Development of fully functional proteins with novel glycosylation via enzymatic glycan trimming

Journal of Pharmaceutical Sciences

Volumn 98, Issue 8, 2009, Pages 2581-2591

  Toumi, Melinda L ^a   Go, Eden P ^a   Desaire, Heather ^a  

^a UNIVERSITY OF KANSAS   (United States)

Author keywords

Circular dichroism; Enzymes; Glycoprotein; Glycosylation; Mass spectrometry; Protein structure; Structure activity relationship (SAR)

Indexed keywords

ALPHA MANNOSIDASE; GLYCAN; GLYCOPROTEIN; RIBONUCLEASE;

ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME GLYCOSYLATION; ENZYME MODIFICATION; ION CYCLOTRON RESONANCE MASS SPECTROMETRY; PROTEIN SECONDARY STRUCTURE;

EID: 68249113087     PISSN: 00223549     EISSN: 15206017     Source Type: Journal    
DOI: 10.1002/jps.21645     Document Type: Article

References (51)

1. Walsh G. 2005. Biopharmaceuticals: Recent approvals and likely directions. Trends Biotechnol 23:553-558. (Pubitemid 41483772)
2. Helenius A, Aebi M. 2004. Roles of N-linked glycans in the endoplasmic reticulum. Annu Rev Biochem 73:1019-1049. (Pubitemid 39050393)
3. Grogan MJ, Pratt MR, Marcaurelle LA, Bertozzi CR. 2002. Homogeneous glycopeptides and glycoproteins for biological investigation. Annu Rev Biochem 71:593-634.
4. Tomiya N, Narang S, Lee YC, Betenbaugh MJ. 2004. Comparing N-glycan processing in mammalian cell lines to native and engineered lepidopteran insect cell lines. Glycoconj J 21:343-360. (Pubitemid 39434562)
5. Hamilton SR, Gerngross TU. 2007. Glycosylation engineering in yeast: The advent of fully humanized yeast. Curr Opin Biotechnol 18:387-392.
6. Narhi LO, Arakawa T, Aoki KH, Elmore R, Rohde MF, Boone T, Strickland TW. 1991. The effect of carbohydrate on the structure and stability of erythropoieitin. J Biol Chem 266:23022-23026. (Pubitemid 21908754)
7. Arnold U, Ulbrich-Hofmann R. 1997. Kinetic and thermodynamic thermal stabilities of ribonuclease A and ribonuclease B. Biochemistry 36:2166-2172. (Pubitemid 27104708)
8. Xu G, Narayan M, Scheraga HA. 2005. The oxidative folding rate of bovine pancreatic ribonuclease is enhanced by a covalently attached oligosaccharide. Biochemistry 44:9817-9823. (Pubitemid 40994375)
9. Takeuchi M, Takasaki S, Shimada M, Kobata A. 1990. Role of sugar chains in the in vitro biological activity of human erythropoietin produced in recombinant Chinese hamster ovary cells. J Biol Chem 265:12127-12130. (Pubitemid 20226863)
10. Seppala M, Koistinen H, Koistinen R, Chiu PCN, Yeung WSB. 2007. Glycosylation related actions of glycodelin: Gamete, cumulus cell, immune cell and clinical associations. Hum Reprod Update 13:275-287. (Pubitemid 47061634)
11. Mukhopadhyay D, SundarRaj S, Alok A, Karande AA. 2004. Glycodelin A, not glycodelin S, is apoptotically active. Relevance of sialic acid modification. J Biol Chem 279:8577-8584. (Pubitemid 38295911)
12. Jayachandran R, Radcliffe CM, Royle L, Harvey DJ, Dwek RA, Rudd PM, Karande AA. 2006. Oligosaccharides modulate the apoptotic activity of glycodelin. Glycobiology 16:1052-1063. (Pubitemid 44530698)
13. Goldwasser E, Kung CKH, Eliason J. 1974. Mechanism of erythropoietin-induced differentiation. XIII. The role of sialic acid in erythropoietin action. J Biol Chem 249:4202-4206.
14. Tsuda E, Kawanishi G, Ueda M, Masuda S, Sasaki R. 1990. The role of carbohydrate in recombinant human erythropoietin. Eur J Biochem 188:405-411. (Pubitemid 20106255)
15. Sethuraman N, Stadheim TA. 2006. Challenges in therapeutic glycoprotein production. Curr Opin Biotechnol 17:341-346.
16. Czlapinski JL, Bertozzi CR. 2006. Synthetic glycobiology: Exploits in the Golgi compartment. Curr Opin Chem Biol 10:645-651.
17. Hamilton SR, Davidson RC, Sethuraman N, Nett JH, Jiang Y, Rios S, Bobrowicz P, Stadheim TA, Li H, Choi B-K, Hopkins D, Wischnewski H, Roser J, Mitchell T, Strawbridge RR, Hoopes J, Wildt S, Gerngross TU. 2006. Humanization of yeast to produce complex terminally sialylated glycoproteins. Science 313:1441-1443. (Pubitemid 44360273)
18. Bobrowicz P, Davidson RC, Li H, Potgieter TI, Nett JH, Hamilton SR, Stadheim TA, Miele RG, Bobrowicz B, Mitchell T, Rausch S, Renfer E, 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)
19. Ferrara C, Brunker P, Suter T, Moser S, Puntener U, Umana P. 2006. Modulation of therapeutic antibody effector functions by glycosylation engineering: Influence of Golgi enzyme localization domain and co-expression of heterologous β1,4-N-acetylglucosaminyltransferase III and Golgi α-mannosidase II. Biotechnol Bioeng 93:851-861.
20. Wildt S, Gerngross TU. 2005. The humanization of N-glycosylation pathways in yeast. Nat Rev Microbiol 3:119-128.
21. Nett JH, Gerngross TU. 2003. Cloning and disruption of the PpURA5 gene and construction of a set of integration vectors for the stable genetic modification of Pichia pastoris. Yeast 20:1279-1290.
22. Witte K, Sears P, Martin R, Wong C-H. 1997. Enzymic glycoprotein synthesis: Preparation of ribonuclease glycoforms via enzymic glycopeptide condensation and glycosylation. J Am Chem Soc 119:2114-2118. (Pubitemid 27159977)
23. Xu G, Zhai H, Narayan M, McLafferty FW, Scheraga HA. 2004. Simultaneous characterization of the reductive unfolding pathways of RNase B isoforms by top-down mass spectrometry. Chem Biol 11:517-524. (Pubitemid 38503586)
24. Wang S, Wang PG, Qi Q. 2007. Influence of substrate conformation on the deglycosylation of ribonuclease B by recombinant yeast peptide: N-glycanase. Acta Biochim Biophys Sin 39:8-14. (Pubitemid 46115031)
25. Takahashi T, Irie M, Ukita T. 1969. A comparative study on enzymatic activity of bovine pancreatic ribonuclease A, ribonuclease S and ribonuclease S*. J Biochem 65:55-62.
26. Tarelli E, Byers HL, Wilson M, Roberts G, Homer KA, Beighton D. 2000. Detecting mannosidase activities using ribonuclease B and matrix-assisted laser desorption/ionization-time of flight mass spectrometry. Anal Biochem 282:165-172. (Pubitemid 30439488)
27. Rudd PM, Joao HC, Coghill E, Fiten P, Saunders MR, Opdenakker G, Dwek RA. 1994. Glycoforms modify the dynamic stability and functional activity of an enzyme. Biochemistry 33:17-22. (Pubitemid 24046491)
28. Mistry PK, Wraight EP, Cox TM. 1996. Therapeutic delivery of proteins to macrophages: Implications for treatment of Gaucher's disease. Lancet 348: 1555-1559. (Pubitemid 26411655)
29. H2-associated carbohydrate structure on the functional properties and in vivo fate of chimeric mouse-human immunoglobulin G1. J Exp Med 180:1087-1096.
30. Sreerama N, Woody RW. 1993. A self-consistant method for the analysis of protein secondary structure from circular dichroism. Anal Biochem 209: 32-44. (Pubitemid 23084702)
31. Lobley A, Whitmore L, Wallace BA. 2002. DICHROWEB: An interactive website for the analysis of protein secondary structure from circular dichroism spectra. Bioinformatics 18:211-212. (Pubitemid 34145057)
32. Lees JG, Miles AJ, Wien F, Wallace BA. 2006. A reference database for circular dichroism spectroscopy covering fold and secondary structure space. Bioinformatics 22:1955-1962. (Pubitemid 44283007)
33. Whitmore L, Wallace BA. 2004. DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res 32:W668-W673. (Pubitemid 38997420)
34. Leonard NJ, McDonald JJ, Reichmann ME. 1970. Reaction of diethyl pyrocarbonate with nucleic acid components, I. Adenine. Proc Natl Acad Sci USA 67: 93-98.
35. n. Anal Chem 79:355-363.
36. Pitchayawasin S, Isobe M. 2004. Mass spectrometric assignment of Smith degradation glycopeptides derived from ribonuclease B. Biosci Biotechnol Biochem 68:1424-1433. (Pubitemid 40059204)
37. Reid GE, Stephenson JL, McLuckey SA. 2002. Tandem mass spectrometry of ribonuclease A and B: N-linked glycosylation site analysis of whole protein ions. Anal Chem 74:577-583.
38. Rudd PM, Scragg IG, Coghill E, Dwek RA. 1992. Separation and analysis of the glycoform populations of ribonuclease B using capillary electrophoresis. Glycoconj J 9:86-91.
39. Joao HC, Dwek RA. 1993. Effects of glycosylation on protein structure and dynamics in ribonuclease B and some of its individual glycoform. Eur J Biochem 218:239-244.
40. White FH. 1982. Studies on the relationship of disulfide bonds to the formation and maintenance of secondary structure in chicken egg white lysozyme. Biochemistry 21:967-977.
41. Laity JH, Shimotakahara S, Scheraga HA. 1993. Expression of wild-type and mutant bovine pancreatic ribonuclease A in Escherichia coli. Proc Natl Acad Sci USA 90:615-619. (Pubitemid 23028914)
42. Opitz JG, Ciglic MI, Haugg M, Trautwein-Fritz K, Raillard SA, Jermann TM, Benner SA. 1998. Origin of the catalytic activity of bovine seminal ribonuclease against double-stranded RNA. Biochemistry 37:4023-4033. (Pubitemid 28166423)
43. Go EP, Irungu J, Zhang Y, Dalpathado DS, Liao H-X, Sutherland LL, Alam SM, Haynes BF, Desaire H. 2008. 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.
44. Zhang Y, Go EP, Desaire H. 2008. Maximizing coverage of glycosylation heterogeneity in MALDI-MS analysis of glycoproteins with up to 27 glycosylation sites. Anal Chem 80:3144-3158. (Pubitemid 351620698)
45. Dalpathado DS, Irungu J, Go EP, Butnev VY, Norton K, Bousfield GR, Desaire H. 2006. Comparative glycomics of the glycoprotein follicle stimulating hormone: Glycopeptide analysis of isolates from two mammalian species. Biochemistry 45:8665-8673. (Pubitemid 44078887)
46. Go EP, Rebecchi KR, Dalpathado DS, Bandu ML, Zhang Y, Desaire H. 2007. GlycoPep DB: A tool for glycopeptide analysis using a "smart search". Anal Chem 79:1708-1713.
47. Irungu J, Go EP, Dalpathado DS, Desaire H. 2007. Simplification of mass spectral analysis of acidic glycopeptides using GlycoPep ID. Anal Chem 79: 3065-3074. (Pubitemid 46640528)
48. O'Conner SE, Imperiali B. 1996. Modulation of protein structure and function by asparaginelinked glycosylation. Chem Biol 3:803-812. (Pubitemid 27005735)
49. Wormald MR, Dwek RA. 1999. Glycoproteins: Glycan presentation and protein-fold stability. Structure 7:R155-R160.
50. Williams RL, Greene SM, McPherson A. 1987. The crystal structure of ribonuclease B at 2.5 Å resolution. J Biol Chem 262:16020-16031.
51. Laiko VV, Baldwin MA, Burlingame AL. 2000. Atmospheric pressure matrix-assisted laser desorption/ ionization mass spectrometry. Anal Chem72:652-657. (Pubitemid 30111503)