Structural basis for HIV-1 neutralization by 2F5-like antibodies m66 and m66.6

Journal of Virology

Volumn 88, Issue 5, 2014, Pages 2426-2441

  Ofek, Gilad ^a   Zirkle, Brett ^a   Yang, Yongping ^a   Zhu, Zhongyu ^b   McKee, Krisha ^a   Zhang, Baoshan ^a   Chuang, Gwo Yu ^a   Georgiev, Ivelin S ^a   O'Dell, Sijy ^a   Doria Rose, Nicole ^a   Mascola, John R ^a   Dimitrov, Dimiter S ^b   Kwong, Peter D ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN GP 41; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 2F5; MONOCLONAL ANTIBODY M66; MONOCLONAL ANTIBODY M66.6; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANTIGEN BINDING; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA CONFORMATION; HUMAN IMMUNODEFICIENCY VIRUS 1; MUTAGENESIS; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; VIRUS MORPHOLOGY; VIRUS NEUTRALIZATION;

AMINO ACID SEQUENCE; ANTIBODIES, NEUTRALIZING; ANTIGEN-ANTIBODY COMPLEX; COMPLEMENTARITY DETERMINING REGIONS; EPITOPES; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP41; HIV-1; HUMANS; MODELS, MOLECULAR; MOLECULAR DOCKING SIMULATION; MOLECULAR SEQUENCE DATA; MUTATION; NEUTRALIZATION TESTS; PEPTIDES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS;

EID: 84896737636     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02837-13     Document Type: Article

References (45)

1. Kwong PD, Mascola JR. 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.
2. Salzwedel K, West JT, Hunter E. 1999. A conserved tryptophan-rich motif in the membrane-proximal region of the human immunodeficiency virus type 1 gp41 ectodomain is important for Env-mediated fusion and virus infectivity. J. Virol. 73:2469-2480.
3. Munoz-Barroso I, Salzwedel K, Hunter E, Blumenthal R. 1999. Role of the membrane-proximal domain in the initial stages of human immunodeficiency virus type 1 envelope glycoprotein-mediated membrane fusion. J. Virol. 73:6089-6092.
4. Shang L, Yue L, Hunter E. 2008. Role of the membrane-spanning domain of human immunodeficiency virus type 1 envelope glycoprotein in cell-cell fusion and virus infection. J. Virol. 82:5417-5428. http://dx.doi.org/10.1128/JVI.02666-07.
5. Suarez T, Gallaher WR, Agirre A, Goni FM, Nieva JL. 2000. Membrane interface-interacting sequences within the ectodomain of the human immunodeficiency virus type 1 envelope glycoprotein: putative role during viral fusion. J. Virol. 74:8038-8047. http://dx.doi.org/10.1128/JVI.74.17.8038-8047.2000.
6. 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, Connors M. 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.
7. Gray ES, Taylor N, Wycuff D, Moore PL, Tomaras GD, Wibmer CK, Puren A, DeCamp A, Gilbert PB, Wood B, Montefiori DC, Binley JM, Shaw GM, Haynes BF, Mascola JR, Morris L. 2009. Antibody specificities associated with neutralization breadth in plasma from human immunodeficiency virus type 1 subtype C-infected blood donors. J. Virol. 83: 8925-8937. http://dx.doi.org/10.1128/JVI.00758-09.
8. Zhu Z, Qin HR, Chen W, Zhao Q, Shen X, Schutte R, Wang Y, Ofek G, Streaker E, Prabakaran P, Fouda GG, Liao HX, Owens J, Louder M, Yang Y, Klaric KA, Moody MA, Mascola JR, Scott JK, Kwong PD, Montefiori D, Haynes BF, Tomaras GD, Dimitrov DS. 2011. Crossreactive HIV-1-neutralizing human monoclonal antibodies identified from a patient with 2F5-like antibodies. J. Virol. 85:11401-11408. http://dx.doi.org/10.1128/JVI.05312-11.
9. Muster T, Steindl F, Purtscher M, Trkola A, Klima A, Himmler G, Ruker F, Katinger H. 1993. A conserved neutralizing epitope on gp41 of human immunodeficiency virus type 1. J. Virol. 67:6642-6647.
10. Zwick MB, Labrijn AF, Wang M, Spenlehauer C, Saphire EO, Binley JM, Moore JP, Stiegler G, Katinger H, Burton DR, Parren PW. 2001. Broadly neutralizing antibodies targeted to the membrane-proximal external region of human immunodeficiency virus type 1 glycoprotein gp41. J. Virol. 75: 10892-10905. http://dx.doi.org/10.1128/JVI.75.22.10892-10905.2001.
11. Nelson JD, Brunel FM, Jensen R, Crooks ET, Cardoso RM, Wang M, Hessell A, Wilson IA, Binley JM, Dawson PE, Burton DR, Zwick MB. 2007. An affinity-enhanced neutralizing antibody against the membraneproximal external region of human immunodeficiency virus type 1 gp41 recognizes an epitope between those of 2F5 and 4E10. J. Virol. 81:4033- 4043. http://dx.doi.org/10.1128/JVI.02588-06.
12. Morris L, Chen X, Alam M, Tomaras G, Zhang R, Marshall DJ, Chen B, Parks R, Foulger A, Jaeger F, Donathan M, Bilska M, Gray ES, Abdool Karim SS, Kepler TB, Whitesides J, Montefiori D, Moody MA, Liao HX, Haynes BF. 2011. Isolation of a human anti-HIV gp41 membrane proximal region neutralizing antibody by antigen-specific single B cell sorting. PLoS One 6:e23532. http://dx.doi.org/10.1371/journal.pone .0023532.
13. Kim M, Sun ZY, Rand KD, Shi X, Song L, Cheng Y, Fahmy AF, Majumdar S, Ofek G, Yang Y, Kwong PD, Wang JH, Engen JR, Wagner G, Reinherz EL. 2011. Antibody mechanics on a membrane-bound HIV segment essential for GP41-targeted viral neutralization. Nat. Struct. Mol. Biol. 18:1235-1243. http://dx.doi.org/10.1038/nsmb.2154.
14. Sun ZY, Oh KJ, Kim M, Yu J, Brusic V, Song L, Qiao Z, Wang JH, Wagner G, Reinherz EL. 2008. HIV-1 broadly neutralizing antibody extracts its epitope from a kinked gp41 ectodomain region on the viral membrane. Immunity 28:52-63. http://dx.doi.org/10.1016/j.immuni.2007.11.018.
15. Ofek G, Tang M, Sambor A, Katinger H, Mascola JR, Wyatt R, Kwong PD. 2004. Structure and mechanistic analysis of the anti-human immunodeficiency virus type 1 antibody 2F5 in complex with its gp41 epitope. J. Virol. 78:10724-10737. http://dx.doi.org/10.1128/JVI.78.19.10724-10737.2004.
16. Haynes BF, Fleming J, St Clair EW, Katinger H, Stiegler G, Kunert R, Robinson J, Scearce RM, Plonk K, Staats HF, Ortel TL, Liao HX, Alam SM. 2005. Cardiolipin polyspecific autoreactivity in two broadly neutralizing HIV-1 antibodies. Science 308:1906-1908. http://dx.doi.org/10.1126/science.1111781.
17. Frey G, Peng H, Rits-Volloch S, Morelli M, Cheng Y, Chen B. 2008. A fusion-intermediate state of HIV-1 gp41 targeted by broadly neutralizing antibodies. Proc. Natl. Acad. Sci. U. S. A. 105:3739-3744. http://dx.doi.org/10.1073/pnas.0800255105.
18. Golding H, Zaitseva M, de Rosny E, King LR, Manischewitz J, Sidorov I, Gorny MK, Zolla-Pazner S, Dimitrov DS, Weiss CD. 2002. Dissection of human immunodeficiency virus type 1 entry with neutralizing antibodies to gp41 fusion intermediates. J. Virol. 76:6780-6790. http://dx.doi.org/10.1128/JVI.76.13.6780-6790.2002.
19. de Rosny E, Vassell R, Jiang S, Kunert R, Weiss CD. 2004. Binding of the 2F5 monoclonal antibody to native and fusion-intermediate forms of human immunodeficiency virus type 1 gp41: implications for fusioninducing conformational changes. J. Virol. 78:2627-2631. http://dx.doi.org/10.1128/JVI.78.5.2627-2631.2004.
20. Julien JP, Huarte N, Maeso R, Taneva SG, Cunningham A, Nieva JL, Pai EF. 2010. Ablation of the complementarity-determining region H3 apex of the anti-HIV-1 broadly neutralizing antibody 2F5 abrogates neutralizing capacity without affecting core epitope binding. J. Virol. 84: 4136-4147. http://dx.doi.org/10.1128/JVI.02357-09.
21. Ofek G, McKee K, Yang Y, Yang ZY, Skinner J, Guenaga FJ, Wyatt R, Zwick MB, Nabel GJ, Mascola JR, Kwong PD. 2010. Relationship between antibody 2F5 neutralization of HIV-1 and hydrophobicity of its heavy chain third complementarity-determining region. J. Virol. 84: 2955-2962. http://dx.doi.org/10.1128/JVI.02257-09.
22. Nicely NI, Dennison SM, Spicer L, Scearce RM, Kelsoe G, Ueda Y, Chen H, Liao HX, Alam SM, Haynes BF. 2010. Crystal structure of a nonneutralizing antibody to the HIV-1 gp41 membrane-proximal external region. Nat. Struct. Mol. Biol. 17:1492-1494. http://dx.doi.org/10.1038/nsmb.1944.
23. Cardoso RM, Zwick MB, Stanfield RL, Kunert R, Binley JM, Katinger H, Burton DR, Wilson IA. 2005. Broadly neutralizing anti-HIV antibody 4E10 recognizes a helical conformation of a highly conserved fusionassociated motif in gp41. Immunity 22:163-173. http://dx.doi.org/10.1016/j.immuni.2004.12.011.
24. Pejchal R, Gach JS, Brunel FM, Cardoso RM, Stanfield RL, Dawson PE, Burton DR, Zwick MB, Wilson IA. 2009. A conformational switch in human immunodeficiency virus gp41 revealed by the structures of overlapping epitopes recognized by neutralizing antibodies. J. Virol. 83:8451- 8462. http://dx.doi.org/10.1128/JVI.00685-09.
25. Julien JP, Bryson S, Nieva JL, Pai EF. 2008. Structural details of HIV-1 recognition by the broadly neutralizing monoclonal antibody 2F5: epitope conformation, antigen-recognition loop mobility, and anion-binding site. J. Mol. Biol. 384:377-392. http://dx.doi.org/10.1016/j.jmb.2008.09.024.
26. Shen X, Parks RJ, Montefiori DC, Kirchherr JL, Keele BF, Decker JM, Blattner WA, Gao F, Weinhold KJ, Hicks CB, Greenberg ML, Hahn BH, Shaw GM, Haynes BF, Tomaras GD. 2009. In vivo gp41 antibodies targeting the 2F5 monoclonal antibody epitope mediate human immunodeficiency virus type 1 neutralization breadth. J. Virol. 83:3617-3625. http://dx.doi.org/10.1128/JVI.02631-08.
27. 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.
28. Ofek G, Guenaga FJ, Schief WR, Skinner J, Baker D, Wyatt R, Kwong PD. 2010. Elicitation of structure-specific antibodies by epitope scaffolds. Proc. Natl. Acad. Sci. U. S. A. 107:17880-17887. http://dx.doi.org/10.1073/pnas.1004728107.
29. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:307-326. http://dx.doi.org/10.1016/S0076-6879(97)76066-X.
30. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. J. Appl. Crystallogr. 40: 658-674. http://dx.doi.org/10.1107/S0021889807021206.
31. Guex N, Peitsch MC. 1997. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18: 2714-2723. http://dx.doi.org/10.1002/elps.1150181505.
32. Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, Moriarty NW, Read RJ, Sacchettini JC, Sauter NK, Terwilliger TC. 2002. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. Sect. D Biol. Crystallogr. 58: 1948-1954. http://dx.doi.org/10.1107/S0907444902016657.
33. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. Sect. D Biol. Crystallogr. 60:2126-2132. http://dx.doi.org/10.1107/S0907444904019158.
34. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, Wang X, Murray LW, Arendall WB, Snoeyink J, Richardson JS, Richardson DC. 2007. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic acids research 35:W375-W383. http://dx.doi.org/10.1093/nar/gkm216.
35. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA. 2001. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. U. S. A. 98:10037-10041. http://dx.doi.org/10.1073/pnas.181342398.
36. McDonald IK, Thornton JM. 1994. Satisfying hydrogen-bonding potential in proteins. J. Mol. Biol. 238:777-793. http://dx.doi.org/10.1006/jmbi.1994.1334.
37. Krissinel E, Henrick K. 2007. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372:774-797. http://dx.doi.org/10.1016/j.jmb.2007.05.022.
38. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A, McNicholas SJ, Murshudov GN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A, Wilson KS. 2011. Overview of the CCP4 suite and current developments. Acta Crystallogr. Sect. D Biol. Crystallogr. 67:235-242. http://dx.doi.org/10.1107/S0907444910045749.
39. 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.
40. Brugger B, Glass B, Haberkant P, Leibrecht I, Wieland FT, Krausslich HG. 2006. The HIV lipidome: a raft with an unusual composition. Proc. Natl. Acad. Sci. U. S. A. 103:2641-2646. http://dx.doi.org/10.1073/pnas.0511136103.
41. Snider C, Jayasinghe S, Hristova K, White SH. 2009. MPEx: a tool for exploring membrane proteins. Protein Sci. 18:2624-2628. http://dx.doi.org/10.1002/pro.256.
42. Wimley WC, White SH. 1996. Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nat. Struct. Biol. 3:842-848. http://dx.doi.org/10.1038/nsb1096-842.
43. Chuang GY, Acharya P, Schmidt SD, Yang Y, Louder MK, Zhou T, Kwon YD, Pancera M, Bailer RT, Doria-Rose NA, Nussenzweig MC, Mascola JR, Kwong PD, Georgiev IS. 2013. Residue-level prediction of HIV-1 antibody epitopes based on neutralization of diverse viral strains. J. Virol. 87:10047-10058. http://dx.doi.org/10.1128/JVI.00984-13.
44. Doria-Rose NA, Georgiev I, O'Dell S, Chuang GY, Staupe RP, McLellan JS, Gorman J, Pancera M, Bonsignori M, Haynes BF, Burton DR, Koff WC, Kwong PD, Mascola JR. 2012. A short segment of the HIV-1 gp120 V1/V2 region is a major determinant of resistance to V1/V2 neutralizing antibodies. J. Virol. 86:8319-8323. http://dx.doi.org/10.1128/JVI.00696-12.
45. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66: 213-221. http://dx.doi.org/10.1107/S0907444909052925.