High-mannose glycan-dependent epitopes are frequently targeted in broad neutralizing antibody responses during human immunodeficiency virus type 1 infection

Journal of Virology

Volumn 86, Issue 4, 2012, Pages 2153-2164

  Lavine, Christy L ^a   Lao, Socheata ^a   Montefiori, David C ^b   Haynes, Barton F ^b   Sodroski, Joseph G ^c   Yang, Xinzhen ^a  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GLYCAN; MANNOSE; NEUTRALIZING ANTIBODY; VIRUS ANTIBODY; VIRUS GLYCOPROTEIN;

ANTIBODY RESPONSE; ANTIGEN ANTIBODY REACTION; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MAJOR CLINICAL STUDY; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN DEPLETION; PROTEIN TARGETING; VIRUS NEUTRALIZATION;

ANTIBODIES, NEUTRALIZING; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; EPITOPE MAPPING; EPITOPES; HIV ANTIBODIES; HIV INFECTIONS; HIV-1; HUMANS; MANNOSE; NEUTRALIZATION TESTS; POLYSACCHARIDES;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84863115983     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.06201-11     Document Type: Article

References (65)

1. Agrawal-Gamse C, et al. 2011. Yeast-elicited cross-reactive antibodies to HIV Env glycans efficiently neutralize virions expressing exclusively highmannose N-linked glycans. J. Virol. 85:470-480.
2. Astronomo RD, et al. 2010. Defining criteria for oligomannose immunogens for HIV using icosahedral virus capsid scaffolds. Chem. Biol. 17:357-370.
3. Astronomo RD, et al. 2008. A glycoconjugate antigen based on the recognition motif of a broadly neutralizing human immunodeficiency virus antibody, 2G12, is immunogenic but elicits antibodies unable to bind to the self glycans of gp120. J. Virol. 82:6359-6368.
4. Bernstein HB, Tucker SP, Hunter E, Schutzbach JS, Compans RW. 1994. Human immunodeficiency virus type 1 envelope glycoprotein is modified by O-linked oligosaccharides. J. Virol. 68:463-468.
5. Binley JM, et al. 2008. 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.
6. Blixt O, et al. 2004. Printed covalent glycan array for ligand profiling of diverse glycan binding proteins. Proc. Natl. Acad. Sci. U. S. A. 101:17033-17038.
7. Bonay P, Hughes RC. 1991. Purification and characterization of a novel broad-specificity (alpha 1-2, alpha 1-3 and alpha 1-6) mannosidase from rat liver. Eur. J. Biochem. 197:229-238.
8. Bonsignori M, et al. 2011. 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.
9. Buchacher A, et al. 1994. Generation of human monoclonal antibodies against HIV-1 proteins; electrofusion and Epstein-Barr virus transformation for peripheral blood lymphocyte immortalization. AIDS Res. Hum. Retroviruses 10:359-369.
10. Burton DR, et al. 1991. A large array of human monoclonal antibodies to type 1 human immunodeficiency virus from combinatorial libraries of asymptomatic seropositive individuals. Proc. Natl. Acad. Sci. U. S. A. 88:10134-10137.
11. Burton DR, et al. 1994. Efficient neutralization of primary isolates of HIV-1 by a recombinant human monoclonal antibody. Science 266:1024-1027.
12. Capon DJ, et al. 1989. Designing CD4 immunoadhesins for AIDS therapy. Nature 337:525-531.
13. Dieltjens T, et al. 2009. HIV type 1 subtype A envelope genetic evolution in a slow progressing individual with consistent broadly neutralizing antibodies. AIDS Res. Hum. Retroviruses 25:1165-1169.
14. Doms RW. 2010. Immunology. Prime, boost, and broaden. Science 329:1021-1022.
15. Doores KJ, et al. 2010. Envelope glycans of immunodeficiency virions are almost entirely oligomannose antigens. Proc. Natl. Acad. Sci. U. S. A. 107:13800-13805.
16. Doores KJ, Burton DR. 2010. Variable loop glycan dependency of the broad and potent HIV-1-neutralizing antibodies PG9 and PG16. J. Virol. 84:10510-10521.
17. Doores KJ, et al. 2010. A nonself sugar mimic of the HIV glycan shield shows enhanced antigenicity. Proc. Natl. Acad. Sci. U. S. A. 107:17107-17112.
18. Doria-Rose NA, et al. 2010. Breadth of human immunodeficiency virusspecific neutralizing activity in sera: clustering analysis and association with clinical variables. J. Virol. 84:1631-1636.
19. Dunlop DC, et al. 2010. Polysaccharide mimicry of the epitope of the broadly neutralizing anti-HIV antibody, 2G12, induces enhanced antibody responses to self oligomannose glycans. Glycobiology 20:812-823.
20. Finzi A, et al. 2010. Topological layers in the HIV-1 gp120 inner domain regulate gp41 interaction and CD4-triggered conformational transitions. Mol. Cell 37:656-667.
21. Geyer H, Holschbach C, Hunsmann G, Schneider J. 1988. Carbohydrates of human immunodeficiency virus. Structures of oligosaccharides linked to the envelope glycoprotein 120. J. Biol. Chem. 263:11760-11767.
22. Go EP, et al. 2011. Characterization of glycosylation profiles of HIV-1 transmitted/founder envelopes by mass spectrometry. J. Virol. 85:8270-8284.
23. Go EP, et al. 2007. GlycoPep DB: a tool for glycopeptide analysis using a "smart search." Anal. Chem. 79:1708-1713.
24. Gray ES, et al. 2009. Antibody specificities associated with neutralization breadth in plasma from human immunodeficiency virus type 1 subtype C-infected blood donors. J. Virol. 83:8925-8937.
25. Joyce JG, et al. 2008. An oligosaccharide-based HIV-1 2G12 mimotope vaccine induces carbohydrate-specific antibodies that fail to neutralize HIV-1 virions. Proc. Natl. Acad. Sci. U. S. A. 105:15684-15689.
26. Kong L, et al. 2010. Expression-system-dependent modulation of HIV-1 envelope glycoprotein antigenicity and immunogenicity. J. Mol. Biol. 403:131-147.
27. Korber BF, Kuiken FC, Pillai S, Sodroksi J. 1998. Numbering positions in HIV relative to HXBc2, p. III-102-111. In Korber BK, et al (ed), Human retroviruses and AIDS. Los Alamos National Laboratories, Los Alamos, NM.
28. Kornfeld R, Kornfeld S. 1985. Assembly of asparagine-linked oligosaccharides. Annu. Rev. Biochem. 54:631-664.
29. Kwong PD, et al. 1998. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393:648-659.
30. Leonard CK, et al. 1990. 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.
31. Li M, et al. 2006. Genetic and neutralization properties of subtype C human immunodeficiency virus type 1 molecular env clones from acute and early heterosexually acquired infections in Southern Africa. J. Virol. 80:11776-11790.
32. Li Y, et al. 2007. Broad HIV-1 neutralization mediated by CD4-binding site antibodies. Nat. Med. 13:1032-1034.
33. Li Y, et al. 2009. Analysis of neutralization specificities in polyclonal sera derived from human immunodeficiency virus type 1-infected individuals. J. Virol. 83:1045-1059.
34. Luallen RJ, et al. 2010. Antibodies against Manalpha1,2-Manalpha1,2-Man oligosaccharide structures recognize envelope glycoproteins from HIV-1 and SIV strains. Glycobiology 20:280-286.
35. Luallen RJ, et al. 2009. A yeast glycoprotein shows high-affinity binding to the broadly neutralizing human immunodeficiency virus antibody 2G12 and inhibits gp120 interactions with 2G12 and DC-SIGN. J. Virol. 83:4861-4870.
36. Merkle RK, et al. 1991. gp160 of HIV-I synthesized by persistently infected Molt-3 cells is terminally glycosylated: evidence that cleavage of gp160 occurs subsequent to oligosaccharide processing. Arch. Biochem. Biophys. 290:248-257.
37. Mizuochi T, et al. 1990. Diversity of oligosaccharide structures on the envelope glycoprotein gp120 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.
38. Nandi A, et al. 2010. Epitopes for broad and potent neutralizing antibody responses during chronic infection with human immunodeficiency virus type 1. Virology 396:339-348.
39. Pancera M, et al. 2010. Structure of HIV-1 gp120 with gp41-interactive region reveals layered envelope architecture and basis of conformational mobility. Proc. Natl. Acad. Sci. U. S. A. 107:1166-1171.
40. Piantadosi A, et al. 2009. Breadth of neutralizing antibody response to human immunodeficiency virus type 1 is affected by factors early in infection but does not influence disease progression. J. Virol. 83:10269-10274.
41. Posner MR, Cavacini LA, Emes CL, Power J, Byrn R. 1993. Neutralization of HIV-1 by F105, a human monoclonal antibody to the CD4 binding site of gp120. J. Acquir. Immune Defic. Syndr. 6:7-14.
42. Purtscher M, et al. 1994. A broadly neutralizing human monoclonal antibody against gp41 of human immunodeficiency virus type 1. AIDS Res. Hum. Retroviruses 10:1651-1658.
43. Raska M, et al. 2010. Glycosylation patterns of HIV-1 gp120 depend on the type of expressing cells and affect antibody recognition. J. Biol. Chem. 285:20860-20869.
44. Sather DN, Stamatatos L. 2010. Epitope specificities of broadly neutralizing plasmas from HIV-1 infected subjects. Vaccine 28(Suppl 2):B8-B12.
45. Scanlan CN, et al. 2007. Inhibition of mammalian glycan biosynthesis produces non-self antigens for a broadly neutralising, HIV-1 specific antibody. J. Mol. Biol. 372:16-22.
46. Simek MD, et al. 2009. Human immunodeficiency virus type 1 elite neutralizers: individuals with broad and potent neutralizing activity identified by using a high-throughput neutralization assay together with an analytical selection algorithm. J. Virol. 83:7337-7348.
47. Stein BS, Engleman EG. 1990. Intracellular processing of the gp160 HIV-1 envelope precursor. Endoproteolytic cleavage occurs in a cis or medial compartment of the Golgi complex. J. Biol. Chem. 265:2640-2649.
48. Sullivan N, et al. 1998. Determinants of human immunodeficiency virus type 1 envelope glycoprotein activation by soluble CD4 and monoclonal antibodies. J. Virol. 72:6332-6338.
49. Tomaras GD, et al. 2011. Polyclonal B cell responses to conserved neutralization epitopes in a subset of HIV-1-infected individuals. J. Virol. 85:11502-11519.
50. Traunecker A, Schneider J, Kiefer H, Karjalainen K. 1989. Highly efficient neutralization of HIV with recombinant CD4-immunoglobulin molecules. Nature 339:68-70.
51. Trkola A, et al. 1996. Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1. J. Virol. 70:1100-1108.
52. Tulsiani DR, Harris TM, Touster O. 1982. Swainsonine inhibits the biosynthesis of complex glycoproteins by inhibition of Golgi mannosidase II. J. Biol. Chem. 257:7936-7939.
53. Varki A, et al (ed). 2009. Essentials of glycobiology, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, NY.
54. Walker LM, et al. 2011. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477:466-470.
55. Walker LM, et al. 2009. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326:285-289.
56. Walker LM, et al. 2010. A limited number of antibody specificities mediate broad and potent serum neutralization in selected HIV-1 infected individuals. PLoS Pathog. 6:e1001028.
57. Wang SK, et al. 2008. Targeting the carbohydrates on HIV-1: interaction of oligomannose dendrons with human monoclonal antibody 2G12 and DC-SIGN. Proc. Natl. Acad. Sci. U. S. A. 105:3690-3695.
58. Workman CJ, Rice DS, Dugger KJ, Kurschner C, Vignali DA. 2002. Phenotypic analysis of the murine CD4-related glycoprotein, CD223 (LAG-3). Eur. J. Immunol. 32:2255-2263.
59. Wu X, et al. 2010. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329:856-861.
60. Wyatt R, et al. 1998. The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 393:705-711.
61. Xiang SH, et al. 2005. Functional mimicry of a human immunodeficiency virus type 1 coreceptor by a neutralizing monoclonal antibody. J. Virol. 79:6068-6077.
62. Xiang SH, et al. 2003. Epitope mapping and characterization of a novel CD4-induced human monoclonal antibody capable of neutralizing primary HIV-1 strains. Virology 315:124-134.
63. Yang X, Mahony E, Holm GH, Kassa A, Sodroski J. 2003. Role of the gp120 inner domain beta-sandwich in the interaction between the human immunodeficiency virus envelope glycoprotein subunits. Virology 313:117-125.
64. Yang X, et al. 2004. Characterization of the outer domain of the gp120 glycoprotein from human immunodeficiency virus type 1. J. Virol. 78:12975-12986.
65. Yang X, Wyatt R, Sodroski J. 2001. Improved elicitation of neutralizing antibodies against primary human immunodeficiency viruses by soluble stabilized envelope glycoprotein trimers. J. Virol. 75:1165-1171.