sites persist in the population; the other changes are detected only at the tips of the phylogenetic tree and appear deleterious in the long term. Additionally, we have identified seven amino acid sites in protease and reverse transcriptase that are selected differentially in the two samples, demonstrating specific population-level adaptation of HIV to human populations.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1371/journal.pcbi.0020062

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Approaches estimating the number of sites under strong purifying selection in one region versus another and directly testing for differences in site-specific ! estimates are relevant primarily for comparing selective pressures across regions within a gene.

    “Relaxed selection across sites in a gene has also been explored by estimating the number of sites under strong purifying selection in one region versus another (Wertheim and Worobey 2009) and by directly testing for differences in sitespecific !estimates (Pond et al. 2006); however, such approaches are relevant primarily for comparing selective pressures across regions within a gene.”

    From RELAX: Detecting Relaxed Selection in a Phylogenetic Framework (2015) · cites this paper as Pond et al. 2006

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 62

  1. Dobzhansky T 1948 Genetics of natural populations. XVI. Altitudinal and seasonal changes produced by natural selection in certain populations of Drosophila pseudoobscura and Drosophila persimilis Genetics 33 158 176 18856563 PMC1209402
  2. Johnson F Schaffer H 1973 Isoenzyme variability in species of genus Drosophila. Genotype–environment relationships in populations of D. melanogaster from eastern United States Biochem Genet 10 149 163 4201524
  3. Oakeshott JG Gibson J Anderson PR Knibb WR Anderson D 1982 Alcohol dehydrogenase and glycerol-3-phosphate dehydrogenase clines in Drosophila melanogaster on different continents Evolution 36 86 96 28581103
  4. Hill RE Hastie ND 1987 Accelerated evolution in the reactive centre regions of serine protease inhibitors Nature 326 96 99 3493437
  5. Hughes AL Nei M 1988 Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection Nature 335 167 170 3412472
  6. Nielsen R Yang Z 1998 Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene Genetics 148 929 936 9539414 PMC1460041
  7. Borrow P Lewicki H Wei X Horwitz M Peffer N 1997 Antiviral pressure exerted by HIV-1-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape virus Nat Med 3 205 211 9018240
  8. Goulder P Phillips R Colbert R McAdam S Ogg G 1997 Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS Nat Med 3 212 217 9018241
  9. Kelleher AD Long C Holmes EC Allen RL Wilson J 2001 Clustered mutations in HIV-1 gag are consistently required for escape from HLA-B27-restricted cytotoxic T lymphocyte responses J Exp Med 193 375 386 11157057 PMC2195921
  10. Goulder PJR Brander C Tang Y Tremblay C Colbert RA 2001 Evolution and transmission of stable CTL escape mutations in HIV infection Nature 412 334 338 11460164
  11. O'Connor DH Allen TM Vogel TU Jing P DeSouza IP 2002 Acute phase cytotoxic T lymphocyte escape is a hallmark of simian immunodeficiency virus infection Nat Med 8 493 499 11984594
  12. Yang OO Sarkis PTN Ali A Harlow JD Brander C 2003 Determinant of HIV-1 mutational escape from cytotoxic T lymphocytes J Exp Med 197 1365 1375 12743169 PMC2193781
  13. Leslie AJ Pfafferott KJ Chetty P Draenert R Addo MM 2004 HIV evolution: CTL escape mutation and reversion after transmission Nat Med 10 282 289 14770175
  14. Friedrich TC Dodds EJ Yant LJ Vojnov L Rudersdorf R 2004 Reversion of CTL escape-variant immunodeficiency viruses in vivo Nat Med 10 275 281 14966520
  15. Moore CB John M James IR Christiansen FT Witt CS 2002 Evidence of HIV-1 adaptation to HLA-restricted immune responses at a population level Science 296 1439 1443 12029127
  16. Yang Z Nielsen R Goldman N Pedersen AM 2000 Codon-substitution models for heterogeneous selection pressure at amino acid sites Genetics 155 431 449 10790415 PMC1461088
  17. Zanotto PM Kallas EG de Souza RF Holmes EC 1999 Genealogical evidence for positive selection in the nef gene of HIV-1 Genetics 153 1077 1089 10545443 PMC1460812
  18. Williamson S 2003 Adaptation in the env gene of HIV-1 and evolutionary theories of disease progression Mol Biol Evol 20 1318 1325 12777505
  19. Choisy M Woelk CH Guegan JF Robertson DL 2004 Comparative study of adaptive molecular evolution in different human immunodeficiency virus groups and subtypes J Virol 78 1962 1970 14747561 PMC369455
  20. de Oliveira T Salemi M Gordon M Vandamme AM van Rensburg EJ 2004 Mapping sites of positive selection and amino acid diversification in the HIV genome: An alternative approach to vaccine design? Genetics 167 1047 1058 15280222 PMC1470929
  21. Travers SAA O'Connell MJ McCormack GP McInerney JO 2005 Evidence for heterogeneous selective pressures in the evolution of the env gene in different human immunodeficiency virus type 1 subtypes J Virol 79 1836 1841 15650207 PMC544114
  22. Kosakovsky Pond SL Frost SDW 2005 Not so different after all: A comparison of methods for detecting amino acid sites under selection Mol Biol Evol 22 1208 1222 15703242
  23. Ray SC Fanning L Wang XH Netski DM Kenny–Walsh E 2005 Divergent and convergent evolution after a common-source outbreak of hepatitis C virus J Exp Med 201 1753 1759 15939791 PMC2213258
  24. Kosakovsky Pond SL Frost SDW 2005 A simple hierarchical approach to modeling distributions of substitution rates Mol Biol Evol 22 223 234 15483327
  25. Gordon M De Oliveira T Bishop K Coovadia HM Madurai L 2003 Molecular characteristics of human immunodeficiency virus type 1 subtype C viruses from KwaZulu–Natal, South Africa: Implications for vaccine and antiretroviral control strategies J Virol 77 2587 2599 12551997 PMC141090
  26. Grossman Z Vardinon N Chemtob D Alkan ML Bentwich Z 2001 Genotypic variation of HIV-1 reverse transcriptase and protease: Comparative analysis of clade C and clade B AIDS 15 1453 1460 11504976
  27. Shafer R Stevenson D Chan B 1999 Human immunodeficiency virus reverse transcriptase and protease sequence database Nucleic Acids Res 27 348 352 9847225 PMC148180
  28. Kantor R Machekano R Gonzales MJ Dupnik K Schapiro JM 2001 Human immunodeficiency virus reverse transcriptase and protease sequence database: An expanded data model integrating natural language text and sequence analysis programs Nucleic Acids Res 29 296 299 11125118 PMC29795
  29. Johnson V Brun–Vézinet F Bonaventura C Conway B Kuritzkes D 2005 Update to the drug resistance mutations in HIV-1: Fall 2005 IAS Top HIV Med 13 125 131 16304457
  30. Guindon S Gascuel O 2003 A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood Syst Biol 52 696 704 14530136
  31. Huelsenbeck JP Ronquist F 2001 MRBAYES: Bayesian inference of phylogenetic trees Bioinformatics 17 754 755 11524383
  32. Anisimova M Nielsen R Yang Z 2003 Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites Genetics 164 1229 1236 12871927 PMC1462615
  33. Shriner D Nickle DC Jensen MA Mullins J 2003 Potential impact of recombination on sitewise approaches for detecting positive natural selection Genet Res 81 115 121 12872913
  34. Holmes EC Worobey M Rambaut A 1999 Phylogenetic evidence for recombination in dengue virus Mol Biol Evol 16 405 409 10331266
  35. Chare ER Gould EA Holmes EC 2003 Phylogenetic analysis reveals a low rate of homologous recombination in negative-sense RNA viruses J Gen Virol 84 2691 2703 13679603
  36. Saitou N Nei M 1987 The neighbor-joining method: A new method for reconstructing phylogenetic trees Mol Biol Evol 4 406 425 3447015
  37. Martin DP Williamson C Posada D 2005 RDP2: Recombination detection and analysis from sequence alignments Bioinformatics 21 260 262 15377507
  38. Kosakovsky Pond SL Muse SV 2005 Site-to-site variation of synonymous substitution rates Mol Biol Evol 22 2375 2385 16107593
  39. Sharp PM Bailes E Chaudhuri RR Rodenburg CM Santiago MO 2001 The origins of acquired immune deficiency syndrome viruses: Where and when? Phil Trans R Soc Lond B Biol Sci 356 867 876 11405934 PMC1088480
  40. Holmes EC 2003 Patterns of intra- and interhost nonsynonymous variation reveal strong purifying selection in Dengue virus J Virol 77 11296 11298 14512579 PMC224983
  41. Lawlor DA Ward FE Ennis PD Jackson AP Parham P 1988 HLA-A and B polymorphisms predate the divergence of humans and chimpanzees Nature 335 268 271 3412487
  42. Lucotte G Smets P 1999 Origins of Falasha Jews studied by haplotypes of the Y chromosome Hum Biol 71 989 993 10592688
  43. Fort M de Stefano GF Cambon–Thomsen A Giraldo–Alvarez P Dugoujon JM 1998 HLA class II allele and haplotype frequencies in Ethiopian Amhara and Oromo populations Tissue Antigens 51 327 336 9583804
  44. Williams F Meenagh A Darke C Acosta A Daar AS 2001 Analysis of the distribution of HLA-B alleles in populations from five continents Hum Immunol 62 645 650 11390040
  45. Middleton D Williams F Meenagh A Daar AS Gorodezky C 2000 Analysis of the distribution of HLA-A alleles in populations from five continents Hum Immunol 61 1048 1052 11082518
  46. Fernandez CS Stratov I De Rose R Walsh K Dale CJ 2005 Rapid viral escape at an immunodominant simian–human immunodeficiency virus cytotoxic T-lymphocyte epitope exacts a dramatic fitness cost J Virol 79 5721 5731 15827187 PMC1082732
  47. Asquith B Edwards C Lipsitch M McLean A 2004 Inefficient cytotoxic T lymphocyte–mediated killing of HIV-1–infected cells in vivo PLoS Biol 4 e90. DOI: 10.1371/journal.pbio.004090 PMC1395353 16515366 · DOI
  48. Yusim K Kesmir C Gaschen B Addo MM Altfeld M 2002 Clustering patterns of cytotoxic T-lymphocyte epitopes in human immunodeficiency virus type 1 (HIV-1) proteins reveal imprints of immune evasion on HIV-1 global variation J Virol 76 8757 8768 12163596 PMC136996
  49. Yang ZH Nielsen R 2002 Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages Mol Biol Evol 19 908 917 12032247
  50. Bielawski J Yang Z 2004 A maximum likelihood method for detecting functional divergence at individual codon sites, with application to gene family evolution J Mol Evol 59 121 132 15383915
  51. Zhang JZ 2004 Frequent false detection of positive selection by the likelihood method with branch-site models Mol Biol Evol 21 1332 1339 15014150
  52. Zhang J Nielsen R Yang Z 2005 Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level Mol Biol Evol 22 2472 2479 16107592
  53. Ross HA Rodrigo AG 2002 Immune-mediated positive selection drives human immunodeficiency virus type 1 molecular variation and predicts disease duration J Virol 76 11715 11720 12388731 PMC136752
  54. Kosakovsky Pond SL Frost SDW Muse SV 2005 HyPhy: Hypothesis testing using phylogenies Bioinformatics 21 676 679 15509596
  55. McMichael A Klenerman P 2002 HLA leaves its footprints on HIV Science 296 1410 1411 12029119
  56. Lanave C Preparata G Saccone C Serio G 1984 A new method for calculating evolutionary substitution rates J Mol Evol 20 86 93 6429346
  57. Kosakovsky Pond SL Muse SV 2004 Column sorting: Rapid calculation of the phylogenetic likelihood function Syst Biol 53 685 692 15545249
  58. Muse SV Gaut BS 1994 A likelihood approach for comparing synonymous and nonsynonymous nucleotide substitution rates, with application to the chloroplast genome Mol Biol Evol 11 715 724 7968485
  59. Yang ZH Swanson WJ 2002 Codon-substitution models to detect adaptive evolution that account for heterogeneous selective pressures among site classes Mol Biol Evol 19 49 57 11752189
  60. Suzuki Y 2004 New methods for detecting positive selection at single amino acid sites J Mol Evol 59 11 19 15383903 PMC1513646
  61. Massingham T Goldman N 2005 Detecting amino acid sites under positive selection and purifying selection Genetics 169 1753 1762 15654091 PMC1449526
  62. Tamura K Nei M 1993 Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees Mol Biol Evol 10 512 526 8336541

Cited by

Sorted by citations

Authors
Kosakovsky Pond, S. L., Frost, S. D. W., Grossman, Z., Gravenor, M. B., Richman, D. D., & Brown, A. J. L.
Affiliations
  • University of California San Diego (US)
  • Israel Ministry of Health (IL)
  • University of Edinburgh (GB)
Corresponding author
Brown, Andrew J. Leigh
Venue
PLoS Computational Biology
Published
2006-06-23
Volume
2
Issue
6
Pages
e62
ISSN
  • 1553-734X (ISSN-L)
  • 1553-7358
OpenAlex
W1964475452
Cited by
223
References
1
Citations by year
2026: 2 · 2025: 2 · 2024: 4 · 2023: 3 · 2022: 7 · 2021: 6 · 2020: 11 · 2019: 3 · 2018: 15 · 2017: 16 · 2016: 24 · 2015: 14 · 2014: 24 · 2013: 20 · 2012: 17
FWCI
5.61
Type
journal article
Language
en
Open access
Locations
  • PLoS Computational Biology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
  • TUScholarShare (Temple University) (submittedVersion, cc-by)
Funders
  • U.S. Department of Veterans Affairs
  • National Institutes of Health (AI-38858, AI 27670, AI47745, AI-36214, AI29164)
  • Center for AIDS Research, University of Washington
  • University of California, San Diego
  • National Institute of Allergy and Infectious Diseases (AI38858, R01AI057167, AI-47745, AI57167, R21AI047745, AI 43638, AI-29164, R56AI047745, AI-36214, R37AI029164, U01AI038858, R01AI047745, U01AI027670, U01AI043638, AI2-7670, P30AI036214)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
  • Life Sciences › Immunology and Microbiology › Virology › HIV Research and Treatment
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Keywords
HIV-1, adaptive evolution, positive selection, HIV protease, HIV reverse transcriptase, amino acid sites, deleterious mutations
MeSH terms
Adaptation, Physiological, Codon, Biological Evolution, Genetics, Population, Humans, Selection, Genetic, Genetic Variation, HIV-1, HIV Infections, Sequence Analysis, DNA, Genetic Predisposition to Disease

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review