Mechanisms of brain evolution: Regulation of neural progenitor cell diversity and cell cycle length

Neuroscience Research

Volumn 86, Issue , 2014, Pages 14-24

  Borrell, Victor ^a   Calegari, Federico ^b  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^b CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

Author keywords

Brain evolution; Cell cycle; Cell fate determination; Cortical architecture; Gyrification; Neural progenitor cells

Indexed keywords

ASTRONOMY; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN SIZE; CELL CYCLE PHASE; CELL CYCLE REGULATION; CELL FUNCTION; CELL TYPE; EVOLUTION; HUMAN; MOLECULAR MECHANICS; NEURAL STEM CELL; NEUROANATOMY; PHENOTYPE; PHYLOGENY; REVIEW; ANIMAL; BRAIN; CELL CYCLE; CELL DIFFERENTIATION; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY;

ANIMALS; BIOLOGICAL EVOLUTION; BRAIN; CELL CYCLE; CELL DIFFERENTIATION; HUMANS; NEURAL STEM CELLS; NEUROGENESIS;

EID: 84912570165     PISSN: 01680102     EISSN: 18728111     Source Type: Journal    
DOI: 10.1016/j.neures.2014.04.004     Document Type: Review

References (100)

1. Agata K., Inoue T. Survey of the differences between regenerative and non-regenerative animals. Dev. Growth Differ. 2012, 54:143-152.
2. Ali F., Hindley C., McDowell G., Deibler R., Jones A., Kirschner M., Guillemot F., Philpott A. Cell cycle-regulated multi-site phosphorylation of Neurogenin 2 coordinates cell cycling with differentiation during neurogenesis. Development 2011, 138:4267-4277.
3. Altman J. Are new neurons formed in the brains of adult mammals?. Science 1962, 135:1127-1128.
4. Arai Y., Pulvers J.N., Haffner C., Schilling B., Nusslein I., Calegari F., Huttner W.B. Neural stem and progenitor cells shorten S-phase on commitment to neuron production. Nat. Commun. 2011, 2:154.
5. Artegiani B., Lindemann D., Calegari F. Overexpression of cdk4 and cyclinD1 triggers greater expansion of neural stem cells in the adult mouse brain. J. Exp. Med. 2011, 208:937-948.
6. Attardo A., Calegari F., Haubensak W., Wilsch-Brauninger M., Huttner W.B. Live imaging at the onset of cortical neurogenesis reveals differential appearance of the neuronal phenotype in apical versus basal progenitor progeny. PLoS ONE 2008, 3:e2388.
7. Betizeau M., Cortay V., Patti D., Pfister S., Gautier E., Bellemin-Menard A., Afanassieff M., Huissoud C., Douglas R.J., Kennedy H., et al. Precursor diversity and complexity of lineage relationships in the outer subventricular zone of the primate. Neuron 2013, 80:442-457.
8. Beukelaers P., Vandenbosch R., Caron N., Nguyen L., Belachew S., Moonen G., Kiyokawa H., Barbacid M., Santamaria D., Malgrange B. Cdk6-dependent regulation of G(1) length controls adult neurogenesis. Stem Cells 2011, 29:713-724.
9. 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., et al. Transcriptional role of cyclin D1 in development revealed by a genetic-proteomic screen. Nature 2010, 463:374-378.
10. Borrell V., Reillo I. Emerging roles of neural stem cells in cerebral cortex development and evolution. Dev. Neurobiol. 2012, 72:955-971.
11. Boulder Committee Embryonic vertebrate central nervous system: revised terminology. The Boulder Committee. Anat. Rec. 1970, 166:257-261.
12. Calegari F., Haubensak W., Haffner C., Huttner W.B. Selective lengthening of the cell cycle in the neurogenic subpopulation of neural progenitor cells during mouse brain development. J. Neurosci. 2005, 25:6533-6538.
13. Calegari F., Huttner W.B. An inhibition of cyclin-dependent kinases that lengthens, but does not arrest, neuroepithelial cell cycle induces premature neurogenesis. J. Cell Sci. 2003, 116:4947-4955.
14. Callaway E.M. Prenatal development of layer-specific local circuits in primary visual cortex of the macaque monkey. J. Neurosci. 1998, 18:1505-1527.
15. Caviness V.S., Takahashi T., Nowakowski R.S. Numbers, time and neocortical neuronogenesis: a general developmental and evolutionary model. Trends Neurosci. 1995, 18:379-383.
16. Chen C.C., Balaban E., Jarvis E.D. Interspecies avian brain chimeras reveal that large brain size differences are influenced by cell-interdependent processes. PLoS One 2012, 7:e42477.
17. Cheung A.F., Kondo S., Abdel-Mannan O., Chodroff R.A., Sirey T.M., Bluy L.E., Webber N., DeProto J., Karlen S.J., Krubitzer L., et al. The subventricular zone is the developmental milestone of a 6-layered neocortex: comparisons in metatherian and eutherian mammals. Cereb. Cortex 2010, 20:1071-1081.
18. Cheung A.F., Pollen A.A., Tavare A., DeProto J., Molnar Z. Comparative aspects of cortical neurogenesis in vertebrates. J. Anat. 2007, 211:164-176.
19. Defelipe J. The evolution of the brain, the human nature of cortical circuits, and intellectual creativity. Front. Neuroanat. 2011, 5:29.
20. Dehay C., Giroud P., Berland M., Smart I., Kennedy H. Modulation of the cell cycle contributes to the parcellation of the primate visual cortex. Nature 1993, 366:464-466.
21. Dehay C., Kennedy H. Cell-cycle control and cortical development. Nat. Rev. Neurosci. 2007, 8:438-450.
22. Felleman D.J., Van Essen D.C. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1991, 1:1-47.
23. Fietz S.A., Huttner W.B. Cortical progenitor expansion, self-renewal and neurogenesis - a polarized perspective. Curr. Opin. Neurobiol. 2011, 21:23-35.
24. 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. OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling. Nat. Neurosci. 2010, 13:690-699.
25. Fietz S.A., Lachmann R., Brandl H., Kircher M., Samusik N., Schroder R., Lakshmanaperumal N., Henry I., Vogt J., Riehn A., et al. Transcriptomes of germinal zones of human and mouse fetal neocortex suggest a role of extracellular matrix in progenitor self-renewal. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:11836-11841.
26. Finlay B.L., Darlington R.B. Linked regularities in the development and evolution of mammalian brains. Science 1995, 268:1578-1584.
27. Fujita S. Kinetics of cellular proliferation. Exp. Cell Res. 1962, 28:52-60.
28. Garcia-Moreno F., Vasistha N.A., Trevia N., Bourne J.A., Molnar Z. Compartmentalization of cerebral cortical germinal zones in a lissencephalic primate and gyrencephalic rodent. Cereb. Cortex 2012, 22:482-492.
29. Gotz M., Huttner W.B. The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 2005, 6:777-788.
30. Guo C., Eckler M.J., McKenna W.L., McKinsey G.L., Rubenstein J.L., Chen B. Fezf2 expression identifies a multipotent progenitor for neocortical projection neurons, astrocytes, and oligodendrocytes. Neuron 2013, 80:1167-1174.
31. Han X., Chen M., Wang F., Windrem M., Wang S., Shanz S., Xu Q., Oberheim N.A., Bekar L., Betstadt S., et al. Forebrain engraftment by human glial progenitor cells enhances synaptic plasticity and learning in adult mice. Cell Stem Cell 2013, 12:342-353.
32. Hansen D.V., Lui J.H., Parker P.R., Kriegstein A.R. Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 2010, 464:554-561.
33. Herculano-Houzel S. The human brain in numbers: a linearly scaled-up primate brain. Front. Hum. Neurosci. 2009, 3:31.
34. Hevner R.F., Haydar T.F. The (not necessarily) convoluted role of basal radial glia in cortical neurogenesis. Cereb. Cortex 2012, 22:465-468.
35. Hindley C., Philpott A. Co-ordination of cell cycle and differentiation in the developing nervous system. Biochem. J. 2012, 444:375-382.
36. Hodge R.D., D'Ercole A.J., O'Kusky J.R. Insulin-like growth factor-I accelerates the cell cycle by decreasing g1 phase length and increases cell cycle reentry in the embryonic cerebral cortex. J. Neurosci. 2004, 24:10201-10210.
37. Jerison H.J. Quantitative analysis of evolution of the brain in mammals. Science 1961, 133:1012-1014.
38. Kandel E.R., Schwartz J.H., Jessell T.M. Principles of Neural Science 2000, McGraw-Hill. 4th ed.
39. Kawauchi T., Shikanai M., Kosodo Y. Extra-cell cycle regulatory functions of cyclin-dependent kinases (CDK) and CDK inhibitor proteins contribute to brain development and neurological disorders. Genes Cells 2013, 18:176-194.
40. Kelava I., Lewitus E., Huttner W.B. The secondary loss of gyrencephaly as an example of evolutionary phenotypical reversal. Front. Neuroanat. 2013, 7:16.
41. Kelava I., Reillo I., Murayama A.Y., Kalinka A.T., Stenzel D., Tomancak P., Matsuzaki F., Lebrand C., Sasaki E., Schwamborn J.C., et al. Abundant occurrence of basal radial glia in the subventricular zone of embryonic neocortex of a lissencephalic primate, the common marmoset Callithrix jacchus. Cereb. Cortex 2012, 22:469-481.
42. King N. The unicellular ancestry of animal development. Dev. Cell 2004, 7:313-325.
43. Kornack D.R., Rakic P. Changes in cell-cycle kinetics during the development and evolution of primate neocortex. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:1242-1246.
44. Korr H. Proliferation of different cell types in the brain. Adv. Anat. Embryol. Cell Biol. 1980, 61:1-72.
45. Kowalczyk T., Pontious A., Englund C., Daza R.A., Bedogni F., Hodge R., Attardo A., Bell C., Huttner W.B., Hevner R.F. Intermediate neuronal progenitors (basal progenitors) produce pyramidal-projection neurons for all layers of cerebral cortex. Cereb. Cortex 2009, 19:2439-2450.
46. Krubitzer L. The magnificent compromise: cortical field evolution in mammals. Neuron 2007, 56:201-208.
47. Kurosaka H., Takano-Yamamoto T., Yamashiro T., Agata K. Comparison of molecular and cellular events during lower jaw regeneration of newt (Cynops pyrrhogaster) and West African clawed frog (Xenopus tropicalis). Dev. Dyn. 2008, 237:354-365.
48. Lange C., Calegari F. Cdks and cyclins link G(1) length and differentiation of embryonic, neural and hematopoietic stem cells. Cell Cycle 2010, 9:1893-1900.
49. Lange C., Huttner W.B., Calegari F. Cdk4/cyclinD1 overexpression in neural stem cells shortens G1, delays neurogenesis, and promotes the generation and expansion of basal progenitors. Cell Stem Cell 2009, 5:320-331.
50. Lim S., Kaldis P. Cdks, cyclins and CKIs: roles beyond cell cycle regulation. Development 2013, 140:3079-3093.
51. Lui J.H., Hansen D.V., Kriegstein A.R. Development and evolution of the human neocortex. Cell 2011, 146:18-36.
52. Lukaszewicz A., Savatier P., Cortay V., Giroud P., Huissoud C., Berland M., Kennedy H., Dehay C. G1 phase regulation, area-specific cell cycle control, and cytoarchitectonics in the primate cortex. Neuron 2005, 47:353-364.
53. Lukaszewicz A., Savatier P., Cortay V., Kennedy H., Dehay C. Contrasting effects of basic fibroblast growth factor and neurotrophin 3 on cell cycle kinetics of mouse cortical stem cells. J. Neurosci. 2002, 22:6610-6622.
54. McConnell S.K. Constructing the cerebral cortex: neurogenesis and fate determination. Neuron 1995, 15:761-768.
55. McConnell S.K., Kaznowski C.E. Cell cycle dependence of laminar determination in developing neocortex. Science 1991, 254:282-285.
56. McNamara J.M., Houston A.I. State-dependent life histories. Nature 1996, 380:215-221.
57. Molnar Z., Metin C., Stoykova A., Tarabykin V., Price D.J., Francis F., Meyer G., Dehay C., Kennedy H. Comparative aspects of cerebral cortical development. Eur. J. Neurosci. 2006, 23:921-934.
58. Molnar Z., Pollen A. How unique is the human neocortex?. Development 2014, 141:11-16.
59. Morton A.J., Avanzo L. Executive decision-making in the domestic sheep. PLoS One 2011, 6:e15752.
60. Newmark P.A., Sanchez Alvarado A. Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev. Biol. 2000, 220:142-153.
61. Nguyen L., Besson A., Heng J.I., Schuurmans C., Teboul L., Parras C., Philpott A., Roberts J.M., Guillemot F. p27kip1 independently promotes neuronal differentiation and migration in the cerebral cortex. Genes Dev. 2006, 20:1511-1524.
62. Noctor S.C., Martinez-Cerdeno V., Ivic L., Kriegstein A.R. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 2004, 7:136-144.
63. Nomura T., Gotoh H., Ono K. Changes in the regulation of cortical neurogenesis contribute to encephalization during amniote brain evolution. Nat. Commun. 2013, 4:2206.
64. Nonaka-Kinoshita M., Reillo I., Artegiani B., Angeles Martinez-Martinez M., Nelson M., Borrell V., Calegari F. Regulation of cerebral cortex size and folding by expansion of basal progenitors. EMBO J. 2013, 32:1817-1828.
65. Orford K.W., Scadden D.T. Deconstructing stem cell self-renewal: genetic insights into cell-cycle regulation. Nat. Rev. Genet. 2008, 9:115-128.
66. Panhuysen M., Vogt Weisenhorn D.M., Blanquet V., Brodski C., Heinzmann U., Beisker W., Wurst W. Effects of Wnt1 signaling on proliferation in the developing mid-/hindbrain region. Mol. Cell. Neurosci. 2004, 26:101-111.
67. Pilaz L.J., Patti D., Marcy G., Ollier E., Pfister S., Douglas R.J., Betizeau M., Gautier E., Cortay V., Doerflinger N., et al. Forced G1-phase reduction alters mode of division, neuron number, and laminar phenotype in the cerebral cortex. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:21924-21929.
68. Pilz G.A., Shitamukai A., Reillo I., Pacary E., Schwausch J., Stahl R., Ninkovic J., Snippert H.J., Clevers H., Godinho L., et al. Amplification of progenitors in the mammalian telencephalon includes a new radial glial cell type. Nat. Commun. 2013, 4:2125.
69. Ponti G., Obernier K., Guinto C., Jose L., Bonfanti L., Alvarez-Buylla A. Cell cycle and lineage progression of neural progenitors in the ventricular-subventricular zones of adult mice. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:E1045-E1054.
70. Porlan E., Morante-Redolat J.M., Marques-Torrejon M.A., Andreu-Agullo C., Carneiro C., Gomez-Ibarlucea E., Soto A., Vidal A., Ferron S.R., Farinas I. Transcriptional repression of Bmp2 by p21(Waf1/Cip1) links quiescence to neural stem cell maintenance. Nat. Neurosci. 2013, 16:1567-1575.
71. Purves D. Body and Brain: A Trophic Theory of Neural Connections 1988, Harvard University Press, Cambridge, MA.
72. Rakic P. Radial versus tangential migration of neuronal clones in the developing cerebral cortex. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:11323-11327.
73. Rakic P. A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. Trends Neurosci. 1995, 18:383-388.
74. Rakic P. Evolution of the neocortex: a perspective from developmental biology. Nat. Rev. Neurosci. 2009, 10:724-735.
75. Ramón, Cajal S. Histologie du Système Nerveux de l'Homme et des Vertébrés 1911, Maloine, Paris.
76. Ratineau C., Petry M.W., Mutoh H., Leiter A.B. Cyclin D1 represses the basic helix-loop-helix transcription factor, BETA2/NeuroD. J. Biol. Chem. 2002, 277:8847-8853.
77. Reillo I., Borrell V. Germinal zones in the developing cerebral cortex of ferret: ontogeny, cell cycle kinetics, and diversity of progenitors. Cereb. Cortex 2012, 22:2039-2054.
78. Reillo I., de Juan Romero C., Garcia-Cabezas M.A., Borrell V. A role for intermediate radial glia in the tangential expansion of the mammalian cerebral cortex. Cereb. Cortex 2011, 21:1674-1694.
79. Rink J.C. Stem cell systems and regeneration in planaria. Dev. Genes Evol. 2013, 223:67-84.
80. Roth G., Dicke U. Evolution of the brain and intelligence. Trends Cogn. Sci. 2005, 9:250-257.
81. Salomoni P., Calegari F. Cell cycle control of mammalian neural stem cells: putting a speed limit on G1. Trends Cell Biol. 2010, 5:332-342.
82. Schultze B., Korr H. Cell kinetic studies of different cell types in the developing and adult brain of the rat and the mouse: a review. Cell Tissue Kinet. 1981, 14:309-325.
83. Shitamukai A., Konno D., Matsuzaki F. 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. 2011, 31:3683-3695.
84. Sidman R.L., Rakic P. Neuronal migration, with special reference to developing human brain: a review. Brain Res. 1973, 62:1-35.
85. Singh A.M., Dalton S. The cell cycle and Myc intersect with mechanisms that regulate pluripotency and reprogramming. Cell Stem Cell 2009, 5:141-149.
86. Smart I.H., Dehay C., Giroud P., Berland M., Kennedy H. Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. Cereb. Cortex 2002, 12:37-53.
87. 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., et al. Trnp1 regulates expansion and folding of the mammalian cerebral cortex by control of radial glial fate. Cell 2013, 153:535-549.
88. Takahashi T., Nowakowski R.S., Caviness V.S. The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J. Neurosci. 1995, 15:6046-6057.
89. Taylor J.H., Woods P.S., Hughes W.L. The organization and duplication of chromosomes as revealed by autoradiographic studies using tritium-labeled thymidinee. Proc. Natl. Acad. Sci. U. S. A. 1957, 43:122-128.
90. Tissir F., Lambert De Rouvroit C., Sire J.Y., Meyer G., Goffinet A.M. Reelin expression during embryonic brain development in Crocodylus niloticus. J. Comp. Neurol. 2003, 457:250-262.
91. True J.R., Carroll S.B. Gene co-option in physiological and morphological evolution. Annu. Rev. Cell Dev. Biol. 2002, 18:53-80.
92. Tuoc T.C., Boretius S., Sansom S.N., Pitulescu M.E., Frahm J., Livesey F.J., Stoykova A. Chromatin regulation by BAF170 controls cerebral cortical size and thickness. Dev. Cell 2013, 25:256-269.
93. Tury A., Mairet-Coello G., DiCicco-Bloom E. The cyclin-dependent kinase inhibitor p57Kip2 regulates cell cycle exit, differentiation, and migration of embryonic cerebral cortical precursors. Cereb. Cortex 2011, 21:1840-1856.
94. von Waechter R., Jaensch B. Generation times of the matrix cells during embryonic brain development: an autoradiographic study in rats. Brain Res. 1972, 46:235-250.
95. Wang S.S., Shultz J.R., Burish M.J., Harrison K.H., Hof P.R., Towns L.C., Wagers M.W., Wyatt K.D. Functional trade-offs in white matter axonal scaling. J. Neurosci. 2008, 28:4047-4056.
96. Wang X., Tsai J.W., LaMonica B., Kriegstein A.R. A new subtype of progenitor cell in the mouse embryonic neocortex. Nat. Neurosci. 2011, 14:555-561.
97. Weissman I.L. Stem cells: units of development, units of regeneration, and units in evolution. Cell 2000, 100:157-168.
98. Welker W.I. The significance of foliation and fissuration of cerebellar cortex. The cerebellar folium as a fundamental unit of sensorimotor integration. Arch. Ital. Biol. 1990, 128:87-109.
99. Wilson D.B., Hendrickx A.G. Quantitative aspects of the cell cycle in the cranial neural tube of the rhesus monkey (Macaca mulatta) during early stages of gestation. J. Craniofac. Genet. Dev. Biol. 1986, 6:363-368.
100. Zilles K., Palomero-Gallagher N., Amunts K. Development of cortical folding during evolution and ontogeny. Trends Neurosci. 2013, 36:275-284.