A comparative view of regenerative neurogenesis in vertebrates

Alunni, Alessandro; Bally‐Cuif, Laure

doi:10.1242/dev.122796

Cited by 169 publications

(179 citation statements)

References 119 publications

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“…Humans and other mammals have limited ability for regenerative repair following traumatic brain injury. In contrast to mammals, zebrafish have substantially greater regenerative ability in central nervous system (CNS) (Alunni & Bally‐Cuif, ; Kaslin, Ganz, & Brand, ; Kizil, Kaslin, Kroehne, & Brand, ; Zupanc, ). Therefore, zebrafish models are important to elucidate mechanisms which enable neuronal regeneration.…”

Section: Introductionmentioning

confidence: 99%

Involvement of sonic hedgehog and notch signaling in regenerative neurogenesis in adult zebrafish optic tectum after stab injury

Ueda

Shimizu

et al. 2018

J of Comparative Neurology

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Unlike humans and other mammals, adult zebrafish have the superior capability to recover from central nervous system (CNS) injury. We previously found that proliferation of radial glia (RG) is induced in response to stab injury in optic tectum and that new neurons are generated from RG after stab injury. However, molecular mechanisms which regulate proliferation and differentiation of RG are not well known. In the present study, we investigated Shh and Notch signaling as potential mechanisms regulating regeneration in the optic tectum of adult zebrafish. We used Shh reporter fish and confirmed that canonical Shh signaling is activated specifically in RG after stab injury. Moreover, we have shown that Shh signaling promotes RG proliferation and suppresses their differentiation into neurons after stab injury. In contrast, Notch signaling was down-regulated after stab injury, indicated by the decrease in the expression level of her4 and her6, a target gene of Notch signaling. We also found that inhibition of Notch signaling after stab injury induced more proliferative RG, but that inhibition of Notch signaling inhibited generation of newborn neurons from RG after stab injury. These results suggest that high level of Notch signaling keeps RG quiescent and that appropriate level of Notch signaling is required for generation of newborn neurons from RG. Under physiological condition, activation of Shh signaling or inhibition of Notch signaling also induced RG proliferation. In adult optic tectum of zebrafish, canonical Shh signaling and Notch signaling play important roles in proliferation and differentiation of RG in physiological and regenerative conditions.

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Section: Introductionmentioning

confidence: 99%

Involvement of sonic hedgehog and notch signaling in regenerative neurogenesis in adult zebrafish optic tectum after stab injury

Ueda

Shimizu

et al. 2018

J of Comparative Neurology

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“…One focuses on adult neurogenesis as a potential repair mechanism in the human brain, investigating molecular mechanisms controlling it or at least mediating proliferation, cell fate, and survival of newly generated neurons, with emphasis on potential applications for brain repair [Martino et al, 2011;Lindvall and Kokaia, 2015;Alunni and Bally-Cuif, 2016]. This approach, which also includes comparative studies, is more fact-related, and emerging contradictions and conclusions can be reconciled.…”

Section: Introductionmentioning

confidence: 99%

Adult Neurogenesis in Mammals: Variations and Confusions

Lipp

Bonfanti

2016

Brain Behav Evol

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Mammalian adult neurogenesis has remained enigmatic. Two lines of research have emerged. One focuses on a potential repair mechanism in the human brain. The other aims at elucidating its functional role in the hippocampal formation, chiefly in cognitive processes; however, thus far it has been unsuccessful. Here, we try to recognize the sources of errors and conceptual confusion in comparative studies and neurobehavioral approaches with a focus on mice. Evolutionarily, mammalian adult neurogenesis appears as protracted juvenile neurogenesis originating from precursor cells in the secondary proliferation zones, from where newly formed cells migrate to target regions in the forebrain. This late developmental process is downregulated differentially in various brain structures depending on species and age. Adult neurogenesis declines substantially during early adulthood and persists at low levels into senescence. Short-lasting episodes in proliferation or reduction of adult neurogenesis may reflect a multitude of factors, and have been studied chiefly in mice and rats. Comparative studies face both species-specific variations in staining and technical abilities of laboratories, lacking quantification of important reference measures (e.g. granule cell number) and evaluation of maturational markers whose persistence might be functionally more relevant than proliferation rates. Likewise, the confusion about the functional role of variations in adult hippocampal neurogenesis has many causes. Prominent is an inferential statistical approach, usually with low statistical power. Interpretation is complicated by multiple theories about hippocampal function, often unrealistically extrapolating from humans to rodents. We believe that the field of mammalian adult neurogenesis needs more critical thinking, more sophisticated hypotheses, better statistical, technical and behavioral approaches, and a broader conceptual perspective incorporating comparative aspects rather than neglecting them.

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“…While a primary component of this difference relates to neuronal maturation and survival, several studies also hint to huge variations in neural progenitor cell properties, such as their propensity for recruitment and their lineage progression (Alunni and Bally-Cuif, 2016). Overall, it remains an intense subject of investigation to understand which lineages can underlie successful neurogenesis in the adult brain.…”

Section: Introductionmentioning

confidence: 99%

Embryonic origin and lineage hierarchies of the neural progenitor subtypes building the zebrafish adult midbrain

Galant

Furlan

Coolen

et al. 2016

Developmental Biology

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Neurogenesis in the post-embryonic vertebrate brain varies in extent and efficiency between species and brain territories. Distinct neurogenesis modes may account for this diversity, and several neural progenitor subtypes, radial glial cells (RG) and neuroepithelial progenitors (NE), have been identified in the adult zebrafish brain. The neurogenic sequences issued from these progenitors, and their contribution to brain construction, remain incompletely understood. Here we use genetic tracing techniques based on conditional Cre recombination and Tet-On neuronal birthdating to unravel the neurogenic sequence operating from NE progenitors in the zebrafish post-embryonic optic tectum. We reveal that a subpopulation of her5-positive NE cells of the posterior midbrain layer stands at the top of a neurogenic hierarchy involving, in order, the amplification pool of the tectal proliferation zone (TPZ), followed by her4-positive RG cells with transient neurogenic activity. We further demonstrate that the adult her5-positive NE pool is issued in lineage from an identically located NE pool expressing the same gene in the embryonic neural tube. Finally, we show that these features are reminiscent of the neurogenic sequence and embryonic origin of the her9-positive progenitor NE pool involved in the construction of the lateral pallium at post-embryonic stages. Together, our results highlight the shared recruitment of an identical neurogenic strategy by two remote brain territories, where long-lasting NE pools serve both as a growth zone and as the life-long source of young neurogenic RG cells.

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A comparative view of regenerative neurogenesis in vertebrates

Cited by 169 publications

References 119 publications

Involvement of sonic hedgehog and notch signaling in regenerative neurogenesis in adult zebrafish optic tectum after stab injury

Involvement of sonic hedgehog and notch signaling in regenerative neurogenesis in adult zebrafish optic tectum after stab injury

Adult Neurogenesis in Mammals: Variations and Confusions

Embryonic origin and lineage hierarchies of the neural progenitor subtypes building the zebrafish adult midbrain

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