Neurochemical Research

, Volume 27, Issue 7–8, pp 649–663 | Cite as

Recent Development in Mammalian Sialidase Molecular Biology

  • Eugenio Monti
  • Augusto Preti
  • Bruno Venerando
  • Giuseppe Borsani

Abstract

This review summarizes the recent research development on mammalian sialidase molecular cloning. Sialic acid–containing compounds are involved in several physiological processes, and sialidases, as glycohydrolytic enzymes that remove sialic acid residues, play a pivotal role as well. Sialidases hydrolyze the nonreducing, terminal sialic acid linkage in various natural substrates, such as glycoproteins, glycolipids, gangliosides, and polysaccharides. Mammalian sialidases are present in several tissues/organs and cells with a typical subcellular distribution: they are the lysosomal, the cytosolic, and the plasma membrane–associated sialidases. Starting in 1993, 12 different mammalian sialidases have been cloned and sequenced. A comparison of their amino acid sequences revealed the presence of highly conserved regions. These conserved regions are shared with viral and microbial sialidases that have been characterized at three-dimensional structural level, allowing us to perform the molecular modeling of the mammalian proteins and suggesting a monophyletic origin of the sialidase enzymes. Overall, the availability of the cDNA species encoding mammalian sialidases is an important step leading toward a comprehensive picture of the relationships between the structure and biological function of these enzymes.

Mammalian sialidase molecular cloning gene structure and expression molecular properties transgenic expression 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

REFERENCES

  1. 1.
    Saito, N. and Yu, R. K. 1995. Biochemistry and function of sialidases. Pages 261-313 in Rosemberg, A. (ed.), Biology of Sialic Acids, Plenum Press, New York and London.Google Scholar
  2. 2.
    Gubareva, L. V., Kaiser, L., and Hayden, F. G. 2000. Influenza virus neuraminidase inhibitors. Lancet, 355:827-835.Google Scholar
  3. 3.
    Thomas, G. H. 2001. Disorders of glycoprotein degradetion: α-mannosidosis, β-mannosidosis, fucosidosis and sialidosis. Pages 3507-3534, in Scriver, C. R., Beaudet, A. L., Sly, W. S., and Valle, D. (eds.), The Metabolic and Molecular Bases of Inherited Disease, vol III, 8th ed., McGraw-Hill, New York.Google Scholar
  4. 4.
    D'Azzo, A., Andria, G., Strisciuglio, P., and Galjaard, H. 2001. Galactosialidosis. Pages 3811-3826, in Scriver, C. R., Beaudet, A. L., Sly, W. S., and Valle, D. (eds.), The Metabolic and Molecular Bases of Inherited Disease, vol III, 8th ed., McGraw-Hill, New York.Google Scholar
  5. 5.
    Achyuthan, K. E. and Achyuthan, A. M. 2001. Comparative enzymology, biochemistry and pathophysiology of human exo-asialidases (neuraminidases). Comp. Biochem. Physiol. Part B, 129:29-64.Google Scholar
  6. 6.
    Miyagi, T., Konno, K., Emori, Y., Kawasaki, H., Suzuki, K., Yasui, A., and Tsuik, S. 1993. Molecular cloning and expression of cDNA encoding rat skeletal muscle cytosolic sialidase. J. Biol. Chem., 268:26435-26440.Google Scholar
  7. 7.
    Roggentin, P., Rothe, B., Kaper, J., Galen, J., Lawrisuk, L., Vimr, E., and Schauer, R. 1989. Conserved sequences in bacterial and viral sialidases. Glycoconj. J., 6:349-353.Google Scholar
  8. 8.
    Ferrari, J., Harris, R., and Warner, T. G. 1994. Cloning and expression of a soluble sialidase from Chinese hamster ovary cells: Sequence alignment similarities to bacterial sialidases. Glycobiology, 4:367-373.Google Scholar
  9. 9.
    Potier, M., Yan, D., and Womack, J. 1979. Neuraminidase deficiency in the mouse. FEBS Lett. 108:345-348.Google Scholar
  10. 10.
    Womack, J., Yan, D., and Potier, M. 1981. Gene for neuraminidase activity on mouse chromosome 17 near H-2: Pleiotropic effect on multiple hydrolases. Science 212:63-65.Google Scholar
  11. 11.
    Samollow, P., VandeBerg, J., Ford, A., Douglas, T., and David, C. 1986. Electrophoretic analysis of liver neuraminidase-1 variation in mice and additional evidence concerning the location of NEU-1. J. Immunogenet. 13:29-39.Google Scholar
  12. 12.
    Harada, F., Nishimura, Y., Suzuki, K., Matsumoto, H., Oohira, T., Matsuda, I., and Sasazuki, T. 1987. The patient with combined deficiency of neuraminidase and 21-hydroxylase. Hum. Genet. 75:91-92.Google Scholar
  13. 13.
    Campbell, R. D. and Trowsdale, J. 1993. Map of the human MHC. Immunol Today. 14:349-352.Google Scholar
  14. 14.
    Milner, C., Smith, S., Carrillo, M., Taylor, G., Hollinshead, M., and Campbell, R. 1997. Identification of a sialidase encoded in the human major histocompatibility complex. J. Biol. Chem. 272:4549-4558.Google Scholar
  15. 15.
    Bonten, E., van der Spoel, A., Fornerod, M., Grosveld, G., and d'Azzo, A. 1996. Characterization of human lysosomal neuraminidase defines the molecular basis of the metabolic storage disorder sialidosis. Genes Dev. 10:3156-3169.Google Scholar
  16. 16.
    Pshezhetsky, A., Richard, C., Michaud, L., Igdoura, S., Wang, S., Elsliger, M., Qu, J., Leclerc, D., Gravel, R., Dallaire, L., and Potier, M. 1997. Cloning, expression and chromosomal mapping of human lysosomal sialidase and characterization of mutations in sialidosis. Nat. Genet. 15:316-320.Google Scholar
  17. 17.
    Boguski, M. S. and Schuler, G. D. 1995. ESTablishing a human transcript map. Nat. Genet. 10:369-373.Google Scholar
  18. 18.
    Carrillo, M. B., Milner, C. M., Ball, S. T., Snoek, M., and Campbell, R. D. 1997. Glycobiology 7:975.Google Scholar
  19. 19.
    Igdoura, S. A., Gafuik, C., Mertineit, C., Saberi, F., Pshezhetsky, A., Potier, M., Trasler, J., and Gravel, R. 1998. Cloning of the cDNA and gene encoding mouse lysososmal sialidase and correction of sialidase deficiency in human sialidosis and mouse SM/J fibroblasts. Hum. Mol. Genet. 7:115-121.Google Scholar
  20. 20.
    Rottier, R., Bonten, E., and d'Azzo, A. 1998. A point mutation in the neu-1 locus causes the neuraminidase defect in the SM/J mouse. Hum. Mol. Genet. 7:313-321.Google Scholar
  21. 21.
    Monti, E., Preti, A., Rossi, E., Ballabio, A., and Borsani, G. 1999. Cloning and characterization of NEU2, a human gene homologous to rodent soluble sialidases. Genomics 57:137-143.Google Scholar
  22. 22.
    Monti, E., Preti, A., Nesti, C., Ballabio, A., and Borsani, G. 1999. Expression of a novel human sialidase encoded by the NEU2 gene. Glycobiology 9:1313-1321.Google Scholar
  23. 23.
    Hata, K., Wada, T., Hasegawa, A., Kiso, M., and Miyagi, T. 1998. J. Biochem. 248:527-544.Google Scholar
  24. 24.
    Miyagi, T. Wada, T., Iwamatsu, A., Hata, K., Yoshikawa, Y., Tokuyama, S., and Sawada, M. 1999. Molecular cloning and characterization of a plasma membrane-associated sialidase specific for gangliosides. J. Biol. Chem. 274:5004-5011.Google Scholar
  25. 25.
    Wada, T., Yoshikawa, Y., Tokuyama, S., Kuwabara, M., Akida, H., and Miyagi, T. 1999. Cloning, expression, and chromosomal mapping od a human ganglioside sialidase. Biochem. Biophys. Res. Commun. 261:21-27.Google Scholar
  26. 26.
    Monti, E., Bassi, M. T., Papini, N., Riboni, M., Manzoni, M., Venerando, B., Croci, G. L., Preti, A., Ballabio, A., Tettamanti, G., and Borsani, G. 2000. Identification and expression of NEU3, a novel human sialidase associated to the plasma membrane. Biochem. J. 349:343-351.Google Scholar
  27. 27.
    Fronda, C. L., Zeng, G., Gao, L., and Yu, R. K. 1999, Molecular cloning and expression of mouse brain sialidase. Biochem. Biophys. Res. Commun. 258:727-731.Google Scholar
  28. 28.
    Hasegawa, T., Yamaghchi, K., Wada, T., Takeda, A., Itoyama, Y., and Miyagi, T. 2000. Molecular cloning of mause ganglioside sialidase and its increased expression in Neuro2a cell differentiation. J. Biol. Chem. 275:8007-8015.Google Scholar
  29. 29.
    Hasegawa, T., Feijoo Carnero, C., Wada, T., Itoyama, Y., and Miyagi, T. 2001. Differential expression of three sialidase genes in rat development. Biochem. Biophys. Res. Commun. 280:726-732.Google Scholar
  30. 30.
    Miyagi, T., Wada, T., and Yamaguchi, K. 1999. Multiple forms of mammalian sialidase and their altered expression in physiological and pathological conditions. Pages 197-205, in Inoue, Y., Lee, Y. C., and Troy, F. A., II (eds.), Sialobiology and Other Novel Forms of Glycosylation. Gagushin Publishing Co.Google Scholar
  31. 31.
    Sato, K. and Miyagi, T. 1995. Genomic organization and the 58-upstream sequence of the rat cytosolic sialidase gene. Glycobiology 5:511-516.Google Scholar
  32. 32.
    Murre, C., McCaw, P. S., and Baltimore, D. 1989. A new DNA binding and dimerization motif in immunoglobulin enhancer binding, duaghterless, myoD, and Myc proteins. Cell 56:777-784.Google Scholar
  33. 33.
    Crennell, S. J., Garman, E. F., Laver, W. G., Vimr, E. R., and Taylor, G. L. (1993) Crystal structure of a bacterial sialidase (from Salmonella typhimurium LT2) shows the same fold as an influenza virus neuraminidase. Proc. Natl. Acad. Sci. U.S.A. 90:9852-9856.Google Scholar
  34. 34.
    Hoyer, L. L., Hamilton, A. C., Steenbergen, S. M., and Vimr, E. R. 1992. Cloning, sequencing and distribution of the Salmonella typhimurium LT2 sialidase gene, nanH, provides evidence for interspecies gene transfer. Mol. Microbiol. 6:873-874.Google Scholar
  35. 35.
    Wang, Y., Yamaguchi, K., Shimada, Y., Zhao, X., and Miyagi, T. 2001. Site-directed mutagenesis of human membrane-associated ganglioside sialidase: Identification of amino-acid residues contributing to substrate specificity. Eur. J. Biochem. 268:2201-2208.Google Scholar
  36. 36.
    Burmeister, W. P., Henrissat, B., Bosso, C., Cusack, S., and Ruigrok, R. W. 1993. Influenza B virus neuraminidase can synthesize its own inhibitor. Structure 1:19-26.Google Scholar
  37. 37.
    Roggetin, T., et al. 1992. Glycoconj. J. 9:235-240.Google Scholar
  38. 38.
    Taylor, G. 1996. Sialidases: Structures, biological significance and therapeutic potential. Curr. Opin. Struct. Biol. 6:830-837.Google Scholar
  39. 39.
    Sango, K., Yamanaka, S., Hoffmann, A., Okuda, Y., Grinberg, A., Westphal, H., McDonald, M. P., Crawley, J. N., Sandhoff, K., Suzuki, K., and Proia, R. 1995. Mouse models of Tay-Sachs and Sandhoff diseases differ in neurologic phenotype and ganglioside metabolism. Nat. Genet. 11:170-176.Google Scholar
  40. 40.
    Li, S.-C., Li, Y.-T., Moriya, S., and Miyagy, T. 2001. Degradation of GM1 and GM2 by mammalian sialidase. Biochem. J. 360:233-237.Google Scholar
  41. 41.
    Gravel, R. A., Clarke, J. T. R., Kaback, M. M., Mahuran, D., Sandhoff, K., and Suzuki, K. 1995. The GM2 gangliosidosis. Pages 2839-2879, in Schriver, C. W., Beaudet, A. L., Sly, W. S., and Valle, D. (eds.), Metabolic Basis of Inherited Diseases. McGraw-Hill Book Co, New York.Google Scholar
  42. 42.
    Wu, Y. Y., Lockyer, J. M., Sugiyama, E., Pavlova, N. V., Li, Y.-T., and Li, S.-C. 1994. Expression and specificity of human GM2 activator protein. J. Biol. Chem. 269:16276-16283.Google Scholar
  43. 43.
    Crennell, S., Garman, E., Laver, Vimr, E., and Taylor, G. L. 1994. Crystal structure of Vibrio cholerae neuraminidase reveals dual lectin-like domains in addition to the catalytic domain. Structure 2:535-544.Google Scholar
  44. 44.
    Varghese, J. N., Laver, W. G., and Colman, P. M.. 1983. Structure of the influenza virus glycoprotein antigen neuraminidase at 2.9 A resolution. Nature. 303:35-40.Google Scholar
  45. 45.
    Burmeister, W. P., Ruigrok, R. W., and Cusack, S. 1992. The 2.2 A resolution crystal structure of influenza B neuraminidase and its complex with sialic acid. EMBO J. 11:49-56.Google Scholar
  46. 46.
    Crennell, S., Takimoto, T., Portner, A., and Tailor, G. 2000. Crystal structure of the multifunctional paramyxovirus hemagglutinin-neuraminidase. Nat. Struct. Biol. 7:1068-1074.Google Scholar
  47. 47.
    Kao, Y. H., Lerner, L., and Warner, T. G. 1997. Stereoselectivity of the Chinese hamster ovary cell sialidase: Sialoside hydrolysis with overall retention of configuration. Glycobiology 7:559-563.Google Scholar
  48. 48.
    Gebler, J., Gilkes, N. R., Claeyssens, M., Wilson, D. B., Beguin, P., Wakarchuk, W. W., Kilburn, D. G., Miller, R. C., Jr., Warren, R. A., and Withers, S. G. 1992. Stereoselective hydrolysis catalyzed by related beta-1,4-glucanases and beta-1,4-xylanases. J. Biol. Chem. 267:12559-12561.Google Scholar
  49. 49.
    Olson, E. and Klein, W. 1994. bHLH factors in muscle development: Dead lines and commitments, what to leave in and what to leave out. Genes Dev. 8:1-8.Google Scholar
  50. 50.
    Sato, K. and Miyagi, T. 1996. Involvement of an endogenous sialidase in skeletal muscle cell differentiation. Biochem. Biophys. Res. Commun. 221:826-830.Google Scholar
  51. 51.
    Akita, H., Miygi, T., Hata, K., and Kagayama, M. 1997. Immunohistochemical evidence for the existence of rat cytosolic sialidase in rat skeletal muscles. Histochem. Cell. Biol. 107:495-503.Google Scholar
  52. 52.
    Tokuyama, S., Moriya, S., Taniguchi, S., Yasui, A., Miyazaki, J., Orikasa, S., and Miyagi, T. 1997. Suppression of pulmonary metastasis in murine B16 melanoma cells by transfection of a sialidase cDNA. Int. J. Cancer. 73:410-415.Google Scholar
  53. 53.
    Gillard, B. K., Thurmon, L. T., and Marcus, D. M. 1993. Variable subcellular localization of glycosphingolipids. Glycobiology 3:57-67.Google Scholar
  54. 54.
    Sawada, M., Moriya, S., Saito, S., Shineha, R., Satomi, S., Yamori, T., Tsuruo, T., Kannagi, R., and Miyagi, T. 2002. Reduced sialidase expression in highly metastatic variants of mouse colon adenocarcinoma 26 and retardation of their metastatic ability by sialidase overexpression. Int. J. Cancer 97:180-185.Google Scholar
  55. 55.
    Kato, T., Wang, T., Yamaguchi, K., Milner, C. M., Shineha, R., Satomi, S., and Miyagi, T. 2001. Overexpression of lysosomaltype sialidase leads to suppression of metastasis associated with reversion of malignant phenotype in murine melanoma cells. Int. J. Cancer 92:797-804.Google Scholar
  56. 56.
    Pshezhetsky, A. V. and Potier, M. 1996. Association of N-acetylgalactosamine-6-sulfate sulfatase with the multienzyme lysosomal complex of beta-galactosidase, cathepsin A, and neuraminidase. Possible implication for intralysosomal catabolism of keratan sulfate. J. Biol. Chem. 271:28359-28365.Google Scholar
  57. 57.
    Hiraiwa, M., Saitoh, M., Arai, N., Shiraishi, T., Odani, S., Uda, Y., Ono, T., and O'Brien, J. S. 1997. Protective protein in the bovine lysosomal beta-galactosidase complex. Biochim. Biophys. Acta 1341:189-199.Google Scholar
  58. 58.
    Bonten, E. J. and d'Azzo, A. 2000. Lysosomal neuraminidase. Catalytic activation in insect cells is controlled by the protective protein/cathepsin A. J. Biol. Chem. 275:37657-37663.Google Scholar
  59. 59.
    Vinogradova, M. V., Michaud, L., Mezentsev, A. V., Lukong, K. E., El-Alfy, M., Morales, C. R., Potier, M., and Pshezhetsky, A. V. 1998. Molecular mechanism of lysosomal sialidase deficiency in galactosialidosis involves its rapid degradation. Biochem. J. 330:641-650.Google Scholar
  60. 60.
    Naraparaju, V. R. and Yamamoto, N. 1994. Roles of beta-galactosidase of B lymphocytes and sialidase of T lymphocytes in inflammation-primed activation of macrophages. Immunol. Lett. 43:143-148.Google Scholar
  61. 61.
    Chen, X. P., Enioutina, E. Y., and Daynes, R. A. 1997. The control of IL-4 gene expression in activated murine T lymphocytes: A novel role for neu-1 sialidase. J. Immunol. 158:3070-3080.Google Scholar
  62. 62.
    Chen, X. P., Ding, X., and Daynes, R. A. 2000. Ganglioside control over IL-4 priming and cytokine production in activated T cells. Cytokine 12:972-985.Google Scholar
  63. 63.
    Lukong, K. E., Seyrantepe, V., Landry, K., Trudel, S., Ahmad, A., Gahl, W. A., Lefrancois, S., Morales, C. R., and Pshezhetsky, A. V. 2001. Intracellular distribution of lysosomal sialidase is controlled by the internalization signal in its cytoplasmic tail. J. Biol. Chem. 276:46172-46181.Google Scholar
  64. 64.
    Jarousse, N. and Kelly, R. B. 2000. Selective inhibition of adaptor complex-mediated vesiculation. Traffic 1:378-384.Google Scholar
  65. 65.
    Dell'Angelica, E. C., Shotelersuk, V., Aguilar, R. C., Gahl, W. A., and Bonifacino, J. S. 1999. Altered trafficking of lysosomal proteins in Hermansky-Pudlak syndrome due to mutations in the beta 3A subunit of the AP-3 adaptor. Mol. Cell. 3:11-21.Google Scholar
  66. 66.
    Ostrov, D. A., Shi, W., Schwartz, J. C., Almo, S. C., and Nathenson, S. G. 2000. Structure of murine CTLA-4 and its role in modulating T cell responsiveness. Science 290:816-819.Google Scholar
  67. 67.
    Lukong, K. E., Elsliger, M.-A., Chang, Y., Richard, C., Thomas, G., Carey, W., Tylki-Szymanska, A., Czartoryska, B., Buchholz, T., Rodriguez Criado, G., Palmeri, S., and Pshezhetsky, A. V. 2000. Characterization of the sialidase molecular defects in sialidosis patients suggests the structural organization of the lysosomal multienzyme complex. Hum. Mol. Genet. 9:1075-1085.Google Scholar
  68. 68.
    Bonten, E. J., Arts, W. F., Beck, M., Covanis, A., Donati, M. A., Parini, R., Zammarchi., E., and d'Azzo, A. 2000. Novel mutations in lysosomal neuraminidase identify functional domains and determine clinical severity in sialidosis. Hum. Mol. Genet. 9:2715-2725.Google Scholar
  69. 69.
    Naganawa, Y., Itoh, K., Shimmoto, M., Takiguchi, K., Doi, H., Nishizawa, Y., Kobayashi, T., Kamei, S., Lukong, K. E., Pshezhetsky, A. V., and Sakuraba, H. 2000. Molecular and structural studies of Japanese patients with sialidosis type 1. J. Hum. Genet. 45:241-249.Google Scholar
  70. 70.
    Penzel, R., Uhl, J., Kopitz, J., Beck, M., Otto, H. F., and Cantz, M. 2001. Splice donor site mutation in the lysosomal neuraminidase gene causing exon skipping and complete loss of enzyme activity in a sialidosis patient. FEBS Lett. 501:135-138.Google Scholar
  71. 71.
    Sergi, C., Penzel, R., Uhl, J., Zoubaa, S., Dietrich, H., Decker, N., Rieger, P., Kopitz, J., Otto, H. F., Kiessling, M., and Cantz, M. 2001. Prenatal diagnosis and fetal pathology in a Turkish family harboring a novel nonsense mutation in the lysosomal alpha-N-acetyl-neuraminidase (sialidase) gene. Hum. Genet. 109:421-428.Google Scholar
  72. 72.
    Itoh, K., Naganawa, Y., Matsuzawa, F., Aikawa, S., Doi, H., Sasagasako, N., Yamada, T., Kira, J., Kobayashi, T., Pshezhetsky, A. V., and Sakuraba, H. 2002. Novel missense mutations in the human lysosomal sialidase gene in sialidosis patients and prediction of structural alterations of mutant enzymes. J. Hum. Genet. 47:29-37.Google Scholar
  73. 73.
    Lukong, K. E., Landry, K., Elsliger, M. A., Chang, Y., Lefrancois, S., Morales, C. R., and Pshezhetsky, A. V. 2001. Mutations in sialidosis impair sialidase binding to the lysosomal multienzyme complex. J. Biol. Chem. 276:17286-17290.Google Scholar
  74. 74.
    Preti, A., Fiorilli, A., Lombardo, A., Caimi, L., and Tettamanti, G. 1980. Occurrence of sialyltransferase activity in the synaptosomal membranes prepared from calf brain cortex. J. Neurochem. 35:281-296.Google Scholar
  75. 75.
    Tettamanti, G. and Riboni, L. 1993. Gangliosides and modulation of the function of neural cells. Adv. Lipid Res. 25:235-267.Google Scholar
  76. 76.
    Kopitz, J., von Reitzenstein, C., Muhl, C., and Cantz, M. 1994. Role of plasma membrane ganglioside sialidase of human neuroblastoma cells in growth control and differentiation. Biochem. Biophys. Res. Commun. 199:1188-1193.Google Scholar
  77. 77.
    Kopitz, J., von Reitzenstein, C., Sinz, K., and Cantz, M. 1996. Selective ganglioside desialylation in the plasma membrane of human neuroblastoma cells. Glycobiology 6:367-376.Google Scholar
  78. 78.
    Kopitz, J., Oehler, C., and Cantz, M. 2001. Desialylation of extracellular GD1a-neoganglioprotein suggests cell surface orientation of the plasma membrane-bound ganglioside sialidase activity in human neuroblastoma cells. FEBS Lett. 491:233-236.Google Scholar
  79. 79.
    Kalka, D., von Reitzenstein, C., Kopitz, J., and Cantz, M. 2001. The plasma membrane ganglioside sialidase cofractionates with markers of lipids rafts. Biochem. Biophys. Res. Commun. 283:989-993.Google Scholar
  80. 80.
    Simon, K. and Ikonen, E. 1997. Functional rafts in cell membranes. Nature 387:569-572.Google Scholar
  81. 81.
    Brown, D. A. and London, E. 2000. Structure and function of sphingolipid-and cholesterol-rich membrane rafts. J. Biol. Chem. 275:17221-17224.Google Scholar
  82. 82.
    Saito, M. and Yu, R. K. 1992. Role of myelin-associated neuraminidase in the ganglioside metabolism of rat brain myelin. J. Neurochem. 58:83-87.Google Scholar
  83. 83.
    Pitto, M., Chigorno, V., Giglioni, A., Valsecchi, M., and Tettamanti, G. 1989. Sialidase in cerebellar granule cells differentiating in culture. J. Neurochem. 53:1464-1470.Google Scholar
  84. 84.
    Wu, G. and Ledeen, R. W. 1991. Stimulation of neurite outgrowth in neuroblastoma cells by neuraminidase: Putative role of GM1 ganglioside in differentiation. J. Neurochem. 56:95-104.Google Scholar
  85. 85.
    Saito, M., Tanaka, Y., Tang, C. P., Yu, R. K., and Ando, S. 1995. Characterization of sialidase activity in mouse synaptic plasma membranes and its age-related changes. J. Neurosci. Res. 40:401-406.Google Scholar
  86. 86.
    Rodriguez, J. A., Piddini, E., Hasegawa, T., Miyagi, T., and Dotti, C. G. 2001. Plasma membrane ganglioside sialidase regulates axonal growth and regeneration in hippocampal neurons in culture. J. Neurosci. 21:8387-8395.Google Scholar
  87. 87.
    Hata, K., Sasaki, A., Sawada, M., Wada, T., Tateno, H., and Miyagi, T. 2001. Overexpression of ganglioside sialidase in transgenic mice leads to non-insulin dependent diabetes mellitus. Glycoconj. J. 18:90.Google Scholar
  88. 88.
    Chiarini, A., Fiorilli, A., Di Francesco, L., Venerando, B., and Tettamanti, G. 1993. Human erythrocyte sialidase is linked to the plasma membrane by a glycosylphosphatidylinositol anchor and partly located on the outer surface. Glycoconj. J. 10:64-71.Google Scholar
  89. 89.
    Venerando, B., Fiorilli, A., Croci, G. L., and Tettamanti, G. 1997. Presence in human erythrocyte membranes of a novel form of sialidase acting optimally at neutral pH. Blood 90:2047-2056.Google Scholar
  90. 90.
    Tringali, C., Fiorilli, A., Venerando, B., and Tettamanti, G. 2001. Different behavior of ghost-linked acidic and neutral sialidases during human erythrocyte ageing. Glycoconj. J. 18: 407-418.Google Scholar
  91. 91.
    Venerando, B., Fiorilli, A., Croci, G. L., Trincali, C., Goi, G., Mazzanti, L., Curatola, G., Segalini, G., Massaccesi, L., Lombardo, A., and Tettamanti, G. 2002. Acidic and neutral sialidase in the erythrocyte membrane of type 2 diabetic patients. Blood 99:1064-1070.Google Scholar

Copyright information

© Plenum Publishing Corporation 2002

Authors and Affiliations

  • Eugenio Monti
    • 1
  • Augusto Preti
    • 1
  • Bruno Venerando
    • 2
  • Giuseppe Borsani
    • 1
  1. 1.Department of Biomedical Sciences and BiotechnologyUniversity of BresciaBresciaItaly
  2. 2.Department of Chemistry and Medical BiochemistryL.I.T.A.SegrateItaly

Personalised recommendations