Emerging technologies for making glycan-defined glycoproteins

ACS Chemical Biology

Volumn 7, Issue 1, 2012, Pages 110-122

  Wang, Lai Xi ^a   Lomino, Joseph V ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCAN; GLYCOPROTEIN;

IN VITRO STUDY; NONHUMAN; PLANT CELL; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN GLYCOSYLATION; PROTEIN SYNTHESIS; REVIEW; STRUCTURE ACTIVITY RELATION; YEAST CELL;

ANIMALS; CARBOHYDRATE CONFORMATION; CARBOHYDRATE SEQUENCE; CHO CELLS; CRICETINAE; ESCHERICHIA COLI; GENE EXPRESSION; GLYCOCONJUGATES; GLYCOPROTEINS; GLYCOSYLATION; HEK293 CELLS; HUMANS; ISOMERISM; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PLANT CELLS; POLYSACCHARIDES; PROTEIN ENGINEERING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, SECONDARY; STRUCTURE-ACTIVITY RELATIONSHIP; YEASTS;

EID: 84862908666     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb200429n     Document Type: Review

References (121)

1. Hart, G. W. and Copeland, R. J. (2010) Glycomics hits the big time Cell 143, 672-676
2. Varki, A. (1993) Biological roles of oligosaccharides: all of the theories are correct Glycobiology 3, 97-130 (Pubitemid 23132602)
3. Dwek, R. A. (1996) Glycobiology: Toward understanding the function of sugars Chem. Rev. 96, 683-720 (Pubitemid 126649163)
4. Haltiwanger, R. S. and Lowe, J. B. (2004) Role of glycosylation in development Annu. Rev. Biochem. 73, 491-537 (Pubitemid 39050378)
5. Dube, D. H. and Bertozzi, C. R. (2005) Glycans in cancer and inflammation - potential for therapeutics and diagnostics Nat. Rev. Drug Discovery 4, 477-488 (Pubitemid 40861990)
6. Nimmerjahn, F. and Ravetch, J. V. (2008) Fcgamma receptors as regulators of immune responses Nat. Rev. Immunol. 8, 34-47
7. Jefferis, R. (2009) Glycosylation as a strategy to improve antibody-based therapeutics Nat. Rev. Drug Discovery 8, 226-234
8. Helenius, A. and Aebi, M. (2001) Intracellular functions of N-linked glycans Science 291, 2364-2369 (Pubitemid 32231791)
9. Spiro, R. G. (2002) Protein glycosylation: nature, distribution, enzymatic formation, and disease implications of glycopeptide bonds Glycobiology 12, 43R-56R (Pubitemid 34760066)
10. Zachara, N. E. and Hart, G. W. (2002) The emerging significance of O-GlcNAc in cellular regulation Chem. Rev. 102, 431-438 (Pubitemid 35377621)
11. Hart, G. W., Slawson, C., Ramirez-Correa, G., and Lagerlof, O. (2011) Cross talk between O-GlcNAcylation and phosphorylation: roles in signaling, transcription, and chronic disease Annu. Rev. Biochem. 80, 825-858
12. Sethuraman, N. and Stadheim, T. A. (2006) Challenges in therapeutic glycoprotein production Curr. Opin. Biotechnol. 17, 341-346 (Pubitemid 44163459)
13. Aggarwal, S. (2010) What's fueling the biotech engine-2009 - 2010 Nat. Biotechnol. 28, 1165-1171
14. Kaneko, Y., Nimmerjahn, F., and Ravetch, J. V. (2006) Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation Science 313, 670-673 (Pubitemid 44201145)
15. Anthony, R. M., Nimmerjahn, F., Ashline, D. J., Reinhold, V. N., Paulson, J. C., and Ravetch, J. V. (2008) Recapitulation of IVIG anti-inflammatory activity with a recombinant IgG Fc Science 320, 373-376 (Pubitemid 351555659)
16. Anthony, R. M., Wermeling, F., Karlsson, M. C., and Ravetch, J. V. (2008) Identification of a receptor required for the anti-inflammatory activity of IVIG Proc. Natl. Acad. Sci. U.S.A. 105, 19571-19578
17. Chirino, A. J. and Mire-Sluis, A. (2004) Characterizing biological products and assessing comparability following manufacturing changes Nat. Biotechnol. 22, 1383-1391 (Pubitemid 39482857)
18. Schiestl, M., Stangler, T., Torella, C., Cepeljnik, T., Toll, H., and Grau, R. (2011) Acceptable changes in quality attributes of glycosylated biopharmaceuticals Nat. Biotechnol. 29, 310-312
19. Koeller, K. M. and Wong, C. H. (2000) Emerging themes in medicinal glycoscience Nat. Biotechnol. 18, 835-841 (Pubitemid 30640907)
20. Herzner, H., Reipen, T., Schultz, M., and Kunz, H. (2000) Synthesis of glycopeptides containing carbohydrate and Peptide recognition motifs Chem. Rev. 100, 4495-4538
21. Hang, H. C. and Bertozzi, C. R. (2001) Chemoselective approaches to glycoprotein assembly Acc. Chem. Res. 34, 727-736 (Pubitemid 32884838)
22. Davis, B. G. (2002) Synthesis of glycoproteins Chem. Rev. 102, 579-601 (Pubitemid 35377624)
23. Grogan, M. J., Pratt, M. R., Marcaurelle, L. A., and Bertozzi, C. R. (2002) Homogeneous glycopeptides and glycoproteins for biological investigation Annu. Rev. Biochem. 71, 593-634 (Pubitemid 34800231)
24. Wildt, S. and Gerngross, T. U. (2005) The humanization of N-glycosylation pathways in yeast Nat. Rev. Microbiol. 3, 119-128 (Pubitemid 40207593)
25. Buskas, T., Ingale, S., and Boons, G. J. (2006) Glycopeptides as versatile tools for glycobiology Glycobiology 16, 113R-136R (Pubitemid 44288233)
26. Bennett, C. S. and Wong, C. H. (2007) Chemoenzymatic approaches to glycoprotein synthesis Chem. Soc. Rev. 36, 1227-1238
27. Wang, L. X. and Huang, W. (2009) Enzymatic transglycosylation for glycoconjugate synthesis Curr. Opin. Chem. Biol. 13, 592-600
28. Bernardes, G. J., Castagner, B., and Seeberger, P. H. (2009) Combined approaches to the synthesis and study of glycoproteins ACS Chem. Biol. 4, 703-713
29. Gamblin, D. P., Scanlan, E. M., and Davis, B. G. (2009) Glycoprotein synthesis: an update Chem. Rev. 109, 131-163
30. Rich, J. R. and Withers, S. G. (2009) Emerging methods for the production of homogeneous human glycoproteins Nat. Chem. Biol. 5, 206-215
31. Yuan, Y., Chen, J., Wan, Q., Wilson, R. M., and Danishefsky, S. J. (2010) Toward fully synthetic, homogeneous glycoproteins: advances in chemical ligation Biopolymers 94, 373-384
32. Chalker, J. M., Bernardes, G. J., and Davis, B. G. (2011) A "tag-and-modify" approach to site-selective protein modification Acc. Chem. Res. 44, 730-741
33. Schmaltz, R. M., Hanson, S. R., and Wong, C. H. (2011) Enzymes in the synthesis of glycoconjugates Chem. Rev. 111, 4259-4307
34. Wang, L. X. (2011) The amazing transglycosylation activity of endo-beta-N-acetylglucosaminidases Trends Glycosci. Glycotechnol. 23, 33-52
35. Macmillan, D. and Bertozzi, C. R. (2004) Modular assembly of glycoproteins: towards the synthesis of GlyCAM-1 by using expressed protein ligation Angew. Chem., Int. Ed. 43, 1355-1359 (Pubitemid 39257913)
36. Warren, J. D., Miller, J. S., Keding, S. J., and Danishefsky, S. J. (2004) Toward fully synthetic glycoproteins by ultimately convergent routes: a solution to a long-standing problem J. Am. Chem. Soc. 126, 6576-6578 (Pubitemid 38697358)
37. Yamamoto, N., Tanabe, Y., Okamoto, R., Dawson, P. E., and Kajihara, Y. (2008) Chemical synthesis of a glycoprotein having an intact human complex-type sialyloligosaccharide under the Boc and Fmoc synthetic strategies J. Am. Chem. Soc. 130, 501-510 (Pubitemid 351455564)
38. Piontek, C., Ring, P., Harjes, O., Heinlein, C., Mezzato, S., Lombana, N., Pohner, C., Puttner, M., Varon Silva, D., Martin, A., Schmid, F. X., and Unverzagt, C. (2009) Semisynthesis of a homogeneous glycoprotein enzyme: ribonuclease C: part 1 Angew. Chem., Int. Ed. 48, 1936-1940
39. Piontek, C., Varon Silva, D., Heinlein, C., Pohner, C., Mezzato, S., Ring, P., Martin, A., Schmid, F. X., and Unverzagt, C. (2009) Semisynthesis of a homogeneous glycoprotein enzyme: ribonuclease C: part 2 Angew. Chem., Int. Ed. 48, 1941-1945
40. Nagorny, P., Fasching, B., Li, X., Chen, G., Aussedat, B., and Danishefsky, S. J. (2009) Toward fully synthetic homogeneous beta-human follicle-stimulating hormone (beta-hFSH) with a biantennary N-linked dodecasaccharide. synthesis of beta-hFSH with chitobiose units at the natural linkage sites J. Am. Chem. Soc. 131, 5792-5799
41. Tan, Z., Shang, S., Halkina, T., Yuan, Y., and Danishefsky, S. J. (2009) Toward homogeneous erythropoietin: non-NCL-based chemical synthesis of the Gln78-Arg166 glycopeptide domain J. Am. Chem. Soc. 131, 5424-5431
42. Wu, C. Y. and Wong, C. H. (2011) Chemistry and glycobiology Chem. Commun. (Cambridge) 47, 6201-6207
43. Hossler, P., Khatak, S. F., and Li, Z. J. (2009) Optimal and consistent protein glycosylation in mammalian cell culture Glycobiology 19, 936-949
44. Patnaik, S. K. and Stanley, P. (2006) Lectin-resistant CHO glycosylation mutants Methods Enzymol. 416, 159-182 (Pubitemid 44750110)
45. Esko, J. D. and Stanley, P. (2009) Glycosylation Mutants of Cultured Cells, in Essentials of Glycobiology (Varki, A., Cummings, R., Esko, J., Freeze, H., Stanley, P., Bertozzi, C., Hart, G., and Etzler, M., Eds.) 2010/03/20 ed., pp 649-660, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
46. Chen, W. and Stanley, P. (2003) Five Lec1 CHO cell mutants have distinct Mgat1 gene mutations that encode truncated N-acetylglucosaminyltransferase I Glycobiology 13, 43-50 (Pubitemid 36372514)
47. Stefanich, E. G., Ren, S., Danilenko, D. M., Lim, A., Song, A., Iyer, S., and Fielder, P. J. (2008) Evidence for an asialoglycoprotein receptor on nonparenchymal cells for O-linked glycoproteins J. Pharmacol. Exp. Ther. 327, 308-315
48. Shields, R. L., Lai, J., Keck, R., O'Connell, L. Y., Hong, K., Meng, Y. G., Weikert, S. H., and Presta, L. G. (2002) Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fcgamma RIII and antibody-dependent cellular toxicity J. Biol. Chem. 277, 26733-26740 (Pubitemid 34951677)
49. North, S. J., Huang, H. H., Sundaram, S., Jang-Lee, J., Etienne, A. T., Trollope, A., Chalabi, S., Dell, A., Stanley, P., and Haslam, S. M. (2010) Glycomics profiling of Chinese hamster ovary cell glycosylation mutants reveals N-glycans of a novel size and complexity J. Biol. Chem. 285, 5759-5775
50. Reeves, P. J., Callewaert, N., Contreras, R., and Khorana, H. G. (2002) Structure and function in rhodopsin: high-level expression of rhodopsin with restricted and homogeneous N-glycosylation by a tetracycline-inducible N-acetylglucosaminyltransferase I-negative HEK293S stable mammalian cell line Proc. Natl. Acad. Sci. U.S.A. 99, 13419-13424 (Pubitemid 35215396)
51. Crispin, M., Chang, V. T., Harvey, D. J., Dwek, R. A., Evans, E. J., Stuart, D. I., Jones, E. Y., Lord, J. M., Spooner, R. A., and Davis, S. J. (2009) A human embryonic kidney 293T cell line mutated at the Golgi alpha-mannosidase II locus J. Biol. Chem. 284, 21684-21695
52. Chang, V. T., Crispin, M., Aricescu, A. R., Harvey, D. J., Nettleship, J. E., Fennelly, J. A., Yu, C., Boles, K. S., Evans, E. J., Stuart, D. I., Dwek, R. A., Jones, E. Y., Owens, R. J., and Davis, S. J. (2007) Glycoprotein structural genomics: solving the glycosylation problem Structure 15, 267-273 (Pubitemid 46366717)
53. Zhou, Q., Shankara, S., Roy, A., Qiu, H., Estes, S., McVie-Wylie, A., Culm-Merdek, K., Park, A., Pan, C., and Edmunds, T. (2008) Development of a simple and rapid method for producing non-fucosylated oligomannose containing antibodies with increased effector function Biotechnol. Bioeng. 99, 652-665 (Pubitemid 351158263)
54. Scanlan, C. N., Ritchie, G. E., Baruah, K., Crispin, M., Harvey, D. J., Singer, B. B., Lucka, L., Wormald, M. R., Wentworth, P., Jr. , Zitzmann, N., Rudd, P. M., Burton, D. R., and Dwek, R. A. (2007) Inhibition of mammalian glycan biosynthesis produces non-self antigens for a broadly neutralising, HIV-1 specific antibody J. Mol. Biol. 372, 16-22 (Pubitemid 47225174)
55. Doores, K. J. and Burton, D. R. (2010) Variable loop glycan dependency of the broad and potent HIV-1-neutralizing antibodies PG9 and PG16 J. Virol. 84, 10510-10521
56. Yang, Q., Li, C., Wei, Y., Huang, W., and Wang, L. X. (2010) Expression, glycoform characterization, and antibody-binding of HIV-1 V3 glycopeptide domain fused with human IgG1-Fc Bioconjugate Chem. 21, 875-883
57. Weikert, S., Papac, D., Briggs, J., Cowfer, D., Tom, S., Gawlitzek, M., Lofgren, J., Mehta, S., Chisholm, V., Modi, N., Eppler, S., Carroll, K., Chamow, S., Peers, D., Berman, P., and Krummen, L. (1999) Engineering Chinese hamster ovary cells to maximize sialic acid content of recombinant glycoproteins Nat. Biotechnol. 17, 1116-1121 (Pubitemid 29533554)
58. Fukuta, K., Abe, R., Yokomatsu, T., Kono, N., Asanagi, M., Omae, F., Minowa, M. T., Takeuchi, M., and Makino, T. (2000) Remodeling of sugar chain structures of human interferon-gamma Glycobiology 10, 421-430 (Pubitemid 30184613)
59. Goh, J. S., Zhang, P., Chan, K. F., Lee, M. M., Lim, S. F., and Song, Z. (2010) RCA-I-resistant CHO mutant cells have dysfunctional GnT I and expression of normal GnT I in these mutants enhances sialylation of recombinant erythropoietin Metab. Eng. 12, 360-368
60. Davies, J., Jiang, L., Pan, L. Z., LaBarre, M. J., Anderson, D., and Reff, M. (2001) Expression of GnTIII in a recombinant anti-CD20 CHO production cell line: Expression of antibodies with altered glycoforms leads to an increase in ADCC through higher affinity for FC gamma RIII Biotechnol. Bioeng. 74, 288-294 (Pubitemid 32678662)
61. Ferrara, C., Brunker, P., Suter, T., Moser, S., Puntener, U., and Umana, P. (2006) Modulation of therapeutic antibody effector functions by glycosylation engineering: influence of Golgi enzyme localization domain and co-expression of heterologous beta1, 4-N-acetylglucosaminyltransferase III and Golgi alpha-mannosidase II Biotechnol. Bioeng. 93, 851-861
62. Gemmill, T. R. and Trimble, R. B. (1999) Overview of N- and O-linked oligosaccharide structures found in various yeast species Biochim. Biophys. Acta 1426, 227-237 (Pubitemid 29027941)
63. Chiba, Y. and Jigami, Y. (2007) Production of humanized glycoproteins in bacteria and yeasts Curr. Opin. Chem. Biol. 11, 670-676 (Pubitemid 350180566)
64. Choi, B. K., Bobrowicz, P., Davidson, R. C., Hamilton, S. R., Kung, D. H., Li, H., Miele, R. G., Nett, J. H., Wildt, S., and Gerngross, T. U. (2003) Use of combinatorial genetic libraries to humanize N-linked glycosylation in the yeast Pichia pastoris Proc. Natl. Acad. Sci. U.S.A. 100, 5022-5027 (Pubitemid 36546252)
65. Davidson, R. C., Nett, J. H., Renfer, E., Li, H., Stadheim, T. A., Miller, B. J., Miele, G., Hamilton, S. R., Choi, B. K., Mitchell, T. I., and Wildt, S. (2004) Functional analysis of the ALG3 gene encoding the Dol-P-Man: Man(5)GlcNAc(2)-PP-Dol mannosyltransferase enzyme of P. pastoris Glycobiology 14, 399-407 (Pubitemid 38744921)
66. Vervecken, W., Kaigorodov, V., Callewaert, N., Geysens, S., De Vusser, K., and Contreras, R. (2004) In vivo synthesis of mammalian-like, hybrid-type N-glycans in Pichia pastoris Appl. Environ. Microbiol. 70, 2639-2646 (Pubitemid 38657773)
67. Hamilton, S. R., Bobrowicz, P., Bobrowicz, B., Davidson, R. C., Li, H., Mitchell, T., Nett, J. H., Rausch, S., Stadheim, T. A., Wischnewski, H., Wildt, S., and Gerngross, T. U. (2003) Production of complex human glycoproteins in yeast Science 301, 1244-1246 (Pubitemid 37052215)
68. Bobrowicz, P., Davidson, R. C., Li, H., Potgieter, T. I., Nett, J. H., Hamilton, S. R., Stadheim, T. A., Miele, R. G., Bobrowicz, B., Mitchell, T., Rausch, S., Renfer, E., and Wildt, S. (2004) Engineering of an artificial glycosylation pathway blocked in core oligosaccharide assembly in the yeast Pichia pastoris: production of complex humanized glycoproteins with terminal galactose Glycobiology 14, 757-766 (Pubitemid 39206878)
69. Hamilton, S. R., Davidson, R. C., Sethuraman, N., Nett, J. H., Jiang, Y., Rios, S., Bobrowicz, P., Stadheim, T. A., Li, H., Choi, B. K., Hopkins, D., Wischnewski, H., Roser, J., Mitchell, T., Strawbridge, R. R., Hoopes, J., Wildt, S., and Gerngross, T. U. (2006) Humanization of yeast to produce complex terminally sialylated glycoproteins Science 313, 1441-1443 (Pubitemid 44360273)
70. Li, H., Sethuraman, N., Stadheim, T. A., Zha, D., Prinz, B., Ballew, N., Bobrowicz, P., Choi, B. K., Cook, W. J., Cukan, M., Houston-Cummings, N. R., Davidson, R., Gong, B., Hamilton, S. R., Hoopes, J. P., Jiang, Y., Kim, N., Mansfield, R., Nett, J. H., Rios, S., Strawbridge, R., Wildt, S., and Gerngross, T. U. (2006) Optimization of humanized IgGs in glycoengineered Pichia pastoris Nat. Biotechnol. 24, 210-215 (Pubitemid 43221706)
71. Choi, B. K., Actor, J. K., Rios, S., d'Anjou, M., Stadheim, T. A., Warburton, S., Giaccone, E., Cukan, M., Li, H., Kull, A., Sharkey, N., Gollnick, P., Kocieba, M., Artym, J., Zimecki, M., Kruzel, M. L., and Wildt, S. (2008) Recombinant human lactoferrin expressed in glycoengineered Pichia pastoris: effect of terminal N-acetylneuraminic acid on in vitro secondary humoral immune response Glycoconjugate J. 25, 581-593
72. Jacobs, P. P., Geysens, S., Vervecken, W., Contreras, R., and Callewaert, N. (2009) Engineering complex-type N-glycosylation in Pichia pastoris using GlycoSwitch technology Nat. Protoc. 4, 58-70
73. Amano, K., Chiba, Y., Kasahara, Y., Kato, Y., Kaneko, M. K., Kuno, A., Ito, H., Kobayashi, K., Hirabayashi, J., Jigami, Y., and Narimatsu, H. (2008) Engineering of mucin-type human glycoproteins in yeast cells Proc. Natl. Acad. Sci. U.S.A. 105, 3232-3237 (Pubitemid 351723536)
74. Cox, K. M., Sterling, J. D., Regan, J. T., Gasdaska, J. R., Frantz, K. K., Peele, C. G., Black, A., Passmore, D., Moldovan-Loomis, C., Srinivasan, M., Cuison, S., Cardarelli, P. M., and Dickey, L. F. (2006) Glycan optimization of a human monoclonal antibody in the aquatic plant Lemna minor Nat. Biotechnol. 24, 1591-1597 (Pubitemid 44967485)
75. Strasser, R., Stadlmann, J., Schahs, M., Stiegler, G., Quendler, H., Mach, L., Glossl, J., Weterings, K., Pabst, M., and Steinkellner, H. (2008) Generation of glyco-engineered Nicotiana benthamiana for the production of monoclonal antibodies with a homogeneous human-like N-glycan structure Plant Biotechnol. J. 6, 392-402 (Pubitemid 351490228)
76. Castilho, A., Gattinger, P., Grass, J., Jez, J., Pabst, M., Altmann, F., Gorfer, M., Strasser, R., and Steinkellner, H. (2011) N-glycosylation engineering of plants for the biosynthesis of glycoproteins with bisected and branched complex N-glycans Glycobiology 21, 813-823
77. Castilho, A., Strasser, R., Stadlmann, J., Grass, J., Jez, J., Gattinger, P., Kunert, R., Quendler, H., Pabst, M., Leonard, R., Altmann, F., and Steinkellner, H. (2010) In planta protein sialylation through overexpression of the respective mammalian pathway J. Biol. Chem. 285, 15923-15930
78. Witte, K., Sears, P., Martin, R., and Wong, C. H. (1997) Enzymatic glycoprotein synthesis: Preparation of ribonuclease glycoforms via enzymatic glycopeptide condensation and glycosylation J. Am. Chem. Soc. 119, 2114-2118 (Pubitemid 27159977)
79. Wang, L. X. (2008) Chemoenzymatic synthesis of glycopeptides and glycoproteins through endoglycosidase-catalyzed transglycosylation Carbohydr. Res. 343, 1509-1522
80. Fujita, M., Shoda, S., Haneda, K., Inazu, T., Takegawa, K., and Yamamoto, K. (2001) A novel disaccharide substrate having 1,2-oxazoline moiety for detection of transglycosylating activity of endoglycosidases Biochim. Biophys. Acta 1528, 9-14 (Pubitemid 32763144)
81. Li, B., Zeng, Y., Hauser, S., Song, H., and Wang, L. X. (2005) Highly efficient endoglycosidase-catalyzed synthesis of glycopeptides using oligosaccharide oxazolines as donor substrates J. Am. Chem. Soc. 127, 9692-9693 (Pubitemid 40981526)
82. Li, H., Li, B., Song, H., Breydo, L., Baskakov, I. V., and Wang, L. X. (2005) Chemoenzymatic synthesis of HIV-1 V3 glycopeptides carrying two N-glycans and effects of glycosylation on the peptide domain J. Org. Chem. 70, 9990-9996 (Pubitemid 41689165)
83. Rising, T. W., Claridge, T. D., Davies, N., Gamblin, D. P., Moir, J. W., and Fairbanks, A. J. (2006) Synthesis of N-glycan oxazolines: donors for endohexosaminidase catalysed glycosylation Carbohydr. Res. 341, 1574-1596 (Pubitemid 43795415)
84. Zeng, Y., Wang, J., Li, B., Hauser, S., Li, H., and Wang, L. X. (2006) Glycopeptide synthesis through endo-glycosidase-catalyzed oligosaccharide transfer of sugar oxazolines: probing substrate structural requirement Chem.? - ?Eur. J. 12, 3355-3364
85. Rising, T. W., Heidecke, C. D., Moir, J. W., Ling, Z., and Fairbanks, A. J. (2008) Endohexosaminidase-catalysed glycosylation with oxazoline donors: fine tuning of catalytic efficiency and reversibility Chem.? - ?Eur. J. 14, 6444-6464
86. Rising, T. W., Claridge, T. D., Moir, J. W., and Fairbanks, A. J. (2006) Endohexosaminidase M: exploring and exploiting enzyme substrate specificity ChemBioChem 7, 1177-1180 (Pubitemid 44230840)
87. Li, B., Song, H., Hauser, S., and Wang, L. X. (2006) A highly efficient chemoenzymatic approach toward glycoprotein synthesis Org. Lett. 8, 3081-3084 (Pubitemid 44154435)
88. Ochiai, H., Huang, W., and Wang, L. X. (2008) Expeditious chemoenzymatic synthesis of homogeneous N-glycoproteins carrying defined oligosaccharide ligands J. Am. Chem. Soc. 130, 13790-13803
89. Umekawa, M., Huang, W., Li, B., Fujita, K., Ashida, H., Wang, L. X., and Yamamoto, K. (2008) Mutants of Mucor hiemalis endo-beta-N-acetylglucosaminidase show enhanced transglycosylation and glycosynthase-like activities J. Biol. Chem. 283, 4469-4479
90. Huang, W., Li, C., Li, B., Umekawa, M., Yamamoto, K., Zhang, X., and Wang, L. X. (2009) Glycosynthases enable a highly efficient chemoenzymatic synthesis of N-glycoproteins carrying intact natural N-glycans J. Am. Chem. Soc. 131, 2214-2223
91. Heidecke, C. D., Ling, Z., Bruce, N. C., Moir, J. W., Parsons, T. B., and Fairbanks, A. J. (2008) Enhanced glycosylation with mutants of endohexosaminidase A (endo A) ChemBioChem 9, 2045-2051
92. Ling, Z., Suits, M. D., Bingham, R. J., Bruce, N. C., Davies, G. J., Fairbanks, A. J., Moir, J. W., and Taylor, E. J. (2009) The X-ray crystal structure of an Arthrobacter protophormiae endo-beta-N-acetylglucosaminidase reveals a (beta/alpha)(8) catalytic domain, two ancillary domains and active site residues key for transglycosylation activity J. Mol. Biol. 389, 1-9
93. Yin, J., Li, L., Shaw, N., Li, Y., Song, J. K., Zhang, W., Xia, C., Zhang, R., Joachimiak, A., Zhang, H. C., Wang, L. X., Liu, Z. J., and Wang, P. (2009) Structural basis and catalytic mechanism for the dual functional endo-beta-N-acetylglucosaminidase A PLoS One 4, e4658
94. Huang, W., Yang, Q., Umekawa, M., Yamamoto, K., and Wang, L. X. (2010) Arthrobacter endo-beta-N-acetylglucosaminidase shows transglycosylation activity on complex-type N-glycan oxazolines: one-pot conversion of ribonuclease B to sialylated ribonuclease C ChemBioChem 11, 1350-1355
95. Umekawa, M., Higashiyama, T., Koga, Y., Tanaka, T., Noguchi, M., Kobayashi, A., Shoda, S., Huang, W., Wang, L. X., Ashida, H., and Yamamoto, K. (2010) Efficient transfer of sialo-oligosaccharide onto proteins by combined use of a glycosynthase-like mutant of Mucor hiemalis endoglycosidase and synthetic sialo-complex-type sugar oxazoline Biochim. Biophys. Acta 1800, 1203-1209
96. Huang, W., Zhang, X., Ju, T., Cummings, R. D., and Wang, L. X. (2010) Expeditious chemoenzymatic synthesis of CD52 glycopeptide antigens Org. Biomol. Chem. 8, 5224-5233
97. Huang, W., Wang, D., Yamada, M., and Wang, L. X. (2009) Chemoenzymatic synthesis and lectin array characterization of a class of N-glycan clusters J. Am. Chem. Soc. 131, 17963-17971
98. Amin, M. N., Huang, W., Mizanur, R. M., and Wang, L. X. (2011) Convergent synthesis of homogeneous Glc(1)Man(9)GlcNAc(2)-protein and derivatives as ligands of molecular chaperones in protein quality control J. Am. Chem. Soc. 133, 14404-14417
99. Umekawa, M., Li, C., Higashiyama, T., Huang, W., Ashida, H., Yamamoto, K., and Wang, L. X. (2010) Efficient glycosynthase mutant derived from Mucor hiemalis endo-beta-N-acetylglucosaminidase capable of transferring oligosaccharide from both sugar oxazoline and natural N-glycan J. Biol. Chem. 285, 511-521
100. Parsons, T. B., Patel, M. K., Boraston, A. B., Vocadlo, D. J., and Fairbanks, A. J. (2010) Streptococcus pneumoniae endohexosaminidase D; feasibility of using N-glycan oxazoline donors for synthetic glycosylation of a GlcNAc-asparagine acceptor Org. Biomol. Chem. 8, 1861-1869
101. Huang, W., Li, J., and Wang, L. X. (2011) Unusual transglycosylation activty of Flavobacterium meningosepticum endoglycosidases enables convergent chemoenzymatic synthesis of core fucosylated complex N-glycopeptides ChemBioChem 12, 932-941
102. Szymanski, C. M., Yao, R., Ewing, C. P., Trust, T. J., and Guerry, P. (1999) Evidence for a system of general protein glycosylation in Campylobacter jejuni Mol. Microbiol. 32, 1022-1030 (Pubitemid 29255768)
103. Young, N. M., Brisson, J. R., Kelly, J., Watson, D. C., Tessier, L., Lanthier, P. H., Jarrell, H. C., Cadotte, N., Michael, F., St, Aberg, E., and Szymanski, C. M. (2002) Structure of the N-linked glycan present on multiple glycoproteins in the Gram-negative bacterium, Campylobacter jejuni J. Biol. Chem. 277, 42530-42539 (Pubitemid 35285620)
104. Wacker, M., Linton, D., Hitchen, P. G., Nita-Lazar, M., Haslam, S. M., North, S. J., Panico, M., Morris, H. R., Dell, A., Wren, B. W., and Aebi, M. (2002) N-linked glycosylation in Campylobacter jejuni and its functional transfer into E. coli Science 298, 1790-1793 (Pubitemid 35404123)
105. Kowarik, M., Numao, S., Feldman, M. F., Schulz, B. L., Callewaert, N., Kiermaier, E., Catrein, I., and Aebi, M. (2006) N-linked glycosylation of folded proteins by the bacterial oligosaccharyltransferase Science 314, 1148-1150 (Pubitemid 44789045)
106. Schwarz, F., Huang, W., Li, C., Schulz, B. L., Lizak, C., Palumbo, A., Numao, S., Neri, D., Aebi, M., and Wang, L. X. (2010) A combined method for producing homogeneous glycoproteins with eukaryotic N-glycosylation Nat. Chem. Biol. 6, 264-266
107. Wei, Y., Li, C., Huang, W., Li, B., Strome, S., and Wang, L. X. (2008) Glycoengineering of human IgG1-Fc through combined yeast expression and in vitro chemoenzymatic glycosylation Biochemistry 47, 10294-10304
108. Zou, G., Ochiai, H., Huang, W., Yang, Q., Li, C., and Wang, L. X. (2011) Chemoenzymatic synthesis and Fcgamma receptor binding of homogeneous glycoforms of antibody Fc domain. Presence of a bisecting sugar moiety enhances the affinity of Fc to FcgammaIIIa receptor J. Am. Chem. Soc. 133, 18975-18991
109. Macmillan, D., Bill, R. M., Sage, K. A., Fern, D., and Flitsch, S. L. (2001) Selective in vitro glycosylation of recombinant proteins: semi-synthesis of novel homogeneous glycoforms of human erythropoietin Chem. Biol. 8, 133-145 (Pubitemid 32300208)
110. Hirano, K., Macmillan, D., Tezuka, K., Tsuji, T., and Kajihara, Y. (2009) Design and synthesis of a homogeneous erythropoietin analogue with two human complex-type sialyloligosaccharides: combined use of chemical and bacterial protein expression methods Angew. Chem., Int. Ed. 48, 9557-9560
111. Watt, G. M., Lund, J., Levens, M., Kolli, V. S., Jefferis, R., and Boons, G. J. (2003) Site-specific glycosylation of an aglycosylated human IgG1-Fc antibody protein generates neoglycoproteins with enhanced function Chem. Biol. 10, 807-814 (Pubitemid 37171899)
112. Rendle, P. M., Seger, A., Rodrigues, J., Oldham, N. J., Bott, R. R., Jones, J. B., Cowan, M. M., and Davis, B. G. (2004) Glycodendriproteins: a synthetic glycoprotein mimic enzyme with branched sugar-display potently inhibits bacterial aggregation J. Am. Chem. Soc. 126, 4750-4751 (Pubitemid 38490121)
113. Liu, H., Wang, L., Brock, A., Wong, C. H., and Schultz, P. G. (2003) A method for the generation of glycoprotein mimetics J. Am. Chem. Soc. 125, 1702-1703 (Pubitemid 36232557)
114. Kiick, K. L., Saxon, E., Tirrell, D. A., and Bertozzi, C. R. (2002) Incorporation of azides into recombinant proteins for chemoselective modification by the Staudinger ligation Proc. Natl. Acad. Sci. U.S.A. 99, 19-24 (Pubitemid 34060308)
115. Wang, A., Winblade Nairn, N., Johnson, R. S., Tirrell, D. A., and Grabstein, K. (2008) Processing of N-terminal unnatural amino acids in recombinant human interferon-beta in Escherichia coli ChemBioChem 9, 324-330 (Pubitemid 351196801)
116. Wiltschi, B., Wenger, W., Nehring, S., and Budisa, N. (2008) Expanding the genetic code of Saccharomyces cerevisiae with methionine analogues Yeast 25, 775-786
117. Fernández-González, M., Boutureira, O., Bernardes, G. J., Chalker, J. M., Young, M. A., Errey, J. C., and Davis, B. G. (2010) Site-selective chemoenzymatic construction of synthetic glycoproteins using endoglycosidases Chem. Sci. 1, 709-715
118. Carrico, I. S., Carlson, B. L., and Bertozzi, C. R. (2007) Introducing genetically encoded aldehydes into proteins Nat. Chem. Biol. 3, 321-322 (Pubitemid 46789266)
119. Wu, P., Shui, W., Carlson, B. L., Hu, N., Rabuka, D., Lee, J., and Bertozzi, C. R. (2009) Site-specific chemical modification of recombinant proteins produced in mammalian cells by using the genetically encoded aldehyde tag Proc. Natl. Acad. Sci. U.S.A. 106, 3000-3005
120. Hudak, J. E., Yu, H. H., and Bertozzi, C. R. (2011) Protein glycoengineering enabled by the versatile synthesis of aminooxy glycans and the genetically encoded aldehyde tag J. Am. Chem. Soc. 133, 16127-16135
121. van Kasteren, S. I., Kramer, H. B., Jensen, H. H., Campbell, S. J., Kirkpatrick, J., Oldham, N. J., Anthony, D. C., and Davis, B. G. (2007) Expanding the diversity of chemical protein modification allows post-translational mimicry Nature 446, 1105-1109 (Pubitemid 46676061)