Anti-HIV-1 antibodies 2F5 and 4E10 interact differently with lipids to bind their epitopes

AIDS

Volumn 25, Issue 4, 2011, Pages 419-428

  Franquelim, Henri G ^a   Chiantia, Salvatore ^b   Veiga, Ana Salomé ^a,c   Santos, Nuno C ^a   Schwille, Petra ^b   Castanho, Miguel A R B ^a  

^a INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

2F5; 4E10; gp41; HIV 1; membrane proximal external region; microscopy; supported lipid bilayers

Indexed keywords

1,2 DIOLEYL SN GLYCRO 3 PHOSPHOCHOLINE; CHOLINE; EPITOPE; GLYCOPROTEIN GP 41; MONOCLONAL ANTIBODY 2F5; MONOCLONAL ANTIBODY 4E10; UNCLASSIFIED DRUG;

ATOMIC FORCE MICROSCOPY; CONFERENCE PAPER; CONFOCAL MICROSCOPY; FLUORESCENCE MICROSCOPY; LIPID BILAYER; MEMBRANE BINDING; MEMBRANE PROXIMAL EXTERNAL REGION; MOLECULAR INTERACTION; PRIORITY JOURNAL; VIRUS ENVELOPE;

ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; ANTIBODY SPECIFICITY; EPITOPES; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP41; HIV-1; HUMANS; LIPIDS; PROTEIN BINDING;

EID: 79951514918     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0b013e328342ff11     Document Type: Conference Paper

References (54)

1. Chan DC, Kim PS. HIV entry and its inhibition. Cell 1998; 93:681-684. (Pubitemid 28257575)
2. Root MJ, Steger HK. HIV-1 gp41 as a target for viral entry inhibition. Curr Pharm Des 2004; 10:1805-1825. (Pubitemid 38647463)
3. Castagna A, Biswas P, Beretta A, Lazzarin A. The appealing story of HIV entry inhibitors: from discovery of biological mechanisms to drug development. Drugs 2005; 65:879-904. (Pubitemid 40663619)
4. Montero M, van Houten NE, Wang X, Scott JK. The membrane-proximal external region of the human immunodeficiency virus type 1 envelope: dominant site of antibody neutralization and target for vaccine design. Microbiol Mol Biol Rev 2008; 72: 54-84. (Pubitemid 351398055)
5. Nelson JD, Brunel FM, Jensen R, Crooks ET, Cardoso RM, Wang M, et al. An affinity-enhanced neutralizing antibody against the membrane-proximal external region of human immunodeficiency virus type 1 gp41 recognizes an epitope between those of 2F5 and 4E10. J Virol 2007; 81:4033-4043. (Pubitemid 46586898)
6. Muster T, Steindl F, Purtscher M, Trkola A, Klima A, Himmler G, et al. A conserved neutralizing epitope on gp41 of human immunodeficiency virus type 1. J Virol 1993; 67:6642-6647. (Pubitemid 23309131)
7. Zwick MB, Labrijn AF, Wang M, Spenlehauer C, Saphire EO, Binley JM, et al. Broadly neutralizing antibodies targeted to the membrane-proximal external region of human immunodeficiency virus type 1 glycoprotein gp41. J Virol 2001; 75:10892-10905. (Pubitemid 33034579)
8. Bures R, Gaitan A, Zhu T, Graziosi C, McGrath KM, Tartaglia J, et al. Immunization with recombinant canarypox vectors expressing membrane-anchored glycoprotein 120 followed by glycoprotein 160 boosting fails to generate antibodies that neutralize R5 primary isolates of human immunodeficiency virus type 1. AIDS Res Hum Retroviruses 2000; 16:2019-2035. (Pubitemid 32048460)
9. Gao F, Weaver EA, Lu Z, Li Y, Liao HX, Ma B, et al. Antigenicity and immunogenicity of a synthetic human immunodeficiency virus type 1 group m consensus envelope glycoprotein. J Virol 2005; 79:1154-1163. (Pubitemid 40053898)
10. Zhu P, Liu J, Bess J Jr, Chertova E, Lifson JD, Grise H, et al. Distribution and three-dimensional structure of AIDS virus envelope spikes. Nature 2006; 441:847-852.
11. Alam SM, Morelli M, Dennison SM, Liao HX, Zhang R, Xia SM, et al. Role of HIV membrane in neutralization by two broadly neutralizing antibodies. Proc Natl Acad Sci USA 2009; 106:20234-20239.
12. Suarez T, Nir S, Goni FM, Saez-Cirion A, Nieva JL. The pre-transmembrane region of the human immunodeficiency virus type-1 glycoprotein: a novel fusogenic sequence. FEBS Lett 2000; 477:145-149. (Pubitemid 30438873)
13. Lorizate M, Huarte N, Saez-Cirion A, Nieva JL. Interfacial pretransmembrane domains in viral proteins promoting membrane fusion and fission. Biochim Biophys Acta 2008; 1778: 1624-1639.
14. Sun ZY, Oh KJ, Kim M, Yu J, Brusic V, Song L, et al. HIV-1 broadly neutralizing antibody extracts its epitope from a kinked gp41 ectodomain region on the viral membrane. Immunity 2008; 28:52-63.
15. Veiga AS, Castanho MA. The influence of cholesterol on the interaction of HIV gp41 membrane proximal region-derived peptides with lipid bilayers. FEBS J 2007; 274:5096-5104. (Pubitemid 47481181)
16. Saez-Cirion A, Nir S, Lorizate M, Agirre A, Cruz A, Perez-Gil J, Nieva JL. Sphingomyelin and cholesterol promote HIV-1 gp41 pretransmembrane sequence surface aggregation and membrane restructuring. J Biol Chem 2002; 277:21776-21785. (Pubitemid 34952329)
17. Trkola A, Pomales AB, Yuan H, Korber B, Maddon PJ, Allaway GP, et al. Cross-clade neutralization of primary isolates of human immunodeficiency virus type 1 by human monoclonal antibodies and tetrameric CD4-IgG. J Virol 1995; 69:6609-6617.
18. Stiegler G, Kunert R, Purtscher M, Wolbank S, Voglauer R, Steindl F, Katinger H. A potent cross-clade neutralizing human monoclonal antibody against a novel epitope on gp41 of human immunodeficiency virus type 1. AIDS Res Hum Retro-viruses 2001; 17:1757-1765. (Pubitemid 34114213)
19. Julg B, Goebel FD. What's new inHIV/AIDS? Neutralizing HIV antibodies: do they really protect? Infection 2005; 33:405-407. (Pubitemid 41552024)
20. Vcelar B, Stiegler G, Wolf HM, Muntean W, Leschnik B, Mehandru S, et al. Reassessment of autoreactivity of the broadly neutralizing HIV antibodies 4E10 and 2F5 and retrospective analysis of clinical safety data. AIDS 2007; 21:2161-2170. (Pubitemid 350287213)
21. Grundner C, Mirzabekov T, Sodroski J, Wyatt R. Solid-phase proteoliposomes containing human immunodeficiency virus envelope glycoproteins. J Virol 2002; 76:3511-3521. (Pubitemid 34224552)
22. Lenz O, Dittmar MT, Wagner A, Ferko B, Vorauer-Uhl K, Stiegler G, Weissenhorn W. Trimeric membrane-anchored gp41 inhibits HIV membrane fusion. J Biol Chem 2005; 280:4095-4101. (Pubitemid 40288573)
23. Ofek G, Tang M, Sambor A, Katinger H, Mascola JR, Wyatt R, Kwong PD. Structure and mechanistic analysis of the antihu-man immunodeficiency virus type 1 antibody 2F5 in complex with its gp41 epitope. J Virol 2004; 78:10724-10737. (Pubitemid 39258398)
24. Cardoso RM, Zwick MB, Stanfield RL, Kunert R, Binley JM, Katinger H, et al. Broadly neutralizing anti-HIV antibody 4E10 recognizes a helical conformation of a highly conserved fusion-associated motif in gp41. Immunity 2005; 22:163-173. (Pubitemid 40255708)
25. Julien JP, Bryson S, Nieva JL, Pai EF. 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 2008; 384:377-392.
26. Veiga AS, Castanho MA. The membranes' role in the HIV-1 neutralizing monoclonal antibody 2F5 mode of action needs re-evaluation. Antiviral Res 2006; 71:69-72.
27. Veiga AS, Pattenden LK, Fletcher JM, Castanho MA, Aguilar MI. Interactions of HIV-1 antibodies 2F5 and 4E10 with a gp41 epitope prebound to host and viral membrane model systems. Chembiochem 2009; 10:1032-1044.
28. Haynes BF, Fleming J, St Clair EW, Katinger H, Stiegler G, Kunert R, et al. Cardiolipin polyspecific autoreactivity in two broadly neutralizing HIV-1 antibodies. Science 2005; 308: 1906-1908. (Pubitemid 40941873)
29. Sanchez-Martinez S, Lorizate M, Hermann K, Kunert R, Basanez G, Nieva JL. Specific phospholipid recognition by human immunodeficiency virus type-1 neutralizing antigp41 2F5 antibody. FEBS Lett 2006; 580:2395-2399. (Pubitemid 43675634)
30. Sanchez-Martinez S, Lorizate M, Katinger H, Kunert R, Nieva JL. Membrane association and epitope recognition by HIV-1 neutralizing antigp41 2F5 and 4E10 antibodies. AIDS Res Hum Retroviruses 2006; 22:998-1006. (Pubitemid 46100685)
31. Alam SM, McAdams M, Boren D, Rak M, Scearce RM, Gao F, et al. The role of antibody polyspecificity and lipid reactivity in binding of broadly neutralizing anti-HIV-1 envelope human monoclonal antibodies 2F5 and 4E10 to glycoprotein 41 membrane proximal envelope epitopes. J Immunol 2007; 178:4424-4435. (Pubitemid 46492394)
32. Beck Z, Karasavvas N, Tong J, Matyas GR, Rao M, Alving CR. Calcium modulation of monoclonal antibody binding to phos-phatidylinositol phosphate. Biochem Biophys Res Commun 2007; 354:747-751. (Pubitemid 46186248)
33. Brown BK, Karasavvas N, Beck Z, Matyas GR, Birx DL, Polonis VR, Alving CR. Monoclonal antibodies to phosphatidylinositol phosphate neutralize human immunodeficiency virus type 1: role of phosphate-binding subsites. J Virol 2007; 81:2087-2091. (Pubitemid 46214483)
34. Alving CR. 4E10 and 2F5 monoclonal antibodies: binding specificities to phospholipids, tolerance, and clinical safety issues. AIDS 2008; 22:649-651. (Pubitemid 351640599)
35. Beck Z, Karasavvas N, Matyas GR, Alving CR. Membrane-specific antibodies induced by liposomes can simultaneously bind to HIV-1 protein, peptide, and membrane lipid epitopes. J Drug Target 2008; 16:535-542.
36. Huarte N, Lorizate M, Kunert R, Nieva JL. Lipid modulation of membrane-bound epitope recognition and blocking by HIV-1 neutralizing antibodies. FEBS Lett 2008; 582:3798-3804.
37. Huarte N, Lorizate M, Maeso R, Kunert R, Arranz R, Valpuesta JM, Nieva JL. The broadly neutralizing antihuman immunodeficiency virus type 1 4E10 monoclonal antibody is better adapted to membrane-bound epitope recognition and blocking than 2F5. J Virol 2008; 82:8986-8996.
38. Matyas GR, Beck Z, Karasavvas N, Alving CR. Lipid binding propertiesof 4E10, 2F5, and WR304 monoclonal antibodies that neutralize HIV-1. Biochim Biophys Acta 2009; 1788:660-665.
39. Matyas GR, Wieczorek L, Beck Z, Ochsenbauer-Jambor C, Kappes JC, Michael NL, et al. Neutralizing antibodies induced by liposomal HIV-1 glycoprotein 41 peptide simultaneously bind to both the 2F5 or 4E10 epitope and lipid epitopes. AIDS 2009; 23:2069-2077.
40. Julien JP, HuarteN,MaesoR, Taneva SG, CunninghamA, Nieva JL, Pai EF. 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 2010; 84:4136-4147.
41. Pejchal R, Gach JS, Brunel FM, Cardoso RM, Stanfield RL, Dawson PE, et al. A conformational switch in human immunodeficiency virus gp41 revealed by the structures of overlapping epitopes recognized by neutralizing antibodies. J Virol 2009; 83:8451-8462.
42. Scherer EM, Leaman DP, Zwick MB, McMichael AJ, Burton DR. Aromatic residues at the edge of the antibody combining site facilitate viral glycoprotein recognition through membrane interactions. Proc Natl Acad Sci USA 2010; 107:1529-1534.
43. Shen X, Dennison SM, Liu P, Gao F, Jaeger F, Montefiori DC, et al. Prolonged exposure of the HIV-1 gp41 membrane proximal region with L669S substitution. Proc Natl Acad Sci USA 2010; 107:5972-5977.
44. Xu H, Song L, Kim M, Holmes MA, Kraft Z, Sellhorn G, et al. Interactions between lipids and human anti-HIV antibody 4E10 can be reduced without ablating neutralizing activity. J Virol 2010; 84:1076-1088.
45. Chiantia S, Kahya N, Schwille P. Dehydration damage of domain-exhibiting supported bilayers: an AFM study on the protective effects of disaccharides and other stabilizing substances. Langmuir 2005; 21:6317-6323. (Pubitemid 41006445)
46. Chiantia S, Kahya N, Ries J, Schwille P. Effects of ceramide on liquid-ordered domains investigated by simultaneous AFM and FCS. Biophys J 2006; 90:4500-4508. (Pubitemid 43830895)
47. Chiantia S, Ries J, Schwille P. Fluorescence correlation spectro-scopy in membrane structure elucidation. Biochim Biophys Acta 2009; 1788:225-233.
48. Ries J, Chiantia S, Schwille P. Accurate determination of membrane dynamics with line-scan FCS. Biophys J 2009; 96:1999-2008.
49. Filippov A, Oradd G, Lindblom G. Lipid lateral diffusion in ordered and disordered phases in raft mixtures. Biophys J 2004; 86:891-896. (Pubitemid 38209533)
50. Chiantia S, Ries J, Kahya N, Schwille P. Combined AFM and two-focus SFCS study of raft-exhibiting model membranes. Chemphyschem 2006; 7:2409-2418.
51. Brugger B, Glass B, Haberkant P, Leibrecht I, Wieland FT, Krausslich HG. The HIV lipidome: a raft with an unusual composition. Proc Natl Acad Sci USA 2006; 103:2641-2646.
52. Moreno MR, Pascual R, Villalain J. Identification of membrane-active regions of the HIV-1 envelope glycoprotein gp41 using a 15-mer gp41-peptide scan. Biochim Biophys Acta 2004; 1661:97-105. (Pubitemid 38201575)
53. Dennison SM, Stewart SM, Stempel KC, Liao HX, Haynes BF, Alam SM. Stable docking of neutralizing human immunodeficiency virus type 1 gp41 membrane-proximal external region monoclonal antibodies 2F5 and 4E10 is dependent on the membrane immersion depth of their epitope regions. J Virol 2009; 83:10211-10223.
54. Song L, Sun ZY, Coleman KE, Zwick MB, Gach JS, Wang JH, et al. Broadly neutralizing anti-HIV-1 antibodies disrupt a hinge-related function of gp41 at the membrane interface. Proc Natl Acad Sci USA 2009; 106:9057-9062.