Cortical development and asymmetric cell divisions

doi:10.1007/s11515-012-1235-x

Front Biol

2012, Vol. 7

Issue (4) : 297-306 https://doi.org/10.1007/s11515-012-1235-x

REVIEW

Cortical development and asymmetric cell divisions

Yan ZHOU(

)

College of Life Sciences, Wuhan University, Luojia Hill, Wuhan 430072, China

Download: PDF(285 KB) HTML
Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks

Abstract

The development of the mammalian neocortex involves rounds of symmetric and asymmetric cell division of neural progenitors to fulfill needs of both self-renewal of progenitors and production of differentiated progenies such as neurons and glia. The machinery for asymmetric cell division is evolutionarily conserved and extensively used in organogenesis and homeostasis of adult tissues. Here we summarize recent progress regarding cellular characteristics of different types of neural progenitors in mammals, highlighting how asymmetric cell division is utilized during cortical development.

Keywords asymmetric cell division radial glial cells centrosome spindle orientation

Corresponding Author(s): ZHOU Yan,Email:yan.zhou@whu.edu.cn

Issue Date: 01 August 2012

Cite this article:

Yan ZHOU. Cortical development and asymmetric cell divisions[J]. Front Biol, 2012, 7(4): 297-306.

URL:

https://academic.hep.com.cn/fib/EN/10.1007/s11515-012-1235-x
https://academic.hep.com.cn/fib/EN/Y2012/V7/I4/297

Fig.1 Asymmetric cell division of neuroblasts. (A) Neuroblasts are neural progenitor cells that delaminate from the ventral neuroectoderm during embryogenesis of . (B) Neuroblast asymmetric divisions are controlled by two apically localized protein complexes linked by Inscuteable. The first protein complex is showed in blue and comprises Bazooka/Par3, Par6 and aPKC, with aPKC acting though the tumor suppressor Lethal giant larvae (Lgl) to exclude the basally localized proteins from the apical cortex. The second apical protein complex includes Partner of Inscuteable (Pins), Gαi and Locomotion defects (Loco). The Gαi/Pins/Loco complex mediates mitotic spindle orientation to ensure the cleavage plane is orthogonal to the apico-basal polarity axis. Pins also associates with the NuMa-related protein, Mushroom body defective (Mud), Disc Large (Dlg), and the astral microtubule plus end protein Khc-73 to ensure proper cortical polarity and spindle alignment. The apical daughter cell will remain as a neuroblast. (C) Cell-fate determinants like Brat, Prospero (Pros), Staufen (Stau) and Numb are localized to the basal cortex of the mitotic neuroblast, where they promote the daughter cell to differentiate into a ganglion mother cell (GMC).

Tab.1 Comparison of the properties of cortical neural progenitors

Fig.2 Asymmetric cell division of radial glial (RG) cells and outer radial glial (oRG) cells in cortical neurogenesis. (A) RG cells (RGC) have thin processes touching both the ventricular lumen and the pial surface of the developing brain, with their nuclei residing in the ventricular zone of the neuroepithelium. During indirect neurogenesis, a RG cell (RGC) divides asymmetrically to self-renew and produce a basal progenitor cell (BP), which then divides symmetrically into two postmitotic neurons that migrate radially to form the cortical plate (CP). BP cells are not polarized and reside in the subventricular zone (SVZ). BP cells can also divide symmetrically a few more rounds to expand themselves before terminal neurogenic divisions (not shown). (B) Outer radial glial (oRG) cells can be derived from asymmetric divisions of RG cells but lack apical processes. The somas of oRG cells localize in the outer subventricular zone (oSVZ) and express most RG cell markers. Similar to RG cells, most oRG cells divide asymmetrically during the peak phase of cortical neurogenesis.

	Drosophila	Mouse homologs
Functional categories	Symbol/name	Roles in cell fate specification of neuroblasts	Symbol	Roles in cortical neurogenesis
Cell polarity establishment	Par3/ Bazooka	After delamination of the neuroblast from the neuroepithelium, Bazooka provides an asymmetric cue in the apical cytocortex that is required to anchor Inscuteable. Bazooka is also responsible for the maintenance of apical-basal polarity in epithelial tissues (Kuchinke et al., 1998; Schober et al., 1999).	mPar3	1) mPar3 is enriched at the lateral membrane domain in the ventricular endfeet of RG cells during interphase, whereas it becomes dispersed and shows asymmetric localization during mitosis. mPar3 acts through the Notch signaling pathway in generating the asymmetry in radial glial daughter cell fate specification (Bultje et al., 2009).2) Specifies axon-dendrite polarity in hippocampal neurons (Shi et al., 2003).
	Par6	Sets up apico-basal polarity. Loss of Par-6 leads to defects in the apical localization of Baz and Insc in neuroblasts and defects in the basal localization of Numb and Miranda, as well as the randomization of neuroblast spindle orientation; its loss also leads to defects in epithelial polarity (Petronczki and Knoblich, 2001).	Par6 (Pard6A)Pard6BPard6G	1) Par6 specifies axon-dendrite polarity in hippocampal neurons (Shi et al., 2003).2) Par6 Controls glial-guided neuronal migration (Solecki et al., 2004).3) Par6 overexpression promotes the generation of RG cells in vitro and in vivo (Costa et al., 2008).
	aPKC	Sets up apico-basal polarity. aPKC mutation results in loss of apico-basal polarity, multilayering of epithelia, mislocalization of Insc, and abnormal spindle orientation in neuroblasts (Wodarz et al., 2000; Rolls et al., 2003).	aPKCλ & aPKCζ	aPKCλ is required for the maintenance of adherens junctions between endfeet of RG cells. In conditional aPKCλ knockout mice, adherens junctions are lost but neurons were produced at a normal rate (Imai et al., 2006).
	Lgl	Controls basal localization of cell-fate determinants(Ohshiro et al., 2000; Peng et al., 2000).	Lgl1	Maintains cell polarity of RG cells. Loss of Lgl1 in mice results in formation of neuroepithelial rosette-like structures. A large proportion of Lgl1^–/– neural progenitor cells fail to exit the cell cycle and differentiate, but continue to proliferate and die by apoptosis. Dividing Lgl1^–/– cells are unable to asymmetrically localize Numb (Klezovitch et al., 2004).
Mitotic spindle positioning	Insc	Inscuteable tethers together the Par and Pins complexes at the apical side. Loss of Insc results in misoriented mitotic spindles and randomized crescents of determinants. Ectopic expression of Insc in epithelial cells triggers a reorientation of the mitotic spindle into an apical-basal direction (Kraut et al., 1996).	mInsc	Orients mitotic spindles in retinal progenitors and RG cells:1) In rat retinal explants, downregulation of mInsc inhibits vertical divisions and leads to proliferation and cell fate specification defects (Zigman et al., 2005).2) Loss of mInsc results in defects of neurogenesis and depletion of basal progenitors. mInsc overexpression leads to expansion of basal progenitors (Postiglione et al., 2011).
	Pins	Pins and Inscuteable are dependent on each other for asymmetric localization in neuroblasts. In Pins mutants, neuroblasts showed defects in the orientation of their mitotic spindle and the basal asymmetric localization of Numb and Miranda (Schaefer et al., 2000; Yu et al., 2000).	LGN(Gpsm2)	Maintains planar divisions and RG cell fates.Knocking out LGN randomized the orientation of normally planar divisions of RG cells. The resultant loss of the apical membrane from daughter cells converted them into abnormally localized progenitors without affecting neuronal production rate (Konno et al., 2008).
	Ags3(Gpsm1)	Receptor-independent activators of Gβγ signaling. Regulates spindle orientation and asymmetric cell fate of RG cells (Sanada and Tsai, 2005).
	Hetero-trimeric G proteins	The signaling mediated by the Gβ subunit of heterotrimeric G proteins determines asymmetric spindle formation. Lack of Gβ induces a large symmetric spindle and causes division into nearly equal-sized cells with normal segregation of the determinants (Fuse et al., 2003).Interfering with G protein function by Gαi overexpression or depletion of heterotrimeric G protein complexes causes defects in spindle orientation and asymmetric localization of determinants (Schaefer et al., 2001).	Hetero-trimeric G proteins	Interfering with Gβγ function in mouse neural progenitors causes a shift in spindle orientation from apical-basal divisions to planar divisions. This results in overproduction of neurons as a consequence of both daughter cells adopting the neuronal fate (Sanada and Tsai, 2005).
Cell fate determination	Miranda	Directs the basal cortical localization of multiple molecules, including Staufen and prospero RNA, in mitotic neuroblasts in an actin-dependent manner(Ikeshima-Kataoka et al., 1997; Shen et al., 1997).	N/A	N/A
	Numb	1) Specifies cell fates in the development of central and peripheral nervous system and myogenic lineage by antagonizing Notch signaling (Rhyu et al., 1994; Knoblich et al., 1995; Ruiz Gómez and Bate, 1997).2) Numb mutation results in overproliferation of neuroblasts and tumor formation in larval brain (Bowman et al., 2008).	Numb &Numbl	1) Numb and Numbl are redundant in asymmetric cell-fate specification of neural precursors.2) Numb loss leads to depletion or hyperproliferation of neural progenitor cells in different genetic settings (Petersen et al., 2002; Li et al., 2003; Petersen et al., 2004).3) Numb may be also required for maintenance of cadherin-based adhesion and polarity of RG cells (Rasin et al., 2007).
	Prospero	As a homeodomain-containing transcription factor, prospero represses genes required for self-renewal and activates genes for terminal differentiation. Loss of prospero causes neuroblast overproliferation (Doe et al., 1991; Choksi et al., 2006).	Prox1 & Prox2	1) Inhibit progenitor cell proliferation and promote horizontal cell genesis in the mouse retina (Dyer et al., 2003).2) Prox1 mediates suppression of Notch1, thus relieves Notch’s inhibition on neurogenesis and allows NPCs to exit the cell cycle and differentiate in chick and mouse spinal cords (Kaltezioti et al., 2010).
	Staufen	Mediates asymmetric localization and segregation of prospero RNA but not of Pros protein (Li et al., 1997; Broadus et al., 1998).	Stau1 & Stau2	Both are RNA binding proteins. Stau1 mediates mRNA decay including mRNA of ADP-ribosylation factor-1 (ARF1) (Kim et al., 2005; Gong and Maquat, 2011; Cho et al., 2012).
	Brat	Promotes neuronal differentiation and inhibits neuroblast self-renewal by inhibiting dMyc (Betschinger et al., 2006; Lee et al., 2006).	Trim32	Induces neuronal differentiation by inhibiting c-Myc and activating let-7 (Schwamborn et al., 2009).

Tab.2 Components of asymmetrical cell division and their roles in and mouse

1	Anthony T E, Klein C, Fishell G, Heintz N (2004). Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron , 41(6): 881-890 doi: 10.1016/S0896-6273(04)00140-0 pmid:15046721
2	Betschinger J, Knoblich J A (2004). Dare to be different: asymmetric cell division in Drosophila, C. elegans and vertebrates. Current Biology , CB 14: R674-685
3	Betschinger J, Mechtler K, Knoblich J A (2006). Asymmetric segregation of the tumor suppressor brat regulates self-renewal in Drosophila neural stem cells. Cell , 124(6): 1241-1253 doi: 10.1016/j.cell.2006.01.038 pmid:16564014
4	Bowman S K, Rolland V, Betschinger J, Kinsey K A, Emery G, Knoblich J A (2008). The tumor suppressors Brat and Numb regulate transit-amplifying neuroblast lineages in Drosophila. Dev Cell , 14(4): 535-546 doi: 10.1016/j.devcel.2008.03.004 pmid:18342578
5	Broadus J, Fuerstenberg S, Doe C Q (1998). Staufen-dependent localization of prospero mRNA contributes to neuroblast daughter-cell fate. Nature , 391(6669): 792-795 doi: 10.1038/35861 pmid:9486649
6	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(2): 189-202 doi: 10.1016/j.neuron.2009.07.004 pmid:19640478
7	Cappello S, Attardo A, Wu X, Iwasato T, Itohara S, Wilsch-Br?uninger M, Eilken H M, Rieger M A, Schroeder T T, Huttner W B, Brakebusch C, G?tz M (2006). The Rho-GTPase cdc42 regulates neural progenitor fate at the apical surface. Nat Neurosci , 9(9): 1099-1107 doi: 10.1038/nn1744 pmid:16892058
8	Chenn A, McConnell S K (1995). Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis. Cell , 82(4): 631-641 doi: 10.1016/0092-8674(95)90035-7 pmid:7664342
9	Cho H, Kim K M, Han S, Choe J, Park S G, Choi S S, Kim YK (2012). Staufen1-Mediated mRNA Decay Functions in Adipogenesis. Molecular cell , 46(4):495-506
10	Choksi S P, Southall T D, Bossing T, Edoff K, de Wit E, Fischer B E, van Steensel B, Micklem G, Brand A H (2006). Prospero acts as a binary switch between self-renewal and differentiation in Drosophila neural stem cells. Dev Cell , 11(6): 775-789 doi: 10.1016/j.devcel.2006.09.015 pmid:17141154
11	Costa M R, Wen G, Lepier A, Schroeder T, G?tz M (2008). Par-complex proteins promote proliferative progenitor divisions in the developing mouse cerebral cortex. Development , 135(1): 11-22 doi: 10.1242/dev.009951 pmid:18032449
12	Delattre M, G?nczy P (2004). The arithmetic of centrosome biogenesis. J Cell Sci , 117(9): 1619-1630 doi: 10.1242/jcs.01128 pmid:15075224
13	Doe C Q, Chu-LaGraff Q, Wright D M, Scott M P (1991). The prospero gene specifies cell fates in the Drosophila central nervous system. Cell , 65(3): 451-464 doi: 10.1016/0092-8674(91)90463-9 pmid:1673362
14	Dyer M A, Livesey F J, Cepko C L, Oliver G (2003). Prox1 function controls progenitor cell proliferation and horizontal cell genesis in the mammalian retina. Nat Genet , 34(1): 53-58 doi: 10.1038/ng1144 pmid:12692551
15	Englund C, Fink A, Lau C, Pham D, Daza R A, Bulfone A, Kowalczyk T, Hevner R F (2005). Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. The Journal of neuroscience: the official journal of the Society for Neuroscience , 25: 247-251
16	Fietz S A, Huttner W B (2011). Cortical progenitor expansion, self-renewal and neurogenesis-a polarized perspective. Curr Opin Neurobiol , 21(1): 23-35 doi: 10.1016/j.conb.2010.10.002 pmid:21036598
17	Fietz S A, Kelava I, Vogt J, Wilsch-Br?uninger 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(6): 690-699 doi: 10.1038/nn.2553 pmid:20436478
18	Fish J L, Kosodo Y, Enard W, P??bo S, Huttner W B (2006). Aspm specifically maintains symmetric proliferative divisions of neuroepithelial cells. Proc Natl Acad Sci USA , 103(27): 10438-10443 doi: 10.1073/pnas.0604066103 pmid:16798874
19	Fuse N, Hisata K, Katzen A L, Matsuzaki F (2003). Heterotrimeric G proteins regulate daughter cell size asymmetry in Drosophila neuroblast divisions. Current Biology , CB(13): 947-954
20	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. The Journal of neuroscience: the official journal of the Society for Neuroscience , 26: 1045-1056
21	Gong C, Maquat L E (2011). lncRNAs transactivate STAU1-mediated mRNA decay by duplexing with 3′ UTRs via Alu elements. Nature , 470(7333): 284-288 doi: 10.1038/nature09701 pmid:21307942
22	G?tz M, Huttner W B (2005). The cell biology of neurogenesis. Nat Rev Mol Cell Biol , 6(10): 777-788 doi: 10.1038/nrm1739 pmid:16314867
23	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(7288): 554-561 doi: 10.1038/nature08845 pmid:20154730
24	Huttner W B, Brand M (1997). Asymmetric division and polarity of neuroepithelial cells. Curr Opin Neurobiol , 7(1): 29-39 doi: 10.1016/S0959-4388(97)80117-1 pmid:9039800
25	Ikeshima-Kataoka H, Skeath J B, Nabeshima Y, Doe C Q, Matsuzaki F (1997). Miranda directs Prospero to a daughter cell during Drosophila asymmetric divisions. Nature , 390(6660): 625-629 doi: 10.1038/37641 pmid:9403694
26	Imai F, Hirai S, Akimoto K, Koyama H, Miyata T, Ogawa M, Noguchi S, Sasaoka T, Noda T, Ohno S (2006). Inactivation of aPKClambda results in the loss of adherens junctions in neuroepithelial cells without affecting neurogenesis in mouse neocortex. Development , 133(9): 1735-1744 doi: 10.1242/dev.02330 pmid:16571631
27	Kaltezioti V, Kouroupi G, Oikonomaki M, Mantouvalou E, Stergiopoulos A, Charonis A, Rohrer H, Matsas R, Politis P K (2010). Prox1 regulates the notch1-mediated inhibition of neurogenesis. PLoS Biol , 8(12): e1000565 doi: 10.1371/journal.pbio.1000565 pmid:21203589
28	Kim Y K, Furic L, Desgroseillers L, Maquat L E (2005). Mammalian Staufen1 recruits Upf1 to specific mRNA 3’UTRs so as to elicit mRNA decay. Cell , 120(2): 195-208 doi: 10.1016/j.cell.2004.11.050 pmid:15680326
29	Klezovitch O, Fernandez T E, Tapscott S J, Vasioukhin V (2004). Loss of cell polarity causes severe brain dysplasia in Lgl1 knockout mice. Genes Dev , 18(5): 559-571 doi: 10.1101/gad.1178004 pmid:15037549
30	Knoblich J A (2008). Mechanisms of asymmetric stem cell division. Cell , 132(4): 583-597 doi: 10.1016/j.cell.2008.02.007 pmid:18295577
31	Knoblich J A, Jan L Y, Jan Y N (1995). Asymmetric segregation of Numb and Prospero during cell division. Nature , 377(6550): 624-627 doi: 10.1038/377624a0 pmid:7566172
32	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(1): 93-101 doi: 10.1038/ncb1673 pmid:18084280
33	Kraut R, Chia W, Jan L Y, Jan Y N, Knoblich J A (1996). Role of inscuteable in orienting asymmetric cell divisions in Drosophila. Nature , 383(6595): 50-55 doi: 10.1038/383050a0 pmid:8779714
34	Kuchinke U, Grawe F, Knust E (1998). Control of spindle orientation in Drosophila by the Par-3-related PDZ-domain protein Bazooka. Current biology , CB(8): 1357-1365
35	Lee C Y, Wilkinson B D, Siegrist S E, Wharton R P, Doe C Q (2006). Brat is a Miranda cargo protein that promotes neuronal differentiation and inhibits neuroblast self-renewal. Dev Cell , 10(4): 441-449 doi: 10.1016/j.devcel.2006.01.017 pmid:16549393
36	Li H S, Wang D, Shen Q, Schonemann M D, Gorski J A, Jones K R, Temple S, Jan L Y, Jan Y N (2003). Inactivation of Numb and Numblike in embryonic dorsal forebrain impairs neurogenesis and disrupts cortical morphogenesis. Neuron , 40(6): 1105-1118 doi: 10.1016/S0896-6273(03)00755-4 pmid:14687546
37	Li P, Yang X, Wasser M, Cai Y, Chia W (1997). Inscuteable and Staufen mediate asymmetric localization and segregation of prospero RNA during Drosophila neuroblast cell divisions. Cell , 90(3): 437-447 doi: 10.1016/S0092-8674(00)80504-8 pmid:9267024
38	Lui J H, Hansen D V, Kriegstein A R (2011). Development and evolution of the human neocortex. Cell , 146(1): 18-36 doi: 10.1016/j.cell.2011.06.030 pmid:21729779
39	Meraldi P, Nigg E A (2002). The centrosome cycle. FEBS Lett , 521(1-3): 9-13 doi: 10.1016/S0014-5793(02)02865-X pmid:12067716
40	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(11): 1440-1448 doi: 10.1038/nn1984 pmid:17934458
41	Noctor S C, Martínez-Cerde?o V, Ivic L, Kriegstein A R (2004). Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci , 7(2): 136-144 doi: 10.1038/nn1172 pmid:14703572
42	Ohshiro T, Yagami T, Zhang C, Matsuzaki F (2000). Role of cortical tumour-suppressor proteins in asymmetric division of Drosophila neuroblast. Nature , 408(6812): 593-596 doi: 10.1038/35046087 pmid:11117747
43	Peng C Y, Manning L, Albertson R, Doe C Q (2000). The tumour-suppressor genes lgl and dlg regulate basal protein targeting in Drosophila neuroblasts. Nature , 408(6812): 596-600 doi: 10.1038/35046094 pmid:11117748
44	Petersen P H, Zou K, Hwang J K, Jan Y N, Zhong W (2002). Progenitor cell maintenance requires numb and numblike during mouse neurogenesis. Nature , 419(6910): 929-934 doi: 10.1038/nature01124 pmid:12410312
45	Petersen P H, Zou K, Krauss S, Zhong W (2004). Continuing role for mouse Numb and Numbl in maintaining progenitor cells during cortical neurogenesis. Nat Neurosci , 7(8): 803-811 doi: 10.1038/nn1289 pmid:15273690
46	Petronczki M, Knoblich J A (2001). DmPAR-6 directs epithelial polarity and asymmetric cell division of neuroblasts in Drosophila. Nat Cell Biol , 3(1): 43-49 doi: 10.1038/35050550 pmid:11146625
47	Postiglione M P, Jüschke 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(2): 269-284 doi: 10.1016/j.neuron.2011.09.022 pmid:22017987
48	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(7): 819-827 doi: 10.1038/nn1924 pmid:17589506
49	Rebollo E, Sampaio P, Januschke J, Llamazares S, Varmark H, González C (2007). Functionally unequal centrosomes drive spindle orientation in asymmetrically dividing Drosophila neural stem cells. Dev Cell , 12(3): 467-474 doi: 10.1016/j.devcel.2007.01.021 pmid:17336911
50	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(3): 477-491 doi: 10.1016/0092-8674(94)90112-0 pmid:8313469
51	Rolls M M, Albertson R, Shih H P, Lee C Y, Doe C Q (2003). Drosophila aPKC regulates cell polarity and cell proliferation in neuroblasts and epithelia. J Cell Biol , 163(5): 1089-1098 doi: 10.1083/jcb.200306079 pmid:14657233
52	Ruiz Gómez M, Bate M (1997). Segregation of myogenic lineages in Drosophila requires numb. Development , 124(23): 4857-4866 pmid:9428422
53	Sanada K, Tsai L H (2005). G protein betagamma subunits and AGS3 control spindle orientation and asymmetric cell fate of cerebral cortical progenitors. Cell , 122(1): 119-131 doi: 10.1016/j.cell.2005.05.009 pmid:16009138
54	Schaefer M, Petronczki M, Dorner D, Forte M, Knoblich J A (2001). Heterotrimeric G proteins direct two modes of asymmetric cell division in the Drosophila nervous system. Cell , 107(2): 183-194 doi: 10.1016/S0092-8674(01)00521-9 pmid:11672526
55	Schaefer M, Shevchenko A, Shevchenko A, Knoblich J A (2000). A protein complex containing Inscuteable and the Galpha-binding protein Pins orients asymmetric cell divisions in Drosophila. Current biology , CB(10): 353-362
56	Schober M, Schaefer M, Knoblich J A (1999). Bazooka recruits Inscuteable to orient asymmetric cell divisions in Drosophila neuroblasts. Nature , 402(6761): 548-551 doi: 10.1038/990135 pmid:10591217
57	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(5): 913-925 doi: 10.1016/j.cell.2008.12.024 pmid:19269368
58	Shen C P, Jan L Y, Jan Y N (1997). Miranda is required for the asymmetric localization of Prospero during mitosis in Drosophila. Cell , 90(3): 449-458 doi: 10.1016/S0092-8674(00)80505-X pmid:9267025
59	Shen Q, Wang Y, Dimos J T, Fasano C A, Phoenix T N, Lemischka I R, Ivanova N B, Stifani S, Morrisey E E, Temple S (2006). The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells. Nat Neurosci , 9(6): 743-751 doi: 10.1038/nn1694 pmid:16680166
60	Shi S H, Jan L Y, Jan Y N (2003). Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI 3-kinase activity. Cell , 112(1): 63-75 doi: 10.1016/S0092-8674(02)01249-7 pmid:12526794
61	Solecki D J, Model L, Gaetz J, Kapoor T M, Hatten M E (2004). Par6alpha signaling controls glial-guided neuronal migration. Nat Neurosci , 7(11): 1195-1203 doi: 10.1038/nn1332 pmid:15475953
62	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. The Journal of neuroscience: the official journal of the Society for Neuroscience , 30: 7028-7036
63	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(7266): 947-955 doi: 10.1038/nature08435 pmid:19829375
64	Wang X, Tsai J W, LaMonica B, Kriegstein A R (2011). A new subtype of progenitor cell in the mouse embryonic neocortex. Nat Neurosci , 14(5): 555-561 doi: 10.1038/nn.2807 pmid:21478886
65	Wodarz A, Ramrath A, Grimm A, Knust E (2000). Drosophila atypical protein kinase C associates with Bazooka and controls polarity of epithelia and neuroblasts. J Cell Biol , 150(6): 1361-1374 doi: 10.1083/jcb.150.6.1361 pmid:10995441
66	Wodarz A, Ramrath A, Kuchinke U, Knust E (1999). Bazooka provides an apical cue for inscuteable localization in Drosophila neuroblasts. Nature , 402(6761): 544-547 doi: 10.1038/990128 pmid:10591216
67	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(4): 399-409 doi: 10.1016/S0092-8674(00)80676-5 pmid:10693757
68	Zhong W, Chia W (2008). Neurogenesis and asymmetric cell division. Curr Opin Neurobiol , 18(1): 4-11 doi: 10.1016/j.conb.2008.05.002 pmid:18513950
69	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(4): 539-545 doi: 10.1016/j.neuron.2005.09.030 pmid:16301171

[1]	Sneha RAO, Shaoyu GE, Maya SHELLY. Centrosome positioning and primary cilia assembly orchestrate neuronal development[J]. Front Biol, 2012, 7(5): 412-427.

Viewed

Full text

Abstract

Cited

Shared

Discussed