Synthesis of paucimannose N-glycans by Caenorhabditis elegans requires prior actions of UDP-N-acetyl-D-glucosamine:α-3-D-mannoside β1,2-N-acetylglucosaminyltransferase I, α3,6-mannosidase II and a specific membrane-bound β-N-acetylglucosaminidase

Biochemical Journal

Volumn 372, Issue 1, 2003, Pages 53-64

  Zhang, Wenli ^a   Cao, Pinjiang ^a   Chen, Shihao ^a,d   Spence, Andrew M ^b   Zhu, Shaoxian ^b   Staudacher, Erika ^c   Schachter, Harry ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^d BURNHAM INSTITUTE   (United States)

Author keywords

Caenorhabditis elegans; Mannosidase II; N acetylglucosaminidase; N acetylglucosaminyltransferase I; N glycan biosynthesis; Paucimannose N glycans

Indexed keywords

AMINES; ENZYMES; GENES; PH EFFECTS; REACTION KINETICS; SUBSTRATES; SYNTHESIS (CHEMICAL);

KINETIC CONSTANTS;

BIOCHEMISTRY;

ALPHA 3,6 MANNOSIDASE II; GLYCAN DERIVATIVE; GLYCOPROTEIN; MANNOSE; METAL ION; N ACETYL BETA GLUCOSAMINIDASE; N ACETYLGLUCOSAMINE; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE N ACETYLGLUCOSAMINE; URIDINE DIPHOSPHATE N ACETYLGLUCOSAMINE:ALPHA 3 DEXTRO MANNOSIDE BETA 1,2 N ACETYLGLUCOSAMINYLTRANSFERASE I;

ARTICLE; CAENORHABDITIS ELEGANS; CARBOHYDRATE SYNTHESIS; CONCENTRATION (PARAMETERS); KINETICS; MOLECULAR CLONING; NONHUMAN; PH; PRIORITY JOURNAL; SYNTHESIS;

ACETYLGLUCOSAMINIDASE; ANIMALS; CAENORHABDITIS ELEGANS; KINETICS; MANNOSIDASES; MICROSOMES; N-ACETYLGLUCOSAMINYLTRANSFERASES; POLYSACCHARIDES;

CAENORHABDITIS ELEGANS; HEXAPODA; INVERTEBRATA; NEMATODA;

EID: 0038630876     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20021931     Document Type: Article

References (60)

1. Brenner, S. (1974) The genetics of Caenorhabditis efegans. Genetics 77, 71-94
2. Riddle, D. L., Blumenthal, T., Meyer, B. J. and Priess, J. R. (1997) C. elegans II. Cold Spring Harbor Monograph Series, vol. 33, Cold Spring Harbor Laboratory Press, Plainview, NY
3. Wood, W. B. (1988) The nematode Caenorhabditis elegans. Cold Spring Harbor Laboratory Press, Plainview, NY
4. Epstein, H. F. and Shakes, D.C. (1995) Caenorhabditis elegans: modern biological analysis of an organism. Methods Cell Biol. 48
5. Altmann, F., Fabini, G., Ahorn, H. and Wilson, I. B. (2001) Genetic model organisms in the study of N-glycans. Biochimie 83, 703-12
6. Cipollo, J. F., Cestello, C. E. and Hirschberg, C. B. (2002) The fine structure of Caenorhabditis elegans N-glycans. J. Biol. Chem. 277, 49143-49157
7. Haslam, S. M., Gems, D., Morris, H. R. and Dell, A. (2002) The glycomes of Caenorhabditis elegans and other model organisms. Biochem. Soc. Symp. 69, 117-134
8. Natsuka, S., Adachi, J., Kawaguchi, M., Nakakita, S.-I., Hase, S., Ichikawa, A. and Ikura, K. (2002) Structure analysis of N-linked glycans in Caenorhabditis elegans. J. Biochem. (Tokyo) 131, 807-813
9. Rosa, J. C., Schachter, H., Reinhold, B. and Reinhold, V. N. (2001) The glycome of Caenorhabditis elegans, a pathway to function. Glycobiology 11, 884-885
10. 1-acid glycoprotein. Biochem. Biophys. Res. Commun. 72, 909-916
11. Staudacher, E., Dalik, T., Wawra, P., Altmann, F. and Marz, L. (1995) Functional purification and characterization of a GDP-fucose: β-N-acetyl-D-glucosamine (Fuc to Asn linked GlcNAc) α1,3-fucosyltransferase from mung beans. Grycoconj. J. 12, 780-786
12. Leiter, H., Mucha, J., Staudacher, E., Grimm, R., Glössl, J. and Altmann, F. (1999) Purification, cDNA cloning, and expression of GDP-L-Fuc:Asn-linked GlcNAc-α1,3-fucosyltransferase from mung beans. J. Biol. Chem. 274, 21830-21839
13. März, L., Altmann, F., Staudacher, E. and Kubelka, V. (1995) Protein glycosylation in insects. Glycoproteins 29a, 543-563
14. Chen, S., Spence, A. M. and Schachter, H. (2001) Complex N-glycans - when, why? Trends Glycosci. Glycotechnol. 13, 447-462
15. Chen, S. H., Zhou, S. H., Sarkar, M., Spence, A. M. and Schachter, H. (1999) Expression of three Caenorhabditis elegans N-acetylglucosaminyltransferase I genes during development. J. Biol. Chem. 274, 288-297
16. Schachter, H., Chen, S., Zhang, W., Spence, A. M., Zhu, S., Callahan, J. W., Mahuran, D. J., Fan, X., Bagshaw, R. D., She, Y. M. et al. (2002) Functional post-translational proteomics approach to study the role of N-glycans in the development of Caenorhabditis elegans. Biochem. Soc. Symp. 69, 1-21
17. Chen, S., Tan, J., Reinhold, V. N., Spence, A. M. and Schachter, H. (2002) UDP-N-acetyl-D-glucosamine:α-3-D-mannoside β-1,2-N-acetylglucosaminyltransferase I and UDP-N-acetyl-D-glucosamine:α-6-D-mannoside β-1,2-N-acetylglucosaminyltransferase II in Caenorhabditis elegans. Biochim. Biophys. Acta 1573, 271-279
18. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A. and Struhl, K. (1993) Current Protocols in Molecular Biology, John Wiley and Sons, New York
19. Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
20. Sanger, F., Nicklen, S. and Coulson, A. R. (1977) DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. U.S.A. 74, 5463-5467
21. Church, D. L., Guan, K. L. and Lambie, E. J. (1995) Three genes of the MAP kinase cascade, mek-2, mpk-1/sur-1 and let-60 ras, are required for meiotic cell cycle progression in Caenorhabditis elegans. Development 121, 2525-2535
22. Mello, C. and Fire, A. (1995) DNA transformation. Methods Cell Biol. 48, 451-482
23. 2-N-acetylglucosaminyltransferase I. Can. J. Biochem. Cell Biol. 52, 409-417
24. 1H NMR spectroscopy and mass spectrometry. Carbohydr. Res. 261, 173-186
25. Staudacher, E., Kubelka, V. and März, L. (1992) Distinct N-glycan fucosylation potentials of three lepidopteran cell lines. Eur. J. Biochem. 207, 987-993
26. 2. Eur. J. Biochem. 213, 1193-1204
27. Altmann, F., Kornfeld, G., Dalik, T., Staudacher, E. and Glossl, J. (1993) Processing of asparagine-linked oligosaccharides in insect cells -N-acetylglucosaminyltransferase I and II activities in cultured lepidopteran cells. Glycobiology 3, 619-625
28. Altmann, F., Schwihla, H., Staudacher, E., Glossl, J. and Marz, L. (1995) Insect cells contain an unusual, membrane-bound β-N-acetylglucosaminidase probably involved in the processing of protein N-grycans. J. Biol. Chem. 270, 17344-17349
29. Altmann, F. and Marz, L. (1995) Processing of asparagine-linked oligosaccharides in insect cells: evidence for α-mannosidase II. Glycoconj. J. 12, 150-155
30. van den Elsen, J. M., Kuntz, D. A. and Rose, D. R. (2001) Structure of Golgi α-mannosidase II: a target for inhibition of growth and metastasis of cancer cells. EMBO J. 20, 3008-3017
31. Chen, S., Spence, A. M. and Schachter, H. (2003) Isolation of null alleles of the Caenorhabditis elegans gly-12, gly-13 and gly-14 genes, all of which encode UDP-GlcNAc:α-3-D-mannoside β1,2-N-acetylglucosaminyrtransferase I activity. Biochimie, in the press
32. Palcic, M. M., Heerze, L. D., Pierce, M. and Hindsgaul, O. (1988) The use of hydrophobic synthetic glycosides as aeceptors in glycosyltransferase assays. Glycoconj. J. 5, 49-63
33. Sarkar, M. (1994) Expression of recombinant rabbit UDP-GlcNAc:α3-D-mannoside β-1,2-N-acetylglucosaminyltransferase I catalytic domain in Sf9 insect cells. Glycoconj. J. 11, 204-209
34. Dixon, M. and Webb, E. C. (1964) Enzymes, Longmans, London
35. Sarkar, M. and Schachter, H. (2001) Cloning and expression of Drosophila melanogaster UDP-GlcNAc:α-3-D-mannoside β1,2-N-acetylglucosaminyltransferase I. Biol. Chem. 382, 209-217
36. Khoo, K. H., Huang, H. H. and Lee, K. M. (2001) Characteristic structural features of schistosome cercarial N-grycans: expression of Lewis X and core xylosylation. Glycobiology 11, 149-163
37. Kolarich, D and Altmann, F. (2000) N-glycan analysis by matrix-assisted laser desorption/ionization mass spectrometry of electrophoretically separated nonmammalian proteins: application to peanut allergen Ara h 1 and olive pollen allergen Ole e 1. Anal. Biochem. 285, 64-75
38. Narasimhan, S., Wilson, J. R., Martin, E. and Schachter, H. (1979) Structural basis for four distinct erution profiles on concanavalin A-Sepharose affinity chromatography of glycopeptides. Can. J. Biochem. 57, 83-96
39. Reck, F., Springer, M., Paulsen, H., Brockhausen, I., Sarkar, M. and Schachter, H. (1994) Synthesis of tetrasaccharide analogues of the N-glycan substrate of β-(1→ 2)-N-acetylglucosaminyltransferase II using trisaccharide precursors and recombinant β-(1→ 2)-N-acetylguucosaminyltransferase I. Carbohydr. Res. 259, 93-101
40. Allen, S. D., Tsai, D. and Schachter, H. (1984) Control of glycoprotein synthesis. X. The in vitro synthesis by hen oviduct membrane preparations of hybrid asparagine-linked oligosaccharides containing 5 mannose residues. J. Biol. Chem. 259, 6984-6990
41. Schachter, H. (1991) The "yellow brick road" to branched complex N-glycans. Glycobiology 1, 453-461
42. Metzler, M., Gertz, A., Sarkar, M., Schachter, H., Schrader, J. W. and Marth, J. D. (1994) Complex asparagine-linked oligosaccharides are required for morphogenic events during post-implantation development. EMBO J. 13, 2056-2065
43. Ioffe, E. and Stanley, P. (1994) Mice lacking N-acetylglucosaminyltransferase I activity die at mid-gestation, revealing an essential role for complex or hybrid N-linked carbohydrates. Proc. Natl. Acad. Sci. U.S.A. 91, 728-732
44. Tan, J., Dunn, J., Jaeken, J. and Schachter, H. (1996) Mutations in the MGAT2 gene controlling complex N-glycan synthesis cause carbohydrate-deficient glycoprotein syndrome type II, an autosomal recessive disease with defective brain development. Am. J. Hum. Genet. 59, 810-817
45. Strasser, R., Mucha, J., Schwihla, H., Altmann, E, Glössl, J. and Steinkellner, H. (1999) Molecular cloning and characterization of cDNA coding for β1,2-N-acetylglucosaminyltransferase I (GlcNAc-TI) from Nicotiana tabacum. Glycobiology 9, 779-785
46. Hagen, F. K. and Nehrke., K. (1998) cDNA cloning and expression of a family of UDP-N-acetylgalactosamine:polypeptide N-acetylgalactosaminyltransferase sequence homologs from Caenorhabditis elegans. J. Biol. Chem. 273, 8268-8277
47. Wilson, I. B., Zeleny, R., Kolarich, D., Staudacher, E., Stroop, C. J., Kamerling, J. P. and Altmann, F. (2001) Analysis of Asn-linked glycans from vegetable foodstuffs: widespread occurrence of Lewis a, core alpha 1,3-1inked fucose and xylose substitutions. Glycobiology 11, 261-274
48. Sturm, A. (1995) N-glycosylation of plant proteins. Glycoproteins 29a, 521-541
49. Johnson, K. D. and Chrispeels, M. J. (1987) Substrate specificities of N-acetylglucosaminyl-, fucosyl-, and xylosyltransferases that modify glycoproteins in the Golgi apparatus of bean cotyledons. Plant Physiol. 84, 1301-1308
50. Vitale, A. and Chrispeels, M. J. (1984) Transient N-acetylglucosamine in the biosynthesis of phytohemagglutinin: attachment in the Golgi apparatus and removal in protein bodies. J. Cell Biol. 99, 133-140
51. Wagner, R., Geyer, H., Geyer, R. and Klenk, H. D. (1996) N-acetyl-β-glucosaminidase accounts for differences in glycosylation of influenza virus hemagglutinin expressed in insect cells from a baculovirus vector. J. Virol. 70, 4103-4109
52. Watanabe, S., Kokuho, T., Takahashi, H., Takahashi, M., Kubota, T. and Inumaru, S. (2002) Sialylation of N-glycans on the recombinant proteins expressed by a baculovirus-insect cell system under β-N-acetylglucosaminidase inhibition. J Biol. Chem. 277, 5090-5093
53. Akama, T. O., Nakagawa, H., Sugihara, K., Narisawa, S., Ohyama, C., Nishimura, S., O'Brien, D. A., Moremen, K. W., Millan, J. L. and Fukuda, M. N. (2002) Germ cell survival through carbohydrate-mediated interaction with Sertoli cells. Science 295, 124-127
54. Misago, M., Liao, Y. F., Kudo, S., Eto, S., Mattei, M. G., Moremen, K. W. and Fukuda, M. N. (1995) Molecular cloning and expression of cDNAs encoding human α-mannosidase II and a previously unrecognized α-mannosidase IIx isozyme. Proc. Natl. Acad. Sci. U.S.A. 92, 11766-11770
55. Ogawa, R., Misago, M., Fukuda, M. N., Kudo, S., Tsukada, J., Morimoto, I. and Eto, S. (1996) Structure and transcriptional regulation of human α-mannosidase IIx (α-mannosidase II isotype) gene. Eur. J. Biochem. 242, 446-453
56. Oh-Eda, M., Nakagawa, H., Akama, T. O., Lowitz, K., Misago, M., Moremen, K. W. and Fukuda, M. N. (2001) Overexpression of the Golgi-localized enzyme α-mannosidase IIx in Chinese hamster ovary cells results in the conversion of hexamannosyl-N-acetylchitobiose to tetramannosyl-N-acetylchitobiose in the N-glycan-processing pathway. Eur. J. Biochem. 268, 1280-1288
57. Chui, D., Oh-Eda, M., Liao, Y. F., Panneerselvam, K., Lal, A., Marek, K. W., Freeze, H. H., Moremen, K. W., Fukuda, M. N. and Marth, J. D. (1997) α-Mannosidase-II deficiency results in dyserythropoiesis and unveils an alternate pathway in oligosaccharide biosynthesis. Cell 90, 157-167
58. Tan, J., Chen, S., Spence, A .M. and Schachter, H. (2000) Cloning and expression of Caenorhabditis elegans UDP-GlcNAc:α-6-D-mannoside β-1,2-N-acetylglucosaminyl-transferase II (GnT II). Glycobiology 10, 1115
59. 2-protein: transfer 'en bloc' and processing. Glycoproteins 29a, 145-152
60. Schachter, H. (1995) Glycosyltransferases involved in the synthesis of N-glycan antennae. Glycoproteins 29a, 153-199