Oligodendrocyte specification in zebrafish requires notch-regulated cyclin-dependent kinase inhibitor function

Journal of Neuroscience

Volumn 25, Issue 29, 2005, Pages 6836-6844

  Park, Hae Chul ^a   Boyce, Janene ^a   Shin, Jimann ^a   Appel, Bruce ^a  

^a VANDERBILT UNIVERSITY   (United States)

Author keywords

Cell cycle; Cell fate; Neural precursor; Neurogenesis; Oligodendrocyte; Spinal cord

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR; CYCLIN DEPENDENT KINASE INHIBITOR 1C; NOTCH RECEPTOR; PROTEIN P57; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CYCLE; CELL DIFFERENTIATION; CELL FATE; CELL FUNCTION; CELL SPECIFICITY; CONTROLLED STUDY; DELTA NERVE FIBER; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; GLIA; NERVE CELL; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; VERTEBRATE; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL DIFFERENTIATION; CELL DIVISION; CYCLIN-DEPENDENT KINASE INHIBITOR P57; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; MALE; NERVE TISSUE PROTEINS; NEURONS; OLIGODENDROGLIA; RECEPTOR, NOTCH1; SIGNAL TRANSDUCTION; SPINAL CORD; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 22544443908     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0981-05.2005     Document Type: Article

References (57)

1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403-410.
2. Appel B, Eisen JS (1998) Regulation of neuronal specification in the zebrafish spinal cord by Delta function. Development 125:371-380.
3. Appel B, Korzh V, Glasgow E, Thor S, Edlund T, Dawid IB, Eisen JS (1995) Motoneuron fate specification revealed by patterned LIM homeobox gene expression in embryonic zebrafish. Development 121:4117-4125.
4. Appel B, Fritz A, Westerfield M, Grunwald DJ, Eisen JS, Riley BB (1999) Delta-mediated specification of midline cell fates in zebrafish embryos. Curr Biol 9:247-256.
5. Appel B, Givan LA, Eisen JS (2001) Delta-Notch signaling and lateral inhibition in zebrafish spinal cord development. BMC Dev Biol 1:13.
6. Baumann N, Pham-Dinh D (2001) Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol Rev 81:871-927.
7. Brosamle C, Halpern ME (2002) Characterization of myelination in the developing zebrafish. Glia 39:47-57.
8. Carruthers S, Mason J, Papalopulu N (2003) Depletion of the cell-cycle inhibitor p27(Xic1) impairs neuronal differentiation and increases the number of ElrC(+) progenitor cells in Xenopus tropicalis. Mech Dev 120:607-616.
9. Casaccia-Bonnefil P, Tikoo R, Kiyokawa H, Friedrich Jr V, Chao MV, Koff A (1997) Oligodendrocyte precursor differentiation is perturbed in the absence of the cyclin-dependent kinase inhibitor p27Kip1. Genes Dev 11:2335-2346.
10. Casaccia-Bonnefil P, Hardy RJ, Teng KK, Levine JM, Koff A, Chao MV (1999) Loss of p27Kip1 function results in increased proliferative capacity of oligodendrocyte progenitors but unaltered timing of differentiation. Development 126:4027-4037.
11. Cunningham JJ, Roussel MF (2001) Cyclin-dependent kinase inhibitors in the development of the central nervous system. Cell Growth Differ 12:387-396.
12. de Nooij JC, Letendre MA, Hariharan IK (1996) A cyclin-dependent kinase inhibitor, Dacapo, is necessary for timely exit from the cell cycle during Drosophila embryogenesis. Cell 87:1237-1247.
13. Durand B, Gao FB, Raff M (1997) Accumulation of the cyclin-dependent kinase inhibitor p27/Kip1 and the timing of oligodendrocyte differentiation. EMBO J 16:306-317.
14. Durand B, Fero ML, Roberts JM, Raff MC (1998) p27Kip1 alters the response of cells to mitogen and is part of a cell-intrinsic timer that arrests the cell cycle and initiates differentiation. Curr Biol 8:431-440.
15. Farah MH, Olson JM, Sucic HB, Hume RI, Tapscott SJ, Turner DL (2000) Generation of neurons by transient expression of neural bHLH proteins in mammalian cells. Development 127:693-702.
16. Fukuyama M, Gendreau SB, Derry WB, Rothman JH (2003) Essential embryonic roles of the CKI-1 cyclin-dependent kinase inhibitor in cell-cycle exit and morphogenesis in C. elegans. Dev Biol 260:273-286.
17. Furukawa T, Mukherjee S, Bao ZZ, Morrow EM, Cepko CL (2000) rax, Hes1, and notch1 promote the formation of Muller glia by postnatal retinal progenitor cells. Neuron 26:383-394.
18. Hardcastle Z, Papalopulu N (2000) Distinct effects of XBF-1 in regulating the cell cycle inhibitor p27(XIC1) and imparting a neural fate. Development 127:1303-1314.
19. Hauptmann G, Gerster T (2000) Multicolor whole-mount in situ hybridization. Methods Mol Biol 137:139-148.
20. Holley SA, Geisler R, Nusslein-Volhard C (2000) Control of her1 expression during zebrafish somitogenesis by a delta-dependent oscillator and an independent wave-front activity. Genes Dev 14:1678-1690.
21. Hong Y, Roy R, Ambros V (1998) Developmental regulation of a cyclin-dependent kinase inhibitor controls postembryonic cell cycle progression in Caenorhabditis elegans. Development 125:3585-3597.
22. Horner PJ, Power AE, Kempermann G, Kuhn HG, Palmer TD, Winkler J, Thal LJ, Gage FH (2000) Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J Neurosci 20:2218-2228.
23. 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.
24. 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.
25. Kadesch T (2004) Notch signaling: the demise of elegant simplicity. Curr Opin Genet Dev 14:506-512.
26. Kageyama R, Ohtsuka T (1999) The Notch-Hes pathway in mammalian neural development. Cell Res 9:179-188.
27. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253-310.
28. Kiyokawa H, Kineman RD, Manova-Todorova KO, Soares VC, Hoffman ES, Ono M, Khanam D, Hayday AC, Frohman LA, Koff A (1996) Enhanced growth of mice lacking the cyclin-dependent kinase inhibitor function of p27(Kip1). Cell 85:721-732.
29. Lane ME, Sauer K, Wallace K, Jan YN, Lehner CF, Vaessin H (1996) Dacapo, a cyclin-dependent kinase inhibitor, stops cell proliferation during Drosophila development. Cell 87:1225-1235.
30. Latimer AJ, Shin J, Appel B (2005) her9 promotes floor plate development in zebrafish. Dev Dyn 232:1098-1104.
31. Levine EM, Close J, Fero M, Ostrovsky A, Reh TA (2000) p27(Kip1) regulates cell cycle withdrawal of late multipotent progenitor cells in the mammalian retina. Dev Biol 219:299-314.
32. Levison SW, Young GM, Goldman JE (1999) Cycling cells in the adult rat neocortex preferentially generate oligodendroglia. J Neurosci Res 57:435-446.
33. Lowenheim H, Furness DN, Kil J, Zinn C, Gultig K, Fero ML, Frost D, Gummer AW, Roberts JM, Rubel EW, Hackney CM, Zenner HP (1999) Gene disruption of p27(Kip1) allows cell proliferation in the postnatal and adult organ of Corti. Proc Natl Acad Sci USA 96:4084-4088.
34. McConnell SK, Kaznowski CE (1991) Cell cycle dependence of laminar determination in developing neocortex. Science 254:282-285.
35. Miller RH (2002) Regulation of oligodendrocyte development in the vertebrate CNS. Prog Neurobiol 67:451-467.
36. Miyazawa K, Himi T, Garcia V, Yamagishi H, Sato S, Ishizaki Y (2000) A role for p27/Kip1 in the control of cerebellar granule cell precursor proliferation. J Neurosci 20:5756-5763.
37. Ohnuma S, Philpott A, Wang K, Holt CE, Harris WA (1999) p27Xic1, a Cdk inhibitor, promotes the determination of glial cells in Xenopus retina. Cell 99:499-510.
38. Pagliuca A, Gallo P, De Luca P, Lania L (2000) Class A helix-loop-helix proteins are positive regulators of several cyclin-dependent kinase inhibitors' promoter activity and negatively affect cell growth. Cancer Res 60:1376-1382.
39. Park H, Mehta A, Richardson JS, Appel B (2002) olig2 is required for zebrafish primary motor neuron and oligodendrocyte development. Dev Biol 248:356-368.
40. Park H, Shin J, Appel B (2004) Spatial and temporal regulation of ventral spinal cord precursor specification by Hedgehog signaling. Development 131:5959-5969.
41. Park H-C, Appel B (2003) Delta-Notch signaling regulates oligodendrocyte specification. Development 130:3747-3755.
42. Scheer N, Campos-Ortega JA (1999) Use of the Gal4-UAS technique for targeted gene expression in the zebrafish. Mech Dev 80:153-158.
43. Scheer N, Groth A, Hans S, Campos-Ortega JA (2001) An instructive function for Notch in promoting gliogenesis in the zebrafish retina. Development 128:1099-1107.
44. 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.
45. 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.
46. Shin J, Park HC, Topczewska JM, Mawdsley DJ, Appel B (2003) Neural cell fate analysis in zebrafish using olig2 BAC transgenics. Methods Cell Sci 25:7-14.
47. Shoji W, Yee CS, Kuwada JY (1998) Zebrafish semaphorin Zla collapses specific growth cones and alters their pathway in vivo. Development 125:1275-1283.
48. Sprague J, Doerry E, Douglas S, Westerfield M (2001) The Zebrafish Information Network (ZFIN): a resource for genetic, genomic and developmental research. Nucleic Acids Res 29:87-90.
49. Thermes V, Grabher C, Ristoratore F, Bourrat F, Choulika A, Wittbrodt J, Joly JS (2002) I-SceI meganuclease mediates highly efficient transgenesis in fish. Mech Dev 118:91-98.
50. Turner DL, Weintraub H (1994) Expression of achaete-scute homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate. Genes Dev 8:1434-1447.
51. Vernon AE, Devine C, Philpott A (2003) The cdk inhibitor p27Xic1 is required for differentiation of primary neurones in Xenopus. Development 130:85-92.
52. Wallace K, Liu TH, Vaessin H (2000) The pan-neural bHLH proteins DEADPAN and ASENSE regulate mitotic activity and cdk inhibitor dacapo expression in the Drosophila larval optic lobes. Genesis 26:77-85.
53. Wang S, Sdrulla AD, diSibio G, Bush G, Nofziger D, Hicks C, Weinmaster G, Barres BA (1998) Notch receptor activation inhibits oligodendrocyte differentiation. Neuron 21:63-75.
54. Westerfield M (2000) The zebrafish book. Eugene, OR: University of Oregon.
55. Wettstein DA, Turner DL, Kintner C (1997) The Xenopus homolog of Drosophila Suppressor of Hairless mediates Notch signaling during primary neurogenesis. Development 124:693-702.
56. Zezula J, Casaccia-Bonnefil P, Ezhevsky SA, Osterhout DJ, Levine JM, Dowdy SF, Chao MV, Koff A (2001) p21cip1 is required for the differentiation of oligodendrocytes independently of cell cycle withdrawal. EMBO Rep 2:27-34.
57. Zhu L, Skoultchi AI (2001) Coordinating cell proliferation and differentiation. Curr Opin Genet Dev 11:91-97.