From embryo to adult: persistent neurogenesis and apoptotic cell death shape the lobster deutocerebrum (original) (raw)
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Regulation of life-long neurogenesis in the decapod crustacean brain
Arthropod Structure & Development, 2003
This article provides an overview of our understanding of lifelong neurogenesis in the decapod crustacean brain, where the proliferation of sensory and interneurons is controlled by many of the same factors as is neurogenesis in the mammalian brain. The relative simplicity, spatial organization and accessibility of the crustacean brain provide opportunities to examine specific neuronal pathways that regulate neurogenesis and the sequence of gene expression that leads to neuronal differentiation.
The Journal of Comparative Neurology, 2007
Continuous neurogenesis persists during adulthood in the olfactory midbrain of decapod crustaceans, including spiny lobsters, Panulirus argus. This encompasses generation of projection and local interneurons, whose somata are in the lateral soma cluster (LC) and medial soma cluster (MC), respectively. Both neuronal types originate from immediate precursors labeled by a single injection of BrdU and located in a small proliferation zone within each cluster. The aim of this study was to identify neuroblasts as a source of the dividing cells by multiple injections of BrdU over 2 days. All animals receiving multiple injections had one or a few 'extra' BrdU-positive nuclei near the proliferation zones, and these nuclei were significantly larger than nuclei of neurons or BrdU-positive cells in the proliferation zones. Since the defining morphological feature of neuroblasts in preadult neurogenesis in arthropods is being larger than their progeny, these large extra BrdU-positive nuclei represent "putative adult neuroblasts." Multiple BrdU-injections revealed a clump of small cells enclosing the putative adult neuroblasts in LC and MC, and these cells shared morphological characteristics with newly identified putative glial cells in the soma clusters and perivascular cells in the walls of arterioles. These results on P. argus suggest that adult neurogenesis is based on one adult neuroblast per soma cluster, adult neurogenesis appears to be a continuation of embryonic and larval neurogenesis, and the newly identified clumps of cells surrounding the putative adult neuroblasts might provide them with specific microenvironments necessary for their unusual lifelong proliferative and self-renewal capacity. J. Comp. Neurol. 503:64 -84, 2007.
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.
Adult neurogenesis: A common strategy across diverse species
The Journal of Comparative Neurology, 2006
Adult neurogenesis, the generation of new neurons from adult precursor cells, occurs in the brains of a phylogenetically diverse array of animals. In the higher (amniotic) vertebrates, these precursor cells are glial cells that reside within specialized regions, known as neurogenic niches, the elements of which both support and regulate neurogenesis. The in vivo identity and location of the precursor cells responsible for adult neurogenesis in nonvertebrate taxa, however, remain largely unknown. Among the invertebrates, adult neurogenesis has been particularly well characterized in freshwater crayfish (Arthropoda, Crustacea), although the identity of the precursor cells sustaining continuous neuronal proliferation in these animals has yet to be established. Here we provide evidence suggesting that, as in the higher vertebrates, the precursor cells maintaining adult neurogenesis in the crayfish Procambarus clarkii are glial cells. These precursor cells reside within a specialized region, or niche, on the ventral surface of the brain, and their progeny migrate from this niche along glial fibers and then proliferate to form new neurons in the central olfactory pathway. The niche in which these precursor cells reside has many features in common with the neurogenic niches of higher vertebrates. These commonalities include: glial cells functioning as both precursor and support cells, directed migration, close association with the brain vasculature, and specialized basal laminae. The cellular machinery maintaining adult neurogenesis appears, therefore, to be shared by widely disparate taxa. These extensive structural and functional parallels suggest a common strategy for the generation of new neurons in adult brains.
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
2012
Background: In the decapod crustacean brain, neurogenesis persists throughout the animal's life. After embryogenesis, the central olfactory pathway integrates newborn olfactory local and projection interneurons that replace old neurons or expand the existing population. In crayfish, these neurons are the descendants of precursor cells residing in a neurogenic niche. In this paper, the development of the niche was documented by monitoring proliferating cells with S-phase-specific markers combined with immunohistochemical, dye-injection and pulsechase experiments. Results: Between the end of embryogenesis and throughout the first post-embryonic stage (POI), a defined transverse band of mitotically active cells (which we will term 'the deutocerebral proliferative system' (DPS) appears. Just prior to hatching and in parallel with the formation of the DPS, the anlagen of the niche appears, closely associated with the vasculature. When the hatchling molts to the second post-embryonic stage (POII), the DPS differentiates into the lateral (LPZ) and medial (MPZ) proliferative zones. The LPZ and MPZ are characterized by a high number of mitotically active cells from the beginning of post-embryonic life; in contrast, the developing niche contains only very few dividing cells, a characteristic that persists in the adult organism.
Journal of Molecular Histology, 2007
Adult neurogenesis is a characteristic feature of the olfactory pathways of decapod crustaceans. In crayfish and clawed lobsters, adult-born neurons are the progeny of precursor cells with glial characteristics located in a neurogenic niche on the ventral surface of the brain. The daughters of these precursor cells migrate during S and G 2 stages of the cell cycle along glial fibers to lateral (cluster 10) and medial (cluster 9) proliferation zones. Here, they divide (M phase) producing offspring that differentiate into olfactory interneurons. The complete lineage of cells producing neurons in these animals, therefore, is arranged along the migratory stream according to cell cycle stage. We have exploited this model to examine the influence of environmental and endogenous factors on adult neurogenesis. We find that increased levels of serotonin upregulate neuronal production, as does maintaining animals in an enriched (versus deprived) environment or augmenting their diet with omega-3 fatty acids; increased levels of nitric oxide, on the other hand, decrease the rate of neurogenesis. The features of the neurogenic niche and migratory streams, and the fact that these continue to function in vitro, 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.
Exploring neurogenesis in crustaceans
Journal of undergraduate neuroscience education : JUNE : a publication of FUN, Faculty for Undergraduate Neuroscience, 2002
Plasticity, learning and memory, and neurological disease are exciting topics for students. Discussion around these subjects often results in the consideration of the role of neurogenesis in development, or its involvement in a potential cure for some diseases. We have therefore designed a lab that allows students to experimentally examine how the rate of neurogenesis can be altered by environmental factors. Neuronal cell division in crayfish is identified with fluorescently-labeled BrdU and quantified using conventional or confocal microscopy. Recent studies indicate a conservation of mechanisms that control neurogenesis from insects and crustaceans to mammals. Yet the use of invertebrate models such as crayfish or lobsters has advantages over mammalian models. Invertebrate nervous systems have a simpler organization and larger, identifiable neurons - qualities that make such preparations easier for students to manage. This lab offers many opportunities for student designed experim...
Journal of Neurobiology, 2002
in the olfactory pathway of many decapod crustaceans. However, the relationships between precursor cells and the temporal characteristics of mitotic events in these midbrain regions have not been examined. We have conducted studies aimed at characterizing the sequence of proliferative events that leads to the production of new deutocerebral projection neurons in embryos of the American lobster, Homarus americanus. In vivo bromodeoxyuridine (BrdU) labeling patterns show that three distinct cell types are involved in neurogenesis in this region. Quantitative and temporal analyses suggest that the clearing time for BrdU is 2-3 days in lobster embryos, and that the sequence of proliferative events in the midbrain is significantly different from the stereotypical pattern for the generation of neurons in the ventral nerve cord ganglia of insects and crustaceans. The unusual pattern of proliferation in the crustacean midbrain may be related to the persistence of neurogenesis throughout life in these regions.
Adult neurogenesis and functional plasticity in neuronal circuits
Nature Reviews Neuroscience, 2006
New neurons are continually being generated in the adult brain. Two regions -the olfactory bulb and the dentate gyrus of the hippocampus -receive and integrate newborn neurons throughout adult life. In these regions, the addition of new neurons represents another means, further to molecular, synaptic or morphological alterations in individual cells, by which the brain can make changes to its own functional circuitry. Indeed, this cell-level renovation is not static or merely restorative -instead, adult neurogenesis constitutes an adaptive response to challenges imposed by an animal's environment and/or its internal state. This raises some important questions about the role of neurogenesis in mature neuronal circuits. Owing to space constraints, we concentrate on the neurogenic systems of vertebrates, and primarily those of mammals.