The role of Pax6 in regulating the orientation and mode of cell division of progenitors in the mouse cerebral cortex

Development

Volumn 138, Issue 23, 2011, Pages 5067-5078

  Asami, Maki ^a   Pilz, Gregor A ^a   Ninkovic, Jovica ^a,d   Godinho, Leanne ^b   Schroeder, Timm ^a   Huttner, Wieland B ^c   Götz, Magdalena ^a,d  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

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

^d UNIVERSITY OF MUNICH   (Germany)

Author keywords

Asymmetric cell division; Neurogenesis; Radial glia; Spag5

Indexed keywords

MICROTUBULE ASSOCIATED PROTEIN; SPAG5 PROTEIN; TRANSCRIPTION FACTOR PAX6; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APICAL MEMBRANE; ARTICLE; BRAIN CORTEX; CELL CYCLE REGULATION; CELL DIVISION; CELL INTERACTION; EMBRYO; FEMALE; GENE DELETION; IMAGING; IN VITRO STUDY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; STEM CELL;

ANALYSIS OF VARIANCE; ANIMALS; CELL CYCLE PROTEINS; CELL DIVISION; CELL POLARITY; CEREBRAL CORTEX; CHROMATIN IMMUNOPRECIPITATION; DNA PRIMERS; ELECTROPORATION; EYE PROTEINS; FEMALE; HOMEODOMAIN PROTEINS; IMMUNOHISTOCHEMISTRY; LUCIFERASES; MICE; PAIRED BOX TRANSCRIPTION FACTORS; POLYMERASE CHAIN REACTION; PREGNANCY; REPRESSOR PROTEINS; STEM CELLS;

MUS;

EID: 80755150056     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.074591     Document Type: Article

References (88)

1. Adams, R. J. (1996). Metaphase spindles rotate in the neuroepithelium of rat cerebral cortex. J. Neurosci. 16, 7610-7618.
2. Alexandre, P., Reugels, A. M., Barker, D., Blanc, E. and Clarke J. D. (2010). Neurons derive from the more apical daughter in asymmetric divisions in the zebrafish neural tube. Nat. Neurosci. 13, 673-679.
3. Ashery-Padan, R., Marquardt, T., Zhou, X. and Gruss, P. (2000). Pax6 activity in the lens primordium is required for lens formation and for correct placement of a single retina in the eye. Genes Dev. 14, 2701-2711.
4. Attardo, A., Calegari, F., Haubensak, W., Wilsch-Brauninger, M. and 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.
5. Berger, J., Berger, S., Tuoc, T. C., D'Amelio, M., Cecconi, F., Gorski, J. A., Jones, K. R., Gruss, P. and Stoykova, A. (date2007/date). Conditional activation of Pax6 in the developing cortex of transgenic mice causes progenitor apoptosis. Development 134, 1311-1322.
6. Bultje, R. S., Castaneda-Castellanos, D. R., Jan, L. Y., Jan, Y. N., Kriegstein, A. R. and Shi, S. H. (2009). Mammalian Par3 regulates progenitor cell asymmetric division via notch signaling in the developing neocortex. Neuron 63, 189-202.
7. 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. et al. (2006). The Rho-GTPase cdc42 regulates neural progenitor fate at the apical surface. Nat. Neurosci. 9, 1099-1107.
8. Carey, M. F., Peterson, C. L. and Smale, S. T. (2009). Chromatin immunoprecipitation (ChIP). Cold Spring Harb. Protoc. 9, Prot5279.
9. Chang, M. S., Huang, C. J., Chen, M. L., Chen, S. T., Fan, C. C., Chu, J. M., Lin, W. C. and Yang, Y. C. (2001). Cloning and characterization of hMAP126, a new member of mitotic spindle-associated proteins. Biochem. Biophys. Res. Commun. 287, 116-121.
10. Cheng, T. S., Hsiao, Y. L., Lin, C. C., Hsu, C. M., Chang, M. S., Lee, C. I., Yu, R. C., Huang, C. Y., Howng, S. L. and Hong, Y. R. (2007). hNinein is required for targeting spindle-associated protein Astrin to the centrosome during the S and G2 phases. Exp. Cell Res. 313, 1710-1721.
11. Chenn, A. and McConnell, S. K. (1995). Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis. Cell 82, 631-641.
12. Costa, M. R., Wen, G., Lepier, A., Schroeder, T. and Gotz, M. (2008). Parcomplex proteins promote proliferative progenitor divisions in the developing mouse cerebral cortex. Development 135, 11-22.
13. Doe, C. Q. (2008). Neural stem cells: balancing self-renewal with differentiation. Development 135, 1575-1587.
14. Du, J., Jablonski, S., Yen, T. J. and Hannon, G. J. (2008). Astrin regulates Aurora-A localization. Biochem. Biophys. Res. Commun. 370, 213-219.
15. Estivill-Torrus, G., Pearson, H., van Heyningen, V., Price, D. J. and Rashbass, P. (2002). Pax6 is required to regulate the cell cycle and the rate of progression from symmetrical to asymmetrical division in mammalian cortical progenitors. Development 129, 455-466.
16. Farkas, L. M. and Huttner, W. B. (2008). The cell biology of neural stem and progenitor cells and its significance for their proliferation versus differentiation during mammalian brain development. Curr. Opin. Cell Biol. 20, 707-715.
17. Fietz, S. A., Kelava, I., Vogt, J., Wilsch-Brauninger, M., Stenzel, D., Fish, J. L., Corbeil, D., Riehn, A., Distler, W., Nitsch, R. et al. (2010). OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling. Nat. Neurosci. 13, 690-699.
18. Fish, J. L., Kosodo, Y., Enard, W., Paabo, S. and Huttner, W. B. (2006). Aspm specifically maintains symmetric proliferative divisions of neuroepithelial cells. Proc. Natl. Acad. Sci. USA 103, 10438-10443.
19. Fish, J. L., Dehay, C., Kennedy, H. and Huttner, W. B. (2008). Making bigger brains-the evolution of neural-progenitor-cell division. J. Cell Sci. 121, 2783-2793.
20. Fumalski, J. K., Trivedi, N., Howell, D., Yang, Y., Tong, Y., Gilbertson, R. and Solecki, D. J. (2010). Siah regulation of Pard3A controls neuronal cell adhesion during germinal zone exit. Science 330, 1834.
21. George, S. H., Gertsenstein, M., Vintersten, K., Korets-Smith, E., Murphy, J., Stevens, M. E., Haigh, J. J. and Nagy, A. (2007). Developmental and adult phenotyping directly from mutant embryonic stem cells. Proc. Natl. Acad. Sci. USA 104, 4455-4460.
22. Godin, J. D., Colombo, K., Molina-Calavita, M., Keryer, G., Zala, D., Charrin, B. C., Dietrich, P., Volvert, M. L., Guillemot, F., Dragatsis, I. et al. (2010). Huntingtin is required for mitotic spindle orientation and mammalian neurogenesis. Neuron 67, 392-406.
23. Götz, M. and Huttner, W. B. (2005). The cell biology of neurogenesis. Nat. Rev. Mol. Cell. Biol. 6, 777-788.
24. Götz, M., Stoykova, A. and Gruss, P. (1998). Pax6 controls radial glia differentiation in the cerebral cortex. Neuron 21, 1031-1044.
25. Grinchuk, O., Kozmik, Z., Wu, X. and Tomarev, S. (2005). The Optimedin gene is a downstream target of Pax6. J. Biol. Chem. 280, 35228-35237.
26. Hand, R., Bortone, D., Mattar, P., Nguyen, L., Heng, J. I., Guerrier, S., Boutt, E., Peters, E., Barnes, A. P., Parras, C. et al. (2005). Phosphorylation of Neurogenin2 specifies the migration properties and the dendritic morphology of pyramidal neurons in the neocortex. Neuron 48, 45-62.
27. Hansen, D. V., Lui, J. H., Parker, P. R. and Kriegstein, A. R. (2010). Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 464, 554-561.
28. Haubensak, W., Attardo, A., Denk, W. and 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.
29. Haubst, N., Berger, J., Radjendirane, V., Graw, J., Favor, J., Saunders, G. F., Stoykova, A. and Gotz, M. (2004). Molecular dissection of Pax6 function: the specific roles of the paired domain and homeodomain in brain development. Development 131, 6131-6140.
30. Haydar, T. F., Ang, E., Jr and Rakic, P. (2003). Mitotic spindle rotation and mode of cell division in the developing telencephalon. Proc. Natl. Acad. Sci. USA 100, 2890-2895.
31. Heins, N., Malatesta, P., Cecconi, F., Nakafuku, M., Tucker, K. L., Hack, M. A., Chapouton, P., Barde, Y. A. and Götz, M. (2002). Glial cells generate neurons: the role of the transcription factor Pax6. Nat. Neurosci. 5, 308-315.
32. Hill, R. E., Favor, J., Hogan, B. L., Ton, C. C., Saunders, G. F., Hanson, I. M., Prosser, J., Jordan, T., Hastie, N. D. and van Heyningen, V. (1991). Mouse small eye results from mutations in a paired-like homeobox-containing gene. Nature 354, 522-525.
33. Holm, P. C., Mader, M. T., Haubst, N., Wizenmann, A., Sigvardsson, M. and Götz, M. (2007). Loss- and gain-of-function analyses reveal targets of Pax6 in the developing mouse telencephalon. Mol. Cell. Neurosci. 34, 99-119.
34. Huttner, W. B. and Kosodo, Y. (2005). Symmetric versus asymmetric cell division during neurogenesis in the developing vertebrate central nervous system. Curr. Opin. Cell Biol. 17, 648-657.
35. Knoblich, J. A. (2008). Mechanisms of asymmetric stem cell division. Cell 132, 583-597.
36. Konno, D., Shioi, G., Shitamukai, A., Mori, A., Kiyonari, H., Miyata, T. and Matsuzaki, F. (2008). Neuroepithelial progenitors undergo LGN-dependent planar divisions to maintain self-renewability during mammalian neurogenesis. Nat. Cell Biol. 10, 93-101.
37. Kosodo, Y., Roper, K., Haubensak, W., Marzesco, A. M., Corbeil, D. and Huttner, W. B. (2004). Asymmetric distribution of the apical plasma membrane during neurogenic divisions of mammalian neuroepithelial cells. EMBO J. 23, 2314-2324.
38. Kriegstein, A., Noctor, S. and Martinez-Cerdeno, V. (2006). Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat. Rev. Neurosci. 7, 883-890.
39. Lechler, T. and Fuchs, E. (2005). Asymmetric cell divisions promote stratification and differentiation of mammalian skin. Nature 437, 275-280.
40. Lee, T. I., Johnstone, S. E. and Young, R. A. (2006). Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat. Protoc. 1, 729-748.
41. Machon, O., van den Bout, C. J., Backman, M., Kemler, R. and Krauss, S. (2003). Role of beta-catenin in the developing cortical and hippocampal neuroepithelium. Neuroscience 122, 129-143.
42. Mack, G. J. and Compton, D. A. (2001). Analysis of mitotic microtubuleassociated proteins using mass spectrometry identifies astrin, a spindleassociated protein. Proc. Natl. Acad. Sci. USA 98, 14434-14439.
43. Manning, A. L., Bakhoum, S. F., Maffini, S., Correia-Melo, C., Maiato, H. and Compton, D. A. (2010). CLASP1, astrin and Kif2b form a molecular switch that regulates kinetochore-microtubule dynamics to promote mitotic progression and fidelity. EMBO J. 29, 3531-3543.
44. Marthiens, V. and ffrench-Constant, C. (2009). Adherens junction domains are split by asymmetric division of embryonic neural stem cells. EMBO Rep. 10, 515-520.
45. Matsuzaki, F. (2000). Asymmetric division of Drosophila neural stem cells: a basis for neural diversity. Curr. Opin. Neurobiol. 10, 38-44.
46. Miyata, T. (2007). Asymmetric cell division during brain morphogenesis. Prog. Mol. Subcell. Biol. 45, 121-142.
47. Miyata, T., Kawaguchi, A., Saito, K., Kawano, M., Muto, T. and Ogawa, M. (2004). Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 131, 3133-3145.
48. Molnar, Z., Metin, C., Stoykova, A., Tarabykin, V., Price, D. J., Francis, F., Meyer, G., Dehay, C. and Kennedy, H. (2006). Comparative aspects of cerebral cortical development. Eur. J. Neurosci. 23, 921-934.
49. Morin, X., Jaouen, F. and Durbec, P. (2007). Control of planar divisions by the Gprotein regulator LGN maintains progenitors in the chick neuroepithelium. Nat. Neurosci. 10, 1440-1448.
50. Ninkovic, J., Pinto, L., Petricca, S., Lepier, A., Sun, J., Rieger, M. A., Schroeder, T., Cvekl, A., Favor, J. and Gotz, M. (2010). The transcription factor Pax6 regulates survival of dopaminergic olfactory bulb neurons via crystallin alphaA. Neuron 68, 682-694.
51. Noctor, S. C., Martinez-Cerdeno, V., Ivic, L. and Kriegstein, A. R. (2004). Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7, 136-144.
52. Osumi, N. (2001). The role of Pax6 in brain patterning. Tohoku J. Exp. Med. 193, 163-174.
53. Osumi, N., Shinohara, H., Numayama-Tsuruta, K. and Maekawa, M. (2008). Concise review: Pax6 transcription factor contributes to both embryonic and adult neurogenesis as a multifunctional regulator. Stem Cells 26, 1663-1672.
54. Pinto, L., Mader, M. T., Irmler, M., Gentilini, M., Santoni, F., Drechsel, D., Blum, R., Stahl, R., Bulfone, A., Malatesta, P. et al. (2008). Prospective isolation of functionally distinct radial glial subtypes-lineage and transcriptome analysis. Mol. Cell. Neurosci. 38, 15-42.
55. Pinto, L., Drechsel, D., Schmid, M. T., Ninkovic, J., Irmler, M., Brill, M. S., Restani, L., Gianfranceschi, L., Cerri, C., Weber, S. N. et al. (2009). AP2gamma regulates basal progenitor fate in a region- and layer-specific manner in the developing cortex. Nat. Neurosci. 12, 1229-1237.
56. Plageman, T. F., Jr, Chung, M. I., Lou, M., Smith, A. N., Hildebrand, J. D., Wallingford, J. B. and Lang, R. A. (2010). Pax6-dependent Shroom3 expression regulates apical constriction during lens placode invagination. Development 137, 405-415.
57. Polleux, F. and Ghosh, A. (2002). The slice overlay assay: a versatile tool to study the influence of extracellular signals on neuronal development. Sci. STKE 2002, p.l9.
58. Poulson, N. D. and Lechler, T. (2010). Robust control of mitotic spindle orientation in the developing epidermis. J. Cell Biol. 191, 915-922.
59. Quinn, J. C., Molinek, M., Martynoga, B. S., Zaki, P. A., Faedo, A., Bulfone, A., Hevner, R. F., West, J. D. and Price, D. J. (2007). Pax6 controls cerebral cortical cell number by regulating exit from the cell cycle and specifies cortical cell identity by a cell autonomous mechanism. Dev. Biol. 302, 50-65.
60. Rakic, P. (2009). Evolution of the neocortex: a perspective from developmental biology. Nat. Rev. Neurosci. 10, 724-735.
61. Reillo, I., de Juan Romero, C., Garcia-Cabezas, M. A. and Borrell, V. (2011). A role for intermediate radial glia in the tangential expansion of the mammalian cerebral cortex. Cereb. Cortex 21, 1674-1694.
62. Rieger, M. A., Hoppe, P. S., Smejkal, B. M., Eitelhuber, A. C. and Schroeder, T. (2009). Hematopoietic cytokines can instruct lineage choice. Science 325, 217-218.
63. Saito, T. (2006). In vivo electroporation in the embryonic mouse central nervous system. Nat. Protoc. 1, 1552-1558.
64. Sanada, K. and Tsai, L. H. (2005). G protein betagamma subunits and AGS3 control spindle orientation and asymmetric cell fate of cerebral cortical progenitors. Cell 122, 119-131.
65. Sansom, S. N., Griffiths, D. S., Faedo, A., Kleinjan, D. J., Ruan, Y., Smith, J., van Heyningen, V., Rubenstein, J. L. and Livesey, F. J. (2009). The level of the transcription factor Pax6 is essential for controlling the balance between neural stem cell self-renewal and neurogenesis. PLoS Genet. 5, e1000511.
66. Schmahl, W., Knoedlseder, M., Favor, J. and Davidson, D. (1993). Defects of neuronal migration and the pathogenesis of cortical malformations are associated with Small eye (Sey) in the mouse, a point mutation at the Pax-6- locus. Acta Neuropathol. 86, 126-135.
67. Schwamborn, J. C., Berezikov, E. and Knoblich, J. A. (2009). The TRIM-NHL protein TRIM32 activates microRNAs and prevents self-renewal in mouse neural progenitors. Cell 136, 913-925.
68. Stoykova, A. and Gruss, P. (1994). Roles of Pax-genes in developing and adult brain as suggested by expression patterns. J. Neurosci. 14, 1395-1412.
69. Stoykova, A., Fritsch, R., Walther, C. and Gruss, P. (1996). Forebrain patterning defects in Small eye mutant mice. Development 122, 3453-3465.
70. Stoykova, A., Götz, M., Gruss, P. and Price, J. (1997). Pax6-dependent regulation of adhesive patterning, R-cadherin expression and boundary formation in developing forebrain. Development 124, 3765-3777.
71. Stoykova, A., Treichel, D., Hallonet, M. and Gruss, P. (2000). Pax6 modulates the dorsoventral patterning of the mammalian telencephalon. J. Neurosci. 20, 8042-8050.
72. Stoykova, A., Hatano, O., Gruss, P. and Götz, M. (2003). Increase in reelinpositive cells in the marginal zone of Pax6 mutant mouse cortex. Cereb. Cortex 13, 560-571.
73. Stricker, S. H., Meiri, K. and Götz, M. (2006). P-GAP-43 is enriched in horizontal cell divisions throughout rat cortical development. Cereb. Cortex 16 Suppl. 1, i121-i131.
74. Tamai, H., Shinohara, H., Miyata, T., Saito, K., Nishizawa, Y., Nomura, T. and Osumi, N. (2007). Pax6 transcription factor is required for the interkinetic nuclear movement of neuroepithelial cells. Genes Cells 12, 983-996.
75. Thein, K. H., Kleylein-Sohn, J., Nigg, E. A. and Gruneberg, U. (2007). Astrin is required for the maintenance of sister chromatid cohesion and centrosome integrity. J. Cell Biol. 178, 345-354.
76. Toresson, H., Potter, S. S. and Campbell, K. (2000). Genetic control of dorsalventral identity in the telencephalon: opposing roles for Pax6 and Gsh2. Development 127, 4361-4371.
77. Walther, C. and Gruss, P. (1991). Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113, 1435-1449.
78. Wang, X., Tsai, J. W., Imai, J. H., Lian, W. N., Vallee, R. B. and Shi, S. H. (2009). Asymmetric centrosome inheritance maintains neural progenitors in the neocortex. Nature 461, 947-955.
79. Warren, N., Caric, D., Pratt, T., Clausen, J. A., Asavaritikrai, P., Mason, J. O., Hill, R. E. and Price, D. J. (1999). The transcription factor, Pax6, is required for cell proliferation and differentiation in the developing cerebral cortex. Cereb. Cortex 9, 627-635.
80. Weigmann, A., Corbeil, D., Hellwig, A. and Huttner, W. B. (1997). 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, 12425-12430.
81. Wilcock, A. C., Swedlow, J. R. and 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.
82. Wolf, L. V., Yang, Y., Wang, J., Xie, Q., Braunger, B., Tamm, E. R., Zavadil, J. and Cvekl, A. (2009). Identification of pax6-dependent gene regulatory networks in the mouse lens. PLoS ONE 4, e4159.
83. Woodhead, G. J., Mutch, C. A., Olson, E. C. and Chenn, A. (2006). Cellautonomous beta-catenin signaling regulates cortical precursor proliferation. J. Neurosci. 29, 12620-12630.
84. Wu, S. X., Goebbels, S., Nakamura, K., Nakamura, K., Kometani, K., Minato, N., Kaneko, T., Nave, K. A. and Tamamaki, N. (2005). Pyramidal neurons of upper cortical layers generated by NEX-positive progenitor cells in the subventricular zone. Proc. Natl. Acad. Sci. USA 102, 17172-17177.
85. Yuan, J., Li, M., Wei, L., Yin, S., Xiong, B., Li, S., Lin, S. L., Schatten, H. and Sun, Q. Y. (2009). Astrin regulates meiotic spindle organization, spindle pole tethering and cell cycle progression in mouse oocyte. Cell Cycle 8, 3384-3395.
86. Yun, K., Potter, S. and Rubenstein, J. L. (2001). Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon. Development 128, 193-205.
87. Zhang, J., Woodhead, G. J., Swaminathan, S. K., Noles, S. R., McQuinn, E. R., Pisarek, A. J., Stocker, A. M., Mutch, C. A., Funatsu, N. and Chenn, A. (2010). Cortical neural precursors inhibit their own differentiation via N-cadherin maintenance of beta-catenin signaling. Dev. Cell 18, 472-479.
88. Zheng, Z., Zhu, H., Wan, Q., Liu, J., Xiao, Z., Siderovski, D. P. and Du, Q. (2010). LGN regulates mitotic spindle orientation during epithelial morphogenesis. J. Cell Biol. 189, 275-288.