Mapping the complete glycoproteome of virion-derived HIV-1 gp120 provides insights into broadly neutralizing antibody binding

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Panico, Maria ^a   Bouché, Laura ^a   Binet, Daniel ^b   O'Connor, Michael John ^b   Rahman, Dinah ^a   Pang, Poh Choo ^a   Canis, Kevin ^a,e   North, Simon J ^a   Desrosiers, Ronald C ^c   Chertova, Elena ^d   Keele, Brandon F ^d   Bess, Julian W ^d   Lifson, Jeffrey D ^d   Haslam, Stuart M ^a   Dell, Anne ^a   Morris, Howard R ^a,b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b BioPharmaSpec Ltd   (United Kingdom)

^c UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^d FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^e SGS   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN GP 120; GP120 PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; MANNOSE OLIGOSACCHARIDE; NEUTRALIZING ANTIBODY; OLIGOSACCHARIDE; POLYSACCHARIDE; PROTEIN BINDING; PROTEOME;

AMINO ACID SEQUENCE; ANTIGEN ANTIBODY REACTION; BINDING SITE; CARBOHYDRATE ANALYSIS; CELL LINE; CHEMISTRY; GENETICS; GLYCOSYLATION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; METABOLISM; PROTEIN SECONDARY STRUCTURE; PROTEOMICS; VIRUS GENOME;

AMINO ACID SEQUENCE; ANTIBODIES, NEUTRALIZING; ANTIGEN-ANTIBODY REACTIONS; BINDING SITES; CARBOHYDRATE SEQUENCE; CELL LINE; GENOME, VIRAL; GLYCOSYLATION; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; OLIGOSACCHARIDES; POLYSACCHARIDES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEOME; PROTEOMICS;

EID: 84986628335     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep32956     Document Type: Article

References (52)

1. Pejchal, R. et al. A potent and broad neutralizing antibody recognizes and penetrates the HIV glycan shield. Science 334, 1097-1103, doi: 10.1126/science.1213256 (2011).
2. Qi, Y., Jo, S. & Im, W. Roles of glycans in interactions between gp120 and HIV broadly neutralizing antibodies. Glycobiology 26, 251-260, doi: 10.1093/glycob/cwv101 (2016).
3. 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).
4. 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).
5. Go, E. P. et al. Glycosylation site-specific analysis of clade C HIV-1 envelope proteins. Journal of proteome research 8, 4231-4242, doi: 10.1021/pr9002728 (2009).
6. 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. The Journal of biological chemistry 265, 10373-10382 (1990).
7. Go, E. P. et al. Characterization of host-cell line specific glycosylation profiles of early transmitted/founder HIV-1 gp120 envelope proteins. Journal of proteome research 12, 1223-1234, doi: 10.1021/pr300870t (2013).
8. Doores, K. J. et al. Envelope glycans of immunodeficiency virions are almost entirely oligomannose antigens. Proc Natl Acad Sci USA 107, 13800-13805, doi: 10.1073/pnas.1006498107 (2010).
9. Pritchard, L. K. et al. Glycan clustering stabilizes the mannose patch of HIV-1 and preserves vulnerability to broadly neutralizing antibodies. Nat Commun 6, 7479, doi: 10.1038/ncomms8479 (2015).
10. Go, E. P. et al. Comparative Analysis of the Glycosylation Profiles of Membrane-Anchored HIV-1 Envelope Glycoprotein Trimers and Soluble gp140. J Virol 89, 8245-8257, doi: 10.1128/JVI.00628-15 (2015).
11. Behrens, A. J. et al. Composition and Antigenic Effects of Individual Glycan Sites of a Trimeric HIV-1 Envelope Glycoprotein. Cell Rep 14, 2695-2706, doi: 10.1016/j.celrep.2016.02.058 (2016).
12. Guttman, M. et al. CD4-induced activation in a soluble HIV-1 Env trimer. Structure 22, 974-984, doi: 10.1016/j.str.2014.05.001 (2014).
13. Chertova, E. et al. Envelope glycoprotein incorporation, not shedding of surface envelope glycoprotein (gp120/SU), Is the primary determinant of SU content of purified human immunodeficiency virus type 1 and simian immunodeficiency virus. J Virol 76, 5315-5325 (2002).
14. Zhu, P. et al. Electron tomography analysis of envelope glycoprotein trimers on HIV and simian immunodeficiency virus virions. Proc Natl Acad Sci USA 100, 15812-15817, doi: 10.1073/pnas.2634931100 (2003).
15. Louder, M. K. et al. HIV-1 envelope pseudotyped viral vectors and infectious molecular clones expressing the same envelope glycoprotein have a similar neutralization phenotype, but culture in peripheral blood mononuclear cells is associated with decreased neutralization sensitivity. Virology 339, 226-238, doi: 10.1016/j.virol.2005.06.003 (2005).
16. Jones, D. R., Suzuki, K. & Piller, S. C. A 100-amino acid truncation in the cytoplasmic tail of glycoprotein 41 in the reference HIV type 1 strain RF. AIDS Res Hum Retroviruses 18, 513-517, doi: 10.1089/088922202317406664 (2002).
17. Bonomelli, C. et al. The glycan shield of HIV is predominantly oligomannose independently of production system or viral clade. PLoS One 6, e23521, doi: 10.1371/journal.pone.0023521 (2011).
18. Doores, K. J. The HIV glycan shield as a target for broadly neutralizing antibodies. FEBS J 282, 4679-4691, doi: 10.1111/febs.13530 (2015).
19. Johnston, P. B., Dubay, J. W. & Hunter, E. Truncations of the simian immunodeficiency virus transmembrane protein confer expanded virus host range by removing a block to virus entry into cells. J Virol 67, 3077-3086 (1993).
20. Yuste, E., Johnson, W., Pavlakis, G. N. & Desrosiers, R. C. Virion envelope content, infectivity, and neutralization sensitivity of simian immunodeficiency virus. J Virol 79, 12455-12463, doi: 10.1128/JVI.79.19.12455-12463.2005 (2005).
21. Yuste, E., Reeves, J. D., Doms, R. W. & Desrosiers, R. C. Modulation of Env content in virions of simian immunodeficiency virus: correlation with cell surface expression and virion infectivity. J Virol 78, 6775-6785, doi: 10.1128/JVI.78.13.6775-6785.2004 (2004).
22. Pritchard, L. K., Harvey, D. J., Bonomelli, C., Crispin, M. & Doores, K. J. Cell- and Protein-Directed Glycosylation of Native Cleaved HIV-1 Envelope. J Virol 89, 8932-8944, doi: 10.1128/JVI.01190-15 (2015).
23. Yang, W. et al. Glycoform analysis of recombinant and human immunodeficiency virus envelope protein gp120 via higher energy collisional dissociation and spectral-aligning strategy. Anal Chem 86, 6959-6967, doi: 10.1021/ac500876p (2014).
24. Stewart-Jones, G. B. et al. Trimeric HIV-1-Env Structures Define Glycan Shields from Clades A, B, and G. Cell 165, 813-826, doi: 10.1016/j.cell.2016.04.010 (2016).
25. Lee, J. H., Ozorowski, G. & Ward, A. B. Cryo-EM structure of a native, fully glycosylated, cleaved HIV-1 envelope trimer. Science 351, 1043-1048, doi: 10.1126/science.aad2450 (2016).
26. Scanlan, C. N. et al. The broadly neutralizing anti-human immunodeficiency virus type 1 antibody 2G12 recognizes a cluster of alpha1-> 2 mannose residues on the outer face of gp120. J Virol 76, 7306-7321 (2002).
27. Doores, K. J., Fulton, Z., Huber, M., Wilson, I. A. & Burton, D. R. Antibody 2G12 recognizes di-mannose equivalently in domainand nondomain-exchanged forms but only binds the HIV-1 glycan shield if domain exchanged. J Virol 84, 10690-10699, doi: 10.1128/JVI.01110-10 (2010).
28. Sok, D. et al. Promiscuous glycan site recognition by antibodies to the high-mannose patch of gp120 broadens neutralization of HIV. Sci Transl Med 6, 236ra263, doi: 10.1126/scitranslmed.3008104 (2014).
29. McLellan, J. S. et al. Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9. Nature 480, 336-343, doi: 10.1038/nature10696 (2011).
30. Pancera, M. et al. Structural basis for diverse N-glycan recognition by HIV-1-neutralizing V1-V2-directed antibody PG16. Nat Struct Mol Biol 20, 804-813, doi: 10.1038/nsmb.2600 (2013).
31. Zhou, T. et al. Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 329, 811-817, doi: 10.1126/ science.1192819 (2010).
32. Means, R. E. et al. Ability of the V3 loop of simian immunodeficiency virus to serve as a target for antibody-mediated neutralization: correlation of neutralization sensitivity, growth in macrophages, and decreased dependence on CD4. J Virol 75, 3903-3915, doi: 10.1128/JVI.75.8.3903-3915.2001 (2001).
33. Del Prete, G. Q. et al. Derivation and characterization of a simian immunodeficiency virus SIVmac239 variant with tropism for CXCR4. J Virol 83, 9911-9922, doi: 10.1128/JVI.00533-09 (2009).
34. Keele, B. F. et al. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci USA 105, 7552-7557, doi: 10.1073/pnas.0802203105 (2008).
35. Del Prete, G. Q. et al. Comparative characterization of transfection- and infection-derived simian immunodeficiency virus challenge stocks for in vivo nonhuman primate studies. J Virol 87, 4584-4595, doi: 10.1128/JVI.03507-12 (2013).
36. Moody, A. M. et al. Sialic acid capping of CD8beta core 1-O-glycans controls thymocyte-major histocompatibility complex class I interaction. The Journal of biological chemistry 278, 7240-7246, doi: 10.1074/jbc.M210468200 (2003).
37. van Der Wel, H. et al. A non-Golgi alpha 1,2-fucosyltransferase that modifies Skp1 in the cytoplasm of Dictyostelium. The Journal of biological chemistry 276, 33952-33963, doi: 10.1074/jbc.M102555200 (2001).
38. Haslam, S. M., North, S. J. & Dell, A. Mass spectrometric analysis of N- and O-glycosylation of tissues and cells. Curr Opin Struct Biol 16, 584-591, doi: 10.1016/j.sbi.2006.08.006 (2006).
39. Jang-Lee, J. et al. Glycomic profiling of cells and tissues by mass spectrometry: fingerprinting and sequencing methodologies. Methods Enzymol 415, 59-86, doi: 10.1016/S0076-6879(06)15005-3 (2006).
40. North, S. J. et al. Mass spectrometric analysis of mutant mice. Methods Enzymol 478, 27-77, doi: 10.1016/S0076-6879(10)78002-2 (2010).
41. Ciucanu, I. & Kerek, F. A simple and rapid method for the permethylation of carbohydrates. Carbohydrate Research 131, 209-217, doi: http://dx.doi.org/10.1016/0008-6215(84)85242-8 (1984).
42. Morris, H. R. Studies towards the complete sequence determination of proteins by mass spectrometry; a rapid procedure for the successful permethylation of histidine containing peptides. FEBS Lett 22, 257-260 (1972).
43. Ceroni, A. et al. GlycoWorkbench: a tool for the computer-assisted annotation of mass spectra of glycans. Journal of proteome research 7, 1650-1659, doi: 10.1021/pr7008252 (2008).
44. Damerell, D. et al. Annotation of glycomics MS and MS/MS spectra using the GlycoWorkbench software tool. Methods Mol Biol 1273, 3-15, doi: 10.1007/978-1-4939-2343-4-1 (2015).
45. Harrison, R. et al. Glycoproteomic characterization of recombinant mouse alpha-dystroglycan. Glycobiology 22, 662-675, doi: 10.1093/glycob/cws002 (2012).
46. Tissot, B. et al. Glycoproteomics: past, present and future. FEBS Lett 583, 1728-1735, doi: 10.1016/j.febslet.2009.03.049 (2009).
47. Teng-umnuay, P. et al. The cytoplasmic F-box binding protein SKP1 contains a novel pentasaccharide linked to hydroxyproline in Dictyostelium. The Journal of biological chemistry 273, 18242-18249 (1998).
48. Dell, A. & Morris, H. R. Glycoprotein structure determination by mass spectrometry. Science 291, 2351-2356 (2001).
49. Morris, H. R. et al. High sensitivity collisionally-activated decomposition tandem mass spectrometry on a novel quadrupole/ orthogonal-acceleration time-of-flight mass spectrometer. Rapid Commun Mass Spectrom 10, 889-896, doi: 10.1002/(SICI)1097- 0231(19960610)10:8 889::AID-RCM6153.0.CO;2-F (1996).
50. Arthur, L. O. et al. Chemical inactivation of retroviral infectivity by targeting nucleocapsid protein zinc fingers: a candidate SIV vaccine. AIDS Res Hum Retroviruses 14 Suppl 3, S311-S319 (1998).
51. Rossio, J. L. et al. Inactivation of human immunodeficiency virus type 1 infectivity with preservation of conformational and functional integrity of virion surface proteins. J Virol 72, 7992-8001 (1998).
52. Chertova, E. et al. Sites, mechanism of action and lack of reversibility of primate lentivirus inactivation by preferential covalent modification of virion internal proteins. Curr Mol Med 3, 265-272 (2003).