Special Issue "Neurogenesis and Regeneration in Teleost Central Nervous System"

A special issue of Cells (ISSN 2073-4409). This special issue belongs to the section "Cells of the Nervous System".

Deadline for manuscript submissions: 25 July 2022 | Viewed by 8638

Special Issue Editors

Dr. Sepand Rastegar
E-Mail Website1 Website2
Guest Editor
Institute of Biological and Chemical Systems-Biological Information Processing (IBCS-BIP), Karlsruhe Institute of Technology (KIT), Postfach 3640, 76021 Karlsruhe, Germany
Interests: gene regulation; transcription; neurogenesis; zebrafish; regeneration; neural stem cell
Special Issues, Collections and Topics in MDPI journals
Ms. Luisa Lübke
E-Mail Website1 Website2
Assistant Guest Editor
Institute of Biological and Chemical Systems - Biological Information Processing Karlsruhe Institute of Technology, Postfach 3640, D-76021 Karlsruhe, Germany
Interests: developmental biology; zebrafish regeneration; neurogenesis; development of the CNS

Special Issue Information

Dear Colleagues,

In our modern society, neurodegenerative diseases, along with cancer, pose one of the main health threats, as the number of older citizens is rising. These diseases are characterized by a progressive degeneration of neurons, which eventually leads to their death and to the disintegration of the nervous system structure.

Currently, neurodegenerative diseases are incurable, as the available treatments either only manage the symptoms or slow down disease progression.

Deciphering the cellular and molecular mechanisms of adult neurogenesis and regeneration is of great importance because it will eventually allow us to identify specific reactive neurogenesis mechanisms and re-instruct neurogenesis in patients suffering from neurodegenerative conditions.

Lately, zebrafish has become a popular model in biomedical research due to its experimental advantages, the existence of numerous genetic manipulation tools and various genetic resources, and the fact that the genetic basis of most diseases is shared between human and zebrafish.

The present Special Issue aims to summarize some of the latest advances in the field of adult neurogenesis and regeneration, using zebrafish as a model organism. We intend to highlight the key molecular mechanisms involved in neurogenesis, under normal physiological conditions and regenerative conditions, in the zebrafish nervous system, focusing on different regions of the brain, retina, and spinal cord.

Dr. Sepand Rastegar
Dr. Luisa Lübke
Guest Editors

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Keywords

  • Zebrafish
  • Adult neurogenesis
  • Neural stem cells
  • Glial Cells
  • Regeneration
  • Neurodegeneration
  • Brain injury
  • Olfactory bulb
  • Telencephalon
  • Retina
  • Optic tectum
  • Cerebellum
  • Spinal cord

Published Papers (6 papers)

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Research

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Article
Incomplete Recovery of Zebrafish Retina Following Cryoinjury
Cells 2022, 11(8), 1373; https://doi.org/10.3390/cells11081373 - 18 Apr 2022
Viewed by 435
Abstract
Zebrafish show an extraordinary potential for regeneration in several organs from fins to central nervous system. Most impressively, the outcome of an injury results in a near perfect regeneration and a full functional recovery. Indeed, among the various injury paradigms previously tested in [...] Read more.
Zebrafish show an extraordinary potential for regeneration in several organs from fins to central nervous system. Most impressively, the outcome of an injury results in a near perfect regeneration and a full functional recovery. Indeed, among the various injury paradigms previously tested in the field of zebrafish retina regeneration, a perfect layered structure is observed after one month of recovery in most of the reported cases. In this study, we applied cryoinjury to the zebrafish eye. We show that retina exposed to this treatment for one second undergoes an acute damage affecting all retinal cell types, followed by a phase of limited tissue remodeling and regrowth. Surprisingly, zebrafish developed a persistent retinal dysplasia observable through 300 days post-injury. There is no indication of fibrosis during the regeneration period, contrary to the regeneration process after cryoinjury to the zebrafish cardiac ventricle. RNA sequencing analysis of injured retinas at different time points has uncovered enriched processes and a number of potential candidate genes. By means of this simple, time and cost-effective technique, we propose a zebrafish injury model that displays a unique inability to completely recover following focal retinal damage; an outcome that is unreported to our knowledge. Furthermore, RNA sequencing proved to be useful in identifying pathways, which may play a crucial role not only in the regeneration of the retina, but in the first initial step of regeneration, degeneration. We propose that this model may prove useful in comparative and translational studies to examine critical pathways for successful regeneration. Full article
(This article belongs to the Special Issue Neurogenesis and Regeneration in Teleost Central Nervous System)
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Article
Innate Immune Pathways Promote Oligodendrocyte Progenitor Cell Recruitment to the Injury Site in Adult Zebrafish Brain
Cells 2022, 11(3), 520; https://doi.org/10.3390/cells11030520 - 02 Feb 2022
Viewed by 933
Abstract
The oligodendrocyte progenitors (OPCs) are at the front of the glial reaction to the traumatic brain injury. However, regulatory pathways steering the OPC reaction as well as the role of reactive OPCs remain largely unknown. Here, we compared a long-lasting, exacerbated reaction of [...] Read more.
The oligodendrocyte progenitors (OPCs) are at the front of the glial reaction to the traumatic brain injury. However, regulatory pathways steering the OPC reaction as well as the role of reactive OPCs remain largely unknown. Here, we compared a long-lasting, exacerbated reaction of OPCs to the adult zebrafish brain injury with a timely restricted OPC activation to identify the specific molecular mechanisms regulating OPC reactivity and their contribution to regeneration. We demonstrated that the influx of the cerebrospinal fluid into the brain parenchyma after injury simultaneously activates the toll-like receptor 2 (Tlr2) and the chemokine receptor 3 (Cxcr3) innate immunity pathways, leading to increased OPC proliferation and thereby exacerbated glial reactivity. These pathways were critical for long-lasting OPC accumulation even after the ablation of microglia and infiltrating monocytes. Importantly, interference with the Tlr1/2 and Cxcr3 pathways after injury alleviated reactive gliosis, increased new neuron recruitment, and improved tissue restoration. Full article
(This article belongs to the Special Issue Neurogenesis and Regeneration in Teleost Central Nervous System)
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Article
Neuron-Radial Glial Cell Communication via BMP/Id1 Signaling Is Key to Long-Term Maintenance of the Regenerative Capacity of the Adult Zebrafish Telencephalon
Cells 2021, 10(10), 2794; https://doi.org/10.3390/cells10102794 - 19 Oct 2021
Cited by 3 | Viewed by 1093
Abstract
The central nervous system of adult zebrafish displays an extraordinary neurogenic and regenerative capacity. In the zebrafish adult brain, this regenerative capacity relies on neural stem cells (NSCs) and the careful management of the NSC pool. However, the mechanisms controlling NSC pool maintenance [...] Read more.
The central nervous system of adult zebrafish displays an extraordinary neurogenic and regenerative capacity. In the zebrafish adult brain, this regenerative capacity relies on neural stem cells (NSCs) and the careful management of the NSC pool. However, the mechanisms controlling NSC pool maintenance are not yet fully understood. Recently, Bone Morphogenetic Proteins (BMPs) and their downstream effector Id1 (Inhibitor of differentiation 1) were suggested to act as key players in NSC maintenance under constitutive and regenerative conditions. Here, we further investigated the role of BMP/Id1 signaling in these processes, using different genetic and pharmacological approaches. Our data show that BMPs are mainly expressed by neurons in the adult telencephalon, while id1 is expressed in NSCs, suggesting a neuron-NSC communication via the BMP/Id1 signaling axis. Furthermore, manipulation of BMP signaling by conditionally inducing or repressing BMP signaling via heat-shock, lead to an increase or a decrease of id1 expression in the NSCs, respectively. Induction of id1 was followed by an increase in the number of quiescent NSCs, while knocking down id1 expression caused an increase in NSC proliferation. In agreement, genetic ablation of id1 function lead to increased proliferation of NSCs, followed by depletion of the stem cell pool with concomitant failure to heal injuries in repeatedly injured mutant telencephala. Moreover, pharmacological inhibition of BMP and Notch signaling suggests that the two signaling systems cooperate and converge onto the transcriptional regulator her4.1. Interestingly, brain injury lead to a depletion of NSCs in animals lacking BMP/Id1 signaling despite an intact Notch pathway. Taken together, our data demonstrate how neurons feedback on NSC proliferation and that BMP1/Id1 signaling acts as a safeguard of the NSC pool under regenerative conditions. Full article
(This article belongs to the Special Issue Neurogenesis and Regeneration in Teleost Central Nervous System)
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Article
KYNA/Ahr Signaling Suppresses Neural Stem Cell Plasticity and Neurogenesis in Adult Zebrafish Model of Alzheimer’s Disease
Cells 2021, 10(10), 2748; https://doi.org/10.3390/cells10102748 - 14 Oct 2021
Cited by 1 | Viewed by 1790
Abstract
Neurogenesis decreases in Alzheimer’s disease (AD) patients, suggesting that restoring the normal neurogenic response could be a disease modifying intervention. To study the mechanisms of pathology-induced neuro-regeneration in vertebrate brains, zebrafish is an excellent model due to its extensive neural regeneration capacity. Here, [...] Read more.
Neurogenesis decreases in Alzheimer’s disease (AD) patients, suggesting that restoring the normal neurogenic response could be a disease modifying intervention. To study the mechanisms of pathology-induced neuro-regeneration in vertebrate brains, zebrafish is an excellent model due to its extensive neural regeneration capacity. Here, we report that Kynurenic acid (KYNA), a metabolite of the amino acid tryptophan, negatively regulates neural stem cell (NSC) plasticity in adult zebrafish brain through its receptor, aryl hydrocarbon receptor 2 (Ahr2). The production of KYNA is suppressed after amyloid-toxicity through reduction of the levels of Kynurenine amino transferase 2 (KAT2), the key enzyme producing KYNA. NSC proliferation is enhanced by an antagonist for Ahr2 and is reduced with Ahr2 agonists or KYNA. A subset of Ahr2-expressing zebrafish NSCs do not express other regulatory receptors such as il4r or ngfra, indicating that ahr2-positive NSCs constitute a new subset of neural progenitors that are responsive to amyloid-toxicity. By performing transcriptome-wide association studies (TWAS) in three late onset Alzheimer disease (LOAD) brain autopsy cohorts, we also found that several genes that are components of KYNA metabolism or AHR signaling are differentially expressed in LOAD, suggesting a strong link between KYNA/Ahr2 signaling axis to neurogenesis in LOAD. Full article
(This article belongs to the Special Issue Neurogenesis and Regeneration in Teleost Central Nervous System)
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Review

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Review
Inflammation Regulates the Multi-Step Process of Retinal Regeneration in Zebrafish
Cells 2021, 10(4), 783; https://doi.org/10.3390/cells10040783 - 01 Apr 2021
Cited by 3 | Viewed by 1399
Abstract
The ability to regenerate tissues varies between species and between tissues within a species. Mammals have a limited ability to regenerate tissues, whereas zebrafish possess the ability to regenerate almost all tissues and organs, including fin, heart, kidney, brain, and retina. In the [...] Read more.
The ability to regenerate tissues varies between species and between tissues within a species. Mammals have a limited ability to regenerate tissues, whereas zebrafish possess the ability to regenerate almost all tissues and organs, including fin, heart, kidney, brain, and retina. In the zebrafish brain, injury and cell death activate complex signaling networks that stimulate radial glia to reprogram into neural stem-like cells that repair the injury. In the retina, a popular model for investigating neuronal regeneration, Müller glia, radial glia unique to the retina, reprogram into stem-like cells and undergo a single asymmetric division to generate multi-potent retinal progenitors. Müller glia-derived progenitors then divide rapidly, numerically matching the magnitude of the cell death, and differentiate into the ablated neurons. Emerging evidence reveals that inflammation plays an essential role in this multi-step process of retinal regeneration. This review summarizes the current knowledge of the inflammatory events during retinal regeneration and highlights the mechanisms whereby inflammatory molecules regulate the quiescence and division of Müller glia, the proliferation of Müller glia-derived progenitors and the survival of regenerated neurons. Full article
(This article belongs to the Special Issue Neurogenesis and Regeneration in Teleost Central Nervous System)
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Review
Cellular Mechanisms Participating in Brain Repair of Adult Zebrafish and Mammals after Injury
Cells 2021, 10(2), 391; https://doi.org/10.3390/cells10020391 - 14 Feb 2021
Cited by 7 | Viewed by 1619
Abstract
Adult neurogenesis is an evolutionary conserved process occurring in all vertebrates. However, striking differences are observed between the taxa, considering the number of neurogenic niches, the neural stem cell (NSC) identity, and brain plasticity under constitutive and injury-induced conditions. Zebrafish has become a [...] Read more.
Adult neurogenesis is an evolutionary conserved process occurring in all vertebrates. However, striking differences are observed between the taxa, considering the number of neurogenic niches, the neural stem cell (NSC) identity, and brain plasticity under constitutive and injury-induced conditions. Zebrafish has become a popular model for the investigation of the molecular and cellular mechanisms involved in adult neurogenesis. Compared to mammals, the adult zebrafish displays a high number of neurogenic niches distributed throughout the brain. Furthermore, it exhibits a strong regenerative capacity without scar formation or any obvious disabilities. In this review, we will first discuss the similarities and differences regarding (i) the distribution of neurogenic niches in the brain of adult zebrafish and mammals (mainly mouse) and (ii) the nature of the neural stem cells within the main telencephalic niches. In the second part, we will describe the cascade of cellular events occurring after telencephalic injury in zebrafish and mouse. Our study clearly shows that most early events happening right after the brain injury are shared between zebrafish and mouse including cell death, microglia, and oligodendrocyte recruitment, as well as injury-induced neurogenesis. In mammals, one of the consequences following an injury is the formation of a glial scar that is persistent. This is not the case in zebrafish, which may be one of the main reasons that zebrafish display a higher regenerative capacity. Full article
(This article belongs to the Special Issue Neurogenesis and Regeneration in Teleost Central Nervous System)
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