Transient Loss of Voltage Control of Ca2+ Release in the Presence of Maurocalcine in Skeletal Muscle

Overview

Journal Biophys J

Publisher Cell Press

Specialty Biophysics

Date 2006 Jun 20

PMID 16782801

Citations 20

Authors

Sandrine Pouvreau

Laszlo Csernoch

Bruno Allard

Jean Marc Sabatier

Michel De Waard

Michel Ronjat

Vincent Jacquemond

Affiliations

Soon will be listed here.

Abstract

In skeletal muscle, sarcoplasmic reticulum (SR) calcium release is controlled by the plasma membrane voltage through interactions between the voltage-sensing dihydropyridine receptor (DHPr) and the ryanodine receptor (RYr) calcium release channel. Maurocalcine (MCa), a scorpion toxin peptide presenting some homology with a segment of a cytoplasmic loop of the DHPr, has been previously shown to strongly affect the activity of the isolated RYr. We injected MCa into mouse skeletal muscle fibers and measured intracellular calcium under voltage-clamp conditions. Voltage-activated calcium transients exhibited similar properties in control and in MCa-injected fibers during the depolarizing pulses, and the voltage dependence of calcium release was similar under the two conditions. However, MCa was responsible for a pronounced sustained phase of Ca(2+) elevation that proceeded for seconds following membrane repolarization, with no concurrent alteration of the membrane current. The magnitude of the underlying uncontrolled extra phase of Ca(2+) release correlated well with the peak calcium release during the pulse. Results suggest that MCa binds to RYr that open on membrane depolarization and that this interaction specifically alters the process of repolarization-induced closure of the channels.

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References

Baylor S, Chandler W, Marshall M . Sarcoplasmic reticulum calcium release in frog skeletal muscle fibres estimated from Arsenazo III calcium transients. J Physiol. 1983; 344:625-66. PMC: 1193860. DOI: 10.1113/jphysiol.1983.sp014959. View

Ahern C, Bhattacharya D, Mortenson L, Coronado R . A component of excitation-contraction coupling triggered in the absence of the T671-L690 and L720-Q765 regions of the II-III loop of the dihydropyridine receptor alpha(1s) pore subunit. Biophys J. 2001; 81(6):3294-307. PMC: 1301787. DOI: 10.1016/S0006-3495(01)75963-2. View

Jacquemond V, Schneider M . Low myoplasmic Mg2+ potentiates calcium release during depolarization of frog skeletal muscle fibers. J Gen Physiol. 1992; 100(1):137-54. PMC: 2229125. DOI: 10.1085/jgp.100.1.137. View

Lu X, Xu L, Meissner G . Activation of the skeletal muscle calcium release channel by a cytoplasmic loop of the dihydropyridine receptor. J Biol Chem. 1994; 269(9):6511-6. View

Antoniu B, Wang J, Hamilton S, Ikemoto N . Identification of calcium release-triggering and blocking regions of the II-III loop of the skeletal muscle dihydropyridine receptor. J Biol Chem. 1995; 270(38):22116-8. DOI: 10.1074/jbc.270.38.22116. View

Lokuta A, Arevalo C, Valdivia H . Peptide probe of ryanodine receptor function. Imperatoxin A, a peptide from the venom of the scorpion Pandinus imperator, selectively activates skeletal-type ryanodine receptor isoforms. J Biol Chem. 1995; 270(48):28696-704. DOI: 10.1074/jbc.270.48.28696. View

Jacquemond V . Indo-1 fluorescence signals elicited by membrane depolarization in enzymatically isolated mouse skeletal muscle fibers. Biophys J. 1997; 73(2):920-8. PMC: 1180988. DOI: 10.1016/S0006-3495(97)78124-4. View

Timmer J, Muller T, Melzer W . Numerical methods to determine calcium release flux from calcium transients in muscle cells. Biophys J. 1998; 74(4):1694-707. PMC: 1299515. DOI: 10.1016/S0006-3495(98)77881-6. View

Tripathy A, Resch W, Xu L, Valdivia H, Meissner G . Imperatoxin A induces subconductance states in Ca2+ release channels (ryanodine receptors) of cardiac and skeletal muscle. J Gen Physiol. 1998; 111(5):679-90. PMC: 2217137. DOI: 10.1085/jgp.111.5.679. View

10.

Csernoch L, Bernengo J, Szentesi P, Jacquemond V . Measurements of intracellular Mg2+ concentration in mouse skeletal muscle fibers with the fluorescent indicator mag-indo-1. Biophys J. 1998; 75(2):957-67. PMC: 1299769. DOI: 10.1016/S0006-3495(98)77584-8. View

11.

Nakai J, Tanabe T, Konno T, Adams B, Beam K . Localization in the II-III loop of the dihydropyridine receptor of a sequence critical for excitation-contraction coupling. J Biol Chem. 1998; 273(39):24983-6. DOI: 10.1074/jbc.273.39.24983. View

12.

Gurrola G, Arevalo C, Sreekumar R, Lokuta A, Walker J, Valdivia H . Activation of ryanodine receptors by imperatoxin A and a peptide segment of the II-III loop of the dihydropyridine receptor. J Biol Chem. 1999; 274(12):7879-86. DOI: 10.1074/jbc.274.12.7879. View

13.

Dulhunty A, Laver D, Gallant E, Casarotto M, Pace S, Curtis S . Activation and inhibition of skeletal RyR channels by a part of the skeletal DHPR II-III loop: effects of DHPR Ser687 and FKBP12. Biophys J. 1999; 77(1):189-203. PMC: 1300321. DOI: 10.1016/S0006-3495(99)76881-5. View

14.

Collet C, Allard B, Tourneur Y, Jacquemond V . Intracellular calcium signals measured with indo-1 in isolated skeletal muscle fibres from control and mdx mice. J Physiol. 1999; 520 Pt 2:417-29. PMC: 2269592. DOI: 10.1111/j.1469-7793.1999.00417.x. View

15.

Pouvreau S, Allard B, Berthier C, Jacquemond V . Control of intracellular calcium in the presence of nitric oxide donors in isolated skeletal muscle fibres from mouse. J Physiol. 2004; 560(Pt 3):779-94. PMC: 1665293. DOI: 10.1113/jphysiol.2004.072397. View

16.

Altafaj X, Cheng W, Esteve E, Urbani J, Grunwald D, Sabatier J . Maurocalcine and domain A of the II-III loop of the dihydropyridine receptor Cav 1.1 subunit share common binding sites on the skeletal ryanodine receptor. J Biol Chem. 2004; 280(6):4013-6. PMC: 2712624. DOI: 10.1074/jbc.C400433200. View

17.

Szappanos H, Smida-Rezgui S, Cseri J, Simut C, Sabatier J, De Waard M . Differential effects of maurocalcine on Ca2+ release events and depolarization-induced Ca2+ release in rat skeletal muscle. J Physiol. 2005; 565(Pt 3):843-53. PMC: 1464547. DOI: 10.1113/jphysiol.2005.086074. View

18.

Fajloun Z, Kharrat R, Chen L, Lecomte C, Di Luccio E, Bichet D . Chemical synthesis and characterization of maurocalcine, a scorpion toxin that activates Ca(2+) release channel/ryanodine receptors. FEBS Lett. 2000; 469(2-3):179-85. DOI: 10.1016/s0014-5793(00)01239-4. View

19.

OReilly F, Robert M, Jona I, Szegedi C, Albrieux M, Geib S . FKBP12 modulation of the binding of the skeletal ryanodine receptor onto the II-III loop of the dihydropyridine receptor. Biophys J. 2001; 82(1 Pt 1):145-55. PMC: 1302456. DOI: 10.1016/S0006-3495(02)75381-2. View

20.

Collet C, Jacquemond V . Sustained release of calcium elicited by membrane depolarization in ryanodine-injected mouse skeletal muscle fibers. Biophys J. 2002; 82(3):1509-23. PMC: 1301951. DOI: 10.1016/S0006-3495(02)75504-5. View