Frequent toggling between alternative amino acids is driven by selection in HIV-1

PLoS Pathogens

Volumn 4, Issue 12, 2008, Pages

  Delport, Wayne ^a,b   Scheffler, Konrad ^c   Seoighe, Cathal ^a,b  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b CENTRE FOR HIGH PERFORMANCE COMPUTING   (South Africa)

^c STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; EPITOPE; HUMAN IMMUNODEFICIENCY VIRUS PROTEIN; HLA ANTIGEN CLASS 1; HUMAN IMMUNODEFICIENCY VIRUS ANTIGEN; MEMBRANE ANTIGEN;

AMINO ACID SEQUENCE; ANTIGEN RECOGNITION; ARTICLE; CODING; DISEASE ASSOCIATION; ESCAPE BEHAVIOR; GENETIC MODEL; HLA SYSTEM; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNE RESPONSE; LEUKOCYTE; NONHUMAN; PATHOGENESIS; PRESSURE; REVERTANT; SIMULATION; VIRUS DETECTION; VIRUS REPLICATION; WILD TYPE; BIOLOGICAL MODEL; CODON; COMPUTER SIMULATION; GENETIC POLYMORPHISM; GENETIC SELECTION; GENETICS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGY; THEORETICAL MODEL;

HUMAN IMMUNODEFICIENCY VIRUS 1;

AMINO ACID SEQUENCE; AMINO ACIDS; ANTIGENS, SURFACE; CODON; COMPUTER SIMULATION; HISTOCOMPATIBILITY ANTIGENS CLASS I; HIV ANTIGENS; HIV INFECTIONS; HIV-1; HUMANS; IMMUNE TOLERANCE; MODELS, GENETIC; MODELS, THEORETICAL; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMORPHISM, GENETIC; SELECTION (GENETICS);

EID: 58149240271     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000242     Document Type: Article

References (73)

1. Goulder PJR, Watkins DI (2004) HIV and SIV CTL escape: Implications for vaccine design. Nature Reviews Immunology 4: 630-640.
2. Leslie AJ, Pfafferott KJ, Chetty P, Draenert R, Addo MM, et al. (2004) HIV evolution: CTL escape mutation and reversion after transmission. Nat Med 10: 282-289.
3. Serwold T, Shastri N (1999) Specific proteolytic cleavages limit the diversity of the pool of peptides available to MHC class I molecules in living cells. J Immunol 162: 4712-4719.
4. Brumme ZL, Brumme CJ, Heckerman D, Korber BT, Daniels M, et al. (2007) Evidence of differential HLA class I-mediated viral evolution in functional and accessory/regulatory genes of HIV-1. PLoS Pathogens 3: e94. doi:10.1371/journal. ppat.0030094.
5. Brumme ZL, Tao I, Szeto S, Brumme CJ, Carlson JM, et al. (2008) Human leukocyte antigen-specific polymorphisms in HIV-1 Gag and their association with viral load in chronic untreated infection. Aids 22: 1277-1286.
6. Wei X, Decker JM, Wang S, Hui H, Kappes JC, et al. (2003) Antibody neutralization and escape by HIV-1. Nature 422: 307-312.
7. 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.
8. Borrow P, Lewicki H, Wei X, Horwitz MS, Peffer N, et al. (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.
9. Price DA, Goulder PJ, Klenerman P, Sewell AK, Easterbrook PJ, et al. (1997) Positive selection of HIV-1 cytotoxic T lymphocyte escape variants during primary infection. Proc Natl Acad Sci U S A 94: 1890-1895.
10. Frost SDW, Wrin T, Smith DM, Pond SLK, Liu Y, et al. (2005) Neutralizing antibody responses drive the evolution of human immunodeficiency virus type 1 envelope during recent HIV infection. Proc Natl Acad Sci U S A 102: 18514-18519.
11. Richman DD, Wrin T, Little SJ, Petropoulos CJ (2003) Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc Natl Acad Sci U S A 100: 4144-4149.
12. Cecilia D, Kleeberger C, Munoz A, Giorgi JV, Zolla-Pazner S (1999) A longitudinal study of neutralizing antibodies and disease progression in HIV-1 infected subjects. Journal of Infectious Diseases 179: 1365-1374.
13. Borghans JAM, Mølgaard A, de Boer RJ, Kesmir C (2007) HLA alleles associated with slow progression to AIDS truly prefer to present HIV-1 p24. PLoS ONE 2: e920. doi/10.1371/journal.pone.0000920.
14. Chopera DR, Woodman Z, Mlisana K, Mlotshwa M, Martin DP, et al. (2008) Transmission of HIV-1 CTL escape variants provides HLA-mismatched recipients with a survival advantage. PLoS Pathogens 4: e1000033. doi:10.1371/journal.ppat. 1000033.
15. Crawford H, Prado JG, Leslie A, Hue S, Honeyborne I, et al. (2007) Compensatory mutation partially restores fitness and delays reversion of escape mutation within the immunodominant HLA-B*5703-restricted Gag epitope in chronic human immunodeficiency virus type 1 infection. J Virol 81: 8346-8351.
16. Kiepiela P, Ngumbela K, Thobakgale C, Ramduth D, Honeyborne I, et al. (2007) CD8+ T-cell responses to different HIV proteins have discordant associations with viral load. Nat Med 13: 46-53.
17. Altfeld M, Addo MM, Rosenberg ES, Hecht FM, Lee PK, et al. (2003) Influence of HLA-B57 on clinical presentation and viral control during acute HIV-1 infection. Aids 17: 2581-2591.
18. Altfeld M, Kalife ET, Qi Y, Streeck H, Lichterfeld M, et al. (2006) HLA alleles associated with delayed progression to AIDS contribute strongly to the initial CD8(+) T cell response against HIV-1. PLoS Med 3: e403. doi:10.1371/journal.pmed.0030403.
19. Carrington M, O'Brien SJ (2003) The influence of HLA genotype on AIDS. Annu Rev Med 54: 535-551.
20. Streeck H, Lichterfeld M, Alter G, Meier A, Teigen N, et al. (2007) Recognition of a defined region within p24 gag by CD8+ T cells during primary human immunodeficiency virus type 1 infection in individuals expressing protective HLA class I alleles. J Virol 81: 7725-7731.
21. Allen TM, Altfeld M, Geer SC, Kalife ET, Moore C, et al. (2005) Selective escape from CD8+ T-Cell responses represents a major driving force of Human Immunodeficiency Virus Type 1 (HIV-1) sequence diversity and reveals constraints on HIV-1 evolution. J Virol 79: 13239-13249.
22. Kelleher AD, Long C, Holmes EC, Allen RL, Wilson J, et al. (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.
23. Moore CB, John M, James IR, Christiansen FT, Witt CS, et al. (2002) Evidence of HIV-1 adaptation to HLA-restricted immune responses at a population level. Science 296: 1439-1443.
24. Bhattacharya T, Daniels M, Heckerman D, Foley B, Frahm N, et al. (2007) Founder effects in the assessment of HIV polymorphisms and HLA allele associations. Science 315: 1583-1586.
25. Brumme ZL, Brumme CJ, Carlson J, Streeck H, John M, et al. (2008) Marked epitope and allele-specific differences in rates of mutation in HIV-1 Gag, Pol and Nef CTL epitopes in acute/early HIV-1 infection. J Virol 82: 9216-9227.
26. Matthews PC, Prendergast A, Leslie A, Crawford H, Payne R, et al. (2008) Central role of reverting mutations in HLA associations with HIV viral setpoint. J Virol 82: 8548-8559.
27. Allen TM, Altfeld M, Yu XG, O'Sullivan KM, Lichterfeld M, et al. (2004) Selection, transmission, and reversion of an antigen-processing Cytotoxic T-Lymphocyte escape mutation in Human Immunodeficiency Virus Type 1 Infection. J Virol 78: 7069-7078.
28. Friedrich TC, Dodds EJ, Yant LJ, Vojnov L, Rudersdorf R, et al. (2004) Reversion of CTL escape-variant immunodeficiency viruses in vivo. Nat Med 10: 275-281.
29. Li B, Gladden AD, Altfeld M, Kaldor JM, Cooper DA, et al. (2007) Rapid reversion of sequence polymorphisms dominates early Human Immunodeficiency Virus Type 1 evolution. J Virol 81: 193-201.
30. Poon AF, Kosakovsky Pond SL, Bennett P, Richman DD, Leigh Brown AJ, et al. (2007) Adaptation to human populations is revealed by within-host polymorphisms in HIV-1 and hepatitis C virus. PLoS Pathog 3: e45. doi:10.1371/journal.ppat.0030045.
31. Iversen AK, Stewart-Jones G, Learn GH, Christie N, Sylvester-Hviid C, et al. (2006) Conflicting selective forces affect T cell receptor contacts in an immunodominant human immunodeficiency virus epitope. Nat Immunol 7: 179-189.
32. Fernandez CS, Stratov I, De Rose R, Walsh K, Dale CJ, et al. (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.
33. Brockman MA, Schneidewind A, Lahaie M, Schmidt A, Miura T, et al. (2007) Escape and compensation from early HLA-B57-mediated cytotoxic T-lymphocyte pressure on human immunodeficiency virus type 1 Gag alter capsid interactions with cyclophilin A. J Virol 81: 12608-12618.
34. Martinez-Picado J, Prado JG, Fry EE, Pfafferott K, Leslie A, et al. (2006) Fitness cost of escape mutations in p24 Gag in association with control of human immunodeficiency virus type 1. J Virol 80: 3617-3623.
35. Schneidewind A, Brockman MA, Yang R, Adam RI, Li B, et al. (2007) Escape from the dominant HLA-B27-restricted cytotoxic T-lymphocyte response in Gag is associated with a dramatic reduction in human immunodeficiency virus type 1 replication. J Virol 81: 12382-12393.
36. Bazykin GA, Dushoff J, Levin SA, Kondrashov AS (2006) Bursts of nonsynonymous substitutions in HIV-1 evolution reveal instances of positive selection at conservative protein sites. Proc Natl Acad Sci U S A 103: 19396-19401.
37. Chen L, Perlina A, Lee CJ (2004) Positive selection detection in 40,000 Human Immunodeficiency Virus (HIV) Type 1 sequences automatically identifies drug resistance and positive fitness mutations in HIV protease and reverse transcriptase. J Virol 78: 3722-3732.
38. de Oliveira T, Salemi M, Gordon M, Vandamme A-M, van Rensburg EJ, et al. (2004) Mapping sites of positive selection and amino acid diversification in the HIV genome: An alternative approach to vaccine design? Genetics 167: 1047-1058.
39. Kosakovsky Pond SL, Frost S, Grossman Z, Gravenor M, Richman DD, et al. (2006) Adaptation to different human populations by HIV-1 revealed by codon-based analysis. PloS Comput Biol 2 preprint: e62. eor. doi/10.1371/journal.pcbi.0020062.
40. Zanotto PMdA, Kallas EG, de Souza RF, Holmes EC (1999) Genealogical evidence for positive selection in the nef gene of HIV-1. Genetics 153: 1077-1089.
41. Goldman N, Yang Z (1994) A codon-based model of nucleotide substitution for protein-coding DNA sequences. Molecular Biology and Evolution 11: 725-736.
42. 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.
43. Felsenstein J (1981) Evolutionary trees from DNA sequences: A maximum likelihood approach. J Mol Evol 17: 368-376.
44. 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.
45. Guindon S, Gascuel O (2003) A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52: 696-704.
46. Tavaré S (1986) Some probabilistic and statistical problems in the analysis of DNA sequences. Lectures on Mathematics in the Life Sciences 17: 57-86.
47. Yang Z (1996) Among-site rate variation and its impact on phylogenetic analyses. Trends in Ecology and Evolution 11: 367-372.
48. 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.
49. Shriner D, Nickle DC, Jensen MA, Mullins JI (2003) Potential impact of recombination on sitewise approaches for detecting positive natural selection. Genet Res 81: 115-121.
50. Scheffler K, Martin DP, Seoighe C (2006) Robust inference of positive selection from recombining coding sequences. Bioinformatics 22: 2493-2499.
51. Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SDW (2006) GARD: A genetic algorithm for recombination detection. Bioinformatics 22: 3096-3098.
52. Kosakovsky Pond SL, Frost SDW, Muse SV (2005) HyPhy: Hypothesis testing using phylogenies. Bioinformatics 21: 676-679.
53. Kiepiela P, Leslie AJ, Honeyborne I, Ramduth D, Thobakgale C, et al. (2004) Dominant influence of HLA-B in mediating the potential co-evolution of HIV and HLA. Nature 432: 769-775.
54. nd edition. Budapest: Akadémiai Kiadi. pp 267-281.
55. Edwards CTT, Holmes EC, Pybus OG, Wilson DJ, Viscidi RP, et al. (2006) Evolution of the Human Immunodeficiency Virus envelope gene Is dominated by purifying selection. Genetics 174: 1441-1453.
56. Rambaut A, Posada D, Crandall KA, Holmes EC (2004) The causes and consequences of HIV evolution. Nature Reviews Genetics 5: 52-61.
57. Kobayashi M, Igarashi H, Takeda A, Kato M, Matano T (2005) Reversion in vivo after inoculation of a molecular proviral DNA clone of simian immunodeficiency virus with a cytotoxic-T-lymphocyte escape mutation. J Virol 79: 11529-11532.
58. Leslie A, Kavanagh D, Honeyborne I, Pfafferott K, Edwards C, et al. (2005) Transmission and accumulation of CTL escape variants drive negative associations between HIV polymorphisms and HLA. J Exp Med 201: 891-902.
59. Lartillot N, Philippe H (2004) A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol Biol Evol 21: 1095-1109.
60. Koup RA, Safrit JT, Cao Y, Andrews CA, McLeod G, et al. (1994) Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J Virol 68: 4650-4655.
61. Whelan S, Goldman N (2004) Estimating the frequency of events that cause multiple-nucleotide changes. Genetics 167: 2027-2043.
62. Lichterfeld M, Yu XG, Cohen D, Addo MM, Malenfant J, et al. (2004) HIV-1 Nef is preferentially recognized by CD8 T cells in primary HIV-1 infection despite a relatively high degree of genetic diversity. Aids 18: 1383-1392.
63. Calarese DA, Scanlan CN, Zwick MB, Deechongkit S, Mimura Y, et al. (2003) Antibody domain exchange is an immunological solution to carbohydrate cluster recognition. Science 300: 2065-2071.
64. Scanlan CN, Offer J, Zitzmann N, Dwek RA (2007) Exploiting the defensive sugars of HIV-1 for drug and vaccine design. Nature 446: 1038-1045.
65. Edwards BH, Bansal A, Sabbaj S, Bakari J, Mulligan MJ, et al. (2002) Magnitude of functional CD8+ T-cell responses to the gag protein of human immunodeficiency virus type 1 correlates inversely with viral load in plasma. J Virol 76: 2298-2305.
66. Gog JR, Rimmelzwaan GF, Osterhaus AD, Grenfell BT (2003) Population dynamics of rapid fixation in cytotoxic T lymphocyte escape mutants of influenza A. Proc Natl Acad Sci U S A 100: 11143-11147.
67. Shih AC-C, Hsiao T-C, Ho M-S, Li W-H (2007) Simultaneous amino acid substitutions at antigenic sites drive influenza A hemagglutinin evolution. Proc Natl Acad Sci U S A 104: 6283-6288.
68. Smith DJ, Lapedes AS, de Jong JC, Bestebroer TM, Rimmelzwaan GF, et al. (2004) Mapping the antigenic and genetic evolution of Influenza Virus. Science 305: 371-376.
69. Deeks SG, Hoh R, Grant RM, Wrin T, Barbour JD, et al. (2002) CD4+ T cell kinetics and activation in human immunodeficiency virus-infected patients who remain viremic despite long-term treatment with protease inhibitor-based therapy. J Infect Dis 185: 315-323.
70. Handel A, Regoes RR, Antia R (2006) The role of compensatory mutations in the emergence of drug resistance. PLoS Comput Biol 2: e137. doi:10.1371/journal.pcbi.0020137.
71. Seoighe C, Ketwaroo F, Pillay V, Scheffler K, Wood N, et al. (2007) A model of directional selection applied to the evolution of drug resistance in HIV-1. Mol Biol Evol 24: 1025-1031.
72. Altfeld M, Allen TM (2006) Hitting HIV where it hurts: An alternative approach to HIV vaccine design. Trends Immunol 27: 504-510.
73. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: A sequence logo generator. Genome Res 14: 1188-1190.