Role of gangliosides in the differentiation of human mesenchymal-derived stem cells into osteoblasts and neuronal cells

BMB Reports

Volumn 46, Issue 11, 2013, Pages 527-532

  Moussavou, Ghislain ^a   Kwak, Dong Hoon ^b   Lim, Malg Um ^a   Kim, Ji Su ^c   Kim, Sun Uk ^c   Chang, Kyu Tae ^c   Choo, Young Kug ^a  

^a Wonkwang University   (South Korea)

^b Korea Institute of Oriental Medicine (KIOM)   (South Korea)

^c Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

Author keywords

Differentiation; Gangliosides; Human mesenchymal stem cells (hMSCs); Neuronal cells; Osteoblasts

Indexed keywords

GANGLIOSIDE;

ADULT STEM CELL; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL LINEAGE; CYTOLOGY; DRUG EFFECT; HUMAN; MESENCHYMAL STROMA CELL; METABOLISM; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; OSTEOBLAST; SHORT SURVEY;

ADULT STEM CELLS; CELL DIFFERENTIATION; CELL LINEAGE; GANGLIOSIDES; HUMANS; MESENCHYMAL STROMAL CELLS; NEUROGENESIS; NEURONS; OSTEOBLASTS; OSTEOGENESIS;

EID: 84890210837     PISSN: 19766696     EISSN: 1976670X     Source Type: Journal    
DOI: 10.5483/BMBRep.2013.46.11.179     Document Type: Short Survey

References (58)

1. Yu, R. K., Nakatani, Y. and Yanagisawa, M. (2009). The role of glycosphingolipid metabolism in the developing brain. J. Lipid Res. 50 (Suppl), S440-445.
2. Allende, M. L. and Proia, R. L. (2002). Lubricating cell signaling pathways with gangliosides. Curr. Opin. Struct. Biol. 12, 587-592.
3. Spiegel, S. and Fishman, P. H. (1987). Gangliosides as bimodal regulators of cell growth. Proc. Nat. Acad. Sci. U. S. A. 84, 141-145.
4. Hannun, Y. A. and Bell, R. M. (1989). Functions of sphingolipids and sphingolipid breakdown products in cellular regulation. Science 243, 500-507.
5. Hakomori, S. and Igarashi, Y. (1993). Gangliosides and glycosphingolipids as modulators of cell growth, adhesion, and transmembrane signaling. Adv. Lipid Res. 25, 147-162.
6. Oliver, S. P., Lewis, M. J., Gillespie, B. E. and Dowlen, H. H. (1992). Influence of prepartumantibiotic therapy on intramammary infections in primigravid heifers during early lactation. J. Dairy Sci. 75, 406-414.
7. Hakomori, S. (1990). Bifunctional role of glycosphingolipids. Modulators for transmembrane signaling and mediators for cellular interactions. J. Biol. Chem. 265, 18713-18716.
8. Martini, F., Riondino, S., Pignatelli, P., Gazzaniga, P. P., Ferroni, P. and Lenti, L. (2002). Involvement of GD3 in platelet activation. A novel association with Fcgamma receptor. Biochim. Biophys. Acta 1583, 297-304.
9. Wang, X. Q., Sun, P. and Paller, A. S. (2002). Ganglioside modulation regulates epithelial cell adhesion and spreading via ganglioside-specific effects on signaling. J. Biol. Chem. 277, 40410-40419.
10. 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.
11. Yu, R. K. (1994). Development regulation of ganglioside metabolism. Prog. Brain Res. 101, 31-44.
12. 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.
13. Matsuzaki, K. (2010). Ganglioside cluster-mediated aggregation and cytotoxicity of amyloid beta-peptide: molecular mechanism and inhibition. Yakugaku Zasshi 130, 511-515.
14. Fortier, L. A. (2005). Stem cells: classifications, controversies, and clinical applications. Vet. Surg. 34, 415-423.
15. Evans, M. J. and Kaufman, M. H. (1981). Establishment in culture of pluripotential cells from mouse embryos. Nature 292, 154-156.
16. Kulterer, B., Friedl, G., Jandrositz, A., Sanchez-Cabo, F., Prokesch, A., Paar, C., Scheideler, M., Windhager, R., Preisegger, K. H. and Trajanoski, Z. (2007). Gene expression profiling of human mesenchymal stem cells derived from bone marrow during expansion and osteoblast differentiation. BMC Genomics 8, 70.
17. Bron, D., De Bruyn, C., Balasse, H., Ley, P., De Hemptinne, D., von Lennep, E., Homans, C., Marckowicz, E., Mathieu, P., Deleuse, M. D., Francotte, J., Thomas, d., Dorval, C., Dejeneffe, M., Andrien, M. and Delforge, A. (2008). Cord blood: from bench to bedside.Bull Cancer 95, 314-319.
18. Kern, S., Eichler, H., Stoeve, J., Kluter, H. and Bieback, K. (2006). Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 24, 1294-1301.
19. Fukuchi, Y., Nakajima, H., Sugiyama, D., Hirose, I., Kitamura, T. and Tsuji, K. (2004). Human placenta-derived cells have mesenchymal stem/progenitor cell potential. Stem Cells 22, 649-658.
20. Gronthos, S., Mankani, M., Brahim, J., Robey, P. G. and Shi, S. (2000). Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc. Nat. Acad. Sci. U. S. A. 97, 13625-13630.
21. Fu, L., Zhu, L., Huang, Y., Lee, T. D., Forman, S. J. and Shih, C. C. (2008). Derivation of neural stem cells from mesenchymalstemcells: evidence for a bipotential stem cell population. Stem Cells Dev. 17, 1109-1121.
22. Deng, J., Petersen, B. E., Steindler, D. A., Jorgensen, M. L. and Laywell, E. D. (2006). Mesenchymal stem cells spontaneously express neural proteins in culture and are neurogenic after transplantation. Stem Cells 24, 1054-1064.
23. Yang, Q., Mu, J., Li, Q., Li, A., Zeng, Z., Yang, J., Zhang, X., Tang, J. and Xie, P. (2008). A simple and efficient method for deriving neurospheres from bone marrow stromal cells. Biochem. Biophys. Res. Commun. 372, 520-524.
24. Gerstenfeld, L. C., Barnes, G. L., Shea, C. M. and Einhorn, T. A. (2003). Osteogenic differentiation is selectively promoted by morphogenetic signals from chondrocytes and synergized by a nutrient rich growth environment. Connect. Tissue Res. 44(Suppl 1), 85-91.
25. Ikeda, E., Hirose, M., Kotobuki, N., Shimaoka, H., Tadokoro, M., Maeda, M., Hayashi, Y., Kirita, T. and Ohgushi, H. (2006). Osteogenic differentiation of human dental papilla mesenchymal cells. Biochem. Bbiophys. Res. Commun. 342, 1257-1262.
26. Ledeen, R. W. and Yu, R. K. (1982). Gangliosides: structure, isolation, and analysis. Methods Enzymol. 83, 139-191.
27. Lee, S. H., Ryu, J. S., Lee, J. W., Kwak, D. H., Ko, K. and Choo, Y. K. (2010). Comparison of ganglioside expression between human adipose- and dental pulp-derived stem cell differentiation into osteoblasts. Arch. Pharm. Res. 33, 585-591.
28. Prinetti, A., Iwabuchi, K. and Hakomori, S. (1999). Glycosphingolipid- enriched signaling domain in mouse neuroblastoma Neuro2a cells. Mechanism of ganglioside- dependent neuritogenesis. J. Biol. Chem. 274, 20916-20924.
29. Frey, M. R., Golovin, A. and Polk, D. B. (2004). Epidermal growth factor-stimulated intestinal epithelial cell migration requires Src family kinase-dependent p38 MAPK signaling. J. Biol. Chem. 279, 44513-44521.
30. Jaiswal, R. K., Jaiswal, N., Bruder, S. P., Mbalaviele, G., Marshak, D. R. and Pittenger, M. F. (2000). Adult human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by mitogen-activated protein kinase. J. Biol. Chem. 275, 9645-9652.
31. Mirkin, B. L., Clark, S. H. and Zhang, C. (2002). Inhibition of human neuroblastoma cell proliferation and EGF receptor phosphorylation by gangliosides GM1, GM3, GD1A and GT1B. Cell Prolif. 35, 105-115.
32. Radio, N. M., Doctor, J. S. and Witt-Enderby, P. A. (2006). Melatonin enhances alkaline phosphatase activity in differentiating human adult mesenchymal stem cells grown in osteogenic medium via MT2 melatonin receptors and the MEK/ERK (1/2) signaling cascade. J. Pineal Res. 40, 332-342.
33. Tanikawa, R., Tanikawa, T., Okada, Y., Nakano, K., Hirashima, M., Yamauchi, A., Hosokawa, R. and Tanaka, Y. (2008). Interaction of galectin-9 with lipid rafts induces osteoblast proliferation through the c-Src/ERK signaling pathway. J. Bone Miner. Res. 23, 278-286.
34. Kim, S. M., Jung, J. U., Ryu, J. S., Jin, J. W., Yang, H. J., Ko, K., You, H. K., Jung, K. Y. and Choo, Y. K. (2008). Effects of gangliosides on the differentiation of human mesenchymal stem cells into osteoblasts by modulating epidermal growth factor receptors. Biochem. Biophys. Res. Commun. 371, 866-871.
35. Liu, Y., Li, R. and Ladisch, S. (2004). Exogenous ganglioside GD1a enhances epidermal growth factor receptor binding and dimerization. J. Biol. Chem. 279, 36481-36489.
36. Lee, D. H., Koo, D. B., Ko, K., Ko, K., Kim, S. M., Jung, J. U., Ryu, J. S., Jin, J. W., Yang, H. J., Do, S. I., Jung, K. Y. and Choo, Y. K. (2007). Effects of daunorubicin on ganglioside expression and neuronal differentiation of mouse embryonic stem cells. Biochem. Biophys. Res. Commun. 362, 313-318.
37. Yang, H. J., Jung, K. Y., Kwak, D. H., Lee, S. H., Ryu, J. S., Kim, J. S., Chang, K. T., Lee, J. W. and Choo, Y. K. (2011). Inhibition of ganglioside GD1a synthesis suppresses the differentiation of human mesenchymal stem cells into osteoblasts. Dev. Growth Differ. 53, 323-332.
38. Liang, L., Ma, T., Chen, W., Hu, J., Bai, X., Li, J. and Liang, T. (2009). Therapeutic potential and related signal pathway of adipose-derived stem cell transplantation for rat liver injury. Hepatol. Res. 39, 822-832.
39. Zuberbier, T., Guhl, S., Hantke, T., Hantke, C., Welker, P., Grabbe, J. and Henz, B. M. (1999). Alterations in ganglioside expression during the differentiation of human mast cells. Exp. Dermatol. 8, 380-387.
40. Ryu, J. S., Ko, K., Lee, J. W., Park, S. B., Byun, S. J., Jeong, E. J., Ko, K. and Choo, Y. K. (2009). Gangliosides are involved in neural differentiation of human dental pulp-derived stem cells. Biochem. Biophys. Res. Commun. 387, 266-271.
41. Ledeen, R. W., Wu, G., Lu, Z. H., Kozireski-Chuback, D. and Fang, Y. (1998). The role of GM1 and other gangliosides in neuronal differentiation. Overview and new finding. Ann. N. Y. Acad. Sci. 845, 161-175.
42. Todeschini, A. R., Dos Santos, J. N., Handa, K. and Hakomori, S. I. (2008). Ganglioside GM2/GM3 complex affixed on silica nanospheres strongly inhibits cell motility through CD82/cMet-mediated pathway. Proc. Nat. Acad. Sci. U. S. A. 105, 1925-1930.
43. Kotani, M., Kawashima, I., Ozawa, H., Terashima, T. and Tai, T. (1993). Differential distribution of major gangliosides in rat central nervous system detected by specific monoclonal antibodies. Glycobiology 3, 137-146.
44. Higashi, H. and Chen, N. H. (2004). Ganglioside/protein kinase signals triggering cytoskeletal actin reorganization. Glycoconj. J. 20, 49-58.45. Osanai, T., Kotani, M., Yuen, C. T., Kato, H., Sanai, Y. and Takeda, S. (2003). Immunohistochemical and biochemical analyses of GD3, GT1b, and GQ1b gangliosides during neural differentiation of P19 EC cells. FEBS Letters 537, 73-78.
45. Osanai, T., Kotani, M., Yuen, C. T., Kato, H., Sanai, Y. and Takeda, S. (2003). Immunohistochemical and biochemical analyses of GD3, GT1b, and GQ1b gangliosides during neural differentiation of P19 EC cells. FEBS Letters 537, 73-78
46. Kwak, D. H., Yu, K., Kim, S. M., Lee, D. H., Kim, S. M., Jung, J. U., Seo, J. W., Kim, N., Lee, S., Jung, K. Y., You, H. K., Kim, H. A. and Choo, Y. K. (2006). Dynamic changes of gangliosides expression during the differentiation of embryonic and mesenchymal stem cells into neural cells. Exp. Mol. Med 38, 668-676.
47. Giraudo, C. G., Rosales Fritz, V. M. and Maccioni, H. J. (1999). GA2/GM2/GD2 synthase localizes to the trans-golgi network of CHO-K1 cells. Biochem. J. 342 Pt 3, 633-640.
48. Jin, H. J., Park, S. K., Oh, W., Yang, Y. S., Kim, S. W. and Choi, S. J. (2009). Down-regulation of CD105 is associated with multi-lineage differentiation in human umbilical cord blood-derived mesenchymal stem cells. Biochem. Biophys. Res. Commun. 381, 676-681.
49. Martinez, C., Hofmann, T. J., Marino, R., Dominici, M. and Horwitz, E. M. (2007). Human bone marrow mesenchymal stromal cells express the neural ganglioside GD2: a novel surface marker for the identification of MSCs. Blood 109, 4245-4248.
50. Xu, J., Liao, W., Gu, D., Liang, L., Liu, M., Du, W., Liu, P., Zhang, L., Lu, S., Dong, C., Zhou, B. and Han, Z. (2009). Neural ganglioside GD2 identifies a subpopulation of mesenchymal stem cells in umbilical cord. Cell. Physiol. Biochem. 23, 415-424.
51. Takamiya, K., Yamamoto, A., Furukawa, K., Yamashiro, S., Shin, M., Okada, M., Fukumoto, S., Haraguchi, M., Takeda, N., Fujimura, K., Sakae, M., Kishikawa, K., Shiku, H., Furukawa, K. and Aizawa, S. (1996). Mice with disrupted GM2/GD2 synthase gene lack complex gangliosides but exhibit only subtle defects in their nervous system. Proc. Nat. Acad. Sci. U. S. A. 93, 10662-10667.
52. Ferrari, G., Anderson, B. L., Stephens, R. M., Kaplan, D. R. and Greene, L. A. (1995). Prevention of apoptotic neuronal death by GM1 ganglioside.Involvement of Trkneurotrophin receptors. J. Biol. Chem. 270, 3074-3080.
53. Cavallini, L., Venerando, R., Miotto, G. and Alexandre, A. (1999). Ganglioside GM1 protection from apoptosis of rat heart fibroblasts. Arch. Biochem. Bioph. 370, 156-162.
54. Stojiljkovic, M., Blagojevic, T., Vukosavic, S., Zvezdina, N. D., Pekovic, S., Nikezic, G. and Rakic, L. (1996). Ganglioside GM1 and GM3 in early human brain development: an immunocytochemical study. Int. J. Dev. Neurosci. 14, 35-44.
55. Vinson, M., Strijbos, P. J., Rowles, A., Facci, L., Moore, S. E., Simmons, D. L. and Walsh, F. S. (2001). Myelin-associated glycoprotein interacts with ganglioside GT1b. A mechanism for neurite outgrowth inhibition. J. Biol. Chem. 276, 20280-20285.
56. Jennemann, R., Sandhoff, R., Wang, S., Kiss, E., Gretz, N., Zuliani, C., Martin-Villalba, A., Jager, R., Schorle, H., Kenzelmann, M., Bonrouhi, M., Wiegandt, H. and Grone, H. J. (2005). Cell-specific deletion of glucosylceramide synthase in brain leads to severe neural defects after birth. Proc. Nat. Acad. Sci. U. S. A. 102, 12459-12464.
57. Yamashita, T., Yamauchi, A., Miyai, A., Taniguchi, M., Yoshimine, T. and Tohyama, M. (1999). Differential regulation of adenine nucleotide translocators by hypertonicity in the brain. J. Neurochem. 72, 1259-1265.
58. Kwak, D. H., Seo, B. B., Chang, K. T. and Choo, Y. K. (2011). Roles of gangliosides in mouse embryogenesis and embryonic stem cell differentiation. Exp. Mol. Med. 43, 379-388.