REVIEW

Cortical development and asymmetric cell divisions

  • Yan ZHOU
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  • College of Life Sciences, Wuhan University, Luojia Hill, Wuhan 430072, China

Received date: 25 Apr 2012

Accepted date: 01 Jun 2012

Published date: 01 Aug 2012

Copyright

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg

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.

Cite this article

Yan ZHOU . Cortical development and asymmetric cell divisions[J]. Frontiers in Biology, 2012 , 7(4) : 297 -306 . DOI: 10.1007/s11515-012-1235-x

Acknowledgments

We thank Drs. Weimin ZHONG and Daria BANCESCU at Yale University for valuable comments. Yan ZHOU is supported by the National Basic Research Program of China (2011CBA01102 and 2012CB967000), the National Natural Science Foundation of China (Grant No. 31171314) and Chinese 111 project (B06018).
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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

7
Cappello S, Attardo A, Wu X, Iwasato T, Itohara S, Wilsch-Bräuninger M, Eilken H M, Rieger M A, Schroeder T T, Huttner W B, Brakebusch C, Götz M (2006). The Rho-GTPase cdc42 regulates neural progenitor fate at the apical surface. Nat Neurosci, 9(9): 1099-1107

DOI PMID

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 PMID

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 PMID

11
Costa M R, Wen G, Lepier A, Schroeder T, Götz M (2008). Par-complex proteins promote proliferative progenitor divisions in the developing mouse cerebral cortex. Development, 135(1): 11-22

DOI PMID

12
Delattre M, Gönczy P (2004). The arithmetic of centrosome biogenesis. J Cell Sci, 117(9): 1619-1630

DOI PMID

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 PMID

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 PMID

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 PMID

17
Fietz S A, Kelava I, Vogt J, Wilsch-Bräuninger 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 PMID

18
Fish J L, Kosodo Y, Enard W, Pääbo S, Huttner W B (2006). Aspm specifically maintains symmetric proliferative divisions of neuroepithelial cells. Proc Natl Acad Sci USA, 103(27): 10438-10443

DOI PMID

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 PMID

22
Götz M, Huttner W B (2005). The cell biology of neurogenesis. Nat Rev Mol Cell Biol, 6(10): 777-788

DOI PMID

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 PMID

24
Huttner W B, Brand M (1997). Asymmetric division and polarity of neuroepithelial cells. Curr Opin Neurobiol, 7(1): 29-39

DOI PMID

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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

30
Knoblich J A (2008). Mechanisms of asymmetric stem cell division. Cell, 132(4): 583-597

DOI PMID

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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

38
Lui J H, Hansen D V, Kriegstein A R (2011). Development and evolution of the human neocortex. Cell, 146(1): 18-36

DOI PMID

39
Meraldi P, Nigg E A (2002). The centrosome cycle. FEBS Lett, 521(1-3): 9-13

DOI PMID

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 PMID

41
Noctor S C, Martínez-Cerdeño 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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

52
Ruiz Gómez M, Bate M (1997). Segregation of myogenic lineages in Drosophila requires numb. Development, 124(23): 4857-4866

PMID

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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

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 PMID

68
Zhong W, Chia W (2008). Neurogenesis and asymmetric cell division. Curr Opin Neurobiol, 18(1): 4-11

DOI PMID

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 PMID

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