Essential genes for astroglial development and axon pathfinding during zebrafish embryogenesis

Developmental Dynamics

Volumn 239, Issue 10, 2010, Pages 2603-2618

  Barresi, Michael J F ^a   Burton, Sean ^a,b   Dipietrantonio, Kristina ^a   Amsterdam, Adam ^c   Hopkins, Nancy ^c   Karlstrom, Rolf O ^b  

^a SMITH COLLEGE   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Astroglia; Axon guidance; Chiasm; Gfap; Glia; Gliogenesis; Hindbrain; Insertional mutants; Motor axon; Neurogenesis; Poc; Radial glia; Zebrafish

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; NERVE CELL ADHESION MOLECULE; TUBULIN; ZEBRAFISH PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; CELL ADHESION; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL TYPE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO DEVELOPMENT; FOREBRAIN; GENE IDENTIFICATION; GENE INSERTION; GENETIC ANALYSIS; GENETIC SCREENING; MACROGLIA; MOLECULAR INTERACTION; MOTOR NERVE; NERVE FIBER; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OPTIC CHIASM; OPTIC NERVE; PHENOTYPE; PRIORITY JOURNAL; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; TELENCEPHALON; ZEBRA FISH; ANIMAL; ASTROCYTE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PRENATAL DEVELOPMENT; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ASTROCYTES; AXONS; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 79952553190     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22393     Document Type: Article

References (145)

1. Abdelilah S, Mountcastle-Shah E, Harvey M, Solnica-Krezel L, Schier AF, Stemple DL, Malicki J, Neuhauss SC, Zwartkruis F, Stainier DY, Rangini Z, Driever W. 1996. Mutations affecting neural survival in the zebrafish Danio rerio. Development 123:217-227.
2. Agalliu D, Takada S, Agalliu I, McMahon AP, Jessell TM. 2009. Motor neurons with axial muscle projections specified by Wnt4/5 signaling. Neuron 61:708-720.
3. Akanuma T, Koshida S, Kawamura A, Kishimoto Y, Takada S. 2007. Paf1 complex homologues are required for Notchregulated transcription during somite segmentation. EMBO Rep 8:858-863.
4. Alexandre P, Reugels AM, Barker D, Blanc E, Clarke JD. 2010. Neurons derive from the more apical daughter in asymmetric divisions in the zebrafish neural tube. Nat Neurosci 13:673-679.
5. Amsterdam A, Hopkins N. 1999. Retrovirus-mediated insertional mutagenesis in zebrafish. Methods Cell Biol 60:87-98.
6. Amsterdam A, Hopkins N. 2004. Retroviral-mediated insertional mutagenesis in zebrafish. Methods Cell Biol 77:3-20.
7. Amsterdam A, Nissen RM, Sun Z, Swindell EC, Farrington S, Hopkins N. 2004. Identification of 315 genes essential for early zebrafish development. Proc Natl Acad Sci USA 101:12792-12797.
8. Barresi MJ, Hutson LD, Chien CB, Karlstrom RO. 2005. Hedgehog regulated Slit expression determines commissure and glial cell position in the zebrafish forebrain. Development 132:3643-3656.
9. Barsi JC, Rajendra R, Wu JI, Artzt K. 2005. Mind bomb1 is a ubiquitin ligase essential for mouse embryonic development and Notch signaling. Mech Dev 122:1106-1117.
10. Beischlag TV, Luis Morales J, Hollingshead BD, Perdew GH. 2008. The aryl hydrocarbon receptor complex and the control of gene expression. Crit Rev Eukaryot Gene Expr 18:207-250.
11. Bernardos RL, Lentz SI, Wolfe MS, Raymond PA. 2005. Notch-Delta signaling is required for spatial patterning and Muller glia differentiation in the zebrafish retina. Dev Biol 278:381-395.
12. Bernardos RL, Barthel LK, Meyers JR, Raymond PA. 2007. Late-stage neuronal progenitors in the retina are radial Muller glia that function as retinal stem cells. J Neurosci 27:7028-7040.
13. Bingham S, Chaudhari S, Vanderlaan G, Itoh M, Chitnis A, Chandrasekhar A. 2003. Neurogenic phenotype of mind bomb mutants leads to severe patterning defects in the zebrafish hindbrain. Dev Dyn 228:451-463.
14. Bixby JL, Zhang R. 1990. Purified N-cadherin is a potent substrate for the rapid induction of neurite outgrowth. J Cell Biol 110:1253-1260.
15. Bixby JL, Lilien J, Reichardt LF. 1988. Identification of the major proteins that promote neuronal process outgrowth on Schwann cells in vitro. J Cell Biol 107: 353-361.
16. Brand M, Heisenberg CP, Warga RM, Pelegri F, Karlstrom RO, Beuchle D, Picker A, Jiang YJ, Furutani-Seiki M, van Eeden FJ, Granato M, Haffter P, Hammerschmidt M, Kane DA, Kelsh RN, Mullins MC, Odenthal J, Nusslein-Volhard C. 1996. Mutations affecting development of the midline and general body shape during zebrafish embryogenesis. Development 123:129-142.
17. Brier S, Lemaire D, Debonis S, Forest E, Kozielski F. 2004. Identification of the protein binding region of S-trityl-L-cysteine, a new potent inhibitor of the mitotic kinesin Eg5. Biochemistry 43:13072-13082.
18. Briscoe J. 2009. Making a grade: Sonic Hedgehog signalling and the control of neural cell fate. EMBO J 28:457-465.
19. Burns CE, Galloway JL, Smith AC, Keefe MD, Cashman TJ, Paik EJ, Mayhall EA, Amsterdam AH, Zon LI. 2009. A genetic screen in zebrafish defines a hierarchical network of pathways required for hematopoietic stem cell emergence. Blood 113: 5776-5782.
20. Campbell K, Gotz M. 2002. Radial glia: multi-purpose cells for vertebrate brain development. Trends Neurosci 25:235-238.
21. Carney SA, Prasch AL, Heideman W, Peterson RE. 2006. Understanding dioxin developmental toxicity using the zebrafish model. Birth Defects Res A Clin Mol Teratol 76:7-18.
22. Chanal P, Labouesse M. 1997. A screen for genetic loci required for hypodermal cell and glial-like cell development during Caenorhabditis elegans embryogenesis. Genetics 146:207-226.
23. Chanas-Sacre G, Rogister B, Moonen G, Leprince P. 2000. Radial glia phenotype: origin, regulation, and transdifferentiation. J Neurosci Res 61:357-363.
24. Chen W, Burgess S, Hopkins N. 2001. Analysis of the zebrafish smoothened mutant reveals conserved and divergent functions of hedgehog activity. Development 128:2385-2396.
25. Chitnis AB, Kuwada JY. 1990. Axonogenesis in the brain of zebrafish embryos. J Neurosci 10:1892-1905.
26. Choe EA, Liao L, Zhou JY, Cheng D, Duong DM, Jin P, Tsai LH, Peng J. 2007. Neuronal morphogenesis is regulated by the interplay between cyclin-dependent kinase 5 and the ubiquitin ligase mind bomb 1. J Neurosci 27:9503-9512.
27. Choe SK, Hirsch N, Zhang X, Sagerstrom CG. 2008. hnf1b genes in zebrafish hindbrain development. Zebrafish 5:179-187.
28. Cochran JC, Gatial JE, 3rd, Kapoor TM, Gilbert SP. 2005. Monastrol inhibition of the mitotic kinesin Eg5. J Biol Chem 280:12658-12667.
29. Coutinho P, Parsons MJ, Thomas KA, Hirst EM, Saude L, Campos I, Williams PH, Stemple DL. 2004. Differential requirements for COPI transport during vertebrate early development. Dev Cell 7:547-558.
30. Crosnier C, Vargesson N, Gschmeissner S, Ariza-McNaughton L, Morrison A, Lewis J. 2005. Delta-Notch signalling controls commitment to a secretory fate in the zebrafish intestine. Development 132:1093-1104.
31. Culverwell J, Karlstrom RO. 2002. Making the connection: retinal axon guidance in the zebrafish. Semin Cell Dev Biol 13:497-506.
32. DeBonis S, Simorre JP, Crevel I, Lebeau L, Skoufias DA, Blangy A, Ebel C, Gans P, Cross R, Hackney DD, Wade RH, Kozielski F. 2003. Interaction of the mitotic inhibitor monastrol with human kinesin Eg5. Biochemistry 42:338-349.
33. Dutta S, Dietrich JE, Westerfield M, Varga ZM. 2008. Notch signaling regulates endocrine cell specification in the zebrafish anterior pituitary. Dev Biol 319:248-257.
34. Freese JL, Pino D, Pleasure SJ. 2010. Wnt signaling in development and disease. Neurobiol Dis 38:148-153.
35. Gaiano N, Amsterdam A, Kawakami K, Allende M, Becker T, Hopkins N. 1996. Insertional mutagenesis and rapid cloning of essential genes in zebrafish. Nature 383:829-832.
36. Goh ES, Li C, Horsburgh S, Kasai Y, Kolomietz E, Morel CF. 2010. The Roberts syndrome/SC phocomelia spectrum--a case report of an adult with review of the literature. Am JMed Genet A 152A:472-478.
37. Golling G, Amsterdam A, Sun Z, Antonelli M, Maldonado E, Chen W, Burgess S, Haldi M, Artzt K, Farrington S, Lin SY, Nissen RM, Hopkins N. 2002. Insertional mutagenesis in zebrafish rapidly identifies genes essential for early vertebrate development. Nat Genet 31:135-140.
38. Goomer RS, Holst BD, Wood IC, Jones FS, Edelman GM. 1994. Regulation in vitro of an L-CAM enhancer by homeobox genes HoxD9 and HNF-1. Proc Natl Acad Sci U S A 91:7985-7989.
39. Gordillo M, Vega H, Trainer AH, Hou F, Sakai N, Luque R, Kayserili H, Basaran S, Skovby F, Hennekam RC, Uzielli ML, Schnur RE, Manouvrier S, Chang S, Blair E, Hurst JA, Forzano F, Meins M, Simola KO, Raas-Rothschild A, Schultz RA, McDaniel LD, Ozono K, Inui K, Zou H, Jabs EW. 2008. The molecular mechanism underlying Roberts syndrome involves loss of ESCO2 acetyltransferase activity. Hum Mol Genet 17:2172-2180.
40. Gotz M. 1995. Getting there and being there in the cerebral cortex. Experientia 51: 301-316.
41. Granato M, van Eeden FJ, Schach U, Trowe T, Brand M, Furutani-Seiki M, Haffter P, Hammerschmidt M, Heisenberg CP, Jiang YJ, Kane DA, Kelsh RN, Mullins MC, Odenthal J, Nusslein-Volhard C. 1996. Genes controlling and mediating locomotion behavior of the zebrafish embryo and larva. Development 123:399-413.
42. Gross JM, Perkins BD, Amsterdam A, Egana A, Darland T, Matsui JI, Sciascia S, Hopkins N, Dowling JE. 2005. Identification of zebrafish insertional mutants with defects in visual system development and function. Genetics 170:245-261.
43. Gulati-Leekha A, Goldman D. 2006. A reporter-assisted mutagenesis screen using alpha 1-tubulin-GFP transgenic zebrafish uncovers missteps during neuronal development and axonogenesis. Dev Biol 296:29-47.
44. Haddon C, Jiang YJ, Smithers L, Lewis J. 1998. Delta-Notch signalling and the patterning of sensory cell differentiation in the zebrafish ear: evidence from themind bomb mutant. Development 125:4637-4644.
45. Hammerschmidt M, Pelegri F, Mullins MC, Kane DA, Brand M, van Eeden FJ, Furutani-Seiki M, Granato M, Haffter P, Heisenberg CP, Jiang YJ, Kelsh RN, Odenthal J, Warga RM, Nusslein-Volhard C. 1996. Mutations affecting morphogenesis during gastrulation and tail formation in the zebrafish, Danio rerio. Development 123:143-151.
46. Hegde A, Qiu NC, Qiu X, Ho SH, Tay KQ, George J, Ng FS, Govindarajan KR, Gong Z, Mathavan S, Jiang YJ. 2008. Genomewide expression analysis in zebrafish mind bomb alleles with pancreas defects of different severity identifies putative Notch responsive genes. PLoS One 3:e1479.
47. Ho RK, Kane DA. 1990. Cell-autonomous action of zebrafish spt-1 mutation in specific mesodermal precursors. Nature 348: 728-730.
48. Huang G, Elferink CJ. 2005. Multiple mechanisms are involved in Ah receptor-mediated cell cycle arrest. Mol Pharmacol 67:88-96.
49. Ito M, Nakano T, Erdodi F, Hartshorne DJ. 2004. Myosin phosphatase: structure, regulation and function. Mol Cell Biochem 259:197-209.
50. Itoh M, Kim CH, Palardy G, Oda T, Jiang YJ, Maust D, Yeo SY, Lorick K, Wright GJ, Ariza-McNaughton L, Weissman AM, Lewis J, Chandrasekharappa SC, Chitnis AB. 2003. Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta. Dev Cell 4:67-82.
51. Jackson EL, Alvarez-Buylla A. 2008. Characterization of adult neural stem cells and their relation to brain tumors. Cells Tissues Organs 188:212-224.
52. Jeong HW, Jeon US, Koo BK, Kim WY, Im SK, Shin J, Cho Y, Kim J, Kong YY. 2009. Inactivation of Notch signaling in the renal collecting duct causes nephrogenic diabetes insipidus in mice. J Clin Invest 119:3290-3300.
53. Jiang YJ, Brand M, Heisenberg CP, Beuchle D, Furutani-Seiki M, Kelsh RN, Warga RM, Granato M, Haffter P, Hammerschmidt M, Kane DA, Mullins MC, Odenthal J, van Eeden FJ, Nusslein-Volhard C. 1996. Mutations affecting neurogenesis and brain morphology in the zebrafish, Danio rerio. Development 123:205-216.
54. Kapoor TM, Mayer TU, Coughlin ML, Mitchison TJ. 2000. Probing spindle assembly mechanisms with monastrol, a small molecule inhibitor of the mitotic kinesin, Eg5. J Cell Biol 150:975-988.
55. Kaprielian Z, Runko E, Imondi R. 2001. Axon guidance at the midline choice point. Dev Dyn 221:154-181.
56. Karlstrom RO, Trowe T, Klostermann S, Baier H, Brand M, Crawford AD, Grunewald B, Haffter P, Hoffmann H, Meyer SU, Muller BK, Richter S, van Eeden FJ, Nusslein-Volhard C, Bonhoeffer F. 1996. Zebrafish mutations affecting retinotectal axon pathfinding. Development 123:427-438.
57. Karlstrom RO, Talbot WS, Schier AF. 1999. Comparative synteny cloning of zebrafish you-too: mutations in the Hedgehog target gli2 affect ventral forebrain patterning. Genes Dev 13:388-393.
58. Kettenmann H, Verkhratsky A. 2008. Neuroglia: the 150 years after. Trends Neurosci 31:653-659.
59. Kim H, Shin J, Kim S, Poling J, Park HC, Appel B. 2008. Notch-regulated oligodendrocyte specification from radial glia in the spinal cord of zebrafish embryos. Dev Dyn 237:2081-2089.
60. Klambt C, Schimmelpfeng K, Hummel T. 1999. Glia development in the embryonic CNS of Drosophila. Adv Exp Med Biol 468:23-32.
61. Klein E, DeBonis S, Thiede B, Skoufias DA, Kozielski F, Lebeau L. 2007. New chemical tools for investigating human mitotic kinesin Eg5. Bioorg Med Chem 15:6474-6488.
62. Koo BK, Lim HS, Song R, Yoon MJ, Yoon KJ, Moon JS, Kim YW, Kwon MC, Yoo KW, Kong MP, Lee J, Chitnis AB, Kim CH, Kong YY. 2005. Mind bomb 1 is essential for generating functional Notch ligands to activate Notch. Development 132:3459-3470.
63. Koo BK, Yoon MJ, Yoon KJ, Im SK, Kim YY, Kim CH, Suh PG, Jan YN, Kong YY. 2007. An obligatory role of mind bomb-1 in notch signaling of mammalian development. PLoS One 2:e1221.
64. Kosan C, Kunz J. 2002. Identification and characterisation of the gene TWIST NEIGHBOR (TWISTNB) located in the microdeletion syndrome 7p21 region. Cytogenet Genome Res 97:167-170.
65. Kriegstein A, Alvarez-Buylla A. 2009. The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32:149-184.
66. Kucenas S, Takada N, Park HC, Woodruff E, Broadie K, Appel B. 2008. CNSderived glia ensheath peripheral nerves and mediate motor root development. Nat Neurosci 11:143-151.
67. Lai K, Amsterdam A, Farrington S, Bronson RT, Hopkins N, Lees JA. 2009. Many ribosomal protein mutations are associated with growth impairment and tumor predisposition in zebrafish. Dev Dyn 238:76-85.
68. Lam CS, Marz M, Strahle U. 2009. gfap and nestin reporter lines reveal characteristics of neural progenitors in the adult zebrafish brain. Dev Dyn 238:475-486.
69. Learte AR, Hidalgo A. 2007. The role of glial cells in axon guidance, fasciculation and targeting. Adv Exp Med Biol 621:156-166.
70. Lee J, Gross JM. 2007. Laminin beta1 and gamma1 containing laminins are essential for basement membrane integrity in the zebrafish eye. Invest Ophthalmol Vis Sci 48:2483-2490.
71. Lele Z, Folchert A, Concha M, Rauch GJ, Geisler R, Rosa F, Wilson SW, Hammerschmidt M, Bally-Cuif L. 2002. parachute/n-cadherin is required for morphogenesis and maintained integrity of the zebrafish neural tube. Development 129:3281-3294.
72. Lindwall C, Fothergill T, Richards LJ. 2007. Commissure formation in the mammalian forebrain. Curr Opin Neurobiol 17:3-14.
73. Liu Y, Pathak N, Kramer-Zucker A, Drummond IA. 2007. Notch signaling controls the differentiation of transporting epithelia and multiciliated cells in the zebrafish pronephros. Development 134:1111-1122.
74. Lowery LA, Rubin J, Sive H. 2007. Whitesnake/sfpq is required for cell survival and neuronal development in the zebrafish. Dev Dyn 236:1347-1357.
75. Lunde K, Belting HG, Driever W. 2004. Zebrafish pou5f1/pou2, homolog of mammalian Oct4, functions in the endoderm specification cascade. Curr Biol 14:48-55.
76. Lowery LA, De Rienzo G, Gutzman JH, Sive H. 2009. Characterization and classification of zebrafish brain morphology mutants. Anat Rec (Hoboken) 292:94-106.
77. Malicki J, Neuhauss SC, Schier AF, Solnica-Krezel L, Stemple DL, Stainier DY, Abdelilah S, Zwartkruis F, Rangini Z, Driever W. 1996. Mutations affecting development of the zebrafish retina. Development 123:263-273.
78. Maliga Z, Mitchison TJ. 2006. Small-molecule and mutational analysis of allosteric Eg5 inhibition by monastrol. BMC Chem Biol 6:2.
79. Maliga Z, Kapoor TM, Mitchison TJ. 2002. Evidence that monastrol is an allosteric inhibitor of the mitotic kinesin Eg5. Chem Biol 9:989-996.
80. Marcus RC, Easter Jr. SS 1995. Expression of glial fibrillary acidic protein and its relation to tract formation in embryonic zebrafish (Danio rerio). J Comp Neurol 359:365-381.
81. Marlow F, Gonzalez EM, Yin C, Rojo C, Solnica-Krezel L. 2004. No tail co-operates with non-canonical Wnt signaling to regulate posterior body morphogenesis in zebrafish. Development 131:203-216.
82. Marthiens V, Gavard J, Lambert M, Mege RM. 2002. Cadherin-based cell adhesion in neuromuscular development. Biol Cell 94:315-326.
83. Masai I, Lele Z, Yamaguchi M, Komori A, Nakata A, Nishiwaki Y, Wada H, Tanaka H, Nojima Y, Hammerschmidt M, Wilson SW, Okamoto H. 2003. N-cadherin mediates retinal lamination, maintenance of forebrain compartments and patterning of retinal neurites. Development 130:2479-2494.
84. Mason CA, Sretavan DW. 1997. Glia, neurons, and axon pathfinding during optic chiasm development. Curr Opin Neurobiol 7:647-653.
85. Mayer TU, Kapoor TM, Haggarty SJ, King RW, Schreiber SL, Mitchison TJ. 1999. Small molecule inhibitor of mitotic spindle bipolarity identified in a phenotypebased screen. Science 286:971-974.
86. Miyamoto DT, Perlman ZE, Burbank KS, Groen AC, Mitchison TJ. 2004. The kinesin Eg5 drives poleward microtubule flux in Xenopus laevis egg extract spindles. J Cell Biol 167:813-818.
87. Nissen RM, Amsterdam A, Hopkins N. 2006. A zebrafish screen for craniofacial mutants identifies wdr68 as a highly conserved gene required for endothelin-1 expression. BMC Dev Biol 6:28.
88. Nona SN, Shehab SA, Stafford CA, Cronly-Dillon JR. 1989. Glial fibrillary acidic protein (GFAP) from goldfish: its localisation in visual pathway. Glia 2:189-200.
89. Odenthal J, Haffter P, Vogelsang E, Brand M, van Eeden FJ, Furutani-Seiki M, Granato M, Hammerschmidt M, Heisenberg CP, Jiang YJ, Kane DA, Kelsh RN, Mullins MC, Warga RM, Allende ML, Weinberg ES, Nusslein-Volhard C. 1996. Mutations affecting the formation of the notochord in the zebrafish, Danio rerio. Development 123:103-115.
90. Park HC, Appel B. 2003. Delta-Notch signaling regulates oligodendrocyte specification. Development 130:3747-3755.
91. Parsons MJ, Pollard SM, Saude L, Feldman B, Coutinho P, Hirst EM, Stemple DL. 2002. Zebrafish mutants identify an essential role for laminins in notochord formation. Development 129:3137-3146.
92. Paulus JD, Halloran MC. 2006. Zebrafish bashful/laminin-alpha 1 mutants exhibit multiple axon guidance defects. Dev Dyn 235:213-224.
93. Pellett S, Tracy JW. 2006. Mak16p is required for the maturation of 25S and 5.8S rRNAs in the yeast Saccharomyces cerevisiae. Yeast 23:495-506.
94. Perdew GH. 2008. Ah receptor binding to its cognate response element is required for dioxin-mediated toxicity. Toxicol Sci 106:301-303.
95. Phi JH, Park SH, Chae JH, Hong KH, Park SS, Kang JH, Jun JK, Cho BK, Wang KC, Kim SK. 2008. Congenital subependymal giant cell astrocytoma: clinical considerations and expression of radial glial cell markers in giant cells. Childs Nerv Syst 24:1499-1503.
96. Pogoda HM, Sternheim N, Lyons DA, Diamond B, Hawkins TA, Woods IG, Bhatt DH, Franzini-Armstrong C, Dominguez C, Arana N, Jacobs J, Nix R, Fetcho JR, Talbot WS. 2006. A genetic screen identifies genes essential for development of myelinated axons in zebrafish. Dev Biol 298:118-131.
97. Powell EM, Meiners S, DiProspero NA, Geller HM. 1997. Mechanisms of astrocyte-directed neurite guidance. Cell Tissue Res 290:385-393.
98. Powell EM, Geller HM. 1999. Dissection of astrocyte-mediated cues in neuronal guidance and process extension. Glia 26:73-83.
99. Ramón y Cajal S. 1911. Histology of the nervous system of man and vertebrates. Cambridge: Oxford University Press.
100. Raymond PA, Barthel LK, Bernardos RL, Perkowski JJ. 2006. Molecular characterization of retinal stem cells and their niches in adult zebrafish. BMC Dev Biol 6:36.
101. Ruiz i Altaba A, Stecca B, Sanchez P. 2004. Hedgehog--Gli signaling in brain tumors: stem cells and paradevelopmental programs in cancer. Cancer Lett 204:145-157.
102. Sadler KC, Amsterdam A, Soroka C, Boyer J, Hopkins N. 2005. A genetic screen in zebrafish identifies the mutants vps18, nf2 and foie gras as models of liver disease. Development 132:3561-3572.
103. Sanchez-Camacho C, Bovolenta P. 2009. Emerging mechanisms in morphogen- mediated axon guidance. Bioessays 31: 1013-1025.
104. Sann S, Wang Z, Brown H, Jin Y. 2009. Roles of endosomal trafficking in neurite outgrowth and guidance. Trends Cell Biol 19:317-324.
105. Sarli V, Giannis A. 2006. Inhibitors of mitotic kinesins: next-generation antimitotics. ChemMedChem 1:293-298.
106. Sarli V, Huemmer S, Sunder-Plassmann N, Mayer TU, Giannis A. 2005. Synthesis and biological evaluation of novel EG5 inhibitors. Chembiochem 6:2005-2013.
107. Sawin KE, Mitchison TJ. 1995. Mutations in the kinesin-like protein Eg5 disrupting localization to the mitotic spindle. Proc Natl Acad Sci USA 92:4289-4293.
108. Sawin KE, LeGuellec K, Philippe M, Mitchison TJ. 1992. Mitotic spindle organization by a plus-end-directed microtubule motor. Nature 359:540-543.
109. Schauerte HE, van Eeden FJ, Fricke C, Odenthal J, Strahle U, Haffter P. 1998. Sonic hedgehog is not required for the induction of medial floor plate cells in the zebrafish. Development 125:2983-2993.
110. Schier AF, Neuhauss SC, Harvey M, Malicki J, Solnica-Krezel L, Stainier DY, Zwartkruis F, Abdelilah S, Stemple DL, Rangini Z, Yang H, Driever W. 1996. Mutations affecting the development of the embryonic zebrafish brain. Development 123:165-178.
111. Shaham S. 2005. Glia-neuron interactions in nervous system function and development. Curr Top Dev Biol 69:39-66.
112. Shin J, Poling J, Park HC, Appel B. 2007. Notch signaling regulates neural precursor allocation and binary neuronal fate decisions in zebrafish. Development 134:1911-1920.
113. Shu T, Butz KG, Plachez C, Gronostajski RM, Richards LJ. 2003a. Abnormal development of forebrain midline glia and commissural projections in Nfia knockout mice. J Neurosci 23:203-212.
114. Shu T, Puche AC, Richards LJ. 2003b. Development of midline glial populations at the corticoseptal boundary. J Neurobiol 57:81-94.
115. Song R, Kim YW, Koo BK, Jeong HW, Yoon MJ, Yoon KJ, Jun DJ, Im SK, Shin J, Kong MP, Kim KT, Yoon K, Kong YY. 2008. Mind bomb 1 in the lymphopoietic niches is essential for T and marginal zone B cell development. J Exp Med 205: 2525-2536.
116. Stuermer CA. 1988. Retinotopic organization of the developing retinotectal projection in the zebrafish embryo. J Neurosci 8:4513-4530.
117. Sun Z, Hopkins N. 2001. vhnf1, the MODY5 and familial GCKD-associated gene, regulates regional specification of the zebrafish gut, pronephros, and hindbrain. Genes Dev 15:3217-3229.
118. Sun Z, Amsterdam A, Pazour GJ, Cole DG, Miller MS, Hopkins N. 2004. A genetic screen in zebrafish identifies cilia genes as a principal cause of cystic kidney. Development 131:4085-4093.
119. Suzuki SC, Takeichi M. 2008. Cadherins in neuronal morphogenesis and function. Dev Growth Differ 50(suppl 1):S119-S130.
120. Taber KH, Hurley RA. 2008. Astroglia: not just glue. J Neuropsychiatry Clin Neurosci 20:iv-129.
121. Tawk M, Araya C, Lyons DA, Reugels AM, Girdler GC, Bayley PR, Hyde DR, Tada M, Clarke JD. 2007. A mirror-symmetric cell division that orchestrates neuroepithelial morphogenesis. Nature 446:797-800.
122. Thiery JP. 2003. Cell adhesion in development: a complex signaling network. Curr Opin Genet Dev 13:365-371.
123. Tokumoto M, Gong Z, Tsubokawa T, Hew CL, Uyemura K, Hotta Y, 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.
124. Tomaselli KJ, Neugebauer KM, Bixby JL, Lilien J, Reichardt LF. 1988. N-cadherin and integrins: two receptor systems that mediate neuronal process outgrowth on astrocyte surfaces. Neuron 1:33-43.
125. Trevarrow B, Marks DL, Kimmel CB. 1990. Organization of hindbrain segments in the zebrafish embryo. Neuron 4:669-679.
126. Trowe T, Klostermann S, Baier H, Granato M, Crawford AD, Grunewald B, Hoffmann H, Karlstrom RO, Meyer SU, Muller B, Richter S, Nusslein-Volhard C, Bonhoeffer F. 1996. Mutations disrupting the ordering and topographic mapping of axons in the retinotectal projection of the zebrafish, Danio rerio. Development 123:439-450.
127. Valentine MT, Fordyce PM, Block SM. 2006a. Eg5 steps it up! Cell Div 1:31.
128. Valentine MT, Fordyce PM, Krzysiak TC, Gilbert SP, Block SM. 2006b. Individual dimers of the mitotic kinesin motor Eg5 step processively and support substantial loads in vitro. Nat Cell Biol 8:470-476.
129. van der Lelij P, Godthelp BC, van Zon W, van Gosliga D, Oostra AB, Steltenpool J, de Groot J, Scheper RJ, Wolthuis RM, Waisfisz Q, Darroudi F, Joenje H, de Winter JP. 2009. The cellular phenotype of Roberts syndrome fibroblasts as revealed by ectopic expression of ESCO2. PLoS One 4:e6936.
130. Varga ZM, Amores A, Lewis KE, Yan YL, Postlethwait JH, Eisen JS, Westerfield M. 2001. Zebrafish smoothened functions in ventral neural tube specification and axon tract formation. Development 128: 3497-3509.
131. Vega H, Waisfisz Q, Gordillo M, Sakai N, Yanagihara I, Yamada M, van Gosliga D, Kayserili H, Xu C, Ozono K, JabsEW, Inui K, Joenje H. 2005. Roberts syndrome is caused by mutations in ESCO2, a human homolog of yeast ECO1 that is essential for the establishment of sister chromatid cohesion. Nat Genet 37:468-470.
132. Wechsler-Reya R, Scott MP. 2001. The developmental biology of brain tumors. Annu Rev Neurosci 24:385-428.
133. Wei X, Malicki J. 2002. nagie oko, encoding a MAGUK-family protein, is essential for cellular patterning of the retina. Nat Genet 31:150-157.
134. Wei X, Zou J, Takechi M, Kawamura S, Li L. 2006. Nok plays an essential role in maintaining the integrity of the outer nuclear layer in the zebrafish retina. Exp Eye Res 83:31-44.
135. Westerfield M. 2007. The Zebrafish Book, A guide for the laboratory use of zebrafish (Danio rerio). Eugene: University of Oregon Press.
136. Westfall TA, Brimeyer R, Twedt J, Gladon J, Olberding A, Furutani-Seiki M, Slusarski DC. 2003. Wnt-5/pipetail functions in vertebrate axis formation as a negative regulator of Wnt/beta-catenin activity. J Cell Biol 162:889-898.
137. Wickner RB. 1988. Host function of MAK16: G1 arrest by a mak16 mutant of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 85:6007-6011.
138. Wiellette EL, Sive H. 2003. vhnf1 and Fgf signals synergize to specify rhombomere identity in the zebrafish hindbrain. Development 130:3821-3829.
139. Wilson SW, Ross LS, Parrett T, Easter Jr. SS 1990. The development of a simple scaffold of axon tracts in the brain of the embryonic zebrafish, Brachydanio rerio. Development 108:121-145.
140. Yamagata K, Nammo T, Moriwaki M, Ihara A, Iizuka K, Yang Q, Satoh T, Li M, Uenaka R, Okita K, Iwahashi H, Zhu Q, Cao Y, Imagawa A, Tochino Y, Hanafusa T, Miyagawa J, Matsuzawa Y. 2002. Overexpression of dominantnegative mutant hepatocyte nuclear fctor-1 alpha in pancreatic beta-cells causes abnormal islet architecture with decreased expression of E-cadherin, reduced beta-cell proliferation, and diabetes. Diabetes 51:114-123.
141. Yang X, Zou J, Hyde DR, Davidson LA, Wei X. 2009. Stepwise maturation of apicobasal polarity of the neuroepithelium is essential for vertebrate neurulation. J Neurosci 29:11426-11440.
142. Yeo SY. 2009. Zebrafish CiA interneurons are late-born primary neurons. Neurosci Lett 466:131-134.
143. Yoo KW, Kim EH, Jung SH, Rhee M, Koo BK, Yoon KJ, Kong YY, Kim CH. 2006. Snx5, as a Mind bomb-binding protein, is expressed in hematopoietic and endothelial precursor cells in zebrafish. FEBS Lett 580:4409-4416.
144. Zolessi FR, Poggi L, Wilkinson CJ, Chien CB, Harris WA. 2006. Polarization and orientation of retinal ganglion cells in vivo. Neural Develop 1:2.
145. Zou J, Lathrop KL, Sun M, Wei X. 2008. Intact retinal pigment epithelium maintained by Nok is essential for retinal epithelial polarity and cellular patterning in zebrafish. J Neurosci 28:13684-13695.