DOI QR코드

DOI QR Code

Roles of gangliosides in mouse embryogenesis and embryonic stem cell differentiation

  • Kwak, Dong-Hoon (Department of Biological Science, College of Natural Sciences, Biotechnology Institute, Wonkwang University) ;
  • Seo, Byoung-Boo (Department of Animal Resources, College of Life and Environmental Sciences, Daegu University) ;
  • Chang, Kyu-Tae (National Primate Research Center, Korea Research Institute of Bioscience and Biotechnology) ;
  • Choo, Young-Kug (Department of Biological Science, College of Natural Sciences, Biotechnology Institute, Wonkwang University)
  • Accepted : 2011.06.01
  • Published : 2011.07.31

Abstract

Gangliosides have been suggested to play important roles in various functions such as adhesion, cell differentiation, growth control, and signaling. Mouse follicular development, ovulation, and luteinization during the estrous cycle are regulated by several hormones and cell-cell interactions. In addition, spermatogenesis in seminiferous tubules of adult testes is also regulated by several hormones, including follicle- stimulating hormone (FSH) and luteinizing hormone (LH) and cell-cell interactions. The regulation of these processes by hormones and cell-cell interactions provides evidence for the importance of surface membrane components, including gangliosides. During preimplantation embryo development, a mammalian embryo undergoes a series of cleavage divisions whereby a zygote is converted into a blastocyst that is sufficiently competent to be implanted in the maternal uterus and continue its development. Mouse embryonic stem (mES) cells are pluripotent cells derived from mouse embryo, specifically, from the inner cell mass of blastocysts. Differentiated neuronal cells are derived from mES cells through the formation of embryonic bodies (EBs). EBs recapitulate many aspects of lineage-specific differentiation and temporal and spatial gene expression patterns during early embryogenesis. Previous studies on ganglioside expression during mouse embryonic development (including during $in$ $vitro$ fertilization, ovulation, spermatogenesis, and embryogenesis) reported that gangliosides were expressed in both undifferentiated and differentiated (or differentiating) mES cells. In this review, we summarize some of the advances in our understanding of the functional roles of gangliosides during the stages of mouse embryonic development, including ovulation, spermatogenesis, and embryogenesis, focusing on undifferentiated and differentiated mES cells (neuronal cells).

Keywords

Acknowledgement

Supported by : National Research Foundation, Ministry of Education, Science and Technology

References

  1. Bouvier JD, Seyfried TN. Ganglioside composition of normal and mutant mouse embryos. J Neurochem 1989;52:460-466 https://doi.org/10.1111/j.1471-4159.1989.tb09143.x
  2. Chen X, Xu H, Yuan P, Fang F, Huss M, Vega VB, Wong E, Orlov YL, Zhang W, Jiang J. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 2008;133:1106-1117 https://doi.org/10.1016/j.cell.2008.04.043
  3. Choo YK, Chiba K, Tai T, Ogiso M, Hoshi M. Differential distribution of gangliosides in adult rat ovary during the oestrous cycle. Glycobiology 1995;5:299-309 https://doi.org/10.1093/glycob/5.3.299
  4. Choo YK. Distribution of ganglioside GM3 in the rat ovary after gonadotropin stimulation. Mol Cells 1999;9:365-375
  5. Comiskey M, Warner CM. Spatio-temporal localization of membrane lipid rafts in mouse oocytes and cleaving preimplantation embryos. Dev Biol 2007;303:727-739 https://doi.org/10.1016/j.ydbio.2006.12.009
  6. Erickson GF. Normal ovarian function. Clin Obstet Gynecol 1978;21:31-52 https://doi.org/10.1097/00003081-197803000-00004
  7. Fawcett DW. The mammalian spermatozoon. Dev Biol 1975;44:394-436 https://doi.org/10.1016/0012-1606(75)90411-X
  8. Ferrari G, Fabris M, Gorio A. Gangliosides enhance neurite outgrowth in PC12 cells. Brain Res 1983;284:215-221
  9. Fujino Y, Ozaki K, Yamamasu S, Ito F, Matsuoka I, Hayashi E, Nakamura H, Ogita S, Sato E, Inoue M. DNA fragmentation of oocytes in aged mice. Hum Reprod 1996; 11:1480-1483 https://doi.org/10.1093/oxfordjournals.humrep.a019421
  10. Furukawa K, Tajima O, Okuda T, Tokuda N, Furukawa K. Knockout mice and glycolipids. In Comprehensive Glycoscience from Chemistry to Systems Biology, 2007, 149-57
  11. Furukawa K, Takamiya K, Okada M, Inoue M, Fukumoto S. Novel functions of complex carbohydrates elucidated by the mutant mice of glycosyltransferase genes. Biochim Biophys Acta 2001;1525:1-12 https://doi.org/10.1016/S0304-4165(00)00185-9
  12. Furukawa K. [Study on the functions of glycoprotein sugar chains in mammalian development: functions and expression of the beta 1-4 linked galactose residues]. Tanpakushitsu Kakusan Koso 1998;43:2309-2317
  13. Galway AB, Lapolt PS, Tsafriri A, Dargan CM, Boime I, Hsueh AJ. Recombinant follicle-stimulating hormone induces ovulation and tissue plasminogen activator expression in hypophysectomized rats. Endocrinology 1990;127:3023-3028 https://doi.org/10.1210/endo-127-6-3023
  14. Gooi HC, Feizi T, Kapadia A, Knowles BB, Solter D, Evans MJ. Stage-specific embryonic antigen involves alpha 1 goes to 3 fucosylated type 2 blood group chains. Nature 1981; 292:156-158 https://doi.org/10.1038/292156a0
  15. Hakomori S. Glycosphingolipids in cellular interaction, differentiation, and oncogenesis. Annu Rev Biochem 1981;50:733-764 https://doi.org/10.1146/annurev.bi.50.070181.003505
  16. Hakomori S. Bifunctional role of glycosphingolipids. Modulators for transmembrane signaling and mediators for cellular interactions. J Biol Chem 1990;265:18713-18716
  17. Hakomori S, Handa K, Iwabuchi K, Yamamura S, Prinetti A. New insights in glycosphingolipid function: "glycosignaling domain," a cell surface assembly of glycosphingolipids with signal transducer molecules, involved in cell adhesion coupled with signaling. Glycobiology 1998;8:xi-xix https://doi.org/10.1093/oxfordjournals.glycob.a018822
  18. Hattori M, Horiuchi R. Biphasic effects of exogenous ganglioside GM3 on follicle-stimulating hormone-dependent expression of luteinizing hormone receptor in cultured granulosa cells. Mol Cell Endocrinol 1992;88:47-54 https://doi.org/10.1016/0303-7207(92)90008-T
  19. Huwiler A, Kolter T, Pfeilschifter J, Sandhoff K. Physiology and pathophysiology of sphingolipid metabolism and signaling. Biochim Biophys Acta 2000;1485:63-99 https://doi.org/10.1016/S1388-1981(00)00042-1
  20. Ishii A, Ikeda T, Hitoshi S, Fujimoto I, Torii T, Sakuma K, Nakakita S, Hase S, Ikenaka K. Developmental changes in the expression of glycogenes and the content of N-glycans in the mouse cerebral cortex. Glycobiology 2007;17:261-276 https://doi.org/10.1093/glycob/cwl076
  21. Ji MY, Lee YC, Do S 2nd, Nam SY, Jung KY, Kim HM, Park LK, Choo YK. Developmental patterns of mST3GalV mRNA expression in the mouse: in situ hybridization using DIG-labeled RNA probes. Arch Pharm Res 2000;23:525-530 https://doi.org/10.1007/BF02976584
  22. Ji MY, Lee YC, Kim KS, Cho JW, Jung KY, Kim CH, Choo YK. Developmental patterns of GalBeta1,3(4)GlcNAc alpha2,3- sialyltransferase (ST3Gal III) expression in the mouse: in situ hybridization using DIG-labeled RNA probes. Arch Pharm Res 1999;22:243-248 https://doi.org/10.1007/BF02976357
  23. Jung JU, Ko K, Lee DH, Chang KT, Choo YK. The roles of glycosphingolipids in the proliferation and neural differentiation of mouse embryonic stem cells. Exp Mol Med 2009;41:935-945 https://doi.org/10.3858/emm.2009.41.12.099
  24. Jung KY, Kim BH, Hwang MR, Cho JR, Kim HM, Lee YC, Kim CH, Kim JK, Kim BJ, Choo YK. Differential distribution of ganglioside GM3 in seminiferous tubule and epididymis of adult rats. Arch Pharm Res 2001;24:360366 https://doi.org/10.1007/BF02975107
  25. Kaida K, Ariga T, Yu RK. Antiganglioside antibodies and their pathophysiological effects on Guillain-Barre syndrome and related disorders--a review. Glycobiology 2009;19:676-692 https://doi.org/10.1093/glycob/cwp027
  26. Kanai Y, Kawakami H, Takata K, Kurohmaru M, Hayashi Y, Nishida T, Hirano H. Localization of Forssman glycolipid and GM1 ganglioside intracellularly and on the surface of germ cells during fetal testicular and ovarian development of mice. Histochemistry 1990;94:561-568
  27. Kawai H, Sango K, Mullin KA, Proia RL. Embryonic stem cells with a disrupted GD3 synthase gene undergo neuronal differentiation in the absence of b-series gangliosides. J Biol Chem 1998;273:19634-19638 https://doi.org/10.1074/jbc.273.31.19634
  28. Kim BH, Jung JU, Ko K, Kim WS, Kim SM, Ryu JS, Jin JW, Yang HJ, Kim JS, Kwon HC, Nam SY, Kwak DH, Park YI, Koo DB, Choo YK. Expression of ganglioside GT1b in mouse embryos at different developmental stages after cryopreservation. Arch Pharm Res 2008a;31:88-95 https://doi.org/10.1007/s12272-008-1125-6
  29. Kim J, Chu J, Shen X, Wang J, Orkin SH. An extended transcriptional network for pluripotency of embryonic stem cells. Cell 2008b;132:1049-1061 https://doi.org/10.1016/j.cell.2008.02.039
  30. Kim SM, Kwak DH, Jung JU, Lee DH, Lee S, Jung KY, Do SI, Choo YK. Differential expression of gangliosides in the ovary and uterus of streptozotocin-induced and db/db diabetic mice. Arch Pharm Res 2006;29:666-676 https://doi.org/10.1007/BF02968251
  31. Kimber SJ, Brown DG, Pahlsson P, Nilsson B. Carbohydrate antigen expression in murine embryonic stem cells and embryos. II. Sialylated antigens and glycolipid analysis. Histochem J 1993;25:628-641 https://doi.org/10.1007/BF00157877
  32. Kittaka D, Itoh M, Kondo Y, Fukumoto S, Urano T, Tajima O, Furukawa K, Furukawa K. Impaired hypoglossal nerve regeneration in complex ganglioside-lacking mutant mice: down-regulation of neurotrophic factors and receptors as possible mechanisms. Glycobiology 2008;18:509-516 https://doi.org/10.1093/glycob/cwn032
  33. Kojima N, Kono M, Yoshida Y, Tachida Y, Nakafuku M, Tsuji S. Biosynthesis and expression of polysialic acid on the neural cell adhesion molecule is predominantly directed by ST8Sia II/STX during in vitro neuronal differentiation. J Biol Chem 1996;271:22058-22062 https://doi.org/10.1074/jbc.271.36.22058
  34. Kolter T, Proia RL, Sandhoff K. Combinatorial ganglioside biosynthesis. J Biol Chem 2002;277:25859-25862 https://doi.org/10.1074/jbc.R200001200
  35. Kotani M, Kawashima I, Ozawa H, Terashima T, Tai T. Differential distribution of major gangliosides in rat central nervous system detected by specific monoclonal antibodies. Glycobiology 1993;3:137-46 https://doi.org/10.1093/glycob/3.2.137
  36. Kwak DH, Jung KY, Lee YC, Choo YK. Expressional changes of ganglioside GM3 during ovarian maturation and early embryonic development in db/db mice. Dev Growth Differ 2003;45:95-102 https://doi.org/10.1046/j.1440-169X.2003.00678.x
  37. Kwak DH, Yu K, Kim SM, Lee DH, Jung JU, Seo JW, Kim N, Lee S, Jung KY, You HK, Kim HA, Choo YK. Dynamic changes of gangliosides expression during the differentiation of embryonic and mesenchymal stem cells into neural cells. Exp Mol Med 2006;38:668-676 https://doi.org/10.1038/emm.2006.79
  38. Leahy A, Xiong JW, Kuhnert F, Stuhlmann H. Use of developmental marker genes to define temporal and spatial patterns of differentiation during embryoid body formation. J Exp Zool 1999;284:67-81 https://doi.org/10.1002/(SICI)1097-010X(19990615)284:1<67::AID-JEZ10>3.0.CO;2-O
  39. Lee DH, Koo DB, Ko K, Kim SM, Jung JU, Ryu JS, Jin JW, Yang HJ, Do SI, Jung KY, Choo YK. Effects of daunorubicin on ganglioside expression and neuronal differentiation of mouse embryonic stem cells. Biochem Biophys Res Commun 2007;362:313-318 https://doi.org/10.1016/j.bbrc.2007.07.142
  40. Lee SY, Kim B, Yoon S, Kim YJ, Liu T, Woo JH, Chwae YJ, Joe EH, Jou I. Phophatidylinositol 4-phospate 5-kinase $\alpha$ is induced in ganglioside-stimulated brain astrocytes and contributes to inflammatory responses. Exp Mol Med 2010;42:662-673 https://doi.org/10.3858/emm.2010.42.9.066
  41. Liour SS, Yu RK. Differential effects of three inhibitors of glycosphingolipid biosynthesis on neuronal differentiation of embryonal carcinoma stem cells. Neurochem Res 2002; 27:1507-1512 https://doi.org/10.1023/A:1021652506370
  42. Liu J, Schoonjans L, Tielens S, Speleman F, Cornelissen M, De Sutter P, Dhont M, Van der Elst J. Culturing in vitro produced blastocysts in sequential media promotes ES cell derivation. Mol Reprod Dev 2006;73:1017-1021 https://doi.org/10.1002/mrd.20512
  43. Mackie AR, James PS, Ladha S, Jones R. Diffusion barriers in ram and boar sperm plasma membranes: directionality of lipid diffusion across the posterior ring. Biol Reprod 2001;64:113-119 https://doi.org/10.1095/biolreprod64.1.113
  44. 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 1981;78:7634-7638 https://doi.org/10.1073/pnas.78.12.7634
  45. Matsuzaki K, Kato K, Yanagisawa K. A beta polymerization through interaction with membrane gangliosides. Biochim Biophys Acta 2010;1801:868-877 https://doi.org/10.1016/j.bbalip.2010.01.008
  46. Munro MG. Factors affecting capacitive current diversion with a uterine resectoscope: an in vitro study. J Am Assoc Gynecol Laparosc 2003;10:450-460 https://doi.org/10.1016/S1074-3804(05)60144-2
  47. Muramatsu T, Muramatsu H. Carbohydrate antigens expressed on stem cells and early embryonic cells. Glycoconj J 2004;21:41-45 https://doi.org/10.1023/B:GLYC.0000043746.77504.28
  48. Nagai Y, Hoshi M. Sialosphingolipids of sea urchin eggs and spermatozoa showing a characteristic composition for species and gamete. Biochim Biophys Acta 1975;388: 146-151 https://doi.org/10.1016/0005-2760(75)90070-3
  49. Nakamura K, Inagaki F, Tamai Y. A novel ganglioside in dogfish brain. Occurrence of a trisialoganglioside with a sialic acid linked to N-acetylgalactosamine. J Biol Chem 1988; 263:9896-9900
  50. Ngamukote S, Yanagisawa M, Ariga T, Ando S, Yu RK. Developmental changes of glycosphingolipids and expression of glycogenes in mouse brains. J Neurochem 2007; 103:2327-2341 https://doi.org/10.1111/j.1471-4159.2007.04910.x
  51. Niwa H. How is pluripotency determined and maintained? Development 2007;134:635-646 https://doi.org/10.1242/dev.02787
  52. Nojiri H, Takaku F, Terui Y, Miura Y, Saito M. Ganglioside GM3: an acidic membrane component that increases during macrophage-like cell differentiation can induce monocytic differentiation of human myeloid and monocytoid leukemic cell lines HL-60 and U937. Proc Natl Acad Sci USA 1986; 83:782-786 https://doi.org/10.1073/pnas.83.3.782
  53. Ohmi Y, Tajima O, Ohkawa Y, Mori A, Sugiura Y, Furukawa K. Gangliosides play pivotal roles in the regulation of complement systems and in the maintenance of integrity in nerve tissues. Proc Natl Acad Sci USA 2009;106:22405-22410 https://doi.org/10.1073/pnas.0912336106
  54. Okada M, Itoh M, Haraguchi M, Okajima T, Inoue M, Oishi H, Matsuda Y, Iwamoto T, Kawano T, Fukumoto S, Miyazaki H, Furukawa K, Aizawa S. b-series ganglioside deficiency exhibits no definite changes in the neurogenesis and the sensitivity to Fas-mediated apoptosis but impairs regeneration of the lesioned hypoglossal nerve. J Biol Chem 2002;277:1633-1636 https://doi.org/10.1074/jbc.C100395200
  55. Osanai T, Watanabe Y, Sanai Y. Glycolipid sialyltransferases are enhanced during neural differentiation of mouse embryonic carcinoma cells, P19. Biochem Biophys Res Commun 1997;241:327-333 https://doi.org/10.1006/bbrc.1997.7817
  56. Osanai T, Kotani M, Yuen CT, Kato H, Sanai Y, Takeda S. Immunohistochemical and biochemical analyses of GD3, GT1b, and GQ1b gangliosides during neural differentiation of P19 EC cells. FEBS Lett 2003;537:73-78 https://doi.org/10.1016/S0014-5793(03)00083-8
  57. Proia RL. Glycosphingolipid functions: insights from engineered mouse models. Phil Trans R Soc Lond B Biol Sci 2003;358:879-883 https://doi.org/10.1098/rstb.2003.1268
  58. Rosner H. Significance of gangliosides in neuronal differentiation of neuroblastoma cells and neurite growth in tissue culture. Ann N Y Acad Sci 1998;845:200-214 https://doi.org/10.1111/j.1749-6632.1998.tb09672.x
  59. Schengrund CL. The roles of gangliosides in neural differentiation and repair: a perspective. Brain Res Bull 1990;24: 134-141
  60. Selvaraj V, Asano A, Buttke DE, McElwee JL, Nelson JL, Wolff CA, Merdiushev T, Fornes MW, Cohen AW, Lisanti MP, Rothblat GH, Kopf GS, Travis AJ. Segregation of micronscale membrane sub-domains in live murine sperm. J Cell Physiol 2006;206:636-646 https://doi.org/10.1002/jcp.20504
  61. Shadan S, James PS, Howes EA, Jones R. Cholesterol efflux alters lipid raft stability and distribution during capacitation of boar spermatozoa. Biol Reprod 2004;71:253-265 https://doi.org/10.1095/biolreprod.103.026435
  62. Simons K, Toomre D. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 2000;1:31-39 https://doi.org/10.1038/35036052
  63. 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. Infantile-onset symptomatic epilepsy syndrome caused by a homozygous loss-of-function mutation of GM3 synthase. Nat Genet 2004;36:1225-1229 https://doi.org/10.1038/ng1460
  64. Smith AG. Embryo-derived stem cells: Of mice and men. Annu Rev Cell Dev Biol 2001;17:435-462 https://doi.org/10.1146/annurev.cellbio.17.1.435
  65. Sridharan R, Tchieu J, Mason MJ, Yachechko R, Kuoy E, Horvath S, Zhou Q, Plath K. Role of the murine reprogramming factors in the induction of pluripotency. Cell 2009;136:364-377 https://doi.org/10.1016/j.cell.2009.01.001
  66. Stern CA, Braverman TR, Tiemeyer M. Molecular identification, tissue distribution and subcellularlocalization of mST3GalV/GM3 synthase. Glycobiology 2000;10:365-374 https://doi.org/10.1093/glycob/10.4.365
  67. Svennerholm L. Ganglioside designation. Adv Exp Med Biol 1980;125:11
  68. Takamiya K, Yamamoto A, Furukawa K, Yamashiro S, Shin M, Okada M, Fukumoto S, Haraguchi M, Takeda N, Fujimura K, Sakae M, Kishikawa M, Shiku H, Aizawa S. Mice with disrupted GM2/GD2 synthase gene lack complex gangliosides but exhibit only subtle defects in their nervous system. Proc Natl Acad Sci USA 1996;93:10662-10667 https://doi.org/10.1073/pnas.93.20.10662
  69. Trevino CL, Serrano CJ, Beltran C, Felix R, Darszon A. Identification of mouse trp homologs and lipid rafts from spermatogenic cells and sperm. FEBS Lett 2001;509: 119-125 https://doi.org/10.1016/S0014-5793(01)03134-9
  70. Uemura K, Sugiyama E, Taketomi T. Effects of an inhibitor of glucosylceramide synthase on glycosphingolipid synthesis and neurite outgrowth in murine neuroblastoma cell lines. J Biochem 1991;110:96-102 https://doi.org/10.1093/oxfordjournals.jbchem.a123549
  71. Vinson M, Strijbos PJ, Rowles A, Facci L, Moore SE, Simmons DL, Walsh FS. Myelin-associated glycoprotein interacts with ganglioside GT1b. A mechanism for neurite outgrowth inhibition. J Biol Chem 2001;276:20280-20285 https://doi.org/10.1074/jbc.M100345200
  72. Yamamoto HA, Mohanan PV. Ganglioside GT1B and melatonin inhibit brain mitochondrial DNA damage and seizures induced by kainic acid in mice. Brain Res 2003; 964:100-106 https://doi.org/10.1016/S0006-8993(02)04083-0
  73. Yamashita T, Wada R, Sasaki T, Deng C, Bierfreund U, Sandhoff K, Proia RL. A vital role for glycosphingolipid synthesis during development and differentiation. Proc Natl Acad Sci USA 1999;96:9142-9147 https://doi.org/10.1073/pnas.96.16.9142
  74. Yanagisawa M, Yu RK. The expression and functions of glycoconjugates in neural stem cells. Glycobiology 2007;17:57R-74R https://doi.org/10.1093/glycob/cwm018
  75. Yu RK, Bieberich E, Xia T, Zeng G. Regulation of ganglioside biosynthesis in the nervous system. J Lipid Res 2004;45: 783-793 https://doi.org/10.1194/jlr.R300020-JLR200
  76. Yu RK, Macala LJ, Taki T, Weinfield HM, Yu FS. Developmental changes in ganglioside composition and synthesis in embryonic rat brain. J Neurochem 1988;50:1825-1829 https://doi.org/10.1111/j.1471-4159.1988.tb02484.x
  77. Yu RK, Yanagisawa M. Glycosignaling in neural stem cells: involvement of glycoconjugates in signal transduction modulating the neural stem cell fate. J Neurochem 2007;103 Suppl 1:39-46 https://doi.org/10.1111/j.1471-4159.2007.04710.x

Cited by

  1. Relationship between ganglioside expression and anti-cancer effects of the monoclonal antibody against epithelial cell adhesion molecule in colon cancer vol.43, pp.12, 2011, https://doi.org/10.3858/emm.2011.43.12.080
  2. Regulatory roles of ganglioside GQ1b in neuronal cell differentiation of mouse embryonic stem cells vol.44, pp.12, 2011, https://doi.org/10.5483/bmbrep.2011.44.12.799
  3. Ganglioside Biochemistry vol.2012, pp.None, 2011, https://doi.org/10.5402/2012/506160
  4. Scientific literature on monosialoganglioside in the Science Citation Index-Expanded : A bibliometric analysis of articles from 1942 to 2011 by each decade vol.7, pp.1, 2011, https://doi.org/10.3969/j.issn.1673-5374.2012.01.012
  5. Impaired Neural Differentiation of Induced Pluripotent Stem Cells Generated from a Mouse Model of Sandhoff Disease vol.8, pp.1, 2011, https://doi.org/10.1371/journal.pone.0055856
  6. Isolation and Characterization of 2 New Human Rotator Cuff and Long Head of Biceps Tendon Cells Possessing Stem Cell–Like Self-Renewal and Multipotential Differentiation Capacity vol.41, pp.7, 2011, https://doi.org/10.1177/0363546512473572
  7. Plant-derived mAbs have effective anti-cancer activities by increasing ganglioside expression in colon cancers vol.35, pp.12, 2011, https://doi.org/10.1007/s10529-013-1318-z
  8. Role of gangliosides in the differentiation of human mesenchymal-derived stem cells into osteoblasts and neuronal cells vol.46, pp.11, 2013, https://doi.org/10.5483/bmbrep.2013.46.11.179
  9. Expression of ganglioside 9-O acetyl GD3 in undifferentiated embryonic stem cells : 9-O-acetyl GD3 in mouse embryonic stem cells vol.39, pp.1, 2011, https://doi.org/10.1002/cbin.10335
  10. Effect of ganglioside GT1b on the in vitro maturation of porcine oocytes and embryonic development vol.61, pp.6, 2011, https://doi.org/10.1262/jrd.2015-049
  11. Role of lipid rafts in neuronal differentiation of dental pulp-derived stem cells vol.339, pp.2, 2011, https://doi.org/10.1016/j.yexcr.2015.11.012
  12. Changes of Ganglioside GM3 Expression in Porcine Oocyte Maturation and Early Embryonic Development In Vitro vol.30, pp.4, 2015, https://doi.org/10.12750/jet.2015.30.4.319
  13. Alterations of Glycosphingolipids in Embryonic Stem Cell Differentiation and Development of Glycan-Targeting Cancer Immunotherapy vol.25, pp.20, 2011, https://doi.org/10.1089/scd.2016.0138
  14. Ganglioside as a Therapy Target in Various Types of Cancer vol.17, pp.4, 2011, https://doi.org/10.7314/apjcp.2016.17.4.1643
  15. Ganglioside GD1a promotes oocyte maturation, furthers preimplantation development, and increases blastocyst quality in pigs vol.62, pp.3, 2011, https://doi.org/10.1262/jrd.2015-083
  16. Follicular fluid lipidomics reveals lipid alterations by LH addition during IVF cycles vol.13, pp.6, 2017, https://doi.org/10.1007/s11306-017-1207-x
  17. Ganglioside GD1a Activates the Phosphorylation of EGFR in Porcine Oocytes Maturation in vitro vol.32, pp.1, 2011, https://doi.org/10.12750/jet.2017.32.1.17
  18. Ganglioside GD1a Activates the Phosphorylation of EGFR in Porcine Oocytes Maturation in vitro vol.32, pp.1, 2011, https://doi.org/10.12750/jet.2017.32.1.17
  19. Ganglioside GM3 induces cumulus cell apoptosis through inhibition of epidermal growth factor receptor‐mediated PI3K/AKT signaling pathways during in vitro maturation of pig oocytes vol.84, pp.8, 2011, https://doi.org/10.1002/mrd.22848
  20. Reversible Effects of Exogenous GM3 on Meiotic Maturation and Cumulus Cells Expansion of Porcine Cumulus-oocyte Complexes vol.33, pp.4, 2011, https://doi.org/10.12750/jet.2018.33.4.287
  21. Exogenous Ganglioside GT1b Enhances Porcine Oocyte Maturation, Including the Cumulus Cell Expansion and Activation of EGFR and ERK1/2 Signaling vol.27, pp.1, 2011, https://doi.org/10.1007/s43032-019-00004-9
  22. S1P-lyase deficiency uncouples ganglioside formation – Potential contribution to tumorigenic capacity vol.1865, pp.8, 2011, https://doi.org/10.1016/j.bbalip.2020.158708
  23. The Structural Role of Gangliosides: Insights from X-ray Scattering on Model Membranes vol.27, pp.38, 2011, https://doi.org/10.2174/0929867327666200103093340
  24. Anti-oxidative effects of exogenous ganglioside GD1a and GT1b on embryonic developmental competence in pigs vol.35, pp.4, 2011, https://doi.org/10.12750/jarb.35.4.347
  25. Inhibition of Ganglioside Synthesis Suppressed Liver Cancer Cell Proliferation through Targeting Kinetochore Metaphase Signaling vol.11, pp.3, 2011, https://doi.org/10.3390/metabo11030167
  26. Genome‐wide selective detection of Mile red‐bone goat using next‐generation sequencing technology vol.11, pp.21, 2011, https://doi.org/10.1002/ece3.8165