A model of a gp120 V3 peptide in complex with an HIV-neutralizing antibody based on NMR and mutant cycle-derived constraints

European Journal of Biochemistry

Volumn 267, Issue 3, 2000, Pages 767-779

  Zvi, Anat ^a   Tugarinov, Vitali ^a   Faiman, Gabriel A ^a   Horovitz, Amnon ^a   Anglister, Jacob ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Deuteration; Double mutant cycles; Neutralizing antibody; NMR; V3 peptide

Indexed keywords

AMINO ACID; GLYCOPROTEIN GP 120; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY;

ANTIGEN ANTIBODY COMPLEX; ANTIGEN BINDING; ANTIGEN RECOGNITION; ARTICLE; CONTROLLED STUDY; DRUG BINDING SITE; DRUG STRUCTURE; MOLECULAR INTERACTION; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; REACTION ANALYSIS; STRUCTURE ANALYSIS; SURFACE CHARGE;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGEN-ANTIBODY COMPLEX; BASE SEQUENCE; DNA PRIMERS; ELECTROSTATICS; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; MACROMOLECULAR SUBSTANCES; MAGNETIC RESONANCE SPECTROSCOPY; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NEUTRALIZATION TESTS; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; RUMEX;

EID: 0033950367     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1327.2000.01055.x     Document Type: Article

References (43)

1. 1. Al-Lazikani, B., Lesk, A.M. & Chothia, C. (1997) Standard conformations for the canonical structures of immunoglobulins. J. Mol. Biol. 273, 927-948.
2. 2. Palker, T.J., Clark, M.E., Langlois, A.J., Matthews, T.J., Weinhold, K.J., Randall, R.R., Bolognesi, D.P. & Haynes, B.F. (1988) Type-specific neutralization of the human immunodeficiency virus with antibodies to env-encoded synthetic peptides. Proc. Natl Acad. Sci. USA 85, 1932-1936.
3. 3. Goudsmit, J., Debouck, C., Meloen, R.H., Smit, L., Bakker, M., Asher, D.M., Wolff, A.V., Gibbs, C.J. Jr & Gajdusek, D.C. (1988) Human immunodeficiency virus type 1 neutralization epitope with conserved architecture elicits early type-specific antibodies in experimentally infected chimpanzees. Proc. Natl Acad. Sci. USA 85, 4478-4482.
4. 4. Rusche, J.R., Javaherian, K., McDanal, C., Petro, J., Lynn, D.L., Grimaila, R., Langlois, A., Gallo, R.C., Arthur, L.O., Fischinger, P.J. et al. (1988) Antibodies that inhibit fusion of human immunodeficiency virus-infected cells bind a 24-amino acid sequence of the viral envelope, gp120. Proc. Natl Acad. Sci. USA 85, 3198-3202.
5. 5. Spear, G.T., Takefman, D.M., Sharpe, S., Ghassemi, M. & Zolla Pazner, S. (1994) Antibodies to the HIV-1 V3 loop in serum from infected persons contribute a major proportion of immune effector functions including complement activation, antibody binding, and neutralization. Virology 204, 609-615.
6. 6. Vogel, T., Kurth, R. & Norley, S. (1994) The majority of neutralizing Abs in HIV-1-infected patients recognize linear V3 loop sequences. Studies using HIV-1MN multiple antigenic peptides. J. Immunol. 153, 1895-1904.
7. 7. Javaherian, K., Langlois, A.J., McDanal, C., Ross, K.L., Eckler, L.I., Jellis, C.L., Profy, A.T., Rusche, J.R., Bolognesi, D.P., Putney, S.D. et al. (1989) Principal neutralizing domain of the human immunodeficiency virus type 1 envelope protein. Proc. Natl Acad. Sci. USA 86, 6768-6772.
8. 8. Matsushita, S., Robert Guroff, M., Rusche, J., Koito, A., Hattori, T., Hoshino, H., Javaherian, K., Takatsuki, K. & Putney, S. (1988) Characterization of a human immunodeficiency virus neutralizing monoclonal antibody and mapping of the neutralizing epitope. J. Virol. 62, 2107-2714.
9. 9. Wu, L., Gerard, N.P., Wyatt, R., Choe, H., Parolin, C., Ruffing, N., Borsetti, A., Cardoso, A.A., Desjardin, E., Newman, W., Gerard, C. & Sodroski, J. (1996) CD4-induced interaction of primary HIV-1 gp120 glycoproteins with the chemokine receptor CCR-5. Nature (London) 384, 179-183.
10. 10. Trkola, A., Dragic, T., Arthos, J., Binley, J.M., Oison, W.C., Allaway, G.P., Cheng Mayer, C., Robinson, J., Maddon, P.J. & Moore, J.P. (1996) CD4-dependent, antibody-sensitive interactions between HIV-1 and its co-receptor CCR-5. Nature (London) 384, 184-187.
11. 11. Hwang, S.S., Boyle, T.J., Lyerly, H.K. & Cullen, B.R. (1992) Identification of envelope V3 loop as the major determinant of CD4 neutralization sensitivity of HIV-1. Science 257, 535-537.
12. 12. Hamajima, K., Bukawa, H., Fukushima, J., Kawamoto, S., Kaneko, T., Sekigawa, K., Tanaka, S., Tsukuda, M. & Okuda, K. (1995) A macromolecular multicomponent peptide vaccine prepared using the glutaraldehyde conjugation method with strong immunogenicity for HIV-1. Clin. Immunol. Immunopathol. 77, 374-379.
13. 13. Honda, M., Matsuo, K., Nakasone, T., Okamoto, Y., Yoshizaki, H., Kitamura, K., Sugiura, W., Watanabe, K., Fukushima, Y., Haga, S. et al. (1995) Protective immune responses induced by secretion of a chimeric soluble. Proc. Natl Acad. Sci. USA 92, 10693-10697.
14. 14. Kwong, P.D., Wyatt, R., Robinson, J., Sweet, R.W., Sodroski, J. & Hendrickson, W.A. (1998) Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature (London) 393, 648-659.
15. 15. Ghiara, J.B., Stura, E.A., Stanfield, R.L., Profy, A.T. & Wilson, I.A. (1994) Crystal structure of the principal neutralization site of HIV-1. Science 264, 82-85.
16. 16. Stanfield, R., Cabezas, E., Satterthwait, A., Stura, E., Profy, A. & Wilson, I. (1999) Dual conformations for the HIV-1 gp120, V3 loop in complexes with different neutralizing fabs. Struct. Fold Des. 7, 131-142.
17. 17. Rini, J.M., Stanfield, R.L., Stura, E.A., Salinas, P.A., Profy, A.T. & Wilson, I.A. (1993) Crystal structure of a human immunodeficiency virus type 1 neutralizing antibody, 50.1, in complex with its V3 loop peptide antigen. Proc. Natl Acad. Sci. USA 90, 6325-6329.
18. 18. Skinner, M.A., Ting, R., Langlois, A.J., Weinhold, K.J., Lyerly, H.K., Javaherian, K. & Matthews, T.J. (1988) Characteristics of a neutralizing monoclonal antibody to the HIV envelope glycoprotein. AIDS Res. Hum. Retroviruses 4, 187-197.
19. 19. Zvi, A., Kustanovich, I., Feigelson, D., Levy, R., Eisenstein, M., Matsushita, S., Richalet Secordel, P., Regenmortel, V.M.H. & Anglister, J. (1995) NMR mapping of the antigenic determinant recognized by an anti-gp120, human immunodeficiency virus neutralizing antibody. Eur. J. Biochem. 229, 178-187.
20. 20. Tugarinov, V., Zvi, A., Levy, R. & Anglister, J. (1999) A cis proline turn linking two beta-hairpin strands in the solution structure of an antibody-bound HIV-1IIIB V3 peptide. Nat. Struct. Biol. 6, 331-335.
21. 21. Zvi, A., Feigelson, D.J., Hayek, Y. & Anglister, J. (1997) Conformation of the principal neutralizing determinant of human immunodeficiency virus type 1 in complex with an anti-gp120 virus neutralizing antibody studied by two-dimensional nuclear magnetic resonance difference spectroscopy. Biochemistry 36, 8619-8627.
22. 22. Zilber, B., Scherf, T., Levitt, M. & Anglister, J. (1990) NMR-derived model for a peptide-antibody complex. Biochemistry 29, 10032-10041.
23. 23. Scherf, T., Hiller, R., Naider, F., Levitt, M. & Anglister, J. (1992) Induced peptide conformations in different antibody complexes: molecular modeling of the three-dimensional structure of peptide-antibody complexes using NMR-derived distance restraints. Biochemistry 31, 6884-6897.
24. 24. Ikura, M. & Bax, A. (1992) Isotope-filtered 2D NMR of a protein-peptide complex: study of a skeletal muscle myosin light chain kinase fragment bound to calmodulin. J. Am. Chem. Soc. 114, 2433-2440.
25. 25. Bax, A., Grzesiek, S., Gronenborn, A.M. & Clore, M.G. (1994) Isotope-filtered 2D HOHAHA spectroscopy of a peptide-protein complex using heteronuclear Hartmann-Hahn dephasing. J. Magn. Res. 106, 269-273.
26. 26. Petros, A.M., Kawai, M., Luly, J.R. & Fesik, S.W. (1992) Conformation of two non-immunosuppressive FK506 analogs when bound to FKBP by isotope-filtered NMR. FEBS Lett. 308, 309-314.
27. 27. Horovitz, A. (1996) Double-mutant cycles: a powerful tool for analyzing protein structure and function. Fold Des. 1, R121-R126.
28. 28. Hidalgo, P. & MacKinnon, R. (1995) Revealing the architecture of a K+ channel pore through mutant cycles with a peptide inhibitor. Science 268, 307-310.
29. 29. Faiman, G.A., Levy, R., Anglister, J. & Horovitz, A. (1996) Contribution of arginine residues in the RP135 peptide derived from the V3 loop of gp120 to its interaction with the Fv fragment of the 0.5β HIV-1 neutralizing antibody. J. Biol. Chem. 271, 13829-13833.
30. 30. Snyder, S.L. & Sobocinski, P.Z. (1975) An improved 2,4,6-trinitrobenzenesulfonic acid method for the determination of amines. Anal. Biochem. 64, 284-288.
31. 31. Sayers, J.R., Schmidt, W. & Eckstein, F. (1988) 5′-3′ Exonucleases in phosphorothioate-based oligonucleotide-directed mutagenesis. Nucleic Acids Res. 16, 791-802.
32. 32. Gill, S.C. & von Hippel, P.M. (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182, 319-326.
33. 33. Zvi, A., Kustanovich, I., Hayek, Y., Matsushita, S. & Anglister, J. (1995) The principal neutralizing determinant of HIV-1 located in V3 of gp120 forms a 12-residue loop by internal hydrophobic interactions. FEBS Lett. 368, 267-270.
34. 34. Bax, A. & Davis, D.G. (1985) MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy. J. Magn. Res. 65, 355-360.
35. 35. Brunger, A.T. (1992) X-PLOR 3.1 Manual. Yale University Press, New Haven, CT.
36. IIIB: a two-dimensional NMR study. Biochemistry 31, 6972-6979.
37. 37. LaRosa, G.J., Davide, J.P., Weinhold, K., Waterbury, J.A., Profy, A.T., Lewis, J.A., Langlois, A.J., Dreesman, G.R., Boswell, R.N., Shadduck, P. et al. (1990) Conserved sequence and structural elements in the HIV-1 principal neutralizing determinant. Science 249, 932-935.
38. 38. Shoham, M., Scherf, T., Anglister, J., Levitt, M., Merritt, E.A. & Hol, W.G. (1995) Structural diversity in a conserved cholera toxin epitope involved in ganglioside binding. Protein Sci. 4, 841-848.
39. 39. Javaherian, K. & McDanal, C. (1995) Random copolymers containing specific ratios of negatively charged and aromatic amino acids bind V3 disulfide loop and neutralize diverse HIV type 1 isolates. AIDS Res. Hum. Retroviruses 11, 1163-1168.
40. 40. Callahan, L.N., Phelan, M., Mallinson, M. & Norcross, M.A. (1991) Dextran sulfate blocks antibody binding to the principal neutralizing domain of human immunodeficiency virus type 1 without interfering with gp120-CD4 interactions. J. Virol. 65, 1543-1550.
41. 41. Javaherian, K., Khiroya, R., Quinlan, C., Boyd, J.G. & Hanham, K.A. (1994) V3-mediated heparin neutralization of HIV type 1. AIDS Res. Hum. Retroviruses 10, 1421-1423.
42. 42. MacCallum, R.M., Martin, A.C. & Thornton, J.M. (1996) Antibody-antigen interactions: contact analysis and binding site topography. J. Mol. Biol. 262, 732-745.
43. 43. Mian, I.S., Bradwell, A.R. & Oison, A.J. (1991) Structure, function and properties of antibody binding sites. J. Mol. Biol. 217, 133-151.