Progenitor Cell Dynamics in the Newt Telencephalon during Homeostasis and Neuronal Regeneration

Kirkham, Matthew; Hameed, L. Shahul; Berg, Daniel A.; Wang, Heng; Simon, András

doi:10.1016/j.stemcr.2014.01.018

Cited by 43 publications

(94 citation statements)

References 37 publications

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“…For spheres in all the three groups, we observed that most cells in the spheres expressed Nestin and only a few sphere cells expressed GFAP (Figure S1B). The characteristics of these spheres correspond with that of neurospheres described in the literature …”

Section: Resultssupporting

confidence: 79%

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Exosomal 2′,3′-CNP from mesenchymal stem cells promotes hippocampus CA1 neurogenesis/neuritogenesis and contributes to rescue of cognition/learning deficiencies of damaged brain

Chen

Lin

Tsai

et al. 2020

Stem Cells Translational Medicine

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Mesenchymal stem cells (MSCs) have been used in clinical studies to treat neurological diseases and damage. However, implanted MSCs do not achieve their regenerative effects by differentiating into and replacing neural cells. Instead, MSC secretome components mediate the regenerative effects of MSCs. MSC‐derived extracellular vesicles (EVs)/exosomes carry cargo responsible for rescuing brain damage. We previously showed that EP4 antagonist‐induced MSC EVs/exosomes have enhanced regenerative potential to rescue hippocampal damage, compared with EVs/exosomes from untreated MSCs. Here we show that EP4 antagonist‐induced MSC EVs/exosomes promote neurosphere formation in vitro and increase neurogenesis and neuritogenesis in damaged hippocampi; basal MSC EVs/exosomes do not contribute to these regenerative effects. 2′,3′‐Cyclic nucleotide 3′‐phosphodiesterase (CNP) levels in EP4 antagonist‐induced MSC EVs/exosomes are 20‐fold higher than CNP levels in basal MSC EVs/exosomes. Decreasing elevated exosomal CNP levels in EP4 antagonist‐induced MSC EVs/exosomes reduced the efficacy of these EVs/exosomes in promoting β3‐tubulin polymerization and in converting toxic 2′,3′‐cAMP into neuroprotective adenosine. CNP‐depleted EP4 antagonist‐induced MSC EVs/exosomes lost the ability to promote neurogenesis and neuritogenesis in damaged hippocampi. Systemic administration of EV/exosomes from EP4‐antagonist derived MSC EVs/exosomes repaired cognition, learning, and memory deficiencies in mice caused by hippocampal damage. In contrast, CNP‐depleted EP4 antagonist‐induced MSC EVs/exosomes failed to repair this damage. Exosomal CNP contributes to the ability of EP4 antagonist‐elicited MSC EVs/exosomes to promote neurogenesis and neuritogenesis in damaged hippocampi and recovery of cognition, memory, and learning. This experimental approach should be generally applicable to identifying the role of EV/exosomal components in eliciting a variety of biological responses.

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Section: Resultssupporting

confidence: 79%

“…The characteristics of these spheres correspond with that of neurospheres described in the literature. [48][49][50][51][52][53]…”

Section: Ep 4 Antagonist-induced Msc Evs/exosomes Promote the Formamentioning

confidence: 99%

Exosomal 2′,3′-CNP from mesenchymal stem cells promotes hippocampus CA1 neurogenesis/neuritogenesis and contributes to rescue of cognition/learning deficiencies of damaged brain

Chen

Lin

Tsai

et al. 2020

Stem Cells Translational Medicine

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“…? troublesHootInG 20| Perform the same procedure (Steps [11][12][13][14][15][16][17][18][19] for each fish in every imaging session.  crItIcal step The frequency of repetitive imaging sessions and the total duration of the experiment depend on the type of behavior the researcher wants to observe.…”

Section: |mentioning

confidence: 99%

“…However, only in some species such as zebrafish or salamanders do aNSCs contribute to successful neuronal regeneration after injury [13][14][15][16] . Given the importance of aNSCs in the intact brain and the potential therapeutic applications of NSCs for brain regeneration in the case of brain injury or neurodegenerative diseases, it is important to investigate their cellular behavior with the aim of understanding the processes controlling their maintenance in the intact brain or recruitment during regeneration.…”

mentioning

confidence: 99%

Single-cell in vivo imaging of adult neural stem cells in the zebrafish telencephalon

et al. 2016

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Adult neural stem cells (aNSCs) in zebrafish produce mature neurons throughout their entire life span in both the intact and regenerating brain. An understanding of the behavior of aNSCs in their intact niche and during regeneration in vivo should facilitate the identification of the molecular mechanisms controlling regeneration-specific cellular events. A greater understanding of the process in regeneration-competent species may enable regeneration to be achieved in regeneration-incompetent species, including humans. Here we describe a protocol for labeling and repetitive imaging of aNSCs in vivo. We label single aNSCs, allowing nonambiguous re-identification of single cells in repetitive imaging sessions using electroporation of a red-reporter plasmid in Tg(gfap:GFP)mi2001 transgenic fish expressing GFP in aNSCs. We image using two-photon microscopy through the thinned skull of anesthetized and immobilized fish. Our protocol allows imaging every 2 d for a period of up to 1 month. This methodology allowed the visualization of aNSC behavior in vivo in their natural niche, in contrast to previously available technologies, which rely on the imaging of either dissociated cells or tissue slices. We used this protocol to follow the mode of aNSC division, fate changes and cell death in both the intact and injured zebrafish telencephalon. This experimental setup can be widely used, with minimal prior experience, to assess key factors for processes that modulate aNSC behavior. A typical experiment with data analysis takes up to 1.5 months.

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“…Adult neurogenesis has also been studied in the telencephalon of other non-mammalian species such as birds (Goldman and Nottebohm, 1983;Nordeen and Nordeen, 1988a, b;Álvarez-Buylla et al 1990Álvarez-Buylla et al , 19921998, Walton et al 2012Mazengenya et al 2018), reptiles (Pérez-Cañellas and García-Verdugo, 1996;Font et al 2001), amphibians (Simmons et al 2008;Kirkham et al 2014;Joven and Simon, 2018) and fish (Adolf et al 2006;Grandel et al 2006;Zupanc, 2006;März et al 2010;Quintana-Urzainqui et al 6 2015; reviewed by Ganz and Brand, 2016). Similarities between mammals and these groups have been found regarding the main types of cells found in the telencephalic neurogenic niche and the molecular markers they express.…”

Section: Introductionmentioning

confidence: 99%

Characterization of neurogenic niches in the telencephalon of juvenile and adult sharks

Docampo-Seara

Pereira-Guldrís

Sánchez-Farías

et al. 2019

Preprint

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Neurogenesis is a multistep process by which progenitor cells become terminally differentiated neurons. Adult neurogenesis has gathered increasing interest with the aim of developing new cell-based treatments for neurodegenerative diseases in humans. Active sites of adult neurogenesis exist from fish to mammals, although in the adult mammalian brain the number and extension of neurogenic areas is considerably reduced in comparison to non-mammalian vertebrates, and they become mostly reduced to the telencephalon. Much of our understanding in this field is based in studies on mammals and zebrafish, a modern bony fish. The use of the cartilaginous fish Scyliorhinus canicula (representative of basal gnathostomes) as a model expands the comparative framework to a species that shows highly neurogenic activity in the adult brain. In this work, we studied the proliferation pattern in the telencephalon of juvenile and adult specimens of S. canicula by using antibodies against the proliferation marker PCNA. We have characterized proliferating niches by using stem cell markers (Sox2), glial markers (GFAP, BLBP and GS), intermediate progenitor cell markers (Dlx2 and Tbr2) and markers for migrating neuroblasts (DCX). Based in the expression pattern of these markers, we demonstrate the existence of different cell subtypes within the PCNA immunoreactive zones including non-glial stem cells, glial progenitors, intermediate progenitor-like cells and migratory neuroblasts, which were widely distributed in the ventricular zone of the pallium, suggesting that the main progenitor types that constitute the neurogenic niche in mammals are already present in cartilaginous fishes.

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Progenitor Cell Dynamics in the Newt Telencephalon during Homeostasis and Neuronal Regeneration

Cited by 43 publications

References 37 publications

Exosomal 2′,3′-CNP from mesenchymal stem cells promotes hippocampus CA1 neurogenesis/neuritogenesis and contributes to rescue of cognition/learning deficiencies of damaged brain

Exosomal 2′,3′-CNP from mesenchymal stem cells promotes hippocampus CA1 neurogenesis/neuritogenesis and contributes to rescue of cognition/learning deficiencies of damaged brain

Single-cell in vivo imaging of adult neural stem cells in the zebrafish telencephalon

Characterization of neurogenic niches in the telencephalon of juvenile and adult sharks

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