The origins of sexually transmitted HIV among men who have sex with men

Science Translational Medicine

Volumn 2, Issue 18, 2010, Pages

  Butler, David M ^a   Delport, Wayne ^a   Pond, Sergei L Kosakovsky ^a   Lakdawala, Malcolm K ^a   Cheng, Pok Man ^a   Little, Susan J ^a   Richman, Douglas D ^a,b   Smith, Davey M ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR5;

ADULT; ARTICLE; BLOOD ANALYSIS; CD4 LYMPHOCYTE COUNT; CELL COMPARTMENTALIZATION; CELL FREE SYSTEM; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; GENETIC CORRELATION; GLYCOSYLATION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MALE; MALE HOMOSEXUAL; PHYLOGENETIC TREE; PRIORITY JOURNAL; SEMEN ANALYSIS; SEXUAL TRANSMISSION; VIRUS GENOME; VIRUS LOAD; VIRUS TRANSMISSION;

ACUTE DISEASE; ADULT; CELL COMPARTMENTATION; CHRONIC DISEASE; HIV INFECTIONS; HIV-1; HOMOSEXUALITY, MALE; HUMANS; MALE; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, VIRAL; SEMEN; YOUNG ADULT;

EID: 77953003196     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3000447     Document Type: Article

References (51)

1. UNAIDS, "AIDS epidemic update: December 2007" (2007).
2. T. C. Quinn, M. J. Wawer, N. Sewankambo, D. Serwadda, C. Li, F. Wabwire-Mangen, M. O. Meehan, T. Lutalo, R. H. Gray, Viral load and heterosexual transmission of human immunodeficiency virus type 1. Rakai Project Study Group. N. Engl. J. Med. 342, 921-929 (2000).
3. D. M. Butler, D. M. Smith, E. R. Cachay, G. K. Hightower, C. T. Nugent, D. D. Richman, S. J. Little, Herpes simplex virus 2 serostatus and viral loads of HIV-1 in blood and semen as risk factors for HIV transmission among men who have sex with men. AIDS 22, 1667-1671 (2008).
4. M. J. Wawer, R. H. Gray, N. K. Sewankambo, D. Serwadda, X. Li, O. Laeyendecker, N. Kiwanuka, G. Kigozi, M. Kiddugavu, T. Lutalo, F. Nalugoda, F. Wabwire-Mangen, M. P. Meehan, T. C. Quinn, Rates of HIV-1 transmission per coital act, by stage of HIV-1 infection, in Rakai, Uganda. J. Infect. Dis. 191, 1403-1409 (2005).
5. M. S. Cohen, Sexually transmitted diseases enhance HIV transmission: No longer a hypothesis. Lancet 351 (Suppl. 3), 5-7 (1998).
6. E. Vittinghoff, J. Douglas, F. Judson, D. McKirnan, K. MacQueen, S. P. Buchbinder, Per-contact risk of human immunodeficiency virus transmission between male sexual partners. Am. J. Epidemiol. 150, 306-311 (1999).
7. M. C. Boily, R. F. Baggaley, L. Wang, B. Masse, R. G. White, R. J. Hayes, M. Alary, Heterosexual risk of HIV-1 infection per sexual act: Systematic review and meta-analysis of observational studies. Lancet Infect. Dis. 9, 118-129 (2009).
8. K. Gupta, P. J. Klasse, How do viral and host factors modulate the sexual transmission of HIV? Can transmission be blocked? PLoS Med. 3, e79 (2006).
9. S. K. Pillai, B. Good, S. L. Kosakovsky Pond, J. K. Wong, M. C. Strain, D. D. Richman, D. M. Smith, Semen-specific genetic characteristics of human immunodeficiency virus type 1 env. J. Virol. 79, 1734-1742 (2005).
10. M. Sagar, O. Laeyendecker, S. Lee, J. Gamiel, M. J. Wawer, R. H. Gray, D. Serwadda, N. K. Sewankambo, J. C. Shepherd, J. Toma, W. Huang, T. C. Quinn, Selection of HIV variants with signature genotypic characteristics during heterosexual transmission. J. Infect. Dis. 199, 580-589 (2009).
11. D. H. Owen, D. F. Katz, A review of the physical and chemical properties of human semen and the formulation of a semen simulant. J. Androl. 26, 459-469 (2005).
12. J. A. Levy, The transmission of AIDS: The case of the infected cell. JAMA 259, 3037-3038 (1988).
13. T. Zhu, N. Wang, A. Carr, D. S. Nam, R. Moor-Jankowski, D. A. Cooper, D. D. Ho, Genetic characterization of human immunodeficiency virus type 1 in blood and genital secretions: Evidence for viral compartmentalization and selection during sexual transmission. J. Virol. 70, 3098-3107 (1996).
14. M. Stürmer, H. W. Doerr, A. Berger, P. Gute, Is transmission of HIV-1 in non-viraemic serodiscordant couples possible? Antivir. Ther. 13, 729-732 (2008).
15. K. Ritola, C. D. Pilcher, S. A. Fiscus, N. G. Hoffman, J. A. Nelson, K. M. Kitrinos, C. B. Hicks, J. J. Eron Jr., R. Swanstrom, Multiple V1/V2 env variants are frequently present during primary infection with human immunodeficiency virus type 1. J. Virol. 78, 11208-11218 (2004).
16. T. Zhu, N. Wang, A. Carr, S. Wolinsky, D. D. Ho, Evidence for coinfection by multiple strains of human immunodeficiency virus type 1 subtype B in an acute seroconvertor. J. Virol. 69, 1324-1327 (1995).
17. M. Kearney, F. Maldarelli, W. Shao, J. B. Margolick, E. S. Daar, J. W. Mellors, V. Rao, J. M. Coffin, S. Palmer, Human immunodeficiency virus type 1 population genetics and adaptation in newly infected individuals. J. Virol. 83, 2715-2727 (2009).
18. B. F. Keele, E. E. Giorgi, J. F. Salazar-Gonzalez, J. M. Decker, K. T. Pham, M. G. Salazar, C. Sun, T. Grayson, S. Wang, H. Li, X. Wei, C. Jiang, J. L. Kirchherr, F. Gao, J. A. Anderson, L. H. Ping, R. Swanstrom, G. D. Tomaras, W. A. Blattner, P. A. Goepfert, J. M. Kilby, M. S. Saag, E. L. Delwart, M. P. Busch, M. S. Cohen, D. C. Montefiori, B. F. Haynes, B. Gaschen, G. S. Athreya, H. Y. Lee, N. Wood, C. Seoighe, A. S. Perelson, T. Bhattacharya, B. T. Korber, B. H. Hahn, G. M. Shaw, 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 (2008).
19. A. Singh, G. Besson, A. Mobasher, R. G. Collman, Patterns of chemokine receptor fusion cofactor utilization by human immunodeficiency virus type 1 variants from the lungs and blood. J. Virol. 73, 6680-6690 (1999).
20. J. K. Wong, C. C. Ignacio, F. Torriani, D. Havlir, N. J. Fitch, D. D. Richman, In vivo compartmentalization of human immunodeficiency virus: Evidence from the examination of pol sequences from autopsy tissues. J. Virol. 71, 2059-2071 (1997).
21. A. A. Kiessling, L. M. Fitzgerald, D. Zhang, H. Chhay, D. Brettler, R. C. Eyre, J. Steinberg, K. McGowan, R. A. Byrn, Human immunodeficiency virus in semen arises from a genetically distinct virus reservoir. AIDS Res. Hum. Retroviruses 14 (Suppl. 1), S33-S41 (1998).
22. D. C. Nickle, M. A. Jensen, D. Shriner, S. J. Brodie, L. M. Frenkel, J. E. Mittler, J. I. Mullins, Evolutionary indicators of human immunodeficiency virus type 1 reservoirs and compartments. J. Virol. 77, 5540-5546 (2003).
23. J. F. Salazar-Gonzalez, E. Bailes, K. T. Pham, M. G. Salazar, M. B. Guffey, B. F. Keele, C. A. Derdeyn, P. Farmer, E. Hunter, S. Allen, O. Manigart, J. Mulenga, J. A. Anderson, R. Swanstrom, B. F. Haynes, G. S. Athreya, B. T. Korber, P. M. Sharp, G. M. Shaw, B. H. Hahn, Deciphering human immunodeficiency virus type 1 transmission and early envelope diversification by single-genome amplification and sequencing. J. Virol. 82, 3952-3970 (2008).
24. C. A. Derdeyn, J. M. Decker, F. Bibollet-Ruche, J. L. Mokili, M. Muldoon, S. A. Denham, M. L. Heil, F. Kasolo, R. Musonda, B. H. Hahn, G. M. Shaw, B. T. Korber, S. Allen, E. Hunter, Envelope-constrained neutralization-sensitive HIV-1 after heterosexual transmission. Science 303, 2019-2022 (2004). (Pubitemid 38393277)
25. S. D. Frost, Y. Liu, S. L. Kosakovsky Pond, C. Chappey, T. Wrin, C. J. Petropoulos, S. J. Little, D. D. Richman, Characterization of human immunodeficiency virus type 1 (HIV-1) envelope variation and neutralizing antibody responses during transmission of HIV-1 subtype B. J. Virol. 79, 6523-6527 (2005). (Pubitemid 40617256)
26. B. Joos, M. Fischer, H. Kuster, S. K. Pillai, J. K. Wong, J. Böni, B. Hirschel, R. Weber, A. Trkola, H. F. Gunthard; Swiss HIV Cohort Study, HIV rebounds from latently infected cells, rather than from continuing low-level replication. Proc. Natl. Acad. Sci. U.S.A. 105, 16725-16730 (2008).
27. S. L. Kosakovsky Pond, S. D. Frost, A genetic algorithm approach to detecting lineage-specific variation in selection pressure. Mol. Biol. Evol. 22, 478-485 (2005).
28. T. Bhattacharya, M. Daniels, D. Heckerman, B. Foley, N. Frahm, C. Kadie, J. Carlson, K. Yusim, B. McMahon, B. Gaschen, S. Mallal, J. I. Mullins, D. C. Nickle, J. Herbeck, C. Rousseau, G. H. Learn, T. Miura, C. Brander, B. Walker, B. Korber, Founder effects in the assessment of HIV polymorphisms and HLA allele associations. Science 315, 1583-1586 (2007).
29. E. W. Fiebig, D. J.Wright, B. D. Rawal, P. E. Garrett, R. T. Schumacher, L. Peddada, C. Heldebrant, R. Smith, A. Conrad, S. H. Kleinman, M. P. Busch, Dynamics of HIV viremia and antibody seroconversion in plasma donors: Implications for diagnosis and staging of primary HIV infection. AIDS 17, 1871-1879 (2003).
30. D. M. Smith, J. D. Kingery, J. K. Wong, C. C. Ignacio, D. D. Richman, S. J. Little, The prostate as a reservoir for HIV-1. AIDS 18, 1600-1602 (2004).
31. K. K. Koelsch, D. M. Smith, S. J. Little, C. C. Ignacio, T. R. Macaranas, A. J. Brown, C. J. Petropoulos, D. D. Richman, J. K. Wong, Clade B HIV-1 superinfection with wild-type virus after primary infection with drug-resistant clade B virus. AIDS 17, F11-F16 (2003).
32. L. H. Ping, J. A. Nelson, I. F. Hoffman, J. Schock, S. L. Lamers, M. Goodman, P. Vernazza, P. Kazembe, M. Maida, D. Zimba, M. M. Goodenow, J. J. Eron Jr., S. A. Fiscus, M. S. Cohen, R. Swanstrom, Characterization of V3 sequence heterogeneity in subtype C human immunodeficiency virus type 1 isolates from Malawi: Underrepresentation of X4 variants. J. Virol. 73, 6271-6281 (1999).
33. D.M. Smith, J. K.Wong, H. Shao, G. K. Hightower, S. H. Mai, J. M. Moreno, C. C. Ignacio, S. D. Frost, D. D. Richman, S. J. Little, Long-term persistence of transmitted HIV drug resistance in male genital tract secretions: Implications for secondary transmission. J. Infect. Dis. 196, 356-360 (2007).
34. Los Alamos National Laboratory; www.lanl.gov.
35. R. C. Edgar, MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004).
36. M. A. Jensen, F. S. Li, A. B. van 't Wout, D. C. Nickle, D. Shriner, H. X. He, S. McLaughlin, R. Shankarappa, J. B. Margolick, J. I. Mullins, 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. 77, 13376-13388 (2003).
37. S. L. Kosakovsky Pond, S. D. Frost, S. V. Muse, HyPhy: Hypothesis testing using phylogenies. Bioinformatics 21, 676-679 (2005).
38. S. L. Kosakovsky Pond, D. Posada, E. Stawiski, C. Chappey, A. F. Poon, G. Hughes, E. Fearnhill, M. B. Gravenor, A. J. Leigh Brown, S. D. Frost, An evolutionary model-based algorithm for accurate phylogenetic breakpoint mapping and subtype prediction in HIV-1. PLoS Comput. Biol. 5, e1000581 (2009).
39. D. Sankoff, Minimal mutation trees of sequences. SIAM J. Appl. Math. 28, 35-42 (1975).
40. Z. Yang, S. Kumar, M. Nei, A new method of inference of ancestral nucleotide and amino acid sequences. Genetics 141, 1641-1650 (1995).
41. R.W. Shafer, S. Y. Rhee, D. Pillay, V.Miller, P. Sandstrom, J. M. Schapiro, D. R. Kuritzkes, D. Bennett, HIV-1 protease and reverse transcriptase mutations for drug resistance surveillance. AIDS 21, 215-223 (2007). (Pubitemid 46036930)
42. S. Guindon, O. Gascuel, A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696-704 (2003).
43. S. Tavaré, Some probabilistic and statistical problems in the analysis of DNA sequences. Lect. Math. Life Sci. 17, 57-86 (1986).
44. Z. Yang, Among-site rate variation and its impact on phylogenetic analyses. Trends Ecol. Evol. 11, 367-372 (1996).
45. R. R. Hudson, M. Slatkin, W. P. Maddison, Estimation of levels of gene flow from DNA sequence data. Genetics 132, 583-589 (1992).
46. A. J. Drummond, S. Y. Ho, M. J. Phillips, A. Rambaut, Relaxed phylogenetics and dating with confidence. PLoS Biol. 4, e88 (2006).
47. A. J. Drummond, A. Rambaut, BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214 (2007).
48. M. Anisimova, C. Kosiol, Investigating protein-coding sequence evolution with probabilistic codon substitution models. Mol. Biol. Evol. 26, 255-271 (2009).
49. W. Delport, K. Scheffler, C. Seoighe, Models of coding sequence evolution. Brief. Bioinform. 10, 97-109 (2009).
50. S. L. Kosakovsky Pond, D. Posada, M. B. Gravenor, C. H. Woelk, S. D. Frost, GARD: A genetic algorithm for recombination detection. Bioinformatics 22, 3096-3098 (2006).
51. S. L. Kosakovsky Pond, S. D. Frost, Datamonkey: Rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21, 2531-2533 (2005).