Abstract
Aberrant glycosylation is a characteristic feature of cancer cells. In particular, altered sialylation is closely associated with malignant properties, including invasiveness and metastatic potential. To elucidate the molecular mechanisms underlying the aberrancy, our studies have focused on mammalian sialidase, which catalyzes the removal of sialic acid residues from glycoproteins and glycolipids. The four types of mammalian sialidase identified to date show altered expression and behave in different manners during carcinogenesis. The present review briefly summarizes results on altered expression of sialidases and their possible roles in cancer progression. These enzymes are indeed factors defining cancer malignancy and thus potential targets for cancer diagnosis and therapy.
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Abbreviations
- DANA:
-
2-deoxy-2,3dehydro-N-acetylneuraminic acid
- 4MU-NANA:
-
4-methylumbelliferyl sialic acid
- NeuAc:
-
N-acetyl neuraminic acid
- EGFR:
-
Epidermal growth factor receptor
- siRNA:
-
Small interfering RNA
- RT-PCR:
-
Reverse transcription polymerase chain reaction
References
Lau, K.S., Dennis, J.W.: N-Glycans in cancer progression. Glycobiology. 18, 750–760 (2008)
Hakomori, S.I.: Glycosynaptic, microdomains controlling tumor cell phenotype through alteration of cell growth, adhesion, and motility. FEBS Lett. 584, 1901–1906 (2010)
Santer, U.V., DeSantis, R., Hard, K.J., van Kuik, J.A., Vliegenthart, J.F., Won, B., Glick, M.C.: N-linked oligosaccharide changes with oncogenic transformation require sialylation of multiantennae. Eur. J. Biochem. 181, 249–260 (1989)
Easton, E.W., Bolscher, J.G., van den Eijnden, D.H.: Enzymatic amplification involving glycosyltransferases forms the basis for the increased size of asparagine-linked glycans at the surface of NIH 3 T3 cells expressing the N-ras proto-oncogene. J. Biol. Chem. 266, 21674–21680 (1991)
Hakomori, S.I.: Tumor malignancy defined by aberrant glycosylation and sphingo(glyco)lipid metabolism. Cancer Res. 56, 5309–5318 (1996)
Miura, Y., Kainuma, M., Jiang, H., Velasco, H., Vogt, P.K., Hakomori, S.: Reversion of the Jun-induced oncogenic phenotype by enhanced synthesis of sialosyllactosylceramide (GM3 ganglioside). Proc. Natl. Acad. Sci. U S A. 101, 16204–16209 (2004)
Corfield, T.: Bacterial sialidases–roles in pathogenicity and nutrition. Glycobiology. 2, 509–521 (1992)
Monti, E., Bonten, E., D’Azzo, A., Bresciani, R., Venerando, B., Borsani, G., Schauer, R., Tettamanti, G.: Sialidases in vertebrates: a family of enzymes tailored for several cell functions. Adv. Carbohydr. Chem. Biochem. 64, 403–479 (2010)
Miyagi, T., Yamaguchi, K.: Mammalian sialidases: physiological and pathological roles in cellular functions, Glycobiology. in press (2012)
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, 3156–3169 (1996)
Milner, C.M., Smith, S.V., Carrillo, M.B., Taylor, G.L., Hollinshead, M., Campbell, R.D.: Identification of a sialidase encoded in the human major histocompatibility complex. J. Biol. Chem. 272, 4549–4558 (1997)
Pshezhetsky, A.V., Richard, C., Michaud, L., Igdoura, S., Wang, S., Elsliger, M.A., 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, 316–320 (1997)
Carrillo, M.B., Milner, C.M., Ball, S.T., Snoek, M., Campbell, R.D.: 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, 975–986 (1997)
Igdoura, S. A., Gafuik, C., Mertineit, C., Saberi, F., Pshezhetsky, A. V., Potier, M., Trasler, J. M.,Gravel, R. A. : 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, 115–121 (1998)
Rottier, R.J., Bonten, E., d’Azzo, A.: A point mutation in the neu-1 locus causes the neuraminidase defect in the SM/J mouse. Hum. Mol. Genet. 7, 313–321 (1998)
D’Azzo, A., Hoogeveen, A., Reuser, A.J., Robinson, D., Galjaard, H.: Molecular defect in combined beta-galactosidase and neuraminidase deficiency in man. Proc. Natl. Acad. Sci. U S A. 79, 4535–4539 (1982)
Galjart, N.J., Gillemans, N., Harris, A., van der Horst, G.T., Verheijen, F.W., Galjaard, H., d’Azzo, A.: Expression of cDNA encoding the human “protective protein” associated with lysosomal beta-galactosidase and neuraminidase: homology to yeast proteases. Cell. 54, 755–764 (1988)
Seyrantepe, V., Poupetova, H., Froissart, R., Zabot, M.T., Maire, I., Pshezhetsky, A.V.: Molecular pathology of NEU1 gene in sialidosis. Hum. Mutat. 22, 343–352 (2003)
Lukong, K.E., Seyrantepe, V., Landry, K., Trudel, S., Ahmad, A., Gahl, W.A., Lefrancois, S., Morales, C.R., Pshezhetsky, A.V.: Intracellular distribution of lysosomal sialidase is controlled by the internalization signal in its cytoplasmic tail. J. Biol. Chem. 276, 46172–46181 (2001)
Cross, A.S., Sakarya, S., Rifat, S., Held, T.K., Drysdale, B.E., Grange, P.A., Cassels, F.J., Wang, L.X., Stamatos, N., Farese, A., Casey, D., Powell, J., Bhattacharjee, A.K., Kleinberg, M., Goldblum, S.E.: Recruitment of murine neutrophils in vivo through endogenous sialidase activity. J. Biol. Chem. 278, 4112–4120 (2003)
Liang, F., Seyrantepe, V., Landry, K., Ahmad, R., Ahmad, A., Stamatos, N.M., Pshezhetsky, A.V.: Monocyte differentiation up-regulates the expression of the lysosomal sialidase, Neu1, and triggers its targeting to the plasma membrane via major histocompatibility complex class II-positive compartments. J. Biol. Chem. 281, 27526–27538 (2006)
Miyagi, T., Tsuiki, S.: Rat-liver lysosomal sialidase. Solubilization, substrate specificity and comparison with the cytosolic sialidase. Eur. J. Biochem. 141, 75–81 (1984)
Yogalingam, G., Bonten, E.J., van de Vlekkert, D., Hu, H., Moshiach, S., Connell, S.A., d’Azzo, A.: Neuraminidase 1 is a negative regulator of lysosomal exocytosis. Dev Cell. 15, 74–86 (2008)
Pshezhetsky, A.V., Hinek, A.: Where catabolism meets signalling: neuraminidase 1 as a modulator of cell receptors. Glycoconj. J. 28, 441–452 (2011)
Seyrantepe, V., Iannello, A., Liang, F., Kanshin, E., Jayanth, P., Samarani, S., Szewczuk, M.R., Ahmad, A., Pshezhetsky, A.V.: Regulation of phagocytosis in macrophages by neuraminidase 1. J. Biol. Chem. 285, 206–215 (2010)
Hinek, A., Pshezhetsky, A.V., von Itzstein, M., Starcher, B.: Lysosomal sialidase (neuraminidase-1) is targeted to the cell surface in a multiprotein complex that facilitates elastic fiber assembly. J. Biol. Chem. 281, 3698–310 (2006)
Seyrantepe, V., Hinek, A., Peng, J., Fedjaev, M., Ernest, S., Kadota, Y., Canuel, M., Itoh, K., Morales, C.R., Lavoie, J., Tremblay, J., Pshezhetsky, A.V.: Enzymatic activity of lysosomal carboxypeptidase (cathepsin) A is required for proper elastic fiber formation and inactivation of endothelin-1. Circulation. 117, 1973–1981 (2008)
Hinek, A., Bodnaruk, T.D., Bunda, S., Wang, Y., Liu, K.: Neuraminidase-1, a subunit of the cell surface elastin receptor, desialylates and functionally inactivates adjacent receptors interacting with the mitogenic growth factors PDGF-BB and IGF-2. Am. J. Pathol. 173, 1042–1056 (2008)
Arabkhari, M., Bunda, S., Wang, Y., Wang, A., Pshezhetsky, A.V., Hinek, A.: Desialylation of insulin receptors and IGF-1 receptors by neuraminidase-1 controls the net proliferative response of L6 myoblasts to insulin. Glycobiology. 20, 603–616 (2010)
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, 255–259 (1994)
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, 180–185 (2002)
Kato, T., Wang, Y., Yamaguchi, K., Milner, C.M., 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)
Miyagi, T., Wada, T., Yamaguchi, K., Shiozaki, K., Sato, I., Kakugawa, Y., Yamanami, H., Fujiya, T.: Human sialidase as a cancer marker. Proteomics. 8, 3303–3311 (2008)
Uemura, T., Shiozaki, K., Yamaguchi, K., Miyazaki, S., Satomi, S., Kato, K., Sakuraba, H., Miyagi, T.: Contribution of sialidase NEU1 to suppression of metastasis of human colon cancer cells through desialylation of integrin beta4. Oncogene. 28, 1218–1229 (2009)
Miyagi, T., Konno, K., Emori, Y., Kawasaki, H., Suzuki, K., Yasui, A., Tsuik, S.: Molecular cloning and expression of cDNA encoding rat skeletal muscle cytosolic sialidase. J. Biol. Chem. 268, 26435–26440 (1993)
Ferrari, J., Harris, R., Warner, T.G.: Cloning and expression of a soluble sialidase from Chinese hamster ovary cells: sequence alignment similarities to bacterial sialidases. Glycobiology. 4, 367–373 (1994)
Fronda, C.L., Zeng, G., Gao, L., Yu, R.K.: Molecular cloning and expression of mouse brain sialidase. Biochem. Biophys. Res. Commun. 258, 727–731 (1999)
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, 8007–8015 (2000)
Kotani, K., Kuroiwa, A., Saito, T., Matsuda, Y., Koda, T., Kijimoto-Ochiai, S.: Cloning, chromosomal mapping, and characteristic 5′-UTR sequence of murine cytosolic sialidase. Biochem. Biophys. Res. Commun. 286, 250–258 (2001)
Monti, E., Preti, A., Rossi, E., Ballabio, A., Borsani, G.: Cloning and characterization of NEU2, a human gene homologous to rodent soluble sialidases. Genomics. 57, 137–143 (1999)
Chavas, L.M., Tringali, C., Fusi, P., Venerando, B., Tettamanti, G., Kato, R., Monti, E., Wakatsuki, S.: Crystal structure of the human cytosolic sialidase Neu2. Evidence for the dynamic nature of substrate recognition. J. Biol. Chem. 280, 469–475 (2005)
Sato, K., Miyagi, T.: Involvement of an endogenous sialidase in skeletal muscle cell differentiation. Biochem. Biophys. Res. Commun. 221, 826–830 (1996)
Fanzani, A., Giuliani, R., Colombo, F., Zizioli, D., Presta, M., Preti, A., Marchesini, S.: Overexpression of cytosolic sialidase Neu2 induces myoblast differentiation in C2C12 cells. FEBS Lett. 547, 183–188 (2003)
Suzuki, N., Aoki, M., Hinuma, Y., Takahashi, T., Onodera, Y., Ishigaki, A., Kato, M., Warita, H., Tateyama, M., Itoyama, Y.: Expression profiling with progression of dystrophic change in dysferlin-deficient mice (SJL). Neurosci. Res. 52, 47–60 (2005)
Fanzani, A., Colombo, F., Giuliani, R., Preti, A., Marchesini, S.: Cytosolic sialidase Neu2 upregulation during PC12 cells differentiation. FEBS Lett. 566, 178–182 (2004)
Hata, K., Koseki, K., Yamaguchi, K., Moriya, S., Suzuki, Y., Yingsakmongkon, S., Hirai, G., Sodeoka, M., von Itzstein, M., Miyagi, T.: Limited inhibitory effects of oseltamivir and zanamivir on human sialidases. Antimicrob. Agents Chemother. 52, 3484–3491 (2008)
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, 410–415 (1997)
Funakoshi, Y., Suzuki, T.: Glycobiology in the cytosol: the bitter side of a sweet world. Biochim. Biophys. Acta. 1790, 81–94 (2009)
Meuillet, E.J., Kroes, R., Yamamoto, H., Warner, T.G., Ferrari, J., Mania-Farnell, B., George, D., Rebbaa, A., Moskal, J.R., Bremer, E.G.: Sialidase gene transfection enhances epidermal growth factor receptor activity in an epidermoid carcinoma cell line, A431. Cancer Res. 59, 234–240 (1999)
Tringali, C., Lupo, B., Anastasia, L., Papini, N., Monti, E., Bresciani, R., Tettamanti, G., Venerando, B.: Expression of sialidase Neu2 in leukemic K562 cells induces apoptosis by impairing Bcr-Abl/Src kinases signaling. J. Biol. Chem. 282, 14364–14372 (2007)
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, 5004–5011 (1999)
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, 21–27 (1999)
Monti, E., Bassi, M.T., 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, 343–351 (2000)
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, 726–732 (2001)
Papini, N., Anastasia, L., Tringali, C., Croci, G., Bresciani, R., Yamaguchi, K., Miyagi, T., Preti, A., Prinetti, A., Prioni, S., Sonnino, S., Tettamanti, G., Venerando, B., Monti, E.: The plasma membrane-associated sialidase MmNEU3 modifies the ganglioside pattern of adjacent cells supporting its involvement in cell-to-cell interactions. J. Biol. Chem. 279, 16989–16995 (2004)
Yamaguchi, K., Hata, K., Wada, T., Moriya, S., Miyagi, T.: Epidermal growth factor-induced mobilization of a ganglioside-specific sialidase (NEU3) to membrane ruffles. Biochem. Biophys. Res. Commun. 346, 484–490 (2006)
Zanchetti, G., Colombi, P., Manzoni, M., Anastasia, L., Caimi, L., Borsani, G., Venerando, B., Tettamanti, G., Preti, A., Monti, E., Bresciani, R.: Sialidase NEU3 is a peripheral membrane protein localized on the cell surface and in endosomal structures. Biochem. J. 408, 211–219 (2007)
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, 841–846 (2002)
Rodriguez, J.A., Piddini, E., Hasegawa, T., Miyagi, T., Dotti, C.G.: Plasma membrane ganglioside sialidase regulates axonal growth and regeneration in hippocampal neurons in culture. J. Neurosci. 21, 8387–8395 (2001)
Da Silva, J.S., Hasegawa, T., Miyagi, T., Dotti, C.G., Abad-Rodriguez, J.: Asymmetric membrane ganglioside sialidase activity specifies axonal fate. Nat. Neurosci. 8, 606–615 (2005)
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, 989–993 (2001)
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, 26252–26259 (2002)
Miyagi, T., Wada, T., Yamaguchi, K., Hata, K., Shiozaki, K.: Plasma membrane-associated sialidase as a crucial regulator of transmembrane signalling. J. Biochem. 144, 279–285 (2008)
Mandal, C., Tringali, C., Mondal, S., Anastasia, L., Chandra, S., Venerando, B.: Down regulation of membrane-bound Neu3 constitutes a new potential marker for childhood acute lymphoblastic leukemia and induces apoptosis suppression of neoplastic cells. Int. J. Cancer. 126, 337–349 (2010)
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. U S A. 99, 10718–10723 (2002)
Kato, K., Shiga, K., Yamaguchi, K., Hata, K., Kobayashi, T., Miyazaki, K., Saijo, S., Miyagi, T.: Plasma-membrane-associated sialidase (NEU3) differentially regulates integrin-mediated cell proliferation through laminin- and fibronectin-derived signalling. Biochem. J. 394, 647–656 (2006)
Ueno, S., Saito, S., Wada, T., Yamaguchi, K., Satoh, M., Arai, Y., Miyagi, T.: Plasma membrane-associated sialidase is up-regulated in renal cell carcinoma and promotes interleukin-6-induced apoptosis suppression and cell motility. J. Biol. Chem. 281, 7756–7764 (2006)
Kawamura, S., Sato, I., Wada, T., Yamaguchi, K., Li, Y., Li, D., Zhao, X., Ueno, S., Aoki, H., Tochigi, T., Kuwahara, M., Kitamura, T., Takahashi, K., Moriya, S., Miyagi, T.: Plasma membrane-associated sialidase (NEU3) regulates progression of prostate cancer to androgen-independent growth through modulation of androgen receptor signaling. Cell. Death Differ. 19, 170–179 (2012)
Li, X., Zhang, L., Shao, Y., Liang, Z., Shao, C., Wang, B., Guo, B., Li, N., Zhao, X., Li, Y., Xu, D.: Effects of a human plasma membrane-associated sialidase siRNA on prostate cancer invasion. Biochem. Biophys. Res. Commun. 416, 270–276 (2011)
Wada, T., Hata, K., Yamaguchi, K., Shiozaki, K., Koseki, K., Moriya, S., Miyagi, T.: A crucial role of plasma membrane-associated sialidase in the survival of human cancer cells. Oncogene. 26, 2483–2490 (2007)
Shiozaki, K., Yamaguchi, K., Sato, I., Miyagi, T.: Plasma membrane-associated sialidase (NEU3) promotes formation of colonic aberrant crypt foci in azoxymethane-treated transgenic mice. Cancer Sci. 100, 588–594 (2009)
Miyagi, T., Wada, T., Yamaguchi, K.: Roles of plasma membrane-associated sialidase NEU3 in human cancers. Biochim. Biophys. Acta. 1780, 532–537 (2008)
Comelli, E.M., Amado, M., Lustig, S.R., Paulson, J.C.: Identification and expression of Neu4, a novel murine sialidase. Gene. 321, 155–161 (2003)
Monti, E., Bassi, M.T., Bresciani, R., Civini, S., Croci, G.L., Papini, N., Riboni, M., Zanchetti, G., Ballabio, A., Preti, A., Tettamanti, G., Venerando, B., Borsani, G.: Molecular cloning and characterization of NEU4, the fourth member of the human sialidase gene family. Genomics. 83, 445–453 (2004)
Seyrantepe, V., Landry, K., Trudel, S., Hassan, J.A., Morales, C.R., Pshezhetsky, A.V.: Neu4, a novel human lysosomal lumen sialidase, confers normal phenotype to sialidosis and galactosialidosis cells. J. Biol. Chem. 279, 37021–37029 (2004)
Yamaguchi, K., Hata, K., Koseki, K., Shiozaki, K., Akita, H., Wada, T., Moriya, S., Miyagi, T.: Evidence for mitochondrial localization of a novel human sialidase (NEU4). Biochem. J. 390, 85–93 (2005)
Bigi, A., Morosi, L., Pozzi, C., Forcella, M., Tettamanti, G., Venerando, B., Monti, E., Fusi, P.: Human sialidase NEU4 long and short are extrinsic proteins bound to outer mitochondrial membrane and the endoplasmic reticulum, respectively. Glycobiology. 20, 148–157 (2010)
Shiozaki, K., Koseki, K., Yamaguchi, K., Shiozaki, M., Narimatsu, H., Miyagi, T.: Developmental change of sialidase neu4 expression in murine brain and its involvement in the regulation of neuronal cell differentiation. J. Biol. Chem. 284, 21157–21164 (2009)
Seyrantepe, V., Canuel, M., Carpentier, S., Landry, K., Durand, S., Liang, F., Zeng, J., Caqueret, A., Gravel, R.A., Marchesini, S., Zwingmann, C., Michaud, J., Morales, C.R., Levade, T., Pshezhetsky, A.V.: Mice deficient in Neu4 sialidase exhibit abnormal ganglioside catabolism and lysosomal storage. Hum. Mol. Genet. 17, 1556–1568 (2008)
Takahashi, K., Mitoma, J., Hosono, M., Shiozaki, K., Sato, C., Yamaguchi, K., Kitajima, K., Higashi, H., Nitta, K., Shima, H., Miyagi, T.: Sialidase NEU4 hydrolyzes polysialic acids of neural cell adhesion molecules and negatively regulates neurite formation by hippocampal neurons. J. Biol. Chem. in press (2012)
Hasegawa, T., Sugeno, N., Takeda, A., Matsuzaki-Kobayashi, M., Kikuchi, A., Furukawa, K., Miyagi, T., Itoyama, Y.: Role of Neu4L sialidase and its substrate ganglioside GD3 in neuronal apoptosis induced by catechol metabolites. FEBS Lett. 581, 406–412 (2007)
Malisan, F., Testi, R.: GD3 ganglioside and apoptosis. Biochim. Biophys. Acta. 1585, 179–187 (2002)
Kleene, R., Schachner, M.: Glycans and neural cell interactions. Nat. Rev. Neurosci. 5, 195–208 (2004)
Rutishauser, U.: Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat. Rev. Neurosci. 9, 26–35 (2008)
Seki, T., Arai, Y.: Distribution and possible roles of the highly polysialylated neural cell adhesion molecule (NCAM-H) in the developing and adult central nervous system. Neurosci. Res. 17, 265–290 (1993)
Angata, K., Fukuda, M.: Polysialyltransferases: major players in polysialic acid synthesis on the neural cell adhesion molecule. Biochimie. 85, 195–206 (2003)
Yamanami, H., Shiozaki, K., Wada, T., Yamaguchi, K., Uemura, T., Kakugawa, Y., Hujiya, T., Miyagi, T.: Down-regulation of sialidase NEU4 may contribute to invasive properties of human colon cancers. Cancer Sci. 98, 299–307 (2007)
Shiozaki, K., Yamaguchi, K., Takahashi, K., Moriya, S., Miyagi, T.: Regulation of Sialyl Lewis Antigen Expression in Colon Cancer Cells by Sialidase NEU4. J. Biol. Chem. 286, 21052–21061 (2011)
Tanaka, F., Otake, Y., Nakagawa, T., Kawano, Y., Miyahara, R., Li, M., Yanagihara, K., Inui, K., Oyanagi, H., Yamada, T., Nakayama, J., Fujimoto, I., Ikenaka, K., Wada, H.: Prognostic significance of polysialic acid expression in resected non-small cell lung cancer. Cancer Res. 61, 1666–16670 (2001)
Suzuki, M., Nakayama, J., Suzuki, A., Angata, K., Chen, S., Sakai, K., Hagihara, K., Yamaguchi, Y., Fukuda, M.: Polysialic acid facilitates tumor invasion by glioma cells. Glycobiology. 15, 887–894 (2005)
Tringali, C., Cirillo, F., Lamorte, G., Papini, N., Anastasia, L., Lupo, B., Silvestri, I., Tettamanti, G., Venerando, B.: NEU4L sialidase overexpression promotes beta-catenin signaling in neuroblastoma cells, enhancing stem-like malignant cell growth. Int. J. Cancer (2012) in press
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This study was supported in part by Grants-in Aid for Exploratory Research and Scientific Research on Priority Areas in Cancer from the Ministry of Education, Culture, Sports, Science and Technology of Japan.
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Miyagi, T., Takahashi, K., Hata, K. et al. Sialidase significance for cancer progression. Glycoconj J 29, 567–577 (2012). https://doi.org/10.1007/s10719-012-9394-1
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DOI: https://doi.org/10.1007/s10719-012-9394-1