The glycobiology of brain tumors: disease relevance and therapeutic potential

References

• Louis DN, Posner J, Jacobs T et al; National Cancer Institute/National Institute of Neurological Disorders and Stroke. Report of the Brain Tumor Progress Review Group. NIH, MD, USA (2000).
   Google Scholar
• Asher A, Burger PC, Demes J et al. Facts and statistics. In: A Primer of Brain Tumors: a Patient’s Reference Manual (8th Edition). American Brain Tumor Association, IL, USA (2008).
   Google Scholar
• CBTRUS (2007–2008). Primary Brain Tumors in the United States Statistical Report 2000–2004. Central Brain Tumor Registry of the United States, IL, USA (2008).
   Google Scholar
• SEER Pediatric Monograph, 1975–94, Table XXVII–7.
   Google Scholar
• Jemal A, Siegel R, Ward E et al. American Cancer Society: cancer statistics. CA Cancer J. Clin.58(2) 71–96 (2008).
   PubMed Web of Science ®Google Scholar
• Kleihues P, Louis DN, Scheithauer BW et al. The WHO classification of tumors of the nervous system. J. Neuropathol. Exp. Neurol.61(3), 215–225 (2002).
   PubMed Web of Science ®Google Scholar
• Cancer Facts and Figures 2000. American Cancer Society, GA, USA (2000).
   Google Scholar
• Yung A, Sawaya R, Curran W, Fuller G. Intracranial metastatic central nervous system tumors. In: Cancer in the Nervous System. Levin V (Ed.). Churchill Livingstone Inc., NY, USA (1996).
   Google Scholar
• CBTRUS (2002–2003). Primary Brain Tumors in the United States Statistical Report 1995–1999. Central Brain Tumor Registry of the United States, IL, USA (2003).
   Google Scholar
• Hakomori S. Glycosylation defining cancer malignancy: new wine in an old bottle. Proc. Natl Acad. Sci. USA99(16), 10231–10233 (2002).
   PubMed Web of Science ®Google Scholar
• Traylor TD, Hogan EL. Gangliosides of human cerebral astrocytomas. J. Neurochem.34(1), 126–131 (1980).
   PubMed Web of Science ®Google Scholar
• Fredman P, von Holst H, Collins VP et al. Potential ganglioside antigens associated with human gliomas. Neurol. Res.8(2), 123–126 (1986).
   PubMedGoogle Scholar
• Wikstrand CJ, He XM, Fuller GN et al. Occurrence of lacto series gangliosides 3’-isoLM1 and 3’,6’-isoLD1 in human gliomas in vitro and in vivo. J. Neuropathol. Exp. Neurol.50(6), 756–769 (1991).
   PubMed Web of Science ®Google Scholar
• Jennemann R, Mennel HD, Bauer BL, Wiegandt H. Glycosphingolipid component profiles of human gliomas correlate with histological tumour types: analysis of inter-individual and tumour-regional distribution. Acta Neurochir.126(2–4), 170–178 (1994).
   PubMed Web of Science ®Google Scholar
• Jennemann R, Rodden A, Bauer BL, Mennel HD, Wiegandt H. Glycosphingolipids of human gliomas. Cancer Res.50(23), 7444–7449 (1990).
   PubMed Web of Science ®Google Scholar
• Shinoura N, Dohi T, Kondo T, Yoshioka M, Takakura K, Oshima M. Ganglioside composition and its relation to clinical data in brain tumors. Neurosurgery31(3), 541–549 (1992).
   PubMed Web of Science ®Google Scholar
• Pan XL, Izumi T, Yamada H, Akiyoshi K, Suenobu S, Yokoyama S. Ganglioside patterns in neuroepithelial tumors of childhood. Brain Dev.22(3), 196–198 (2000).
   PubMed Web of Science ®Google Scholar
• Chang F, Li R, Noon K, Gage D, Ladisch S. Human medulloblastoma gangliosides. Glycobiology7(4), 523–530 (1997).
   PubMed Web of Science ®Google Scholar
• Markowska-Woyciechowska A, Bronowicz A, Ugorski M, Gamian E, Jablonski P. Study on ganglioside composition in brain tumours supra- and infratentorial. Neurol. Neurochir. Pol.34(6 Suppl.), 124–130 (2000).
   PubMedGoogle Scholar
• Comas TC, Tai T, Kimmel D et al. Immunohistochemical staining for ganglioside GD1b as a diagnostic and prognostic marker for primary human brain tumors. Neuro. Oncol.1(4), 261–267 (1999).
   PubMedGoogle Scholar
• Popko B, Pearl DK, Walker DM et al. Molecular markers that identify human astrocytomas and oligodendrogliomas. J. Neuropathol. Exp. Neurol.61(4), 329–338 (2002).
   PubMed Web of Science ®Google Scholar
• Hamasaki H, Aoyagi M, Kasama T, Handa S, Hirakawa K, Taki T. GT1b in human metastatic brain tumors: GT1b as a brain metastasis-associated ganglioside. Biochim. Biophys. Acta1437(1), 93–99 (1999).
   PubMed Web of Science ®Google Scholar
• Mennel HD, Lell B. Ganglioside (GD2) expression and intermediary filaments in astrocytic tumors. Clin. Neuropathol.24(1), 13–18 (2005).
   PubMed Web of Science ®Google Scholar
• Ladisch S, Chang F, Li R, Cogen P, Johnson D. Detection of medulloblastoma and astrocytoma-associated ganglioside GD3 in cerebrospinal fluid. Cancer Lett.120(1), 71–78 (1997).
   PubMed Web of Science ®Google Scholar
• Ladisch S, Wu ZL, Feig S et al. Shedding of GD2 ganglioside by human neuroblastoma. Int. J. Cancer39(1), 73–76 (1987).
   PubMed Web of Science ®Google Scholar
• Nakamura O, Iwamori M, Matsutani M, Takakura K. Ganglioside GD3 shedding by human gliomas. Acta Neurochir.109(1–2), 34–36 (1991).
   PubMed Web of Science ®Google Scholar
• Li R, Gage D, McKallip R, Ladisch S. Structural characterization and in vivo immunosuppressive activity of neuroblastoma GD2. Glycoconj. J.13(3), 385–389 (1996).
   PubMed Web of Science ®Google Scholar
• Wiranowska M, Ladd S, Smith SR, Gottschall PE. CD44 adhesion molecule and neuro-glial proteoglycan NG2 as invasive markers of glioma. Brain Cell Biol.35(2–3), 159–172 (2006).
   PubMedGoogle Scholar
• Prag S, Lepekhin EA, Kolkova K et al. NCAM regulates cell motility. J. Cell Sci.115(Pt 2), 283–292 (2002).
   PubMed Web of Science ®Google Scholar
• Sasaki H, Yoshida K, Ikeda E et al. Expression of the neural cell adhesion molecule in astrocytic tumors: an inverse correlation with malignancy. Cancer82(10), 1921–1931 (1998).
   PubMed Web of Science ®Google Scholar
• Perego C, Vanoni C, Massari S et al. Invasive behaviour of glioblastoma cell lines is associated with altered organisation of the cadherin-catenin adhesion system. J. Cell. Sci.115(Pt 16), 3331–3340 (2002).
   PubMed Web of Science ®Google Scholar
• Asano K, Duntsch CD, Zhou Q et al. Correlation of N-cadherin expression in high grade gliomas with tissue invasion. J. Neurooncol.70(1), 3–15 (2004).
   PubMed Web of Science ®Google Scholar
• Utsuki S, Sato Y, Oka H, Tsuchiya B, Suzuki S, Fujii K. Relationship between the expression of E-, N-cadherins and β-catenin and tumor grade in astrocytomas. J. Neurooncol.57(3), 187–192 (2002).
   PubMed Web of Science ®Google Scholar
• Rorive S, Belot N, Decaestecker C et al. Galectin-1 is highly expressed in human gliomas with relevance for modulation of invasion of tumor astrocytes into the brain parenchyma. Glia33(3), 241–255 (2001).
   PubMed Web of Science ®Google Scholar
• Jung TY, Jung S, Ryu HH et al. Role of galectin-1 in migration and invasion of human glioblastoma multiforme cell lines. J. Neurosurg.109(2), 273–284 (2008).
   PubMed Web of Science ®Google Scholar
• Gratsa A, Rooprai HK, Rogers JP, Martin KK, Pilkington GJ. Correlation of expression of NCAM and GD3 ganglioside to motile behaviour in neoplastic glia. Anticancer Res.17(6B), 4111–4117 (1997).
   PubMed Web of Science ®Google Scholar
• Hasan SS, Ashraf GM, Banu N. Galectins – potential targets for cancer therapy. Cancer Lett.253(1), 25–33 (2007).
   PubMed Web of Science ®Google Scholar
• Tucker GC. Integrins: molecular targets in cancer therapy. Curr. Oncol. Rep.8(2), 96–103 (2006).
   PubMedGoogle Scholar
• Paulus W, Baur I, Beutler AS, Reeves SA. Diffuse brain invasion of glioma cells requires b 1 integrins. Lab. Invest.75(6), 819–826 (1996).
   PubMed Web of Science ®Google Scholar
• Gu J, Taniguchi N. Regulation of integrin functions by N-glycans. Glycoconj. J.21(1–2), 9–15 (2004).
   PubMed Web of Science ®Google Scholar
• Zhao Y, Sato Y, Isaji T et al. Branched N-glycans regulate the biological functions of integrins and cadherins. FEBS J.275(9), 1939–1948 (2008).
   PubMed Web of Science ®Google Scholar
• Yamamoto H, Kaneko Y, Rebbaa A, Bremer EG, Moskal JR. α2,6-Sialyltransferase gene transfection into a human glioma cell line (U373 MG) results in decreased invasivity. J. Neurochem.68(6), 2566–2576 (1997).
   PubMed Web of Science ®Google Scholar
• Yamamoto H, Oviedo A, Sweeley C, Saito T, Moskal JR. α2,6-sialylation of cell-surface N-glycans inhibits glioma formation in vivo. Cancer Res.61(18), 6822–6829 (2001).
   PubMed Web of Science ®Google Scholar
• Viapiano MS, Matthews RT, Hockfield S. A novel membrane-associated glycovariant of BEHAB/brevican is up-regulated during rat brain development and in a rat model of invasive glioma. J. Biol. Chem.278(35), 33239–33247 (2003).
   PubMed Web of Science ®Google Scholar
• Viapiano MS, Bi WL, Piepmeier J, Hockfield S, Matthews RT. Novel tumor-specific isoforms of BEHAB/brevican identified in human malignant gliomas. Cancer Res.65(15), 6726–6733 (2005).
   PubMed Web of Science ®Google Scholar
• Nicholas MK, Lukas RV, Jafri NF, Faoro L, Salgia R. Epidermal growth factor receptor-mediated signal transduction in the development and therapy of gliomas. Clin. Cancer Res.12(24), 7261–7270 (2006).
   PubMed Web of Science ®Google Scholar
• Huang PH, Mukasa A, Bonavia R et al. Quantitative analysis of EGFRvIII cellular signaling networks reveals a combinatorial therapeutic strategy for glioblastoma. Proc. Natl Acad. Sci. USA104(31), 12867–12872 (2007).
   PubMed Web of Science ®Google Scholar
• Rao RD, Uhm JH, Krishnan S, James CD. Genetic and signaling pathway alterations in glioblastoma: relevance to novel targeted therapies. Front Biosci.8, E270–E280 (2003).
   Web of Science ®Google Scholar
• Guo HB, Randolph M, Pierce M. Inhibition of a specific N-glycosylation activity results in attenuation of breast carcinoma cell invasiveness-related phenotypes: inhibition of epidermal growth factor-induced dephosphorylation of focal adhesion kinase. J. Biol. Chem.282(30), 22150–22162 (2007).
   PubMed Web of Science ®Google Scholar
• Wang X, Gu J, Ihara H, Miyoshi E, Honke K, Taniguchi N. Core fucosylation regulates epidermal growth factor receptor-mediated intracellular signaling. J. Biol. Chem.281(5), 2572–2577 (2006).
   PubMed Web of Science ®Google Scholar
• Scott AM, Lee FT, Tebbutt N et al. A Phase I clinical trial with monoclonal antibody ch806 targeting transitional state and mutant epidermal growth factor receptors. Proc. Natl Acad. Sci.USA104(10), 4071–4076 (2007).
   PubMed Web of Science ®Google Scholar
• Nister M, Claesson-Welsh L, Eriksson A, Heldin CH, Westermark B. Differential expression of platelet-derived growth factor receptors in human malignant glioma cell lines. J. Biol. Chem.266(25), 16755–16763 (1991).
   PubMed Web of Science ®Google Scholar
• Fish RG. Role of gangliosides in tumour progression: a molecular target for cancer therapy? Med. Hypotheses46(2), 140–144 (1996).
   PubMed Web of Science ®Google Scholar
• Pilkington GJ. Glioma heterogeneity in vitro: the significance of growth factors and gangliosides. Neuropathol. Appl. Neurobiol.18(5), 434–442 (1992).
   PubMed Web of Science ®Google Scholar
• Yates AJ. Glycolipids and gliomas: a review. Neurochem. Pathol.8(3), 157–180 (1988).
   PubMedGoogle Scholar
• Brain Tumor Invasion. Mikkelsen T, Bjerkvig R, Laerum O, Rosenblum ML (Eds). Wiley Liss, New York, USA (1998).
   Google Scholar
• Burchell B. Genetic variation of human UDP-glucuronosyltransferase: implications in disease and drug glucuronidation. Am. J. Pharmacogenomics3(1), 37–52 (2003).
   PubMedGoogle Scholar
• Chakraborty AK, Pawelek JM. GnT-V, macrophage and cancer metastasis: a common link. Clin. Exp. Metastasis20(4), 365–373 (2003).
   PubMed Web of Science ®Google Scholar
• Dall’Olio F, Chiricolo M. Sialyltransferases in cancer. Glycoconj. J.18(11–12), 841–850 (2001).
   PubMed Web of Science ®Google Scholar
• Drinnan NB, Halliday J, Ramsdale T. Inhibitors of sialyltransferases: potential roles in tumor growth and metastasis. Mini Rev. Med. Chem.3(6), 501–517 (2003).
   PubMed Web of Science ®Google Scholar
• Kaneko Y, Yamamoto H, Kersey DS, Colley KJ, Leestma JE, Moskal JR. The expression of Gal β 1,4GlcNAc α 2,6 sialyltransferase and a 2,6-linked sialoglycoconjugates in human brain tumors. Acta Neuropathol.91(3), 284–292 (1996).
   PubMed Web of Science ®Google Scholar
• Yamamoto H, Saito T, Kaneko Y et al. α2,3-sialyltransferase mRNA and α2,3-linked glycoprotein sialylation are increased in malignant gliomas. Brain Res.755(1), 175–179 (1997).
   PubMed Web of Science ®Google Scholar
• Yamamoto H, Swoger J, Greene S et al. β1,6-N-acetylglucosamine-bearing N-glycans in human gliomas: implications for a role in regulating invasivity. Cancer Res.60(1), 134–142 (2000).
   PubMed Web of Science ®Google Scholar
• Dawson G, Moskal JR, Dawson SA. Transfection of 2,6 and 2,3-sialyltransferase genes and GlcNAc-transferase genes into human glioma cell line U-373 MG affects glycoconjugate expression and enhances cell death. J. Neurochem.89(6), 1436–1444 (2004).
   PubMed Web of Science ®Google Scholar
• Xu S, Zhu X, Zhang S et al. Over-expression of β-1,4-galactosyltransferase I, II, and V in human astrocytoma. J. Cancer Res. Clin. Oncol.127(8), 502–506 (2001).
   PubMed Web of Science ®Google Scholar
• Hoon DS, Kuo CT, Wen S et al. Ganglioside GM2/GD2 synthetase mRNA is a marker for detection of infrequent neuroblastoma cells in bone marrow. Am. J. Pathol.159(2), 493–500 (2001).
   PubMed Web of Science ®Google Scholar
• Bevilacqua M, Butcher E, Furie B et al. Selectins: a family of adhesion receptors. Cell67(2), 233 (1991).
   PubMed Web of Science ®Google Scholar
• Kjellen L, Lindahl U. Proteoglycans: structures and interactions. Annu. Rev. Biochem.60, 443–475 (1991).
   PubMed Web of Science ®Google Scholar
• Goss PE, Reid CL, Bailey D, Dennis JW. Phase IB clinical trial of the oligosaccharide processing inhibitor swainsonine in patients with advanced malignancies. Clin. Cancer Res.3(7), 1077–1086 (1997).
   PubMed Web of Science ®Google Scholar
• Becker R, Eichler MK, Jennemann R, Bertalanffy H. Phase I clinical trial on adjuvant active immunotherapy of human gliomas with GD2-conjugate. Br. J. Neurosurg.16(3), 269–275 (2002).
   PubMed Web of Science ®Google Scholar
• Fujimoto Y, Izumoto S, Suzuki T et al. Ganglioside GM3 inhibits proliferation and invasion of glioma. J. Neurooncol.71(2), 99–106 (2005).
   PubMed Web of Science ®Google Scholar
• Ishikawa D, Kikkawa H, Ogino K, Hirabayashi Y, Oku N, Taki T. GD1α-replica peptides functionally mimic GD1α, an adhesion molecule of metastatic tumor cells, and suppress the tumor metastasis. FEBS Lett.441(1), 20–24 (1998).
   PubMed Web of Science ®Google Scholar
• Hanessian S, Zhan L, Bovey R, Saavedra OM, Juillerat-Jeanneret L. Functionalized glycomers as growth inhibitors and inducers of apoptosis in human glioblastoma cells. J. Med. Chem.46(17), 3600–3611 (2003).
   PubMed Web of Science ®Google Scholar
• Abad-Rodriguez J, Bernabe M, Romero-Ramirez L, Vallejo-Cremades M, Fernandez-Mayoralas A, Nieto-Sampedro M. Purification and structure of neurostatin, an inhibitor of astrocyte division of mammalian brain. J. Neurochem.74(6), 2547–2556 (2000).
   PubMed Web of Science ®Google Scholar
• Aguilera B, Romero-Ramirez L, Abad-Rodriguez J, Corrales G, Nieto-Sampedro M, Fernandez-Mayoralas A. Novel disaccharide inhibitors of human glioma cell division. J. Med. Chem.41(23), 4599–4606 (1998).
   PubMed Web of Science ®Google Scholar
• Vallejo-Cremades M, Nieto-Sampedro M. Neurostatin: cellular sources and cellular targets of the inhibitor. Neuron Glia. Biol.2(2), 115–123 (2006).
   PubMedGoogle Scholar
• Rebbaa A, Chou PM, Bremer EG. Modulation of growth factor response in brain tumors by complex carbohydrates. Bull. Cancer91(4), E15–E60 (2004).
   PubMed Web of Science ®Google Scholar
• Hakomori S. Tumor malignancy defined by aberrant glycosylation and sphingo(glyco)lipid metabolism. Cancer Res.56(23), 5309–5318 (1996).
   PubMed Web of Science ®Google Scholar
• Harduin-Lepers A, Mollicone R, Delannoy P, Oriol R. The animal sialyltransferases and sialyltransferase-related genes: a phylogenetic approach. Glycobiology15(8), 805–817 (2005).
   PubMed Web of Science ®Google Scholar
• Harduin-Lepers A, Vallejo-Ruiz V, Krzewinski-Recchi MA, Samyn-Petit B, Julien S, Delannoy P. The human sialyltransferase family. Biochimie83(8), 727–737 (2001).
   PubMed Web of Science ®Google Scholar
• Kitagawa H, Paulson JC. Differential expression of five sialyltransferase genes in human tissues. J. Biol. Chem.269(27), 17872–17878 (1994).
   PubMed Web of Science ®Google Scholar
• Recchi MA, Hebbar M, Hornez L, Harduin-Lepers A, Peyrat JP, Delannoy P. Multiplex reverse transcription polymerase chain reaction assessment of sialyltransferase expression in human breast cancer. Cancer Res.58(18), 4066–4070 (1998).
   PubMed Web of Science ®Google Scholar
• Peyrat JP, Recchi MA, Hebbar M et al. Regulation of sialyltransferase expression by estradiol and 4-OH-tamoxifen in the human breast cancer cell MCF-7. Mol. Cell Biol. Res. Commun.3(1), 48–52 (2000).
   PubMedGoogle Scholar
• Julien S, Krzewinski-Recchi MA, Harduin-Lepers A et al. Expression of sialyl-Tn antigen in breast cancer cells transfected with the human CMP-Neu5Ac: GalNAc α2,6-sialyltransferase (ST6GalNac I) cDNA. Glycoconj. J.18(11–12), 883–893 (2001).
   PubMed Web of Science ®Google Scholar
• Marcos NT, Pinho S, Grandela C et al. Role of the human ST6GalNAc-I and ST6GalNAc-II in the synthesis of the cancer-associated sialyl-Tn antigen. Cancer Res.64(19), 7050–7057 (2004).
   PubMed Web of Science ®Google Scholar
• Grimes WJ. Glycosyltransferase and sialic acid levels of normal and transformed cells. Biochemistry12(5), 990–996 (1973).
   PubMed Web of Science ®Google Scholar
• Nicolson GL. Cancer metastasis. Organ colonization and the cell-surface properties of malignant cells. Biochim. Biophys. Acta695(2), 113–176 (1982).
   PubMed Web of Science ®Google Scholar
• Roth J. Cellular sialoglycoconjugates: a histochemical perspective. Histochem. J.25(10), 687–710 (1993).
   PubMedGoogle Scholar
• Schirrmacher V, Altevogt P, Fogel M et al. Importance of cell surface carbohydrates in cancer cell adhesion, invasion and metastasis: does sialic acid direct metastatic behaviour? Invasion Metastasis2, 313–360 (1982).
   Google Scholar
• Varki A. Biological roles of oligosaccharides: all of the theories are correct. Glycobiology3(2), 97–130 (1993).
   PubMed Web of Science ®Google Scholar
• Warren L, Fuhrer JP, Buck CA. Surface glycoproteins of normal and transformed cells: a difference determined by sialic acid and a growth-dependent sialyl transferase. Proc. Natl Acad. Sci. USA69(7), 1838–1842 (1972).
   PubMed Web of Science ®Google Scholar
• 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(7), 3521–3527 (1986).
   PubMed Web of Science ®Google Scholar
• 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(16), 7591–7603 (1988).
   PubMed Web of Science ®Google Scholar
• Werkmeister JA, Pross HF, Roder JC. Modulation of K562 cells with sodium butyrate: association of impaired NK susceptibility with sialic acid and analysis of other parameters. Int. J. Cancer32(1), 71–78 (1983).
   PubMed Web of Science ®Google Scholar
• Broquet P, Baubichon-Cortay H, George P, Peschard MJ, Louisot P. Effect of desipramine on a glycoprotein sialyltransferase activity in C6 cultured glioma cells. J. Neurochem.54(2), 388–394 (1990).
   PubMed Web of Science ®Google Scholar
• Broquet P, George P, Geoffroy J, Reboul P, Louisot P. Study of O-glycan sialylation in C6 cultured glioma cells: evidence for post-translational regulation of a β-galactoside α 2,3 sialyltransferase activity by N-glycosylation. Biochem. Biophys. Res. Commun.178(3), 1437–1443 (1991).
   PubMed Web of Science ®Google Scholar
• Moskal JR, Gardner DA, Basu S. Changes in glycolipid glycosyltransferases and glutamate decarboxylase and their relationship to differentiation in neuroblastoma cells. Biochem. Biophys. Res. Commun.61(2), 751–758 (1974).
   PubMed Web of Science ®Google Scholar
• Reboul P, Broquet P, George P, Louisot P. Effect of retinoic acid on two glycosyltransferase activities in C6 cultured glioma cells. Int. J. Biochem.22(8), 889–893 (1990).
   PubMedGoogle Scholar
• Stoykova LI, Glick MC. Purification of an α-2,8-sialyltransferase, a potential initiating enzyme for the biosynthesis of polysialic acid in human neuroblastoma cells. Biochem. Biophys. Res. Commun.217(3), 777–783 (1995).
   PubMed Web of Science ®Google Scholar
• Shen AL, Chou MD, Chi CW, Lee LS. Alterations in serum sialyltransferase activities in patients with brain tumors. Surg. Neurol.22(5), 509–514 (1984).
   PubMedGoogle Scholar
• Gornati R, Basu S, Montorfano G, Berra B. Glycosyltransferase activities in human meningiomas: preliminary results. Cancer Biochem. Biophys.15(1), 1–10 (1995).
   PubMedGoogle Scholar
• Yamamoto H, Kaneko Y, Vandermulen D et al. The expression of CMP-NeuAc: Gal β 1,4GlcNAc α 2,6 sialyltransferase [EC 2.4.99.1] and glycoproteins bearing αp 2,6-linked sialic acids in human brain tumours. Glycoconj. J.12(6), 848–856 (1995).
   PubMed Web of Science ®Google Scholar
• Wen DX, Livingston BD, Medzihradszky KF, Kelm S, Burlingame AL, Paulson JC. Primary structure of Gal β 1,3(4)GlcNAc α 2,3-sialyltransferase determined by mass spectrometry sequence analysis and molecular cloning. Evidence for a protein motif in the sialyltransferase gene family. J. Biol. Chem.267(29), 21011–21019 (1992).
   PubMed Web of Science ®Google Scholar
• Dennis JW, Granovsky M, Warren CE. Glycoprotein glycosylation and cancer progression. Biochim. Biophys. Acta1473(1), 21–34 (1999).
   PubMed Web of Science ®Google Scholar
• Varki A. Glycosylation changes in cancer. In: Essentials of Glycobiology. Varki A, Cummings R, Esko J, Freeze H, Hart G, Marth J. (Eds). Cold Spring Harbor Laboratory Press, NY, USA 535–549 (1999).
   Google Scholar
• Luo J, Isaacs WB, Trent JM, Duggan DJ. Looking beyond morphology: cancer gene expression profiling using DNA microarrays. Cancer Invest.21(6), 937–949 (2003).
   PubMed Web of Science ®Google Scholar
• Luo Z, Geschwind DH. Microarray applications in neuroscience. Neurobiol. Dis.8(2), 183–193 (2001).
   PubMed Web of Science ®Google Scholar
• Russo G, Zegar C, Giordano A. Advantages and limitations of microarray technology in human cancer. Oncogene22(42), 6497–6507 (2003).
   PubMed Web of Science ®Google Scholar
• Kemmner W, Roefzaad C, Haensch W, Schlag PM. Glycosyltransferase expression in human colonic tissue examined by oligonucleotide arrays. Biochim. Biophys. Acta1621(3), 272–279 (2003).
   PubMed Web of Science ®Google Scholar
• Kroes RA, Panksepp J, Burgdorf J, Otto NJ, Moskal JR. Modeling depression: social dominance-submission gene expression patterns in rat neocortex. Neuroscience137(1), 37–49 (2006).
   PubMed Web of Science ®Google Scholar
• Russell & Rubinstein’s; Pathology of Tumors of the Nervous System, Sixth Edition. Bigner DD, McLendon RE, Bruner JM (Eds). Arnold, NY, USA (1998).
   Google Scholar
• Churchill GA. Fundamentals of experimental design for cDNA microarrays. Nat. Genet.32(Suppl.), 490–495 (2002).
   PubMed Web of Science ®Google Scholar
• Kroes RA, Dawson G, Moskal JR. Focused microarray analysis of glycogene expression in human glioblastomas. J. Neurochem.103(Suppl. 1), 14–24 (2007).
   PubMed Web of Science ®Google Scholar
• Chen RZ, Pettersson U, Beard C, Jackson-Grusby L, Jaenisch R. DNA hypomethylation leads to elevated mutation rates. Nature395(6697), 89–93 (1998).
   PubMed Web of Science ®Google Scholar
• Gonzalo S, Jaco I, Fraga MF et al. DNA methyltransferases control telomere length and telomere recombination in mammalian cells. Nat. Cell Biol.8(4), 416–424 (2006).
   PubMed Web of Science ®Google Scholar
• Hansen RS, Wijmenga C, Luo P et al. The DNMT3B DNA methyltransferase gene is mutated in the ICF immunodeficiency syndrome. Proc. Natl Acad. Sci. USA96(25), 14412–14417 (1999).
   PubMed Web of Science ®Google Scholar
• Maraschio P, Zuffardi O, Dalla Fior T, Tiepolo L. Immunodeficiency, centromeric heterochromatin instability of chromosomes 1, 9, and 16, and facial anomalies: the ICF syndrome. J. Med. Genet.25(3), 173–180 (1988).
   PubMed Web of Science ®Google Scholar
• Okano M, Bell DW, Haber DA, Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell99(3), 247–257 (1999).
   PubMed Web of Science ®Google Scholar
• Trasler JM, Trasler DG, Bestor TH, Li E, Ghibu F. DNA methyltransferase in normal and Dnmtn/Dnmtn mouse embryos. Dev. Dyn.206(3), 239–247 (1996).
   PubMed Web of Science ®Google Scholar
• Xu GL, Bestor TH, Bourc’his D et al. Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature402(6758), 187–191 (1999).
   PubMed Web of Science ®Google Scholar
• Costello JF. DNA methylation in brain development and gliomagenesis. Front. Biosci.8, S175–S184 (2003).
   Google Scholar
• Fan G, Beard C, Chen RZ et al. DNA hypomethylation perturbs the function and survival of CNS neurons in postnatal animals. J. Neurosci.21(3), 788–797 (2001).
   PubMed Web of Science ®Google Scholar
• Kawai J, Hirotsune S, Hirose K, Fushiki S, Watanabe S, Hayashizaki Y. Methylation profiles of genomic DNA of mouse developmental brain detected by restriction landmark genomic scanning (RLGS) method. Nucleic Acids Res.21(24), 5604–5608 (1993).
   PubMed Web of Science ®Google Scholar
• Kazazian HH Jr, Moran JV. The impact of L1 retrotransposons on the human genome. Nat. Genet.19(1), 19–24 (1998).
   PubMed Web of Science ®Google Scholar
• Li E, Bestor TH, Jaenisch R. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell69(6), 915–926 (1992).
   PubMed Web of Science ®Google Scholar
• Takizawa T, Nakashima K, Namihira M et al. DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev. Cell1(6), 749–758 (2001).
   PubMed Web of Science ®Google Scholar
• Baylin S, Bestor TH. Altered methylation patterns in cancer cell genomes: cause or consequence? Cancer Cell1(4), 299–305 (2002).
   PubMed Web of Science ®Google Scholar
• Costello JF, Plass C. Methylation matters. J. Med. Genet.38(5), 285–303 (2001).
   PubMed Web of Science ®Google Scholar
• Feinberg AP. Cancer epigenetics is no mickey mouse. Cancer Cell8(4), 267–268 (2005).
   PubMed Web of Science ®Google Scholar
• Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat. Rev. Genet.3(6), 415–428 (2002).
   PubMed Web of Science ®Google Scholar
• Kawamura YI, Toyota M, Kawashima R et al. DNA hypermethylation contributes to incomplete synthesis of carbohydrate determinants in gastrointestinal cancer. Gastroenterology135(1), 142–151 E143 (2008).
   PubMed Web of Science ®Google Scholar
• Kunwar S, Prados MD, Chang SM et al. Direct intracerebral delivery of cintredekin besudotox (IL13-PE38QQR) in recurrent malignant glioma: a report by the Cintredekin Besudotox Intraparenchymal study group. J. Clin. Oncol.25(7), 837–844 (2007).
   PubMed Web of Science ®Google Scholar
• Sonabend AM, Ulasov IV, Lesniak MS. Conditionally replicative adenoviral vectors for malignant glioma. Rev. Med. Virol.16(2), 99–115 (2006).
   PubMed Web of Science ®Google Scholar
• Piao Y, Jiang H, Alemany R et al. Oncolytic adenovirus retargeted to δ-EGFR induces selective antiglioma activity. Cancer Gene Ther.16(3), 256–265 (2009).
   PubMed Web of Science ®Google Scholar
• Fueyo J, Alemany R, Gomez-Manzano C et al. Preclinical characterization of the antiglioma activity of a tropism-enhanced adenovirus targeted to the retinoblastoma pathway. J. Natl Cancer Inst.95(9), 652–660 (2003).
   PubMed Web of Science ®Google Scholar
• Fueyo J, Gomez-Manzano C, Alemany R et al. A mutant oncolytic adenovirus targeting the Rb pathway produces anti-glioma effect in vivo. Oncogene19(1), 2–12 (2000).
   PubMed Web of Science ®Google Scholar
• Paulson JC, Weinstein J, Schauer A. Tissue-specific expression of sialyltransferases. J. Biol. Chem.264(19), 10931–10934 (1989).
   PubMed Web of Science ®Google Scholar
• Alavi A, Axford JS. Sweet and sour: the impact of sugars on disease. Rheumatology (Oxford)47(6), 760–770 (2008).
   PubMed Web of Science ®Google Scholar
• Jefferis R. Glycosylation as a strategy to improve antibody-based therapeutics. Nat. Rev. Drug Discov.8(3), 226–234 (2009).
   PubMed Web of Science ®Google Scholar
• Tarp MA, Clausen H. Mucin-type O-glycosylation and its potential use in drug and vaccine development. Biochim. Biophys. Acta1780(3), 546–563 (2008).
   PubMed Web of Science ®Google Scholar