Abstract
Aim:
Ca2+ release from the endoplasmic reticulum (ER) is an integral component of neuronal Ca2+ signaling. The present study is to investigate properties of local Ca2+ release events in superior cervical ganglion (SCG) neurons.
Methods:
Primary cultured SCG neurons were prepared from neonatal rats (P3-P7). Low concentration of caffeine was used to induce Ca2+ release from the ER Ca2+ store, and intracellular Ca2+was recorded by high-resolution line scan confocal imaging and the Ca2+ indicator Fluo-4.
Results:
Two populations of local Ca2+ release events with distinct temporal characteristics were evoked by 1.5 mmol/L caffeine near the surface membrane in the soma and the neurites of SCG neurons. Brief events similar to classic Ca2+ sparks lasted a few hundreds of milliseconds, whereas long-lasting events displayed duration up to tens of seconds. Typical somatic and neurite sparks were of 0.3- and 0.52-fold increase in local Fluo-4 fluorescence, respectively. Typical Ca2+ glows were brighter (ΔF/F0 approximately 0.6), but were highly confined in space. The half maximum of full duration of neurite sparks was much longer than those in the soma (685 vs 381 ms).
Conclusion:
Co-existence of Ca2+ sparks and Ca2+ glows in SCG neurons indicates distinctive local regulation of Ca2+ release kinetics. The local Ca2+ signals of variable, site-specific temporal length may bear important implications in encoding a “memory” of the trigger signal.
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References
Berridge MJ . Neuronal calcium signaling. Neuron 1998; 21: 13–26.
Cheng H, Lederer WJ, Cannell MB . Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle. Science 1993; 262: 740–4.
Klein MG, Cheng H, Santana LF, Jiang YH, Lederer WJ, Schneider MF . Two mechanisms of quantized calcium release in skeletal muscle. Nature 1996; 379: 455–8.
Nelson MT, Cheng H, Rubart M, Santana LF, Bonev AD, Knot HJ, et al. Relaxation of arterial smooth muscle by calcium sparks. Science 1995; 270: 633–7.
Tsugorka A, Rios E, Blatter LA . Imaging elementary events of calcium release in skeletal muscle cells. Science 1995; 269: 1723–6.
Koizumi S, Bootman MD, Bobanovic LK, Schell MJ, Berridge MJ, Lipp P . Characterization of elementary Ca2+ release signals in NGF-differentiated PC 12 cells and hippocampal neurons. Neuron 1999; 22: 125–37.
Ouyang K, Zheng H, Qin X, Zhang C, Yang D, Wang X, et al. Ca2+ sparks and secretion in dorsal root ganglion neurons. Proc NatlAcad Sci USA 2005; 102: 12259–64.
De Crescenzo V, Zhu Ge R, Velazquez-Marrero C, Lifshitz LM, Custer E, Carmichael J, et al. Ca2+ syntillas, miniature Ca2+ release events in terminals of hypothalamic neurons, are increased in frequency by depolarization in the absence of Ca2+ influx. J Neurosci 2004; 24: 1226–35.
Alkadhi KA, Alzoubi KH, Aleisa AM . Plasticity of synaptic transmission in autonomic ganglia. Prog Neurobiol 2005; 75: 83–108.
Zhou Z, Misler S . Amperometric detection of stimulus-induced quantal release of catecholamines from cultured superior cervical ganglion neurons. Proc Natl Acad Sci USA 1995; 92: 6938–42.
Wu B, Wang YM, Xiong W, Zheng LH, Fu CL, Bruce IC, et al. Optimization of a multi-channel puffer system for rapid delivery of solutions during patch-clamp experiments. Front Biosci 2005; 10: 761–7.
Verkhratsky A . Physiology and pathophysiology of the calcium store in the endoplasmic reticulum of neurons. Physiol Rev 2005; 85: 201–79.
Ouyang K, Wu C, Cheng H . Ca2+-induced Ca2+ release in sensory neurons: low gain amplification confers intrinsic stability. J Biol Chem 2005; 280: 15898–902.
Burdyga T, Wray S . Action potential refractory period in ureter smooth muscle is set by Ca sparks and BK channels. Nature 2005; 436: 559–62.
Vinogradova TM, Lyashkov AE, Zhu W, Ruknudin AM, Sirenko S, Yang D, et al. High basal protein kinase A-dependent phosphorylation drives rhythmic internal Ca2+ store oscillations and spontaneous beating of cardiac pacemaker cells. Circ Res 2006; 98: 505–14.
Deisseroth K, Heist EK, Tsien RW . Translocation of calmodulin to the nucleus supports CREB phosphorylation in hippocampal neurons. Nature 1998; 392: 198–202.
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This work was supported by grants from the National Basic Research Program of China (ZZ and HC) and the National Natural Science Foundation of China (ZZ, HC, JL, XHW).
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Yao, Lj., Wang, G., Ou-yang, Kf. et al. Ca2+ sparks and Ca2+ glows in superior cervical ganglion neurons. Acta Pharmacol Sin 27, 848–852 (2006). https://doi.org/10.1111/j.1745-7254.2006.00402.x
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DOI: https://doi.org/10.1111/j.1745-7254.2006.00402.x
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