Activation ofryanodine receptors influences the pair-pulsed depression in cultured rat hippocampalneurons
M.A. Kravchenko, A.O. Moskalyuk, Y.O. Kolodin, N.S. Veselovsky, S.A. Fedulova
International Center for Molecular Physiology, Kiev;A.A. Bogomoletz Institute of Physiology National Academy ofSciences of Ukraine, Kiev.
Abstract
Role of intraterminal calcium stores in modulation of shortterm
plasticity of evoked inhibitory postsynaptic currents
(IPSCs) was studied in synaptically connected cultured hippocampal
neurons using patch-clamp technique in whole-cell
configuration. Currents were induced by voltage stimulation
which were applied externally to presynaptic fiber. Paired
stimuli resulted in paired-pulse depression (n=18) or facilitation
(n=7) of the second IPSC at interpulse intervals 150 and
500 ms. Calcium release from intracellular calcium stores was
activated by local application of caffeine and ryanodine, ryanodine
receptor agonists. One of the characteristics of shortterm
plasticity, the pair-pulsed ratio (ratio of amplitudes of
second IPSC to first IPSC), decreased during addition of ryanodine
(50 nM) from 0.79±0.02 to 0.71±0.04 (n=10). This
change was observed only for cells that demonstrated pairpulsed
depression. We also studied the influence of caffeine
and ryanodine on spontaneous currents. Attenuation of the
mean amplitude to 0.71±0,06 and frequency to 0.42±0.08
(n=7) of spontaneous IPSCs was observed during application
of caffeine (10 mM). Upon ryanodine application the mean
amplitude did not change but frequency of spontaneous events
decreased to 0.74±0.09 (n=12). The amplitudes of currents
evoked by fast local application of g-aminobutyric acid (GABA
100 mM) were diminished in the presence of caffeine (10 mM)
to 0.59±0.03 (n=5) and in the presence of ryanodine (50 nM)
to 0.56±0.11 (n=7). Thus we conclude that endoplasmic
reticular calcium stores are able to modulate synaptic transmission
from both presynaptic (in assumption that short
term plasticity and spontaneous activity are believed to have
presynaptic nature) and postsynaptic (since GABA-receptors
are situated on postsynaptic cell) sides.
References
- Andreasen M., Hablitz J. J. Paired-pulse facilitation in the dentate gyrus: a patch–clamp study in rat hip- pocampus in vitro / / J.Neurophysiol. – 1994. – 72. – P.326–336.
- Berridge M. J. Neuronal calcium signaling / / Neuron. – 1998. – 21. – P.13–26.
- Collingridge G. L., Gage P. W., Robertson, B. Inhibito- ry post-synaptic currents in rat hippocampal CA1 neurones / / J.Physiol. – 1984. – 356. – P.551–564.
- De Koninck Y., Mody I. Noise analysis of miniature IPSCs in adult rat brain slices: properties and modulation of synaptic GABAA receptor channels / / J.Neurophysiol. – 1994. – 71. – P.1318–1335.
- Debanne D., Guerineau N. C., Gahwiler B. H., Th- ompson, S. M. Paired-pulse facilitation and depres- sion at unitary synapses in rat hippocampus: quantal fluctuation affects subsequent release / / J.Physiol. – 1996. – 491. – P.163–176.
- Dittman J. S., Kreitzer A. C., Regehr, W. G. Interplay between facilitation, depression, and residual calcium at three presynaptic terminals / / J.Neurosci. – 2000.– 20. – P.1374–1385.
- Emptage N. J., Reid C. A., Fine, A. Calcium stores in hippocampal synaptic boutons mediate short–term plas- ticity, store-operated Ca2+ entry, and spontaneous trans- mitter release / / Neuron. – 2001. – 29. – P.197–208.
- Galante M., Marty, A. Presynaptic ryanodine–sensi- tive calcium stores contribute to evoked neurotrans- mitter release at the basket cell-Purkinje cell synapse / / J.Neurosci. – 2003. – 23. – P.11229–11234.
- 9. Garaschuk O., Yaari Y., Konnerth A. Release and sequestration of calcium by ryanodine-sensitive stores in rat hippocampal neurones / / J.Physiol.–1997. – 502. – P.13–30.
- 10. Gomez T. M., Snow D. M., Letourneau P. C. Characterization of spontaneous calcium transients in nerve growth cones and their effect on growth cone migration / / Neuron. – 1995 – 14. – P.1233–1246.
- Grabauskas G., Bradley R. M. Tetanic stimulation induces short-term potentiation of inhibitory synap- tic activity in the rostral nucleus of the solitary tract / / J.Neurophysiol. – 1998. – 79. – P.595–604.
- Jensen K., Lambert J. D., Jensen M. S. Activity- dependent depression of GABAergic IPSCs in cultured hippocampal neurons / / J.Neurophysiol. – 1999. – 82. – P.42–49.
- Jones M. V., Westbrook G. L. The impact of receptor desensitization on fast synaptic transmission / / Trends Neurosci. – 1996. – 19. – P.96–101.
- Kano M., Garaschuk O., Verkhratsky A., Konnerth A. Ryanodine receptor-mediated intracellular calcium release in rat cerebellar Purkinje neurones / / J.Physiol. – 1995. – 487. – P.1–16.
- Katz B., Miledi, R. The timing of calcium action during neuromuscular transmission / / J.Physiol. – 1967. – 189. – P.535–544.
- Korkotian E., Segal M. Fast confocal imaging of calcium released from stores in dendritic spines / / Eur. J.Neurosci. – 1998. – 10. – P.2076–2084.
- Lacaille J. C., Schwartzkroin P. A. Intracellular responses of rat hippocampal granule cells in vitro to discrete applications of norepinephrine / / Neuro- sci.Lett. – 1988. – 89. – P.176–181.
- Lin Y. Q., Brain K. L., Bennett M. R. Calcium in sympathetic boutons of rat superior cervical ganglion during facilitation, augmentation and potentiation / / J.Auton.Nerv.Syst. – 1998. – 73. – P.26–37.
- 19. Llano I., Gonzalez J., Caputo C., Lai F. A., Blayney L. M., Tan Y. P., Marty A. Presynaptic calcium stores underlie large-amplitude miniature IPSCs and sponta- neous calcium transients / / Nat.Neurosci. – 2000. – 3. – P.1256–1265.
- 20. McBain C. J., DiChiara T. J., Kauer J. A. Activation of metabotropic glutamate receptors differentially af- fects two classes of hippocampal interneurons and potentiates excitatory synaptic transmission / / J.Neurosci. – 1994. – 14. – P.4433–4445.
- Meissner G. Ryanodine activation and inhibition of the Ca2+ release channel of sarcoplasmic reticulum / / J.Biol.Chem. – 1986. – 261. – P.6300–6306.
- Mennerick S., Zorumski C. F. Paired-pulse modula- tion of fast excitatory synaptic currents in microcul- tures of rat hippocampal neurons / / J.Physiol.–1995. – 488. – P.85–101.
- Neher E. Vesicle pools and Ca2+ microdomains: new tools for understanding their roles in neurotransmitter release / / Neuron. – 1998. – 20. – P.389–399.
- Ogawa Y. Role of ryanodine receptors / / Crit Rev.Biochem.Mol.Biol. – 1994. – 29. – P.229–274.
- Otis T. S., Mody I. Differential activation of GABAA and GABAB receptors by spontaneously released transmitter / / J.Neurophysiol. – 1992. – 67. – P.227–235.
- Poncer J. C., McKinney R. A., Gahwiler B. H., Th- ompson S. M. Differential control of GABA release at synapses from distinct interneurons in rat hippocam- pus / / J.Physiol. – 2000. – 528. – P.123–130.
- Rosato-Siri M., Grandolfo M., Ballerini, L. Activity- dependent modulation of GABAergic synapses in developing rat spinal networks in vitro / / Eur.J. Neurosci. – 2002. – 16. – P.2123–2135.
- Savic N., Sciancalepore M. Intracellular calcium stores modulate miniature GABA-mediated synaptic currents in neonatal rat hippocampal neurons / / Eur.J.Neurosci. – 1998. – 10. – P.3379–3386.
- 29. Seymour-Laurent K. J., Barish M. E. Inositol 1,4,5- trisphosphate and ryanodine receptor distributions and patterns of acetylcholine- and caffeine-induced calcium release in cultured mouse hippocampal neurons / /J.Neurosci. – 1995. – 15. – P.2592–2608.
- 30. Shmigol A., Verkhratsky, A., Isenberg G. Calcium- induced calcium release in rat sensory neurons / / J.Physiol. – 1995. – 489. – P.627–636.
- Storozhuk M. V., Ivanova S. Y., Pivneva T. A., Melnick I. V., Skibo G. G., Belan P. V., Kostyuk P. G. Post- tetanic depression of GABAergic synaptic transmis- sion in rat hippocampal cell cultures / / Neurosci.Lett. – 2002. – 323. – P.5–8.
- Swandulla D., Hans M., Zipser K., Augustine G. J. Role of residual calcium in synaptic depression and posttetanic potentiation: fast and slow calcium signaling in nerve terminals / / Neuron. – 1991. – 7. – P.915–926.
- Usachev Y., Shmigol A., Pronchuk N., Kostyuk P., Verkhratsky A. Caffeine-induced calcium release from internal stores in cultured rat sensory neurons / / Neu- roscience. – 1993. – 57. – P.845–859.
- Verkhratsky A. J., Petersen O. H. Neuronal calcium stores / / Cell Calcium. – 1998. – 24. – P.333–343.
- Veselovsky N. S., Engert F., Lux H. D. Fast local superfusion technique / / Pflugers Arch. – 1996. – 432. – P.351–354.
- Zengel J. E., Magleby K. L., Horn J. P., McAfee D. A., Yarowsky P. J. Facilitation, augmentation, and potentiation of synaptic transmission at the superior cervical ganglion of the rabbit / / J.Gen.Physiol. – 1980. – 76. – P.213–231.
- Zucker R. S. Short-term synaptic plasticity / / Annu.Rev.Neurosci. – 1989.–31. – P.13–31.
- Zucker R. S. Calcium- and activity-dependent synap- tic plasticity / / Curr.Opin.Neurobiol. – 1999. – 9. – P.305–313.
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