Mosaic Heterochrony in Neural Progenitors Sustains Accelerated Brain Growth and Neurogenesis in the Juvenile Killifish N. furzeri

Coolen, Marion; Labusch, Miriam; Mannioui, Abdelkrim; Bally‐Cuif, Laure

doi:10.1016/j.cub.2019.12.046

Cited by 18 publications

(56 citation statements)

References 47 publications

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“…They can however also use symmetric divisions for self-renewal (reviewed in Daynac et al, 2017). Indeed, we and others discovered that killifish RGs, are mostly quiescent, have low division potential and can also selfrenew (Coolen et al, 2020).Whether killifish RGs can also generate NGPs via asymmetric division the way mammalian NSCs create transit amplifying cells remains however elusive. There are some similarities between NGPs and mammalian transient amplifying progenitors.…”

Section: Discussionmentioning

confidence: 99%

“…Early in development, killifish RGs enter a premature quiescent state and proliferation is supported by the NGPs. This is in sharp contrast to the situation in zebrafish, where RGs represent the neurogenic population in the dorsal pallium (Kroehne et al ., 2011; Rothenaigner et al ., 2011; Coolen et al ., 2020). How these two different progenitor classes, with the NGPs appearing unique to the killifish, behave in the neuroregenesis process, and whether their neurogenic capacity is influenced by aging, remains unexplored.…”

Section: Introductionmentioning

confidence: 99%

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Aging impairs the essential contributions of non-glial progenitors to neurorepair in the dorsal telencephalon of the KillifishN. furzeri

houcke

Marien²,

Zandecki

et al. 2021

Preprint

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The aging central nervous system (CNS) of mammals displays progressive limited regenerative abilities. Recovery after loss of neurons is extremely restricted in the aged brain. Many research models fall short in recapitulating mammalian aging hallmarks or have an impractically long lifespan. We established a traumatic brain injury model in the African turquoise killifish (Nothobranchius furzeri), a regeneration-competent vertebrate model that evolved to naturally age extremely fast. Stab-wound injury of the aged killifish dorsal telencephalon unveils an impaired and incomplete regeneration response when compared to young individuals. Remarkably, killifish brain regeneration is mainly supported by atypical non-glial progenitors, yet their proliferation capacity appears declined with age. We identified a high inflammatory response and glial scarring to also underlie the hampered generation of new neurons in aged fish. These primary results will pave the way for further research to unravel the factor age in relation to neurorepair, and to improve therapeutic strategies to restore the injured and/or diseased aged mammalian CNS.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Aging impairs the essential contributions of non-glial progenitors to neurorepair in the dorsal telencephalon of the KillifishN. furzeri

houcke

Marien²,

Zandecki

et al. 2021

Preprint

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show abstract

“…Finally, lineage‐tracing experiments revealed that the heterogenous adult neural stem cells are hierarchically organized into deeply quiescent and self‐renewing reservoir stem cells supporting constitutive neurogenesis across the zebrafish life (Than‐Trong et al, 2020). Recently, a fast‐growing teleost fish N. furzerii (killifish) was shown to contain non‐glial progenitors that are rapidly dividing and contributing the quick growth of the brain (Coolen, Labusch, Mannioui, & Bally‐Cuif, 2020). Non‐glial progenitors were suggested to delay their entry into the quiescence and therefore can contribute to the fast growth needed for the short‐living killifish (Coolen et al, 2020).…”

Section: Neurogenesis and Neural Regeneration From Gliamentioning

confidence: 99%

“…Recently, a fast‐growing teleost fish N. furzerii (killifish) was shown to contain non‐glial progenitors that are rapidly dividing and contributing the quick growth of the brain (Coolen, Labusch, Mannioui, & Bally‐Cuif, 2020). Non‐glial progenitors were suggested to delay their entry into the quiescence and therefore can contribute to the fast growth needed for the short‐living killifish (Coolen et al, 2020). Such heterochrony of neural progenitors might be an underlying determining factor for the neurogenic and regenerative properties of the teleost brains, and can be instrumental in understanding the balance between quiescence and proliferation in health and disease.…”

Section: Neurogenesis and Neural Regeneration From Gliamentioning

confidence: 99%

Radial glia in the zebrafish brain: Functional, structural, and physiological comparison with the mammalian glia

Jurisch‐Yaksi

Yaksi

Kızıl

2020

Glia

114

107

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The neuroscience community has witnessed a tremendous expansion of glia research. Glial cells are now on center stage with leading roles in the development, maturation, and physiology of brain circuits. Over the course of evolution, glia have highly diversified and include the radial glia, astroglia or astrocytes, microglia, oligodendrocytes, and ependymal cells, each having dedicated functions in the brain. The zebrafish, a small teleost fish, is no exception to this and recent evidences point to evolutionarily conserved roles for glia in the development and physiology of its nervous system. Due to its small size, transparency, and genetic amenability, the zebrafish has become an increasingly prominent animal model for brain research. It has enabled the study of neural circuits from individual cells to entire brains, with a precision unmatched in other vertebrate models. Moreover, its high neurogenic and regenerative potential has attracted a lot of attention from the research community focusing on neural stem cells and neurodegenerative diseases. Hence, studies using zebrafish have the potential to provide fundamental insights about brain development and function, and also elucidate neural and molecular mechanisms of neurological diseases. We will discuss here recent discoveries on the diverse roles of radial glia and astroglia in neurogenesis, in modulating neuronal activity and in regulating brain homeostasis at the brain barriers. By comparing insights made in various animal models, particularly mammals and zebrafish, our goal is to highlight the similarities and differences in glia biology among species, which could set new paradigms relevant to humans.

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“…Our analysis of cellular volumes in this study does not indicate that a distinctive density dependent niche would be in place. In this context, it is also interesting to note that 2 intermingled types of progenitors with radial morphology in the killifish telencephalon reveal distinct proliferative behaviors [ 58 ] even if sharing the same environment, arguing for a small contribution of environmental effects on stem cell activities.…”

Section: Discussionmentioning

confidence: 99%

Reoccurring neural stem cell divisions in the adult zebrafish telencephalon are sufficient for the emergence of aggregated spatiotemporal patterns

2020

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Regulation of quiescence and cell cycle entry is pivotal for the maintenance of stem cell populations. Regulatory mechanisms, however, are poorly understood. In particular, it is unclear how the activity of single stem cells is coordinated within the population or if cells divide in a purely random fashion. We addressed this issue by analyzing division events in an adult neural stem cell (NSC) population of the zebrafish telencephalon. Spatial statistics and mathematical modeling of over 80,000 NSCs in 36 brain hemispheres revealed weakly aggregated, nonrandom division patterns in space and time. Analyzing divisions at 2 time points allowed us to infer cell cycle and S-phase lengths computationally. Interestingly, we observed rapid cell cycle reentries in roughly 15% of newly born NSCs. In agent-based simulations of NSC populations, this redividing activity sufficed to induce aggregated spatiotemporal division patterns that matched the ones observed experimentally. In contrast, omitting redivisions leads to a random spatiotemporal distribution of dividing cells. Spatiotemporal aggregation of dividing stem cells can thus emerge solely from the cells’ history.

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Mosaic Heterochrony in Neural Progenitors Sustains Accelerated Brain Growth and Neurogenesis in the Juvenile Killifish N. furzeri

Cited by 18 publications

References 47 publications

Aging impairs the essential contributions of non-glial progenitors to neurorepair in the dorsal telencephalon of the KillifishN. furzeri

Aging impairs the essential contributions of non-glial progenitors to neurorepair in the dorsal telencephalon of the KillifishN. furzeri

Radial glia in the zebrafish brain: Functional, structural, and physiological comparison with the mammalian glia

Reoccurring neural stem cell divisions in the adult zebrafish telencephalon are sufficient for the emergence of aggregated spatiotemporal patterns

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