Modeling buffered Ca2+ diffusion near the membrane: implications for secretion in neuroendocrine cells - PubMed (original) (raw)
Modeling buffered Ca2+ diffusion near the membrane: implications for secretion in neuroendocrine cells
J Klingauf et al. Biophys J. 1997 Feb.
Abstract
Secretion of catecholamines from neuroendocrine cells is relatively slow and it is likely that redistribution and buffering of Ca2+ is a major factor for delaying the response after a stimulus. In fact, in a recent study (Chow, R. H., J. Klingauf, and E. Neher. 1994. Time course of Ca2+ concentration triggering exocytosis in neuroendocrine cells. Proc. Natl. Acad. Sci. U.S.A. 91:12765-12769) Chow et al. concluded that the concentration of free calcium ([Ca2+]i) at a release site peaks at < 10 microM during short-step depolarizations, and then decays to baseline over tens of milliseconds. To check whether such a time course is consistent with diffusion theory, we modeled buffered diffusion in the vicinity of a Ca2+ channel pore. Peak [Ca2+]i and the slow decay were well simulated when release-ready granules were randomly distributed within a regular grid of Ca2+ channels with mean interchannel distances of 300-600 nm. For such large spacings, however, the initial rise in [Ca2+]i was underestimated, suggesting that a small fraction of the release-ready pool (approximately 10%) experiences much higher [Ca2+]i, and thus might be colocalized with Ca2+ channels. A model that accommodates these findings then correctly predicts many recent observations, including the result that single action potentials evoke near-synchronous transmitter release with low quantal yield, whereas trains of action potentials lead to desynchronized release, but with severalfold increased quantal yield. The simulations emphasize the role of Ca2+ not only in triggering, but also in modulating the secretory response: buffers are locally depleted by residual Ca2+ of a preceding stimulus, so that a second pulse leads to a larger peak [Ca2+]i at the fusion sites.
Similar articles
- Time course of Ca2+ concentration triggering exocytosis in neuroendocrine cells.
Chow RH, Klingauf J, Neher E. Chow RH, et al. Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12765-9. doi: 10.1073/pnas.91.26.12765. Proc Natl Acad Sci U S A. 1994. PMID: 7809118 Free PMC article. - Voltage inactivation of Ca2+ entry and secretion associated with N- and P/Q-type but not L-type Ca2+ channels of bovine chromaffin cells.
Villarroya M, Olivares R, Ruíz A, Cano-Abad MF, de Pascual R, Lomax RB, López MG, Mayorgas I, Gandía L, García AG. Villarroya M, et al. J Physiol. 1999 Apr 15;516 ( Pt 2)(Pt 2):421-32. doi: 10.1111/j.1469-7793.1999.0421v.x. J Physiol. 1999. PMID: 10087342 Free PMC article. - Short-term changes in the Ca2+-exocytosis relationship during repetitive pulse protocols in bovine adrenal chromaffin cells.
Engisch KL, Chernevskaya NI, Nowycky MC. Engisch KL, et al. J Neurosci. 1997 Dec 1;17(23):9010-25. doi: 10.1523/JNEUROSCI.17-23-09010.1997. J Neurosci. 1997. PMID: 9364048 Free PMC article. - Calcium signaling and exocytosis in adrenal chromaffin cells.
García AG, García-De-Diego AM, Gandía L, Borges R, García-Sancho J. García AG, et al. Physiol Rev. 2006 Oct;86(4):1093-131. doi: 10.1152/physrev.00039.2005. Physiol Rev. 2006. PMID: 17015485 Review. - Regulation of exocytosis in neuroendocrine cells: spatial organization of channels and vesicles, stimulus-secretion coupling, calcium buffers and modulation.
Kits KS, Mansvelder HD. Kits KS, et al. Brain Res Brain Res Rev. 2000 Aug;33(1):78-94. doi: 10.1016/s0165-0173(00)00023-0. Brain Res Brain Res Rev. 2000. PMID: 10967354 Review.
Cited by
- From calcium blips to calcium puffs: theoretical analysis of the requirements for interchannel communication.
Swillens S, Dupont G, Combettes L, Champeil P. Swillens S, et al. Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):13750-5. doi: 10.1073/pnas.96.24.13750. Proc Natl Acad Sci U S A. 1999. PMID: 10570144 Free PMC article. - Two Forms of Synaptic Depression Produced by Differential Neuromodulation of Presynaptic Calcium Channels.
Burke KJ Jr, Keeshen CM, Bender KJ. Burke KJ Jr, et al. Neuron. 2018 Sep 5;99(5):969-984.e7. doi: 10.1016/j.neuron.2018.07.030. Epub 2018 Aug 16. Neuron. 2018. PMID: 30122380 Free PMC article. - The probability of quantal secretion near a single calcium channel of an active zone.
Bennett MR, Farnell L, Gibson WG. Bennett MR, et al. Biophys J. 2000 May;78(5):2201-21. doi: 10.1016/S0006-3495(00)76769-5. Biophys J. 2000. PMID: 10777721 Free PMC article. - α3β4 Acetylcholine Nicotinic Receptors Are Components of the Secretory Machinery Clusters in Chromaffin Cells.
Villanueva J, Criado M, Giménez-Molina Y, González-Vélez V, Gil A, Gutiérrez LM. Villanueva J, et al. Int J Mol Sci. 2022 Aug 14;23(16):9101. doi: 10.3390/ijms23169101. Int J Mol Sci. 2022. PMID: 36012367 Free PMC article. - Calcium current inactivation rather than pool depletion explains reduced exocytotic rate with prolonged stimulation in insulin-secreting INS-1 832/13 cells.
Pedersen MG, Salunkhe VA, Svedin E, Edlund A, Eliasson L. Pedersen MG, et al. PLoS One. 2014 Aug 8;9(8):e103874. doi: 10.1371/journal.pone.0103874. eCollection 2014. PLoS One. 2014. PMID: 25105407 Free PMC article.
References
- Biophys J. 1985 Sep;48(3):485-98 - PubMed
- Neuron. 1996 Feb;16(2):369-76 - PubMed
- Biophys J. 1985 Dec;48(6):1003-17 - PubMed
- FEBS Lett. 1986 Dec 1;209(1):1-8 - PubMed
- FEBS Lett. 1987 May 25;216(1):35-9 - PubMed
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Miscellaneous