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

Journal of Virology

Volumn 83, Issue 19, 2009, Pages 10211-10223

  Dennison, S Moses ^a   Stewart, Shelley M ^a   Stempel, Kathryn C ^a   Liao, Hua Xin ^a   Haynes, Barton F ^a   Alam, S Munir ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; EPITOPE; GLYCOPROTEIN GP 41; LIPID; LIPOSOME; MEMBRANE LIPID; MONOCLONAL ANTIBODY 2F5; MONOCLONAL ANTIBODY 4E10; NEUTRALIZING ANTIBODY;

ANTIGEN BINDING; ARTICLE; BINDING KINETICS; CIRCULAR DICHROISM; CONTROLLED STUDY; ENERGY TRANSFER; FLUORESCENCE; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN IMMUNODEFICIENCY VIRUS 1; HYDROPHOBICITY; LIPID BILAYER; NONHUMAN; PHOTOCHEMICAL QUENCHING; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; SPECTROSCOPY; TEMPERATURE SENSITIVITY; THERMODYNAMICS; VIRUS ENVELOPE; VIRUS MORPHOLOGY; VIRUS NEUTRALIZATION;

ANTIBODIES, MONOCLONAL; CELL MEMBRANE; CIRCULAR DICHROISM; EPITOPES; FLUORESCENCE RESONANCE ENERGY TRANSFER; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP41; KINETICS; LIPOSOMES; NEUTRALIZATION TESTS; PEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; SURFACE PLASMON RESONANCE; TEMPERATURE;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 70349272203     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00571-09     Document Type: Article

References (32)

1. Alam, S. M., S. Dennison, M. Morelli, H. Liao, R. Zhang, B. F. Haynes, S. C. Harrison, and B. Chen. 2008. The role of lipid reactivity of HIV-1 gp41 membrane proximal antibodies in neutralization of HIV-1: novel liposome based immunogen design, abstr. OA07 to 06. Abstracts from AIDS Vaccine 2008, Cape Town, South Africa. October 13-16, 2008. AIDS Res. Hum Retrovir. 24(Suppl. 1):23-24.
2. Alam, S. M., M. McAdams, D. Boren, M. Rak, R. M. Scearce, F. Gao, Z. T. Camacho, D. Gewirth, G. Kelsoe, P. Chen, and B. F. Haynes. 2007. 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. 178:4424-4435.
3. Andrade, M. A., P. Chacon, J. J. Merelo, and F. Moran. 1993. Evaluation of secondary structure of proteins from UV circular dichroism spectra using an unsupervised learning neural network. Protein Eng. 6:383-390.
4. Barenholz, Y., D. Gibbes, B. J. Litman, J. Goll, T. E. Thompson, and R. D. Carlson. 1977. A simple method for the preparation of homogeneous phospholipid vesicles. Biochemistry 16:2806-2810.
5. Bolen, E. J., and P. W. Holloway. 1990. Quenching of tryptophan fluorescence by brominated phospholipid. Biochemistry 29:9638-9643.
6. Cardoso, R. M., M. B. Zwick, R. L. Stanfield, R. Kunert, J. M. Binley, H. Katinger, D. R. Burton, and I. A. Wilson. 2005. Broadly neutralizing anti-HIV antibody 4E10 recognizes a helical conformation of a highly conserved fusion-associated motif in gp41. Immunity 22:163-173.
7. Chang, D. K., S. F. Cheng, E. A. Kantchev, C. H. Lin, and Y. T. Liu. 2008. Membrane interaction and structure of the transmembrane domain of influenza hemagglutinin and its fusion peptide complex. BMC Biol. 6:2.
8. Coutant, J., H. Yu, M. J. Clement, A. Alfsen, F. Toma, P. A. Curmi, and M. Bomsel. 2008. Both lipid environment and pH are critical for determining physiological solution structure of 3-D-conserved epitopes of the HIV-1 gp41-MPER peptide P1. FASEB J. 22:4338-4351.
9. D'Souza, M. P., D. Livnat, J. A. Bradac, S. H. Bridges, et al. 1997. Evaluation of monoclonal antibodies to human immunodeficiency virus type 1 primary isolates by neutralization assays: performance criteria for selecting candidate antibodies for clinical trials. J. Infect. Dis. 175:1056-1062.
10. Eckert, D. M., and P. S. Kim. 2001. Mechanisms of viral membrane fusion and its inhibition. Ann. Rev. Biochem. 70:777-810.
11. Frey, G., H. Peng, S. Rits-Volloch, M. Morelli, Y. Cheng, and B. Chen. 2008. A fusion-intermediate state of HIV-1 gp41 targeted by broadly neutralizing antibodies. Proc. Natl. Acad. Sci. USA 105:3739-3744.
12. Grundner, C., T. Mirzabekov, J. Sodroski, and R. Wyatt. 2002. Solid-phase proteoliposomes containing human immunodeficiency virus envelope glycoproteins. J. Virol. 76:3511-3521.
13. Haynes, B. F., and S. M. Alam. 2008. HIV-1 hides an Achilles' heel in virion lipids. Immunity 28:10-12.
14. Haynes, B. F., J. Fleming, E. W. St. Clair, H. Katinger, G. Stiegler, R. Kunert, J. Robinson, R. M. Scearce, K. Plonk, H. F. Staats, T. L. Ortel, H. X. Liao, and S. M. Alam. 2005. Cardiolipin polyspecific autoreactivity in two broadly neutralizing HIV-1 antibodies. Science 308:1906-1908.
15. Haynes, B. F., and D. C. Montefiori. 2006. Aiming to induce broadly reactive neutralizing antibody responses with HIV-1 vaccine candidates. Exp. Rev. Vaccines 5:347-363.
16. Huarte, N., M. Lorizate, R. Kunert, and J. L. Nieva. 2008. Lipid modulation of membrane-bound epitope recognition and blocking by HIV-1 neutralizing antibodies. FEBS Lett. 582:3798-3804.
17. Huarte, N., M. Lorizate, R. Maeso, R. Kunert, R. Arranz, J. M. Valpuesta, and J. L. Nieva. 2008. The broadly neutralizing anti-human immunodeficiency virus type 1 4E10 monoclonal antibody is better adapted to membrane-bound epitope recognition and blocking than 2F5. J. Virol. 82:8986-8996.
18. Julien, J. P., S. Bryson, J. L. Nieva, and E. F. Pai. 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.
19. Kowalski, M., J. Potz, L. Basiripour, T. Dorfman, W. C. Goh, E. Terwilliger, A. Dayton, C. Rosen, W. Haseltine, and J. Sodroski. 1987. Functional regions of the envelope glycoprotein of human immunodeficiency virus type 1. Science 237:1351-1355.
20. Lakowicz, J. 2006. Principles of fluorescence spectroscopy, 3rd ed., Springer, New York, NY.
21. Lawless, M. K., S. Barney, K. I. Guthrie, T. B. Bucy, S. R. Petteway, Jr., and G. Merutka. 1996. HIV-1 membrane fusion mechanism: structural studies of the interactions between biologically-active peptides from gp41. Biochemistry 35:13697-13708.
22. Liu, J., Y. Deng, A. K. Dey, J. P. Moore, and M. Lu. 2009. Structure of the HIV-1 gp41 membrane-proximal ectodomain region in a putative prefusion conformation. Biochemistry. 48:2915-2923. doi:10.1021/bi802303b.
23. Matyas, G. R., Z. Beck, N. Karasavvas, and C. R. Alving. 2009. Lipid binding properties of 4E10, 2F5, and WR304 monoclonal antibodies that neutralize HIV-1. Biochim. Biophys. Acta 1788:660-665.
24. Montefiori, D., Q. Sattentau, J. Flores, J. Esparza, and J. Mascola. 2007. Antibody-based HIV-1 vaccines: recent developments and future directions. PLoS Med. 4:e348.
25. Ofek, G., M. Tang, A. Sambor, H. Katinger, J. R. Mascola, R. Wyatt, and P. D. Kwong. 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.
26. Saez-Cirion, A., J. L. Arrondo, M. J. Gomara, M. Lorizate, I. Iloro, G. Melikyan, and J. L. Nieva. 2003. Structural and functional roles of HIV-1 gp41 pretransmembrane sequence segmentation. Biophys. J. 85:3769-3780.
27. Sanchez-Martinez, S., M. Lorizate, H. Katinger, R. Kunert, and J. L. Nieva. 2006. Membrane association and epitope recognition by HIV-1 neutralizing anti-gp41 2F5 and 4E10 antibodies. AIDS Res. Hum. Retrovir. 22:998-1006.
28. Sattentau, Q. J., and J. P. Moore. 1991. Conformational-changes induced in the human-immunodeficiency-virus envelope glycoprotein by soluble Cd4 binding. J. Exp. Med. 174:407-415.
29. Stiegler, G., R. Kunert, M. Purtscher, S. Wolbank, R. Voglauer, F. Steindl, and H. Katinger. 2001. A potent cross-clade neutralizing human monoclonal antibody against a novel epitope on gp41 of human immunodeficiency virus type 1. AIDS Res. Hum. Retrovir. 17:1757-1765.
30. Suarez, T., S. Nir, F. M. Goni, A. Saez-Cirion, and J. L. Nieva. 2000. The pre-transmembrane region of the human immunodeficiency virus type-1 glycoprotein: a novel fusogenic sequence. FEBS Lett. 477:145-149.
31. Sun, Z. Y., K. J. Oh, M. Kim, J. Yu, V. Brusic, L. Song, Z. Qiao, J. H. Wang, G. Wagner, and E. L. Reinherz. 2008. HIV-1 broadly neutralizing antibody extracts its epitope from a kinked gp41 ectodomain region on the viral membrane. Immunity 28:52-63.
32. Vaz, W. L., and G. Schoellmann. 1976. Specific fluorescent derivatives of macromolecules. A fluorescence study of some specifically modified derivatives of chymotrypsin, trypsin and subtilisin. Biochim. Biophys. Acta 439:206-218.