Hiv-1 envelope subregion length variation during disease progression

PLoS Pathogens

Volumn 6, Issue 12, 2010, Pages

  Curlin, Marcel E ^a   Zioni, Rafael ^a,c   Hawes, Stephen E ^b   Liu, Yi ^a   Deng, Wenjie ^a   Gottlieb, Geoffrey S ^a   Zhu, Tuofu ^a   Mullins, James I ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN GP 120;

ARTICLE; CD4 LYMPHOCYTE COUNT; DISEASE COURSE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; MAJOR CLINICAL STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN GLYCOSYLATION; VIRUS ENVELOPE; VIRUS LOAD; CHEMISTRY; CROSS-SECTIONAL STUDY; DISEASE TRANSMISSION; HOST PATHOGEN INTERACTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE EVASION; IMMUNOLOGY; PANDEMIC; PATHOGENICITY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

CROSS-SECTIONAL STUDIES; DISEASE PROGRESSION; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; PANDEMICS;

EID: 78651237643     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001228     Document Type: Article

References (80)

1. Starcich BR, Hahn BH, Shaw GM, McNeely PD, Modrow S, et al. (1986) Identification and characterization of conserved and variable regions in the envelope gene of HTLV-III/LAV, the retrovirus of AIDS. Cell 45: 637-648.
2. Willey RL, Rutledge RA, Dias S, Folks T, Theodore T, et al. (1986) Identification of conserved and divergent domains within the envelope gene of the acquired immunodeficiency syndrome retrovirus. Proc Natl Acad Sci USA 83: 5038-5042.
3. Modrow S, Hahn BE, Shaw GM, Gallo RC, Wong-Staal F, et al. (1987) Computer-assisted analysis of envelope protein sequences of seven human immunodeficiency virus isolates: Prediction of antigenic epitopes in conserved and variable regions. J Virol 61: 570-578.
4. Wood N, Bhattacharya T, Keele BF, Giorgi E, Liu M, et al. (2009) HIV evolution in early infection: selection pressures, patterns of insertion and deletion, and the impact of APOBEC. PLoS Pathog 5: e1000414.
5. Cocchi F, DeVico AL, Garzino-Demo A, Cara A, Gallo RC, et al. (1996) The V3 domain of the HIV-1 gp120 envelope glycoprotein is critical for chemokine-mediated blockade of infection [see comments]. Nat Med 2: 1244-1247.
6. Feng Y, Broder CC, Kennedy PE, Berger EA (1996) HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272: 872-877.
7. Speck RF, Wehrly K, Platt EJ, Atchison RE, Charo IF, et al. (1997) Selective employment of chemokine receptors as human immunodeficiency virus type 1 coreceptors determined by individual amino acids within the envelope V3 loop. J Virol 71: 7136-7139.
8. Goudsmit J, Debouck C, Meloen RH, Smit L, Bakker M, et al. (1988) Human immunodeficiency virus type 1 neutralization epitope with conserved architec-ture elicits early type-specific antibodies in experimentally infected chimpanzees. ProcNatlAcadSciUSA 85: 4478-4482.
9. Javaherian K, Langlois AJ, McDanal C, Ross KL, Eckler LI, et al. (1989) Principal neutralizing domain of the human immunodeficiency virus type 1 envelope protein. ProcNatlAcadSciUSA 86: 6768-6772.
10. Luo L, Li Y, Chang JS, Cho SY, Kim TY, et al. (1998) Induction of V3-specific cytotoxic T lymphocyte responses by HIV gag particles carrying multiple immunodominant V3 epitopes of gp120. Virology 240: 316-325.
11. Watanabe N, McAdam SN, Boyson JE, Piekarczyk MS, Yasutomi Y, et al. (1994) A simian immunodeficiency virus envelope V3 cytotoxic T-lymphocyte epitope in rhesus monkeys and its restricting major histocompatibility complex class I molecule Mamu-A*02. J Virol 68: 6690-6696.
12. Hartley O, Klasse PJ, Sattentau QJ, Moore JP (2005) V3: HIV's switch-hitter. AIDS Res Hum Retroviruses 21: 171-189.
13. Hill MD, Lorenzo E, Kumar A (2004) Changes in the human immunodeficiency virus V3 region that correspond with disease progression: a meta-analysis. Virus Res 106: 27-33.
14. Ida S, Gatanaga H, Shioda T, Nagai Y, Kobayashi N, et al. (1997) HIV type 1 V3 variation dynamics in vivo: Long-term persistence of non-syncytium-inducing genotypes and transient presence of syncytium-inducing genotypes during the course of progressive AIDS. AIDS Res and Human Retrovir 13: 1597-1609.
15. Palmer C, Balfe P, Fox D, May JC, Frederiksson R, et al. (1996) Functional characterization of the V1V2 region of human immunodeficiency virus type 1. Virology 220: 436-449.
16. Masciotra S, Owen SM, Rudolph D, Yang C, Wang B, et al. (2002) Temporal relationship between V1V2 variation, macrophage replication, and coreceptor adaptation during HIV-1 disease progression. Aids 16: 1887-1898.
17. Kitrinos KM, Hoffman NG, Nelson JA, Swanstrom R (2003) Turnover of env variable region 1and2genotypes in subjects with late-stage human immunodeficiency virus type 1 infection. J Virol 77: 6811-6822.
18. Shioda T, Oka S, Xin X, Liu H, Harukuni R, et al. (1997) In vivo sequence variability of human immunodeficiency virus type 1 envelope gp120: association of V2 extension with slow disease progression. J Virol 71: 4871-4881.
19. Chohan B, Lang D, Sagar M, Korber B, Lavreys L, et al. (2005) 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 79: 6528-6531.
20. Sagar M, Wu X, Lee S, Overbaugh J (2006) Human immunodeficiency virus type 1 V1-V2 envelope loop sequences expand and add glycosylation sites over the course of infection, and these modifications affect antibody neutralization sensitivity. J Virol 80: 9586-9598.
21. Chackerian B, Rudensey LM, Overbaugh J (1997) Specific N-linked and O-linked glycosylation modifications in the envelope V1 domain of simian immunodeficiency virus variants that evolve in the host alter recognition by neutralizing antibodies. J Virol 71: 7719-7727.
22. Kwong PD, Wyatt R, Robinson J, Sweet RW, Sodroski J, et al. (1998) Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393: 648-659.
23. Chen B, Vogan EM, Gong H, Skehel JJ, Wiley DC, et al. (2005) Determining the structure of an unliganded and fully glycosylated SIV gp120 envelope glycoprotein. Structure 13: 197-211.
24. Cartier L, Hartley O, Dubois-Dauphin M, Krause KH (2005) Chemokine receptors in the central nervous system: role in brain inflammation and neurodegenerative diseases. Brain Res Brain Res Rev 48: 16-42.
25. Andeweg A, Leeflang P, Osterhaus A, Bosch M (1993) Both the V2 and V3 regions of the human immunodeficiency virus type 1 surface glycoprotein functionally interact with other envelope regions in syncytium formation. J Virol 67: 3232-3239.
26. Groenink M, Fouchier RAM, Broersen S, Baker CH, Koot M, et al. (1993) Relation of phenotype evolution of HIV-1 to envelope V2 configuration. Science 260: 1513-1516.
27. Koito A, Harrowe G, Levy JA, Cheng-Mayer C (1994) Functional role of the V1/V2 region of human immunodeficiency virus type 1 envelope glycoprotein gp120 in infection of primary macrophages and soluble CD4 neutralization. J Virol 68: 2253-2259.
28. O'Brien WA, Koyanagi Y, Namazie A, Zhao JQ, Diagne A, et al. (1990) HIV-1 tropism for mononuclear phagocytes can be determined by regions of gp120 outside the CD4-binding domain. Nature 348: 69-73.
29. Sullivan N, Thali M, Furman C, Ho DD, Sodroski J (1993) Effect of amino acid changes in the V1/V2 region of the human immunodeficiency virus type 1 gp120 glycoprotein on subunit association, syncytium formation, and recogni- tion by a neutralizing antibody. J Virol 67: 3674-3679.
30. Westervelt P, Trowbridge DB, Epstein LG, Blumberg BM, Li Y, et al. (1992) Macrophage tropism determinants of human immunodeficiency virus type 1 in vivo. J Virol 66: 2577-2582.
31. Toohey K, Wehrly K, Nishio J, Perryman S, Chesebro B (1995) Human immunodeficiency virus envelope V1 and V2 regions influence replication efficiency in macrophages by affecting virus spread. Virology 213: 70-79.
32. Wang N, Zhu T, Ho DD (1995) Sequence diversity of V1 and V2 domains of gp120 from human immunodeficiency virus type 1: lack of correlation with viral phenotype. J Virol 69: 2708-2715.
33. Pastore C, Nedellec R, Ramos A, Pontow S, Ratner L, et al. (2006) Human immunodeficiency virus type 1 coreceptor switching: V1/V2 gain-of-fitness mutations compensate for V3 loss-of-fitness mutations. J Virol 80: 750-758.
34. Benichou S, Legrand R, Nakagawa N, Faure T, Traincard F, et al. (1992) Identification of a neutralizing domain in the external envelope glycoprotein of simian immunodeficiency virus. AIDS Res Hum Retroviruses 8: 1165-1170.
35. Kent KA, Rud E, Corcoran T, Powell C, Thiriart C, et al. (1992) Identification of two neutralizing and 8 non-neutralizing epitopes on simian immunodeficiency virus envelope using monoclonal antibodies. AIDS Res Hum Retroviruses 8: 1147-1151.
36. Matsumi S, Matsushita S, Yoshimura K, Javaherian K, Takatsuki K (1995) Neutralizing monoclonal antibody against a external envelope glycoprotein (gp110) of SIVmac251. AIDS Res Hum Retroviruses 11: 501-508.
37. Jurkiewicz E, Hunsmann G, Schaffner J, Nisslein T, Luke W, et al. (1997) Identification of the V1 region as a linear neutralizing epitope of the simian immunodeficiency virus SIVmac envelope glycoprotein. J Virol 71: 9475-9481.
38. Pinter A, Honnen WJ, He Y, Gorny MK, Zolla-Pazner S, et al. (2004) The V1/ V2 domain of gp120 is a global regulator of the sensitivity of primary human immunodeficiency virus type 1 isolates to neutralization by antibodies commonly induced upon infection. J Virol 78: 5205-5215.
39. Lamers S, Sleasman JW, She JX, Barrie KA, Pomeroy SM, et al. (1993) Independent variation and positive selection in env V1-V2 domains within maternal-infant strains of human immunodeficiency virus type-1 in vivo. Jvirol 67: 3951-3960.
40. Rybarczyk BJ, Montefiori D, Johnson PR, West A, Johnston RE, 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.
41. Frost SD, Wrin T, Smith DM, Pond SL, Liu Y, et al. (2005) Neutralizing antibody responses drive the evolution of human immunodeficiency virus type 1 envelope during recent HIV infection. Proc Natl Acad Sci U S A 102: 18514-18519.
42. Li B, Decker JM, Johnson RW, Bibollet-Ruche F, Wei X, et al. (2006) Evidence for potent autologous neutralizing antibody titers and compact envelopes in early infection with subtype C human immunodeficiency virus type 1. J Virol 80: 5211-5218.
43. Johnson WE, Morgan J, Reitter J, Puffer BA, Czajak S, et al. (2002) A replication-competent, neutralization-sensitive variant of simian immunodeficiency virus lacking 100 amino acids of envelope. J Virol 76: 2075-2086.
44. Cao J, Sullivan N, Desjardin E, Parolin C, Robinson J, et al. (1997) Replication and neutralization of human immunodeficiency virus type 1 lacking the V1 and V2 variable loops of the gp120 envelope glycoprotein. J Virol 71: 9808-9812.
45. Derdeyn CA, Decker JM, Bibollet-Ruche F, Mokili JL, Muldoon M, et al. (2004) Envelope-constrained neutralization-sensitive HIV-1 after heterosexual transmission. Science 303: 2019-2022.
46. Liu Y, Curlin ME, Diem K, Zhao H, Ghosh AK, et al. (2008) Env length and N-linked glycosylation following transmission of human immunodeficiency virus Type 1 subtype B viruses. Virology 374: 229-233.
47. Frost SD, Liu Y, Pond SL, Chappey C, Wrin T, et al. (2005) 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.
48. Hughes ES, Bell JE, Simmonds P (1997) Investigation of population diversity of human immunodeficiency virus type 1 in vivo by nucleotide sequencing and length polymorphism analysis of the V1/V2 hypervariable region of env. J Gen Virol 78((Pt 11)): 2871-2882.
49. Schacker T, Collier AC, Hughes J, Shea T, Corey L (1996) Clinical and epidemiologic features of primary HIV infection. Ann Intern Med 125: 257-264.
50. Kaslow RA, Ostrow DG, Detels R, Phair JP, Polk BF, et al. (1987) The Multicenter AIDS Cohort Study: rationale, organization, and selected characteristics of the participants. Am J Epidemiol 126: 310-318.
51. Poss M, Rodrigo AG, Gosink JJ, Learn GH, de Vange Panteleeff D, et al. (1998) Evolution of envelope sequences from the genital tract and peripheral blood of women infected with clade A human immunodeficiency virus type 1. J Virol 72: 8240-8251.
52. Dacheux L, Moreau A, Ataman-Onal Y, Biron F, Verrier B, et al. (2004) Evolutionary dynamics of the glycan shield of the human immunodeficiency virus envelope during natural infection and implications for exposure of the 2G12 epitope. J Virol 78: 12625-12637.
53. Liu Y, McNevin J, Cao J, Zhao H, Genowati I, et al. (2006) Selection on the human immunodeficiency virus type 1 proteome following primary infection. J Virol 80: 9519-9529.
54. Trkola A, Kuhmann SE, Strizki JM, Maxwell E, Ketas T, et al. (2002) HIV-1 escape from a small molecule, CCR5-specific entry inhibitor does not involve CXCR4 use. Proc Natl Acad Sci U S A 99: 395-400.
55. McDonald RA, Mayers DL, Chung RC, Wagner KF, Ratto-Kim S, et al. (1997) Evolution of human immunodeficiency virus type 1 env sequence variation in patients with diverse rates of disease progression and T-cell function. J Virol 71: 1871-1879.
56. Shankarappa R, Margolick JB, Gange SJ, Rodrigo AG, Upchurch D, et al. (1999) Consistent viral evolutionary changes associated with the progression of human immunodeficiency virus type 1 infection. J Virol 73: 10489-10502.
57. Tobin NH, Learn GH, Holte SE, Wang Y, Melvin AJ, et al. (2005) Evidence that low-level viremias during effective highly active antiretroviral therapy result from two processes: expression of archival virus and replication of virus. J Virol 79: 9625-9634.
58. Rodrigo AG, Goracke PC, Rowhanian K, Mullins JI (1997) Quantitation of target molecules from polymerase chain reaction-based limiting dilution assays. AIDS Res and Hum Retrovir 13: 737-742.
59. Altfeld M, Rosenberg ES, Shankarappa R, Mukherjee JS, Hecht FM, et al. (2001) Cellular immune responses and viral diversity in individuals treated during acute and early HIV-1 infection. J Exp Med 193: 169-180.
60. Delwart EL, Herring B, Rodrigo AG, Mullins JI (1995) Genetic Subtyping of Human Immunodeficiency Virus Using a Heteroduplex Mobility Assay. PCR Methods and Applications 4: S202-216.
61. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
62. Jensen MA, Li FS, van't Wout AB, Nickle DC, Shriner D, et al. (2003) 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.
63. Lengauer T, Sander O, Sierra S, Thielen A, Kaiser R (2007) Bioinformatics prediction of HIV coreceptor usage. Nat Biotechnol 25: 1407-1410.
64. Pillai S, Good B, Richman D, Corbeil J (2003) A new perspective on V3 phenotype prediction. AIDS Res Hum Retroviruses 19: 145-149.
65. Boisvert S, Marchand M, Laviolette F, Corbeil J (2008) HIV-1 coreceptor usage prediction without multiple alignments: an application of string kernels. Retrovirology 5: 110.
66. Busch MP, Satten GA (1997) Time course of viremia and antibody seroconversion following human immunodeficiency virus exposure. Am J Med 102: 117-124; discussion 125-116.
67. Constantine NT, van der Groen G, Belsey EM, Tamashiro H (1994) Sensitivity of HIV-antibody assays determined by seroconversion panels. Aids 8: 1715-1720.
68. Hanley JA, Negassa A, Edwardes MD, Forrester JE (2003) Statistical analysis of correlated data using generalized estimating equations: an orientation. Am J Epidemiol 157: 364-375.
69. Burton P, Gurrin L, Sly P (1998) Extending the simple linear regression model to account for correlated responses: an introduction to generalized estimating equations and multi-level mixed modelling. Stat Med 17: 1261-1291.
70. Zeger SL, Liang KY (1986) Longitudinal data analysis for discrete and continuous outcomes. Biometrics 42: 121-130.
71. Edmonson P, Murphey-Corb M, Martin LN, Delahunty C, Heeney J, et al. (1998) Evolution of a Simian Immunodeficiency Virus pathogen. J Virol 72: 405-414.
72. Bunnik EM, Pisas L, van Nuenen AC, Schuitemaker H (2008) Autologous neutralizing humoral immunity and evolution of the viral envelope in the course of subtype B human immunodeficiency virus type 1 infection. J Virol 82: 7932-7941.
73. Liu SL, Rodrigo AG, Shankarappa R, Learn GH, Hsu L, et al. (1996) HIV quasispecies and resampling. Science 273: 415-416.
74. Delwart EL, Pan H, Sheppard HW, Wolpert D, Neumann AU, et al. (1997) Slower evolution of human immunodeficiency virus type 1 quasispecies duringprogression to AIDS. J Virol 71: 7498-7508.
75. Pilcher CD, Tien HC, Eron JJ, Jr., Vernazza PL, Leu SY, et al. (2004) Brief but Efficient: Acute HIV Infection and the Sexual Transmission of HIV. J Infect Dis 189: 1785-1792.
76. Wawer MJ, Gray RH, Sewankambo NK, Serwadda D, Li X, et al. (2005) Rates of HIV-1 transmission per coital act, by stage of HIV-1 infection, in Rakai, Uganda. J Infect Dis 191: 1403-1409.
77. Kawashima Y, Pfafferott K, Frater J, Matthews P, Payne R, et al. (2009) Adaptation of HIV-1 to human leukocyte antigen class I. Nature 458: 641-645.
78. Moore CB, John M, James IR, Christiansen FT, Witt CS, et al. (2002) Evidence of HIV-1 adaptation to HLA-restricted immune responses at a population level. Science 296: 1439-1443.
79. Yusim K, Kesmir C, Gaschen B, Addo MM, Altfeld M, et al. (2002) 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 76: 8757-8768.
80. Poss M, Martin HL, Kreiss JK, Granville L, Chohan B, et al. (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.