GD3 synthase overexpression enhances proliferation and migration of MDA-MB-231 breast cancer cells

Biological Chemistry

Volumn 390, Issue 7, 2009, Pages 601-609

  Cazet, Aurélie ^a   Groux Degroote, Sophie ^a   Teylaert, Béatrice ^a   Kwon, Kyung Min ^b   Lehoux, Sylvain ^a   Slomianny, Christian ^c   Kim, Cheorl Ho ^b   Le Bourhis, Xuefen ^c   Delannoy, Philippe ^a  

^a UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

^b Sungkyunkwan University   (South Korea)

^c INSERM   (France)

Author keywords

Breast cancer; Cell proliferation; GD3 synthase; Gangliosides; MDA MB 231

Indexed keywords

GANGLIOSIDE; GANGLIOSIDE GD2; GANGLIOSIDE GD3; GANGLIOSIDE GD3 SYNTHASE; GANGLIOSIDE GM3; GANGLIOSIDE GT3; SYNTHETASE; UNCLASSIFIED DRUG; ALPHA N ACETYLNEURAMINATE ALPHA 2,8 SIALYLTRANSFERASE; ALPHA-N-ACETYLNEURAMINATE ALPHA-2,8-SIALYLTRANSFERASE; SIALYLTRANSFERASE;

ARTICLE; BIOSYNTHESIS; BREAST CANCER; BREAST EPITHELIUM; CANCER CELL; CANCER CELL CULTURE; CELL CULTURE; CELL FUNCTION; CELL GROWTH; CELL LINE; CELL MIGRATION; CELL PROLIFERATION; CELL SURFACE; COMPARATIVE STUDY; CONTROLLED STUDY; EPITHELIUM CELL; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SERUM; BREAST TUMOR; CELL MOTION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; GANGLIOSIDES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; SIALYLTRANSFERASES;

EID: 68149179191     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2009.054     Document Type: Article

References (46)

1. Ariga, T., McDonald, M.P., and Yu, R.K. (2008). Role of ganglioside metabolism in the pathogenesis of Alzheimer's disease. J. Lipid Res. 49, 1157-1175.
2. Birklé, S., Zeng, G., Gao, L., Yu, R.K., and Aubry, J. (2003). Role of tumor-associated gangliosides in cancer progression. Biochimie 85, 455-463.
3. Brockhausen, I., Yang, J., Dickinson, N., Ogata, S., and Itzkowitz, S.H. (1998). Enzymatic basis for sialyl-Tn expression in human colon cancer cells. Glycoconj. J. 15, 595-603.
4. Descamps, S., Toillon, R.A., Adriaenssens, E., Pawlowski, V., Cool, S.M., Nurcombe, V., Le Bourhis, X., Boilly, B., Peyrat, J.P., and Hondermarck, H. (2001). Nerve growth factor stimulates proliferation and survival of human breast cancer cells through two distinct signaling pathways. J. Biol. Chem. 276, 17864-17870.
5. Dollé, L., Adriaenssens, E., El Yazidi-Belkoura, I., Le Bourhis, X., Nurcombe, V., and Hondermarck, H. (2004). Nerve growth factor receptors and signaling in breast cancer. Curr. Cancer Drug Targets 4, 463-470.
6. Fukuda, M. (1996). Possible roles of tumor-associated carbohydrate antigens. Cancer Res. 56, 2237-2244.
7. Fukumoto, S., Mutoh, T., Hasegawa, T., Miyazaki, H., Okada, M., Goto, G., Furukawa, K., Urano, T., and Furukawa, K. (2000). GD3 synthase gene expression in PC12 cells results in the continuous activation of TrkA and ERK1/2 and enhanced proliferation. J. Biol. Chem. 275, 5832-5838.
8. Furukawa, K., Hamamura, K., Nakashima, H., and Furukawa, K. (2008). Molecules in the signaling pathway activated by gangliosides can be targets of therapeutics for malignant melanomas. Proteomics 8, 3312-3316.
9. Garcìa-Vallero, J.J., Gringhuis, S.I., Van Dijk, W., and Van Die, I. (2006). Gene expression analysis of glycosylation-related genes by real-time polymerase chain reaction. Methods Mol. Biol. 347, 187-209.
10. Hakomori, S. (1996). Tumor malignancy defined by aberrant glycosylation and sphingo(glyco)lipid metabolism. Cancer Res. 56, 5309-5318.
11. Hakomori, S. (2001). Tumor-associated carbohydrate antigens defining tumor malignancy: basis for development of anti-cancer vaccines. Adv. Exp. Med. Biol. 491, 369-402.
12. Hamamura, K., Furukawa, K., Hayashi, T., Hattori, T., Nakano, J., Nakashima, H., Okuda, T., Mizutani, H., Hattori, H., Ueda, M., et al. (2005). Ganglioside GD3 promotes cell growth and invasion through p130Cas and paxillin in malignant melanoma cells. Proc. Natl. Acad. Sci. USA 102, 11041-11046.
13. Harduin-Lepers, A., Krzewinski-Recchi, M.A., Samyn-Petit, B., Vallejo-Ruiz, V., Julien, S., and Delannoy, S. (2001). The human sialyltransferases family. Biochimie 83, 727-737.
14. Hebbar, M., Krzewinski-Recchi, M.A., Hornez, L., Verdière, A., Harduin-Lepers, A., Bonneterre, J., Delannoy, P., and Peyrat, J.P. (2003). Prognostic value of tumoral sialyltransferases expression and circulating E-selectin concentrations in node-negative breast cancer patients. Int. J. Biol. Markers 18, 116-122.
15. Ichikawa, S., Nakajo, N., Sakiyama, H., and Hirabayashi, Y. (1994). A mouse B16 melanoma mutant deficient in glycolipids. Proc. Natl. Acad. Sci. USA 91, 2703-2707.
16. Julien, S., Krzewinski-Recchi, M.A., Harduin-Lepers, A., Gouyer, V., Huet, G., Le Bourhis, X., and Delannoy, P. (2001). 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, 883-893.
17. Kamimura, Y., Furukawa, K., Kittaka, D., Nishio, M., Hamamura, K., Fukumoto, S., and Furukawa, K. (2005). Differential enhancing effects of alpha 2,8-sialyltransferase on the cell proliferation and mobility. Int. J. Oncol. 26, 337-344.
18. Kang, N.Y., Kim, C.H., Kim, K.S., Ko, J.H., Lee, J.H., Jeong, Y.K., and Lee, Y.C. (2007). Expression of the human CMP-NeuAc:GM3 alpha2,8- sialyltransferase (GD3 synthase) gene through the NF-κB activation in human melanoma SK-MEL-2 cells. Biochim. Biophys. Acta 1769, 622-630.
19. Ko, K., Furukawa, K., Takahashi, T., Urano, T., Sanai, Y., Nagino, M., Nimura, Y., and Furukawa, K. (2006). Fundamental study of small interfering RNAs for ganglioside GD3 synthase gene as a therapeutic target of lung cancers. Oncogene 25, 6924-6935.
20. Lagadec, C., Meignan, S., Adriaenssens, E., Foveau, B., Vanhecke, E., Romon, R., Toillon, R.A., Oxombre, B., Hondermarck, H., and Le Bourhis, X. (2009). TrkA overexpression enhances growth and metastasis of breast cancer cells. Oncogene, in press.
21. (-ΔΔCT) method. Methods 25, 402-408.
22. Malisan, F. and Testi, R. (2005). The ganglioside GD3 as the Greek goddess Hecate: several faces turned towards as many directions. IUBMB Life 57, 477-482.
23. Marquina, G., Waki, H., Fernandez, L.E., Kon, K., Carr, A., Valiente, O., Perez, R., and Ando, S. (1996). Gangliosides expressed in human breast cancer. Cancer Res. 56, 5165-5171.
24. Modak, S. and Cheung, N.K. (2007). Disialoganglioside directed immunotherapy of neuroblastoma. Cancer Invest. 25, 67-77.
25. Moon, S.K., Kang, S.K., and Kim, C.H. (2006). Reactive oxygen species mediates disialoganglioside GD3-induced inhibition of ERK1/2 and matrix metalloproteinase-9 expression in vascular smooth muscle cells. FASEB J. 20, 1387-1395.
26. Nakashima, H., Hamamura, K., Houjou, T., Taguchi, R., Yamamoto, N., Mitsudo, K., Tohnai, I., Ueda, M., Urano, T., Furukawa, K., et al. (2007). Overexpression of caveolin-1 in a human melanoma cell line results in dispersion of ganglioside GD3 from lipid rafts and alteration of leading edges, leading to attenuation of malignant properties. Cancer Sci. 98, 512-520.
27. Narita, T., Funahashi, H., Satoh, Y., Watanabe, T., Sakamoto, J., and Takagi, H. (1993). Association of expression of blood group-related carbohydrate antigens with prognosis in breast cancer. Cancer 71, 3044-3053.
28. Nohara, K., Wang, F., and Spiegel, S. (1997). Glycosphingolipid composition of MDA-MB-231 and MCF-7 human breast cancer cell lines. Breast Cancer Res. Treat. 48, 49-57.
29. Oblinger, J.L., Pearl, D.K., Boardman, C.L., Saqr, H., Prior, T.W., Scheithauer, B.W., Jenkins, R.B., Burger, P.C., and Yates, A.J. (2006). Diagnostic and prognostic value of glycosyltransferase mRNA in glioblastoma multiforme patients. Neuropathol. Appl. Neurobiol. 32, 410-418.
30. Prokazova, N.V. and Bergelson, L.D. (1994). Gangliosides and atherosclerosis. Lipids 29, 1-5.
31. Recchi, M.A., Harduin-Lepers, A., Boilly-Marer, Y., Verbert, A., and Delannoy, P. (1998a). Multiplex RT-PCR method for the analysis of the expression of human sialyltransferases: application to breast cancer cells. Glycoconj. J. 15, 19-27.
32. Recchi, M.A., Hebbar, M., Hornez, L., Harduin-Lepers, A., Peyrat, J.P., and Delannoy, P. (1998b). Multiplex reverse transcriptase polymerase chain reaction assessment of sialyltransferases expression in human breast cancer. Cancer Res. 58, 4066-4070.
33. Ruan, S., Raj, B.K., and Lloyd, K.O. (1999). Relationship of glycosyltransferases and mRNA levels to ganglioside expression in neuroblastoma and melanoma cells. J. Neurochem. 72, 514-521.
34. Ruckhä berle, E., Rody, A., Engels, K., Gaetje, R., von Minckwitz, G., Schiffmann, S., Grösch, S., Geisslinger, G., Holtrich, U., Karn, T., et al. (2008). Microarray analysis of altered sphingolipid metabolism reveals prognostic significance of sphingosine kinase 1 in breast cancer. Breast Cancer Res. Treat. 112, 41-52.
35. Ruckhäberle, E., Karn, T., Rody, A., Hanker, L., Gätje, R., Metzler, D., Holtrich, U., and Kaufmann, M. (2009). Gene expression of ceramide kinase, galactosyl ceramide synthase and ganglioside GD3 synthase is associated with prognosis in breast cancer. J. Cancer Res. Clin. Oncol., Epub ahead of print, DOI: 10.1007/s00432-008-0536-6.
36. Sabel, M.S. and Sondak, V.K. (2002). Tumor vaccines: a role in preventing recurrence in melanoma? Am. J. Clin. Dermatol. 3, 609-616.
37. Soares, R., Marinho, A., and Schmitt, F. (1996). Expression of sialyl-Tn in breast cancer. Correlation with pronostic parameters. Pathol. Res. Pract. 192, 1181-1186.
38. Tettamanti, G. (2004). Ganglioside/glycosphingolipid turnover: new concepts. Glycoconj. J. 20, 301-317.
39. Ura, Y., Dion, A.S., Williams, C.J., Olsen, B.D., Redfield, E.S., Ishida, M., Herlyn, M., and Major, P.P. (1992). Quantitative dot blot analyses of blood-group-related antigens in paired normal and malignant human breast tissues. Int. J. Cancer 50, 57-63.
40. Wiesner, D.A. and Sweeley, C.C. (1995). Circulating gangliosides of breast cancer patients. Int. J. Cancer 60, 294-299.
41. Yamashita, T., Wada, R., Sasaki, T., Deng, C., Bierfreund, U., Sandhoff, K., and Proia, R.L. (1999). A vital role for glycosphingolipid synthesis during development and differentiation. Proc. Natl. Acad. Sci. USA 96, 9142-9147.
42. Yanagisawa, M., Liour, S.S., and Yu, R.K. (2004). Involvement of gangliosides in proliferation of immortalized neural progenitor cells. J. Neurochem. 91, 804-812.
43. Yoshida, S., Fukumoto, S., Kawaguchi, H., Sato, S., Ueda, R., and Furukawa, K. (2001) Ganglioside G(D2) in small cell lung cancer cell lines: enhancement of cell proliferation and mediation of apoptosis. Cancer Res. 61, 4244-4252.
44. D3 expression in a rat F-11 tumor cell line reduces tumor growth, angiogenesis, and vascular endothe-lial growth factor production. Cancer Res. 60, 6670-6676.
45. Zeng, G. and Yu, R.K. (2008). Cloning and transcriptional regulation of genes responsible for synthesis of gangliosides. Curr. Drug Targets 9, 317-324.
46. Zhang, X., Ding, L., and Sandford, A.J. (2005). Selection of reference genes for gene expression studies in human neutrophils by real-time PCR. BMC Mol. Biol. 6, 4.