Cell Surface β1,4-Galactosyltransferase

A Signal Transducing Receptor?
  • Daniel H. Dubois
  • Barry D. Shur
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 376)

Abstract

The carbohydrate components of membrane-bound and secreted glycoproteins are composed of a variety of simple and complex oligosaccharides that directly influence protein structure, intracellular targeting, biological activity, half-life, and/or specificity of action (1, 2). The enzymes responsible for the biosynthesis of these oligosaccharide chains are the glycosyltransferases, which demonstrate exquisite specificity by recognizing specific glycoside structures on maturing proteins and lipids. It is generally thought that each glycosyl-transferase is responsible for catalyzing one specific glycosidic linkage. From the variety of known carbohydrate linkages, it is speculated that there are more than 100 glycosyltransferases (3), only a few of which have been cloned and well characterized (4, 5).

Keywords

Carbohydrate Retina Compaction Glucocorticoid Integrin 

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References

  1. 1.
    Krag SS. Mechanisms and functional role of glycosylation in membrane protein synthesis. In: Current Topics in Membranes and Transport. Vol 21, Academic Press, Inc. 1985:181–249.Google Scholar
  2. 2.
    Varki A. Biological roles of oligosaccharides: all of the theories are correct. Glycobiology 1993;3:97–130.PubMedCrossRefGoogle Scholar
  3. 3.
    Beyer TA, Hill RL. Glycosylation pathway in the biosynthesis of nonreducing terminal sequences in oligosaccharides of glycoproteins. In: The Glycoconjugates (Horowitz, M., ed.), Vol III, 1982:25–45, Academic Press, New York.Google Scholar
  4. 4.
    Paulson JC, Colley KJ. Glycosyltransferases. J. Biol. Chem. 1989;264:17615–17618.PubMedGoogle Scholar
  5. 5.
    Lowe JB. Molecular cloning, expression, and uses of mammalian glycosyltransferases. Seminars in Cell Biol. 1991;2:289–307.Google Scholar
  6. 6.
    Roth J, Berger EG. Immunocytochemical localization of galactosyltransferase in HeLa cells: codistribution with thiamine pyrophosphate in trans Golgi cisternal. J. Cell Biol. 1982;93:223–229.PubMedCrossRefGoogle Scholar
  7. 7.
    Hollis GF, Douglas JG, Shaper JG, Shaper JH, Stafford-Hollis JM, Evans, RJ, Kirsh IR. Genomic structure of murine β1,4-galactosyltransferase. Biochem. Biophys. Res. Commun. 1989;162:1069–1075.PubMedCrossRefGoogle Scholar
  8. 8.
    Narimatsu H, Sinha S, Brew K, Okayama H, Qasba PK. Cloning and sequencing of cDNA of bovine N-acetylglucosamine (β1,4) galactosyltransferase. Proc. Natl. Acad. Sci. USA 1986;83:4720–4724.PubMedCrossRefGoogle Scholar
  9. 9.
    Appert HE, Rutherford TJ, Tarr GE, Wiest JS, Thomford NR, McCorgguodale DJ. Isolation of a complementary DNA coding for human galactosyltransferase. Biochem. Biophys. Res. Comm. 1986;139:163–168.PubMedCrossRefGoogle Scholar
  10. 10.
    Shaper NL, Hollis GF, Douglas JG, Kirsh ER, Shaper JH. Characterization of the full length cDNA for murine β1,4-galactosyltransferase. J. Biol. Chem. 1988;263:10420–10428.PubMedGoogle Scholar
  11. 11.
    Russo RN, Shaper NL, Shaper JH. Bovine β1,4-galactosyltransferase: two sets of mRNA transcripts encode two forms of the protein with different amino-terminal domains. J. Biol. Chem. 1990;265:3324–3331.PubMedGoogle Scholar
  12. 12.
    Russo RN, Shaper NL, Taatjes DJ, Shaper JG. β1,4-galactosyltransferase: a short NH2 terminal fragment that includes the cytoplasmic and transmembrane domain is sufficient for Golgi retention. J. Biol. Chem. 1992;267:9241–9247.PubMedGoogle Scholar
  13. 13.
    Teasdale RD, D’Agostaro G, Gleeson PA. The signal for Golgi retention of bovine β1,4-galactosyltransferase is in the transmembrane domain. J. Biol. Chem. 1992;267:4084–4096.PubMedGoogle Scholar
  14. 14.
    Masibay AS, Balaji PV, Boeggeman EE, Qasba PK. Mutational analysis of the golgi retention signal of bovine β1,4-galactosyltransferase. J. Biol. Chem. 1993;268:9908–9916.PubMedGoogle Scholar
  15. 15.
    Harduin-Lepers A, Shaper JH, Shaper NL. Characterization of two cis-regulatory regions in the murine β1,4-galactosyltransferase gene. J. Biol. Chem. 1993;268:14348–14359.PubMedGoogle Scholar
  16. 16.
    Shaper NL, Wright WW, Shaper JH, Murine β1,4-galactosyltransferase: both amounts and structure of the mRNA are regulated during spermatogenesis. Proc. Natl. Acad. Sci. USA 1990;87:791–795.PubMedCrossRefGoogle Scholar
  17. 17.
    Lopez LC, Maillet C, Oleszkowicz K, Shur B.D. Cell-surface and Golgi pools of β1,4-galactosyltransferase are differentially regulated during embryonal carcinoma cell differentiation. Mol. Cell. Biol. 1989;9:2370–2377.PubMedGoogle Scholar
  18. 18.
    Lopez LC, Youakim A, Evans SC, Shur BD. Evidence for a molecular distinction between Golgi and cell surface forms of β1,4-galactosyltransferase. J. Biol. Chem. 1991;266:15984–15991.PubMedGoogle Scholar
  19. 19.
    Roseman S. The synthesis of complex carbohydrates by multiglycosyltransferase systems and their potential function in intercellular adhesion. Chem. Phys. Lipids 1971;5:270–297.CrossRefGoogle Scholar
  20. 20.
    Roth S, White D. Intercellular contact and cell-surface galactosyltransferase activity. Proc. Natl. Acad. Sci. USA 1972;69:485–489.PubMedCrossRefGoogle Scholar
  21. 21.
    Shur BD. β1,4-Galactosyltransferase: twenty years later. Glycobiology 1991;1:563–575.PubMedCrossRefGoogle Scholar
  22. 22.
    Shur BD. Expression and function of cell surface galactosyltransferase. Biochem. Biophys. Acta 988:389–409.Google Scholar
  23. 23.
    Shur BD. (1993). Glycosyltransferases as cell adhesion molecules. Curr. Opin. Cell Biol. 1993;5:854–863.PubMedCrossRefGoogle Scholar
  24. 24.
    Cooke SV, Shur BS. Cell Surface β1,4-galactosyltransferase: expression and function. Develop. Growth and Differ. 1994;36:125–132.CrossRefGoogle Scholar
  25. 25.
    Bayna EM, Shaper JH, Shur BD. Temporally specific involvement of cell surface galactosyltransferase during mouse embryo morula compaction. Cell. 1988;53:145–157.PubMedCrossRefGoogle Scholar
  26. 26.
    Shur BD, Neely CA. Plasma membrane association, purification and characterization of mouse sperm β1,4-galactosyltransferase. J. Biol. Chem. 1988;263:17706–17714.PubMedGoogle Scholar
  27. 27.
    Cumming RD, Cebula TA, Roth S. Characterization of a galactosyltransferase in plasma membrane-enriched fractions from Balb/c 3T12 cells. J. Biol. Chem. 1979;254:1233–1240.Google Scholar
  28. 28.
    Eckstein DJ, Shur BD. Laminin induces the expression of cell surface galactosyltransferase to lamellipodia on migrating cells. J. Cell Biol. 1989;108:2507–2517.PubMedCrossRefGoogle Scholar
  29. 29.
    Lopez LC, Shur BD. Redistribution of the mouse egg receptor on sperm following the acrosome reaction. J. Cell Biol. 1987;105:1663–1670.PubMedCrossRefGoogle Scholar
  30. 30.
    Youakim A, Dubois DH, Shur BD. Localization of the long form of β1,4-galactosyltransferase to the plasma membrane and Golgi complex of 3T3 and F9 cells by immunofluorescence confocal microscopy. Proc. Natl. Acad. Sci. USA 1994; in pressGoogle Scholar
  31. 31.
    Evans S, Lopez LC, Shur BD. Dominant negative mutation in cell surface β1,4-galactosyl-transferase inhibits cell-cell and cell-matrix interactions. J. Cell Biol. 1993;120:1045–1057.PubMedCrossRefGoogle Scholar
  32. 32.
    Appeddu PA, Shur BD. Molecular analysis of cell surface β1,4-galactosyltransferase function during cell migration. Proc. Natl. Acad. Sci. USA 1993; 91:2095–2099.CrossRefGoogle Scholar
  33. 33.
    Begovac PC, Hall D, Shur BD. Laminin fragment E8 mediates PC12 cell neurite outgrowth by binding to cell surface β1,4-galactosyltransferase. J. Cell Biol. 1991;113:637–644.PubMedCrossRefGoogle Scholar
  34. 34.
    Runyan RB, Versalovic J, Shur BD. Functionally distinct laminin receptors mediate cell adhesion and spreading: the requirement for surface galactosyltransferase in cell spreading. J. Cell Biol. 1988;107:1863–1871.PubMedCrossRefGoogle Scholar
  35. 35.
    Huang Q, Shur BD, Begovac PC. Overexpressing cell surface β1,4-galactosyltransferase increases neurite formation from PC12 cells on laminin. J. Cell Sci., in pressGoogle Scholar
  36. 36.
    Bleil JD, Wasserman PM. Identification of a ZP3-binding protein on acrosome-intact mouse sperm by photoaffmity cross linking. Proc. Nat. Acad. Sci. USA 1990;87:5563–5567,CrossRefGoogle Scholar
  37. 37.
    Florman H, Wasserman PM. O-linked oligosaccharides of mouse egg ZP3 account for its sperm receptor activity. Cell 1985;41:313–324.PubMedCrossRefGoogle Scholar
  38. 38.
    Shur BD, Hall NG. A role for mouse sperm surface galactosyltransferase in sperm binding to the egg zona pellucida. J. Cell Biol. 1982;95:1501–1510.Google Scholar
  39. 39.
    Lopez LC, Bayna EM, Litoff D, Shaper NL, Shaper JH, Shur BD. The receptor function of mouse sperm surface galactosyltransferase during fertilization. J. Cell Biol. 1985;101:1501–1510.PubMedCrossRefGoogle Scholar
  40. 40.
    Miller DJ, Macek MB, Shur BD. Complementarity between sperm surface β1,4-galactosyltransferase and egg coat ZP3 mediates sperm-egg binding. Nature 1992;357:589–593.PubMedCrossRefGoogle Scholar
  41. 41.
    O’Tool TE, Kasuhiro Y, Faull RJ, Peter K, Tamura R, Quaranta V, Loftus JC, Shatill SJ, Ginsberg MH. Integrin cytoplasmic domains mediate inside-out signal transduction. J. Cell Biol. 1994;124:1047–1059.CrossRefGoogle Scholar
  42. 42.
    Youakim A, Hathaway HJ, Miller DJ, Gong X, Shur BD. Overexpressing sperm surface β1,4-galactosyltransferase in transgenic mice affects multiple aspects of sperm-egg interactions. J. Cell Biol. 1994;126:1573–1583.PubMedCrossRefGoogle Scholar
  43. 43.
    Roth S, McGuire EJ, Roseman S. Evidence for cell surface glycosyltransferases: their potential role in cellular recognition. J. Cell Biol. 1971;51:536–547.PubMedCrossRefGoogle Scholar
  44. 44.
    Dutt A, Tang JP, Carson DD. Lactosaminoglycans are involved in uterine epithelial cell adhesion in vitro. Dev.Biol. 1987;119:27–37.PubMedCrossRefGoogle Scholar
  45. 45.
    Maillet C, Shur BD. Uvomorulin, LAMP-1, and laminin are substrates for cell-surface β1,4-galactosyltransferase on F9 embryonal carcinoma cells: comparison between wild-type and mutant 5.51 art-cells. Exp. Cell Res. 1993;208:282–295.PubMedCrossRefGoogle Scholar
  46. 46.
    Barcellos-Hoff MH. Mammary epithelial reorganization on extracellular matrix is mediated by cell-surface galactosyltransferase. Exp. Cell Res. 1992;201:225–234.PubMedCrossRefGoogle Scholar
  47. 47.
    Pratt SA, Scully NF, Shur BD. Cell surface β1,4-galactosyltransferase on primary spermatocytes facilitates their initial adhesion to Sertoli cells in vitro. Biol. Reprod. 1993;49:470–482.PubMedCrossRefGoogle Scholar
  48. 48.
    Bennett V. Ankrins. Biol. Chem. 1992;13:8703–8706.Google Scholar
  49. 49.
    Newman PJ, Hillery CA, Albrecht R, Parise LV, Berndt MC, Mazurov AV, Dunlop LC, Zhang J, Rittenhouse SF. Activation-dependent changes in human platelet PECAM-1: phosphorylation, cytoskeletal association, and surface membrane redistribution. J. Cell Biol. 1992;1:239–246.CrossRefGoogle Scholar
  50. 50.
    Horwitz A, Duggan K, Buck C, Beckerle MC, Burridge K. Interaction of plasma membrane fibronectin receptor with talin-A transmembrane linkage. Nature 1986;320:531–533.PubMedCrossRefGoogle Scholar
  51. 51.
    Hagman J, Burger MM. Phosphorylation of vinculin in human platelets spreading on a solid surface. J. Cell. Biochem. 1992;50:237–244.CrossRefGoogle Scholar
  52. 52.
    Hynes RO.Integrins:versatility, modulation and signaling in cell adhesion. Cell. 1992;69:11–25.PubMedCrossRefGoogle Scholar
  53. 53.
    Sastry KS, Horwitz AF. Integrin cytoplasmic domains: mediators of cytoskeletal linkages and extra-and intracellular initiated transmembrane signaling. Curr. Opin. Cell Biol. 1993;5:819–831.PubMedCrossRefGoogle Scholar
  54. 54.
    Eckstein DJ, Shur BD. Cell surface β1,4-galactosyltransferase is associated with the detergent-insoluble cytoskeleton on migrating mesenchymal cells. Exp. Cell Res. 1992;201:83–90.PubMedCrossRefGoogle Scholar
  55. 55.
    Juliano RL, Varner JA. Adhesion molecules in cancer: the role of integrins. Curr. Opin. Cell Biol. 1993;5:812–818.PubMedCrossRefGoogle Scholar
  56. 56.
    Hirano S, Kimoto N, Shimoyama Y, Hiroshashi S, Takeichi M. Identification of a neural α-catenin as a key regulator of Cadherin function and multicellular organization. Cell 1992;70:293–301.PubMedCrossRefGoogle Scholar
  57. 57.
    Doherty P, Rowett LH, Moore SE, Mann DA, Walsh FS. Neurite outgrowth in response to transfected NCAM and N-cadherin reveals fundamental differences in neuronal responsiveness to CAMs. Neuron. 1991;6:247–258.PubMedCrossRefGoogle Scholar
  58. 58.
    Safell JL, Walsh FS, Doherty P. Direct activation of second messenger pathways mimics cell adhesion molecule-dependent neurite outgrowth. J. Cell Biol. 1992;118:663–670.CrossRefGoogle Scholar
  59. 59.
    McClay DR, Ettensohn CA. Cell adhesion in morphogenesis. Arm. Rev. Cell Biol. 1987;3:319–345.CrossRefGoogle Scholar
  60. 60.
    Guan J, Shalloway D. Regulation of focal adhesion-associated protein tyrosine kinase by both cellular adhesion and oncogenic transformation. Nature 1992;358:690–692.PubMedCrossRefGoogle Scholar
  61. 61.
    Macek MB, Lopez LC, Shur BD. Aggregation of β1,4-galactosyltransferase on mouse sperm induces the acrosome reaction. Devel. Biol. 1991;147:440–444.CrossRefGoogle Scholar
  62. 62.
    Ward CR, Storey BT, Kopf GS. Activation of a Gi protein in mouse sperm membranes by solubilized proteins of the zona pellucida, the egg’s extracellular matrix. J. Biol. Chem. 992;267:14061–14067.PubMedGoogle Scholar
  63. 63.
    Podolsky DK, Weiser MM, Isselbacher KJ. Inhibition of growth of transformed cells and tumors by an endogenous acceptor of galactosyltransferase. Proc. Natl. Acad. Sci.USA 1978;75:4426–4430.PubMedCrossRefGoogle Scholar
  64. 64.
    Pernio MB, Passaniti A, Fridman R, Hart GW, Jordan C, Kumar S, Scott AF. In vitro galactosylation of a 110-Kda glycoprotein by an endogenous cell-surface galactosyltransferase correlates with the invasiveness of adrenal carcinoma cells. Proc. Natl. Acad. Sci. USA 1989;86:6057–6061.CrossRefGoogle Scholar
  65. 65.
    Passaniti A, Hart GW. Metastasis-associated murine melanoma cell-surface galactosyltransferase: characterization of enzyme activity and identification of the major surface substrates. Cancer Res. 1990;50:7261–7271.PubMedGoogle Scholar
  66. 66.
    Uemura M, Sakaguchi T, Uejima T, Nozawa S, Narimatsu H. Mouse monoclonal antibodies which recognize a human (β1–4)Galactosyltransferase associated with tumor in body fluids. Cancer Res. 1992;52:6153–6157.PubMedGoogle Scholar
  67. 67.
    Humphreys-Beyer MG, Schneyer CA, Kidd VJ, Marchase RB. Isoproteranol-mediated parotid gland hypertrophy is inhibited by effectors of β-galactosyltransferase. J. Biol. Chem. 1987;262:11706–11713.Google Scholar
  68. 68.
    Bunnel B, Humphreys-Beyer MG, Kidd VJ. In: Advances in Gene Technology: The Molecular Biology of Development, Nineteenth Miami Winter Symposium ICSU Short Reports (Voellmy, R.W. et al., eds) 1987;7:122.Google Scholar
  69. 69.
    Purushotham KR, Bologna J, Nakagawa Y, Humphreys-Beher MG. Isolation and characterization of a new Ca2+/calmodulin-dependent protein kinase from isoproterenol-stimulated proliferating rat parotid acinar cells. Biochem. Cell. Biol. 1992;70:250–255.PubMedCrossRefGoogle Scholar
  70. 70.
    Strous GJ, van Kerkhof P, Fallon RJ, Schwartz AL. Golgi galactosyltransferase contains serine-linked phosphate. Eur. J. Biochem. 1987;169:307–311.PubMedCrossRefGoogle Scholar
  71. 71.
    Camp RL, Kraus TA, Pure’E. Variations in the cytoskeletal interaction and posttranslational modification of the CD44 homing receptor in marcrophages. J. Cell Biol. 1991;115:1283–1292.PubMedCrossRefGoogle Scholar
  72. 72.
    Bunnell BA, Adams DE, Kidd VJ. Transient expression of a p58 protein kinase cDNA enhances mammalian glycosyltransferase activity. Biochem. Biophys. Res. Comm. 1990;171:196–203.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1995

Authors and Affiliations

  • Daniel H. Dubois
    • 1
  • Barry D. Shur
    • 1
  1. 1.Department of Biochemistry and Molecular BiologyUniversity of Texas, M. D. Anderson Cancer CenterHoustonUSA

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