The lewis X-relatedα1,3-fucosyltransferase, Fut10, is required for the maintenance of stem cell populations

Journal of Biological Chemistry

Volumn 288, Issue 40, 2013, Pages 28859-28868

  Kumar, Akhilesh ^a   Torii, Tomohiro ^a   Ishino, Yugo ^a   Muraoka, Daisuke ^a   Yoshimura, Takeshi ^a   Togayachi, Akira ^b   Narimatsu, Hisashi ^b   Ikenaka, Kazuhiro ^a   Hitoshi, Seiji ^a,c  

^a GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^b NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^c SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL FUNCTIONS; CELL POPULATIONS; LEWIS X; NEURAL DEVELOPMENT;

CELL CULTURE; CELL PROLIFERATION; MAINTENANCE;

STEM CELLS;

ALPHA 1,3 FUCOSYLTRANSFERASE; CARBOHYDRATE ANTIGEN; GLYCAN DERIVATIVE; LEWIS X; MICRORNA; N GLYCAN DERIVATIVE; PROTEIN FUT10; UNCLASSIFIED DRUG;

ALPHA 1,3 FUCOSYLTRANSFERASE GENE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN VENTRICLE; CARBOHYDRATE SYNTHESIS; CELL COUNT; CELL FUNCTION; CELL MIGRATION; CELL POPULATION; CELL RENEWAL; CONTROLLED STUDY; ELECTROPORATION; EMBRYO; EMBRYONIC STEM CELL; ENZYME ACTIVITY; ENZYME DEFICIENCY; ENZYME SPECIFICITY; FUT10 GENE; GENE EXPRESSION REGULATION; GENE LOCATION; GENE OVEREXPRESSION; GENE SILENCING; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION;

BISECTING N-GLYCANS; EMBRYONIC STEM CELL; GLYCOBIOLOGY; GLYCOSYLTRANSFERASES; HPLC; NEURAL STEM CELL; STEMNESS;

ANIMALS; ANTIGENS, CD15; CELL COUNT; CELL DIFFERENTIATION; CELL MOVEMENT; CERCOPITHECUS AETHIOPS; CEREBRAL CORTEX; COS CELLS; EMBRYO, MAMMALIAN; EMBRYONIC STEM CELLS; FUCOSYLTRANSFERASES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE KNOCKDOWN TECHNIQUES; MICE; MICE, INBRED C57BL; MICRORNAS; NEURAL STEM CELLS; POLYSACCHARIDES;

EID: 84885124797     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.469403     Document Type: Article

References (31)

1. Solter, D., and Knowles, B. B. (1978) Monoclonal antibody defining a stage-specific mouse embryonic antigen (SSEA-1). Proc. Natl. Acad. Sci. U.S.A. 75, 5565-5569
2. Bird, J. M., and Kimber, S. J. (1984) Oligosaccharides containing fucose linked(1-3) and(1-4) to N-acetylglucosamine cause decompaction of mouse morulae. Dev. Biol. 104, 449-460
3. Muramatsu, T. (1988) Alterations of cell-surface carbohydrates during differentiation and development. Biochimie 70, 1587-1596
4. Toumadje, A., Kusumoto, K., Parton, A., Mericko, P., Dowell, L., Ma, G., Chen, L., Barnes, D. W., and Sato, J. D. (2003) Pluripotent differentiation in vitro of murine ES-D3 embryonic stem cells. In Vitro Cell Dev. Biol. Anim. 39, 449-453
5. Yamamoto, M., Boyer, A. M., and Schwarting, G. A. (1985) Fucose-containing glycolipids are stage-and region-specific antigens in developing embryonic brain of rodents. Proc. Natl. Acad. Sci. U.S.A. 82, 3045-3049
6. Allendoerfer, K. L., Magnani, J. L., and Patterson, P. H. (1995) FORSE-1, an antibody that labels regionally restricted subpopulations of progenitor cells in the embryonic central nervous system, recognizes the LeX carbohydrate on a proteoglycan and two glycolipid antigens. Mol. Cell Neurosci. 6, 381-395
7. Capela, A., and Temple, S. (2006) LeX is expressed by the principle progenitor cells in the embryonic nervous system, is secreted into their environment and binds Wnt-1. Dev. Biol. 291, 300-313
8. 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
9. Gooi, H. C., Feizi, T., Kapadia, A., Knowles, B. B., Solter, D., and Evans, M. J. (1981) Stage-specific embryonic antigen involves 1-3 fucosylated type 2 blood group chains. Nature 292, 156-158
10. Nishihara, S., Iwasaki, H., Nakajima, K., Togayachi, A., Ikehara, Y., Kudo, T., Kushi, Y., Furuya, A., Shitara, K., and Narimatsu, H. (2003) 1,3-Fucosyltransferase IX (Fut9) determines Lewis X expression in brain. Glycobiology 13, 445-455
11. Kudo, T., Kaneko, M., Iwasaki, H., Togayachi, A., Nishihara, S., Abe, K., and Narimatsu, H. (2004) Normal embryonic and germ cell development in mice lacking 1,3-fucosyltransferase IX (Fut9) which show disappearance of stage specific embryonic antigen 1. Mol. Cell Biol. 24, 4221-4228
12. Kudo, T., Fujii, T., Ikegami, S., Inokuchi, K., Takayama, Y., Ikehara, Y., Nishihara, S., Togayachi, A., Takahashi, S., Tachibana, K., Yuasa, S., and Narimatsu, H. (2007) Mice lacking 1,3-fucosyltransferase IX demonstrate disappearance of Lewis x structure in brain and increased anxietylike behaviors. Glycobiology 17, 1-9
13. Roos, C., Kolmer, M., Mattila, P., and Renkonen, R. (2002) Composition of Drosophila melanogaster proteome involved in fucosylated glycan metabolism. J. Biol. Chem. 277, 3168-3175
14. Baboval, T., and Smith, F. I. (2002) Comparison of human and mouse Fuc-TX and Fuc-TXI genes, and expression studies in the mouse. Mamm. Genome 13, 538-541
15. Patnaik, S. K. (2007) Characterization of Fut10 and Fut11, putative1-3/4 fucosyltransferase genes important for vertebrate development. Nature Precedings http://precedings.nature.com/documents/141/version/1
16. Mollicone, R., Moore, S. E., Bovin, N., Garcia-Rosasco, M., Candelier, J. J., Martinez-Duncker, I., and Oriol, R. (2009) Activity, splice variants, conserved peptide motifs, and phylogeny of two new 1,3-fucosyltransferase families (FUT10 and FUT11). J. Biol. Chem. 284, 4723-4738
17. 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
18. Hitoshi, S., Kippin, T., and van der Kooy, D. (2011) in Neurogenesis in the Adult Brain II: Clinical Implications (Seki, T., Sawamoto, K., Parent, J. M., and Alvarez-Buylla, A., eds) pp. 189-207, Springer, New York
19. Nagy, A., Rossant, J., Nagy, R., Abramow-Newerly, W., and Roder, J. C. (1993) Derivation of completely cell culture-derived mice from earlypassage embryonic stem cells. Proc. Natl. Acad. Sci. U.S.A. 90, 8424-8428
20. 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
21. Naruse, M., Nakahira, E., Miyata, T., Hitoshi, S., Ikenaka, K., and Bansal, R. (2006) Induction of oligodendrocyte progenitors in dorsal forebrain by intraventricular microinjection of FGF-2. Dev. Biol. 297, 262-273
22. Tanabe, K., and Ikenaka, K. (2006) In-column removal of hydrazine and N-acetylation of oligosaccharides released by hydrazinolysis. Anal. Biochem. 348, 324-326
23. Yoshimura, T., Yamada, G., Narumi, M., Koike, T., Ishii, A., Sela, I., Mitrani-Rosenbaum, S., and Ikenaka, K. (2012) Detection of N-glycans on small amounts of glycoproteins in tissue samples and sodium dodecyl sulfate-polyacrylamide gels. Anal. Biochem. 423, 253-260
24. Yan, L., Wilkins, P. P., Alvarez-Manilla, G., Do, S. I., Smith, D. F., and Cummings, R. D. (1997) Immobilized Lotus tetragonolobus agglutinin binds oligosaccharides containing the Le(x) determinant. Glycoconj. J. 14, 45-55
25. Nishihara, S., Iwasaki, H., Kaneko, M., Tawada, A., Ito, M., and Narimatsu, H. (1999) 1,3-Fucosyltransferase 9 (FUT9; Fuc-TIX) preferentially fucosylates the distal GlcNAc residue of polylactosamine chain while the other four 1,3FUT members preferentially fucosylate the inner GlcNAc residue. FEBS Lett. 462, 289-294
26. Kudo, T., Iwai, T., Kubota, T., Iwasaki, H., Takayma, Y., Hiruma, T., Inaba, N., Zhang, Y., Gotoh, M., Togayachi, A., and Narimatsu, H. (2002) Molecular cloning and characterization of a novel UDP-Gal:GalNACδ peptide 1,3-galactosyltransferase (C1Gal-T2), an enzyme synthesizing a core 1 structure of O-glycan. J. Biol. Chem. 277, 47724-47731
27. Ju, T., and Cummings, R. D. (2002) A unique molecular chaperone Cosmc required for activity of the mammalian core 1 3-galactosyltransferase. Proc. Natl. Acad. Sci. U.S.A. 99, 16613-16618
28. Weninger, W., Ulfman, L. H., Cheng, G., Souchkova, N., Quackenbush, E. J., Lowe, J. B., and von Andrian, U. H. (2000) Specialized contributions by (1,3)-fucosyltransferase-IV and FucT-VII during leukocyte rolling in dermal microvessels. Immunity 12, 665-676
29. 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
30. Yagi, H., Saito, T., Yanagisawa, M., Yu, R. K., and Kato, K. (2012) Lewis X-carrying N-glycans regulate the proliferation of mouse embryonic neural stem cells via the Notch signaling pathway. J. Biol. Chem. 287, 24356-24364
31. Rebbaa, A., Yamamoto, H., Moskal, J. R., and Bremer, E. G. (1996) Binding of erythroagglutinating phytohemagglutinin lectin from Phaseolus vulgaris to the epidermal growth factor receptor inhibits receptor function in the human glioma cell line, U373 MG. J. Neurochem. 67, 2265-2272