Roles of gangliosides in the differentiation of mouse pluripotent stem cells to neural stem cells and neural cells (Review)
- Authors:
- Jae‑Sung Ryu
- Kinarm Ko
- Kisung Ko
- Ji‑Su Kim
- Sun‑Uk Kim
- Kyu‑Tae Chang
- Young‑Kug Choo
-
Affiliations: Stem Cell Research Center, Korea Institute of Bioscience and Biotechnology, Daejeon 34141, Republic of Korea, Department of Stem Cell Biology, School of Medicine, Konkuk University, Seoul 05029, Republic of Korea, Department of Medicine, College of Medicine, Chung‑Ang University, Seoul 06974, Republic of Korea, National Primate Research Center, Korea Institute of Bioscience and Biotechnology, Cheongju, Chungcheongbuk 28116, Republic of Korea, Department of Biological Science, College of Natural Sciences, Wonkwang University, Iksan, Jeollabuk 54538, Republic of Korea - Published online on: June 8, 2017 https://doi.org/10.3892/mmr.2017.6719
- Pages: 987-993
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|
Schengrund CL: The role(s) of gangliosides in neural differentiation and repair: A perspective. Brain Res Bull. 24:131–141. 1990. View Article : Google Scholar : PubMed/NCBI | |
|
Hakomori S: Structure, organization, and function of glycosphingolipids in membrane. Curr Opin Hematol. 10:16–24. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Yu RK, Nakatani Y and Yanagisawa M: The role of glycosphingolipid metabolism in the developing brain. J Lipid Res. 50 Suppl:S440–S445. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Anderson RG: The caveolae membrane system. Annu Rev Biochem. 67:199–225. 1998. View Article : Google Scholar : PubMed/NCBI | |
|
Simons K and Toomre D: Lipid rafts and signal transduction. Nat Rev Mol Cell Biol. 1:31–39. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Hakomori S, Yamamura S and Handa AK: Signal transduction through glyco(sphingo)lipids. Introduction and recent studies on glyco(sphingo)lipid-enriched microdomains. Ann N Y Acad Sci. 845:1–10. 1998. View Article : Google Scholar : PubMed/NCBI | |
|
Yu RK, Tsai YT, Ariga T and Yanagisawa M: Structures, biosynthesis, and functions of gangliosides-an overview. J Oleo Sci. 60:537–44. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Fortier LA: Stem cells: Classifications, controversies, and clinical applications. Vet Surg. 34:415–423. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Smith AG: Embryo-derived stem cells: Of mice and men. Annu Rev Cell Dev Biol. 17:435–462. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Takahashi K and Yamanaka S: Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 126:663–676. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Ko K, Tapia N, Wu G, Kim JB, Bravo MJ, Sasse P, Glaser T, Ruau D, Han DW, Greber B, et al: Induction of pluripotency in adult unipotent germline stem cells. Cell Stem Cell. 5:87–96. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Ko K, Araúzo-Bravo MJ, Kim J, Stehling M and Schöler HR: Conversion of adult mouse unipotent germline stem cells into pluripotent stem cells. Nature Protoc. 5:921–928. 2010. View Article : Google Scholar | |
|
Kim JB, Zaehres H, Wu G, Gentile L, Ko K, Sebastiano V, Araúzo-Bravo MJ, Ruau D, Han DW, Zenke M and Schöler HR: Pluripotent stem cells induced from adult neural stem cells by reprogramming with two factors. Nature. 454:646–650. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Kim JB, Sebastiano V, Wu G, Araúzo-Bravo MJ, Sasse P, Gentile L, Ko K, Ruau D, Ehrich M, van den Boom D, et al: Oct4-induced pluripotency in adult neural stem cells. Cell. 136:411–419. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Molyneaux BJ, Arlotta P, Menezes JR and Macklis JD: Neuronal subtype specification in the cerebral cortex. Nat Rev Neurosci. 8:427–437. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Shamblott MJ, Axelman J, Wang S, Bugg EM, Littlefield JW, Donovan PJ, Blumenthal PD, Huggins GR and Gearhart JD: Derivation of pluripotent stem cells from cultured human primordial germ cells. Proc Natl Acad Sci USA. 95:13726–13731. 1998. View Article : Google Scholar : PubMed/NCBI | |
|
Solter D and Knowles BB: Monoclonal antibody defining a stage-specific mouse embryonic antigen (SSEA-1). Proc Natl Acad Sci USA. 75:5565–5569. 1978. View Article : Google Scholar : PubMed/NCBI | |
|
Xu J, Hardin H, Zhang R, Sundling K, Buehler D and Lloyd RV: Stage-specific embryonic antigen-1 (SSEA-1) expression in thyroid tissues. Endocr Pathol. 27:271–275. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Liebert M, Jaffe R, Taylor RJ, Ballou BT, Solter D and Hakala TR: Detection of SSEA-1 on human renal tumors. Cancer. 59:1404–1408. 1987. View Article : Google Scholar : PubMed/NCBI | |
|
Suzuki Y, Haraguchi N, Takahashi H, Uemura M, Nishimura J, Hata T, Takemasa I, Mizushima T, Ishii H, Doki Y, et al: SSEA-3 as a novel amplifying cancer cell surface marker in colorectal cancers. Int J Oncol. 42:161–167. 2013.PubMed/NCBI | |
|
Cheung SK, Chuang PK, Huang HW, Hwang-Verslues WW, Cho CH, Yang WB, Shen CN, Hsiao M, Hsu TL, Chang CF and Wong CH: Stage-specific embryonic antigen-3 (SSEA-3) and β3GalT5 are cancer specific and significant markers for breast cancer stem cells. Proc Natl Acad Sci USA. 113:960–965. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Noto Z, Yoshida T, Okabe M, Koike C, Fathy M, Tsuno H, Tomihara K, Arai N, Noguchi M and Nikaido T: CD44 and SSEA-4 positive cells in an oral cancer cell line HSC-4 possess cancer stem-like cell characteristics. Oral Oncol. 49:787–795. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Gottschling S, Jensen K, Warth A, Herth FJ, Thomas M, Schnabel PA and Herpel E: Stage-specific embryonic antigen-4 is expressed in basaloid lung cancer and associated with poor prognosis. Eur Respir J. 41:656–663. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Knowles BB, Aden DP and Solter D: Monoclonal antibody detecting a stage-specific embryonic antigen (SSEA-1) on preimplantation mouse embryos and teratocarcinoma cells. Curr Top Microbiol Immunol. 81:51–53. 1978.PubMed/NCBI | |
|
Fox N, Damjanov I, Martinez-Hernandez A, Knowles BB and Solter D: Immunohistochemical localization of the early embryonic antigen (SSEA-1) in postimplantation mouse embryos and fetal and adult tissues. Dev Biol. 83:391–398. 1981. View Article : Google Scholar : PubMed/NCBI | |
|
Fox N, Shevinsky L, Knowles BB, Solter D and Dawjanov I: Distribution of murine stage-specific embryonic antigens in the kidneys of three rodent species. Exp Cell Res. 140:331–339. 1982. View Article : Google Scholar : PubMed/NCBI | |
|
Kannagi R, Cochran NA, Ishigami F, Hakomori S, Andrews PW, Knowles BB and Solter D: 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. 1983.PubMed/NCBI | |
|
Tettamanti G: Ganglioside/glycosphingolipid turnover: New concepts. Glycoconj J. 20:301–317. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Basu S, Kaufman B and Roseman S: Enzymatic synthesis of glucocerebroside by a glucosyltransferase from embryonic chicken brain. J Biol Chem. 248:1388–1394. 1973.PubMed/NCBI | |
|
Ichikawa S, Sakiyama H, Suzuki G, Hidari KI and Hirabayashi Y: 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. 1996. View Article : Google Scholar : PubMed/NCBI | |
|
Paul P, Kamisaka Y, Marks DL and Pagano RE: Purification and characterization of UDP-glucose: Ceramide glucosyltransferase from rat liver Golgi membranes. J Biol Chem. 271:2287–2293. 1996. View Article : Google Scholar : PubMed/NCBI | |
|
Basu S, Kaufman B and Roseman S: Enzymatic synthesis of ceramide-glucose and ceramide-lactose by glycosyltransferases from embryonic chicken brain. J Biol Chem. 243:5802–5804. 1968.PubMed/NCBI | |
|
Nomura T, Takizawa M, Aoki J, Arai H, Inoue K, Wakisaka E, Yoshizuka N, Imokawa G, Dohmae N, Takio K, et al: Purification, cDNA cloning, and expression of UDP-Gal: Glucosylceramide beta-1,4-galactosyltransferase from rat brain. J Biol Chem. 273:13570–13577. 1998. View Article : Google Scholar : PubMed/NCBI | |
|
Sundaram KS and Lev M: Purification and activation of brain sulfotransferase. J Biol Chem. 267:24041–24044. 1992.PubMed/NCBI | |
|
Huwiler A, Kolter T, Pfeilschifter J and Sandhoff K: Physiology and pathophysiology of sphingolipid metabolism and signaling. Biochim Biophys Acta. 1485:63–99. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Kolter T, Proia RL and Sandhoff K: Combinatorial ganglioside biosynthesis. J Biol Chem. 277:25859–25862. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Martin GR: 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. 1981. View Article : Google Scholar : PubMed/NCBI | |
|
Kimber SJ, Brown DG, Pahlsson P and Nilsson B: Carbohydrate antigen expression in murine embryonic stem cells and embryos. II. Sialylated antigens and glycolipid analysis. Histochem J. 25:628–641. 1993. View Article : Google Scholar : PubMed/NCBI | |
|
Ryu JS, Chang KT, Lee JT, Lim MU, Min HK, Na YJ, Lee SB, Moussavou G, Kim SU, Kim JS, et al: Ganglioside GM1 influences the proliferation rate of mouse induced pluripotent stem cells. BMB Rep. 45:713–718. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Yamashita T, Wada R, Sasaki T, Deng C, Bierfreund U, Sandhoff K and Proia RL: A vital role for glycosphingolipid synthesis during development and differentiation. Proc Natl Acad Sci USA. 96:9142–9147. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Jung JU, Ko K, Lee DH, Ko K, Chang KT and Choo YK: The roles of glycosphingolipids in the proliferation and neural differentiation of mouse embryonic stem cells. Exp Mol Med. 41:935–345. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Kwak DH, Yu K, Kim SM, Lee DH, Kim SM, Jung JU, Seo JW, Kim N, Lee S, Jung KY, et al: Dynamic changes of gangliosides expression during the differentiation of embryonic and mesenchymal stem cells into neural cells. Exp Mol Med. 38:668–676. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Lee DH, Koo DB, Ko K, Ko K, Kim SM, Jung JU, Ryu JS, Jin JW, Yang HJ, Do SI, et al: Effects of daunorubicin on ganglioside expression and neuronal differentiation of mouse embryonic stem cells. Biochem Biophys Res Commun. 362:313–318. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Azevedo-Pereira RL, Morrot A, Machado GS, Paredes BD, Dde C Rodrigues, de Carvalho AC and Mendez-Otero R: Expression of ganglioside 9-O acetyl GD3 in undifferentiated embryonic stem cells. Cell Biol Int. 39:121–127. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Cheresh DA, Pierschbacher MD, Herzig MA and Mujoo K: Disialogangliosides GD2 and GD3 are involved in the attachment of human melanoma and neuroblastoma cells to extracellular matrix proteins. J Cell Biol. 102:688–696. 1986. View Article : Google Scholar : PubMed/NCBI | |
|
Kwak DH, Rho YI, Kwon OD, Ahan SH, Song JH, Choo YK, Kim SJ, Choi BK and Jung KY: Decreases of ganglioside GM3 in streptozotocin-induced diabetic glomeruli of rats. Life Sci. 72:1997–2006. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Duan JG, Xiang T, Chen H and Liu M: Role of extrinsic ganglioside GM1 in proliferation and differentiation of neural stem cells. Sichuan Da Xue Xue Bao Yi Xue Ban. 38:260–263. 2007.(In Chinese). PubMed/NCBI | |
|
Gouni-Berthold I, Seul C, Ko Y, Hescheler J and Sachinidis A: Gangliosides GM1 and GM2 induce vascular smooth muscle cell proliferation via extracellular signal-regulated kinase 1/2 pathway. Hypertension. 38:1030–1037. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Nishio M, Tajima O and Furukawa K, Urano T and Furukawa K: Over-expression of GM1 enhances cell proliferation with epidermal growth factor without affecting the receptor localization in the microdomain in PC12 cells. Int J Oncol. 26:191–199. 2005.PubMed/NCBI | |
|
Lee SW, Lee HJ, Hwang HS and Ko K, Han DW and Ko K: Optimization of Matrigel-based culture for expansion of neural stem cells. Anim Cells Syst. 19:175–180. 2015. View Article : Google Scholar | |
|
Itokazu Y, Kato-Negishi M, Nakatani Y, Ariga T and Yu RK: Effects of amyloid β-peptides and gangliosides on mouse neural stem cells. Neurochem Res. 38:2019–2027. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Klassen H, Schwartz MR, Bailey AH and Young MJ: Surface markers expressed by multipotent human and mouse neural progenitor cells include tetraspanins and non-protein epitopes. Neurosci Lett. 312:180–182. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Nakatani Y, Yanagisawa M, Suzuki Y and Yu RK: Characterization of GD3 ganglioside as a novel biomarker of mouse neural stem cells. Glycobiology. 20:78–86. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Wang J, Cheng A, Wakade C and Yu RK: Ganglioside GD3 is required for neurogenesis and long-term maintenance of neural stem cells in the postnatal mouse brain. J Neurosci. 34:13790–13800. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Wang J and Yu RK: Interaction of ganglioside GD3 with an EGF receptor sustains the self-renewal ability of mouse neural stem cells in vitro. Proc Natl Acad Sci USA. 110:19137–19142. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Irvine RA and Seyfried TN: Phylogenetic conservation of ganglioside GD3 expression during early vertebrate ontogeny. Comp Biochem Physiol B Biochem Mol Biol. 109:603–612. 1994. View Article : Google Scholar : PubMed/NCBI | |
|
Seyfried TN and Yu RK: Ganglioside GD3: Structure, cellular distribution, and possible function. Mol Cell Biochem. 68:3–10. 1985.PubMed/NCBI | |
|
Yanagisawa M, Nakamura K and Taga T: Roles of lipid rafts in integrin-dependent adhesion and gp130 signalling pathway in mouse embryonic neural precursor cells. Genes Cells. 9:801–809. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Doetsch F, Caillé I, Lim DA, Garcia-Verdugo JM and Alvarez-Buylla A: Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell. 97:703–716. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Goldman JE, Hirano M, Yu RK and Seyfried TN: GD3 ganglioside is a glycolipid characteristic of immature neuroectodermal cells. J Neuroimmunol. 7:179–192. 1984. View Article : Google Scholar : PubMed/NCBI | |
|
Cammer W and Zhang H: Ganglioside GD3 in radial glia and astrocytes in situ in brains of young and adult mice. J Neurosci Res. 46:18–23. 1996. View Article : Google Scholar : PubMed/NCBI | |
|
Ngamukote S, Yanagisawa M, Ariga T, Ando S and Yu RK: Developmental changes of glycosphingolipids and expression of glycogenes in mouse brains. J Neurochem. 103:2327–2341. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Liu Y, Li R and Ladisch S: Exogenous ganglioside GD1a enhances epidermal growth factor receptor binding and dimerization. J Biol Chem. 279:36481–36489. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Yanagisawa M, Nakamura K and Taga T: Glycosphingolipid synthesis inhibitor represses cytokine-induced activation of the Ras-MAPK pathway in embryonic neural precursor cells. J Biochem. 138:285–291. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Bouvier JD and Seyfried TN: Ganglioside composition of normal and mutant mouse embryos. J Neurochem. 52:460–466. 1989. View Article : Google Scholar : PubMed/NCBI | |
|
Yu RK: Development regulation of ganglioside metabolism. Prog Brain Res. 101:31–44. 1994. View Article : Google Scholar : PubMed/NCBI | |
|
Yu RK, Macala LJ, Taki T, Weinfield HM and Yu FS: Developmental changes in ganglioside composition and synthesis in embryonic rat brain. J Neurochem. 50:1825–1829. 1988. View Article : Google Scholar : PubMed/NCBI | |
|
Yanagisawa M and Yu RK: The expression and functions of glycoconjugates in neural stem cells. Glycobiology. 17:57R–74R. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Yanagisawa M, Taga T, Nakamura K, Ariga T and Yu RK: Characterization of glycoconjugate antigens in mouse embryonic neural precursor cells. J Neurochem. 95:1311–1320. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Moussavou G, Kwak DH, Lim MU, Kim JS, Kim SU, Chang KT and Choo YK: Role of gangliosides in the differentiation of human mesenchymal-derived stem cells into osteoblasts and neuronal cells. BMB Rep. 46:527–532. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Lee SH, Kwak DH, Ryu JS, Lim MU, Kim JS, Chang KT and Choo YK: Differential expression pattern of gangliosides during the differentiation of human dental pulp-derived mesenchymal stem cells into dopaminergic neural-like cells. Anim Cells Syst. 18:210–216. 2014. View Article : Google Scholar | |
|
Ryu JS, Ko K, Lee JW, Park SB, Byun SJ, Jeong EJ, Ko K and Choo YK: Gangliosides are involved in neural differentiation of human dental pulp-derived stem cells. Biochem Biophys Res Commun. 387:266–271. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Kwak DH, Jin JW, Ryu JS, Ko K, Lee SD, Lee JW, Kim JS, Jung KY, Ko K, Ma JY, et al: Regulatory roles of ganglioside GQ1b in neuronal cell differentiation of mouse embryonic stem cells. BMB Rep. 44:799–804. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Vinson M, Strijbos PJ, Rowles A, Facci L, Moore SE, Simmons DL and Walsh FS: Myelin-associated glycoprotein interacts with ganglioside GT1b. A mechanism for neurite outgrowth inhibition. J Biol Chem. 276:20280–20285. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Osanai T, Kotani M, Yuen CT, Kato H, Sanai Y and Takeda S: Immunohistochemical and biochemical analyses of GD3, GT1b, and GQ1b gangliosides during neural differentiation of P19 EC cells. FEBS Lett. 537:73–78. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Tsuji S, Arita M and Nagai Y: GQ1b, a bioactive ganglioside that exhibits novel nerve growth factor (NGF)-like activities in the two neuroblastoma cell lines. J Biochem. 94:303–306. 1983. View Article : Google Scholar : PubMed/NCBI |
