Identification and expression analysis of Drosophila melanogaster genes encoding β-hexosaminidases of the sperm plasma membrane

Glycobiology

Volumn 16, Issue 9, 2006, Pages 786-800

  Cattaneo, F ^a   Intra, J ^a   Matsumoto, M ^b   Briani, F ^a   Hoshi, M ^b   Perotti, M E ^a,b  

^a UNIVERSITY OF MILAN   (Italy)

^b KEIO UNIVERSITY   (Japan)

Author keywords

fdl; Fertilization; Gamete interactions; Hexo2; Hexol

Indexed keywords

BETA N ACETYLHEXOSAMINIDASE; BETA N ACETYLHEXOSAMINIDASE A; BETA N ACETYLHEXOSAMINIDASE B; BETA N ACETYLHEXOSAMINIDASE B1; BETA N ACETYLHEXOSAMINIDASE B2; HETERODIMER; POLYPEPTIDE; UNCLASSIFIED DRUG;

ARTICLE; BETA CHAIN; CELL MEMBRANE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ENZYME ANALYSIS; ENZYME ASSAY; FEMALE; GENE EXPRESSION; GENE IDENTIFICATION; GENE LOCATION; GENE STRUCTURE; GENETIC CODE; GENOME ANALYSIS; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; IN VIVO STUDY; MALE; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; PREDICTION; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; SEQUENCE HOMOLOGY; SPERMATOZOON; TISSUE DISTRIBUTION;

AMINO ACID SEQUENCE; ANIMALS; BETA-N-ACETYLHEXOSAMINIDASE; CELL MEMBRANE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; MALE; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; SPERM-OVUM INTERACTIONS; SPERMATOZOA;

DROSOPHILA MELANOGASTER; HEXAPODA; INVERTEBRATA; MAMMALIA; VERTEBRATA;

EID: 33748703846     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwl007     Document Type: Article

References (47)

1. Altmann, F., Schwihla, H., Staudacher, E., Glossl, J., and Marz, L. (1995) Insect cells contain an unusual, membrane-bound β-N-acetylglucosaminidase probably involved in the processing of protein N-glycans. J. Biol. Chem., 2270, 17344-17349.
2. Andersson, S.V., Sjogren, E.C., Magnusson, C., and Gierow, J.P. (2005) Sequencing, expression and enzymatic characterization of β-hexosaminidase in rabbit lacrimal gland and primary cultured acinar cells. Glycobiology, 15, 211-220.
3. Andrews, J., Bouffard, G.G., Jining Lü, C.C., Becker, K.G., and Oliver, B. (2000) Gene discovery using computational and microarray analysis of transcription in the Drosophila melanogaster testis. Genome Res., 10, 2030-2043.
4. Beccari, T., Mancuso, F., Costanzi, E., Tassi, C., Barone, R., Fiumara, A., Orlacchio, A., Aisa, M.C., and Orlacchio, A. (2000) β-Hexosaminidases, α-D-mannosidase and β-mannosidase expression in serum from patients with carbohydrate-deficient glycoprotein syndrome type I. Clin. Chim. Acta, 302, 125-132.
5. Bendtsen, J.D., Jensen, L.J., Blom, N., von Heijne, G., and Brunak, S. (2004) Feature-based prediction of non-classical and leaderless protein secretion. Protein Eng., 17, 349-356.
6. Boquet, I., Hitier, R., Dumas, M., Chaminade, M., and Preat, T. (2000) Central brain postembryonic development in Drosophila: Implication of genes expressed at the interhemispheric junction. J. Neurobiol., 42, 33-48.
7. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72, 248-254.
8. Cattaneo, F., Ogiso, M., Hoshi, M., Perotti, M.E., and Pasini, M.E. (2002) Purification and characterization of the plasma membrane glycosidases, of Drosophila melanogaster spermatozoa. Insect Biochem. Mol. Biol., 32, 929-941.
9. Cooper, K.W. (1950) Normal spermatogenesis in Drosophila. In Demerec, M. (ed.), Biology of Drosophila. John Wiley & Sons Inc., New York, pp. 1-61.
10. Cordero, O.J., Merino, A., de la Cadena, M.P., Bugía, B., Nogueira, M., Viñuela, J.E., Martínez-Zorzano, V.S., de Carlos, A., and Rodríguez-Berrocal, F.J. (2001) Cell surface human α-L-fucosidase. Eur. J. Biochem. 268, 3321-3331.
11. De Bie, I., Savaria, D., Roebroek, A.J.M., Lazure, C., Van de Ven, W.J.M., and Seudah, N.G. (1995) Processing specificity and biosynthesis of the Drosophila melanogaster convertase dfurin1, dfurin1-CCR, dfurin1-x and dfurin2. J. Biol. Chem., 270, 1020-1028.
12. Dehò, G., Zangrossi, S., Sabbatini, P., Sironi, G., and Ghisotti, D. (1992) Bacteriophage P4 immunity controlled by small RNAs via transcription termination. Mol. Microbiol., 6, 3415-3425.
13. Del Pino, F.A.B., Brandelli, A., Termignoni, C., Gonzales, J.C., Henriques, J.A.P., and Dewes, H. (1999) Purification and characterization of β-N-acetylhexosaminidase from tick Boophilus microplus (Ixodide) larvae. Comp. Biochem. Physiol. B, 123, 193-200.
14. Dell, A., Morris, H.R., Easton, R.L., Patankar, M., and Clark, G.F. (1999) The glycobiology of gametes and fertilisation. Biochem. Biophys. Acta, 1473, 196-205.
15. Drysdale, R.A., Crosby, M.A., and The Flybase Consortium (2005) FlyBase: genes and gene models. Nucleic Acids Res., 33, D390-D395.
16. Eddy, E.M. (2002) Male germ cell gene expression. Recent Prog. Horm. Res., 57, 103-128.
17. Filho, B.P.D., Lermos, F.J.A., Secundino, N.F.C., Pascoa, V., Pereira, S.T., and Pimenta, P.F.P. (2002) Presence of chitinase and beta-N-acetylglucosaminidase in the Aedes aegypti A chitinolitic system involving peritrophic matrix formation and degradation. Insect Biochem. Mol. Biol., 32, 1723-1729.
18. Fleischer, B. (1994) CD26: A surface protease involved in T-cell activation. Immunol. Today, 15, 180-183.
19. Focarelli, R., La Sala, G.B., Balasini, M., and Rosati, F. (2001) Carbohydrate-mediated sperm-egg interaction and species specificity: A clue from the Unio elongatus model. Cells Tissues Organs, 168, 76-81.
20. Fuller, M.T. (1998) Genetic control of cell proliferation and differentiation in Drosophila spermatogenesis. Semin. Cell. Dev. Biol., 9, 433-444.
21. Gibson, K.R., Vanek, P.G., Kaloss, W.D., Collier, G.B., Connaughton, J.F., Angelichio, M., Livi, G.P., and Fleming, P.J. (1993) Expression of dopamine β-hydroxylase in Drosophila Schneider 2 cells. J. Biol. Chem., 268, 9490-9495.
22. Henrissat, B. and Bairoch, A. (1993) New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem. J., 293, 781-788.
23. Khunsook, S., Bean, B.S., McGowan, S.R., and Alhadeff, J.A. (2003) Purification and characterization of plasma membrane-associated human sperm α-L-fucosidase. Biol. Reprod., 68, 709-716.
24. Koyanagi, R. and Honegger, T.G. (2003) Molecular cloning and sequence analysis of an ascidian egg β-N-acetylhexosaminidase with a potential role in fertilization. Dev. Growth Differ., 45, 209-218.
25. Lehane, M.J. (1997) Peritrophic matrix structure and function. Annu. Rev. Entomol., 42, 525-550.
26. Leonard, R., Rendic, D., Rabouille, C., Wilson, I.B.H., Preat, T., and Altmann, F. (2006) The Drosophila fused lobes gene encodes an N-acetylglucosaminidase involved in N-glycan processing. J. Biol. Chem., 281, 4867-4875.
27. Mahuran, D.J. (1995) β-Hesosaminidase: Biosynthesis and processing of the normal enzyme, and identification of mutations causing Jewish Tay-Sachs disease. Clin. Biochem., 28, 101-106.
28. Marchini, D., Bertini, L.F., and Dallai, R. (1989) β-N-acetylhexosaminidases in the secretion of the female reproductive accessory glands of Ceratitis capitata (Diptera). Insect Biochem., 19, 549-555.
29. Mark, B.L., Mahuran, D.J., Cherney, M.M., Zhao, D., Knapp, S., and James, M.N.G. (2003) Crystal structure of human β-hexosaminidase B: understanding the molecular basis of Sandhoff and Tay-Sachs disease. J. Mol. Biol., 327, 1093-1109.
30. Martinez, M.L., Martelotto, L., and Cabda, M.O. (2000) Purification and biological characterization of N-acetyl-β-D-glucosaminidase from Bufo arenarum spermatozoa. Mol. Reprod. Dev., 57, 194-203.
31. Miranda, P.V., Gonzalez-Echeverria, V., Blaquier, J.A., Mahuran, D.J., and Tezon, J.G. (2000) Evidence for the participation of β-hexosaminidase in human sperm-zona pellucida interaction in vitro. Mol. Hum. Reprod., 6, 699-706.
32. Olivari, S., Galli, C., Alanen, H., Ruddock, L., and Molinari, M. (2005) A novel stress-induce EDEM variant regulating endoplasmic reticulum-associated glycoprotein degradation. J. Biol. Chem., 280, 2424-2428.
33. Perotti, M.E., Cattaneo, F., Pasini, M.E., Verni, F., and Hackstein, J.H.P. (2001) Male sterile mutant casanova gives clues to mechanisms of sperm-egg interactions in Drosophila melanogaster. Mol. Reprod. Dev., 60, 248-259.
34. Perotti, M.E. and Pasini, M.E. (1995) Glycoconjugates of the surface of the spermatozoa of Drosophila melanogaster: A qualitative and quantitative study. J. Exp. Zool., 271, 311-318.
35. Prag, G., Papanikolau, Y., Tavlas, G., Vorgias, C.E., Petratos, K., and Oppenheim, A.B. (2000) Structures of chitobiase mutants complexed with the substrate di-N-acetyl-D-glucosamine: The catalytic role of the conserved acidic pair, Aspartate 539 and Glutamate 540. J. Mol. Biol., 300, 611-617.
36. Proia, R.L., d'Azzo, A., and Neufeld, E. F. (1984) Association of α and β-subunits during the biosynthesis of β-hexosaminidase in cultured human fibroblasts. J. Biol. Chem., 259, 3350-3354.
37. Rodeheffer, C. and Shur, B.D. (2002) Targeted mutations in β1,4-galactosyltransferase I reveals its multiple cellular functions. Biochim. Biophys. Acta, 1573, 258-270.
38. c cells. Arch. Insect Biochem. Physiol., 17, 3-13.
39. c cells. Arch. Insect Biochem. Physiol., 18, 45-53.
40. Stapleton, M., Carlson, J., Borkstein, P., Yu, C., Champe, M., George, R., Guarin, H., Kronmiller, B., Pacleb, J., Park, S., and others (2002) A Drosophila full-length cDNA resource. Genome Biol., 3, 0080.1-0080.8.
41. Talbot, P., Shur, B.D., and Myles, D.G. (2003) Cell adhesion and fertilization: Steps in oocyte transport, sperm-zona pellucida interactions, and sperm-egg fusion. Biol. Reprod., 68, 1-9.
42. Thomas, G. (2002) Furin at the cutting edge: From protein traffic to embryogenesis and disease. Nat. Rev. Mol. Cell Biol., 3, 753-766.
43. 2-terminal, non-hydrophobic motif targets a male germ cell-specific hexokinase to the endoplasmic reticulum and plasma membrane. J. Biol. Chem., 274, 34467-34475.
44. Tulsiani, D.R.P. (2003) Glycan modifying enzymes in the luminal fluid of rat epididymis: Are they involved in altering sperm surface glycoproteins during maturation? Microsc. Res. Tech., 61, 1827.
45. Tulsiani, D.R.P. and Abou-Haila, A. (2001) Mammalian sperm molecules that are potentially important in interaction with female genital tract and egg vestments. Zygote, 9, 51-69.
46. Vo, L.H., Yen, T.Y., Macher, B.A., and Hedrick, J.L. (2003) Identification of the ZPC oligosaccharide ligand involved in sperm binding and the glycan structures of Xenopus laevis vitelline envelope glycoproteins. Biol. Reprod., 69, 1822-1830.
47. White-Cooper, H., Schaefer, M.A., Alphey, L.S., and Fuller, M.T. (1998) Transcriptional and post-transcriptional control mechanisms coordinate the onset of spermatid differentiation with meiosis I in Drosophila. Development, 125, 125-134.