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Stem Cell Glycolipids

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Abstract

Glycolipids are compounds containing one or more monosaccharide residues bound by a glycosidic linkage to a hydrophobic moiety. Because of their expression patterns and the intracellular localization patterns, glycolipids, including stage-specific embryonic antigens (SSEA-3, SSEA-4, and possibly SSEA-1) and gangliosides (e.g., GD3, GD2, and A2B5 antigens), have been used as marker molecules of stem cells. In this review, I will introduce glycolipids expressed in pluripotent stem cells (embryonic stem cells, induced pluripotent stem cells, very small embryonic-like stem cells, amniotic stem cells, and multilineage-differentiating stress enduring cells), multipotent stem cells (neural stem cells, mesenchymal stem cells, fetal liver multipotent progenitor cells, and hematopoietic stem cells), and cancer stem cells (brain cancer stem cells and breast cancer stem cells), and discuss their availability as biomarkers for identifying and isolating stem cells.

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References

  1. Yu RK, Yanagisawa M, Ariga T (2007) Glycosphingolipid structures. In: Kamerling JP (ed) Comprehensive Glycoscience. Elsevier, Oxford, pp 73–122

    Google Scholar 

  2. Yu RK, Nakatani Y, Yanagisawa M (2009) The role of glycosphingolipid metabolism in the developing brain. J Lipid Res 50 Suppl:S440–445

    Google Scholar 

  3. Yu RK, Bieberich E, Xia T, Zeng G (2004) Regulation of ganglioside biosynthesis in the nervous system. J Lipid Res 45:783–793

    PubMed  CAS  Google Scholar 

  4. Hakomori S (2003) Structure, organization, and function of glycosphingolipids in membrane. Curr Opin Hematol 10:16–24

    PubMed  CAS  Google Scholar 

  5. Ledeen RW, Wu G (2008) Nuclear sphingolipids: metabolism and signaling. J Lipid Res 49:1176–1186

    PubMed  CAS  Google Scholar 

  6. Anderson RG (1998) The caveolae membrane system. Annu Rev Biochem 67:199–225

    PubMed  CAS  Google Scholar 

  7. Simons K, Toomre D (2000) Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1:31–39

    PubMed  CAS  Google Scholar 

  8. Hakomori S (2002) Inaugural article: the glycosynapse. Proc Natl Acad Sci USA 99:225–232

    CAS  Google Scholar 

  9. Yoshikawa M, Go S, Takasaki K, Kakazu Y, Ohashi M, Nagafuku M, Kabayama K, Sekimoto J, Suzuki S, Takaiwa K, Kimitsuki T, Matsumoto N, Komune S, Kamei D, Saito M, Fujiwara M, Iwasaki K, Inokuchi J (2009) Mice lacking ganglioside GM3 synthase exhibit complete hearing loss due to selective degeneration of the organ of Corti. Proc Natl Acad Sci USA 106:9483–9488

    PubMed  CAS  Google Scholar 

  10. Ohmi Y, Tajima O, Ohkawa Y, Mori A, Sugiura Y, Furukawa K, Furukawa K (2009) Gangliosides play pivotal roles in the regulation of complement systems and in the maintenance of integrity in nerve tissues. Proc Natl Acad Sci USA 106:22405–22410

    PubMed  CAS  Google Scholar 

  11. Furukawa K, Takamiya K, Okada M, Inoue M, Fukumoto S, Furukawa K (2001) Novel functions of complex carbohydrates elucidated by the mutant mice of glycosyltransferase genes. Biochim Biophys Acta 1525:1–12

    PubMed  CAS  Google Scholar 

  12. Proia RL (2003) Glycosphingolipid functions: insights from engineered mouse models. Philos Trans R Soc Lond B Biol Sci 358:879–883

    PubMed  CAS  Google Scholar 

  13. Kaida K, Ariga T, Yu RK (2009) Antiganglioside antibodies and their pathophysiological effects on Guillain-Barré syndrome and related disorders–a review. Glycobiology 19:676–692

    PubMed  CAS  Google Scholar 

  14. Futerman AH, van Meer G (2004) The cell biology of lysosomal storage disorders. Nat Rev Mol Cell Biol 5:554–565

    PubMed  CAS  Google Scholar 

  15. Simpson MA, Cross H, Proukakis C, Priestman DA, Neville DC, Reinkensmeier G, Wang H, Wiznitzer M, Gurtz K, Verganelaki A, Pryde A, Patton MA, Dwek RA, Butters TD, Platt FM, Crosby AH (2004) Infantile-onset symptomatic epilepsy syndrome caused by a homozygous loss-of-function mutation of GM3 synthase. Nat Genet 36:1225–1229

    PubMed  CAS  Google Scholar 

  16. Ariga T, McDonald MP, Yu RK (2008) Role of ganglioside metabolism in the pathogenesis of Alzheimer’s disease–a review. J Lipid Res 49:1157–1175

    PubMed  CAS  Google Scholar 

  17. Bernardo A, Harrison FE, McCord M, Zhao J, Bruchey A, Davies SS, Jackson Roberts L, 2nd, Mathews PM, Matsuoka Y, Ariga T, Yu RK, Thompson R, McDonald MP (2009) Elimination of GD3 synthase improves memory and reduces amyloid-β plaque load in transgenic mice. Neurobiol Aging 30:1777–1791

    Google Scholar 

  18. Matsuzaki K, Kato K, Yanagisawa K (2010) Aβ polymerization through interaction with membrane gangliosides. Biochim Biophys Acta 1801:868–877

    PubMed  CAS  Google Scholar 

  19. Kawakami Y, Nakamura K, Kojima H, Suzuki M, Inagaki F, Suzuki A, Ikuta J, Uchida A, Murata Y, Tamai Y (1996) A novel fucosyltetrahexosylceramide in plerocercoids of the parasite Spirometra erinacei. Eur J Biochem 239:905–911

    PubMed  CAS  Google Scholar 

  20. Hada N (2006) Syntheses and biological activities of glycosphingolipids from invertebrate species. Trends Glycosci Glycotechnol 18:383–399

    CAS  Google Scholar 

  21. Nakamura K, Inagaki F, Tamai Y (1988) A novel ganglioside in dogfish brain. Occurrence of a trisialoganglioside with a sialic acid linked to N-acetylgalactosamine. J Biol Chem 263:9896–9900

    PubMed  CAS  Google Scholar 

  22. Yu RK, Macala LJ, Taki T, Weinfield HM, Yu FS (1988) Developmental changes in ganglioside composition and synthesis in embryonic rat brain. J Neurochem 50:1825–1829

    PubMed  CAS  Google Scholar 

  23. Bouvier JD, Seyfried TN (1989) Ganglioside composition of normal and mutant mouse embryos. J Neurochem 52:460–466

    PubMed  CAS  Google Scholar 

  24. Yu RK (1994) Development regulation of ganglioside metabolism. Prog Brain Res 101:31–44

    PubMed  CAS  Google Scholar 

  25. Ngamukote S, Yanagisawa M, Ariga T, Ando S, Yu RK (2007) Developmental changes of glycosphingolipids and expression of glycogenes in mouse brains. J Neurochem 103:2327–2341

    PubMed  CAS  Google Scholar 

  26. Ishii A, Ikeda T, Hitoshi S, Fujimoto I, Torii T, Sakuma K, Nakakita S, Hase S, Ikenaka K (2007) Developmental changes in the expression of glycogenes and the content of N-glycans in the mouse cerebral cortex. Glycobiology 17:261–276

    PubMed  CAS  Google Scholar 

  27. Yu RK, Ariga T, Yanagisawa M, Zeng G (2008) Gangliosides in the nervous system: Biosynthesis and degradation. In: Fraser-Reid B, Tatsuka K, Thiem J (eds) Glycoscience. Springer, Berlin, pp 1671–1695

    Google Scholar 

  28. Suzuki Y, Yanagisawa M, Ariga T, Yu RK (2011) Histone acetylation-mediated glycosyltransferase gene regulation in mouse brain during development. J Neurochem. in press

  29. Yanagisawa M, Yu RK (2007) The expression and functions of glycoconjugates in neural stem cells. Glycobiology 17:57R–74R

    PubMed  CAS  Google Scholar 

  30. Evans MJ, Kaufman MH (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292:154–156

    PubMed  CAS  Google Scholar 

  31. Muramatsu T, Muramatsu H (2004) Carbohydrate antigens expressed on stem cells and early embryonic cells. Glycoconj J 21:41–45

    PubMed  CAS  Google Scholar 

  32. Wright AJ, Andrews PW (2009) Surface marker antigens in the characterization of human embryonic stem cells. Stem Cell Res 3:3–11

    CAS  Google Scholar 

  33. Solter D, Knowles BB (1978) Monoclonal antibody defining a stage-specific mouse embryonic antigen (SSEA-1). Proc Natl Acad Sci USA 75:5565–5569

    PubMed  CAS  Google Scholar 

  34. Gooi HC, Feizi T, Kapadia A, Knowles BB, Solter D, Evans MJ (1981) Stage-specific embryonic antigen involves α 1 goes to 3 fucosylated type 2 blood group chains. Nature 292:156–158

    PubMed  CAS  Google Scholar 

  35. Martin GR (1981) Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci USA 78:7634–7638

    PubMed  CAS  Google Scholar 

  36. Cui L, Johkura K, Yue F, Ogiwara N, Okouchi Y, Asanuma K, Sasaki K (2004) Spatial distribution and initial changes of SSEA-1 and other cell adhesion-related molecules on mouse embryonic stem cells before and during differentiation. J Histochem Cytochem 52:1447–1457

    PubMed  CAS  Google Scholar 

  37. Thomson JA, Kalishman J, Golos TG, Durning M, Harris CP, Becker RA, Hearn JP (1995) Isolation of a primate embryonic stem cell line. Proc Natl Acad Sci USA 92:7844–7848

    PubMed  CAS  Google Scholar 

  38. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM (1998) Embryonic stem cell lines derived from human blastocysts. Science 282:1145–1147

    PubMed  CAS  Google Scholar 

  39. Kannagi R, Cochran NA, Ishigami F, Hakomori S, Andrews PW, Knowles BB, Solter D (1983) Stage-specific embryonic antigens (SSEA-3 and -4) are epitopes of a unique globo-series ganglioside isolated from human teratocarcinoma cells. EMBO J 2:2355–2361

    PubMed  CAS  Google Scholar 

  40. Draper JS, Pigott C, Thomson JA, Andrews PW (2002) Surface antigens of human embryonic stem cells: changes upon differentiation in culture. J Anat 200:249–258

    PubMed  CAS  Google Scholar 

  41. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676

    PubMed  CAS  Google Scholar 

  42. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861–872

    PubMed  CAS  Google Scholar 

  43. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, Slukvin II, Thomson JA (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318:1917–1920

    PubMed  CAS  Google Scholar 

  44. Kucia M, Reca R, Campbell FR, Zuba-Surma E, Majka M, Ratajczak J, Ratajczak MZ (2006) A population of very small embryonic-like (VSEL) CXCR4(+)SSEA-1(+)Oct-4 + stem cells identified in adult bone marrow. Leukemia 20:857–869

    PubMed  CAS  Google Scholar 

  45. Kucia M, Halasa M, Wysoczynski M, Baskiewicz-Masiuk M, Moldenhawer S, Zuba-Surma E, Czajka R, Wojakowski W, Machalinski B, Ratajczak MZ (2007) Morphological and molecular characterization of novel population of CXCR4 + SSEA-4 + Oct-4 + very small embryonic-like cells purified from human cord blood: preliminary report. Leukemia 21:297–303

    PubMed  CAS  Google Scholar 

  46. De Coppi P, Bartsch G Jr, Siddiqui MM, Xu T, Santos CC, Perin L, Mostoslavsky G, Serre AC, Snyder EY, Yoo JJ, Furth ME, Soker S, Atala A (2007) Isolation of amniotic stem cell lines with potential for therapy. Nat Biotechnol 25:100–106

    PubMed  Google Scholar 

  47. Kuroda Y, Kitada M, Wakao S, Nishikawa K, Tanimura Y, Makinoshima H, Goda M, Akashi H, Inutsuka A, Niwa A, Shigemoto T, Nabeshima Y, Nakahata T, Nabeshima YI, Fujiyoshi Y, Dezawa M (2010) Unique multipotent cells in adult human mesenchymal cell populations. Proc Natl Acad Sci USA 107:8639–8643

    PubMed  CAS  Google Scholar 

  48. Shamblott MJ, Axelman J, Wang S, Bugg EM, Littlefield JW, Donovan PJ, Blumenthal PD, Huggins GR, Gearhart JD (1998) Derivation of pluripotent stem cells from cultured human primordial germ cells. Proc Natl Acad Sci USA 95:13726–13731

    PubMed  CAS  Google Scholar 

  49. Kimber SJ, Brown DG, Pahlsson P, Nilsson B (1993) Carbohydrate antigen expression in murine embryonic stem cells and embryos. II. Sialylated antigens and glycolipid analysis. Histochem J 25:628–641

    PubMed  CAS  Google Scholar 

  50. Yamashita T, Wada R, Sasaki T, Deng C, Bierfreund U, Sandhoff K, Proia RL (1999) A vital role for glycosphingolipid synthesis during development and differentiation. Proc Natl Acad Sci USA 96:9142–9147

    PubMed  CAS  Google Scholar 

  51. Kwak DH, Yu K, Kim SM, Lee DH, Kim SM, Jung JU, Seo JW, Kim N, Lee S, Jung KY, You HK, Kim HA, Choo YK (2006) Dynamic changes of gangliosides expression during the differentiation of embryonic and mesenchymal stem cells into neural cells. Exp Mol Med 38:668–676

    PubMed  CAS  Google Scholar 

  52. Lee DH, Koo DB, Ko K, Ko K, Kim SM, Jung JU, Ryu JS, Jin JW, Yang HJ, Do SI, Jung KY, Choo YK (2007) Effects of daunorubicin on ganglioside expression and neuronal differentiation of mouse embryonic stem cells. Biochem Biophys Res Commun 362:313–318

    PubMed  CAS  Google Scholar 

  53. Jung JU, Ko K, Lee DH, Ko K, Chang KT, Choo YK (2009) The roles of glycosphingolipids in the proliferation and neural differentiation of mouse embryonic stem cells. Exp Mol Med 41:935–945

    PubMed  CAS  Google Scholar 

  54. Fenderson BA, Zehavi U, Hakomori S (1984) A multivalent lacto-N-fucopentaose III-lysyllysine conjugate decompacts preimplantation mouse embryos, while the free oligosaccharide is ineffective. J Exp Med 160:1591–1596

    PubMed  CAS  Google Scholar 

  55. Eggens I, Fenderson B, Toyokuni T, Dean B, Stroud M, Hakomori S (1989) Specific interaction between Lex and Lex determinants. A possible basis for cell recognition in preimplantation embryos and in embryonal carcinoma cells. J Biol Chem 264:9476–9484

    PubMed  CAS  Google Scholar 

  56. Kudo T, Kaneko M, Iwasaki H, Togayachi A, Nishihara S, Abe K, Narimatsu H (2004) Normal embryonic and germ cell development in mice lacking α 1,3-fucosyltransferase IX (Fut9) which show disappearance of stage-specific embryonic antigen 1. Mol Cell Biol 24:4221–4228

    PubMed  CAS  Google Scholar 

  57. Klassen H, Schwartz MR, Bailey AH, Young MJ (2001) Surface markers expressed by multipotent human and mouse neural progenitor cells include tetraspanins and non-protein epitopes. Neurosci Lett 312:180–182

    PubMed  CAS  Google Scholar 

  58. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703–716

    PubMed  CAS  Google Scholar 

  59. Capela A, Temple S (2002) LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 35:865–875

    PubMed  Google Scholar 

  60. Yanagisawa M, Taga T, Nakamura K, Ariga T, Yu RK (2005) Characterization of glycoconjugate antigens in mouse embryonic neural precursor cells. J Neurochem 95:1311–1320

    PubMed  CAS  Google Scholar 

  61. Piao JH, Odeberg J, Samuelsson EB, Kjaeldgaard A, Falci S, Seiger A, Sundstrom E, Akesson E (2006) Cellular composition of long-term human spinal cord- and forebrain-derived neurosphere cultures. J Neurosci Res 84:471–482

    PubMed  CAS  Google Scholar 

  62. Yanagisawa M, Nakamura K, Taga T (2004) Roles of lipid rafts in integrin-dependent adhesion and gp130 signalling pathway in mouse embryonic neural precursor cells. Genes Cells 9:801–809

    PubMed  CAS  Google Scholar 

  63. Nakatani Y, Yanagisawa M, Suzuki Y, Yu RK (2010) Characterization of GD3 ganglioside as a novel biomarker of mouse neural stem cells. Glycobiology 20:78–86

    PubMed  CAS  Google Scholar 

  64. Seyfried TN, Yu RK (1985) Ganglioside GD3: structure, cellular distribution, and possible function. Mol Cell Biochem 68:3–10

    PubMed  CAS  Google Scholar 

  65. Irvine RA, Seyfried TN (1994) Phylogenetic conservation of ganglioside GD3 expression during early vertebrate ontogeny. Comp Biochem Physiol B Biochem Mol Biol 109:603–612

    PubMed  CAS  Google Scholar 

  66. Birkle S, Ren S, Slominski A, Zeng G, Gao L, Yu RK (1999) Down-regulation of the expression of O-acetyl-GD3 by the O-acetylesterase cDNA in hamster melanoma cells: effects on cellular proliferation, differentiation, and melanogenesis. J Neurochem 72:954–961

    PubMed  CAS  Google Scholar 

  67. Birkle S, Gao L, Zeng G, Yu RK (2000) Down-regulation of GD3 ganglioside and its O-acetylated derivative by stable transfection with antisense vector against GD3-synthase gene expression in hamster melanoma cells: effects on cellular growth, melanogenesis, and dendricity. J Neurochem 74:547–554

    PubMed  CAS  Google Scholar 

  68. Goldman JE, Hirano M, Yu RK, Seyfried TN (1984) GD3 ganglioside is a glycolipid characteristic of immature neuroectodermal cells. J Neuroimmunol 7:179–192

    PubMed  CAS  Google Scholar 

  69. Cammer W, Zhang H (1996) Ganglioside GD3 in radial glia and astrocytes in situ in brains of young and adult mice. J Neurosci Res 46:18–23

    PubMed  CAS  Google Scholar 

  70. Maric D, Maric I, Chang YH, Barker JL (2003) Prospective cell sorting of embryonic rat neural stem cells and neuronal and glial progenitors reveals selective effects of basic fibroblast growth factor and epidermal growth factor on self-renewal and differentiation. J Neurosci 23:240–251

    PubMed  CAS  Google Scholar 

  71. Androutsellis-Theotokis A, Walbridge S, Park DM, Lonser RR, McKay RD (2010) Cholera toxin regulates a signaling pathway critical for the expansion of neural stem cell cultures from the fetal and adult rodent brains. PLoS One 5:e10841

    PubMed  Google Scholar 

  72. Campos LS, Decker L, Taylor V, Skarnes W (2006) Notch, epidermal growth factor receptor, and β1-integrin pathways are coordinated in neural stem cells. J Biol Chem 281:5300–5309

    PubMed  CAS  Google Scholar 

  73. Yanagisawa M, Nakamura K, Taga T (2005) Glycosphingolipid synthesis inhibitor represses cytokine-induced activation of the Ras-MAPK pathway in embryonic neural precursor cells. J Biochem 138:285–291

    PubMed  CAS  Google Scholar 

  74. 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, Grone HJ (2005) Cell-specific deletion of glucosylceramide synthase in brain leads to severe neural defects after birth. Proc Natl Acad Sci USA 102:12459–12464

    PubMed  CAS  Google Scholar 

  75. Ryu JS, Ko K, Lee JW, Park SB, Byun SJ, Jeong EJ, Ko K, Choo YK (2009) Gangliosides are involved in neural differentiation of human dental pulp-derived stem cells. Biochem Biophys Res Commun 387:266–271

    PubMed  CAS  Google Scholar 

  76. Jin HJ, Nam HY, Bae YK, Kim SY, Im IR, Oh W, Yang YS, Choi SJ, Kim SW (2010) GD2 expression is closely associated with neuronal differentiation of human umbilical cord blood-derived mesenchymal stem cells. Cell Mol Life Sci 67:1845–1858

    PubMed  CAS  Google Scholar 

  77. Yu RK, Yanagisawa M (2007) Glycosignaling in neural stem cells: involvement of glycoconjugates in signal transduction modulating the neural stem cell fate. J Neurochem 1:39–46 103 Suppl

    Google Scholar 

  78. Yanagisawa M, Ariga T, Yu RK (2006) Cholera toxin B subunit binding does not correlate with GM1 expression: a study using mouse embryonic neural precursor cells. Glycobiology 16:19G–22G

    PubMed  CAS  Google Scholar 

  79. Nagatsuka Y, Kasama T, Ohashi Y, Uzawa J, Ono Y, Shimizu K, Hirabayashi Y (2001) A new phosphoglycerolipid, ‘phosphatidylglucose’, found in human cord red cells by multi-reactive monoclonal anti-i cold agglutinin, mAb GL-1/GL-2. FEBS Lett 497:141–147

    PubMed  CAS  Google Scholar 

  80. Nagatsuka Y, Hara-Yokoyama M, Kasama T, Takekoshi M, Maeda F, Ihara S, Fujiwara S, Ohshima E, Ishii K, Kobayashi T, Shimizu K, Hirabayashi Y (2003) Carbohydrate-dependent signaling from the phosphatidylglucoside-based microdomain induces granulocytic differentiation of HL60 cells. Proc Natl Acad Sci USA 100:7454–7459

    PubMed  CAS  Google Scholar 

  81. Kinoshita MO, Furuya S, Ito S, Shinoda Y, Yamazaki Y, Greimel P, Ito Y, Hashikawa T, Machida T, Nagatsuka Y, Hirabayashi Y (2009) Lipid rafts enriched in phosphatidylglucoside direct astroglial differentiation by regulating tyrosine kinase activity of epidermal growth factor receptors. Biochem J 419:565–575

    PubMed  CAS  Google Scholar 

  82. Kim SM, Jung JU, Ryu JS, Jin JW, Yang HJ, Ko K, You HK, Jung KY, Choo YK (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

    PubMed  CAS  Google Scholar 

  83. Lee SH, Ryu JS, Lee JW, Kwak DH, Ko K, Choo YK (2010) Comparison of ganglioside expression between human adipose- and dental pulp-derived stem cell differentiation into osteoblasts. Arch Pharm Res 33:585–591

    PubMed  CAS  Google Scholar 

  84. Martinez C, Hofmann TJ, Marino R, Dominici M, Horwitz EM (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

    PubMed  CAS  Google Scholar 

  85. Freund D, Fonseca AV, Janich P, Bornhauser M, Corbeil D (2010) Differential expression of biofunctional GM1 and GM3 gangliosides within the plastic-adherent multipotent mesenchymal stromal cell population. Cytotherapy 12:131–142

    PubMed  CAS  Google Scholar 

  86. Xu J, Liao W, Gu D, Liang L, Liu M, Du W, Liu P, Zhang L, Lu S, Dong C, Zhou B, Han Z (2009) Neural ganglioside GD2 identifies a subpopulation of mesenchymal stem cells in umbilical cord. Cell Physiol Biochem 23:415–424

    PubMed  CAS  Google Scholar 

  87. Gang EJ, Bosnakovski D, Figueiredo CA, Visser JW, Perlingeiro RC (2007) SSEA-4 identifies mesenchymal stem cells from bone marrow. Blood 109:1743–1751

    PubMed  CAS  Google Scholar 

  88. Trubiani O, Zalzal SF, Paganelli R, Marchisio M, Giancola R, Pizzicannella J, Buhring HJ, Piattelli M, Caputi S, Nanci A (2010) Expression profile of the embryonic markers nanog, OCT-4, SSEA-1, SSEA-4, and frizzled-9 receptor in human periodontal ligament mesenchymal stem cells. J Cell Physiol 225:123–131

    PubMed  CAS  Google Scholar 

  89. Dan YY, Riehle KJ, Lazaro C, Teoh N, Haque J, Campbell JS, Fausto N (2006) Isolation of multipotent progenitor cells from human fetal liver capable of differentiating into liver and mesenchymal lineages. Proc Natl Acad Sci USA 103:9912–9917

    PubMed  CAS  Google Scholar 

  90. Yamazaki S, Iwama A, Takayanagi S, Morita Y, Eto K, Ema H, Nakauchi H (2006) Cytokine signals modulated via lipid rafts mimic niche signals and induce hibernation in hematopoietic stem cells. EMBO J 25:3515–3523

    PubMed  CAS  Google Scholar 

  91. Chae HD, Lee KE, Williams DA, Gu Y (2008) Cross-talk between RhoH and Rac1 in regulation of actin cytoskeleton and chemotaxis of hematopoietic progenitor cells. Blood 111:2597–2605

    PubMed  CAS  Google Scholar 

  92. Yamazaki S, Iwama A, Takayanagi S, Eto K, Ema H, Nakauchi H (2009) TGF-β as a candidate bone marrow niche signal to induce hematopoietic stem cell hibernation. Blood 113:1250–1256

    PubMed  CAS  Google Scholar 

  93. Yanagisawa M, Ariga T, Yu RK (2006) Fucosyl-GM1 expression and amyloid-β protein accumulation in PC12 cells. J Neurosci Res 84:1343–1349

    PubMed  CAS  Google Scholar 

  94. Barraud P, Stott S, Mollgard K, Parmar M, Bjorklund A (2007) In vitro characterization of a human neural progenitor cell coexpressing SSEA4 and CD133. J Neurosci Res 85:250–259

    PubMed  CAS  Google Scholar 

  95. Seyfried TN (1987) Ganglioside abnormalities associated with failed neural differentiation in a T-locus mutant mouse embryo. Dev Biol 123:286–291

    PubMed  CAS  Google Scholar 

  96. Liour SS, Dinkins MB, Su CY, Yu RK (2005) Spatiotemporal expression of GM1 in murine medial pallial neural progenitor cells. J Comp Neurol 491:330–338

    PubMed  CAS  Google Scholar 

  97. Raff MC, Miller RH, Noble M (1983) A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 303:390–396

    PubMed  CAS  Google Scholar 

  98. Kasai N, Yu RK (1983) The monoclonal antibody A2B5 is specific to ganglioside GQ1c. Brain Res 277:155–158

    PubMed  CAS  Google Scholar 

  99. Saito M, Kitamura H, Sugiyama K (2001) The specificity of monoclonal antibody A2B5 to c-series gangliosides. J Neurochem 78:64–74

    PubMed  CAS  Google Scholar 

  100. Farrer RG, Quarles RH (1999) GT3 and its O-acetylated derivative are the principal A2B5-reactive gangliosides in cultured O2A lineage cells and are down-regulated along with O-acetyl GD3 during differentiation to oligodendrocytes. J Neurosci Res 57:371–380

    PubMed  CAS  Google Scholar 

  101. Barres BA, Hart IK, Coles HS, Burne JF, Voyvodic JT, Richardson WD, Raff MC (1992) Cell death and control of cell survival in the oligodendrocyte lineage. Cell 70:31–46

    PubMed  CAS  Google Scholar 

  102. Cizkova D, Cizek M, Nagyova M, Slovinska L, Novotna I, Jergova S, Radonak J, Hlucilova J, Vanicky I (2009) Enrichment of rat oligodendrocyte progenitor cells by magnetic cell sorting. J Neurosci Methods 184:88–94

    PubMed  CAS  Google Scholar 

  103. Ogden AT, Waziri AE, Lochhead RA, Fusco D, Lopez K, Ellis JA, Kang J, Assanah M, McKhann GM, Sisti MB, McCormick PC, Canoll P, Bruce JN (2008) Identification of A2B5+ CD133-tumor-initiating cells in adult human gliomas. Neurosurgery 62:505–514

    PubMed  Google Scholar 

  104. Tchoghandjian A, Baeza N, Colin C, Cayre M, Metellus P, Beclin C, Ouafik L, Figarella-Branger D (2010) A2B5 cells from human glioblastoma have cancer stem cell properties. Brain Pathol 20:211–221

    PubMed  Google Scholar 

  105. Son MJ, Woolard K, Nam DH, Lee J, Fine HA (2009) SSEA-1 is an enrichment marker for tumor-initiating cells in human glioblastoma. Cell Stem Cell 4:440–452

    PubMed  CAS  Google Scholar 

  106. Mao XG, Zhang X, Xue XY, Guo G, Wang P, Zhang W, Fei Z, Zhen HN, You SW, Yang H (2009) Brain tumor stem-like cells identified by neural stem cell marker CD15. Transl Oncol 2:247–257

    PubMed  Google Scholar 

  107. Patru C, Romao L, Varlet P, Coulombel L, Raponi E, Cadusseau J, Renault-Mihara F, Thirant C, Leonard N, Berhneim A, Mihalescu-Maingot M, Haiech J, Bieche I, Moura-Neto V, Daumas-Duport C, Junier MP, Chneiweiss H (2010) CD133, CD15/SSEA-1, CD34 or side populations do not resume tumor-initiating properties of long-term cultured cancer stem cells from human malignant glio-neuronal tumors. BMC Cancer 10:66

    PubMed  Google Scholar 

  108. Read TA, Fogarty MP, Markant SL, McLendon RE, Wei Z, Ellison DW, Febbo PG, Wechsler-Reya RJ (2009) Identification of CD15 as a marker for tumor-propagating cells in a mouse model of medulloblastoma. Cancer Cell 15:135–147

    PubMed  CAS  Google Scholar 

  109. Ward RJ, Lee L, Graham K, Satkunendran T, Yoshikawa K, Ling E, Harper L, Austin R, Nieuwenhuis E, Clarke ID, Hui CC, Dirks PB (2009) Multipotent CD15+ cancer stem cells in patched-1-deficient mouse medulloblastoma. Cancer Res 69:4682–4690

    PubMed  CAS  Google Scholar 

  110. Takaishi S, Okumura T, Tu S, Wang SS, Shibata W, Vigneshwaran R, Gordon SA, Shimada Y, Wang TC (2009) Identification of gastric cancer stem cells using the cell surface marker CD44. Stem Cells 27:1006–1020

    PubMed  CAS  Google Scholar 

  111. Chang WW, Lee CH, Lee P, Lin J, Hsu CW, Hung JT, Lin JJ, Yu JC, Shao LE, Yu J, Wong CH, Yu AL (2008) Expression of Globo H and SSEA3 in breast cancer stem cells and the involvement of fucosyl transferases 1 and 2 in Globo H synthesis. Proc Natl Acad Sci USA 105:11667–11672

    PubMed  CAS  Google Scholar 

  112. Yagi H, Yanagisawa M, Kato K, Yu RK (2010) Lysosome-associated membrane protein 1 is a major SSEA-1-carrier protein in mouse neural stem cells. Glycobiology 20:976–981

    PubMed  CAS  Google Scholar 

  113. Inoko E, Nishiura Y, Tanaka H, Takahashi T, Furukawa K, Kitajima K, Sato C (2010) Developmental stage-dependent expression of an α2,8-trisialic acid unit on glycoproteins in mouse brain. Glycobiology 20:916–928

    PubMed  CAS  Google Scholar 

  114. Ledeen RW, Yu RK (1982) Gangliosides: structure, isolation, and analysis. Methods Enzymol 83:139–191

    PubMed  CAS  Google Scholar 

  115. Yu RK, Ariga T (2000) Ganglioside analysis by high-performance thin-layer chromatography. Methods Enzymol 312:115–134

    PubMed  CAS  Google Scholar 

  116. IUPAC-IUBMB Joint Commission on Biochemical Nomenclature (1997) Nomenclature of glycolipids. Pure Appl Chem 69:2475–2487

    Google Scholar 

  117. Svennerholm L (1963) Chromatographic separation of human brain gangliosides. J Neurochem 10:613–623

    PubMed  CAS  Google Scholar 

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Acknowledgments

The author thanks Dr. Robert K. Yu (Medical College of Georgia) for his support and Ms. Akiko Yanagisawa for her assistance.

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Correspondence to Makoto Yanagisawa.

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Special Issue: In Honor of Dr. Robert K. Yu.

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Yanagisawa, M. Stem Cell Glycolipids. Neurochem Res 36, 1623–1635 (2011). https://doi.org/10.1007/s11064-010-0358-1

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