The role of the humoral immune response in the molecular evolution of the envelope C2, V3 and C3 regions in chronically HIV-2 infected patients

Retrovirology

Volumn 5, Issue , 2008, Pages

  Borrego, Pedro ^a   Marcelino, José Maria ^b   Rocha, Cheila ^a   Doroana, Manuela ^c   Antunes, Francisco ^c   Maltez, Fernando ^d   Gomes, Perpétua ^e,f   Novo, Carlos ^b   Barroso, Helena ^a,f   Taveira, Nuno ^a,f  

^a RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

^b INETI   (Portugal)

^c HOSPITAL DE SANTA MARIA   (Portugal)

^d HOSPITAL CURRY CABRAL   (Portugal)

^e HOSPITAL EGAS MONIZ   (Portugal)

^f INSTITUTO SUPERIOR DE CIÊNCIAS DA SAÚDE EGAS MONIZ   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ANTIRETROVIRUS AGENT; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; NUCLEOSIDE ANALOG; NUCLEOTIDE; PROTEINASE INHIBITOR; GLYCOPROTEIN GP 120; GP120 PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 2; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G;

ARTICLE; CD4+ T LYMPHOCYTE; CLINICAL ARTICLE; CODON; COHORT ANALYSIS; DNA EXTRACTION; GENETIC VARIABILITY; GLYCOSYLATION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 2; HUMAN IMMUNODEFICIENCY VIRUS 2 INFECTION; HUMORAL IMMUNITY; MOLECULAR CLONING; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; UNINDEXED SEQUENCE; VIREMIA; VIRUS ENVELOPE; CD4 LYMPHOCYTE COUNT; DNA SEQUENCE; GENETIC POLYMORPHISM; GENETIC SELECTION; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; ISOLATION AND PURIFICATION; LONGITUDINAL STUDY; MOLECULAR GENETICS; PROTEIN PROCESSING; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2;

CD4 LYMPHOCYTE COUNT; COHORT STUDIES; EVOLUTION, MOLECULAR; GLYCOSYLATION; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HIV-2; HUMANS; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; LONGITUDINAL STUDIES; MOLECULAR SEQUENCE DATA; POLYMORPHISM, GENETIC; PROTEIN PROCESSING, POST-TRANSLATIONAL; SELECTION (GENETICS); SEQUENCE ANALYSIS, DNA;

EID: 53549101005     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-5-78     Document Type: Article

References (82)

1. Hu DJ Dondero TJ Rayfield MA George JR Schochetman G Jaffe HW Luo CC Kalish ML Weniger BG Pau CP et al. The emerging genetic diversity of HIV. The importance of global surveillance for diagnostics, research, and prevention JAMA 1996, 275:210-216. 10.1001/jama.275.3.210 8604174
2. Andersson S Norrgren H da Silva Z Biague A Bamba S Kwok S Christopherson C Biberfeld G Albert J Plasma viral load in HIV-1 and HIV-2 singly and dually infected individuals in Guinea-Bissau, West Africa: Significantly lower plasma virus set point in HIV-2 infection than in HIV-1 infection Arch Intern Med 2000, 160:3286-3293. 10.1001/archinte.160.21.3286 11088091
3. Kanki PJ Travers KU S MB Hsieh CC Marlink RG Gueye NA Siby T Thior I Hernandez-Avila M Sankale JL et al. Slower heterosexual spread of HIV-2 than HIV-1 Lancet 1994, 343:943-946. 10.1016/S0140-6736(94)90065-5 7909009
4. Marlink R Kanki P Thior I Travers K Eisen G Siby T Traore I Hsieh CC Dia MC Gueye EH et al. Reduced rate of disease development after HIV-2 infection as compared to HIV-1 Science 1994, 265:1587-1590. 10.1126/ science.7915856 7915856
5. Whittle H Morris J Todd J Corrah T Sabally S Bangali J Ngom PT Rolfe M Wilkins A HIV-2-infected patients survive longer than HIV-1-infected patients AIDS 1994, 8:1617-1620. 10.1097/00002030-199411000-00015 7848600
6. Reeves JD Doms RW Human immunodeficiency virus type 2 J Gen Virol 2002, 83:1253-1265. 12029140
7. Berry N Ariyoshi K Jaffar S Sabally S Corrah T Tedder R Whittle H Low peripheral blood viral HIV-2 RNA in individuals with high CD4 percentage differentiates HIV-2 from HIV-1 infection J Hum Virol 1998, 1:457-468. 10195267
8. Soares R Foxall R Albuquerque A Cortesao C Garcia M Victorino RM Sousa AE Increased frequency of circulating CCR5+ CD4+ T cells in human immunodeficiency virus type 2 infection J Virol 2006, 80:12425-12429. 1676275 17035326 10.1128/JVI.01557-06
9. Anderson DE Llenado RA Torres JV Humoral immunity and the evolution of HIV-2 Viral Immunol 2004, 17:436-439. 10.1089/vim.2004.17.436 15357909
10. Berry N Jaffar S Schim van der Loeff M Ariyoshi K Harding E N'Gom PT Dias F Wilkins A Ricard D Aaby P et al. Low level viremia and high CD4% predict normal survival in a cohort of HIV type-2-infected villagers AIDS Res Hum Retroviruses 2002, 18:1167-1173. 10.1089/08892220260387904 12487822
11. Lizeng Q Nilsson C Sourial S Andersson S Larsen O Aaby P Ehnlund M Bjorling E Potent neutralizing serum immunoglobulin A (IgA) in human immunodeficiency virus type 2-exposed IgG-seronegative individuals J Virol 2004, 78:7016-7022. 421651 15194778 10.1128/ JVI.78.13.7016-7022.2004
12. MacNeil A Sarr AD Sankale JL Meloni ST Mboup S Kanki P Direct evidence of lower viral replication rates in vivo in human immunodeficiency virus type 2 (HIV-2) infection than in HIV-1 infection J Virol 2007, 81:5325-5330. 1900238 17329334 10.1128/JVI.02625-06
13. Blaak H Ende van der ME Boers PH Schuitemaker H Osterhaus AD In vitro replication capacity of HIV-2 variants from long-term aviremic individuals Virology 2006, 353:144-154. 10.1016/j.virol.2006.05.029 16814357
14. Levy JA HIV and the pathogenesis of AIDS Washington, D.C.: ASM Press 2 1998.
15. Lemey P Rambaut A Pybus OG HIV evolutionary dynamics within and among hosts AIDS Rev 2006, 8:125-140. 17078483
16. Delwart EL Pan H Sheppard HW Wolpert D Neumann AU Korber B Mullins JI Slower evolution of human immunodeficiency virus type 1 quasispecies during progression to AIDS J Virol 1997, 71:7498-7508. 192096 9311829
17. Shankarappa R Margolick JB Gange SJ Rodrigo AG Upchurch D Farzadegan H Gupta P Rinaldo CR Learn GH He X et al. Consistent viral evolutionary changes associated with the progression of human immunodeficiency virus type 1 infection J Virol 1999, 73:10489-10502. 113104 10559367
18. Williamson S Perry SM Bustamante CD Orive ME Stearns MN Kelly JK A statistical characterization of consistent patterns of human immunodeficiency virus evolution within infected patients Mol Biol Evol 2005, 22:456-468. 10.1093/molbev/msi029 15509726
19. Castiglione F Poccia F D'Offizi G Bernaschi M Mutation, fitness, viral diversity, and predictive markers of disease progression in a computational model of HIV type 1 infection AIDS Res Hum Retroviruses 2004, 20:1314-1323. 10.1089/aid.2004.20.1314 15650424
20. Markham RB Wang WC Weisstein AE Wang Z Munoz A Templeton A Margolick J Vlahov D Quinn T Farzadegan H Yu XF Patterns of HIV-1 evolution in individuals with differing rates of CD4 T cell decline Proc Natl Acad Sci USA 1998, 95:12568-12573. 22871 9770526 10.1073/pnas.95.21.12568
21. Bello G Casado C Sandonis V Alvaro-Cifuentes T Dos Santos CA Garcia S Rodriguez C Del Romero J Pilotto JH Grinsztejn B et al. Plasma viral load threshold for sustaining intrahost HIV type 1 evolution AIDS Res Hum Retroviruses 2007, 23:1242-1250. 10.1089/aid.2007.0074 17961111
22. Barroso H Taveira N Evidence for negative selective pressure in HIV-2 evolution in vivo Infect Genet Evol 2005, 5:239-246. 10.1016/ j.meegid.2004.07.008 15737915
23. Sankale JL de la Tour RS Renjifo B Siby T Mboup S Marlink RG Essex ME Kanki PJ Intrapatient variability of the human immunodeficiency virus type 2 envelope V3 loop AIDS Res Hum Retroviruses 1995, 11:617-623. 7576918
24. MacNeil A Sankale JL Meloni ST Sarr AD Mboup S Kanki P Long-term intrapatient viral evolution during HIV-2 infection J Infect Dis 2007, 195:726-733. 10.1086/511308 17262716
25. Choisy M Woelk CH Guegan JF Robertson DL Comparative study of adaptive molecular evolution in different human immunodeficiency virus groups and subtypes J Virol 2004, 78:1962-1970. 369455 14747561 10.1128/ JVI.78.4.1962-1970.2004
26. Mikhail M Wang B Lemey P Beckthold B Vandamme AM Gill MJ Saksena NK Role of viral evolutionary rate in HIV-1 disease progression in a linked cohort Retrovirology 2005, 2:41. 1190217 15985187 10.1186/1742-4690-2-41
27. Yamaguchi Y Gojobori T Evolutionary mechanisms and population dynamics of the third variable envelope region of HIV within single hosts Proc Natl Acad Sci USA 1997, 94:1264-1269. 19779 9037041 10.1073/ pnas.94.4.1264
28. Zhang H Hoffmann F He J He X Kankasa C Ruprecht R West JT Orti G Wood C Evolution of subtype C HIV-1 Env in a slowly progressing Zambian infant Retrovirology 2005, 2:67. 1308862 16274482 10.1186/1742-4690-2-67
29. De Jong JJ De Ronde A Keulen W Tersmette M Goudsmit J Minimal requirements for the human immunodeficiency virus type 1 V3 domain to support the syncytium-inducing phenotype: Analysis by single amino acid substitution J Virol 1992, 66:6777-6780. 240176 1404617
30. Delobel P Nugeyre MT Cazabat M Pasquier C Marchou B Massip P Barre-Sinoussi F Israel N Izopet J Population-based sequencing of the V3 region of env for predicting the coreceptor usage of human immunodeficiency virus type 1 quasispecies J Clin Microbiol 2007, 45:1572-1580. 1865905 17329448 10.1128/JCM.02090-06
31. Huang CC Tang M Zhang MY Majeed S Montabana E Stanfield RL Dimitrov DS Korber B Sodroski J Wilson IA et al. Structure of a V3-containing HIV-1 gp120 core Science 2005, 310:1025-1028. 2408531 16284180 10.1126/ science.1118398
32. Isaka Y Sato A Miki S Kawauchi S Sakaida H Hori T Uchiyama T Adachi A Hayami M Fujiwara T Yoshie O Small amino acid changes in the V3 loop of human immunodeficiency virus type 2 determines the coreceptor usage for CXCR4 and CCR5 Virology 1999, 264:237-243. 10.1006/viro.1999.0006 10544150
33. Zolla-Pazner S Improving on nature: Focusing the immune response on the V3 loop Hum Antibodies 2005, 14:69-72. 16720976
34. Bjorling E Scarlatti G von Gegerfelt A Albert J Biberfeld G Chiodi F Norrby E Fenyo EM Autologous neutralizing antibodies prevail in HIV-2 but not in HIV-1 infection Virology 1993, 193:528-530. 10.1006/ viro.1993.1160 8438591
35. Andersson S HIV-2 and the immune response AIDS Reviews 2001, 3:11-23.
36. Shi Y Brandin E Vincic E Jansson M Blaxhult A Gyllensten K Moberg L Brostrom C Fenyo EM Albert J Evolution of human immunodeficiency virus type 2 coreceptor usage, autologous neutralization, envelope sequence and glycosylation J Gen Virol 2005, 86:3385-3396. 10.1099/vir.0.81259-0 16298986
37. Rodriguez SK Sarr AD MacNeil A Thakore-Meloni S Gueye-Ndiaye A Traore I Dia MC Mboup S Kanki PJ Comparison of heterologous neutralizing antibody responses of human immunodeficiency virus type 1 (HIV-1)- and HIV-2-infected Senegalese patients: Distinct patterns of breadth and magnitude distinguish HIV-1 and HIV-2 infections J Virol 2007, 81:5331-5338. 1900200 17301136 10.1128/JVI.02789-06
38. Soriano V Gomes P Heneine W Holguin A Doruana M Antunes R Mansinho K Switzer WM Araujo C Shanmugam V et al. Human immunodeficiency virus type 2 (HIV-2) in Portugal: Clinical spectrum, circulating subtypes, virus isolation, and plasma viral load J Med Virol 2000, 61:111-116. 10.1002/ (SICI)1096-9071(200005)61:1<111::AID-JMV18>3.0.CO;2-W 10745242
39. Cavaco-Silva P Taveira NC Rosado L Lourenco MH Moniz-Pereira J Douglas NW Daniels RS Santos-Ferreira MO Virological and molecular demonstration of human immunodeficiency virus type 2 vertical transmission J Virol 1998, 72:3418-3422. 109839 9525673
40. Sambrook J Maniatis T Fritsch EF Molecular cloning: A laboratory manual Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory 2 1989.
41. Thompson JD Gibson TJ Plewniak F Jeanmougin F Higgins DG The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools Nucleic Acids Res 1997, 25:4876-4882. 147148 9396791 10.1093/nar/25.24.4876
42. Nicholas KB Nicholas Hugh B Jr GeneDoc: A tool for editing and annotating multiple sequence alignments. Distributed by the author 1997.
43. Tamura K Dudley J Nei M Kumar S MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0 Mol Biol Evol 2007, 24:1596-1599. 10.1093/molbev/msm092 17488738
44. Felsenstein J Evolutionary trees from DNA sequences: A maximum likelihood approach J Mol Evol 1981, 17:368-376. 10.1007/BF01734359 7288891
45. Posada D Crandall KA MODELTEST: Testing the model of DNA substitution Bioinformatics 1998, 14:817-818. 10.1093/bioinformatics/14.9.817 9918953
46. Swofford DL PAUP. Phylogenetic Analysis using Parsimony (and other Methods). Version 4. Sinauer-Associates, Sunderland, Massachusetts 1998. 12064242
47. Felsenstein J Confidence limits on phylogenies: An approach using the bootstrap Evolution 1985, 39:783-791. 10.2307/2408678
48. Salazar-Gonzalez JF Bailes E Pham KT Salazar MG Guffey MB Keele BF Derdeyn CA Farmer P Hunter E Allen S et al. Deciphering human immunodeficiency virus type 1 transmission and early envelope diversification by single-genome amplification and sequencing J Virol 2008, 82:3952-3970. 2293010 18256145 10.1128/JVI.02660-07
49. Branchlength Calculator http://www.hiv.lanl.gov/content/sequence/ BRANCHLENGTH/branchlength.html
50. Pond SL Frost SD Muse SV HyPhy: Hypothesis testing using phylogenies Bioinformatics 2005, 21:676-679. 10.1093/bioinformatics/bti079 15509596
51. Zhang M Gaschen B Blay W Foley B Haigwood N Kuiken C Korber B Tracking global patterns of N-linked glycosylation site variation in highly variable viral glycoproteins: HIV, SIV, and HCV envelopes and influenza hemagglutinin Glycobiology 2004, 14:1229-1246. 10.1093/glycob/cwh106 15175256
52. Korber BT Kunstman KJ Patterson BK Furtado M McEvilly MM Levy R Wolinsky SM Genetic differences between blood- and brain-derived viral sequences from human immunodeficiency virus type 1-infected patients: Evidence of conserved elements in the V3 region of the envelope protein of brain-derived sequences J Virol 1994, 68:7467-7481. 237189 7933130
53. Marcelino JM Barroso H Goncalves F Silva SM Novo C Gomes P Camacho R Taveira N Use of a new dual-antigen enzyme-linked immunosorbent assay to detect and characterize the human antibody response to the human immunodeficiency virus type 2 envelope gp125 and gp36 glycoproteins J Clin Microbiol 2006, 44:607-611. 1392652 16455923 10.1128/ JCM.44.2.607-611.2006
54. Botarelli P Houlden BA Haigwood NL Servis C Montagna D Abrignani S N-glycosylation of HIV-gp120 may constrain recognition by T lymphocytes J Immunol 1991, 147:3128-3132. 1717587
55. Clevestig P Pramanik L Leitner T Ehrnst A CCR5 use by human immunodeficiency virus type 1 is associated closely with the gp120 V3 loop N-linked glycosylation site J Gen Virol 2006, 87:607-612. 10.1099/ vir.0.81510-0 16476981
56. Pollakis G Kang S Kliphuis A Chalaby MI Goudsmit J Paxton WA N-linked glycosylation of the HIV type-1 gp120 envelope glycoprotein as a major determinant of CCR5 and CXCR4 coreceptor utilization J Biol Chem 2001, 276:13433-13441. 10.1074/jbc.M009779200 11278567
57. Polzer S Dittmar MT Schmitz H Schreiber M The N-linked glycan g15 within the V3 loop of the HIV-1 external glycoprotein gp120 affects coreceptor usage, cellular tropism, and neutralization Virology 2002, 304:70-80. 10.1006/viro.2002.1760 12490404
58. Joos B Fischer M Schweizer A Kuster H Boni J Wong JK Weber R Trkola A Gunthard HF Positive in vivo selection of the HIV-1 envelope protein gp120 occurs at surface-exposed regions J Infect Dis 2007, 196:313-320. 10.1086/518935 17570120
59. Barroso H Araujo F Gomes MH Mota-Miranda A Taveira N Phylogenetic demonstration of two cases of perinatal human immunodeficiency virus type 2 infection diagnosed in adulthood AIDS Res Hum Retroviruses 2004, 20:1373-1376. 10.1089/aid.2004.20.1373 15650432
60. Rambaut A Posada D Crandall KA Holmes EC The causes and consequences of HIV evolution Nat Rev Genet 2004, 5:52-61. 10.1038/nrg1246 14708016
61. Gomes P Taveira NC Pereira JM Antunes F Ferreira MO Lourenco MH Quantitation of human immunodeficiency virus type 2 DNA in peripheral blood mononuclear cells by using a quantitative-competitive PCR assay J Clin Microbiol 1999, 37:453-456. 84340 9889242
62. Jobe O Ariyoshi K Marchant A Sabally S Corrah T Berry N Jaffar S Whittle H Proviral load and immune function in blood and lymph node during HIV-1 and HIV-2 infection Clin Exp Immunol 1999, 116:474-478. 1905295 10361237 10.1046/j.1365-2249.1999.00914.x
63. Parreira R Esteves A Santos C Piedade J Venenno T Canas-Ferreira WF Genetic variability of human immunodeficiency virus type 2 C2V3 region within and between individuals from Bissau, Guinea-Bissau, West Africa AIDS Res Hum Retroviruses 2000, 16:1307-1312. 10.1089/08892220050117069 10957727
64. Yamaguchi-Kabata Y Gojobori T Reevaluation of amino acid variability of the human immunodeficiency virus type 1 gp120 envelope glycoprotein and prediction of new discontinuous epitopes J Virol 2000, 74:4335-4350. 111951 10756049 10.1128/JVI.74.9.4335-4350.2000
65. Yang W Bielawski JP Yang Z Widespread adaptive evolution in the human immunodeficiency virus type 1 genome J Mol Evol 2003, 57:212-221. 10.1007/s00239-003-2467-9 14562964
66. Lemey P Kosakovsky Pond SL Drummond AJ Pybus OG Shapiro B Barroso H Taveira N Rambaut A Synonymous substitution rates predict HIV disease progression as a result of underlying replication dynamics PLoS Comput Biol 2007, 3:e29. 1797821 17305421 10.1371/journal.pcbi.0030029
67. Ross HA Rodrigo AG Immune-mediated positive selection drives human immunodeficiency virus type 1 molecular variation and predicts disease duration J Virol 2002, 76:11715-11720. 136752 12388731 10.1128/ JVI.76.22.11715-11720.2002
68. Korber M BT Brander C Haynes BF Koup R Moore JP Walker BD Watkins DI HIV Molecular Immunology 2006/2007 Los Alamos National Laboratory, Theoretical Biology and Biophysics, Los Alamos, New Mexico. LA-UR 07-4752.
69. Scanlan CN Offer J Zitzmann N Dwek RA Exploiting the defensive sugars of HIV-1 for drug and vaccine design Nature 2007, 446:1038-1045. 10.1038/ nature05818 17460665
70. Fischer PB Karlsson GB Butters TD Dwek RA Platt FM N-butyldeoxynojirimycin-mediated inhibition of human immunodeficiency virus entry correlates with changes in antibody recognition of the V1/V2 region of gp120 J Virol 1996, 70:7143-7152. 190767 8794361
71. Poon AF Lewis FI Pond SL Frost SD Evolutionary interactions between N-linked glycosylation sites in the HIV-1 envelope PLoS Comput Biol 2007, 3:e11. 1779302 17238283 10.1371/journal.pcbi.0030011
72. Grenfell BT Pybus OG Gog JR Wood JL Daly JM Mumford JA Holmes EC Unifying the epidemiological and evolutionary dynamics of pathogens Science 2004, 303:327-332. 10.1126/science.1090727 14726583
73. Zolla-Pazner S Identifying epitopes of HIV-1 that induce protective antibodies Nat Rev Immunol 2004, 4:199-210. 10.1038/nri1307 15039757
74. Richman DD Wrin T Little SJ Petropoulos CJ Rapid evolution of the neutralizing antibody response to HIV type 1 infection Proc Natl Acad Sci USA 2003, 100:4144-4149. 153062 12644702 10.1073/pnas.0630530100
75. Frost SD Wrin T Smith DM Kosakovsky Pond SL Liu Y Paxinos E Chappey C Galovich J Beauchaine J Petropoulos CJ et al. Neutralizing antibody responses drive the evolution of human immunodeficiency virus type 1 envelope during recent HIV infection Proc Natl Acad Sci USA 2005, 102:18514-18519. 1310509 16339909 10.1073/pnas.0504658102
76. Moore PL Gray ES Choge IA Ranchobe N Mlisana K Abdool Karim SS Williamson C Morris L The c3-v4 region is a major target of autologous neutralizing antibodies in human immunodeficiency virus type 1 subtype C infection J Virol 2008, 82:1860-1869. 2258729 18057243 10.1128/ JVI.02187-07
77. Williamson S Adaptation in the env gene of HIV-1 and evolutionary theories of disease progression Mol Biol Evol 2003, 20:1318-1325. 10.1093/molbev/msg144 12777505
78. Marchant D Neil SJ McKnight A Human immunodeficiency virus types 1 and 2 have different replication kinetics in human primary macrophage culture J Gen Virol 2006, 87:411-418. 10.1099/vir.0.81391-0 16432029
79. Lizeng Q Skott P Sourial S Nilsson C Andersson SS Ehnlund M Taveira N Bjorling E Serum immunoglobulin A (IgA)-mediated immunity in human immunodeficiency virus type 2 (HIV-2) infection Virology 2003, 308:225-232. 10.1016/S0042-6822(02)00088-0 12706073
80. Chackerian B Rudensey LM Overbaugh J 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 1997, 71:7719-7727. 192123 9311856
81. Wei X Decker JM Wang S Hui H Kappes JC Wu X Salazar-Gonzalez JF Salazar MG Kilby JM Saag MS et al. Antibody neutralization and escape by HIV-1 Nature 2003, 422:307-312. 10.1038/nature01470 12646921
82. Sagar M Wu X Lee S Overbaugh J 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 2006, 80:9586-9598. 1617272 16973562 10.1128/JVI.00141-06