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Bioscience, Biotechnology, and Biochemistry Volume 72, 2008 - Issue 5
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Original Articles

Characterization of Mouse Sialyltransferase Genes: Their Evolution and Diversity

Shou TAKASHIMAGlyco-Chain Functions Laboratory, RIKEN-FRS
Pages 1155-1167 | Published online: 22 May 2014

  • 1) Tsuji, S., Datta, A. K., and Paulson, J. C., Systematic nomenclature for sialyltransferases. Glycobiology, 6, (2) v-vii (1996).
  • 2) Takashima, S., Tsuji, S., and Tsujimoto, M., Comparison of the enzymatic properties of mouse β-galactoside α2,6-sialyltransferases, ST6Gal I and II. J. Biochem., 134, 287–296 (2003).
  • 3) Coutinho, P. M., Deleury, E., Davies, G. J., and Henrissat, B., An evolving hierarchical family classification for glycosyltransferases. J. Mol. Biol., 328, 307–317 (2003).
  • 4) Drickamer, K., A conserved disulphide bond in sialyltransferases. Glycobiology, 3, 2–3 (1993).
  • 5) Livingston, B. D., and Paulson, J. C., Polymerase chain reaction cloning of a developmentally regulated member of the sialyltransferase gene family. J. Biol. Chem., 268, 11504–11507 (1993).
  • 6) Jeanneau, C., Chazalet, V., Augé, C., Soumpasis, D. M., Harduin-Lepers, A., Delannoy, P., Imberty, A., and Breton, C., Structure-function analysis of the human sialyltransferase ST3Gal I. J. Biol. Chem., 279, 13461–13468 (2004).
  • 7) Geremia, R. A., Harduin-Lepers, A., and Delannoy, P., Identification of two novel conserved amino acid residues in eukaryotic sialyltransferases: implications for their mechanism of action. Glycobiology, 7, (2) v-vii (1997).
  • 8) Datta, A. K., and Paulson, J. C., The sialyltransferase “sialylmotif” participates in binding the donor substrate CMP-NeuAc. J. Biol. Chem., 270, 1497–1500 (1995).
  • 9) Datta, A. K., Sinha, A., and Paulson, J. C., Mutation of the sialyltransferase S-sialylmotif alters the kinetics of the donor and acceptor substrates. J. Biol. Chem., 273, 9608–9614 (1998).
  • 10) Kitazume-Kawaguchi, S., Kabata, S., and Arita, M., Differential biosynthesis of polysialic or disialic acid structure by ST8Sia II and ST8Sia IV. J. Biol. Chem., 276, 15696–15703 (2001).
  • 11) Jackson, R. J., Hall, D. F., and Kerr, P. J., Myxoma virus encodes an α2,3-sialyltransferase that enhances virulence. J. Virol., 73, 2376–2384 (1999).
  • 12) Sujino, K., Jackson, R. J., Chan, N. W., Tsuji, S., and Palcic, M. M., A novel viral α2,3-sialyltransferase (v-ST3Gal I): transfer of sialic acid to fucosylated acceptors. Glycobiology, 10, 313–320 (2000).
  • 13) Koles, K., Irvine, K. D., and Panin, V. M., Functional characterization of Drosophila sialyltransferase. J. Biol. Chem., 279, 4346–4357 (2004).
  • 14) Harduin-Lepers, A., Mollicone, R., Delannoy, P., and Oriol, R., The animal sialyltransferases and sialyltransferase-related genes: a phylogenetic approach. Glycobiology, 15, 805–817 (2005).
  • 15) Tsuji, S., Molecular cloning and functional analysis of sialyltransferases. J. Biochem., 120, 1–13 (1996).
  • 16) Tsuji, S., Molecular cloning and characterization of sialyltransferases. In “Sialobiology and Other Novel Forms of Glycosylation,” eds. Inoue, Y., Lee, Y. C., and Troy, F. A., II, Gakushin Publishing, Osaka, pp. 145–154 (1999).
  • 17) Séveno, S., Bardor, M., Paccalet, T., Gomord, V., Lerouge, P., and Faye, L., Glycoprotein sialylation in plants? Nat. Biotechnol., 22, 1351–1352 (2004).
  • 18) Zeleny, R., Kolarich, D., Strasser, R., and Altmann, F., Sialic acid concentrations in plants are in the range of inadvertent contamination. Planta, 224, 222–227 (2006).
  • 19) Bourbouze, R., Akiki, C., Chardon-Loriaux, I., and Percheron, F., Mise en evidence de derives de l’acide neuraminique dans des glycoprotéines végétales. Carbohydr. Res., 106, 21–30 (1982).
  • 20) Shah, M. M., Fujiyama, K., Flynn, C. R., and Joshi, L., Sialylated endogenous glycoconjugates in plant cells. Nat. Biotechnol., 21, 1470–1471 (2003).
  • 21) Takashima, S., Abe, T., Yoshida, S., Kawahigashi, H., Saito, T., Tsuji, S., and Tsujimoto, M., Analysis of sialyltransferase-like proteins from Oryza sativa. J. Biochem., 139, 279–287 (2006).
  • 22) Freiberger, F., Claus, H., Gunzel, A., Oltmann-Norden, I., Vionnet, J., Muhlenhoff, M., Vogel, U., Vann, W. F., Gerardy-Schahn, R., and Stummeyer, K., Biochemical characterization of a Neisseria meningitides polysialyltransferase reveals novel functional motifs in bacterial sialyltransferases. Mol. Microbiol., 65, 1258–1275 (2007).
  • 23) Yamamoto, T., Ichikawa, M., and Takakura, Y., Conserved amino acid sequences in the bacterial sialyltransferases belonging to Glycosyltransferase family 80. Biochem. Biophys. Res. Commun., 365, 340–343 (2008).
  • 24) Lee, Y.-C., Kurosawa, N., Hamamoto, T., Nakaoka, T., and Tsuji, S., Molecular cloning and expression of Galβ1,3GalNAc α2,3-sialyltransferase from mouse brain. Eur. J. Biochem., 216, 377–385 (1993).
  • 25) Lee, Y.-C., Kojima, N., Wada, E., Kurosawa, N., Nakaoka, T., Hamamoto, T., and Tsuji, S., Cloning and expression of cDNA for a new type of Galβ1,3GalNAc α2,3-sialyltransferase. J. Biol. Chem., 269, 10028–10033 (1994).
  • 26) Kono, M., Ohyama, Y., Lee, Y.-C., Hamamoto, T., Kojima, N., and Tsuji, S., Mouse β-galactoside α2,3-sialyltransferases: comparison of in vitro substrate specificities and tissue specific expression. Glycobiology, 7, 469–479 (1997).
  • 27) Priatel, J. J., Chui, D., Hiraoka, N., Simmons, C. J., Richardson, K. B., Page, D. M., Fukuda, M., Varki, N. M., and Marth, J. D., The ST3Gal-I sialyltransferase controls CD8+ T lymphocyte homeostasis by modulating O-glycan biosynthesis. Immunity, 12, 273–283 (2000).
  • 28) Takashima, S., and Tsuji, S., Comparison of genomic structures of four members of mouse β-galactoside α2,3-sialyltransferase genes. Cytogenet. Cell Genet., 89, 101–106 (2000).
  • 29) Takashima, S., Tsuji, S., and Tsujimoto, M., Characterization of the second type of human β-galactoside α2,6-sialyltransferase (ST6Gal II), which sialylates Galβ1,4GlcNAc structures on oligosaccharides preferentially. J. Biol. Chem., 277, 45719–45728 (2002).
  • 30) Sasaki, K., Watanabe, E., Kawashima, K., Sekine, S., Dohi, T., Oshima, M., Hanai, N., Nishi, T., and Hasegawa, M., Expression cloning of a novel Galβ(1-3/1-4)GlcNAc α2,3-sialyltransferase using lectin resistance selection. J. Biol. Chem., 268, 22782–22787 (1993).
  • 31) Ellies, L. G., Ditto, D., Levy, G. G., Wahrenbrock, M., Ginsburg, D., Varki, A., Le, D. T., and Marth, J. D., Sialyltransferase ST3Gal-IV operates as a dominant modifier of hemostasis by concealing asialoglycoprotein receptor ligands. Proc. Natl. Acad. Sci. USA, 99, 10042–10047 (2002).
  • 32) Ellies, L. G., Sperandio, M., Underhill, G. H., Yousif, J., Smith, M., Priatel, J. J., Kansas, G. S., Ley, K., and Marth, J. D., Sialyltransferase specificity in selectin ligand formation. Blood, 100, 3618–3625 (2002).
  • 33) Svennerholm, L., The gangliosides. J. Lipid Res., 5, 145–155 (1964).
  • 34) Ishii, A., Ohta, M., Watanabe, Y., Matsuda, K., Ishiyama, K., Sakoe, K., Nakamura, M., Inokuchi, J., Sanai, Y., and Saito, M., Expression cloning and functional characterization of human cDNA for ganglioside GM3 synthase. J. Biol. Chem., 273, 31652–31655 (1998).
  • 35) Kono, M., Takashima, S., Liu, H., Inoue, M., Kojima, N., Lee, Y.-C., Hamamoto, T., and Tsuji, S., Molecular cloning and functional expression of a fifth-type α2,3-sialyltransferase (mST3Gal V: GM3 synthase). Biochem. Biophys. Res. Commun., 253, 170–175 (1998).
  • 36) Fukumoto, S., Miyazaki, H., Goto, G., Urano, T., Furukawa, K., and Furukawa, K., Expression cloning of mouse cDNA of CMP-NeuAc:lactosylceramide α2,3-sialyltransferase, an enzyme that initiates the synthesis of gangliosides. J. Biol. Chem., 274, 9271–9276 (1999).
  • 37) Kapitonov, D., Bieberich, E., and Yu, R. K., Combinatorial PCR approach to homology-based cloning: cloning and expression of mouse and human GM3-synthase. Glycoconj. J., 16, 337–350 (1999).
  • 38) Yamashita, T., Hashiramoto, A., Haluzik, M., Mizukami, H., Beck, S., Norton, A., Kono, M., Tsuji, S., Daniotti, J. L., Werth, N., Sandhoff, R., Sandhoff, K., and Proia, R. L., Enhanced insulin sensitivity in mice lacking ganglioside GM3. Proc. Natl. Acad. Sci. USA, 100, 3445–3449 (2003).
  • 39) Okajima, T., Fukumoto, S., Miyazaki, H., Ishida, H., Kiso, M., Furukawa, K., Urano, T., and Furukawa, K., Molecular cloning of a novel α2,3-sialyltransferase (ST3Gal VI) that sialylates type II lactosamine structures on glycoproteins and glycolipids. J. Biol. Chem., 274, 11479–11486 (1999).
  • 40) Grundnann, V., Nerlich, C., Rein, T., and Zettlmeissl, G., Complete cDNA sequence encoding human β-galactoside α2,6-sialyltransferase. Nucleic Acid Res., 18, 667 (1990).
  • 41) Hamamoto, T., Kawasaki, M., Kurosawa, N., Nakaoka, T., Lee, Y.-C., and Tsuji, S., Two step single primer mediated polymerase chain reaction: application to cloning of putative mouse, β-galactoside α2,6-sialyltransferase cDNA. Bioorg. Med. Chem., 1, 141–145 (1993).
  • 42) Krzewinski-Recchi, M.-A., Julien, S., Juliant, S., Teintenier-Lelièvre, M., Samyn-Petit, B., Montiel, M.-D., Mir, A.-M., Cerutti, M., Harduin-Lepers, A., and Delannoy, P., Identification and functional expression of a second human β-galactoside α2,6-sialyltransferase, ST6Gal II. Eur. J. Biochem., 270, 950–961 (2003).
  • 43) Takashima, S., and Tsuji, S., Unique enzymatic properties of mouse sialyltransferases, ST6Gal II and ST8Sia VI. Trends Glycosci. Glycotech., 16, 345–356 (2004).
  • 44) Hennet, T., Chui, D., Paulson, J. C., and Marth, J. D., Immune regulation by the ST6Gal sialyltransferase. Proc. Natl. Acad. Sci. USA, 95, 4504–4509 (1998).
  • 45) Kurosawa, N., Takashima, S., Kono, M., Ikehara, Y., Inoue, M., Tachida, Y., Narimatsu, H., and Tsuji, S., Molecular cloning and genomic analysis of mouse GalNAc α2,6-sialyltransferase (ST6GalNAc I). J. Biochem., 127, 845–854 (2000).
  • 46) Kurosawa, N., Inoue, M., Yoshida, Y., and Tsuji, S., Molecular cloning and genomic analysis of mouse Galβ1,3GalNAc-specific GalNAc α2,6-sialyltransferase. J. Biol. Chem., 271, 15109–15116 (1996).
  • 47) Kono, M., Tsuda, T., Ogata, S., Takashima, S., Liu, H., Hamamoto, T., Itzkowitz, S. H., Nishimura, S., and Tsuji, S., Redefined substrate specificity of ST6GalNAc II: a second candidate sialyl-Tn synthase. Biochem. Biophys. Res. Commun., 272, 94–97 (2000).
  • 48) Lee, Y.-C., Kaufmann, M., Kitazume-Kawaguchi, S., Kono, M., Takashima, S., Kurosawa, N., Liu, H., Pircher, H., and Tsuji, S., Molecular cloning and functional expression of two members of mouse NeuAcα2,3Galβ1,3GalNAc GalNAcα2,6-sialyltransferase family, ST6GalNAc III and IV. J. Biol. Chem., 274, 11958–11967 (1999).
  • 49) Kaufmann, M., Blaser, C., Takashima, S., Schwartz-Albiez, R., Tsuji, S., and Pircher, H., Identification of an α2,6-sialyltransferase induced early after lymphocyte activation. Int. Immunol., 11, 731–738 (1999).
  • 50) Okajima, T., Fukumoto, S., Ito, H., Kiso, M., Hirabayashi, Y., Urano, T., and Furukawa, K., Molecular cloning of brain-specific GD1α synthase (ST6GalNAc V) containing CAG/Glutamine repeats. J. Biol. Chem., 274, 30557–30562 (1999).
  • 51) Ikehara, Y., Shimizu, N., Kono, M., Nishihara, S., Nakanishi, H., Kitamura, T., Narimatsu, H., Tsuji, S., and Tatematsu, M., A novel glycosyltransferase with a polyglutamine repeat; a new candidate for GD1α synthase (ST6GalNAc V). FEBS Lett., 463, 92–96 (1999).
  • 52) Okajima, T., Chen, H. H., Ito, H., Kiso, M., Tai, T., Furukawa, K., Urano, T., and Furukawa, K., Molecular cloning and expression of mouse GD1α/GT1aα/GQ1bα synthase (ST6GalNAc VI) gene. J. Biol. Chem., 275, 6717–6723 (2000).
  • 53) Tsuchida, A., Okajima, T., Furukawa, K., Ando, T., Ishida, H., Yoshida, A., Nakamura, Y., Kannagi, R., Kiso, M., and Furukawa, K., Synthesis of disialyl Lewis a (Lea) structure in colon cancer cell lines by a sialyltransferase, ST6GalNAc VI, responsible for the synthesis of α-series gangliosides. J. Biol. Chem., 278, 22787–22794 (2003).
  • 54) Takashima, S., Kurosawa, N., Tachida, Y., Inoue, M., and Tsuji, S., Comparative analysis of the genomic structures and promoter activities of mouse Siaα2,3Galβ1,3GalNAcα2,6-sialyltransferase genes (ST6GalNAc III and IV): characterization of their Sp1 binding sites. J. Biochem., 127, 399–409 (2000).
  • 55) Yamamoto, A., Haraguchi, M., Yamashiro, S., Fukumoto, S., Furukawa, K., Takamiya, K., Atsuta, M., Shiku, H., and Furukawa, K., Heterogeneity in the expression pattern of two ganglioside synthase genes during mouse brain development. J. Neurochem., 66, 26–34 (1996).
  • 56) Kono, M., Yoshida, Y., Kojima, N., and Tsuji, S., Molecular cloning and expression of a fifth type of α2,8-sialyltransferase (ST8Sia V): its substrate specificity is similar to that of SAT-V/III, which synthesize GD1c, GT1a, GQ1b and GT3. J. Biol. Chem., 271, 29366–29371 (1996).
  • 57) Takashima, S., Ishida, H.-K., Inazu, T., Ando, T., Ishida, H., Kiso, M., Tsuji, S., and Tsujimoto, M., Molecular cloning and expression of a sixth type of α2,8-sialyltransferase (ST8Sia VI) that sialylates O-glycans. J. Biol. Chem., 277, 24030–24038 (2002).
  • 58) Okada, M., Itoh, M., Haraguchi, M., Okajima, T., Inoue, M., Oishi, H., Matsuda, Y., Iwamoto, T., Kawano, T., Fukumoto, S., Miyazaki, H., Furukawa, K., Aizawa, S., and Furukawa, K., b-Series ganglioside deficiency exhibits no definite changes in the neurogenesis and the sensitivity to Fas-mediated apoptosis but impairs regeneration of the lesioned hypoglossal nerve. J. Biol. Chem., 277, 1633–1636 (2002).
  • 59) Handa, Y., Ozaki, N., Honda, T., Furukawa, K., Tomita, Y., Inoue, M., Furukawa, K., Okada, M., and Sugiura, Y., GD3 synthase gene knockout mice exhibit thermal hyperalgesia and mechanical allodynia but decreased response to formalin-induced prolonged noxious stimulation. Pain, 117, 271–279 (2005).
  • 60) Kawai, H., Allende, M. L., Wada, R., Kono, M., Sango, K., Deng, C., Miyakawa, T., Crawley, J. N., Werth, N., Bierfreund, U., Sandhoff, K., and Proia, R. L., Mice expressing only monosialoganglioside GM3 exhibit lethal audiogenic seizures. J. Biol. Chem., 276, 6885–6888 (2001).
  • 61) Inoue, M., Fujii, Y., Furukawa, K., Okada, M., Okumura, K., Hayakawa, T., Furukawa, K., and Sugiura, Y., Refractory skin injury in complex knock-out mice expressing only the GM3 ganglioside. J. Biol. Chem., 277, 29881–29888 (2002).
  • 62) Takashima, S., Kono, M., Kurosawa, N., Yoshida, Y., Tachida, Y., Inoue, M., Kanematsu, T., and Tsuji, S., Genomic organization and transcriptional regulation of the mouse GD3 synthase gene (ST8Sia I): comparison of genomic organization of the mouse sialyltransferase genes. J. Biochem., 128, 1033–1043 (2000).
  • 63) Kojima, N., Yoshida, Y., Kurosawa, N., Lee, Y.-C., and Tsuji, S., 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 (1995).
  • 64) Yoshida, Y., Kojima, N., and Tsuji, S., Molecular cloning and characterization of a third type of N-glycan α2,8-sialyltransferase from mouse lung. J. Biochem., 118, 658–664 (1995).
  • 65) Yoshida, Y., Kojima, N., Kurosawa, N., Hamamoto, T., and Tsuji, S., Molecular cloning of Siaα2,3Galβ1,4GlcNAc α2,8-sialyltransferase from mouse brain. J. Biol. Chem., 270, 14628–14633 (1995).
  • 66) Angata, K., Suzuki, M., McAuliffe, J., Ding, Y., Hindsgaul, O., and Fukuda, M., 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 (2000).
  • 67) Zuber, C., Lackie, P. M., Catterall, W. A., and Roth, J., 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 (1992).
  • 68) Sato, C., Fukuoka, H., Ohta, K., Matsuda, T., Koshino, R., Kobayashi, K., Troy, F. A., 2nd, and Kitajima, K., Frequent occurrence of pre-existing α2→8-linked disialic and oligosialic acids with chain lengths up to 7 Sia residues in mammalian brain glycoproteins. J. Biol. Chem., 275, 15422–15431 (2000).
  • 69) Yabe, U., Sato, C., Matsuda, T., and Kitajima, K., Polysialic acid in human milk. J. Biol. Chem., 278, 13875–13880 (2003).
  • 70) Angata, K., Suzuki, M., and Fukuda, M., Differential and cooperative polysialylation of the neural cell adhesion molecule by two polysialyltransferases, PST and STX. J. Biol. Chem., 273, 28524–28532 (1998).
  • 71) Angata, K., Suzuki, M., and Fukuda, M., ST8Sia II and ST8Sia IV polysialyltransferases exhibit marked differences in utilizing various acceptors containing oligosialic acid and short polysialic acid. J. Biol. Chem., 277, 36808–36817 (2002).
  • 72) Eckhardt, M., Bukalo, O., Chazal, G., Wang, L., Goridis, C., Schachner, M., Gerardy-Schahn, R., Cremer, H., and Dityatev, A., 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 (2000).
  • 73) Angata, K., Long, J. M., Bukalo, O., Lee, W., Dityatev, A., Wynshaw-Boris, A., Schachner, M., Fukuda, M., and Marth, J. D., Sialyltransferase ST8Sia-II assembles a subset of polysialic acid that directs hippocampal axonal targeting and promotes fear behavior. J. Biol. Chem., 279, 32603–32613 (2004).
  • 74) Sato, C., Yasukawa, Z., Honda, N., Matsuda, T., and Kitajima, K., 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 (2001).
  • 75) Yoshida, Y., Kurosawa, N., Kanematsu, T., Kojima, N., and Tsuji, S., Genomic structure and promoter activity of the mouse polysialic acid synthase gene (mST8Sia II). J. Biol. Chem., 271, 30167–30173 (1996).
  • 76) Takashima, S., Yoshida, Y., Kanematsu, T., Kojima, N., and Tsuji, S., Genomic structure and promoter activity of the mouse polysialic acid synthase (mST8Sia IV/PST) gene. J. Biol. Chem., 273, 7675–7683 (1998).
  • 77) Eckhardt, M., and Gerardy-Schahn, R., Genomic organization of the murine polysialyltransferase gene ST8Sia IV (PST-1). Glycobiology, 8, 1165–1172 (1998).
  • 78) Yoshida, Y., Kurosawa, N., Kanematsu, T., Taguchi, A., Arita, M., Kojima, N., and Tsuji, S., Unique genomic structure and expression of the mouse α2,8-sialyltransferase (ST8Sia III) gene. Glycobiology, 6, 573–580 (1996).
  • 79) Chenna, R., Sugawara, H., Koike, T., Lopez, R., Gibson, T. J., Higgins, D. G., and Thompson, J. D., Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res., 31, 3497–3500 (2003).
  • 80) Page, R. D. M., TREEVIEW: an application to display phylogenetic trees on personal computers. Comp. Appl. Biosci., 12, 357–358 (1996).
  • 81) Wakarchuk, W. W., Watson, D., St. Michael, F., Li, J., Wu, Y., Brisson, J. R., Young, N. M., and Gilbert, M., Dependence of the bi-functional nature of a sialyltransferase from Neisseria meningitidis on a single amino acid substitution. J. Biol. Chem., 276, 12785–12790 (2001).
  • 82) Chiu, C. P., Watts, A. G., Lairson, L. L., Gilbert, M., Lim, D., Wakarchuk, W. W., Withers, S. G., and Strynadka, N. C., Structural analysis of the sialyltransferase CstII from Campylobacter jejuni in complex with a substrate analog. Nat. Struct. Mol. Biol., 11, 163–170 (2004).
  • 83) Takashima, S., Tachida, Y., Nakagawa, T., Hamamoto, T., and Tsuji, S., Quantitative analysis of expression of mouse sialyltransferase genes by competitive PCR. Biochem. Biophys. Res. Commun., 260, 23–27 (1999).

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