DeltaA/DeltaD regulate multiple and temporally distinct phases of notch signaling during dopaminergic neurogenesis in zebrafish

Journal of Neuroscience

Volumn 30, Issue 49, 2010, Pages 16621-16635

  Mahler, Julia ^a   Filippi, Alida ^a   Driever, Wolfgang ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOTROPIN RELEASING FACTOR; NOTCH RECEPTOR; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; PROTEIN; PROTEIN DELTAA; PROTEIN DELTAD; PROTEIN OTPA; PROTEIN SIM1A; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DIENCEPHALON; DOPAMINERGIC NERVE CELL; DOPAMINERGIC SYSTEM; EMBRYO; FOREBRAIN; GENE EXPRESSION; GENE OVEREXPRESSION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NORADRENERGIC NERVE; PRIORITY JOURNAL; PULVINAR; SIGNAL TRANSDUCTION; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BRAIN; CELL CYCLE; CORTICOTROPIN-RELEASING HORMONE; DEOXYURIDINE; DIPEPTIDES; DOPAMINE; EMBRYO, NONMAMMALIAN; ENZYME INHIBITORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HSP70 HEAT-SHOCK PROTEINS; MEMBRANE PROTEINS; MUTATION; NERVE TISSUE PROTEINS; NEUROGENESIS; OLIGODEOXYRIBONUCLEOTIDES, ANTISENSE; RECEPTORS, NOTCH; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TYROSINE 3-MONOOXYGENASE; UBIQUITIN-PROTEIN LIGASES; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 78650065982     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4769-10.2010     Document Type: Article

References (83)

1. Adolf B, Chapouton P, Lam CS, Topp S, Tannhäuser B, Strähle U, Götz M, Bally-Cuif L (2006) Conserved and acquired features of adult neurogenesis in the zebrafish telencephalon. Dev Biol 295:278-293.
2. Akimenko MA, Ekker M, Wegner J, Lin W, Westerfield M (1994) Combinatorial expression of three zebrafish genes related to distal-less: part of a homeobox gene code for the head. J Neurosci 14:3475-3486.
3. Allende ML, Weinberg ES (1994) The expression pattern of two zebrafish achaete-scute homolog (ash) genes is altered in the embryonic brain of the cyclops mutant. Dev Biol 166:509-530.
4. Amsterdam A, Hopkins N (2004) Retroviral-mediated insertional mutagenesis in zebrafish. Methods Cell Biol 77:3-20.
5. Andersson E, Jensen JB, Parmar M, Guillemot F, Björklund A (2006) Development of the mesencephalic dopaminergic neuron system is compromised in the absence of neurogenin 2. Development 133:507-516.
6. Androutsellis-Theotokis A, Rueger MA, Park DM, Mkhikian H, Korb E, Poser SW, Walbridge S, Munasinghe J, Koretsky AP, Lonser RR, McKay RD (2009) Targeting neural precursors in the adult brain rescues injured dopamine neurons. Proc Natl Acad Sci U S A 106:13570-13575.
7. Ang SL (2006) Transcriptional control of midbrain dopaminergic neuron development. Development 133:3499-3506.
8. Appel B, Givan LA, Eisen JS (2001) Delta-Notch signaling and lateral inhibition in zebrafish spinal cord development. BMC Dev Biol 1:13.
9. Bae YK, Shimizu T, Hibi M (2005) Patterning of proneuronal and inter-proneuronal domains by hairy- and enhancer of split-related genes in zebrafish neuroectoderm. Development 132:1375-1385.
10. Barth KA, Wilson SW (1995) Expression of zebrafish nk2.2 is influenced by sonic hedgehog/vertebrate hedgehog-1 and demarcates a zone of neuronal differentiation in the embryonic forebrain. Development 121:1755-1768.
11. Bauer M, Szulc J, Meyer M, Jensen CH, Terki TA, Meixner A, Kinkl N, Gasser T, Aebischer P, Ueffing M (2008) Delta-like 1 participates in the specification of ventral midbrain progenitor derived dopaminergic neurons. J Neurochem 104:1101-1115. (Pubitemid 351146578)
12. Bertrand N, Castro DS, Guillemot F (2002) Proneural genes and the specification of neural cell types. Nat Rev Neurosci 3:517-530.
13. Björklund A, Dunnett SB (2007) Dopamine neuron systems in the brain: an update. Trends Neurosci 30:194-202.
14. Blader P, Fischer N, Gradwohl G, Guillemot F, Strähle U (1997) The activity of neurogenin1 is controlled by local cues in the zebrafish embryo. Development 124:4557-4569.
15. Blechman J, Borodovsky N, Eisenberg M, Nabel-Rosen H, Grimm J, Levkowitz G (2007) Specification of hypothalamic neurons by dual regulation of the homeodomain protein Orthopedia. Development 134:4417-4426.
16. Borodovsky N, Ponomaryov T, Frenkel S, Levkowitz G (2009) Neural protein Olig2 acts upstream of the transcriptional regulator Sim1 to specify diencephalic dopaminergic neurons. Dev Dyn 238:826-834.
17. Buck SB, Bradford J, Gee KR, Agnew BJ, Clarke ST, Salic A (2008) Detection of S-phase cell cycle progression using 5-ethynyl-2′- deoxyuridine incorporation with click chemistry, an alternative to using 5-bromo-2′-deoxyuridine antibodies. Biotechniques 44:927-929.
18. Cameron HA, McKay RD (2001) Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435:406-417.
19. Cau E, Quillien A, Blader P (2008) Notch resolves mixed neural identities in the zebrafish epiphysis. Development 135:2391-2401.
20. Chan RW, Gargett CE (2006) Identification of label-retaining cells in mouse endometrium. Stem Cells 24:1529-1538.
21. Chandrasekar G, Lauter G, Hauptmann G (2007) Distribution of corticotropin-releasing hormone in the developing zebrafish brain. J Comp Neurol 505:337-351.
22. Chen YC, Priyadarshini M, Panula P (2009) Complementary developmental expression of the two tyrosine hydroxylase transcripts in zebrafish. Histochem Cell Biol 132:375-381.
23. Dauer W, Przedborski S (2003) Parkinson's disease: mechanisms and models. Neuron 39:889-909.
24. Del Giacco L, Sordino P, Pistocchi A, Andreakis N, Tarallo R, Di Benedetto B, Cotelli F (2006) Differential regulation of the zebrafish orthopedia 1 gene during fate determination of diencephalic neurons. BMC Dev Biol 6:50.
25. Dovey HF, John V, Anderson JP, Chen LZ, de Saint Andrieu P, Fang LY, Freedman SB, Folmer B, Goldbach E, Holsztynska EJ, Hu KL, Johnson-Wood KL, Kennedy SL, Kholodenko D, Knops JE, Latimer LH, Lee M, Liao Z, Lieberburg IM, Motter RN, et al. (2001) Functional gamma-secretase inhibitors reduce beta-amyloid peptide levels in brain. J Neurochem 76:173-181.
26. Eaton JL, Glasgow E (2006) The zebrafish bHLH PAS transcriptional regulator, single-minded 1 (sim1), is required for isotocin cell development. Dev Dyn 235:2071-2082.
27. Filippi A, Dürr K, Ryu S, Willaredt M, Holzschuh J, Driever W (2007) Expression and function of nr4a2, lmx1b, and pitx3 in zebrafish dopaminergic and noradrenergic neuronal development. BMC Dev Biol 7:135.
28. Filippi A, Mahler J, Schweitzer J, Driever W (2010) Expression of the paralogous tyrosine hydroxylase encoding genes th1 and th2 reveals the full complement of dopaminergic and noradrenergic neurons in zebrafish larval and juvenile brain. J Comp Neurol 518:423-438.
29. Fortini ME, Artavanis-Tsakonas S (1994) The suppressor of hairless protein participates in notch receptor signaling. Cell 79:273-282. (Pubitemid 2154297)
30. Geling A, Steiner H, Willem M, Bally-Cuif L, Haass C (2002) A gamma-secretase inhibitor blocks Notch signaling in vivo and causes a severe neurogenic phenotype in zebrafish. EMBO Rep 3:688-694.
31. Grandel H, Kaslin J, Ganz J, Wenzel I, Brand M (2006) Neural stem cells and neurogenesis in the adult zebrafish brain: origin, proliferation dynamics, migration and cell fate. Dev Biol 295:263-277.
32. Guo S, Wilson SW, Cooke S, Chitnis AB, Driever W, Rosenthal A (1999) Mutations in the zebrafish unmask shared regulatory pathways controlling the development of catecholaminergic neurons. Dev Biol 208:473-487.
33. 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 the mind bomb mutant. Development 125:4637-4644.
34. Hartenstein V (1989) Early neurogenesis in Xenopus: the spatio-temporal pattern of proliferation and cell lineages in the embryonic spinal cord. Neuron 3:399-411.
35. Hauptmann G, Gerster T (1994) Two-color whole-mount in situ hybridization to vertebrate and Drosophila embryos. Trends Genet 10:266.
36. Havrda MC, Harris BT, Mantani A, Ward NM, Paolella BR, Cuzon VC, Yeh HH, Israel MA (2008) Id2 is required for specification of dopaminergic neurons during adult olfactory neurogenesis. J Neurosci 28:14074-14086.
37. Hitoshi S, Alexson T, Tropepe V, Donoviel D, Elia AJ, Nye JS, Conlon RA, Mak TW, Bernstein A, 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.
38. Holzschuh J, Ryu S, Aberger F, Driever W (2001) Dopamine transporter expression distinguishes dopaminergic neurons from other catecholaminergic neurons in the developing zebrafish embryo. Mech Dev 101:237-243.
39. Holzschuh J, Hauptmann G, Driever W (2003) Genetic analysis of the roles of Hh, FGF8, and nodal signaling during catecholaminergic system development in the zebrafish brain. J Neurosci 23:5507-5519.
40. 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.
41. Iversen SD, Iversen LL (2007) Dopamine: 50 years in perspective. Trends Neurosci 30:188-193.
42. Jeong JY, Einhorn Z, Mercurio S, Lee S, Lau B, Mione M, Wilson SW, Guo S (2006) Neurogenin1 is a determinant of zebrafish basal forebrain dopaminergic neurons and is regulated by the conserved zinc finger protein Tof/Fezl. Proc Natl Acad Sci U S A 103:5143-5148.
43. Kastenhuber E, Kratochwil CF, Ryu S, Schweitzer J, Driever W (2010) Genetic dissection of dopaminergic and noradrenergic contributions to catecholaminergic tracts in early larval zebrafish. J Comp Neurol 518:439-458.
44. Katoh Y, Katoh M (2005) Comparative genomics on SOX2 orthologs. Oncol Rep 14:797-800.
45. Kele J, Simplicio N, Ferri AL, Mira H, Guillemot F, Arenas E, Ang SL (2006) Neurogenin 2 is required for the development of ventral midbrain dopaminergic neurons. Development 133:495-505.
46. Kimmel CB, Westerfield M (1990) Primary neurons of the zebrafish. In: Signals and senses: local and global order in perceptual maps (Edelman GM, Gal WR, Cowan WM, eds), pp 561-588. New York: Wiley.
47. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253-310.
48. 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.
49. Korzh V, Edlund T, Thor S (1993) Zebrafish primary neurons initiate expression of the LIM homeodomain protein Isl-1 at the end of gastrulation. Development 118:417-425. (Pubitemid 23214029)
50. Lewis J (1998) Notch signalling and the control of cell fate choices in vertebrates. Semin Cell Dev Biol 9:583-589.
51. Löhr H, Ryu S, Driever W (2009) Zebrafish diencephalic A11-related dopaminergic neurons share a conserved transcriptional network with neuroendocrine cell lineages. Development 136:1007-1017.
52. Louvi A, Artavanis-Tsakonas S (2006) Notch signalling in vertebrate neural development. Nat Rev Neurosci 7:93-102.
53. Nasevicius A, Ekker SC (2000) Effective targeted gene "knockdown" in zebrafish. Nat Genet 26:216-220.
54. Nielsen AL, Jørgensen AL (2003) Structural and functional characterization of the zebrafish gene for glial fibrillary acidic protein, GFAP. Gene 310:123-132. (Pubitemid 36703306)
55. Ohyama K, Ellis P, Kimura S, Placzek M (2005) Directed differentiation of neural cells to hypothalamic dopaminergic neurons. Development 132:5185-5197.
56. Park HC, Mehta A, Richardson JS, Appel B (2002) olig2 is required for zebrafish primary motor neuron and oligodendrocyte development. Dev Biol 248:356-368.
57. Puelles L, Verney C (1998) Early neuromeric distribution of tyrosine-hydroxylase-immunoreactive neurons in human embryos. J Comp Neurol 394:283-308.
58. Rink E, Wullimann MF (2001) The teleostean (zebrafish) dopaminergic system ascending to the subpallium (striatum) is located in the basal diencephalon (posterior tuberculum). Brain Res 889:316-330.
59. Rink E, Wullimann MF (2002a) Connections of the ventral telencephalon and tyrosine hydroxylase distribution in the zebrafish brain (Danio rerio) lead to identification of an ascending dopaminergic system in a teleost. Brain Res Bull 57:385-387.
60. Rink E, Wullimann MF (2002b) Development of the catecholaminergic system in the early zebrafish brain: an immunohistochemical study. Brain Res Dev Brain Res 137:89-100.
61. Robu ME, Larson JD, Nasevicius A, Beiraghi S, Brenner C, Farber SA, Ekker SC (2007) p53 activation by knockdown technologies. PLoS Genet 3:e78.
62. Russek-Blum N, Gutnick A, Nabel-Rosen H, Blechman J, Staudt N, Dorsky RI, Houart C, Levkowitz G (2008) Dopaminergic neuronal cluster size is determined during early forebrain patterning. Development 135:3401-3413.
63. Ryu S, Holzschuh J, Erhardt S, Ettl AK, Driever W (2005) Depletion of minichromosome maintenance protein 5 in the zebrafish retina causes cell-cycle defect and apoptosis. Proc Natl Acad Sci U S A 102:18467-18472.
64. Ryu S, Mahler J, Acampora D, Holzschuh J, Erhardt S, Omodei D, Simeone A, Driever W (2007) Orthopedia homeodomain protein is essential for diencephalic dopaminergic neuron development. Curr Biol 17:873-880.
65. Salic A, Mitchison TJ (2008) Achemical method for fast and sensitive detection of DNA synthesis in vivo. Proc Natl Acad Sci U S A 105:2415-2420.
66. Scheer N, Campos-Ortega JA (1999) Use of the Gal4-UAS technique for targeted gene expression in the zebrafish. Mech Dev 80:153-158. (Pubitemid 29125426)
67. Scheer N, Riedl I, Warren JT, Kuwada JY, Campos-Ortega JA (2002) A quantitative analysis of the kinetics of Gal4 activator and effector gene expression in the zebrafish. Mech Dev 112:9-14.
68. 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. (Pubitemid 27056745)
69. Schweitzer J, Driever W (2008) Development of the dopamine systems in zebrafish. In: Development and engineering of dopamine neurons (Pasterkamp RJ, Smidt MP, Burbach JPH, eds), pp 1-14. New York: Springer Science+Business Media.
70. 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.
71. Smidt MP, Burbach JP (2007) How to make a mesodiencephalic dopaminergic neuron. Nat Rev Neurosci 8:21-32.
72. Spana EP, Doe CQ (1996) Numb antagonizes Notch signaling to specify sibling neuron cell fates. Neuron 17:21-26.
73. Takada M, Li ZK, Hattori T (1988) Single thalamic dopaminergic neurons project to both the neocortex and spinal cord. Brain Res 455:346-352.
74. Tsarovina K, Schellenberger J, Schneider C, Rohrer H (2008) Progenitor cell maintenance and neurogenesis in sympathetic ganglia involves Notch signaling. Mol Cell Neurosci 37:20-31.
75. van Eeden FJ, Granato M, Schach U, Brand M, Furutani-Seiki M, Haffter P, Hammerschmidt M, Heisenberg CP, Jiang YJ, Kane DA, Kelsh RN, Mullins MC, Odenthal J, Warga RM, Allende ML, Weinberg ES, Nüsslein-Volhard C (1996) Mutations affecting somite formation and patterning in the zebrafish, Danio rerio. Development 123:153-164. (Pubitemid 27056744)
76. Vetter ML, Brown NL (2001) The role of basic helix-loop-helix genes in vertebrate retinogenesis. Semin Cell Dev Biol 12:491-498.
77. Warren M, Puskarczyk K, Chapman SC (2009) Chick embryo proliferation studies using EdU labeling. Dev Dyn 238:944-949.
78. Wullimann MF, Puelles L, Wicht H (1999) Early postembryonic neural development in the zebrafish: a 3-D reconstruction of forebrain proliferation zones shows their relation to prosomeres. Eur J Morphol 37:117-121.
79. Yun K, Fischman S, Johnson J, Hrabe de Angelis M, Weinmaster G, Rubenstein JL (2002) Modulation of the notch signaling by Mash1 and Dlx1/2 regulates sequential specification and differentiation of progenitor cell types in the subcortical telencephalon. Development 129:5029-5040.
80. Zecchin E, Conigliaro A, Tiso N, Argenton F, Bortolussi M (2005) Expression analysis of jagged genes in zebrafish embryos. Dev Dyn 233:638-645.
81. Zecchin E, Filippi A, Biemar F, Tiso N, Pauls S, Ellertsdottir E, Gnügge L, Bortolussi M, Driever W, Argenton F (2007) Distinct delta and jagged genes control sequential segregation of pancreatic cell types from precursor pools in zebrafish. Dev Biol 301:192-204.
82. Zhang C, Li Q, Jiang YJ (2007a) Zebrafish Mib and Mib2 are mutual E3 ubiquitin ligases with common and specific delta substrates. J Mol Biol 366:1115-1128.
83. Zhang C, Li Q, Lim CH, Qiu X, Jiang YJ (2007b) The characterization of zebrafish antimorphic mib alleles reveals that Mib and Mind bomb-2 (Mib2) function redundantly. Dev Biol 305:14-27. (Pubitemid 46613794)