Mass spectrometry approach and ELISA reveal the effect of codon optimization on N-linked glycosylation of HIV-1 gp120

Journal of Proteome Research

Volumn 13, Issue 12, 2014, Pages 5801-5811

  Honarmand Ebrahimi, Kourosh ^a,b   West, Graham M ^a,c   Flefil, Ricardo ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^c PFIZER INC   (United States)

Author keywords

codon optimization; envelope glycoprotein; glycosylation; gp 120; HIV 1

Indexed keywords

DOLICHOL PHOSPHATE; DOLICHOL PYROPHOSPHATE; GLYCAN; GLYCOPROTEIN; GLYCOPROTEIN GP 120; NEUTRALIZING ANTIBODY; OLIGOSACCHARIDE; OLIGOSACCHARIDE TRANSFERASE; PEPTIDE; TRANSFERASE; UNCLASSIFIED DRUG; CODON; GP120 PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1;

ARTICLE; BINDING SITE; CODON; CODON USAGE; CONTROLLED STUDY; DEGLYCOSYLATION; ENZYME ACTIVE SITE; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MASS SPECTROMETRY; PROCESS OPTIMIZATION; PROTEIN BINDING; PROTEIN GLYCOSYLATION; PROTEIN MOTIF; VIRUS STRAIN; WORKFLOW; AMINO ACID SEQUENCE; GENETICS; GLYCOSYLATION; HEK293 CELL LINE; METABOLISM; MOLECULAR GENETICS; MUTATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROCEDURES; PROTEOMICS; TANDEM MASS SPECTROMETRY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

AMINO ACID SEQUENCE; BINDING SITES; CODON; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME-LINKED IMMUNOSORBENT ASSAY; GLYCOPROTEINS; GLYCOSYLATION; HEK293 CELLS; HIV ENVELOPE PROTEIN GP120; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; OLIGOSACCHARIDES; PEPTIDES; PROTEOMICS; TANDEM MASS SPECTROMETRY;

EID: 84915748609     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr500740n     Document Type: Article

References (47)

1. Haas, J.; Park, E.-C.; Seed, B. Codon usage limitation in the expression of HIV-1 envelope glycoprotein Curr. Biol. 1996, 6, 315
2. Go, E. P.; Irungu, J.; Zhang, Y.; Dalpathado, D. S.; Liao, H.-X.; Sutherland, L. L.; Alam, S. M.; Haynes, B. F.; Desaire, H. 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, 1660
3. Go, E. P.; Liao, H.-X.; Alam, S. M.; Hua, D.; Haynes, B. F.; Desaire, H. Characterization of Host-Cell Line Specific Glycosylation Profiles of Early Transmitted/Founder HIV-1 gp120 Envelope Proteins J. Proteome Res. 2013, 12, 1223
4. Spearman, P.; Lally, M. A.; Elizaga, M.; Montefiori, D.; Tomaras, G. D.; McElrath, M. J.; Hural, J.; De Rosa, S. C.; Sato, A.; Huang, Y.; Frey, S. E.; Sato, P.; Donnelly, J.; Barnett, S.; Corey, L. J.; NIAID, t. H. V. T. N. o. A Trimeric, V2-Deleted HIV-1 Envelope Glycoprotein Vaccine Elicits Potent Neutralizing Antibodies but Limited Breadth of Neutralization in Human Volunteers J. Infect. Dis. 2011, 203, 1165
5. Zolla-Pazner, S.; deCamp, A.; Gilbert, P. B.; Williams, C.; Yates, N. L.; Williams, W. T.; Howington, R.; Fong, Y.; Morris, D. E.; Soderberg, K. A.; Irene, C.; Reichman, C.; Pinter, A.; Parks, R.; Pitisuttithum, P.; Kaewkungwal, J.; Rerks-Ngarm, S.; Nitayaphan, S.; Andrews, C.; O'Connell, R. J.; Yang, Z.-y.; Nabel, G. J.; Kim, J. H.; Michael, N. L.; Montefiori, D. C.; Liao, H.-X.; Haynes, B. F.; Tomaras, G. D. Vaccine-Induced IgG Antibodies to V1V2 Regions of Multiple HIV-1 Subtypes Correlate with Decreased Risk of HIV-1 Infection PLoS One 2014, 9, e87572
6. Liu, F.; Mboudjeka, I.; Shen, S.; Chou, T.-H. W.; Wang, S.; Ross, T. M.; Lu, S. Independent but not synergistic enhancement to the immunogenicity of DNA vaccine expressing HIV-1 gp120 glycoprotein by codon optimization and C3d fusion in a mouse model Vaccine 2004, 22, 1764
7. Gao, F.; Li, Y.; Decker, J. M.; Peyerl, F. W.; Bibollet-Ruche, F.; Rodenburg, C. M.; Chen, Y.; Shaw, D. R.; Allen, S.; Musonda, R.; Shaw, G. M.; Zajac, A. J.; Letvin, N.; Hahn, B. H. Codon usage optimization of HIV type 1 subtype C gag, pol, env, and nef genes: in vitro expression and immune responses in DNA-vaccinated mice AIDS Res. Hum. Retroviruses 2003, 19, 817
8. Wei, X.; Decker, J. M.; Wang, S.; Hui, H.; Kappes, J. C.; Wu, X.; Salazar-Gonzalez, J. F.; Salazar, M. G.; Kilby, J. M.; Saag, M. S. Antibody neutralization and escape by HIV-1 Nature 2003, 422, 307
9. Chen, M. M.; Glover, K. J.; Imperiali, B. From peptide to protein: comparative analysis of the substrate specificity of N-linked glycosylation in C. jejuni Biochemistry 2007, 46, 5579
10. Shakin-Eshleman, S. H.; Spitalnik, S. L.; Kasturi, L. The amino acid at the X position of an Asn-X-Ser sequon is an important determinant of N-linked core-glycosylation efficiency J. Biol. Chem. 1996, 271, 6363
11. Mellquist, J.; Kasturi, L.; Spitalnik, S.; Shakin-Eshleman, S. The amino acid following an asn-X-Ser/Thr sequon is an important determinant of N-linked core glycosylation efficiency Biochemistry 1998, 37, 6833
12. McLellan, J. S.; Pancera, M.; Carrico, C.; Gorman, J.; Julien, J.-P.; Khayat, R.; Louder, R.; Pejchal, R.; Sastry, M.; Dai, K. Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9 Nature 2011, 480, 336
13. Doores, K. J.; Burton, D. R. Variable loop glycan dependency of the broad and potent HIV-1-neutralizing antibodies PG9 and PG16 J. Virol. 2010, 84, 10510
14. Walker, L. M.; Huber, M.; Doores, K. J.; Falkowska, E.; Pejchal, R.; Julien, J.-P.; Wang, S.-K.; Ramos, A.; Chan-Hui, P.-Y.; Moyle, M. Broad neutralization coverage of HIV by multiple highly potent antibodies Nature 2011, 477, 466
15. Tarentino, A. L.; Gomez, C. M.; Plummer, T. H., Jr. Deglycosylation of asparagine-linked glycans by peptide: N-glycosidase F Biochemistry 1985, 24, 4665
16. Mohorko, E.; Glockshuber, R.; Aebi, M. Oligosaccharyltransferase: the central enzyme of N-linked protein glycosylation J. Inherited Metab. Dis. 2011, 34, 869
17. Aebi, M. N-linked protein glycosylation in the ER BBA, Biochim. Biophys. Acta, Mol. Cell Res. 2013, 1833, 2430
18. Robinson, A. B.; McKerrow, J. H.; Cary, P. Controlled deamidation of peptides and proteins: an experimental hazard and a possible biological timer Proc. Natl. Acad. Sci. U.S.A. 1970, 66, 753
19. 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 2000, 39, 11194
20. Balzarini, J.; Van Laethem, K.; Hatse, S.; Froeyen, M.; Van Damme, E.; Bolmstedt, A.; Peumans, W.; De Clercq, E.; Schols, D. Marked depletion of glycosylation sites in HIV-1 gp120 under selection pressure by the mannose-specific plant lectins of Hippeastrum hybrid and Galanthus nivalis Mol. Pharm. 2005, 67, 1556
21. Maley, F.; Trimble, R. B.; Tarentino, A. L.; Plummer, T. H., Jr. Characterization of glycoproteins and their associated oligosaccharides through the use of endoglycosidases Anal. Biochem. 1989, 180, 195
22. Katiyar, S.; Suzuki, T.; Balgobin, B. J.; Lennarz, W. J. Site-directed mutagenesis study of yeast peptide: N-glycanase Insight into the reaction mechanism of deglycosylation J. Biol. Chem. 2002, 277, 12953
23. Morelle, W.; Michalski, J.-C. Analysis of protein glycosylation by mass spectrometry Nat. Protoc. 2007, 2, 1585
24. Lundby, A.; Olsen, J. V. GeLCMS for in-Depth Protein Characterization and Advanced Analysis of Proteomes Methods Mol. Biol. 2011, 753, 143
25. Tyler-Cross, R.; Schirch, V. Effects of amino acid sequence, buffers, and ionic strength on the rate and mechanism of deamidation of asparagine residues in small peptides J. Biol. Chem. 1991, 266, 22549
26. Wright, H. T. Sequence and structure determinants of the nonenzymatic deamidation of asparagine and glutamine residues in proteins Protein Eng. 1991, 4, 283
27. Wright, H. T. Nonenzymatic deamidation of asparaginyl and glutaminyl residues in proteins Crit. Rev. Biochem. Mol. Biol. 1990, 26, 1
28. Amin, M. N.; McLellan, J. S.; Huang, W.; Orwenyo, J.; Burton, D. R.; Koff, W. C.; Kwong, P. D.; Wang, L.-X. Synthetic glycopeptides reveal the glycan specificity of HIV-neutralizing antibodies Nat. Chem. Biol. 2013, 9, 521
29. Julien, J.-P.; Lee, J. H.; Cupo, A.; Murin, C. D.; Derking, R.; Hoffenberg, S.; Caulfield, M. J.; King, C. R.; Marozsan, A. J.; Klasse, P. J. Asymmetric recognition of the HIV-1 trimer by broadly neutralizing antibody PG9 Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 4351
30. Walker, L. M.; Phogat, S. K.; Chan-Hui, P.-Y.; Wagner, D.; Phung, P.; Goss, J. L.; Wrin, T.; Simek, M. D.; Fling, S.; Mitcham, J. L. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target Science 2009, 326, 285
31. Davenport, T. M.; Friend, D.; Ellingson, K.; Xu, H.; Caldwell, Z.; Sellhorn, G.; Kraft, Z.; Strong, R. K.; Stamatatos, L. Binding interactions between soluble HIV envelope glycoproteins and quaternary-structure-specific monoclonal antibodies PG9 and PG16 J. Virol. 2011, 85, 7095
32. Euler, Z.; Bunnik, E. M.; Burger, J. A.; Boeser-Nunnink, B. D.; Grijsen, M. L.; Prins, J. M.; Schuitemaker, H. 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. 2011, 85, 7236
33. Ménétret, J.-F.; Neuhof, A.; Morgan, D. G.; Plath, K.; Radermacher, M.; Rapoport, T. A.; Akey, C. W. The structure of ribosome-channel complexes engaged in protein translocation Mol. Cell 2000, 6, 1219
34. Bause, E.; Legler, G. The role of the hydroxy amino acid in the triplet sequence Asn-Xaa-Thr (Ser) for the N-glycosylation step during glycoprotein biosynthesis Biochem. J. 1981, 195, 639
35. Shrimal, S.; Ng, B. G.; Losfeld, M.-E.; Gilmore, R.; Freeze, H. H. Mutations in STT3A and STT3B cause two congenital disorders of glycosylation Hum. Mol. Genet. 2013, 22, 4638
36. Shrimal, S.; Gilmore, R. Glycosylation of closely spaced acceptor sites in human glycoproteins J. Cell Sci. 2013, 126, 5513
37. Újvári, A.; Aron, R.; Eisenhaure, T.; Cheng, E.; Parag, H. A.; Smicun, Y.; Halaban, R.; Hebert, D. N. Translation Rate of Human Tyrosinase Determines ItsN-Linked Glycosylation Level J. Biol. Chem. 2001, 276, 5924
38. André, S.; Seed, B.; Eberle, J.; Schraut, W.; Bültmann, A.; Haas, J. Increased immune response elicited by DNA vaccination with a synthetic gp120 sequence with optimized codon usage J. Virol. 1998, 72, 1497
39. Kutzler, M. A.; Weiner, D. B. DNA vaccines: ready for prime time? Nat. Rev. Gen. 2008, 9, 776
40. Komar, A. A.; Lesnik, T.; Reiss, C. Synonymous codon substitutions affect ribosome traffic and protein folding during in vitro translation FEBS Lett. 1999, 462, 387
41. Orešič, M.; Shalloway, D. Specific correlations between relative synonymous codon usage and protein secondary structure J. Mol. Biol. 1998, 281, 31
42. Cortazzo, P.; Cerveñansky, C.; Marín, M.; Reiss, C.; Ehrlich, R.; Deana, A. Silent mutations affect in vivo protein folding in Escherichia coli Biochem. Biophys. Res. Commun. 2002, 293, 537
43. Kasturi, L.; Eshleman, J. R.; Wunner, W. H.; Shakin-Eshleman, S. H. The hydroxy amino acid in an Asn-X-Ser/Thr sequon can influence N-linked core glycosylation efficiency and the level of expression of a cell surface glycoprotein J. Biol. Chem. 1995, 270, 14756
44. Kong, L.; Lee, J. H.; Doores, K. J.; Murin, C. D.; Julien, J.-P.; McBride, R.; Liu, Y.; Marozsan, A.; Cupo, A.; Klasse, P.-J. Supersite of immune vulnerability on the glycosylated face of HIV-1 envelope glycoprotein gp120 Nat. Struct. Mol. Biol. 2013, 20, 796
45. Falkowska, E.; Le, K. M.; Ramos, A.; Doores, K. J.; Lee, J. H.; Blattner, C.; Ramirez, A.; Derking, R.; van Gils, M. J.; Liang, C.-H. Broadly neutralizing HIV antibodies define a glycan-dependent epitope on the prefusion conformation of gp41 on cleaved envelope trimers Immunity 2014, 40, 657
46. Tretter, V.; Altmann, F.; März, L. Peptide-N4-(N-acetyl-β-glucosaminyl) asparagine amidase F cannot release glycans with fucose attached α1→ 3 to the asparagine-linked N-acetylglucosamine residue Eur. J. Biochem. 1991, 199, 647
47. Wilson, I. B. Glycosylation of proteins in plants and invertebrates Curr. Opin. Struct. Biol. 2002, 12, 569