307
Views
17
CrossRef citations to date
0
Altmetric
Review

Glycosylation profiling to evaluate glycoprotein immunogens against HIV-1

, &
Pages 881-890 | Received 22 Jun 2017, Accepted 04 Sep 2017, Published online: 14 Sep 2017

References

  • Behrens A-J, Vasiljevic S, Pritchard LK, et al. Composition and antigenic effects of individual glycan sites of a trimeric HIV-1 envelope glycoprotein. Cell Rep. 2016;14(11):2695–2706.
  • Burton DR, Ahmed R, Barouch DH, et al. A blueprint for HIV vaccine discovery. Cell Host Microbe. 2012;12(4):396–407.
  • Haynes BF, Mascola JR. The quest for an antibody-based HIV vaccine. Immunol Rev. 2017;275(1):5–10.
  • Sanders RW, Moore JP. Native-like Env trimers as a platform for HIV-1 vaccine design. Immunol Rev. 2017;275(1):161–182.
  • Lasky LA, Groopman JE, Fennie CW, et al. Neutralization of the AIDS retrovirus by antibodies to a recombinant envelope glycoprotein. Science. 1986;233(4760):209–212.
  • Fischer PB, Collin M, Karlsson GB, et al. The alpha-glucosidase inhibitor N-butyldeoxynojirimycin inhibits human immunodeficiency virus entry at the level of post-CD4 binding. J Virol. 1995;69(9):5791–5797.
  • Cassol E, Cassetta L, Rizzi C, et al. Dendritic cell-specific intercellular adhesion molecule-3 grabbing nonintegrin mediates HIV-1 infection of and transmission by M2a-polarized macrophages in vitro. Aids. 2013;27(5):707–716.
  • Wang W, Nie J, Prochnow C, et al. A systematic study of the N-glycosylation sites of HIV-1 envelope protein on infectivity and antibody-mediated neutralization. Retrovirology. 2013;10:14.
  • McCoy LE, Burton DR. Identification and specificity of broadly neutralizing antibodies against HIV. Immunological Reviews. 2017;275(1):11–20.
  • Scanlan CN, Offer J, Zitzmann N, et al. Exploiting the defensive sugars of HIV-1 for drug and vaccine design. Nature. 2007;446(7139):1038–1045.
  • Crispin M, Doores KJ. Targeting host-derived glycans on enveloped viruses for antibody-based vaccine design. Curr Opin Virol. 2015;11:63–69.
  • Bonomelli C, Doores KJ, Dunlop DC, et al. The glycan shield of HIV is predominantly oligomannose independently of production system or viral clade. PloS One. 2011;6(8):e23521.
  • Pritchard LK, Vasiljevic S, Ozorowski G, et al. Structural constraints determine the glycosylation of HIV-1 envelope trimers. Cell Rep. 2015;11(10):1604–1613.
  • Go EP, Liao H-X, Alam SM, et al. Characterization of host-cell line specific glycosylation profiles of early transmitted/founder HIV-1 gp120 envelope proteins. Journal of Proteome Research. 2013;12(3):1223–1234.
  • Leonard CK, Spellman MW, Riddle L, 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. 1990;265(18):10373–10382.
  • Doores KJ, Bonomelli C, Harvey DJ, et al. Envelope glycans of immunodeficiency virions are almost entirely oligomannose antigens. Proc Natl Acad Sciences USA. 2010;107(31):13800–13805.
  • Go EP, Herschhorn A, Gu C, et al. Comparative analysis of the glycosylation profiles of membrane-anchored HIV-1 envelope glycoprotein trimers and soluble gp140. J Virol. 2015;89(16):8245–8257.
  • Panico M, Bouche L, Binet D, et al. Mapping the complete glycoproteome of virion-derived HIV-1 gp120 provides insights into broadly neutralizing antibody binding. Sci Rep. 2016;6:32956.
  • Behrens AJ, Harvey DJ, Milne E, et al. Molecular architecture of the cleavage-dependent mannose patch on a soluble HIV-1 envelope glycoprotein trimer. J Virol. 2017;91(2):e01894–01816.
  • Behrens AJ, Seabright GE, Crispin M. Targeting glycans of HIV envelope glycoproteins for vaccine design. In: Tan Z, Wang L-X, Eds. Chemical Biology of Glycoproteins. UK: Royal society of chemistry. 2017.
  • Behrens AJ, Crispin M. Structural principles controlling HIV envelope glycosylation. Curr Opin Struct Biol. 2017;44:125–133.
  • Ward AB, Wilson IA. The HIV-1 envelope glycoprotein structure: nailing down a moving target. Immunological Reviews. 2017;275(1):21–32.
  • Go EP, Ding H, Zhang S, et al. A glycosylation benchmark profile for HIV-1 envelope glycoprotein production based on eleven Env trimers. J Virol. 2017 Apr 13;91(9):e02428–16.
  • Van Gils MJ, Van Den Kerkhof TL, Ozorowski G, et al. An HIV-1 antibody from an elite neutralizer implicates the fusion peptide as a site of vulnerability. Nat Microbiology. 2016;2:16199.
  • De Taeye SW, Ozorowski G. Torrents de la Pena A et al. Immunogenicity of stabilized HIV-1 envelope trimers with reduced exposure of non-neutralizing epitopes. Cell. 2015;163(7):1702–1715.
  • Sliepen K, Van Montfort T, Ozorowski G, et al. Engineering and characterization of a fluorescent native-like HIV-1 envelope glycoprotein trimer. Biomolecules. 2015;5(4):2919–2934.
  • Stewart-Jones GB, Soto C, Lemmin T, et al. Trimeric HIV-1-env structures define glycan shields from clades A, B, and G. Cell. 2016;165(4):813–826.
  • Medina-Ramirez M, Garces F, Escolano A, et al. Design and crystal structure of a native-like HIV-1 envelope trimer that engages multiple broadly neutralizing antibody precursors in vivo. J Exp Med, 2017;214(9):2573–2590.
  • Torrents De La Pena A, Julien JP, De Taeye SW, et al. Improving the immunogenicity of native-like HIV-1 envelope trimers by hyperstabilization. Cell Rep. 2017;20(8):1805–1817.
  • Bigge JC, Patel TP, Bruce JA, et al. Nonselective and efficient fluorescent labeling of glycans using 2-amino benzamide and anthranilic acid. Anal Biochem. 1995;230(2):229–238.
  • Anumula KR, Dhume ST. High resolution and high sensitivity methods for oligosaccharide mapping and characterization by normal phase high performance liquid chromatography following derivatization with highly fluorescent anthranilic acid. Glycobiology. 1998;8(7):685–694.
  • Kozak RP, Tortosa CB, Fernandes DL, et al. Comparison of procainamide and 2-aminobenzamide labeling for profiling and identification of glycans by liquid chromatography with fluorescence detection coupled to electrospray ionization-mass spectrometry. Anal Biochem. 2015;486:38–40.
  • Ahn J, Bones J, Yu YQ, et al. Separation of 2-aminobenzamide labeled glycans using hydrophilic interaction chromatography columns packed with 1.7 microm sorbent. J Chromatogr B Analyt Technol Biomed Life Sci. 2010;878(3–4):403–408.
  • Takegawa Y, Deguchi K, Ito H, et al. Simple separation of isomeric sialylated N-glycopeptides by a zwitterionic type of hydrophilic interaction chromatography. J Sep Sci. 2006;29(16):2533–2540.
  • Ruhaak LR, Zauner G, Huhn C, et al. Glycan labeling strategies and their use in identification and quantification. Analytical and Bioanalytical Chemistry. 2010;397(8):3457–3481.
  • Pritchard LK, Spencer DI, Royle L, et al. Glycan clustering stabilizes the mannose patch of HIV-1 and preserves vulnerability to broadly neutralizing antibodies. Nature Communications. 2015;6:7479.
  • Termini JM, Church ES, Silver ZA, et al. HIV and SIV maintain high levels of infectivity in the complete absence of mucin type O-glycosylation. J Virol. 2017.
  • Go EP, Hua D, Desaire H. Glycosylation and disulfide bond analysis of transiently and stably expressed clade C HIV-1 gp140 trimers in 293T cells identifies disulfide heterogeneity present in both proteins and differences in O-linked glycosylation. Journal of Proteome Research. 2014;13(9):4012–4027.
  • Stansell E, Panico M, Canis K, et al. Gp120 on HIV-1 virions lacks O-linked carbohydrate. PloS One. 2015;10(4):e0124784.
  • Hansen JE, Jansson B, Gram GJ, et al. Sensitivity of HIV-1 to neutralization by antibodies against O-linked carbohydrate epitopes despite deletion of O-glycosylation signals in the V3 loop. Archives of Virology. 1996;141(2):291–300.
  • Yang W, Shah P, Toghi Eshghi S, et al. Glycoform analysis of recombinant and human immunodeficiency virus envelope protein gp120 via higher energy collisional dissociation and spectral-aligning strategy. Anal Chem. 2014;86(14):6959–6967.
  • Stansell E, Canis K, Haslam SM, et al. Simian immunodeficiency virus from the sooty mangabey and rhesus macaque is modified with O-linked carbohydrate. J Virol. 2011;85(1):582–595.
  • Amin MN, McLellan JS, Huang W, et al. Synthetic glycopeptides reveal the glycan specificity of HIV-neutralizing antibodies. Nat Chem Biol. 2013;9(8):521–526.
  • Pancera M, Shahzad-Ul-Hussan S, Doria-Rose NA, et al. Structural basis for diverse N-glycan recognition by HIV-1-neutralizing V1-V2-directed antibody PG16. Nature Structural & Molecular Biology. 2013;20(7):804–813.
  • Falkowska E, Le KM, Ramos A, et al. Broadly neutralizing HIV antibodies define a glycan-dependent epitope on the prefusion conformation of gp41 on cleaved envelope trimers. Immunity. 2014;40(5):657–668.
  • Harvey DJ. Matrix-assisted laser desorption/ionization mass spectrometry of carbohydrates. Mass Spectrom Rev. 1999;18(6):349–450.
  • Harvey DJ, Scarff CA, Edgeworth M, et al. Travelling-wave ion mobility mass spectrometry and negative ion fragmentation of hybrid and complex N-glycans. J Spectrom. 2016;51(11):1064–1079.
  • Harvey DJ, Scarff CA, Edgeworth M, et al. Travelling-wave ion mobility and negative ion fragmentation of high-mannose N-glycans. J Mass Spectrom. 2016;51(3):219–235.
  • Harvey DJ, Sobott F, Crispin M, et al. Ion mobility mass spectrometry for extracting spectra of N-glycans directly from incubation mixtures following glycan release: application to glycans from engineered glycoforms of intact, folded HIV gp120. J Am Soc Mass Spectrom. 2011;22(3):568–581.
  • Pritchard LK, Harvey DJ, Bonomelli C, et al. Cell- and protein-directed glycosylation of native cleaved HIV-1 envelope. J Virol. 2015;89(17):8932–8944.
  • Harvey DJ, Crispin M, Bonomelli C, et al. Ion mobility mass spectrometry for ion recovery and clean-up of MS and MS/MS spectra obtained from low abundance viral samples. J Am Soc Mass Spectrom. 2015;26(10):1754–1767.
  • Bitto D, Harvey DJ, Halldorsson S, et al. Determination of N-linked glycosylation in viral glycoproteins by negative ion mass spectrometry and ion mobility. Methods Mol Biol. 2015;1331:93–121.
  • Fenn LS, Kliman M, Mahsut A, et al. Characterizing ion mobility-mass spectrometry conformation space for the analysis of complex biological samples. Anal Bioanal Chem. 2009;394(1):235–244.
  • Struwe WB, Benesch JL, Harvey DJ, et al. Collision cross sections of high-mannose N-glycans in commonly observed adduct states - identification of gas-phase conformers unique to [M - H]- ions. The Analyst. 2015;140(20):6799–6803.
  • Struwe WB, Baldauf C, Hofmann J, et al. Ion mobility separation of deprotonated oligosaccharide isomers - evidence for gas-phase charge migration. Chemical Communications (Cambridge, England). 2016;52(83):12353–12356.
  • Zhu X, Borchers C, Bienstock RJ, et al. Mass spectrometric characterization of the glycosylation pattern of HIV-gp120 expressed in CHO cells. Biochemistry. 2000;39(37):11194–11204.
  • Cutalo JM, Deterding LJ, Tomer KB. Characterization of glycopeptides from HIV-I(SF2) gp120 by liquid chromatography mass spectrometry. J Am Soc Mass Spectrom. 2004;15(11):1545–1555.
  • Pritchard LK, Spencer DI, Royle L, et al. Glycan microheterogeneity at the PGT135 antibody recognition site on HIV-1 gp120 reveals a molecular mechanism for neutralization resistance. J Virol. 2015;89(13):6952–6959.
  • Wang Z, Lorin C, Koutsoukos M, et al. Comprehensive characterization of reference standard lots of HIV-1 subtype c gp120 proteins for clinical trials in southern African regions. Vaccines. 2016;4:2.
  • Irungu J, Go EP, Zhang Y, et al. Comparison of HPLC/ESI-FTICR MS versus MALDI-TOF/TOF MS for glycopeptide analysis of a highly glycosylated HIV envelope glycoprotein. J Am Soc Mass Spectrom. 2008;19(8):1209–1220.
  • Go EP, Irungu J, Zhang Y, 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. 2008;7(4):1660–1674.
  • Go EP, Chang Q, Liao H-X, et al. Glycosylation site-specific analysis of clade C HIV-1 envelope proteins. J Proteome Res. 2009;8(9):4231–4242.
  • Go EP, Hewawasam G, Liao H-X, et al. Characterization of glycosylation profiles of HIV-1 transmitted/founder envelopes by mass spectrometry. J Virol. 2011;85(16):8270–8284.
  • Pabst M, Chang M, Stadlmann J, et al. Glycan profiles of the 27 N-glycosylation sites of the HIV envelope protein CN54gp140. Biol Chem. 2012;393(8):719–730.
  • Guttman M, Garcia NK, Cupo A, et al. CD4-induced activation in a soluble HIV-1 Env trimer. Structure (London, England: 1993). 2014;22(7):974–984.
  • Ongay S, Boichenko A, Govorukhina N, et al. Glycopeptide enrichment and separation for protein glycosylation analysis. J Sep Sci. 2012;35(18):2341–2372.
  • Wuhrer M, Catalina MI, Deelder AM, et al. Glycoproteomics based on tandem mass spectrometry of glycopeptides. Journal of Chromatography. B, Analytical Technologies in the Biomedical and Life Sciences. 2007;849(1–2):115–128.
  • Di Palma S, Boersema PJ, Heck AJR, et al. Zwitterionic hydrophilic interaction liquid chromatography (ZIC-HILIC and ZIC-cHILIC) provide high resolution separation and increase sensitivity in proteome analysis. Anal Chem. 2011;83(9):3440–3447.
  • Domon B, Costello CE. A systematic nomenclature for carbohydrate fragmentations in FAB-MS/MS spectra of glycoconjugates. Glycoconjugate Journal. 1988;5(4):397–409.
  • Mechref Y. Use of CID/ETD mass spectrometry to analyze glycopeptides. Current Protocols in Protein Science. 2012;12:Unit 12.11.11-11.
  • Cao L, Tolic N, Qu Y, et al. Characterization of intact N- and O-linked glycopeptides using higher energy collisional dissociation. Analytical Biochemistry. 2014;452:96–102.
  • Kong L, Lee JH, Doores KJ, et al. Supersite of immune vulnerability on the glycosylated face of HIV-1 envelope glycoprotein gp120. Nat Struct Mol Biol. 2013;20(7):796–803.
  • Wada Y. Glycan profiling: label-free analysis of glycoproteins. Methods in Molecular Biology. 2013;951:245–253.
  • Wada Y, Azadi P, Costello CE, et al. Comparison of the methods for profiling glycoprotein glycans–HUPO human disease glycomics/proteome initiative multi-institutional study. Glycobiology. 2007;17(4):411–422.
  • Walsh I, Zhao S, Campbell M, et al. Quantitative profiling of glycans and glycopeptides: an informatics’ perspective. Curr Opin Struct Biol. 2016;40:70–80.
  • Woodin CL, Maxon M, Desaire H. Software for automated interpretation of mass spectrometry data from glycans and glycopeptides. The Analyst. 2013;138(10):2793–2803.
  • Dallas DC, Martin WF, Hua S, et al. Automated glycopeptide analysis–review of current state and future directions. Brief Bioinform. 2013;14(3):361–374.
  • Struwe WB, Stuckmann A, Behrens A-J, et al. Global N-glycan site occupancy of HIV-1 gp120 by metabolic engineering and high-resolution intact mass spectrometry. ACS Chemical Biology. 2017;12(2):357–361.
  • Cao L, Diedrich JK, Kulp DW, et al. Global site-specific N-glycosylation analysis of HIV envelope glycoprotein. Nat Commun. 2017;8:14954.
  • Honarmand Ebrahimi K, West GM, Flefil R. Mass spectrometry approach and ELISA reveal the effect of codon optimization on N-linked glycosylation of HIV-1 gp120. Journal of Proteome Research. 2014;13(12):5801–5811.
  • Lee JH, Ozorowski G, Ward AB. Cryo-EM structure of a native, fully glycosylated, cleaved HIV-1 envelope trimer. Science. 2016;351(6277):1043–1048.
  • Bonsignori M, Zhou T, Sheng Z, et al. Maturation pathway from germline to broad HIV-1 neutralizer of a CD4-mimic antibody. Cell. 2016;165(2):449–463.
  • Haynes BF, Kelsoe G, Harrison SC, et al. B-cell-lineage immunogen design in vaccine development with HIV-1 as a case study. Nature Biotechnology. 2012;30(5):423–433.
  • Malherbe DC, Doria-Rose NA, Misher L, et al. Sequential immunization with a subtype B HIV-1 envelope quasispecies partially mimics the in vivo development of neutralizing antibodies. J Virol. 2011;85(11):5262–5274.
  • Ota T, Doyle-Cooper C, Cooper AB, et al. Anti-HIV B Cell lines as candidate vaccine biosensors. Journal of Immunology. 2012;189(10):4816–4824.
  • Glaskin RS, Khatri K, Wang Q, et al. Construction of a database of collision cross section values for glycopeptides, glycans, and peptides determined by IM-MS. Anal Chem. 2017;89(8):4452–4460.
  • Yang Y, Liu F, Franc V, et al. Hybrid mass spectrometry approaches in glycoprotein analysis and their usage in scoring biosimilarity. Nat Commun. 2016;7:13397.
  • Yang Y, Barendregt A, Kamerling JP, et al. Analyzing protein micro-heterogeneity in chicken ovalbumin by high-resolution native mass spectrometry exposes qualitatively and semi-quantitatively 59 proteoforms. Anal Chem. 2013;85(24):12037–12045.
  • Leney AC, Rafie K, Van Aalten DMF, et al. Direct monitoring of protein O-GlcNAcylation by high-resolution native mass spectrometry. ACS Chem Biol. 2017.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.