Skip to main content
Log in

Sialidase and malignancy: A minireview

  • Published:
Glycoconjugate Journal Aims and scope Submit manuscript

Abstract

Aberrant sialylation in cancer cells is thought to be a characteristic feature associated with malignant properties including invasiveness and metastatic potential. Sialidase which catalyzes the removal of sialic acid residues from glycoproteins and glycolipids, has been suggested to play important roles in many biological processes through regulation of cellular sialic acid contents. The altered expression of sialidase observed in cancer would, therefore, suggest its involvement in the malignant process. In mammalian cells, three types of sialidase cloned and characterized to date were found to behave in different manners during carcinogenesis. Recent progress in molecular cloning of these sialidases has facilitated elucidation of the molecular mechanisms and significance of these alterations. Herein we briefly describe our own studies on sialidase changes associated with malignant transformation and summarize the topic from both a retrospective and a prospective viewpoint. Sialidases are indeed closely related to malignancy and are thus potential targets for cancer diagnosis and therapy. Published in 2004.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Abercrombie M, Ambrose EJ, The surface properties of cancer cells, Cancer Res 22, 525-48 (1962).

    PubMed  CAS  Google Scholar 

  2. Weiss L, Neuraminidase, sialic acids, and cell interactions, J Natl Cancer Inst 50, 3-19 (1973).

    PubMed  CAS  Google Scholar 

  3. Warren L, Buck CA, Tuszynski GP, Glycopeptide changes and malignant transformation, a possible role for carbohydrate in malignant behaviour, Biochim Biophys Acta 516, 97-127 (1978).

    PubMed  CAS  Google Scholar 

  4. Dennis JW, Laferte S, Tumor cell surface carbohydrate and the metastatic phenotype, Cancer Metastasis Rev 5, 185-204 (1987).

    Article  PubMed  CAS  Google Scholar 

  5. Kobata A, Altered glycosylation of surface glycoproteins in tumor cells and its clinical application, Pigment Cell Res 2, 304-8 (1989).

    Article  PubMed  CAS  Google Scholar 

  6. Bhavanandan VP, Cancer-associated mucins and mucin-type glycoproteins, Glycobiology 1, 493-503 (1991).

  7. Hakomori S, Tumor malignancy defined by aberrant glycosylation and sphingo(glyco)lipid metabolism, Cancer Res 56, 5309-18 (1996).

    PubMed  CAS  Google Scholar 

  8. Hakomori S, Glycosylation defining cancer malignancy:Newwine in an old bottle, Proc Natl Acad Sci USA 99, 10231-3 (2002).

    Article  PubMed  CAS  Google Scholar 

  9. Yogeeswaran G, Salk PL, Metastatic potential is positively correlated with cell surface sialylation of cultured murine tumor cell lines, Science 212, 1514-6 (1981).

    PubMed  CAS  Google Scholar 

  10. Fogel M, Altevogt P, Schirrmacher V, Metastatic potential severely altered by changes in tumor cell adhesiveness and cell-surface sialylation, J Exp Med 157, 371-6 (1983).

    Article  PubMed  CAS  Google Scholar 

  11. Collard JG, Schijven JF, Bikker A, La Riviere G, Bolscher JG, Roos E, Cell surface sialic acid and the invasive and metastatic potential of T-cell hybridomas, Cancer Res 46, 3521-7 (1986).

    PubMed  CAS  Google Scholar 

  12. Dennis JW, Lafarté S, Waghorne C, Breitman ML, Kerbel RS, ?1-6 Branching of Asn-linked oligosaccharides is directly associated with metastasis, Science 236, 582-5 (1987).

    PubMed  CAS  Google Scholar 

  13. Passaniti A, Hart GW, Cell surface sialylation and tumor metastasis. Metastatic potential of B16 melanoma variants correlates with their relative numbers of specific penultimate oligosaccharide structures, J Biol Chem 263, 7591-603 (1988).

    PubMed  CAS  Google Scholar 

  14. Basu S, Basu M, Basu SS, Biological specificity of sialyltransferases. In Biology of the sialic acids, edited by Rosenberg A (Plenum Press, New York, 1995), pp. 69-94.

    Google Scholar 

  15. Basu S, Basu M, Dastgheib S, Hawes JW, Biosynthesis and regulation of glycoshingolipids. In Comprehensive natural products chemistry, edited by Barton D, Nakanishi K, Meth-Cohen O, vol. 3 (Pinto BM ed.). (Pergamon Press, New York, 1999), pp. 107-28.

    Google Scholar 

  16. Pilatte Y, Bignon J, Lambré CR, Bacterial sialidases-roles in pathogenicity and nutrition, Glycobiology 3, 201-17 (1993).

    PubMed  CAS  Google Scholar 

  17. Saito M, Yu RK, Biochemistry and function of sialidases. In Biology of the sialic acids, edited by Rosenberg A (Plenum Press, New York, 1995), pp. 261-313.

    Google Scholar 

  18. Miyagi T, Wada T, Yamaguchi K, Multiple forms of mammalian sialidase and their altered expression in physiological and pathological conditions. In Sialobiology and other novel forms of glycosylation, edited by Inoue Y, Lee YC, Troy II FA (Gakushin Publishing Co., Osaka, 1999), pp. 197-205.

    Google Scholar 

  19. Monti E, Preti A, Venerando B, Borsani G, Recent development in mammalian sialidase molecular biology, Neurochem Res 27, 649-63 (2002).

    Article  PubMed  CAS  Google Scholar 

  20. Warren L, Spearing CW, Mammalian sialidase(neuraminidase), Biochem Biophys Res Commun 3, 489-92 (1960).

    Article  PubMed  CAS  Google Scholar 

  21. Carubelli R, Trucco RE, Caputto R, Neuraminidase activity in mammalian organs, Biochim Biophys Acta 60, 196-7 (1962).

    Article  PubMed  CAS  Google Scholar 

  22. Mahadevan S, Nduaguba JC, Tappel AL, Sialidase of rat liver and kidney, J Biol Chem 242, 4409-13 (1967).

    PubMed  CAS  Google Scholar 

  23. Taha BH, Carubelli R, Mammalian neuraminidase: Intracellular distribution and changes of enzyme activity during lactation, Arch Biochem Biophys 119, 55-61 (1967).

    Article  PubMed  CAS  Google Scholar 

  24. Horvat A, Touster O, On the lysosomal occurance and the properties of the neuraminidase of rat liver and of Ehrlich ascites tumor cells, J Biol Chem 243, 4380-90 (1968).

    PubMed  CAS  Google Scholar 

  25. Schengrund C-L, Rosenberg A, Intracellular location and properties of bovine brain sialidase, J Biol Chem 245, 6196-6200 (1970).

    PubMed  CAS  Google Scholar 

  26. Schengrund C-L, Jensen DS, Rosenberg A, Localization of sialidase in the plasma membrane of rat liver cells, J Biol Chem 247, 2742-6 (1972).

    PubMed  CAS  Google Scholar 

  27. Tettamanti G, Preti A, Lombardo A, Bonali F, Zambotti V, Parallelism of subcellular location of major particulate neuraminidase and gangliosides in rabbit brain cortex, Biochim Biophys Acta 306, 466-77 (1973).

    PubMed  CAS  Google Scholar 

  28. Visser AEP, Studies on plasma membranes.XXsialidase in hepatic plasma membranes, J Membrane Biol 14, 73-84 (1973).

    Article  CAS  Google Scholar 

  29. Kishore GS, Tulsiani DRP, Bhavanandan VP, Carubelli R, Membrane-bound neuraminidases of rat liver. Neuraminidase activity in Golgi apparatus, J Biol Chem 250, 2655-9 (1975).

    PubMed  CAS  Google Scholar 

  30. Saito M, Fronda CL, Yu RK, Sialidase activity in nuclear membranes of rat brain, J Neurochem 66, 2205-8 (1996).

    Article  PubMed  CAS  Google Scholar 

  31. Miyagi T, Tsuiki S, Rat-liver lysosomal sialidase. Solubilization, substrate specificity and comparison with the cytosolic sialidase, Eur J Biochem 141, 75-81 (1984).

    Article  PubMed  CAS  Google Scholar 

  32. Miyagi T, Tsuiki S, Purification and characterization of cytosolic sialidase from rat liver, J Biol Chem 260, 6710-16 (1985).

    PubMed  CAS  Google Scholar 

  33. Miyagi T, Sagawa J, Konno K, Handa S, Tsuiki S, Biochemical and immunological studies on two distinct ganglioside-hydrolyzing sialidases from the particulate fraction of rat brain, J Biochem (Tokyo) 107, 787-93 (1990).

    CAS  Google Scholar 

  34. Miyagi T, Konno K, Emori Y, Kawasaki H, Suzuki K, Yasui A, Tsuiki S, Molecular cloning and expression of cDNA encoding rat skeletal muscle cytosolic sialidase, J Biol Chem 268, 26435-40 (1993).

    PubMed  CAS  Google Scholar 

  35. Ferrari J, Harris R, Warner TG, Cloning and expression of a soluble sialidase from Chinese hamster ovary cells: Sequence alignment similarities to bacterial sialidases, Glycobiology 4, 367-73 (1993).

    Google Scholar 

  36. Monti E, Rossi PA, Ballabio E, Borsani A, Cloning and characterization of NEU2, a human gene homologous to rodent soluble sialidases, Genomics 57, 137-43 (1999).

    Article  PubMed  CAS  Google Scholar 

  37. Fronda CL, Zeng G, Gao L, Yu RK, Molecular cloning and expression of mouse brain sialidase, Biochem Biophys Res Commun 258, 727-31 (1999).

    Article  PubMed  CAS  Google Scholar 

  38. Hasegawa T, Yamaguchi K, Wada T, Takeda A, Itoyama Y, Miyagi T, Molecular cloning of mouse ganglioside sialidase and its increased expression in Neuro2a cell differentiation, J Biol Chem 275, 8007-15 (2000).

    Article  PubMed  CAS  Google Scholar 

  39. Kotani K, Kuroiwa A, Saito T, Matsuda Y, Koda T, K-Ochiai S, Cloning, chromosomal mapping, and characteristic 5?-UTR sequence of murine cytosolic sialidase, Biochem Biophys Res Commun 286, 250-8 (2001).

    Article  PubMed  CAS  Google Scholar 

  40. d'Azzo A, Hoogeveen A, Reuser AJ, Robinson D, Galjaard H, Molecular defect in combined beta-galactosidase and neuraminidase deficiency in man, Proc Natl Acad Sci USA 79, 4535-9 (1982).

    Google Scholar 

  41. van der Horst GT, Galjart NJ, d'Azzo A, Galjaard H, Verheijen FW, Identification and in vitro reconstitution of lysosomal neuraminidase from human placenta, J Biol Chem 264, 1317-22 (1989).

    PubMed  CAS  Google Scholar 

  42. Bonten E, van der Spoel A, Fornerod M, Grosveld G, d'Azzo A, Characterization of human lysosomal neuraminidase defines the molecular basis of the metabolic storage disorder sialidosis, Genes Dev 10, 3156-69 (1996).

    PubMed  CAS  Google Scholar 

  43. Milner CM, Smith SV, Carrillo MB, Taylor GL, Hollinshead M, Campbell RD, Identification of a sialidase encoded in the human major histocompatibility complex, J Biol Chem 272, 4549-58 (1997).

    Article  PubMed  CAS  Google Scholar 

  44. Pshezhetsky AV, Richard C, Michaud L, Igdoura S, Wang S, Elsliger MA, Qu J, Leclerc D, Gravel R, Dallaire L, Potier M, Cloning, expression and chromosomal mapping of human lysosomal sialidase and characterization of mutations in sialidosis, Nat Genet 15, 316-20 (1997).

    Article  PubMed  CAS  Google Scholar 

  45. Carrillo MB, Milner CM, Ball ST, Snoek M, Campbell RD, Cloning and characterization of a sialidase from the murine histocompatibility-2 complex: Low levels of mRNA and a single amino acid mutation are responsible for reduced sialidase activity in mice carrying the Neu1a allele, Glycobiology 7, 975-86 (1997).

    PubMed  CAS  Google Scholar 

  46. Igdoura SA, Gafuik C, Mertineit C, Saberi F, Pshezhetsky AV, Potier M, Trasler JM, Gravel RA, Cloning of the cDNA and gene encoding mouse lysosomal sialidase and correction of sialidase deficiency in human sialidosis and mouse SM/J fibroblasts, Hum Mol Genet 7, 115-21 (1998).

    Article  PubMed  CAS  Google Scholar 

  47. Rottier RJ, Bonten E, d'Azzo A,HumMol Genet.Apoint mutation in the neu-1 locus causes the neuraminidase defect in the SM/J mouse, 7, 313-21 (1998).

    CAS  Google Scholar 

  48. van der Spoel A, Bonten E, d'Azoo A, Transport of human lysosomal neuraminidase to mature lysosomes requires protective protein/cathepsin A, EMBO J 17, 1588-97 (1998).

    Article  PubMed  CAS  Google Scholar 

  49. Lukong KE, Seyrantepe V, Landry K, Trudel S, Ahmad A, Gahl WA, Lefrancois S, Morales CR, Pshezhetsky AV, Intracellular distribution of lysosomal sialidase is controlled by the internalization signal in its cytoplasmic tail, J Biol Chem 276, 46172-81 (2001).

    Article  PubMed  CAS  Google Scholar 

  50. Miyagi T, Wada T, Iwamatsu A, Hata K, Yoshikawa Y, Tokuyama S, Sawada M, Molecular cloning and characterization of a plasma membrane-associated sialidase specific for gangliosides, J Biol Chem 274, 5004-11 (1999).

    Article  PubMed  CAS  Google Scholar 

  51. Hata K, Wada T, Hasegawa A, Kiso M, Miyagi T, Purification and characterization of a membrane-associated ganglioside sialidase from bovine brain, J Biochem (Tokyo) 123, 899-905 (1998).

    CAS  Google Scholar 

  52. Wada T, Yoshikawa Y, Tokuyama S, Kuwabara M, Akita H, Miyagi T, Cloning, expression, and chromosomal mapping of a human ganglioside sialidase, Biochem Biophys Res Commun 261, 21-7 (1999).

    Article  PubMed  CAS  Google Scholar 

  53. Monti E, Bassi MT, Papini N, Riboni M, Manzoni M, Venerando B, Croci G, Preti A, Ballabio A, Tettamanti G, Borsani G, Identification and expression of NEU3, a novel human sialidase associated to the plasma membrane, Biochem J 349, 343-51 (2000).

    Article  PubMed  CAS  Google Scholar 

  54. Hasegawa T, Feijoo Carnero C, Wada T, Itoyama Y, Miyagi T, Differential expression of three sialidase genes in rat development, Biochem Biophys Res Commun 280, 726-32 (2001).

    Article  PubMed  CAS  Google Scholar 

  55. Roggentin P, Rothe B, Lottspeich F, Schauer R, Cloning and sequencing of a Clostridium perfringens sialidase gene, FEBS Lett 238, 31-4 (1988).

    Article  PubMed  CAS  Google Scholar 

  56. Hoyer LL, Hamilton AC, Steenbergen SM, Vimr ER, Cloning, sequencing and distribution of the Salmonella typhimurium LT2 Sialidase and malignancy: A minireview 197 sialidase gene, nanH, provides evidence for interspecies gene transfer, Mol Microbiol 6, 873-84 (1992).

    PubMed  CAS  Google Scholar 

  57. Crennell SJ, Garman EF, Laver WG, Vimir ER, Taylor GL, Crystal structure of a bacterial sialidase (from Salmonella typhimurium LT2) shows the same fold as an influenza virus neuraminidase, Proc Natl Acad Sci USA 90, 9852-6 (1992).

    Article  Google Scholar 

  58. Wang Y, Yamaguchi K, Shimada Y, Zhao X, Miyagi T, Site-directed mutagenesis of human membrane-associated ganglioside sialidase: Identification of amino-acid residues contributing to substrate specificity, Eur J Biochem 268, 2201-8 (2001).

    Article  PubMed  CAS  Google Scholar 

  59. Sato K, Miyagi T, Genomic organization and the 5?-upstream sequence of the rat cytosolic sialidase gene, Glycobiology 5, 511-6 (1995).

    PubMed  CAS  Google Scholar 

  60. Sato K, Miyagi T, Involvement of an endogenous sialidase in skeletal muscle cell differentiation, Biochem Biophys Res Commun 221, 826-30 (1996).

    Article  PubMed  CAS  Google Scholar 

  61. Landolfi NF, Leone J, Womack JE, Cook RG, Activation of T lymphocytes results in an increase in H-2-encoded neuraminidase, Immunogenetics 22, 159-67 (1985).

    Article  PubMed  CAS  Google Scholar 

  62. Chen XP, Enioutina EY, Daynes RA, The control of IL-4 gene expression in activated murine T lymphocytes: A novel role for neu-1 sialidase, J Immunol 158, 3070-80 (1997).

    PubMed  CAS  Google Scholar 

  63. Chen XP, Ding X, Daynes RA, Ganglioside control over IL-4 priming and cytokine production in activated T cells, Cytokine 12, 972-85 (2000).

    Article  PubMed  CAS  Google Scholar 

  64. Yamamoto N, Kumashiro R, Conversion of vitamin D3 binding protein (group-specific component) to a macrophage activating factor by the stepwise action of beta-galactosidase of B cells and sialidase of T cells, J Immunol 151, 2794-802 (1993).

    PubMed  CAS  Google Scholar 

  65. Yamamoto N, Naraparaju VR, Role of vitamin D3-binding protein in activation of mouse macrophages, J Immunol 157, 1744-9 (1996).

    PubMed  CAS  Google Scholar 

  66. Usuki S, Hoops P, Sweeley CC, Growth control of human foreskin fibroblasts and inhibition of extracellular sialidase activity by 2-deoxy-2,3-dehydro-N-acetylneuraminic acid, J Biol Chem 263, 10595-9 (1988).

    PubMed  CAS  Google Scholar 

  67. Kopitz J, von Reitzenstein C, Muhl C, Cantz M, Role of plasma membrane ganglioside sialidase of human neuroblastoma cells in growth control and differentiation, Biochem Biophys Res Commun 199, 1188-93 (1994).

    Article  PubMed  CAS  Google Scholar 

  68. Kopitz J, Muhl C, Ehemann V, Lehmann C, Cantz M, Effects of cell surface ganglioside sialidase inhibition on growth control and differentiation of human neuroblastoma cells, Eur J Cell Biol 73, 1-9 (1997).

    Article  PubMed  CAS  Google Scholar 

  69. Kopitz J, von Reitzenstein C, Burchert M, Cantz M, Gabius HJ, Galectin-1 is a major receptor for ganglioside GM1, a product of the growth-controlling activity of a cell surface ganglioside sialidase, on human neuroblastoma cells in culture, J Biol Chem 273, 11205-11 (1998).

    Article  PubMed  CAS  Google Scholar 

  70. Kopitz J, von Reitzenstein C, Andre S, Kaltner H, Uhl J, Ehemann V, Cantz M, Gabius HJ, Negative regulation of neuroblastoma cell growth by carbohydrate-dependent surface binding of galectin-1 and functional divergence from galectin-3, J Biol Chem 276, 35917-23 (2001).

    Article  PubMed  CAS  Google Scholar 

  71. Proshin S, Yamaguchi K, Wada T, Miyagi T, Modulation of neuritogenesis by ganglioside-specific sialidase (Neu 3) in human neuroblastoma NB-1 cells, Neurochem Res 27, 841-6(2002).

    Article  PubMed  CAS  Google Scholar 

  72. Rodriguez JA, Piddini E, Hasegawa T, Miyagi T, Dotti CG, Plasma membrane ganglioside sialidase regulates axonal growth and regeneration in hippocampal neurons in culture, J Neurosci 21, 8387-95 (2001).

    PubMed  CAS  Google Scholar 

  73. Kalka D, von Reitzenstein C, Kopitz J, Cantz M, The plasma membrane ganglioside sialidase cofractionates with markers of lipid rafts, Biochem Biophys Res Commun 283, 989-93 (2001).

    Article  PubMed  CAS  Google Scholar 

  74. Wang Y, Yamaguchi K, Wada T, Hata K, Zhao X, Fujimoto T, Miyagi T, A close association of the ganglioside-specific sialidase Neu3 with caveolin in membrane microdomains, J Biol Chem 277, 26252-9 (2002).

    Article  PubMed  CAS  Google Scholar 

  75. Sun P, Wang XQ, Lopatka K, Bangash S, Paller AS, Ganglioside loss promotes survival primarily by activating integrin-linked kinase/ Akt without phosphoinositide 3-OH kinase signaling, J Invest Dermatol 119, 107-17 (2002).

    Article  PubMed  CAS  Google Scholar 

  76. Schengrund CL, Lausch RN, Rosenberg A, Sialidase activity in transformed cells, J Biol Chem 248, 4424-8 (1973).

    PubMed  CAS  Google Scholar 

  77. Bosmann HB, Hall TC, Enzyme activity in invasive tumors of human breast and colon, Proc Natl Acad Sci USA 71, 1833-7 (1974).

    Article  PubMed  CAS  Google Scholar 

  78. Yogeeswaran G, Hakomori S, Cell contact-dependent ganglioside changes in mouse 3T3 fibroblasts and a suppressed sialidase activity on cell contact, Biochemistry 14, 2151-6 (1975).

    Article  PubMed  CAS  Google Scholar 

  79. Nojiri N, Takaku F, Tetsuka T, Saito M, Stimulation of sialidase activity during cell differentiation of human promyelocytic leukemia cell line HL-60, Biochem Biophys Res Commun 104, 1239-46 (1982).

    Article  PubMed  CAS  Google Scholar 

  80. Miyagi T, Goto T, Tsuiki S, Sialidase of rat hepatomas: Qualitative and quantitative comparison with rat liver sialidase, Gann 75, 1076-82 (1984).

    PubMed  CAS  Google Scholar 

  81. Miyagi T, Konno K, Sagawa J, Tsuiki S, Neoplastic alteration of a membrane-associated sialidase of rat liver, Jpn J Cancer Res 81, 915-9 (1990).

    PubMed  CAS  Google Scholar 

  82. Miyagi T, Sagawa J, Kuroki T, Matsuya Y, Tsuiki S, Tumorpromoting phorbol ester induces alterations of sialidase and sialyltransferase activities of JB6 cells, Jpn J Cancer Res 81, 1286-92 (1990).

    PubMed  CAS  Google Scholar 

  83. Miyagi T, Sato K, Hata K, Taniguchi S, Metastatic potential of transformed rat 3Y1 cell lines is inversely correlated with lysosomal-type sialidase activity, FEBS Lett 349, 255-9 (1994).

    Article  PubMed  CAS  Google Scholar 

  84. Martinez-Zorzano VS, Feijoo C, Paez de la Cadena M, Butron M, Fernandez-Briera A, Rodriguez-Berrocal FJ, Human colon sialidase: Characterization and activity levels in normal mucosa and colonic adenocarcinoma, Enzyme Protein 48, 282-90 (1994).

    PubMed  CAS  Google Scholar 

  85. Sawada M, Moriya S, Saito S, Shineha R, Satomi S, Yamori T, Tsuruo T, Kannagi R, Miyagi T, 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, 180-85 (2002).

    Article  PubMed  CAS  Google Scholar 

  86. Tokuyama S, Moriya S, Taniguchi S, Yasui A, Miyazaki J, Orikasa S, Miyagi T, Suppression of pulmonary metastasis in murine B16 melanoma cells by transfection of a sialidase cDNA, Int J Cancer 73, 410-5 (1997).

    Article  PubMed  CAS  Google Scholar 

  87. Gillard BK, Thurmon LT, Marcus DM, Variable subcellular localization of glycosphingolipids, Glycobiology 3, 57-67 (1993).

    PubMed  CAS  Google Scholar 

  88. Sakakibara K, Momoi T, Uchida T, Nagai Y, Evidence for association of glycosphingolipid with a colchicine-sensitive microtubulelike cytoskeletal structure of cultured cells, Nature 293, 76-8 (1981).

    Article  PubMed  CAS  Google Scholar 

  89. Gillard BK, Thurmon LT, Marcus DM, Association of glycosphingolipids with intermediate filaments of mesenchymal, epithelial, glial, and muscle cells, Cell Motil Cytoskeleton 21, 255-71 (1992).

    Article  PubMed  CAS  Google Scholar 

  90. Meuillet EJ, Kroes R, Yamamoto H, Warner TG, Ferrari J, Mania-Farnell B, George D, Rebbaa A, Moskal JR, Bremer EG, Sialidase gene transfection enhances epidermal growth factor receptor activity in an epidermoid carcinoma cell line, A431, Cancer Res 59, 234-40 (1999).

    PubMed  CAS  Google Scholar 

  91. Kato T, Wang Y, Yamaguchi K, Milner CM, Shineha R, Satomi S, Miyagi T, Overexpression of lysosomal-type sialidase leads to suppression of metastasis associated with reversion of malignant phenotype in murine B16 melanoma cells, Int J Cancer 92, 797-804 (2001).

    Article  PubMed  CAS  Google Scholar 

  92. Kakugawa Y, Wada T, Yamaguchi K, Yamanami H, Ouchi K, Sato I, Miyagi T, Up-regulation of plasma membrane-associated ganglioside sialidase (Neu3) in human colon cancer and its involvement in apoptosis suppression, Proc Natl Acad Sci USA 99, 10718-23 (2002).

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Miyagi, T., Wada, T., Yamaguchi, K. et al. Sialidase and malignancy: A minireview. Glycoconj J 20, 189–198 (2003). https://doi.org/10.1023/B:GLYC.0000024250.48506.bf

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:GLYC.0000024250.48506.bf

Navigation