Diverse antibody genetic and recognition properties revealed following HIV-1 envelope glycoprotein immunization

Journal of Immunology

Volumn 194, Issue 12, 2015, Pages 5903-5914

  Phad, Ganesh E ^a   Bernat, Néstor Vázquez ^a   Feng, Yu ^b   Ingale, Jidnyasa ^b   Murillo, Paola Andrea Martinez ^a   O'Dell, Sijy ^c   Li, Yuxing ^b,d   Mascola, John R ^c   Sundling, Christopher ^a,e   Wyatt, Richard T ^b   Hedestam, Gunilla B Karlsson ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d UNIVERSITY OF MARYLAND   (United States)

^e GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN GP 140; MONOCLONAL ANTIBODY; CD4 ANTIGEN; EPITOPE; GLYCOPROTEIN GP 120; HIV ENVELOPE PROTEIN GP120 (305-321); HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; NEUTRALIZING ANTIBODY; PEPTIDE FRAGMENT; PROTEIN BINDING; RECOMBINANT PROTEIN; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY ISOLATION; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ANTIGEN BINDING; ANTIGEN RECOGNITION; ARTICLE; BINDING SITE; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNIZATION; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; RHESUS MONKEY; VIRUS NEUTRALIZATION; AMINO ACID SEQUENCE; ANIMAL; ANTIBODY COMBINING SITE; CHEMISTRY; GENETICS; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; PROTEIN DOMAIN; SERODIAGNOSIS;

AIDS VACCINES; AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; ANTIBODY DIVERSITY; ANTIGENS, CD4; BINDING SITES, ANTIBODY; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; EPITOPES; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV-1; IMMUNIZATION; MACACA MULATTA; MOLECULAR SEQUENCE DATA; NEUTRALIZATION TESTS; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECOMBINANT PROTEINS;

EID: 84931309311     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1500122     Document Type: Article

References (65)

1. Wibmer, C. K., J. N. Bhiman, E. S. Gray, N. Tumba, S. S. Abdool Karim, C. Williamson, L. Morris, and P. L. Moore. 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.
2. Moore, P. L., E. S. Gray, C. K. Wibmer, J. N. Bhiman, M. Nonyane, D. J. Sheward, T. Hermanus, S. Bajimaya, N. L. Tumba, M. R. Abrahams, et al. 2012. Evolution of an HIV glycan-dependent broadly neutralizing antibody epitope through immune escape. Nat. Med. 18: 1688-1692.
3. Liao, H. X., R. Lynch, T. Zhou, F. Gao, S. M. Alam, S. D. Boyd, A. Z. Fire, K. M. Roskin, C. A. Schramm, Z. Zhang, et al; NISC Comparative Sequencing Program. 2013. Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature 496: 469-476.
4. Doria-Rose, N. A., C. A. Schramm, J. Gorman, P. L. Moore, J. N. Bhiman, B. J. DeKosky, M. J. Ernandes, I. S. Georgiev, H. J. Kim, M. Pancera, et al; NISC Comparative Sequencing Program. 2014. Developmental pathway for potent V1V2-directed HIV-neutralizing antibodies. Nature 509: 55-62.
5. Gao, F., M. Bonsignori, H. X. Liao, A. Kumar, S. M. Xia, X. Lu, F. Cai, K. K. Hwang, H. Song, T. Zhou, et al. 2014. Cooperation of B cell lineages in induction of HIV-1-broadly neutralizing antibodies. Cell 158: 481-491.
6. Haynes, B. F., G. Kelsoe, S. C. Harrison, and T. B. Kepler. 2012. B-cell-lineage immunogen design in vaccine development with HIV-1 as a case study. Nat. Biotechnol. 30: 423-433.
7. Jardine, J., J. P. Julien, S. Menis, T. Ota, O. Kalyuzhniy, A. McGuire, D. Sok, P. S. Huang, S. MacPherson, M. Jones, et al. 2013. Rational HIV immunogen design to target specific germline B cell receptors. Science 340: 711-716.
8. Davis, K. L., E. S. Gray, P. L. Moore, J. M. Decker, A. Salomon, D. C. Montefiori, B. S. Graham, M. C. Keefer, A. Pinter, L. Morris, et al. 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.
9. + T cell decline and high viral load during acute infection. J. Virol. 85: 4828-4840.
10. Ho, D. D., J. A. McKeating, X. L. Li, T. Moudgil, E. S. Daar, N. C. Sun, and J. E. Robinson. 1991. Conformational epitope on gp120 important in CD4 binding and human immunodeficiency virus type 1 neutralization identified by a human monoclonal antibody. J. Virol. 65: 489-493.
11. Matsushita, S., M. Robert-Guroff, J. Rusche, A. Koito, T. Hattori, H. Hoshino, K. Javaherian, K. Takatsuki, and S. Putney. 1988. Characterization of a human immunodeficiency virus neutralizing monoclonal antibody and mapping of the neutralizing epitope. J. Virol. 62: 2107-2114.
12. Posner, M. R., T. Hideshima, T. Cannon, M. Mukherjee, K. H. Mayer, and R. A. Byrn. 1991. An IgG human monoclonal antibody that reacts with HIV-1/GP120, inhibits virus binding to cells, and neutralizes infection. J. Immunol. 146: 4325-4332.
13. Huang, J., B. H. Kang, M. Pancera, J. H. Lee, T. Tong, Y. Feng, H. Imamichi, I. S. Georgiev, G. Y. Chuang, A. Druz, et al. 2014. Broad and potent HIV-1 neutralization by a human antibody that binds the gp41-gp120 interface. Nature 515: 138-142.
14. Huang, J., G. Ofek, L. Laub, M. K. Louder, N. A. Doria-Rose, N. S. Longo, H. Imamichi, R. T. Bailer, B. Chakrabarti, S. K. Sharma, et al. 2012. Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature 491: 406-412.
15. Scheid, J. F., H. Mouquet, B. Ueberheide, R. Diskin, F. Klein, T. Y. Oliveira, J. Pietzsch, D. Fenyo, A. Abadir, K. Velinzon, et al. 2011. Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science 333: 1633-1637.
16. Walker, L. M., M. Huber, K. J. Doores, E. Falkowska, R. Pejchal, J. P. Julien, S. K. Wang, A. Ramos, P. Y. Chan-Hui, M. Moyle, et al; Protocol G Principal Investigators. 2011. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477: 466-470.
17. Walker, L. M., S. K. Phogat, P. Y. Chan-Hui, D. Wagner, P. Phung, J. L. Goss, T. Wrin, M. D. Simek, S. Fling, J. L. Mitcham, et al; Protocol G Principal Investigators. 2009. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326: 285-289.
18. Wu, X., Z. Y. Yang, Y. Li, C. M. Hogerkorp, W. R. Schief, M. S. Seaman, T. Zhou, S. D. Schmidt, L. Wu, L. Xu, et al. 2010. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329: 856-861.
19. Barouch, D. H., J. B. Whitney, B. Moldt, F. Klein, T. Y. Oliveira, J. Liu, K. E. Stephenson, H. W. Chang, K. Shekhar, S. Gupta, et al. 2013. Therapeutic efficacy of potent neutralizing HIV-1-specific monoclonal antibodies in SHIVinfected rhesus monkeys. Nature 503: 244-248.
20. Shingai, M., Y. Nishimura, F. Klein, H. Mouquet, O. K. Donau, R. Plishka, A. Buckler-White, M. Seaman, M. Piatak, Jr., J. D. Lifson, et al. 2013. Antibody-mediated immunotherapy of macaques chronically infected with SHIV suppresses viraemia. Nature 503: 277-280.
21. Chakrabarti, B., Y. Feng, S. K. Kumar, K. McKee, G. B. Karlsson Hedestam, C. C. Labranche, D. C. Montefiori, J. R. Mascola, and R. T. Wyatt. 2013. Robust neutralizing antibodies elicited by HIV-1 JRFL envelope glycoprotein trimers in nonhuman primates. J. Virol. 87: 13239-13251.
22. Sundling, C., M. N. Forsell, S. O'Dell, Y. Feng, B. Chakrabarti, S. S. Rao, K. Loré, J. R. Mascola, R. T. Wyatt, I. Douagi, and G. B. Karlsson Hedestam. 2010. Soluble HIV-1 Env trimers in adjuvant elicit potent and diverse functional B cell responses in primates. J. Exp. Med. 207: 2003-2017.
23. Kovacs, J. M., J. P. Nkolola, H. Peng, A. Cheung, J. Perry, C. A. Miller, M. S. Seaman, D. H. Barouch, and B. Chen. 2012. HIV-1 envelope trimer elicits more potent neutralizing antibody responses than monomeric gp120. Proc. Natl. Acad. Sci. USA 109: 12111-12116.
24. Sellhorn, G., Z. Kraft, Z. Caldwell, K. Ellingson, C. Mineart, M. S. Seaman, D. C. Montefiori, E. Lagerquist, and L. Stamatatos. 2012. Engineering, expression, purification, and characterization of stable clade A/B recombinant soluble heterotrimeric gp140 proteins. J. Virol. 86: 128-142.
25. Malherbe, D. C., N. A. Doria-Rose, L. Misher, T. Beckett, W. B. Puryear, J. T. Schuman, Z. Kraft, J. O'Malley, M. Mori, I. Srivastava, et al. 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.
26. Bontjer, I., M. Melchers, T. Tong, T. van Montfort, D. Eggink, D. Montefiori, W. C. Olson, J. P. Moore, J. M. Binley, B. Berkhout, and R. W. Sanders. 2013. Comparative immunogenicity of evolved V1V2-deleted HIV-1 envelope glycoprotein trimers. PLoS ONE 8: e67484.
27. Moody, M. A., S. Santra, N. A. Vandergrift, L. L. Sutherland, T. C. Gurley, M. S. Drinker, A. A. Allen, S. M. Xia, R. R. Meyerhoff, R. Parks, et al. 2014. Toll-like receptor 7/8 (TLR7/8) and TLR9 agonists cooperate to enhance HIV-1 envelope antibody responses in rhesus macaques. J. Virol. 88: 3329-3339.
28. Berman, P. W., W. Huang, L. Riddle, A. M. Gray, T. Wrin, J. Vennari, A. Johnson, M. Klaussen, H. Prashad, C. Köhne, et al. 1999. Development of bivalent (B/E) vaccines able to neutralize CCR5-dependent viruses from the United States and Thailand. Virology 265: 1-9.
29. Montefiori, D. C., C. Karnasuta, Y. Huang, H. Ahmed, P. Gilbert, M. S. de Souza, R. McLinden, S. Tovanabutra, A. Laurence-Chenine, E. Sanders-Buell, et al. 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.
30. Sundling, C., Y. Li, N. Huynh, C. Poulsen, R. Wilson, S. O'Dell, Y. Feng, J. R. Mascola, R. T. Wyatt, and G. B. Karlsson Hedestam. 2012. High-resolution definition of vaccine-elicited B cell responses against the HIV primary receptor binding site. Sci. Transl. Med. 4: 142ra196.
31. Chen, Y., M. Vaine, A. Wallace, D. Han, S. Wan, M. S. Seaman, D. Montefiori, S. Wang, and S. Lu. 2013. A novel rabbit monoclonal antibody platform to dissect the diverse repertoire of antibody epitopes for HIV-1 Env immunogen design. J. Virol. 87: 10232-10243.
32. Bonsignori, M., J. Pollara, M. A. Moody, M. D. Alpert, X. Chen, K. K. Hwang, P. B. Gilbert, Y. Huang, T. C. Gurley, D. M. Kozink, et al. 2012. Antibody-dependent cellular cytotoxicity-mediating antibodies from an HIV-1 vaccine efficacy trial target multiple epitopes and preferentially use the VH1 gene family. J. Virol. 86: 11521-11532.
33. Liao, H. X., M. Bonsignori, S. M. Alam, J. S. McLellan, G. D. Tomaras, M. A. Moody, D. M. Kozink, K. K. Hwang, X. Chen, C. Y. Tsao, et al. 2013. Vaccine induction of antibodies against a structurally heterogeneous site of immune pressure within HIV-1 envelope protein variable regions 1 and 2. Immunity 38: 176-186.
34. Moody, M. A., N. L. Yates, J. D. Amos, M. S. Drinker, J. A. Eudailey, T. C. Gurley, D. J. Marshall, J. F. Whitesides, X. Chen, A. Foulger, et al. 2012. HIV-1 gp120 vaccine induces affinity maturation in both new and persistent antibody clonal lineages. J. Virol. 86: 7496-7507.
35. Sundling, C., Z. Zhang, G. E. Phad, Z. Sheng, Y. Wang, J. R. Mascola, Y. Li, R. T. Wyatt, L. Shapiro, and G. B. Karlsson Hedestam. 2014. Single-cell and deep sequencing of IgG-switched macaque B cells reveal a diverse Ig repertoire following immunization. J. Immunol. 192: 3637-3644.
36. Yang, X., J. Lee, E. M. Mahony, P. D. Kwong, R. Wyatt, and J. Sodroski. 2002. Highly stable trimers formed by human immunodeficiency virus type 1 envelope glycoproteins fused with the trimeric motif of T4 bacteriophage fibritin. J. Virol. 76: 4634-4642.
37. Forsell, M. N., B. Dey, A. Mörner, K. Svehla, S. O'dell, C. M. Högerkorp, G. Voss, R. Thorstensson, G. M. Shaw, J. R. Mascola, et al. 2008. B cell recognition of the conserved HIV-1 co-receptor binding site is altered by endogenous primate CD4. PLoS Pathog. 4: e1000171.
38. Sundling, C., P. Martinez, M. Soldemo, M. Spångberg, K. L. Bengtsson, L. Stertman, M. N. Forsell, and G. B. Karlsson Hedestam. 2013. Immunization of macaques with soluble HIV type 1 and influenza virus envelope glycoproteins results in a similarly rapid contraction of peripheral B-cell responses after boosting. J. Infect. Dis. 207: 426-431.
39. Sundling, C., G. Phad, I. Douagi, M. Navis, and G. B. Karlsson Hedestam. 2012. Isolation of antibody V(D)J sequences from single cell sorted rhesus macaque B cells. J. Immunol. Methods 386: 85-93.
40. Tiller, T., E. Meffre, S. Yurasov, M. Tsuiji, M. C. Nussenzweig, and H. Wardemann. 2008. Efficient generation of monoclonal antibodies from single human B cells by single cell RT-PCR and expression vector cloning. J. Immunol. Methods 329: 112-124.
41. Ye, J., N. Ma, T. L. Madden, and J. M. Ostell. 2013. IgBLAST: an immunoglobulin variable domain sequence analysis tool. Nucleic Acids Res. 41: W34-40.
42. Brochet, X., M. P. Lefranc, and V. Giudicelli. 2008. IMGT/V-QUEST: the highly customized and integrated system for IG and TR standardized V-J and V-D-J sequence analysis. Nucleic Acids Res. 36: W503-508.
43. Feng, Y., K. McKee, K. Tran, S. O'Dell, S. D. Schmidt, A. Phogat, M. N. Forsell, G. B. Karlsson Hedestam, J. R. Mascola, and R. T. Wyatt. 2012. Biochemically defined HIV-1 envelope glycoprotein variant immunogens display differential binding and neutralizing specificities to the CD4-binding site. J. Biol. Chem. 287: 5673-5686.
44. Li, Y., S. O'Dell, L. M. Walker, X. Wu, J. Guenaga, Y. Feng, S. D. Schmidt, K. McKee, M. K. Louder, J. E. Ledgerwood, et al. 2011. Mechanism of neutralization by the broadly neutralizing HIV-1 monoclonal antibody VRC01. J. Virol. 85: 8954-8967.
45. Li, M., F. Gao, J. R. Mascola, L. Stamatatos, V. R. Polonis, M. Koutsoukos, G. Voss, P. Goepfert, P. Gilbert, K. M. Greene, et al. 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.
46. Shu, Y., S. Winfrey, Z. Y. Yang, L. Xu, S. S. Rao, I. Srivastava, S. W. Barnett, G. J. Nabel, and J. R. Mascola. 2007. Efficient protein boosting after plasmid DNA or recombinant adenovirus immunization with HIV-1 vaccine constructs. Vaccine 25: 1398-1408.
47. Dosenovic, P., B. Chakrabarti, M. Soldemo, I. Douagi, M. N. Forsell, Y. Li, A. Phogat, S. Paulie, J. Hoxie, R. T. Wyatt, and G. B. Karlsson Hedestam. 2009. Selective expansion of HIV-1 envelope glycoprotein-specific B cell subsets recognizing distinct structural elements following immunization. J. Immunol. 183: 3373-3382.
48. Douagi, I., M. N. Forsell, C. Sundling, S. O'Dell, Y. Feng, P. Dosenovic, Y. Li, R. Seder, K. Loré, J. R. Mascola, et al. 2010. Influence of novel CD4 bindingdefective HIV-1 envelope glycoprotein immunogens on neutralizing antibody and T-cell responses in nonhuman primates. J. Virol. 84: 1683-1695.
49. Yang, X., L. Florin, M. Farzan, P. Kolchinsky, P. D. Kwong, J. Sodroski, and R. Wyatt. 2000. Modifications that stabilize human immunodeficiency virus envelope glycoprotein trimers in solution. J. Virol. 74: 4746-4754.
50. Navis, M., K. Tran, S. Bale, G. E. Phad, J. Guenaga, R. Wilson, M. Soldemo, K. McKee, C. Sundling, J. Mascola, et al. 2014. HIV-1 receptor binding sitedirected antibodies using a VH1-2 gene segment orthologue are activated by Env trimer immunization. PLoS Pathog. 10: e1004337.
51. Tran, K., C. Poulsen, J. Guenaga, N. de Val, R. Wilson, C. Sundling, Y. Li, R. L. Stanfield, I. A. Wilson, A. B. Ward, et al. 2014. Vaccine-elicited primate antibodies use a distinct approach to the HIV-1 primary receptor binding site informing vaccine redesign. Proc. Natl. Acad. Sci. USA 111: E738-E747.
52. Seaman, M. S., H. Janes, N. Hawkins, L. E. Grandpre, C. Devoy, A. Giri, R. T. Coffey, L. Harris, B. Wood, M. G. Daniels, et al. 2010. Tiered categorization of a diverse panel of HIV-1 Env pseudoviruses for assessment of neutralizing antibodies. J. Virol. 84: 1439-1452.
53. Huang, C. C., M. Tang, M. Y. Zhang, S. Majeed, E. Montabana, R. L. Stanfield, D. S. Dimitrov, B. Korber, J. Sodroski, I. A. Wilson, et al. 2005. Structure of a V3-containing HIV-1 gp120 core. Science 310: 1025-1028.
54. Julien, J. P., A. Cupo, D. Sok, R. L. Stanfield, D. Lyumkis, M. C. Deller, P. J. Klasse, D. R. Burton, R. W. Sanders, J. P. Moore, et al. 2013. Crystal structure of a soluble cleaved HIV-1 envelope trimer. Science 342: 1477-1483.
55. Koch, M., M. Pancera, P. D. Kwong, P. Kolchinsky, C. Grundner, L. Wang, W. A. Hendrickson, J. Sodroski, and R. Wyatt. 2003. Structure-based, targeted deglycosylation of HIV-1 gp120 and effects on neutralization sensitivity and antibody recognition. Virology 313: 387-400.
56. Ingale, J., K. Tran, L. Kong, B. Dey, K. McKee, W. Schief, P. D. Kwong, J. R. Mascola, and R. T. Wyatt. 2014. Hyperglycosylated stable core immunogens designed to present the CD4 binding site are preferentially recognized by broadly neutralizing antibodies. J. Virol. 88: 14002-14016.
57. Li, Y., S. A. Migueles, B. Welcher, K. Svehla, A. Phogat, M. K. Louder, X. Wu, G. M. Shaw, M. Connors, R. T. Wyatt, and J. R. Mascola. 2007. Broad HIV-1 neutralization mediated by CD4-binding site antibodies. Nat. Med. 13: 1032-1034.
58. Mörner, A., I. Douagi, M. N. Forsell, C. Sundling, P. Dosenovic, S. O'Dell, B. Dey, P. D. Kwong, G. Voss, R. Thorstensson, et al. 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.
59. Haynes, B. F., P. B. Gilbert, M. J. McElrath, S. Zolla-Pazner, G. D. Tomaras, S. M. Alam, D. T. Evans, D. C. Montefiori, C. Karnasuta, R. Sutthent, et al. 2012. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N. Engl. J. Med. 366: 1275-1286.
60. Gottardo, R., R. T. Bailer, B. T. Korber, S. Gnanakaran, J. Phillips, X. Shen, G. D. Tomaras, E. Turk, G. Imholte, L. Eckler, et al. 2013. Plasma IgG to linear epitopes in the V2 and V3 regions of HIV-1 gp120 correlate with a reduced risk of infection in the RV144 vaccine efficacy trial. PLoS ONE 8: e75665.
61. Gorny, M. K., X. H. Wang, C. Williams, B. Volsky, K. Revesz, B. Witover, S. Burda, M. Urbanski, P. Nyambi, C. Krachmarov, et al. 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.
62. Gorny, M. K., J. Sampson, H. Li, X. Jiang, M. Totrov, X. H. Wang, C. Williams, T. O'Neal, B. Volsky, L. Li, et al. 2011. Human anti-V3 HIV-1 monoclonal antibodies encoded by the VH5-51/VL lambda genes define a conserved antigenic structure. PLoS ONE 6: e27780.
63. Stanfield, R. L., M. K. Gorny, C. Williams, S. Zolla-Pazner, and I. A. Wilson. 2004. Structural rationale for the broad neutralization of HIV-1 by human monoclonal antibody 447-52D. Structure 12: 193-204.
64. Pan, R., J. M. Sampson, Y. Chen, M. Vaine, S. Wang, S. Lu, and X. P. Kong. 2013. Rabbit anti-HIV-1 monoclonal antibodies raised by immunization can mimic the antigen-binding modes of antibodies derived from HIV-1-infected humans. J. Virol. 87: 10221-10231.
65. Pettersen, E. F., T. D. Goddard, C. C. Huang, G. S. Couch, D. M. Greenblatt, E. C. Meng, and T. E. Ferrin. 2004. UCSF chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25: 1605-1612.