Zebrafish V2 cells develop into excitatory CiD and Notch signalling dependent inhibitory VeLD interneurons

Developmental Biology

Volumn 322, Issue 2, 2008, Pages 263-275

  Batista, Manuel F ^a   Jacobstein, Jeffrey ^a   Lewis, Katharine E ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Chx10; CiD; GABA; Gata2; Gata3; Glycine; Interneuron; KA; Mind bomb; Notch; Scl; Spinal cord; V2; VeLD; Vsx1; Zebrafish

Indexed keywords

NOTCH RECEPTOR; TRANSCRIPTION FACTOR GATA 2; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR LHX3; TRANSCRIPTION FACTOR TAL1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CELL STRUCTURE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINAL CORD; V2 CELL; ZEBRA FISH;

AMNIOTA; DANIO RERIO; VERTEBRATA;

EID: 53049106219     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2008.07.015     Document Type: Article

References (66)

1. Abramoff M.D., Magelhaes P.J., and Ram S.J. Image processing with Image. J. Biophotonics International 11 (2004) 36-42
2. Al-Mosawie A., Wilson J.M., and Brownstone R.M. Heterogeneity of V2-derived interneurons in the adult mouse spinal cord. Eur. J. Neurosci. 26 (2007) 3003-3015
3. Alvarez F.J., Jonas P.C., Sapir T., Hartley R., Berrocal M.C., Geiman E.J., Todd A.J., and Goulding M. Postnatal phenotype and localization of spinal cord V1 derived interneurons. J. Comp. Neurol. 493 (2005) 177-192
4. Appel B., Korzh V., Glasgow E., Thor S., Edlund T., Dawid I.B., and Eisen J.S. Motoneuron fate specification revealed by patterned LIM homeobox gene expression in embryonic zebrafish. Development 121 (1995) 4117-4125
5. Appel B., Givan L.A., and Eisen J.S. Delta-Notch signaling and lateral inhibition in zebrafish spinal cord development. BMC Dev. Biol. 1 (2001) 13
6. Bernhardt R.R., Chitnis A.B., Lindamer L., and Kuwada J.Y. Identification of spinal neurons in the embryonic and larval zebrafish. J. Comp. Neurol. 302 (1990) 603-616
7. Bernhardt R.R., Patel C.K., Wilson S.W., and Kuwada J.Y. Axonal trajectories and distribution of GABAergic spinal neurons in wildtype and mutant zebrafish lacking floor plate cells. J. Comp. Neurol. 326 (1992) 263-272
8. Bray S. Notch signalling in Drosophila: three ways to use a pathway. Semin. Cell Dev. Biol. 9 (1998) 591-597
9. Briscoe J., Pierani A., Jessell T.M., and Ericson J. A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101 (2000) 435-445
10. Chen C.M., and Cepko C.L. Expression of Chx10 and Chx10-1 in the developing chicken retina. Mech. Dev. 90 (2000) 293-297
11. Chow R.L., Snow B., Novak J., Looser J., Freund C., Vidgen D., Ploder L., and McInnes R.R. Vsx1, a rapidly evolving paired-like homeobox gene expressed in cone bipolar cells. Mech. Dev. 109 (2001) 315-322
12. Clark A.M., Yun S., Veien E.S., Wu Y.Y., Chow R.L., Dorsky R.I., and Levine E.M. Negative regulation of Vsx1 by its paralog Chx10/Vsx2 is conserved in the vertebrate retina. Brain Res. (2007)
13. Concordet J.P., Lewis K.E., Moore J.W., Goodrich L.V., Johnson R.L., Scott M.P., and Ingham P.W. Spatial regulation of a zebrafish patched homologue reflects the roles of sonic hedgehog and protein kinase A in neural tube and somite patterning. Development 122 (1996) 2835-2846
14. D'Autilia S., Decembrini S., Casarosa S., He R.Q., Barsacchi G., Cremisi F., and Andreazzoli M. Cloning and developmental expression of the Xenopus homeobox gene Xvsx1. Dev. Genes Evol. 216 (2006) 829-834
15. Dale N., Roberts A., Ottersen O.P., and Storm-Mathisen J. The morphology and distribution of 'Kolmer-Agduhr cells', a class of cerebrospinal-fluid-contacting neurons revealed in the frog embryo spinal cord by GABA immunocytochemistry. Proc. Natl. Acad. Sci. 232 (1987) 193-203
16. Del Barrio M.G., Taveira-Marques R., Muroyama Y., Yuk D.I., Li S., Wines-Samuelson M., Shen J., Smith H.K., Xiang M., Rowitch D., and Richardson W.D. A regulatory network involving Foxn4, Mash1 and delta-like 4/Notch1 generates V2a and V2b spinal interneurons from a common progenitor pool. Development 134 (2007) 3427-3436
17. Gosgnach S., Lanuza G.M., Butt S.J., Saueressig H., Zhang Y., Velasquez T., Riethmacher D., Callaway E.M., Kiehn O., and Goulding M. V1 spinal neurons regulate the speed of vertebrate locomotor outputs. Nature 440 (2006) 215-219
18. Goulding M., and Pfaff S.L. Development of circuits that generate simple rhythmic behaviors in vertebrates. Curr. Opin. Neurobiol. 15 (2005) 14-20
19. Hayashi T., Huang J., and Deeb S.S. RINX(VSX1), a novel homeobox gene expressed in the inner nuclear layer of the adult retina. Genomics 67 (2000) 128-139
20. Hayashi T., Huang J., and Deeb S.S. Expression of rinx/vsx1 during postnatal eye development in cone-bipolar, differentiating ganglion, and lens fiber cells. Jpn. J. Ophthalmol. 49 (2005) 93-105
21. Higashijima S., Mandel G., and Fetcho J.R. Distribution of prospective glutamatergic, glycinergic, and GABAergic neurons in embryonic and larval zebrafish. J. Comp. Neurol. 480 (2004) 1-18
22. Higashijima S., Masino M., Mandel G., and Fetcho J.R. Engrailed-1 expression marks a primitive class of inhibitory spinal interneuron. J. Neurosci. 24 (2004) 5827-5839
23. Higashijima S., Schaefer M., and Fetcho J.R. Neurotransmitter properties of spinal interneurons in embryonic and larval zebrafish. J. Comp. Neurol. 480 (2004) 19-37
24. Itoh M., Kim C., Palardy G., Oda T., Jiang Y., Maust D., Yeo S., Lorick K., Wright G., Ariza-McNaughton L., Weissman A., Lewis J., Chandrasekharappa S., and Chitnis A. Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta. Dev. Cell. 4 (2003) 67-82
25. Jiang Y.J., Brand M., Heisenberg C.P., Beuchle D., Furutani-Seiki M., Kelsh R.N., Warga R.M., Granato M., Haffter P., Hammerschmidt M., Kane D.A., Mullins M.C., Odenthal J., Van Eeden F.J.M., and Nüsslein-Volhard C. Mutations affecting neurogenesis and brain morphology in the zebrafish, Danio rerio. Development 123 (1996) 205-216
26. Karunaratne A., Hargrave M., Poh A., and Yamada T. GATA proteins identify a novel ventral interneuron subclass in the developing chick spinal cord. Dev. Biol. 249 (2002) 30-43
27. Kimmel C.B., and Westerfield M. Primary neurons of the zebrafish. In: Edelman G.M., Gall W.E., and Cowan W.M. (Eds). "Signals and Sense: Local and Global Order in Perceptual Maps" (1990), Wiley-Liss, New York 561-588
28. Kimmel C.B., Warga R.M., and Kane D.A. Cell cycles, clonal strings, and the origin of the zebrafish central nervous system. Development 120 (1994) 265-276
29. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., and Schilling T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 203 (1995) 253-310
30. Kimura Y., Okamura Y., and Higashijima S. alx, a zebrafish homolog of Chx10, marks ipsilateral descending excitatory interneurons that participate in the regulation of spinal locomotor circuits. J. Neurosci. 26 (2006) 5684-5697
31. Kobayashi M., Nishikawa K., and Yamamoto M. Hematopoietic regulatory domain of gata1 gene is positively regulated by GATA1 protein in zebrafish embryos. Development 128 (2001) 2341-2350
32. Kuwada J.Y., Bernhardt R.R., and Nguyen N. Development of spinal neurons and tracts in the zebrafish embryo. J. Comp. Neurol. 302 (1990) 617-628
33. Lewis J. Notch signalling and the control of cell fate choices in vertebrates. Semin. Cell Dev. Biol. 9 (1998) 583-589
34. Lewis K.E. How do genes regulate simple behaviours? Understanding how different neurons in the vertebrate spinal cord are genetically specified. Philos. Trans. R Soc. Lond. B Biol. Sci. 361 (2006) 45-66
35. Lewis K.E., Bates J., and Eisen J.S. Regulation of iro3 expression in the zebrafish spinal cord. Dev. Dyn. 232 (2005) 140-148
36. Li W.C., Higashijima S., Parry D.M., Roberts A., and Soffe S.R. Primitive roles for inhibitory interneurons in developing frog spinal cord. J. Neurosci. 24 (2004) 5840-5848
37. Li S., Misra K., Matise M.P., and Xiang M. Foxn4 acts synergistically with Mash1 to specify subtype identity of V2 interneurons in the spinal cord. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 10688-10693
38. Li W.C., Sautois B., Roberts A., and Soffe S.R. Reconfiguration of a vertebrate motor network: specific neuron recruitment and context-dependent synaptic plasticity. J. Neurosci. 27 (2007) 12267-12276
39. Lundfald L., Restrepo C.E., Butt S.J., Peng C.Y., Droho S., Endo T., Zeilhofer H.U., Sharma K., and Kiehn O. Phenotype of V2-derived interneurons and their relationship to the axon guidance molecule EphA4 in the developing mouse spinal cord. Eur. J. Neurosci. 26 (2007) 2989-3002
40. Mizuguchi R., Sugimori M., Takebayashi H., Kosako H., Nagao M., Yoshida S., Nabeshima Y., Shimamura K., and Nakafuku M. Combinatorial roles of olig2 and neurogenin2 in the coordinated induction of pan-neuronal and subtype-specific properties of motoneurons. Neuron 31 (2001) 757-771
41. Mizuguchi R., Kriks S., Cordes R., Gossler A., Ma Q., and Goulding M. Ascl1 and Gsh1/2 control inhibitory and excitatory cell fate in spinal sensory interneurons. Nat. Neurosci. 9 (2006) 770-778
42. Muroyama Y., Fujiwara Y., Orkin S.H., and Rowitch D.H. Specification of astrocytes by bHLH protein SCL in a restricted region of the neural tube. Nature 438 (2005) 360-363
43. Myers P.Z., Eisen J.S., and Westerfield M. Development and axonal outgrowth of identified motoneurons in the zebrafish. J. Neurosci 6 (1986) 2278-2289
44. Neave B., Rodaway A., Wilson S.W., Patient R., and Holder N. Expression of zebrafish GATA 3 (gta3) during gastrulation and neurulation suggests a role in the specification of cell fate. Mech. Dev. 51 (1995) 169-182
45. Novitch B.G., Chen A.I., and Jessell T.M. Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron 31 (2001) 773-789
46. Ohtoshi A., Justice M.J., and Behringer R.R. Isolation and characterization of Vsx1, a novel mouse CVC paired-like homeobox gene expressed during embryogenesis and in the retina. Biochem. Biophys. Res. Commun. 286 (2001) 133-140
47. Park H.C., and Appel B. Delta-Notch signaling regulates oligodendrocyte specification. Development 130 (2003) 3747-3755
48. Park H.C., Mehta A., Richardson J.S., and Appel B. olig2 is required for zebrafish primary motor neuron and oligodendrocyte development. Dev. Biol. 248 (2002) 356-368
49. Park H.C., Shin J., and Appel B. Spatial and temporal regulation of ventral spinal cord precursor specification by Hedgehog signaling. Development 131 (2004) 5959-5969
50. Passini M.A., Kurtzman A.L., Canger A.K., Asch W.S., Wray G.A., Raymond P.A., and Schechter N. Cloning of zebrafish vsx1: expression of a paired-like homeobox gene during CNS development. Dev. Genet. 23 (1998) 128-141
51. Peng C.Y., Yajima H., Burns C.E., Zon L.I., Sisodia S.S., Pfaff S.L., and Sharma K. Notch and MAML signaling drives Scl-dependent interneuron diversity in the spinal cord. Neuron 53 (2007) 813-827
52. Read E.M., Rodaway A.R., Neave B., Brandon N., Holder N., Patient R.K., and Walmsley M.E. Evidence for non-axial A/P patterning in the nonneural ectoderm of Xenopus and zebrafish pregastrula embryos. Int. J. Dev. Biol. 42 (1998) 763-774
53. Roberts A. Early functional organization of spinal neurons in developing lower vertebrates. Brain Res. Bull. 53 (2000) 585-593
54. Roberts A., and Clarke J.D. The neuroanatomy of an amphibian embryo spinal cord. Philos. Trans. R Soc. Lond. B Biol. Sci. 296 (1982) 195-212
55. Saint-Amant L., and Drapeau P. Synchronization of an embryonic network of identified spinal interneurons solely by electrical coupling. Neuron 31 (2001) 1035-1046
56. Sapir T., Geiman E.J., Wang Z., Velasquez T., Mitsui S., Yoshihara Y., Frank E., Alvarez F.J., and Goulding M. Pax6 and engrailed 1 regulate two distinct aspects of renshaw cell development. J. Neurosci. 24 (2004) 1255-1264
57. Schier A.F., Neuhauss S.C., Harvey M., Malicki J., Solnica K.L., Stainier D.Y., Zwartkruis F., Abdelilah S., Stemple D.L., Rangini Z., Yang H., and Driever W. Mutations affecting the development of the embryonic zebrafish brain. Development 123 (1996) 165-178
58. Schier A.F., Neuhauss S.C.F., Harvey M., Malicki J., Solnica-Krezel L., Stainier D.Y.R., Zwartkruis F., Abdelilah S., Stemple D.L., Rangini Z., Yang H., and Driever W. Mutations affecting the development of the embryonic zebrafish brain. Development 123 (1996) 165-178
59. Semina E.V., Mintz-Hittner H.A., and Murray J.C. Isolation and characterization of a novel human paired-like homeodomain-containing transcription factor gene, VSX1, expressed in ocular tissues. Genomics 63 (2000) 289-293
60. Shin J., Poling J., Park H.C., and Appel B. Notch signaling regulates neural precursor allocation and binary neuronal fate decisions in zebrafish. Development 134 (2007) 1911-1920
61. Smith E., Hargrave M., Yamada T., Begley C.G., and Little M.H. Coexpression of SCL and GATA3 in the V2 interneurons of the developing mouse spinal cord. Dev. Dyn. 224 (2002) 231-237
62. Tan J.T.T., Korzh V., and Gong Z. Expression of a zebrafish iroquois homeobox gene, Ziro3, in the midline axial structures and central nervous system. Mechanisms of Development 87 (1999) 165-168
63. Vigh B., Vigh-Teichmann I., Manzano e Silva M.J., and van den Pol A.N. Cerebrospinal fluid-contacting neurons of the central canal and terminal ventricle in various vertebrates. Cell Tissue Res 231 (1983) 615-621
64. Yang X., Tomita T., Wines-Samuelson M., Beglopoulos V., Tansey M.G., Kopan R., and Shen J. Notch1 signaling influences v2 interneuron and motor neuron development in the spinal cord. Dev. Neurosci. 28 (2006) 102-117
65. Yeo S.Y., and Chitnis A.B. Jagged-mediated Notch signaling maintains proliferating neural progenitors and regulates cell diversity in the ventral spinal cord. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 5913-5918
66. Zhou Y., Yamamoto M., and Engel J.D. GATA2 is required for the generation of V2 interneurons. Development 127 (2000) 3829-3838