Molecular evolution analysis of the human immunodeficiency virus type 1 envelope in simian/human immunodeficiency virus-infected macaques: Implications for challenge dose selection

Journal of Virology

Volumn 85, Issue 19, 2011, Pages 10332-10345

  Varela, Mariana ^a   Landskron, Lisa ^a,d   Lai, Rachel P J ^a   McKinley, Trevelyan J ^a   Bogers, Willy M ^b   Verschoor, Ernst J ^b   Dubbes, Rob ^b   Barnett, Susan W ^c   Frost, Simon D W ^a   Heeney, Jonathan L ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b BIOMEDICAL PRIMATE RESEARCH CENTRE   (Netherlands)

^c Novartis Vaccines and Diagnostics ^*  (United Kingdom)

^d ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; INOCULATION; MACACA; MICROBIAL KINETICS; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; SIMIAN IMMUNODEFICIENCY VIRUS; VIRAL KINETICS; VIRUS ENVELOPE; VIRUS LOAD; VIRUS TRANSMISSION;

ANIMALS; CLUSTER ANALYSIS; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; EVOLUTION, MOLECULAR; GENOTYPE; HIV-1; MACACA; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIRULENCE;

ANIMALIA; HUMAN IMMUNODEFICIENCY VIRUS 1; MACACA; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 80053948552     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.05290-11     Document Type: Article

References (60)

1. Abrahams, M. R., et al. 2009. Quantitating the multiplicity of infection with human immunodeficiency virus type 1 subtype C reveals a non-Poisson distribution of transmitted variants. J. Virol. 83:3556-3567.
2. 2 microglobulin level and CD4 lymphocyte count to predict development of AIDS in persons with human immunodeficiency virus infection. Arch. Intern. Med. 150:73-77.
3. Baba, T. W., et al. 2000. Human neutralizing monoclonal antibodies of the IgG1 subtype protect against mucosal simian-human immunodeficiency virus infection. Nat. Med. 6:200-206.
4. Bogers, W. M., et al. 2008. Systemic neutralizing antibodies induced by long interval mucosally primed systemically boosted immunization correlate with protection from mucosal SHIV challenge. Virology 382:217-225.
5. DeGruttola, V., G. R. Seage III, K. H. Mayer, and C. R. Horsburgh, Jr. 1989. Infectiousness of HIV between male homosexual partners. J. Clin. Epidemiol. 42:849-856.
6. Derdeyn, C. A., et al. 2004. Envelope-constrained neutralization-sensitive HIV-1 after heterosexual transmission. Science 303:2019-2022.
7. Edwards, C. T., et al. 2006. Population genetic estimation of the loss of genetic diversity during horizontal transmission of HIV-1. BMC Evol. Biol. 6:28.
8. Ellenberger, D., et al. 2006. HIV-1 DNA/MVA vaccination reduces the per exposure probability of infection during repeated mucosal SHIV challenges. Virology 352:216-225.
9. Emini, E. A., et al. 1992. Prevention of HIV-1 infection in chimpanzees by gp120 V3 domain-specific monoclonal antibody. Nature 355:728-730.
10. European Council. 24 November 1986. Council Directive on the approximation of laws, regulations and administrative provisions of the Member States regarding the protection of animals used for experimental and other scientific purposes (86/609/EEC). http://ec.europa.eu/food/fs/aw/aw_legislation/scientific/86-609-eec_en.pdf.
11. European Council. 18 March 1986. European Convention for the Protection of Vertebrate Animals used for Experimental and Other Scientific Purposes (ETS no. 123), including the revised Appendix A. http://conventions.coe.int/treaty/en/treaties/html/123.htm.
12. Felber, B. K., et al. 2009. Monospecific expansion of SIVmac251 during acute infection masks multiple transmitted virus variants revealed during the chronic phase. Retrovirology 6(Suppl. 3):O38.
13. Galvin, S. R., and M. S. Cohen. 2004. The role of sexually transmitted diseases in HIV transmission. Nat. Rev. Microbiol. 2:33-42.
14. Giorgi, E. E., et al. 2010. Estimating time since infection in early homogeneous HIV-1 samples using a Poisson model. BMC Bioinform. 11:532.
15. Gottlieb, G. S., et al. 2008. 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. 197:1011-1015.
16. Gray, R. H., et al. 2001. Probability of HIV-1 transmission per coital act in monogamous, heterosexual, HIV-1-discordant couples in Rakai, Uganda. Lancet 357:1149-1153.
17. Haaland, R. E., et al. 2009. Inflammatory genital infections mitigate a severe genetic bottleneck in heterosexual transmission of subtype A and C HIV-1. PLoS Pathog. 5:e1000274.
18. Harouse, J. M., A. Gettie, R. C. Tan, J. Blanchard, and C. Cheng-Mayer. 1999. Distinct pathogenic sequela in rhesus macaques infected with CCR5 or CXCR4 utilizing SHIVs. Science 284:816-819.
19. Heeney, J. L., et al. 1998. β-Chemokines and neutralizing antibody titers correlate with sterilizing immunity generated in HIV-1 vaccinated macaques. Proc. Natl. Acad. Sci. U. S. A. 95:10803-10808.
20. Jewell, N. P. 1990. Some statistical issues in studies of the epidemiology of AIDS. Stat. Med. 9:1387-1416.
21. Jewell, N. P., and S. C. Shiboski. 1990. Statistical analysis of HIV infectivity based on partner studies. Biometrics 46:1133-1150.
22. Jombart, T., R. M. Eggo, P. J. Dodd, and F. Balloux. 2011. Reconstructing disease outbreaks from genetic data: a graph approach. Heredity 106:383-390.
23. Kearney, M., et al. 2009. Human immunodeficiency virus type 1 population genetics and adaptation in newly infected individuals. J. Virol. 83:2715-2727.
24. Keele, B. F., et al. 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.
25. Keele, B. F., et al. 2009. Low-dose rectal inoculation of rhesus macaques by SIVsmE660 or SIVmac251 recapitulates human mucosal infection by HIV-1. J. Exp. Med. 206:1117-1134.
26. Kim, C. N., et al. 2006. Repetitive exposures with simian/human immunodeficiency viruses: strategy to study HIV pre-clinical interventions in nonhuman primates. J. Med. Primatol. 35:210-216.
27. Kosakovsky Pond, S. L., D. Posada, M. B. Gravenor, C. H. Woelk, and S. D. Frost. 2006. Automated phylogenetic detection of recombination using a genetic algorithm. Mol. Biol. Evol. 23:1891-1901.
28. Kraft, Z., et al. 2007. Macaques infected with a CCR5-tropic simian/human immunodeficiency virus (SHIV) develop broadly reactive anti-HIV neutralizing antibodies. J. Virol. 81:6402-6411.
29. Li, M., et al. 2005. Human immunodeficiency virus type 1 env clones from acute and early subtype B infections for standardized assessments of vaccineelicited neutralizing antibodies. J. Virol. 79:10108-10125.
30. Liu, J., et al. 2010. Low-dose mucosal simian immunodeficiency virus infection restricts early replication kinetics and transmitted virus variants in rhesus monkeys. J. Virol. 84:10406-10412.
31. McKinley, T. J., P. R. Murcia, J. R. Gog, M. Varela, and J. L. Wood. 2011. A Bayesian approach to analyse genetic variation within RNA viral populations. PLoS Comput. Biol. 7:e1002027.
32. Mooij, P., et al. 1998. A clinically relevant HIV-1 subunit vaccine protects rhesus macaques from in vivo passaged simian-human immunodeficiency virus infection. AIDS (London, England) 12:F15-F22.
33. Nazli, A., et al. 2010. Exposure to HIV-1 directly impairs mucosal epithelial barrier integrity allowing microbial translocation. PLoS Pathog. 6:e1000852.
34. Neuhaus, J. M., and N. P. Jewell. 1990. The effect of retrospective sampling on binary regression models for clustered data. Biometrics 46:977-990.
35. Padian, N. S., S. C. Shiboski, and N. P. Jewell. 1990. The effect of number of exposures on the risk of heterosexual HIV transmission. J. Infect. Dis. 161:883-887.
36. Parren, P. W., et al. 2001. Antibody protects macaques against vaginal challenge with a pathogenic R5 simian/human immunodeficiency virus at serum levels giving complete neutralization in vitro. J. Virol. 75:8340-8347.
37. Pilcher, C. D., J. J. Eron, Jr., S. Galvin, C. Gay, and M. S. Cohen. 2004. Acute HIV revisited: new opportunities for treatment and prevention. J. Clin. Invest. 113:937-945.
38. Pilcher, C. D., et al. 2004. Frequent detection of acute primary HIV infection in men in Malawi. AIDS (London, England) 18:517-524.
39. Pilcher, C. D., et al. 2004. Brief but efficient: acute HIV infection and the sexual transmission of HIV. J. Infect. Dis. 189:1785-1792.
40. Pond, S. L., and S. D. Frost. 2005. Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics (Oxford, England) 21:2531-2533.
41. Posada, D., and K. A. Crandall. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics (Oxford, England) 14:817-818.
42. Quinn, T. C., et al. 2000. Viral load and heterosexual transmission of human immunodeficiency virus type 1. Rakai Project Study Group. N. Engl. J. Med. 342:921-929.
43. R Development Core Team. 2011. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org.
44. Regoes, R. R., I. M. Longini, M. B. Feinberg, and S. I. Staprans. 2005. Preclinical assessment of HIV vaccines and microbicides by repeated lowdose virus challenges. PLoS Med. 2:e249.
45. Rerks-Ngarm, S., et al. 2009. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med. 361:2209-2220.
46. Rybarczyk, B. J., et al. 2004. Correlation between env V1/V2 region diversification and neutralizing antibodies during primary infection by simian immunodeficiency virus sm in rhesus macaques. J. Virol. 78:3561-3571.
47. Salazar-Gonzalez, J. F., et al. 2008. Deciphering human immunodeficiency virus type 1 transmission and early envelope diversification by single-genome amplification and sequencing. J. Virol. 82:3952-3970.
48. Salazar-Gonzalez, J. F., et al. 2009. Genetic identity, biological phenotype, and evolutionary pathways of transmitted/founder viruses in acute and early HIV-1 infection. J. Exp. Med. 206:1273-1289.
49. Shankarappa, R., et al. 1999. Consistent viral evolutionary changes associated with the progression of human immunodeficiency virus type 1 infection. J. Virol. 73:10489-10502.
50. Shedlock, D. J., G. Silvestri, and D. B. Weiner. 2009. Monkeying around with HIV vaccines: using rhesus macaques to define 'gatekeepers' for clinical trials. Nat. Rev. 9:717-728.
51. Shibata, R., et al. 1999. Neutralizing antibody directed against the HIV-1 envelope glycoprotein can completely block HIV-1/SIV chimeric virus infections of macaque monkeys. Nat. Med. 5:204-210.
52. Stone, M., et al. 2010. A limited number of simian immunodeficiency virus (SIV) env variants are transmitted to rhesus macaques vaginally inoculated with SIVmac251. J. Virol. 84:7083-7095.
53. Subbarao, S., et al. 2006. Chemoprophylaxis with tenofovir disoproxil fumarate provided partial protection against infection with simian human immunodeficiency virus in macaques given multiple virus challenges. J. Infect. Dis. 194:904-911.
54. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599.
55. ten Haaft, P., et al. 2004. Readily acquired secondary infections of human and simian immunodeficiency viruses following single intravenous exposure in non-human primates. J. Gen. Virol. 85:3735-3745.
56. Tsai, L., et al. 2007. Efficient repeated low-dose intravaginal infection with X4 and R5 SHIVs in rhesus macaque: implications for HIV-1 transmission in humans. Virology 362:207-216.
57. Watkins, D. I., D. R. Burton, E. G. Kallas, J. P. Moore, and W. C. Koff. 2008. Nonhuman primate models and the failure of the Merck HIV-1 vaccine in humans. Nat. Med. 14:617-621.
58. Wolinsky, S. M., et al. 1992. Selective transmission of human immunodeficiency virus type-1 variants from mothers to infants. Science 255:1134-1137.
59. Yeh, W. W., et al. 2010. Autologous neutralizing antibodies to the transmitted/ founder viruses emerge late after simian immunodeficiency virus SIVmac251 infection of rhesus monkeys. J. Virol. 84:6018-6032.
60. Zhang, M., et al. 2004. Tracking global patterns of N-linked glycosylation site variation in highly variable viral glycoproteins: HIV, SIV, and HCV envelopes and influenza hemagglutinin. Glycobiology 14:1229-1246.