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Journal of Oncology
Volume 2010 (2010), Article ID 961243, 8 pages
Ganglioside GM3 Is Antiangiogenic in Malignant Brain Cancer
Department of Biology, Boston College, Chestnut Hill, MA 02467, USA
Received 17 December 2009; Revised 12 March 2010; Accepted 10 April 2010
Academic Editor: Arkadiusz Dudek
Copyright © 2010 Thomas N. Seyfried and Purna Mukherjee. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
- J. K. Lowry, J. J. Snyder, and P. W. Lowry, “Brain tumors in the elderly: recent trends in a Minnesota cohort study,” Archives of Neurology, vol. 55, no. 7, pp. 922–928, 1998.
- J. Kaiser, “No meeting of minds on childhood cancer,” Science, vol. 286, no. 5446, pp. 1832–1834, 1999.
- P. Kaatsch, C. H. Rickert, J. Kühl, J. Schüz, and J. Michaelis, “Population-based epidemiologic data on brain tumors in German children,” Cancer, vol. 92, no. 12, pp. 3155–3164, 2001.
- P. J. Jukich, B. J. McCarthy, T. S. Surawicz, S. Freels, and F. G. Davis, “Trends in incidence of primary brain tumors in the United States, 1985–1994,” Neuro-Oncology, vol. 3, no. 3, pp. 141–151, 2001.
- H. Sontheimer, “A role for glutamate in growth and invasion of primary brain tumors,” Journal of Neurochemistry, vol. 105, no. 2, pp. 287–295, 2008.
- C.-L. Tso, P. Shintaku, J. Chen, et al., “Primary glioblastomas express mesenchymal stem-like properties,” Molecular Cancer Research, vol. 4, no. 9, pp. 607–619, 2006.
- L. E. Abate, P. Mukherjee, and T. N. Seyfried, “Gene-linked shift in ganglioside distribution influences growth and vascularity in a mouse astrocytoma,” Journal of Neurochemistry, vol. 98, no. 6, pp. 1973–1984, 2006.
- D. Zagzag, M. Esencay, O. Mendez, et al., “Hypoxia- and vascular endothelial growth factor-induced stromal cell-derived factor-1/CXCR4 expression in glioblastomas: one plausible explanation of Scherer's structures,” American Journal of Pathology, vol. 173, no. 2, pp. 545–560, 2008.
- M. Kirsch, G. Schackert, and P. M. Black, “Anti-angiogenic treatment strategies for malignant brain tumors,” Journal of Neuro-Oncology, vol. 50, no. 1-2, pp. 149–163, 2000.
- H. Bai, J. Orlando, and T. N. Seyfried, “Altered ganglioside composition in virally transformed rat embryo fibroblast,” Biochimica et Biophysica Acta, vol. 1136, no. 1, pp. 23–27, 1992.
- M. El-Abbadi, T. N. Seyfried, A. J. Yates, C. Orosz, and M. C. Lee, “Ganglioside composition and histology of a spontaneous metastatic brain tumour in the VM mouse,” British Journal of Cancer, vol. 85, no. 2, pp. 285–292, 2001.
- S. Hakomori, “Glycosylation defining cancer malignancy: new wine in an old bottle,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 16, pp. 10231–10233, 2002.
- H.-J. Choi, T.-W. Chung, S.-K. Kang, et al., “Ganglioside GM3 modulates tumor suppressor PTEN-mediated cell cycle progression—transcriptional induction of and by inhibition of PI-3K/AKT pathway,” Glycobiology, vol. 16, no. 7, pp. 573–583, 2006.
- H. Bai and T. N. Seyfried, “Influence of ganglioside GM3 and high density lipoprotein on the cohesion of mouse brain tumor cells,” Journal of Lipid Research, vol. 38, no. 1, pp. 160–172, 1997.
- A. J. Yates and A. Rampersaud, “Sphingolipids as receptor modulators: an overview,” Annals of the New York Academy of Sciences, vol. 845, pp. 57–71, 1998.
- T. N. Seyfried, R. K. Yu, M. Saito, and M. Albert, “Ganglioside composition of an experimental mouse brain tumor,” Cancer Research, vol. 47, no. 13, pp. 3538–3542, 1987.
- J. A. Ecsedy, K. A. Holthaus, H. C. Yohe, and T. N. Seyfried, “Expression of mouse sialic acid on gangliosides of a human glioma grown as a xenograft in SCID mice,” Journal of Neurochemistry, vol. 73, no. 1, pp. 254–259, 1999.
- H.-H. Chou, H. Takematsu, S. Diaz, et al., “A mutation in human CMP-sialic acid hydroxylase occurred after the Homo-Pan divergence,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 20, pp. 11751–11756, 1998.
- E. A. Muchmore, M. Milewski, A. Varki, and S. Diaz, “Biosynthesis of N-glycolyneuraminic acid. The primary site of hydroxylation of N-acetylneuraminic acid is the cytosolic sugar nucleotide pool,” Journal of Biological Chemistry, vol. 264, no. 34, pp. 20216–20223, 1989.
- I. Kawashima, H. Ozawa, M. Kotani, et al., “Characterization of ganglioside expression in human melanoma cells: immunological and biochemical analysis,” Journal of Biochemistry, vol. 114, no. 2, pp. 186–193, 1993.
- M. El-Abbadi and T. N. Seyfried, “Influence of growth environment on the ganglioside composition of an experimental mouse brain tumor,” Molecular and Chemical Neuropathology, vol. 21, no. 2-3, pp. 273–285, 1994.
- M. Ziche, G. Alessandri, and P. M. Gullino, “Gangliosides promote the angiogenic response,” Laboratory Investigation, vol. 61, no. 6, pp. 629–634, 1989.
- W. Song, M. F. Vacca, R. Welti, and D. A. Rintoul, “Effects of gangliosides and de-N-acetyl on epidermal growth factor receptor kinase activity and cell growth,” Journal of Biological Chemistry, vol. 266, no. 16, pp. 10174–10181, 1991.
- A. Rebbaa, J. Hurh, H. Yamamoto, D. S. Kersey, and E. G. Bremer, “Ganglioside GM3 inhibition of EGF receptor mediated signal transduction,” Glycobiology, vol. 6, no. 4, pp. 399–406, 1996.
- K. Kabayama, T. Sato, F. Kitamura, et al., “TNA-induced insulin resistance in adipocytes as a membrane microdomain disorder: involvement of ganglioside GM3,” Glycobiology, vol. 15, no. 1, pp. 21–29, 2005.
- S. Tagami, J.-I. Inokuchi, K. Kabayama, et al., “Ganglioside GM3 participates in the pathological conditions of insulin resistance,” Journal of Biological Chemistry, vol. 277, no. 5, pp. 3085–3092, 2002.
- E. G. Bremer, J. Schlessinger, and S. Hakomori, “Ganglioside-mediated modulation of cell growth. Specific effects of on tyrosine phosphorylation of the epidermal growth factor receptor,” Journal of Biological Chemistry, vol. 261, no. 5, pp. 2434–2440, 1986.
- M. S. Toledo, E. Suzuki, K. Handa, and S. Hakomori, “Effect of ganglioside and tetraspanins in microdomains on interaction of integrins with fibroblast growth factor receptor,” Journal of Biological Chemistry, vol. 280, no. 16, pp. 16227–16234, 2005.
- Y. Nakatsuji and R. H. Miller, “Selective cell-cycle arrest and induction of apoptosis in proliferating neural cells by ganglioside GM3,” Experimental Neurology, vol. 168, no. 2, pp. 290–299, 2001.
- G. Alessandri, K. S. Raju, and P. M. Gullino, “Interaction of gangliosides with fibronectin in the mobilization of capillary endothelium. Possible influence on the growth of metastasis,” Invasion and Metastasis, vol. 6, no. 3, pp. 145–165, 1986.
- G. Alessandri, P. Cornaglia-Ferraris, and P. M. Gullino, “Angiogenic and angiostatic microenvironment in tumors: role of gangliosides,” Acta Oncologica, vol. 36, no. 4, pp. 383–387, 1997.
- M. Ziche, L. Morbidelli, G. Alessandri, and P. M. Gullino, “Angiogenesis can be stimulated or repressed in vivo by a change in GM3:GD3 ganglioside ratio,” Laboratory Investigation, vol. 67, no. 6, pp. 711–715, 1992.
- G. Alessandri, S. Filippeschi, P. Sinibaldi, et al., “Influence of gangliosides on primary and metastatic neoplastic growth in human and murine cells,” Cancer Research, vol. 47, no. 16, pp. 4243–4247, 1987.
- M. G. Manfredi, S. Lim, K. P. Claffey, and T. N. Seyfried, “Gangliosides influence angiogenesis in an experimental mouse brain tumor,” Cancer Research, vol. 59, no. 20, pp. 5392–5397, 1999.
- M. H. Ravindranath, T. Tsuchida, D. L. Morton, and R. F. Irie, “Ganglioside GM3:GD3 ratio as an index for the management of melanoma,” Cancer, vol. 67, no. 12, pp. 3029–3035, 1991.
- R. Jennemann, H.-D. Mennel, B. L. Bauer, and H. Wiegandt, “Glycosphingolipid component profiles of human gliomas correlate with histological tumour types: analysis of inter-individual and tumour-regional distribution,” Acta Neurochirurgica, vol. 126, no. 2-4, pp. 170–178, 1994.
- S. Koochekpour and G. J. Pilkington, “Vascular and perivascular GD3 expression in human glioma,” Cancer Letters, vol. 104, no. 1, pp. 97–102, 1996.
- P. Fredman, H. von Holst, V. P. Collins, B. Dellheden, and L. Svennerholm, “Expression of gangliosides GD3 and -isoLM1 in autopsy brains from patients with malignant tumors,” Journal of Neurochemistry, vol. 60, no. 1, pp. 99–105, 1993.
- B. Berra, S. M. Gaini, and L. Riboni, “Correlation between ganglioside distribution and histological grading of human astrocytomas,” International Journal of Cancer, vol. 36, no. 3, pp. 363–366, 1985.
- T. D. Traylor and E. L. Hogan, “Gangliosides of human cerebral astrocytomas,” Journal of Neurochemistry, vol. 34, no. 1, pp. 126–131, 1980.
- G. Zeng, L. Gao, S. Birkle, and R. K. Yu, “Suppression of ganglioside GD3 expression in a rat F-11 tumor cell line reduces tumor growth, angiogenesis, and vascular endothelial growth factor production,” Cancer Research, vol. 60, no. 23, pp. 6670–6676, 2000.
- L. Manuelidis, R. K. Yu, and E. E. Manuelidis, “Ganglioside content and pattern in human gliomas in culture. Correlation of morphological changes with altered gangliosides,” Acta Neuropathologica, vol. 38, no. 2, pp. 129–135, 1977.
- L. C. Huysentruyt, P. Mukherjee, D. Banerjee, L. M. Shelton, and T. N. Seyfried, “Metastatic cancer cells with macrophage properties: evidence from a new murine tumor model,” International Journal of Cancer, vol. 123, no. 1, pp. 73–84, 2008.
- T. N. Seyfried, M. El-Abbadi, and M. L. Roy, “Ganglioside distribution in murine neural tumors,” Molecular and Chemical Neuropathology, vol. 17, no. 2, pp. 147–167, 1992.
- P. Mukherjee, L. E. Abate, and T. N. Seyfried, “Antiangiogenic and proapoptotic effects of dietary restriction on experimental mouse and human brain tumors,” Clinical Cancer Research, vol. 10, no. 16, pp. 5622–5629, 2004.
- E. G. Bremer and S. I. Hakomori, “GM3 ganglioside induces hamster fibroblast growth inhibition in chemically-defined medium: ganglioside may regulate growth factor receptor function,” Biochemical and Biophysical Research Communications, vol. 106, no. 3, pp. 711–718, 1982.
- T.-W. Chung, S.-J. Kim, H.-J. Choi, et al., “Ganglioside GM3 inhibits VEGF/VEGFR-2-mediated angiogenesis: direct interaction of GM3 with VEGFR-2,” Glycobiology, vol. 19, no. 3, pp. 229–239, 2009.
- E. N. E. Noll, J. Lin, Y. Nakatsuji, R. H. Miller, and P. M. Black, “GM3 as a novel growth regulator for human gliomas,” Experimental Neurology, vol. 168, no. 2, pp. 300–309, 2001.
- P. Mukherjee, A. C. Faber, L. M. Shelton, R. C. Baek, T. C. Chiles, and T. N. Seyfried, “Ganglioside GM3 suppresses the proangiogenic effects of vascular endothelial growth factor and ganglioside GD1A,” Journal of Lipid Research, vol. 49, no. 5, pp. 929–938, 2008.
- H. M. Zimmerman and H. Arnold, “Experimental brain tumors: I. tumors produced with methylcholanthrene,” Cancer Research, vol. 1, pp. 919–938, 1941.
- J. Marsh, P. Mukherjee, and T. N. Seyfried, “Akt-dependent proapoptotic effects of dietary restriction on late-stage management of a phosphatase and tensin homologue/tuberous sclerosis complex 2-deficient mouse astrocytoma,” Clinical Cancer Research, vol. 14, no. 23, pp. 7751–7762, 2008.
- R. Martínez-Murillo and A. Martínez, “Standardization of an orthotopic mouse brain tumor model following transplantation of CT-2A astrocytoma cells,” Histology and Histopathology, vol. 22, no. 12, pp. 1309–1326, 2007.
- J. Jośko and M. Mazurek, “Transcription factors having impact on vascular endothelial growth factor (VEGF) gene expression in angiogenesis,” Medical Science Monitor, vol. 10, no. 4, pp. RA89–RA98, 2004.
- J. Fang, M. Ding, L. Yang, L.-Z. Liu, and B.-H. Jiang, “PI3K/PTEN/AKT signaling regulates prostate tumor angiogenesis,” Cellular Signalling, vol. 19, no. 12, pp. 2487–2497, 2007.
- H. D. Skinner, J. Z. Zheng, J. Fang, F. Agani, and B.-H. Jiang, “Vascular endothelial growth factor transcriptional activation is mediated by hypoxia-inducible factor 1, HDM2, and p70S6K1 in response to phosphatidylinositol 3-kinase/AKT signaling,” Journal of Biological Chemistry, vol. 279, no. 44, pp. 45643–45651, 2004.
- O. Nakamura, M. Iwamori, M. Matsutani, and K. Takakura, “Ganglioside GD3 shedding by human gliomas,” Acta Neurochirurgica, vol. 109, no. 1-2, pp. 34–36, 1991.
- K. Kaucic, Y. Liu, and S. Ladisch, “Modulation of growth factor signaling by gangliosides: positive or negative?” Methods in Enzymology, vol. 417, pp. 168–185, 2006.
- S. Ladisch, S. Kitada, and E. F. Hays, “Gangliosides shed by tumor cells enhance tumor formation in mice,” Journal of Clinical Investigation, vol. 79, no. 6, pp. 1879–1882, 1987.
- R. Olshefski and S. Ladisch, “Intercellular transfer of shed tumor cell gangliosides,” FEBS Letters, vol. 386, no. 1, pp. 11–14, 1996.
- Y. Liu, R. Li, and S. Ladisch, “Exogenous ganglioside GD1a enhances epidermal growth factor receptor binding and dimerization,” Journal of Biological Chemistry, vol. 279, no. 35, pp. 36481–36489, 2004.
- Z. Lang, M. Guerrera, R. Li, and S. Ladisch, “Ganglioside GD1a enhances VEGF-induced endothelial cell proliferation and migration,” Biochemical and Biophysical Research Communications, vol. 282, no. 4, pp. 1031–1037, 2001.
- H. van Cruijsen, M. Ruiz, P. van der Valk, T. D. de Gruijl, and G. Giaccone, “Tissue micro array analysis of ganglioside N-glycolyl GM3 expression and signal transducer and activator of transcription (STAT)-3 activation in relation to dendritic cell infiltration and microvessel density in non-small cell lung cancer,” BMC Cancer, vol. 9, article 180, 2009.