Neurogenesis and Neuronal Regeneration in the Adult Reptilian Brain (original) (raw)
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Proliferation, neurogenesis and regeneration in the non-mammalian vertebrate brain
Philosophical Transactions of the Royal Society B: Biological Sciences, 2008
Post-embryonic neurogenesis is a fundamental feature of the vertebrate brain. However, the level of adult neurogenesis decreases significantly with phylogeny. In the first part of this review, a comparative analysis of adult neurogenesis and its putative roles in vertebrates are discussed. Adult neurogenesis in mammals is restricted to two telencephalic constitutively active zones. On the contrary, non-mammalian vertebrates display a considerable amount of adult neurogenesis in many brain regions. The phylogenetic differences in adult neurogenesis are poorly understood. However, a common feature of vertebrates (fish, amphibians and reptiles) that display a widespread adult neurogenesis is the substantial post-embryonic brain growth in contrast to birds and mammals. It is probable that the adult neurogenesis in fish, frogs and reptiles is related to the coordinated growth of sensory systems and corresponding sensory brain regions. Likewise, neurons are substantially added to the olfactory bulb in smell-oriented mammals in contrast to more visually oriented primates and songbirds, where much fewer neurons are added to the olfactory bulb. The second part of this review focuses on the differences in brain plasticity and regeneration in vertebrates. Interestingly, several recent studies show that neurogenesis is suppressed in the adult mammalian brain. In mammals, neurogenesis can be induced in the constitutively neurogenic brain regions as well as ectopically in response to injury, disease or experimental manipulations. Furthermore, multipotent progenitor cells can be isolated and differentiated in vitro from several otherwise silent regions of the mammalian brain. This indicates that the potential to recruit or generate neurons in non-neurogenic brain areas is not completely lost in mammals. The level of adult neurogenesis in vertebrates correlates with the capacity to regenerate injury, for example fish and amphibians exhibit the most widespread adult neurogenesis and also the greatest capacity to regenerate central nervous system injuries. Studying these phenomena in non-mammalian vertebrates may greatly increase our understanding of the mechanisms underlying regeneration and adult neurogenesis. Understanding mechanisms that regulate endogenous proliferation and neurogenic permissiveness in the adult brain is of great significance in therapeutical approaches for brain injury and disease.
Journal of Proteomics, 2014
The molecular pathways that trigger the amazing intrinsic regenerative ability of echinoderm nervous system are still unknown. In order to approach this subject, a 2D-DIGE proteomic strategy was used, to screen proteome changes during neuronal regeneration in vivo, using starfish (Asteroidea, Echinodermata) as a model. A total of 528 proteins showed significant variations during radial nerve cord regeneration in both soluble and membrane proteinenriched fractions. Several functional classes of proteins known to be involved in axon regeneration events in other model organisms, such as chordates, were identified for the first time in the regenerating echinoderm nervous system. Unexpectedly, most of the identified proteins presented a molecular mass either higher or lower than expected. Such results suggest a functional modulation through protein post-translational modifications, such as proteolysis.
Progenitor Radial Cells and Neurogenesis in Pejerrey Fish Forebrain
Brain, Behavior and Evolution, 2010
The central nervous system of adult teleost fish is peculiar because of the following features: (1) the persistence of radial glial cells, (2) an important neurogenic activity and (3) a high aromatase expression by radial cells. In this study, the proliferative zones of the forebrain were described using bromodeoxyuridine (BrdU) treatment in the brain of the pejerrey, an Acanthopterygian teleost fish. These cells were shown to have morphological and immunoreactive characteristics of radial cells and to express aromatase. Three different progenitor populations were identified based on the mobility and proliferation capacity 6 weeks after BrdU treatment: transit amplifying progenitors, slowly proliferating stem cells, and cells remaining in the proliferative zones showing no signs of mitotic activity. The proliferative cells were always located in the ventricular zone and were never observed in the brain parenchyma; however, 3 weeks later they were found away from these proliferative zones and displayed acetylated tubulin immunoreactivity. Other BrdU-positive cells showed astrocyte morphology and were immunoreactive to the S100 glial marker. These results show that in this fish, radial cells are true progenitors generating neurons and possibly astrocytes.
Isolation and characterization of a neural progenitor cell line from tilapia brain
Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 2008
Astroglial cell lines have many applications for advancing neural developmental and functional studies. However, few astroglial cell lines have been reported from fish. In this study, we report the characterization of the immortal cell line TB2 isolated from adult tilapia brain tissue. The cell line was established at 25°C in L15 medium supplemented with 15% fetal bovine serum. Most of the cells displayed a fibrous morphology and were immunoreactive for A2B5 antigen, glial fibrillary acidic protein (GFAP), keratin, vimentin, and the gap junction protein connexin 43 (Cx43). They weakly expressed glutamine synthetase (GS), S100 protein, and the neural stem cell markers Sox2 and brain lipid binding protein (BLBP). In contrast to astroglia in vivo, most TB2 cells also expressed galactocerebroside (GalC), substance P (SP), and tyrosine hydroxylase (TH). By immunoblot and RT-PCR, the cells also expressed myelin basic protein (MBP), proteolipid protein (PLP), and Cx35. On a poly-L-lysine-coated substrate in vitro, TB2 cells showed increases in neuronal dopamine decarboxylase (DDC) and microtubule-associated protein 2 (MAP2), indicating that they can initiate differentiation into neurons. Taken together, the results suggest that TB2 cells are astroglial progenitor cells (neural stem cells) and may develop into oligodendrocytes and neurons in a suitable environment. The present study advances our knowledge of fish astroglia. However, the factors that affect neural development in fish remain unknown, as do the characteristics of the intermediate differentiation stages between stem cells and mature nerve cells. The TB2 cell line will promote these investigations.
Neurogenesis in the Adult Goldfish Cerebellum
The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology, 2010
Neurogenesis was studied in the cerebellum of adult goldfish, to establish the phenomenon in this popular laboratory animal model. BrdU and proliferating cell nuclear antigen labeling revealed a high rate of cell proliferation within the molecular layer of the cerebellar corpus and valve. Most newborn cells expressed the neuronal marker beta-III-tubulin after 24 hr, supporting the goldfish cerebellum as an excellent paradigm to study vertebrate adult neurogenesis.
Journal of Bioprocessing & Biotechniques, 2014
Neural Progenitor Cells (NPCs) have gathered more and more attention in the field of Neural Stem Cells (NSCs). However, the multilineage differentiating behavior of these cells and their contribution to tissue regeneration, almost in lower vertebrate taxa, remain unknown. Since the early 1970s, many comparative studies have been performed using immunocytochemical screening on the brains of several vertebrate taxa, including teleosts, in order to identify these cells, even if the data are sometimes contrasting. This study aims: (1) to investigate in vitro the potential proliferative role of NPCs and Radial Glia Progenitors (RGP) in seabream neurogenesis; (2) to reveal the strict ability of fish NSCs to undertake the multilineage development and differentiation in neurons, astrocytes and oligodendrocytes. By the use of double Immunofluorescence (IF) analysis and phase contrast microscopy, we identified the multilineage differentiation and the exact cell morphology. We demonstrated that NSC can self-renew and differentiate into different types of neurons or glial cells during extended culturing. Mature neurons expressed specific neuronal markers; they could differentiate during long term culturing, generating an extensive neurite growth. Glia was found highly mitotic and could developed mature astrocytes and oligodendrocytes. Glial cells were assessed by Glial Fibrillary Acidic Protein (GFAP) reactivity; neurons and myelinating oligodendrocytes were immunostained with cell-specific markers. This work provide that the multilineage differentiation potential of seabream neural cell progenitors might be a useful tool for neurodegenerative diseases, being a promising approach for repairing the CNS injuries, also in other animals, as a new coming strategy for function recovery of damaged nerves.
Neuronal regeneration in a zebrafish model of adult brain injury
Disease models & mechanisms, 2012
Neural stem cells in the subventricular zone (SVZ) of the adult mammalian forebrain are a potential source of neurons for neural tissue repair after brain insults such as ischemic stroke and traumatic brain injury (TBI). Recent studies show that neurogenesis in the ventricular zone (VZ) of the adult zebrafish telencephalon has features in common with neurogenesis in the adult mammalian SVZ. Here, we established a zebrafish model to study injury-induced neurogenesis in the adult brain. We show that the adult zebrafish brain possesses a remarkable capacity for neuronal regeneration. Telencephalon injury prompted the proliferation of neuronal precursor cells (NPCs) in the VZ of the injured hemisphere, compared with in the contralateral hemisphere. The distribution of NPCs, viewed by BrdU labeling and ngn1-promoter-driven GFP, suggested that they migrated laterally and reached the injury site via the subpallium and pallium. The number of NPCs reaching the injury site significantly decre...
Acute stress promotes post-injury brain regeneration in fish
Brain Research, 2017
The central nervous system and the immune system, the two major players in homeostasis, operate in the ongoing bidirectional interaction. Stress is the third player that exerts strong effect on these two 'supersystems'; yet, its impact is studied much less. In this work employing carp model, we studied the influence of preliminary stress on neural and immune networks involved in post-injury brain regeneration. The relevant in-vivo models of air-exposure stress and precisely directed cerebellum injury have been developed. Neuronal regeneration was evaluated by using specific tracers of cell proliferation and differentiation. Involvement of immune networks was accessed by monitoring the expression of selected T cells markers. Contrast difference between acute and chronic stress manifested in the fact that chronically stressed fish did not survive the brain injury. Neuronal regeneration appeared as a biphasic process whereas involvement of immune system proceeded as a monophasic route. In stressed fish, immune response was fast and accompanied or even preceded neuronal regeneration. In unstressed subjects, immune response took place on the second phase of neuronal regeneration. These findings imply an intrinsic regulatory impact of acute stress on neuronal and immune factors involved in post-injury brain regeneration. Stress activates both neuronal and immune defense mechanisms and thus contributes to faster regeneration. In this context, paradoxically, acute preliminary stress might be considered a distinct asset in speeding up the following post-injury brain regeneration.
Adult neurogenesis in the decapod crustacean brain: a hematopoietic connection?
European Journal of Neuroscience, 2011
New neurons are produced and integrated into circuits in the adult brains of many organisms, including crustaceans. In some crustacean species, the 1 st -generation neuronal precursors reside in a niche exhibiting characteristics analogous to mammalian neurogenic niches. However, unlike mammalian niches where several generations of neuronal precursors coexist, the lineage of precursor cells in crayfish is spatially separated allowing the influence of environmental and endogenous regulators on specific generations in the neuronal precursor lineage to be defined. Experiments also demonstrate that the 1 st -generation neuronal precursors in the crayfish Procambarus clarkii are not self-renewing. A source external to the neurogenic niche must therefore provide cells that replenish the 1 st -generation precursor pool, because although these cells divide and produce a continuous efflux of 2 nd -generation cells from the niche, the population of 1 st -generation niche precursors is not diminished with growth and aging. In vitro studies show that cells extracted from the hemolymph, but not other tissues, are attracted to and incorporated into the neurogenic niche, a phenomenon that appears to involve serotonergic mechanisms. We propose that in crayfish, the hematopoietic system may be a source of cells that replenish the niche cell pool. These and other studies reviewed here establish decapod crustaceans as model systems in which the processes underlying adult neurogenesis, such as stem cell origins and transformation, can be readily explored. Studies in diverse species where adult neurogenesis occurs will result in a broader understanding of fundamental mechanisms and how evolutionary processes may have shaped the vertebrate/mammalian condition.