Structural basis for diverse N-glycan recognition by HIV-1-neutralizing V1-V2-directed antibody PG16

Nature Structural and Molecular Biology

Volumn 20, Issue 7, 2013, Pages 804-813

  Pancera, Marie ^a   Shahzad Ul Hussan, Syed ^b   Doria Rose, Nicole A ^a   McLellan, Jason S ^a   Bailer, Robert T ^a   Dai, Kaifan ^a   Loesgen, Sandra ^b   Louder, Mark K ^a   Staupe, Ryan P ^a   Yang, Yongping ^a   Zhang, Baoshan ^a   Parks, Robert ^c   Eudailey, Joshua ^c   Lloyd, Krissey E ^c   Blinn, Julie ^c   Alam, S Munir ^c   Haynes, Barton F ^c   Amin, Mohammed N ^d   Wang, Lai Xi ^d   Burton, Dennis R ^e,f   Koff, Wayne C ^g   Nabel, Gary J ^a   Mascola, John R ^a   Bewley, Carole A ^b   Kwong, Peter D ^a   more..

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

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

^d UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^e SCRIPPS RESEARCH INSTITUTE   (United States)

^f MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^g INTERNATIONAL AIDS VACCINE INITIATIVE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC ANTIBODY; NEUTRALIZING ANTIBODY; PG16 ANTIBODY; SIALIC ACID; UNCLASSIFIED DRUG;

ANTIBODY STRUCTURE; ANTIGEN BINDING; ANTIGEN RECOGNITION; ARTICLE; BINDING AFFINITY; BINDING SITE; CRYSTAL STRUCTURE; CRYSTALLIZATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HYDROGEN BOND; IC 50; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN PROTEIN INTERACTION; SOMATIC HYPERMUTATION; VIRUS INFECTIVITY; VIRUS NEUTRALIZATION;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANTIBODIES, NEUTRALIZING; ANTIBODY SPECIFICITY; ANTIGEN-ANTIBODY REACTIONS; BINDING SITES, ANTIBODY; CARBOHYDRATE CONFORMATION; CARBOHYDRATE SEQUENCE; CRYSTALLOGRAPHY, X-RAY; EPITOPES; GLYCOSYLATION; HEK293 CELLS; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HUMANS; IMMUNOGLOBULIN FAB FRAGMENTS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; POLYSACCHARIDES; PROTEIN CONFORMATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; STRUCTURE-ACTIVITY RELATIONSHIP; SWAINSONINE;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84880149399     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2600     Document Type: Article

References (62)

1. Pantophlet, R. & Burton, D.R. GP120: target for neutralizing HIV-1 antibodies. Annu. Rev. Immunol. 24, 739-769 (2006).
2. Wyatt, R. & Sodroski, J. The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280, 1884-1888 (1998).
3. Binley, J.M. et al. Analysis of the interaction of antibodies with a conserved enzymatically deglycosylated core of the HIV type 1 envelope glycoprotein 120. AIDS Res. Hum. Retroviruses 14, 191-198 (1998).
4. Walker, L.M. et al. A limited number of antibody specificities mediate broad and potent serum neutralization in selected HIV-1 infected individuals. PLoS Pathog. 6, e1001028 (2010).
5. Walker, L.M. et al. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477, 466-470 (2011).
6. Kwong, P.D. et al. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393, 648-659 (1998).
7. Wyatt, R. et al. The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 393, 705-711 (1998).
8. Trkola, A. et al. Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type J. Virol. 70, 1100-1108 (1996).
9. Sanders, R.W. et al. The mannose-dependent epitope for neutralizing antibody 2G12 on human immunodeficiency virus type 1 glycoprotein gp120. J. Virol. 76, 7293-7305 (2002).
10. Scanlan, C.N. et al. The broadly neutralizing anti-human immunodeficiency virus type 1 antibody 2G12 recognizes a cluster of 12 mannose residues on the outer face of gp120. J. Virol. 76, 7306-7321 (2002).
11. Binley, J.M. et al. Profiling the specificity of neutralizing antibodies in a large panel of plasmas from patients chronically infected with human immunodeficiency virus type 1 subtypes B and C. J. Virol. 82, 11651-11668 (2008).
12. Walker, L.M. et al. Rapid development of glycan-specific, broad, and potent anti-HIV-1 gp120 neutralizing antibodies in an R5 SIV/HIV chimeric virus infected macaque. Proc. Natl. Acad. Sci. USA 108, 20125-20129 (2011).
13. Walker, L.M. et al. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326, 285-289 (2009).
14. Calarese, D.A. et al. Dissection of the carbohydrate specificity of the broadly neutralizing anti-HIV-1 antibody 2G12. Proc. Natl. Acad. Sci. USA 102, 13372-13377 (2005).
15. Calarese, D.A. et al. Antibody domain exchange is an immunological solution to carbohydrate cluster recognition. Science 300, 2065-2071 (2003).
16. Doores, K.J., Fulton, Z., Huber, M., Wilson, I.A. & Burton, D.R. Antibody 2G12 recognizes di-mannose equivalently in domain-and nondomain-exchanged forms but only binds the HIV-1 glycan shield if domain exchanged. J. Virol. 84, 10690-10699 (2010).
17. Wang, L.X., Ni, J., Singh, S. & Li, H. Binding of high-mannose-type oligosaccharides and synthetic oligomannose clusters to human antibody 2G12: implications for HIV-1 vaccine design. Chem. Biol. 11, 127-134 (2004).
18. McLellan, J.S. et al. Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9. Nature 480, 336-343 (2011).
19. Pejchal, R. et al. A potent and broad neutralizing antibody recognizes and penetrates the HIV glycan shield. Science 334, 1097-1103 (2011).
20. Sattentau, Q.J. Vaccinology: a sweet cleft in HIV's armour. Nature 480, 324-325 (2011).
21. Leonard, C.K. et al. Assignment of intrachain disulfide bonds and characterization of potential glycosylation sites of the type 1 recombinant human immunodeficiency virus envelope glycoprotein (gp120) expressed in Chinese hamster ovary cells. J. Biol. Chem. 265, 10373-10382 (1990).
22. Mizuochi, T. et al. Carbohydrate structures of the human- immunodeficiency-virus (HIV) recombinant envelope glycoprotein gp120 produced in Chinese-hamster ovary cells. Biochem. J. 254, 599-603 (1988).
23. Zhu, X., Borchers, C., Bienstock, R.J. & Tomer, K.B. Mass spectrometric characterization of the glycosylation pattern of HIV-gp120 expressed in CHO cells. Biochemistry 39, 11194-11204 (2000).
24. Bonomelli, C. et al. The glycan shield of HIV is predominantly oligomannose independently of production system or viral clade. PLoS ONE 6, e23521 (2011).
25. Doores, K.J. et al. Envelope glycans of immunodeficiency virions are almost entirely oligomannose antigens. Proc. Natl. Acad. Sci. USA 107, 13800-13805 (2010).
26. Eggink, D. et al. Lack of complex N-glycans on HIV-1 envelope glycoproteins preserves protein conformation and entry function. Virology 401, 236-247 (2010).
27. Go, E.P. et al. Characterization of glycosylation profiles of HIV-1 transmitted/founder envelopes by mass spectrometry. J. Virol. 85, 8270-8284 (2011).
28. Pabst, M., Chang, M., Stadlmann, J. & Altmann, F. Glycan profiles of the 27 N-glycosylation sites of the HIV envelope protein CN54gp140. Biol. Chem. 393, 719-730 (2012).
29. Mizuochi, T. et al. Diversity of oligosaccharide structures on the envelope glycoprotein gp 120 of human immunodeficiency virus 1 from the lymphoblastoid cell line H9. Presence of complex-type oligosaccharides with bisecting N-acetylglucosamine residues. J. Biol. Chem. 265, 8519-8524 (1990).
30. Kong, L. et al. Expression-system-dependent modulation of HIV-1 envelope glycoprotein antigenicity and immunogenicity. J. Mol. Biol. 403, 131-147 (2010).
31. Binley, J.M. et al. Role of complex carbohydrates in human immunodeficiency virus type 1 infection and resistance to antibody neutralization. J. Virol. 84, 5637-5655 (2010).
32. Ouellet, M. et al. Galectin-1 acts as a soluble host factor that promotes HIV-1 infectivity through stabilization of virus attachment to host cells. J. Immunol. 174, 4120-4126 (2005).
33. St-Pierre, C. et al. Host-soluble galectin-1 promotes HIV-1 replication through a direct interaction with glycans of viral gp120 and host CD4. J. Virol. 85, 11742-11751 (2011).
34. van Montfort, T. et al. HIV-1 N-glycan composition governs a balance between dendritic cell-mediated viral transmission and antigen presentation. J. Immunol. 187, 4676-4685 (2011).
35. Reitter, J.N., Means, R.E. & Desrosiers, R.C. A role for carbohydrates in immune evasion in AIDS. Nat. Med. 4, 679-684 (1998).
36. Wei, X. et al. Antibody neutralization and escape by HIV-1. Nature 422, 307-312 (2003).
37. Mouquet, H. et al. Complex-type N-glycan recognition by potent broadly neutralizing HIV antibodies. Proc. Natl. Acad. Sci. USA 109, E3268-E3277 (2012).
38. Bonsignori, M. et al. Analysis of a clonal lineage of HIV-1 envelope V2/V3 conformational epitope-specific broadly neutralizing antibodies and their inferred unmutated common ancestors. J. Virol. 85, 9998-10009 (2011).
39. Doores, K.J. & Burton, D.R. Variable loop glycan dependency of the broad and potent HIV-1-neutralizing antibodies PG9 and PG16. J. Virol. 84, 10510-10521 (2010).
40. Kabat, E.A., Wu, T.T., Perry, H.M., Gottesman, K.S. & Foeller, C. Sequences of Proteins of Immunological Interest (U.S. Department of Health and Human Services, National Institutes of Health, 1991).
41. Pancera, M. et al. Crystal structure of PG16 and chimeric dissection with somatically related PG9: structure-function analysis of two quaternary-specific antibodies that effectively neutralize HIV-1. J. Virol. 84, 8098-8110 (2010).
42. Otto, V.I., Schurpf, T., Folkers, G. & Cummings, R.D. Sialylated complex-type N-glycans enhance the signaling activity of soluble intercellular adhesion molecule-1 in mouse astrocytes. J. Biol. Chem. 279, 35201-35209 (2004).
43. Snchez -Felipe, L., Villar, E. & Munoz-Barroso, I. 2-3-and 2-6-N-linked sialic acids allow efficient interaction of Newcastle Disease Virus with target cells. Glycoconj. J. 29, 539-549 (2012).
44. Guo, Y. et al. Analysis of hemagglutinin-mediated entry tropism of H5N1 avian influenza. Virol. J. 6, 39 (2009).
45. Durocher, Y. & Butler, M. Expression systems for therapeutic glycoprotein production. Curr. Opin. Biotechnol. 20, 700-707 (2009).
46. Scheid, J.F. et al. Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science 333, 1633-1637 (2011).
47. Wu, X. et al. Focused evolution of HIV-1 neutralizing antibodies revealed by structures and deep sequencing. Science 333, 1593-1602 (2011).
48. Zhu, J. et al. Somatic populations of PGT135-137 HIV-1-neutralizing antibodies identified by 454 pyrosequencing and bioinformatics. Front. Microbiol. 3, 315 (2012).
49. Wu, X. et al. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329, 856-861 (2010).
50. Heyndrickx, L. et al. International network for comparison of HIV neutralization assays: the NeutNet report II. PLoS ONE 7, e36438 (2012).
51. Euler, Z. et al. Activity of broadly neutralizing antibodies, including PG9, PG16, and VRC01, against recently transmitted subtype B HIV-1 variants from early and late in the epidemic. J. Virol. 85, 7236-7245 (2011).
52. May, A.P., Robinson, R.C., Vinson, M., Crocker, P.R. & Jones, E.Y. Crystal structure of the N-terminal domain of sialoadhesin in complex with 3 sialyllactose at 1.85 A resolution. Mol. Cell 1, 719-728 (1998).
53. Somers, W.S., Tang, J., Shaw, G.D. & Camphausen, R.T. Insights into the molecular basis of leukocyte tethering and rolling revealed by structures of P-and E-selectin bound to SLe(X) and PSGL-1. Cell 103, 467-479 (2000).
54. Zhuravleva, M.A., Trandem, K. & Sun, P.D. Structural implications of Siglec-5-mediated sialoglycan recognition. J. Mol. Biol. 375, 437-447 (2008).
55. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997).
56. McCoy, A.J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
57. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
58. Adams, P.D. et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58, 1948-1954 (2002).
59. Davis, I.W. et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375-W383 (2007).
60. Li, M. et al. 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 (2005).
61. Seaman, M.S. et al. Multiclade human immunodeficiency virus type 1 envelope immunogens elicit broad cellular and humoral immunity in rhesus monkeys. J. Virol. 79, 2956-2963 (2005).
62. Haynes, B.F. et al. Cardiolipin polyspecific autoreactivity in two broadly neutralizing HIV-1 antibodies. Science 308, 1906-1908 (2005).