Ca2+ entry through a non-selective cation channel in Aplysia bag cell neurons

Geiger, Julia E.; Hickey, Charlene M.; Magoski, Neil S.

doi:10.1016/j.neuroscience.2009.05.006

Cited by 16 publications

(29 citation statements)

References 99 publications

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“…Ca 2+ imaging was performed under whole‐cell voltage clamp, during which the intracellular saline was supplemented with 1 m m fura‐PE3 (Teflabs, Austin, TX, USA) to dye‐fill neurons via passive dialysis, as previously done in our laboratory (Geiger et al . ; Groten et al . ; Groten & Magoski, ).…”

Section: Methodsmentioning

confidence: 99%

Diacylglycerol‐mediated regulation of Aplysia bag cell neuron excitability requires protein kinase C

Sturgeon

Magoski

2016

The Journal of Physiology

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Following synaptic input, the bag cell neurons of Aplysia undergo a long-term afterdischarge of action potentials to secrete egg-laying hormone and initiate reproduction. Early in the afterdischarge, phospholipase C (PLC) hydrolyses phosphatidylinositol-4,5-bisphosphate into inositol trisphosphate (IP3 ) and diacylglycerol (DAG). In Aplysia, little is known about the action of DAG, or any interaction with IP3 ; thus, we examined the effects of a synthetic DAG analogue, 1-oleoyl-2-acetyl-sn-glycerol (OAG), on whole-cell voltage-clamped cultured bag cell neurons. OAG induced a large, prolonged, Ca(2+) -permeable, concentration-dependent inward current (IOAG ) that reversed at ∼-20 mV and was enhanced by intracellular IP3 . A similar current was evoked by either another DAG analogue, 1,2-dioctanoyl-sn-glycerol (DOG), or activating PLC with N-(3-trifluoromethylphenyl)-2,4,6-trimethylbenzenesulfonamide (m-3M3FBS). IOAG was reduced by the general cation channel blockers Gd(3+) or flufenamic acid. Work in other systems indicated that OAG activates channels independently of protein kinase C (PKC); however, we found pretreating bag cell neurons with any of the PKC inhibitors bisindolylmaleimide, sphinganine, or H7, attenuated IOAG . However, stimulating PKC with phorbol 12-myristate 13-acetate (PMA) did not evoke current or enhance IOAG ; moreover, unlike PMA, OAG failed to trigger PKC, as confirmed by an independent bioassay. Finally, OAG or m-3M3FBS depolarized cultured neurons, and while OAG did not provoke afterdischarges from bag cell neurons in the nervous system, it did double the duration of synaptically elicited afterdischarges. To our knowledge, this is the first report of obligate PKC activity for IOAG gating. An interaction between phosphoinositol metabolites and PKC could control the cation channel to influence afterdischarge duration.

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Section: Methodsmentioning

confidence: 99%

Diacylglycerol‐mediated regulation of Aplysia bag cell neuron excitability requires protein kinase C

Sturgeon

Magoski

2016

The Journal of Physiology

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“…Previous studies have proposed that inhalational anesthetics induce apoptosis via dysregulated intracellular calcium homeostasis (5,7,13). Ca 2+ regulation in neurons is complex.…”

Section: Discussionmentioning

confidence: 99%

“…Similar to IP3R, RyR has an important role in normal cell function and various neurodegenerative diseases. Since IP3R and RyR interact, it remains unclear as to whether one or both of these receptors are direct targets of isoflurane; however, calcium influx from the extracellular space also has a role in isoflurane cytotoxicity (13). Memantine is a noncompetitive partial antagonist of N-methyl-D-aspartate receptor (NMDAR), which inhibits calcium influx and markedly suppresses isoflurane-induced apoptosis and cell death (24).…”

Section: Discussionmentioning

confidence: 99%

A mutation in β-amyloid precursor protein renders SH-SY5Y cells vulnerable to isoflurane toxicity: The role of inositol 1,4,5-trisphosphate receptors

Liu

Song

Wang

et al. 2016

Molecular Medicine Reports

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Isoflurane is a commonly used inhaled anesthetic, which induces apoptosis of SH-SY5Y cells in a dose- and time-dependent manner; however, the underlying mechanisms remain unknown. The authors of the present study hypothesized that a mutation in β-amyloid precursor protein (APP), which is a gene associated with familial Alzheimer's disease, may render cells vulnerable to isoflurane-induced cytotoxicity via activation of inositol 1,4,5-trisphosphate receptors (IP3R). In the present study, SH-SY5Y cells were transfected with a vector or with mutated APP, and were treated with the equivalent of 1 minimum alveolar concentration (MAC) isoflurane for 8 h. Cell apoptosis rate, alterations to cytosolic calcium concentrations ([Ca2+]c), and protein levels of IP3R were determined following exposure of cells to isoflurane. In addition, the effects of the IP3R antagonist xestospongin C were determined on isoflurane-induced cytotoxicity and calcium release from the endoplasmic reticulum (ER) of mutated APP- and vector-transfected SH-SY5Y cells. Treatment with isoflurane (1 MAC) for 8 h induced a higher degree of cytotoxicity, and a marked increase in [Ca2+]c and IP3R protein levels in mutated APP-transfected SH-SY5Y cells compared with vector-transfected SH-SY5Y cells. Xestospongin C significantly attenuated isoflurane-mediated cytotoxicity and inhibited calcium release from the ER of SH-SY5Y cells. These results indicated that the APP mutation may render SH-SY5Y cells vulnerable to isoflurane neurotoxicity, and the underlying mechanism may be associated with Ca2+ dysregulation via overactivation of IP3R.

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“…It has been previously shown that Mn 2+ crosses the plasma membrane through voltage-gated calcium or nonspecific cationic channels (13,14,16). Consequently, the neuronal depolarization and opening of the ionic channels contribute to intracellular accumulation of Mn…”

Section: Discussionmentioning

confidence: 99%

“…MEMRI uses manganese, an MR contrast agent, to label active neurons. The amount of manganese that accumulates intracellularly is directly linked to neuronal activity, because the Mn 2+ ion enters the neurons through calcium and nonspecific cationic channels (13)(14)(15)(16). MEMRI was also applied to invertebrate animal models to visualize their nervous system and label activity-dependent Mn 2+ uptake (17,18).…”

mentioning

confidence: 99%

Functional magnetic resonance microscopy at single-cell resolution in Aplysia californica

Radecki

Nargeot

Jelescu

et al. 2014

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

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In this work, we show the feasibility of performing functional MRI studies with single-cell resolution. At ultrahigh magnetic field, manganese-enhanced magnetic resonance microscopy allows the identification of most motor neurons in the buccal network of Aplysia at low, nontoxic Mn 2+ concentrations. We establish that Mn 2+ accumulates intracellularly on injection into the living Aplysia and that its concentration increases when the animals are presented with a sensory stimulus. We also show that we can distinguish between neuronal activities elicited by different types of stimuli. This method opens up a new avenue into probing the functional organization and plasticity of neuronal networks involved in goal-directed behaviors with single-cell resolution.neuroimaging | manganese-enhanced MRI O ne of the current goals of neuroscience is to decipher the functional properties of the neuronal networks generating behaviors and their modulations by sensory stimuli. Studies on a variety of animal models have considerably advanced our understanding of the sensory control of automatic behaviors, including motor reflexes and rhythmic behaviors (locomotion and respiration) (1-4). In contrast, much less is known about the neuronal organization and adaptability of networks responsible for goal-directed actions. These complex behaviors, such as feeding or sexual activities, depend on the interaction between internally driven neuronal activity and external sensory inputs. Several macroscopic structures in the central nervous system (CNS) of vertebrates have been found to play a role in the organization of these behaviors (5). However, investigations of the cellular operations in these networks remain difficult because of their high degree of structural complexity.Functional neuroimaging techniques have reached levels of performance that make possible the mapping of neural circuits (6). Among these techniques, MRI has been extensively applied to functional studies of mammalian brains. At present, the highest spatial resolution of such MRI experiments is of the order of (0.3 mm) 3 , averaging the signal from clusters of hundreds of neurons (7). Magnetic resonance (MR) microscopy (MRM) achieves higher resolution (of only a few micrometers) but requires long acquisition times, which prohibit its application to studying individual neurons in mammalian brains (8, 9). In the last decade, a new functional MR technique, manganese-enhanced MRI (MEMRI), has been successfully proven on various vertebrate animal models (10-12). MEMRI uses manganese, an MR contrast agent, to label active neurons. The amount of manganese that accumulates intracellularly is directly linked to neuronal activity, because the Mn 2+ ion enters the neurons through calcium and nonspecific cationic channels (13-16). MEMRI was also applied to invertebrate animal models to visualize their nervous system and label activity-dependent Mn 2+ uptake (17, 18). In a previous study, we showed that MEMRI can be used to track axonal projections and follow changes in Mn 2+ distri...

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Ca2+ entry through a non-selective cation channel in Aplysia bag cell neurons

Cited by 16 publications

References 99 publications

Diacylglycerol‐mediated regulation of Aplysia bag cell neuron excitability requires protein kinase C

Diacylglycerol‐mediated regulation of Aplysia bag cell neuron excitability requires protein kinase C

A mutation in β-amyloid precursor protein renders SH-SY5Y cells vulnerable to isoflurane toxicity: The role of inositol 1,4,5-trisphosphate receptors

Functional magnetic resonance microscopy at single-cell resolution in Aplysia californica

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