Lewis X-carrying N-glycans regulate the proliferation of mouse embryonic neural stem cells via the notch signaling pathway

Journal of Biological Chemistry

Volumn 287, Issue 29, 2012, Pages 24356-24364

  Yagi, Hirokazu ^a   Saito, Takuya ^a   Yanagisawa, Makoto ^b   Yu, Robert K ^b   Kato, Koichi ^a,c  

^a NAGOYA CITY UNIVERSITY   (Japan)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

^c INSTITUTE FOR MOLECULAR SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DEVELOPMENT; CARBOHYDRATE EPITOPES; DIFFERENTIATED CELLS; EXPRESSION LEVELS; FUCOSYLTRANSFERASES; GLYCANS; LEWIS X; MOLECULAR MECHANISM; N-GLYCANS; N-GLYCOSYLATION; NATURAL KILLER; NEURAL CELLS; NEURAL STEM CELL; NOTCH SIGNALING PATHWAYS; SHORT INTERFERING RNA; SIGNALING PATHWAYS; UNDIFFERENTIATED CELLS;

CARBOHYDRATES; CYTOLOGY; MAINTENANCE; MAMMALS; RNA; SIGNALING; STEM CELLS;

PIGMENTS;

BLOOD GROUP ANTIGEN; CELL PROTEIN; FUCOSYLTRANSFERASE; FUCOSYLTRANSFERASE 9; GLYCAN; LEWIS X ANTIGEN; MANNOSE; MUSASHI 1; N GLYCAN; NOTCH RECEPTOR; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIGEN PRESENTATION; ARTICLE; BRAIN DEVELOPMENT; CELL DIFFERENTIATION; CELL FATE; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; GENE SILENCING; GLYCOSYLATION; GROWTH REGULATION; MOUSE; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD15; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELLS, CULTURED; EMBRYONIC STEM CELLS; GLYCOSYLATION; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; MICE; NEURAL STEM CELLS; POLYSACCHARIDES; RECEPTORS, NOTCH; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY;

EID: 84863808553     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.365643     Document Type: Article

References (52)

1. Gage, F. H. (2000) Mammalian neural stem cells. Science 287, 1433-1438
2. McKay, R. (1997) Stem cells in the central nervous system. Science 276, 66-71
3. Temple, S., and Alvarez-Buylla, A. (1999) Stem cells in the adult mammalian central nervous system. Curr. Opin. Neurobiol. 9, 135-141 (Pubitemid 29084100)
4. Temple, S. (1989) Division and differentiation of isolated CNS blast cells in microculture. Nature 340, 471-473
5. Doetsch, F., Caillé, I., Lim, D. A., García-Verdugo, J. M., and Alvarez- Buylla, A. (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703-716 (Pubitemid 29278045)
6. Seri, B., García-Verdugo, J. M., McEwen, B. S., and Alvarez-Buylla, A. (2001) Astrocytes give rise to new neurons in the adult mammalian hippocampus. J. Neurosci. 21, 7153-7160 (Pubitemid 32846963)
7. Lendahl, U., Zimmerman, L. B., and McKay, R. D. (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60, 585-595
8. Uchida, N., Buck, D. W., He, D., Reitsma, M. J., Masek, M., Phan, T. V., Tsukamoto, A. S., Gage, F. H., and Weissman, I. L. (2000) Direct isolation of human central nervous system stem cells. Proc. Natl. Acad. Sci. U.S.A. 97, 14720-14725 (Pubitemid 32016642)
9. Zappone, M. V., Galli, R., Catena, R., Meani, N., De Biasi, S., Mattei, E., Tiveron, C., Vescovi, A. L., Lovell-Badge, R., Ottolenghi, S., and Nicolis, S. K. (2000) Sox2 regulatory sequences direct expression of a β-geo transgene to telencephalic neural stem cells and precursors of the mouse embryo, revealing regionalization of gene expression in CNS stem cells. Development 127, 2367-2382 (Pubitemid 30386576)
10. Klassen, H., Schwartz, M. R., Bailey, A. H., and Young, M. J. (2001) Surface markers expressed by multipotent human and mouse neural progenitor cells include tetraspanins and non-protein epitopes. Neurosci. Lett. 312, 180-182 (Pubitemid 32972153)
11. Capela, A., and Temple, S. (2002) LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 35, 865-875
12. Sakakibara, S., Nakamura, Y., Yoshida, T., Shibata, S., Koike, M., Takano, H., Ueda, S., Uchiyama, Y., Noda, T., and Okano, H. (2002) RNA-binding protein Musashi family. Roles for CNS stem cells and a subpopulation of ependymal cells revealed by targeted disruption and antisense ablation. Proc. Natl. Acad. Sci. U.S.A. 99, 15194-15199 (Pubitemid 35334632)
13. Imai, T., Tokunaga, A., Yoshida, T., Hashimoto, M., Mikoshiba, K., Weinmaster, G., Nakafuku, M., and Okano, H. (2001) The neural RNA-binding protein Musashi1 translationally regulates mammalian numb gene expression by interacting with its mRNA. Mol. Cell. Biol. 21, 3888-3900 (Pubitemid 32476451)
14. Okano, H., Kawahara, H., Toriya, M., Nakao, K., Shibata, S., and Imai, T. (2005) Function of RNA-binding protein Musashi-1 in stem cells. Exp. Cell Res. 306, 349-356 (Pubitemid 40732760)
15. Nakashima, K., Wiese, S., Yanagisawa, M., Arakawa, H., Kimura, N., Hisatsune, T., Yoshida, K., Kishimoto, T., Sendtner, M., and Taga, T. (1999) Developmental requirement of gp130 signaling in neuronal survival and astrocyte differentiation. J. Neurosci. 19, 5429-5434 (Pubitemid 29300208)
16. Hitoshi, S., Alexson, T., Tropepe, V., Donoviel, D., Elia, A. J., Nye, J. S., Conlon, R. A., Mak, T. W., Bernstein, A., and van der Kooy, D. (2002) Notch pathway molecules are essential for the maintenance, but not the generation, of mammalian neural stem cells. Genes Dev. 16, 846-858 (Pubitemid 34280108)
17. Campos, L. S., Leone, D. P., Relvas, J. B., Brakebusch, C., Fässler, R., Suter, U., and ffrench-Constant, C. (2004) β1 integrins activate a MAPK signaling pathway in neural stem cells that contributes to their maintenance. Development 131, 3433-3444
18. Backman, M., Machon, O., Mygland, L., van den Bout, C. J., Zhong, W., Taketo, M. M., and Krauss, S. (2005) Effects of canonical Wnt signaling on dorso-ventral specification of the mouse telencephalon. Dev. Biol. 279, 155-168 (Pubitemid 40222176)
19. Yanagisawa, M., Nakamura, K., and 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 (Pubitemid 41441960)
20. Bithell, A., and Williams, B. P. (2005) Neural stem cells and cell replacement therapy. Making the right cells. Clin. Sci. 108, 13-22 (Pubitemid 40052281)
21. de Filippis, L. (2011) Neural stem cell-mediated therapy for rare brain diseases. Perspectives in the near future for LSDs and MNDs. Histol. Histopathol. 26, 1093-1109
22. Yagi, H., Yanagisawa, M., Suzuki, Y., Nakatani, Y., Ariga, T., Kato, K., and Yu, R. K. (2010) HNK-1 epitope-carrying tenascin-C spliced variant regulates the proliferation of mouse embryonic neural stem cells. J. Biol. Chem. 285, 37293-37301
23. Yanagisawa, M., Kojima, H., Kawakami, Y., Iriko, H., Nakamura, T., Nakamura, K., Uchida, A., Murata, Y., and Tamai, Y. (1999) A monoclonal antibody against a glycolipid SEGLx from Spirometra erinaceieuropaei plerocercoid. Mol. Biochem. Parasitol. 102, 225-235 (Pubitemid 29387388)
24. Nakatani, Y., Yanagisawa, M., Suzuki, Y., and Yu, R. K. (2010) Characterization of GD3 ganglioside as a novel biomarker of mouse neural stem cells. Glycobiology 20, 78-86
25. Nakagawa, H., Kawamura, Y., Kato, K., Shimada, I., Arata, Y., and Takahashi, N. (1995) Identification of neutral and sialyl N-linked oligosaccharide structures from human serum glycoproteins using three kinds of high performance liquid chromatography. Anal. Biochem. 226, 130-138
26. Takahashi, N., and Kato, K. (2003) GALAXY (Glycoanalysis by the Three Axes of MS and Chromatography): a Web Application That Assists Structural Analyses of N-Glycans. Trends Glycosci. Glycotech. 15, 235-251 (Pubitemid 37281016)
27. Yagi, H., Takahashi, N., Yamaguchi, Y., Kimura, N., Uchimura, K., Kannagi, R., and Kato, K. (2005) Development of structural analysis of sulfated N-glycans by multidimensional high performance liquid chromatography mapping methods. Glycobiology 15, 1051-1060 (Pubitemid 41511500)
28. Yagi, H., Nakagawa, M., Takahashi, N., Kondo, S., Matsubara, M., and Kato, K. (2008) Neural complex-specific expression of xylosyl N-glycan in Ciona intestinalis. Glycobiology 18, 145-151 (Pubitemid 351168252)
29. Tanabe, K., and Ikenaka, K. (2006) In-column removal of hydrazine and N-acetylation of oligosaccharides released by hydrazinolysis. Anal. Biochem. 348, 324-326 (Pubitemid 41832539)
30. Yagi, H., Yamamoto, M., Yu, S. Y., Takahashi, N., Khoo, K. H., Lee, Y. C., and Kato, K. (2010) N-Glycosylation profiling of turtle egg yolk. Expression of galabiose structure. Carbohydr. Res. 345, 442-448
31. Yagi, H., Yasukawa, N., Yu, S. Y., Guo, C. T., Takahashi, N., Takahashi, T., Bukawa, W., Suzuki, T., Khoo, K. H., Suzuki, Y., and Kato, K. (2008) The expression of sialylated high antennary N-glycans in edible bird's nest. Carbohydr. Res. 343, 1373-1377
32. Kanemura, Y., Mori, H., Kobayashi, S., Islam, O., Kodama, E., Yamamoto, A., Nakanishi, Y., Arita, N., Yamasaki, M., Okano, H., Hara, M., and Miyake, J. (2002) Evaluation of in vitro proliferative activity of human fetal neural stem/progenitor cells using indirect measurements of viable cells based on cellular metabolic activity. J. Neurosci. Res. 69, 869-879 (Pubitemid 34984704)
33. Yanagisawa, M., and Yu, R. K. (2009) O-Linked β-N- acetylglucosaminylation in mouse embryonic neural precursor cells. J. Neurosci. Res. 87, 3535-3545
34. Suzuki, Y., Yanagisawa, M., Yagi, H., Nakatani, Y., and Yu, R. K. (2010) Involvement of β1-integrin up-regulation in basic fibroblast growth factor- and epidermal growth factor-induced proliferation of mouse neuroepithelial cells. J. Biol. Chem. 285, 18443-18451
35. Reynolds, B. A., and Weiss, S. (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255, 1707-1710
36. Yagi, H., Yanagisawa, M., Kato, K., and Yu, R. K. (2010) Lysosome-associated membrane protein 1 is a major SSEA-1-carrier protein in mouse neural stem cells. Glycobiology 20, 976-981
37. Moriguchi, K., Takemoto, T., Aoki, T., Nakakita, S., Natsuka, S., and Hase, S. (2007) Free oligosaccharides with Lewis x structure expressed in the segmentation period of zebrafish embryo. J. Biochem. 142, 213-227 (Pubitemid 350044700)
38. Yanagisawa, M., Taga, T., Nakamura, K., Ariga, T., and Yu, R. K. (2005) Characterization of glycoconjugate antigens in mouse embryonic neural precursor cells. J. Neurochem. 95, 1311-1320 (Pubitemid 41779256)
39. Shimoda, Y., Tajima, Y., Osanai, T., Katsume, A., Kohara, M., Kudo, T., Narimatsu, H., Takashima, N., Ishii, Y., Nakamura, S., Osumi, N., and Sanai, Y. (2002) Pax6 controls the expression of Lewis x epitope in the embryonic forebrain by regulating α1,3-fucosyltransferase IX expression. J. Biol. Chem. 277, 2033-2039 (Pubitemid 34968785)
40. Sansom, S. N., Griffiths, D. S., Faedo, A., Kleinjan, D. J., Ruan, Y., Smith, J., van Heyningen, V., Rubenstein, J. L., and Livesey, F. J. (2009) The level of the transcription factor Pax6 is essential for controlling the balance between neural stem cell self-renewal and neurogenesis. PLoS Genet. 5, e1000511
41. Yanagisawa, M., Yoshimura, S., and Yu, R. K. (2011) Expression of GD2 and GD3 gangliosides in human embryonic neural stem cells. ASN Neuro. 3, pll e00054
42. Streit, A., Faissner, A., Gehrig, B., and Schachner, M. (1990) Isolation and biochemical characterization of a neural proteoglycan expressing the L5 carbohydrate epitope. J. Neurochem. 55, 1494-1506
43. Garwood, J., Schnädelbach, O., Clement, A., Schütte, K., Bach, A., and Faissner, A. (1999) DSD-1-proteoglycan is the mouse homolog of phosphacan and displays opposing effects on neurite outgrowth dependent on neuronal lineage. J. Neurosci. 19, 3888-3899 (Pubitemid 29222264)
44. x and α2,3-sialyl glycans and their receptors TAG-1, Contactin, and L1 mediate CD24-dependent neurite outgrowth. J. Neurosci. 29, 6677-6690
45. Hennen, E., Czopka, T., and Faissner, A. (2011) Structurally distinct Lewis X glycans distinguish subpopulations of neural stem/progenitor cells. J. Biol. Chem. 286, 16321-16331
46. Sarafian, V., Jadot, M., Foidart, J. M., Letesson, J. J., Van den BrÛle, F., Castronovo, V., Wattiaux, R., and Coninck, S. W. (1998) Expression of Lamp-1 and Lamp-2 and their interactions with galectin-3 in human tumor cells. Int. J. Cancer 75, 105-111 (Pubitemid 28113984)
47. Tomlinson, J., Wang, J. L., Barsky, S. H., Lee, M. C., Bischoff, J., and Nguyen, M. (2000) Human colon cancer cells express multiple glycoprotein ligands for E-selectin. Int. J. Oncol. 16, 347-353
48. Eggens, I., Fenderson, B., Toyokuni, T., Dean, B., Stroud, M., and 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 (Pubitemid 19157590)
49. Streit, A., Nolte, C., Rásony, T., and Schachner, M. (1993) Interaction of astrochondrin with extracellular matrix components and its involvement in astrocyte process formation and cerebellar granule cell migration. J. Cell Biol. 120, 799-814 (Pubitemid 23035148)
50. Berdnik, D., Török, T., González-Gaitán, M., and Knoblich, J. A. (2002) The endocytic protein α-Adaptin is required for numb-mediated asymmetric cell division in Drosophila. Dev. Cell 3, 221-231
51. Chen, J., Zacharek, A., Li, A., Cui, X., Roberts, C., Lu, M., and Chopp, M. (2008) Atorvastatin promotes presenilin-1 expression and Notch1 activity and increases neural progenitor cell proliferation after stroke. Stroke 39, 220-226
52. Zhou, Z. D., Kumari, U., Xiao, Z. C., and Tan, E. K. (2010) Notch as a molecular switch in neural stem cells. IUBMB Life 62, 618-623