Analysis of Puff Dynamics in Oocytes: Interdependence of Puff Amplitude and Interpuff Interval

Overview

Journal Biophys J

Publisher Cell Press

Specialty Biophysics

Date 2006 Mar 15

PMID 16533853

Citations 18

Authors

Daniel Fraiman

Bernardo Pando

Sheila Dargan

Ian Parker

Silvina Ponce Dawson

Affiliations

Soon will be listed here.

Abstract

Puffs are localized Ca(2+) signals that arise in oocytes in response to inositol 1,4,5-trisphosphate (IP(3)). They are analogous to the sparks of myocytes and are believed to be the result of the liberation of Ca(2+) from the endoplasmic reticulum through the coordinated opening of IP(3) receptor/channels clustered at a functional release site. In this article, we analyze sequences of puffs that occur at the same site to help elucidate the mechanisms underlying puff dynamics. In particular, we show a dependence of the interpuff time on the amplitude of the preceding puff, and of the amplitude of the following puff on the preceding interval. These relationships can be accounted for by an inhibitory role of the Ca(2+) that is liberated during puffs. We construct a stochastic model for a cluster of IP(3) receptor/channels that quantitatively replicates the observed behavior, and we determine that the characteristic time for a channel to escape from the inhibitory state is of the order of seconds.

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References

Mak D, McBride S, Foskett J . ATP-dependent adenophostin activation of inositol 1,4,5-trisphosphate receptor channel gating: kinetic implications for the durations of calcium puffs in cells. J Gen Physiol. 2001; 117(4):299-314. PMC: 2217258. DOI: 10.1085/jgp.117.4.299. View

Callamaras N, Parker I . Phasic characteristic of elementary Ca(2+) release sites underlies quantal responses to IP(3). EMBO J. 2000; 19(14):3608-17. PMC: 313983. DOI: 10.1093/emboj/19.14.3608. View

Dargan S, Parker I . Buffer kinetics shape the spatiotemporal patterns of IP3-evoked Ca2+ signals. J Physiol. 2003; 553(Pt 3):775-88. PMC: 2343635. DOI: 10.1113/jphysiol.2003.054247. View

Fraiman D, Ponce Dawson S . A model of IP3 receptor with a luminal calcium binding site: stochastic simulations and analysis. Cell Calcium. 2004; 35(5):403-13. DOI: 10.1016/j.ceca.2003.10.004. View

Thul R, Falcke M . Release currents of IP(3) receptor channel clusters and concentration profiles. Biophys J. 2004; 86(5):2660-73. PMC: 1304139. DOI: 10.1016/S0006-3495(04)74322-2. View

Szentesi P, Pignier C, Egger M, Kranias E, Niggli E . Sarcoplasmic reticulum Ca2+ refilling controls recovery from Ca2+-induced Ca2+ release refractoriness in heart muscle. Circ Res. 2004; 95(8):807-13. DOI: 10.1161/01.RES.0000146029.80463.7d. View

Parker I, Ivorra I . Inhibition by Ca2+ of inositol trisphosphate-mediated Ca2+ liberation: a possible mechanism for oscillatory release of Ca2+. Proc Natl Acad Sci U S A. 1990; 87(1):260-4. PMC: 53242. DOI: 10.1073/pnas.87.1.260. View

Iino M . Biphasic Ca2+ dependence of inositol 1,4,5-trisphosphate-induced Ca release in smooth muscle cells of the guinea pig taenia caeci. J Gen Physiol. 1990; 95(6):1103-22. PMC: 2216357. DOI: 10.1085/jgp.95.6.1103. View

Finch E, Turner T, Goldin S . Calcium as a coagonist of inositol 1,4,5-trisphosphate-induced calcium release. Science. 1991; 252(5004):443-6. DOI: 10.1126/science.2017683. View

10.

Bezprozvanny I, WATRAS J, Ehrlich B . Bell-shaped calcium-response curves of Ins(1,4,5)P3- and calcium-gated channels from endoplasmic reticulum of cerebellum. Nature. 1991; 351(6329):751-4. DOI: 10.1038/351751a0. View

11.

Parker I, Ivorra I . Characteristics of membrane currents evoked by photoreleased inositol trisphosphate in Xenopus oocytes. Am J Physiol. 1992; 263(1 Pt 1):C154-65. DOI: 10.1152/ajpcell.1992.263.1.C154. View

12.

De Young G, Keizer J . A single-pool inositol 1,4,5-trisphosphate-receptor-based model for agonist-stimulated oscillations in Ca2+ concentration. Proc Natl Acad Sci U S A. 1992; 89(20):9895-9. PMC: 50240. DOI: 10.1073/pnas.89.20.9895. View

13.

Bezprozvanny I, Ehrlich B . Inositol (1,4,5)-trisphosphate (InsP3)-gated Ca channels from cerebellum: conduction properties for divalent cations and regulation by intraluminal calcium. J Gen Physiol. 1994; 104(5):821-56. PMC: 2229238. DOI: 10.1085/jgp.104.5.821. View

14.

Yao Y, Choi J, Parker I . Quantal puffs of intracellular Ca2+ evoked by inositol trisphosphate in Xenopus oocytes. J Physiol. 1995; 482 ( Pt 3):533-53. PMC: 1157780. DOI: 10.1113/jphysiol.1995.sp020538. View

15.

Parker I, Callamaras N, Wier W . A high-resolution, confocal laser-scanning microscope and flash photolysis system for physiological studies. Cell Calcium. 1997; 21(6):441-52. DOI: 10.1016/s0143-4160(97)90055-5. View

16.

Huser J, Blatter L . Elementary events of agonist-induced Ca2+ release in vascular endothelial cells. Am J Physiol. 1997; 273(5):C1775-82. DOI: 10.1152/ajpcell.1997.273.5.C1775. View

17.

Sun X, Callamaras N, Marchant J, Parker I . A continuum of InsP3-mediated elementary Ca2+ signalling events in Xenopus oocytes. J Physiol. 1998; 509 ( Pt 1):67-80. PMC: 2230949. DOI: 10.1111/j.1469-7793.1998.067bo.x. View

18.

Fill M, Mignery G . Isoform-specific function of single inositol 1,4,5-trisphosphate receptor channels. Biophys J. 1998; 75(2):834-9. PMC: 1299757. DOI: 10.1016/S0006-3495(98)77572-1. View

19.

Marchant J, Taylor C . Rapid activation and partial inactivation of inositol trisphosphate receptors by inositol trisphosphate. Biochemistry. 1998; 37(33):11524-33. DOI: 10.1021/bi980808k. View

20.

Nguyen T, Chin W, Verdugo P . Role of Ca2+/K+ ion exchange in intracellular storage and release of Ca2+. Nature. 1998; 395(6705):908-12. DOI: 10.1038/27686. View