Charged Surface Area of Maurocalcine Determines Its Interaction with the Skeletal Ryanodine Receptor

Overview

Journal Biophys J

Publisher Cell Press

Specialty Biophysics

Date 2008 Jul 16

PMID 18621823

Citations 18

Authors

Balazs Lukacs

Monika Sztretye

Janos Almassy

Sandor Sarkozi

Beatrix Dienes

Kamel Mabrouk

Cecilia Simut

Laszlo Szabo

Peter Szentesi

Michel De Waard

Michel Ronjat

Istvan Jona

Laszlo Csernoch

Affiliations

Soon will be listed here.

Abstract

The 33 amino acid scorpion toxin maurocalcine (MCa) has been shown to modify the gating of the skeletal-type ryanodine receptor (RyR1). Here we explored the effects of MCa and its mutants ([Ala(8)]MCa, [Ala(19)]MCa, [Ala(20)]MCa, [Ala(22)]MCa, [Ala(23)]MCa, and [Ala(24)]MCa) on RyR1 incorporated into artificial lipid bilayers and on elementary calcium release events (ECRE) in rat and frog skeletal muscle fibers. The peptides induced long-lasting subconductance states (LLSS) on RyR1 that lasted for several seconds. However, their average length and frequency were decreased if the mutation was placed farther away in the 3D structure from the critical (24)Arg residue. The effect was strongly dependent on the direction of the current through the channel. If the direction was similar to that followed by calcium during release, the peptides were 8- to 10-fold less effective. In fibers long-lasting calcium release events were observed after the addition of the peptides. The average length of these events correlated well with the duration of LLSS. These data suggest that the effect of the peptide is governed by the large charged surface formed by residues Lys(20), Lys(22), Arg(23), Arg(24), and Lys(8). Our observations also indicate that the results from bilayer experiments mimic the in situ effects of MCa on RyR1.

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References

Szentesi P, Jacquemond V, Kovacs L, Csernoch L . Intramembrane charge movement and sarcoplasmic calcium release in enzymatically isolated mammalian skeletal muscle fibres. J Physiol. 1998; 505 ( Pt 2):371-84. PMC: 1160071. DOI: 10.1111/j.1469-7793.1997.371bb.x. View

Chen L, Esteve E, Sabatier J, Ronjat M, De Waard M, Allen P . Maurocalcine and peptide A stabilize distinct subconductance states of ryanodine receptor type 1, revealing a proportional gating mechanism. J Biol Chem. 2003; 278(18):16095-106. DOI: 10.1074/jbc.M209501200. View

Klein M, Cheng H, Santana L, Jiang Y, Lederer W, Schneider M . Two mechanisms of quantized calcium release in skeletal muscle. Nature. 1996; 379(6564):455-8. DOI: 10.1038/379455a0. View

Meissner G . Ryanodine as a functional probe of the skeletal muscle sarcoplasmic reticulum Ca2+ release channel. Mol Cell Biochem. 1992; 114(1-2):119-23. DOI: 10.1007/BF00240306. View

Esteve E, Smida-Rezgui S, Sarkozi S, Szegedi C, Regaya I, Chen L . Critical amino acid residues determine the binding affinity and the Ca2+ release efficacy of maurocalcine in skeletal muscle cells. J Biol Chem. 2003; 278(39):37822-31. DOI: 10.1074/jbc.M305798200. View

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

Pouvreau S, Csernoch L, Allard B, Sabatier J, De Waard M, Ronjat M . Transient loss of voltage control of Ca2+ release in the presence of maurocalcine in skeletal muscle. Biophys J. 2006; 91(6):2206-15. PMC: 1557560. DOI: 10.1529/biophysj.105.078089. View

Szentesi P, Szappanos H, Szegedi C, Gonczi M, Jona I, Cseri J . Altered elementary calcium release events and enhanced calcium release by thymol in rat skeletal muscle. Biophys J. 2004; 86(3):1436-53. PMC: 1303980. DOI: 10.1016/S0006-3495(04)74213-7. View

Mosbah A, Kharrat R, Fajloun Z, Renisio J, Blanc E, Sabatier J . A new fold in the scorpion toxin family, associated with an activity on a ryanodine-sensitive calcium channel. Proteins. 2000; 40(3):436-42. DOI: 10.1002/1097-0134(20000815)40:3<436::aid-prot90>3.0.co;2-9. View

10.

Zhou J, Brum G, Gonzalez A, Launikonis B, Stern M, Rios E . Ca2+ sparks and embers of mammalian muscle. Properties of the sources. J Gen Physiol. 2003; 122(1):95-114. PMC: 2234470. DOI: 10.1085/jgp.200308796. View

11.

Tsugorka A, Rios E, Blatter L . Imaging elementary events of calcium release in skeletal muscle cells. Science. 1995; 269(5231):1723-6. DOI: 10.1126/science.7569901. View

12.

Herrmann-Frank A, Richter M, Sarkozi S, Mohr U, Lehmann-Horn F . 4-Chloro-m-cresol, a potent and specific activator of the skeletal muscle ryanodine receptor. Biochim Biophys Acta. 1996; 1289(1):31-40. DOI: 10.1016/0304-4165(95)00131-x. View

13.

Gonzalez A, Kirsch W, Shirokova N, Pizarro G, Stern M, Rios E . The spark and its ember: separately gated local components of Ca(2+) release in skeletal muscle. J Gen Physiol. 2000; 115(2):139-58. PMC: 2217200. DOI: 10.1085/jgp.115.2.139. View

14.

Merrifield B . Solid phase synthesis. Science. 1986; 232(4748):341-7. DOI: 10.1126/science.3961484. View

15.

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

16.

Sarkozi S, Szegedi C, Lukacs B, Ronjat M, Jona I . Effect of gadolinium on the ryanodine receptor/sarcoplasmic reticulum calcium release channel of skeletal muscle. FEBS J. 2005; 272(2):464-71. DOI: 10.1111/j.1742-4658.2004.04486.x. View

17.

Almassy J, Sztretye M, Lukacs B, Dienes B, Szabo L, Szentesi P . Effects of K-201 on the calcium pump and calcium release channel of rat skeletal muscle. Pflugers Arch. 2008; 457(1):171-83. DOI: 10.1007/s00424-008-0504-7. View

18.

Gonzalez A, Kirsch W, Shirokova N, Pizarro G, Brum G, Pessah I . Involvement of multiple intracellular release channels in calcium sparks of skeletal muscle. Proc Natl Acad Sci U S A. 2000; 97(8):4380-5. PMC: 18250. DOI: 10.1073/pnas.070056497. View

19.

Cheng H, Song L, Shirokova N, Gonzalez A, Lakatta E, Rios E . Amplitude distribution of calcium sparks in confocal images: theory and studies with an automatic detection method. Biophys J. 1999; 76(2):606-17. PMC: 1300067. DOI: 10.1016/S0006-3495(99)77229-2. View

20.

Shahbazzadeh D, Srairi-Abid N, Feng W, Ram N, Borchani L, Ronjat M . Hemicalcin, a new toxin from the Iranian scorpion Hemiscorpius lepturus which is active on ryanodine-sensitive Ca2+ channels. Biochem J. 2007; 404(1):89-96. PMC: 1868827. DOI: 10.1042/BJ20061404. View