Neuroepithelial cells require fucosylated glycans to guide the migration of vagus motor neuron progenitors in the developing zebrafish hindbrain

Development

Volumn 136, Issue 10, 2009, Pages 1653-1663

  Ohata, Shinya ^a   Kinoshita, Shigeharu ^a,b   Aoki, Ryo ^a,c   Tanaka, Hideomi ^a,d   Wada, Hironori ^a,e   Tsuruoka Kinoshita, Sachiko ^a   Tsuboi, Takashi ^c   Watabe, Shugo ^b   Okamoto, Hitoshi ^a  

^a RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d WASEDA UNIVERSITY   (Japan)

^e NIIGATA UNIVERSITY   (Japan)

Author keywords

Fucosylation; GMDS; Neural migration; Neuroepithelial cells; Vagus motor neurons; Zebrafish

Indexed keywords

ALPHA 1,3 FUCOSYLTRANSFERASE; ALPHA 1,6 FUCOSYLTRANSFERASE; ETHYLNITROSOUREA; FUCOSYLTRANSFERASE; GLYCAN; GREEN FLUORESCENT PROTEIN; GUANOSINE DIPHOSPHATE MANNOSE 4,6 DEHYDRATASE; HYDROLYASE; MESSENGER RNA; MUTANT PROTEIN; NOTCH RECEPTOR; PROTEIN O FUCOSYLTRANSFERASE 1; PROTEIN O FUCOSYLTRANSFERASE 2; TOWHEAD PROTEIN; UNCLASSIFIED DRUG; GDPMANNOSE 4,6-DEHYDRATASE; POLYSACCHARIDE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL MIGRATION; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; ENZYME REPRESSION; FUCOSYLATION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE LOCUS; GENE MAPPING; IMAGING; MIGRATION INHIBITION; MOLECULAR DYNAMICS; MOTONEURON; MUTATIONAL ANALYSIS; NEURAL STEM CELL; NEURAL STEM CELL TRANSPLANTATION; NEUROEPITHELIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ISOLATION; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; SPECIES COMPARISON; SUBVENTRICULAR ZONE; TRANSGENIC ANIMAL; VAGUS NERVE; WILD TYPE; ZEBRA FISH; AMINO ACID SEQUENCE; ANIMAL; ANIMAL EMBRYO; BIOSYNTHESIS; CELL MOTION; CYTOLOGY; GENETICS; MOLECULAR GENETICS; MORPHOGENESIS; MUTATION; PHYSIOLOGY; PRENATAL DEVELOPMENT; STEM CELL;

DANIO RERIO;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BODY PATTERNING; CELL MOVEMENT; EMBRYO, NONMAMMALIAN; GREEN FLUORESCENT PROTEINS; HYDRO-LYASES; MOLECULAR SEQUENCE DATA; MOTOR NEURONS; MUTATION; NEUROEPITHELIAL CELLS; POLYSACCHARIDES; RHOMBENCEPHALON; STEM CELLS; VAGUS NERVE; ZEBRAFISH;

EID: 68549115664     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.033290     Document Type: Article

References (43)

1. Aizawa, H., Goto, M., Sato, T. and Okamoto, H. (2007). Temporally regulated asymmetric neurogenesis causes left-right difference in the zebrafish habenular structures. Dev. Cell 12, 87-98.
2. Ando, H., Kobayashi, M., Tsubokawa, T., Uyemura, K., Furuta, T. and Okamoto, H. (2005). Lhx2 mediates the activity of Six3 in zebrafish forebrain growth. Dev. Biol. 287, 456-468.
3. Becker, D. J. and Lowe, J. B. (2003). Fucose: biosynthesis and biological function in mammals. Glycobiology 13, 41R-53R.
4. Botella-Lopez, A., Burgaya, F., Gavin, R., Garcia-Ayllon, M. S., Gomez-Tortosa, E., Pena-Casanova, J., Urena, J. M., Del Rio, J. A., Blesa, R., Soriano, E. et al. (2006). Reelin expression and glycosylation patterns are altered in Alzheimer's disease. Proc. Natl. Acad. Sci. USA 103, 5573-5578.
5. Cheng, Y. C., Amoyel, M., Qiu, X., Jiang, Y. J., Xu, Q. and Wilkinson, D. G. (2004). Notch activation regulates the segregation and differentiation of rhombomere boundary cells in the zebrafish hindbrain. Dev. Cell 6, 539-550.
6. Freeze, H. H. (2001). Update and perspectives on congenital disorders of glycosylation. Glycobiology 11, 129R-143R.
7. Gilland, E. and Baker, R. (2005). Evolutionary patterns of cranial nerve efferent nuclei in vertebrates. Brain Behav. Evol. 66, 234-254.
8. Gressens, P. (2006). Pathogenesis of migration disorders. Curr. Opin. Neurol. 19, 135-140.
9. Higashijima, S., Hotta, Y. and Okamoto, H. (2000). Visualization of cranial motor neurons in live transgenic zebrafish expressing green fluorescent protein under the control of the islet-1 promoter/enhancer. J. Neurosci. 20, 206-218.
10. Inoue, A., Takahashi, M., Hatta, K., Hotta, Y. and Okamoto, H. (1994). Developmental regulation of islet-1 mRNA expression during neuronal differentiation in embryonic zebrafish. Dev. Dyn. 199, 1-11.
11. Ishikawa, H. O., Higashi, S., Ayukawa, T., Sasamura, T., Kitagawa, M., Harigaya, K., Aoki, K., Ishida, N., Sanai, Y. and Matsuno, K. (2005). Notch deficiency implicated in the pathogenesis of congenital disorder of glycosylation IIc. Proc. Natl. Acad. Sci. USA 102, 18532-18537.
12. Kageyama, N., Natsuka, S. and Hase, S. (1999). Molecular cloning and characterization of two zebrafish alpha(1,3)fucosyltransferase genes developmentally regulated in embryogenesis. J. Biochem. 125, 838-845.
13. Louvi, A., Sisodia, S. S. and Grove, E. A. (2004). Presenilin 1 in migration and morphogenesis in the central nervous system. Development 131, 3093-3105.
14. Lubke, T., Marquardt, T., von Figura, K. and Korner, C. (1999). A new type of carbohydrate-deficient glycoprotein syndrome due to a decreased import of GDP-fucose into the golgi. J. Biol. Chem. 274, 25986-25989.
15. Lubke, T., Marquardt, T., Etzioni, A., Hartmann, E., von Figura, K. and Korner, C. (2001). Complementation cloning identifies CDG-IIc, a new type of congenital disorders of glycosylation, as a GDP-fucose transporter deficiency. Nat. Genet. 28, 73-76.
16. Luhn, K., Wild, M. K., Eckhardt, M., Gerardy-Schahn, R. and Vestweber, D. (2001). The gene defective in leukocyte adhesion deficiency II encodes a putative GDP-fucose transporter. Nat. Genet. 28, 69-72.
17. Ma, B., Simala-Grant, J. L. and Taylor, D. E. (2006). Fucosylation in prokaryotes and eukaryotes. Glycobiology 16, 158R-184R.
18. Macchi, V., Snenghi, R., De Caro, R. and Parenti, A. (2002). Monolateral hypoplasia of the motor vagal nuclei in a case of sudden infant death syndrome. J. Anat. 200, 195-198.
19. Metcalfe, W. K., Myers, P. Z., Trevarrow, B., Bass, M. B. and Kimmel, C. B. (1990). Primary neurons that express the L2/HNK-1 carbohydrate during early development in the zebrafish. Development 110, 491-504.
20. Mollicone, R., Moore, S., Bovin, N., Garcia-Rosasco, M., Candelier, J., Martinez-Duncker, I. and Oriol, R. (2008). Activity, splice variants, conserved peptide motifs and phylogeny of two new alpha 1,3-fucosyltransferase families (FUT10 and FUT11). J. Biol. Chem. 284, 4723-4738.
21. Moon, R. Y., Horne, R. S. and Hauck, F. R. (2007). Sudden infant death syndrome. Lancet 370, 1578-1587.
22. Mulichak, A. M., Bonin, C. P., Reiter, W. D. and Garavito, R. M. (2002). Structure of the MUR1 GDP-mannose 4,6-dehydratase from Arabidopsis thaliana: implications for ligand binding and specificity. Biochemistry 41, 15578-15589.
23. Ohata, S., Nawa, M., Kasama, T., Yamasaki, T., Sawanobori, K., Hata, S., Nakamura, T., Asaoka, Y., Watanabe, T., Okamoto, H. et al. (2009). Hematopoiesis-dependent expression of CD44 in murine hepatic progenitor cells. Biochem. Biophys. Res. Commun. 379, 817-823.
24. 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.
25. Sasamura, T., Ishikawa, H., Sasaki, N., Higashi, S., Kanai, M., Nakao, S., Ayukawa, T., Aigaki, T., Noda, K., Miyoshi, E. et al. (2007). The O-fucosyltransferase O-fut1 is an extracellular component that is essential for the constitutive endocytic trafficking of Notch in Drosophila. Development 134, 1347-1356.
26. Sassa, T., Aizawa, H. and Okamoto, H. (2007). Visualization of two distinct classes of neurons by gad2 and zic1 promoter/enhancer elements in the dorsal hindbrain of developing zebrafish reveals neuronal connectivity related to the auditory and lateral line systems. Dev. Dyn. 236, 706-718.
27. Shepard, J., Stern, H., Pfaff, K. and Amatruda, J. (2004). Analysis of the cell cycle in zebrafish embryos. Methods Cell Biol. 76, 109-125.
28. Smith, P. L., Myers, J. T., Rogers, C. E., Zhou, L., Petryniak, B., Becker, D. J., Homeister, J. W. and Lowe, J. B. (2002). Conditional control of selectin ligand expression and global fucosylation events in mice with a targeted mutation at the FX locus. J. Cell Biol. 158, 801-815.
29. Somoza, J. R., Menon, S., Schmidt, H., Joseph-McCarthy, D., Dessen, A., Stahl, M. L., Somers, W. S. and Sullivan, F. X. (2000). Structural and kinetic analysis of Escherichia coli GDP-mannose 4,6 dehydratase provides insights into the enzyme's catalytic mechanism and regulation by GDP-fucose. Structure 8, 123-135.
30. Staudacher, E., Altmann, F., Wilson, I. B. and Marz, L. (1999). Fucose in N-glycans: from plant to man. Biochim. Biophys. Acta 1473, 216-236.
31. Sullivan, F. X., Kumar, R., Kriz, R., Stahl, M., Xu, G. Y., Rouse, J., Chang, X. J., Boodhoo, A., Potvin, B. and Cumming, D. A. (1998). Molecular cloning of human GDP-mannose 4,6-dehydratase and reconstitution of GDP-fucose biosynthesis in vitro. J. Biol. Chem. 273, 8193-8202.
32. Takke, C., Dornseifer, P. v., Weizsacker, E. and Campos-Ortega, J. A. (1999). her4, a zebrafish homologue of the Drosophila neurogenic gene E(spl), is a target of NOTCH signalling. Development 126, 1811-1821.
33. Tanaka, H., Maeda, R., Shoji, W., Wada, H., Masai, I., Shiraki, T., Kobayashi, M., Nakayama, R. and Okamoto, H. (2007). Novel mutations affecting axon guidance in zebrafish and a role for plexin signalling in the guidance of trigeminal and facial nerve axons. Development 134, 3259-3269.
34. Taylor, E. W., Jordan, D. and Coote, J. H. (1999). Central control of the cardiovascular and respiratory systems and their interactions in vertebrates. Physiol. Rev. 79, 855-916.
35. Tokumoto, M., Gong, Z., Tsubokawa, T., Hew, C. L., Uyemura, K., Hotta, Y. and Okamoto, H. (1995). Molecular heterogeneity among primary motoneurons and within myotomes revealed by the differential mRNA expression of novel islet-1 homologs in embryonic zebrafish. Dev. Biol. 171, 578-589.
36. Trevarrow, B., Marks, D. L. and Kimmel, C. B. (1990). Organization of hindbrain segments in the zebrafish embryo. Neuron 4, 669-679.
37. Varki, A., Cummings, R., Esko, J., Freeze, H., Hart, G. and Marth, J. (1999). Essential of Glycobiology. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
38. Wada, H., Iwasaki, M., Sato, T., Masai, I., Nishiwaki, Y., Tanaka, H., Sato, A., Nojima, Y. and Okamoto, H. (2005). Dual roles of zygotic and maternal Scribble1 in neural migration and convergent extension movements in zebrafish embryos. Development 132, 2273-2285.
39. Wada, H., Tanaka, H., Nakayama, S., Iwasaki, M. and Okamoto, H. (2006). Frizzled3a and Celsr2 function in the neuroepithelium to regulate migration of facial motor neurons in the developing zebrafish hindbrain. Development 133, 4749-4759.
40. Wang, X., Inoue, S., Gu, J., Miyoshi, E., Noda, K., Li, W., Mizuno-Horikawa, Y., Nakano, M., Asahi, M., Takahashi, M. et al. (2005). Dysregulation of TGF-beta1 receptor activation leads to abnormal lung development and emphysemalike phenotype in core fucose-deficient mice. Proc. Natl. Acad. Sci. USA 102, 15791-15796.
41. Wang, X., Gu, J., Ihara, H., Miyoshi, E., Honke, K. and Taniguchi, N. (2006). Core fucosylation regulates epidermal growth factor receptor-mediated intracellular signaling. J. Biol. Chem. 281, 2572-2577.
42. Webb, N. A., Mulichak, A. M., Lam, J. S., Rocchetta, H. L. and Garavito, R. M. (2004). Crystal structure of a tetrameric GDP-D-mannose 4,6-dehydratase from a bacterial GDP-D-rhamnose biosynthetic pathway. Protein Sci. 13, 529-539.
43. Westerfield, M. (2007). The Zebrafish Book. Eugene, OR: University of Oregon Press.