Gangliosides in breast cancer: New perspectives

Biochemistry (Moscow)

Volumn 80, Issue 7, 2015, Pages 808-819

  Groux Degroote, S ^a   Guerardel Y ^a   Julien, S ^a   Delannoy, P ^a  

^a UNIV LILLE   (France)

Author keywords

breast cancer; c Met; GD3 synthase; gangliosides; mass spectrometry; metastasis

Indexed keywords

GANGLIOSIDE;

ANIMAL; BIOSYNTHESIS; BREAST TUMOR; CELL MEMBRANE; FEMALE; GENETICS; HUMAN; METABOLISM; SIGNAL TRANSDUCTION;

ANIMALS; BREAST NEOPLASMS; CELL MEMBRANE; FEMALE; GANGLIOSIDES; HUMANS; SIGNAL TRANSDUCTION;

EID: 84937695027     PISSN: 00062979     EISSN: 16083040     Source Type: Journal    
DOI: 10.1134/S0006297915070020     Document Type: Review

References (99)

1. Hakomori, S. I. (2002) The glycosynapse, Proc. Natl. Acad. Sci. USA, 99, 225-232.
2. Regina Todeschini, A., and Hakomori, S. I. (2008) Functional role of glycosphingolipids and gangliosides in control of cell adhesion, motility, and growth, through glycosynaptic microdomains, Biochim. Biophys. Acta, 1780, 421-433.
3. Birkle, S., Zeng, G., Gao, L., Yu, R. K., and Aubry, J. (2003) Role of tumor-associated gangliosides in cancer progression, Biochimie, 85, 455-463.
4. Prokazova, N. V., and Bergelson, L. D. (1994) Gangliosides and atherosclerosis, Lipids, 29, 1-5.
5. Ariga, T, McDonald, M. P., and Yu, R. K. (2008) Role of ganglioside metabolism in the pathogenesis of Alzheimer's disease- a review, J. Lipid Res., 49, 1157-1175.
6. Furukawa, K., Hamamura, K., Aixinjueluo, W., and Furukawa, K. (2006) Biosignals modulated by tumor-associated carbohydrate antigens: novel targets for cancer therapy, Ann. N. Y. Acad. Sci., 1086, 185-198.
7. Krengel, U., and Bousquet, P. A. (2014) Molecular recognition of gangliosides and their potential for cancer immunotherapies, Front. Immunol., 5, 325.
8. Rabu, C., McIntosh, R., Jurasova, Z., and Durrant, L. (2012) Glycans as targets for therapeutic antitumor antibodies, Future Oncol., 8, 943-960.
9. Yu, R. K., Yanagisawa, M., and Ariga, T (2007) Glycosphingolipid structures, in Comprehensive Glycoscience (Kamerling, H., ed.) Elsevier, Oxford, UK, pp. 73-122.
10. Ichikawa, S., Sakiyama, H., Suzuki, G., Hidari, K. I., and Hirabayashi, Y (1996) Expression cloning of a cDNA for human ceramide glucosyltransferase that catalyzes the first glycosylation step of glycosphingolipid synthesis, Proc. Natl. Acad. Sci. USA, 93, 4638-4643.
11. Abe, A., Inokuchi, J., Jimbo, M., Shimeno, H., Nagamatsu, A., Shayman, J. A., Shukla, G. S., and Radin, N. S. (1992) Improved inhibitors of glucosylceramide synthase, J. Biochem., 111, 191-196.
12. Nomura, T, Takizawa, M., Aoki, J., Arai, H., Inoue, K., Wakisaka, E., Yoshizuka, N., Imokawa, G., Dohmae, N., Takio, K., Hattori, M., and Matsuo, N. (1998) J. Biol. Chem., 273, 13570-13577.
13. Takizawa, M., Nomura, T, Wakisaka, E., Yoshizuka, N., Aoki, J., Arai, H., Inoue, K., Hattori, M., and Matsuo, N. (1999) cDNA cloning and expression of human lactosylceramide synthase, Biochim. Biophys. Acta, 1438, 301-304.
14. Zeng, G., and Yu, R. K. (2008) Cloning and transcriptional regulation of genes responsible for synthesis of gangliosides, Curr. Drug Targets, 9, 317-324.
15. Ishii, A., Ohta, M., Watanabe, Y, Matsuda, K., Ishiyama, K., Sakoe, K., Nakamura, M., Inokuchi, J., Sanai, Y, and Saito, M. (1998) Expression cloning and functional characterization of human cDNA for ganglioside GM3 synthase, J. Biol. Chem., 273, 31652-31655.
16. Haraguchi, M., Yamashiro, S., Yamamoto, A., Furukawa, K., Takamiya, K., Lloyd, K. O., Shiku, H., and Furukawa, K. (1994) Isolation of GD3 synthase gene by expression cloning of GM3 alpha-2,8-sialyltransferase cDNA using anti-GD2 monoclonal antibody, Proc. Natl. Acad. Sci. USA, 91, 10455-10459.
17. Nakayama, J., Fukuda, M. N., Hirabayashi, Y, Kanamori, A., Sasaki, K., Nishi, T, and Fukuda, M. (1996) Expression cloning of a human GT3 synthase. GD3 and GT3 are synthesized by a single enzyme, J. Biol. Chem., 271, 3684-3691.
18. Kim, Y. J., Kim, K. S., Do, S., Kim, C. H., Kim, S. K., and Lee, Y. C. (1997) Molecular cloning and expression of human alpha2,8-sialyltransferase (hST8Sia V), Biochem. Biophys. Res. Commun., 235, 327-330.
19. Svennerholm, L. (1980) Ganglioside designation, Adv. Exp. Med. Biol., 125, 11.
20. Nagata, Y, Yamashiro, S., Yodoi, J., Lloyd, K. O., Shiku, H., and Furukawa, K. (1992) Expression cloning of beta- I,4-N-acetylgalactosaminyltransferase cDNAs that determine the expression of GM2 and GD2 gangliosides, J. Biol. Chem., 267, 12082-12089.
21. Amado, M., Almeida, R., Carneiro, F., Levery, S. B., Holmes, E. H., Nomoto, M., Hollingsworth, M. A., Hassan, H., Schwientek, T, Nielsen, P. A., Bennett, E. P., and Clausen, H. (1998) A family of human beta3-galactosyltransferases. Characterization of four members of a UDP-galactose:beta-N-acetyl-glucosamine/beta-N-acetylgalactosamine/ beta-1,3-galactosyltransferase family, J. Biol. Chem., 273, 12770-12778.
22. Iber, H., Zacharias, C., and Sandhoff, K. (1992) The cseries gangliosides GT3, GT2, and GP1c are formed in rat liver Golgi by the same set of glycosyltransferases that catalyze the biosynthesis of asialo-, a- and b-series gangliosides, Glycobiology, 2, 137-142.
23. Yamashiro, S., Haraguchi, M., Furukawa, K., Takamiya, K., Yamamoto, A., Nagata, Y, Lloyd, K. O., Shiku, H., and Furukawa, K. (1995) Substrate specificity of beta 1,4- N-acetylgalactosaminyltransferase in vitro and in cDNAtransfected cells. GM2/GD2 synthase efficiently generates asialo-GM2 in certain cells, J. Biol. Chem., 270, 61496155.
24. Kitagawa, H., and Paulson, J. C. (1994) Cloning of a novel alpha 2,3-sialyltransferase that sialylates glycoprotein and glycolipid carbohydrate groups, J. Biol. Chem., 269, 13941401.
25. Giordanengo, V., Bannwarth, S., Laffont, C., Van Miegem, V., Harduin-Lepers, A., Delannoy, P., and Lefebvre, J. C. (1997) Cloning and expression of cDNA for a human Gal(beta1-3)GalNAc alpha2,3-sialyltransferase from the CEM T-cell line, Eur. J. Biochem., 247, 558-566.
26. Sturgill, E. R., Aoki, K., Lopez, P. H., Colacurcio, D., Vajn, K., Lorenzini, I., Majic, S., Yang, W. H., Heffer, M., Tiemeyer, M., Marth, J. D., and Schnaar, R. L. (2012) Biosynthesis of the major brain gangliosides GD1a and GT1b, Glycobiology, 22, 1289-1301.
27. Harduin-Lepers, A. (2013) Vertebrate sialyltransferases, in Sialobiology: Structure, Biosynthesis and Function of Sialic Acid Glycoconjugates in Health and Disease (Tiralongo, J., and Martinez-Duncker, J. T, eds.) Bentham Science Publishers, pp. 139-187.
28. Okajima, T, Fukumoto, S., Ito, H., Kiso, M., Hirabayashi, Y, Urano, T, and Furukawa, K. (1999) Molecular cloning of brain-specific GD1alpha synthase (ST6GalNAc V) containing CAG/Glutamine repeats, J. Biol. Chem., 274, 30557-30562.
29. Bobowski, M., Cazet, A., Steenackers, A., and Delannoy, P. (2012) Role of complex gangliosides in cancer progression, Carbohydr. Chem., 37, 1-20.
30. Giraudo, C. G., and Maccioni, H. J. (2003) Ganglioside glycosyltransferases organize in distinct multienzyme complexes in CHO-K1 cells, J. Biol. Chem., 278, 40262-40271.
31. Hidari, J. K., Ichikawa, S., Furukawa, K., Yamasaki, M., and Hirabayashi, Y. (1994) beta-1-4-N-acetylgalactosaminyltransferase can synthesize both asialoglycosphingolipid GM2 and glycosphingolipid GM2 in vitro and in vivo: isolation and characterization of a beta-1-4-N-acetylgalactosaminyltransferase cDNA clone from rat ascites hepatoma cell line AH7974F, Biochem. J., 303, 957-965.
32. Schnaar, R. L. (1994) Isolation of glycosphingolipids, Methods Enzymol., 230, 348-370.
33. Hakomori, S. I. (1983) Chemistry of glycosphingolipids, in Sphingolipid Biochemistry- Handbook of Lipid Research (Kanfer, J. N., and Hakomori, S. I., eds.) Plenum Press, New York, pp. 1-165.
34. Svennerholm, L., and Fredman, P. (1980) A procedure for the quantitative isolation of brain gangliosides, Biochim. Biophys. Acta, 617, 97-109.
35. Ijuin, T, Kitajima, K., Song, Y, Kitazume, S., Inoue, S., Haslam, S. M., Morris, H. R., Dell, A., and Inoue, Y (1996) Isolation and identification of novel sulfated and nonsulfated oligosialylglycosphingolipids from sea urchin sperm, Glycoconj. J., 13, 401-413.
36. Powell, A. K., and Harvey, D. J. (1996) Stabilization of sialic acids in N-linked oligosaccharides and gangliosides for analysis by positive ion matrix-assisted laser desorption/ionization mass spectrometry, Rapid Commun. Mass Spectrom., 10, 1027-1032.
37. Wheeler, S. F., Domann, P., and Harvey, D. J. (2009) Derivatization of sialic acids for stabilization in matrixassisted laser desorption/ionization mass spectrometry and concomitant differentiation of alpha(2 3)- and alpha(2 6)-isomers, Rapid Commun. Mass Spectrom., 23, 303-312.
38. Liang, Y. J., Kuo, H. H., Lin, C. H., Chen, Y. Y, Yang, B. C., Cheng, Y. Y, Yu, A. L., Khoo, K. H., and Yu, J. (2010) Switching of the core structures of glycosphingolipids from globo- and lacto- to ganglio-series upon human embryonic stem cell differentiation, Proc. Natl. Acad. Sci. USA, 107, 22564-22569.
39. Boccuto, L., Aoki, K., Flanagan-Steet, H., Chen, C. F., Fan, X., Bartel, F., Petukh, M., Pittman, A., Saul, R., Chaubey, A., Alexov, E., Tiemeyer, M., Steet, R., and Schwartz, C. E. (2014) A mutation in a ganglioside biosynthetic enzyme, ST3GAL5, results in salt and pepper syndrome, a neurocutaneous disorder with altered glycolipid and glycoprotein glycosylation, Hum. Mol. Genet., 23, 418433.
40. Lee, D., and Cha, S. (2014) 5-Methoxysalicylic acid matrix for ganglioside analysis with matrix-assisted laser desorption/ ionization mass spectrometry, J. Am. Soc. Mass Spectrom., Dec 11, Epub ahead of print.
41. Colsch, B., and Woods, A. S. (2010) Localization and imaging of sialylated glycosphingolipids in brain tissue sections by MALDI mass spectrometry, Glycobiology, 20, 661667.
42. Mank, M., Stahl, B., and Boehm, G. (2004) 2,5- Dihydroxybenzoic acid butylamine and other ionic liquid matrixes for enhanced MALDI-MS analysis of biomolecules, Anal. Chem., 76, 2938-2950.
43. Sugiura, Y, Shimma, S., Konishi, Y, Yamada, M. K., and Setou, M. (2008) Imaging mass spectrometry technology and application on ganglioside study; visualization of agedependent accumulation of C20-ganglioside molecular species in the mouse hippocampus, PLoS One, 3, e3232.
44. Chan, K., Lanthier, P., Liu, X., Sandhu, J. K., Stanimirovic, D., and Li, J. (2009) MALDI mass spectrometry imaging of gangliosides in mouse brain using ionic liquid matrix, Anal. Chim. Acta, 639, 57-61.
45. Goto-Inoue, N., Hayasaka, T, Zaima, N., Kashiwagi, Y, Yamamoto, M., Nakamoto, M., and Setou, M. (2010) The detection of glycosphingolipids in brain tissue sections by imaging mass spectrometry using gold nanoparticles, J. Am. Soc. Mass Spectrom., 21, 1940-1943.
46. Richards, A. L., Lietz, C. B., Wager-Miller, J., Mackie, K., and Trimpin, S. (2012) Localization and imaging of gangliosides in mouse brain tissue sections by laserspray ionization inlet, J. Lipid Res., 53, 1390-1398.
47. Whitehead, S. N., Chan, K. H., Gangaraju, S., Slinn, J., Li, J., and Hou, S. T (2011) Imaging mass spectrometry detection of gangliosides species in the mouse brain following transient focal cerebral ischemia and long-term recovery, PLoS One, 6, e20808.
48. Snel, M. F., and Fuller, M. (2010) High-spatial resolution matrix-assisted laser desorption ionization imaging analysis of glucosylceramide in spleen sections from a mouse model of Gaucher disease, Anal. Chem., 82, 3664-3670.
49. Kettling, H., Vens-Cappell, S., Soltwisch, J., Pirkl, A., Haier, J., Müthing, J., and Dreisewerd, K. (2014) MALDI mass spectrometry imaging of bioactive lipids in mouse brain with a Synapt G2-S mass spectrometer operated at elevated pressure: improving the analytical sensitivity and the lateral resolution to ten micrometers, Anal. Chem., 86, 7798-7805.
50. Cheng, S. C., Huang, M. Z., and Shiea, J. (2011) Thin layer chromatography/mass spectrometry, J. Chromatogr. A, 1218, 2700-2711.
51. Mlinac, K., Fabris, D., Vukelic, Z., Rozman, M., Heffer, M., and Bognar, S. K. (2013) Structural analysis of brain ganglioside acetylation patterns in mice with altered ganglioside biosynthesis, Carbohydr. Res., 382, 1-8.
52. Suzuki, A., Miyazaki, M., Matsuda, J., and Yoneshige, A. (2011) High-performance thin-layer chromatography/ mass spectrometry for the analysis of neutral glycosphingolipids, Biochim. Biophys. Acta, 1811, 861-874.
53. Miyazaki, M., Yonesige, A., Matsuda, J., Kuroda, Y, Kojima, N., and Suzuki, A. (2008) High-performance thin-layer chromatography/mass spectrometry for rapid analysis of neutral glycosphingolipids, J. AOAC Int., 91, 1218-1226.
54. Valdes-Gonzalez, T, Goto-Inoue, N., Hirano, W., Ishiyama, H., Hayasaka, T, Setou, M., and Taki, T (2011) New approach for glyco- and lipidomics- molecular scanning of human brain gangliosides by TLC-Blot and MALDI-QIT-TOF MS, J. Neurochem., 116, 678683.
55. Ivleva, V. B., Elkin, Y. N., Budnik, B. A., Moyer, S. C., O'Connor, P. B., and Costello, C. E. (2004) Coupling thinlayer chromatography with vibrational cooling matrixassisted laser desorption/ionization Fourier transform mass spectrometry for the analysis of ganglioside mixtures, Anal. Chem., 76, 6484-6491.
56. Ivleva, V. B., Sapp, L. M., O'Connor, P. B., and Costello, C. E. (2005) Ganglioside analysis by thin-layer chromatography matrix-assisted laser desorption/ionization orthogonal time-of-flight mass spectrometry, J. Am. Soc. Mass Spectrom., 16, 1552-1560.
57. Park, H., Zhou, Y, and Costello, C. E. (2014) Direct analysis of sialylated or sulfated glycosphingolipids and other polar and neutral lipids using TLC-MS interfaces, J. Lipid Res., 55, 773-781.
58. Sorensen, L. K. (2006) A liquid chromatography/tandem mass spectrometric approach for the determination of gangliosides GD3 and GM3 in bovine milk and infant formulae, Rapid Commun. Mass Spectrom., 20, 3625-3633.
59. Fuller, M., Duplock, S., Hein, L. K., Rigat, B. A., and Mahuran, D. J. (2014) Liquid chromatography/electrospray ionization-tandem mass spectrometry quantification of GM2 gangliosides in human peripheral cells and plasma, Anal. Biochem., 458, 20-26.
60. Fong, B., Norris, C., Lowe, E., and McJarrow, P. (2009) Liquid chromatography-high-resolution mass spectrometry for quantitative analysis of gangliosides, Lipids, 44, 867874.
61. Lee, H., Lerno, L. A., Jr., Choe, Y, Chu, C. S., Gillies, L. A., Grimm, R., Lebrilla, C. B., and German, J. B. (2012) Multiple precursor ion scanning of gangliosides and sulfatides with a reversed-phase microfluidic chip and quadrupole time-of-flight mass spectrometry, Anal. Chem., 84, 5905-5912.
62. Zhang, J., Ren, Y, Huang, B., Tao, B., Pedersen, M. R., and Li, D. (2012) Determination of disialoganglioside GD3 and monosialoganglioside GM3 in infant formulas and whey protein concentrates by ultra-performance liquid chromatography/electrospray ionization tandem mass spectrometry, J. Sep. Sci., 35, 937-946.
63. Steenackers, A., Vanbeselaere, J., Cazet, A., Bobowski, M., Rombouts, Y, Colomb, F, Le Bourhis, X., Guerardel, Y, and Delannoy, P. (2012) Accumulation of unusual gangliosides G(Q3) and G(P3) in breast cancer cells expressing the G(D3) synthase, Molecules, 17, 9559-9572.
64. Nara, K., Watanabe, Y, Kawashima, I., Tai, T, Nagai, Y, and Sanai, Y (1996) Acceptor substrate specificity of a cloned GD3 synthase that catalyzes the biosynthesis of both GD3 and GD1c/GT1a/GQ1b, Eur. J. Biochem., 238, 647-652.
65. Nara, K., Watanabe, Y, Maruyama, K., Kasahara, K., Nagai Y, and Sanai, Y. (1994) Expression cloning of a CMP-NeuAc:NeuAc alpha 2-3Gal beta 1-4Glc beta 1- 1'Cer alpha 2,8-sialyltransferase (GD3 synthase) from human melanoma cells, Proc. Natl. Acad. Sci. USA, 91, 7952-7956.
66. Sasaki, K., Kurata, K., Kojima, N., Kurosawa, N., Ohta, S., Hanai, N., Tsuji, S., and Nishi, T (1994) Expression cloning of a GM3-specific alpha-2,8-sialyltransferase (GD3 synthase), J. Biol. Chem., 269, 15950-15956.
67. Furukawa, K., Horie, M., Okutomi, K., Sugano, S., and Furukawa, K. (2003) Isolation and functional analysis of the melanoma specific promoter region of human GD3 synthase gene, Biochim. Biophys. Acta, 1627, 71-78.
68. Yamamoto, A., Haraguchi, M., Yamashiro, S., Fukumoto, S., Furukawa, K., Takamiya, K., Atsuta, M., Shiku, H., and Furukawa, K. (1996) Heterogeneity in the expression pattern of two ganglioside synthase genes during mouse brain development, J. Neurochem., 66, 26-34.
69. Yu, R. K., Macala, L. J., Taki, T., Weinfield, H. M., and Yu, F S. (1988) Developmental changes in ganglioside composition and synthesis in embryonic rat brain, J. Neurochem., 50, 1825-1829.
70. 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-kappaB activation in human melanoma SK-MEL-2 cells, Biochim. Biophys. Acta, 1769, 622-630.
71. Dae, H. M., Kwon, H. Y., Kang, N. Y, Song, N. R., Kim, K. S., Kim, C. H., Lee, J. H., and Lee, Y. C. (2009) Isolation and functional analysis of the human glioblastoma- specific promoter region of the human GD3 synthase (hST8Sia I) gene, Acta Biochim. Biophys. Sin. (Shanghai), 41, 237-245.
72. 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.
73. Oliva, J. P., Valdes, Z., Casaco, A., Pimentel, G., Gonzalez, J., Alvarez, I., Osorio, M., Velazco, M., Figueroa, M., Ortiz, R., Escobar, X., Orozco, M., Cruz, J., Franco, S., Diaz, M., Roque, L., Carr, A., Vazquez, A. M., Mateos, C., Rubio, M. C., Perez, R., and Fernandez, L. E. (2006) Clinical evidences of GM3 (NeuGc) ganglioside expression in human breast cancer using the 14F7 monoclonal antibody labelled with (99m)Tc, Breast Cancer Res. Treat., 96, 115-121.
74. Ruckhaberle, E., Rody, A., Engels, K., Gaetje, R., von Minckwitz, G., Schiffmann, S., Grosch, S., Geisslinger, G., Holtrich, U., Karn, T, and Kaufmann, M. (2008) Microarray analysis of altered sphingolipid metabolism reveals prognostic significance of sphingosine kinase 1 in breast cancer, Breast Cancer Res. Treat., 112, 41-52.
75. Ruckhaberle, E., Karn, T, Rody, A., Hanker, L., Gatje, 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., 135, 1005-1013.
76. Carcel-Trullols, J., Stanley, J. S., Saha, R., Shaaf, S., Bendre, M. S., Monzavi-Karbassi, B., Suva, L. J., and Kieber-Emmons, T. (2006) Characterization of the glycosylation profile of the human breast cancer cell line, MDA- 231, and a bone colonizing variant, Int. J. Oncol., 28, 11731183.
77. Gu, Y, Zhang, J., Mi, W., Yang, J., Han, F., Lu, X., and Yu, W (2008) Silencing of GM3 synthase suppresses lung metastasis of murine breast cancer cells, Breast Cancer Res., 10, R1.
78. Cazet, A., Groux-Degroote, S., Teylaert, B., Kwon, K. M., Lehoux, S., Slomianny, C., Kim, C. H., Le Bourhis, X., and Delannoy, P. (2009) GD3 synthase overexpression enhances proliferation and migration of MDA-MB-231 breast cancer cells, Biol. Chem., 390, 601-609.
79. Cazet, A., Lefebvre, J., Adriaenssens, E., Julien, S., Bobowski, M., Grigoriadis, A., Tutt, A., Tulasne, D., Le Bourhis, X., and Delannoy, P. (2010) GD3 synthase expression enhances proliferation and tumor growth of MDAMB- 231 breast cancer cells through c-Met activation, Mol. Cancer Res., 8, 1526-1535.
80. Cazet, A., Bobowski, M., Rombouts, Y, Lefebvre, J., Steenackers, A., Popa, I., Guerardel, Y, Le Bourhis, X., Tulasne, D., and Delannoy, P. (2012) The ganglioside G(D2) induces the constitutive activation of c-Met in MDA-MB-231 breast cancer cells expressing the G(D3) synthase, Glycobiology, 22, 806-816.
81. Battula, V. L., Shi, Y, Evans, K. W., Wang, R. Y, Spaeth, E. L., Jacamo, R. O., Guerra, R., Sahin, A. A., Marini, F. C., Hortobagyi, G., Mani, S. A., and Andreeff, M. (2012) Ganglioside GD2 identifies breast cancer stem cells and promotes tumorigenesis, J. Clin. Invest., 122, 2066-2078.
82. Liang, Y. J., Ding, Y, Levery, S. B., Lobaton, M., Handa, K., and Hakomori, S. I. (2013) Differential expression profiles of glycosphingolipids in human breast cancer stem cells vs. cancer non-stem cells, Proc. Natl. Acad. Sci. USA, 110, 4968-4973.
83. Sarkar, T R., Battula, V. L., Werden, S. J., Vijay, G. V., Ramirez-Pena, E. Q., Taube, J. H., Chang, J. T, Miura, N., Porter, W, Sphyris, N., Andreeff, M., and Mani, S. A. (2015) GD3 synthase regulates epithelial-mesenchymal transition and metastasis in breast cancer, Oncogene, 34, 2958-2967.
84. Taki, T, Hirabayashi, Y, Ishikawa, H., Ando, S., Kon, K., Tanaka, Y, and Matsumoto, M. (1986) A ganglioside of rat ascites hepatoma AH 7974F cells. Occurrence of a novel disialoganglioside (GD1 alpha) with a unique N-acetylneuraminosyl(alpha 2-6)-N-acetylgalactosamine structure, J. Biol. Chem., 261, 3075-3078.
85. Hirabayashi, Y, Hyogo, A., Nakao, T, Tsuchiya, K., Suzuki, Y, Matsumoto, M., Kon, K., and Ando, S. (1990) Isolation and characterization of extremely minor gangliosides, GM1b and GD1 alpha, in adult bovine brains as developmentally regulated antigens, J. Biol. Chem., 265, 8144-8151.
86. Furuya, S., Irie, F., Hashikawa, T, Nakazawa, K., Kozakai, A., Hasegawa, A., Sudo, K., and Hirabayashi, Y (1994) Ganglioside GD1 alpha in cerebellar Purkinje cells. Its specific absence in mouse mutants with Purkinje cell abnormality and altered immunoreactivity in response to conjunctive stimuli causing long-term desensitization, J. Biol. Chem., 269, 32418-32425.
87. Ikehara, Y., Shimizu, N., Kono, M., Nishihara, S., Nakanishi, H., Kitamura, T, Narimatsu, H., Tsuji, S., and Tatematsu, M. (1999) A novel glycosyltransferase with a polyglutamine repeat; a new candidate for GD1alpha synthase (ST6GalNAc V), FEBSLett., 463, 92-96.
88. Kroes, R. A., He, H., Emmett, M. R., Nilsson, C. L., Leach, F. E., Amster, I. J., Marshall, A. G., and Moskal, J. R. (2010) Overexpression of ST6GalNAcV, a ganglioside-specific alpha2,6-sialyltransferase, inhibits glioma growth in vivo, Proc. Natl. Acad. Sci. USA, 107, 12646-12651.
89. Taki, T, Ishikawa, D., Ogura, M., Nakajima, M., and Handa, S. (1997) Ganglioside GD1alpha functions in the adhesion of metastatic tumor cells to endothelial cells of the target tissue, Cancer Res., 57, 1882-1888.
90. Bos, P. D., Zhang, X. H., Nadal, C., Shu, W, Gomis, R. R., Nguyen, D. X., Minn, A. J., van de Vijver, M. J., Gerald, W L., Foekens, J. A., and Massague, J. (2009) Genes that mediate breast cancer metastasis to the brain, Nature, 459, 1005-1009.
91. Modak, S., and Cheung, N. K. (2007) Disialoganglioside directed immunotherapy of neuroblastoma, Cancer Invest., 25, 67-77.
92. Gajdosik, Z. (2014) Racotumomab- a novel anti-idiotype monoclonal antibody vaccine for the treatment of cancer, Drugs Today (Barc.), 50, 301-307.
93. Osorio, M., Gracia, E., Reigosa, E., Hernandez, J., de la Torre, A., Saurez, G., Perez, K., Viada, C., Cepeda, M., Carr, A., Avila, Y., Rodriguez, M., and Fernandez, L. E. (2012) Effect of vaccination with N-glycolyl GM3/VSSP vaccine by subcutaneous injection in patients with advanced cutaneous melanoma, Cancer Manag. Res., 4, 341-345.
94. Alfonso, S., Valdes-Zayas, A., Santiesteban, E. R., Flores, Y. I., Areces, F., Hernandez, M., Viada, C. E., Mendoza, I. C., Guerra, P. P., Garcia, E., Ortiz, R. A., de la Torre, A. V., Cepeda, M., Perez, K., Chong, E., Hernandez, A. M., Toledo, D., Gonzalez, Z., Mazorra, Z., Crombet, T, Perez, R., Vazquez, A. M., and Macias, A. E. (2014) A randomized, multicenter, placebo-controlled clinical trial of racotumomab-alum vaccine as switch maintenance therapy in advanced non-small cell lung cancer patients, Clin. Cancer Res., 20, 3660-3671.
95. Kim, Y J., Choi, J. S., Seo, J., Song, J. Y, Lee, S. E., Kwon, M. J., Kwon, M. J., Kundu, J., Jung, K., Oh, E., Shin, Y K., and Choi, Y L. (2014) MET is a potential target for use in combination therapy with EGFR inhibition in triple-negative/basal-like breast cancer, Int. J. Cancer, 134, 2424-2436.
96. Fu, P., Du, F., Yao, M., Lv, K., and Liu, Y. (2014) MicroRNA-185 inhibits proliferation by targeting c-Met in human breast cancer cells, Exp. Ther. Med., 8, 1879-1883.
97. Dobrenkov, K., and Cheung, N. K. (2014) GD2-targeted immunotherapy and radioimmunotherapy, Semin. Oncol., 41, 589-612.
98. Chames, P., and Baty, D. (2009) Bispecific antibodies for cancer therapy: the light at the end of the tunnel? MAbs, 1, 539-547.
99. Li, J., Liu, R., Yang, Y, Huang, Y, Li, X., Liu, R., and Shen, X. (2014) Triptolide-induced in vitro and in vivo cytotoxicity in human breast cancer stem cells and primary breast cancer cells, Oncol. Rep., 31, 2181-2186.