Characterization of the N-linked oligosaccharides from human chorionic gonadotropin expressed in the methylotrophic yeast Pichia pastoris

Glycoconjugate Journal

Volumn 24, Issue 1, 2007, Pages 33-47

  Blanchard, Véronique ^a   Gadkari, Rupali A ^b   Gerwig, Gerrit J ^a   Leeflang, Bas R ^a   Dighe, Rajan R ^b   Kamerling, Johannis P ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

Glycosylation; High mannose type N glycans; Human chorionic gonadotropin; Phosphorylation; Pichia pastoris

Indexed keywords

2 AMINOBENZAMIDE; AMIDASE; ASPARAGINE LINKED OLIGOSACCHARIDE; CHORIONIC GONADOTROPIN; GLYCOPEPTIDASE; PHOSPHATE;

ANION EXCHANGE CHROMATOGRAPHY; CHEMICAL STRUCTURE; CONFERENCE PAPER; CULTURE MEDIUM; FRACTIONATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; PICHIA PASTORIS; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; STRUCTURE ANALYSIS; YEAST;

ACETYLGLUCOSAMINE; CHORIONIC GONADOTROPIN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CHROMATOGRAPHY, ION EXCHANGE; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; OLIGOSACCHARIDES; PEPTIDE-N4-(N-ACETYL-BETA-GLUCOSAMINYL) ASPARAGINE AMIDASE; PICHIA; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

PICHIA PASTORIS;

EID: 33845587326     PISSN: 02820080     EISSN: 15734986     Source Type: Journal    
DOI: 10.1007/s10719-006-9010-3     Document Type: Conference Paper

References (58)

1. Talwar, G.P.: Human chorionic gonadotropin and ovarian and placental steroidogenesis. J. Steroid Biochem. 11, 27-34 (1979)
2. Endo, T., Yamashita, K., Tachibana, Y., Tojo, S., Kobata, A.: Structures of the asparagine-linked sugar chains of human chorionic gonadotropin. J. Biochem. (Tokyo) 85, 669-679 (1979)
3. Blithe, D.L.: Carbohydrate composition of the α-subunit of human chorionic gonadotropin (hCGα) and the free α molecules produced in pregnancy: most free a and some combined hCGα molecules are fucosylated. Endocrinology 126, 2788-2799 (1990)
4. 1H NMR spectroscopy. Glycobiology 1, 393-404 (1991)
5. Damm, J.B.L., Voshol, H., Hård, K., Kamerling, J.P., van Dedem, G.W.K., Vliegenthart, J.F.G.: The β-subunit of human chorionic gonadotropin contains N-glycosidic trisialo tri- and tri′-antennary carbohydrate chains. Glycoconj. J. 5, 221-233 (1988)
6. Damm, J.B.L., Kamerling, J.P., van Dedem, G.W.K., Vliegenthart, J.F.G.: A general strategy for the isolation of carbohydrate chains from N-,O-glycoproteins and its application to human chorionic gonadotrophin. Glycoconj. J. 4, 129-144 (1987)
7. Amano, J., Nishimura, R., Mochizuki, M., Kobata, A.: Comparative study of the mucin-type sugar chains of human chorionic gonadotropin present in the urine of patients with trophoblastic diseases and healthy pregnant women. J. Biol. Chem. 263, 1157-1165 (1988)
8. Liu, C.L., Bowers, L.D.: Mass spectrometry characterisation of the beta-subunit of human chorionic gonadotropin. J. Mass Spectrom. 32, 33-42 (1997)
9. Cole, L.A.: Distribution of O-linked sugar units on hCG and its free alpha-subunit. Mol. Cell. Endocrinol. 50, 45-57 (1987)
10. Bielinska, M., Boime, I.: The glycoprotein hormone family: structure and function of the carbohydrate chains. In: Montreuil, J., Vliegenthart, J.F.G., Schachter, H. (eds.) Glycoproteins, Vol. 29a, pp. 565-587. New Comprehensive Biochemistry, Elsevier Science BV, Amsterdam, The Netherlands (1995)
11. Kamerling, J.P., Hård, K., Vliegenthart, J.F.G.: Structural analysis of carbohydrate chains of native and recombinant-DNA glycoproteins. In: Crommelin, D.J.A., Schellekens, H. (eds.) Developments in Biotherapy, Vol. 1, From Clone to Clinic, pp. 295-304. Kluwer Academic Publishers, Dordrecht, The Netherlands (1990)
12. Gervais, A., Hammel, Y.-A., Pelloux, S., Lepage, P., Baer, G., Carte, N., Sorokine, O., Strub, J.-M., Koerner, R., Leize, E., Van Dorsselaer, A.: Glycosylation of human recombinant gonadotrophins: characterization and batch-to-batch consistency. Glycobiology 13, 179-189 (2003)
13. Lustbader, J.W., Birken, S., Pollak, S., Pound, A., Chait, B.T., Mirza, U.A., Ramnarain, S., Canfield, R.E., Brown, J.M.: Expression of human chorionic gonadotropin uniformly labeled with NMR isotopes in Chinese hamster ovary cells: An advance toward rapid determination of glycoprotein structures. J. Biomol. NMR 7, 295-304 (1996)
14. Chen, W., Shen, Q.X., Bahl, O.P.: Carbohydrate variant of the recombinant beta-subunit of human choriogonadotropin expressed in baculovirus expression system. J. Biol. Chem. 266, 4081-4087 (1991)
15. Chen, W., Bahl, O.P.: Recombinant carbohydrate variant of human choriogonadotropin beta-subunit (hCGbeta) descarboxyl terminus (115-145). Expression and characterization of carboxyl-terminal deletion mutant of hCG beta in the baculovirus system. J. Biol. Chem. 266, 6246-6251 (1991)
16. Chen, W., Bahl, O.P.: Recombinant carbohydrate and selenome-thionyl variants of human choriogonadotropin. J. Biol. Chem. 266, 8192-8197 (1991)
17. Jung, E., Williams, K.L.: The production of recombinant glycoproteins with special reference to simple eukaryotes including Dictyostelium discoideum. Biotechnol. Appl. Biochem. 25, 3-8 (1997)
18. Linskens, M.H.K., Grootenhuis, P.D.J., Blaauw, M., Huisman-de Winkel, B., van Ravenstein, A., van Haastert, P.J.M., Heikoop, J. C.: Random mutagenesis and screening of complex glycoproteins: expression of human gonadotropins in Dictyostelium discoideum. FASEB J. 13, 639-645 (1999)
19. Peters, B.P., Krzesicki, R.F., Hartle, R.J., Perini, F., Ruddon, R. W.: A kinetic comparison of the processing and secretion of the alpha beta dimer and the uncombined alpha and beta subunits of chorionic gonadotropin synthetized by human choriocarcinoma cells. J. Biol. Chem. 258, 15123-15130 (1984)
20. Cole, L.A., Kroll, T.D., Ruddon, R.W., Hussa, R.O.: Differential occurrence of free beta and free alpha subunits of human chorionic gonadotropin (hCG) in pregnancy sera. J. Clin. Endocrinol. Metab. 58, 1200-1202 (1984)
21. Lustbader, J., Birken, S., Pollak, S., Levinson, L., Berstine, E., Hsiung, N., Cornfield, R.: Characterization of the expression products of recombinant human choriogonadotropin and subunits. J. Biol. Chem. 262, 14204-14212 (1987)
22. Sen Gupta, C., Dighe, R.R.: Hyperexpression of biologically active human chorionic gonadotropin using the methylotropic yeast, Pichia pastoris. J. Mol. Endocrinol. 22, 273-283 (1999)
23. Gadkari, R., Deshpande, R., Dighe, R.R.: Hyperexpression and purification of biologically active human luteinizing hormone and human chorionic gonadotropin using the methylotrophic yeast, Pichia pastoris. Protein Expr. Purif. 32, 175-184 (2003)
24. Grinna, L.S., Tschopp, J.F.: Size distribution and general structural features of N-linked oligosaccharides from the methylotrophic yeast, Pichia pastoris. Yeast 5, 107-115 (1989)
25. Trimble, R.B., Atkinson, P.H., Tschopp, J.F., Townsend, R.R., Maley, F.: Structure of oligosaccharides on Saccharomyces SUC2 invertase secreted by the methylotrophic yeast Pichia pastoris. J. Biol. Chem. 266, 22807-22817 (1991)
26. Miele, R.G., Nilsen, S.L., Brito, T., Bretthauer, R.K., Castellino, F.J.: Glycosylation properties of the Pichia pastoris-expressed recombinant kringle 2 domain of tissue-type plasminogen activator. Biotechnol. Appl. Biochem. 25, 151-157 (1997)
27. Gemmill, T.R., Trimble, R.B.: Overview of N- and O-linked oligosaccharide structures found in various yeast species. Biochim. Biophys. Acta 1426, 227-237 (1999)
28. Hirose, M., Kameyama, S., Ohi, H.: Characterization of N-linked oligosaccharides attached to recombinant human antithrombin expressed in the yeast Pichia pastoris. Yeast 19, 1191-1202 (2002)
29. Boraston, A.B., Sandercock, L.E., Warren, R.A.J., Kilburn, D.G.: O-Glycosylation of a recombinant carbohydrate-binding module mutant secreted by Pichia pastoris. J. Mol. Microbiol. Biotechnol. 5, 29-36 (2003)
30. Cereghino, J.L., Cregg, J.M.: Heterologous protein expression in the methylotrophic yeast Pichia pastoris. FEMS Microbiol. Rev. 24, 45-66 (2000)
31. Letourneur, O., Gervasi, G., Gaïa, S., Pagès, J., Watelet, B., Jolivet, M.: Characterization of Toxoplasma gondii surface antigen I (SAGI) secreted from Pichia pastoris: evidence of hyper O-glycosylation. Biotechnol. Appl. Biochem. 33, 35-45 (2001)
32. González, L.J., Cremata, J.A., Guanche, Y., Ramos, Y., Triguero, A., Cabrera, G., Montesino, R., Huerta, V., Pons, T., Boué, O., Farnós, O., Rodríguez, M.: The cattle tick antigen, Bm95, expressed in Pichia pastoris contains short chains of N- and O-glycans. Arch. Biochem. Biophys. 432, 205-211 (2004)
33. Kamerling, J.P., Vliegenthart, J.F.G.: Carbohydrates. In: Lawson, A.M. (ed.) Clinical Biochemistry - Principles, Methods, Applications, Vol 1, Mass Spectrometry, pp. 175-263. Walter de Gruyter, Berlin, Germany (1989)
34. Packer, N.H., Lawson, M.A., Jardine, D.R., Redmond, J.W.: A general approach to desalting oligosaccharides released from glycoproteins. Glycoconj. J. 15, 737-747 (1988)
35. Thieme, T.R., Ballou, C.E.: Nature of the phosphodiester linkage of the phosphomannan from the yeast Kloeckera brevis. Biochemistry 10, 4121-4129 (1971)
36. Bigge, J.C., Patel, T.P., Bruce, J.A., Goulding, P.N., Charles, S. M., Parekh, R.B.: Nonselective and efficient fluorescent labeling of glycans using 2-aminobenzamide and anthranilic acid. Anal. Biochem. 230, 229-238 (1995)
37. Stroop, C.J.M., Weber, W., Gerwig, G.J., Nimtz, M., Kamerling, J.P., Vliegenthart, J.F.G.: Characterization of the carbohydrate chains of the secreted form of the human epidermal growth factor receptor. Glycobiology 10, 901-917 (2000)
38. Narui, T., Iwata, S., Takahashi, K., Shibata, S.: Partial hydrolysis of α-D-glucans with acid in the presence of 1,1,3,3-tetramethylurea. Carbohydr. Res. 170, 269-273 (1987)
39. Guile, G.R., Rudd, P.M., Wing, D.R., Prime, S.B., Dwek, R.A.: A rapid high-resolution high-performance liquid chromatographic method for separating glycan mixtures and analyzing oligosaccharide profiles. Anal. Biochem. 240, 210-226 (1996)
40. Papac, D.I., Briggs, J.B., Chin, E.T., Jones, A.J.S.: A highthroughput microscale method to release N-linked oligosaccharides from glycoproteins for matrix-assisted laser desorption/ionization time-of-flight mass spectrometric analysis. Glycobiology 8, 445-454 (1998)
41. 1H-nuclear magnetic resonance spectroscopy as a tool in the structural analysis of carbohydrates related to glycoproteins. Adv. Carbohydr. Chem. Biochem. 41, 209-374 (1983)
42. Hård, K., van Zadelhoff, G., Moonen, P., Kamerling, J.P., Vliegenthart, J.F.G.: The Asn-linked carbohydrate chains of human Tamm-Horsfall glycoprotein of one male. Novel sulfated and novel N-acetylgalactosamine- containing N-linked carbohydrate chains. Eur. J. Biochem. 209, 895-915 (1992)
43. Hernández, L.M., Ballou, L., Alvarado, E., Gillece-Castro, B.L., Burlingame, A.L., Ballou, C.E.: A new Saccharomyces cerevisiae mnn mutant N-linked oligosaccharide structure. J. Biol. Chem. 264, 11849-11856 (1989)
44. Koles, K., van Berkel, P.H.C., Pieper, F.R., Nuijens, J.H., Mannesse, M.L.M., Vliegenthart, J.F.G., Kamerling, J.P.: N- and O-glycans of recombinant human C1 inhibitor expressed in the milk of transgenic rabbits. Glycobiology 14, 51-64 (2004)
45. Michalski, J.-C., Haeuw, J.-F., Wieruszeski, J.-M., Montreuil, J., Strecker, G.: In vitro hydrolysis of oligomannosyl oligosaccharides by the lysosomal α-D-mannosidases. Eur. J. Biochem. 189, 369-379 (1990)
46. Tseneklidou-Stoeter, D., Gerwig, G.J., Kamerling, J.P., Spindler, K.-D.: Characterization of N-linked carbohydrate chains of the crayfish, Astacus leptodactylus hemocyanin. Biol. Chem. Hoppe-Seyler 376, 531-537 (1995)
47. 2 as an essential intermediate in oligosaccharide processing. J. Biol. Chem. 257, 14657-14666 (1982)
48. De Waard, P., Kamerling, J.P., van Halbeek, H., Vliegenthart, J.F. G., Broertjes, J.S.S.: Characterization of N-linked gluco-oligomannose type of carbohydrate chains of glycoproteins from the ovary of the starfish Asterias rubens (L.). Eur. J. Biochem. 168, 679-685 (1987)
49. 1H NMR spectroscopy. J. Biol. Chem. 261, 9815-9824 (1986)
50. Cohen, R.E., Ballou, C.E.: Linkage and sequence analysis of mannose-rich glycoprotein core oligosaccharides by proton nuclear magnetic resonance spectroscopy. Biochemistry 19, 4345-4358 (1980)
51. Hardy, M.R., Townsend, R.R.: Separation of fucosylated oligosaccharides using high-pH anion-exchange chromatography with pulsed-amperometric detection. Carbohydr. Res. 188, 1-7 (1989)
52. Hernández, L.M., Ballou, L., Ballou, C.E.: Separation of yeast asparagine-linked oligosaccharides by high-performance anion-exchange chromatography. Carbohydr. Res. 203, 1-11 (1990)
53. Hernández, L.M., Ballou, L., Alvarado, E., Tsai, P., Ballou, C.E.: Structure of the phosphorylated N-linked oligosaccharides from the mnn9 and mnn10 mutants of Saccharomyces cerevisiae. J. Biol. Chem. 264, 13648-13659 (1989)
54. Hernández, L.M., Olivero, I., Alvarado, E., Larriba, G.: Oligosaccharide structures of the major exoglucanase secreted by Saccharomyces cerevisiae. Biochemistry 31, 9823-9831 (1992)
55. De Waard, P., Vliegenthart, J.F.G., Kozutsumi, Y., Kawasaki, T., Yamashina, I.: Structural studies on phosphorylated oligosaccharides derived from yeast mannan by 1H(31P) relayed spin-echo difference spectroscopy (RESED). J. Biol. Chem. 264, 12141-12144 (1989)
56. Matzuk, M.M., Hsueh, A.J.W., Lapolt, P., Tsafriri, A., Keene, J.L., Boime, I.: The biological role of the carboxy-terminal extension of human chorionic gonadotropin β-subunit. Endocrinology 126, 376-383 (1990)
57. Sairam, M.R., Jiang, L.G.: Comparison of the biological and immunological properties of glycosylation deficient human chorionic gonadotropin variants produced by site directed mutagenesis and chemical deglycosylation. Mol. Cell. Endocrinol. 85, 227-235 (1992)
58. Erbel, P.J., Haseley, S.R., Kamerling, J.P., Vliegenthart, J.F.G.: Studies on the relevance of the glycan at Asn-52 of the α-subunit of human chorionic gonadotropin in the αβ dimer. Biochem. J. 364, 485-495 (2002)