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The Regulation of the Cytoskeleton in the Healthy and Diseased Central Nervous System

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 (31 March 2021) | Viewed by 22248

Special Issue Editor

Prof. Dr. Thomas Fath

E-Mail Website
Guest Editor
Department of Biomedical Sciences, Macquarie University, Sydney, NSW 2109, Australia
Interests: actin cytoskeleton; microtubules; Alzheimer’s disease; motor neuron disease; neurite growth
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

The regulation of the cell architecture and particularly the cytoskelelton plays a pivotal role in controlling neuronal connectivity and neuronal function in the central nervous system (CNS). For a long time, changes in the cytoskeletal organisation of neurons has been considered to be largely a byproduct in the pathology of CNS diseases. However, the disruption of the regluatory mechanisms of the cell architecture has been increasingly implicated in the pathogenesis of a large number of neurological and neurodegenerative diseases and CNS injuries, including Alzheimer’s disease, motor neuron disease, epilepsy, schizphrenia, brain trauma and spinal cord injury. Gaining a detailed understanding of the physiological regulation of the cytoskeleton as well as the disease-associated alterations of its regulation will be crucial to develop new therapeutic approaches of dieases that affect the CNS. This Special Issue aims to feature recent advances in the field, of studying the  cytoskeleton in the healthy and dieased nervous system. For this, we are welcoming original resarch article and review contributions, discussing the fundamental regulation of the cytoskeleton in neurons and glial cells in the brain and spinal cord, the molecular basis of disease-associated pathomechanisms of CNS diseases and the use of cytoskeletal building blocks as biomarkers and as drug targets in CNS diseases.

Prof. Dr. Thomas Fath
Guest Editor

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Keywords

  • Actin cytoskeleton
  • Microtubules
  • Intermediate filaments
  • Neurodegenerative diseases
  • Alzheimer’ disease
  • Motor neuron disease
  • Spinal cord injury

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Published Papers (5 papers)

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Research

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16 pages, 2790 KiB  
Article
Overexpression of Tropomyosin Isoform Tpm3.1 Does Not Alter Synaptic Function in Hippocampal Neurons
by Chanchanok Chaichim, Tamara Tomanic, Holly Stefen, Esmeralda Paric, Lucy Gamaroff, Alexandra K. Suchowerska, Peter W. Gunning, Yazi D. Ke, Thomas Fath and John Power
Int. J. Mol. Sci. 2021, 22(17), 9303; https://doi.org/10.3390/ijms22179303 - 27 Aug 2021
Viewed by 2652
Abstract
Tropomyosin (Tpm) has been regarded as the master regulator of actin dynamics. Tpms regulate the binding of the various proteins involved in restructuring actin. The actin cytoskeleton is the predominant cytoskeletal structure in dendritic spines. Its regulation is critical for spine formation and [...] Read more.
Tropomyosin (Tpm) has been regarded as the master regulator of actin dynamics. Tpms regulate the binding of the various proteins involved in restructuring actin. The actin cytoskeleton is the predominant cytoskeletal structure in dendritic spines. Its regulation is critical for spine formation and long-term activity-dependent changes in synaptic strength. The Tpm isoform Tpm3.1 is enriched in dendritic spines, but its role in regulating the synapse structure and function is not known. To determine the role of Tpm3.1, we studied the synapse structure and function of cultured hippocampal neurons from transgenic mice overexpressing Tpm3.1. We recorded hippocampal field excitatory postsynaptic potentials (fEPSPs) from brain slices to examine if Tpm3.1 overexpression alters long-term synaptic plasticity. Tpm3.1-overexpressing cultured neurons did not show a significantly altered dendritic spine morphology or synaptic activity. Similarly, we did not observe altered synaptic transmission or plasticity in brain slices. Furthermore, expression of Tpm3.1 at the postsynaptic compartment does not increase the local F-actin levels. The results suggest that although Tpm3.1 localises to dendritic spines in cultured hippocampal neurons, it does not have any apparent impact on dendritic spine morphology or function. This is contrary to the functional role of Tpm3.1 previously observed at the tip of growing neurites, where it increases the F-actin levels and impacts growth cone dynamics. Full article
(This article belongs to the Special Issue The Regulation of the Cytoskeleton in the Healthy and Diseased Central Nervous System)
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20 pages, 2319 KiB  
Article
New Partners Identified by Mass Spectrometry Assay Reveal Functions of NCAM2 in Neural Cytoskeleton Organization
by Antoni Parcerisas, Alba Ortega-Gascó, Marc Hernaiz-Llorens, Maria Antonia Odena, Fausto Ulloa, Eliandre de Oliveira, Miquel Bosch, Lluís Pujadas and Eduardo Soriano
Int. J. Mol. Sci. 2021, 22(14), 7404; https://doi.org/10.3390/ijms22147404 - 9 Jul 2021
Cited by 7 | Viewed by 3016
Abstract
Neuronal cell adhesion molecule 2 (NCAM2) is a membrane protein with an important role in the morphological development of neurons. In the cortex and the hippocampus, NCAM2 is essential for proper neuronal differentiation, dendritic and axonal outgrowth and synapse formation. However, little is [...] Read more.
Neuronal cell adhesion molecule 2 (NCAM2) is a membrane protein with an important role in the morphological development of neurons. In the cortex and the hippocampus, NCAM2 is essential for proper neuronal differentiation, dendritic and axonal outgrowth and synapse formation. However, little is known about NCAM2 functional mechanisms and its interactive partners during brain development. Here we used mass spectrometry to study the molecular interactome of NCAM2 in the second postnatal week of the mouse cerebral cortex. We found that NCAM2 interacts with >100 proteins involved in numerous processes, including neuronal morphogenesis and synaptogenesis. We validated the most relevant interactors, including Neurofilaments (NEFs), Microtubule-associated protein 2 (MAP2), Calcium/calmodulin kinase II alpha (CaMKIIα), Actin and Nogo. An in silico analysis of the cytosolic tail of the NCAM2.1 isoform revealed specific phosphorylation site motifs with a putative affinity for some of these interactors. Our results expand the knowledge of NCAM2 interactome and confirm the key role of NCAM2 in cytoskeleton organization, neuronal morphogenesis and synaptogenesis. These findings are of interest in explaining the phenotypes observed in different pathologies with alterations in the NCAM2 gene. Full article
(This article belongs to the Special Issue The Regulation of the Cytoskeleton in the Healthy and Diseased Central Nervous System)
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Review

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23 pages, 2763 KiB  
Review
The Hidden Side of NCAM Family: NCAM2, a Key Cytoskeleton Organization Molecule Regulating Multiple Neural Functions
by Antoni Parcerisas, Alba Ortega-Gascó, Lluís Pujadas and Eduardo Soriano
Int. J. Mol. Sci. 2021, 22(18), 10021; https://doi.org/10.3390/ijms221810021 - 16 Sep 2021
Cited by 21 | Viewed by 4926
Abstract
Although it has been over 20 years since Neural Cell Adhesion Molecule 2 (NCAM2) was identified as the second member of the NCAM family with a high expression in the nervous system, the knowledge of NCAM2 is still eclipsed by NCAM1. The first [...] Read more.
Although it has been over 20 years since Neural Cell Adhesion Molecule 2 (NCAM2) was identified as the second member of the NCAM family with a high expression in the nervous system, the knowledge of NCAM2 is still eclipsed by NCAM1. The first studies with NCAM2 focused on the olfactory bulb, where this protein has a key role in axonal projection and axonal/dendritic compartmentalization. In contrast to NCAM1, NCAM2’s functions and partners in the brain during development and adulthood have remained largely unknown until not long ago. Recent studies have revealed the importance of NCAM2 in nervous system development. NCAM2 governs neuronal morphogenesis and axodendritic architecture, and controls important neuron-specific processes such as neuronal differentiation, synaptogenesis and memory formation. In the adult brain, NCAM2 is highly expressed in dendritic spines, and it regulates synaptic plasticity and learning processes. NCAM2’s functions are related to its ability to adapt to the external inputs of the cell and to modify the cytoskeleton accordingly. Different studies show that NCAM2 interacts with proteins involved in cytoskeleton stability and proteins that regulate calcium influx, which could also modify the cytoskeleton. In this review, we examine the evidence that points to NCAM2 as a crucial cytoskeleton regulation protein during brain development and adulthood. This key function of NCAM2 may offer promising new therapeutic approaches for the treatment of neurodevelopmental diseases and neurodegenerative disorders. Full article
(This article belongs to the Special Issue The Regulation of the Cytoskeleton in the Healthy and Diseased Central Nervous System)
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43 pages, 11429 KiB  
Review
Neuronal Cytoskeleton in Intellectual Disability: From Systems Biology and Modeling to Therapeutic Opportunities
by Carla Liaci, Mattia Camera, Giovanni Caslini, Simona Rando, Salvatore Contino, Valentino Romano and Giorgio R. Merlo
Int. J. Mol. Sci. 2021, 22(11), 6167; https://doi.org/10.3390/ijms22116167 - 7 Jun 2021
Cited by 14 | Viewed by 6530
Abstract
Intellectual disability (ID) is a pathological condition characterized by limited intellectual functioning and adaptive behaviors. It affects 1–3% of the worldwide population, and no pharmacological therapies are currently available. More than 1000 genes have been found mutated in ID patients pointing out that, [...] Read more.
Intellectual disability (ID) is a pathological condition characterized by limited intellectual functioning and adaptive behaviors. It affects 1–3% of the worldwide population, and no pharmacological therapies are currently available. More than 1000 genes have been found mutated in ID patients pointing out that, despite the common phenotype, the genetic bases are highly heterogeneous and apparently unrelated. Bibliomic analysis reveals that ID genes converge onto a few biological modules, including cytoskeleton dynamics, whose regulation depends on Rho GTPases transduction. Genetic variants exert their effects at different levels in a hierarchical arrangement, starting from the molecular level and moving toward higher levels of organization, i.e., cell compartment and functions, circuits, cognition, and behavior. Thus, cytoskeleton alterations that have an impact on cell processes such as neuronal migration, neuritogenesis, and synaptic plasticity rebound on the overall establishment of an effective network and consequently on the cognitive phenotype. Systems biology (SB) approaches are more focused on the overall interconnected network rather than on individual genes, thus encouraging the design of therapies that aim to correct common dysregulated biological processes. This review summarizes current knowledge about cytoskeleton control in neurons and its relevance for the ID pathogenesis, exploiting in silico modeling and translating the implications of those findings into biomedical research. Full article
(This article belongs to the Special Issue The Regulation of the Cytoskeleton in the Healthy and Diseased Central Nervous System)
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18 pages, 1049 KiB  
Review
Glycosylation in Axonal Guidance
by Sampada P. Mutalik and Stephanie L. Gupton
Int. J. Mol. Sci. 2021, 22(10), 5143; https://doi.org/10.3390/ijms22105143 - 13 May 2021
Cited by 13 | Viewed by 4074
Abstract
How millions of axons navigate accurately toward synaptic targets during development is a long-standing question. Over decades, multiple studies have enriched our understanding of axonal pathfinding with discoveries of guidance molecules and morphogens, their receptors, and downstream signalling mechanisms. Interestingly, classification of attractive [...] Read more.
How millions of axons navigate accurately toward synaptic targets during development is a long-standing question. Over decades, multiple studies have enriched our understanding of axonal pathfinding with discoveries of guidance molecules and morphogens, their receptors, and downstream signalling mechanisms. Interestingly, classification of attractive and repulsive cues can be fluid, as single guidance cues can act as both. Similarly, guidance cues can be secreted, chemotactic cues or anchored, adhesive cues. How a limited set of guidance cues generate the diversity of axonal guidance responses is not completely understood. Differential expression and surface localization of receptors, as well as crosstalk and spatiotemporal patterning of guidance cues, are extensively studied mechanisms that diversify axon guidance pathways. Posttranslational modification is a common, yet understudied mechanism of diversifying protein functions. Many proteins in axonal guidance pathways are glycoproteins and how glycosylation modulates their function to regulate axonal motility and guidance is an emerging field. In this review, we discuss major classes of glycosylation and their functions in axonal pathfinding. The glycosylation of guidance cues and guidance receptors and their functional implications in axonal outgrowth and pathfinding are discussed. New insights into current challenges and future perspectives of glycosylation pathways in neuronal development are discussed. Full article
(This article belongs to the Special Issue The Regulation of the Cytoskeleton in the Healthy and Diseased Central Nervous System)
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