Structural Rationale for the Broad Neutralization of HIV-1 by Human Monoclonal Antibody 447-52D

Structure

Volumn 12, Issue 2, 2004, Pages 193-204

  Stanfield, Robyn L ^a   Gorny, Miroslaw K ^b   Williams, Constance ^b   Zolla Pazner, Susan ^b   Wilson, Ian A ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; HUMAN MONOCLONAL ANTIBODY; IMMUNOGLOBULIN F(AB) FRAGMENT; PEPTIDE DERIVATIVE;

AMINO ACID SEQUENCE; ANALYTIC METHOD; ANTIBODY ISOLATION; ANTIBODY SPECIFICITY; ANTIBODY STRUCTURE; ANTIGEN BINDING; ARTICLE; BETA SHEET; CRYSTAL STRUCTURE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; PRIORITY JOURNAL; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; VIRUS NEUTRALIZATION;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 1242351232     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2004.01.003     Document Type: Article

References (79)

1. Al-Lazikani B., Lesk A.M., Chothia C. Standard conformations for the canonical structures of immunoglobulins. J. Mol. Biol. 273:1997;927-948.
2. Basmaciogullari S., Babcock G.J., Van Ryk D., Wojtowicz W., Sodroski J. Identification of conserved and variable structures in the human immunodeficiency virus gp120 glycoprotein of importance for CXCR4 binding. J. Virol. 76:2002;10791-10800.
3. Bhattacharyya D., Brooks B.R., Callahan L. Positioning of positively charged residues in the V3 loop correlates with HIV type 1 syncytium-inducing phenotype. AIDS Res. Hum. Retroviruses. 12:1996;83-90.
4. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S.et al. Crystallography & NMR system. a new software suite for macromolecular structure determination Acta Crystallogr. D. 54:1998;905-921.
5. Cabezas E., Wang M., Parren P.W., Stanfield R.L., Satterthwait A.C. A structure-based approach to a synthetic vaccine for HIV-1. Biochemistry. 39:2000;14377-14391.
6. Calarese D.A., Scanlan C.N., Zwick M.B., Deechongkit S., Mimura Y., Kunert R., Zhu P., Wormald M.R., Stanfield R.L., Roux K.H.et al. Antibody domain exchange is an immunological solution to carbohydrate cluster recognition. Science. 300:2003;2065-2071.
7. Catasti P., Fontenot J.D., Bradbury E.M., Gupta G. Local and global structural properties of the HIV-MN V3 loop. J. Biol. Chem. 270:1995;2224-2232.
8. Catasti P., Bradbury E.M., Gupta G. Structure and polymorphism of HIV-1 third variable loops. J. Biol. Chem. 271:1996;8236-8242.
9. Chandrasekhar K., Profy A.T., Dyson H.J. Solution conformational preferences of immunogenic peptides derived from the principal neutralizing determinant of the HIV-1 envelope glycoprotein gp120. Biochemistry. 30:1991;9187-9194.
10. Collis A.V., Brouwer A.P., Martin A.C. Analysis of the antigen combining site. correlations between length and sequence composition of the hypervariable loops and the nature of the antigen J. Mol. Biol. 325:2003;337-354.
11. Conley A.J., Gorny M.K., Kessler J.A. II, Boots L.J., Ossorio-Castro M., Koenig S., Lineberger D.W., Emini E.A., Williams C., Zolla-Pazner S. Neutralization of primary human immunodeficiency virus type 1 isolates by the broadly reactive anti-V3 monoclonal antibody, 447-52D. J. Virol. 68:1994;6994-7000.
12. Cormier E.G., Tran D.N., Yukhayeva L., Olson W.C., Dragic T. Mapping the determinants of the CCR5 amino-terminal sulfopeptide interaction with soluble human immunodeficiency virus type 1 gp120-CD4 complexes. J. Virol. 75:2001;5541-5549.
13. H3 gene family expression in plasma cells of HIV-infected patients. Int. Immunol. 8:1996;1329-1333.
14. de Jong J.J., Goudsmit J., Keulen W., Klaver B., Krone W., Tersmette M., de Ronde A. Human immunodeficiency virus type 1 clones chimeric for the envelope V3 domain differ in syncytium formation and replication capacity. J. Virol. 66:1992;757-765.
15. de Lorimier R., Moody M.A., Haynes B.F., Spicer L.D. NMR-derived solution conformations of a hybrid synthetic peptide containing multiple epitopes of envelope protein gp120 from the RF strain of human immunodeficiency virus. Biochemistry. 33:1994;2055-2062.
16. Dettin M., De Rossi A., Autiero M., Guardiola J., Chieco-Bianchi L., Di Bello C. Structural studies on synthetic peptides from the principal neutralizing domain of HIV-1 gp120 that bind to CD4 and enhance HIV-1 infection. Biochem. Biophys. Res. Commun. 191:1993;364-370.
17. Dettin M., Roncon R., Simonetti M., Tormene S., Falcigno L., Paolillo L., Di Bello C. Synthesis, characterization and conformational analysis of gp 120-derived synthetic peptides that specifically enhance HIV-1 infectivity. J. Pept. Sci. 3:1997;15-30.
18. Ding J., Smith A.D., Geisler S.C., Ma X., Arnold G.F., Arnold E. Crystal structure of a human rhinovirus that displays part of the HIV-1 V3 loop and induces neutralizing antibodies against HIV-1. Structure. 10:2002;999-1011.
19. Esnouf R.M. Further additions to MolScript version 1.4, including reading and contouring of electron-density maps. Acta Crystallogr. D. 55:1999;938-940.
20. Fitzgerald P.M.D. MERLOT, an integrated package of computer programs for the determination of crystal structures by molecular replacement. J. Appl. Crystallogr. 21:1988;273-278.
21. Fontenot J.D., Gatewood J.M., Mariappan S.V., Pau C.P., Parekh B.S., George J.R., Gupta G. Human immunodeficiency virus (HIV) antigens. structure and serology of multivalent human mucin MUC1-HIV V3 chimeric proteins Proc. Natl. Acad. Sci. USA. 92:1995;315-319.
22. Ghiara J.B., Stura E.A., Stanfield R.L., Profy A.T., Wilson I.A. Crystal structure of the principal neutralization site of HIV-1. Science. 264:1994;82-85.
23. Ghiara J.B., Ferguson D.C., Satterthwait A.C., Dyson H.J., Wilson I.A. Structure-based design of a constrained peptide mimic of the HIV-1 V3 loop neutralization site. J. Mol. Biol. 266:1997;31-39.
24. Gorny M.K., Conley A.J., Karwowska S., Buchbinder A., Xu J.Y., Emini E.A., Koenig S., Zolla-Pazner S. Neutralization of diverse human immunodeficiency virus type 1 variants by an anti-V3 human monoclonal antibody. J. Virol. 66:1992;7538-7542.
25. Gorny M.K., VanCott T.C., Hioe C., Israel Z.R., Michael N.L., Conley A.J., Williams C., Kessler J.A. II, Chigurupati P., Burda S.et al. Human monoclonal antibodies to the V3 loop of HIV-1 with intra- and interclade cross-reactivity. J. Immunol. 159:1997;5114-5122.
26. Gorny M.K., Williams C., Volsky B., Revesz K., Cohen S., Polonis V.R., Honnen W.J., Kayman S.C., Krachmarov C., Pinter A.et al. Human monoclonal antibodies specific for conformation-sensitive epitopes of V3 neutralize human immunodeficiency virus type 1 primary isolates from various clades. J. Virol. 76:2002;9035-9045.
27. Goudsmit J., Debouck C., Meloen R.H., Smit L., Bakker M., Asher D.M., Wolff A.V., Gibbs C.J. Jr., Gajdusek D.C. Human immunodeficiency virus type 1 neutralization epitope with conserved architecture elicits early type-specific antibodies in experimentally infected chimpanzees. Proc. Natl. Acad. Sci. USA. 85:1988;4478-4482.
28. Graille M., Stura E.A., Corper A.L., Sutton B.J., Taussig M.J., Charbonnier J.B., Silverman G.J. Crystal structure of a Staphylococcus aureus protein A domain complexed with the Fab fragment of a human IgM antibody. structural basis for recognition of B-cell receptors and superantigen activity Proc. Natl. Acad. Sci. USA. 97:2000;5399-5404.
29. Gupta G., Anantharamaiah G.M., Scott D.R., Eldridge J.H., Myers G. Solution structure of the V3 loop of a Thailand HIV isolate. J. Biomol. Struct. Dyn. 11:1993;345-366.
30. Hoffman T.L., Doms R.W. HIV-1 envelope determinants for cell tropism and chemokine receptor use. Mol. Membr. Biol. 16:1999;57-65.
31. Huang X., Smith M.C., Berzofsky J.A., Barchi J.J. Jr. Structural comparison of a 15 residue peptide from the V3 loop of HIV-1IIIb and an O-glycosylated analogue. FEBS Lett. 393:1996;280-286.
32. Huang X., Barchi J.J. Jr., Lung F.D., Roller P.P., Nara P.L., Muschik J., Garrity R.R. Glycosylation affects both the three-dimensional structure and antibody binding properties of the HIV-1IIIB GP120 peptide RP135. Biochemistry. 36:1997;10846-10856.
33. Huisman J.G., Carotenuto A., Labrijn A.F., Papavoine C.H., Laman J.D., Schellekens M.M., Koppelman M.H., Hilbers C.W. Recognition properties of V3-specific antibodies to V3 loop peptides derived from HIV-1 gp120 presented in multiple conformations. Biochemistry. 39:2000;10866-10876.
34. 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. Principal neutralizing domain of the human immunodeficiency virus type 1 envelope protein. Proc. Natl. Acad. Sci. USA. 86:1989;6768-6772.
35. Jeffrey P.D., Strong R.K., Sieker L.C., Chang C.Y., Campbell R.L., Petsko G.A., Haber E., Margolies M.N., Sheriff S. 26-10 Fab-digoxin complex. affinity and specificity due to surface complementarity Proc. Natl. Acad. Sci. USA. 90:1993;10310-10314.
36. Jelinek R., Valente A.P., Valentine K.G., Opella S.J. Two-dimensional NMR spectroscopy of peptides on beads. J. Magn. Reson. 125:1997;185-187. a.
37. Jelinek R., Terry T.D., Gesell J.J., Malik P., Perham R.N., Opella S.J. NMR structure of the principal neutralizing determinant of HIV-1 displayed in filamentous bacteriophage coat protein. J. Mol. Biol. 266:1997;649-655. b.
38. Keller P.M., Arnold B.A., Shaw A.R., Tolman R.L., van Middlesworth F., Bondy S., Rusiecki V.K., Koenig S., Zolla-Pazner S., Conard P.et al. Identification of HIV vaccine candidate peptides by screening random phage epitope libraries. Virology. 193:1993;709-716.
39. Kraulis P.J. Molscript. a program to produce both detailed and schematic plots of protein structures J. Appl. Crystallogr. 24:1991;946-950.
40. Kwong P.D., Wyatt R., Robinson J., Sweet R.W., Sodroski J., Hendrickson W.A. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature. 393:1998;648-659.
41. Kwong P.D., Wyatt R., Majeed S., Robinson J., Sweet R.W., Sodroski J., Hendrickson W.A. Structures of HIV-1 gp120 envelope glycoproteins from laboratory-adapted and primary isolates. Struct. Fold. Des. 8:2000;1329-1339.
42. Markert R.L., Ruppach H., Gehring S., Dietrich U., Mierke D.F., Kock M., Rubsamen-Waigmann H., Griesinger C. Secondary structural elements as a basis for antibody recognition in the immunodominant region of human immunodeficiency viruses 1 and 2. Eur. J. Biochem. 237:1996;188-204.
43. Martin A.C., Thornton J.M. Structural families in loops of homologous proteins. automatic classification, modelling and application to antibodies J. Mol. Biol. 263:1996;800-815.
44. Matthews B.W. Determination of protein molecular weight, hydration, and packing from crystal density. Methods Enzymol. 114:1985;176-187.
45. McDonald I.K., Thornton J.M. Satisfying hydrogen bonding potential in proteins. J. Mol. Biol. 238:1994;777-793.
46. Merritt E.A., Bacon D.J. Raster3D. photorealistic molecular graphics Methods Enzymol. 277:1997;505-524.
47. H domain of immunoglobulins. J. Mol. Biol. 275:1998;269-294.
48. Navaza J. AMoRe. an automated package for molecular replacement Acta Crystallogr. A. 50:1994;157-163.
49. Nicholls A., Sharp K.A., Honig B. Protein folding and association. insights from the interfacial and thermodynamic properties of hydrocarbons Proteins. 11:1991;281-296.
50. Nyambi P.N., Mbah H.A., Burda S., Williams C., Gorny M.K., Nadas A., Zolla-Pazner S. Conserved and exposed epitopes on intact, native, primary human immunodeficiency virus type 1 virions of group M. J. Virol. 74:2000;7096-7107.
51. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276A:1997;307-326.
52. Palker T.J., Clark M.E., Langlois A.J., Matthews T.J., Weinhold K.J., Randall R.R., Bolognesi D.P., Haynes B.F. Type-specific neutralization of the human immunodeficiency virus with antibodies to env-encoded synthetic peptides. Proc. Natl. Acad. Sci. USA. 85:1988;1932-1936.
53. Ratner L., Fisher A., Jagodzinski L.L., Mitsuya H., Liou R.S., Gallo R.C., Wong-Staal F. Complete nucleotide sequences of functional clones of the AIDS virus. AIDS Res. Hum. Retroviruses. 3:1987;57-69.
54. Rini J.M., Stanfield R.L., Stura E.A., Salinas P.A., Profy A.T., Wilson I.A. 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. 90:1993;6325-6329.
55. Rizzuto C., Sodroski J. Fine definition of a conserved CCR5-binding region on the human immunodeficiency virus type 1 glycoprotein 120. AIDS Res. Hum. Retroviruses. 16:2000;741-749.
56. Rizzuto C.D., Wyatt R., Hernandez-Ramos N., Sun Y., Kwong P.D., Hendrickson W.A., Sodroski J. A conserved HIV gp120 glycoprotein structure involved in chemokine receptor binding. Science. 280:1998;1949-1953.
57. 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. 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. 85:1988;3198-3202.
58. Saphire E.O., Parren P.W., Pantophlet R., Zwick M.B., Morris G.M., Rudd P.M., Dwek R.A., Stanfield R.L., Burton D.R., Wilson I.A. Crystal structure of a neutralizing human IgG against HIV-1. a template for vaccine design Science. 293:2001;1155-1159.
59. Sarma A.V., Raju T.V., Kunwar A.C. NMR study of the peptide present in the principal neutralizing determinant (PND) of HIV-1 envelope glycoprotein gp120. J. Biochem. Biophys. Methods. 34:1997;83-98.
60. H3 gene repertoire of naive human B cells. J. Immunol. 164:2000;5482-5491.
61. Sharon M., Kessler N., Levy R., Zolla-Pazner S., Gorlach M., Anglister J. Alternative conformations of HIV-1 V3 loops mimic β hairpins in chemokines, suggesting a mechanism for coreceptor selectivity. Structure. 11:2003;225-236.
62. Sheriff S., Hendrickson W.A., Smith J.L. Structure of myohemerythrin in the azidomet state at 1.7/1.3 Å resolution. J. Mol. Biol. 197:1987;273-296.
63. Shirai H., Kidera A., Nakamura H. Structural classification of CDR-H3 in antibodies. FEBS Lett. 399:1996;1-8.
64. Spiegel P.C. Jr., Jacquemin M., Saint-Remy J.M., Stoddard B.L., Pratt K.P. Structure of a factor VIII C2 domain-immunoglobulin G4κ Fab complex. identification of an inhibitory antibody epitope on the surface of factor VIII Blood. 98:2001;13-19.
65. Stanfield R.L., Cabezas E., Satterthwait A.C., Stura E.A., Profy A.T., Wilson I.A. Dual conformations for the HIV-1 gp120 V3 loop in complexes with different neutralizing Fabs. Struct. Fold. Des. 7:1999;131-142.
66. Stanfield R.L., Ghiara J.B., Saphire E.O., Profy A.T., Wilson I.A. Recurring conformation of the human immunodeficiency virus Type 1 gp120 V3 loop. Virology. in press:2003.
67. Tolman R.L., Bednarek M.A., Johnson B.A., Leanza W.J., Marburg S., Underwood D.J., Emini E.A., Conley A.J. Cyclic V3-loop-related HIV-1 conjugate vaccines. Synthesis, conformation and immunological properties. Int. J. Pept. Protein Res. 41:1993;455-466.
68. Tugarinov V., Zvi A., Levy R., Hayek Y., Matsushita S., Anglister J. NMR structure of an anti-gp120 antibody complex with a V3 peptide reveals a surface important for co-receptor binding. Struct. Fold. Des. 8:2000;385-395.
69. Turner B.G., Summers M.F. Structural biology of HIV. J. Mol. Biol. 285:1999;1-32.
70. Vranken W.F., Budesinsky M., Fant F., Boulez K., Borremans F.A. The complete consensus V3 loop peptide of the envelope protein gp120 of HIV-1 shows pronounced helical character in solution. FEBS Lett. 374:1995;117-121.
71. Vranken W.F., Budesinsky M., Martins J.C., Fant F., Boulez K., Gras-Masse H., Borremans F.A. Conformational features of a synthetic cyclic peptide corresponding to the complete V3 loop of the RF HIV-1 strain in water and water/trifluoroethanol solutions. Eur. J. Biochem. 236:1996;100-108.
72. Vranken W.F., Fant F., Budesinsky M., Borremans F.A. Conformational model for the consensus V3 loop of the envelope protein gp120 of HIV-1 in a 20% trifluoroethanol/water solution. Eur. J. Biochem. 268:2001;2620-2628.
73. Vu H.M., de Lorimier R., Moody M.A., Haynes B.F., Spicer L.D. Conformational preferences of a chimeric peptide HIV-1 immunogen from the C4-V3 domains of gp120 envelope protein of HIV-1 CAN0A based on solution NMR. comparison to a related immunogenic peptide from HIV-1 RF Biochemistry. 35:1996;5158-5165.
74. Vu H.M., Myers D., de Lorimier R., Matthews T.J., Moody M.A., Heinly C., Torres J.V., Haynes B.F., Spicer L. Nuclear magnetic resonance analysis of solution conformations in C4-V3 hybrid peptides derived from human immunodeficiency virus (HIV) type 1 gp120. relation to specificity of peptide-induced anti-HIV neutralizing antibodies J. Virol. 73:1999;746-750.
75. White-Scharf M.E., Potts B.J., Smith L.M., Sokolowski K.A., Rusche J.R., Silver S. Broadly neutralizing monoclonal antibodies to the V3 region of HIV-1 can be elicited by peptide immunization. Virology. 192:1993;197-206.
76. Wu G., MacKenzie R., Durda P.J., Tsang P. The binding of a glycoprotein 120 V3 loop peptide to HIV-1 neutralizing antibodies. Structural implications. J. Biol. Chem. 275:2000;36645-36652.
77. York J., Follis K.E., Trahey M., Nyambi P.N., Zolla-Pazner S., Nunberg J.H. Antibody binding and neutralization of primary and T-cell line-adapted isolates of human immunodeficiency virus type 1. J. Virol. 75:2001;2741-2752.
78. Zolla-Pazner S., Gorny M.K., Nyambi P.N., VanCott T.C., Nadas A. Immunotyping of human immunodeficiency virus type 1 (HIV). an approach to immunologic classification of HIV J. Virol. 73:1999;4042-4051.
79. Zvi A., Hiller R., Anglister J. Solution conformation of a peptide corresponding to the principal neutralizing determinant of HIV-1IIIB. a two-dimensional NMR study Biochemistry. 31:1992;6972-6979.