Type IV Collagen Controls the Axogenesis of Cerebellar Granule Cells by Regulating Basement Membrane Integrity in Zebrafish

Takeuchi, Miki; Yamaguchi, Shingo; Yonemura, Shigenobu; Kakiguchi, Kisa; Sato, Yoshikatsu; Higashiyama, Tetsuya; Shimizu, Takashi; Hibi, Masahiko

doi:10.1371/journal.pgen.1005587

Cited by 35 publications

(41 citation statements)

References 49 publications

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“…The LCa and EG contain GCs, whose axons make synapses with the PC dendrites in the cerebellum ( Fig. 1A) and further extend caudally to connect with the dendrites of PC-like cells called crest cells in the dorsal hindbrain (Volkmann et al 2008;Bae et al 2009;Takeuchi et al 2015b). Similar extra-cerebellar projections from auricle GCs are also seen in cartilaginous fish (Montgomery 1981), but not in amniotes.…”

Section: Ray-finned Fishesmentioning

confidence: 82%

“…; Takeuchi et al . ). Similar extra‐cerebellar projections from auricle GCs are also seen in cartilaginous fish (Montgomery ), but not in amniotes.…”

Section: Diversity In Cerebellum Structurementioning

confidence: 97%

“…; Takeuchi et al . ). Distinct genetic programs may differentially control the development and function of the GCs in the Va/CCe and the EG/LCa in ray‐finned fish.…”

Section: Mechanisms For the Development Of Cerebellum Diversitymentioning

confidence: 97%

“…In addition, the medial and caudal GC progenitors in zebrafish show distinct spatial and temporal expression patterns of the three atoh1 genes: atoh1a expression is restricted to the rostral domain (Va), whereas the atoh1b/c expressions are maintained longer in the rostro-caudal axis at the larval and adult stages (Chaplin et al 2010;Kani et al 2010). Furthermore, GCs in the CCe and the EG/LCa show distinct expressions of some GC genes (Bae et al 2009;Takeuchi et al 2016) and form different neural circuits (Volkmann et al 2008;Bae et al 2009;Takeuchi et al 2015b). Distinct genetic programs may differentially control the development and function of the GCs in the Va/CCe and the EG/LCa in ray-finned fish.…”

Section: Layer Formation and Generation Of Eurydendroid Cells In Ray-mentioning

confidence: 99%

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Evolutionary mechanisms that generate morphology and neural‐circuit diversity of the cerebellum

et al. 2017

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The cerebellum is derived from the dorsal part of the anterior-most hindbrain. The vertebrate cerebellum contains glutamatergic granule cells (GCs) and gamma-aminobutyric acid (GABA)ergic Purkinje cells (PCs). These cerebellar neurons are generated from neuronal progenitors or neural stem cells by mechanisms that are conserved among vertebrates. However, vertebrate cerebella are widely diverse with respect to their gross morphology and neural circuits. The cerebellum of cyclostomes, the basal vertebrates, has a negligible structure. Cartilaginous fishes have a cerebellum containing GCs, PCs, and deep cerebellar nuclei (DCNs), which include projection neurons. Ray-finned fish lack DCNs but have projection neurons termed eurydendroid cells (ECs) in the vicinity of the PCs. Among ray-finned fishes, the cerebellum of teleost zebrafish has a simple lobular structure, whereas that of weakly electric mormyrid fish is large and foliated. Amniotes, which include mammals, independently evolved a large, foliated cerebellum, which contains massive numbers of GCs and has functional connections with the dorsal telencephalon (neocortex). Recent studies of cyclostomes and cartilaginous fish suggest that the genetic program for cerebellum development was already encoded in the genome of ancestral vertebrates. In this review, we discuss how alterations of the genetic and cellular programs generated diversity of the cerebellum during evolution.

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Section: Ray-finned Fishesmentioning

confidence: 82%

“…; Takeuchi et al . ). Similar extra‐cerebellar projections from auricle GCs are also seen in cartilaginous fish (Montgomery ), but not in amniotes.…”

Section: Diversity In Cerebellum Structurementioning

confidence: 97%

“…; Takeuchi et al . ). Distinct genetic programs may differentially control the development and function of the GCs in the Va/CCe and the EG/LCa in ray‐finned fish.…”

Section: Mechanisms For the Development Of Cerebellum Diversitymentioning

confidence: 97%

Section: Layer Formation and Generation Of Eurydendroid Cells In Ray-mentioning

confidence: 99%

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Evolutionary mechanisms that generate morphology and neural‐circuit diversity of the cerebellum

et al. 2017

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“…2G-L, Movie 1). Their axons appear starting at 3.5 dpf and resemble granule neuron parallel fibers (Hibi and Shimizu, 2012;Takeuchi et al, 2015). In addition to the parallel fibers across the surface of the cerebellum (Fig.…”

Section: Atoh1c Is Cell-autonomously Required For the Specification Omentioning

confidence: 91%

Multiple zebrafishatoh1genes specify a diversity of neuronal types in the zebrafish cerebellum

Kidwell

Hibi

et al. 2017

Preprint

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Summary statement: atoh1 genes specify distinct populations of tegmental and granule neurons in the zebrafish hindbrain and promote their delamination from the neuroepithelium, a process critical for neuronal maturation.peer-reviewed) is the author/funder. All rights reserved. No reuse allowed without permission.The copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/098012 doi: bioRxiv preprint first posted online Jan. 4, 2017; 2 ABSTRACTThe basic Helix-Loop-Helix transcription factor Atoh1 is required for the specification of multiple neuron types in the mammalian hindbrain including tegmental, precerebellar output neurons and cerebellar granule neurons. How a single proneural gene specifies so many neuron types from a single progenitor zone, the upper rhombic lip (URL), is not known. Here we use the zebrafish to explore the role of atoh1 in cerebellar neurogenesis. Using transgenic reporters we show that zebrafish atoh1c-expressing cells give rise to tegmental and granule cell populations that, together with previously described atoh1a-derived neuron populations, resemble the diversity of atoh1 derivatives observed in mammals. Using genetic mutants we find that of the three zebrafish atoh1 paralogs, atoh1c and atoh1a are required for the full complement of granule neurons in the zebrafish cerebellum. Interestingly, atoh1a and atoh1c specify non-overlapping granule populations, indicating that fish use multiple atoh1 genes to generate granule neuron diversity that is not detected in mammals. By live imaging of neurogenesis at the URL we show that atoh1c is not required for the specification of granule neuron progenitors but promotes their delamination from the URL epithelium and this process is critical for neuronal maturation. This study thus provides a better understanding of how proneural transcription factors regulate neurogenesis in the vertebrate cerebellum.

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Gene expression profiling of granule cells and Purkinje cells in the zebrafish cerebellum

Takeuchi

Yamaguchi

Sakakibara

et al. 2016

J of Comparative Neurology

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The structure of the neural circuitry of the cerebellum, which functions in some types of motor learning and coordination, is generally conserved among vertebrates. However, some cerebellar features are species specific. It is not clear which genes are involved in forming these conserved and species-specific structures and functions. This study uses zebrafish transgenic larvae expressing fluorescent proteins in granule cells, Purkinje cells, or other cerebellar neurons and glial cells to isolate each type of cerebellar cells by fluorescence-activated cell sorting and to profile their gene expressions by RNA sequencing and in situ hybridization. We identify genes that are upregulated in granule cells or Purkinje cells, including many genes that are also expressed in mammalian cerebella. Comparison of the transcriptomes in granule cells and Purkinje cells in zebrafish larvae reveals that more developmental genes are expressed in granule cells, whereas more neuronal-function genes are expressed in Purkinje cells. We show that some genes that are upregulated in granule cells or Purkinje cells are also expressed in the cerebellum-like structures. Our data provide a platform for understanding the development and function of the cerebellar neural circuits in zebrafish and the evolution of cerebellar circuits in vertebrates. J. Comp. Neurol. 525:1558-1585, 2017. © 2016 Wiley Periodicals, Inc.

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Type IV Collagen Controls the Axogenesis of Cerebellar Granule Cells by Regulating Basement Membrane Integrity in Zebrafish

Cited by 35 publications

References 49 publications

Evolutionary mechanisms that generate morphology and neural‐circuit diversity of the cerebellum

Evolutionary mechanisms that generate morphology and neural‐circuit diversity of the cerebellum

Multiple zebrafishatoh1genes specify a diversity of neuronal types in the zebrafish cerebellum

Gene expression profiling of granule cells and Purkinje cells in the zebrafish cerebellum

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