HIV populations are large and accumulate high genetic diversity in a nonlinear fashion

Journal of Virology

Volumn 87, Issue 18, 2013, Pages 10313-10323

  Maldarelli, Frank ^a   Kearney, Mary ^a   Palmer, Sarah ^a,h   Stephens, Robert ^b   Mican, JoAnn ^c   Polis, Michael A ^c   Davey, Richard T ^c   Kovacs, Joseph ^d   Shao, Wei ^b   Rock Kress, Diane ^c   Metcalf, Julia A ^c   Rehm, Catherine ^c   Greer, Sarah E ^d   Lucey, Daniel L ^e   Danley, Kristen ^a   Alter, Harvey ^d   Mellors, John W ^f   Coffina, John M ^a,g  

^a NATIONAL CANCER INSTITUTE   (United States)

^b SAIC FREDERICK INC   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

^e WASHINGTON HOSPITAL CENTER   (United States)

^f UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^g TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h WESTMEAD HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BIOACCUMULATION; CD4 LYMPHOCYTE COUNT; CLINICAL ARTICLE; EFFECTIVE POPULATION SIZE; FEMALE; GENE FREQUENCY; GENE SEQUENCE; GENETIC VARIABILITY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IN VIVO STUDY; LYMPHOCYTOPENIA; MALE; NONHUMAN; NONLINEAR SYSTEM; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PRO GENE; STRUCTURAL GENE; UNINDEXED SEQUENCE; VIRUS GENE; VIRUS MUTATION; VIRUS PARTICLE; VIRUS REPLICATION;

ADULT; AMINO ACID SUBSTITUTION; FEMALE; GENETIC VARIATION; HIV; HIV INFECTIONS; HIV PROTEASE; HUMANS; MALE; MIDDLE AGED; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; POL GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; SEQUENCE ANALYSIS, DNA; YOUNG ADULT;

EID: 84883274824     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01225-12     Document Type: Article

References (61)

1. Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, Salazar MG, Sun C, Grayson T, Wang S, Li H, Wei X, Jiang C, Kirchherr JL, Gao F, Anderson JA, Ping LH, Swanstrom R, Tomaras GD, Blattner WA, Goepfert PA, Kilby JM, Saag MS, Delwart EL, Busch MP, Cohen MS, Montefiori DC, Haynes BF, Gaschen B, Athreya GS, Lee HY, Wood N, Seoighe C, Perelson AS, Bhattacharya T, Korber BT, Hahn BH, Shaw GM. 2008. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc. Natl. Acad. Sci. U. S. A. 105:7552-7557.
2. Poss M. Martin HL, Kreiss JK, Granville L, Chohan B, Nyange P, Mandaliya K, Overbaugh J. 1995. Diversity in virus populations from genital secretions and peripheral blood from women recently infected with human immunodeficiency virus type 1. J. Virol. 69:8118-8122.
3. Salazar-Gonzalez JF, Bailes E, Pham KT, Salazar MG, Guffey MB, Keele BF, Derdeyn CA, Farmer P, Hunter E, Allen S, Manigart O, Mulenga J, Anderson JA, Swanstrom R, Haynes BF, Athreya GS, Korber BT, Sharp PM, Shaw GM, Hahn BH. 2008. Deciphering human immunodeficiency virus type 1 transmission and early envelope diversification by singlegenome amplification and sequencing. J. Virol. 82:3952-3970.
4. Wolinsky SM, Wike CM, Korber BT, Hutto C, Parks WP, Rosenblum LL, Kunstman KJ, Furtado MR, Munoz JL. 1992. Selective transmission of human immunodeficiency virus type-1 variants from mothers to infants. Science 255:1134-1137.
5. Kearney M, Maldarelli F, Shao W, Margolick JB, Daar ES, Mellors JW, Rao V, Coffin JM, Palmer S. 2009. Human immunodeficiency virus type 1 population genetics and adaptation in newly infected individuals. J. Virol. 83:2715-2727.
6. Mansky LM, Temin HM. 1995. Lower in vivo mutation rate of human immunodeficiency virus type 1 than that predicted from the fidelity of purified reverse transcriptase. J. Virol. 69:5087-5094.
7. Althaus CL, Bonhoeffer S. 2005. Stochastic interplay between mutation and recombination during the acquisition of drug resistance mutations in human immunodeficiency virus type 1. J. Virol. 79:13572-13578.
8. Coffin JM. 1995. HIV population dynamics in vivo: implications for genetic variation, pathogenesis, and therapy. Science 267:483-489.
9. Daar ES, Richman DD. 2005. Confronting the emergence of drugresistant HIV type 1: impact of antiretroviral therapy on individual and population resistance. AIDS Res. Hum. Retroviruses 21:343-357.
10. Frost SD, McLean AR. 1994. Quasispecies dynamics and the emergence of drug resistance during zidovudine therapy of HIV infection. AIDS 8:323-332.
11. Frost SD, Nijhuis M, Schuurman R, Boucher CA, Brown AJ. 2000. Evolution of lamivudine resistance in human immunodeficiency virus type 1-infected individuals: the relative roles of drift and selection. J. Virol. 74:6262-6268.
12. Mullins JI, Jensen MA. 2006. Evolutionary dynamics of HIV-1 and the control of AIDS. Curr. Top. Microbiol. Immunol. 299:171-192.
13. Overbaugh J, Bangham CR. 2001. Selection forces and constraints on retroviral sequence variation. Science 292:1106-1109.
14. Rong L, Gilchrist MA, Feng Z, Perelson AS. 2007. Modeling within-host HIV-1 dynamics and the evolution of drug resistance: trade-offs between viral enzyme function and drug susceptibility. J. Theor. Biol. 247:804-818.
15. Rouzine IM, Coffin JM. 1999. Linkage disequilibrium test implies a large effective population number for HIV in vivo. Proc. Natl. Acad. Sci. U. S. A. 96:10758-10763.
16. Rouzine IM, Rodrigo A, Coffin JM. 2001. Transition between stochastic evolution and deterministic evolution in the presence of selection: general theory and application to virology. Microbiol. Mol. Biol. Rev. 65:151-185.
17. Shankarappa R, Margolick JB, Gange SJ, Rodrigo AG, Upchurch D, Farzadegan H, Gupta P, Rinaldo CR, Learn GH, He X, Huang XL, Mullins JI. 1999. Consistent viral evolutionary changes associated with the progression of human immunodeficiency virus type 1 infection. J. Virol. 73:10489-10502.
18. Jordan MR, Kearney M, Palmer S, Shao W, Maldarelli F, Coakley EP, Chappey C, Wanke C, Coffin JM. 2010. Comparison of standard PCR/ cloning to single genome sequencing for analysis of HIV-1 populations. J. Virol. Methods 168:114-120.
19. Mens H, Kearney M, Wiegand A, Shao W, Schonning K, Gerstoft J, Obel N, Maldarelli F, Mellors JW, Benfield T, Coffin JM. 2010. HIV-1 continues to replicate and evolve in patients with natural control of HIV infection. J. Virol. 84:12971-12981.
20. Palmer S, Kearney M, Maldarelli F, Halvas EK, Bixby CJ, Bazmi H, Rock D, Falloon J, Davey RT, Jr, Dewar RL, Metcalf JA, Hammer S, Mellors JW, Coffin JM. 2005. Multiple, linked human immunodeficiency virus type 1 drug resistance mutations in treatment-experienced patients are missed by standard genotype analysis. J. Clin. Microbiol. 43:406-413.
21. Achaz G, Palmer S, Kearney M, Maldarelli F, Mellors JW, Coffin JM, Wakeley J. 2004. A robust measure of HIV-1 population turnover within chronically infected individuals. Mol. Biol. Evol. 21:1902-1912.
22. Batorsky R, Kearney MF, Palmer SE, Maldarelli F, Rouzine IM, Coffin JM. 2011. Estimate of effective recombination rate and average selection coefficient for HIV in chronic infection. Proc. Natl. Acad. Sci. U. S. A. 108:5661-5666.
23. Dykes C, Najjar J, Bosch RJ, Wantman M, Furtado M, Hart S, Hammer SM, Demeter LM. 2004. Detection of drug-resistant minority variants of HIV-1 during virologic failure of indinavir, lamivudine, and zidovudine. J. Infect. Dis. 189:1091-1096.
24. Elbeik T, Alvord WG, Trichavaroj R, de Souza M, Dewar R, Brown A, Chernoff D, Michael NL, Nassos P, Hadley K, Ng VL. 2002. Comparative analysis of HIV-1 viral load assays on subtype quantification: Bayer Versant HIV-1 RNA 3.0 versus Roche Amplicor HIV-1 Monitor version 1.5. J. Acquir. Immune Defic. Syndr. 29:330-339.
25. Kearney M, Palmer S, Maldarelli F, Shao W, Polis MA, Mican J, Rock-Kress D, Margolick JB, Coffin JM, Mellors JW. 2008. Frequent polymorphism at drug resistance sites in HIV-1 protease and reverse transcriptase. AIDS 22:497-501.
26. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R. 2003. DnaSP, DNApolymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496-2497.
27. Nei M, Kumar S. 2000. Molecular evolution and phylogenetics. Oxford University Press, Inc, New York, NY.
28. Nei M. 1987. Molecular evolutionary genetics. Columbia University Press, New York, NY.
29. Watterson GA. 1975. On the number of segregating sites in genetical models without recombination. Theor. Popul. Biol. 7:256-276.
30. Tajima F. 1983. Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437-460.
31. Tajima F, Nei M. 1984. Note on genetic drift and estimation of effective population size. Genetics 106:569-574.
32. Waples RS. 1989. A generalized approach for estimating effective population size from temporal changes in allele frequency. Genetics 121:379-391.
33. Brown AJ. 1997. Analysis of HIV-1 env gene sequences reveals evidence for a low effective number in the viral population. Proc. Natl. Acad. Sci. U. S. A. 94:1862-1865.
34. Perelson AS, Essunger P, Cao Y, Vesanen M, Hurley A, Saksela K, Markowitz M, Ho DD. 1997. Decay characteristics of HIV-1-infected compartments during combination therapy. Nature 387:188-191.
35. Perelson AS, Neumann AU, Markowitz M, Leonard JM, Ho DD. 1996. HIV-1 dynamics in vivo: virion clearance rate, infected cell life-span, and viral generation time. Science 271:1582-1586.
36. Josefsson L, King MS, Makitalo B, Brannstrom J, Shao W, Maldarelli F, Kearney MF, Hu WS, Chen J, Gaines H, Mellors JW, Albert J, Coffin JM, Palmer SE. 2011. Majority of CD4+ T cells from peripheral blood of HIV-1-infected individuals contain only one HIV DNA molecule. Proc. Natl. Acad. Sci. U. S. A. 108:11199-11204.
37. Hudson R.R. 1983. Properties of a neutral allele model with intragenic recombination. Theor. Popul. Biol. 23:183-201.
38. Drummond AJ, Nicholls GK, Rodrigo AG, Solomon W. 2002. Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics 161:1307-1320.
39. Frost SD, Dumaurier MJ, Wain-Hobson S, Brown AJ. 2001. Genetic drift and within-host metapopulation dynamics of HIV-1 infection. Proc. Natl. Acad. Sci. U. S. A. 98:6975-6980.
40. Seo TK, Thorne JL, Hasegawa M, Kishino H. 2002. Estimation of effective population size of HIV-1 within a host: a pseudomaximumlikelihood approach. Genetics 160:1283-1293.
41. Shriner D, Shankarappa R, Jensen MA, Nickle DC, Mittler JE, Margolick JB, Mullins JI. 2004. Influence of random genetic drift on human immunodeficiency virus type 1 env evolution during chronic infection. Genetics 166:1155-1164.
42. Liu Y, Mittler JE. 2008. Selection dramatically reduces effective population size in HIV-1 infection. BMC Evol. Biol. 8:133. doi:10.1186/1471-2148-8-133.
43. Rossenkhan R, Novitsky V, Sebunya TK, Musonda R, Gashe BA, Essex M. 2012. Viral diversity and diversification of major non-structural genes vif, vpr, vpu, tat exon 1 and rev exon 1 during primary HIV-1 subtype C infection. PLoS One 7:e35491. doi:10.1371/journal.pone.0035491.
44. Bello G, Casado C, Garcia S, Rodriguez C, del Romero J, Borderia AV, Lopez-Galindez C. 2004. Plasma RNA viral load is not associated with intrapatient quasispecies heterogeneity in HIV-1 infection. Arch. Virol. 149:1761-1771.
45. Lemey P, Kosakovsky Pond SL, Drummond AJ, Pybus OG, Shapiro B, Barroso H, Taveira N, Rambaut A. 2007. Synonymous substitution rates predict HIV disease progression as a result of underlying replication dynamics. PLoS Comput. Biol. 3:e29. doi:10.1371/journal.pcbi.0030029.
46. Bello G, Casado C, Garcia S, Rodriguez C, del Romero J, Carvajal-Rodriguez A, Posada D, Lopez-Galindez C. 2007. Lack of temporal structure in the short term HIV-1 evolution within asymptomatic naive patients. Virology 362:294-303.
47. Yusim K, Peeters M, Pybus OG, Bhattacharya T, Delaporte E, Mulanga C, Muldoon M, Theiler J, Korber B. 2001. Using human immunodeficiency virus type 1 sequences to infer historical features of the acquired immune deficiency syndrome epidemic and human immunodeficiency virus evolution. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356:855-866.
48. Leslie AJ, Pfafferott KJ, Chetty P, Draenert R, Addo MM, Feeney M, Tang Y, Holmes EC, Allen T, Prado JG, Altfeld M, Brander C, Dixon C, Ramduth D, Jeena P, Thomas SA, St John A, Roach TA, Kupfer B, Luzzi G, Edwards A, Taylor G, Lyall H, Tudor-Williams G, Novelli V, Martinez-Picado J, Kiepiela P, Walker BD, Goulder PJ. 2004. HIV evolution: CTL escape mutation and reversion after transmission. Nat. Med. 10:282-289.
49. Liu Y, McNevin JP, Holte S, McElrath MJ, Mullins JI. 2011. Dynamics of viral evolution and CTL responses in HIV-1 infection. PLoS One 6:e15639. doi:10.1371/journal.pone.0015639.
50. Troyer RM, McNevin J, Liu Y, Zhang SC, Krizan RW, Abraha A, Tebit DM, Zhao H, Avila S, Lobritz MA, McElrath MJ, Le Gall S, Mullins JI, Arts EJ. 2009. Variable fitness impact of HIV-1 escape mutations to cytotoxic T lymphocyte (CTL) response. PLoS Pathog. 5:e1000365. doi:10 .1371/journal.ppat.1000365.
51. Edwards CT, Holmes EC, Pybus OG, Wilson DJ, Viscidi RP, Abrams EJ, Phillips RE, Drummond AJ. 2006. Evolution of the human immunodeficiency virus envelope gene is dominated by purifying selection. Genetics 174:1441-1453.
52. Rouzine IM, Coffin JM. 2005. Evolution of human immunodeficiency virus under selection and weak recombination. Genetics 170:7-18.
53. Rouzine IM, Coffin JM. 1999. Search for the mechanism of genetic variation in the pro gene of human immunodeficiency virus. J. Virol. 73:8167-8178.
54. Johnson JA, Li JF, Morris L, Martinson N, Gray G, McIntyre J, Heneine W. 2005. Emergence of drug-resistant HIV-1 after intrapartum administration of single-dose nevirapine is substantially underestimated. J. Infect. Dis. 192:16-23.
55. Sheldon J, Ramos B, Garcia-Samaniego J, Rios P, Bartholomeusz A, Romero M, Locarnini S, Zoulim F, Soriano V. 2007. Selection of hepatitis B virus (HBV) vaccine escape mutants in HBV-infected and HBV/ HIV-coinfected patients failing antiretroviral drugs with anti-HBV activity. J. Acquir. Immune Defic. Syndr. 46:279-282.
56. Zoulim F, Locarnini S. 2009. Hepatitis B virus resistance to nucleos(t)ide analogues. Gastroenterology 137:1593-1608.e2. doi:10.1053/j.gastro.2009.08 .063.
57. Bernini F, Ebranati E, De Maddalena C, Shkjezi R, Milazzo L, Lo Presti A, Ciccozzi M, Galli M, Zehender G. 2011. Within-host dynamics of the hepatitis C virus quasispecies population in HIV-1/HCV coinfected patients. PLoS One 6:e16551. doi:10.1371/journal.pone.0016551.
58. Honda M, Kaneko S, Sakai A, Unoura M, Murakami S, Kobayashi K. 1994. Degree of diversity of hepatitis C virus quasispecies and progression of liver disease. Hepatology 20:1144-1151.
59. Liu L, Fisher BE, Dowd KA, Astemborski J, Cox AL, Ray SC. 2010. Acceleration of hepatitis C virus envelope evolution in humans is consistent with progressive humoral immune selection during the transition from acute to chronic infection. J. Virol. 84:5067-5077.
60. Liu Z, Netski DM, Mao Q, Laeyendecker O, Ticehurst JR, Wang XH, Thomas DL, Ray SC. 2004. Accurate representation of the hepatitis C virus quasispecies in 5.2-kilobase amplicons. J. Clin. Microbiol. 42:4223-4229.
61. Netski DM, Mao Q, Ray SC, Klein RS. 2008. Genetic divergence of hepatitis C virus: the role of HIV-related immunosuppression. J. Acquir. Immune Defic. Syndr. 49:136-141.