An introduction to a novel population genetic approach for HIV characterization

Infection, Genetics and Evolution

Volumn 10, Issue 8, 2010, Pages 1155-1164

  Perez Sweeney, Beatriz ^a   DeSalle, Rob ^a   Ho, John L ^b  

^a DIVISION OF INVERTEBRATE ZOOLOGY   (United States)

^b The Hospitalist Service   (United States)

Author keywords

Adaptation; Codon; Haiti; HIV; Parallel evolution; Phylogenetic; Population genetics; Selection; Variation

Indexed keywords

HLA ANTIGEN CLASS 1;

AMINO ACID COMPOSITION; ARTICLE; CODON; CONTROLLED STUDY; GENETIC VARIABILITY; GLYCOSYLATION; HAITI; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; MONOPHYLY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POPULATION DIFFERENTIATION; POPULATION GENETICS; PRIORITY JOURNAL; UNITED STATES; VIRUS GENOME; VIRUS ISOLATION;

AMINO ACID SEQUENCE; CODON; EVOLUTION, MOLECULAR; GENETIC VARIATION; HAITI; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HIV-1; HLA-A ANTIGENS; HUMANS; IMMUNE EVASION; PHYLOGENY; SELECTION, GENETIC; UNITED STATES;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 77957303086     PISSN: 15671348     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.meegid.2010.07.010     Document Type: Article

References (72)

1. Abascal F., Zardoya R., Posada D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005, 21:2104-2105.
2. Agosti D., Jacobs D., DeSalle R. On combining protein sequences and nucleic acid sequences in phylogenetic analysis: the homeobox protein case. Cladistics 1996, 12:65-82.
3. Barouch D.H., O'Brien K.L., Simmons N.L., King S.L., Abbink P., Maxfield L.F., Sun Y.H., La Porte A., Riggs A.M., Lynch D.M., Clark S.L., Backus K., Perry J.R., Seaman M.S., Carville A., Mansfield K.G., Szinger J.J., Fischer W., Muldoon M., Korber B. Mosaic HIV-1 vaccines expand the breadth and depth of cellular immune responses in rhesus monkeys. Nat. Med. 2010, 16:319-323.
4. Berger C.T., Carlson J.M., Brumme C.J., Hartman K.L., Brumme Z.L., Henry L.M., Rosato P.C., Piechocka-Trocha A., Brockman M.A., Harrigan P.R., Heckerman D., Kaufmann D.E., Brander C. Viral adaptation to immune selection pressure by HLA class I-restricted CTL responses targeting epitopes in HIV frameshift sequences. J. Exp. Med. 2010, 207:61-75. S61-12.
5. Bonhoeffer S., Holmes E.C., Nowak M.A. Causes of HIV diversity. Nature 1995, 376:125.
6. Botarelli P., Houlden B.A., Haigwood N.L., Servis C., Montagna D., Abrignani S. N-glycosylation of HIV-gp120 may constrain recognition by T lymphocytes. J. Immunol. 1991, 147:3128-3132.
7. Brumme Z.L., Brumme C.J., Carlson J., Streeck H., John M., Eichbaum Q., Block B.L., Baker B., Kadie C., Markowitz M., Jessen H., Kelleher A.D., Rosenberg E., Kaldor J., Yuki Y., Carrington M., Allen T.M., Mallal S., Altfeld M., Heckerman D., Walker B.D. Marked epitope- and allele-specific differences in rates of mutation in human immunodeficiency type 1 (HIV-1) Gag, Pol, and Nef cytotoxic T-lymphocyte epitopes in acute/early HIV-1 infection. J. Virol. 2008, 82:9216-9227.
8. Choisy M., Woelk C.H., Guegan J.F., Robertson D.L. Comparative study of adaptive molecular evolution in different human immunodeficiency virus groups and subtypes. J. Virol. 2004, 78:1962-1970.
9. Corey L., McElrath M.J. HIV vaccines: mosaic approach to virus diversity. Nat. Med. 2010, 16:268-270.
10. Daniels R.S., Kang C., Patel D., Xiang Z., Douglas N.W., Zheng N.N., Cho H.W., Lee J.S. An HIV type 1 subtype B founder effect in Korea: gp160 signature patterns infer circulation of CTL-escape strains at the population level. AIDS Res. Hum. Retroviruses 2003, 19:631-641.
11. de Jong J.J., Goudsmit J., Keulen W., Klaver B., Krone W., Tersmette M., de Ronde A. Human immunodeficiency virus type 1 clones chimeric for the envelope V3 domain differ in syncytium formation and replication capacity. J. Virol. 1992, 66:757-765.
12. Dighe P.K., Korber B.T., Foley B.T. Global Variation in the HIV-1 V3 Region 1997, Los Alamos National Laboratory, Los Alamos.
13. Douek D.C., Picker L.J., Koup R.A. T cell dynamics in HIV-1 infection. Annu. Rev. Immunol. 2003, 21:265-304.
14. Excoffier L. Analysis of population subdivision. Handbook of Statistical Genetics 2000, Wiley and Sons, Ltd. D. Balding, M. Bishop, C. Cannings (Eds.).
15. Excoffier L., Smouse P.E., Quattro J.M. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 1992, 131:479-491.
16. Fouchier R.A., Groenink M., Kootstra N.A., Tersmette M., Huisman H.G., Miedema F., Schuitemaker H. Phenotype-associated sequence variation in the third variable domain of the human immunodeficiency virus type 1 gp120 molecule. J. Virol. 1992, 66:3183-3187.
17. Gaschen B., Taylor J., Yusim K., Foley B., Gao F., Lang D., Novitsky V., Haynes B., Hahn B.H., Bhattacharya T., Korber B. Diversity considerations in HIV-1 vaccine selection. Science 2002, 296:2354-2360.
18. Gilbert M.T., Rambaut A., Wlasiuk G., Spira T.J., Pitchenik A.E., Worobey M. The emergence of HIV/AIDS in the Americas and beyond. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:18566-18570.
19. Goonetilleke N., Liu M.K., Salazar-Gonzalez J.F., Ferrari G., Giorgi E., Ganusov V.V., Keele B.F., Learn G.H., Turnbull E.L., Salazar M.G., Weinhold K.J., Moore S., Letvin N., Haynes B.F., Cohen M.S., Hraber P., Bhattacharya T., Borrow P., Perelson A.S., Hahn B.H., Shaw G.M., Korber B.T., McMichael A.J. The first T cell response to transmitted/founder virus contributes to the control of acute viremia in HIV-1 infection. J. Exp. Med. 2009, 206:1253-1272.
20. Hasegawa M., Yano T., Kishino H. A new molecular clock of mitochondrial DNA and the evolution of Hominoids. Proc. Jpn. Acad. B 1984, 60:95-98.
21. Hasegawa M., Kishino H., Yano T. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol. 1985, 22:160-174.
22. Hwang S.S., Boyle T.J., Lyerly H.K., Cullen B.R. Identification of the envelope V3 loop as the primary determinant of cell tropism in HIV-1. Science 1991, 253:71-74.
23. Jensen M.A., Li F.S., van't Wout A.B., Nickle D.C., Shriner D., He H.X., McLaughlin S., Shankarappa R., Margolick J.B., Mullins J.I. Improved coreceptor usage prediction and genotypic monitoring of R5-to-X4 transition by motif analysis of human immunodeficiency virus type 1 env V3 loop sequences. J. Virol. 2003, 77:13376-13388.
24. Kawashima Y., Pfafferott K., Frater J., Matthews P., Payne R., Addo M., Gatanaga H., Fujiwara M., Hachiya A., Koizumi H., Kuse N., Oka S., Duda A., Prendergast A., Crawford H., Leslie A., Brumme Z., Brumme C., Allen T., Brander C., Kaslow R., Tang J., Hunter E., Allen S., Mulenga J., Branch S., Roach T., John M., Mallal S., Ogwu A., Shapiro R., Prado J.G., Fidler S., Weber J., Pybus O.G., Klenerman P., Ndung'u T., Phillips R., Heckerman D., Harrigan P.R., Walker B.D., Takiguchi M., Goulder P. Adaptation of HIV-1 to human leukocyte antigen class I. Nature 2009, 458:641-645.
25. Kelleher A.D., Long C., Holmes E.C., Allen R.L., Wilson J., Conlon C., Workman C., Shaunak S., Olson K., Goulder P., Brander C., Ogg G., Sullivan J.S., Dyer W., Jones I., McMichael A.J., Rowland-Jones S., Phillips R.E. Clustered mutations in HIV-1 gag are consistently required for escape from HLA-B27-restricted cytotoxic T lymphocyte responses. J. Exp. Med. 2001, 193:375-386.
26. Kiepiela P., Ngumbela K., Thobakgale C., Ramduth D., Honeyborne I., Moodley E., Reddy S., de Pierres C., Mncube Z., Mkhwanazi N., Bishop K., van der Stok M., Nair K., Khan N., Crawford H., Payne R., Leslie A., Prado J., Prendergast A., Frater J., McCarthy N., Brander C., Learn G.H., Nickle D., Rousseau C., Coovadia H., Mullins J.I., Heckerman D., Walker B.D., Goulder P. CD8+ T-cell responses to different HIV proteins have discordant associations with viral load. Nat. Med. 2007, 13:46-53.
27. Korber B., Muldoon M., Theiler J., Gao F., Gupta R., Lapedes A., Hahn B.H., Wolinsky S., Bhattacharya T. Timing the ancestor of the HIV-1 pandemic strains. Science 2000, 288:1789-1796.
28. Li W.H., Tanimura M., Sharp P.M. Rates and dates of divergence between AIDS virus nucleotide sequences. Mol. Biol. Evol. 1988, 5:313-330.
29. Maddison D.R., Maddison W.P. MacClade4 2003, Sinauer Associates, Inc., Sunderland.
30. Moore C.B., John M., James I.R., Christiansen F.T., Witt C.S., Mallal S.A. Evidence of HIV-1 adaptation to HLA-restricted immune responses at a population level. Science 2002, 296:1439-1443.
31. Moore J.P., Kitchen S.G., Pugach P., Zack J.A. The CCR5 and CXCR4 coreceptors - central to understanding the transmission and pathogenesis of human immunodeficiency virus type 1 infection. AIDS Res. Hum. Retroviruses 2004, 20:111-126.
32. Muse S.V., Gaut B.S. A likelihood approach for comparing synonymous and nonsynonymous nucleotide substitution rates, with application to the chloroplast genome. Mol. Biol. Evol. 1994, 11:715-724.
33. Nei M., Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 1986, 3:418-426.
34. Nickle D.C., Rolland M., Jensen M.A., Pond S.L., Deng W., Seligman M., Heckerman D., Mullins J.I., Jojic N. Coping with viral diversity in HIV vaccine design. PLoS Comput. Biol. 2007, 3:e75.
35. Ogg G.S., Jin X., Bonhoeffer S., Dunbar P.R., Nowak M.A., Monard S., Segal J.P., Cao Y., Rowland-Jones S.L., Cerundolo V., Hurley A., Markowitz M., Ho D.D., Nixon D.F., McMichael A.J. Quantitation of HIV-1-specific cytotoxic T lymphocytes and plasma load of viral RNA. Science 1998, 279:2103-2106.
36. Oliveira T., Salemi M., Gordon M., Vandamme A.-M., Rensburg E.J., Engelbrecht S., Hoosen M., Cassol S. Mapping sites of positive selection and amino acid diversification in the HIV genome: an alternative approach to vaccine design?. Genetics 2004, 167:1047-1058.
37. Ota T., Nei M. Variance and covariances of the numbers of synonymous and nonsynonymous substitutions per site. Mol. Biol. Evol. 1994, 11:613-619.
38. Papandreou M.J., Idziorek T., Miquelis R., Fenouillet E. Glycosylation and stability of mature HIV envelope glycoprotein conformation under various conditions. FEBS Lett. 1996, 379:171-176.
39. Pape J.W., Liautaud B., Thomas F., Mathurin J.R., St Amand M.M., Boncy M., Pean V., Pamphile M., Laroche A.C., Johnson W.D. Characteristics of the acquired immunodeficiency syndrome (AIDS) in Haiti. N. Engl. J. Med. 1983, 309:945-950.
40. Peakall R., Smouse P.E. Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes 2006, 6:288-295.
41. Phillips R.E., Rowland-Jones S., Nixon D.F., Gotch F.M., Edwards J.P., Ogunlesi A.O., Elvin J.G., Rothbard J.A., Bangham C.R., Rizza C.R., et al. Human immunodeficiency virus genetic variation that can escape cytotoxic T cell recognition. Nature 1991, 354:453-459.
42. Pollakis G., Kang S., Kliphuis A., Chalaby M.I., Goudsmit J., Paxton W.A. N-linked glycosylation of the HIV type-1 gp120 envelope glycoprotein as a major determinant of CCR5 and CXCR4 coreceptor utilization. J. Biol. Chem. 2001, 276:13433-13441.
43. Pond S.L., Frost S.D. Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 2005, 21:2531-2533.
44. Pond S.L., Frost S.D.W. Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol. Biol. Evol. 2005, 22:1208-1222.
45. Pond S.L., Frost S.D., Grossman Z., Gravenor M.B., Richman D.D., Brown A.J. Adaptation to different human populations by HIV-1 revealed by codon-based analyses. PLoS Comput. Biol. 2006, 2:e62.
46. Posada D., Crandall K.A. Modeltest: testing the model of DNA substitution. Bioinformatics 1998, 14:817-818.
47. Rambaut A., Posada D., Crandall K.A., Holmes E.C. The causes and consequences of HIV evolution. Nat. Rev. Genet. 2004, 5:52-61.
48. Raymond M., Rousset F. An exact test for population differentiation. Evolution 1995, 49:1280-1283.
49. Richman D.D., Wrin T., Little S.J., Petropoulos C.J. Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:4144-4149.
50. Ronquist F., Huelsenbeck J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
51. Ross H.A., Rodrigo A.G. Immune-mediated positive selection drives human immunodeficiency virus type 1 molecular variation and predicts disease duration. J. Virol. 2002, 76:11715-11720.
52. Salazar-Gonzalez J.F., Salazar M.G., Keele B.F., Learn G.H., Giorgi E.E., Li H., Decker J.M., Wang S., Baalwa J., Kraus M.H., Parrish N.F., Shaw K.S., Guffey M.B., Bar K.J., Davis K.L., Ochsenbauer-Jambor C., Kappes J.C., Saag M.S., Cohen M.S., Mulenga J., Derdeyn C.A., Allen S., Hunter E., Markowitz M., Hraber P., Perelson A.S., Bhattacharya T., Haynes B.F., Korber B.T., Hahn B.H., Shaw G.M. Genetic identity, biological phenotype, and evolutionary pathways of transmitted/founder viruses in acute and early HIV-1 infection. J. Exp. Med. 2009, 206:1273-1289.
53. Samson M., Libert F., Doranz B.J., Rucker J., Liesnard C., Farber C.M., Saragosti S., Lapoumeroulie C., Cognaux J., Forceille C., Muyldermans G., Verhofstede C., Burtonboy G., Georges M., Imai T., Rana S., Yi Y., Smyth R.J., Collman R.G., Doms R.W., Vassart G., Parmentier M. Resistance to HIV-1 infection in caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature 1996, 382:722-725.
54. Sanjuan R., Codoner F.M., Moya A., Elena S.F. Natural selection and the organ-specific differentiation of HIV-1 V3 hypervariable region. Evolution 2004, 58:1185-1194.
55. Santra S., Liao H.X., Zhang R., Muldoon M., Watson S., Fischer W., Theiler J., Szinger J., Balachandran H., Buzby A., Quinn D., Parks R.J., Tsao C.Y., Carville A., Mansfield K.G., Pavlakis G.N., Felber B.K., Haynes B.F., Korber B.T., Letvin N.L. Mosaic vaccines elicit CD8+ T lymphocyte responses that confer enhanced immune coverage of diverse HIV strains in monkeys. Nat. Med. 2010, 16:324-328.
56. Schneider S., Roessli D., Excoffier L. Arlequin Ver 2.0: A Software for Population Genetics Data Analysis 2000, Genetics and Biometry Laboratory, University of Geneva, Switzerland.
57. Shioda T., Levy J.A., Cheng-Mayer C. Small amino acid changes in the V3 hypervariable region of gp120 can affect the T-cell-line and macrophage tropism of human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:9434-9438.
58. Slobod K.S., Bonsignori M., Brown S.A., Zhan X.Y., Stambas J., Hurwitz J.L. HIV vaccines: brief review and discussion of future directions. Exp. Rev. Vac. 2005, 4:305-313.
59. Stamatakis A., Hoover P., Rougemont J. A rapid bootstrap algorithm for the RAxML Web servers. Syst. Biol. 2008, 57:758-771.
60. Suzuki Y., Gojobori T. A method for detecting positive selection at single amino acid sites. Mol. Biol. Evol. 1999, 16:1315-1328.
61. Swofford D.L. PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods) 2001, Sinauer Associates, Sunderland, MA.
62. Travers S.A., O'Connell M.J., McCormack G.P., McInerney J.O. Evidence for heterogeneous selective pressures in the evolution of the env gene in different human immunodeficiency virus type 1 subtypes. J. Virol. 2005, 79:1836-1841.
63. Wei X., Decker J.M., Wang S., Hui H., Kappes J.C., Wu X., Salazar-Gonzalez J.F., Salazar M.G., Kilby J.M., Saag M.S., Komarova N.L., Nowak M.A., Hahn B.H., Kwong P.D., Shaw G.M. Antibody neutralization and escape by HIV-1. Nature 2003, 422:307-312.
64. Williamson S. Adaptation in the env gene of HIV-1 and evolutionary theories of disease progression. Mol. Biol. Evol. 2003, 20:1318-1325.
65. Wyatt R., Sullivan N., Thali M., Repke H., Ho D., Robinson J., Posner M., Sodroski J. Functional and immunologic characterization of human immunodeficiency virus type 1 envelope glycoproteins containing deletions of the major variable regions. J. Virol. 1993, 67:4557-4565.
66. Yamaguchi Y., Gojobori T. Evolutionary mechanisms and population dynamics of the third variable envelope region of HIV within single hosts. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:1264-1269.
67. Yamaguchi-Kabata Y., Gojobori T. Reevaluation of amino acid variability of the human immunodeficiency virus type 1 gp120 envelope glycoprotein and prediction of new discontinuous epitopes. J. Virol. 2000, 74:4335-4350.
68. Yang O.O. Retracing our STEP towards a successful CTL-based HIV-1 vaccine. Vaccine 2008, 26:3138-3141.
69. Yang Z., Nelson R. Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol. Biol. Evol. 2000, 17:32-43.
70. Yang W., Bielawski J.P., Ziheng Y. Widespread adaptive evolution in the human immunodeficiency virus type 1 genome. J. Mol. Evol. 2003, 57:212-221.
71. Yusim K., Kesmir C., Gaschen B., Addo M.M., Altfeld M., Brunak S., Chigaev A., Detours V., Korber B.T. 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. 2002, 76:8757-8768.
72. Zanotto P.M., Kallas E.G., de Souza R.F., Holmes E.C. Genealogical evidence for positive selection in the nef gene of HIV-1. Genetics 1999, 153:1077-1089.