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Responsible Factors for Neuromorphogenesis in the Brain

A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Neurobiology".

Deadline for manuscript submissions: closed (30 June 2023) | Viewed by 4614

Special Issue Editor

Department of Neurobiology and Anatomy, Drexel University College of Medicine, 2900 Queen Lane, Philadelphia, PA 19129, USA
Interests: neurodevelopmental disorder; neurodevelopment; brain development; neurite formation; neuronal migration; spine formation; synapse formation; neural connectivity; electrophysiology; behavior; mouse genetics; autism spectrum disorder
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Special Issue Information

Dear Colleagues,

A population of post-mitotic pyramidal neurons starts migrating after mitosis at the ventricular zone and subventricular zone and reaches its terminal destination at the cortical plate, where they undergo neuronal morphogenesis. This process includes neurite formation, spine formation, and synaptogenesis, all of which contribute to the formation of a proper nervous network. Various molecules have been identified as contributing to these complex cellular events. As a result of flaws in neuronal morphogenesis, there are devastating diseases such as autism spectrum disorder and schizophrenia. Thus, unravelling the key players, cellular signalling pathways, as well as signalling interplay is paramount.

The Special Issue will publish original articles on molecules responsible for controlling the morphology of neurons as well as review articles on the responsible proteins that have been implicated in the regulation of neuronal morphogenesis. We seek articles that focus not only on molecules in development but also on molecules regulating neuronal morphology in the adult brain in any model systems, including fish, flies, worms, and mammals. It is also encouraging to submit articles regarding regulatory molecules implicated in disease-related processes, such as axon regeneration.

Dr. Kazuhito Toyooka
Guest Editor

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Keywords

  • neuroscience
  • brain
  • neuronal morphology
  • neurite
  • axon
  • dendrite
  • spine
  • synapse
  • signaling pathway
  • cytoskeleton

Published Papers (3 papers)

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Research

24 pages, 7907 KiB  
Article
Calcium Signaling during Cortical Apical Dendrite Initiation: A Role for Cajal-Retzius Neurons
by Joshua R. Enck and Eric C. Olson
Int. J. Mol. Sci. 2023, 24(16), 12965; https://doi.org/10.3390/ijms241612965 - 19 Aug 2023
Cited by 1 | Viewed by 1006
Abstract
The apical dendrite of a cortical projection neuron (CPN) is generated from the leading process of the migrating neuron as the neuron completes migration. This transformation occurs in the cortical marginal zone (MZ), a layer that contains the Cajal-Retzius neurons and their axonal [...] Read more.
The apical dendrite of a cortical projection neuron (CPN) is generated from the leading process of the migrating neuron as the neuron completes migration. This transformation occurs in the cortical marginal zone (MZ), a layer that contains the Cajal-Retzius neurons and their axonal projections. Cajal-Retzius neurons (CRNs) are well known for their critical role in secreting Reelin, a glycoprotein that controls dendritogenesis and cell positioning in many regions of the developing brain. In this study, we examine the possibility that CRNs in the MZ may provide additional signals to arriving CPNs, that may promote the maturation of CPNs and thus shape the development of the cortex. We use whole embryonic hemisphere explants and multiphoton microscopy to confirm that CRNs display intracellular calcium transients of <1-min duration and high amplitude during early corticogenesis. In contrast, developing CPNs do not show high-amplitude calcium transients, but instead show a steady increase in intracellular calcium that begins at the time of dendritic initiation, when the leading process of the migrating CPN is encountering the MZ. The possible existence of CRN to CPN communication was revealed by the application of veratridine, a sodium channel activator, which has been shown to preferentially stimulate more mature cells in the MZ at an early developmental time. Surprisingly, veratridine application also triggers large calcium transients in CPNs, which can be partially blocked by a cocktail of antagonists that block glutamate and glycine receptor activation. These findings outline a model in which CRN spontaneous activity triggers the release of glutamate and glycine, neurotransmitters that can trigger intracellular calcium elevations in CPNs. These elevations begin as CPNs initiate dendritogenesis and continue as waves in the post-migratory cells. Moreover, we show that the pharmacological blockade of glutamatergic signaling disrupts migration, while forced expression of a bacterial voltage-gated calcium channel (CavMr) in the migrating neurons promotes dendritic growth and migration arrest. The identification of CRN to CPN signaling during early development provides insight into the observation that many autism-linked genes encode synaptic proteins that, paradoxically, are expressed in the developing cortex well before the appearance of synapses and the establishment of functional circuits. Full article
(This article belongs to the Special Issue Responsible Factors for Neuromorphogenesis in the Brain)
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22 pages, 4193 KiB  
Article
Local Microtubule and F-Actin Distributions Fully Constrain the Spatial Geometry of Drosophila Sensory Dendritic Arbors
by Sumit Nanda, Shatabdi Bhattacharjee, Daniel N. Cox and Giorgio A. Ascoli
Int. J. Mol. Sci. 2023, 24(7), 6741; https://doi.org/10.3390/ijms24076741 - 04 Apr 2023
Viewed by 1220
Abstract
Dendritic morphology underlies the source and processing of neuronal signal inputs. Morphology can be broadly described by two types of geometric characteristics. The first is dendrogram topology, defined by the length and frequency of the arbor branches; the second is spatial embedding, mainly [...] Read more.
Dendritic morphology underlies the source and processing of neuronal signal inputs. Morphology can be broadly described by two types of geometric characteristics. The first is dendrogram topology, defined by the length and frequency of the arbor branches; the second is spatial embedding, mainly determined by branch angles and straightness. We have previously demonstrated that microtubules and actin filaments are associated with arbor elongation and branching, fully constraining dendrogram topology. Here, we relate the local distribution of these two primary cytoskeletal components with dendritic spatial embedding. We first reconstruct and analyze 167 sensory neurons from the Drosophila larva encompassing multiple cell classes and genotypes. We observe that branches with a higher microtubule concentration tend to deviate less from the direction of their parent branch across all neuron types. Higher microtubule branches are also overall straighter. F-actin displays a similar effect on angular deviation and branch straightness, but not as consistently across all neuron types as microtubule. These observations raise the question as to whether the associations between cytoskeletal distributions and arbor geometry are sufficient constraints to reproduce type-specific dendritic architecture. Therefore, we create a computational model of dendritic morphology purely constrained by the cytoskeletal composition measured from real neurons. The model quantitatively captures both spatial embedding and dendrogram topology across all tested neuron groups. These results suggest a common developmental mechanism regulating diverse morphologies, where the local cytoskeletal distribution can fully specify the overall emergent geometry of dendritic arbors. Full article
(This article belongs to the Special Issue Responsible Factors for Neuromorphogenesis in the Brain)
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25 pages, 5097 KiB  
Article
The Zinc-BED Transcription Factor Bedwarfed Promotes Proportional Dendritic Growth and Branching through Transcriptional and Translational Regulation in Drosophila
by Shatabdi Bhattacharjee, Eswar Prasad R. Iyer, Srividya Chandramouli Iyer, Sumit Nanda, Myurajan Rubaharan, Giorgio A. Ascoli and Daniel N. Cox
Int. J. Mol. Sci. 2023, 24(7), 6344; https://doi.org/10.3390/ijms24076344 - 28 Mar 2023
Cited by 1 | Viewed by 1677
Abstract
Dendrites are the primary points of sensory or synaptic input to a neuron and play an essential role in synaptic integration and neural function. Despite the functional importance of dendrites, relatively less is known about the underlying mechanisms regulating cell type-specific dendritic patterning. [...] Read more.
Dendrites are the primary points of sensory or synaptic input to a neuron and play an essential role in synaptic integration and neural function. Despite the functional importance of dendrites, relatively less is known about the underlying mechanisms regulating cell type-specific dendritic patterning. Herein, we have dissected the functional roles of a previously uncharacterized gene, CG3995, in cell type-specific dendritic development in Drosophila melanogaster. CG3995, which we have named bedwarfed (bdwf), encodes a zinc-finger BED-type protein that is required for proportional growth and branching of dendritic arbors. It also exhibits nucleocytoplasmic expression and functions in both transcriptional and translational cellular pathways. At the transcriptional level, we demonstrate a reciprocal regulatory relationship between Bdwf and the homeodomain transcription factor (TF) Cut. We show that Cut positively regulates Bdwf expression and that Bdwf acts as a downstream effector of Cut-mediated dendritic development, whereas overexpression of Bdwf negatively regulates Cut expression in multidendritic sensory neurons. Proteomic analyses revealed that Bdwf interacts with ribosomal proteins and disruption of these proteins resulted in phenotypically similar dendritic hypotrophy defects as observed in bdwf mutant neurons. We further demonstrate that Bdwf and its ribosomal protein interactors are required for normal microtubule and F-actin cytoskeletal architecture. Finally, our findings reveal that Bdwf is required to promote protein translation and ribosome trafficking along the dendritic arbor. These findings shed light on the complex, combinatorial, and multi-functional roles of transcription factors (TFs) in directing the diversification of cell type-specific dendritic development. Full article
(This article belongs to the Special Issue Responsible Factors for Neuromorphogenesis in the Brain)
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