Asymmetric cell division during neurogenesis in Drosophila and vertebrates

Mechanisms of Development

Volumn 120, Issue 11, 2003, Pages 1297-1309

  Wodarz, Andreas ^a   Huttner, Wieland B ^b  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

Author keywords

Asymmetric cell division; Drosophila; Neurogenesis; Stem cells; Vertebrates

Indexed keywords

CELL DIFFERENTIATION; CELL DIVISION; CELL FATE; DROSOPHILA; EMBRYO DEVELOPMENT; GLIA CELL; MITOSIS SPINDLE; MOLECULAR MECHANICS; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; REVIEW; STEM CELL; VERTEBRATE;

ANIMALIA; HEXAPODA; VERTEBRATA;

EID: 0242496395     PISSN: 09254773     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mod.2003.06.003     Document Type: Review

References (123)

1. Aaku-Saraste E., Hellwig A., Huttner W.B. Loss of occludin and functional tight junctions, but not ZO-1, during neural tube closure - remodeling of the neuroepithelium prior to neurogenesis. Dev. Biol. 180:1996;664-679.
2. Aaku-Saraste E., Oback B., Hellwig A., Huttner W.B. Neuroepithelial cells downregulate their plasma membrane polarity prior to neural tube closure and neurogenesis. Mech. Dev. 69:1997;71-81.
3. Albertson R., Doe C.Q. Dlg, Scrib and Lgl regulate neuroblast cell size and mitotic spindle asymmetry. Nat. Cell Biol. 5:2003;166-170.
4. Ashraf S.I., Ip Y.T. The Snail protein family regulates neuroblast expression of inscuteable and string, genes involved in asymmetry and cell division in Drosophila. Development. 128:2001;4757-4767.
5. Bachmann A., Schneider M., Theilenberg E., Grawe F., Knust E. Drosophila Stardust is a partner of Crumbs in the control of epithelial cell polarity. Nature. 414:2001;638-643.
6. Bellaiche Y., Gho M., Kaltschmidt J.A., Brand A.H., Schweisguth F. Frizzled regulates localization of cell-fate determinants and mitotic spindle rotation during asymmetric cell division. Nat. Cell Biol. 3:2001;50-57.
7. Bellaiche Y., Radovic A., Woods D.F., Hough C.D., Parmentier M.L., O'Kane C.J., et al. The Partner of Inscuteable/Discs-large complex is required to establish planar polarity during asymmetric cell division in Drosophila. Cell. 106:2001;355-366.
8. Betschinger J., Mechtler K., Knoblich J.A. The Par complex directs asymmetric cell division by phosphorylating the cytoskeletal protein Lgl. Nature. 422:2003;326-330.
9. Bilder D., Perrimon N. Localization of apical epithelial determinants by the basolateral PDZ protein Scribble. Nature. 403:2000;676-680.
10. Bilder D., Li M., Perrimon N. Cooperative regulation of cell polarity and growth by Drosophila tumor suppressors. Science. 289:2000;113-116.
11. Bilder D., Schober M., Perrimon N. Integrated activity of PDZ protein complexes regulates epithelial polarity. Nat. Cell Biol. 5:2003;53-58.
12. Broadus J., Doe C.Q. Extrinsic cues, intrinsic cues and microfilaments regulate asymmetric protein localization in Drosophila neuroblasts. Curr. Biol. 7:1997;827-835.
13. Cai Y., Chia W., Yang X. A family of snail-related zinc finger proteins regulates two distinct and parallel mechanisms that mediate Drosophila neuroblast asymmetric divisions. Embo J. 20:2001;1704-1714.
14. Cai Y., Yu F., Lin S., Chia W., Yang X. Apical complex genes control mitotic spindle geometry and relative size of daughter cells in Drosophila neuroblast and pI asymmetric divisions. Cell. 112:2003;51-62.
15. Campos-Ortega J.A. Early neurogenesis in Drosophila melanogaster. Bate M., Martinez-Arias A. The Development of Drosophila melanogaster. vol. 2:1993;1091-1129 Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
16. Campos-Ortega J.A., Hartenstein V. The Embryonic Development of Drosophila melanogaster. 1997;Springer, Berlin.
17. Cayouette M., Whitmore A.V., Jeffery G., Raff M. Asymmetric segregation of Numb in retinal development and the influence of the pigmented epithelium. J. Neurosci. 21:2001;5643-5651.
18. Chenn A., McConnell S.K. Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis. Cell. 82:1995;631-641.
19. Chenn A., Walsh C.A. Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science. 297:2002;365-369.
20. Chenn A., Zhang Y.A., Chang B.T., McConnell S.K. Intrinsic polarity of mammalian neuroepithelial cells. Mol. Cell. Neurosci. 11:1998;183-193.
21. Corbeil D., Röper K., Fargeas C.A., Joester A., Huttner W.B. Prominin: a story of cholesterol, plasma membrane protrusions and human pathology. Traffic. 2:2001;82-91.
22. Das T., Payer B., Cayouette M., Harris W.A. In vivo time-lapse imaging of cell divisions during neurogenesis in the developing zebrafish retina. Neuron. 37:2003;597-609.
23. Doe C.Q., Chu-LaGraff Q., Wright D.M., Scott M.P. The prospero gene specifies cell fates in the Drosophila central nervous system. Cell. 65:1991;451-464.
24. Dooley C.M., James J., McGlade C.J., Ahmad I. Involvement of numb in vertebrate retinal development: evidence for multiple roles of numb in neural differentiation and maturation. J. Neurobiol. 54:2003;313-325.
25. Estivill-Torrus G., Pearson H., van Heyningen V., Price D.J., Rashbass P. Pax6 is required to regulate the cell cycle and the rate of progression from symmetrical to asymmetrical division in mammalian cortical progenitors. Development. 129:2002;455-466.
26. Faulkner N.E., Dujardin D.L., Tai C.Y., Vaughan K.T., O'Connell C.B., Wang Y., Vallee R.B. A role for the lissencephaly gene LIS1 in mitosis and cytoplasmic dynein function. Nat. Cell Biol. 2:2000;784-791.
27. Fishell G., Kriegstein A.R. Neurons from radial glia: the consequences of asymmetric inheritance. Curr. Opin. Neurobiol. 13:2003;34-41.
28. Fotaki V., Dierssen M., Alcantara S., Martinez S., Marti E., Casas C., et al. Dyrk1A haploinsufficiency affects viability and causes developmental delay and abnormal brain morphology in mice. Mol. Cell. Biol. 22:2002;6636-6647.
29. Fuse N., Hisata K., Katzen A.L., Matsuzaki F. Heterotrimeric g proteins regulate daughter cell size asymmetry in Drosophila neuroblast divisions. Curr. Biol. 13:2003;947-954.
30. Geldmacher-Voss B., Reugels A.M., Pauls S., Campos-Ortega J. A 90° rotation of the mitotic spindle changes the orientation of mitoses of zebrafish neuroepithelial cells. Development. 130:(16):2003;3767-3780.
31. Gho M., Schweisguth F. Frizzled signalling controls orientation of asymmetric sense organ precursor cell divisions in Drosophila. Nature. 393:1998;178-181.
32. Gho M., Bellaiche Y., Schweisguth F. Revisiting the Drosophila microchaete lineage: a novel intrinsically asymmetric cell division generates a glial cell. Development. 126:1999;3573-3584.
33. Giansanti M.G., Gatti M., Bonaccorsi S. The role of centrosomes and astral microtubules during asymmetric division of Drosophila neuroblasts. Development. 128:2001;1137-1145.
34. Gonczy P., Grill S., Stelzer E.H., Kirkham M., Hyman A.A. Spindle positioning during the asymmetric first cell division of Caenorhabditis elegans embryos. Novartis Found. Symp. 237:2001;164-175. discussion 176-181.
35. Goodman C.S., Doe C.Q. Embryonic development of the Drosophila central nervous system. Bate M., Martinez-Arias A. The development of Drosophila melanogaster. vol. 2:1993;1131-1206 Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
36. Groszer M., Erickson R., Scripture-Adams D.D., Lesche R., Trumpp A., Zack J.A., et al. Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene in vivo. Science. 294:2001;2186-2189.
37. Guimera J., Casas C., Pucharcos C., Solans A., Domenech A., Planas A.M., et al. A human homologue of Drosophila minibrain (MNB) is expressed in the neuronal regions affected in Down syndrome and maps to the critical region. Hum. Mol. Genet. 5:1996;1305-1310.
38. Hämmerle B., Vera-Samper E., Speicher S., Arencibia R., Martinez S., Tejedor F.J. Mnb/Dyrk1A is transiently expressed and asymmetrically segregated in neural progenitor cells at the transition to neurogenic divisions. Dev. Biol. 246:2002;259-273.
39. Haydar T.F., Ang E. Jr., Rakic P. Mitotic spindle rotation and mode of cell division in the developing telencephalon. Proc. Natl Acad. Sci. USA. 100:(5):2003;2890-2895.
40. Heins N., Cremisi F., Malatesta P., Gangemi R.M., Corte G., Price J., et al. Emx2 promotes symmetric cell divisions and a multipotential fate in precursors from the cerebral cortex. Mol. Cell. Neurosci. 18:2001;485-502.
41. Ho C., Zhou J., Medina M., Goto T., Jacobson M., Bhide P.G., Kosik K.S. Delta-catenin is a nervous system-specific adherens junction protein which undergoes dynamic relocalization during development. J. Comp. Neurol. 420:2000;261-276.
42. Hong Y., Stronach B., Perrimon N., Jan L.Y., Jan Y.N. Drosophila Stardust interacts with Crumbs to control polarity of epithelia but not neuroblasts. Nature. 414:2001;634-638.
43. Hurd T.W., Gao L., Roh M.H., Macara I.G., Margolis B. Direct interaction of two polarity complexes implicated in epithelial tight junction assembly. Nat. Cell Biol. 5:2003;137-142.
44. Huttner W.B., Brand M. Asymmetric division and polarity of neuroepithelial cells. Curr. Opin. Neurobiol. 7:1997;29-39.
45. Iacopetti P., Michelini M., Stuckmann I., Oback B., Aaku-Saraste E., Huttner W.B. Expression of the antiproliferative gene TIS21 at the onset of neurogenesis identifies single neuroepithelial cells that switch from proliferative to neuron-generating division. Proc. Natl Acad. Sci. USA. 96:1999;4639-4644.
46. Jan Y.N., Jan L.Y. The peripheral nervous system. Bate M., Martinez-Arias A. The development of Drosophila melanogaster. vol. 2:1993;1207-1244 Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
47. Joberty G., Petersen C., Gao L., Macara I.G. The cell polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42. Nat. Cell Biol. 2:2000;531-539.
48. Johansson A., Driessens M., Aspenstrom P. The mammalian homologue of the Caenorhabditis elegans polarity protein PAR-6 is a binding partner for the &Rgr; GTPases cdc42 and rac1 [in process citation]. J. Cell Sci. 113:2000;3267-3275.
49. Johnson K., Wodarz A. A genetic hierarchy controlling cell polarity. Nat. Cell Biol. 5:2003;12-14.
50. Kaltschmidt J.A., Davidson C.M., Brown N.H., Brand A.H. Rotation and asymmetry of the mitotic spindle direct asymmetric cell division in the developing central nervous system. Nat. Cell Biol. 2:2000;7-12.
51. Knoblich J.A., Jan L.Y., Jan Y.N. The N terminus of the Drosophila Numb protein directs membrane association and actin-dependent asymmetric localization. Proc. Natl Acad. Sci. USA. 94:1997;13005-13010.
52. Kornack D.R., Rakic P. Radial and horizontal deployment of clonally related cells in the primate neocortex: relationship to distinct mitotic lineages. Neuron. 15:1995;311-321.
53. Kosodo Y., Röper K., Haubensak W., Corbeil D., Huttner W.B. Asymmetric distribution of the apical plasma membrane during neuron-generating divisions of mammlian neuroepithelial cells. Mol. Biol. Cell. 13:(Suppl.):2002;8a. 42nd ASCB Meeting, Abstr. #38.
54. Kraut R., Chia W., Jan L.Y., Jan Y.N., Knoblich J.A. Role of inscuteable in orienting asymmetric cell divisions in Drosophila. Nature. 383:1996;50-55.
55. Kuchinke U., Grawe F., Knust E. Control of spindle orientation in Drosophila by the Par-3-related PDZ-domain protein Bazooka. Curr. Biol. 8:1998;1357-1365.
56. Landrieu P., Goffinet A. Mitotic spindle fiber orientation in relation to cell migration in the neo-cortex of normal and reeler mouse. Neurosci. Lett. 13:1979;69-72.
57. Langman J., Guerrant R.L., Freeman B.G. Behavior of neuro-epithelial cells during closure of the neural tube. J. Comp. Neurol. 127:1966;399-411.
58. Lehman K., Rossi G., Adamo J.E., Brennwald P. Yeast homologues of tomosyn and lethal giant larvae function in exocytosis and are associated with the plasma membrane SNARE, Sec9. J. Cell Biol. 146:1999;125-140.
59. Li L., Vaessin H. Pan-neural Prospero terminates cell proliferation during Drosophila neurogenesis. Genes Dev. 14:2000;147-151.
60. Lin D., Edwards A.S., Fawcett J.P., Mbamalu G., Scott J.D., Pawson T. A mammalian Par-3-Par-6 complex implicated in CdC42/Rac1 and aPKC signalling and cell polarity. Nat. Cell Biol. 2:2000;540-547.
61. Lu B., Rothenberg M., Jan L.Y., Jan Y.N. Partner of Numb colocalizes with Numb during mitosis and directs Numb asymmetric localization in Drosophila neural and muscle progenitors. Cell. 95:1998;225-235.
62. Lu B., Ackerman L., Jan L.Y., Jan Y.N. Modes of protein movement that lead to the asymmetric localization of partner of Numb during Drosophila neuroblast division. Mol. Cell. 4:1999;883-891.
63. Lu B., Usui T., Uemura T., Jan L., Jan Y.N. Flamingo controls the planar polarity of sensory bristles and asymmetric division of sensory organ precursors in Drosophila. Curr. Biol. 9:1999;1247-1250.
64. Manabe N., Hirai S., Imai F., Nakanishi H., Takai Y., Ohno S. Association of ASIP/mPAR-3 with adherens junctions of mouse neuroepithelial cells. Dev. Dyn. 225:2002;61-69.
65. Mione M.C., Cavanagh J.F., Harris B., Parnavelas J.G. Cell fate specification and symmetrical/asymmetrical divisions in the developing cerebral cortex. J. Neurosci. 17:1997;2018-2029.
66. Miyata T., Kawaguchi A., Okano H., Ogawa M. Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron. 31:2001;727-741.
67. Müller H.A., Wieschaus E. Armadillo, bazooka, and stardust are critical for early stages in formation of the zonula adherens and maintenance of the polarized blastoderm epithelium in Drosophila. J. Cell Biol. 134:1996;149-163.
68. Murciano A., Zamora J., Lopez-Sanchez J., Frade J.M. Interkinetic nuclear movement may provide spatial clues to the regulation of neurogenesis. Mol. Cell. Neurosci. 21:2002;285-300.
69. Musch A., Cohen D., Yeaman C., Nelson W.J., Rodriguez-Boulan E., Brennwald P.J. Mammalian homolog of Drosophila tumor suppressor lethal (2) giant larvae interacts with basolateral exocytic machinery in Madin-Darby canine kidney cells. Mol. Biol. Cell. 13:2002;158-168.
70. Noctor S.C., Flint A.C., Weissman T.A., Dammerman R.S., Kriegstein A.R. Neurons derived from radial glial cells establish radial units in neocortex. Nature. 409:2001;714-720.
71. Noctor S.C., Flint A.C., Weissman T.A., Wong W.S., Clinton B.K., Kriegstein A.R. Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J. Neurosci. 22:2002;3161-3173.
72. Ohno S. Intercellular junctions and cellular polarity: the PAR-aPKC complex, a conserved core cassette playing fundamental roles in cell polarity. Curr. Opin. Cell Biol. 13:2001;641-648.
73. Ohshiro T., Yagami T., Zhang C., Matsuzaki F. Role of cortical tumour-suppressor proteins in asymmetric division of Drosophila neuroblast. Nature. 408:2000;593-596.
74. Olson E.C., Walsh C.A. Smooth, rough and upside-down neocortical development. Curr. Opin. Genet. Dev. 12:2002;320-327.
75. Parmentier M.L., Woods D., Greig S., Phan P.G., Radovic A., Bryant P., O'Kane C.J. Rapsynoid/Partner of inscuteable controls asymmetric division of larval neuroblasts in Drosophila. J. Neurosci. (Online). 20:2000;RC84.
76. Parnavelas J.G., Nadarajah B. Radial glial cells. are they really glia? Neuron. 31:2001;881-884.
77. Peng C.Y., Manning L., Albertson R., Doe C.Q. The tumour-suppressor genes lgl and dlg regulate basal protein targeting in Drosophila neuroblasts. Nature. 408:2000;596-600.
78. Petersen P.H., Zou K., Hwang J.K., Jan Y.N., Zhong W. Progenitor cell maintenance requires numb and numblike during mouse neurogenesis. Nature. 419:2002;929-934.
79. Petritsch C., Tavosanis G., Turck C.W., Jan L.Y., Jan Y.N. The Drosophila Myosin VI Jaguar is required for basal protein targeting and correct spindle orientation in mitotic neuroblasts. Dev. Cell. 4:2003;273-281.
80. Petronczki M., Knoblich J.A. DmPAR-6 directs epithelial polarity and asymmetric cell division of neuroblasts in Drosophila. Nat. Cell Biol. 3:2001;43-49.
81. Qian X., Goderie S.K., Shen Q., Stern J.H., Temple S. Intrinsic programs of patterned cell lineages in isolated vertebrate CNS ventricular zone cells. Development. 125:1998;3143-3152.
82. Qian X., Shen Q., Goderie S.K., He W., Capela A., Davis A.A., Temple S. Timing of CNS cell generation: a programmed sequence of neuron and glial cell production from isolated murine cortical stem cells. Neuron. 28:2000;69-80.
83. Qiu R.G., Abo A., Martin G.S. A human homolog of the C. elegans polarity determinant par-6 links rac and cdc42 to PKCzeta signaling and cell transformation [in process citation]. Curr. Biol. 10:2000;697-707.
84. Reid C.B., Tavazoie S.F., Walsh C.A. Clonal dispersion and evidence for asymmetric cell division in ferret cortex. Development. 124:1997;2441-2450.
85. Rhyu M.S., Jan L.Y., Jan Y.N. Asymmetric distribution of numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells [see comments]. Cell. 76:1994;477-491.
86. Roegiers F., Younger-Shepherd S., Jan L.Y., Jan Y.N. Bazooka is required for localization of determinants and controlling proliferation in the sensory organ precursor cell lineage in Drosophila. Proc. Natl Acad. Sci. USA. 98:2001;14469-14474.
87. Roegiers F., Younger-Shepherd S., Jan L.Y., Jan Y.N. Two types of asymmetric divisions in the Drosophila sensory organ precursor cell lineage. Nat. Cell Biol. 3:2001;58-67.
88. Roh M.H., Makarova O., Liu C.J., Shin K., Lee S., Laurinec S., et al. The Maguk protein, Pals1, functions as an adapter, linking mammalian homologues of Crumbs and Discs Lost. J. Cell Biol. 157:2002;161-172.
89. Röper K., Corbeil D., Huttner W.B. Retention of prominin in microvilli reveals distinct cholesterol-based lipid microdomains in the apical plasma membrane. Nat. Cell Biol. 2:2000;582-592.
90. Sauer F.C. Mitosis in the neural tube. J. Comp. Neurol. 62:1935;377-405.
91. Schaefer M., Shevchenko A., Knoblich J.A. A protein complex containing Inscuteable and the Galpha-binding protein Pins orients asymmetric cell divisions in Drosophila [see comments]. Curr. Biol. 10:2000;353-362.
92. Schaefer M., Petronczki M., Dorner D., Forte M., Knoblich J.A. Heterotrimeric g proteins direct two modes of asymmetric cell division in the Drosophila nervous system. Cell. 107:2001;183-194.
93. Schober M., Schaefer M., Knoblich J.A. Bazooka recruits Inscuteable to orient asymmetric cell divisions in Drosophila neuroblasts. Nature. 402:1999;548-551.
94. Shen Q., Temple S. Creating asymmetric cell divisions by skewing endocytosis. Sci. STKE. 2002:2002;PE52.
95. Shen Q., Zhong W., Jan Y.N., Temple S. Asymmetric Numb distribution is critical for asymmetric cell division of mouse cerebral cortical stem cells and neuroblasts. Development. 129:2002;4843-4853.
96. Shi S.H., Jan L.Y., Jan Y.N. Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI 3-kinase activity. Cell. 112:2003;63-75.
97. Shindoh N., Kudoh J., Maeda H., Yamaki A., Minoshima S., Shimizu Y., Shimizu N. Cloning of a human homolog of the Drosophila minibrain/rat Dyrk gene from 'the Down syndrome critical region' of chromosome 21. Biochem. Biophys. Res. Commun. 225:1996;92-99.
98. Silva A.O., Ercole C.E., McLoon S.C. Plane of cell cleavage and numb distribution during cell division relative to cell differentiation in the developing retina. J. Neurosci. 22:2002;7518-7525.
99. Simons K., Ikonen E. Functional rafts in cell membranes. Nature. 387:1997;569-572.
100. Smart I.H. Proliferative characteristics of the ependymal layer during the early development of the mouse neocortex: a pilot study based on recording the number, location and plane of cleavage of mitotic figures. J. Anat. 116:1973;67-91.
101. Song W.J., Sternberg L.R., Kasten-Sportes C., Keuren M.L., Chung S.H., Slack A.C., et al. Isolation of human and murine homologues of the Drosophila minibrain gene: human homologue maps to 21q22.2 in the Down syndrome 'critical region'. Genomics. 38:1996;331-339.
102. Spana E.P., Doe C.Q. The prospero transcription factor is asymmetrically localized to the cell cortex during neuroblast mitosis in Drosophila. Development. 121:1995;3187-3195.
103. Strand D., Jakobs R., Merdes G., Neumann B., Kalmes A., Heid H.W., et al. The Drosophila lethal(2)giant larvae tumor suppressor protein forms homo-oligomers and is associated with nonmuscle myosin II heavy chain. J. Cell Biol. 127:1994;1361-1373.
104. Stuckmann I., Weigmann A., Shevchenko A., Mann M., Huttner W.B. Ephrin B1 is expressed on neuroepithelial cells in correlation with neocortical neurogenesis. J. Neurosci. 21:2001;2726-2737.
105. Tanentzapf G., Tepass U. Interactions between the crumbs, lethal giant larvae and bazooka pathways in epithelial polarization. Nat. Cell Biol. 5:2003;46-52.
106. Tejedor F., Zhu X.R., Kaltenbach E., Ackermann A., Baumann A., Canal I., et al. minibrain: a new protein kinase family involved in postembryonic neurogenesis in Drosophila. Neuron. 14:1995;287-301.
107. Tio M., Udolph G., Yang X., Chia W. cdc2 links the Drosophila cell cycle and asymmetric division machineries. Nature. 409:2001;1063-1067.
108. Urbach R., Schnabel R., Technau G.M. The pattern of neuroblast formation, mitotic domains and proneural gene expression during early brain development in Drosophila. Development. 130:2003;3589-3606.
109. Vaessin H., Grell E., Wolff E., Bier E., Jan L.Y., Jan Y.N. Prospero is expressed in neuronal precursors and encodes a nuclear protein that is involved in the control of axonal outgrowth in Drosophila. Cell. 67:1991;941-953.
110. Wakamatsu Y., Maynard T.M., Jones S.U., Weston J.A. NUMB localizes in the basal cortex of mitotic avian neuroepithelial cells and modulates neuronal differentiation by binding to NOTCH-1. Neuron. 23:1999;71-81.
111. Weigmann A., Corbeil D., Hellwig A., Huttner W.B. Prominin, a novel microvilli-specific polytopic membrane protein of the apical surface of epithelial cells, is targeted to plasmalemmal protrusions of non-epithelial cells. Proc. Natl Acad. Sci. USA. 94:1997;12425-12430.
112. Wodarz A. Tumor suppressors: linking cell polarity and growth control. Curr. Biol. 10:2000;R624-R626.
113. Wodarz A. Cell polarity: no need to reinvent the wheel. Curr. Biol. 11:2001;R975-R978.
114. Wodarz A. Establishing cell polarity in development. Nat. Cell Biol. 4:2002;E39-E44.
115. Wodarz A., Ramrath A., Kuchinke U., Knust E. Bazooka provides an apical cue for Inscuteable localization in Drosophila neuroblasts. Nature. 402:1999;544-547.
116. Wodarz A., Ramrath A., Grimm A., Knust E. Drosophila atypical protein kinase C associates with Bazooka and controls polarity of epithelia and neuroblasts. J. Cell Biol. 150:2000;1361-1374.
117. Yu F., Morin X., Cai Y., Yang X., Chia W. Analysis of partner of inscuteable, a novel player of Drosophila asymmetric divisions, reveals two distinct steps in inscuteable apical localization. Cell. 100:2000;399-409.
118. Yu F., Ong C.T., Chia W., Yang X. Membrane targeting and asymmetric localization of Drosophila partner of inscuteable are discrete steps controlled by distinct regions of the protein. Mol. Cell. Biol. 22:2002;4230-4240.
119. Zhadanov A.B., Provance D.W. Jr., Speer C.A., Coffin J.D., Goss D., Blixt J.A., et al. Absence of the tight junctional protein AF-6 disrupts epithelial cell-cell junctions and cell polarity during mouse development. Curr. Biol. 9:1999;880-888.
120. Zhong W. Diversifying neural cells through order of birth and asymmetry of division. Neuron. 37:2003;11-14.
121. Zhong W., Jiang M.M., Schonemann M.D., Meneses J.J., Pedersen R.A., Jan L.Y., Jan Y.N. Mouse numb is an essential gene involved in cortical neurogenesis. Proc. Natl Acad. Sci. USA. 97:2000;6844-6849.
122. Zilian O., Saner C., Hagedorn L., Lee H.Y., Sauberli E., Suter U., et al. Multiple roles of mouse Numb in tuning developmental cell fates. Curr. Biol. 11:2001;494-501.
123. Zimmermann P., Meerschaert K., Reekmans G., Leenaerts I., Small J.V., Vandekerckhove J., et al. PIP(2)-PDZ domain binding controls the association of syntenin with the plasma membrane. Mol. Cell. 9:2002;1215-1225.