Production of heterologous glycoproteins by a glycosylation-defective alg3och1 mutant of Schizosaccharomyces pombe

Journal of Biotechnology

Volumn 150, Issue 3, 2010, Pages 348-356

  Ohashi, Takao ^a,b   Nakakita, Shin ichi ^c   Sumiyoshi, Wataru ^c   Takegawa, Kaoru ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b ASAHI GLASS CO LTD   (Japan)

^c KAGAWA UNIVERSITY   (Japan)

Author keywords

Alg3; Galactosylation; N Linked oligosaccharide; Och1; Schizosaccharomyces pombe

Indexed keywords

ALG3; GALACTOSYLATION; N-LINKED; OCH1; SCHIZOSACCHAROMYCES POMBE;

BIOCHEMISTRY; ESTERIFICATION; GENES; GLYCOPROTEINS; GLYCOSYLATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MAMMALS; YEAST;

OLIGOSACCHARIDES;

GLYCOPROTEIN; GLYCOSIDASE; GLYCOSYLTRANSFERASE; OLIGOSACCHARIDE; TRANSFERRIN;

ARTICLE; BIOSYNTHESIS; CARBOXY TERMINAL SEQUENCE; CELL STRUCTURE; ENDOPLASMIC RETICULUM; GLYCOSYLATION; METHYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; SCHIZOSACCHAROMYCES POMBE;

BLOTTING, WESTERN; CARBOHYDRATE CONFORMATION; CELL PROLIFERATION; CELL SHAPE; GLYCOPROTEINS; GLYCOSIDE HYDROLASES; GLYCOSYLATION; HUMANS; MANNOSYLTRANSFERASES; MEMBRANE PROTEINS; MUTATION; OLIGOSACCHARIDES; PEANUT AGGLUTININ; RECOMBINANT PROTEINS; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; TRANSFERRIN;

MAMMALIA; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE;

EID: 78149468557     PISSN: 01681656     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2010.09.942     Document Type: Article

References (58)

1. Aebi M., Gassenhuber J., Domdey H., te Heesen S. Cloning and characterization of the ALG3 gene of Saccharomyces cerevisiae. Glycobiology 1996, 6:439-444.
2. Alfa C., Fantes P., Hyams J., Mcleod M., Warbrick E. Experiments with Fission Yeast: A Laboratory Manual 2003, Cold Spring Harbor Laboratory Press, New York.
3. Arnold J.N., Wormald M.R., Sim R.B., Rudd P.M., Dwek R.A. The impact of glycosylation on the biological function and structure of human immunoglobulins. Annu. Rev. Immunol. 2007, 24:21-50.
4. Bates S., Hughes H.B., Munro C.A., Thomas W.P.H., MacCallum D.M., Bertram G., Atrih A., Ferguson M.A.J., Brown A.J.P., Odds F.C., Gow N.A.R. Outer chain N-glycans are required for cell wall integrity and virulence of Candida albicans. J. Biol. Chem. 2006, 281:90-98.
5. Borowicz P., Davidson R.C., Li H., Potgieter R.I., Nett J.H., Hamilton S.R., Stadheim T.A., Miele R.G., Borowicz B., Mitchell T., Rausch S., Renfer E., Wildt S. Engineering of an artificial glycosylation pathway blocked in core oligosaccharide assembly in the Pichia pastoris: production of complex humanized glycoproteins with terminal galactose. Glycobiology 2004, 14:757-766.
6. Benoit R.M., Wilhelm R.N., Scherer-Becker D., Ostermeier C. An improved method for fast, robust, and seamless integration of DNA fragments into multiple plasmids. Protein Expr. Purif. 2006, 45:66-71.
7. Burda P., Aebi M. The dolichol pathway of N-linked glycosylation. Biochim. Biophys. Acta 1999, 1426:239-257.
8. Burda P., te Heesen S., Brachat A., Wach A., Düsterhöft A., Aebi M. Stepwise assembly of the lipid-linked oligosaccharide in the endoplasmic reticulum of Saccharomyces cerevisiae: identification of the ALG9 gene encoding a putative mannosyl transferase. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:7160-7165.
9. Chiba Y., Akeboshi H. Glycan engineering and production of 'Humanized' glycoprotein in yeast cells. Biol. Pharm. Bull. 2009, 32:786-795.
10. 2-PP-dolichol in the Saccharomyces cerevisiae Δalg9 mutant reveals a regulatory role for the Alg3p α1,3-Man middle-arm addition in downstream oligosaccharide-lipid and glycoprotein glycan processing. J. Biol. Chem. 2000, 275:4267-4277.
11. Cueva R., Muñoz M.D., Andaluz E., Basco R.D. Preferential transfer of truncated oligosaccharides to the first sequon of yeast exoglucanase in Saccharomyces cerevisiae alg3 cells. Biochim. Biophys. Acta 1996, 1289:336-342.
12. 2-PP-Dol mannosyltransferase enzyme of P. pastoris. Glycobiology 2004, 14:399-407.
13. Gemmill T.R., Trimble R.B. Overview of N- and O-linked oligosaccharide structures found in various yeast species. Biochim. Biophys. Acta 1999, 1426:227-237.
14. Giga-Hama Y., Tohda H., Takegawa K., Kumagai H. Schizosaccharomyces pombe minimum genome factory. Biotechnol. Appl. Biochem. 2007, 46:147-155.
15. Hakomori S. A rapid permethylation of glycolipid, and polysaccharide catalyzed by methylsulfinyl carbanion in dimethyl sulfoxide. J. Biochem. 1964, 55:205-208.
16. Hase S. High-performance liquid chromatography of pyridylaminated saccharides. Methods Enzymol. 1994, 230:225-237.
17. Hase S., Ikenaka T., Matsushima Y. Structure analysis of oligosaccharides by tagging of the reducing end sugars with a fluorescent compound. Biochem. Biophys. Res. Commun. 1978, 85:257-263.
18. Henquet M., Lehle L., Schreuder M., Rouwendal G., Molthoff J., Helsper J., van der Krol S., Bosch D. Identification of the gene encoding the α1,3-mannosyltransferase (ALG3) in Arabidopsis and characterization of downstream N-glycan processing. Plant Cell 2008, 20:1652-1664.
19. Huffaker T.C., Robbins P.W. Yeasts mutants deficient in protein glycosylation. Proc. Natl. Acad. Sci. U.S.A. 1983, 80:7466-7470.
20. Idiris A., Tohda H., Kumagai H., Takegawa K. Engineering of protein secretion in yeast: strategies and impact on protein production. Appl. Microbiol. Biotechnol. 2010, 86:403-417.
21. Ikeda Y., Ohashi T., Tanaka N., Takegawa K. Identification and characterization of a gene required for α1,2-mannose extension in the O-linked glycan synthesis pathway in Schizosaccharomyces pombe. FEMS Yeast Res. 2009, 9:115-125.
22. Jacobs P.P., Geysens S., Vervecken W., Contreras R., Callewaert N. Engineering complex-type N-glycosylation in Pichia pastoris using GlycoSwich technology. Nat. Protoc. 2009, 4:58-70.
23. Jigami Y. Yeast glycosylation and its application. Biosci. Biotechnol. Biochem. 2008, 72:637-648.
24. Kainz E., Gallmetzer A., Hatzl C., Nett J.H., Li H., Schinko T., Pachlinger R., Berger H., Reyes-Dominguez Y., Bernreiter A., Gerngross T., Wildt S., Strauss J. N-glycan modification in Aspergillus species. Appl. Environ. Microbiol. 2008, 74:1076-1086.
25. Kajiura H., Seki T., Fujiyama K. Arabidopsis thaliana ALG3 mutant synthesizes immature oligosaccharides in the ER and accumulates unique N-glycans. Glycobiology 2010, 20:736-751.
26. Kim M.W., Kim E.J., Kim J.-Y., Park J.-S., Oh D.-B., Shimma Y., Chiba Y., Jigami Y., Rhee S.K., Kang H.A. Functional characterization of the Hansenula polymorpha HOC1, OCH1, and OCR1 genes as members of the yeast OCH1 mannosyltransferase family involved in protein glycosylation. J. Biol. Chem. 2006, 281:6261-6271.
27. Kitajima T., Chiba Y., Jigami Y. Saccharomyces cerevisiae α1,6-mannosyltransferase has a catalytic potential to transfer a second mannose molecule. FEBS J. 2006, 273:5074-5085.
28. 2-PP-dolichyl mannosyltransferase. EMBO J. 1999, 18:6816-6822.
29. Kuroda K., Kobayashi K., Tsumura H., Komeda T., Chiba Y., Jigami Y. Production of Man5GlcNAc2-type sugar chain by the methylotrophic yeast Ogataea minuta. FEMS Yeast Res. 2006, 6:1052-1062.
30. Kurzik-Dumke U., Kaymer M., Gundacker D., Debes A., Labitzke K. Gene within gene configuration and expression of the Drosophila melanogaster genes lethal(2) neighbour of tid [l(2)not] and lethal(2) relative of tid [l(2)rot]. Gene 1997, 200:45-58.
31. Liu B., Gong X., Chang S., Yang Y., Song M., Duan D., Wang L., Ma Q., Wu J. Disruption of the OCH1 and MNN1 genes decrease N-glycosylation on glycoprotein expressed in Kluyveromyces lactis. J. Biotechnol. 2009, 143:95-102.
32. Macher B.A., Galili U. The Galα1,3Galβ1,4GlcNAc-R (α-Gal) epitope: a carbohydrate of unique evolution and clinical relevance. Biochim. Biophys. Acta 2008, 1780:75-88.
33. Manthri S., Güther M.L.S., Izquierdo L., Acosta-Serrano A., Ferguson M.A.J. Deletion of the TbALG3 gene demonstrates site-specific N-glycosylation and N-glycan processing in Trypanosoma brucei. Glycobiology 2008, 18:367-383.
34. Morita T., Takegawa K. A simple and efficient procedure for transformation of Schizosaccharomyces pombe. Yeast 2004, 21:613-617.
35. Mukaiyama H., Giga-Hama Y., Tohda H., Takegawa K. Dextran sodium sulfate enhances secretion of recombinant human transferring in Schizosaccharomyces pombe. Appl. Microbiol. Biotechnol. 2009, 85:64-155.
36. Mukaiyama H., Tohda H., Takegawa K. Overexpression of protein disulfide isomerases enhances secretion of recombinant human transferrin in Schizosaccharomyces pombe. Appl. Microbiol. Biotechnol. 2010, 86:1135-1143.
37. Nakanishi-Shindo Y., Nakayama K., Tanaka A., Toda Y., Jigami Y. Structure of the N-linked oligosaccharides that show the complete loss of α-1,6-polymannose outer chain from och1, och1 mnn1, and och1 mnn1 alg3 mutants of Saccharomyces cerevisiae. J. Biol. Chem. 1993, 268:26338-26345.
38. Nakayama K., Nagasu T., Shinma Y., Kuromitsu J., Jigami Y. OCH1 encodes a novel membrane bound mannosyltransferase: outer chain elongation of asparagines-linked oligosaccharides. EMBO J. 1992, 11:2511-2519.
39. Nakayama K., Nakanishi-Shindo Y., Tanaka A., Haga-Toda Y., Jigami Y. Substrate specificity of α-1,6-mannosyltransferase that initiates N-linked mannose outer chain elongation in Saccharomyces cerevisiae. FEBS Lett. 1997, 412:547-550.
40. Oh D.-B., Park J.-S., Kim M.W., Cheon S.A., Kim E.J., Moon H.Y., Kwon O., Rhee S.K., Kang H.A. Glycoengineering of the methylotrophic yeast Hansenula polymorpha for the production of glycoproteins with trimannosyl core N-glycan by blocking core oligosaccharide assembly. Biotechnol. J. 2008, 3:659-668.
41. Ohashi T., Ikeda Y., Tanaka N., Nakakita S., Natsuka S., Giga-Hama Y., Takegawa K. The och1 mutant of Schizosaccharomyces pombe produces galactosylated core structures of N-linked oligosaccharides. Biosci. Biotechnol. Biochem. 2009, 73:407-414.
42. Ohashi T., Takegawa K. N- and O-Linked oligosaccharides completely lack galactose residues in the gms1och1 mutant of Schizosaccharomyces pombe. Appl. Microbiol. Biotechnol. 2010, 86:263-272.
43. Okazaki K., Okazaki N., Kume K., Jinno S., Tanaka K., Okayama H. High-frequency transformation method and library transducing vectors for cloning mammalian cDNAs by trans-complementation of Schizosaccharomyces pombe. Nucleic Acids Res. 1990, 18:6485-6489.
44. 2-PP-Dol mannosyltransferase. Biol. Chem. 2001, 382:321-328.
45. Song Y., Choi M.H., Park J.-N., Kim M.W., Kim E.J., Kang H.A., Kim J.-Y. Engineering of the yeast Yarrowia lipolytica for the production of glycoproteins lacking the outer-chain mannose residues of N-glycans. Appl. Environ. Microbiol. 2007, 73:4446-4454.
46. + gene encodes an UDP-galactose transporter homologue required for protein galactosylation. Biochem. Biophys. Res. Commun. 1997, 232:121-125.
47. Takegawa K., Tanaka N., Tabuchi M., Iwahara S. Isolation and characterization of a glycosylation mutant from Schizosaccharomyces pombe. Biosci. Biotechnol. Biochem. 1996, 60:1156-1159.
48. Takegawa K., Tohda H., Sasaki M., Idris A., Ohashi T., Mukaiyama H., Giga-Hama Y., Kumagai H. Production of heterologous proteins using the fission-yeast (Schizosaccharomyces pombe) expression system. Biotechnol. Appl. Biochem. 2009, 53:227-235.
49. Tanaka N., Takegawa K. Functional characterization of Gms1p/UDP-galactose transporter in Schizosaccharomyces pombe. Yeast 2001, 18:745-757.
50. Verostek M.F., Atkinson P.H., Trimble R.B. Structure of Saccharomyces cerevisiae alg3, sec18 mutant oligosaccharides. J. Biol. Chem. 1991, 266:5547-5551.
51. Verostek M.F., Atkinson P.H., Trimble R.B. Glycoprotein biosynthesis in the alg3 Saccharomyces cerevisiae mutant. I. Role of glucose in the initial glycosylation of invertase in the endoplasmic reticulum. J. Biol. Chem. 1993, 268:12095-12103.
52. 2 processing intermediates on secreted invertase. J. Biol. Chem. 1993, 268:12104-12115.
53. Vervecken W., Kaigorodov V., Callewaert N., Geysens S., Vusser K.D., Contreras R. In vivo synthesis of mammalian-like, hybrid-type N-glycans in Pichia pastoris. Appl. Environ. Microbiol. 2004, 70:2639-2646.
54. 4-3GlcAβ1-3Galβ1-3(±Siaα2-6)Galβ1-4Xyl. J. Biol. Chem. 1999, 274:5436-5442.
55. + encodes α-1,6-mannosyltransferase that is involved in outer chain elongation of N-linked oligosaccharides. FEBS Lett. 2001, 489:75-80.
56. 9GlcNAc isomers: role of the Golgi GMA12 galactosyltransferase in core glycan galactosylation. Glycobiology 1999, 9:497-505.
57. Zhu B., Cai G., Hall E.O., Freeman G.J. In-Fusion™ assembly: seamless engineering of multidomain fusion proteins, modular vectors, and mutations. Biotechniques 2007, 43:354-359.
58. Zufferey R., Knauer R., Burda P., Stagljar I., te Heesen S., Lehle L., Aebi M. STT3, a highly conserved protein required for yeast oligosacchryl transferase in vivo. EMBO J. 1995, 14:4949-4960.