Hilar Mossy Cells Provide the First Glutamatergic Synapses to Adult-Born Dentate Granule Cells

Chancey, Jessica Hotard; Poulsen, David J.; Wadiche, Jacques I.; Overstreet-Wadiche, Linda

doi:10.1523/jneurosci.3620-13.2014

Cited by 98 publications

(87 citation statements)

References 37 publications

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“…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). Cell-specific stimulation of these neurons may help determine their action on the regulation of adult neuronal stem cells.…”

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.

110

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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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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.

110

View full text Add to dashboard Cite

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“…Hilar mossy cell and GABA interneuron, immature, and mature newborn granule neuron are marked with calretinin and GAD67, DCX, and NeuN, respectively. In the early stage and the indirect pathway, hilar glutamatergic mossy cells input excitatory action on GABA interneurons (53). The latter exerts initially excitatory actions on immature neurons, which are depolarized by GABA due to high expression levels of the chloride importer NKCC1 (Na ϩ /K ϩ /2Cl Ϫ co-transporter), to activate phosphorylated CREB (p-CREB) signaling pathway (54) and thus to promote early maturation of newborn neurons.…”

Section: Discussionmentioning

confidence: 99%

Dysbindin-1C Is Required for the Survival of Hilar Mossy Cells and the Maturation of Adult Newborn Neurons in Dentate Gyrus

Wang

Yuan

Zhang

et al. 2014

Journal of Biological Chemistry

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Background: Dysbindin-1 isoforms are selectively reduced in schizophrenic brains. Results: Dysbindin-1C is required for the survival of hilar mossy cells and the maturation of adult newborn neurons in the dentate gyrus. Conclusion: Dysbindin-1C, but not -1A, regulates adult hippocampal neurogenesis in a non-cell autonomous manner. Significance: Reduced dysbindin-1C in the schizophrenic hippocampal formation likely contributes to the development of cognitive deficits.

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“…We have also showed that methamphetamine treatment significantly enhanced neurogenesis of granule neurons in the hippocampus following severe TBI (Rau et al, 2012). Recent evidence indicates that mossy cells are the first glutamatergic neurons to make contact with newborn granule neurons (Chancey et al, 2014). Mossy cells also provide considerable feed forward inhibition onto granule neurons via parvalbumin (PV) and somatostatin (SST) positive inhibitory interneurons.…”

Section: Impact Of Amphetamines On Cognition and Neurogenesismentioning

confidence: 78%

The neuroprotective potential of low-dose methamphetamine in preclinical models of stroke and traumatic brain injury

Rau

Ziemniak

Poulsen

2016

Progress in Neuro-Psychopharmacology and Biological Psychiatry

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Methamphetamine is a psychostimulant that was initially synthesized in 1920. Since then it has been used to treat attention deficit hyperactive disorder (ADHD), obesity and narcolepsy. However, methamphetamine has also become a major drug of abuse worldwide. Under conditions of abuse, which involve the administration of high repetitive doses, methamphetamine can produce considerable neurotoxic effects. However, recent evidence from our laboratory indicates that low doses of methamphetamine can produce robust neuroprotection when administered within 12h after severe traumatic brain injury (TBI) in rodents. Thus, it appears that methamphetamine under certain circumstances and correct dosing can produce a neuroprotective effect. This review addresses the neuroprotective potential of methamphetamine and focuses on the potential beneficial application for TBI.

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Hilar Mossy Cells Provide the First Glutamatergic Synapses to Adult-Born Dentate Granule Cells

Cited by 98 publications

References 37 publications

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

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

Dysbindin-1C Is Required for the Survival of Hilar Mossy Cells and the Maturation of Adult Newborn Neurons in Dentate Gyrus

The neuroprotective potential of low-dose methamphetamine in preclinical models of stroke and traumatic brain injury

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