Adult neurogenesis in the decapod crustacean brain: a hematopoietic connection? (original) (raw)
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The common properties of neurogenesis in the adult brain: from invertebrates to vertebrates
Comparative Biochemistry and Physiology B-biochemistry & Molecular Biology, 2002
Until recently, it was believed that adult brains were unable to generate any new neurons. However, it is now commonly known that stem cells remain in the adult central nervous system and that adult vertebrates as well as adult invertebrates are currently adding new neurons in some specialized structures of their central nervous system. In vertebrates, the subventricular zone and
Journal of Comparative Neurology
Two decades after the discovery of adult-born neurons in the brains of decapod crustaceans, the deutocerebral proliferative system (DPS) producing these neural lineages has become a model of adult neurogenesis in invertebrates. Studies on crayfish have provided substantial insights into the anatomy, cellular dynamics, and regulation of the DPS. Contrary to traditional thinking, recent evidence suggests that the neurogenic niche in the crayfish DPS lacks self-renewing stem cells, its cell pool being instead sustained via integration of hemocytes generated by the innate immune system. Here, we investigated the origin, division and migration patterns of the adultborn neural progenitor (NP) lineages in detail. We show that the niche cell pool is not only replenished by hemocyte integration but also by limited numbers of symmetric cell divisions with some characteristics reminiscent of interkinetic nuclear migration. Once specified in the niche, first generation NPs act as transit-amplifying intermediate NPs that eventually exit and produce multicellular clones as they move along migratory streams toward target brain areas. Different clones may migrate simultaneously in the streams but occupy separate tracks and show spatio-temporally flexible division patterns. Based on this, we propose an extended DPS model that emphasizes structural similarities to pseudostratified neuroepithelia in other arthropods and vertebrates. This model includes hemocyte integration and intrinsic cell proliferation to synergistically counteract niche cell pool depletion during the animal's lifespan. Further, we discuss parallels to recent findings on mammalian adult neurogenesis, as both systems seem to exhibit a similar decoupling of proliferative replenishment divisions and consuming neurogenic divisions.
Developmental Neurobiology, 2009
The birth of new neurons and their incorporation into functional circuits in the adult brain is a characteristic of many vertebrate and invertebrate organisms, including decapod crustaceans. Precursor cells maintaining lifelong proliferation in the brains of crayfish (Procambarus clarkii, Cherax destructor) and clawed lobsters (Homarus americanus) reside within a specialized niche on the ventral surface of the brain; their daughters migrate to two proliferation zones along a stream formed by processes of the niche precursors. Here they divide again, finally producing interneurons in the olfactory pathway. The present studies in P. clarkii explore (1) differential proliferative activity among the niche precursor cells with growth and aging, (2) morphological characteristics of cells in the niche and migratory streams, and (3) aspects of the cell cycle in this lineage. Morphologically symmetrical divisions of neuronal precursor cells were observed in the niche near where the migratory streams emerge, as well as in the streams and proliferation zones. The nuclei of migrating cells elongate and undergo shape changes consistent with nucleokinetic movement. LIS1, a highly conserved dynein-binding protein, is expressed in cells in the migratory stream and neurogenic niche, implicating this protein in the translocation of crustacean brain neuronal precursor cells. Symmetrical divisions of the niche precursors and migration of both daughters raised the question of how the niche precursor pool is replenished. We present here preliminary evidence for an association between vascular cells and the niche precursors, which may relate to the lifelong growth and maintenance of the crustacean neurogenic niche.
First-generation neuronal precursors in the crayfish brain are not self-renewing
International Journal of Developmental Neuroscience, 2013
Adult-born neurons in crayfish (Procambarus clarkii) are the progeny of 1st-generation precursor cells (functionally analogous to neuronal stem cells in vertebrates) that are located in a neurogenic niche on the ventral surface of the brain. The daughters of these precursor cells migrate along the processes of bipolar niche cells to proliferation zones in the cell clusters where the somata of the olfactory interneurons reside. Here they divide again, producing offspring that differentiate into olfactory local and projection neurons. The features of this neuronal assembly line, and the fact that it continues to function when the brain is isolated and perfused or maintained in organotypic culture, provide opportunities unavailable in other organisms to explore the sequence of cellular and molecular events leading to the production of new neurons in adult brains. Further, we have determined that the 1st-generation precursor cells are not a self-renewing population, and that the niche is, nevertheless, not depleted as the animals grow and age. We conclude, therefore, that the niche is not a closed system and that there must be an extrinsic source of neuronal stem cells. Based on in vitro studies demonstrating that cells extracted from the hemolymph are attracted to the niche, as well as the intimate relationship between the niche and vasculature, we hypothesize that the hematopoietic system is a likely source of these cells.
An identified serotonergic neuron regulates adult neurogenesis in the crustacean brain
Developmental Neurobiology, 2009
New neurons are born and integrated into functional circuits in the brains of many adult organisms. In virtually all of these systems, serotonin is a potent regulator of neuronal proliferation. Specific neural pathways underlying these serotonergic influences have not, however, been identified and manipulated. The goal of the present study was to test whether adult neurogenesis in the crustacean brain is influenced by electrical activity in the serotonergic dorsal giant neurons (DGNs) innervating the primary olfactory processing areas, the olfactory lobes (OLs), and higher order centers, the accessory lobes (ALs). Adult-born neurons occur in two interneuronal cell clusters that are part of the olfactory pathway. The present study demonstrates that neurogenesis also continues in these areas in a dissected, perfused brain preparation, although the rate of neuronal production is lower than in brains from intact same-sized animals. Inclusion of 10 −9 M serotonin in the perfusate delivered to the dissected brain preparation restores the rate of neurogenesis to in vivo levels. While subthreshold stimulation of the DGN does not significantly alter the rate of neurogenesis, electrical activation of a single DGN results in significant increases in neurogenesis in Cluster 10 (CL10) on the same side of the brain, compared with levels on the contralateral, unstimulated side. Measurements of serotonin levels in the perfusate using high performance liquid chromatography established that serotonin levels are elevated about ten-fold during DGN stimulation, confirming that serotonin is released during DGN activity. This is the first identified neural pathway through which adult neurogenesis has been directly manipulated.
Primary Neuronal Precursors in Adult Crayfish Brain: Replenishment from a Non-neuronal Source
BMC Neuroscience, 2011
Background: Adult neurogenesis, the production and integration of new neurons into circuits in the brains of adult animals, is a common feature of a variety of organisms, ranging from insects and crustaceans to birds and mammals. In the mammalian brain the 1 st -generation neuronal precursors, the astrocytic stem cells, reside in neurogenic niches and are reported to undergo self-renewing divisions, thereby providing a source of new neurons throughout an animal's life. In contrast, our work shows that the 1 st -generation neuronal precursors in the crayfish (Procambarus clarkii) brain, which also have glial properties and lie in a neurogenic niche resembling that of vertebrates, undergo geometrically symmetrical divisions and both daughters appear to migrate away from the niche. However, in spite of this continuous efflux of cells, the number of neuronal precursors in the crayfish niche continues to expand as the animals grow and age. Based on these observations we have hypothesized that (1) the neuronal stem cells in the crayfish brain are not self-renewing, and (2) a source external to the neurogenic niche must provide cells that replenish the stem cell pool.
Solving the Neurogenesis Puzzle: Looking for Pieces Outside the Traditional Box
Frontiers in Neuroscience
The vast majority of what is considered fact about adult neurogenesis comes from research on laboratory mice and rats: where it happens, how it works, what it does. However, this relative exclusive focus on two rodent species has resulted in a bias on how we think about adult neurogenesis. While it might not prevent us from making conclusions about the evolutionary significance of the process or even prevent us from generalizing to diverse mammals, it certainly does not help us achieve these outcomes. Here, we argue that there is every reason to expect striking species differences in adult neurogenesis: where it happens, how it works, what it does. Species-specific adaptations in brain and behavior are paramount to survival and reproduction in diverse ecological niches and it is naive to think adult neurogenesis escaped these evolutionary pressures. A neuroethological approach to the study of adult neurogenesis is essential for a comprehensive understanding of the phenomenon. Furthermore, most of us are guilty of making strong assertions about our data in order to have impact yet this ultimately creates bias in how work is performed, interpreted, and applied. By taking a step back and actually placing our results in a much larger, non-biomedical context, we can help to reduce dogmatic thinking and create a framework for discovery.
Adult neurogenesis in mammals - a theme with many variations
European Journal of Neuroscience, 2011
Investigations of adult neurogenesis in recent years have revealed numerous differences among mammalian species, reflecting the remarkable diversity in brain anatomy and function of mammals. As a mechanism of brain plasticity, adult neurogenesis might also differ due to behavioural specialization or adaptation to specific ecological niches. Because most research has focused on rodents and only limited data are available on other mammalian orders, it is hotly debated whether, in some species, adult neurogenesis also takes place outside of the well-characterized subventricular zone of the lateral ventricle and subgranular zone of the dentate gyrus. In particular, evidence for the functional integration of new neurons born in 'non-neurogenic' zones is controversial. Considering the promise of adult neurogenesis for regenerative medicine, we posit that differences in the extent, regional occurrence and completion of adult neurogenesis need to be considered from a speciesspecific perspective. In this review, we provide examples underscoring that the mechanisms of adult neurogenesis cannot simply be generalized to all mammalian species. Despite numerous similarities, there are distinct differences, notably in neuronal maturation, survival and functional integration in existing synaptic circuits, as well as in the nature and localization of neural precursor cells. We also propose a more appropriate use of terminology to better describe these differences and their relevance for brain plasticity under physiological and pathophysiological conditions. In conclusion, we emphasize the need for further analysis of adult neurogenesis in diverse mammalian species to fully grasp the spectrum of variation of this adaptative mechanism in the adult CNS.