Global panel of HIV-1 env reference strains for standardized assessments of vaccine-elicited neutralizing antibodies

Journal of Virology

Volumn 88, Issue 5, 2014, Pages 2489-2507

  de Camp, Allan ^a   Hraber, Peter ^b   Bailer, Robert T ^c   Seaman, Michael S ^d   Ochsenbauer, Christina ^e   Kappes, John ^e,f   Gottardo, Raphael ^a   Edlefsen, Paul ^a   Self, Steve ^a   Tang, Haili ^g   Greene, Kelli ^g   Gao, Hongmei ^g   Daniell, Xiaoju ^g   Sarzotti Kelsoe, Marcella ^g   Gorny, Miroslaw K ^h   Zolla Pazner, Susan ^h,i   LaBranche, Celia C ^g   Mascola, John R ^c   Korber, Bette T ^b   Montefiori, David C ^g  

^a Fred Hutchinson Cancer Research Center   (United States)

^b LOS ALAMOS NATIONAL LABORATORY   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^f BIRMINGHAM VA MEDICAL CENTER   (United States)

^g DUKE UNIVERSITY MEDICAL CENTER   (United States)

^h NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

ⁱ VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HUMAN IMMUNODEFICIENCY VIRUS VACCINE; VIRUS ENVELOPE PROTEIN;

ANTIBODY DETECTION; ANTIBODY RESPONSE; ANTIGENIC VARIATION; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; GENETIC VARIABILITY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IN VITRO STUDY; MAJOR CLINICAL STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REFERENCE VALUE; RENILLA LUCIFERASE REPORTER GENE; REPORTER GENE; SEQUENCE ANALYSIS; SEROLOGY; STATISTICAL MODEL; SYSTEMATIC REVIEW; VIRAL TROPISM; VIRUS NEUTRALIZATION; VIRUS STRAIN;

AIDS VACCINES; AMINO ACID SEQUENCE; ANTIBODIES, NEUTRALIZING; ANTIBODY SPECIFICITY; CELL LINE; CLUSTER ANALYSIS; CROSS REACTIONS; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; EPITOPES; HIV ANTIBODIES; HIV-1; HUMANS; MOLECULAR SEQUENCE DATA; NEUTRALIZATION TESTS; PHYLOGENY; RECEPTORS, HIV; REPRODUCIBILITY OF RESULTS; SEQUENCE ALIGNMENT; VIRAL TROPISM;

EID: 84896739535     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02853-13     Document Type: Article

References (85)

1. Mascola JR, Montefiori DC. 2010. The role of antibodies in HIV vaccines. Annu. Rev. Immunol. 28:413-444. http://dx.doi.org/10.1146/annurev-immunol-030409-101256.
2. Hemelaar J, Gouws E, Ghys PD, Osmanov S. 2011. Global trends in molecular epidemiology of HIV-1 during 2000-2007. AIDS 25:679-689. http://dx.doi.org/10.1097/QAD.0b013e328342ff93.
3. Hemelaar J. 2013. Implications of HIV diversity for the HIV-1 pandemic. J. Infect. 66:391-400. http://dx.doi.org/10.1016/j.jinf.2012.10.026.
4. Seaman MS, Janes H, Hawkins N, Grandpre LE, Devoy C, Giri A, Coffey RT, Harris L, Wood B, Daniels MG, Bhattacharya T, Lapedes A, Polonis VR, McCutchan FE, Gilbert PB, Self SG, Korber BT, Montefiori DC, Mascola JR. 2010. Tiered categorization of a diverse panel of HIV-1 Env pseudoviruses for assessments of neutralizing antibodies. J. Virol. 84:1439-1452. http://dx.doi.org/10.1128/JVI.02108-09.
5. Bou-Habib DC, Roderiquez G, Oravecz T, Berman PW, Lusso P, Norcross MA. 1994. Cryptic nature of envelope V3 region epitopes protects primary monocytotropic human immunodeficiency virus type 1 from antibody neutralization. J. Virol. 68:6006-6013.
6. Davis KL, Gray ES, Moore PL, Decker JM, Salomon A, Montefiori DC, Graham BS, Keefer MC, Pinter A, Morris L, Hahn BH, Shaw GM. 2009. High titer HIV-1 V3-specific antibodies with broad reactivity but low neutralizing potency in acute infection and following vaccination. Virology 387:414-426. http://dx.doi.org/10.1016/j.virol.2009.02.022.
7. Decker JM, Bibollet-Ruche F, Wei X, Wang S, Levy DN, Wang W, Delaporte E, Peeters M, Derdeyn CA, Allen S, Hunter E, Saag MS, Hoxie JA, Hahn BH, Kwong PD, Robinson JE, Shaw GM. 2005. Antigenic conservation and immunogenicity of the HIV coreceptor binding site. J. Exp. Med. 201:1407-1419. http://dx.doi.org/10.1084/jem.20042510.
8. Matthews TJ. 1994. Dilemma of neutralization resistance of HIV-1 field isolates and vaccine development. AIDS Res. Hum. Retroviruses 10:631- 632. http://dx.doi.org/10.1089/aid.1994.10.631.
9. Moore JP, Burton DR. 2004. Urgently needed: a filter for the HIV-1 vaccine pipeline. Nat. Med. 10:769-771. http://dx.doi.org/10.1038/nm0804-769.
10. Burton DR, Ahmed R, Barouch DH, Butera ST, Crotty S, Godzik A, Kaufmann DE, McElrath MJ, Nussenzweig MC, Pulendran B, Scanlan CN, Schief WR, Silvestri G, Streeck H, Walker BD, Walker LM, Ward AB, Wilson IA, Wyatt R. 2012. A blueprint for HIV vaccine discovery. Cell Host Microbe 12:396-407. http://dx.doi.org/10.1016/j.chom.2012.09.008.
11. Kwong PD, Mascola JR. 2012. Human antibodies that neutralize HIV-1: identification, structures, and B cell ontogenies. Immunity 37:412-425. http://dx.doi.org/10.1016/j.immuni.2012.08.012.
12. Corti D, Lanzavecchia A. 2013. Broadly neutralizing antiviral antibodies. Annu. Rev. Immunol. 31:705-742. http://dx.doi.org/10.1146/annurev-immunol-032712-095916.
13. Huang J, Ofek G, Laub L, Louder MK, Doria-Rose NA, Longo NS, Imamichi H, Bailer RT, Chakrabarti B, Sharma SK, Munir Alam S, Wang T, Yang Y, Zhang B, Migueles SA, Wyatt R, Haynes BF, Kwong PD, Mascola JR, Connors M. 2012. Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature 491:406-414. http://dx.doi.org/10.1038/nature11544.
14. Burton DR, Desrosiers RC, Doms RW, Koff WC, Kwong PD, Moore JP, Nabel GJ, Sodroski J, Wilson IA, Wyatt RT. 2004. HIV vaccine design and the neutralizing antibody problem. Nat. Immunol. 5:233-236. http://dx.doi.org/10.1038/ni0304-233.
15. Douek DC, Kwong PD, Nabel GJ. 2006. The rational design of an AIDS vaccine. Cell 124:677-681. http://dx.doi.org/10.1016/j.cell.2006.02.005.
16. Dey B, Svehla K, Xu L, Wycuff D, Zhou T, Voss G, Phogat A, Chakrabarti BK, Li Y, Shaw G, Kwong PD, Nabel GJ, Mascola JR, Wyatt RT. 2009. Structure-based stabilization of HIV-1 gp120 enhances humoral immune responses to the induced co-receptor binding site. PLoS Pathog. 5:e1000445. http://dx.doi.org/10.1371/journal.ppat.1000445.
17. Wu L, Zhou T, Yang ZY, Svehla K, O'Dell S, Louder MK, Xu L, Mascola JR, Burton DR, Hoxie JA, Doms RW, Kwong PD, Nabel GJ. 2009. Enhanced exposure of the CD4-binding site to neutralizing antibodies by structural design of a membrane-anchored human immunodeficiency virus type 1 gp120 domain. J. Virol. 83:5077-5086. http://dx.doi.org/10.1128/JVI.02600-08.
18. Ho J, Uger RA, Zwick MB, Luscher MA, Barber BH, MacDonald KS. 2005. Conformational constraints imposed on a pan-neutralizing HIV-1 antibody epitope result in increased antigenicity but not neutralizing responses. Vaccine 23:1559-1573. http://dx.doi.org/10.1016/j.vaccine.2004.09.037.
19. DeVico A, Fouts T, Lewis GK, Gallo RC, Godfrey K, Charurat M, Harris I, Galmin L, Pal R. 2007. Antibodies to CD4-induced sites in HIV gp120 correlate with the control of SHIV challenge in macaques vaccinated with subunit immunogens. Proc. Natl. Acad. Sci. U. S. A. 104: 17477-17482. http://dx.doi.org/10.1073/pnas.0707399104.
20. Joyce JG, Hurni WM, Bogusky MJ, Garsky VM, Liang X, Citron MP, Danzeisen RC, Miller MD, Shiver JW, Keller PM. 2002. Enhancement of α-helicity in the HIV-1 inhibitory peptide DP178 leads to an increased affinity for human monoclonal antibody 2F5 but does not elicit neutralizing antibody responses in vitro. J. Biol. Chem. 277:45811-45820. http://dx.doi.org/10.1074/jbc.M205862200.
21. Kim M, Qiao Z, Yu J, Montefiori D, Reinherz EL. 2007. Immunogenicity of recombinant human immunodeficiency virus type 1-like particles expressing gp41 derivatives in a pre-fusion state. Vaccine 25:5102- 5114. http://dx.doi.org/10.1016/j.vaccine.2006.09.071.
22. Cardoso RM, Zwick MB, Stanfield RL, Kunert R, Binley JM, Katinger H, Burton DR, Wilson IA. 2005. Broadly neutralizing anti-HIV antibody 4E10 recognizes a helical conformation of a highly conserved fusionassociated motif in gp41. Immunity 22:163-173. http://dx.doi.org/10.1016/j.immuni.2004.12.011.
23. Ofek G, Tang M, Sambor A, Katinger H, Mascola JR, Wyatt R, Kwong PD. 2004. Structure and mechanistic analysis of the anti-human immunodeficiency virus type 1 antibody 2F5 in complex with its gp41 epitope. J. Virol. 78:10724-10737. http://dx.doi.org/10.1128/JVI.78.19.10724-10737.2004. 24. Saphire EO, Parren PW, Pantophlet R, Zwick MB, Morris GM, Rudd PM, Dwek RA, Stanfield RL, Burton DR, Wilson IA. 2001. Crystal structure of a neutralizing human IgG against HIV-1: a template for vaccine design. Science 293:1155-1159. http://dx.doi.org/10.1126/science.1061692.
24. Saphire EO, Parren PW, Pantophlet R, Zwick MB, Morris GM, Rudd PM, Dwek RA, Stanfield RL, Burton DR, Wilson IA. 2001. Crystal structure of a neutralizing human IgG against HIV-1: a template for vaccine design. Science 293:1155-1159. http://dx.doi.org/10.1126/science.1061692
25. Stanfield RL, Gorny MK, Williams C, Zolla-Pazner S, Wilson IA. 2004. Structural rationale for the broad neutralization of HIV-1 by human monoclonal antibody 447-52D. Structure (Camb.) 12:193-204. http://dx.doi.org/10.1016/j.str.2004.01.003.
26. Zhou T, Xu L, Dey B, Hessell AJ, Van Ryk D, Xiang SH, Yang X, Zhang MY, Zwick MB, Arthos J, Burton DR, Dimitrov DS, Sodroski J, Wyatt R, Nabel GJ, Kwong PD. 2007. Structural definition of a conserved neutralization epitope on HIV-1 gp120. Nature 445:732-737. http://dx.doi.org/10.1038/nature05580.
27. Haynes BF, Fleming J, St Clair EW, Katinger H, Stiegler G, Kunert R, Robinson J, Scearce RM, Plonk K, Staats HF, Ortel TL, Liao HX, Alam SM. 2005. Cardiolipin polyspecific autoreactivity in two broadly neutralizing HIV-1 antibodies. Science 308:1906-1908. http://dx.doi.org/10.1126/science.1111781.
28. Haynes BF, Moody MA, Verkoczy L, Kelsoe G, Alam SM. 2005. Antibody polyspecificity and neutralization of HIV-1: a hypothesis. Hum. Antibodies 14:59-67. http://www.ncbi.nlm.nih.gov/pmc/article/PMC2673565.
29. Fernando K, Hu H, Ni H, Hoxie JA, Weissman D. 2007. Vaccinedelivered HIV envelope inhibits CD4+T-cell activation, a mechanism for poor HIV vaccine responses. Blood 109:2538-2544. http://dx.doi.org/10.1182/blood-2006-08-038661.
30. He B, Qiao X, Klasse PJ, Chiu A, Chadburn A, Knowles DM, Moore JP, Cerutti A. 2006. HIV-1 envelope triggers polyclonal IgG class switch recombination through a CD40-independent mechanism involving BAFF and C-type lectin receptors. J. Immunol. 176:3931-3941. http:www.jimmunol.org/content/176/7/3931.long.
31. Shan M, Klasse PJ, Banerjee K, Dey AK, Iyer SPN, Dionisio R, Charles D, Campbell-Gardener L, Olson WC, Sanders RW, Moore JP. 2007. HIV-1 gp120 mannoses induce immunosuppressive responses from dendritic cells. PLoS Pathog. 3:e169. http://dx.doi.org/10.1371/journal.ppat.0030169.
32. McMichael AJ, Haynes BF. 2012. Lessons learned from HIV-1 vaccine trials: new priorities and directions. Nat. Immunol. 13:423-427. http://dx.doi.org/10.1038/ni.2264.
33. Liao H-X, Lynch R, Zhou T, Gao F, Alam SM, Boyd SD, Fire AZ, Roskin KM, Schramm CA, Zhang Z, Zhu J, Shapiro L, Comparative Sequencing Program NISC, Mullikin JC, Gnanakaran S, Hraber P, Wiehe K, Kelsoe G, Yang G, Xia SM, Montefiori DC, Parks R, Lloyd KE, Scearce RM, Soderberg KA, Cohen M, Kamanga G, Louder MK, Tran LM, Chen Y, Cai F, Chen S, Moquin S, Du X, Joyce MG, Srivatsan S, Zhang B, Zheng A, Shaw GM, Hahn BH, Kepler TB, Korber BT, Kwong PD, Mascola JR, Haynes BF. 2013. Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature 496:469-476. http://dx.doi.org/10.1038/nature12053.
34. Jardine J, Julien JP, Menis S, Ota T, Kalyuzhniy O, McGuire A, Sok D, Huang PS, MacPherson S, Jones M, Nieusma T, Mathison J, Baker D, Ward AB, Burton DR, Stamatatos L, Nemazee D, Wilson IA, Schief WR. 2013. Rational HIV immunogen design to target specific germline B cell receptors. Science 340:711-716. http://dx.doi.org/10.1126/science.1234150.
35. Li M, Gao F, Mascola JR, Stamatatos L, Polonis VR, Koutsoukos M, Voss G, Goepfert P, Gilbert P, Greene KM, Bilska M, Kothe DL, Salazar-Gonzalez JF, Wei X, Decker JM, Hahn BH, Montefiori DC. 2005. Human immunodeficiency virus type 1 env clones from acute and early subtype B infections for standardized assessments of vaccine-elicited neutralizing antibodies. J. Virol. 79:10108-10125. http://dx.doi.org/10.1128/JVI.79.16.10108-10125.2005.
36. Li M, Salazar-Gonzalez JF, Derdeyn CA, Morris L, Williamson C, Robinson JE, Decker JM, Li Y, Salazar MG, Polonis VR, Mlisana K, Karim SA, Hong K, Greene KM, Bilska M, Zhou J, Allen S, Chomba E, Mulenga J, Vwalika C, Gao F, Zhang M, Korber BT, Hunter E, Hahn BH, Montefiori DC. 2006. Genetic and neutralization properties of subtype C human immunodeficiency virus type 1 molecular env clones from acute and early heterosexually acquired infections in southern Africa. J. Virol. 80:11776-11790. http://dx.doi.org/10.1128/JVI.01730-06.
37. Mascola JR, D'Souza P, Gilbert P, Hahn B, Haigwood NL, Morris L, Petropoulos CJ, Polonis VR, Sarzotti M, Montefiori DC. 2005. Recommendations for the design and use of standard virus panels to assess the neutralizing antibody response elicited by candidate human immunodeficiency virus type 1 vaccines. J. Virol. 79:10103-10107. http://dx.doi.org/10.1128/JVI.79.16.10103-10107.2005.
38. Brown BK, Darden JM, Tovanabutra S, Oblander T, Frost J, Sanders-Buell E, de Souza MS, Birx DL, McCutchan FE, Polonis VR. 2005. Biologic and genetic characterization of a panel of 60 human immunodeficiency virus type 1 isolates, representing clades A, B, C, D, CRF01 AE, and CRF02 AG, for the development and assessment of candidate vaccines. J. Virol. 79:6089-6101. http://dx.doi.org/10.1128/JVI.79.10.6089-6101.2005.
39. Simek MD, Rida W, Priddy FH, Pung P, Carrow E, Laufer DS, Lehrman JK, Boaz M, Tarragona-Fiol T, Miiro G, Birungi J, Pozniak A, McPhee DA, Manigart O, Karita E, Inwoley A, Jaoko W, Dehovitz J, Bekker LG, Pitisuttithum P, Paris R, Walker LM, Poignard P, Wrin T, Fast PE, Burton DR, Koff WC. 2009. Human immunodeficiency virus type 1 elite neutralizers: individuals with broad and potent neutralizing activity identified by using a high-throughput neutralization assay together with an analytical selection algorithm. J. Virol. 83:7337-7348. http://dx.doi.org/10.1128/JVI.00110-09.
40. Wu X, Yang ZY, Li Y, Hogerkorp CM, Schief WR, Seaman MS, Zhou T, Schmidt SD, Wu L, Xu L, Longo NS, McKee K, O'Dell S, Louder MK, Wycuff DL, Feng Y, Nason M, Doria-Rose N, Connors M, Kwong PD, Roederer M, Wyatt RT, Nabel GJ, Mascola JR. 2010. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329:856-861. http://dx.doi.org/10.1126/science.1187659.
41. Zhou T, Georgiev I, Wu X, Yang ZY, Dai K, Finzi A, Kwon YD, Scheid JF, Shi W, Xu L, Yang Y, Zhu J, Nussenzweig MC, Sodroski J, Shapiro L, Nabel GJ, Mascola JR, Kwong PD. 2010. Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 329:811-817. http://dx.doi.org/10.1126/science.1192819.
42. Bonsignori M, Montefiori DC, Wu X, Chen X, Hwang KK, Tsao CY, Kozink DM, Parks RJ, Tomaras GD, Crump JA, Kapiga SH, Sam NE, Kwong PD, Kepler TB, Liao HX, Mascola R, Haynes BF. 2012. Two distinct broadly neutralizing antibody specificities of different clonal lineages in a single HIV-1-infected donor: implications for vaccine design. J. Virol. 86:4688-4692. http://dx.doi.org/10.1128/JVI.07163-11.
43. Wu X, Zhou T, Zhu J, Zhang B, Georgiev I, Wang C, Chen X, Longo NS, Louder M, McKee K, O'Dell S, Perfetto S, Schmidt SD, Shi W, Wu L, Yang Y, Yang ZY, Yang Z, Zhang Z, Bonsignori M, Crump JA, Kapiga SH, Sam NE, Haynes BF, Simek M, Burton DR, Koff WC, Doria-Rose NA, Connors M, Comparative Sequencing Program NISC, Mullikin JC, Nabel GJ, Roederer M, Shapiro L, Kwong PD, Mascola JR. 2011. Focused evolution of HIV-1 neutralizing antibodies revealed by structures and deep sequencing. Science 333:1593-1602. http://dx.doi.org/10.1126/science.1207532.
44. Corti D, Langedijk JP, Hinz A, Seaman MS, Vanzetta F, Fernandez- Rodriguez BM, Silacci C, Pinna D, Jarrossay D, Balla-Jhagjhoorsingh S, Willems B, Zekveld MJ, Dreja H, O'Sullivan E, Pade C, Orkin C, Jeffs SA, Montefiori DC, Davis D, Weissenhorn W, McKnight A, Heeney JL, Sallusto F, Sattentau QJ, Weiss RA, Lanzavecchia A. 2010. Analysis of memory B cell responses and isolation of novel monoclonal antibodies with neutralizing breadth from HIV-1-infected individuals. PLoS One 5:e8805. http://dx.doi.org/10.1371/journal.pone.0008805.
45. Burton DR, Pyati J, Koduri R, Sharp SJ, Thornton GB, Parren PW, Sawyer LS, Hendry RM, Dunlop N, Nara PL, et al. 1994. Efficient neutralization of primary isolates of HIV-1 by a recombinant human monoclonal antibody. Science 266:1024-1027. http://dx.doi.org/10.1126/science.7973652.
46. 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. 2009. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326:285-289. http://dx.doi.org/10.1126/science.1178746.
47. Bonsignori M, Hwang K-K, Chen X, Tsao C-Y, 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, Tomaras GD, Alam SM, Liao HX, Haynes BF. 2011. 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. 85:9998-10009. http://dx.doi.org/10.1128/JVI.05045-11.
48. Walker LM, Huber M, Doores KJ, Falkowska E, Pejchal R, Julien J-P, Wang S-K, Ramos A, Chan-Hui PY, Moyle M, Mitcham JL, Hammond PW, Olsen OA, Phung P, Fling S, Wong C-H, Phogat S, Wrin T, Simek MD, Protocol G Principal Investigators, Koff WC, Wilson IA, Burton DR, Poignard P. 2011. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477:466-470. http://dx.doi.org/10.1038/nature10373.
49. Calarese DA, Scanlan CN, Zwick MB, Deechongkit S, Mimura Y, Kunert R, Zhu P, Wormald MR, Stanfield RL, Roux KH, Kelly JW, Rudd PM, Dwek RA, Katinger H, Burton DR, Wilson IA. 2003. Antibody domain exchange is an immunologic solution to carbohydrate cluster recognition. Science 300:2065-2071. http://dx.doi.org/10.1126/science.1083182.
50. Zwick MB, Labrijn AF, Wang M, Spenlehauer C, Saphire EO, Binley JM, Moore JP, Stiegler G, Katinger H, Burton DR, Parren PWHI. 2001. Broadly neutralizing antibodies targeted to the membrane-proximal external region of human immunodeficiency virus type 1 glycoprotein gp41. J. Virol. 75:10892-10905. http://dx.doi.org/10.1128/JVI.75.22.10892-10905.2001.
51. Nyambi PN, Gorny MK, Bastiani L, van der Groen G, Williams C, Zolla-Pazner S. 1998. Mapping of epitopes exposed on intact human immunodeficiency virus type 1 (HIV-1) virions: a new strategy for studying the immunologic relatedness of HIV-1. J. Virol. 72:9384-9391.
52. Jeffs SA, Gorny MK, Williams C, Revesz K, Volsky B, Burda S, Wang XH, Bandres J, Zolla-Pazner S, Holmes H. 2001. Characterization of human monoclonal antibodies selected with a hypervariable loop-deleted recombinant HIV-1(IIIB) gp120. Immunol. Lett. 79:209-213. http://dx.doi.org/10.1016/S0165-2478(01)00289-9.
53. Zolla-Pazner S, O'Leary J, Burda S, Gorny MK, Kim M, Mascola J, McCutchan FE. 1995. Serotyping of primary human immunodeficiency virus type 1 isolates from diverse geographic locations by flow cytometry. J. Virol. 69:3807-3815.
54. Gorny MK, Williams C, Volsky B, Revesz K, Cohen S, Polonis VR, Honnen WJ, Kayman SC, Krachmarov CP, Pinter A, Zolla-Pazner S. 2002. Human monoclonal antibodies specific for conformation-sensitive epitopes ofV3neutralizeHIV-1primary isolates from various clades. J. Virol. 76:9035- 9045. http://dx.doi.org/10.1128/JVI.76.18.9035-9045.2002.
55. Gorny MK, Revesz K, Williams C, Volsky B, Louder MK, Anyangwe CA, Krachmarov CP, Kayman SC, Pinter A, Nadas A, Nyambi PN, Mascola JR, Zolla-Pazner S. 2004. The V3 loop is accessible on the surface of most human immunodeficiency virus type 1 primary isolates and serves as a neutralization epitope. J. Virol. 78:2394-2404. http://dx.doi.org/10.1128/JVI.78.5.2394-2404.2004.
56. Gorny MK, Williams C, Volsky B, Revesz K, Wang XH, Burda S, Kimura T, Koning FA, Nadas A, Anyangwe C, Nyambi P, Krachmarov C, Pinter A, Zolla-Pazner S. 2006. Cross-clade neutralizing activity of human anti-V3 monoclonal antibodies derived from the cells of individuals infected with non-B clades of HIV-1. J. Virol. 80:6865-6872. http://dx.doi.org/10.1128/JVI.02202-05.
57. Gorny MK, Wang XH, Williams C, Volsky B, Revesz K, Witover B, Burda S, Urbanski M, Nyambi P, Krachmarov C, Pinter A, Zolla- Pazner S, Nadas A. 2009. Preferential use of the VH5-51 gene segment by the human immune response to code for antibodies against the V3 domain of HIV-1. Mol. Immunol. 46:917-926. http://dx.doi.org/10.1016/j.molimm.2008.09.005.
58. Gorny MK, Xu J-Y, Karwowska S, Buchbinder A, Zolla-Pazner S. 1993. Repertoire of neutralizing human monoclonal antibodies specific for the V3 domain of HIV-1 gp120. J. Immunol. 150:635-643.
59. Gorny MK, VanCott TC, Hioe C, Israel Z, Michael NL, Conley AJ, Williams C, Kessler JA, II, Chigurupati P, Burda S, Zolla-Pazner S. 1997. Human monoclonal antibodies to the V3 loop of HIV-1 with intraand interclade cross-reactivity. J. Immunol. 159:5114-5122.
60. Gorny MK, VanCott TC, Williams C, Revesz K, Zolla-Pazner S. 2000. Effects of oligomerization on the epitopes of the human immunodeficiency virus type 1 envelope glycoproteins. Virology 267:220-228. http://dx.doi.org/10.1006/viro.1999.0095.
61. Nyambi PN, Mbah HA, Burda S, Williams C, Gorny MK, Nadas A, Zolla-Pazner S. 2000. Conserved and exposed epitopes on intact, native, primary human immunodeficiency virus type 1 virions of group M. J. Virol. 74:7096-7107. http://dx.doi.org/10.1128/JVI.74.15.7096-7107.2000.
62. Gorny MK, Moore JP, Conley AJ, Karwowska S, Sodroski J, Williams C, Burda S, Boots LJ, Zolla-Pazner S. 1994. Human anti-V2 monoclonal antibody that neutralizes primary but not laboratory isolates of HIV-1. J. Virol. 68:8312-8320.
63. Gorny MK, Pan R, Williams C, Wang XH, Volsky B, O'Neal T, Spurrier B, Sampson JM, Li L, Seaman MS, Kong XP, Zolla-Pazner S. 2012. Functional and immunochemical cross-reactivity of V2-specific monoclonal antibodies from human immunodeficiency virus type 1-infected individuals. Virology 427:198-207. http://dx.doi.org/10.1016/j.virol.2012.02.003.
64. Xu J-Y, Gorny MK, Palker T, Karwowska S, Zolla-Pazner S. 1991. Epitope mapping of two immunodominant domains of gp41, the transmembrane protein of human immunodeficiency virus type 1, using ten human monoclonal antibodies. J. Virol. 65:4832-4838.
65. Gorny MK, Gianakakos V, Sharpe S, Zolla-Pazner S. 1989. Generation of human monoclonal antibodies to HIV. Proc. Natl. Acad. Sci. U. S. A. 86:1624-1628. http://dx.doi.org/10.1073/pnas.86.5.1624.
66. Gigler A, Dorsch S, Hemauer A, Williams C, Kim S, Young NS, Zolla-Pazner S, Wolf H, Gorny MK, Modrow S. 1999. Generation of neutralizing human monoclonal antibodies against parvovirus B19 proteins. J. Virol. 73:1974-1979.
67. Edmonds TG, Ding H, Yuan X, Wei Q, Smith KS, Conway JA, Wieczorek L, Brown B, Polonis V, West JT, Montefiori DC, Kappes JC, Ochsenbauer C. 2010. Replication competent molecular clones of HIV-1 expressing Renilla luciferase facilitate the analysis of antibody inhibition in PBMC. Virology 408:1-13. http://dx.doi.org/10.1016/j.virol.2010.08.028.
68. Montefiori DC. 2009. Measuring HIV neutralization in a luciferase reporter gene assay. Methods Mol. Biol. 485:395-405. http://dx.doi.org/10.1007/978-1-59745-170-3_26.
69. McLinden RJ, LaBranche CC, Chenine A-L, Polonis VR, Eller M, Ochsenbauer C, Kappes JC, Perfetto S, Montefiori DC, Michael NL, Kim JH. 2013. Detection of HIV-1 neutralizing antibodies in a human CD4+/CCR5+/CXCR4+T-lymphoblastoid cell assay system. PLoS One 8:e77756. http://dx.doi.org/10.1371/journal.pone.0077756.
70. Sarzotti-Kelsoe M, Bailer RT, Turk E, Lin CL, Bilska M, Greene KM, Gao H, Todd CA, Ozaki DA, Seaman MS, Mascola JR, Montefiori DC. 1 December 2013. Optimization and validation of the TZM-bl assay for standardized assessments of neutralizing antibodies against HIV-1. J. Immunol. Methods http://dx.doi.org/10.1016/j.jim.2013.11.022.
71. Sarzotti-Kelsoe M, Daniell X, Todd CA, Bilska M, Martelli A, LaBranche C, Perez LG, Ochsenbauer C, Kappes JC, Rountree W, Denny TN, Montefiori DC. Optimization and validation of a neutralizing antibody assay for HIV-1 in A3R5 cells. J. Immunol. Methods, in press.
72. Yu X, Gilbert PB, Hioe CE, Zolla-Pazner S, Self SG. 2012. Statistical approaches to analyzing HIV-1 neutralizing antibody assay data. Stat. Biopharm. Res. 4, 1-13, http://dx.doi.org/10.1080/19466315.2011.633860
73. Huang Y, Gilbert PB, Montefiori DC, Self SG. 2009. Simultaneous evaluation of the magnitude and breadth of a left- and right-censored multivariate response, with application to HIV vaccine development. Stat. Biopharm. Res. 1:81-91. http://dx.doi.org/10.1198/sbr.2009.0008.
74. Tibshirani R. 1996. Regression shrinkage and selection via the lasso. J. R. Stat. Soc. Ser. B. 58:267-288.
75. Yuan M, Lin Y. 2006. Model selection and estimation in regression with grouped variables. J. R. Stat. Soc. Ser. B. 68:49-67. http://dx.doi.org/10.1111/j.1467-9868.2005.00532.x.
76. Gottschalk PG, Dunn JR. 2005. The five-parameter logistic: a characterization and comparison with the four-parameter logistic. Anal. Biochem. 343:54-65. http://dx.doi.org/10.1016/j.ab.2005.04.035.
77. Ritz C, Streibig JC. 2005. Bioassay analysis using R. J. Stat. Software 12(5). http://www.jstatsoft.org/v12/i05/paper.
78. West AP, Scharf L, Horwitz J, Klein F, Nussenzweig MC, Bjorkman PJ. 2013. Computational analysis of anti-HIV-1 antibody neutralization panel data to identify potential functional epitope residues. Proc. Natl. Acad. Sci. U. S. A. 110:10598-10603. http://dx.doi.org/10.1073/pnas.1309215110.
79. Balla-Jhagjhoorsingh SS, Corti D, Heyndrickx L, Willems E, Vereecken K, Davis D, Vanham G. 2013. The N276 glycosylation site is required for HIV-1 neutralization by the CD4 binding site specific HJ16 monoclonal antibody. PLoS One 8:e68863. http://dx.doi.org/10.1371/journal.pone.0068863.
80. 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, Sam NE, Haynes BF, Burton DR, Koff WC, Walker LM, Phogat S, Wyatt R, Orwenyo J, Wang LX, Arthos J, Bewley CA, Mascola JR, Nabel GJ, Schief WR, Ward AB, Wilson IA, Kwong PD. 2011. Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9. Nature 480:336-343. http://dx.doi.org/10.1038/nature10696.
81. West AP, Jr, Diskin R, Nussenzweig MC, Bjorkman PJ. 2012. Structural basis for germ-line gene usage of a potent class of antibodies targeting the CD4-binding site of HIV-1 gp120. Proc. Natl. Acad. Sci. U. S. A. 109: E2083-E2090. http://dx.doi.org/10.1073/pnas.1208984109.
82. Li Y, O'Dell S, Walker LM, Wu X, Guenaga J, Feng Y, Schmidt SD, McKee K, Louder MK, Ledgerwood JE, Graham BS, Haynes BF, Burton DR, Wyatt RT, Mascola JR. 2011. Mechanism of neutralization by the broadly neutralizing HIV-1 monoclonal antibody VRC01. J. Virol. 85: 8954-8967. http://dx.doi.org/10.1128/JVI.00754-11.
83. Hraber P, Seaman MS, Bailer RT, Mascola JR, Montefiori DC, Korber BT. 2014. Prevalence of broadly neutralizing antibody responses during chronic HIV-1 infection. AIDS 28:163-169.
84. Binley J, Wrin T, Korber B, Zwick M, Wang M, Chappey C, Stiegler G, Kunert R, Zolla-Pazner S, Katinger H, Petropoulos C, Burton D. 2004. Comprehensive cross-subtype neutralization analysis of a panel of antihuman immunodeficiency virus type 1 monoclonal antibodies. J. Virol. 78:13232-13252. http://dx.doi.org/10.1128/JVI.78.23.13232-13252.2004.
85. Montefiori DC, Karnasuta C, Huang Y, Ahmed H, Gilbert P, de Souza MS, McLinden R, Tovanabutra S, Laurence-Chenine A, Sanders-Buell E, Moody MA, Bonsignori M, Ochsenbauer C, Kappes J, Tang H, Greene K, Gao H, LaBranche CC, Andrews C, Polonis VR, Rerks- Ngarm S, Pitisuttithum P, Nitayaphan S, Kaewkungwal J, Self SG, Berman PW, Francis D, Sinangil F, Lee C, Tartaglia J, Robb ML, Haynes BF, Michael NL, Kim JH. 2012. Magnitude and breadth of the neutralizing antibody response in the RV144 and Vax003 HIV-1 vaccine efficacy trials. J. Infect. Dis. 206:431-441. http://dx.doi.org/10.1093/infdis/jis367.