Envelope variants circulating as initial neutralization breadth developed in two HIV-infected subjects stimulate multiclade neutralizing antibodies in rabbits

Journal of Virology

Volumn 88, Issue 22, 2014, Pages 12949-12967

  Malherbe, Delphine C ^a   Pissani, Franco ^a,b,c   Noah Sather, D ^d   Guo, Biwei ^a   Pandey, Shilpi ^a   Sutton, William F ^a   Stuart, Andrew B ^d   Robins, Harlan ^e   Park, Byung ^a   Krebs, Shelly J ^b,c   Schuman, Jason T ^f   Kalams, Spyros ^g   Hessell, Ann J ^a   Haigwood, Nancy L ^a,h  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b US Military HIV Research Program   (United States)

^c HENRY M JACKSON FOUNDATION FOR THE ADVANCEMENT OF MILITARY MEDICINE   (United States)

^d Seattle BioMed   (United States)

^e Fred Hutchinson Cancer Research Center   (United States)

^f GE Healthcare Life Sciences   (United States)

^g VANDERBILT UNIVERSITY   (United States)

^h OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENVELOPE PROTEIN; GLYCOPROTEIN GP 140; GLYCOPROTEIN GP 160; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG; VC10014 VACCINE; VC20013 VACCINE; VIRUS VACCINE; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; NEUTRALIZING ANTIBODY; VIRUS ENVELOPE PROTEIN; VIRUS RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY AFFINITY; ANTIBODY RESPONSE; ANTIGEN BINDING; ANTIGENICITY; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; ENVELOPE GENE; FEMALE; FTN MOTIF; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOGENICITY; ITN MOTIF; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROTEIN MOTIF; RABBIT; VIRUS NEUTRALIZATION; ANIMAL; BLOOD; DNA SEQUENCE; GENETICS; HUMAN; IMMUNOLOGY; ISOLATION AND PURIFICATION; MOLECULAR GENETICS; VIROLOGY;

AIDS VACCINES; ANIMALS; ANTIBODIES, NEUTRALIZING; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; FEMALE; HIV ANTIBODIES; HIV INFECTIONS; HIV-1; HUMANS; MOLECULAR SEQUENCE DATA; RABBITS; RNA, VIRAL; SEQUENCE ANALYSIS, DNA;

EID: 84908388832     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01812-14     Document Type: Article

References (88)

1. 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, Berman PW, Frahm N, De Rosa SC, Alpert MD, Yates NL, Shen X, Koup RA, Pitisuttithum P, Kaewkungwal J, Nitayaphan S, Rerks-Ngarm S, Michael NL, Kim JH. 2012. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N. Engl. J. Med. 366:1275-1286. http://dx.doi.org/10.1056/NEJMoa1113425.
2. 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, MOPH-TAVEG Investigators. 2009. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med. 361:2209-2220. http://dx.doi.org/10.1056/NEJMoa0908492.
3. Rolland M, Edlefsen PT, Larsen BB, Tovanabutra S, Sanders-Buell E, Hertz T, deCamp 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, deSouza MS, Nitayaphan S, Rerks-Ngarm S, Robb ML, McLellan JS, Georgiev I, Kwong PD, Carlson JM, Michael NL, Schief WR, Gilbert PB, Mullins JI, Kim JH. 2012. Increased HIV-1 vaccine efficacy against viruses with genetic signatures in Env V2. Nature 490:417-420. http://dx.doi.org/10.1038/nature11519.
4. Barouch DH, Whitney JB, Moldt B, Klein F, Oliveira TY, Liu J, Stephenson KE, Chang HW, Shekhar K, Gupta S, Nkolola JP, Seaman MS, Smith KM, Borducchi EN, Cabral C, Smith JY, Blackmore S, Sanisetty S, Perry JR, Beck M, Lewis MG, Rinaldi W, Chakraborty AK, Poignard P, Nussenzweig MC, Burton DR. 2013. Therapeutic efficacy of potent neutralizing HIV-1-specific monoclonal antibodies in SHIVinfected rhesus monkeys. Nature 503:224-228. http://dx.doi.org/10.1038/nature12744.
5. Shingai M, Nishimura Y, Klein F, Mouquet H, Donau OK, Plishka R, Buckler-White A, Seaman M, Piatak M, Jr, Lifson JD, Dimitrov DS, Nussenzweig MC, Martin MA. 2013. Antibody-mediated immunotherapy of macaques chronically infected with SHIV suppresses viraemia. Nature 503:277-280. http://dx.doi.org/10.1038/nature12746.
6. Hessell AJ, Haigwood NL. 2012. Neutralizing antibodies and control of HIV: moves and countermoves. Curr. HIV/AIDS Rep. 9:64-72. http://dx.doi.org/10.1007/s11904-011-0105-5.
7. Lifson JD, Haigwood NL. 2012. Lessons in nonhuman primate models for AIDS vaccine research: from minefields to milestones. Cold Spring Harb. Perspect. Med. 2:a007310. http://dx.doi.org/10.1101/cshperspect.a007310.
8. Stamatatos L, Morris L, Burton DR, Mascola JR. 2009. Neutralizing antibodies generated during natural HIV-1 infection: good news for an HIV-1 vaccine? Nat. Med. 15:866-870. http://dx.doi.org/10.1038/nm.1949.
9. Moore PL, Gray ES, Wibmer CK, Bhiman JN, Nonyane M, Sheward DJ, Hermanus T, Bajimaya S, Tumba NL, Abrahams MR, Lambson BE, Ranchobe N, Ping L, Ngandu N, Abdool Karim Q, Abdool Karim SS, Swanstrom RI, Seaman MS, Williamson C, Morris L. 2012. Evolution of an HIV glycan-dependent broadly neutralizing antibody epitope through immune escape. Nat. Med. 18:1688-1692. http://dx.doi.org/10.1038/nm.2985.
10. Doria-Rose NA, Schramm CA, Gorman J, Moore PL, Bhiman JN, Dekosky BJ, Ernandes MJ, Georgiev IS, Kim HJ, Pancera M, Staupe RP, Altae-Tran HR, Bailer RT, Crooks ET, Cupo A, Druz A, Garrett NJ, Hoi KH, Kong R, Louder MK, Longo NS, McKee K, Nonyane M, O'Dell S, Roark RS, Rudicell RS, Schmidt SD, Sheward DJ, Soto C, Wibmer CK, Yang Y, Zhang Z, NISC Comparative Sequencing Program, Mullikin JC, Binley JM, Sanders RW, Wilson IA, Moore JP, Ward AB, Georgiou G, Williamson C, Abdool Karim SS, Morris L, Kwong PD, Shapiro L, Mascola JR. 2014. Developmental pathway for potent V1V2-directed HIV-neutralizing antibodies. Nature 509:55-62. http://dx.doi.org/10.1038/nature13036.
11. 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.
12. Chakrabarti BK, Feng Y, Sharma SK, McKee K, Karlsson Hedestam GB, Labranche CC, Montefiori DC, Mascola JR, Wyatt RT. 2013. Robust neutralizing antibodies elicited by HIV-1 JRFL envelope glycoprotein trimers in nonhuman primates. J. Virol. 87:13239-13251. http://dx.doi.org/10.1128/JVI.01247-13.
13. Derby NR, Gray S, Wayner E, Campogan D, Vlahogiannis G, Kraft Z, Barnett SW, Srivastava IK, Stamatatos L. 2007. Isolation and characterization of monoclonal antibodies elicited by trimeric HIV-1 Env gp140 protein immunogens. Virology 366:433-445. http://dx.doi.org/10.1016/j.virol.2007.05.020.
14. Morner A, Douagi I, Forsell MN, Sundling C, Dosenovic P, O'Dell S, Dey B, Kwong PD, Voss G, Thorstensson R, Mascola JR, Wyatt RT, Karlsson Hedestam GB. 2009. Human immunodeficiency virus type 1 Env trimer immunization of macaques and impact of priming with viral vector or stabilized core protein. J. Virol. 83:540-551. http://dx.doi.org/10.1128/JVI.01102-08.
15. Zolla-Pazner S, Kong XP, Jiang X, Cardozo T, Nadas A, Cohen S, Totrov M, Seaman MS, Wang S, Lu S. 2011. Cross-clade HIV-1 neutralizing antibodies induced with V3-scaffold protein immunogens following priming with gp120 DNA. J. Virol. 85:9887-9898. http://dx.doi.org/10.1128/JVI.05086-11.
16. Dey AK, Burke B, Sun Y, Hartog K, Heeney JL, Montefiori D, Srivastava IK, Barnett SW. 2012. Use of a polyanionic carbomer, Carbopol971P, in combination with MF59, improves antibody responses to HIV-1 envelope glycoprotein. Vaccine 30:2749-2759. http://dx.doi.org/10.1016/j.vaccine.2012.02.027.
17. Liao HX, Tsao CY, Alam SM, Muldoon M, Vandergrift N, Ma BJ, Lu X, Sutherland LL, Scearce RM, Bowman C, Parks R, Chen H, Blinn JH, Lapedes A, Watson S, Xia SM, Foulger A, Hahn BH, Shaw GM, Swanstrom R, Montefiori DC, Gao F, Haynes BF, Korber B. 2013. Antigenicity and immunogenicity of transmitted/founder, consensus, and chronic envelope glycoproteins of human immunodeficiency virus type 1. J. Virol. 87:4185-4201. http://dx.doi.org/10.1128/JVI.02297-12.
18. Narayan KM, Agrawal N, Du SX, Muranaka JE, Bauer K, Leaman DP, Phung P, Limoli K, Chen H, Boenig RI, Wrin T, Zwick MB, Whalen RG. 2013. Prime-boost immunization of rabbits with HIV-1 gp120 elicits potent neutralization activity against a primary viral isolate. PLoS One 8:e52732. http://dx.doi.org/10.1371/journal.pone.0052732.
19. Carbonetti S, Oliver BG, Glenn J, Stamatatos L, Sather DN. 2014. Soluble HIV-1 envelope immunogens derived from an elite neutralizer elicit cross-reactive V1V2 antibodies and low potency neutralizing antibodies. PLoS One 9:e86905. http://dx.doi.org/10.1371/journal.pone.0086905.
20. Sanders RW, Derking R, Cupo A, Julien JP, Yasmeen A, de Val N, Kim HJ, Blattner C, de la Pena AT, Korzun J, Golabek M, de Los Reyes K, Ketas TJ, van Gils MJ, King CR, Wilson IA, Ward AB, Klasse PJ, Moore JP. 2013. A next-generation cleaved, soluble HIV-1 Env trimer, BG505 SOSIP. 664 gp140, expresses multiple epitopes for broadly neutralizing but not non-neutralizing antibodies. PLoS Pathog. 9:e1003618. http://dx.doi.org/10.1371/journal.ppat.1003618.
21. Liao HX, Lynch R, Zhou T, Gao F, Alam SM, Boyd SD, Fire AZ, Roskin KM, Schramm CA, Zhang Z, Zhu J, Shapiro L, NISC Comparative Sequencing Program, 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.
22. Moir S, Malaspina A, Fauci AS. 2011. Prospects for an HIV vaccine: leading B cells down the right path. Nat. Struct. Mol. Biol. 18:1317-1321. http://dx.doi.org/10.1038/nsmb.2194.
23. Frost SD, Wrin T, Smith DM, Kosakovsky Pond SL, Liu Y, Paxinos E, Chappey C, Galovich J, Beauchaine J, Petropoulos CJ, Little SJ, Richman DD. 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. http://dx.doi.org/10.1073/pnas.0504658102.
24. Mahalanabis M, Jayaraman P, Miura T, Pereyra F, Chester EM, Richardson B, Walker B, Haigwood NL. 2009. Continuous viral escape and selection by autologous neutralizing antibodies in drug-naive human immunodeficiency virus controllers. J. Virol. 83:662-672. http://dx.doi.org/10.1128/JVI.01328-08.
25. Richman DD, Wrin T, Little SJ, Petropoulos CJ. 2003. Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc. Natl. Acad. Sci. U. S. A. 100:4144-4149. http://dx.doi.org/10.1073/pnas.0630530100.
26. Wei X, Decker JM, Wang S, Hui H, Kappes JC, Wu X, Salazar-Gonzalez JF, Salazar MG, Kilby JM, Saag MS, Komarova NL, Nowak MA, Hahn BH, Kwong PD, Shaw GM. 2003. Antibody neutralization and escape by HIV-1. Nature 422:307-312. http://dx.doi.org/10.1038/nature01470.
27. 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.
28. 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.
29. 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, Miiro G, Serwanga J, Pozniak A, McPhee D, Manigart O, Mwananyanda L, Karita E, Inwoley A, Jaoko W, Dehovitz J, Bekker LG, Pitisuttithum P, Paris R, Allen S, 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.
30. 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.
31. Doria-Rose NA, Klein RM, Daniels MG, O'Dell S, Nason M, Lapedes A, Bhattacharya T, Migueles SA, Wyatt RT, Korber BT, Mascola JR, Connors M. 2010. Breadth of human immunodeficiency virus-specific neutralizing activity in sera: clustering analysis and association with clinical variables. J. Virol. 84:1631-1636. http://dx.doi.org/10.1128/JVI.01482-09.
32. Mikell I, Sather DN, Kalams SA, Altfeld M, Alter G, Stamatatos L. 2011. Characteristics of the earliest cross-neutralizing antibody response to HIV-1. PLoS Pathog. 7:e1001251. http://dx.doi.org/10.1371/journal.ppat.1001251.
33. Sather DN, Armann J, Ching LK, Mavrantoni A, Sellhorn G, Caldwell Z, Yu X, Wood B, Self S, Kalams S, Stamatatos L. 2009. Factors associated with the development of cross-reactive neutralizing antibodies during human immunodeficiency virus type 1 infection. J. Virol. 83:757-769. http://dx.doi.org/10.1128/JVI.02036-08.
34. Wibmer CK, Bhiman JN, Gray ES, Tumba N, Abdool Karim SS, Williamson C, Morris L, Moore PL. 2013. Viral escape from HIV-1 neutralizing antibodies drives increased plasma neutralization breadth through sequential recognition of multiple epitopes and immunotypes. PLoS Pathog. 9:e1003738. http://dx.doi.org/10.1371/journal.ppat.1003738.
35. Blish CA, Sather DN, Sellhorn G, Stamatatos L, Sun Y, Srivastava I, Barnett SW, Cleveland B, Overbaugh J, Hu SL. 2010. Comparative immunogenicity of subtype A human immunodeficiency virus type 1 envelope exhibiting differential exposure of conserved neutralization epitopes. J. Virol. 84:2573-2584. http://dx.doi.org/10.1128/JVI.01687-09.
36. Kraft Z, Strouss K, Sutton WF, Cleveland B, Tso FY, Polacino P, Overbaugh J, Hu SL, Stamatatos L. 2008. Characterization of neutralizing antibody responses elicited by clade A envelope immunogens derived from early transmitted viruses. J. Virol. 82:5912-5921. http://dx.doi.org/10.1128/JVI.00389-08.
37. Mikell I, Stamatatos L. 2012. Evolution of cross-neutralizing antibody specificities to the CD4-BS and the carbohydrate cloak of the HIV Env in an HIV-1-infected subject. PLoS One 7:e49610. http://dx.doi.org/10.1371/journal.pone.0049610.
38. Moore PL, Sheward D, Nonyane M, Ranchobe N, Hermanus T, Gray ES, Abdool Karim SS, Williamson C, Morris L. 2013. Multiple pathways of escape from HIV broadly cross-neutralizing V2-dependent antibodies. J. Virol. 87:4882-4894. http://dx.doi.org/10.1128/JVI.03424-12.
39. Binley JM, Lybarger EA, Crooks ET, Seaman MS, Gray E, Davis KL, Decker JM, Wycuff D, Harris L, Hawkins N, Wood B, Nathe C, Richman D, Tomaras GD, Bibollet-Ruche F, Robinson JE, Morris L, Shaw GM, Montefiori DC, Mascola JR. 2008. Profiling the specificity of neutralizing antibodies in a large panel of plasmas from patients chronically infected with human immunodeficiency virus type 1 subtypes B and C. J. Virol. 82:11651-11668. http://dx.doi.org/10.1128/JVI.01762-08.
40. Li Y, Svehla K, Louder MK, Wycuff D, Phogat S, Tang M, Migueles SA, Wu X, Phogat A, Shaw GM, Connors M, Hoxie J, Mascola JR, Wyatt R. 2009. Analysis of neutralization specificities in polyclonal sera derived from human immunodeficiency virus type 1-infected individuals. J. Virol. 83:1045-1059. http://dx.doi.org/10.1128/JVI.01992-08.
41. Lynch RM, Tran L, Louder MK, Schmidt SD, Cohen M, Dersimonian R, Euler Z, Gray ES, Abdool Karim S, Kirchherr J, Montefiori DC, Sibeko S, Soderberg K, Tomaras G, Yang ZY, Nabel GJ, Schuitemaker H, Morris L, Haynes BF, Mascola JR. 2012. The development of CD4 binding site antibodies during HIV-1 infection. J. Virol. 86:7588-7595. http://dx.doi.org/10.1128/JVI.00734-12.
42. 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, 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.
43. Klein F, Mouquet H, Dosenovic P, Scheid JF, Scharf L, Nussenzweig MC. 2013. Antibodies in HIV-1 vaccine development and therapy. Science 341:1199-1204. http://dx.doi.org/10.1126/science.1241144.
44. 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. http://dx.doi.org/10.1097/QAD.0000000000000106.
45. Doria-Rose NA, Klein RM, Manion MM, O'Dell S, Phogat A, Chakrabarti B, Hallahan CW, Migueles SA, Wrammert J, Ahmed R, Nason M, Wyatt RT, Mascola JR, Connors M. 2009. Frequency and phenotype of human immunodeficiency virus envelope-specific B cells from patients with broadly cross-neutralizing antibodies. J. Virol. 83:188-199. http://dx.doi.org/10.1128/JVI.01583-08.
46. 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. 2009. Broad diversity of neutralizing antibodies isolated from memory B cells in HIV-infected individuals. Nature 458:636-640. http://dx.doi.org/10.1038/nature07930.
47. Malherbe DC, Doria-Rose NA, Misher L, Beckett T, Puryear WB, Schuman JT, Kraft Z, O'Malley J, Mori M, Srivastava I, Barnett S, Stamatatos L, Haigwood NL. 2011. Sequential immunization with a subtype B HIV-1 envelope quasispecies partially mimics the in vivo development of neutralizing antibodies. J. Virol. 85:5262-5274. http://dx.doi.org/10.1128/JVI.02419-10.
48. Pissani F, Malherbe DC, Robins H, DeFilippis VR, Park B, Sellhorn G, Stamatatos L, Overbaugh J, Haigwood NL. 2012. Motif-optimized subtype A HIV envelope-based DNA vaccines rapidly elicit neutralizing antibodies when delivered sequentially. Vaccine 30:5519-5526. http://dx.doi.org/10.1016/j.vaccine.2012.06.042.
49. Jaworski JP, Krebs SJ, Trovato M, Kovarik DN, Brower Z, Sutton WF, Waagmeester G, Sartorius R, D'Apice L, Caivano A, Doria-Rose NA, Malherbe D, Montefiori DC, Barnett S, De Berardinis P, Haigwood NL. 2012. Co-immunization with multimeric scaffolds and DNA rapidly induces potent autologous HIV-1 neutralizing antibodies and CD8+T cells. PLoS One 7:e31464. http://dx.doi.org/10.1371/journal.pone.0031464.
50. Pissani F, Malherbe DC, Schuman JT, Robins H, Park BS, Krebs SJ, Barnett SW, Haigwood NL. 2014. Improvement of antibody responses by HIV envelope DNA and protein co-immunization. Vaccine 32:507-513. http://dx.doi.org/10.1016/j.vaccine.2013.11.022.
51. Sather DN, Carbonetti S, Malherbe D, Pissani F, Stuart AB, Hessell AJ, Gray MD, Mikell I, Kalams SA, Haigwood NL, Stamatatos L. 2014. Emergence of broadly neutralizing antibodies and viral coevolution in two subjects during the early stages of infection with human immunodeficiency virus type 1. J. Virol. 88:12968-12981. http://dx.doi.org/10.1128/JVI.01816-14.
52. Salazar-Gonzalez JF, Bailes E, Pham KT, Salazar MG, Guffey MB, Keele BF, Derdeyn CA, Farmer P, Hunter E, Allen S, Manigart O, Mulenga J, Anderson JA, Swanstrom R, Haynes BF, Athreya GS, Korber BT, Sharp PM, Shaw GM, Hahn BH. 2008. Deciphering human immunodeficiency virus type 1 transmission and early envelope diversification by singlegenome amplification and sequencing. J. Virol. 82:3952-3970. http://dx.doi.org/10.1128/JVI.02660-07.
53. Robins H, Krasnitz M, Barak H, Levine AJ. 2005. A relative-entropy algorithm for genomic fingerprinting captures host-phage similarities. J. Bacteriol. 187:8370-8374. http://dx.doi.org/10.1128/JB.187.24.8370-8374.2005.
54. Srivastava IK, Stamatatos L, Kan E, Vajdy M, Lian Y, Hilt S, Martin L, Vita C, Zhu P, Roux KH, Vojtech L, Montefiori DC, Donnelly J, Ulmer JB, Barnett SW. 2003. Purification, characterization, and immunogenicity of a soluble trimeric envelope protein containing a partial deletion of the V2 loop derived from SF162, an R5-tropic human immunodeficiency virus type 1 isolate. J. Virol. 77:11244-11259. http://dx.doi.org/10.1128/JVI.77.20.11244-11259.2003.
55. Sellhorn G, Caldwell Z, Mineart C, Stamatatos L. 2009. Improving the expression of recombinant soluble HIV envelope glycoproteins using pseudo-stable transient transfection. Vaccine 28:430-436. http://dx.doi.org/10.1016/j.vaccine.2009.10.028.
56. Zolla-Pazner S, deCamp AC, Cardozo T, Karasavvas N, Gottardo R, Williams C, Morris DE, Tomaras G, Rao M, Billings E, Berman P, Shen X, Andrews C, O'Connell RJ, Ngauy V, Nitayaphan S, de Souza M, Korber B, Koup R, Bailer RT, Mascola JR, Pinter A, Montefiori D, Haynes BF, Robb ML, Rerks-Ngarm S, Michael NL, Gilbert PB, Kim JH. 2013. Analysis of V2 antibody responses induced in vaccinees in the ALVAC/AIDSVAX HIV-1 vaccine efficacy trial. PLoS One 8:e53629. http://dx.doi.org/10.1371/journal.pone.0053629.
57. Krebs SJ, McBurney SP, Kovarik DN, Waddell CD, Jaworski JP, Sutton WF, Gomes MM, Trovato M, Waagmeester G, Barnett SJ, De Berardinis P, Haigwood NL. Multimeric scaffolds displaying the HIV-1 envelope MPER induce MPER-specific antibodies and cross-neutralizing antibodies when co-immunized with gp160 DNA. PLoS One, in press.
58. Azzoni L, Foulkes AS, Papasavvas E, Mexas AM, Lynn KM, Mounzer K, Tebas P, Jacobson JM, Frank I, Busch MP, Deeks SG, Carrington M, O'Doherty U, Kostman J, Montaner LJ. 2013. Pegylated interferon alfa-2a monotherapy results in suppression of HIV type 1 replication and decreased cell-associated HIV DNA integration. J. Infect. Dis. 207:213-222. http://dx.doi.org/10.1093/infdis/jis663.
59. Blay WM, Gnanakaran S, Foley B, Doria-Rose NA, Korber BT, Haigwood NL. 2006. Consistent patterns of change during the divergence of human immunodeficiency virus type 1 envelope from that of the inoculated virus in simian/human immunodeficiency virus-infected macaques. J. Virol. 80:999-1014. http://dx.doi.org/10.1128/JVI.80.2.999-1014.2006.
60. 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. http://dx.doi.org/10.1128/JVI.00141-06.
61. Overbaugh J, Rudensey LM. 1992. Alterations in potential sites for glycosylation predominate during evolution of the simian immunodeficiency virus envelope gene in macaques. J. Virol. 66:5937-5948.
62. Moore PL, Ranchobe N, Lambson BE, Gray ES, Cave E, Abrahams MR, Bandawe G, Mlisana K, Abdool Karim SS, Williamson C, Morris L, CAPRISA002 Study, NIAID Center for HIV/AIDS Vaccine Immunology (CHAVI). 2009. Limited neutralizing antibody specificities drive neutralization escape in early HIV-1 subtype C infection. PLoS Pathog. 5:e1000598. http://dx.doi.org/10.1371/journal.ppat.1000598.
63. Gray ES, Madiga MC, Hermanus T, Moore PL, Wibmer CK, Tumba NL, Werner L, Mlisana K, Sibeko S, Williamson C, Abdool Karim SS, Morris L, CAPRISA002 Study Team. 2011. The neutralization breadth of HIV-1 develops incrementally over four years and is associated with CD4+ T cell decline and high viral load during acute infection. J. Virol. 85:4828-4840. http://dx.doi.org/10.1128/JVI.00198-11.
64. Scanlan CN, Pantophlet R, Wormald MR, Ollmann Saphire E, Stanfield R, Wilson IA, Katinger H, Dwek RA, Rudd PM, Burton DR. 2002. The broadly neutralizing anti-human immunodeficiency virus type 1 antibody 2G12 recognizes a cluster of alpha1→2 mannose residues on the outer face of gp120. J. Virol. 76:7306-7321. http://dx.doi.org/10.1128/JVI.76.14.7306-7321.2002.
65. Trkola A, Purtscher M, Muster T, Ballaun C, Buchacher A, Sullivan N, Srinivasan K, Sodroski J, Moore JP, Katinger H. 1996. Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1. J. Virol. 70:1100-1108.
66. van den Kerkhof TL, Feenstra KA, Euler Z, van Gils MJ, Rijsdijk LW, Boeser-Nunnink BD, Heringa J, Schuitemaker H, Sanders RW. 2013. HIV-1 envelope glycoprotein signatures that correlate with the development of cross-reactive neutralizing activity. Retrovirology 10:102. http://dx.doi.org/10.1186/1742-4690-10-102.
67. Gnanakaran S, Daniels MG, Bhattacharya T, Lapedes AS, Sethi A, Li M, Tang H, Greene K, Gao H, Haynes BF, Cohen MS, Shaw GM, Seaman MS, Kumar A, Gao F, Montefiori DC, Korber B. 2010. Genetic signatures in the envelope glycoproteins of HIV-1 that associate with broadly neutralizing antibodies. PLoS Comput. Biol. 6:e1000955. http://dx.doi.org/10.1371/journal.pcbi.1000955.
68. Burton DR, Hessell AJ, Keele BF, Klasse PJ, Ketas TA, Moldt B, Dunlop DC, Poignard P, Doyle LA, Cavacini L, Veazey RS, Moore JP. 2011. Limited or no protection by weakly or nonneutralizing antibodies against vaginal SHIV challenge of macaques compared with a strongly neutralizing antibody. Proc. Natl. Acad. Sci. U. S. A. 108:11181-11186. http://dx.doi.org/10.1073/pnas.1103012108.
69. Nkolola JP, Bricault CA, Cheung A, Shields J, Perry J, Kovacs JM, Giorgi E, van Winsen M, Apetri A, Brinkman-van der Linden EC, Chen B, Korber B, Seaman MS, Barouch DH. 2014. Characterization and immunogenicity of a novel mosaic M HIV-1 gp140 trimer. J. Virol. 88: 9538-9552. http://dx.doi.org/10.1128/JVI.01739-14.
70. Sundling C, Forsell MN, O'Dell S, Feng Y, Chakrabarti B, Rao SS, Lore K, Mascola JR, Wyatt RT, Douagi I, Karlsson Hedestam GB. 2010. Soluble HIV-1 Env trimers in adjuvant elicit potent and diverse functional B cell responses in primates. J. Exp. Med. 207:2003-2017. http://dx.doi.org/10.1084/jem.20100025.
71. Zhao J, Lai L, Amara RR, Montefiori DC, Villinger F, Chennareddi L, Wyatt LS, Moss B, Robinson HL. 2009. Preclinical studies of human immunodeficiency virus/AIDS vaccines: inverse correlation between avidity of anti-Env antibodies and peak postchallenge viremia. J. Virol. 83:4102-4111. http://dx.doi.org/10.1128/JVI.02173-08.
72. Piantadosi A, Panteleeff D, Blish CA, Baeten JM, Jaoko W, McClelland RS, Overbaugh J. 2009. Breadth of neutralizing antibody response to human immunodeficiency virus type 1 is affected by factors early in infection but does not influence disease progression. J. Virol. 83:10269-10274. http://dx.doi.org/10.1128/JVI.01149-09.
73. Hoxie JA. 2010. Toward an antibody-based HIV-1 vaccine. Annu. Rev. Med. 61:135-152. http://dx.doi.org/10.1146/annurev.med.60.042507.164323.
74. Van Regenmortel MH. 2011. Limitations to the structure-based design of HIV-1 vaccine immunogens. J. Mol. Recognit. 24:741-753. http://dx.doi.org/10.1002/jmr.1116.
75. Van Regenmortel MH. 2012. Requirements for empirical immunogenicity trials, rather than structure-based design, for developing an effective HIV vaccine. Arch. Virol. 157:1-20. http://dx.doi.org/10.1007/s00705-011-1145-2.
76. Davenport TM, Friend D, Ellingson K, Xu H, Caldwell Z, Sellhorn G, Kraft Z, Strong RK, Stamatatos L. 2011. Binding interactions between soluble HIV envelope glycoproteins and quaternary-structure-specific monoclonal antibodies PG9 and PG16. J. Virol. 85:7095-7107. http://dx.doi.org/10.1128/JVI.00411-11.
77. Phogat S, Wyatt R. 2007. Rational modifications of HIV-1 envelope glycoproteins for immunogen design. Curr. Pharm. Des. 13:213-227. http://dx.doi.org/10.2174/138161207779313632.
78. Hoot S, McGuire AT, Cohen KW, Strong RK, Hangartner L, Klein F, Diskin R, Scheid JF, Sather DN, Burton DR, Stamatatos L. 2013. Recombinant HIV envelope proteins fail to engage germline versions of anti-CD4bs bNAbs. PLoS Pathog. 9:e1003106. http://dx.doi.org/10.1371/journal.ppat.1003106.
79. McGuire AT, Hoot S, Dreyer AM, Lippy A, Stuart A, Cohen KW, Jardine J, Menis S, Scheid JF, West AP, Schief WR, Stamatatos L. 2013. Engineering HIV envelope protein to activate germline B cell receptors of broadly neutralizing anti-CD4 binding site antibodies. J. Exp. Med. 210: 655-663. http://dx.doi.org/10.1084/jem.20122824.
80. Chan KH, To KK, Hung IF, Zhang AJ, Chan JF, Cheng VC, Tse H, Che XY, Chen H, Yuen KY. 2011. Differences in antibody responses of individuals with natural infection and those vaccinated against pandemic H1N1 2009 influenza. Clin. Vaccine Immunol. 18:867-873. http://dx.doi.org/10.1128/CVI.00555-10.
81. Forsell MN, Dey B, Morner A, Svehla K, O'Dell S, Hogerkorp CM, Voss G, Thorstensson R, Shaw GM, Mascola JR, Karlsson Hedestam GB, Wyatt RT. 2008. B cell recognition of the conserved HIV-1 co-receptor binding site is altered by endogenous primate CD4. PLoS Pathog. 4:e1000171. http://dx.doi.org/10.1371/journal.ppat.1000171.
82. 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.
83. Jalah R, Kulkarni V, Patel V, Rosati M, Alicea C, Bear J, Yu L, Guan Y, Shen X, Tomaras GD, LaBranche C, Montefiori DC, Prattipati R, Pinter A, Bess J, Jr, Lifson JD, Reed SG, Sardesai NY, Venzon DJ, Valentin A, Pavlakis GN, Felber BK. 2014. DNA and protein co-immunization improves the magnitude and longevity of humoral immune responses in macaques. PLoS One 9:e91550. http://dx.doi.org/10.1371/journal.pone.0091550.
84. Li J, Valentin A, Kulkarni V, Rosati M, Beach RK, Alicea C, Hannaman D, Reed SG, Felber BK, Pavlakis GN. 2013. HIV/SIV DNA vaccine combined with protein in a co-immunization protocol elicits highest humoral responses to envelope in mice and macaques. Vaccine 31:3747-3755. http://dx.doi.org/10.1016/j.vaccine.2013.04.037.
85. Konishi E, Terazawa A, Imoto J. 2003. Simultaneous immunization with DNA and protein vaccines against Japanese encephalitis or dengue synergistically increases their own abilities to induce neutralizing antibody in mice. Vaccine 21:1826-1832. http://dx.doi.org/10.1016/S0264-410X (03)00028-8.
86. Sundling C, Li Y, Huynh N, Poulsen C, Wilson R, O'Dell S, Feng Y, Mascola JR, Wyatt RT, Karlsson Hedestam GB. 2012. High-resolution definition of vaccine-elicited B cell responses against the HIV primary receptor binding site. Sci. Transl. Med. 4:142ra96. http://dx.doi.org/10.1126/scitranslmed.3003752.
87. 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.
88. Georgiev IS, Doria-Rose NA, Zhou T, Kwon YD, Staupe RP, Moquin S, Chuang GY, Louder MK, Schmidt SD, Altae-Tran HR, Bailer RT, McKee K, Nason M, O'Dell S, Ofek G, Pancera M, Srivatsan S, Shapiro L, Connors M, Migueles SA, Morris L, Nishimura Y, Martin MA, Mascola JR, Kwong PD. 2013. Delineating antibody recognition in polyclonal sera from patterns of HIV-1 isolate neutralization. Science 340: 751-756. http://dx.doi.org/10.1126/science.1233989.