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Pax6 controls centriole maturation in cortical progenitors through Odf2
- 作者:Marco A. Tylkowski (1) (2)
Kefei Yang (3) Sigrid Hoyer-Fender (3) Anastassia Stoykova (1) (2)
1. Research Group of Molecular Developmental Neurobiology ; Department Molecular Cell Biology ; Max-Planck Institute for Biophysical Chemistry ; Am Fa脽berg 11 ; 37077 ; G枚ttingen ; Germany 2. Center for Nanoscale Microscopy and Molecular Physiology of the Brain (CNMPB) ; 37075 ; G枚ttingen ; Germany 3. Johann-Friedrich-Blumenbach-Institute of Zoology and Anthropology ; Developmental Biology ; GZMB ; Ernst-Caspari-Haus ; Georg-August-Universit盲t G枚ttingen ; Justus-von-Liebig-Weg 11 ; G枚ttingen ; Germany
- 关键词:Centriole structure ; Transcriptional control
- 刊名:Cellular and Molecular Life Sciences (CMLS)
- 出版年:2015
- 出版时间:May 2015
- 年:2015
- 卷:72
- 期:9
- 页码:1795-1809
- 全文大小:8,279 KB
- 参考文献:1. Caviness, VS, Takahashi, T (1995) Proliferative events in the cerebral ventricular zone. Brain Dev 17: pp. 159-163 CrossRef
2. Caviness, VS, Takahashi, T, Nowakowski, RS (1995) Numbers, time and neocortical neuronogenesis: a general developmental and evolutionary model. Trends Neurosci 18: pp. 379-383 CrossRef 3. Gotz, M, Huttner, WB (2005) The cell biology of neurogenesis. Nat Rev Mol Cell Biol 6: pp. 777-788 CrossRef 4. Kriegstein, A, Noctor, S, Martinez-Cerdeno, V (2006) Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat Rev Neurosci 7: pp. 883-890 CrossRef 5. Malatesta, P, Hartfuss, E, Gotz, M (2000) Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127: pp. 5253-5263 6. Miyata, T (2007) Asymmetric cell division during brain morphogenesis. Prog Mol Subcell Biol 45: pp. 121-142 CrossRef 7. Noctor, SC, Flint, AC, Weissman, TA, Dammerman, RS, Kriegstein, AR (2001) Neurons derived from radial glial cells establish radial units in neocortex. Nature 409: pp. 714-720 CrossRef 8. Rakic, P (2009) Evolution of the neocortex: a perspective from developmental biology. Nat Rev Neurosci 10: pp. 724-735 CrossRef 9. McConnell, SK, Kaznowski, CE (1991) Cell cycle dependence of laminar determination in developing neocortex. Science 254: pp. 282-285 CrossRef 10. Angevine, JB, Sidman, RL (1961) Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 192: pp. 766-768 CrossRef 11. Rakic, P, Stensas, LJ, Sayre, E, Sidman, RL (1974) Computer-aided three-dimensional reconstruction and quantitative analysis of cells from serial electron microscopic montages of foetal monkey brain. Nature 250: pp. 31-34 CrossRef 12. Haubensak, W, Attardo, A, Denk, W, Huttner, WB (2004) Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc Natl Acad Sci USA 101: pp. 3196-3201 CrossRef 13. Lukaszewicz, A, Savatier, P, Cortay, V, Giroud, P, Huissoud, C, Berland, M, Kennedy, H, Dehay, C (2005) G1 phase regulation, area-specific cell cycle control, and cytoarchitectonics in the primate cortex. Neuron 47: pp. 353-364 CrossRef 14. Noctor, SC, Martinez-Cerdeno, V, Ivic, L, Kriegstein, AR (2004) Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7: pp. 136-144 CrossRef 15. Bishop, KM, Goudreau, G, O鈥橪eary, DD (2000) Regulation of area identity in the mammalian neocortex by Emx2 and Pax6. Science 288: pp. 344-349 CrossRef 16. Georgala, PA, Carr, CB, Price, DJ (2011) The role of Pax6 in forebrain development. Dev Neurobiol 71: pp. 690-709 CrossRef 17. Hevner, RF, Shi, L, Justice, N, Hsueh, Y, Sheng, M, Smiga, S, Bulfone, A, Goffinet, AM, Campagnoni, AT, Rubenstein, JL (2001) Tbr1 regulates differentiation of the preplate and layer 6. Neuron 29: pp. 353-366 CrossRef 18. Tuoc, TC, Radyushkin, K, Tonchev, AB, Pinon, MC, Ashery-Padan, R, Molnar, Z, Davidoff, MS, Stoykova, A (2009) Selective cortical layering abnormalities and behavioral deficits in cortex-specific Pax6 knock-out mice. J Neurosci 29: pp. 8335-8349 CrossRef 19. Zembrzycki, A, Chou, SJ, Ashery-Padan, R, Stoykova, A, O鈥橪eary, DD (2013) Sensory cortex limits cortical maps and drives top-down plasticity in thalamocortical circuits. Nat Neurosci 16: pp. 1060-1067 CrossRef 20. Hill, RE, Favor, J, Hogan, BL, Ton, CC, Saunders, GF, Hanson, IM, Prosser, J, Jordan, T, Hastie, ND, Heyningen, V (1991) Mouse small eye results from mutations in a paired-like homeobox-containing gene. Nature 354: pp. 522-525 CrossRef 21. Heins, N, Malatesta, P, Cecconi, F, Nakafuku, M, Tucker, KL, Hack, MA, Chapouton, P, Barde, YA, Gotz, M (2002) Glial cells generate neurons: the role of the transcription factor Pax6. Nat Neurosci 5: pp. 308-315 CrossRef 22. Caric, D, Gooday, D, Hill, RE, McConnell, SK, Price, DJ (1997) Determination of the migratory capacity of embryonic cortical cells lacking the transcription factor Pax-6. Development 124: pp. 5087-5096 23. Georgala, PA, Manuel, M, Price, DJ (2011) The generation of superficial cortical layers is regulated by levels of the transcription factor Pax6. Cereb Cortex 21: pp. 81-94 CrossRef 24. Quinn, JC, Molinek, M, Martynoga, BS, Zaki, PA, Faedo, A, Bulfone, A, Hevner, RF, West, JD, Price, DJ (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: pp. 50-65 CrossRef 25. Sansom, SN, Livesey, FJ (2009) Gradients in the brain: the control of the development of form and function in the cerebral cortex. Cold Spring Harb Perspect Biol 1: pp. a002519 CrossRef 26. Schmahl, W, Knoedlseder, M, Favor, J, 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: pp. 126-135 CrossRef 27. Stoykova, A, Fritsch, R, Walther, C, Gruss, P (1996) Forebrain patterning defects in Small eye mutant mice. Development 122: pp. 3453-3465 28. Tarabykin, V, Stoykova, A, Usman, N, Gruss, P (2001) Cortical upper layer neurons derive from the subventricular zone as indicated by Svet1 gene expression. Development 128: pp. 1983-1993 29. Gotz, M, Stoykova, A, Gruss, P (1998) Pax6 controls radial glia differentiation in the cerebral cortex. Neuron 21: pp. 1031-1044 CrossRef 30. Asami, M, Pilz, GA, Ninkovic, J, Godinho, L, Schroeder, T, Huttner, WB, Gotz, M (2011) The role of Pax6 in regulating the orientation and mode of cell division of progenitors in the mouse cerebral cortex. Development 138: pp. 5067-5078 CrossRef 31. Tamai, H, Shinohara, H, Miyata, T, Saito, K, Nishizawa, Y, Nomura, T, Osumi, N (2007) Pax6 transcription factor is required for the interkinetic nuclear movement of neuroepithelial cells. Genes Cells 12: pp. 983-996 CrossRef 32. Tuoc, TC, Stoykova, A (2008) Er81 is a downstream target of Pax6 in cortical progenitors. BMC Dev Biol 8: pp. 23 CrossRef 33. Kosodo, Y (2012) Interkinetic nuclear migration: beyond a hallmark of neurogenesis. Cell Mol Life Sci 69: pp. 2727-2738 CrossRef 34. Bornens, M (2002) Centrosome composition and microtubule anchoring mechanisms. Curr Opin Cell Biol 14: pp. 25-34 CrossRef 35. Higginbotham, HR, Gleeson, JG (2007) The centrosome in neuronal development. Trends Neurosci 30: pp. 276-283 CrossRef 36. Tsou, MF, Stearns, T (2006) Mechanism limiting centrosome duplication to once per cell cycle. Nature 442: pp. 947-951 CrossRef 37. Bouckson-Castaing, V, Moudjou, M, Ferguson, DJ, Mucklow, S, Belkaid, Y, Milon, G, Crocker, PR (1996) Molecular characterisation of ninein, a new coiled-coil protein of the centrosome. J Cell Sci 109: pp. 179-190 38. Lange, BM, Gull, K (1995) A molecular marker for centriole maturation in the mammalian cell cycle. J Cell Biol 130: pp. 919-927 CrossRef 39. Nakagawa, Y, Yamane, Y, Okanoue, T, Tsukita, S, Tsukita, S (2001) Outer dense fiber 2 is a widespread centrosome scaffold component preferentially associated with mother centrioles: its identification from isolated centrosomes. Mol Biol Cell 12: pp. 1687-1697 CrossRef 40. Ou, YY, Mack, GJ, Zhang, M, Rattner, JB (2002) CEP110 and ninein are located in a specific domain of the centrosome associated with centrosome maturation. J Cell Sci 115: pp. 1825-1835 41. Piel, M, Meyer, P, Khodjakov, A, Rieder, CL, Bornens, M (2000) The respective contributions of the mother and daughter centrioles to centrosome activity and behavior in vertebrate cells. J Cell Biol 149: pp. 317-330 CrossRef 42. Wang, X, Tsai, JW, Imai, JH, Lian, WN, Vallee, RB, Shi, SH (2009) Asymmetric centrosome inheritance maintains neural progenitors in the neocortex. Nature 461: pp. 947-955 CrossRef 43. Hoyer-Fender, S (2010) Centriole maturation and transformation to basal body. Semin Cell Dev Biol 21: pp. 142-147 CrossRef 44. Kobayashi, T, Dynlacht, BD (2011) Regulating the transition from centriole to basal body. J Cell Biol 193: pp. 435-444 CrossRef 45. Willaredt, MA, Hasenpusch-Theil, K, Gardner, HA, Kitanovic, I, Hirschfeld-Warneken, VC, Gojak, CP, Gorgas, K, Bradford, CL, Spatz, J, Wolfl, S, Theil, T, Tucker, KL (2008) A crucial role for primary cilia in cortical morphogenesis. J Neurosci 28: pp. 12887-12900 CrossRef 46. Willaredt, MA, Tasouri, E, Tucker, KL (2012) Primary cilia and forebrain development. Mech Dev. 47. Ishikawa, H, Kubo, A, Tsukita, S (2005) Odf2-deficient mother centrioles lack distal/subdistal appendages and the ability to generate primary cilia. Nat Cell Biol 7: pp. 517-524 CrossRef 48. Tong, CK, Han, YG, Shah, JK, Obernier, K, Guinto, CD, Alvarez-Buylla, A (2014) Primary cilia are required in a unique subpopulation of neural progenitors. Proc Natl Acad Sci USA. 49. Imai, JH, Wang, X, Shi, SH (2010) Kaede-centrin1 labeling of mother and daughter centrosomes in mammalian neocortical neural progenitors. Curr Protoc Stem Cell Biol 5: pp. 5A 50. Ashery-Padan, R, Marquardt, T, Zhou, X, 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: pp. 2701-2711 CrossRef 51. Gorski JA, Talley T, Qiu M, Puelles L, Rubenstein JL, Jones KR (2002) Cortical excitatory neurons and glia, but not GABAergic neurons, are produced in the Emx1-expressing lineage. J Neurosci 22(15):6309鈥?314. doi:10.1016/b0-12-227210-2/00147-3 52. Cai, L, Hayes, NL, Nowakowski, RS (1997) Local homogeneity of cell cycle length in developing mouse cortex. J Neurosci 17: pp. 2079-2087 53. Walther, C, Gruss, P (1991) Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113: pp. 1435-1449 54. Ibi, M, Zou, P, Inoko, A, Shiromizu, T, Matsuyama, M, Hayashi, Y, Enomoto, M, Mori, D, Hirotsune, S, Kiyono, T, Tsukita, S, Goto, H, Inagaki, M (2011) Trichoplein controls microtubule anchoring at the centrosome by binding to Odf2 and ninein. J Cell Sci 124: pp. 857-864 CrossRef 55. Pletz, N, Medack, A, Riess, EM, Yang, K, Kazerouni, ZB, Huber, D (1833) Hoyer-Fender S (2013) Transcriptional activation of Odf2/Cenexin by cell cycle arrest and the stress activated signaling pathway (JNK pathway). Biochim Biophys Acta 6: pp. 1338-1346 56. Baumer, N, Marquardt, T, Stoykova, A, Spieler, D, Treichel, D, Ashery-Padan, R, Gruss, P (2003) Retinal pigmented epithelium determination requires the redundant activities of Pax2 and Pax6. Development 130: pp. 2903-2915 CrossRef 57. Stoykova, A, Treichel, D, Hallonet, M, Gruss, P (2000) Pax6 modulates the dorsoventral patterning of the mammalian telencephalon. J Neurosci 20: pp. 8042-8050 58. Yun, K, Potter, S, Rubenstein, JL (2001) Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon. Development 128: pp. 193-205 59. Toresson, H, Potter, SS, Campbell, K (2000) Genetic control of dorsal-ventral identity in the telencephalon: opposing roles for Pax6 and Gsh2. Development 127: pp. 4361-4371 60. Warren, N, Caric, D, Pratt, T, Clausen, JA, Asavaritikrai, P, Mason, JO, Hill, RE, Price, DJ (1999) The transcription factor, Pax6, is required for cell proliferation and differentiation in the developing cerebral cortex. Cereb Cortex 9: pp. 627-635 CrossRef 61. Kroll, TT, O鈥橪eary, DD (2005) Ventralized dorsal telencephalic progenitors in Pax6 mutant mice generate GABA interneurons of a lateral ganglionic eminence fate. Proc Natl Acad Sci USA 102: pp. 7374-7379 CrossRef 62. Estivill-Torrus, G, Pearson, H, Heyningen, V, Price, DJ, 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: pp. 455-466 63. Schuurmans, C, Armant, O, Nieto, M, Stenman, JM, Britz, O, Klenin, N, Brown, C, Langevin, LM, Seibt, J, Tang, H, Cunningham, JM, Dyck, R, Walsh, C, Campbell, K, Polleux, F, Guillemot, F (2004) Sequential phases of cortical specification involve Neurogenin-dependent and -independent pathways. EMBO J 23: pp. 2892-2902 CrossRef 64. Messier, PE, Auclair, C (1973) Inhibition of nuclear migration in the absence of microtubules in the chick embryo. J Embryol Exp Morphol 30: pp. 661-671 65. Osumi, N, Shinohara, H, Numayama-Tsuruta, K, Maekawa, M (2008) Concise review: Pax6 transcription factor contributes to both embryonic and adult neurogenesis as a multifunctional regulator. Stem Cells 26: pp. 1663-1672 CrossRef 66. Azimzadeh, J, Bornens, M (2007) Structure and duplication of the centrosome. J Cell Sci 120: pp. 2139-2142 CrossRef 67. Bornens, M (2012) The centrosome in cells and organisms. Science 335: pp. 422-426 CrossRef 68. Meraldi, P, Nigg, EA (2002) The centrosome cycle. FEBS Lett 521: pp. 9-13 CrossRef 69. Shinohara, H, Sakayori, N, Takahashi, M, Osumi, N (2013) Ninein is essential for the maintenance of the cortical progenitor character by anchoring the centrosome to microtubules. Biol Open 2: pp. 739-749 CrossRef 70. Corbit, KC, Shyer, AE, Dowdle, WE, Gaulden, J, Singla, V, Chen, MH, Chuang, PT, Reiter, JF (2008) Kif3a constrains beta-catenin-dependent Wnt signalling through dual ciliary and non-ciliary mechanisms. Nat Cell Biol 10: pp. 70-76 CrossRef 71. Gerdes, JM, Liu, Y, Zaghloul, NA, Leitch, CC, Lawson, SS, Kato, M, Beachy, PA, Beales, PL, DeMartino, GN, Fisher, S, Badano, JL, Katsanis, N (2007) Disruption of the basal body compromises proteasomal function and perturbs intracellular Wnt response. Nat Genet 39: pp. 1350-1360 CrossRef 72. Muzio, L, DiBenedetto, B, Stoykova, A, Boncinelli, E, Gruss, P, Mallamaci, A (2002) Emx2 and Pax6 control regionalization of the pre-neuronogenic cortical primordium. Cereb Cortex 12: pp. 129-139 CrossRef 73. Epstein, JA, Glaser, T, Cai, J, Jepeal, L, Walton, DS, Maas, RL (1994) Two independent and interactive DNA-binding subdomains of the Pax6 paired domain are regulated by alternative splicing. Genes Dev 8: pp. 2022-2034 CrossRef 74. Muhlfriedel, S, Kirsch, F, Gruss, P, Chowdhury, K, Stoykova, A (2007) Novel genes differentially expressed in cortical regions during late neurogenesis. Eur J Neurosci 26: pp. 33-50 CrossRef
- 刊物类别:Biomedical and Life Sciences
- 刊物主题:Life Sciences
Cell Biology Biomedicine Life Sciences Biochemistry
- 出版者:Birkh盲user Basel
- ISSN:1420-9071
文摘
Cortical glutamatergic neurons are generated by radial glial cells (RGCs), specified by the expression of transcription factor (TF) Pax6, in the germinative zones of the dorsal telencephalon. Here, we demonstrate that Pax6 regulates the structural assembly of the interphase centrosomes. In the cortex of the Pax6-deficient Small eye (Sey/Sey) mutant, we find a defect of the appendages of the mother centrioles, indicating incomplete centrosome maturation. Consequently, RGCs fail to generate primary cilia, and instead of staying in the germinative zone for renewal, RGCs detach from the ventricular surface thus affecting the interkinetic nuclear migration and they exit prematurely from mitosis. Mechanistically, we show that TF Pax6 directly regulates the activity of the Odf2 gene encoding for the appendage-specific protein Odf2 with a role for the assembly of mother centriole. Our findings demonstrate a molecular mechanism that explains important characteristics of the centrosome disassembly and malfunctioning in developing cortex lacking Pax6.
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