An oblique view on the role of spindle orientation in vertebrate neurogenesis

[en] Neurogenesis is a dynamic process that produces a diverse number of glial and neural cell types from a limited number of neural stem cells throughout development and into adulthood. After an initial period of amplification through symmetric division, neural stem cells rely on asymmetric modes of division to self-renew while producing more committed progeny. Understanding the molecular mechanisms regulating the choice between symmetric and asymmetric modes of division is essential to understand human brain development and pathologies, and to explain the increasing cortical complexity observed in evolution. A popular model states the existence of a causal relationship between the orientation of the axis of division of stem cells and the fate of their progeny in many different tissues, but the validity of the model in neural stem cells is not clear. In this review, we briefly present the diversity of neural stem cells and intermediate progenitors in the developing central nervous system. We then draw a historic overview of the assumed causal relationship between spindle orientation and fate determination. We show how this prompted a search for regulators of spindle orientation, and present the current state of knowledge on the mechanism. Finally, we review data on the effect of defective spindle orientation and try to integrate conflicting observations by presenting alternative mechanisms that may regulate the choice between symmetric and asymmetric outcomes.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Peyre, Elise ; Université de Liège - ULiège > Giga - Neurosciences

Morin, Xavier; Ecole Normale Supérieure, Institut de Biologie de l’ENS, IBEN > NSERM, U1024 ; CNRS, UMR 8197

Language :

English

Title :

An oblique view on the role of spindle orientation in vertebrate neurogenesis

Publication date :

April 2012

Journal title :

Development, Growth and Differentiation

ISSN :

0012-1592

eISSN :

1440-169X

Publisher :

Blackwell Publishing, Tokyo, Japan

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 05 January 2015

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Bibliography

Aaku-Saraste, E., Hellwig, A. & Huttner, W. B. 1996. 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, 664-679.
Alexandre, P., Reugels, A. M., Barker, D., Blanc, E. & Clarke, J. D. 2010. Neurons derive from the more apical daughter in asymmetric divisions in the zebrafish neural tube. Nat. Neurosci. 13, 673-679.
Alkuraya, F. S., Cai, X., Emery, C., Mochida, G. H., Al-Dosari, M. S., Felie, J. M., Hill, R. S., Barry, B. J., Partlow, J. N., Gascon, G. G., Kentab, A., Jan, M., Shaheen, R., Feng, Y. & Walsh, C. A. 2011. Human mutations in NDE1 cause extreme microcephaly with lissencephaly [corrected]. Am. J. Hum. Genet. 88, 536-547.
Anderson, C. T. & Stearns, T. 2009. Centriole age underlies asynchronous primary cilium growth in mammalian cells. Curr. Biol. 19, 1498-1502.
Attardo, A., Calegari, F., Haubensak, W., Wilsch-Bräuninger, M. & Huttner, W. B. 2008. Live imaging at the onset of cortical neurogenesis reveals differential appearance of the neuronal phenotype in apical versus basal progenitor progeny. PLoS ONE 3, e2388.
Bakircioglu, M., Carvalho, O. P., Khurshid, M., Cox, J. J., Tuysuz, B., Barak, T., Yilmaz, S., Caglayan, O., Dincer, A., Nicholas, A. K., Quarrell, O., Springell, K., Karbani, G., Malik, S., Gannon, C., Sheridan, E., Crosier, M., Lisgo, S. N., Lindsay, S., Bilguvar, K., Gergely, F., Gunel, M. & Woods, C. G. 2011. The essential role of centrosomal NDE1 in human cerebral cortex neurogenesis. Am. J. Hum. Genet. 88, 523-535.
Boehlke, C., Kotsis, F., Patel, V., Braeg, S., Voelker, H., Bredt, S., Beyer, T., Janusch, H., Hamann, C., Godel, M., Muller, K., Herbst, M., Hornung, M., Doerken, M., Kottgen, M., Nitschke, R., Igarashi, P., Walz, G. & Kuehn, E. W. 2010. Primary cilia regulate mTORC1 activity and cell size through Lkb1. Nat. Cell Biol. 12, 1115-1122.
Buchman, J. J., Tseng, H. C., Zhou, Y., Frank, C. L., Xie, Z. & Tsai, L. H. 2010. Cdk5rap2 interacts with pericentrin to maintain the neural progenitor pool in the developing neocortex. Neuron 66, 386-402.
Bultje, R. S., Castaneda-Castellanos, D. R., Jan, L. Y., Jan, Y. N., Kriegstein, A. R. & Shi, S. H. 2009. Mammalian Par3 regulates progenitor cell asymmetric division via notch signaling in the developing neocortex. Neuron 63, 189-202.
Busson, S., Dujardin, D., Moreau, A., Dompierre, J. & De Mey, J. R. 1998. Dynein and dynactin are localized to astral microtubules and at cortical sites in mitotic epithelial cells. Curr. Biol. 8, 541-544.
Cappello, S., Attardo, A., Wu, X., Iwasato, T., Itohara, S., Wilsch-Brauninger, M., Eilken, H. M., Rieger, M. A., Schroeder, T. T., Huttner, W. B., Brakebusch, C. & Gotz, M. 2006. The Rho-GTPase cdc42 regulates neural progenitor fate at the apical surface. Nat. Neurosci. 9, 1099-1107.
Cayouette M, R. M. 2003. The orientation of cell division influences cell-fate choice in the developing mammalian retina. Development 130, 2329-2339.
Cayouette, M., Whitmore, A. V., Jeffery, G. & Raff, M. 2001. Asymmetric segregation of Numb in retinal development and the influence of the pigmented epithelium. J. Neurosci. 21, 5643-5651.
Chenn, A. & Mcconnell, S. K. 1995. Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis. Cell 82, 631-641.
Costa, M. R., Wen, G., Lepier, A., Schroeder, T. & Gotz, M. 2008. Par-complex proteins promote proliferative progenitor divisions in the developing mouse cerebral cortex. Development 135, 11-22.
Cox, J., Jackson, A. P., Bond, J. & Woods, C. G. 2006. What primary microcephaly can tell us about brain growth. Trends. Mol. Med. 12, 358-366.
Culurgioni, S., Alfieri, A., Pendolino, V., Laddomada, F. & Mapelli, M. 2011. Inscuteable and NuMA proteins bind competitively to Leu-Gly-Asn repeat-enriched protein (LGN) during asymmetric cell divisions. Proc. Natl Acad. Sci. USA 108, 20998-21003.
Das, T., Payer, B., Cayouette, M. & Harris, W. A. 2003. In vivo time-lapse imaging of cell divisions during neurogenesis in the developing zebrafish retina. Neuron 37, 597-609.
Durgan, J., Kaji, N., Jin, D. & Hall, A. 2011. Par6B and atypical PKC regulate mitotic spindle orientation during epithelial morphogenesis. J. Biol. Chem. 286, 12461-12474.
Englund, C., Fink, A., Lau, C., Pham, D., Daza, R. A. M., Bulfone, A., Kowalczyk, T. & Hevner, R. F. 2005. Pax6, Tbr2 & Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells & postmitotic neurons in developing neocortex. Neurosci. J. 25, 247-251.
Farkas, L. M., Haffner, C., Giger, T., Khaitovich, P., Nowick, K., Birchmeier, C., Paabo, S. & Huttner, W. B. 2008. Insulinoma-associated 1 has a panneurogenic role and promotes the generation and expansion of basal progenitors in the developing mouse neocortex. Neuron 60, 40-55.
Faulkner, N. E., Dujardin, D. L., Tai, C. Y., Vaughan, K. T., O'connell, C. B., Wang, Y. & Vallee, R. B. 2000. A role for the lissencephaly gene LIS1 in mitosis and cytoplasmic dynein function. Nat. Cell Biol. 2, 784-791.
Feng, Y. & Walsh, C. A. 2004. Mitotic spindle regulation by Nde1 controls cerebral cortical size. Neuron 44, 279-293.
Fietz, S. A., Kelava, I., Vogt, J., Wilsch-Brauninger, M., Stenzel, D., Fish, J. L., Corbeil, D., Riehn, A., Distler, W., Nitsch, R. & Huttner, W. B. 2010. OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling. Nat. Neurosci. 13, 690-699.
Fish, J. L., Dehay, C., Kennedy, H. & Huttner, W. B. 2008. Making bigger brains-the evolution of neural-progenitor-cell division. J. Cell Sci. 121, 2783-2793.
Fish, J. L., Kosodo, Y., Enard, W., Paabo, S. & Huttner, W. B. 2006. Aspm specifically maintains symmetric proliferative divisions of neuroepithelial cells. Proc. Natl Acad. Sci. USA 103, 10438-10443.
Gaiano, N. & Fishell, G. 2002. The role of notch in promoting glial and neural stem cell fates. Annu. Rev. Neurosci. 25, 471-490.
Gal, J. S., Morozov, Y. M., Ayoub, A. E., Chatterjee, M., Rakic, P. & Haydar, T. F. 2006. Molecular and morphological heterogeneity of neural precursors in the mouse neocortical proliferative zones. J. Neurosci. 26, 1045-1056.
Garcia-Moreno, F., Vasistha, N. A., Trevia, N., Bourne, J. A. & Molnar, Z. 2011. Compartmentalization of cerebral cortical germinal zones in a lissencephalic primate and gyrencephalic rodent. Cereb. Cortex 22, 482-492.
Gauthier-Fisher, A., Lin, D. C., Greeve, M., Kaplan, D. R., Rottapel, R. & Miller, F. D. 2009. Lfc and Tctex-1 regulate the genesis of neurons from cortical precursor cells. Nat. Neurosci. 12, 735-744.
Ge, X., Frank, C. L., Calderon De Anda, F. & Tsai, L. H. 2010. Hook3 interacts with PCM1 to regulate pericentriolar material assembly and the timing of neurogenesis. Neuron 65, 191-203.
Godin, J. D., Colombo, K., Molina-Calavita, M., Keryer, G., Zala, D., Charrin, B. C., Dietrich, P., Volvert, M. L., Guillemot, F., Dragatsis, I., Bellaiche, Y., Saudou, F., Nguyen, L. & Humbert, S. 2010. Huntingtin is required for mitotic spindle orientation and mammalian neurogenesis. Neuron 67, 392-406.
Gonczy, P. 2008. Mechanisms of asymmetric cell division: flies and worms pave the way. Nat. Rev. Mol. Cell Biol. 9, 355-366.
Gotz, M. & Huttner, W. B. 2005. The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 6, 777-788.
Gruber, R., Zhou, Z., Sukchev, M., Joerss, T., Frappart, P. O. & Wang, Z. Q. 2011. MCPH1 regulates the neuroprogenitor division mode by coupling the centrosomal cycle with mitotic entry through the Chk1-Cdc25 pathway. Nat. Cell Biol. 13, 1325-1334.
Hansen, D. V., Lui, J. H., Parker, P. R. & Kriegstein, A. R. 2010. Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 464, 554-561.
Hao, Y., Du, Q., Chen, X., Zheng, Z., Balsbaugh, J. L., Maitra, S., Shabanowitz, J., Hunt, D. F. & Macara, I. G. 2010. Par3 controls epithelial spindle orientation by aPKC-mediated phosphorylation of apical pins. Curr. Biol. 20, 1809-1818.
Haubensak, W., Attardo, A., Denk, W. & Huttner, W. B. 2004. Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc. Natl Acad. Sci. USA 101, 3196-3201.
Haydar, T. F., Ang, E. Jr & Rakic, P. 2003. Mitotic spindle rotation and mode of cell division in the developing telencephalon. Proc. Natl Acad. Sci. USA 100, 2890-2895.
Hirata, J., Nakagoshi, H., Nabeshima, Y. & Matsuzaki, F. 1995. Asymmetric segregation of the homeodomain protein Prospero during Drosophila development. Nature 377, 627-630.
Ho, C., Zhou, J., Medina, M., Goto, T., Jacobson, M., Bhide, P. G. & Kosik, K. S. 2000. Delta-catenin is a nervous system-specific adherens junction protein which undergoes dynamic relocalization during development. J. Comp. Neurol. 420, 261-276.
Hockfield, S. & Mckay, R. D. 1985. Identification of major cell classes in the developing mammalian nervous system. J. Neurosci. 5, 3310-3328.
Huttner, W. B. & Brand, M. 1997. Asymmetric division and polarity of neuroepithelial cells. Curr. Opin. Neurobiol. 7, 29-39.
Ishibashi, M., Ang, S. L., Shiota, K., Nakanishi, S., Kageyama, R. & Guillemot, F. 1995. Targeted disruption of mammalian hairy and enhancer of split homolog-1 (HES-1) leads to up-regulation of neural helix-loop-helix factors, premature neurogenesis, and severe neural tube defects. Genes Dev. 9, 3136-3148.
Izaki, T., Kamakura, S., Kohjima, M. & Sumimoto, H. 2006. Two forms of human Inscuteable-related protein that links Par3 to the Pins homologues LGN and AGS3. Biochem. Biophys. Res. Commun. 341, 1001-1006.
Jaffe, A. B., Kaji, N., Durgan, J. & Hall, A. 2008. Cdc42 controls spindle orientation to position the apical surface during epithelial morphogenesis. J. Cell Biol. 183, 625-633.
Januschke, J., Llamazares, S., Reina, J. & Gonzalez, C. 2011. Drosophila neuroblasts retain the daughter centrosome. Nat. Commun. 2, 243.
Joberty, G., Petersen, C., Gao, L. & Macara, I. G. 2000. The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42. Nat. Cell Biol. 2, 531-539.
Kardon, J. R. & Vale, R. D. 2009. Regulators of the cytoplasmic dynein motor. Nat. Rev. Mol. Cell Biol. 10, 854-865.
Kelava, I., Reillo, I., Murayama, A. Y., Kalinka, A. T., Stenzel, D., Tomancak, P., Matsuzaki, F., Lebrand, C., Sasaki, E., Schwamborn, J. C., Okano, H., Huttner, W. B. & Borrell, V. 2011. Abundant occurrence of basal radial glia in the subventricular zone of embryonic neocortex of a lissencephalic primate, the common marmoset Callithrix jacchus. Cereb. Cortex 22, 469-481.
Kiyomitsu, T., Murakami, H. & Yanagida, M. 2011. Protein interaction domain mapping of human kinetochore protein Blinkin reveals a consensus motif for binding of spindle assembly checkpoint proteins Bub1 and BubR1. Mol. Cell Biol. 31, 998-1011.
Knoblich, J. A., Jan, L. Y. & Jan, Y. N. 1995. Asymmetric segregation of Numb and Prospero during cell division. Nature 377, 624-627.
Konno, D., Shioi, G., Shitamukai, A., Mori, A., Kiyonari, H., Miyata, T. & Matsuzaki, F. 2008. Neuroepithelial progenitors undergo LGN-dependent planar divisions to maintain self-renewability during mammalian neurogenesis. Nat. Cell Biol. 10, 93-101.
Kosodo, Y., Roper, K., Haubensak, W., Marzesco, A. M., Corbeil, D. & Huttner, W. B. 2004. Asymmetric distribution of the apical plasma membrane during neurogenic divisions of mammalian neuroepithelial cells. EMBO J. 23, 2314-2324.
Kosodo, Y., Toida, K., Dubreuil, V., Alexandre, P., Schenk, J., Kiyokage, E., Attardo, A., Mora-Bermudez, F., Arii, T., Clarke, J. D. & Huttner, W. B. 2008. Cytokinesis of neuroepithelial cells can divide their basal process before anaphase. EMBO J. 27, 3151-3163.
Langman, J., Guerrant, R. L. & Freeman, B. G. 1966. Behavior of neuro-epithelial cells during closure of the neural tube. J. Comp. Neurol. 127, 399-411.
Lechler, T. & Fuchs, E. 2005. Asymmetric cell divisions promote stratification and differentiation of mammalian skin. Nature 437, 275-280.
Lin, D., Edwards, A. S., Fawcett, J. P., Mbamalu, G., Scott, J. D. & Pawson, T. 2000. A mammalian PAR-3-PAR-6 complex implicated in Cdc42/Rac1 and aPKC signalling and cell polarity. Nat. Cell Biol. 2, 540-547.
Lizarraga, S. B., Margossian, S. P., Harris, M. H., Campagna, D. R., Han, A. P., Blevins, S., Mudbhary, R., Barker, J. E., Walsh, C. A. & Fleming, M. D. 2010. Cdk5rap2 regulates centrosome function and chromosome segregation in neuronal progenitors. Development 137, 1907-1917.
Loulier, K., Lathia, J. D., Marthiens, V., Relucio, J., Mughal, M. R., Tang, S. C., Coksaygan, T., Hall, P. E., Chigurupati, S., Patton, B., Colognato, H., Rao, M. S., Mattson, M. P., Haydar, T. F. & Ffrench-Constant, C. 2009. Beta1 integrin maintains integrity of the embryonic neocortical stem cell niche. PLoS Biol. 7, e1000176.
Lui, J. H., Hansen, D. V. & Kriegstein, A. R. 2011. Development and evolution of the human neocortex. Cell 146, 18-36.
Luxenburg, C., Pasolli, H. A., Williams, S. E. & Fuchs, E. 2011. Developmental roles for Srf, cortical cytoskeleton and cell shape in epidermal spindle orientation. Nat. Cell Biol. 13, 203-214.
Mahmood, S., Ahmad, W. & Hassan, M. J. 2011. Autosomal recessive primary microcephaly (MCPH): clinical manifestations, genetic heterogeneity and mutation continuum. Orphanet. J. Rare Dis. 6, 39.
Marthiens, V. & Ffrench-Constant, C. 2009. Adherens junction domains are split by asymmetric division of embryonic neural stem cells. EMBO Rep. 10, 515-520.
Martin, A. H. 1967. Significance of mitotic spindle fibre orientation in the neural tube. Nature 216, 1133-1134.
Mcconnell, S. K. 1995. Constructing the cerebral cortex: neurogenesis and fate determination. Neuron 15, 761-768.
Merdes, A., Heald, R., Samejima, K., Earnshaw, W. C. & Cleveland, D. W. 2000. Formation of spindle poles by dynein/dynactin-dependent transport of NuMA. J. Cell Biol. 149, 851-862.
Merdes, A., Ramyar, K., Vechio, J. D. & Cleveland, D. W. 1996. A complex of NuMA and cytoplasmic dynein is essential for mitotic spindle assembly. Cell 87, 447-458.
Merkle, F. T., Tramontin, A. D., Garcia-Verdugo, J. M. & Alvarez-Buylla, A. 2004. Radial glia give rise to adult neural stem cells in the subventricular zone. Proc. Natl Acad. Sci. USA 101, 17528-17532.
Misson, J. P., Austin, C. P., Takahashi, T., Cepko, C. L. & Caviness, V. S. Jr. 1991. The alignment of migrating neural cells in relation to the murine neopallial radial glial fiber system. Cereb. Cortex 1, 221-229.
Miyata, T., Kawaguchi, A., Okano, H. & Ogawa, M. 2001. Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31, 727-741.
Miyata, T., Kawaguchi, A., Saito, K., Kawano, M., Muto, T. & Ogawa, M. 2004. Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 131, 3133-3145.
Morin, X. & Bellaïche, Y. 2011. Mitotic spindle orientation in asymmetric and symmetric cell divisions during animal development. Dev. Cell 21, 102-119.
Morin, X., Jaouen, F. & Durbec, P. 2007. Control of planar divisions by the G-protein regulator LGN maintains progenitors in the chick neuroepithelium. Nat. Neurosci. 10, 1440-1448.
Nguyen-Ngoc, T., Afshar, K. & Gonczy, P. 2007. Coupling of cortical dynein and G alpha proteins mediates spindle positioning in Caenorhabditis elegans. Nat. Cell Biol. 9, 1294-1302.
Nigg, E. A. & Stearns, T. 2011. The centrosome cycle: centriole biogenesis, duplication and inherent asymmetries. Nat. Cell Biol. 13, 1154-1160.
Noctor, S. C., Flint, A. C., Weissman, T. A., Dammerman, R. S. & Kriegstein, A. R. 2001. Neurons derived from radial glial cells establish radial units in neocortex. Nature 409, 714-720.
Noctor, S. C., Martinez-Cerdeno, V., Ivic, L. & Kriegstein, A. R. 2004. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7, 136-144.
Noctor, S. C., Martinez-Cerdeno, V. & Kriegstein, A. R. 2008. Distinct behaviors of neural stem and progenitor cells underlie cortical neurogenesis. J. Comp. Neurol. 508, 28-44.
Ochiai, W., Nakatani, S., Takahara, T., Kainuma, M., Masaoka, M., Minobe, S., Namihira, M., Nakashima, K., Sakakibara, A., Ogawa, M. & Miyata, T. 2009. Periventricular notch activation and asymmetric Ngn2 and Tbr2 expression in pair-generated neocortical daughter cells. Mol. Cell. Neurosci. 40, 225-233.
Pawlisz, A. S., Mutch, C., Wynshaw-Boris, A., Chenn, A., Walsh, C. A. & Feng, Y. 2008. Lis1-Nde1-dependent neuronal fate control determines cerebral cortical size and lamination. Hum. Mol. Genet. 17, 2441-2455.
Pease, J. C. & Tirnauer, J. S. 2011. Mitotic spindle misorientation in cancer-out of alignment and into the fire. J. Cell Sci. 124, 1007-1016.
Peyre, E., Jaouen, F., Saadaoui, M., Haren, L., Merdes, A., Durbec, P. & Morin, X. 2011. A lateral belt of cortical LGN and NuMA guides mitotic spindle movements and planar division in neuroepithelial cells. J. Cell Biol. 193, 141-154.
Pixley, S. K. & De Vellis, J. 1984. Transition between immature radial glia and mature astrocytes studied with a monoclonal antibody to vimentin. Brain Res. 317, 201-209.
Poggi, L., Vitorino, M., Masai, I. & Harris, W. A. 2005. Influences on neural lineage and mode of division in the zebrafish retina in vivo. J. Cell Biol. 171, 991-999.
Pontious, A., Kowalczyk, T., Englund, C. & Hevner, R. F. 2008. Role of intermediate progenitor cells in cerebral cortex development. Dev. Neurosci. 30, 24-32.
Postiglione, M. P., Juschke, C., Xie, Y., Haas, G. A., Charalambous, C. & Knoblich, J. A. 2011. Mouse inscuteable induces apical-basal spindle orientation to facilitate intermediate progenitor generation in the developing neocortex. Neuron 72, 269-284.
Poulson, N. D. & Lechler, T. 2010. Robust control of mitotic spindle orientation in the developing epidermis. J. Cell Biol. 191, 915-922.
Rakic, P. 1971. Guidance of neurons migrating to the fetal monkey neocortex. Brain Res. 33, 471-476.
Rakic, P. 1995. A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. Trends Neurosci. 18, 383-388.
Rasin, M. R., Gazula, V. R., Breunig, J. J., Kwan, K. Y., Johnson, M. B., Liu-Chen, S., Li, H. S., Jan, L. Y., Jan, Y. N., Rakic, P. & Sestan, N. 2007. Numb and Numbl are required for maintenance of cadherin-based adhesion and polarity of neural progenitors. Nat. Neurosci. 10, 819-827.
Redemann, S., Pecreaux, J., Goehring, N. W., Khairy, K., Stelzer, E. H., Hyman, A. A. & Howard, J. 2010. Membrane invaginations reveal cortical sites that pull on mitotic spindles in one-cell C. elegans embryos. PLoS ONE 5, e12301.
Reillo, I., De Juan Romero, C., Garcia-Cabezas, M. A. & Borrell, V. 2011. A role for intermediate radial glia in the tangential expansion of the Mammalian cerebral cortex. Cereb. Cortex 21, 1674-1694.
Rhyu, M. S., Jan, L. Y. & Jan, Y. N. 1994. Asymmetric distribution of numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells. Cell 76, 477-491.
Roszko, I., Afonso, C., Henrique, D. & Mathis, L. 2006. Key role played by RhoA in the balance between planar and apico-basal cell divisions in the chick neuroepithelium. Dev. Biol. 298, 212-224.
Sans, N., Wang, P. Y., Du, Q., Petralia, R. S., Wang, Y. X., Nakka, S., Blumer, J. B., Macara, I. G. & Wenthold, R. J. 2005. mPins modulates PSD-95 and SAP102 trafficking and influences NMDA receptor surface expression. Nat. Cell Biol. 7, 1179-1190.
Schaefer, M., Shevchenko, A. & Knoblich, J. A. 2000. A protein complex containing Inscuteable and the Galpha-binding protein pins orients asymmetric cell divisions in Drosophila. Curr. Biol. 10, 353-362.
Schober, M., Schaefer, M. & Knoblich, J. A. 1999. Bazooka recruits Inscuteable to orient asymmetric cell divisions in Drosophila neuroblasts. Nature 402, 548-551.
Schwamborn, J. C., Berezikov, E. & Knoblich, J. A. 2009. The TRIM-NHL protein TRIM32 activates microRNAs and prevents self-renewal in mouse neural progenitors. Cell 136, 913-925.
Shimojo, H., Ohtsuka, T. & Kageyama, R. 2008. Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron 58, 52-64.
Shitamukai, A., Konno, D. & Matsuzaki, F. 2011. Oblique radial glial divisions in the developing mouse neocortex induce self-renewing progenitors outside the germinal zone that resemble primate outer subventricular zone progenitors. J. Neurosci. 31, 3683-3695.
Siegrist, S. E. & Doe, C. Q. 2005. Microtubule-induced Pins/Galphai cortical polarity in Drosophila neuroblasts. Cell 123, 1323-1335.
Smart, I. H. 1973. 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, 67-91.
Spana, E. P. & Doe, C. Q. 1995. The prospero transcription factor is asymmetrically localized to the cell cortex during neuroblast mitosis in Drosophila. Development 121, 3187-3195.
Spana, E. P. & Doe, C. Q. 1996. Numb antagonizes Notch signaling to specify sibling neuron cell fates. Neuron 17, 21-26.
Spana, E. P., Kopczynski, C., Goodman, C. S. & Doe, C. Q. 1995. Asymmetric localization of numb autonomously determines sibling neuron identity in the Drosophila CNS. Development 121, 3489-3494.
Stancik, E. K., Navarro-Quiroga, I., Sellke, R. & Haydar, T. F. 2010. Heterogeneity in ventricular zone neural precursors contributes to neuronal fate diversity in the postnatal neocortex. J. Neurosci. 30, 7028-7036.
Sun, Y., Goderie, S. K. & Temple, S. 2005. Asymmetric distribution of EGFR receptor during mitosis generates diverse CNS progenitor cells. Neuron 45, 873-886.
Thornton, G. K. & Woods, C. G. 2009. Primary microcephaly: do all roads lead to Rome? Trends Genet. 25, 501-510.
Van der Voet, H., Berends, C. W. H., Perreault, A., Nguyen-Ngoc, T., Gönczy, P., Vidal, M., Boxem, M. & van den Heuvel, S. 2009. NuMA-related LIN-5, ASPM-1, calmodulin and dynein promote meiotic spindle rotation independently of cortical LIN-5/GPR/Gα. Nat. Cell Biol. 11, 269-277.
Vilas-Boas, F., Fior, R., Swedlow, J. R., Storey, K. G. & Henrique, D. 2011. A novel reporter of notch signalling indicates regulated and random notch activation during vertebrate neurogenesis. BMC Biol. 9, 58.
Wang, X., Lui, J. H. & Kriegstein, A. R. 2011a. Orienting fate: spatial regulation of neurogenic divisions. Neuron 72, 191-193.
Wang, X., Tsai, J. W., Imai, J. H., Lian, W. N., Vallee, R. B. & Shi, S. H. 2009. Asymmetric centrosome inheritance maintains neural progenitors in the neocortex. Nature 461, 947-955.
Wang, X., Tsai, J. W., Lamonica, B. & Kriegstein, A. R. 2011b. A new subtype of progenitor cell in the mouse embryonic neocortex. Nat. Neurosci. 14, 555-561.
Wilcock, A. C., Swedlow, J. R. & Storey, K. G. 2007. Mitotic spindle orientation distinguishes stem cell and terminal modes of neuron production in the early spinal cord. Development 134, 1943-1954.
Williams, S. E., Beronja, S., Pasolli, H. A. & Fuchs, E. 2011. Asymmetric cell divisions promote Notch-dependent epidermal differentiation. Nature 470, 353-358.
Wilsch-Brauninger, M., Peters, J., Paridaen, J. T. & Huttner, W. B. 2012. Basolateral rather than apical primary cilia on neuroepithelial cells committed to delamination. Development 139, 95-105.
Wodarz, A., Ramrath, A., Kuchinke, U. & Knust, E. 1999. Bazooka provides an apical cue for Inscuteable localization in Drosophila neuroblasts. Nature 402, 544-547.
Yamashita, Y. M., Mahowald, A. P., Perlin, J. R. & Fuller, M. T. 2007. Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science 315, 518-521.
Yasumi, M., Sakisaka, T., Hoshino, T., Kimura, T., Sakamoto, Y., Yamanaka, T., Ohno, S. & Takai, Y. 2005. Direct binding of Lgl2 to LGN during mitosis and its requirement for normal cell division. J. Biol. Chem. 280, 6761-6765.
Yingling, J., Youn, Y. H., Darling, D., Toyo-Oka, K., Pramparo, T., Hirotsune, S. & Wynshaw-Boris, A. 2008. Neuroepithelial stem cell proliferation requires LIS1 for precise spindle orientation and symmetric division. Cell 132, 474-486.
Yoon K, G. N. 2005. Notch signaling in the mammalian central nervous system: insights from mouse mutants. Nat. Neurosci. 8, 709-715.
Yoon, K. J., Koo, B. K., Im, S. K., Jeong, H. W., Ghim, J., Kwon, M. C., Moon, J. S., Miyata, T. & Kong, Y. Y. 2008. Mind bomb 1-expressing intermediate progenitors generate notch signaling to maintain radial glial cells. Neuron 58, 519-531.
Yu, F., Morin, X., Cai, Y., Yang, X. & Chia, W. 2000. Analysis of partner of inscuteable, a novel player of Drosophila asymmetric divisions, reveals two distinct steps in inscuteable apical localization. Cell 100, 399-409.
Zhadanov, A. B., Provance, D. W. Jr, Speer, C. A., Coffin, J. D., Goss, D., Blixt, J. A., Reichert, C. M. & Mercer, J. A. 1999. Absence of the tight junctional protein AF-6 disrupts epithelial cell-cell junctions and cell polarity during mouse development. Curr. Biol. 9, 880-888.
Zheng, Z., Zhu, H., Wan, Q., Liu, J., Xiao, Z., Siderovski, D. P. & Du, Q. 2010. LGN regulates mitotic spindle orientation during epithelial morphogenesis. J. Cell Biol. 189 275-288.
Zhong, W., Feder, J. N., Jiang, M. M., Jan, L. Y. & Jan, Y. N. 1996. Asymmetric localization of a mammalian numb homolog during mouse cortical neurogenesis. Neuron 17, 43-53.
Zhu, J., Shang, Y., Xia, C., Wang, W., Wen, W. & Zhang, M. 2011a. Guanylate kinase domains of the MAGUK family scaffold proteins as specific phospho-protein-binding modules. EMBO J. 30, 4986-4997.
Zhu, J., Wen, W., Zheng, Z., Shang, Y., Wei, Z., Xiao, Z., Pan, Z., Du, Q., Wang, W. & Zhang, M. 2011b. LGN/mInsc and LGN/NuMA complex structures suggest distinct functions in asymmetric cell division for the Par3/mInsc/LGN and Galphai/LGN/NuMA pathways. Mol. Cell 43, 418-431.
Zigman, M., Cayouette, M., Charalambous, C., Schleiffer, A., Hoeller, O., Dunican, D., Mccudden, C. R., Firnberg, N., Barres, B. A., Siderovski, D. P. & Knoblich, J. A. 2005. Mammalian inscuteable regulates spindle orientation and cell fate in the developing retina. Neuron 48, 539-545.