Mechanisms of escape from the PGT128 family of anti-HIV broadly neutralizing antibodies

Retrovirology

Volumn 13, Issue 1, 2016, Pages

  Krumm, Stefanie A ^a   Mohammed, Hajer ^a   Le, Khoa M ^b   Crispin, Max ^c   Wrin, Terri ^d   Poignard, Pascal ^b   Burton, Dennis R ^b,e   Doores, Katie J ^a  

^a GUY S HOSPITAL   (United Kingdom)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d LABORATORY CORPORATION OF AMERICA   (United States)

^e MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Envelope glycoprotein; HIV 1; N linked glycosylation; Neutralizing antibody; Viral escape

Indexed keywords

GLYCAN; NEUTRALIZING ANTIBODY; PGT128 ANTIBODY; PGT130 ANTIBODY; UNCLASSIFIED DRUG; EPITOPE; GLYCOPROTEIN GP 120; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; POLYSACCHARIDE;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; HUMAN; NONHUMAN; PROTEIN GLYCOSYLATION; VIRUS ISOLATION; VIRUS NEUTRALIZATION; VIRUS RESISTANCE; VIRUS STRAIN; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNE EVASION; IMMUNOLOGY; MUTATION;

ANTIBODIES, NEUTRALIZING; EPITOPES, B-LYMPHOCYTE; HIV; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HUMANS; IMMUNE EVASION; MUTATION; POLYSACCHARIDES;

EID: 84956639986     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/s12977-016-0241-5     Document Type: Article

References (45)

1. Burton DR, Ahmed R, Barouch DH, Butera ST, Crotty S, Godzik A, Kaufmann DE, McElrath MJ, Nussenzweig MC, Pulendran B, et al. A blueprint for hiv vaccine discovery. Cell Host Microbe. 2012;12:396-407.
2. Stamatatos L, Morris L, Burton DR, Mascola JR. Neutralizing antibodies generated during natural HIV-1 infection: good news for an HIV-1 vaccine? Nat Med. 2009;15:866-70.
3. Kwong PD, Mascola JR, Nabel GJ. Broadly neutralizing antibodies and the search for an HIV-1 vaccine: the end of the beginning. Nat Rev Immunol. 2013;13:693-701.
4. Hessell AJ, Poignard P, Hunter M, Hangartner L, Tehrani DM, Bleeker WK, Parren PW, Marx PA, Burton DR. Effective, low-titer antibody protection against low-dose repeated mucosal SHIV challenge in macaques. Nat Med. 2009;15:951-4.
5. Hessell AJ, Rakasz EG, Poignard P, Hangartner L, Landucci G, Forthal DN, Koff WC, Watkins DI, Burton DR. Broadly neutralizing human anti-HIV antibody 2G12 is effective in protection against mucosal SHIV challenge even at low serum neutralizing titers. PLoS Pathog. 2009;5:e1000433.
6. Mascola JR, Stiegler G, VanCott TC, Katinger H, Carpenter CB, Hanson CE, Beary H, Hayes D, Frankel SS, Birx DL, Lewis MG. Protection of macaques against vaginal transmission of a pathogenic HIV-1/SIV chimeric virus by passive infusion of neutralizing antibodies. Nat Med. 2000;6:207-10.
7. Moldt B, Rakasz EG, Schultz N, Chan-Hui PY, Swiderek K, Weisgrau KL, Piaskowski SM, Bergman Z, Watkins DI, Poignard P, Burton DR. Highly potent HIV-specific antibody neutralization in vitro translates into effective protection against mucosal SHIV challenge in vivo. Proc Natl Acad Sci USA. 2012;109:18921-5.
8. Shingai M, Donau OK, Plishka RJ, Buckler-White A, Mascola JR, Nabel GJ, Nason MC, Montefiori D, Moldt B, Poignard P, et al. Passive transfer of modest titers of potent and broadly neutralizing anti-HIV monoclonal antibodies block SHIV infection in macaques. J Exp Med. 2014;211:2061-74.
9. Kong L, Lee JH, Doores KJ, Murin CD, Julien JP, McBride R, Liu Y, Marozsan A, Cupo A, Klasse PJ, et al. Supersite of immune vulnerability on the glycosylated face of HIV-1 envelope glycoprotein gp120. Nat Struct Mol Biol. 2013;20:796-803.
10. Pejchal R, Doores KJ, Walker LM, Khayat R, Huang PS, Wang SK, Stanfield RL, Julien JP, Ramos A, Crispin M, et al. A potent and broad neutralizing antibody recognizes and penetrates the HIV glycan shield. Science. 2011;334:1097-103.
11. Walker LM, Huber M, Doores KJ, Falkowska E, Pejchal R, Julien JP, Wang SK, Ramos A, Chan-Hui PY, Moyle M, et al. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature. 2011;477:466-70.
12. Mouquet H, Scharf L, Euler Z, Liu Y, Eden C, Scheid JF, Halper-Stromberg A, Gnanapragasam PN, Spencer DI, Seaman MS, et al. Complex-type N-glycan recognition by potent broadly neutralizing HIV antibodies. Proc Natl Acad Sci USA. 2012;109:E3268-77.
13. McLellan JS, Pancera M, Carrico C, Gorman J, Julien JP, Khayat R, Louder R, Pejchal R, Sastry M, Dai K, et al. Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9. Nature. 2011;480:336-43.
14. Walker LM, Phogat SK, Chan-Hui PY, Wagner D, Phung P, Goss JL, Wrin T, Simek MD, Fling S, Mitcham JL, et al. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science. 2009;326:285-9.
15. Wu X, Yang ZY, Li Y, Hogerkorp CM, Schief WR, Seaman MS, Zhou T, Schmidt SD, Wu L, Xu L, et al. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science. 2010;329:856-61.
16. Falkowska E, Le KM, Ramos A, Doores KJ, Lee JH, Blattner C, Ramirez A, Derking R, van Gils MJ, Liang CH, et al. Broadly neutralizing hiv antibodies define a glycan-dependent epitope on the prefusion conformation of gp41 on cleaved envelope trimers. Immunity. 2014;40:657-68.
17. Huang J, Ofek G, Laub L, Louder MK, Doria-Rose NA, Longo NS, Imamichi H, Bailer RT, Chakrabarti B, Sharma SK, et al. Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature. 2012;491:406-12.
18. Gray ES, Madiga MC, Hermanus T, Moore PL, Wibmer CK, Tumba NL, Werner L, Mlisana K, Sibeko S, Williamson C, et al. 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. 2011;85:4828-40.
19. Crispin M, Doores KJ. Targeting host-derived glycans on enveloped viruses for antibody-based vaccine design. Curr Opin Virol. 2015;11C:63-9.
20. Doores KJ. The HIV glycan shield as a target for broadly neutralizing antibodies. FEBS J. 2015;282:4679-91.
21. Calarese DA, Scanlan CN, Zwick MB, Deechongkit S, Mimura Y, Kunert R, Zhu P, Wormald MR, Stanfield RL, Roux KH, et al. Antibody domain exchange is an immunological solution to carbohydrate cluster recognition. Science. 2003;300:2065-71.
22. Doores KJ, Fulton Z, Huber M, Wilson IA, Burton DR. Antibody 2G12 recognizes di-mannose equivalently in domain- and nondomain-exchanged forms but only binds the HIV-1 glycan shield if domain exchanged. J Virol. 2010;84:10690-9.
23. Julien JP, Sok D, Khayat R, Lee JH, Doores KJ, Walker LM, Ramos A, Diwanji DC, Pejchal R, Cupo A, et al. Broadly neutralizing antibody PGT121 allosterically modulates CD4 binding via recognition of the HIV-1 gp120 V3 base and multiple surrounding glycans. PLoS Pathog. 2013;9:e1003342.
24. Garces F, Sok D, Kong L, McBride R, Kim HJ, Saye-Francisco KF, Julien JP, Hua Y, Cupo A, Moore JP, et al. Structural Evolution of Glycan Recognition by a Family of Potent HIV Antibodies. Cell. 2014;159:69-79.
25. Barouch DH, Whitney JB, Moldt B, Klein F, Oliveira TY, Liu J, Stephenson KE, Chang HW, Shekhar K, Gupta S, et al. Therapeutic efficacy of potent neutralizing HIV-1-specific monoclonal antibodies in SHIV-infected rhesus monkeys. Nature. 2013;503:224-8.
26. Doores KJ, Kong L, Krumm SA, Le KM, Sok D, Laserson U, Garces F, Poignard P, Wilson IA, Burton DR. Two classes of broadly neutralizing antibodies within a single lineage directed to the high-mannose patch of HIV envelope. J Virol. 2015;89:1105-18.
27. Sok D, Doores KJ, Briney B, Le KM, Saye-Francisco KL, Ramos A, Kulp DW, Julien JP, Menis S, Wickramasinghe L, et al. Promiscuous glycan site recognition by antibodies to the high-mannose patch of gp120 broadens neutralization of HIV. Sci Transl Med. 2014;6:236ra263.
28. Sok D, Laserson U, Laserson J, Liu Y, Vigneault F, Julien JP, Briney B, Ramos A, Saye KF, Le K, et al. The effects of somatic hypermutation on neutralization and binding in the PGT121 family of broadly neutralizing HIV antibodies. PLoS Pathog. 2013;9:e1003754.
29. Klein F, Halper-Stromberg A, Horwitz JA, Gruell H, Scheid JF, Bournazos S, Mouquet H, Spatz LA, Diskin R, Abadir A, et al. HIV therapy by a combination of broadly neutralizing antibodies in humanized mice. Nature. 2012;492:118-22.
30. Moore PL, Gray ES, Wibmer CK, Bhiman JN, Nonyane M, Sheward DJ, Hermanus T, Bajimaya S, Tumba NL, Abrahams MR, et al. Evolution of an HIV glycan-dependent broadly neutralizing antibody epitope through immune escape. Nat Med. 2012;18:1688-92.
31. Sadjadpour R, Donau OK, Shingai M, Buckler-White A, Kao S, Strebel K, Nishimura Y, Martin MA. Emergence of gp120 V3 variants confers neutralization resistance in an R5 simian-human immunodeficiency virus-infected macaque elite neutralizer that targets the N332 glycan of the human immunodeficiency virus type 1 envelope glycoprotein. J Virol. 2013;87:8798-804.
32. Gao F, Bonsignori M, Liao HX, Kumar A, Xia SM, Lu X, Cai F, Hwang KK, Song H, Zhou T, et al. Cooperation of B cell lineages in induction of HIV-1-broadly neutralizing antibodies. Cell. 2014;158:481-91.
33. Doria-Rose NA, Schramm CA, Gorman J, Moore PL, Bhiman JN, DeKosky BJ, Ernandes MJ, Georgiev IS, Kim HJ, Pancera M, et al. Developmental pathway for potent V1V2-directed HIV-neutralizing antibodies. Nature. 2014;509:55-62.
34. Murphy MK, Yue L, Pan R, Boliar S, Sethi A, Tian J, Pfafferot K, Karita E, Allen SA, Cormier E, et al. Viral escape from neutralizing antibodies in early subtype A HIV-1 infection drives an increase in autologous neutralization breadth. PLoS Pathog. 2013;9:e1003173.
35. Falkowska E, Ramos A, Feng Y, Zhou T, Moquin S, Walker LM, Wu X, Seaman MS, Wrin T, Kwong PD, et al. PGV04, an HIV-1 gp120 CD4 binding site antibody, is broad and potent in neutralization but does not induce conformational changes characteristic of CD4. J Virol. 2012;86:4394-403.
36. Doores KJ, Burton DR. Variable loop glycan dependency of the broad and potent HIV-1-neutralizing antibodies PG9 and PG16. J Virol. 2010;84:10510-21.
37. Pritchard LK, Spencer DI, Royle L, Vasiljevic S, Krumm SA, Doores KJ, Crispin M. Glycan microheterogeneity at the PGT135 antibody recognition site on HIV-1 gp120 reveals a molecular mechanism for neutralization resistance. J Virol. 2015;89:6952-9.
38. Garces F, Lee JH, de Val N, de la Pena Torrents A, Kong L, Puchades C, Hua Y, Stanfield RL, Burton DR, Moore JP, et al. Affinity maturation of a potent family of HIV antibodies is primarily focused on accommodating or avoiding glycans. Immunity. 2015;43:1053-63.
39. Lee JH, de Val N, Lyumkis D, Ward AB. Model building and refinement of a natively glycosylated HIV-1 env protein by high-resolution cryoelectron microscopy. Structure. 2015;23:1943-51.
40. Kong L, de la Pena Torrents A, Deller MC, Garces F, Sliepen K, Hua Y, Stanfield RL, Sanders RW, Wilson IA. Complete epitopes for vaccine design derived from a crystal structure of the broadly neutralizing antibodies PGT128 and 8ANC195 in complex with an HIV-1 Env trimer. Acta Crystallogr D Biol Crystallogr. 2015;71:2099-108.
41. Zhou T, Zhu J, Yang Y, Gorman J, Ofek G, Srivatsan S, Druz A, Lees CR, Lu G, Soto C, et al. Transplanting supersites of HIV-1 vulnerability. PLoS One. 2014;9:e99881.
42. Simek MD, Rida W, Priddy FH, Pung P, Carrow E, Laufer DS, Lehrman JK, Boaz M, Tarragona-Fiol T, Miiro G, et al. 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. 2009;83:7337-48.
43. Schweighardt B, Liu Y, Huang W, Chappey C, Lie YS, Petropoulos CJ, Wrin T. Development of an HIV-1 reference panel of subtype B envelope clones isolated from the plasma of recently infected individuals. J Acquir Immune Defic Syndr. 2007;46:1-11.
44. Li M, Gao F, Mascola JR, Stamatatos L, Polonis VR, Koutsoukos M, Voss G, Goepfert P, Gilbert P, Greene KM, et al. Human immunodeficiency virus type 1 env clones from acute and early subtype B infections for standardized assessments of vaccine-elicited neutralizing antibodies. J Virol. 2005;79:10108-25.
45. Montefiori DC: Evaluating neutralizing antibodies against HIV, SIV, and SHIV in luciferase reporter gene assays. Curr Protoc Immunol/edited by John E Coligan [et al]. 2005; Chapter 12:Unit 12. 11.