Role of Reelin in cell positioning in the cerebellum and the cerebellum-like structure in zebrafish

Nimura, Takayuki; Itoh, Tsubasa; Hagio, Hanako; Hayashi, Takuto; Donato, Vincenzo Di; Takeuchi, Miki; Itoh, Takeaki; Inoguchi, Fuduki; Sato, Yoshikatsu; Yamamoto, Naoyuki; Katsuyama, Yu; Bene, Filippo Del; Shimizu, Takashi; Hibi, Masahiko

doi:10.1016/j.ydbio.2019.07.010

Cited by 19 publications

(17 citation statements)

References 98 publications

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“…Altogether, our observations further suggest a major role of the RELN pathway in controlling PC positioning in vertebrates (Caviness and Rakic, 1978;D'Arcangelo et al, 1995;Miyata et al, 1997;Jensen et al, 2002). However, despite the similarities in ectopic arrangement of PCs noticed between the adult cerebellum of snakes (this study and Macrì et al, 2019) and vertebrate mutants affecting the RELN pathway (Heckroth et al, 1989;D'Arcangelo et al, 1995;Sheldon et al, 1997;Ware et al, 1997;Gallagher et al, 1998;Trommsdorff et al, 1999;Nimura et al, 2019), significant phenotypic differences in cortical organization are noticeable. Especially, snake PCs are not found amassed in clusters or trapped in the IGL, as shown in mouse and zebrafish mutants with movement or behavioral defects (Inoue et al, 1990;Nimura et al, 2019).…”

Section: Importance Of Reln Distribution Pattern In Cortical Maturationsupporting

confidence: 56%

“…However, despite the similarities in ectopic arrangement of PCs noticed between the adult cerebellum of snakes (this study and Macrì et al, 2019) and vertebrate mutants affecting the RELN pathway (Heckroth et al, 1989;D'Arcangelo et al, 1995;Sheldon et al, 1997;Ware et al, 1997;Gallagher et al, 1998;Trommsdorff et al, 1999;Nimura et al, 2019), significant phenotypic differences in cortical organization are noticeable. Especially, snake PCs are not found amassed in clusters or trapped in the IGL, as shown in mouse and zebrafish mutants with movement or behavioral defects (Inoue et al, 1990;Nimura et al, 2019). Instead, our developmental data in B. fuliginosus indicate that PCs are arranged in radially oriented columns, each consisting of a different number of cells protruding in the ML, likely reflecting the presence of a proper guidance system provided by an organized radial glia scaffold supporting their migration.…”

Section: Importance Of Reln Distribution Pattern In Cortical Maturationmentioning

confidence: 55%

“…Instead, our developmental data in B. fuliginosus indicate that PCs are arranged in radially oriented columns, each consisting of a different number of cells protruding in the ML, likely reflecting the presence of a proper guidance system provided by an organized radial glia scaffold supporting their migration. This also contrasts with the aberrant and distorted organization of cerebellar radial glia, along with other types of glia located in different brain areas, observed in reeler mice (Bignami and Dahl, 1974;Terashima et al, 1985;Yuasa et al, 1991;Yuasa, 1996;Hartfuss et al, 2003;Weiss et al, 2003) and Reln knockout zebrafish (Nimura et al, 2019). These differences suggest that Reln expression initiating at early stages of cerebellogenesis in differentiating GCPs, a distribution pattern similar among squamate models (Figure 9) but also in mice (Miyata et al, 1996;Rice et al, 1998), could be important for the maturation and migration of other cerebellar cell types, most likely developing glia.…”

Section: Importance Of Reln Distribution Pattern In Cortical Maturationmentioning

confidence: 76%

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Heterochronic Developmental Shifts Underlying Squamate Cerebellar Diversity Unveil the Key Features of Amniote Cerebellogenesis

Macrì

Di‐Poï

2020

Front. Cell Dev. Biol.

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Despite a remarkable conservation of architecture and function, the cerebellum of vertebrates shows extensive variation in morphology, size, and foliation pattern. These features make this brain subdivision a powerful model to investigate the evolutionary developmental mechanisms underlying neuroanatomical complexity both within and between anamniote and amniote species. Here, we fill a major evolutionary gap by characterizing the developing cerebellum in two non-avian reptile speciesbearded dragon lizard and African house snake-representative of extreme cerebellar morphologies and neuronal arrangement patterns found in squamates. Our data suggest that developmental strategies regarded as exclusive hallmark of birds and mammals, including transit amplification in an external granule layer (EGL) and Sonic hedgehog expression by underlying Purkinje cells (PCs), contribute to squamate cerebellogenesis independently from foliation pattern. Furthermore, direct comparison of our models suggests the key importance of spatiotemporal patterning and dynamic interaction between granule cells and PCs in defining cortical organization. Especially, the observed heterochronic shifts in early cerebellogenesis events, including upper rhombic lip progenitor activity and EGL maintenance, are strongly expected to affect the dynamics of molecular interaction between neuronal cell types in snakes. Altogether, these findings help clarifying some of the morphogenetic and molecular underpinnings of amniote cerebellar corticogenesis, but also suggest new potential molecular mechanisms underlying cerebellar complexity in squamates. Furthermore, squamate models analyzed here are revealed as key animal models to further understand mechanisms of brain organization.

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Section: Importance Of Reln Distribution Pattern In Cortical Maturationsupporting

confidence: 56%

Section: Importance Of Reln Distribution Pattern In Cortical Maturationmentioning

confidence: 55%

Section: Importance Of Reln Distribution Pattern In Cortical Maturationmentioning

confidence: 76%

See 1 more Smart Citation

Heterochronic Developmental Shifts Underlying Squamate Cerebellar Diversity Unveil the Key Features of Amniote Cerebellogenesis

Macrì

Di‐Poï

2020

Front. Cell Dev. Biol.

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“…This hypothesis has been confirmed in a study showing synaptic lamination defects in the optic tectum of reln –/– larvae (Di Donato et al, 2018). Although the optic tectum of adult zebrafish reln –/– mutants does not show patterning defects, in the cerebellum Purkinje cells, eurydendroid cells and Bergmann glia are found in ectopic positions in the absence of hypoplasia (Nimura et al, 2019). The localization of Reln in the zebrafish brain fits with the idea that this protein could play a role in synaptic organization or the integration of sensory afferent information from tectal or diencephalic brain areas to the dorsal telencephalon (Costagli et al, 2002).…”

Section: Discussionmentioning

confidence: 99%

Reelin Signaling Controls the Preference for Social Novelty in Zebrafish

Vecchia

Donato

Young

et al. 2019

Front. Behav. Neurosci.

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Reelin (Reln) is an extracellular glycoprotein that is important for brain patterning. During development Reln coordinates the radial migration of postmitotic cortical neurons, cerebellar and hippocampal neurons, whereas it promotes dendrite maturation, synaptogenesis, synaptic transmission, plasticity and neurotransmitter release in the postnatal and adult brain. Genetic studies of human patients have demonstrated association between the RELN locus and autism spectrum disorder, schizophrenia, bipolar disorder, and Alzheimer’s disease. In this study we have characterized the behavioral phenotype of reelin (reln) mutant zebrafish, as well as two canonical signaling pathway targets DAB adaptor protein 1a (dab1a) and the very low density lipoprotein receptor (vldlr). Zebrafish reln–/– mutants display a selective reduction in preference for social novelty that is not observed in dab1a–/– or vldlr–/– mutant lines. They also exhibit an increase in 5-HT signaling in the hindbrain that parallels but does not underpin the alteration in social preference. These results suggest that zebrafish reln–/– mutants can be used to model some aspects of human diseases in which changes to Reln signaling alter social behavior.

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“…The gRNA targets were designed by the web software ZiFit Targeter 4.2 (http://zifit.partners.org/ZiFiT/) (Hwang et al, 2013;Mali et al, 2013 for ptf1a +11 . gRNA and Cas9 mRNA syntheses were performed as previously reported (Nimura et al, 2019). A solution containing 25 ng/µL gRNA and 100 ng/µL Cas9 mRNA or 1000 ng/µL Cas9 protein (Toolgen) was injected into one-cell-stage embryos using a pneumatic microinjector (PV830, WPI).…”

Section: Establishment Of Gsx2 and Ptf1a Mutants By The Crispr/cas9 Smentioning

confidence: 99%

Gsx2 is involved in specification of neurons in the inferior olivary nuclei from Ptf1a-expressing neuronal progenitors in zebrafish

Itoh

Takeuchi

Sakagami

et al. 2020

Preprint

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The homeobox gene gsx2 mediates rostro-caudal positional signaling to specify the identify of neurons in the inferior olivary nuclei from neural progenitors expressing the proneural gene ptf1a. 2 ABSTRACTNeurons in the inferior olivary nuclei (IO neurons) send climbing fibers to Purkinje cells to elicit functions of the cerebellum. IO neurons and Purkinje cells are derived from neural progenitors expressing the proneural gene ptf1a. In this study, we found that the homeobox gene gsx2 was co-expressed with ptf1a in IO progenitors in zebrafish.Both gsx2 and ptf1a zebrafish mutants showed a strong reduction or loss of IO neurons.The expression of ptf1a was not affected in gsx2 mutants and vice versa. In IO progenitors, the ptf1a mutation increased apoptosis whereas the gsx2 mutation did not, suggesting that ptf1a and gsx2 are independently regulated and have distinct roles. The fibroblast growth factors (Fgf) 3/8a and retinoic acid signals negatively and positively, respectively, regulated gsx2 expression and thereby the development of IO neurons.mafba and hox genes are at least partly involved in the Fgf-and retinoic acid-dependent regulation of IO neuronal development. Our results indicate that gsx2 mediates the rostro-caudal positional signals to specify the identity of IO neurons from ptf1a-expressing neural progenitors. K., Suster, M. L., Mizusawa, K., Nagayoshi, S., Kotani, T., Urasaki, A., Kishimoto, Y., Hibi, M. and Kawakami, K. (2008). Genetic dissection of neural circuits by Tol2 transposon-mediated Gal4 gene and enhancer trapping in zebrafish. . Anatomy of zebrafish cerebellum and screen for mutations affecting its development. Dev . Biol. 330, 406-426. Begemann, G., Marx, M., Mebus, K., Meyer, A. and Bastmeyer, M. (2004). Beyond the neckless phenotype: influence of reduced retinoic acid signaling on motor neuron development in the zebrafish hindbrain. Dev. Biol. 271, 119-129. Asakawa,

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Role of Reelin in cell positioning in the cerebellum and the cerebellum-like structure in zebrafish

Cited by 19 publications

References 98 publications

Heterochronic Developmental Shifts Underlying Squamate Cerebellar Diversity Unveil the Key Features of Amniote Cerebellogenesis

Heterochronic Developmental Shifts Underlying Squamate Cerebellar Diversity Unveil the Key Features of Amniote Cerebellogenesis

Reelin Signaling Controls the Preference for Social Novelty in Zebrafish

Gsx2 is involved in specification of neurons in the inferior olivary nuclei from Ptf1a-expressing neuronal progenitors in zebrafish

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