Receptor-mediated glutamate release from volume sensitive channels in astrocytes

Takano, Takahiro; Kang, Jian; Jaiswal, Jyoti K.; Simon, Sanford M.; Lin, Jane H.-C.; Yu, Yufei; Li, Yuxing; Yang, Jay; Dienel, Gerald A.; Zielke, H. Ronald

doi:10.1073/pnas.0506382102

Cited by 186 publications

(188 citation statements)

References 30 publications

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“…Lowering osmolarity enhances the release of multiple transmitters from neurons (Schousboe and Pasantes-Morales, 1992) and glia (Darby et al, 2003;Takano et al, 2005), some of which inhibit I M by releasing Ca 2ϩ from IP 3 -sensitive stores in the endoplasmic reticulum (Delmas and Brown, 2005). However, hyposmotic release of internally stored Ca 2ϩ was observed also in dissociated CA1 pyramidal cells devoid of contacts with other neurons or glia (Borgdorff et al, 2000), as well as in many cell types other than neurons (Fischer et al, 1997;Missiaen et al, 1997).…”

Section: Role Of Internal Camentioning

confidence: 96%

K_V7/M Channels Mediate Osmotic Modulation of Intrinsic Neuronal Excitability

Caspi¹,

Benninger²,

Yaari³

2009

J. Neurosci.

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Modest decreases in extracellular osmolarity induce brain hyperexcitability that may culminate in epileptic seizures. At the cellular level, moderate hyposmolarity markedly potentiates the intrinsic neuronal excitability of principal cortical neurons without significantly affecting their volume. The most conspicuous cellular effect of hyposmolarity is converting regular firing neurons to burst-firing mode. This effect is underlain by hyposmotic facilitation of the spike afterdepolarization (ADP), but its ionic mechanism is unknown. Because blockers of K V 7 (KCNQ) channels underlying neuronal M-type K ϩ currents (K V 7/M channels) also cause spike ADP facilitation and bursting, we hypothesized that lowering osmolarity inhibits these channels. Using current-and voltage-clamp recordings in CA1 pyramidal cells in situ, we have confirmed this hypothesis. Furthermore, we show that hyposmotic inhibition of K V 7/M channels is mediated by an increase in intracellular Ca 2ϩ concentration via release from internal stores but not via influx of extracellular Ca 2ϩ . Finally, we show that interfering with internal Ca 2ϩ -mediated inhibition of K V 7/M channels entirely protects against hyposmotic ADP facilitation and bursting, indicating the exclusivity of this novel mechanism in producing intrinsic neuronal hyperexcitability in hyposmotic conditions.

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Section: Role Of Internal Camentioning

confidence: 96%

K_V7/M Channels Mediate Osmotic Modulation of Intrinsic Neuronal Excitability

Caspi¹,

Benninger²,

Yaari³

2009

J. Neurosci.

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“…Rat astrocytes were isolated as described in ref. 40 and grown in DMEM/F12 media supplemented with 10% FBS and 0.75% glucose (SigmaAldrich, St. Louis, MO) in 5% pCO 2 at 37°C. For imaging, cells were plated onto glass coverslips (Fisher Scientific, Pittsburgh, PA) or on glass-bottom dishes (MatTek, Ashland, MA) coated with 1% gelatin (Sigma-Aldrich) and imaged in OptiMEM (Invitrogen, Carlsbad, CA).…”

Section: Methodsmentioning

confidence: 99%

Resolving vesicle fusion from lysis to monitor calcium-triggered lysosomal exocytosis in astrocytes

Jaiswal

Fix

Takano

et al. 2007

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

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Optical imaging of individual vesicle exocytosis is providing new insights into the mechanism and regulation of secretion by cells. To study calcium-triggered secretion from astrocytes, we used acridine orange (AO) to label vesicles. Although AO is often used for imaging exocytosis, we found that imaging vesicles labeled with AO can result in their photolysis. Here, we define experimental and analytical approaches that permit us to distinguish unambiguously between fusion, leakage, and lysis of individual vesicles. We have used this approach to demonstrate that lysosomes undergo calcium-triggered exocytosis in astrocytes.acridine orange ͉ imaging ͉ secretion ͉ evanescent wave microscopy ͉ ATP E xocytosis, the process by which a vesicle inside of a cell fuses to the cell surface, serves a plethora of important functions in all eukaryotic cells. These include insertion of membrane proteins such as ion channels and receptors, addition of new membranes during neuronal development, and secretion of neurotransmitter at the synapse.Over the past few decades, much has been learned about the physiology of exocytosis in neurons. Through the use of biochemistry, electrophysiology, and genetics, a considerable body of knowledge has been gathered about the molecular participants in exocytosis. However, much remains to be learned about the dynamics of these molecules. Our knowledge has been limited in part by our ability to image single molecules, or even the fusion of single vesicles. Fortunately, the use of total internal reflection fluorescence microscopy (TIR-FM) allows imaging fusion of single vesicles (1-6).Ca 2ϩ -triggered exocytosis, considered a hallmark of excitable cells, has also been reported in nonexcitable cells such as fibroblasts (5,(7)(8)(9). In all nonexcitable cells, Ca 2ϩ -triggered exocytosis is believed to serve a role in membrane repair (10). Additionally, some cells, such as hematopoietic cells, use Ca 2ϩ -triggered exocytosis for specialized functions such as release of cytolytic molecules (11). Astrocytes are nonexcitable cells of the nervous system that were previously thought to have only a protective role for neurons. However, astrocytes have now been shown to be more intricately involved in regulating neuronal physiology (12)(13)(14). This is believed in part to be due to the ability of astrocytes to exocytose a variety of molecules (15).Exocytosis of synaptic vesicles (16), dense core granules (3, 17), and even astrocytic vesicles that undergo Ca 2ϩ -triggered exocytosis (18) have been imaged by using the fluorescence of acridine orange (AO), a weak base that accumulates in acidified vesicles (19). Accumulation at high concentrations causes quenching of AO fluorescence. On release from the vesicle, AO fluorescence is unquenched and thus increases rapidly. Such rapid increase in AO fluorescence followed by its lateral diffusion is called an ''AO flash'' and has been used as a hallmark of exocytosis (3,(20)(21)(22).To examine potential Ca 2ϩ -regulated exocytic vesicles in astrocytes, we incubate...

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“…One reasonable interpretation of this result is that the downregulation of GLT-1 increased the glutamate concentration in the synaptic cleft, which in turn excessively activated NMDARs. As astrocytes may release glutamate from volume-sensitive channels (Takano et al, 2005), there is the possibility that reduced water transport via AQP4 alter glutamate release from volume-sensitive channels in astrocytes. Thus, increased activation of NMDAR in AQP4 KO mice may also result from altered glutamate release and uptake in astrocytes.…”

Section: Aqp4 Regulates Amygdala Ltp and Memory Y-k LI Et Almentioning

confidence: 99%

Aquaporin-4 Deficiency Impairs Synaptic Plasticity and Associative Fear Memory in the Lateral Amygdala: Involvement of Downregulation of Glutamate Transporter-1 Expression

Wang

et al. 2012

Neuropsychopharmacol

101

105

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Astrocytes are implicated in information processing, signal transmission, and regulation of synaptic plasticity. Aquaporin-4 (AQP4) is the major water channel in adult brain and is primarily expressed in astrocytes. A growing body of evidence indicates that AQP4 is a potential molecular target for the regulation of astrocytic function. However, little is known about the role of AQP4 in synaptic plasticity in the amygdala. Therefore, we evaluated long-term potentiation (LTP) in the lateral amygdala (LA) and associative fear memory of AQP4 knockout (KO) and wild-type mice. We found that AQP4 deficiency impaired LTP in the thalamo-LA pathway and associative fear memory. Furthermore, AQP4 deficiency significantly downregulated glutamate transporter-1 (GLT-1) expression and selectively increased NMDA receptor (NMDAR)-mediated EPSCs in the LA. However, low concentration of NMDAR antagonist reversed the impairment of LTP in KO mice. Upregulating GLT-1 expression by chronic treatment with ceftriaxone also reversed the impairment of LTP and fear memory in KO mice. These findings imply a role for AQP4 in synaptic plasticity and associative fear memory in the amygdala by regulating GLT-1 expression.

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Receptor-mediated glutamate release from volume sensitive channels in astrocytes

Abstract: electrophysiology ͉ exocytosis ͉ neurotransmitters ͉ osmolarity ͉ synapses

Cited by 186 publications

References 30 publications

K_V7/M Channels Mediate Osmotic Modulation of Intrinsic Neuronal Excitability

K_V7/M Channels Mediate Osmotic Modulation of Intrinsic Neuronal Excitability

Resolving vesicle fusion from lysis to monitor calcium-triggered lysosomal exocytosis in astrocytes

Aquaporin-4 Deficiency Impairs Synaptic Plasticity and Associative Fear Memory in the Lateral Amygdala: Involvement of Downregulation of Glutamate Transporter-1 Expression

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Receptor-mediated glutamate release from volume sensitive channels in astrocytes

Abstract: electrophysiology ͉ exocytosis ͉ neurotransmitters ͉ osmolarity ͉ synapses

Cited by 186 publications

References 30 publications

KV7/M Channels Mediate Osmotic Modulation of Intrinsic Neuronal Excitability

KV7/M Channels Mediate Osmotic Modulation of Intrinsic Neuronal Excitability

Resolving vesicle fusion from lysis to monitor calcium-triggered lysosomal exocytosis in astrocytes

Aquaporin-4 Deficiency Impairs Synaptic Plasticity and Associative Fear Memory in the Lateral Amygdala: Involvement of Downregulation of Glutamate Transporter-1 Expression

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K_V7/M Channels Mediate Osmotic Modulation of Intrinsic Neuronal Excitability

K_V7/M Channels Mediate Osmotic Modulation of Intrinsic Neuronal Excitability