Role of Reelin in the evolution of the central nervous system

ZHAO Pei-wen YAN Ming-chao LI Rui-ling FU Su WANG Ling WANG Chen-yang DENG Jin-bo*

Acta Anatomica Sinica ›› 2016 ›› Issue (2) : 166-177.

Welcome to visit Acta Anatomica Sinica! Today is Chinese
Acta Anatomica Sinica ›› 2016 ›› Issue (2) : 166-177. DOI: 10.16098/j.issn.0529-1356.2016.02.004

Role of Reelin in the evolution of the central nervous system

  • ZHAO Pei-wen YAN Ming-chao LI Rui-ling FU Su WANG Ling WANG Chen-yang DENG Jin-bo*
Author information +
History +

Abstract

Objective To investigate Reelin’s role in the evolution of the central nervous system and the relevant regulatory mechanisms. Methods A total of 192 wild-type (WT) and reeler mice from embryonic day 16 (E16) to postnatal day 30(P30) were used for this study. The neuronal migration, radial glial cells and neuroproliferation in the cerebral cortex, hippocampus and spinal cord were visualized by immunofluorescent labeling, 5-bromodeoxyuridine immunofluorescence (BrdU method). Nissl staining was also used to observe the histogenesis of the spinal cord, the cerebral cortex and hippocampus. Results During the development of spinal cord, the first neuronal migrate occurred from neuroepithelium to form “H”-like gray matter. Compared WT mice with reeler mice, only nuance was found in histogenesis, cell migration, radial glia and neuropliferation. On the other hand, the development of hippocampus required second neural migrations to eventually form the pyramidal cell layer and granule cell layer with double “C”-like shape. Compared with WT mouse, pyramidal layer in the reeler mouse was splitting into two layers with the disorder of migration and proliferation. In addition, the limitation of granule layer and hilus gradually disappeared to form drumstick-like structure. In the meantime, the number of proliferative neural stem cells reduced and the radial glial cells were arranged in disorder. The formation of the neocortex also required second neural migration to form six-layer cortex with inside-out migration manner. Compared with WT mouse, lamination of neocortex in the reeler mouse was in disorder. The neuroproliferation and radial glial cells reduced, and the radial glials were arranged in disorder. Conclusion Spinal cord, hippocampus and neocortex represent the tubular nervous system, archicortex and neocortex, respectively, in the evolution of the central nervous system(CNS). Reelin may be a key molecule during CNS evolution. Reelin’s important function probably is involved in second migration to affect the formation of cortical plate. Lack of Reelin will induce the changes of cortical structure, especially in the archicortex and neocortex.

Cite this article

Download Citations
ZHAO Pei-wen YAN Ming-chao LI Rui-ling FU Su WANG Ling WANG Chen-yang DENG Jin-bo*. Role of Reelin in the evolution of the central nervous system[J]. Acta Anatomica Sinica. 2016(2): 166-177 https://doi.org/10.16098/j.issn.0529-1356.2016.02.004

References

[1]Deng JB, Xi Y, Li RL. The evolution and gene regulation of the brain [J]. Anatomy Research, 2010, 32(1):59-74. (in Chinese)
邓锦波, 席艳, 李瑞玲. 脑的进化及其基因调控[J]. 解剖学研究, 2010, 32 (1):59-74.
[2]Wu P, Deng J, Deng JB. Development of spinal cord, spinal malformation and spinal injury [J].Journal of He’nan University (Medical Science), 2012, 31(2):134-137.  (in Chinese)
吴萍, 邓娟, 邓锦波. 脊髓的发育与脊髓畸变及脊髓损伤[J]. 河南大学学报(医学版), 2012, 31(2):134-137.
[3]Deng JB, Zhang JSh, Li RL, et al. Development and defects of neural tube[J]. Journal of Medical Research, 2009, (12):103-108. (in Chinese)
邓锦波, 张俊士, 李瑞玲, 等. 神经管的衍变及其发育缺陷[J]. 医学研究杂志, 2009, (12):103-108.
[4]Zhang JK, Zhang L, Guo M. Development and aging of C57/BL6 mouse hippocampus[J]. Journal of Xi’an Jiaotong University (Medical Sciences), 2010, 31(5):544-547 (in Chinese)  
张敬坤, 张莉, 郭敏. C57/BL6小鼠海马的发育和衰老[J]. 西安交通大学学报(医学版), 2010, 31(5):544-547.
[5]Deng JB, Xü XB, Fan WJ. Neocortical development and formation of lamination[J]. Progress of Anatomical Sciences, 2008, (4):423-428,431. (in Chinese)
邓锦波, 徐晓波, 范文娟. 新皮质的发育与片层化构筑的形成[J]. 解剖科学进展, 2008, (4):423-428,431.
[6]Rice DS, Curran T. Role of the reelin signaling pathway in central nervous system development[J]. Annu Rev Neurosci, 2001, 24(1): 1005-1039.
[7]Zhao S, Frotscher M. Go or stop? Divergent roles of Reelin in radial neuronal migration[J]. Neuroscientist, 2010, 16(4): 421-434.
[8]Alcantara S, Ruiz M, D’Arcangelo G, et al. Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse[J]. J Neurosci, 1998, 18(19): 7779-7799.
[9]Teixeira CM, Martin ED, Sahun I, et al. Overexpression of reelin prevents the manifestation of behavioral phenotypes related to schizophrenia and bipolar disorder[J]. Neuropsychopharmacology, 2011, 36(12): 2395-2405.
[10]Wang X, Babayan AH, Basbaum AI, et al. Loss of the reelin-signaling pathway differentially disrupts heat, mechanical and chemical nociceptive processing [J], Neuroscience, 2012, 226: 441-450.
[11]Gui LR, Wang ZhF. Progress of related gene of reelin[J]. Section of Genetics Foreign Medical Sciences, 2006, 28(6): 325-328. (in Chinese) 
桂兰润, 王振福. reelin相关基因研究进展[J]. 国外医学: 遗传学分册, 2006, 28(6): 325-328.
[12]Deng JB, Wang GM,Zhao ShT, et al. Morphological and histochemical study of hippocampal dentate gyrus in reeler mice[J]. Acta Anatomica Sinica, 2009, 40(4):522-526. (in Chinese)
邓锦波, 王桂敏, 赵善廷, 等. Reeler小鼠海马齿状回形态结构与组织化学研究[J]. 解剖学报, 2009, 40(4):522-526.
[13]Yan MCh, Niu YL, Wang XQ, et al. Reelin and the cerebellar development-the regulatory effect of Notch 1 signaling pathways[J]. Acta Anatomica Sinica, 2015, 46(2):182-189. (in Chinese)
鄢明超, 牛艳丽, 王小青,等. Reelin与小脑发育-Notch 1信号通路的调节作用[J]. 解剖学报, 2015, 46(2):182-189.
[14]Zang JF, Niu YL, Wang YH, et al. Neocortical lamination and cell cycle in the mouse [J]. Acta Anatomica Sinica, 2012, 43(1): 19-27. (in Chinese)
臧建峰, 牛艳丽, 王永恒, 等. 小鼠大脑新皮质片层化形成过程和细胞周期变化[J]. 解剖学报, 2012, 43(1):19-27.
[15]Ogawa M, Miyata T, Nakajima K, et al. The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons[J]. Neuron, 1995, 14(5):899-912.
[16]Howell BW, Lanier LM, Frank R, et al. The disabled 1phosphotyrosine-binding domain binds to the internalization signals of transmembrance glycoproteins and to phospholipids[J]. Mol Cell Biol, 1999, 19(7):5179-5188.
[17]Wang X, Babayan AH, Basbaum AI, et al. Loss of the reelin-signaling pathway differentially disrupts heat, mechanical and chemical nociceptive processing[J]. Neuroscience, 2012, 226: 441-450.
[18]Weiss KH, Johanssen C, Tielsch A, et al. Malformation of the radial glial scaffold in the dentate gyrus of reeler mice, scrambler mice, and ApoER2/VLDLR-deficient mice[J]. J Comp Neurol, 2003, 460(1):56-65.
[19]Zhao S, Chai X, Forster E, et al. Reelin is a positional signal for the lamination of dentate granule cells[J]. Development, 2004, 131(20):5117-5125.
[20]Cooper JA. A mechanism for inside-out lamination in the neocortex[J]. Trends Neurosci, 2008, 31(3): 113-119.
[21]Xuejun C, Eckart F,Shanting Z, et al. Reelin Stabilizes the Actin Cytoskeleton of Neuronal Processes bu Inducing n-Cofilin Phosphorylation at Serine3[J]. J Neurosci, 2009, 29(1):288-299.
[22]Hashimoto-Torii K, Torii M, Sarkisian MR, et al. Interaction between Reelin and Notch signaling regulates neuronal migration in the cerebral cortex[J]. Neuron, 2008, 60(2):273-284.
[23]Hawthorne AL. Repurposing Reelin: the new role of radial glia, Reelin and Notch in motor neuron migration[J]. Exp Neurol, 2014, 256(2014):17-20. 
[24]Lakoma J, Garcia-Alonso L, Luque JM. Reelin sets the pace of neocortical neurogenesis[J]. Development, 2011, 138(23):5223-5234.
[25]Kessaris N, Pringle N, Richardson WD. Specification of CNS glia from neural stem cells in the embryonic neuroepithelium[J]. Philos Trans R Soc Lend B BioI Sci, 2008, 363(1489):71-85.
[26]Kriegstein AR, Noctor SC. Patterns of neuronal migration in the embryonic cortex[J]. Trends Neurosci, 2004, 27(7): 392-399.
[27]Rakic P. A century of progress in corticoneurogenesis: from silver impregnation to genetic engineering[J]. Cereb Cortex, 2006, 16 (Suppl. 1): 13-17.
[28]Deng J, Elberger A. The role of pioneer neurons in the development of mouse visual cortex and corpus callosum [J]. Anat Embryol (Berl), 2001, 204(6):437-453.
[29]Li Q, Martin JH. Postnatal development of corticospinal axon terminal morphology in the cat[J]. Comp Neurol, 2001, 435(2):127-141.
[30]Frotsher M. Cajal-Retzius cells, Reelin and the formation of layers[J]. Curr Opin Neurobiol, 1998, 8(5):570-575.
[31]Forster E, Zhao S, Frotscher M. Laminating the hippocampus[J]. Nat Neurosc, 2006, 7(4):259-267.

Accesses

Citation

Detail

Sections
Recommended

/