Common and Distinct Features of Adult Neurogenesis and Regeneration in the Telencephalon of Zebrafish and Mammals

Abstract

In contrast to mammals, the adult zebrafish brain shows neurogenic activity in a multitude of niches present in almost all brain subdivisions. Irrespectively, constitutive neurogenesis in the adult zebrafish and mouse telencephalon share many similarities at the cellular and molecular level. However, upon injury during tissue repair, the situation is entirely different. In zebrafish, inflammation caused by traumatic brain injury or by induced neurodegeneration initiates specific and distinct neurogenic programs that, in combination with signaling pathways implicated in constitutive neurogenesis, quickly, and efficiently overcome the loss of neurons. In the mouse brain, injuryinduced inflammation promotes gliosis leading to glial scar formation and inhibition of regeneration. A better understanding of the regenerative mechanisms occurring in the zebrafish brain could help to develop new therapies to combat the debilitating consequences of brain injury, stroke, and neurodegeneration. The aim of this review is to compare the properties of neural progenitors and the signaling pathways, which control adult neurogenesis and regeneration in the zebrafish and mammalian telencephalon.

Cellular Mechanisms Participating in Brain Repair of Adult Zebrafish and Mammals after Injury

“…Recent studies also documented the expression of the inhibitor of DNA binding 1 (Id1), the chemokine receptor Cxcr4, notch1a/b, notch3, and her4 genes in RGCs [40][41][42][43][44][45]. Most of these markers in zebrafish also label embryonic RGCs in mammals or neurogenic astrocytes during adulthood, as reviewed in [9]. Consequently, RGCs (type 1 and 2 cells) have been established as bona fide NSCs in the telencephalon of adult zebrafish [31,46], able to self-renew and to provide new neurons [9].…”

“…Most of these markers in zebrafish also label embryonic RGCs in mammals or neurogenic astrocytes during adulthood, as reviewed in [9]. Consequently, RGCs (type 1 and 2 cells) have been established as bona fide NSCs in the telencephalon of adult zebrafish [31,46], able to self-renew and to provide new neurons [9].…”

“…In zebrafish, the main neurogenic niches that have been studied during adulthood are located in the telencephalon, the optic tectum, and the cerebellum. The telencephalon remains undoubtedly the most investigated region of the brain, because it shares many features and homologies with the mammalian telencephalon, particularly considering adult neurogenesis [ 9 , 24 , 25 , 26 ]. In the telencephalon, several studies have explored the identity and the diversity of the neural/progenitor cells sustaining the strong neurogenic activity observed in the different telencephalic subdomains of the zebrafish brain [ 11 , 15 , 22 , 24 , 27 , 28 ].…”

“…to vertebrates including fish, amphibians, reptiles, birds, and mammals. However, the number of neurogenic niches, the proliferation rate of neural stem/progenitor cells, the migration, and differentiation of new neurons appears to differ according to species, brain size, and lifespan [ 6 , 7 , 8 , 9 ]. In mammals, the two main neurogenic niches correspond to the subventricular zone of the lateral ventricles (SVZ) and the subgranular zone (SGZ) of the dentate gyrus (DG) of the hippocampus.…”

“…In striking contrast, the small teleost zebrafish ( Danio rerio ) displays a high number of neurogenic niches distributed throughout its entire encephalon. In addition, while regenerative neurogenesis is imperfect in mammals, teleost fish are able to repair their telencephalon from large injuries without any striking consequences and disabilities [ 9 ]. Such outstanding regenerative capacities strongly argue for a more comprehensive study of the molecular and cellular mechanisms allowing brain regeneration in teleost fish, in order to translate some important findings to humans.…”