A directed molecular evolution approach to improved immunogenicity of the HIV-1 envelope glycoprotein

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Du, Sean X ^a,g   Xu, Li ^a,h   Zhang, Wenge ^a   Tang, Susan ^a   Boenig, Rebecca I ^a,f   Chen, Helen ^a   Mariano, Ellaine B ^a,f   Zwick, Michael B ^b   Parren, Paul W H I ^b,i   Burton, Dennis R ^b,c   Wrin, Terri ^d   Petropoulos, Christos J ^d   Ballantyne, John A ^e   Chambers, Michael ^e   Whalen, Robert G ^a,f  

^a MAXYGEN INC   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d MONOGRAM BIOSCIENCES   (United States)

^e Aldevron LLC   (United States)

^f Altravax Inc   (United States)

^g Simcere Pharmaceutical Group   (China)

^h Sea Lane Biotechnologies LLC ^*  (United States)

ⁱ GENMAB   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN GP 120; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; HUMAN IMMUNODEFICIENCY VIRUS PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; MONOCLONAL ANTIBODY B12; NEUTRALIZING ANTIBODY; VIRUS GLYCOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN BINDING; ARTICLE; CHIMERA; CONTROLLED STUDY; CROSS PRESENTATION; DNA IMMUNIZATION; DNA RECOMBINATION; EXPERIMENTAL RABBIT; FEMALE; GENETIC CODE; GENETIC VARIABILITY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOGENICITY; IN VITRO STUDY; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPIC VARIATION; SCREENING TEST; SEQUENCE ANALYSIS; VACCINE PRODUCTION; VIRUS ENVELOPE; VIRUS NEUTRALIZATION; ANIMAL; CHO CELL; CRICETULUS; GENETICS; HAMSTER; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; RABBIT; SURFACE PLASMON RESONANCE;

HUMAN IMMUNODEFICIENCY VIRUS 1; ORYCTOLAGUS CUNICULUS;

ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; EVOLUTION, MOLECULAR; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; MOLECULAR SEQUENCE DATA; RABBITS; SURFACE PLASMON RESONANCE;

EID: 79959654427     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0020927     Document Type: Article

References (87)

1. 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.
2. Walker BD, Burton DR, (2008) Toward an AIDS vaccine. Science 320: 760-764.
3. Karlsson Hedestam GB, Fouchier RA, Phogat S, Burton DR, Sodroski J, et al. (2008) The challenges of eliciting neutralizing antibodies to HIV-1 and to influenza virus. Nat Rev Microbiol 6: 143-155.
4. Haynes BF, Montefiori DC, (2006) Aiming to induce broadly reactive neutralizing antibody responses with HIV-1 vaccine candidates. Expert Rev Vaccines 5: 579-595.
5. Srivastava IK, Ulmer JB, Barnett SW, (2005) Role of neutralizing antibodies in protective immunity against HIV. Hum Vaccin 1: 45-60.
6. Binley JM, Lybarger EA, Crooks ET, Seaman MS, Gray E, et al. (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.
7. Sather DN, Armann J, Ching LK, Mavrantoni A, Sellhorn G, et al. (2009) Factors associated with the development of cross-reactive neutralizing antibodies during human immunodeficiency virus type 1 infection. J Virol 83: 757-769.
8. Carotenuto P, Looij D, Keldermans L, de Wolf F, Goudsmit J, (1998) Neutralizing antibodies are positively associated with CD4+ T-cell counts and T-cell function in long-term AIDS-free infection. Aids 12: 1591-1600.
9. Li Y, Migueles SA, Welcher B, Svehla K, Phogat A, et al. (2007) Broad HIV-1 neutralization mediated by CD4-binding site antibodies. Nat Med 13: 1032-1034.
10. Pilgrim AK, Pantaleo G, Cohen OJ, Fink LM, Zhou JY, et al. (1997) Neutralizing antibody responses to human immunodeficiency virus type 1 in primary infection and long-term-nonprogressive infection. J Infect Dis 176: 924-932.
11. Hessell AJ, Poignard P, Hunter M, Hangartner L, Tehrani DM, et al. (2009) Effective, low-titer antibody protection against low-dose repeated mucosal SHIV challenge in macaques. Nat Med 15: 951-954.
12. Nishimura Y, Igarashi T, Haigwood N, Sadjadpour R, Plishka RJ, et al. (2002) Determination of a statistically valid neutralization titer in plasma that confers protection against simian-human immunodeficiency virus challenge following passive transfer of high-titered neutralizing antibodies. J Virol 76: 2123-2130.
13. Shibata R, Igarashi T, Haigwood N, Buckler-White A, Ogert R, et al. (1999) Neutralizing antibody directed against the HIV-1 envelope glycoprotein can completely block HIV-1/SIV chimeric virus infections of macaque monkeys. Nat Med 5: 204-210.
14. Baba TW, Liska V, Hofmann-Lehmann R, Vlasak J, Xu W, et al. (2000) Human neutralizing monoclonal antibodies of the IgG1 subtype protect against mucosal simian-human immunodeficiency virus infection. Nat Med 6: 200-206.
15. Hofmann-Lehmann R, Vlasak J, Rasmussen RA, Smith BA, Baba TW, et al. (2001) Postnatal passive immunization of neonatal macaques with a triple combination of human monoclonal antibodies against oral simian-human immunodeficiency virus challenge. J Virol 75: 7470-7480.
16. Mascola JR, (2003) Defining the protective antibody response for HIV-1. Curr Mol Med 3: 209-216.
17. (2003) AIDSVAX fails to prove efficacious in large-scale trial. Expert Rev Anti Infect Ther 1: 527.
18. Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, Kaewkungwal J, Chiu J, et al. (2009) Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N Engl J Med 361: 2209-2220.
19. Kwong PD, Wilson IA, (2009) HIV-1 and influenza antibodies: seeing antigens in new ways. Nat Immunol 10: 573-578.
20. Li Y, Cleveland B, Klots I, Travis B, Richardson BA, et al. (2008) Removal of a single N-linked glycan in human immunodeficiency virus type 1 gp120 results in an enhanced ability to induce neutralizing antibody responses. J Virol 82: 638-651.
21. Zhang PF, Cham F, Dong M, Choudhary A, Bouma P, et al. (2007) Extensively cross-reactive anti-HIV-1 neutralizing antibodies induced by gp140 immunization. Proc Natl Acad Sci U S A 104: 10193-10198.
22. Binley JM, Sanders RW, Clas B, Schuelke N, Master A, et al. (2000) A recombinant human immunodeficiency virus type 1 envelope glycoprotein complex stabilized by an intermolecular disulfide bond between the gp120 and gp41 subunits is an antigenic mimic of the trimeric virion-associated structure. J Virol 74: 627-643.
23. Selvarajah S, Puffer BA, Lee FH, Zhu P, Li Y, et al. (2008) Focused dampening of antibody response to the immunodominant variable loops by engineered soluble gp140. AIDS Res Hum Retroviruses 24: 301-314.
24. Yang X, Lee J, Mahony EM, Kwong PD, Wyatt R, et al. (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.
25. Yang X, Farzan M, Wyatt R, Sodroski J, (2000) Characterization of stable, soluble trimers containing complete ectodomains of human immunodeficiency virus type 1 envelope glycoproteins. J Virol 74: 5716-5725.
26. Morner A, Douagi I, Forsell MN, Sundling C, Dosenovic P, 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.
27. Hammonds J, Chen X, Fouts T, DeVico A, Montefiori D, et al. (2005) Induction of neutralizing antibodies against human immunodeficiency virus type 1 primary isolates by Gag-Env pseudovirion immunization. J Virol 79: 14804-14814.
28. Du SX, Idiart RJ, Mariano EB, Chen H, Jiang P, et al. (2009) Effect of trimerization motifs on quaternary structure, antigenicity, and immunogenicity of a noncleavable HIV-1 gp140 envelope glycoprotein. Virology 395: 33-44.
29. Crooks ET, Moore PL, Franti M, Cayanan CS, Zhu P, et al. (2007) A comparative immunogenicity study of HIV-1 virus-like particles bearing various forms of envelope proteins, particles bearing no envelope and soluble monomeric gp120. Virology 366: 245-262.
30. Kang YK, Andjelic S, Binley JM, Crooks ET, Franti M, et al. (2009) Structural and immunogenicity studies of a cleaved, stabilized envelope trimer derived from subtype A HIV-1. Vaccine 27: 5120-5132.
31. Yang X, Wyatt R, Sodroski J, (2001) Improved elicitation of neutralizing antibodies against primary human immunodeficiency viruses by soluble stabilized envelope glycoprotein trimers. J Virol 75: 1165-1171.
32. Dey B, Svehla K, Xu L, Wycuff D, Zhou T, et al. (2009) Structure-based stabilization of HIV-1 gp120 enhances humoral immune responses to the induced co-receptor binding site. PLoS Pathog 5: e1000445.
33. Wang S, Kennedy JS, West K, Montefiori DC, Coley S, et al. (2008) Cross-subtype antibody and cellular immune responses induced by a polyvalent DNA prime-protein boost HIV-1 vaccine in healthy human volunteers. Vaccine 26: 1098-1110.
34. Wang S, Pal R, Mascola JR, Chou TH, Mboudjeka I, et al. (2006) Polyvalent HIV-1 Env vaccine formulations delivered by the DNA priming plus protein boosting approach are effective in generating neutralizing antibodies against primary human immunodeficiency virus type 1 isolates from subtypes A, B, C, D and E. Virology 350: 34-47.
35. Derby NR, Kraft Z, Kan E, Crooks ET, Barnett SW, et al. (2006) Antibody responses elicited in macaques immunized with human immunodeficiency virus type 1 (HIV-1) SF162-derived gp140 envelope immunogens: comparison with those elicited during homologous simian/human immunodeficiency virus SHIVSF162P4 and heterologous HIV-1 infection. J Virol 80: 8745-8762.
36. Barnett SW, Lu S, Srivastava I, Cherpelis S, Gettie A, et al. (2001) The ability of an oligomeric human immunodeficiency virus type 1 (HIV-1) envelope antigen to elicit neutralizing antibodies against primary HIV-1 isolates is improved following partial deletion of the second hypervariable region. J Virol 75: 5526-5540.
37. Pantophlet R, Wilson IA, Burton DR, (2004) Improved design of an antigen with enhanced specificity for the broadly HIV-neutralizing antibody b12. Protein Eng Des Sel 17: 749-758.
38. Pantophlet R, Wilson IA, Burton DR, (2003) Hyperglycosylated mutants of human immunodeficiency virus (HIV) type 1 monomeric gp120 as novel antigens for HIV vaccine design. J Virol 77: 5889-5901.
39. Beddows S, Schulke N, Kirschner M, Barnes K, Franti M, et al. (2005) Evaluating the immunogenicity of a disulfide-stabilized, cleaved, trimeric form of the envelope glycoprotein complex of human immunodeficiency virus type 1. J Virol 79: 8812-8827.
40. Doria-Rose NA, Learn GH, Rodrigo AG, Nickle DC, Li F, et al. (2005) Human immunodeficiency virus type 1 subtype B ancestral envelope protein is functional and elicits neutralizing antibodies in rabbits similar to those elicited by a circulating subtype B envelope. J Virol 79: 11214-11224.
41. Kothe DL, Decker JM, Li Y, Weng Z, Bibollet-Ruche F, et al. (2007) Antigenicity and immunogenicity of HIV-1 consensus subtype B envelope glycoproteins. Virology 360: 218-234.
42. Kothe DL, Li Y, Decker JM, Bibollet-Ruche F, Zammit KP, et al. (2006) Ancestral and consensus envelope immunogens for HIV-1 subtype C. Virology 352: 438-449.
43. Liao HX, Sutherland LL, Xia SM, Brock ME, Scearce RM, et al. (2006) A group M consensus envelope glycoprotein induces antibodies that neutralize subsets of subtype B and C HIV-1 primary viruses. Virology 353: 268-282.
44. Crameri A, Raillard SA, Bermudez E, Stemmer WP, (1998) DNA shuffling of a family of genes from diverse species accelerates directed evolution. Nature 391: 288-291.
45. Ness JE, Kim S, Gottman A, Pak R, Krebber A, et al. (2002) Synthetic shuffling expands functional protein diversity by allowing amino acids to recombine independently. Nat Biotechnol 20: 1251-1255.
46. Castle LA, Siehl DL, Gorton R, Patten PA, Chen YH, et al. (2004) Discovery and directed evolution of a glyphosate tolerance gene. Science 304: 1151-1154.
47. Lazetic S, Leong SR, Chang JC, Ong R, Dawes G, et al. (2002) Chimeric costimulatory molecules that selectively act through CD28 or CTLA-4 on human T cells. J Biol Chem 277: 38660-38668.
48. Leong SR, Chang JC, Ong R, Dawes G, Stemmer WP, et al. (2003) Optimized expression and specific activity of IL-12 by directed molecular evolution. Proc Natl Acad Sci U S A 100: 1163-1168.
49. Brideau-Andersen AD, Huang X, Sun SC, Chen TT, Stark D, et al. (2007) Directed evolution of gene-shuffled IFN-alpha molecules with activity profiles tailored for treatment of chronic viral diseases. Proc Natl Acad Sci U S A 104: 8269-8274.
50. Bacher JM, Reiss BD, Ellington AD, (2002) Anticipatory evolution and DNA shuffling. Genome Biol 3: 1021-1024.
51. Kurtzman AL, Govindarajan S, Vahle K, Jones JT, Heinrichs V, et al. (2001) Advances in directed protein evolution by recursive genetic recombination: applications to therapeutic proteins. Curr Opin Biotechnol 12: 361-370.
52. Apt D, Raviprakash K, Brinkman A, Semyonov A, Yang S, et al. (2006) Tetravalent neutralizing antibody response against four dengue serotypes by a single chimeric dengue envelope antigen. Vaccine 24: 335-344.
53. Dupuy LC, Locher CP, Paidhungat M, Richards MJ, Lind CM, et al. (2009) Directed molecular evolution improves the immunogenicity and protective efficacy of a Venezuelan equine encephalitis virus DNA vaccine. Vaccine 27: 4152-4160.
54. Binley JM, Wrin T, Korber B, Zwick MB, Wang M, et al. (2004) Comprehensive cross-clade neutralization analysis of a panel of anti-human immunodeficiency virus type 1 monoclonal antibodies. J Virol 78: 13232-13252.
55. 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.
56. Frost SD, Wrin T, Smith DM, Kosakovsky Pond SL, Liu Y, et al. (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.
57. Frost SD, Liu Y, Pond SL, Chappey C, Wrin T, et al. (2005) Characterization of human immunodeficiency virus type 1 (HIV-1) envelope variation and neutralizing antibody responses during transmission of HIV-1 subtype B. J Virol 79: 6523-6527.
58. Wei X, Decker JM, Wang S, Hui H, Kappes JC, et al. (2003) Antibody neutralization and escape by HIV-1. Nature 422: 307-312.
59. Roben P, Moore JP, Thali M, Sodroski J, Barbas CF 3rd, et al. (1994) Recognition properties of a panel of human recombinant Fab fragments to the CD4 binding site of gp120 that show differing abilities to neutralize human immunodeficiency virus type 1. J Virol 68: 4821-4828.
60. Pantophlet R, Ollmann Saphire E, Poignard P, Parren PW, Wilson IA, et al. (2003) Fine mapping of the interaction of neutralizing and nonneutralizing monoclonal antibodies with the CD4 binding site of human immunodeficiency virus type 1 gp120. J Virol 77: 642-658.
61. Trkola A, Purtscher M, Muster T, Ballaun C, Buchacher A, et al. (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.
62. Scanlan CN, Pantophlet R, Wormald MR, Ollmann Saphire E, Stanfield R, et al. (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.
63. Kunert R, Wolbank S, Stiegler G, Weik R, Katinger H, (2004) Characterization of molecular features, antigen-binding, and in vitro properties of IgG and IgM variants of 4E10, an anti-HIV type 1 neutralizing monoclonal antibody. AIDS Res Hum Retroviruses 20: 755-762.
64. Wu X, Yang ZY, Li Y, Hogerkorp CM, Schief WR, et al. (2010) Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329: 856-861.
65. Walker LM, Phogat SK, Chan-Hui PY, Wagner D, Phung P, et al. (2009) Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326: 285-289.
66. Saphire EO, Parren PW, Pantophlet R, Zwick MB, Morris GM, et al. (2001) Crystal structure of a neutralizing human IgG against HIV-1: a template for vaccine design. Science 293: 1155-1159.
67. Barbas CF 3rd, Collet TA, Amberg W, Roben P, Binley JM, et al. (1993) Molecular profile of an antibody response to HIV-1 as probed by combinatorial libraries. J Mol Biol 230: 812-823.
68. Wu TT, Johnson G, Kabat EA, (1993) Length distribution of CDRH3 in antibodies. Proteins 16: 1-7.
69. Zhou T, Georgiev I, Wu X, Yang ZY, Dai K, et al. (2010) Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 329: 811-817.
70. Pancera M, McLellan JS, Wu X, Zhu J, Changela A, et al. (2010) Crystal structure of PG16 and chimeric dissection with somatically related PG9: Structure-function analysis of two quaternary-specific antibodies that effectively neutralize HIV-1. J Virol.
71. Xiao X, Chen W, Feng Y, Zhu Z, Prabakaran P, et al. (2009) Germline-like predecessors of broadly neutralizing antibodies lack measurable binding to HIV-1 envelope glycoproteins: implications for evasion of immune responses and design of vaccine immunogens. Biochem Biophys Res Commun 390: 404-409.
72. Liu J, Bartesaghi A, Borgnia MJ, Sapiro G, Subramaniam S, (2008) Molecular architecture of native HIV-1 gp120 trimers. Nature 455: 109-113.
73. Zhu P, Liu J, Bess J Jr, Chertova E, Lifson JD, et al. (2006) Distribution and three-dimensional structure of AIDS virus envelope spikes. Nature 441: 847-852.
74. Zanetti G, Briggs JA, Grunewald K, Sattentau QJ, Fuller SD, (2006) Cryo-electron tomographic structure of an immunodeficiency virus envelope complex in situ. PLoS Pathog 2: e83.
75. Grundner C, Pancera M, Kang JM, Koch M, Sodroski J, et al. (2004) Factors limiting the immunogenicity of HIV-1 gp120 envelope glycoproteins. Virology 330: 233-248.
76. Weaver EA, Lu Z, Camacho ZT, Moukdar F, Liao HX, et al. (2006) Cross-subtype T-cell immune responses induced by a human immunodeficiency virus type 1 group m consensus env immunogen. J Virol 80: 6745-6756.
77. Wu X, Changela A, O'Dell S, Schmidt SD, Pancera M, et al. (2011) Immunotypes of a Quaternary Site of HIV-1 Vulnerability and Their Recognition by Antibodies. Journal of virology 85: 4578-4585.
78. Huang CC, Tang M, Zhang MY, Majeed S, Montabana E, et al. (2005) Structure of a V3-containing HIV-1 gp120 core. Science 310: 1025-1028.
79. Du SX, Xu L, Viswanathan S, Whalen RG, (2008) Inhibition of V3-specific cleavage of recombinant HIV-1 gp120 produced in Chinese hamster ovary cells. Protein Expr Purif 59: 223-231.
80. Haas J, Park EC, Seed B, (1996) Codon usage limitation in the expression of HIV-1 envelope glycoprotein. Curr Biol 6: 315-324.
81. Kwong PD, Wyatt R, Robinson J, Sweet RW, Sodroski J, et al. (1998) Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393: 648-659.
82. Wyatt R, Kwong PD, Desjardins E, Sweet RW, Robinson J, et al. (1998) The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 393: 705-711.
83. Kumar S, Tamura K, Nei M, (2004) MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5: 150-163.
84. Stemmer WP, (1994) DNA shuffling by random fragmentation and reassembly: in vitro recombination for molecular evolution. Proc Natl Acad Sci U S A 91: 10747-10751.
85. Minshull J, Govindarajan S, Cox T, Ness JE, Gustafsson C, (2004) Engineered protein function by selective amino acid diversification. Methods 32: 416-427.
86. Bojang K, Milligan P, Pinder M, Doherty T, Leach A, et al. (2009) Five-year safety and immunogenicity of GlaxoSmithKline's candidate malaria vaccine RTS,S/AS02 following administration to semi-immune adult men living in a malaria-endemic region of The Gambia. Hum Vaccin 5: 242-247.
87. Mooij P, van der Kolk M, Bogers WM, ten Haaft PJ, Van Der Meide P, et al. (1998) A clinically relevant HIV-1 subunit vaccine protects rhesus macaques from in vivo passaged simian-human immunodeficiency virus infection. AIDS 12: F15-22.