Asymmetric inheritance of Cyclin D2 maintains proliferative neural stem/progenitor cells: A critical event in brain development and evolution

Development Growth and Differentiation

Volumn 56, Issue 5, 2014, Pages 349-357

  Tsunekawa, Yuji ^a   Kikkawa, Takako ^b   Osumi, Noriko ^b  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Asymmetric cell division; Cyclin D2; mRNA localization; Post transcriptional regulation; Radial glial cells

Indexed keywords

CYCLIN D2; MESSENGER RNA;

3' UNTRANSLATED REGION; ASYMMETRIC CELL DIVISION; BRAIN DEVELOPMENT; BRAIN SIZE; CELL CYCLE REGULATION; CELL FATE; CELL PROLIFERATION; CELL RENEWAL; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; DAUGHTER CELL; G1 PHASE CELL CYCLE CHECKPOINT; HUMAN; MACROGLIA; MITOSIS; NEOCORTEX; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; PRIMORDIUM; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; REGULATORY SEQUENCE; REVIEW; ANIMAL; BRAIN; CYTOLOGY; EMBRYOLOGY; GENETICS; MAMMAL; METABOLISM;

MAMMALIA; PRIMATES;

ANIMALS; BRAIN; CELL PROLIFERATION; CYCLIN D2; HUMANS; MAMMALS; NEURAL STEM CELLS;

EID: 84903178601     PISSN: 00121592     EISSN: 1440169X     Source Type: Journal    
DOI: 10.1111/dgd.12135     Document Type: Review

References (84)

1. 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.
2. Ali, F., Hindley, C., Mcdowell, G., Deibler, R., Jones, A., Kirschner, M., Guillemot, F. & Philpott, A. 2011. Cell cycle-regulated multi-site phosphorylation of Neurogenin 2 coordinates cell cycling with differentiation during neurogenesis. Development 138, 4267-4277.
3. Arai, Y., Funatsu, N., Numayama-Tsuruta, K., Nomura, T., Nakamura, S. & Osumi, N. 2005. Role of Fabp7, a downstream gene of Pax6, in the maintenance of neuroepithelial cells during early embryonic development of the rat cortex. J. Neurosci. 25, 9752-9761.
4. Arai, Y., Pulvers, J. N., Haffner, C., Schilling, B., Nusslein, I., Calegari, F. & Huttner, W. B. 2011. Neural stem and progenitor cells shorten S-phase on commitment to neuron production. Nat. Commun. 2, 154.
5. Betizeau, M., Cortay, V., Patti, D., Pfister, S., Gautier, E., Bellemin-Menard, A., Afanassieff, M., Huissoud, C., Douglas, R. J., Kennedy, H. & Dehay, C. 2013. Precursor diversity and complexity of lineage relationships in the outer subventricular zone of the primate. Neuron 80, 442-457.
6. Bienvenu, F., Jirawatnotai, S., Elias, J. E., Meyer, C. A., Mizeracka, K., Marson, A., Frampton, G. M., Cole, M. F., Odom, D. T., Odajima, J., Geng, Y., Zagozdzon, A., Jecrois, M., Young, R. A., Liu, X. S., Cepko, C. L., Gygi, S. P. & Sicinski, P. 2010. Transcriptional role of cyclin D1 in development revealed by a genetic-proteomic screen. Nature 463, 374-378.
7. 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.
8. Calegari, F. & Huttner, W. B. 2003. An inhibition of cyclin-dependent kinases that lengthens, but does not arrest, neuroepithelial cell cycle induces premature neurogenesis. J. Cell Sci. 116, 4947-4955.
9. Chenn, A. & Mcconnell, S. K. 1995. Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis. Cell 82, 631-641.
10. 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.
11. Dehay, C. & Kennedy, H. 2007. Cell-cycle control and cortical development. Nat. Rev. Neurosci. 8, 438-450.
12. Delaunay, D., Cortay, V., Patti, D., Knoblauch, K. & Dehay, C. 2014. Mitotic spindle asymmetry: a Wnt/PCP-regulated mechanism generating asymmetrical division in cortical precursors. Cell Rep. 6, 400-414.
13. Ellis, P., Fagan, B. M., Magness, S. T., Hutton, S., Taranova, O., Hayashi, S., Mcmahon, A., Rao, M. & Pevny, L. 2004. SOX2, a persistent marker for multipotential neural stem cells derived from embryonic stem cells, the embryo or the adult. Dev. Neurosci. 26, 148-165.
14. 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.
15. Fishell, G. & Kriegstein, A. R. 2003. Neurons from radial glia: the consequences of asymmetric inheritance. Curr. Opin. Neurobiol. 13, 34-41.
16. Frank, C. L. & Tsai, L. H. 2009. Alternative functions of core cell cycle regulators in neuronal migration, neuronal maturation, and synaptic plasticity. Neuron 62, 312-326.
17. 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.
18. Glickstein, S. B., Alexander, S. & Ross, M. E. 2007. Differences in cyclin D2 and D1 protein expression distinguish forebrain progenitor subsets. Cereb. Cortex 17, 632-642.
19. Glickstein, S. B., Monaghan, J. A., Koeller, H. B., Jones, T. K. & Ross, M. E. 2009. Cyclin D2 is critical for intermediate progenitor cell proliferation in the embryonic cortex. J. Neurosci. 29, 9614-9624.
20. Gonczy, P. 2008. Mechanisms of asymmetric cell division: flies and worms pave the way. Nat. Rev. Mol. Cell Biol. 9, 355-366.
21. Gotz, M. & Huttner, W. B. 2005. The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 6, 777-788.
22. Gotz, M., Stoykova, A. & Gruss, P. 1998. Pax6 controls radial glia differentiation in the cerebral cortex. Neuron 21, 1031-1044.
23. Graus-Porta, D., Blaess, S., Senften, M., Littlewood-Evans, A., Damsky, C., Huang, Z., Orban, P., Klein, R., Schittny, J. C. & Muller, U. 2001. Beta1-class integrins regulate the development of laminae and folia in the cerebral and cerebellar cortex. Neuron 31, 367-379.
24. 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.
25. Hasegawa, H., Ashigaki, S., Takamatsu, M., Suzuki-Migishima, R., Ohbayashi, N., Itoh, N., Takada, S. & Tanabe, Y. 2004. Laminar patterning in the developing neocortex by temporally coordinated fibroblast growth factor signaling. J. Neurosci. 24, 8711-8719.
26. Hatakeyama, J., Bessho, Y., Katoh, K., Ookawara, S., Fujioka, M., Guillemot, F. & Kageyama, R. 2004. Hes genes regulate size, shape and histogenesis of the nervous system by control of the timing of neural stem cell differentiation. Development 131, 5539-5550.
27. 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.
28. Huttner, W. B. & Kosodo, Y. 2005. Symmetric versus asymmetric cell division during neurogenesis in the developing vertebrate central nervous system. Curr. Opin. Cell Biol. 17, 648-657.
29. Jedynak, P., Jaholkowski, P., Wozniak, G., Sandi, C., Kaczmarek, L. & Filipkowski, R. K. 2012. Lack of cyclin D2 impairing adult brain neurogenesis alters hippocampal-dependent behavioral tasks without reducing learning ability. Behav. Brain Res. 227, 159-166.
30. Johnson, D. G. & Walker, C. L. 1999. Cyclins and cell cycle checkpoints. Annu. Rev. Pharmacol. Toxicol. 39, 295-312.
31. Kadowaki, M., Nakamura, S., Machon, O., Krauss, S., Radice, G. L. & Takeichi, M. 2007. N-cadherin mediates cortical organization in the mouse brain. Dev. Biol. 304, 22-33.
32. Kawauchi, T., Shikanai, M. & Kosodo, Y. 2013. Extra-cell cycle regulatory functions of cyclin-dependent kinases (CDK) and CDK inhibitor proteins contribute to brain development and neurological disorders. Genes Cells 18, 176-194.
33. Kikkawa, T., Obayashi, T., Takahashi, M., Fukuzaki-Dohi, U., Numayama-Tsuruta, K. & Osumi, N. 2013. Dmrta1 regulates proneural gene expression downstream of Pax6 in the mammalian telencephalon. Genes Cells 18, 636-649.
34. Knoblich, J. A. 2008. Mechanisms of asymmetric stem cell division. Cell 132, 583-597.
35. Knoblich, J. A. 2010. Asymmetric cell division: recent developments and their implications for tumour biology. Nat. Rev. Mol. Cell Biol. 11, 849-860.
36. Komada, M., Saitsu, H., Kinboshi, M., Miura, T., Shiota, K. & Ishibashi, M. 2008. Hedgehog signaling is involved in development of the neocortex. Development 135, 2717-2727.
37. 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.
38. 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.
39. Kowalczyk, A., Filipkowski, R. K., Rylski, M., Wilczynski, G. M., Konopacki, F. A., Jaworski, J., Ciemerych, M. A., Sicinski, P. & Kaczmarek, L. 2004. The critical role of cyclin D2 in adult neurogenesis. J. Cell Biol. 167, 209-213.
40. Kowalczyk, T., Pontious, A., Englund, C., Daza, R. A., Bedogni, F., Hodge, R., Attardo, A., Bell, C., Huttner, W. B. & Hevner, R. F. 2009. Intermediate neuronal progenitors (basal progenitors) produce pyramidal-projection neurons for all layers of cerebral cortex. Cereb. Cortex 19, 2439-2450.
41. Lakoma, J., Garcia-Alonso, L. & Luque, J. M. 2011. Reelin sets the pace of neocortical neurogenesis. Development 138, 5223-5234.
42. LaMonica, B. E., Lui, J. H., Hansen, D. V. & Kriegstein, A. R. 2013. Mitotic spindle orientation predicts outer radial glial cell generation in human neocortex. Nat. Commun. 4, 1665.
43. Lange, C. & Calegari, F. 2010. Cdks and cyclins link G1 length and differentiation of embryonic, neural and hematopoietic stem cells. Cell Cycle 9, 1893-1900.
44. Lange, C., Huttner, W. B. & Calegari, F. 2009. Cdk4/cyclinD1 overexpression in neural stem cells shortens G1, delays neurogenesis, and promotes the generation and expansion of basal progenitors. Cell Stem Cell 5, 320-331.
45. Lee, H. & Song, M. R. 2013. The structural role of radial glial endfeet in confining spinal motor neuron somata is controlled by the Reelin and Notch pathways. Exp. Neurol. 249, 83-94.
46. Lim, S. & Kaldis, P. 2012. Loss of Cdk2 and Cdk4 induces a switch from proliferation to differentiation in neural stem cells. Stem Cells 30, 1509-1520.
47. Lui, J. H., Hansen, D. V. & Kriegstein, A. R. 2011. Development and evolution of the human neocortex. Cell 146, 18-36.
48. Ma, Q., Kintner, C. & Anderson, D. J. 1996. Identification of neurogenin, a vertebrate neuronal determination gene. Cell 87, 43-52.
49. Matsumoto, Y., Tsunekawa, Y., Nomura, T., Suto, F., Matsumata, M., Tsuchiya, S. & Osumi, N. 2011. Differential proliferation rhythm of neural progenitor and oligodendrocyte precursor cells in the young adult hippocampus. PLoS One 6, e27628.
50. Matsushime, H., Roussel, M. F., Ashmun, R. A. & Sherr, C. J. 1991. Colony-stimulating factor 1 regulates novel cyclins during the G1 phase of the cell cycle. Cell 65, 701-713.
51. Miyata, T., Kawaguchi, A., Okano, H. & Ogawa, M. 2001. Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31, 727-741.
52. 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.
53. Nguyen, L., Besson, A., Heng, J. I., Schuurmans, C., Teboul, L., Parras, C., Philpott, A., Roberts, J. M. & Guillemot, F. 2006a. p27kip1 independently promotes neuronal differentiation and migration in the cerebral cortex. Genes Dev. 20, 1511-1524.
54. Nguyen, L., Besson, A., Roberts, J. M. & Guillemot, F. 2006b. Coupling cell cycle exit, neuronal differentiation and migration in cortical neurogenesis. Cell Cycle 5, 2314-2318.
55. 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.
56. 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.
57. Okamoto, M., Namba, T., Shinoda, T., Kondo, T., Watanabe, T., Inoue, Y., Takeuchi, K., Enomoto, Y., Ota, K., Oda, K., Wada, Y., Sagou, K., Saito, K., Sakakibara, A., Kawaguchi, A., Nakajima, K., Adachi, T., Fujimori, T., Ueda, M., Hayashi, S., Kaibuchi, K. & Miyata, T. 2013. TAG-1-assisted progenitor elongation streamlines nuclear migration to optimize subapical crowding. Nat. Neurosci. 16, 1556-1566.
58. Paridaen, J. T., Wilsch-Brauninger, M. & Huttner, W. B. 2013. Asymmetric inheritance of centrosome-associated primary cilium membrane directs ciliogenesis after cell division. Cell 155, 333-344.
59. Pilaz, L. J., Patti, D., Marcy, G., Ollier, E., Pfister, S., Douglas, R. J., Betizeau, M., Gautier, E., Cortay, V., Doerflinger, N., Kennedy, H. & Dehay, C. 2009. Forced G1-phase reduction alters mode of division, neuron number, and laminar phenotype in the cerebral cortex. Proc. Natl Acad. Sci. USA 106, 21924-21929.
60. Radakovits, R., Barros, C. S., Belvindrah, R., Patton, B. & Muller, U. 2009. Regulation of radial glial survival by signals from the meninges. J. Neurosci. 29, 7694-7705.
61. Rakic, P. 1972. Mode of cell migration to the superficial layers of fetal monkey neocortex. J. Comp. Neurol. 145, 61-83.
62. Ratineau, C., Petry, M. W., Mutoh, H. & Leiter, A. B. 2002. Cyclin D1 represses the basic helix-loop-helix transcription factor, BETA2/NeuroD. J. Biol. Chem. 277, 8847-8853.
63. 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.
64. Ross, M. E., Carter, M. L. & Lee, J. H. 1996. MN20, a D2 cyclin, is transiently expressed in selected neural populations during embryogenesis. J. Neurosci. 16, 210-219.
65. Ross, M. E. & Risken, M. 1994. MN20, a D2 cyclin found in brain, is implicated in neural differentiation. J. Neurosci. 14, 6384-6391.
66. Salomoni, P. & Calegari, F. 2010. Cell cycle control of mammalian neural stem cells: putting a speed limit on G1. Trends Cell Biol. 20, 233-243.
67. Scardigli, R., Baumer, N., Gruss, P., Guillemot, F. & Le Roux, I. 2003. Direct and concentration-dependent regulation of the proneural gene Neurogenin2 by Pax6. Development 130, 3269-3281.
68. Seuntjens, E., Nityanandam, A., Miquelajauregui, A., Debruyn, J., Stryjewska, A., Goebbels, S., Nave, K. A., Huylebroeck, D. & Tarabykin, V. 2009. Sip1 regulates sequential fate decisions by feedback signaling from postmitotic neurons to progenitors. Nat. Neurosci. 12, 1373-1380.
69. Sherr, C. J. 1994. G1 phase progression: cycling on cue. Cell 79, 551-555.
70. Shimoda, Y., Tajima, Y., Osanai, T., Katsume, A., Kohara, M., Kudo, T., Narimatsu, H., Takashima, N., Ishii, Y., Nakamura, S., Osumi, N. & Sanai, Y. 2002. Pax6 controls the expression of Lewis x epitope in the embryonic forebrain by regulating alpha 1, 3-fucosyltransferase IX expression. J. Biol. Chem. 277, 2033-2039.
71. 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, 739-749.
72. Shinohara, H., Udagawa, J., Morishita, R., Ueda, H., Otani, H., Semba, R., Kato, K. & Asano, T. 2004. Gi2 signaling enhances proliferation of neural progenitor cells in the developing brain. J. Biol. Chem. 279, 41141-41148.
73. 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.
74. Shitamukai, A. & Matsuzaki, F. 2012. Control of asymmetric cell division of mammalian neural progenitors. Dev. Growth Differ. 54, 277-286.
75. Siegenthaler, J. A., Ashique, A. M., Zarbalis, K., Patterson, K. P., Hecht, J. H., Kane, M. A., Folias, A. E., Choe, Y., May, S. R., Kume, T., Napoli, J. L., Peterson, A. S. & Pleasure, S. J. 2009. Retinoic acid from the meninges regulates cortical neuron generation. Cell 139, 597-609.
76. Stahl, R., Walcher, T., De Juan Romero, C., Pilz, G. A., Cappello, S., Irmler, M., Sanz-Aquela, J. M., Beckers, J., Blum, R., Borrell, V. & Gotz, M. 2013. Trnp1 regulates expansion and folding of the mammalian cerebral cortex by control of radial glial fate. Cell 153, 535-549.
77. Susaki, E., Nakayama, K. & Nakayama, K. I. 2007. Cyclin D2 translocates p27 out of the nucleus and promotes its degradation at the G0-G1 transition. Mol. Cell. Biol. 27, 4626-4640.
78. Susaki, E. & Nakayama, K. I. 2007. Multiple mechanisms for p27(Kip1) translocation and degradation. Cell Cycle 6, 3015-3020.
79. Takahashi, T., Nowakowski, R. S. & Caviness, V. S. Jr, 1994. Mode of cell proliferation in the developing mouse neocortex. Proc. Natl Acad. Sci. USA 91, 375-379.
80. Takahashi, T., Nowakowski, R. S. & Caviness, V. S. Jr, 1995. The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J. Neurosci. 15, 6046-6057.
81. 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, 983-996.
82. Tsunekawa, Y., Britto, J. M., Takahashi, M., Polleux, F., Tan, S. S. & Osumi, N. 2012. Cyclin D2 in the basal process of neural progenitors is linked to non-equivalent cell fates. EMBO J. 31, 1879-1892.
83. Tsunekawa, Y. & Osumi, N. 2012. How to keep proliferative neural stem/progenitor cells: a critical role of asymmetric inheritance of cyclin D2. Cell Cycle 11, 3550-3554.
84. 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, 555-561.