Differences in the Selection Bottleneck between Modes of Sexual Transmission Influence the Genetic Composition of the HIV-1 Founder Virus

PLoS Pathogens

Volumn 12, Issue 5, 2016, Pages

  Tully, Damien C ^a   Ogilvie, Colin B ^a   Batorsky, Rebecca E ^a   Bean, David J ^a   Power, Karen A ^a   Ghebremichael, Musie ^a   Bedard, Hunter E ^a   Gladden, Adrianne D ^a   Seese, Aaron M ^a   Amero, Molly A ^a   Lane, Kimberly ^a   McGrath, Graham ^b   Bazner, Suzane B ^b   Tinsley, Jake ^c   Lennon, Niall J ^d   Henn, Matthew R ^d   Brumme, Zabrina L ^e   Norris, Philip J ^f   Rosenberg, Eric S ^b   Mayer, Kenneth H ^c   Jessen, Heiko ^g   Kosakovsky Pond, Sergei L ^h   Walker, Bruce D ^a,i   Altfeld, Marcus ^a,j   Carlson, Jonathan M ^k   Allen, Todd M ^a   more..

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c FENWAY INSTITUTE   (United States)

^d BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^e SIMON FRASER UNIVERSITY   (Canada)

^f BLOOD SYSTEMS RESEARCH INSTITUTE   (United States)

^g HIV Clinic Praxis Jessen   (Germany)

^h UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

ⁱ HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^j LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

^k MICROSOFT RESEARCH   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

AREA UNDER THE CURVE; ARTICLE; GENETIC VARIABILITY; HETEROSEXUALITY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; INFECTION RISK; MAJOR CLINICAL STUDY; MEN WHO HAVE SEX WITH MEN; META ANALYSIS (TOPIC); NONHUMAN; PHYLOGENY; RECEIVER OPERATING CHARACTERISTIC; SEQUENCE ANALYSIS; SEXUAL TRANSMISSION; VIRAL GENETICS; VIRUS ENVELOPE; VIRUS REPLICATION; VIRUS TRANSMISSION; GENETIC SELECTION; GENETIC VARIATION; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MALE; MOLECULAR EVOLUTION; POLYMERASE CHAIN REACTION; THEORETICAL MODEL; TRANSMISSION; VIRUS GENOME;

GLYCOPROTEIN GP 120;

EVOLUTION, MOLECULAR; GENETIC VARIATION; GENOME, VIRAL; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HIV-1; HUMANS; MALE; MODELS, THEORETICAL; POLYMERASE CHAIN REACTION; SELECTION, GENETIC;

EID: 84973338484     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005619     Document Type: Article

References (115)

1. UNAIDS. 2013.
2. Zhang LQ, MacKenzie P, Cleland A, Holmes EC, Brown AJ, Simmonds P, Selection for specific sequences in the external envelope protein of human immunodeficiency virus type 1 upon primary infection. J Virol. 1993;67(6):3345–56. Epub 1993/06/01. 8497055
3. Wolinsky SM, Wike CM, Korber BT, Hutto C, Parks WP, Rosenblum LL, et al. Selective transmission of human immunodeficiency virus type-1 variants from mothers to infants. Science. 1992;255(5048):1134–7. Epub 1992/02/28. 1546316
4. Zhu T, Mo H, Wang N, Nam DS, Cao Y, Koup RA, et al. Genotypic and phenotypic characterization of HIV-1 patients with primary infection. Science. 1993;261(5125):1179–81. Epub 1993/08/27. 8356453
5. Wolfs TF, Zwart G, Bakker M, Goudsmit J, HIV-1 genomic RNA diversification following sexual and parenteral virus transmission. Virology. 1992;189(1):103–10. Epub 1992/07/01. 1376536
6. McNearney T, Hornickova Z, Markham R, Birdwell A, Arens M, Saah A, et al. Relationship of human immunodeficiency virus type 1 sequence heterogeneity to stage of disease. Proc Natl Acad Sci U S A. 1992;89(21):10247–51. Epub 1992/11/01. 1438212
7. Haaland RE, Hawkins PA, Salazar-Gonzalez J, Johnson A, Tichacek A, Karita E, et al. Inflammatory genital infections mitigate a severe genetic bottleneck in heterosexual transmission of subtype A and C HIV-1. PLoS Pathog. 2009;5(1):e1000274. Epub 2009/01/24. doi: 10.1371/journal.ppat.100027419165325
8. Zhang ZQ, Wietgrefe SW, Li Q, Shore MD, Duan L, Reilly C, et al. Roles of substrate availability and infection of resting and activated CD4+ T cells in transmission and acute simian immunodeficiency virus infection. Proc Natl Acad Sci U S A. 2004;101(15):5640–5. Epub 2004/04/06. 15064398
9. Naranbhai V, Abdool Karim SS, Altfeld M, Samsunder N, Durgiah R, Sibeko S, et al. Innate immune activation enhances hiv acquisition in women, diminishing the effectiveness of tenofovir microbicide gel. J Infect Dis. 2012;206(7):993–1001. Epub 2012/07/26. 22829639
10. Taha TE, Hoover DR, Dallabetta GA, Kumwenda NI, Mtimavalye LA, Yang LP, et al. Bacterial vaginosis and disturbances of vaginal flora: association with increased acquisition of HIV. AIDS. 1998;12(13):1699–706. Epub 1998/10/09. 9764791
11. Galvin SR, Cohen MS, The role of sexually transmitted diseases in HIV transmission. Nat Rev Microbiol. 2004;2(1):33–42. Epub 2004/03/24. 15035007
12. Carlson JM, Schaefer M, Monaco DC, Batorsky R, Claiborne DT, Prince J, et al. HIV transmission. Selection bias at the heterosexual HIV-1 transmission bottleneck. Science. 2014;345(6193):1254031. Epub 2014/07/12. doi: 10.1126/science.125403125013080
13. Lee HY, Giorgi EE, Keele BF, Gaschen B, Athreya GS, Salazar-Gonzalez JF, et al. Modeling sequence evolution in acute HIV-1 infection. J Theor Biol. 2009;261(2):341–60. Epub 2009/08/08. doi: 10.1016/j.jtbi.2009.07.03819660475
14. Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, Salazar MG, et al. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci U S A. 2008;105(21):7552–7. Epub 2008/05/21. doi: 10.1073/pnas.080220310518490657
15. Abrahams MR, Anderson JA, Giorgi EE, Seoighe C, Mlisana K, Ping LH, et al. Quantitating the multiplicity of infection with human immunodeficiency virus type 1 subtype C reveals a non-poisson distribution of transmitted variants. J Virol. 2009;83(8):3556–67. Epub 2009/02/06. doi: 10.1128/JVI.02132-0819193811
16. Salazar-Gonzalez JF, Salazar MG, Keele BF, Learn GH, Giorgi EE, Li H, et al. Genetic identity, biological phenotype, and evolutionary pathways of transmitted/founder viruses in acute and early HIV-1 infection. J Exp Med. 2009;206(6):1273–89. Epub 2009/06/03. doi: 10.1084/jem.2009037819487424
17. Salazar-Gonzalez JF, Bailes E, Pham KT, Salazar MG, Guffey MB, Keele BF, et al. Deciphering human immunodeficiency virus type 1 transmission and early envelope diversification by single-genome amplification and sequencing. J Virol. 2008;82(8):3952–70. Epub 2008/02/08. doi: 10.1128/JVI.02660-0718256145
18. Fischer W, Ganusov VV, Giorgi EE, Hraber PT, Keele BF, Leitner T, et al. Transmission of single HIV-1 genomes and dynamics of early immune escape revealed by ultra-deep sequencing. PLoS One. 2010;5(8):e12303. Epub 2010/09/03. doi: 10.1371/journal.pone.001230320808830
19. Li H, Bar KJ, Wang S, Decker JM, Chen Y, Sun C, et al. High Multiplicity Infection by HIV-1 in Men Who Have Sex with Men. PLoS Pathog. 2010;6(5):e1000890. Epub 2010/05/21. doi: 10.1371/journal.ppat.100089020485520
20. Patel P, Borkowf CB, Brooks JT, Lasry A, Lansky A, Mermin J, Estimating per-act HIV transmission risk: a systematic review. AIDS. 2014;28(10):1509–19. Epub 2014/05/09. doi: 10.1097/QAD.000000000000029824809629
21. Derdeyn CA, Decker JM, Bibollet-Ruche F, Mokili JL, Muldoon M, Denham SA, et al. Envelope-constrained neutralization-sensitive HIV-1 after heterosexual transmission. Science. 2004;303(5666):2019–22. Epub 2004/03/27. 15044802
22. Liao HX, Tsao CY, Alam SM, Muldoon M, Vandergrift N, Ma BJ, et al. Antigenicity and immunogenicity of transmitted/founder, consensus, and chronic envelope glycoproteins of human immunodeficiency virus type 1. J Virol. 2013;87(8):4185–201. Epub 2013/02/01. doi: 10.1128/JVI.02297-1223365441
23. Parker ZF, Iyer SS, Wilen CB, Parrish NF, Chikere KC, Lee FH, et al. Transmitted/founder and chronic HIV-1 envelope proteins are distinguished by differential utilization of CCR5. J Virol. 2013;87(5):2401–11. Epub 2012/12/28. doi: 10.1128/JVI.02964-1223269796
24. Ping LH, Joseph SB, Anderson JA, Abrahams MR, Salazar-Gonzalez JF, Kincer LP, et al. Comparison of viral Env proteins from acute and chronic infections with subtype C human immunodeficiency virus type 1 identifies differences in glycosylation and CCR5 utilization and suggests a new strategy for immunogen design. J Virol. 2013;87(13):7218–33. Epub 2013/04/26. doi: 10.1128/JVI.03577-1223616655
25. Wilen CB, Parrish NF, Pfaff JM, Decker JM, Henning EA, Haim H, et al. Phenotypic and immunologic comparison of clade B transmitted/founder and chronic HIV-1 envelope glycoproteins. J Virol. 2011;85(17):8514–27. Epub 2011/07/01. doi: 10.1128/JVI.00736-1121715507
26. Parrish NF, Wilen CB, Banks LB, Iyer SS, Pfaff JM, Salazar-Gonzalez JF, et al. Transmitted/founder and chronic subtype C HIV-1 use CD4 and CCR5 receptors with equal efficiency and are not inhibited by blocking the integrin alpha4beta7. PLoS Pathog. 2012;8(5):e1002686. Epub 2012/06/14. doi: 10.1371/journal.ppat.100268622693444
27. Parrish NF, Gao F, Li H, Giorgi EE, Barbian HJ, Parrish EH, et al. Phenotypic properties of transmitted founder HIV-1. Proc Natl Acad Sci U S A. 2013;110(17):6626–33. Epub 2013/04/02. doi: 10.1073/pnas.130428811023542380
28. Nawaz F, Cicala C, Van Ryk D, Block KE, Jelicic K, McNally JP, et al. The genotype of early-transmitting HIV gp120s promotes alpha (4) beta(7)-reactivity, revealing alpha (4) beta(7) +/CD4+ T cells as key targets in mucosal transmission. PLoS Pathog. 2011;7(2):e1001301. Epub 2011/03/09. doi: 10.1371/journal.ppat.100130121383973
29. Herbeck JT, Nickle DC, Learn GH, Gottlieb GS, Curlin ME, Heath L, et al. Human immunodeficiency virus type 1 env evolves toward ancestral states upon transmission to a new host. J Virol. 2006;80(4):1637–44. Epub 2006/01/28. 16439520
30. Redd AD, Collinson-Streng AN, Chatziandreou N, Mullis CE, Laeyendecker O, Martens C, et al. Previously transmitted HIV-1 strains are preferentially selected during subsequent sexual transmissions. J Infect Dis. 2012;206(9):1433–42. Epub 2012/09/22. doi: 10.1093/infdis/jis50322997233
31. Frost SD, Liu Y, Pond SL, Chappey C, Wrin T, Petropoulos CJ, et al. Characterization of human immunodeficiency virus type 1 (HIV-1) envelope variation and neutralizing antibody responses during transmission of HIV-1 subtype B. J Virol. 2005;79(10):6523–7. Epub 2005/04/29. 15858036
32. Chohan B, Lang D, Sagar M, Korber B, Lavreys L, Richardson B, et al. Selection for human immunodeficiency virus type 1 envelope glycosylation variants with shorter V1–V2 loop sequences occurs during transmission of certain genetic subtypes and may impact viral RNA levels. J Virol. 2005;79(10):6528–31. Epub 2005/04/29. 15858037
33. Liu Y, Curlin ME, Diem K, Zhao H, Ghosh AK, Zhu H, et al. Env length and N-linked glycosylation following transmission of human immunodeficiency virus Type 1 subtype B viruses. Virology. 2008;374(2):229–33. Epub 2008/03/04. doi: 10.1016/j.virol.2008.01.02918314154
34. Gnanakaran S, Bhattacharya T, Daniels M, Keele BF, Hraber PT, Lapedes AS, et al. Recurrent signature patterns in HIV-1 B clade envelope glycoproteins associated with either early or chronic infections. PLoS Pathog. 2011;7(9):e1002209. Epub 2011/10/08. doi: 10.1371/journal.ppat.100220921980282
35. Asmal M, Hellmann I, Liu W, Keele BF, Perelson AS, Bhattacharya T, et al. A signature in HIV-1 envelope leader peptide associated with transition from acute to chronic infection impacts envelope processing and infectivity. PLoS One. 2011;6(8):e23673. Epub 2011/08/31. doi: 10.1371/journal.pone.002367321876761
36. Ochsenbauer C, Edmonds TG, Ding H, Keele BF, Decker J, Salazar MG, et al. Generation of transmitted/founder HIV-1 infectious molecular clones and characterization of their replication capacity in CD4 T lymphocytes and monocyte-derived macrophages. J Virol. 2011;86(5):2715–28. Epub 2011/12/23. doi: 10.1128/JVI.06157-1122190722
37. Margolis L, Shattock R, Selective transmission of CCR5-utilizing HIV-1: the 'gatekeeper' problem resolved?Nat Rev Microbiol. 2006;4(4):312–7. Epub 2006/03/17. 16541138
38. Fenton-May AE, Dibben O, Emmerich T, Ding H, Pfafferott K, Aasa-Chapman MM, et al. Relative resistance of HIV-1 founder viruses to control by interferon-alpha. Retrovirology. 2013;10:146. Epub 2013/12/05. doi: 10.1186/1742-4690-10-14624299076
39. Etemad B, Gonzalez OA, White L, Laeyendecker O, Kirk GD, Mehta S, et al. Characterization of HIV-1 envelopes in acutely and chronically infected injection drug users. Retrovirology. 2014;11(1):106. Epub 2014/11/29.
40. Deymier MJ, Ende Z, Fenton-May AE, Dilernia DA, Kilembe W, Allen SA, et al. Heterosexual Transmission of Subtype C HIV-1 Selects Consensus-Like Variants without Increased Replicative Capacity or Interferon-alpha Resistance. PLoS Pathog. 2015;11(9):e1005154. Epub 2015/09/18. doi: 10.1371/journal.ppat.100515426378795
41. Boeras DI, Hraber PT, Hurlston M, Evans-Strickfaden T, Bhattacharya T, Giorgi EE, et al. Role of donor genital tract HIV-1 diversity in the transmission bottleneck. Proc Natl Acad Sci U S A. 2011;108(46):E1156–63. Epub 2011/11/09. doi: 10.1073/pnas.110376410822065783
42. Pena-Cruz V, Etemad B, Chatziandreou N, Nyein PH, Stock S, Reynolds SJ, et al. HIV-1 envelope replication and alpha4beta7 utilization among newly infected subjects and their corresponding heterosexual partners. Retrovirology. 2013;10:162. Epub 2013/12/29. doi: 10.1186/1742-4690-10-16224369910
43. Sagar M, Laeyendecker O, Lee S, Gamiel J, Wawer MJ, Gray RH, et al. Selection of HIV variants with signature genotypic characteristics during heterosexual transmission. J Infect Dis. 2009;199(4):580–9. Epub 2009/01/16. doi: 10.1086/59655719143562
44. Herbeck JT, Rolland M, Liu Y, McLaughlin S, McNevin J, Zhao H, et al. Demographic processes affect HIV-1 evolution in primary infection before the onset of selective processes. J Virol. 2011;85(15):7523–34. Epub 2011/05/20. doi: 10.1128/JVI.02697-1021593162
45. Isaacman-Beck J, Hermann EA, Yi Y, Ratcliffe SJ, Mulenga J, Allen S, et al. Heterosexual transmission of human immunodeficiency virus type 1 subtype C: Macrophage tropism, alternative coreceptor use, and the molecular anatomy of CCR5 utilization. J Virol. 2009;83(16):8208–20. Epub 2009/06/12. doi: 10.1128/JVI.00296-0919515785
46. Alexander M, Lynch R, Mulenga J, Allen S, Derdeyn CA, Hunter E, Donor and recipient envs from heterosexual human immunodeficiency virus subtype C transmission pairs require high receptor levels for entry. J Virol. 2010;84(8):4100–4. Epub 2010/02/12. doi: 10.1128/JVI.02068-0920147398
47. Masharsky AE, Dukhovlinova EN, Verevochkin SV, Toussova OV, Skochilov RV, Anderson JA, et al. A substantial transmission bottleneck among newly and recently HIV-1-infected injection drug users in St Petersburg, Russia. J Infect Dis. 2010;201(11):1697–702. Epub 2010/04/29. doi: 10.1086/65270220423223
48. Gottlieb GS, Heath L, Nickle DC, Wong KG, Leach SE, Jacobs B, et al. HIV-1 variation before seroconversion in men who have sex with men: analysis of acute/early HIV infection in the multicenter AIDS cohort study. J Infect Dis. 2008;197(7):1011–5. Epub 2008/04/19. doi: 10.1086/52920618419538
49. Bar KJ, Li H, Chamberland A, Tremblay C, Routy JP, Grayson T, et al. Wide variation in the multiplicity of HIV-1 infection among injection drug users. J Virol. 2010;84(12):6241–7. Epub 2010/04/09. doi: 10.1128/JVI.00077-1020375173
50. Dukhovlinova E, Masharsky A, Verevochkin S, Toussova O, Shevchenko A, Montefiori D, et al. AHI Detection Among People Who Inject Drugs in Russia Reveals the HIV-1 Transmission Bottleneck. Conference On Retroviruses And Opportunistic Infections (CROI 2014): International Antiviral Society—USA; 2014. p. 299.
51. Wertheim JO, Murrell B, Smith MD, Kosakovsky Pond SL, Scheffler K, RELAX: detecting relaxed selection in a phylogenetic framework. Mol Biol Evol. 2015;32(3):820–32. Epub 2014/12/30. doi: 10.1093/molbev/msu40025540451
52. Kimura M, Preponderance of synonymous changes as evidence for the neutral theory of molecular evolution. Nature. 1977;267(5608):275–6. Epub 1977/05/19. PubMed 865622
53. Yang Z, Bielawski JP, Statistical methods for detecting molecular adaptation. Trends Ecol Evol. 2000;15(12):496–503. Epub 2000/12/15. 11114436
54. Carlson JM, Brumme ZL, Rousseau CM, Brumme CJ, Matthews P, Kadie C, et al. Phylogenetic dependency networks: inferring patterns of CTL escape and codon covariation in HIV-1 Gag. PLoS Comput Biol. 2008;4(11):e1000225. Epub 2008/11/22. doi: 10.1371/journal.pcbi.100022519023406
55. Bhattacharya T, Daniels M, Heckerman D, Foley B, Frahm N, Kadie C, et al. Founder effects in the assessment of HIV polymorphisms and HLA allele associations. Science. 2007;315(5818):1583–6. Epub 2007/03/17. 17363674
56. Storey JD, Tibshirani R, Statistical significance for genomewide studies. Proc Natl Acad Sci U S A. 2003;100(16):9440–5. Epub 2003/07/29. 12883005
57. Chen B, Vogan EM, Gong H, Skehel JJ, Wiley DC, Harrison SC, Structure of an unliganded simian immunodeficiency virus gp120 core. Nature. 2005;433(7028):834–41. Epub 2005/02/25. 15729334
58. Bunnik EM, van Gils MJ, Lobbrecht MS, Pisas L, Nanlohy NM, van Baarle D, et al. Emergence of monoclonal antibody b12-resistant human immunodeficiency virus type 1 variants during natural infection in the absence of humoral or cellular immune pressure. J Gen Virol. 2010;91(Pt 5):1354–64. Epub 2010/01/08. doi: 10.1099/vir.0.017319-020053822
59. Bontjer I, Melchers M, Eggink D, David K, Moore JP, Berkhout B, et al. Stabilized HIV-1 envelope glycoprotein trimers lacking the V1V2 domain, obtained by virus evolution. J Biol Chem. 2010;285(47):36456–70. Epub 2010/09/10. doi: 10.1074/jbc.M110.15658820826824
60. Dunfee RL, Thomas ER, Gorry PR, Wang J, Taylor J, Kunstman K, et al. The HIV Env variant N283 enhances macrophage tropism and is associated with brain infection and dementia. Proc Natl Acad Sci U S A. 2006;103(41):15160–5. Epub 2006/10/04. 17015824
61. Grupping K, Selhorst P, Michiels J, Vereecken K, Heyndrickx L, Kessler P, et al. MiniCD4 protein resistance mutations affect binding to the HIV-1 gp120 CD4 binding site and decrease entry efficiency. Retrovirology. 2012;9:36. Epub 2012/05/04. doi: 10.1186/1742-4690-9-3622551420
62. Ince WL, Zhang L, Jiang Q, Arrildt K, Su L, Swanstrom R, Evolution of the HIV-1 env gene in the Rag2-/- gammaC-/- humanized mouse model. J Virol. 2010;84(6):2740–52. Epub 2010/01/01. doi: 10.1128/JVI.02180-0920042504
63. Madani N, Perdigoto AL, Srinivasan K, Cox JM, Chruma JJ, LaLonde J, et al. Localized changes in the gp120 envelope glycoprotein confer resistance to human immunodeficiency virus entry inhibitors BMS-806 and #155. J Virol. 2004;78(7):3742–52. Epub 2004/03/16. 15016894
64. Mo H, Stamatatos L, Ip JE, Barbas CF, Parren PW, Burton DR, et al. Human immunodeficiency virus type 1 mutants that escape neutralization by human monoclonal antibody IgG1b12. off. J Virol. 1997;71(9):6869–74. Epub 1997/09/01. 9261412
65. Nakamura GR, Byrn R, Wilkes DM, Fox JA, Hobbs MR, Hastings R, et al. Strain specificity and binding affinity requirements of neutralizing monoclonal antibodies to the C4 domain of gp120 from human immunodeficiency virus type 1. J Virol. 1993;67(10):6179–91. Epub 1993/10/01. 7690420
66. Pugach P, Kuhmann SE, Taylor J, Marozsan AJ, Snyder A, Ketas T, et al. The prolonged culture of human immunodeficiency virus type 1 in primary lymphocytes increases its sensitivity to neutralization by soluble CD4. Virology. 2004;321(1):8–22. Epub 2004/03/23. 15033560
67. Shibata J, Yoshimura K, Honda A, Koito A, Murakami T, Matsushita S, Impact of V2 mutations on escape from a potent neutralizing anti-V3 monoclonal antibody during in vitro selection of a primary human immunodeficiency virus type 1 isolate. J Virol. 2007;81(8):3757–68. Epub 2007/01/26. 17251298
68. Sterjovski J, Churchill MJ, Roche M, Ellett A, Farrugia W, Wesselingh SL, et al. CD4-binding site alterations in CCR5-using HIV-1 envelopes influencing gp120-CD4 interactions and fusogenicity. Virology. 2011;410(2):418–28. Epub 2011/01/11. doi: 10.1016/j.virol.2010.12.01021216423
69. Wrin T, Loh TP, Vennari JC, Schuitemaker H, Nunberg JH, Adaptation to persistent growth in the H9 cell line renders a primary isolate of human immunodeficiency virus type 1 sensitive to neutralization by vaccine sera. J Virol. 1995;69(1):39–48. Epub 1995/01/01. 7983734
70. Skums P, Mancuso N, Artyomenko A, Tork B, Mandoiu I, Khudyakov Y, et al. Reconstruction of viral population structure from next-generation sequencing data using multicommodity flows. BMC Bioinformatics. 2013;14Suppl 9:S2. Epub 2013/08/09. doi: 10.1186/1471-2105-14-S9-S223902469
71. Giallonardo FD, Topfer A, Rey M, Prabhakaran S, Duport Y, Leemann C, et al. Full-length haplotype reconstruction to infer the structure of heterogeneous virus populations. Nucleic Acids Res. 2014;42(14):e115. Epub 2014/06/29. doi: 10.1093/nar/gku53724972832
72. Zagordi O, Geyrhofer L, Roth V, Beerenwinkel N, Deep sequencing of a genetically heterogeneous sample: local haplotype reconstruction and read error correction. J Comput Biol. 2010;17(3):417–28. Epub 2010/04/10. doi: 10.1089/cmb.2009.016420377454
73. Zagordi O, Klein R, Daumer M, Beerenwinkel N, Error correction of next-generation sequencing data and reliable estimation of HIV quasispecies. Nucleic Acids Res. 2010;38(21):7400–9. Epub 2010/07/31. doi: 10.1093/nar/gkq65520671025
74. Prosperi MC, Salemi M, QuRe: software for viral quasispecies reconstruction from next-generation sequencing data. Bioinformatics. 2011;28(1):132–3. Epub 2011/11/18. doi: 10.1093/bioinformatics/btr62722088846
75. Pacold M, Smith D, Little S, Cheng PM, Jordan P, Ignacio C, et al. Comparison of methods to detect HIV dual infection. AIDS Res Hum Retroviruses. 2010;26(12):1291–8. Epub 2010/10/20. doi: 10.1089/aid.2010.004220954840
76. Schirmer M, Sloan WT, Quince C, Benchmarking of viral haplotype reconstruction programmes: an overview of the capacities and limitations of currently available programmes. Brief Bioinform. 2012;15(3):431–42. Epub 2012/12/22. doi: 10.1093/bib/bbs08123257116
77. Henn MR, Boutwell CL, Charlebois P, Lennon NJ, Power KA, Macalalad AR, et al. Whole genome deep sequencing of HIV-1 reveals the impact of early minor variants upon immune recognition during acute infection. PLoS Pathog. 2012;8(3):e1002529. Epub 2012/03/14. doi: 10.1371/journal.ppat.100252922412369
78. Rolland M, Tovanabutra S, deCamp AC, Frahm N, Gilbert PB, Sanders-Buell E, et al. Genetic impact of vaccination on breakthrough HIV-1 sequences from the STEP trial. Nat Med. 2011;17(3):366–71. Epub 2011/03/02. doi: 10.1038/nm.231621358627
79. Wagner GA, Pacold ME, Kosakovsky Pond SL, Caballero G, Chaillon A, Rudolph AE, et al. Incidence and prevalence of intrasubtype HIV-1 dual infection in at-risk men in the United States. J Infect Dis. 2013;209(7):1032–8. Epub 2013/11/26. doi: 10.1093/infdis/jit63324273040
80. Rieder P, Joos B, Scherrer AU, Kuster H, Braun D, Grube C, et al. Characterization of human immunodeficiency virus type 1 (HIV-1) diversity and tropism in 145 patients with primary HIV-1 infection. Clin Infect Dis. 2011;53(12):1271–9. Epub 2011/10/15. doi: 10.1093/cid/cir72521998286
81. Giorgi EE, Funkhouser B, Athreya G, Perelson AS, Korber BT, Bhattacharya T, Estimating time since infection in early homogeneous HIV-1 samples using a poisson model. BMC Bioinformatics. 2010;11:532. Epub 2010/10/27. doi: 10.1186/1471-2105-11-53220973976
82. Joseph SB, Swanstrom R, Kashuba AD, Cohen MS, Bottlenecks in HIV-1 transmission: insights from the study of founder viruses. Nat Rev Microbiol. 2015;13(7):414–25. Epub 2015/06/09. doi: 10.1038/nrmicro347126052661
83. Ma ZM, Keele BF, Qureshi H, Stone M, Desilva V, Fritts L, et al. SIVmac251 is inefficiently transmitted to rhesus macaques by penile inoculation with a single SIVenv variant found in ramp-up phase plasma. AIDS Res Hum Retroviruses. 2011;27(12):1259–69. Epub 2011/07/08. doi: 10.1089/aid.2011.009021732792
84. Fieni F, Stone M, Ma ZM, Dutra J, Fritts L, Miller CJ, Viral RNA levels and env variants in semen and tissues of mature male rhesus macaques infected with SIV by penile inoculation. PLoS One. 2013;8(10):e76367. Epub 2013/10/23. doi: 10.1371/journal.pone.007636724146859
85. Keele BF, Li H, Learn GH, Hraber P, Giorgi EE, Grayson T, et al. Low-dose rectal inoculation of rhesus macaques by SIVsmE660 or SIVmac251 recapitulates human mucosal infection by HIV-1. J Exp Med. 2009;206(5):1117–34. Epub 2009/05/06. doi: 10.1084/jem.2008283119414559
86. Dinh MH, Anderson MR, McRaven MD, Cianci GC, McCoombe SG, Kelley ZL, et al. Visualization of HIV-1 interactions with penile and foreskin epithelia: clues for female-to-male HIV transmission. PLoS Pathog. 2015;11(3):e1004729. Epub 2015/03/10. doi: 10.1371/journal.ppat.100472925748093
87. Poles MA, Elliott J, Taing P, Anton PA, Chen IS, A preponderance of CCR5(+) CXCR4(+) mononuclear cells enhances gastrointestinal mucosal susceptibility to human immunodeficiency virus type 1 infection. J Virol. 2001;75(18):8390–9. Epub 2001/08/17. 11507184
88. McElrath MJ, Smythe K, Randolph-Habecker J, Melton KR, Goodpaster TA, Hughes SM, et al. Comprehensive assessment of HIV target cells in the distal human gut suggests increasing HIV susceptibility toward the anus. J Acquir Immune Defic Syndr. 2013;63(3):263–71. Epub 2013/02/09. doi: 10.1097/QAI.0b013e318289839223392465
89. Ribeiro Dos Santos P, Rancez M, Pretet JL, Michel-Salzat A, Messent V, Bogdanova A, et al. Rapid dissemination of SIV follows multisite entry after rectal inoculation. PLoS One. 2011;6(5):e19493. Epub 2011/05/17. doi: 10.1371/journal.pone.001949321573012
90. Miyake A, Ibuki K, Enose Y, Suzuki H, Horiuchi R, Motohara M, et al. Rapid dissemination of a pathogenic simian/human immunodeficiency virus to systemic organs and active replication in lymphoid tissues following intrarectal infection. J Gen Virol. 2006;87(Pt 5):1311–20. Epub 2006/04/11. 16603534
91. Jacobs A, Sen J, Rong L, Caffrey M, Alanine scanning mutants of the HIV gp41 loop. J Biol Chem. 2005;280(29):27284–8. Epub 2005/05/27. 15917239
92. Postler TS, Desrosiers RC, The tale of the long tail: the cytoplasmic domain of HIV-1 gp41. J Virol. 2013;87(1):2–15. Epub 2012/10/19. doi: 10.1128/JVI.02053-1223077317
93. Eisenberg D, Wesson M, The most highly amphiphilic alpha-helices include two amino acid segments in human immunodeficiency virus glycoprotein 41. Biopolymers. 1990;29(1):171–7. Epub 1990/01/01. 2328285
94. Venable RM, Pastor RW, Brooks BR, Carson FW, Theoretically determined three-dimensional structures for amphipathic segments of the HIV-1 gp41 envelope protein. AIDS Res Hum Retroviruses. 1989;5(1):7–22. Epub 1989/02/01. 2541749
95. Kliger Y, Shai Y, A leucine zipper-like sequence from the cytoplasmic tail of the HIV-1 envelope glycoprotein binds and perturbs lipid bilayers. Biochemistry. 1997;36(17):5157–69. Epub 1997/04/29. 9136877
96. Kalia V, Sarkar S, Gupta P, Montelaro RC, Rational site-directed mutations of the LLP-1 and LLP-2 lentivirus lytic peptide domains in the intracytoplasmic tail of human immunodeficiency virus type 1 gp41 indicate common functions in cell-cell fusion but distinct roles in virion envelope incorporation. J Virol. 2003;77(6):3634–46. Epub 2003/03/01. 12610139
97. Piller SC, Dubay JW, Derdeyn CA, Hunter E, Mutational analysis of conserved domains within the cytoplasmic tail of gp41 from human immunodeficiency virus type 1: effects on glycoprotein incorporation and infectivity. J Virol. 2000;74(24):11717–23. Epub 2000/11/23. 11090171
98. Sterjovski J, Churchill MJ, Ellett A, Gray LR, Roche MJ, Dunfee RL, et al. Asn 362 in gp120 contributes to enhanced fusogenicity by CCR5-restricted HIV-1 envelope glycoprotein variants from patients with AIDS. Retrovirology. 2007;4:89. Epub 2007/12/14. 18076768
99. Watkins BA, Reitz MS, Jr.Wilson CA, Aldrich K, Davis AE, Robert-Guroff M, Immune escape by human immunodeficiency virus type 1 from neutralizing antibodies: evidence for multiple pathways. J Virol. 1993;67(12):7493–500. Epub 1993/12/01. 7693973
100. Gardner MR, Kattenhorn LM, Kondur HR, von Schaewen M, Dorfman T, Chiang JJ, et al. AAV-expressed eCD4-Ig provides durable protection from multiple SHIV challenges. Nature. 2015;519(7541):87–91. Epub 2015/02/25. doi: 10.1038/nature1426425707797
101. Grant RM, Lama JR, Anderson PL, McMahan V, Liu AY, Vargas L, et al. Preexposure chemoprophylaxis for HIV prevention in men who have sex with men. N Engl J Med. 2010;363(27):2587–99. doi: 10.1056/NEJMoa101120521091279
102. Garrett NJ, Werner L, Naicker N, Naranbhai V, Sibeko S, Samsunder N, et al. HIV disease progression in seroconvertors from the CAPRISA 004 tenofovir gel pre-exposure prophylaxis trial. J Acquir Immune Defic Syndr. 2015;68(1):55–61. Epub 2014/09/24. doi: 10.1097/QAI.000000000000036725247433
103. Pacold ME, Pond SL, Wagner GA, Delport W, Bourque DL, Richman DD, et al. Clinical, virologic, and immunologic correlates of HIV-1 intraclade B dual infection among men who have sex with men. AIDS. 2011;26(2):157–65. Epub 2011/11/03.
104. Sagar M, Lavreys L, Baeten JM, Richardson BA, Mandaliya K, Chohan BH, et al. Infection with multiple human immunodeficiency virus type 1 variants is associated with faster disease progression. J Virol. 2003;77(23):12921–6. Epub 2003/11/12. 14610215
105. Tsai L, Tasovski I, Leda AR, Chin MP, Cheng-Mayer C, The number and genetic relatedness of transmitted/founder virus impact clinical outcome in vaginal R5 SHIVSF162P3N infection. Retrovirology. 2014;11:22. Epub 2014/03/13. doi: 10.1186/1742-4690-11-2224612462
106. Gottlieb GS, Nickle DC, Jensen MA, Wong KG, Grobler J, Li F, et al. Dual HIV-1 infection associated with rapid disease progression. Lancet. 2004;363(9409):619–22. Epub 2004/02/28. 14987889
107. Cornelissen M, Pasternak AO, Grijsen ML, Zorgdrager F, Bakker M, Blom P, et al. HIV-1 dual infection is associated with faster CD4+ T-cell decline in a cohort of men with primary HIV infection. Clin Infect Dis. 2012;54(4):539–47. Epub 2011/12/14. doi: 10.1093/cid/cir84922157174
108. Burton DR, Hessell AJ, Keele BF, Klasse PJ, Ketas TA, Moldt B, et al. Limited or no protection by weakly or nonneutralizing antibodies against vaginal SHIV challenge of macaques compared with a strongly neutralizing antibody. Proc Natl Acad Sci U S A. 2011;108(27):11181–6. Epub 2011/06/22. doi: 10.1073/pnas.110301210821690411
109. Santra S, Tomaras GD, Warrier R, Nicely NI, Liao HX, Pollara J, et al. Human Non-neutralizing HIV-1 Envelope Monoclonal Antibodies Limit the Number of Founder Viruses during SHIV Mucosal Infection in Rhesus Macaques. PLoS Pathog. 2015;11(8):e1005042. Epub 2015/08/04. doi: 10.1371/journal.ppat.100504226237403
110. Macalalad AR, Zody MC, Charlebois P, Lennon NJ, Newman RM, Malboeuf CM, et al. Highly sensitive and specific detection of rare variants in mixed viral populations from massively parallel sequence data. PLoS Comput Biol. 2012;8(3):e1002417. Epub 2012/03/23. doi: 10.1371/journal.pcbi.100241722438797
111. Huang W, Li L, Myers JR, Marth GT, ART: a next-generation sequencing read simulator. Bioinformatics. 2012;28(4):593–4. Epub 2011/12/27. doi: 10.1093/bioinformatics/btr70822199392
112. Palmer S, Kearney M, Maldarelli F, Halvas EK, Bixby CJ, Bazmi H, et al. Multiple, linked human immunodeficiency virus type 1 drug resistance mutations in treatment-experienced patients are missed by standard genotype analysis. J Clin Microbiol. 2005;43(1):406–13. Epub 2005/01/07. 15635002
113. Fiebig EW, Wright DJ, Rawal BD, Garrett PE, Schumacher RT, Peddada L, et al. Dynamics of HIV viremia and antibody seroconversion in plasma donors: implications for diagnosis and staging of primary HIV infection. AIDS. 2003;17(13):1871–9. Epub 2003/09/10. 12960819
114. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O, New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59(3):307–21. Epub 2010/06/09. doi: 10.1093/sysbio/syq01020525638
115. Carlson JM, Listgarten J, Pfeifer N, Tan V, Kadie C, Walker BD, et al. Widespread impact of HLA restriction on immune control and escape pathways of HIV-1. J Virol. 2012;86(9):5230–43. Epub 2012/03/02. doi: 10.1128/JVI.06728-1122379086