Axonal Control of the Adult Neural Stem Cell Niche

Tong, Cheuk Ka; Chen, Jiadong; Cebrián-Silla, Arantxa; Mirzadeh, Zaman; Obernier, Kirsten; Guinto, Cristina D.; Tecott, Laurence H.; García‐Verdugo, José Manuel; Kriegstein, Arnold R.; Alvarez-Buylla, Arturo

doi:10.1016/j.stem.2014.01.014

Cited by 120 publications

(107 citation statements)

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“…In this sense, uninjured neurons or axon branches can grow in denervated regions and reconstruct the neural circuits to compensate the impaired sensory and motor functions (axonal sprouting) (Chi et al, 2006;Liu et al, 2012). On the other hand, the existence of neural progenitor cells at the brain subventricular and subgranular zones is also well-known (Alvarez-Buylla and Garcia-Verdugo, 2002;Felix et al, 2012;Tong et al, 2014) and also at the subependimal zone of the spinal cord (Liu et al, 2012;Portiansky et al, 2011) that promote neurogenesis during aging , after neurodegenerative processes (Chang et al, 2008;Regensburger et al, 2014) or injury (Darian-Smith, 2009;Zhang et al, 2014). Thus, some of these processes may explain the improvement on the sensory and motor performance and the increase in the number of neurons after a week found in rats of KA0.75 and KA1 groups here reported.…”

Section: Discussionmentioning

confidence: 96%

Functional and histopathological changes induced by intraparenchymal injection of kainic acid in the rat cervical spinal cord

et al. 2015

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Kainic acid (KA) is an analog of the neurotransmitter glutamate and is widely used as an excitotoxic agent to lesion spinal cord networks, thus, providing an interesting model to learn basic mechanisms of spinal cord injury. The present work was aimed to evaluate motor and sensory performance of rats and analyze morphometric parameters of spinal cord neurons after KA injection. Animals were injected either with 0.75, 1 or 1.25 mM of KA at the C5 segment of the cervical spinal cord. Motor and sensory performance of the rats were evaluate at day 0 (before injection) and at days 1, 2, 3 and 7 post-injection (pi) and compared with those of saline-treated and non-operated animals. Animals were sacrificed at each time point for morphometric and histopathological analysis and compared among groups. All KA-treated animals showed a significant impairment at the motor and sensory tests for the ipsilateral forelimb in a concentration-dependent manner in comparison to saline-treated and non-operated animals. Neuronal cell count showed a significant loss of neurons at C4, C5 and C6 cervical segments when compared with those of saline-treated and non-operated animals. The contralateral side of the cervical segments in KA-treated rats remained unchanged. Some improvement at the motor and sensory tests was observed in animals injected with 0.75 and 1mM KA. Moreover, a mild increase in the neuronal count of the damaged segments was also recorded. The improvement recorded in the motor and sensory tests by day 7 pi may be a consequence of a neuron repairing mechanism triggered soon after the KA excitotoxic effect.

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Section: Discussionmentioning

confidence: 96%

Functional and histopathological changes induced by intraparenchymal injection of kainic acid in the rat cervical spinal cord

et al. 2015

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“…This might suggest that any glutamatergic signals received by stem cell processes would reflect the activity of subcortical inputs, such as long-range axons from the supramamillary nucleus (70). Notably, long-range serotonergic axons from the raphe arborize in the SVZ neurogenic niche and regulate the birth of new neurons (71). Other inputs to the inner ML emanate from commissural fibers or hilar mossy cells (72)(73)(74), which provide the first glutamatergic synapses onto newborn neurons of the dentate gyrus (75).…”

Section: Discussionmentioning

confidence: 99%

Fine processes of Nestin-GFP–positive radial glia-like stem cells in the adult dentate gyrus ensheathe local synapses and vasculature

Moss

Gebara

Bushong

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

107

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Adult hippocampal neurogenesis relies on the activation of neural stem cells in the dentate gyrus, their division, and differentiation of their progeny into mature granule neurons. The complex morphology of radial glia-like (RGL) stem cells suggests that these cells establish numerous contacts with the cellular components of the neurogenic niche that may play a crucial role in the regulation of RGL stem cell activity. However, the morphology of RGL stem cells remains poorly described. Here, we used light microscopy and electron microscopy to examine Nestin-GFP transgenic mice and provide a detailed ultrastructural reconstruction analysis of Nestin-GFP-positive RGL cells of the dentate gyrus. We show that their primary processes follow a tortuous path from the subgranular zone through the granule cell layer and ensheathe local synapses and vasculature in the inner molecular layer. They share the ensheathing of synapses and vasculature with astrocytic processes and adhere to the adjacent processes of astrocytes. This extensive interaction of processes with their local environment could allow them to be uniquely receptive to signals from local neurons, glia, and vasculature, which may regulate their fate.adult neurogenesis | adult neural stem cell | neurogenic niche | electron microscopy | hippocampus N eurogenesis in the adult mouse brain primarily occurs within discrete niches, the subventricular zone (SVZ), and the subgranular zone (SGZ) of the dentate gyrus, supplying new neurons to the olfactory bulb and the dentate gyrus, respectively (1-3). Neural stem cells of these niches can be activated to divide and generate other stem cells, astrocytes, or new neurons (4, 5). Newborn neurons of the dentate gyrus have the capacity to integrate into the existing hippocampal circuitry (6-8), influencing processes such as learning and memory (9-11) as well as stress and depression (12).Radial glia-like (RGL) neural stem cells of the SVZ, which supply the olfactory bulb with newborn neurons and astrocytes, express astrocytic markers and form elegant pinwheel structures (13-16). RGL neural stem cells of the adult dentate gyrus also express astrocytic markers, but comprise a heterogeneous population based on the molecular markers they express, the morphologies they exhibit (17-22), and their fate (23-28). Nestin-GFP-positive RGL stem cells account for more than 70% of RGL stem cells in the SGZ of the dentate gyrus (24), but it was recently found that not all Nestin-GFP-positive cells with RGL morphology have stem cell properties (29): type β cells, which arborize in the granule cell layer (GCL) but do not reach the molecular layer (ML) of the dentate gyrus, account for 26% of Nestin-GFP-positive RGL stem cells. They express stem cell (Sox1, Sox2, Prominin 1, GFAP, and Nestin) and astrocytic [GFAP, glial glutamate tranporter 1 (GLT1), and S100β] markers but do not proliferate. In contrast, type α cells, which extend across the GCL and arborize in the inner ML, account for 74% of Nestin-GFP-positive RGL cells. They express stem...

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“…For instance, serotonin (5-HT) acts through receptors in the V-SVZ, regulating cell proliferation and OB neurogenesis (Brezun and Daszuta 1999;Banasr et al 2004). Recent data indicates that most, if not all, 5-HT axons are supraependymal and form a dense plexus contacting both ependymal and type B1 cells (Tong et al 2014a). These supraependymal 5-HT axons directly regulate neurogenesis from type B1 cells.…”

Section: The Role Of Neurotransmitters In the V-svzmentioning

confidence: 99%

The Adult Ventricular–Subventricular Zone (V-SVZ) and Olfactory Bulb (OB) Neurogenesis

Lim

Alvarez-Buylla

2016

Cold Spring Harb Perspect Biol

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A large population of neural stem/precursor cells (NSCs) persists in the ventricular-subventricular zone (V-SVZ) located in the walls of the lateral brain ventricles. V-SVZ NSCs produce large numbers of neuroblasts that migrate a long distance into the olfactory bulb (OB) where they differentiate into local circuit interneurons. Here, we review a broad range of discoveries that have emerged from studies of postnatal V-SVZ neurogenesis: the identification of NSCs as a subpopulation of astroglial cells, the neurogenic lineage, new mechanisms of neuronal migration, and molecular regulators of precursor cell proliferation and migration. It has also become evident that V-SVZ NSCs are regionally heterogeneous, with NSCs located in different regions of the ventricle wall generating distinct OB interneuron subtypes. Insights into the developmental origins and molecular mechanisms that underlie the regional specification of V-SVZ NSCs have also begun to emerge. Other recent studies have revealed new cellintrinsic molecular mechanisms that enable lifelong neurogenesis in the V-SVZ. Finally, we discuss intriguing differences between the rodent V-SVZ and the corresponding human brain region. The rapidly expanding cellular and molecular knowledge of V-SVZ NSC biology provides key insights into postnatal neural development, the origin of brain tumors, and may inform the development regenerative therapies from cultured and endogenous human neural precursors. N ew neurons continue to be added throughout life to the olfactory bulb (OB) in the brain of many mammals. In rodents, the adult germinal region for OB neurogenesis is located along the walls of the brain lateral ventricles. Recent results regarding the spatial arrangement and cellular morphology of the primary neural precursors-or, neural stem cells (NSCs)-indicate that this region has characteristics similar to both the embryonic ventricular zone (VZ) and subventricular zone (SVZ). Given this new understanding, we now refer to this region as the ventricular-subventricular zone (V-SVZ).Neuroblasts born from NSCs in the mouse V-SVZ migrate rostrally into the OB where they then disperse radially and differentiate into functional interneurons (Fig. 1). Several distinct interneuron subtypes are generated by the V-SVZ, and estimates indicate that thousands of new OB neurons are generated every day in the young adult rodent brain.

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Axonal Control of the Adult Neural Stem Cell Niche

Cited by 120 publications

References 44 publications

Functional and histopathological changes induced by intraparenchymal injection of kainic acid in the rat cervical spinal cord

Functional and histopathological changes induced by intraparenchymal injection of kainic acid in the rat cervical spinal cord

Fine processes of Nestin-GFP–positive radial glia-like stem cells in the adult dentate gyrus ensheathe local synapses and vasculature

The Adult Ventricular–Subventricular Zone (V-SVZ) and Olfactory Bulb (OB) Neurogenesis

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