Regional distribution of calcium elevation during sensory transduction in spider mechanoreceptor neurons

Höger, Ulli; Meisner, Shannon; Torkkeli, Päivi H.; French, Andrew S.

doi:10.1016/j.neures.2008.09.006

Cited by 4 publications

(3 citation statements)

References 34 publications

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“…Nevertheless, the bulk of [Ca 2+ ] i is cleared by the Ca 2+ ATP-dependent pumps found in both the plasma membrane (PMCA) and the endoplasmic reticulum (SERCA) [9]. A typical calcium influx results in a rather small elevation in [Ca 2+ ] i, rarely exceeding 1 μM [10,11] (excluding cellular microdomains), which is more effectively cleared by the high-affinity calcium pumps such as PMCA and SERCA. Accordingly, an efficient removal of [Ca 2+ ] i requires an adequate input of ATP to power those pumps.…”

Section: Introductionmentioning

confidence: 99%

Calcium clearance and its energy requirements in cerebellar neurons

2010

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Quick cytosolic calcium clearance is essential for the effective modulation of various cellular functions. An excess of cytosolic calcium after influx is largely removed via ATP-dependent mechanisms located in the plasma membrane and the endoplasmic reticulum. Therefore, calcium clearance depends critically on the adequate supply of ATP, which may come from either glycolysis or mitochondria, or both. However, it presently remains unknown the degree to which individual ATP generating pathways -glycolysis and mitochondria power ATP-dependent calcium as well as other vital ion clearance mechanisms in neurons. In this study, we explored the relationship between the energy generating pathways and ion clearance mechanisms in neurons by characterizing the effects of glycolytic and mitochondrial inhibitors of ATP synthesis on calcium clearance kinetics in the soma, dendrites and spines. Stimulation of cultured cerebellar granule cells by brief pulses of 60 mM potassium ACSF, and electrical stimulation of purkinje cells in acutely prepared slices led to a transient calcium influx, whose clearance was largely mediated by the plasma membrane Ca 2+ -ATPase pump. Inhibition of glycolysis by deoxyglucose or iodoacetic acid resulted in a marked slowing in calcium clearance in the soma, dendrites, and spines with the spines affected the most. However, inhibition of the mitochondrial citric acid cycle with fluoroacetate and arsenite, or mitochondrial ATP-synthase with oligomycin did not produce any immediate effects on calcium clearance kinetics in any of those neuronal regions. Although cytosolic calcium clearance was not affected by the inhibition of mitochondria, the magnitude of the calcium clearance delay induced by glycolytic inhibitors in different neuronal compartments was related to their mitochondrial density. Conversely, the endoplasmic reticulum Ca 2+ -ATPase pump activity is fuelled by both glycolytic and mitochondrial ATP, as evidenced by a minimal change in the endoplasmic reticulum calcium contents in cells treated with either deoxyglucose supplemented with lactate or arsenite. Taken together, these data suggest that calcium clearance in cerebellar granule and purkinje cells relies on the plasma membrane Ca 2+ -ATPase, and is powered by glycolysis.

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Section: Introductionmentioning

confidence: 99%

Calcium clearance and its energy requirements in cerebellar neurons

2010

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“…AP firing in VS‐3 neurons increases intracellular [Ca 2+ ] in all cell regions via voltage‐activated calcium channels in the cell membrane (Höger et al. , 2007, 2008).…”

Section: Resultsmentioning

confidence: 99%

“…Receptor potential of sufficient amplitude produces APs whose rising phase is driven by voltage‐activated sodium channels. Voltage‐activated calcium channels are opened by AP depolarization, but not by smaller receptor potentials (Höger et al. , 2005, 2008), raising intracellular [Ca 2+ ], which reduces receptor current and receptor potential, completing a negative feedback loop.…”

Section: Discussionmentioning

confidence: 99%

Feedback modulation of transduction by calcium in a spider mechanoreceptor

Höger

Torkkeli

French

2010

Eur J of Neuroscience

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Calcium ions play important roles in the adaptation of auditory hair cells, and there is evidence that they are involved in modifying the sensitivity and adaptation of a variety of vertebrate and invertebrate mechanoreceptors. However, there is little direct evidence concerning the concentration changes, signaling pathways or ultimate effects of these proposed modulatory mechanisms. We measured receptor potential, receptor current and action potentials intracellularly during mechanotransduction in a group of sensory neurons of the spider Cupiennius salei, which possesses low-voltage-activated calcium channels. Simultaneously, we elevated intracellular [Ca(2+) ] by UV light release from cage molecules, and observed increases in [Ca(2+) ] as changes in calcium-sensitive dye fluorescence. Increases of 10-15% in [Ca(2+) ] caused reductions of approximately 40% in receptor potential and approximately 20% in receptor current. Mechanically evoked action potential firing caused much larger increases in [Ca(2+) ], and the firing rate fell as [Ca(2+) ] rose during mechanical stimulation. Release of caged calcium just before mechanical stimulation significantly reduced peak firing. Dose-response measurements suggested that the binding of one or two intracellular calcium ions per channel reduces the probability of the mechanotransduction channel being open. Our data indicate that calcium regulates sensitivity in these mechanoreceptor neurons by negative feedback from action potentials onto transduction channels.

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Calcium buffering and clearance in spider mechanosensory neurons

et al. 2012

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Spider VS-3 mechanoreceptor neurons have a low-voltage-activated Ca2+ current that raises intracellular calcium concentration [Ca2+] when they are depolarized by agonists of GABAA receptors or fire action potentials. The Ca2+ rise produces negative feedback by modulating the mechanoreceptor current and regulates Ca2+- and voltage-activated K+ currents. However, nothing is known about Ca2+ buffering in VS-3 neurons. Dynamic changes in VS-3 neuron intracellular [Ca2+] were measured using the fluorescent Ca2+ indicator Oregon Green BAPTA-1 (OG488) to understand Ca2+ buffering and clearance. Intracellular OG488 concentration increased slowly over more than 2 h as it diffused through a sharp intracellular microelectrode and spread through the cell. This slow increase was used to measure endogenous Ca2+ buffering and clearance by the added buffer technique, with OG488 acting as both added exogenous buffer and Ca2+ indicator. [Ca2+] was raised for brief periods by regular action potential firing, produced by pulsed electric current injection through the microelectrode. The resulting rise and fall of [Ca2+] were well fitted by the single compartment model of Ca2+ dynamics. With earlier ratiometric [Ca2+] estimates, these data gave an endogenous Ca2+ binding ratio of 684. Strong Ca2+ buffering may assist these neurons to deal with rapid changes in mechanical inputs.

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Regional distribution of calcium elevation during sensory transduction in spider mechanoreceptor neurons

Cited by 4 publications

References 34 publications

Calcium clearance and its energy requirements in cerebellar neurons

Calcium clearance and its energy requirements in cerebellar neurons

Feedback modulation of transduction by calcium in a spider mechanoreceptor

Calcium buffering and clearance in spider mechanosensory neurons

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