Germinal zones in the developing cerebral cortex of ferret: Ontogeny, cell cycle kinetics, and diversity of progenitors

Cerebral Cortex

Volumn 22, Issue 9, 2012, Pages 2039-2054

  Reillo, Isabel ^a   Borrell, Víctor ^a  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

Author keywords

neurogenesis; OSVZ; Pax6; phosphovimentin; Tbr2

Indexed keywords

CYTOSKELETON PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; CELL CYCLE PARAMETERS; CELL RENEWAL; CELL SUBPOPULATION; COMBINATORIAL LIBRARY; COMPARATIVE ANATOMY; FERRET; GENE EXPRESSION; GENETIC DIFFERENCE; GERM LAYER; MOLECULAR DYNAMICS; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; ONTOGENY; PRIMATE; PRIORITY JOURNAL; STEM CELL; SUBVENTRICULAR ZONE;

ANIMALS; CELL CYCLE; CEREBRAL CORTEX; FERRETS; KINETICS; NEURAL STEM CELLS; NEUROGENESIS;

EID: 84864956222     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhr284     Document Type: Article

References (95)

1. Angevine JB, Sidman RL. 1961. Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature. 192:766-768.
2. Arai Y, Pulvers JN, Haffner C, Schilling B, Nusslein I, Calegari F, Huttner WB. 2011. Neural stem and progenitor cells shorten S-phase on commitment to neuron production. Nat Commun. 2:154.
3. Bayatti N, Moss JA, Sun L, Ambrose P, Ward JF, Lindsay S, Clowry GJ. 2008. A molecular neuroanatomical study of the developing human neocortex from 8 to 17 postconceptional weeks revealing the early differentiation of the subplate and subventricular zone. Cereb Cortex. 18:1536-1548. (Pubitemid 351882032)
4. Bayatti N, Sarma S, Shaw C, Eyre JA, Vouyiouklis DA, Lindsay S, Clowry GJ. 2008. Progressive loss of PAX6, TBR2, NEUROD and TBR1 mRNA gradients correlates with translocation of EMX2 to the cortical plate during human cortical development. Eur J Neurosci. 28:1449-1456.
5. Bayer SA, Altman J. 1991. Neocortical development. New York: Raven Press.
6. Bayer SA, Altman J. 2005. The human brain during the second trimester. New York: CRC Press.
7. Bilguvar K, Ozturk AK, Louvi A, Kwan KY, Choi M, Tatli B, Yalnizoglu D, Tuysuz B, Caglayan AO, Gokben S, et al. 2010. Whole-exome sequencing identifies recessive WDR62 mutations in severe brain malformations. Nature. 467:207-210.
8. Borrell V, Ruiz M, Del Rio JA, Soriano E. 1999. Development of commissural connections in the hippocampus of reeler mice: evidence of an inhibitory influence of Cajal-Retzius cells. Exp Neurol. 156:268-282. (Pubitemid 29205003)
9. Boulder Committee 1970. Embryonic vertebrate central nervous system: revised terminology. Anat Rec. 166:257-261.
10. Briscoe J, Pierani A, Jessell TM, Ericson J. 2000. A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell. 101:435-445.
11. Bystron I, Blakemore C, Rakic P. 2008. Development of the human cerebral cortex: Boulder Committee revisited. Nat Rev Neurosci. 9:110-122.
12. Bystron I, Rakic P, Molnar Z, Blakemore C. 2006. The first neurons of the human cerebral cortex. Nat Neurosci. 9:880-886. (Pubitemid 43980501)
13. Chenn A, McConnell SK. 1995. Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis. Cell. 82:631-641.
14. Chenn A, Walsh CA. 2002. Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science. 297:365-369. (Pubitemid 34790759)
15. Cheung AF, Kondo S, Abdel-Mannan O, Chodroff RA, Sirey TM, Bluy LE, Webber N, DeProto J, Karlen SJ, Krubitzer L, et al. 2010. The subventricular zone is the developmental milestone of a 6-layered neocortex: comparisons in metatherian and eutherian mammals. Cereb Cortex. 20:1071-1081.
16. deAzevedo LC, Fallet C, Moura-Neto V, Daumas-Duport C, Hedin- Pereira C, Lent R. 2003. Cortical radial glial cells in human fetuses: depth-correlated transformation into astrocytes. J Neurobiol. 55:288-298. (Pubitemid 36566148)
17. Dehay C, Kennedy H. 2007. Cell-cycle control and cortical development. Nat Rev Neurosci. 8:438-450. (Pubitemid 46789227)
18. Dorus S, Vallender EJ, Evans PD, Anderson JR, Gilbert SL, Mahowald M, Wyckoff GJ, Malcom CM, Lahn BT. 2004. Accelerated evolution of nervous system genes in the origin of Homo sapiens. Cell. 119:1027-1040. (Pubitemid 40037615)
19. Engel AK, Muller CM. 1989. Postnatal development of vimentinimmunoreactive radial glial cells in the primary visual cortex of the cat. J Neurocytol. 18:437-450. (Pubitemid 19253313)
20. Englund C, Fink A, Lau C, Pham D, Daza RA, Bulfone A, Kowalczyk T, Hevner RF. 2005. Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J Neurosci. 25:247-251. (Pubitemid 40110787)
21. Evans PD, Anderson JR, Vallender EJ, Gilbert SL, Malcom CM, Dorus S, Lahn BT. 2004. Adaptive evolution of ASPM, a major determinant of cerebral cortical size in humans. Hum Mol Genet. 13:489-494. (Pubitemid 38313208)
22. Fietz SA, Huttner WB. 2011. Cortical progenitor expansion, self-renewal and neurogenesis-a polarized perspective. Curr Opin Neurobiol. 21:23-35.
23. Fietz SA, Kelava I, Vogt J, Wilsch-Brauninger M, Stenzel D, Fish JL, 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.
24. Fish JL, Dehay C, Kennedy H, Huttner WB. 2008. Making bigger brains-the evolution of neural-progenitor-cell division. J Cell Sci. 121:2783-2793.
25. Flames N, Pla R, Gelman DM, Rubenstein JL, Puelles L, Marin O. 2007. Delineation of multiple subpallial progenitor domains by the combinatorial expression of transcriptional codes. J Neurosci. 27:9682-9695. (Pubitemid 47492179)
26. Gilbert SL, Dobyns WB, Lahn BT. 2005. Genetic links between brain development and brain evolution. Nat Rev Genet. 6:581-590. (Pubitemid 40910434)
27. Gotz M, Huttner WB. 2005. The cell biology of neurogenesis. Nat Rev Mol Cell Biol. 6:777-788. (Pubitemid 41726116)
28. Hansen DV, Lui JH, Parker PR, Kriegstein AR. 2010. Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature. 464:554-561.
29. 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 U S A. 101:3196-3201. (Pubitemid 38327757)
30. Haydar TF, Ang E, Jr, Rakic P. 2003. Mitotic spindle rotation and mode of cell division in the developing telencephalon. Proc Natl Acad Sci U S A. 100:2890-2895. (Pubitemid 36297594)
31. Hevner RF, Hodge RD, Daza RA, Englund C. 2006. Transcription factors in glutamatergic neurogenesis: conserved programs in neocortex, cerebellum, and adult hippocampus. Neurosci Res. 55:223-233. (Pubitemid 43766416)
32. Howard B, Chen Y, Zecevic N. 2006. Cortical progenitor cells in the developing human telencephalon. Glia. 53:57-66. (Pubitemid 43076212)
33. Huttner WB, Kosodo Y. 2005. Symmetric versus asymmetric cell division during neurogenesis in the developing vertebrate central nervous system. Curr Opin Cell Biol. 17:648-657. (Pubitemid 41540416)
34. Jackson CA, Peduzzi JD, Hickey TL. 1989. Visual cortex development in the ferret. I. Genesis and migration of visual cortical neurons. J Neurosci. 9:1242-1253. (Pubitemid 19116744)
35. Jakovcevski I, Mayer N, Zecevic N. 2011. Multiple origins of human neocortical interneurons are supported by distinct expression of transcription factors. Cereb Cortex. 21:1771-1782.
36. Knoblich JA. 2008. Mechanisms of asymmetric stem cell division. Cell. 132:583-597. (Pubitemid 351253698)
37. Konno D, Shioi G, Shitamukai A, Mori A, Kiyonari H, Miyata T, Matsuzaki F. 2008. Neuroepithelial progenitors undergo LGNdependent planar divisions to maintain self-renewability during mammalian neurogenesis. Nat Cell Biol. 10:93-101.
38. Kornack DR, Rakic P. 1998. Changes in cell-cycle kinetics during the development and evolution of primate neocortex. Proc Natl Acad Sci U S A. 95:1242-1246. (Pubitemid 28124943)
39. Kosodo Y, Roper K, Haubensak W, Marzesco AM, Corbeil D, Huttner WB. 2004. Asymmetric distribution of the apical plasma membrane during neurogenic divisions of mammalian neuroepithelial cells. EMBO J. 23:2314-2324. (Pubitemid 38833240)
40. Kostovic I, Rakic P. 1990. Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J Comp Neurol. 297:441-470. (Pubitemid 20222635)
41. Kowalczyk T, Pontious A, Englund C, Daza RA, Bedogni F, Hodge R, Attardo A, Bell C, Huttner WB, Hevner RF. 2009. Intermediate neuronal progenitors (basal progenitors) produce pyramidal-projection neurons for all layers of cerebral cortex. Cereb Cortex. 19:2439-2450.
42. Kriegstein A, Noctor S, Martinez-Cerdeno V. 2006. Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat Rev Neurosci. 7:883-890. (Pubitemid 44624180)
43. Letinic K, Zoncu R, Rakic P. 2002. Origin of GABAergic neurons in the human neocortex. Nature. 417:645-649. (Pubitemid 34614822)
44. Levitt P, Rakic P. 1980. Immunoperoxidase localization of glial fibrillary acidic protein in radial glial cells and astrocytes of the developing rhesus monkey brain. J Comp Neurol. 193:815-840. (Pubitemid 11233753)
45. Lui JH, Hansen DV, Kriegstein AR. 2011. Development and evolution of the human neocortex. Cell. 146:18-36.
46. Lukaszewicz A, Cortay V, Giroud P, Berland M, Smart I, Kennedy H, Dehay C. 2006. The concerted modulation of proliferation and migration contributes to the specification of the cytoarchitecture and dimensions of cortical areas. Cereb Cortex. 1(Suppl 16):i26-i34.
47. 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. (Pubitemid 41073877)
48. Malatesta P, Hartfuss E, Gotz M. 2000. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development. 127:5253-5263. (Pubitemid 32049182)
49. Martinez-Cerdeno V, Noctor SC, Kriegstein AR. 2006. The role of intermediate progenitor cells in the evolutionary expansion of the cerebral cortex. Cereb Cortex. 1(Suppl 16):i152-i161.
50. Mekel-Bobrov N, Gilbert SL, Evans PD, Vallender EJ, Anderson JR, Hudson RR, Tishkoff SA, Lahn BT. 2005. Ongoing adaptive evolution of ASPM, a brain size determinant in Homo sapiens. Science. 309:1720-1722. (Pubitemid 41285940)
51. Mo Z, Moore AR, Filipovic R, Ogawa Y, Kazuhiro I, Antic SD, Zecevic N. 2007. Human cortical neurons originate from radial glia and neuronrestricted progenitors. J Neurosci. 27:4132-4145. (Pubitemid 46597153)
52. Mo Z, Zecevic N. 2008. Is Pax6 critical for neurogenesis in the human fetal brain? Cereb Cortex. 18:1455-1465. (Pubitemid 351769802)
53. Mo Z, Zecevic N. 2009. Human fetal radial glia cells generate oligodendrocytes in vitro. Glia. 57:490-498.
54. Molnar Z, Vasistha NA, Garcia-Moreno F. 2011. Hanging by the tail: progenitor populations proliferate. Nat Neurosci. 14:538-540.
55. Neal J, Takahashi M, Silva M, Tiao G, Walsh CA, Sheen VL. 2007. Insights into the gyrification of developing ferret brain by magnetic resonance imaging. J Anat. 210:66-77. (Pubitemid 46040502)
56. Neumuller RA, Knoblich JA. 2009. Dividing cellular asymmetry: asymmetric cell division and its implications for stem cells and cancer. Genes Dev. 23:2675-2699.
57. Nicholas AK, Khurshid M, Desir J, Carvalho OP, Cox JJ, Thornton G, Kausar R, Ansar M, Ahmad W, Verloes A, et al. 2010. WDR62 is associated with the spindle pole and is mutated in human microcephaly. Nat Genet. 42:1010-1014.
58. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR. 2001. Neurons derived from radial glial cells establish radial units in neocortex. Nature. 409:714-720. (Pubitemid 32144516)
59. 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. 7:136-144. (Pubitemid 38129789)
60. Noctor SC, Martinez-Cerdeno V, Kriegstein AR. 2008. Distinct behaviors of neural stem and progenitor cells underlie cortical neurogenesis. J Comp Neurol. 508:28-44. (Pubitemid 351532566)
61. Pfaff S, Kintner C. 1998. Neuronal diversification: development of motor neuron subtypes. Curr Opin Neurobiol. 8:27-36. (Pubitemid 28151861)
62. Pollard KS, Salama SR, Lambert N, Lambot MA, Coppens S, Pedersen JS, Katzman S, King B, Onodera C, Siepel A, et al. 2006. An RNA gene expressed during cortical development evolved rapidly in humans. Nature. 443:167-172. (Pubitemid 44387600)
63. Puzzolo E, Mallamaci A. 2010. Cortico-cerebral histogenesis in the opossum Monodelphis domestica: generation of a hexalaminar neocortex in the absence of a basal proliferative compartment. Neural Dev. 5:8.
64. Rakic P. 1988. Specification of cerebral cortical areas. Science. 241:170-176.
65. Rakic P. 1995. A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. Trends Neurosci. 18:383-388.
66. Rakic P. 2009. Evolution of the neocortex: a perspective from developmental biology. Nat Rev Neurosci. 10:724-735.
67. Rakic S, Zecevic N. 2003. Emerging complexity of layer I in human cerebral cortex. Cereb Cortex. 13:1072-1083. (Pubitemid 37163206)
68. Ramón y Cajal S. 1911. Histologie du Système Nerveux de l'Homme et des Vertébrés. Paris: Maloine.
69. Reillo I, de Juan Romero C, Garcia-Cabezas MA, Borrell V. 2011. A role for intermediate radial glia in the tangential expansion of the mammalian cerebral cortex. Cereb Cortex. 21:1674-1694.
70. Ross ME, Walsh CA. 2001. Human brain malformations and their lessons for neuronal migration. Annu Rev Neurosci. 24:1041-1070. (Pubitemid 32695253)
71. Sansom SN, Griffiths DS, Faedo A, Kleinjan DJ, Ruan Y, Smith J, van Heyningen V, Rubenstein JL, Livesey FJ. 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.
72. Sauer ME, Walker BE. 1959. Radioautographic study of interkinetic nuclear migration in the neural tube. Proc Soc Exp Biol Med. 101:557-560.
73. Schmechel DE, Rakic P. 1979. A Golgi study of radial glial cells in developing monkey telencephalon: morphogenesis and transformation into astrocytes. Anat Embryol (Berl). 156:115-152. (Pubitemid 9213953)
74. Sessa A, Mao CA, Hadjantonakis AK, Klein WH, Broccoli V. 2008. Tbr2 directs conversion of radial glia into basal precursors and guides neuronal amplification by indirect neurogenesis in the developing neocortex. Neuron. 60:56-69.
75. Sheen VL, Walsh CA. 2003. Developmental genetic malformations of the cerebral cortex. Curr Neurol Neurosci Rep. 3:433-441. (Pubitemid 38899033)
76. Shirasaki R, Pfaff SL. 2002. Transcriptional codes and the control of neuronal identity. Annu Rev Neurosci. 25:251-281. (Pubitemid 34748018)
77. 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.
78. Sidman RL, Rakic P. 1973. Neuronal migration, with special reference to developing human brain: a review. Brain Res. 62:1-35.
79. Siegenthaler JA, Ashique AM, Zarbalis K, Patterson KP, Hecht JH, Kane MA, Folias AE, Choe Y, May SR, Kume T, et al. 2009. Retinoic acid from the meninges regulates cortical neuron generation. Cell. 139:597-609.
80. Smart IH, Dehay C, Giroud P, Berland M, Kennedy H. 2002. 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. 12:37-53. (Pubitemid 33152016)
81. Smart IH, McSherry GM. 1986. Gyrus formation in the cerebral cortex of the ferret. II. Description of the internal histological changes. J Anat. 147:27-43. (Pubitemid 16051845)
82. Takahashi T, Misson JP, Caviness VS, Jr. 1990. Glial process elongation and branching in the developing murine neocortex: a qualitative and quantitative immunohistochemical analysis. J Comp Neurol. 302:15-28.
83. Takahashi T, Nowakowski RS, Caviness VS, Jr. 1993. Cell cycle parameters and patterns of nuclear movement in the neocortical proliferative zone of the fetal mouse. J Neurosci. 13:820-833. (Pubitemid 23045162)
84. Takahashi T, Nowakowski RS, Caviness VS, Jr. 1995a. Early ontogeny of the secondary proliferative population of the embryonic murine cerebral wall. J Neurosci. 15:6058-6068.
85. Takahashi T, Nowakowski RS, Caviness VS, Jr. 1995b. The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J Neurosci. 15:6046-6057.
86. Tekki-Kessaris N, Woodruff R, Hall AC, Gaffield W, Kimura S, Stiles CD, Rowitch DH, Richardson WD. 2001. Hedgehog-dependent oligodendrocyte lineage specification in the telencephalon. Development. 128:2545-2554. (Pubitemid 32685096)
87. Voigt T. 1989. Development of glial cells in the cerebral wall of ferrets: direct tracing of their transformation from radial glia into astrocytes. J Comp Neurol. 289:74-88. (Pubitemid 19263991)
88. Wang X, Tsai JW, Lamonica B, Kriegstein AR. 2011. A new subtype of progenitor cell in the mouse embryonic neocortex. Nat Neurosci. 14:555-561.
89. Weissman T, Noctor SC, Clinton BK, Honig LS, Kriegstein AR. 2003. Neurogenic radial glial cells in reptile, rodent and human: from mitosis to migration. Cereb Cortex. 13:550-559. (Pubitemid 36613161)
90. Welker W. 1990. Why does cerebral cortex fissure and fold? A review of determinants of gyri and sulci. In: Peters A, Jones EG, editors. Cerebral cortex. New York: Plenum Press. p. 3-136.
91. Yu TW, Mochida GH, Tischfield DJ, Sgaier SK, Flores-Sarnat L, Sergi CM, Topcu M, McDonald MT, Barry BJ, Felie JM, et al. 2010. Mutations in WDR62, encoding a centrosome-associated protein, cause microcephaly with simplified gyri and abnormal cortical architecture. Nat Genet. 42:1015-1020.
92. Yu X, Zecevic N. 2011. Dorsal radial glial cells have the potential to generate cortical interneurons in human but not in mouse brain. J Neurosci. 31:2413-2420.
93. Zecevic N. 2004. Specific characteristic of radial glia in the human fetal telencephalon. Glia. 48:27-35. (Pubitemid 39390845)
94. Zecevic N, Chen Y, Filipovic R. 2005. Contributions of cortical subventricular zone to the development of the human cerebral cortex. J Comp Neurol. 491:109-122. (Pubitemid 41262863)
95. Zecevic N, Hu F, Jakovcevski I. 2011. Interneurons in the developing human neocortex. Dev Neurobiol. 71:18-33.