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eLife Volume 9 ,2020-04-01
A discrete subtype of neural progenitor crucial for cortical folding in the gyrencephalic mammalian brain
Neuroscience
Naoyuki Matsumoto 1 Satoshi Tanaka 1 , 2 Toshihide Horiike 1 Yohei Shinmyo 1 Hiroshi Kawasaki 1
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DOI:10.7554/eLife.54873
Received 2020-01-03, accepted for publication 2020-04-01, Published 2020-04-01
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摘要

An increase in the diversity of neural progenitor subtypes and folding of the cerebral cortex are characteristic features which appeared during the evolution of the mammalian brain. Here, we show that the expansion of a specific subtype of neural progenitor is crucial for cortical folding. We found that outer radial glial (oRG) cells can be subdivided by HOPX expression in the gyrencephalic cerebral cortex of ferrets. Compared with HOPX-negative oRG cells, HOPX-positive oRG cells had high self-renewal activity and were accumulated in prospective gyral regions. Using our in vivo genetic manipulation technique for ferrets, we found that the number of HOPX-positive oRG cells and their self-renewal activity were regulated by sonic hedgehog (Shh) signaling. Importantly, suppressing Shh signaling reduced HOPX-positive oRG cells and cortical folding, while enhancing it had opposing effects. Our results reveal a novel subtype of neural progenitor important for cortical folding in gyrencephalic mammalian cerebral cortex.

关键词

Other;ferret;HOPX;sonic hedgehog;outer radial glial cells;cortical folding

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© 2020, Matsumoto et al
http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

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Naoyuki Matsumoto,Satoshi Tanaka,Toshihide Horiike,Yohei Shinmyo,Hiroshi Kawasaki. A discrete subtype of neural progenitor crucial for cortical folding in the gyrencephalic mammalian brain. eLife ,Vol.9(2020)

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参考文献
[1] C de Juan Romero, C Bruder, U Tomasello, JM Sanz‐Anquela. et al.(2015). Discrete domains of gene expression in germinal layers distinguish the development of gyrencephaly. The EMBO Journal.34:1859-1874. DOI: 10.1016/j.devbrainres.2005.03.013.
[2] V Fernández, C Llinares-Benadero, V Borrell. (2016). Cerebral cortex expansion and folding: what have we learned?. The EMBO Journal.35:1021-1044. DOI: 10.1016/j.devbrainres.2005.03.013.
[3] TJ Nowakowski, AA Pollen, C Sandoval-Espinosa, AR Kriegstein. et al.(2016). Transformation of the radial Glia scaffold demarcates two stages of human cerebral cortex development. Neuron.91:1219-1227. DOI: 10.1016/j.devbrainres.2005.03.013.
[4] C Dehay, H Kennedy, KS Kosik. (2015). The outer subventricular zone and primate-specific cortical complexification. Neuron.85:683-694. DOI: 10.1016/j.devbrainres.2005.03.013.
[5] L Kwong, MF Bijlsma, H Roelink. (2014). Shh-mediated degradation of hhip allows cell autonomous and non-cell autonomous shh signalling. Nature Communications.5. DOI: 10.1016/j.devbrainres.2005.03.013.
[6] H Kawasaki, T Toda, K Tanno. (2013). In vivo genetic manipulation of cortical progenitors in gyrencephalic carnivores using in utero electroporation. Biology Open.2:95-100. DOI: 10.1016/j.devbrainres.2005.03.013.
[7] A Kriegstein, S Noctor, V Martínez-Cerdeño. (2006). Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nature Reviews Neuroscience.7:883-890. DOI: 10.1016/j.devbrainres.2005.03.013.
[8] T Yoshino, H Murai, D Saito. (2016). Hedgehog–BMP signalling establishes dorsoventral patterning in lateral plate mesoderm to trigger gonadogenesis in chicken embryos. Nature Communications.7. DOI: 10.1016/j.devbrainres.2005.03.013.
[9] M Nonaka-Kinoshita, I Reillo, B Artegiani, M Ángeles Martínez-Martínez. et al.(2013). Regulation of cerebral cortex size and folding by expansion of basal progenitors. The EMBO Journal.32:1817-1828. DOI: 10.1016/j.devbrainres.2005.03.013.
[10] OR Yabut, SJ Pleasure. (2018). Sonic hedgehog signaling rises to the surface: emerging roles in neocortical development. Brain Plasticity.3:119-128. DOI: 10.1016/j.devbrainres.2005.03.013.
[11] K Yu, D Mo, M Wu, H Chen. et al.(2014). Activating transcription factor 4 regulates adipocyte differentiation via altering the coordinate expression of CCATT/enhancer binding protein β and peroxisome proliferator-activated receptor γ. FEBS Journal.281:2399-2409. DOI: 10.1016/j.devbrainres.2005.03.013.
[12] Z Molnár, C Métin, A Stoykova, V Tarabykin. et al.(2006). Comparative aspects of cerebral cortical development. European Journal of Neuroscience.23:921-934. DOI: 10.1016/j.devbrainres.2005.03.013.
[13] I Reillo, C de Juan Romero, MÁ García-Cabezas, V Borrell. et al.(2011). A role for intermediate radial Glia in the tangential expansion of the mammalian cerebral cortex. Cerebral Cortex.21:1674-1694. DOI: 10.1016/j.devbrainres.2005.03.013.
[14] M Zakaria, J Ferent, I Hristovska, Y Laouarem. et al.(2019). The shh receptor boc is important for myelin formation and repair. Development.146. DOI: 10.1016/j.devbrainres.2005.03.013.
[15] B Berse, W Szczecinska, I Lopez-Coviella, B Madziar. et al.(2005). Expression of high affinity choline transporter during mouse development in vivo and its upregulation by NGF and BMP-4 in vitro. Developmental Brain Research.157:132-140. DOI: 10.1016/j.devbrainres.2005.03.013.
[16] Y Liu, A Beyer, R Aebersold. (2016). On the dependency of cellular protein levels on mRNA abundance. Cell.165:535-550. DOI: 10.1016/j.devbrainres.2005.03.013.
[17] J Lee, KA Platt, P Censullo, A Ruiz i Altaba. et al.(1997). Gli1 is a target of sonic hedgehog that induces ventral neural tube development. Development.124:2537-2552. DOI: 10.1016/j.devbrainres.2005.03.013.
[18] T Lahav, D Sivam, H Volpin, M Ronen. et al.(2011). Multiple levels of gene regulation mediate differentiation of the intracellular pathogen. The FASEB Journal.25:515-525. DOI: 10.1016/j.devbrainres.2005.03.013.
[19] X Heng, Q Guo, AW Leung, JY Li. et al.(2017). Analogous mechanism regulating formation of neocortical basal radial Glia and cerebellar bergmann Glia. eLife.6. DOI: 10.1016/j.devbrainres.2005.03.013.
[20] K Sawada. (2019). Follow-up study of subventricular zone progenitors with multiple rounds of cell division during sulcogyrogenesis in the ferret cerebral cortex. IBRO Reports.7:42-51. DOI: 10.1016/j.devbrainres.2005.03.013.
[21] CC Harwell, PR Parker, SM Gee, A Okada. et al.(2012). Sonic hedgehog expression in corticofugal projection neurons directs cortical microcircuit formation. Neuron.73:1116-1126. DOI: 10.1016/j.devbrainres.2005.03.013.
[22] K Sehara, T Toda, L Iwai, M Wakimoto. et al.(2010). Whisker-related axonal patterns and plasticity of layer 2/3 neurons in the mouse barrel cortex. Journal of Neuroscience.30:3082-3092. DOI: 10.1016/j.devbrainres.2005.03.013.
[23] PT Chuang, AP McMahon. (1999). Vertebrate hedgehog signalling modulated by induction of a Hedgehog-binding protein. Nature.397:617-621. DOI: 10.1016/j.devbrainres.2005.03.013.
[24] P Rakic. (2009). Evolution of the neocortex: a perspective from developmental biology. Nature Reviews Neuroscience.10:724-735. DOI: 10.1016/j.devbrainres.2005.03.013.
[25] Y Shinmyo, Y Terashita, TA Dinh Duong, T Horiike. et al.(2017). Folding of the cerebral cortex requires Cdk5 in Upper-Layer neurons in Gyrencephalic mammals. Cell Reports.20:2131-2143. DOI: 10.1016/j.devbrainres.2005.03.013.
[26] AA Pollen, TJ Nowakowski, J Chen, H Retallack. et al.(2015). Molecular identity of human outer radial Glia during cortical development. Cell.163:55-67. DOI: 10.1016/j.devbrainres.2005.03.013.
[27] L Iwai, Y Ohashi, D van der List, WM Usrey. et al.(2013). FoxP2 is a parvocellular-specific transcription factor in the visual thalamus of monkeys and ferrets. Cerebral Cortex.23:2204-2212. DOI: 10.1016/j.devbrainres.2005.03.013.
[28] KC Oberg, CU Pira, JP Revelli, B Ratz. et al.(2002). Efficient ectopic gene expression targeting chick mesoderm. Developmental Dynamics.224:291-302. DOI: 10.1016/j.devbrainres.2005.03.013.
[29] N Sasai, E Kutejova, J Briscoe. (2014). Integration of signals along orthogonal axes of the vertebrate neural tube controls progenitor competence and increases cell diversity. PLOS Biology.12. DOI: 10.1016/j.devbrainres.2005.03.013.
[30] DV Hansen, JH Lui, PR Parker, AR Kriegstein. et al.(2010). Neurogenic radial Glia in the outer subventricular zone of human neocortex. Nature.464:554-561. DOI: 10.1016/j.devbrainres.2005.03.013.
[31] A Lukaszewicz, P Savatier, V Cortay, P Giroud. et al.(2005). G1 phase regulation, area-specific cell cycle control, and cytoarchitectonics in the primate cortex. Neuron.47:353-364. DOI: 10.1016/j.devbrainres.2005.03.013.
[32] K Masuda, T Toda, Y Shinmyo, H Ebisu. et al.(2015). Pathophysiological analyses of cortical malformation using gyrencephalic mammals. Scientific Reports.5. DOI: 10.1016/j.devbrainres.2005.03.013.
[33] L Iwai, H Kawasaki. (2009). Molecular development of the lateral geniculate nucleus in the absence of retinal waves during the time of retinal axon eye-specific segregation. Neuroscience.159:1326-1337. DOI: 10.1016/j.devbrainres.2005.03.013.
[34] H Kawasaki, H Fujii, Y Gotoh, T Morooka. et al.(1999). Requirement for mitogen-activated protein kinase in cerebellar long term depression. Journal of Biological Chemistry.274:13498-13502. DOI: 10.1016/j.devbrainres.2005.03.013.
[35] T Toda, Y Shinmyo, TA Dinh Duong, K Masuda. et al.(2016). An essential role of SVZ progenitors in cortical folding in Gyrencephalic mammals. Scientific Reports.6. DOI: 10.1016/j.devbrainres.2005.03.013.
[36] SA Fietz, I Kelava, J Vogt, M Wilsch-Bräuninger. et al.(2010). OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling. Nature Neuroscience.13:690-699. DOI: 10.1016/j.devbrainres.2005.03.013.
[37] C Llinares-Benadero, V Borrell. (2019). Deconstructing cortical folding: genetic, cellular and mechanical determinants. Nature Reviews Neuroscience.20:161-176. DOI: 10.1016/j.devbrainres.2005.03.013.
[38] JH Lui, DV Hansen, AR Kriegstein. (2011). Development and evolution of the human neocortex. Cell.146:18-36. DOI: 10.1016/j.devbrainres.2005.03.013.
[39] MB Johnson, X Sun, A Kodani, R Borges-Monroy. et al.(2018). Aspm knockout ferret reveals an evolutionary mechanism governing cerebral cortical size. Nature.556:370-375. DOI: 10.1016/j.devbrainres.2005.03.013.
[40] M Florio, WB Huttner. (2014). Neural progenitors, neurogenesis and the evolution of the neocortex. Development.141:2182-2194. DOI: 10.1016/j.devbrainres.2005.03.013.
[41] T Toda, D Homma, H Tokuoka, I Hayakawa. et al.(2013). Birth regulates the initiation of sensory map formation through serotonin signaling. Developmental Cell.27:32-46. DOI: 10.1016/j.devbrainres.2005.03.013.
[42] DP Richman, RM Stewart, JW Hutchinson, VS Caviness. et al.(1975). Mechanical model of brain convolutional development. Science.189:18-21. DOI: 10.1016/j.devbrainres.2005.03.013.
[43] ER Thomsen, JK Mich, Z Yao, RD Hodge. et al.(2016). Fixed single-cell transcriptomic characterization of human radial glial diversity. Nature Methods.13:87-93. DOI: 10.1016/j.devbrainres.2005.03.013.
[44] ME Ross, CA Walsh. (2001). Human brain malformations and their lessons for neuronal migration. Annual Review of Neuroscience.24:1041-1070. DOI: 10.1016/j.devbrainres.2005.03.013.
[45] T Sun, RF Hevner. (2014). Growth and folding of the mammalian cerebral cortex: from molecules to malformations. Nature Reviews Neuroscience.15:217-232. DOI: 10.1016/j.devbrainres.2005.03.013.
[46] T Fujimoto, K Anderson, SE Jacobsen, SI Nishikawa. et al.(2007). Cdk6 blocks myeloid differentiation by interfering with Runx1 DNA binding and Runx1-C/EBPalpha interaction. The EMBO Journal.26:2361-2370. DOI: 10.1016/j.devbrainres.2005.03.013.
[47] E McGlinn, KL van Bueren, S Fiorenza, R Mo. et al.(2005). Pax9 and Jagged1 act downstream of Gli3 in vertebrate limb development. Mechanisms of Development.122:1218-1233. DOI: 10.1016/j.devbrainres.2005.03.013.
[48] N Matsumoto, Y Shinmyo, Y Ichikawa, H Kawasaki. et al.(2017b). Gyrification of the cerebral cortex requires FGF signaling in the mammalian brain. eLife.6. DOI: 10.1016/j.devbrainres.2005.03.013.
[49] H Kawasaki, K Mizuseki, S Nishikawa, S Kaneko. et al.(2000). Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron.28:31-40. DOI: 10.1016/j.devbrainres.2005.03.013.
[50] H Kawasaki, H Suemori, K Mizuseki, K Watanabe. et al.(2002). Generation of dopaminergic neurons and pigmented epithelia from primate ES cells by stromal cell-derived inducing activity. PNAS.99:1580-1585. DOI: 10.1016/j.devbrainres.2005.03.013.
[51] H Kawasaki, JC Crowley, FJ Livesey, LC Katz. et al.(2004). Molecular organization of the ferret visual thalamus. Journal of Neuroscience.24:9962-9970. DOI: 10.1016/j.devbrainres.2005.03.013.
[52] L Wang, S Hou, YG Han. (2016). Hedgehog signaling promotes basal progenitor expansion and the growth and folding of the neocortex. Nature Neuroscience.19:888-896. DOI: 10.1016/j.devbrainres.2005.03.013.
[53] N Matsumoto, Y Hoshiba, K Morita, N Uda. et al.(2017a). Pathophysiological analyses of periventricular nodular heterotopia using gyrencephalic mammals. Human Molecular Genetics.26:1173-1181. DOI: 10.1016/j.devbrainres.2005.03.013.
[54] S Vaid, JG Camp, L Hersemann, C Eugster Oegema. et al.(2018). A novel population of Hopx-dependent basal radial glial cells in the developing mouse neocortex. Development.145. DOI: 10.1016/j.devbrainres.2005.03.013.
[55] H Kawasaki, L Iwai, K Tanno. (2012). Rapid and efficient genetic manipulation of gyrencephalic carnivores using in utero electroporation. Molecular Brain.5. DOI: 10.1016/j.devbrainres.2005.03.013.
[56] M Turrero García, Y Chang, Y Arai, WB Huttner. et al.(2016). S-phase duration is the main target of cell cycle regulation in neural progenitors of developing ferret neocortex. Journal of Comparative Neurology.524:456-470. DOI: 10.1016/j.devbrainres.2005.03.013.