Asymmetric localization of numb:EGFP in dividing neuroepithelial cells during neurulation in Danio rerio

Developmental Dynamics

Volumn 235, Issue 4, 2006, Pages 934-948

  Reugels, Alexander M ^a   Boggetti, Barbara ^a   Scheer, Nico ^a,b   Campos Ortega, José A ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b Artemis Pharmaceuticals GmbH   (Germany)

Author keywords

Asymmetric localization; Danio rerio; Neuroepithelial polarity; Neurulation; Numb; Numblike; PRR; PTB domain; Spindle orientation; Zebrafish

Indexed keywords

AMINO ACID; CELL PROTEIN; ENHANCED GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; NUMB 1 PROTEIN; NUMB 3 PROTEIN; NUMB LIKE PROTEIN; NUMB PROTEIN; PHOSPHOTYROSINE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL DIVISION; CELL FATE; CELL MEMBRANE; CELL STRUCTURE; EMBRYO; MITOSIS SPINDLE; MOLECULAR CLONING; NEURAL TUBE; NEUROECTODERM; NEUROEPITHELIUM; NEURULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN POLYMORPHISM; ZEBRA FISH;

AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE; CELL POLARITY; CLONING, MOLECULAR; CONSERVED SEQUENCE; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; GENE DELETION; GREEN FLUORESCENT PROTEINS; INTRONS; JUVENILE HORMONES; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; MICROSCOPY, VIDEO; MITOTIC SPINDLE APPARATUS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; NEUROEPITHELIAL CELLS; PHYLOGENY; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY, AMINO ACID; ZEBRAFISH; ZEBRAFISH PROTEINS;

ANIMALIA; DANIO RERIO;

EID: 33645470190     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.20699     Document Type: Article

References (76)

1. Abascal F, Zardoya R, Posada D. 2005. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104-2105.
2. Artavanis-Tsakonas S, Rand MD, Lake RJ. 1999. Notch signaling: cell fate control and signal integration in development. Science 284:770-776.
3. Bass SH, Mulkerrin MG, Wells JA. 1991. A systematic mutational analysis of hormone-binding determinants in the human growth hormone receptor. Proc Natl Acad Sci USA 88:4498-502.
4. Bellaiche Y, Gho M, Kaltschmidt JA, Brand AH, Schweisguth F. 2001. Frizzled regulates localization of cell-fate determinants and mitotic spindle rotation during asymmetric cell division. Nat Cell Biol 3:50-57.
5. Berdnik D, Torok T, Gonzalez-Gaitan M, Knoblich JA. 2002. The endocytic protein alpha-Adaptin is required for numb-mediated asymmetric cell division in Drosophila. Dev Cell 3:221-231.
6. Bhalerao S, Berdnik D, Torok T, Knoblich JA. 2005. Localization-dependent and -independent roles of numb contribute to cell-fate specification in Drosophila. Curr Biol 15:1583-1590.
7. Brendel V, Bucher P, Nourbakhsh I, Blaisdell BE, Karlin S. 1992. Methods and algorithms for statistical analysis of protein sequences. Proc Natl Acad Sci USA 89:2002-2006.
8. Campos-Ortega JA. 1995. Genetic mechanisms of early neurogenesis in Drosophila melanogaster. Mol Neurobiol 10:75-89.
9. Cayouette M, Raff M. 2003. The orientation of cell division influences cell-fate choice in the developing mammalian retina. Development 130:2329-2339.
10. Cayouette M, Whitmore AV, Jeffery G, Raff M. 2001. Asymmetric segregation of numb in retinal development and the influence of the pigmented epithelium. J Neurosci 21:5643-5651.
11. Chan SL, Pedersen WA, Zhu H, Mattson MP. 2002. Numb modifies neuronal vulnerability to amyloid beta-peptide in an isoform-specific manner by a mechanism involving altered calcium homeostasis: implications for neuronal death in Alzheimer's disease. Neuromol Med 1:55-67.
12. Chien CT, Wang S, Rothenberg M, Jan LY, Jan YN. 1998. Numb-associated kinase interacts with the phosphotyrosine binding domain of Numb and antagonizes the function of Numb in vivo. Mol. Cell Biol. 18:598-607.
13. Concha ML, Adams, RJ. 1998. Oriented cell divisions and cellular morphogenesis in the zebrafish gastrula and neurula: a time-lapse analysis. Development 125: 983-994.
14. Cooper MS, D'Amico LA, Henry CA. 1999. Confocal microscopic analysis of morphogenetic movements. Methods Cell Biol 59:179-204.
15. Cormack BP, Valdivia RH, Falkow S. 1996. FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173:33-38.
16. Cunningham BC, Wells JA. 1989. High-resolution epitope mapping of hGH-receptor interactions by alanine-scanning mutagenesis. Science 244:1081-1085.
17. Das T, Payer B, Cayouette M, Harris WA. 2003. In vivo time-lapse imaging of cell divisions during neurogenesis in the developing zebrafish retina. Neuron 37:597-609.
18. Dho SE, Jacob S, Wolting CD, French MB, Rohrschneider LR, McGlade CJ. 1998. The mammalian numb phosphotyrosine-binding domain. Characterization of binding specificity and identification of a novel PDZ domain-containing numb binding protein, LNX. J Biol Chem 273: 9179-9187.
19. Dho SE, French MB, Woods SA, McGlade CJ. 1999. Characterization of four mammalian numb protein isoforms. Identification of cytoplasmic and membrane-associated variants of the phosphotyrosine binding domain. J Biol Chem 274:33097-33104.
20. Drummond A, Strimmer K. 2001. PAL: an object-oriented programming library for molecular evolution and phylogenetics. Bioinformatics 17:662-663.
21. Edlund T, Jessell TM. 1999. Progression from extrinsic to intrinsic signaling in cell fate specification: a view from the nervous system. Cell 96:211-224.
22. Frise E, Knoblich JA, Younger-Shepherd S, Jan LY, Jan YN. 1996. The Drosophila Numb protein inhibits signaling of the Notch receptor during cell-cell interaction in sensory organ lineage. Proc Natl Acad Sci USA 93:11925-11932.
23. Galtier N, Gouy M, Gautier C. 1996. SEAVIEW and PHYLO_WIN: Two graphic tools for sequence alignment and molecular phylogeny. Comp Appl Biosci 8:275-282.
24. Geldmacher-Voss B, Reugels AM, Pauls S, Campos-Ortega JA. 2003. A 90-degree rotation of the mitotic spindle changes the orientation of mitoses of zebrafish neuroepithelial cells. Development 130: 3767-3780.
25. Gho M, Schweisguth F. 1998. Frizzled signalling controls orientation of asymmetric sense organ precursor cell divisions in Drosophila. Nature 393:178-181.
26. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696-704.
27. Guo M, Jan LY, Jan YN. 1996. Control of daughter cell fates during asymmetric division: interaction of Numb and Notch. Neuron 17:27-41.
28. Hinds JW, Ruffett TL. 1971. Cell proliferation in the neural tube: an electron microscopic and golgi analysis in the mouse cerebral vesicle. Z Zellforsch Mikrosk Anat 115:226-264.
29. Hirata J, Nakagoshi H, Nabeshima Y, Matsuzaki F. 1995. Asymmetric segregation of the homeodomain protein Prospero during Drosophila development. Nature 377:627-630.
30. Horvitz HR, Herskowitz I. 1992. Mechanisms of asymmetric cell division: two Bs or not two Bs, that is the question. Cell 68:237-55.
31. Huang EJ, Li H, Tang AA, Wiggins AK, Neve RL, Zhong W, Jan LY, Jan YN. 2005. Targeted deletion of numb and numblike in sensory neurons reveals their essential functions in axon arborization. Genes Dev 19:138-151.
32. Hutterer A, Knoblich JA. 2005. Numb and alpha-Adaptin regulate Sanpodo endocytosis to specify cell fate in Drosophila external sensory organs. EMBO Rep 6: 836-842.
33. Jan YN, Jan LY. 1998. Asymmetric cell division. Nature 392:775-778.
34. Jones DT, Taylor WR, Thornton JM. 1992. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275-282.
35. Justice N, Roegiers F, Jan LY, Jan YN. 2003. Lethal giant larvae acts together with numb in notch inhibition and cell fate specification in the Drosophila adult sensory organ precursor lineage. Curr Biol 13:778-783.
36. Kaltschmidt JA, Davidson CM, Brown NH, Brand AH. 2000. Rotation and asymmetry of the mitotic spindle direct asymmetric cell division in the developing central nervous system. Nature Cell Biol 2:7-12.
37. Kimmel CB, Warga RM, Schilling TF. 1990. Origin and organization of the zebrafish fate map. Development 108:581-594.
38. Kimmel CB, Warga RM, Kane, DA. 1994. Cell cycles and clonal strings during formation of the zebrafish central nervous system. Development 120:265-276.
39. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. 1995. Stages of embryonic development of the zebrafish. Dev Dyn 203:253-310.
40. Knoblich JA, Jan LY, Jan YN. 1997. The N terminus of the Drosophila Numb protein directs membrane association and actin-dependent asymmetric localization. Proc Natl Acad Sci USA 94:13005-13010.
41. Kosodo Y, Roper K, Haubensak W, Marzesco AM, Corbeil D, Huttner WB. 2004. Asymmetric distribution of the apical plasma membrane during neurogenic divisions of mammalian neuroepithelial cells. EMBO J 2311:2314-2324.
42. Lennon G, Auffray C, Polymeropoulos M, Scares MB. 1996. The I.M.A.G.E. Consortium: an integrated molecular analysis of genomes and their expression. Genomics 33:151-152.
43. Letunic I, Copley RR, Schmidt S, Ciccarelli FD, Doerks T, Schultz J, Ponting CP, Bork P. 2004. SMART 4.0: towards genomic data integration. Nucleic Acids Res. 32:D142-144.
44. Li SC, Zwahlen C, Vincent SJ, McGlade CJ, Kay LE, Pawson T, Forman-Kay JD. 1998. Structure of a Numb PTB domain-peptide complex suggests a basis for diverse binding specificity. Nat Struct Biol 5:1075-1083.
45. Lu B, Rothenberg M, Jan LY, Jan YN. 1998. Partner of Numb colocalizes with Numb during mitosis and directs Numb asymmetric localization in Drosophila neural and muscle progenitors. Cell 95: 225-235.
46. Mayer B, Emery G, Berdnik D, Wirtz-Peitz F, Knoblich JA. 2005. Quantitative analysis of protein dynamics during asymmetric cell division. Curr Biol 15:1847-1854.
47. McConnell SK. 1991. The generation of neuronal diversity in the central nervous system. Annu Rev Neurosci 14:269-300.
48. O'Connor-Giles KM, Skeath JB. 2003. Numb inhibits membrane localization of Sanpodo, a four-pass transmembrane protein, to promote asymmetric divisions in Drosophila. Dev Cell 5:231-243.
49. Papan C, Campos-Ortega JA. 1994. On the formation of the neural keel and neural tube in the zebrafish Danio (Brachydanio) rerio. Roux's Arch Dev Biol 203: 178-186.
50. Papan C, Campos-Ortega, JA. 1997. A clonal analysis of spinal cord development in the zebrafish. Dev Genes Evol 207:71-81.
51. Pauls S, Geldmacher-Voss B, Campos-Ortega JA. 2001. A zebrafish histone variant H2A.F/Z and a transgenic H2A.F/Z-GFP fusion protein for in vivo studies of embryonic development. Dev Genes Evol 211:603-610.
52. Pedersen WA, Chan SL, Zhu H, Abdur-Rahman LA, Verdi JM, Mattson MP. 2002. Numb isoforms containing a short PTB domain promote neurotrophic factor-induced differentiation and neurotrophic factor withdrawal-induced death of PC12 Cells. J Neurochem 82:976-986.
53. Petersen PH, Zou K, Hwang JK, Jan YN, Zhong W. 2002. Progenitor cell maintenance requires numb and numblike during mouse neurogenesis. Nature 419:929-934.
54. Petersen PH, Zou K, Krauss S, Zhong W. 2004. Continuing role for mouse Numb and Numb1 in maintaining progenitor cells during cortical neurogenesis. Nat Neurosci 7:803-811.
55. Qin H, Percival-Smith A, Li C, Jia CY, Gloor G, Li SS. 2004. A novel transmembrane protein recruits numb to the plasma membrane during asymmetric cell division. J. Biol. Chem. 279:11304-11312.
56. Roegiers F, Younger-Shepherd S, Jan LY, Jan YN. 2001. Two types of asymmetric divisions in the Drosophila sensory organ precursor cell lineage. Nat Cell Biol 3:58-67.
57. Salcini AE, Confalonieri S, Doria M, Santolini E, Tassi E, Minenkova O, Cesareni G, Pelicci PG, Di Fiore PP. 1997. Binding specificity and in vivo targets of the EH domain, a novel protein-protein interaction module. Genes Dev 11:2239-2249.
58. Santolini E, Puri C, Salcini AE, Gagliani MC, Pelicci PG, Tacchetti C, Di Fiore PP. 2000. Numb is an endocytic protein. J Cell Biol 151:1345-1352.
59. Schmitz B, Papan C, Campos-Ortega JA. 1993. Neurulation in the anterior trunk region of the zebrafish Brachydanio rerio. Roux's Arch Dev Biol 202:250-259.
60. Schultz J, Milpetz F, Bork P, Ponting CP. 1998. SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci USA 95:5857-5864.
61. Shen Q, Zhong W, Jan YN, Temple S. 2002. Asymmetric Numb distribution is critical for asymmetric cell division of mouse cerebral cortical stem cells and neuroblasts. Development 129:4843-4853.
62. Smith CA, Dho SE, Donaldson J, Tepass U, McGlade CJ. 2004. The cell fate determinant numb interacts with EHD/Rme-1 family proteins and has a role in endocytic recycling. Mol Biol Cell 15:3698-3708.
63. Spana EP, Doe CQ. 1996. Numb antagonizes Notch signaling to specify sibling neuron cell fates. Neuron 17:21-26.
64. 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.
65. Uemura T, Shepherd S, Ackerman L, Jan LY, Jan YN. 1989. numb, a gene required in determination of cell fate during sensory organ formation in Drosophila embryos. Cell 58:349-360.
66. Verdi JM, Schmandt R, Bashirullah A, Jacob S, Salvino R, Craig CG, Program AE, Lipshitz HD, McGlade CJ. 1996. Mammalian NUMB is an evolutionarily conserved signaling adapter protein that specifies cell fate. Curr Biol 6:1134-1145.
67. Verdi JM, Bashirullah A, Goldhawk DE, Kubu CJ, Jamali M, Meakin SO, Lipshitz HD. 1999. Distinct human NUMB isoforms regulate differentiation vs. proliferation in the neuronal lineage. Proc Natl Acad Sci USA 96:10472-10476.
68. Wakamatsu Y, Maynard TM, Jones SU, Weston JA. 1999. NUMB localizes in the basal cortex of mitotic avian neuroepithelial cells and modulates neuronal differentiation by binding to NOTCH-1. Neuron 23:71-81.
69. Wakamatsu Y, Maynard TM, Weston JA. 2000. Fate determination of neural crest cells by NOTCH-mediated lateral inhibition and asymmetrical cell division during gangliogenesis. Development 127: 2811-2821.
70. Wells JA. 1991. Systematic mutational analyzes of protein-protein interfaces. Methods Enzymol 202:390-411.
71. Westerfield M. 1994. The zebrafish book: a guide for laboratory use of the zebrafish (Brachydanio rerio). Edition 2.1. Eugene: University of Oregon Press.
72. Yoshida T, Tokunaga A, Nakao K, Okano H. 2003. Distinct expression patterns of splicing isoforms of mNumb in the endocrine lineage of developing pancreas. Differentiation 71:486-495.
73. Zhong W, Feder JN, Jiang MM, Jan LY, Jan YN. 1996. Asymmetric localization of a mammalian numb homolog during mouse cortical neurogenesis. Neuron 17: 43-53.
74. Zhong W, Jiang MM, Weinmaster G, Jan LY, Jan YN. 1997. Differential expression of mammalian Numb, Numblike and Notch1 suggests distinct roles during mouse cortical neurogenesis. Development 124:1887-1897.
75. Zilian O, Saner C, Hagedorn L, Lee HY, Sauberli E, Suter U, Sommer L, Aguet M. 2001. Multiple roles of mouse Numb in tuning developmental cell fates. Curr Biol 11:494-501.
76. Zwahlen C, Li SC, Kay LE, Pawson T, Forman-Kay JD. 2000. Multiple modes of peptide recognition by the PTB domain of the cell fate determinant Numb. EMBO J 19:1505-1515.