Global site-specific N-glycosylation analysis of HIV envelope glycoprotein

Nature Communications

Volumn 8, Issue , 2017, Pages

  Cao, Liwei ^a   Diedrich, Jolene K ^a   Kulp, Daniel W ^a   Pauthner, Matthias ^a   He, Lin ^a   Park, Sung Kyu Robin ^a   Sok, Devin ^a   Su, Ching Yao ^a   Delahunty, Claire M ^a   Menis, Sergey ^a   Andrabi, Raiees ^a   Guenaga, Javier ^a   Georgeson, Erik ^a   Kubitz, Michael ^a   Adachi, Yumiko ^a   Burton, Dennis R ^a   Schief, William R ^a   Yates, John R ^a   Paulson, James C ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; EPITOPE; GLYCOPROTEIN GP 120; PEPTIDE; POLYSACCHARIDE;

DESIGN; DRUG DEVELOPMENT; IMMUNE RESPONSE; PEPTIDE; PROTEIN; PROTEOMICS; VACCINE;

AMINO ACID SEQUENCE; ARTICLE; MASS SPECTROMETRY; PROTEIN GLYCOSYLATION; PROTEOMICS; QUANTITATIVE ANALYSIS; CHEMISTRY; GLYCOSYLATION; HUMAN IMMUNODEFICIENCY VIRUS 1; METABOLISM; MOLECULAR MODEL; PROTEIN MULTIMERIZATION; REPRODUCIBILITY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EPITOPES; GLYCOSYLATION; HIV ENVELOPE PROTEIN GP120; HIV-1; MASS SPECTROMETRY; MODELS, MOLECULAR; PEPTIDES; POLYSACCHARIDES; PROTEIN MULTIMERIZATION; REPRODUCIBILITY OF RESULTS;

EID: 85016232433     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms14954     Document Type: Article

References (90)

1. Burton, D. R. & Hangartner, L. Broadly neutralizing antibodies to HIV and their role in vaccine design. Annu. Rev. Immunol. 34, 635-659 (2016)
2. Hessell, A. J. et al. Broadly neutralizing monoclonal antibodies 2F5 and 4E10 directed against the human immunodeficiency virus type 1 gp41 membrane-proximal external region protect against mucosal challenge by simian-human immunodeficiency virus SHIVBa-L. J. Virol. 84, 1302-1313 (2010).
3. Moldt, B. et al. Highly potent HIV-specific antibody neutralization in vitro translates into effective protection against mucosal SHIV challenge in vivo. Proc. Natl Acad. Sci. USA 109, 18921-18925 (2012).
4. Kwong, P. D. & Mascola, J. R. Human antibodies that neutralize HIV-1: identification, structures, and B cell ontogenies. Immunity 37, 412-425 (2012).
5. Sanders, R. W. et al. HIV-1 neutralizing antibodies induced by native-like envelope trimers. Science 349, aac4223 (2015).
6. Jardine, J. G. et al. Priming a broadly neutralizing antibody response to HIV-1 using a germline-targeting immunogen. Science 349, 156-161 (2015).
7. Reitter, J. N., Means, R. E. & Desrosiers, R. C. A role for carbohydrates in immune evasion in AIDS. Nat. Med. 4, 679-684 (1998).
8. Wei, X. P. et al. Antibody neutralization and escape by HIV-1. Nature 422, 307-312 (2003).
9. Chackerian, B., Rudensey, L. M. & Overbaugh, J. Specific N-linked and O-linked glycosylation modifications in the envelope V1 domain of simian immunodeficiency virus variants that evolve in the host alter recognition by neutralizing antibodies. J. Virol. 71, 7719-7727 (1997).
10. Back, N. K. T. et al. An N-glycan within the human-immunodeficiency-virus type-1 Gp120 V3 loop affects virus neutralization. Virology 199, 431-438 (1994).
11. Julien, J. P. et al. Crystal structure of a soluble cleaved HIV-1 envelope trimer. Science 342, 1477-1483 (2013).
12. Falkowska, E. et al. Broadly neutralizing HIV antibodies define a glycandependent epitope on the prefusion conformation of gp41 on cleaved envelope trimers. Immunity 40, 657-668 (2014).
13. 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 (2013).
14. Alam, S. M. et al. Recognition of synthetic glycopeptides by HIV-1 broadly neutralizing antibodies and their unmutated ancestors. Proc. Natl Acad. Sci. USA 110, 18214-18219 (2013).
15. Julien, J. P. et al. Broadly neutralizing antibody PGT121 allosterically modulates CD4 binding via recognition of the HIV-1 gp120 V3 base and multiple surrounding glycans. PLoS Pathog. 9, e1003342 (2013).
16. Garces, F. et al. Structural evolution of glycan recognition by a family of potent HIV antibodies. Cell 159, 69-79 (2014).
17. Sok, D. et al. Promiscuous glycan site recognition by antibodies to the highmannose patch of gp120 broadens neutralization of HIV. Sci. Transl. Med. 6, 236ra63 (2014).
18. Amin, M. N. et al. Synthetic glycopeptides reveal the glycan specificity of HIV-neutralizing antibodies. Nat. Chem. Biol. 9, 521-526 (2013).
19. Walker, L. M. et al. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477, 466-U117 (2011).
20. Raska, M. et al. Glycosylation patterns of HIV-1 gp120 depend on the type of expressing cells and affect antibody recognition. J. Biol. Chem. 285, 20860-20869 (2010).
21. Kong, L. et al. Expression-system-dependent modulation of HIV-1 envelope glycoprotein antigenicity and immunogenicity. J. Mol. Biol. 403, 131-147 (2010).
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 (2015).
23. Pritchard, L. K. et al. Structural constraints determine the glycosylation of HIV-1 envelope trimers. Cell Rep. 11, 1604-1613 (2015).
24. 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 (2016).
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. Bonomelli, C. et al. The glycan shield of HIV is predominantly oligomannose independently of production system or viral clade. PLoS ONE 6, e23521 (2011).
27. Go, E. P. et al. Glycosylation site-specific analysis of clade C HIV-1 envelope proteins. J. Proteome. Res. 8, 4231-4242 (2009).
28. Go, E. P. et al. Comparative analysis of the glycosylation profiles of membraneanchored HIV-1 envelope glycoprotein trimers and soluble gp140. J. Virol. 89, 8245-8257 (2015).
29. Go, E. P. et al. Characterization of glycosylation profiles of HIV-1 transmitted/ founder envelopes by mass spectrometry. J. Virol. 85, 8270-8284 (2011).
30. Go, E. P. et al. Glycosylation site-specific analysis of HIV envelope proteins (JR-FL and CON-S) reveals major differences in glycosylation site occupancy, glycoform profiles, and antigenic epitopes' accessibility. J. Proteome Res. 7, 1660-1674 (2008).
31. Go, E. P. et al. Characterization of host-cell line specific glycosylation profiles of early transmitted/founder HIV-1 gp120 envelope proteins. J. Proteome Res. 12, 1223-1234 (2013).
32. 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).
33. Zhu, X. G., 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).
34. Behrens, A. J. et al. Molecular architecture of the cleavage-dependent mannose patch on a soluble HIV-1 envelope glycoprotein trimer. J. Virol. 91, e01894-16 (2017).
35. Go, E. P. et al. Methods development for analysis of partially deglycosylated proteins and application to an HIV envelope protein vaccine candidate. Int. J. Mass Spectrom. 305, 209-216 (2011).
36. Hagglund, P. et al. An enzymatic deglycosylation scheme enabling identification of core fucosylated N-glycans and O-glycosylation site mapping of human plasma proteins. J. Proteome Res. 6, 3021-3031 (2007).
37. Angel, P. M., Lim, J. M., Wells, L., Bergmann, C. & Orlando, R. A potential pitfall in O-18-based N-linked glycosylation site mapping. Rapid Commun. Mass Sp 21, 674-682 (2007).
38. Kaji, H. et al. Lectin affinity capture, isotope-coded tagging and mass spectrometry to identify N-linked glycoproteins. Nat. Biotechnol. 21, 667-672 (2003).
39. Khemiri, A. et al. N-Glycosidase treatment with O-18 labeling and de novo sequencing argues for flagellin FliC glycopolymorphism in Pseudomonas aeruginosa. Anal. Bioanal. Chem. 405, 9835-9842 (2013).
40. Chen, R. et al. Development of a combined chemical and enzymatic approach for the mass spectrometric identification and quantification of aberrant N-glycosylation. J. Proteomics 75, 1666-1674 (2012).
41. Kolarich, D., Jensen, P. H., Altmann, F. & Packer, N. H. Determination of sitespecific glycan heterogeneity on glycoproteins. Nat. Protoc. 7, 1285-1298 (2012).
42. Gatlin, C. L., Eng, J. K., Cross, S. T., Detter, J. C. & Yates, J. R. Automated identification of amino acid sequence variations in proteins by HPLC/ microspray tandem mass spectrometry. Anal. Chem. 72, 757-763 (2000).
43. Eng, J. K., Mccormack, A. L. & Yates, J. R. An approach to correlate tandem mass-spectral data of peptides with amino-acid-sequences in a protein database. J. Am. Soc. Mass Spectrom. 5, 976-989 (1994).
44. Xu, T. et al. ProLuCID: an improved SEQUEST-like algorithm with enhanced sensitivity and specificity. J. Proteomics 129, 16-24 (2015).
45. Tabb, D. L., McDonald, W. H. & Yates, J. R. DTASelect and contrast: tools for assembling and comparing protein identifications from shotgun proteomics. J. Proteome Res. 1, 21-26 (2002).
46. He, L., Diedrich, J., Chu, Y. Y. & Yates, J. R. Extracting accurate precursor information for tandem mass spectra by raw converter. Anal. Chem. 87, 11361-11367 (2015).
47. Park, S. K., Venable, J. D., Xu, T. & Yates, J. R. A quantitative analysis software tool for mass spectrometry-based proteomics. Nat. Methods 5, 319-322 (2008).
48. Lee, P. S. et al. Receptor mimicry by antibody F045-092 facilitates universal binding to the H3 subtype of influenza virus. Nat. Commun. 5, 3614 (2014).
49. Zhu, Z. K., Go, E. P. & Desaire, H. Absolute quantitation of glycosylation site occupancy using isotopically labeled standards and LC-MS. J. Am. Soc. Mass Spectrom. 25, 1012-1017 (2014).
50. An, Y. M., McCullers, J. A., Alymova, I., Parsons, L. M. & Cipollo, J. F. Glycosylation analysis of engineered H3N2 influenza A virus hemagglutinins with sequentially added historically relevant glycosylation sites. J. Proteome Res. 14, 3957-3969 (2015).
51. Khatri, K. et al. Integrated omics and computational glycobiology reveal structural basis for influenza A virus glycan microheterogeneity and host interactions. Mol. Cell. Proteomics 15, 1895-1912 (2016).
52. Sanders, R. W. et al. A next-generation cleaved, soluble HIV-1 Env trimer, BG505 SOSIP.664 gp140, expresses multiple epitopes for broadly neutralizing but not non-neutralizing antibodies. PLoS Pathog. 9, e1003618 (2013).
53. Lyumkis, D. et al. Cryo-EM structure of a fully glycosylated soluble cleaved HIV-1 envelope trimer. Science 342, 1484-1490 (2013).
54. Do Kwon, Y. et al. Crystal structure, conformational fixation and entry-related interactions of mature ligand-free HIV-1 Env. Nat. Struct. Mol. Biol. 22, 522 (2015).
55. Garces, F. et al. Affinity maturation of a potent family of HIV antibodies is primarily focused on accommodating or avoiding glycans. Immunity 43, 1053-1063 (2015).
56. Guttman, M. et al. CD4-induced activation in a soluble HIV-1 Env trimer. Structure 22, 974-984 (2014).
57. McLellan, J. S. et al. Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9. Nature 480, 336-U386 (2011).
58. Mouquet, H. et al. Complex-type N-glycan recognition by potent broadly neutralizing HIV antibodies. Proc. Natl Acad. Sci. USA 109, E3268-E3277 (2012).
59. Mathys, L., Francois, K. O., Quandte, M., Braakman, I. & Balzarini, J. Deletion of the highly conserved N-glycan at Asn260 of HIV-1 gp120 affects folding and lysosomal degradation of gp120, and results in loss of viral infectivity. PLoS ONE 9, e101181 (2014).
60. Blattner, C. et al. Structural delineation of a quaternary, cleavage-dependent epitope at the gp41-gp120 interface on intact HIV-1 Env trimers. Immunity 40, 669-680 (2014).
61. Depetris, R. S. et al. Partial enzymatic deglycosylation preserves the structure of cleaved recombinant HIV-1 envelope glycoprotein trimers. J. Biol. Chem. 287, 24239-24254 (2012).
62. Sliepen, K., van Montfort, T., Melchers, M., Isik, G. & Sanders, R. W. Immunosilencing a highly immunogenic protein trimerization domain. J. Biol. Chem. 290, 7436-7442 (2015).
63. Stavenhagen, K. et al. Quantitative mapping of glycoprotein microheterogeneity and macro-heterogeneity: an evaluation of mass spectrometry signal strengths using synthetic peptides and glycopeptides. J. Mass Spectrom. 48, 627-639 (2013).
64. 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).
65. Pugach, P. et al. A native-like SOSIP.664 trimer based on an HIV-1 subtype B env Gene. J. Virol. 89, 3380-3395 (2015).
66. Westrop, S. J., Jackson, A., Gazzard, B. & Imami, N. HIV-1 clade A infection and viral control: an immunological perspective on a case of underquantification. Int. J. STD AIDS 22, 690-692 (2011).
67. Jardine, J. et al. Rational HIV immunogen design to target specific germline B cell receptors. Science 340, 711-716 (2013).
68. McGuire, A. T. et al. Engineering HIV envelope protein to activate germline B cell receptors of broadly neutralizing anti-CD4 binding site antibodies. J. Exp. Med. 210, 655-663 (2013).
69. McGuire, A. T. et al. Antigen modification regulates competition of broad and narrow neutralizing HIV antibodies. Science 346, 1380-1383 (2014).
70. Jardine, J. G. et al. HIV-1 broadly neutralizing antibody precursor B cells revealed by germline-targeting immunogene. Science 351, 1458-1463 (2016).
71. Steichen, J. M. et al. HIV vaccine design to target germline precursors of glycan-dependent broadly neutralizing antibodies. Immunity 45, 483-496 (2016).
72. Pritchard, L. K. et al. Glycan microheterogeneity at the PGT135 antibody recognition site on HIV-1 gp120 reveals a molecular mechanism for neutralization resistance. J. Virol. 89, 6952-6959 (2015).
73. Rerks-Ngarm, S. et al. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med. 361, 2209-2220 (2009).
74. Struwe, W. B., Stuckmann, A., Behrens, A. J., Pagel, K. & Crispin, M. Global N-glycan site occupancy of HIV-1 gp120 by metabolic engineering and highresolution intact mass spectrometry. ACS Chem. Biol. 12, 357-361 (2016).
75. Guenaga, J. et al. Well-ordered trimeric HIV-1 subtype B and C soluble spike mimetics generated by negative selection display native-like properties. PLoS Pathog. 11, e1004570 (2015).
76. Andrabi, R. et al. Identification of common features in prototype broadly neutralizing antibodies to HIV envelope V2 apex to facilitate vaccine design. Immunity 43, 959-973 (2015).
77. Chang, H. W. et al. Generation and evaluation of clade C simian-human immunodeficiency virus challenge stocks. j. Virol. 89, 1965-1974 (2015).
78. Barbian, H. J. et al. Neutralization properties of simian immunodeficiency viruses infecting chimpanzees and gorillas. Mbio 6, e00296-15 (2015).
79. Panico, M. et al. Mapping the complete glycoproteome of virion-derived HIV-1 gp120 provides insights into broadly neutralizing antibody binding. Sci. Rep. 6, e00296-15 (2016).
80. Livi, G. P. et al. Secretion of N-glycosylated interleukin-1-beta in Saccharomyces-cerevisiae using a leader peptide from Candida-albicans-effect of N-linked glycosylation on biological-activity. J. Biol. Chem. 266, 15348-15355 (1991).
81. Elliott, S., Chang, D., Delorme, E., Eris, T. & Lorenzini, T. Structural requirements for additional N-linked carbohydrate on recombinant human erythropoietin. J. Biol. Chem. 279, 16854-16862 (2004).
82. Ujvari, A. et al. Translation rate of human tyrosinase determines its N-linked glycosylation level. J. Biol. Chem. 276, 5924-5931 (2001).
83. Cao, L. W. et al. N-glycosylation site analysis of proteins from Saccharomyces cerevisiae by using hydrophilic interaction liquid chromatography-based enrichment, parallel deglycosylation, and mass spectrometry. J. Proteome. Res. 13, 1485-1493 (2014).
84. Li, Y., Luo, L. Z., Rasool, N. & Kang, C. Y. Glycosylation is necessary for the correct folding of human immunodeficiency virus-Gp120 in Cd4 binding. J. Virol. 67, 584-588 (1993).
85. Quinones-Kochs, M. I., Buonocore, L. & Rose, J. K. Role of N-linked glycans in a human immunodeficiency virus envelope glycoprotein: effects on protein function and the neutralizing antibody response. J. Virol. 76, 4199-4211 (2002).
86. Gristick, H. B. et al. Natively glycosylated HIV-1 Env structure reveals new mode for antibody recognition of the CD4-binding site. Nat. Struct. Mol. Biol. 23, 906-915 (2016).
87. Hao, P. L., Ren, Y., Alpert, A. J. & Sze, S. K. Detection, evaluation and minimization of nonenzymatic deamidation in proteomic sample preparation. Mol. Cell. Proteomics 10, O111.009381 (2011).
88. Pancera, M. et al. Structure and immune recognition of trimeric pre-fusion HIV-1 Env. Nature 514, 455 (2014).
89. Huang, P. S. et al. RosettaRemodel: a generalized framework for flexible backbone protein design. PLoS ONE 6, e24109 (2011).
90. Pancera, M. et al. Structure of HIV-1 gp120 with gp41-interactive region reveals layered envelope architecture and basis of conformational mobility. Proc. Natl Acad. Sci. USA 107, 1166-1171 (2010).