Polysialic Acid Directs Tumor Cell Growth by Controlling Heterophilic Neural Cell Adhesion Molecule Interactions

REFERENCES

• Amoureux, M. C., B. A. Cunningham, G. M. Edelman, and K. L. Crossin. 2000. N-CAM binding inhibits the proliferation of hippocampal progenitor cells and promotes their differentiation to a neuronal phenotype. J. Neurosci. 20: 3631–3640.
   PubMedGoogle Scholar
• Aubert, I., J. L. Ridet, and F. H. Gage. 1995. Regeneration in the adult mammalian CNS: guided by development. Curr. Opin. Neurobiol. 5: 625–635.
   PubMed Web of Science ®Google Scholar
• Cavallaro, U., J. Niedermeyer, M. Fuxa, and G. Christofori. 2001. N-CAM modulates tumour-cell adhesion to matrix by inducing fibroblast growth factor-receptor signalling. Nat. Cell Biol. 3: 650–657.
   PubMed Web of Science ®Google Scholar
• Cole, G. J., and R. Akeson. 1989. Identification of a heparin binding domain of the neural cell adhesion molecule N-CAM with synthetic peptides. Neuron 2: 1157–1165.
   PubMed Web of Science ®Google Scholar
• Crossin, K. L., and L. A. Krushel. 2000. Cellular signaling by neural cell adhesion molecules of the immunoglobulin superfamily. Dev. Dyn. 218: 260–279.
   PubMed Web of Science ®Google Scholar
• Cunningham, B. A., J. J. Hemperly, B. A. Murray, E. A. Prediger, R. Brackenbury, and G. M. Edelman. 1987. Neural cell adhesion molecule: structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing. Science 236: 799–806.
   PubMed Web of Science ®Google Scholar
• Daniel, L., P. Durbec, E. Gautherot, E. Rouvier, G. Rougon, and D. Figarella-Branger. 2001. A nude mice model of human rhabdomyosarcoma lung metastases for evaluating the role of polysialic acids in the metastatic process. Oncogene 20: 997–1004.
   PubMedGoogle Scholar
• Daniel, L., J. Trouillas, W. Renaud, P. Chevallier, J. Gouvernet, G. Rougon, and D. Figarella-Branger. 2000. Polysialylated-neural cell adhesion molecule expression in rat pituitary transplantable tumors (spontaneous mammotropic transplantable tumor in Wistar-Furth rats) is related to growth rate and malignancy. Cancer Res. 60: 80–85.
   PubMed Web of Science ®Google Scholar
• Durbec, P., and H. Cremer. 2001. Revisiting the function of PSA-NCAM in the nervous system. Mol. Neurobiol. 24: 53–64.
   PubMed Web of Science ®Google Scholar
• Eckhardt, M., M. Mühlenhoff, A. Bethe, J. Koopman, M. Frosch, and R. Gerardy-Schahn. 1995. Molecular characterization of eukaryotic polysialyltransferase- 1. Nature 373: 715–718.
   Google Scholar
• Figarella Branger, D. F., P. L. Durbec, and G. N. Rougon. 1990. Differential spectrum of expression of neural cell adhesion molecule isoforms and L1 adhesion molecules on human neuroectodermal tumors. Cancer Res. 50: 6364–6370.
   PubMedGoogle Scholar
• Frosch, M., I. Gorgen, G. J. Boulnois, K. N. Timmis, and D. Bitter-Suermann. 1985. NZB mouse system for production of monoclonal antibodies to weak bacterial antigens: isolation of an IgG antibody to the polysaccharide capsules of Escherichia coli K1 and group B meningococci. Proc. Natl. Acad. Sci. USA 82: 1194–1198.
   PubMed Web of Science ®Google Scholar
• Fujimoto, I., J. L. Bruses, and U. Rutishauser. 2001. Regulation of cell adhesion by polysialic acid: Effects on cadherin, IgCAM and integrin function and independence from NCAM binding or signaling activity. J. Biol. Chem. 276: 31745–31751.
   PubMed Web of Science ®Google Scholar
• Fukuda, M. 1996. Possible roles of tumor-associated carbohydrate antigens. Cancer Res. 56: 2237–2244.
   PubMed Web of Science ®Google Scholar
• Gerardy-Schahn, R., A. Bethe, T. Brennecke, M. Mühlenhoff, M. Eckhardt, S. Ziesing, F. Lottspeich, and M. Frosch. 1995. Molecular cloning and functional expression of bacteriophage PK1E-encoded endoneuraminidase Endo NE. Mol. Microbiol. 16: 441–450.
   PubMedGoogle Scholar
• Glüer, S., C. Schelp, N. Madry, D. Von Schweinitz, M. Eckhardt, and R. Gerardy-Schahn. 1998. Serum polysialylated neural cell adhesion molecule in childhood neuroblastoma. Br. J. Cancer 78: 106–110.
   PubMedGoogle Scholar
• Glüer, S., C. Schelp, D. Von Schweinitz, and R. Gerardy-Schahn. 1998. Polysialylated neural cell adhesion molecule in childhood rhabdomyosarcoma. Pediatr. Res. 43: 145–147.
   PubMedGoogle Scholar
• Hall, A. K., R. Nelson, and U. Rutishauser. 1990. Binding properties of detergent-solubilized NCAM. J. Cell Biol. 110: 817–824.
   PubMedGoogle Scholar
• Hildebrandt, H., C. Becker, S. Glüer, H. Rüsner, R. Gerardy-Schahn, and H. Rahmann. 1998. Polysialic acid on the neural cell adhesion molecule correlates with expression of polysialyltransferases and promotes neuroblastoma cell growth. Cancer Res. 58: 779–784.
   PubMedGoogle Scholar
• Hoffman, S., and G. M. Edelman. 1983. Kinetics of homophilic binding by embryonic and adult forms of neural cell adhesion molecule. Proc. Natl. Acad. Sci. USA 80: 5762–5766.
   PubMed Web of Science ®Google Scholar
• Horstkorte, R., M. Schachner, J. P. Magyar, T. Vorherr, and B. Schmitz. 1993. The fourth immunoglobulin-like domain of NCAM contains a carbohydrate recognition domain for oligomannosidic glycans implicated in association with L1 and neurite outgrowth. J. Cell Biol. 121: 1409–1421.
   PubMed Web of Science ®Google Scholar
• Joliot, A. H., A. Triller, M. Volovitch, C. Pernelle, and A. Prochiantz. 1991. alpha-2, 8-Polysialic acid is the neuronal surface receptor of antennapedia homeobox peptide. New Biol. 3: 1121–1134.
   PubMedGoogle Scholar
• Kaplan, D. R., K. Matsumoto, E. Lucarelli, and C. J. Thiele. 1993. Induction of TrkB by retinoic acid mediates biologic responsiveness to BDNF and differentiation of human neuroblastoma cells. Neuron 11: 321–331.
   PubMed Web of Science ®Google Scholar
• Kolkova, K., V. Novitskaya, N. Pedersen, V. Berezin, and E. Bock. 2000. Neural cell adhesion molecule-stimulated neurite outgrowth depends on activation of protein kinase C and the ras-mitogen-activated protein kinase pathway. J. Neurosci. 20: 2238–2246.
   PubMed Web of Science ®Google Scholar
• Kolkova, K., N. Pedersen, V. Berezin, and E. Bock. 2000. Identification of an amino acid sequence motif in the cytoplasmic domain of the NCAM-140-kDa isoform essential for its neuritogenic activity. J. Neurochem. 75: 1274–1282.
   PubMed Web of Science ®Google Scholar
• Kürtje, K. H., U. Paulus, M. Ibsch, and H. Rahmann. 1996. Imaging of thick sections of nervous tissue with energy-filtering transmission electron microscopy. J. Microsc. 183: 89–101.
   PubMedGoogle Scholar
• Krushel, L. A., M. H. Tai, B. A. Cunningham, G. M. Edelman, and K. L. Crossin. 1998. Neural cell adhesion molecule (N-CAM) domains and intracellular signaling pathways involved in the inhibition of astrocyte proliferation. Proc. Natl. Acad. Sci. USA 95: 2592–2596.
   PubMed Web of Science ®Google Scholar
• Marshall, C. J. 1995. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80: 179–185.
   PubMed Web of Science ®Google Scholar
• Moolenaar, C. E., E. J. Muller, D. J. Schol, C. G. Figdor, E. Bock, D. Bitter-Suermann, and R. J. Michalides. 1990. Expression of neural cell adhesion molecule-related sialoglycoprotein in small cell lung cancer and neuroblastoma cell lines H69 and CHP-212. Cancer Res. 50: 1102–1106.
   PubMed Web of Science ®Google Scholar
• Mühlenhoff, M., M. Eckhardt, and R. Gerardy-Schahn. 1998. Polysialic acid: three-dimensional structure, biosynthesis and function. Curr. Opin. Struct. Biol. 8: 558–564.
   PubMed Web of Science ®Google Scholar
• Mujoo, K., T. J. Kipps, H. M. Yang, D. A. Cheresh, U. Wargalla, D. J. Sander, and R. A. Reisfeld. 1989. Functional properties and effect on growth suppression of human neuroblastoma tumors by isotype switch variants of monoclonal antiganglioside GD2 antibody 14.18. Cancer Res. 49: 2857–2861.
   PubMed Web of Science ®Google Scholar
• Nait-Oumesmar, B., L. Decker, F. Lachapelle, V. Avellana-Adalid, C. Bachelin, and A. B. Van Evercooren. 1999. Progenitor cells of the adult mouse subventricular zone proliferate, migrate and differentiate into oligodendrocytes after demyelination. Eur. J. Neurosci. 11: 4357–4366.
   PubMed Web of Science ®Google Scholar
• Nakayama, J., M. N. Fukuda, B. Fredette, B. Ranscht, and M. Fukuda. 1995. Expression cloning of a human polysialyltransferase that forms the polysialylated neural cell adhesion molecule present in embryonic brain. Proc. Natl. Acad. Sci. USA 92: 7031–7035.
   PubMed Web of Science ®Google Scholar
• Niethammer, P., M. Delling, V. Sytnyk, A. Dityatev, K. Fukami, and M. Schachner. 2002. Cosignaling of NCAM via lipid rafts and the fibroblast growth factor receptor is required for neuritogenesis. J. Cell Biol. 157: 521–532.
   PubMed Web of Science ®Google Scholar
• Pahlman, S., J. C. Hoehner, E. Nanberg, F. Hedborg, S. Fagerstrom, C. Gestblom, I. Johansson, U. Larsson, E. Lavenius, E. Ortoft, et al. 1995. Differentiation and survival influences of growth factors in human neuroblastoma. Eur. J. Cancer 31A: 453–458.
   PubMed Web of Science ®Google Scholar
• Perl, A. K., U. Dahl, P. Wilgenbus, H. Cremer, H. Semb, and G. Christofori. 1999. Reduced expression of neural cell adhesion molecule induces metastatic dissemination of pancreatic beta tumor cells. Nat. Med. 5: 286–291.
   PubMedGoogle Scholar
• Prag, S., E. A. Lepekhin, K. Kolkova, R. Hartmann-Petersen, A. Kawa, P. S. Walmod, V. Belman, H. C. Gallagher, V. Berezin, E. Bock, and N. Pedersen. 2002. NCAM regulates cell motility. J. Cell Sci. 115: 283–292.
   PubMed Web of Science ®Google Scholar
• Rabinowitz, J. E., U. Rutishauser, and T. Magnuson. 1996. Targeted mutation of Ncam to produce a secreted molecule results in a dominant embryonic lethality. Proc. Natl. Acad. Sci. USA 93: 6421–6424.
   PubMedGoogle Scholar
• Ronn, L. C., M. Olsen, S. Ostergaard, V. Kiselyov, V. Berezin, M. T. Mortensen, M. H. Lerche, P. H. Jensen, V. Soroka, J. L. Saffells, P. Doherty, F. M. Poulsen, E. Bock, and A. Holm. 1999. Identification of a neuritogenic ligand of the neural cell adhesion molecule with a combinatorial library of synthetic peptides. Nat. Biotechnol. 17: 1000–1005.
   PubMed Web of Science ®Google Scholar
• Rudolph, G., K. Schilbach-Stuckle, R. Handgretinger, P. Kaiser, and H. Hameister. 1991. Cytogenetic and molecular characterization of a newly established neuroblastoma cell line LS. Hum. Genet. 86: 562–566.
   PubMedGoogle Scholar
• Rutishauser, U., and L. Landmesser. 1996. Polysialic acid in the vertebrate nervous system — a promoter of plasticity in cell-cell interactions. Trends Neurosci. 19: 422–427.
   PubMed Web of Science ®Google Scholar
• Saffell, J. L., E. J. Williams, I. J. Mason, F. S. Walsh, and P. Doherty. 1997. Expression of a dominant negative fibroblast growth factor receptor inhibits axonal growth and fibroblast growth factor receptor phosphorylation stimulated by CAMs. Neuron. 18: 231–242.
   PubMedGoogle Scholar
• Schmid, R. S., R. D. Graff, M. D. Schaller, S. Chen, M. Schachner, J. J. Hemperly, and P. F. Maness. 1999. NCAM stimulates the Ras-MAPK pathway and CREB phosphorylation in neuronal cells. J. Neurobiol. 38: 542–558.
   PubMedGoogle Scholar
• Seidenfaden, R., R. Gerardy-Schahn, and H. Hildebrandt. 2000. Control of NCAM polysialylation by the differential expression of polysialytransferases ST8SiaII and ST8SiaIV. Eur. J. Cell Biol. 79: 680–688.
   PubMedGoogle Scholar
• Seidenfaden, R., and H. Hildebrandt. 2001. Retinoic acid-induced changes in NCAM polysialylation and polysialyltransferase mRNA expression of human neuroblastoma cells. J. Neurobiol. 46: 11–28.
   PubMedGoogle Scholar
• Sharma, M., P. Sharma, and H. C. Pant. 1999. CDK-5-mediated neurofilament phosphorylation in SHSY5Y human neuroblastoma cells. J. Neurochem. 73: 79–86.
   PubMedGoogle Scholar
• Storms, S. D., and U. Rutishauser. 1998. A role for polysialic acid in neural cell adhesion molecule heterophilic binding to proteoglycans. J. Biol. Chem. 273: 27124–27129.
   PubMedGoogle Scholar
• Tanaka, F., Y. Otake, T. Nakagawa, Y. Kawano, R. Miyahara, M. Li, K. Yanagihara, K. Inui, H. Oyanagi, T. Yamada, J. Nakayama, I. Fujimoto, K. Ikenaka, and H. Wada. 2001. Prognostic significance of polysialic acid expression in resected nonsmall cell lung cancer. Cancer Res. 61: 1666–1670.
   PubMedGoogle Scholar
• Vutskits, L., Z. Djebbara-Hannas, H. Zhang, J. P. Paccaud, P. Durbec, G. Rougon, D. Muller, and J. Z. Kiss. 2001. PSA-NCAM modulates BDNF-dependent survival and differentiation of cortical neurons. Eur. J. Neurosci. 13: 1391–1402.
   PubMed Web of Science ®Google Scholar