Abstract
Glycosylation is one of the most important post-translational modifications and it is clear that the single step of β-1,4-galactosylation is performed by a family of β-1,4-galactosyltransferases (β4-GalTs) and that each member of this family may play a distinct role in different tissues and cells. In this study, we characterized the gene expression of six β4-GalTs in mouse testis and analyzed the changes of galactosylation of testis glycoproteins during postnatal development. Northern blot analysis revealed that β4-GalT-I and β4-GalT-IV were expressed mainly in newborn mouse testis and that the expression of β4-GalT-II increased markedly and persisted at the highest levels in adult mouse testis. The expression of β4-GalT-III and β4-GalT-V, however, remained relatively at low levels during mouse testicular development. In contrast, the expression of β4-GalT-VI was undetectable in mouse testis. The gene expression of β4-GalT-II in mouse testis was further analyzed by in situ hybridization due to its unique expression pattern. Strong hybridization signals were detected in the seminiferous tubules and the expression varied among the different stages of spermatogenic differentiation. The distinct gene expression patterns of β4-GalTs in mouse testis could affect the differential galactosylation of testis glycoproteins, as revealed by lectin histochemistry analysis.
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Trayer IP, Hill RL: The purification and properties of the A protein of lactose synthetase. J Biol Chem 246: 6666-6675, 1971
Fujita-Yamaguchi Y, Yoshida A: Purification and characterization of human serum galactosyltransferase (lactose synthetase A protein). J Biol Chem 256: 2701-2706, 1981
Lowe JB: Selectin ligands, leukocyte trafficking, and fucosyltransferase genes. Kidney Int 51: 1418-1426, 1997
Dell A, Morris HR, Easton RL, Patankar M, Clark GF: The glycobiology of gametes and fertilization. Biochim Biophys Acta 1473: 196-205, 1999
Shur BD, Evans S, Lu Q: Cell surface galactosyltransferase: Current issues. Glycocon J 15: 537-548, 1998
Begovac PC, Hall DE, Shur BD: Laminin fragment E8 mediates PC12 cell neurite outgrowth by binding to cell surface beta 1,4 galactosyl-transferase. J Cell Biol 113: 637-644, 1991
Shur BD: Is sperm galactosyltransferase a signaling subunit of a multimeric gamete receptor? Biochem Biophys Res Commun 250: 537-543, 1998
Asano M, Furukawa K, Kido M, Matsumoto S, Umesaki Y, Kochibe N, Iwakura Y: Growth retardation and early death of beta-1,4-galactosyltransferase knockout mice with augmented proliferation and abnormal differentiation of epithelial cells. EMBO J 16: 1850-1857, 1997
Lu Q, Hasty P, Shur BD: Targeted mutation in beta1,4-galactosyltransferase leads to pituitary insufficiency and neonatal lethality. Dev Biol 181: 257-267, 1997
NW Lo, JH Shaper, J Pevsner, Shaper NL: The expanding beta 4-galactosyltransferase gene family: Messages from the databanks. Glycobiology 8: 517-526, 1998
Almeida R, Amado M, David L, Levery SB, Holmes EH, Merkx G, van Kessel AG, Rygaard E, Hassan H, Bennett E, Clausen H: A family of human beta 4-galactosyltransferases. Cloning and expression of two novel UDP-galactose:beta-N-acetylglucosamine beta1, 4-galactosyltransferases, beta4Gal-T2 and beta4Gal-T3. J Biol Chem 272: 31979-31991, 1997
Amado M, Almeida R, Schwientek T, Clausen H: Identification and characterization of large galactosyltransferase gene families: Galactosyltransferases for all functions. Biochim Biophys Acta 1473: 35-53, 1999
Sato T, Furukawa K, Bakker H, Van den Eijnden DH, Van Die I: Molecular cloning of a human cDNA encoding beta-1,4-galactosyltransferase with 37% identity to mammalian UDP-Gal:GlcNAc beta-1,4-galactosyltransferase. Proc Natl Acad Sci USA 95: 472-477, 1998
Schwientek T, Almeida R, Levery SB, Holmes EH, Bennett E, Clausen H: Cloning of a novel member of the UDP-galactose: β-N-Acetylglucosamine β1,4-galactosyltransferase family, β4Gal-T4, involved in glycosphingolipid biosynthesis. J Biol Chem 273: 29331-29340, 1998
Nakamura N, Yamakawa N, Sato T, Tojo H, Tachi C, Furukawa K: Differential gene expression of beta-1,4-galactosyltransferases I, II and V during mouse brain development. J Neurochem 76: 29-38, 2001
Ertl C, Wrobel KH: Distribution of sugar residues in the bovine testis during postnatal ontogenesis demonstrated with lectin-horseradish peroxidase conjugates. Histochemistry 97: 161-171, 1992
Malmi R, Frojdman K, Soderstrom KO: Differentiation-related changes in the distribution of glycoconjugates in rat testis. Histochemistry 94: 387-395, 1990
Jones CJ, Morrison CA, Stoddart RW: Histochemical analysis of rat testicular glycoconjugates. 1. Subsets of N-linked saccharides in seminiferous tubules. Histochem J 24: 319-326, 1992
Jones CJ, Morrison CA, Stoddart RW: Histochemical analysis of rat testicular glycoconjugates. 2. Beta-galactosyl residues in O-and N-linked glycans in seminiferous tubules. Histochem J 24: 327-336, 1992
Jones CJ, Morrison CA, Stoddart RW: Histochemical analysis of rat testicular glycoconjugates. 3. Non-reducing terminal residues in seminiferous tubules. Histochem J 25: 711-718, 1993
Hennet T, Ellies LG: The remodeling of glycoconjugates in mice. Biochim Biophys Acta 1473: 123-136, 1999
Tulsiani DR, Skudlarek MD, Holland MK, Orgebin-Crist MC: Glycosylation of rat sperm plasma membrane during epididymal maturation. Biol Reprod 48: 417-428, 1993
Damjanov I: Biology of disease. Lectin cytochemistry and histochemistry. Lab Invest 57: 5-20, 1987
Baenziger JU, Fiete D: Structural determinants of Ricinus communis agglutinin and toxin specificity for oligosaccharides. J Biol Chem 254: 9795-9799, 1979
Lee M-C, Damjanov I: Lectin binging sites on human sperm and spermatogenetic cells. Anat Rec 212: 282-287, 1985
Zhou D, Chen C, Jiang S, Shen Z, Chi Z, Gu J: Expression of beta1,4-galactosyltransferase in the development of mouse brain. Biochim Biophys Acta 1425: 204-208, 1998
Nam SY, Fujisawa M, Kim JS, Kurohmaru M, Hayashi Y: Expression pattern of phospholipid hydroperoxide glutathione peroxidase messenger ribonucleic acid in mouse testis. Biol Reprod 58: 1272-1276, 1998
Russell LD, Ettlin RA, Sinha Hikim AP, Klegg ED: In: Histological and Histopathological Evaluation of the Testis. Cache River Press, Clearwater, FL, 1990, pp 119-161
Miller DJ, Macek MB, Shur BD: Complementarity between sperm surface beta-1,4-galactosyltransferase and egg-coat ZP3 mediates sperm-egg binding. Nature 357: 589-593, 1992
Lu Q, Shur BD: Sperm from beta 1,4-galactosyltransferase-null mice are refractory to ZP3-induced acrosome reactions and penetrate the zona pellucida poorly. Development 124: 4121-4131, 1997
Pratt SA, Shur BD: Beta-1,4-galactosyltransferase expression during spermatogenesis: Stage-specific regulation by t alleles and uniform distribution in +-spermatids and t-spermatids. Dev Biol 156: 80-93, 1993
Lopez LC, Youakim A, Evans SC, Shur BD: Evidence for a molecular distinction between Golgi and cell surface forms of beta 1,4-galactosyltransferase. J Biol Chem 266: 15984-15991, 1991
Pratt SA, Scully NF, Shur BD: Cell surface beta 1,4 galactosyltransferase on primary spermatocytes facilitates their initial adhesion to Sertoli cells in vitro. Biol Reprod 49: 470-482, 1993
Furukawa K, Sato T: Beta-1,4-galactosylation of N-glycans is a complex process. Biochim Biophys Acta 1473: 54-66, 1999
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Zhu, D., Shen, A., Sun, M. et al. Distinct patterns of expression of the β-1,4-galactosyltransferases during testicular development in the mouse. Mol Cell Biochem 247, 147–153 (2003). https://doi.org/10.1023/A:1024191829485
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DOI: https://doi.org/10.1023/A:1024191829485