Encoding and decoding time in neural development

Development Growth and Differentiation

Volumn 58, Issue 1, 2016, Pages 59-72

  Toma, Kenichi ^a   Wang, Tien Cheng ^a   Hanashima, Carina ^a,b  

^a RIKEN Center for Biosystems Dynamics Research   (Japan)

^b KOBE UNIVERSITY   (Japan)

Author keywords

Cell cycle; Neural stem cell; Temporal code; Timing; Transcriptional network

Indexed keywords

IDENTITY; NERVOUS SYSTEM DEVELOPMENT; ANIMAL; BIOLOGICAL MODEL; EMBRYOLOGY; HUMAN; NERVOUS SYSTEM; PHYSIOLOGY;

ANIMALS; HUMANS; MODELS, BIOLOGICAL; NERVOUS SYSTEM; NEUROGENESIS;

EID: 84955683661     PISSN: 00121592     EISSN: 1440169X     Source Type: Journal    
DOI: 10.1111/dgd.12257     Document Type: Review

References (69)

1. Angevine, J. B. Jr & Sidman, R. L. 1961. Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 192, 766-768.
2. 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, 881-890.
3. 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.
4. Belliveau, M. J. & Cepko, C. L. 1999. Extrinsic and intrinsic factors control the genesis of amacrine and cone cells in the rat retina. Development 126, 555-566.
5. Berger, C., Urban, J. & Technau, G. M. 2001. Stage-specific inductive signals in the Drosophila neuroectoderm control the temporal sequence of neuroblast specification. Development 128, 3243-3251.
6. Borodinsky, L. N., Root, C. M., Cronin, J. A., Sann, S. B., Gu, X. & Spitzer, N. C. 2004. Activity-dependent homeostatic specification of transmitter expression in embryonic neurons. Nature 429, 523-530.
7. Bossing, T., Udolph, G., Doe, C. Q. & Technau, G. M. 1996. The embryonic central nervous system lineages of Drosophila melanogaster. I. Neuroblast lineages derived from the ventral half of the neuroectoderm. Dev. Biol. 179, 41-64.
8. Burdon, T., Smith, A. & Savatier, P. 2002. Signalling, cell cycle and pluripotency in embryonic stem cells. Trends Cell Biol. 12, 432-438.
9. Carter-Dawson, L. D. & LaVail, M. M. 1979. Rods and cones in the mouse retina. II. Autoradiographic analysis of cell generation using tritiated thymidine. J. Comp. Neurol. 188, 263-272.
10. Charvet, C. J. & Striedter, G. F. 2009. Developmental basis for telencephalon expansion in waterfowl: enlargement prior to neurogenesis. Proc. Biol. Sci. 276, 3421-3427.
11. Charvet, C. J. & Striedter, G. F. 2010. Bigger brains cycle faster before neurogenesis begins: a comparison of brain development between chickens and bobwhite quail. Proc. Biol. Sci. 277, 3469-3475.
12. Chen, C. C., Balaban, E. & Jarvis, E. D. 2012. Interspecies avian brain chimeras reveal that large brain size differences are influenced by cell-interdependent processes. PLoS ONE, 7, e42477.
13. Cleary, M. D. & Doe, C. Q. 2006. Regulation of neuroblast competence: multiple temporal identity factors specify distinct neuronal fates within a single early competence window. Genes Dev. 20, 429-434.
14. Desai, A. R. & McConnell, S. K. 2000. Progressive restriction in fate potential by neural progenitors during cerebral cortical development. Development 127, 2863-2872.
15. Eiraku, M., Watanabe, K., Matsuo-Takasaki, M., Kawada, M., Yonemura, S., Matsumura, M., Wataya, T., Nishiyama, A., Muguruma, K. & Sasai, Y. 2008. Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell 3, 519-532.
16. Eiraku, M., Takata, N., Ishibashi, H., Kawada, M., Sakakura, E., Okuda, S., Sekiguchi, K., Adachi, T. & Sasai, Y. 2011. Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 472, 51-56.
17. Frantz, G. D. & McConnell, S. K. 1996. Restriction of late cerebral cortical progenitors to an upper-layer fate. Neuron 17, 55-61.
18. Fuentealba, L. C., Rompani, S. B., Parraguez, J. I., Obernier, K., Romero, R., Cepko, C. L. & Alvarez-Buylla, A. 2015. Embryonic origin of postnatal neural stem cells. Cell 161, 1644-1655.
19. Furutachi, S., Miya, H., Watanabe, T., Kawai, H., Yamasaki, N., Harada, Y., Imayoshi, I., Nelson, M., Nakayama, K. I., Hirabayashi, Y., et al. 2015. Slowly dividing neural progenitors are an embryonic origin of adult neural stem cells. Nat. Neurosci. 18, 657-665.
20. Gao, P., Postiglione, M. P., Krieger, T. G., Hernandez, L., Wang, C., Han, Z., Streicher, C., Papusheva, E., Insolera, R., Chugh, K., et al. 2014. Deterministic progenitor behavior and unitary production of neurons in the neocortex. Cell 159, 775-788.
21. Gaspard, N., Bouschet, T., Hourez, R., Dimidschstein, J., Naeije, G., van den Ameele, J., Espuny-Camacho, I., Herpoel, A., Passante, L., Schiffmann, S. N., et al. 2008. An intrinsic mechanism of corticogenesis from embryonic stem cells. Nature 455, 351-357.
22. Gomes, F. L., Zhang, G., Carbonell, F., Correa, J. A., Harris, W. A., Simons, B. D. & Cayouette, M. 2011. Reconstruction of rat retinal progenitor cell lineages in vitro reveals a surprising degree of stochasticity in cell fate decisions. Development 138, 227-235.
23. Gonzales, K. A., Liang, H., Lim, Y. S., Chan, Y. S., Yeo, J. C., Tan, C. P., Gao, B., Le, B., Tan, Z. Y., Low, K. Y., et al. 2015. Deterministic restriction on pluripotent state dissolution by Cell-Cycle pathways. Cell 162, 564-579.
24. Gorbunova, Y. V. & Spitzer, N. C. 2002. Dynamic interactions of cyclic AMP transients and spontaneous Ca(2+) spikes. Nature 418, 93-96.
25. Grosskortenhaus, R., Pearson, B. J., Marusich, A. & Doe, C. Q. 2005. Regulation of temporal identity transitions in Drosophila neuroblasts. Dev. Cell 8, 193-202.
26. Hanashima, C., Li, S. C., Shen, L., Lai, E. & Fishell, G. 2004. Foxg1 suppresses early cortical cell fate. Science 303, 56-59.
27. Hirabayashi, Y., Suzki, N., Tsuboi, M., Endo, T. A., Toyoda, T., Shinga, J., Koseki, H., Vidal, M. & Gotoh, Y. 2009. Polycomb limits the neurogenic competence of neural precursor cells to promote astrogenic fate transition. Neuron 63, 600-613.
28. Ikeda, M., Yoshioka, T. & Allen, C. N. 2003. Developmental and circadian changes in Ca2+ mobilization mediated by GABAA and NMDA receptors in the suprachiasmatic nucleus. Eur. J. Neurosci. 17, 58-70.
29. Imayoshi, I. & Kageyama, R. 2014. Oscillatory control of bHLH factors in neural progenitors. Trends Neurosci. 37, 531-538.
30. Imayoshi, I., Isomura, A., Harima, Y., Kawaguchi, K., Kori, H., Miyachi, H., Fujiwara, T., Ishidate, F. & Kageyama, R. 2013. Oscillatory control of factors determining multipotency and fate in mouse neural progenitors. Science 342, 1203-1208.
31. Isshiki, T., Pearson, B., Holbrook, S. & Doe, C. Q. 2001. Drosophila neuroblasts sequentially express transcription factors which specify the temporal identity of their neuronal progeny. Cell 106, 511-521.
32. Kadoshima, T., Sakaguchi, H., Nakano, T., Soen, M., Ando, S., Eiraku, M. & Sasai, Y. 2013. Self-organization of axial polarity, inside-out layer pattern, and species-specific progenitor dynamics in human ES cell-derived neocortex. Proc. Natl Acad. Sci. USA 110, 20284-20289.
33. Kanai, M. I., Okabe, M. & Hiromi, Y. 2005. seven-up Controls switching of transcription factors that specify temporal identities of Drosophila neuroblasts. Dev. Cell 8, 203-213.
34. Kishi, Y., Fujii, Y., Hirabayashi, Y. & Gotoh, Y. 2012. HMGA regulates the global chromatin state and neurogenic potential in neocortical precursor cells. Nat. Neurosci. 15, 1127-1133.
35. Kobayashi, D., Kobayashi, M., Matsumoto, K., Ogura, T., Nakafuku, M. & Shimamura, K. 2002. Early subdivisions in the neural plate define distinct competence for inductive signals. Development 129, 83-93.
36. Koester, H. J. & Sakmann, B. 2000. Calcium dynamics associated with action potentials in single nerve terminals of pyramidal cells in layer 2/3 of the young rat neocortex. J. Physiol. 529(Pt 3), 625-646.
37. Kohwi, M., Lupton, J. R., Lai, S. L., Miller, M. R. & Doe, C. Q. 2013. Developmentally regulated subnuclear genome reorganization restricts neural progenitor competence in Drosophila. Cell 152, 97-108.
38. Kumamoto, T., Toma, K., Gunadi, McKenna, W. L., Kasukawa, T., Katzman, S., Chen, B. & Hanashima, C. 2013. Foxg1 coordinates the switch from nonradially to radially migrating glutamatergic subtypes in the neocortex through spatiotemporal repression. Cell Rep. 3, 931-945.
39. La Vail, M. M., Rapaport, D. H. & Rakic, P. 1991. Cytogenesis in the monkey retina. J. Comp. Neurol. 309, 86-114.
40. Lagutin, O. V., Zhu, C. C., Kobayashi, D., Topczewski, J., Shimamura, K., Puelles, L., Russell, H. R., McKinnon, P. J., Solnica-Krezel, L. & Oliver, G. 2003. Six3 repression of Wnt signaling in the anterior neuroectoderm is essential for vertebrate forebrain development. Genes Dev. 17, 368-379.
41. Lancaster, M. A., Renner, M., Martin, C. A., Wenzel, D., Bicknell, L. S., Hurles, M. E., Homfray, T., Penninger, J. M., Jackson, A. P. & Knoblich, J. A. 2013. Cerebral organoids model human brain development and microcephaly. Nature 501, 373-379.
42. 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.
43. 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, 353-364.
44. Malmersjö, S., Rebellato, P., Smedler, E., Planert, H., Kanatani, S., Liste, I., Nanou, E., Sunner, H., Abdelhady, S., Zhang, S., Andäng, M., El Manira, A., Silberberg, G., Arenas, E. & Uhlén, P. 2013. Neural progenitors organize in small-world networks to promote cell proliferation. Proc. Natl Acad. Sci. USA 110, E1524-E1532.
45. McConnell, S. K. & Kaznowski, C. E. 1991. Cell cycle dependence of laminar determination in developing neocortex. Science 254, 282-285.
46. Nakano, T., Ando, S., Takata, N., Kawada, M., Muguruma, K., Sekiguchi, K., Saito, K., Yonemura, S., Eiraku, M. & Sasai, Y. 2012. Self-formation of optic cups and storable stratified neural retina from human ESCs. Cell Stem Cell 10, 771-785.
47. Nomura, T., Gotoh, H. & Ono, K. 2013. Changes in the regulation of cortical neurogenesis contribute to encephalization during amniote brain evolution. Nat. Commun. 4, 2206.
48. Nonaka-Kinoshita, M., Reillo, I., Artegiani, B., Martinez-Martinez, M. A., Nelson, M., Borrell, V. & Calegari, F. 2013. Regulation of cerebral cortex size and folding by expansion of basal progenitors. EMBO J. 32, 1817-1828.
49. Owens, D. F. & Kriegstein, A. R. 1998. Patterns of intracellular calcium fluctuation in precursor cells of the neocortical ventricular zone. J. Neurosci. 18, 5374-5388.
50. Pearson, B. J. & Doe, C. Q. 2003. Regulation of neuroblast competence in Drosophila. Nature 425, 624-628.
51. Rakic, P. 1974. Neurons in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Science 183, 425-427.
52. Rapaport, D. H. & Dorsky, R. I. 1998. Inductive competence, its signifiance in retinal cell fate determination and a role for Delta-Notch signaling. Semin. Cell Dev. Biol. 9, 241-247.
53. Rapaport, D. H., Wong, L. L., Wood, E. D., Yasumura, D. & LaVail, M. M. 2004. Timing and topography of cell genesis in the rat retina. J. Comp. Neurol. 474, 304-324.
54. Rockel, A. J., Hiorns, R. W. & Powell, T. P. 1980. The basic uniformity in structure of the neocortex. Brain 103, 221-244.
55. Salazar, C., Politi, A. Z. & Hofer, T. 2008. Decoding of calcium oscillations by phosphorylation cycles: analytic results. Biophys. J. 94, 1203-1215.
56. Schmid, A., Chiba, A. & Doe, C. Q. 1999. Clonal analysis of Drosophila embryonic neuroblasts: neural cell types, axon projections and muscle targets. Development 126, 4653-4689.
57. 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.
58. 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, 743-751.
59. Shimamura, K. & Rubenstein, J. L. 1997. Inductive interactions direct early regionalization of the mouse forebrain. Development 124, 2709-2718.
60. Shimojo, H., Ohtsuka, T. & Kageyama, R. 2008. Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron 58, 52-64.
61. Suda, Y., Matsuo, I. & Aizawa, S. 1997. Cooperation between Otx1 and Otx2 genes in developmental patterning of rostral brain. Mech. Dev. 69, 125-141.
62. Taghert, P. H., Doe, C. Q. & Goodman, C. S. 1984. Cell determination and regulation during development of neuroblasts and neurones in grasshopper embryo. Nature 307, 163-165.
63. Takahashi, T., Nowakowski, R. S. & Caviness, V. S. 1995. The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J. Neurosci. 15, 6046-6057.
64. Takahashi, T., Goto, T., Miyama, S., Nowakowski, R. S. & Caviness, V. S. 1999. Sequence of neuron origin and neocortical laminar fate: relation to cell cycle of origin in the developing murine cerebral wall. J. Neurosci. 19, 10357-10371.
65. Toma, K., Kumamoto, T. & Hanashima, C. 2014. The timing of upper-layer neurogenesis is conferred by sequential derepression and negative feedback from deep-layer neurons. J. Neurosci. 34, 13259-13276.
66. Waid, D. K. & McLoon, S. C. 1998. Ganglion cells influence the fate of dividing retinal cells in culture. Development 125, 1059-1066.
67. Weissman, T. A., Riquelme, P. A., Ivic, L., Flint, A. C. & Kriegstein, A. R. 2004. Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex. Neuron 43, 647-661.
68. Young, R. W. 1985. Cell differentiation in the retina of the mouse. Anat. Rec. 212, 199-205.
69. Yu, Y. C., He, S., Chen, S., Fu, Y., Brown, K. N., Yao, X. H., Ma, J., Gao, K. P., Sosinsky, G. E., Huang, K., et al. 2012. Preferential electrical coupling regulates neocortical lineage-dependent microcircuit assembly. Nature 486, 113-117.