Involvement of the α2,8-polysialyltransferases II/STX and IV/PST in the biosynthesis of polysialic acid chains on the O-linked glycoproteins in rainbow trout ovary

Journal of Biochemistry

Volumn 140, Issue 5, 2006, Pages 687-701

  Asahina, Shinji ^a   Sato, Chihiro ^a   Matsuno, Midori ^a   Matsuda, Tsukasa ^a   Colley, Karen ^b   Kitajima, Ken ^a  

^a NAGOYA UNIVERSITY   (Japan)

^b UNIVERSITY OF ILLINOIS   (United States)

Author keywords

Cortical alveolus; O linked glycan; Ooocyte development; Polysialic acid; Polysialoglycoprotein; Polysialyltransferase; Rainbow trout

Indexed keywords

ALPHA2,8 POLYSIALYLTRANSFERASE; COMPLEMENTARY DNA; DNA FRAGMENT; MESSENGER RNA; POLYSIALIC ACID; PST ENZYME; RECOMBINANT ENZYME; STX ENZYME; TRANSFERASE; UNCLASSIFIED DRUG; CMP-N-ACETYLNEURAMINATE-POLY-ALPHA-2,8-SIALOSYL SIALYLTRANSFERASE; POLY ALPHA 2,8 SIALOSYL SIALYLTRANSFERASE; POLYSACCHARIDE; SIALIC ACID DERIVATIVE; SIALOGLYCOPROTEIN; SIALYLTRANSFERASE;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; DNA ISOLATION; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; MALE; MOLECULAR CLONING; NONHUMAN; NORTHERN BLOTTING; OOCYTE DEVELOPMENT; PROTEIN EXPRESSION; RAINBOW TROUT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; ANIMAL; CELL STRAIN COS1; CERCOPITHECUS; ENZYMOLOGY; GENETIC TRANSFECTION; METABOLISM; MOLECULAR GENETICS; OVARY; PHYSIOLOGY; TISSUE DISTRIBUTION;

MAMMALIA; ONCORHYNCHUS MYKISS; SALMONIDAE; VERTEBRATA;

AMINO ACID SEQUENCE; ANIMALS; BLOTTING, NORTHERN; CERCOPITHECUS AETHIOPS; COS CELLS; FEMALE; GENE EXPRESSION; MALE; METABOLIC NETWORKS AND PATHWAYS; MOLECULAR SEQUENCE DATA; ONCORHYNCHUS MYKISS; OOGENESIS; OVARY; POLYSACCHARIDES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SIALIC ACIDS; SIALOGLYCOPROTEINS; SIALYLTRANSFERASES; TISSUE DISTRIBUTION; TRANSFECTION;

EID: 33846093628     PISSN: 0021924X     EISSN: None     Source Type: Journal    
DOI: 10.1093/jb/mvj200     Document Type: Article

References (62)

1. Angata, T. and Varki, A. (2002) Chemical diversity in the sialic acids and related α-keto acids: an evolutionary perspective. Chem. Rev. 102, 439-469
2. Schauer, B. (2004) Sialic acids: fascination sugars in higher animals and man. Zoology 107, 49-64
3. Lasky, L.A. (1992) Selectin: Interpreters of cell-specific carbohydrate information during inflammation. Science 258, 964-969
4. Suzuki, Y. (1994) Gangliosides as influenza virus receptors. Variation of influenza viruses and their recognition of the receptor sialo-sugar chains. Prog. Lipid Res. 33, 429-457
5. Crocker P.R. (2005) Siglecs in innate immunity. Curr. Opin. Pharmacol. 5, 431-437
6. Troy, F.A. (1992) Polysialylation: from bacteria to brain. Glycobiology 2, 5-23
7. Sato, C. and Kitajima, K. (1999) Glycobiology of di- and oligosialyl glycotopes. Trends Glycosci. Glycotechnol. 11, 371-390
8. Sato, C. (2004) Chain length diversity of sialic acids and its biological significance. Trends Glycosci. Glycotechnol. 16, 331-344
9. Robbins, J.B., McCracken, G.H.J., Gotschlich, E.G., Ørskov, F., Ørskov, I., and Hanson, L.A. (1974) Escherichia coli K1 capsular polysaccharide associated with neonatal meningitis. N. Engl. J. Med. 290, 1216-1220
10. Rohr, T.E. and Troy, F.A. (1980) Structure and biosynthesis of surface polymers containing polysialic acid in Escherichia coli. J. Biol. Chem. 255, 2332-2342
11. Inoue, S. and Iwasaki, M. (1978) Isolation of a novel glycoprotein from the eggs of rainbow trout: occurrence of disialosyl groups on all carbohydrate chains. Biochem. Biophys. Res. Commun. 83, 1018-1023
12. Finne, J. (1982) Occurrence of unique polysialosyl carbohydrate units in glycoproteins of developing brain. J. Biol. Chem. 257, 11966-11970
13. + channel from Electophorus electricus: Evidence for α2,8-linked polysialic acid. Biochem. Biophys. Res. Commun. 148, 817-826
14. Zuber, C., Lackie, P.M., Catterall, W.A., and Roth, J. (1992) Polysialic acid is associated with sodium channels and the neural cell adhesion molecule N-CAM in adult rat brain. J. Biol. Chem. 267, 9965-9971
15. Yabe, U., Sato, C., Matsuda, T., and Kitajima, K. (2003) Polysialic acid in human milk. CD36 is a new member of mammalian polysialic acid-containing glycoprotein. J. Biol. Chem. 278, 13875-13880
16. Nelson, R.W., Bates, P.A., and Rutishauser, U. (1995) Protein determinants for specific polysialylation of the neural cell adhesion molecule. J. Biol. Chem. 270, 17171-17179
17. Angata, K., Suzuki, M., and Fukuda, M. (1998) Differential and cooperative polysialylation of the neural cell adhesion molecule by two polysialyltransferases, PST and STX. J. Biol. Chem. 273, 28524-28532
18. Scheidegger, E.P., Sternberg, L.R., Roth, J., and Lowe, J.B. (1995) A human STX cDNA confers polysialic acid expression in mammalian cells. J. Biol. Chem. 270, 22685-22688
19. Kojima, N., Yoshida, Y., Kurosawa, N., Lee, Y.C., and Tsuji, S. (1995) Enzymatic activity of a developmentally regulated member of the sialyltransferase family (STX): evidence for α2,8-sialyltransferase activity toward N-linked oligosaccharides. FEBS. Lett. 360, 1-4.
20. Livingston, B.D. and Paulson, J.C. (1993) Polymerase chain reaction cloning of a developmentally regulated member of the sialyltransferase gene family. J. Biol. Chem. 268, 11504-11507
21. Kudo, M., Takayama, E., Tashiro, K., Fukamachi, H., Nakata, T., Tadakuma, T., Kitajima, K., Inoue, Y., and Shiokawa, K. (1998) Cloning and expression of an α2,8-polysialyltransferase (STX) from Xenopus laevis. Glycobiology 8, 771-777
22. Nakayama, J., Fukuda, M.N., Fredette, B., Ranscht, B., and Fukuda, M. (1995) Expression cloning of a human polysialyltransferase that forms the polysialylated neural cell adhesion molecule present in embryonic brain. Proc. Natl. Acad. Sci. USA 92, 7031-7035
23. Eckhardt, M., Mühlenhoff, M., Bethe, A., Koopman, J., Frosch, M., and Gerardy-Schahn, R. (1995) Molecular characterization of eukaryotic polysialyltransferase-1. Nature 373, 715-718
24. Yoshida, Y., Kojima, N., and Tsuji, S. (1995) Molecular cloning and characterization of a third type of N-glycan α2,8-sialyltransferase from mouse lung. J. Biochem. 118, 658-664
25. Phillips, G.R., Krushel, L.A., and Crossin, K.L. (1997) Developmental expression of two rat sialyltransferases that modify the neural cell adhesion molecule, N-CAM. Brain. Res. Dev. Brain. Res. 102, 143-155
26. Eckhardt, M., Bukalo, O., Chazal, G., Wang, L., Goridis, C., Schachner, M., Gerardy-Schahn, R., Cremer, H., and Dityatev, A. (2000) Mice deficient in the polysialyltransferase ST8SiaIV/ PST-1 allow discrimination of the roles of neural cell adhesion molecule protein and polysialic acid in neural development and synaptic plasticity. J. Neurosci. 20, 5234-5244
27. Angata, K., Long, J.M., Bukalo, O., Lee, W., Dityatev, A., Wynshaw-Boris, A., Schachner, M., Fukuda, M., and Marth, J.D. (2004) Sialyltransferase ST8Sia-II assembles a subset of polysialic acid that directs hippocampal axonal targeting and promotes fear behavior. J. Biol. Chem. 279, 32603-32613
28. Kitajima, K., Inoue, Y., and Inoue, S. (1986) Polysialoglycoproteins of Salmonidae fish eggs. Complete structure of 200-kDa polysialoglycoprotein from the unfertilized eggs of rainbow trout (Salmo gairdneri). J. Biol. Chem. 261, 5262-5269
29. Inoue, S., Kitajima, K., Inoue, Y., and Kudo, S. (1987) Localization of polysialoglycoprotein as a major glycoprotein component in cortical alveoli of the unfertilized eggs of Salmo gairdneri. Dev. Biol. 123, 442-454
30. Inoue, S., and Inoue, Y. (1986) Fertilization (activation)-induced 200- to 9-kDa depolymerization of polysialoglycoprotein, a distinct component of cortical alveoli of rainbow trout eggs. J. Biol. Chem. 261, 5256-5261
31. Inoue, Y. (1993) Glycobiology offish egg polysialoglycoproteins (PSGP) and deaminated neuraminic acid-rich glycopreteins (KDN-gp) in Polysialic Acid from Microbes to Man (Roth, J., Rutishauser, U., and Troy, F.A., eds.) pp. 171-181, Birkhäuser Verlag, Basel
32. Nomoto, H., Iwasaki, M., Endo, T., Inoue, S., Inoue, Y., and Matsumura, G. (1982) Structures of carbohydrate units isolated from trout egg polysialoglycoproteins: short-cored units with oligosialosyl groups. Arch. Biochem. Biophys. 218, 335-341
33. Sorimachi, H., Emori, Y., Kawasaki, H., Kitajima, K., Inoue, S., Suzuki, K., and Inoue, Y. (1988) Molecular cloning and characterization of cDNAs coding for apopolysialoglycoprotein of rainbow trout eggs. Multiple mRNA speciestranscribed from multiple genes contain diverged numbers of exact 39-base (13-amino acid) repeats. J. Biol. Chem. 263, 17678-17684
34. Sato, C., Kitajima, K., Tazawa, I., Inoue, Y., Inoue, S., and Troy, F. A. (1993) Structural diversity in the α2→8-linked polysialic acid chains in salmonid fish egg glycoproteins. Occurrence of poly(Neu5Ac), poly(Neu5Gc), poly(Neu5Ac, Neu5Gc), poly(KDN), and their partially acetylated forms. J. Biol. Chem. 268, 23675-23684
35. Close, B.E. and Colley, K.J. (1998) In vivo autopolysialylation and localization of the polysialyltransferases PST and STX. J. Biol. Chem. 273, 34586-34593
36. Close, B.E., Tao, K., and Colley, K.J. (2000) Polysialyltransferase-1 autopolysialylation is not requisite for polysialylation of neural cell adhesion molecule. J. Biol. Chem. 275, 4484-4491
37. Hallenbeck, P.C., Vimr, E.R., Yu, F., Bassler, B., and Troy, F.A. (1987) Purification and properties of a bacteriophage-induced endo-N- acetylneuraminidase specific for poly-α2,8-sialosyl carbohydrate units. J. Biol. Chem. 262, 3553-3561
38. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K. (1997) Current Protocols in Molecular Biology, Vol. 2, pp. 15.01-15.8.8, John Wily & Sons, New York
39. Asahina, S., Sato, C., and Kitajima, K. (2004) Developmental expression of a sialyltransferase responsible for sialylation of cortical alveolus glycoprotein during oogenesis in rainbow trout (Oncorhynchus mykiss). J. Biochem. 136, 189-198
40. Sanchez-Lopez, R., Nicholson, R., Gesnel, M.C., Matrisian, L.M., and Breathnach, R. (1988) Protein Structure-function relationships in the collagenase family member transin. J. Biol. Chem. 263, 11892-11899
41. Sato, C., Matsuda, T., and Kitajima, K. (2002) Neuronal differentiation-dependent expression of the disialic acid epitope on CD166 and its involvement in neurite formation in Neuro2A cells. J. Biol. Chem. 277, 45299-45305
42. Tsuji, S. (1996) Molecular cloning and functional analysis of sialyltransferases. J. Biochem. 120, 1-13
43. Kitazume, S., Kitajima, K., Inoue, S., Inoue, Y., and Troy, F.A. (1994) Developmental expression of trout egg polysialoglycoproteins and the prerequisite α2,6-, and α2,8-sialyl and α2,8- polysialyltransferase activities required for their synthesis during oogenesis. J. Biol. Chem. 269, 10330-10340
44. Mühlenhoff, M., Eckhardt, M., Bethe, A., Frosch, M., and Gerardy-Schahn, R. (1996) Autocatalytic polysialylation of polysialyltransferase-1. EMBO J. 15, 6943-6950
45. Muhlenhoff, M., Manegold, A., Windfuhr, M., Gotza, B., and Gerardy-Schahn, R. (2001) The impact of N-glycosylation on the functions of polysialyltransferases. J. Biol. Chem. 276, 34066-34073
46. Angata, K., Yen, T.Y., El-Battari, A., Macher, B.A., and Fukuda, M. (2001) Unique disulfide bond structures found in ST8Sia IV polysialyltransferase are required for its activity. J. Biol. Chem. 276, 15369-15377
47. Close, B.E., Wilkinson, J.M., Bohrer, T.J., Goodwin, C.P., Broom, L.J., and Colley, K.J. (2001) The polysialyltransferase ST8Sia II/STX: posttranslational processing and role of autopolysialylation in the polysialylation of neural cell adhesion molecule. Glycobiology 11, 997-1008
48. Angata, K., Chan, D., Thibault, J., and Fukuda, M. (2004) Molecular dissection of the ST8Sia IV polysialyltransferase. Distinct domains are required for neural cell adhesion molecule recognition and polysialylation. J. Biol. Chem. 279, 25883-25890
49. Harduin-Lepers, A., Mollicone, R., Delannoy, P., and Oriol, R. (2005) The animal sialyltransferases and sialyltransferase-related genes: a phylogenetic approach. Glycobiology 15, 805-817
50. Allendorf, F.W. and Thorgaard, G.H. (1984) Tetraploidy and the evolution of salmonid fishes in Evolutionary Genetics of Fishes (Turner, J.B., eds) pp. 1-53, Plenum Press, New York
51. Amores, A., Force, A., Yan, Y.L., Joly, L., Amemiya, C., Fritz, A., Ho, R.K., Langeland, J., Prince, V., Wang, Y.L., Westerfield, M., Ekker, M., and Postlethwait, J.H. (1998) Zebrafish box clusters and vertebrate genome evolution. Science 282, 1711-1714
52. Angata, K., Nakayama, J., Fredette, B., Chong, K., Ranscht, B., and Fukuda, M. (1997) Human STX polysialyltransferase forms the embryonic form of the neural cell adhesion molecule. Tissue-specific expression, neurite outgrowth, and chromosomal localization in comparison with another polysialyltransferase, PST. J. Biol. Chem. 272, 7182-7190
53. Tsuchida, A., Ogiso, M., Nakamura, Y., Kiso, M., Furukawa, K., and Furukawa, K. (2005) Molecular cloning and expression of human ST6GalNAc III: restricted tissue distribution and substrate specificity. J. Biochem. 138, 237-243
54. Sotiropoulou, G., Kono, M., Anisowicz, A., Stenman, G., Tsuji, S., and Sager, R. (2002) Identification and functional characterization of a human GalNAc α2,6-sialyltransferase with altered expression in breast cancer. Mol Med. 8, 42-55
55. Kurosawa, N., Yoshida, Y., Kojima, N., and Tsuji, S. (1997) Polysialic acid synthase (ST8Sia II/STX) mRNA expression in the developing mouse central nervous system. J. Neurochem. 69, 494-503
56. Kojima, N., Kono, M., Yoshida, Y., Tachida, Y., Nakafuku, M., and Tsuji, S. (1996) Biosynthesis and expression of polysialic acid on the neural cell adhesion molecule is predominantly directed by ST8Sia II/STX during in vitro neuronal differentiation. J. Biol. Chem. 271, 22058-22062
57. Sato, C., Yasukawa, Z., Honda, N., Matsuda, T., and Kitajima, K. (2001) Identification and adipocyte differentiation-dependent expression of the unique disialic acid residue in an adipose tissue-specific glycoprotein, adipo Q. J. Biol. Chem. 276, 28849-28856
58. Takashima, S., Ishida, H.K., Inazu, T., Ando, T., Ishida, H., Kiso, M., Tsuji, S., and Tsujimoto, M. (2002) Molecular cloning and expression of a sixth type of α2,8-sialyltransferase (ST8Sia VI) that sialylates O-glycans. J. Biol. Chem. 277, 24030-24038
59. Teintenier-Lelievre, M., Julien, S., Juliant, S., Guerardel, Y., Duonor-Cerutti, M., Delannoy, P., and Harduin-Lepers, A. (2005) Molecular cloning and expression of a human hST8Sia VI (α2,8-sialyltransferase) responsible for the synthesis of the diSia motif on O-glycosylproteins. Biochem. J. 392, 665-674
60. Angata, K., Suzuki, M., McAuliffe, J., Ding, Y., Hindsgaul, O., and Fukuda, M. (2000) Differential biosynthesis of polysialic acid on neural cell adhesion molecule (NCAM) and oligosaccharide acceptors by three distinct α2,8-sialyltransferases, ST8Sia IV (PST), ST8Sia II (STX), and ST8Sia III. J. Biol. Chem. 275, 18594-18601
61. Close, B.E., Mendiratta, S.S., Geiger, K.M., Broom, L.J., Ho, L.L., and Colley, K.J. (2003) The minimal structural domains required for neural cell adhesion molecule polysialylation by PST/ST8Sia IV and STX/ST8Sia II. J. Biol. Chem. 278, 30796-30805
62. Mendiratta, S.S., Sekulic, N., Lavie, A., and Colley, K.J. (2005) Specific amino acids in the first fibronectin type III repeat of the neural cell adhesion molecule play a role in its recognition and polysialylation by the polysialyltransferase ST8Sia IV/ PST. J. Biol. Chem. 280, 32340-32348