Fbxw7 regulates Notch to control specification of neural precursors for oligodendrocyte fate

Neural Development

Volumn 7, Issue 1, 2012, Pages

  Snyder, Julia L ^a,b   Kearns, Christina A ^b   Appel, Bruce ^b  

^a VANDERBILT UNIVERSITY   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Glia; Myelin; Neural precursor; Notch; Oligodendrocyte; Zebrafish

Indexed keywords

CELL CYCLE PROTEIN; F BOX PROTEIN; FBXW7 PROTEIN, ZEBRAFISH; NOTCH1 RECEPTOR; TRANSCRIPTION FACTOR; UBIQUITIN PROTEIN LIGASE; ZEBRAFISH PROTEIN;

ANIMAL; ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OLIGODENDROGLIA; PHYSIOLOGY; PRENATAL DEVELOPMENT; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; STEM CELL; ZEBRA FISH;

ANIMALS; BASE SEQUENCE; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; CELL LINEAGE; F-BOX PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MOLECULAR SEQUENCE DATA; OLIGODENDROGLIA; RECEPTOR, NOTCH1; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; STEM CELLS; TRANSCRIPTION FACTORS; UBIQUITIN-PROTEIN LIGASES; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84860384285     PISSN: None     EISSN: 17498104     Source Type: Journal    
DOI: 10.1186/1749-8104-7-15     Document Type: Article

References (66)

1. Takebayashi H, Yoshida S, Sugimori M, Kosako H, Kominami R, Nakafuku M, Nabeshima Y. Dynamic expression of basic helix-loop-helix Olig family members: implication of Olig2 in neuron and oligodendrocyte differentiation and identification of a new member, Olig3. Mech Dev 2000, 99:143-148. 10.1016/S0925-4773(00)00466-4, 11091082.
2. Lu QR, Yuk D, Alberta JA, Zhu Z, Pawlitzky I, Chan J, Mcmahon AP, Stiles CD, Rowitch DH. Sonic hedgehog-regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron 2000, 25:317-329. 10.1016/S0896-6273(00)80897-1, 10719888.
3. Zhou Q, Wang S, Anderson DJ. Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron 2000, 25:331-343. 10.1016/S0896-6273(00)80898-3, 10719889.
4. Lu QR, Sun T, Zhu Z, Ma N, Garcia M, Stiles CD, Rowitch DH. Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 2002, 109:75-86. 10.1016/S0092-8674(02)00678-5, 11955448.
5. Zhou Q, Anderson DJ. The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 2002, 109:61-73. 10.1016/S0092-8674(02)00677-3, 11955447.
6. Masahira N, Takebayashi H, Ono K, Watanabe K, Ding L, Furusho M, Ogawa Y, Nabeshima Y, Alvarezbuylla A, Shimizu K. Olig2-positive progenitors in the embryonic spinal cord give rise not only to motoneurons and oligodendrocytes, but also to a subset of astrocytes and ependymal cells. Dev Biol 2006, 293:358-369. 10.1016/j.ydbio.2006.02.029, 16581057.
7. Park H-C, Shin J, Appel B. Spatial and temporal regulation of ventral spinal cord precursor specification by Hedgehog signaling. Development 2004, 131:5959-5969. 10.1242/dev.01456, 15539490.
8. Zhou Q, Choi G, Anderson DJ. The bHLH transcription factor Olig2 promotes oligodendrocyte differentiation in collaboration with Nkx2.2. Neuron 2001, 31:791-807. 10.1016/S0896-6273(01)00414-7, 11567617.
9. Stolt CC. The Sox9 transcription factor determines glial fate choice in the developing spinal cord. Genes Dev 2003, 17:1677-1689. 10.1101/gad.259003, 196138, 12842915.
10. Deneen B, Ho R, Lukaszewicz A, Hochstim CJ, Gronostajski RM, Anderson DJ. The transcription factor NFIA controls the onset of gliogenesis in the developing spinal cord. Neuron 2006, 52:953-968. 10.1016/j.neuron.2006.11.019, 17178400.
11. Imayoshi I, Sakamoto M, Yamaguchi M, Mori K, Kageyama R. Essential roles of Notch signaling in maintenance of neural stem cells in developing and adult brains. J Neurosci 2010, 30:3489-3498. 10.1523/JNEUROSCI.4987-09.2010, 20203209.
12. La Pompa De JL, Wakeham A, Correia KM, Samper E, Brown S, Aguilera RJ, Nakano T, Honjo T, Mak TW, Rossant J, Conlon RA. Conservation of the Notch signalling pathway in mammalian neurogenesis. Development 1997, 124:1139-1148.
13. Chitnis A, Henrique D, Lewis J, Ish-Horowicz D, Kintner C. Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta. Nature 1995, 375:761-766. 10.1038/375761a0, 7596407.
14. Appel B, Eisen JS. Regulation of neuronal specification in the zebrafish spinal cord by Delta function. Development 1998, 125:371-380.
15. Park H-C, Appel B. Delta-Notch signaling regulates oligodendrocyte specification. Development 2003, 130:3747-3755. 10.1242/dev.00576, 12835391.
16. Itoh M, Kim C-H, Palardy G, Oda T, Jiang Y-J, Maust D, Yeo S-Y, Lorick K, Wright GJ, Ariza-McNaughton L, Weissman AM, Lewis J, Chandrasekharappa SC, Chitnis AB. Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta. Dev Cell 2003, 4:67-82. 10.1016/S1534-5807(02)00409-4, 12530964.
17. Appel B, Givan LA, Eisen JS. Delta-Notch signaling and lateral inhibition in zebrafish spinal cord development. BMC Dev Biol 2001, 1:13. 10.1186/1471-213X-1-13, 37243, 11495630.
18. Yang X, Tomita T, Wines-Samuelson M, Beglopoulos V, Tansey MUG, Kopan R, Shen J. Notch1 signaling Influences V2 interneuron and motor neuron development in the spinal cord. Dev Neurosci 2006, 28:102-117. 10.1159/000090757, 16508308.
19. Jandke A, Da Costa C, Sancho R, Nye E, Spencer-Dene B, Behrens A. The F-box protein Fbw7 is required for cerebellar development. Dev Biol 2011, 358:201-212. 10.1016/j.ydbio.2011.07.030, 21827743.
20. Hoeck JD, Jandke A, Blake SM, Nye E, Spencer-Dene B, Brandner S, Behrens A. Fbw7 controls neural stem cell differentiation and progenitor apoptosis via Notch and c-Jun. Nat Neurosci 2010, 13:1365-13651372. 10.1038/nn.2644, 20935640.
21. Matsumoto A, Onoyama I, Sunabori T, Kageyama R, Okano H, Nakayama KI. Fbxw7-dependent degradation of Notch is required for control of " stemness" and neuronal-glial differentiation in neural stem cells. J Biol Chem 2011, 286:13754-13764. 10.1074/jbc.M110.194936, 3075719, 21349854.
22. Park H. olig2 is required for Zebrafish primary motor neuron and oligodendrocyte development. Dev Biol 2002, 248:356-368. 10.1006/dbio.2002.0738, 12167410.
23. Hagedorn M, Delugin M, Abraldes I, Allain N, Belaud-Rotureau M-A, Turmo M, Prigent C, Loiseau H, Bikfalvi A, Javerzat S. FBXW7/hCDC4 controls glioma cell proliferation in vitro and is a prognostic marker for survival in glioblastoma patients. Cell Div 2007, 2:9. 10.1186/1747-1028-2-9, 1819378, 17326833.
24. Gu Z, Inomata K, Ishizawa K, Horii A. The FBXW7 beta-form is suppressed in human glioma cells. Biochem Biophys Res Commun 2007, 354:992-998. 10.1016/j.bbrc.2007.01.080, 17274947.
25. Ng PC, Henikoff S. Predicting deleterious amino acid substitutions. Genome Res 2001, 11:863-874. 10.1101/gr.176601, 311071, 11337480.
26. Ramensky V, Bork P, Sunyaev S. Human non-synonymous SNPs: server and survey. Nucleic Acids Res 2002, 30:3894-3900. 10.1093/nar/gkf493, 137415, 12202775.
27. Spruck CH, Strohmaier H, Sangfelt O, Müller HM, Hubalek M, Müller-Holzner E, Marth C, Widschwendter M, Reed SI. hCDC4 gene mutations in endometrial cancer. Cancer Res 2002, 62:4535-4539.
28. Matsumoto A, Onoyama I, Nakayama KI. Expression of mouse Fbxw7 isoforms is regulated in a cell cycle- or p53-dependent manner. Biochem Biophys Res Commun 2006, 350:114-119. 10.1016/j.bbrc.2006.09.003, 16989775.
29. Welcker M. A Nucleolar Isoform of the Fbw7 Ubiquitin Ligase Regulates c-Myc and Cell Size. Curr Biol 2004, 14:1852-1857. 10.1016/j.cub.2004.09.083, 15498494.
30. Almeida AD, Wise HM, Hindley CJ, Slevin MK, Hartley RS, Philpott A. The F-box protein Cdc4/Fbxw7 is a novel regulator of neural crest development in Xenopus laevis. Neural Dev 2010, 5:1. 10.1186/1749-8104-5-1, 2819241, 20047651.
31. Takada N, Kucenas S, Appel B. Sox10 is necessary for oligodendrocyte survival following axon wrapping. Glia 2010, 58:996-1006.
32. Pevny LH, Nicolis SK. Sox2 roles in neural stem cells. Int J Biochem Cell Biol 2010, 42:421-424. 10.1016/j.biocel.2009.08.018, 19733254.
33. Oberg C, Li J, Pauley A, Wolf E, Gurney M, Lendahl U. The Notch intracellular domain is ubiquitinated and negatively regulated by the mammalian Sel-10 homolog. J Biol Chem 2001, 276:35847-35853. 10.1074/jbc.M103992200, 11461910.
34. Wu G, Lyapina S, Das I, Li J, Gurney M, Pauley A, Chui I, Deshaies RJ, Kitajewski J. SEL-10 is an inhibitor of notch signaling that targets notch for ubiquitin-mediated protein degradation. Mol Cell Biol 2001, 21:7403-7415. 10.1128/MCB.21.21.7403-7415.2001, 99913, 11585921.
35. Gupta-Rossi N, Le Bail O, Gonen H, Brou C, Logeat F, Six E, Ciechanover A, Israël A. Functional interaction between SEL-10, an F-box protein, and the nuclear form of activated Notch1 receptor. J Biol Chem 2001, 276:34371-34378. 10.1074/jbc.M101343200, 11425854.
36. Parsons MJ, Pisharath H, Yusuff S, Moore JC, Siekmann AF, Lawson N, Leach SD. Notch-responsive cells initiate the secondary transition in larval zebrafish pancreas. Mech Dev 2009, 126:898-912. 10.1016/j.mod.2009.07.002, 19595765.
37. Park H-C, Shin J, Roberts RK, Appel B. Anolig2 reporter gene marks oligodendrocyte precursors in the postembryonic spinal cord of zebrafish. Dev Dyn 2007, 236:3402-3407. 10.1002/dvdy.21365, 17969181.
38. Geling A, Steiner H, Willem M, Bally-Cuif L, Haass C. A gamma-secretase inhibitor blocks Notch signaling in vivo and causes a severe neurogenic phenotype in zebrafish. EMBO Rep 2002, 3:688-694. 10.1093/embo-reports/kvf124, 1084181, 12101103.
39. Hubbard EJ, Wu G, Kitajewski J, Greenwald I. sel-10, a negative regulator of lin-12 activity in Caenorhabditis elegans, encodes a member of the CDC4 family of proteins. Genes Dev 1997, 11:3182-3193. 10.1101/gad.11.23.3182, 316751, 9389650.
40. Welcker M, Clurman BE. FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation. Nat Rev Cancer 2008, 8:83-93. 10.1038/nrc2290, 18094723.
41. Akhoondi S, Sun D, von der Lehr N, Apostolidou S, Klotz K, Maljukova A, Cepeda D, Fiegl H, Dafou D, Dofou D, Marth C, Mueller-Holzner E, Corcoran M, Dagnell M, Nejad SZ, Nayer BN, Zali MR, Hansson J, Egyhazi S, Petersson F, Sangfelt P, Nordgren H, Grander D, Reed SI, Widschwendter M, Sangfelt O, Spruck C. FBXW7/hCDC4 is a general tumor suppressor in human cancer. Cancer Res 2007, 67:9006-9012. 10.1158/0008-5472.CAN-07-1320, 17909001.
42. O'Neil J, Grim J, Strack P, Rao S, Tibbitts D, Winter C, Hardwick J, Welcker M, Meijerink JP, Pieters R, Draetta G, Sears R, Clurman BE, Look AT. FBW7 mutations in leukemic cells mediate NOTCH pathway activation and resistance to -secretase inhibitors. J Exp Med 2007, 204:1813-1824. 10.1084/jem.20070876, 2118656, 17646409.
43. Lai EC. Protein degradation: four E3s for the notch pathway. Curr Biol 2002, 12:R74-R78. 10.1016/S0960-9822(01)00679-0, 11818085.
44. Fior R, Fior R, Henrique D. " Notch-Off" : a perspective on the termination of Notch signalling. Int J Dev Biol 2002, 16:633-647.
45. Fortini ME. Notch signaling: the core pathway and its posttranslational regulation. Dev Cell 2009, 16:633-647. 10.1016/j.devcel.2009.03.010, 19460341.
46. Kopan R, Ilagan MXG. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 2009, 137:216-233. 10.1016/j.cell.2009.03.045, 2827930, 19379690.
47. Andersson ER, Sandberg R, Lendahl U. Notch signaling: simplicity in design, versatility in function. Development 2011, 138:3593-3612. 10.1242/dev.063610, 21828089.
48. Zhang H, Miller RH. Density-dependent feedback inhibition of oligodendrocyte precursor expansion. J Neurosci 1996, 16:6886-6895.
49. van Heyningen P, Calver AR, Richardson WD. Control of progenitor cell number by mitogen supply and demand. Curr Biol 2001, 11:232-241. 10.1016/S0960-9822(01)00075-6, 11250151.
50. Calver AR, Hall AC, Yu WP, Walsh FS, Heath JK, Betsholtz C, Richardson WD. Oligodendrocyte population dynamics and the role of PDGF in vivo. Neuron 1998, 20:869-882. 10.1016/S0896-6273(00)80469-9, 9620692.
51. Kirby BB, Takada N, Latimer AJ, Shin J, Carney TJ, Kelsh RN, Appel B. In vivo time-lapse imaging shows dynamic oligodendrocyte progenitor behavior during zebrafish development. Nat Neurosci 2006, 9:1506-1511. 10.1038/nn1803, 17099706.
52. Davis H, Lewis A, Spencer-Dene B, Tateossian H, Stamp G, Behrens A, Tomlinson I. FBXW7 mutations typically found in human cancers are distinct from null alleles and disrupt lung development. J Pathol 2011, 224:180-189. 10.1002/path.2874, 21503901.
53. Ge W, Martinowich K, Wu X, He F, Miyamoto A, Fan G, Weinmaster G, Sun YE. Notch signaling promotes astrogliogenesis via direct CSL-mediated glial gene activation. J Neurosci Res 2002, 69:848-860. 10.1002/jnr.10364, 12205678.
54. Grandbarbe L. Delta-Notch signaling controls the generation of neurons/glia from neural stem cells in a stepwise process. Development 2003, 130:1391-1402. 10.1242/dev.00374, 12588854.
55. Anthony TE. Brain lipid-binding protein is a direct target of Notch signaling in radial glial cells. Genes Dev 2005, 19:1028-1033. 10.1101/gad.1302105, 1091737, 15879553.
56. Namihira M, Kohyama J, Semi K, Sanosaka T, Deneen B, Taga T, Nakashima K. Committed neuronal precursors confer astrocytic potential on residual neural precursor cells. Dev Cell 2009, 16:245-255. 10.1016/j.devcel.2008.12.014, 19217426.
57. Scheer N, Groth A, Hans S, Campos-Ortega JA. An instructive function for Notch in promoting gliogenesis in the zebrafish retina. Development 2001, 128:1099-1107.
58. Satow T, Bae SK, Inoue T, Inoue C, Miyoshi G, Tomita K, Bessho Y, Hashimoto N, Kageyama R. The basic helix-loop-helix gene hesr2 promotes gliogenesis in mouse retina. J Neurosci 2001, 21:1265-1273.
59. Gaiano N, Nye J, Fishell G. Radial Glial Identity Is Promoted by Notch1 Signaling in the Murine Forebrain. Neuron 2000, 25:395-395404.
60. Park H-C, Boyce J, Shin J, Appel B. Oligodendrocyte specification in zebrafish requires notch-regulated cyclin-dependent kinase inhibitor function. J Neurosci 2005, 25:6836-6844. 10.1523/JNEUROSCI.0981-05.2005, 16033893.
61. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. Stages of embryonic development of the zebrafish. Dev Dyn 1995, 203:253-310. 10.1002/aja.1002030302, 8589427.
62. Shin J, Park H-C, Topczewska JM, Mawdsley DJ, Appel B. Neural cell fate analysis in zebrafish using olig2 BAC transgenics. Methods Cell Sci 2003, 25:7-14.
63. Solnica-Krezel L, Schier AF, Driever W. Efficient recovery of ENU-induced mutations from the zebrafish germline. Genetics 1994, 136:1401-1420. 1205920, 8013916.
64. Postlethwait JH, Talbot WS. Zebrafish genomics: from mutants to genes. Trends Genet 1997, 13:183-190. 10.1016/S0168-9525(97)01129-3, 9154001.
65. Brosamle C, Halpern M. Characterization of myelination in the developing zebrafish. Glia 2002, 39:45-57.
66. Hauptmann G, Gerster T. Multicolor whole-mount in situ hybridization. Methods Mol Biol 2000, 137:139-148.