Rhesus macaque B-cell responses to an HIV-1 trimer vaccine revealed by unbiased longitudinal repertoire analysis

mBio

Volumn 6, Issue 6, 2015, Pages

  Dai, Kaifan ^a   He, Linling ^a   Khan, Salar N ^a   O’Dell, Sijy ^b   McKee, Krisha ^b   Tran, Karen ^a   Li, Yuxing ^c   Sundling, Christopher ^d   Morris, Charles D ^a   Mascola, John R ^b   Hedestam, Gunilla B Karlsson ^d   Wyatt, Richard T ^a   Zhu, Jiang ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

^d KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; HUMAN IMMUNODEFICIENCY VIRUS 1 TRIMER VACCINE; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; BINDING SITE; CELL SELECTION; CELLULAR IMMUNITY; CONTROLLED STUDY; DRUG SCREENING; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNIZATION; LONGITUDINAL STUDY; NEXT GENERATION SEQUENCING; NONHUMAN; PRIMATE MODEL; PRIORITY JOURNAL; PYROSEQUENCING; RHESUS MONKEY; ANIMAL; ANTIBODY COMBINING SITE; BIOLOGY; CELL LINEAGE; CLASSIFICATION; DNA SEQUENCE; GENETIC DATABASE; GENETICS; HIGH THROUGHPUT SEQUENCING; HIV INFECTIONS; HUMAN; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; VACCINATION; VIROLOGY;

AIDS VACCINES; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; B-LYMPHOCYTES; BINDING SITES, ANTIBODY; CELL LINEAGE; COMPUTATIONAL BIOLOGY; DATABASES, GENETIC; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HIV ANTIBODIES; HIV INFECTIONS; HIV-1; HUMANS; IMMUNOLOGIC MEMORY; MACACA MULATTA; SEQUENCE ANALYSIS, DNA; VACCINATION;

EID: 84952803194     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01375-15     Document Type: Article

References (55)

1. Walker LM, Burton DR. 2010. Rational antibody-based HIV-1 vaccine design: current approaches and future directions. Curr Opin Immunol 22:358-366. http://dx.doi.org/10.1016/j.coi.2010.02.012.
2. Haynes BF, Kelsoe G, Harrison SC, Kepler TB. 2012. B-cell-lineage immunogen design in vaccine development with HIV-1 as a case study. Nat Biotechnol 30:423-433. http://dx.doi.org/10.1038/nbt.2197.
3. Burton D, Ahmed R, Barouch D, Butera S, Crotty S, Godzik A, Kaufmann D, McElrath M, Nussenzweig M, Pulendran B, Scanlan C, Schief W, Silvestri G, Streeck H, Walker B, Walker L, Ward A, Wilson I, 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.
4. 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 Z, 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, Mullikin JC, Nabel GJ, Roederer M, Shapiro L, Kwong PD, Mascola JR, Progra NCS. 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.
5. Walker LM, Huber M, Doores KJ, Falkowska E, Pejchal R, Julien J-P, Wang S-K, Ramos A, Chan-Hui P-Y, Moyle M, Mitcham JL, Hammond PW, Olsen OA, Pham P, Fling S, Wong C-H, Phogat S, Wrin T, Simek MD, Koff WC, Wilson IA, Burton DR, Poignard P, Protocol GPI. 2011. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477:466-470.
6. Walker LM, Phogat SK, Chan-Hui P-Y, 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, Protocol GPI. 2009. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326:285-289.
7. Wu X, Yang Z-Y, Li Y, Hogerkorp C-M, 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.
8. Huang J, Ofek G, Laub L, Louder MK, Doria-Rose NA, Longo NS, Imamichi H, Bailer RT, Chakrabarti B, Sharma SK, Alam SM, Wang T, Yang Y, Zhang B, Migueles SA, Wyatt R, Haynes BF, Kwong PD, Mascola JR, ConnorsM. 2012. Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature 491:406-412. http:// dx.doi.org/10.1038/nature11544.
9. Falkowska E, Le K, Ramos A, Doores K, Lee J, Blattner C, Ramirez A, Derking R, van Gils M, Liang C, McBride R, von Bredow B, Shivatare S, Wu C, Chan-Hui P, Liu Y, Feizi T, Zwick M, Koff W, Seaman M, Swiderek K, Moore JP, Evans D, Paulson JC, Wong C-H, Ward AB, Wilson IA, Sanders RW, Poignard P, Burton DR. 2014. Broadly neutralizing HIV antibodies define a glycan-dependent epitope on the prefusion conformation of gp41 on cleaved envelope trimers. Immunity 40: 657-668. http://dx.doi.org/10.1016/j.immuni.2014.04.009.
10. Zhou T, Zhu J, Wu X, Moquin S, Zhang B, Acharya P, Georgiev I, Altae-Tran H, Chuang G, Joyce M, Do Kwon Y, Longo N, Louder M, Luongo T, McKee K, Schramm C, Skinner J, Yang Y, Yang Z, Zhang Z, Zheng A, Bonsignori M, Haynes BF, Scheid JF, Nussenzweig MC, Simek M, Burton DR, Koff WC, Mullikin JC, Connors M, Shapiro L, Nabel GJ, Mascola JR, Kwong PD, Program NCS. 2013. Multidonor analysis reveals structural elements, genetic determinants, and maturation pathway for HIV-1 neutralization by VRC01-class antibodies. Immunity 39:245-258. http://dx.doi.org/10.1016/j.immuni.2013.04.012.
11. 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, Sequencing NC, 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.
12. Huang J, Kang BH, Pancera M, Lee JH, Tong T, Feng Y, Imamichi H, Georgiev IS, Chuang G, Druz A, Doria-Rose NA, Laub L, Sliepen K, van Gils MJ, de la Peña AT, Derking R, Klasse P, Migueles SA, Bailer RT, Alam M, Pugach P, Haynes BF, Wyatt RT, Sanders RW, Binley JM, Ward AB, Mascola JR, Kwong PD, Connors M. 2014. Broad and potent HIV-1 neutralization by a human antibody that binds the gp41-gp120 interface. Nature 515:138-142. http://dx.doi.org/10.1038/nature13601.
13. Scheid JF, Mouquet H, Ueberheide B, Diskin R, Klein F, Oliveira TYK, Pietzsch J, Fenyo D, Abadir A, Velinzon K, Hurley A, Myung S, Boulad F, Poignard P, Burton DR, Pereyra F, Ho DD, Walker BD, Seaman MS, Bjorkman PJ, Chait BT, Nussenzweig MC. 2011. Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science 333:1633-1637. http://dx.doi.org/10.1126/science.1207227.
14. Liao H, Lynch R, Zhou T, Gao F, Alam SM, Boyd SD, Fire AZ, Roskin KM, Schramm CA, Zhang Z, Zhu J, Shapiro L, Mullikin J, Gnanakaran S, Hraber P, Wiehe K, Kelsoe G, Yang G, Xia S-M, 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 BTM, Kwong PD, Mascola JR, Haynes BF, NISC Comparative Sequencing Program. 2013. Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature 496:469-476. http://dx.doi.org/ 10.1038/nature12053.
15. Sok D, van Gils MJ, Pauthner M, Julien J, Saye-Francisco KL, Hsueh J, Briney B, Lee JH, Le KM, Lee PS, Hua Y, Seaman MS, Moore JP, Ward AB, Wilson IA, Sanders RW, Burton DR. 2014. Recombinant HIV envelope trimer selects for quaternary-dependent antibodies targeting the trimer apex. Proc Natl Acad Sci U S A 111:17624-17629. http:// dx.doi.org/10.1073/pnas.1415789111.
16. Kwong PD, Mascola JR, Nabel GJ. 2013. Broadly neutralizing antibodies and the search for an HIV-1 vaccine: the end of the beginning. Nat Rev Immunol 13:693-701. http://dx.doi.org/10.1038/nri3516.
17. Kwong P, Mascola J. 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.
18. 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.
19. Zhu J, Wu X, Zhang B, McKee K, O'Dell S, Soto C, Zhou T, Casazza JP, Mullikin JC, Kwong PD, Mascola JR, Shapiro L, NISC Comparative Sequencing Program. 2013. De novo identification of VRC01 class HIV-1-neutralizing antibodies by next-generation sequencing of B-cell transcripts. Proc Natl Acad Sci U S A 110:E4088-E4097. http://dx.doi.org/ 10.1073/pnas.1306262110.
20. Zhu J, Ofek G, Yang Y, Zhang B, Louder MK, Lu G, McKee K, Pancera M, Skinner J, Zhang Z, Parks R, Eudailey J, Lloyd KE, Blinn J, Alam SM, Haynes BF, Simek M, Burton DR, Koff WC, Mullikin JC, Mascola JR, Shapiro L, Kwong PD, Progra NCS. 2013. Mining the antibodyome for HIV-1-neutralizing antibodies with next-generation sequencing and phylogenetic pairing of heavy/light chains. Proc Natl Acad Sci U S A 110: 6470-6475. http://dx.doi.org/10.1073/pnas.1219320110.
21. Zhu J, O'Dell S, Ofek G, Pancera M, Wu X, Zhang B, Zhang Z, Mullikin JC, Simek M, Burton DR, Koff WC, Shapiro L, Mascola JR, Kwong PD, NISC Comparative Sequencing Program. 2012. Somatic populations of PGT135-137 HIV-1-neutralizing antibodies identified by 454 pyrosequencing and bioinfornnatics. Front Microbiol 3:315.
22. Sok D, Laserson U, Laserson J, Liu Y, Vigneault F, Julien J, Briney B, Ramos A, Saye KF, Le K, Mahan A, Wang S, Kardar M, Yaari G, Walker LM, Simen BB, John EP, Chan-Hui P, Swiderek K, Kleinstein SH, Alter G, Seaman MS, Chakraborty AK, Koller D, Wilson IA, Church GM, Burton DR, Poignard P. 2013. The effects of somatic hypermutation on neutralization and binding in the PGT121 family of broadly neutralizing HIV antibodies. PLoS Pathog 9:e1003754. http://dx.doi.org/10.1371/ journal.ppat.1003754.
23. Wu X, Zhang Z, Schramm C, Joyce M, Do Kwon Y, Zhou T, Sheng Z, Zhang B, O'Dell S, McKee K, Georgiev I, Chuang G, Longo N, Lynch R, Saunders K, Soto C, Srivatsan S, Yang Y, Bailer R, Louder M, Mullikin JC, Connors M, Kwong PD, Mascola JR, Shapiro L, Program NCS. 2015. Maturation and diversity of the VRC01-antibody lineage over 15 years of chronic HIV-1 infection. Cell 161:470-485. http://dx.doi.org/ 10.1016/j.cell.2015.03.004.
24. Hatziioannou T, Evans DT. 2012. Animal models for HIV/AIDS research. Nat Rev Microbiol 10:852-867. http://dx.doi.org/10.1038/ nrmicro2911.
25. Ambrose Z, KewalRamani VN, Bieniasz PD, Hatziioannou T. 2007. HIV/AIDS: in search of an animal model. Trends Biotechnol 25:333-337. http://dx.doi.org/10.1016/j.tibtech.2007.05.004.
26. Sui Y, Gordon S, Franchini G, Berzofsky JA. 2013. Nonhuman primate models for HIV/AIDS vaccine development. Curr Protoc Immunol 102. 12/14/11 12:14.30.
27. Joag SV. 2000. Primate models of AIDS. Microb Infect 2:223-229.
28. Nath BM, Schumann KE, Boyer JD. 2000. The chimpanzee and other non-human-primate models in HIV-1 vaccine research. Trends Microbiol 8:426-431. http://dx.doi.org/10.1016/S0966-842X(00)01816-3.
29. Morgan C, Marthas M, Miller C, Duerr A, Cheng-Mayer C, Desrosiers R, Flores J, Haigwood N, Hu S, Johnson RP, Lifson J, Montefiori D, Moore J, Robert-Guroff M, Robinson H, Self S, Corey L. 2008. The use of nonhuman primate models in HIV vaccine development. PLoS Med 5:1200-1204. http://dx.doi.org/10.1371/journal.pmed.0050173.
30. Sundling C, Forsell MNE, O'Dell S, Feng Y, Chakrabarti B, Rao SS, Lore K, Mascola JR, Wyatt RT, Douagi I, 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.
31. Sundling C, Phad G, Douagi I, Navis M, Hedestam GB. 2012. Isolation of antibody V(D)J sequences from single cell sorted rhesus macaque B cells. J Immunol Methods 386:85-93. http://dx.doi.org/10.1016/ j.jim.2012.09.003.
32. Sundling C, Li Y, Huynh N, Poulsen C, Wilson R, O'Dell S, Feng Y, Mascola JR, Wyatt RT, Hedestam GB. 2012. High-resolution definition of vaccine-elicited B cell responses against the HIV primary receptor binding site. Sci Transl Med 4:142ra196. http://dx.doi.org/10.1126/ scitranslmed.3003752.
33. Zhou T, Georgiev I, Wu X, Yang Z-Y, Dai K, Finzi A, Do Kwon Y, 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.
34. Sundling C, Zhang Z, Phad GE, Sheng Z, Wang Y, Mascola JR, Li Y, Wyatt RT, Shapiro L, Hedestam GB. 2014. Single-cell and deep sequencing of IgG-switched macaque B cells reveal a diverse Ig repertoire following immunization. J Immunol 192:3637-3644. http://dx.doi.org/10.4049/ jimmunol.1303334.
35. Guo K, Halemano K, Schmitt K, Katuwal M, Wang Y, Harper MS, Heilman KJ, Kuwata T, Stephens EB, Santiago ML. 2015. Immunoglobulin V-H gene diversity and somatic hypermutation during SIV infection of rhesus macaques. Immunogenetics 67:355-370. http://dx.doi.org/ 10.1007/s00251-015-0844-3.
36. Julien J-P, Cupo A, Sok D, Stanfield RL, Lyumkis D, Deller MC, Klasse P-J, Burton DR, Sanders RW, Moore JP, Ward AB, Wilson IA. 2013. Crystal structure of a soluble cleaved HIV-1 envelope trimer. Science 342: 1477-1483. http://dx.doi.org/10.1126/science.1245625.
37. Lyumkis D, Julien J-P, de Val N, Cupo A, Potter CS, Klasse P-J, Burton DR, Sanders RW, Moore JP, Carragher B, Wilson IA, Ward AB. 2013. Cryo-EM structure of a fully glycosylated soluble cleaved HIV-1 envelope trimer. Science 342:1484-1490. http://dx.doi.org/10.1126/ science.1245627.
38. Sanders RW, Derking R, Cupo A, Julien J, Yasmeen A, de Val N, Kim HJ, Blattner C, de la Peña 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.
39. Pancera M, Zhou T, Druz A, Georgiev IS, Soto C, Gorman J, Huang J, Acharya P, Chuang G, Ofek G, Stewart-Jones GBE, Stuckey J, Bailer RT, Joyce MG, Louder MK, Tumba N, Yang Y, Zhang B, Cohen MS, Haynes BF, Mascola JR, Morris L, Munro JB, Blanchard SC, Mothes W, Connors M, Kwong PD. 2014. Structure and immune recognition of trimeric pre-fusion HIV-1 Env. Nature 514:455-461. http://dx.doi.org/ 10.1038/nature13808.
40. Sharma S, de Val N, Bale S, Guenaga J, Tran K, Feng Y, Dubrovskaya V, Ward A, Wyatt R. 2015. Cleavage-independent HIV-1 Env trimers engineered as soluble native spike mimetics for vaccine design. Cell Rep 11:539-550. http://dx.doi.org/10.1016/j.celrep.2015.03.047.
41. He L, Sok D, Azadnia P, Hsueh J, Landais E, Simek M, Koff WC, Poignard P, Burton DR, Zhu J. 2014. Toward a more accurate view of human B-cell repertoire by next-generation sequencing, unbiased repertoire capture and single-molecule barcoding. Sci Rep 4:6778. http:// dx.doi.org/10.1038/srep06778.
42. Bashford-Rogers R, Palser AL, Idris SF, Carter L, Epstein M, Callard RE, Douek DC, Vassiliou GS, Follows GA, Hubank M, Kellam P. 2014. Capturing needles in haystacks: a comparison of B-cell receptor sequencing methods. BMC Immunol 15:9. http://dx.doi.org/10.1186/s12865-014-0029-0.
43. Tran K, Poulsen C, Guenaga J, de Val N, Wilson R, Sundling C, Li Y, Stanfield RL, Wilson IA, Ward AB, Hedestam GB, Wyatt RT. 2014. Vaccine-elicited primate antibodies use a distinct approach to the HIV-1 primary receptor binding site informing vaccine redesign. Proc Natl Acad Sci U S A 111:E738-E747. http://dx.doi.org/10.1073/pnas.1319512111.
44. Koff WC, Burton DR, Johnson PR, Walker BD, King CR, Nabel GJ, Ahmed R, Bhan MK, Plotkin SA. 2013. Accelerating next-generation vaccine development for global disease prevention. Science 340:1232910. http://dx.doi.org/10.1126/science.1232910.
45. Nabel GJ. 2013. Designing tomorrow's vaccines. N Engl J Med 368: 551-560. http://dx.doi.org/10.1056/NEJMra1204186.
46. Koff WC, Gust ID, Plotkin SA. 2014. Toward a human vaccines project. Nat Immunol 15:589-592. http://dx.doi.org/10.1038/ni.2871.
47. He L, Zhu J. 2015. Computational tools for epitope vaccine design and evaluation. Curr Opin Virol 11:103-112. http://dx.doi.org/10.1016/ j.coviro.2015.03.013.
48. Xie J, Yea K, Zhang H, Moldt B, He L, Zhu J, Lerner R. 2014. Prevention of cell death by antibodies selected from intracellular combinatorial libraries. Chem Biol 21:274-283. http://dx.doi.org/10.1016/ j.chembiol.2013.12.006.
49. DeKosky BJ, Ippolito GC, Deschner RP, Lavinder JJ, Wine Y, Rawlings BM, Varadarajan N, Giesecke C, Dörner T, Andrews SF, Wilson PC, Hunicke-Smith SP, Willson CG, Ellington AD, Georgiou G. 2013. Highthroughput sequencing of the paired human immunoglobulin heavy and light chain repertoire. Nat Biotechnol 31:166-169. http://dx.doi.org/ 10.1038/nbt.2492.
50. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948. http://dx.doi.org/10.1093/bioinformatics/ btm404.
51. Altschul S, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389-3402. http://dx.doi.org/10.1093/nar/25.17.3389.
52. Huson DH, Richter DC, Rausch C, Dezulian T, Franz M, Rupp R. 2007. Dendroscope: an interactive viewer for large phylogenetic trees. BMC Bioinformatics 8:460. http://dx.doi.org/10.1186/1471-2105-8-460.
53. 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.
54. Wu X, Zhou T, O'Dell S, Wyatt RT, Kwong PD, Mascola JR. 2009. Mechanism of human immunodeficiency virus type 1 resistance to monoclonal antibody b12 that effectively targets the site of CD4 attachment. J Virol 83:10892-10907. http://dx.doi.org/10.1128/JVI.01142-09.
55. 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 assessment of neutralizing antibodies. J Virol 84: 1439-1452. http://dx.doi.org/10.1128/JVI.02108-09.