Skip to main content
SpringerLink
Log in

Molecular cloning and characterization of the expression pattern of the zebrafish α2, 8-sialyltransferases (ST8Sia) in the developing nervous system

  • Published:
Glycoconjugate Journal Aims and scope Submit manuscript

Abstract

Sialyltransferases are Golgi type II transmembrane glycoproteins involved in the biosynthesis of sialylated glycolipids and glycoproteins. These sialylated compounds play fundamental roles in the development of a variety of tissues including the nervous system. In this study, we have molecularly cloned from zebrafish sources, the orthologues of the six human α2,8-sialyltransferases (ST8Sia), a family of sialyltransferases implicated in the α2-8-mono-, oligo-, and poly-sialylation of glycoproteins and gangliosides and we have analysed their expression pattern in the embryonic zebrafish nervous system, using in situ hybridization. Our results show that all six ST8Sia exhibit distinct and overlapping patterns of expression in the developing zebrafish central nervous system with spatial and temporal regulation of the expression of these genes, which suggests a role for the α2-8-sialylated compounds in the developing nervous system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

ST8Sia:

α2,8-sialyltransferase, nomenclature according to Tsuji, S., Datta, A.K., Paulson, J.C., Glycobiology 6, v–vii (1996), Gangliosides nomenclature according to Svennerholm, L., J. Lipid Res. 5, 145–155 (1964)

ORF:

open reading frame

hpf:

hours post fertilization

dpf:

days post fertilization

diSia:

diSialic acid

Dre:

Danio rerio

Hsa:

Homo sapiens

ISH:

in situ hybridization

NS:

nervous system

CNS:

central nervous system

PNS:

peripheral nervous system

References

  1. Kelm, S., Schauer, R.: Sialic acids in molecular and cellular interactions. Int. Rev. Cytol. 175, 137–240 (1997)

    Article  PubMed  CAS  Google Scholar 

  2. Sato, C., Kitajima, K.: Glycobiology of di- and oligosialyl glycotopes. Trends Glycosci. Glycotechnol. 11, 371–390 (1999)

    CAS  Google Scholar 

  3. Troy, F.A., 2nd: Polysialylation: from bacteria to brains. Glycobiology 2, 5–23 (1992). doi:10.1093/glycob/2.1.5

    Article  PubMed  CAS  Google Scholar 

  4. Barbeau, D., Liang, J.J., Robitalille, Y., Quirion, R., Srivastava, L.K.: Decreased expression of the embryonic form of the neural cell adhesion molecule in schizophrenic brains. Proc. Natl. Acad. Sci. USA 92, 2785–2789 (1995). doi:10.1073/pnas.92.7.2785

    Article  PubMed  CAS  Google Scholar 

  5. Majocha, R.E., Jungalwala, F.B., Rodenrys, A., Marotta, C.A.: Monoclonal antibody to embryonic CNS antigen A2B5 provides evidence for the involvement of membrane components at sites of Alzheimer degeneration and detects sulfatides as well as gangliosides. J. Neurochem. 53, 953–961 (1989). doi:10.1111/j.1471-4159.1989.tb11798.x

    Article  PubMed  CAS  Google Scholar 

  6. Yanagisawa, K.: Role of gangliosides in Alzheimer’s disease. Biochim. Biophys. Acta 1768, 1943–1951 (2007). doi:10.1016/j.bbamem.2007.01.018

    Article  PubMed  CAS  Google Scholar 

  7. Schwarz, A., Futerman, A.H.: The localization of gangliosides in neurons of the central nervous system: the use of anti-ganglioside antibodies. Biochim. Biophys. Acta 1286, 247–267 (1996)

    PubMed  CAS  Google Scholar 

  8. Rauvala, H.: Neurite outgrowth of neuroblastoma cells: dependence on adhesion surface–cell surface interactions. J. Cell Biol. 98, 1010–1016 (1984). doi:10.1083/jcb.98.3.1010

    Article  PubMed  CAS  Google Scholar 

  9. Ngamukote, S., Yanagisawa, M., Ariga, T., Ando, S., Yu, R.K.: Developmental changes of glycosphingolipids and expression of glycogenes in mouse brains. J. Neurochem. 103, 2327–2341 (2007). doi:10.1111/j.1471-4159.2007.04910.x

    Article  PubMed  CAS  Google Scholar 

  10. Yu, R.K., Macala, L.J., Taki, T., Weinfield, H.M., Yu, F.S.: Developmental changes in ganglioside composition and synthesis in embryonic rat brain. J. Neurochem. 50, 1825–1829 (1988). doi:10.1111/j.1471-4159.1988.tb02484.x

    Article  PubMed  CAS  Google Scholar 

  11. Guérardel, Y., Chang, L.Y., Maes, E., Huang, C.J., Khoo, K.H.: Glycomic survey mapping of zebrafish identifies unique sialylation pattern. Glycobiology 16, 244–257 (2006). doi:10.1093/glycob/cwj062

    Article  PubMed  CAS  Google Scholar 

  12. Freischutz, B., Saito, M., Rahmann, H., Yu, R.K.: Activities of five different sialyltransferases in fish and rat brains. J. Neurochem. 62, 1965–1973 (1994)

    Article  PubMed  CAS  Google Scholar 

  13. Finne, J.: Occurrence of unique polysialosyl carbohydrate units in glycoproteins of developing brain. J. Biol. Chem. 257, 11966–11970 (1982)

    PubMed  CAS  Google Scholar 

  14. Sato, C., Fukuoka, H., Ohta, K., Matsuda, T., Koshino, R., Kobayashi, K., et al.: Frequent occurrence of pre-existing alpha 2®8-linked disialic and oligosialic acids with chain lengths up to 7 Sia residues in mammalian brain glycoproteins. Prevalence revealed by highly sensitive chemical methods and anti-di-, oligo-, and poly-Sia antibodies specific for defined chain lengths. J. Biol. Chem. 275, 15422–15431 (2000). doi:10.1074/jbc.275.20.15422

    Article  PubMed  CAS  Google Scholar 

  15. Zuber, C., Lackie, P., Catterall, W., 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)

    PubMed  CAS  Google Scholar 

  16. Muhlenhoff, M., Eckhardt, M., Bethe, A., Frosch, M., Gerardy-Schahn, R.: Autocatalytic polysialylation of polysialyltransferase-1. EMBO J. 15, 6943–6950 (1996)

    PubMed  CAS  Google Scholar 

  17. Close, B.E., Colley, K.J.: In vivo autopolysialylation and localization of the polysialyltransferases PST and STX. J. Biol. Chem. 273, 34586–34593 (1998). doi:10.1074/jbc.273.51.34586

    Article  PubMed  CAS  Google Scholar 

  18. Curreli, S., Arany, Z., Gerardy-Schahn, R., Mann, D., Stamatos, N.M.: Polysialylated neuropilin-2 is expressed on the surface of human dendritic cells and modulates dendritic cell-T lymphocyte interactions. J. Biol. Chem. 282, 30346–30356 (2007). doi:10.1074/jbc.M702965200

    Article  PubMed  CAS  Google Scholar 

  19. Bruses, J.L., Rutishauser, U.: Roles, regulation, and mechanism of polysialic acid function during neural development. Biochimie 83, 635–643 (2001). doi:10.1016/S0300-9084(01)01293-7

    Article  PubMed  CAS  Google Scholar 

  20. Bonfanti, L.: PSA-N-CAM in mammalian structural plasticity and neurogenesis. Prog. Neurobiol. 80, 129–164 (2006). doi:10.1016/j.pneurobio.2006.08.003

    Article  PubMed  CAS  Google Scholar 

  21. Marx, M., Rutishauser, U., Bastmeyer, M.: Dual function of polysialic acid during zebrafish central nervous system development. Development 128, 4949–4958 (2001)

    PubMed  CAS  Google Scholar 

  22. Vutskits, L., Gascon, E., Zgraggen, E., Kiss, J.Z.: The polysialylated neural cell adhesion molecule promotes neurogenesis in vitro. Neurochem. Res. 31, 215–225 (2006). doi:10.1007/s11064-005-9021-7

    Article  PubMed  CAS  Google Scholar 

  23. Rieger, S., Volkmann, K., Koster, R.W.: Polysialyltransferase expression is linked to neuronal migration in the developing and adult zebrafish. Dev. Dyn. 237, 276–285 (2008). doi:10.1002/dvdy.21410

    Article  PubMed  CAS  Google Scholar 

  24. Finne, J., Krusius, T., Rauvala, H.: Occurrence of disialosyl groups in glycoproteins. Biochem. Biophys. Res. Commun. 74, 405–410 (1977). doi:10.1016/0006-291X(77)90318-7

    Article  PubMed  CAS  Google Scholar 

  25. Sato, C., Matsuda, T., Kitajima, K.: 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 (2002). doi:10.1074/jbc.M206046200

    Article  PubMed  CAS  Google Scholar 

  26. Inoue, S., Lin, S.L., Inoue, Y.: Chemical analysis of the developmental pattern of polysialylation in chicken brain. Expression of only an extended form of polysialyl chains during embryogenesis and the presence of disialyl residues in both embryonic and adult chicken brains. J. Biol. Chem. 275, 29968–29979 (2000). doi:10.1074/jbc.M004150200

    Article  PubMed  CAS  Google Scholar 

  27. Coutinho, P.M., Deleury, E., Davies, G.J., Henrissat, B.: An evolving hierarchical family classification for glycosyltransferases. J. Mol. Biol. 328, 307–317 (2003). doi:10.1016/S0022-2836(03)00307-3

    Article  PubMed  CAS  Google Scholar 

  28. Harduin-Lepers, A., Vallejo-Ruiz, V., Krzewinski-Recchi, M.A., Samyn-Petit, B., Julien, S., Delannoy, P.: The human sialyltransferase family. Biochimie 83, 727–737 (2001). doi:10.1016/S0300-9084(01)01301-3

    Article  PubMed  CAS  Google Scholar 

  29. Yu, R., Bieberich, E., Xia, T., Zeng, G.: Regulation of ganglioside biosynthesis in the nervous system. J. Lipid Res. 45, 783–793 (2004). doi:10.1194/jlr.R300020-JLR200

    Article  PubMed  CAS  Google Scholar 

  30. Teintenier-Lelievre, M., Julien, S., Juliant, S., Guerardel, Y., Duonor-Cerutti, M., Delannoy, P., et al.: 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 (2005). doi:10.1042/BJ20051120

    Article  PubMed  CAS  Google Scholar 

  31. Nakayama, J., Angata, K., Ong, E., Katsuyama, T., Fukuda, M.: Polysialic acid, a unique glycan that is developmentally regulated by two polysialyltransferases, PST and STX, in the central nervous system: from biosynthesis to function. Pathol. Int. 48, 665–677 (1998)

    Article  PubMed  CAS  Google Scholar 

  32. Hildebrandt, H., Muhlenhoff, M., Weinhold, B., Gerardy-Schahn, R.: Dissecting polysialic acid and NCAM functions in brain development. J. Neurochem. 103(Suppl 1), 56–64 (2007). doi:10.1111/j.1471-4159.2007.04716.x

    Article  PubMed  CAS  Google Scholar 

  33. Marx, M., Rivera-Milla, E., Stummeyer, K., Gerardy-Schahn, R., Bastmeyer, M.: Divergent evolution of the vertebrate polysialyltransferase Stx and Pst genes revealed by fish-to-mammal comparison. Dev. Biol. 306, 560–571 (2007). doi:10.1016/j.ydbio.2007.03.032

    Article  PubMed  CAS  Google Scholar 

  34. Harduin-Lepers, A., Mollicone, R., Delannoy, P., Oriol, R.: The animal sialyltransferases and sialyltransferase-related genes: a phylogenetic approach. Glycobiology 15, 805–817 (2005). doi:10.1093/glycob/cwi063

    Article  PubMed  CAS  Google Scholar 

  35. Westerfield, M.: The zebrafish book. A guide for laboratory use of zebrafish (Danio rerio), p. 385. Inst of Neuro Science, Boston (1995)

    Google Scholar 

  36. Thisse, C., Thisse, B.: High resolution whole-mount in situ hybridization. In Zebrafish Science Monitor. Vol.5, edited by (University of Oregon Press, Eugene, OR 97403-5274, 1998), pp. http://zfin.org

  37. Thisse, B., Heyer, V., Lux, A., Alunni, V., Degrave, A., Seiliez, I., et al.: Spatial and temporal expression of the zebrafish genome by large-scale in situ hybridization screening. Methods Cell Biol. 77, 505–519 (2004)

    Article  PubMed  CAS  Google Scholar 

  38. Thisse, C., Thisse, B.: High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat. Protocols 3, 59–69 (2008). doi:10.1038/nprot.2007.514

    Article  CAS  Google Scholar 

  39. Thisse, B., Pflumio, S., Fürthauer, M., Loppin, B., Heyer, V., Degrave, A., Woehl, R., Lux, A., Steffan, T., Charbonnier, X.Q., Thisse, C.: Expression of the zebrafish genome during embryogenesis, (2001)

  40. Key, B., Devine, C.A.: Zebrafish as an experimental model: strategies for developmental and molecular neurobiology studies. Methods Cell Sci. 25, 1–6 (2003). doi:10.1023/B:MICS.0000006849.98007.03

    Article  PubMed  CAS  Google Scholar 

  41. Eckhardt, M., Bukalo, O., Chazal, G., Wang, L., Goridis, C., Schachner, M., et al.: 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)

    PubMed  CAS  Google Scholar 

  42. Angata, K., Long, J.M., Bukalo, O., Lee, W., Dityatev, A., Wynshaw-Boris, A., et al.: 8Sia-II assembles a subset of polysialic acid that directs hippocampal axonal targeting and promotes fear behavior. J. Biol. Chem. 279, 32603–32613 (2004). doi:10.1074/jbc.M403429200

    Article  PubMed  CAS  Google Scholar 

  43. Handa, Y., Ozaki, N., Honda, T., Furukawa, K., Tomita, Y., Inoue, M., et al.: 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). doi:10.1016/j.pain.2005.06.016

    Article  PubMed  CAS  Google Scholar 

  44. Weinhold, B., Seidenfaden, R., Rockle, I., Muhlenhoff, M., Schertzinger, F., Conzelmann, S., et al.: Genetic ablation of polysialic acid causes severe neurodevelopmental defects rescued by deletion of the neural cell adhesion molecule. J. Biol. Chem. 280, 42971–42977 (2005). doi:10.1074/jbc.M511097200

    Article  PubMed  CAS  Google Scholar 

  45. Angata, K., Huckaby, V., Ranscht, B., Terskikh, A., Marth, J.D., Fukuda, M.: Polysialic acid-directed migration and differentiation of neural precursors are essential for mouse brain development. Mol. Cell. Biol. 27, 6659–6668 (2007). doi:10.1128/MCB.00205-07

    Article  PubMed  CAS  Google Scholar 

  46. Bentrop, J., Marx, M., Schattschneider, S., Rivera-Milla, E., Bastmeyer, M.: Molecular evolution and expression of zebrafish St8SiaIII, an alpha-2,8-sialyltransferase involved in myotome development. Dev Dyn 237, 808–818 (2008)

    Article  PubMed  CAS  Google Scholar 

  47. Avrova, N.F., Li, Y.T., Obukhova, E.L.: On the composition and structure of individual gangliosides from the brain of elasmobranches. J. Neurochem. 32, 1807–1815 (1979). doi:10.1111/j.1471-4159.1979.tb02295.x

    Article  PubMed  CAS  Google Scholar 

  48. Kustermann, S., Hildebrandt, H., Bolz, S., Kohler, K.: Polysialylated N-CAM in persistent neurogenesis in zebrafish retina, (2007)

  49. Bartsch, U., Kirchhoff, F., Schachner, M.: Highly sialylated N-CAM is expressed in adult mouse optic nerve and retina. J. Neurocytol. 19, 550–565 (1990). doi:10.1007/BF01257243

    Article  PubMed  CAS  Google Scholar 

  50. Sawaguchi, A., Idate, Y., Ide, S., Kawano, J., Nagaike, R., Oinuma, T., et al.: Multistratified expression of polysialic acid and its relationship to VAChT-containing neurons in the inner plexiform layer of adult rat retina. J. Histochem. Cytochem. 47(7), 919–928 (1999)

    PubMed  CAS  Google Scholar 

  51. Zako, M., Iwaki, M., Yoneda, M., Miyaishi, O., Zhao, J., Suzuki, Y., et al.: Molecular cloning and characterization of chick sialoprotein associated with cones and rods, a developmentally regulated glycoprotein of interphotoreceptor matrix. J. Biol. Chem. 277, 25592–25600 (2002). doi:10.1074/jbc.M201279200

    Article  PubMed  CAS  Google Scholar 

  52. Bastmeyer, M., Schlosshauer, B., Stuermer, C.A.: The spatiotemporal distribution of N-CAM in the retinotectal pathway of adult goldfish detected by the monoclonal antibody D3. Development 108, 299–311 (1990)

    PubMed  CAS  Google Scholar 

  53. Yamamoto, A., Haraguchi, M., Yamashiro, S., Fukumoto, S., Furukawa, K., Takamiya, K., et al.: Heterogeneity in the expression pattern of two ganglioside synthase genes during mouse brain development. J. Neurochem. 66, 26–34 (1996)

    PubMed  CAS  Google Scholar 

  54. Yamamoto, A., Yamashiro, S., Fukumoto, S., Haraguchi, M., Atsuta, M., Shiku, H., et al.: Site restricted and neuron dominant expression of alpha 2,8sialyltransferase gene in the adult mouse brain and retina. Glycoconj. J. 13, 471–480 (1996). doi:10.1007/BF00731480

    Article  PubMed  CAS  Google Scholar 

  55. Luque, M.E., Crespo, P.M., Monaco, M.E., Aybar, M.J., Daniotti, J.L., Sanchez, S.S.: Cloning and functional characterization of two key enzymes of glycosphingolipid biosynthesis in the amphibian Xenopus laevis. Dev. Dyn. 237, 112–123 (2008). doi:10.1002/dvdy.21406

    Article  PubMed  CAS  Google Scholar 

  56. Sohn, H., Kim, Y.S., Kim, H.T., Kim, C.H., Cho, E.W., Kang, H.Y., et al.: 3 is involved in neuronal cell death. FASEB J. 20, 1248–1250 (2006). doi:10.1096/fj.05-4911fje

    Article  PubMed  CAS  Google Scholar 

  57. Holm, M., Mansson, J.E., Vanier, M.T., Svennerholm, L.: Gangliosides of human, bovine and rabbit retina. Biochim. Biophys. Acta 280, 356–364 (1972)

    PubMed  CAS  Google Scholar 

  58. Pujic, Z., Omori, Y., Tsujikawa, M., Thisse, B., Thisse, C., Malicki, J.: Reverse genetic analysis of neurogenesis in the zebrafish retina. Dev. Biol. 293, 330–347 (2006). doi:10.1016/j.ydbio.2005.12.056

    Article  PubMed  CAS  Google Scholar 

  59. Patel, R.Y., Balaji, P.V.: Identification of linkage-specific sequence motifs in sialyltransferases. Glycobiology 16, 108–116 (2006). doi:10.1093/glycob/cwj046

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by CNRS (Centre National de la Recherche Scientifique), by INSERM (Institut National de la Santé et de la Recherche Médicale), by the Hôpital Universitaire de Strasbourg, by ARC (Association pour la Recherche sur le Cancer), by the Ligue Nationale Contre le Cancer, by the European Commission as part of the ZF-Models integrated project in the 6th Framework Programme and the National Institute of Health (to C. Thisse and B. Thisse), by EGIDE and the Ministère des Affaires Etrangères (to L.-Y. Chang) and the PPF Bioinformatique de Lille (to A. Harduin-Lepers).

Author information

Authors and Affiliations

  1. Unité de Glycobiologie Structurale et Fonctionnelle (UGSF), Université des Sciences et Technologies de Lille, UMR CNRS 8576, IFR 147, 59655, Villeneuve d’Ascq, France

    Lan-Yi Chang, Anne-Marie Mir, Yann Guérardel, Philippe Delannoy & Anne Harduin-Lepers

  2. Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), UMR CNRS/INSERM/ULP 7104, 1, rue Laurent Fries, BP10142 67404, Illkirch cedex, France

    Christine Thisse & Bernard Thisse

  3. Institute of Biochemical Sciences, National Taiwan University, Taipei, 106, Taiwan

    Lan-Yi Chang

Authors
  1. Lan-Yi Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anne-Marie Mir
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christine Thisse
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yann Guérardel
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Philippe Delannoy
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bernard Thisse
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Anne Harduin-Lepers
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anne Harduin-Lepers.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chang, LY., Mir, AM., Thisse, C. et al. Molecular cloning and characterization of the expression pattern of the zebrafish α2, 8-sialyltransferases (ST8Sia) in the developing nervous system. Glycoconj J 26, 263–275 (2009). https://doi.org/10.1007/s10719-008-9165-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10719-008-9165-1

Keywords

Search

Navigation