Partial rescue of V1V2 mutant infectivity by HIV-1 cell-cell transmission supports the domain's exceptional capacity for sequence variation

Retrovirology

Volumn 11, Issue 1, 2014, Pages

  Brandenberg, Oliver F ^a   Rusert, Peter ^a   Magnus, Carsten ^a   Weber, Jacqueline ^a   Böni, Jürg ^a   Günthard, Huldrych F ^b   Regoes, Roland R ^c   Trkola, Alexandra ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c ETH ZURICH   (Switzerland)

Author keywords

Antibody escape; Cell cell transmission; Entry; HIV; Neutralization; V1V2

Indexed keywords

GLYCOPROTEIN GP 120; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; NEUTRALIZING ANTIBODY; GP120 PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1;

ADULT; ARTICLE; CELL FUSION; CLINICAL ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR EVOLUTION; NONHUMAN; POINT MUTATION; SEQUENCE ANALYSIS; SEQUENCE VARIATION; V1V2 MUTANT; VIRION; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS ENVELOPE; VIRUS INFECTION; VIRUS INFECTIVITY; VIRUS MUTANT; VIRUS MUTATION; VIRUS NEUTRALIZATION; VIRUS REPLICATION; VIRUS RESISTANCE; VIRUS STRAIN; VIRUS TRANSMISSION; AMINO ACID SEQUENCE; CHEMISTRY; IMMUNE EVASION; IMMUNOLOGY; MUTATION; PATHOGENICITY; PHYSIOLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

AMINO ACID SEQUENCE; ANTIBODIES, NEUTRALIZING; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; IMMUNE EVASION; MUTATION; VIRUS INTERNALIZATION;

EID: 84908097029     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/s12977-014-0075-y     Document Type: Article

References (104)

1. Klasse PJ. The molecular basis of HIV entry. Cell Microbiol 2012, 14:1183-1192. 22583677.
2. Zwick MB, Burton DR. HIV-1 neutralization: mechanisms and relevance to vaccine design. Curr HIV Res 2007, 5:608-624. 18045117.
3. Cao J, Sullivan N, Desjardin E, Parolin C, Robinson J, Wyatt R, Sodroski J. Replication and neutralization of human immunodeficiency virus type 1 lacking the V1 and V2 variable loops of the gp120 envelope glycoprotein. J Virol 1997, 71:9808-9812. 9371651.
4. Morikita T, Maeda Y, Fujii S, Matsushita S, Obaru K, Takatsuki K. The V1/V2 region of human immunodeficiency virus type 1 modulates the sensitivity to neutralization by soluble CD4 and cellular tropism. AIDS Res Hum Retroviruses 1997, 13:1291-1299. 9339846.
5. Stamatatos L, Cheng-Mayer C. An envelope modification that renders a primary, neutralization-resistant clade B human immunodeficiency virus type 1 isolate highly susceptible to neutralization by sera from other clades. J Virol 1998, 72:7840-7845. 9733820.
6. Losman B, Bolmstedt A, Schonning K, Bjorndal A, Westin C, Fenyo EM, Olofsson S. Protection of neutralization epitopes in the V3 loop of oligomeric human immunodeficiency virus type 1 glycoprotein 120 by N-linked oligosaccharides in the V1 region. AIDS Res Hum Retroviruses 2001, 17:1067-1076. 11485624.
7. Pinter A, Honnen WJ, He Y, Gorny MK, Zolla-Pazner S, Kayman SC. 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 2004, 78:5205-5215. 15113902.
8. Krachmarov C, Pinter A, Honnen WJ, Gorny MK, Nyambi PN, Zolla-Pazner S, Kayman SC. Antibodies That Are Cross-Reactive for Human Immunodeficiency Virus Type 1 Clade A and Clade B V3 Domains Are Common in Patient Sera from Cameroon, but Their Neutralization Activity Is Usually Restricted by Epitope Masking. J Virol 2005, 79:780-790. 15613306.
9. Saunders CJ, McCaffrey RA, Zharkikh I, Kraft Z, Malenbaum SE, Burke B, Cheng-Mayer C, Stamatatos L. The V1, V2, and V3 regions of the human immunodeficiency virus type 1 envelope differentially affect the viral phenotype in an isolate-dependent manner. J Virol 2005, 79:9069-9080. 15994801.
10. 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. 16973562.
11. 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, 81:3757-3768. 17251298.
12. Ching LK, Vlachogiannis G, Bosch KA, Stamatatos L. The first hypervariable region of the gp120 Env glycoprotein defines the neutralizing susceptibility of heterologous human immunodeficiency virus type 1 isolates to neutralizing antibodies elicited by the SF162gp140 immunogen. J Virol 2008, 82:949-956. 18003732.
13. Rusert P, Krarup A, Magnus C, Brandenberg OF, Weber J, Ehlert AK, Regoes RR, Gunthard HF, Trkola A. Interaction of the gp120 V1V2 loop with a neighboring gp120 unit shields the HIV envelope trimer against cross-neutralizing antibodies. J Exp Med 2011, 208:1419-1433. 21646396.
14. Starcich BR, Hahn BH, Shaw GM, McNeely PD, Modrow S, Wolf H, Parks ES, Parks WP, Josephs SF, Gallo RC, Wong-Staal F. Identification and characterization of conserved and variable regions in the envelope gene of HTLV-III/LAV, the retrovirus of AIDS. Cell 1986, 45:637-648. 2423250.
15. Willey RL, Rutledge RA, Dias S, Folks T, Theodore T, Buckler CE, Martin MA. Identification of conserved and divergent domains within the envelope gene of the acquired immunodeficiency syndrome retrovirus. Proc Natl Acad Sci U S A 1986, 83:5038-5042. 3014529.
16. Hu G, Liu J, Taylor KA, Roux KH. Structural comparison of HIV-1 envelope spikes with and without the V1/V2 loop. J Virol 2011, 85:2741-2750. 21191026.
17. Julien JP, Cupo A, Sok D, Stanfield RL, Lyumkis D, Deller MC, Klasse PJ, Burton DR, Sanders RW, Moore JP, Ward AB, Wilson IA. Crystal Structure of a Soluble Cleaved HIV-1 Envelope Trimer. Science 2013, 342:1477-83. 24179159.
18. Lyumkis D, Julien JP, de Val N, Cupo A, Potter CS, Klasse PJ, Burton DR, Sanders RW, Moore JP, Carragher B, Wilson IA, Ward AB. Cryo-EM Structure of a Fully Glycosylated Soluble Cleaved HIV-1 Envelope Trimer. Science 2013, 342:1484-90. 24179160.
19. Wyatt R, Sullivan N, Thali M, Repke H, Ho D, Robinson J, Posner M, Sodroski J. Functional and immunologic characterization of human immunodeficiency virus type 1 envelope glycoproteins containing deletions of the major variable regions. J Virol 1993, 67:4557-4565. 8331723.
20. Stamatatos L, Wiskerchen M, Cheng-Mayer C. Effect of major deletions in the V1 and V2 loops of a macrophage-tropic HIV type 1 isolate on viral envelope structure, cell entry, and replication. AIDS Res Hum Retroviruses 1998, 14:1129-1139. 9737584.
21. Groenink M, Fouchier RA, Broersen S, Baker CH, Koot M, van't Wout AB, Huisman HG, Miedema F, Tersmette M, Schuitemaker H. Relation of phenotype evolution of HIV-1 to envelope V2 configuration. Science 1993, 260:1513-1516. 8502996.
22. Sullivan N, Thali M, Furman C, Ho DD, Sodroski J. 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 recognition by a neutralizing antibody. J Virol 1993, 67:3674-3679. 8497077.
23. Koito A, Harrowe G, Levy JA, Cheng-Mayer C. 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 1994, 68:2253-2259. 8139010.
24. Palmer C, Balfe P, Fox D, May JC, Frederiksson R, Fenyo EM, McKeating JA. Functional characterization of the V1V2 region of human immunodeficiency virus type 1. Virology 1996, 220:436-449. 8661394.
25. Toohey K, Wehrly K, Nishio J, Perryman S, Chesebro B. Human immunodeficiency virus envelope V1 and V2 regions influence replication efficiency in macrophages by affecting virus spread. Virology 1995, 213:70-79. 7483281.
26. Haim H, Strack B, Kassa A, Madani N, Wang L, Courter JR, Princiotto A, McGee K, Pacheco B, Seaman MS, Smith AB, Sodroski J. Contribution of Intrinsic Reactivity of the HIV-1 Envelope Glycoproteins to CD4-Independent Infection and Global Inhibitor Sensitivity. PLoS Pathog 2011, 7:e1002101. 21731494.
27. Kwon YD, Finzi A, Wu X, Dogo-Isonagie C, Lee LK, Moore LR, Schmidt SD, Stuckey J, Yang Y, Zhou T, Zhu J, Vicic DA, Debnath AK, Shapiro L, Bewley CA, Mascola JR, Sodroski JG, Kwong PD. Unliganded HIV-1 gp120 core structures assume the CD4-bound conformation with regulation by quaternary interactions and variable loops. Proc Natl Acad Sci U S A 2012, 109:5663-5668. 22451932.
28. Harrison SC. Viral membrane fusion. Nat Struct Mol Biol 2008, 15:690-698. 18596815.
29. Myszka DG, Sweet RW, Hensley P, Brigham-Burke M, Kwong PD, Hendrickson WA, Wyatt R, Sodroski J, Doyle ML. Energetics of the HIV gp120-CD4 binding reaction. Proc Natl Acad Sci U S A 2000, 97:9026-9031. 10922058.
30. Rao M, Peachman KK, Kim J, Gao G, Alving CR, Michael NL, Rao VB. HIV-1 Variable Loop 2 and its Importance in HIV-1 Infection and Vaccine Development. Curr HIV Res 2013, 11:427-438. 24191938.
31. Walker LM, Phogat SK, Chan-Hui PY, Wagner D, Phung P, Goss JL, Wrin T, Simek MD, Fling S, Mitcham JL, Lehrman JK, Priddy FH, Olsen OA, Frey SM, Hammond PW, Kaminsky S, Zamb T, Moyle M, Koff WC, Poignard P, Burton DR, Principal Investigators PG, Kaminsky S, Zamb T, Moyle M, Koff WC, Poignard P, Burton DR. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 2009, 326:285-289. 19729618.
32. Bonsignori M, Hwang KK, Chen X, Tsao CY, Morris L, Gray E, Marshall DJ, Crump JA, Kapiga SH, Sam NE, Sinangil F, Pancera M, Yongping Y, Zhang B, Zhu J, Kwong PD, O'Dell S, Mascola JR, Wu L, Nabel GJ, Phogat S, Seaman MS, Whitesides JF, Moody MA, Kelsoe G, Yang X, Sodroski J, Shaw GM, Montefiori DC, Kepler TB, et al. Analysis of a clonal lineage of HIV-1 envelope V2/V3 conformational epitope-specific broadly neutralizing antibodies and their inferred unmutated common ancestors. J Virol 2011, 85:9998-10009. 21795340.
33. Walker LM, Huber M, Doores KJ, Falkowska E, Pejchal R, Julien JP, Wang SK, Ramos A, Chan-Hui PY, Moyle M, Mitcham JL, Hammond PW, Olsen OA, Phung P, Fling S, Wong CH, Phogat S, Wrin T, Simek MD, Principal Investigators PG, Koff WC, Wilson IA, Burton DR, Poignard P. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 2011, 477:466-470. 21849977.
34. Gorny MK, Stamatatos L, Volsky B, Revesz K, Williams C, Wang XH, Cohen S, Staudinger R, Zolla-Pazner S. Identification of a new quaternary neutralizing epitope on human immunodeficiency virus type 1 virus particles. J Virol 2005, 79:5232-5237. 15795308.
35. Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, Kaewkungwal J, Chiu J, Paris R, Premsri N, Namwat C, de Souza M, Adams E, Benenson M, Gurunathan S, Tartaglia J, McNeil JG, Francis DP, Stablein D, Birx DL, Chunsuttiwat S, Khamboonruang C, Thongcharoen P, Robb ML, Michael NL, Kunasol P, Kim JH. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N Engl J Med 2009, 361:2209-2220. 19843557.
36. Haynes BF, Gilbert PB, McElrath MJ, Zolla-Pazner S, Tomaras GD, Alam SM, Evans DT, Montefiori DC, Karnasuta C, Sutthent R, Liao HX, DeVico AL, Lewis GK, Williams C, Pinter A, Fong Y, Janes H, DeCamp A, Huang Y, Rao M, Billings E, Karasavvas N, Robb ML, Ngauy V, de Souza MS, Paris R, Ferrari G, Bailer RT, Soderberg KA, Andrews C, et al. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N Engl J Med 2012, 366:1275-1286. 22475592.
37. Rolland M, Edlefsen PT, Larsen BB, Tovanabutra S, Sanders-Buell E, Hertz T, de Camp AC, Carrico C, Menis S, Magaret CA, Ahmed H, Juraska M, Chen L, Konopa P, Nariya S, Stoddard JN, Wong K, Zhao H, Deng W, Maust BS, Bose M, Howell S, Bates A, Lazzaro M, O'Sullivan A, Lei E, Bradfield A, Ibitamuno G, Assawadarachai V, O'Connell RJ, et al. Increased HIV-1 vaccine efficacy against viruses with genetic signatures in Env V2. Nature 2012, 490:417-420. 22960785.
38. Yates NL, Liao HX, Fong Y, de Camp A, Vandergrift NA, Williams WT, Alam SM, Ferrari G, Yang ZY, Seaton KE, Berman PW, Alpert MD, Evans DT, O'Connell RJ, Francis D, Sinangil F, Lee C, Nitayaphan S, Rerks-Ngarm S, Kaewkungwal J, Pitisuttithum P, Tartaglia J, Pinter A, Zolla-Pazner S, Gilbert PB, Nabel GJ, Michael NL, Kim JH, Montefiori DC, Haynes BF, et al. Vaccine-Induced Env V1-V2 IgG3 Correlates with Lower HIV-1 Infection Risk and Declines Soon After Vaccination. Sci Transl Med 2014, 6:228ra239.
39. 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. 9311856.
40. Fox DG, Balfe P, Palmer CP, May JC, Arnold C, McKeating JA. Length polymorphism within the second variable region of the human immunodeficiency virus type 1 envelope glycoprotein affects accessibility of the receptor binding site. J Virol 1997, 71:759-765. 8985413.
41. Shioda T, Oka S, Xin X, Liu H, Harukuni R, Kurotani A, Fukushima M, Hasan MK, Shiino T, Takebe Y, Iwamoto A, Nagai Y. In vivo sequence variability of human immunodeficiency virus type 1 envelope gp120: association of V2 extension with slow disease progression. J Virol 1997, 71:4871-4881. 9188549.
42. Masciotra S, Owen SM, Rudolph D, Yang C, Wang B, Saksena N, Spira T, Dhawan S, Lal RB. Temporal relationship between V1V2 variation, macrophage replication, and coreceptor adaptation during HIV-1 disease progression. AIDS 2002, 16:1887-1898. 12351948.
43. Kitrinos KM, Hoffman NG, Nelson JA, Swanstrom R. Turnover of env variable region 1 and 2 genotypes in subjects with late-stage human immunodeficiency virus type 1 infection. J Virol 2003, 77:6811-6822. 12768001.
44. Harrington PR, Nelson JA, Kitrinos KM, Swanstrom R. Independent evolution of human immunodeficiency virus type 1 env V1/V2 and V4/V5 hypervariable regions during chronic infection. J Virol 2007, 81:5413-5417. 17329337.
45. Bar KJ, Tsao CY, Iyer SS, Decker JM, Yang Y, Bonsignori M, Chen X, Hwang KK, Montefiori DC, Liao HX, Hraber P, Fischer W, Li H, Wang S, Sterrett S, Keele BF, Ganusov VV, Perelson AS, Korber BT, Georgiev I, McLellan JS, Pavlicek JW, Gao F, Haynes BF, Hahn BH, Kwong PD, Shaw GM. Early low-titer neutralizing antibodies impede HIV-1 replication and select for virus escape. PLoS Pathog 2012, 8:e1002721. 22693447.
46. Curlin ME, Zioni R, Hawes SE, Liu Y, Deng W, Gottlieb GS, Zhu T, Mullins JI. HIV-1 envelope subregion length variation during disease progression. PLoS Pathog 2010, 6:e1001228. 21187897.
47. Doria-Rose NA, Georgiev I, O'Dell S, Chuang GY, Staupe RP, McLellan JS, Gorman J, Pancera M, Bonsignori M, Haynes BF, Burton DR, Koff WC, Kwong PD, Mascola JR. A Short Segment of the HIV-1 gp120 V1/V2 Region Is a Major Determinant of Resistance to V1/V2 Neutralizing Antibodies. J Virol 2012, 86:8319-8323. 22623764.
48. Moore PL, Sheward D, Nonyane M, Ranchobe N, Hermanus T, Gray ES, Abdool Karim SS, Williamson C, Morris L. Multiple pathways of escape from HIV broadly cross-neutralizing V2-dependent antibodies. J Virol 2013, 87:4882-4894. 23408621.
49. Chen P, Hubner W, Spinelli MA, Chen BK. Predominant mode of human immunodeficiency virus transfer between T cells is mediated by sustained Env-dependent neutralization-resistant virological synapses. J Virol 2007, 81:12582-12595. 17728240.
50. Sourisseau M, Sol-Foulon N, Porrot F, Blanchet F, Schwartz O. Inefficient human immunodeficiency virus replication in mobile lymphocytes. J Virol 2007, 81:1000-1012. 17079292.
51. Sattentau Q. Avoiding the void: cell-to-cell spread of human viruses. Nat Rev Microbiol 2008, 6:815-826. 18923409.
52. Duncan CJ, Williams JP, Schiffner T, Gartner K, Ochsenbauer C, Kappes J, Russell RA, Frater J, Sattentau QJ. High-multiplicity HIV-1 infection and neutralizing antibody evasion mediated by the macrophage-T cell virological synapse. J Virol 2014, 88:2025-2034. 24307588.
53. Russell RA, Martin N, Mitar I, Jones E, Sattentau QJ. Multiple proviral integration events after virological synapse-mediated HIV-1 spread. Virology 2013, 443:143-149. 23722103.
54. Del Portillo A, Tripodi J, Najfeld V, Wodarz D, Levy DN, Chen BK. Multiploid inheritance of HIV-1 during cell-to-cell infection. J Virol 2011, 85:7169-7176. 21543479.
55. Zhong P, Agosto LM, Munro JB, Mothes W. Cell-to-cell transmission of viruses. Curr Opin Virol 2012, 3:44-50. 23219376.
56. Zhong P, Agosto LM, Ilinskaya A, Dorjbal B, Truong R, Derse D, Uchil PD, Heidecker G, Mothes W. Cell-to-cell transmission can overcome multiple donor and target cell barriers imposed on cell-free HIV. PLoS One 2013, 8:e53138. 23308151.
57. Sigal A, Kim JT, Balazs AB, Dekel E, Mayo A, Milo R, Baltimore D. Cell-to-cell spread of HIV permits ongoing replication despite antiretroviral therapy. Nature 2011, 477:95-98. 21849975.
58. Abela IA, Berlinger L, Schanz M, Reynell L, Gunthard HF, Rusert P, Trkola A. Cell-cell transmission enables HIV-1 to evade inhibition by potent CD4bs directed antibodies. PLoS Pathog 2012, 8:e1002634. 22496655.
59. Malbec M, Porrot F, Rua R, Horwitz J, Klein F, Halper-Stromberg A, Scheid JF, Eden C, Mouquet H, Nussenzweig MC, Schwartz O. Broadly neutralizing antibodies that inhibit HIV-1 cell to cell transmission. J Exp Med 2013, 210:2813-21. 24277152.
60. Jolly C, Kashefi K, Hollinshead M, Sattentau QJ. HIV-1 cell to cell transfer across an Env-induced, actin-dependent synapse. J Exp Med 2004, 199:283-293. 14734528.
61. O'Rourke SM, Schweighardt B, Phung P, Fonseca DP, Terry K, Wrin T, Sinangil F, Berman PW. Mutation at a single position in the V2 domain of the HIV-1 envelope protein confers neutralization sensitivity to a highly neutralization-resistant virus. J Virol 2010, 84:11200-11209. 20702624.
62. Mazurov D, Ilinskaya A, Heidecker G, Lloyd P, Derse D. Quantitative comparison of HTLV-1 and HIV-1 cell-to-cell infection with new replication dependent vectors. PLoS Pathog 2010, 6:e1000788. 20195464.
63. Dale BM, Alvarez RA, Chen BK. Mechanisms of enhanced HIV spread through T-cell virological synapses. Immunol Rev 2013, 251:113-124. 23278744.
64. Schiffner T, Sattentau QJ, Duncan CJ. Cell-to-cell spread of HIV-1 and evasion of neutralizing antibodies. Vaccine 2013, 31:5789-5797. 24140477.
65. Pantophlet R, Ollmann Saphire E, Poignard P, Parren PW, Wilson IA, Burton DR. Fine mapping of the interaction of neutralizing and nonneutralizing monoclonal antibodies with the CD4 binding site of human immunodeficiency virus type 1 gp120. J Virol 2003, 77:642-658. 12477867.
66. Moore PL, Gray ES, Sheward D, Madiga M, Ranchobe N, Lai Z, Honnen WJ, Nonyane M, Tumba N, Hermanus T, Sibeko S, Mlisana K, Abdool Karim SS, Williamson C, Pinter A, Morris L. Potent and broad neutralization of HIV-1 subtype C by plasma antibodies targeting a quaternary epitope including residues in the V2 loop. J Virol 2011, 85:3128-3141. 21270156.
67. Liao HX, Bonsignori M, Alam SM, McLellan JS, Tomaras GD, Moody MA, Kozink DM, Hwang KK, Chen X, Tsao CY, Liu P, Lu X, Parks RJ, Montefiori DC, Ferrari G, Pollara J, Rao M, Peachman KK, Santra S, Letvin NL, Karasavvas N, Yang ZY, Dai K, Pancera M, Gorman J, Wiehe K, Nicely NI, Rerks-Ngarm S, Nitayaphan S, Kaewkungwal J, et al: Vaccine Induction of Antibodies against a Structurally Heterogeneous Site of Immune Pressure within HIV-1 Envelope Protein Variable Regions 1 and 2.Immunity 2013.
68. Los Alamos HIV Database: HIV-1/SIVcpz env protein sequences curated alignment. 2011, http://www.hiv.lanl.gov/content/sequence/NEWALIGN/align.html
69. Wu X, Changela A, O'Dell S, Schmidt SD, Pancera M, Yang Y, Zhang B, Gorny MK, Phogat S, Robinson JE, Stamatatos L, Zolla-Pazner S, Kwong PD, Mascola JR. Immunotypes of a Quaternary Site of HIV-1 Vulnerability and Their Recognition by Antibodies. J Virol 2011, 85:4578-4585. 21325411.
70. Ho SH, Tasca S, Shek L, Li A, Gettie A, Blanchard J, Boden D, Cheng-Mayer C. Coreceptor switch in R5-tropic simian/human immunodeficiency virus-infected macaques. J Virol 2007, 81:8621-8633. 17537860.
71. Wibmer CK, Bhiman JN, Gray ES, Tumba N, Abdool Karim SS, Williamson C, Morris L, Moore PL. Viral escape from HIV-1 neutralizing antibodies drives increased plasma neutralization breadth through sequential recognition of multiple epitopes and immunotypes. PLoS Pathog 2013, 9:e1003738. 24204277.
72. Honnen WJ, Krachmarov C, Kayman SC, Gorny MK, Zolla-Pazner S, Pinter A. Type-specific epitopes targeted by monoclonal antibodies with exceptionally potent neutralizing activities for selected strains of human immunodeficiency virus type 1 map to a common region of the V2 domain of gp120 and differ only at single positions from the clade B consensus sequence. J Virol 2007, 81:1424-1432. 17121806.
73. Arthos J, Cicala C, Martinelli E, Macleod K, Van Ryk D, Wei D, Xiao Z, Veenstra TD, Conrad TP, Lempicki RA, McLaughlin S, Pascuccio M, Gopaul R, McNally J, Cruz CC, Censoplano N, Chung E, Reitano KN, Kottilil S, Goode DJ, Fauci AS. HIV-1 envelope protein binds to and signals through integrin alpha4beta7, the gut mucosal homing receptor for peripheral T cells. Nat Immunol 2008, 9:301-309. 18264102.
74. Cicala C, Arthos J, Fauci AS. HIV-1 envelope, integrins and co-receptor use in mucosal transmission of HIV. J Transl Med 2011, 9(Suppl 1):S2. 21284901.
75. Parrish NF, Wilen CB, Banks LB, Iyer SS, Pfaff JM, Salazar-Gonzalez JF, Salazar MG, Decker JM, Parrish EH, Berg A, Hopper J, Hora B, Kumar A, Mahlokozera T, Yuan S, Coleman C, Vermeulen M, Ding H, Ochsenbauer C, Tilton JC, Permar SR, Kappes JC, Betts MR, Busch MP, Gao F, Montefiori D, Haynes BF, Shaw GM, Hahn BH, Doms RW. 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:e1002686. 22693444.
76. Pauls E, Ballana E, Moncunill G, Bofill M, Clotet B, Ramo-Tello C, Este JA. Evaluation of the anti-HIV activity of natalizumab, an antibody against integrin alpha4. AIDS 2009, 23:266-268. 19112691.
77. McLinden RJ, Labranche CC, Chenine AL, Polonis VR, Eller MA, Wieczorek L, Ochsenbauer C, Kappes JC, Perfetto S, Montefiori DC, Michael NL, Kim JH. Detection of HIV-1 neutralizing antibodies in a human CD4(+)/CXCR4(+)/CCR5(+) T-lymphoblastoid cell assay system. PLoS One 2013, 8:e77756. 24312168.
78. Mayr LM, Cohen S, Spurrier B, Kong XP, Zolla-Pazner S. Epitope mapping of conformational V2-specific anti-HIV human monoclonal antibodies reveals an immunodominant site in V2. PLoS One 2013, 8:e70859. 23923028.
79. Spurrier B, Sampson J, Gorny MK, Zolla-Pazner S, Kong XP. Functional Implications of the Binding Mode of a Human Conformation-Dependent V2 Monoclonal Antibody against HIV. J Virol 2014, 88:4100-4112. 24478429.
80. Chen BK. T cell virological synapses and HIV-1 pathogenesis. Immunol Res 2012, 54:133-139. 22477441.
81. Murooka TT, Deruaz M, Marangoni F, Vrbanac VD, Seung E, von Andrian UH, Tager AM, Luster AD, Mempel TR. HIV-infected T cells are migratory vehicles for viral dissemination. Nature 2012, 490:283-287. 22854780.
82. McLellan JS, Pancera M, Carrico C, Gorman J, Julien JP, Khayat R, Louder R, Pejchal R, Sastry M, Dai K, O'Dell S, Patel N, Shahzad-ul-Hussan S, Yang Y, Zhang B, Zhou T, Zhu J, Boyington JC, Chuang GY, Diwanji D, Georgiev I, Kwon YD, Lee D, Louder MK, Moquin S, Schmidt SD, Yang ZY, Bonsignori M, Crump JA, Kapiga SH, et al. Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9. Nature 2011, 480:336-343. 22113616.
83. Bunnik EM, Euler Z, Welkers MR, Boeser-Nunnink BD, Grijsen ML, Prins JM, Schuitemaker H. Adaptation of HIV-1 envelope gp120 to humoral immunity at a population level. Nat Med 2010, 16:995-997. 20802498.
84. Freed EO, Martin MA. Evidence for a functional interaction between the V1/V2 and C4 domains of human immunodeficiency virus type 1 envelope glycoprotein gp120. J Virol 1994, 68:2503-2512. 8139032.
85. Wang WK, Essex M, Lee TH. Single amino acid substitution in constant region 1 or 4 of gp120 causes the phenotype of a human immunodeficiency virus type 1 variant with mutations in hypervariable regions 1 and 2 to revert. J Virol 1996, 70:607-611. 8523579.
86. Carrillo A, Ratner L. Cooperative effects of the human immunodeficiency virus type 1 envelope variable loops V1 and V3 in mediating infectivity for T cells. J Virol 1996, 70:1310-1316. 8551601.
87. Muster T, Steindl F, Purtscher M, Trkola A, Klima A, Himmler G, Ruker F, Katinger H. A conserved neutralizing epitope on gp41 of human immunodeficiency virus type 1. J Virol 1993, 67:6642-6647. 7692082.
88. Trkola A, Purtscher M, Muster T, Ballaun C, Buchacher A, Sullivan N, Srinivasan K, Sodroski J, Moore JP, Katinger H. Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1. J Virol 1996, 70:1100-1108. 8551569.
89. Roben P, Moore JP, Thali M, Sodroski J, Barbas CF, Burton DR. Recognition properties of a panel of human recombinant Fab fragments to the CD4 binding site of gp120 that show differing abilities to neutralize human immunodeficiency virus type 1. J Virol 1994, 68:4821-4828. 7518527.
90. Thali M, Moore JP, Furman C, Charles M, Ho DD, Robinson J, Sodroski J. Characterization of conserved human immunodeficiency virus type 1 gp120 neutralization epitopes exposed upon gp120-CD4 binding. J Virol 1993, 67:3978-3988. 7685405.
91. Zolla-Pazner S, Zhong P, Revesz K, Volsky B, Williams C, Nyambi P, Gorny MK. The cross-clade neutralizing activity of a human monoclonal antibody is determined by the GPGR V3 motif of HIV type 1. AIDS Res Hum Retroviruses 2004, 20:1254-1258. 15588347.
92. Scheid JF, Mouquet H, Feldhahn N, Seaman MS, Velinzon K, Pietzsch J, Ott RG, Anthony RM, Zebroski H, Hurley A, Phogat A, Chakrabarti B, Li Y, Connors M, Pereyra F, Walker BD, Wardemann H, Ho D, Wyatt RT, Mascola JR, Ravetch JV, Nussenzweig MC. Broad diversity of neutralizing antibodies isolated from memory B cells in HIV-infected individuals. Nature 2009, 458:636-640. 19287373.
93. Wild C, Greenwell T, Matthews T. A synthetic peptide from HIV-1 gp41 is a potent inhibitor of virus-mediated cell-cell fusion. AIDS Res Hum Retroviruses 1993, 9:1051-1053. 8312047.
94. Wei X, Decker JM, Liu H, Zhang Z, Arani RB, Kilby JM, Saag MS, Wu X, Shaw GM, Kappes JC. Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob Agents Chemother 2002, 46:1896-1905. 12019106.
95. Kueck T, Neil SJ. A cytoplasmic tail determinant in HIV-1 Vpu mediates targeting of tetherin for endosomal degradation and counteracts interferon-induced restriction. PLoS Pathog 2012, 8:e1002609. 22479182.
96. Moore PL, Ranchobe N, Lambson BE, Gray ES, Cave E, Abrahams MR, Bandawe G, Mlisana K, Abdool Karim SS, Williamson C, Morris L. Limited neutralizing antibody specificities drive neutralization escape in early HIV-1 subtype C infection. PLoS Pathog 2009, 5:e1000598. 19763271.
97. Bontjer I, Land A, Eggink D, Verkade E, Tuin K, Baldwin C, Pollakis G, Paxton WA, Braakman I, Berkhout B, Sanders RW. Optimization of human immunodeficiency virus type 1 envelope glycoproteins with V1/V2 deleted, using virus evolution. J Virol 2009, 83:368-383. 18922866.
98. Schoeni-Affolter F, Ledergerber B, Rickenbach M, Rudin C, Gunthard HF, Telenti A, Furrer H, Yerly S, Francioli P. Cohort profile: the Swiss HIV Cohort study. Int J Epidemiol 2010, 39:1179-1189. 19948780.
99. Rieder P, Joos B, von Wyl V, Kuster H, Grube C, Leemann C, Boni J, Yerly S, Klimkait T, Burgisser P, Weber R, Fischer M, Günthard HF. HIV-1 transmission after cessation of early antiretroviral therapy among men having sex with men. AIDS 2010, 24:1177-1183. 20386427.
100. Rusert P, Mann A, Huber M, von Wyl V, Gunthard HF, Trkola A. Divergent effects of cell environment on HIV entry inhibitor activity. AIDS 2009, 23:1319-1327. 19579289.
101. Zufferey R, Nagy D, Mandel RJ, Naldini L, Trono D. Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat Biotechnol 1997, 15:871-875. 9306402.
102. Manrique A, Rusert P, Joos B, Fischer M, Kuster H, Leemann C, Niederost B, Weber R, Stiegler G, Katinger H, Günthard HF, Trkola A. In vivo and in vitro escape from neutralizing antibodies 2G12, 2 F5, and 4E10. J Virol 2007, 81:8793-8808. 17567707.
103. Agosto LM, Zhong P, Munro J, Mothes W. Highly Active Antiretroviral Therapies Are Effective against HIV-1 Cell-to-Cell Transmission. PLoS Pathog 2014, 10:e1003982. 24586176.
104. Richardson MW, Carroll RG, Stremlau M, Korokhov N, Humeau LM, Silvestri G, Sodroski J, Riley JL. Mode of transmission affects the sensitivity of human immunodeficiency virus type 1 to restriction by rhesus TRIM5alpha. J Virol 2008, 82:11117-11128. 18768965.