The Excitation-contraction Coupling Mechanism in Skeletal Muscle

Overview

Journal Biophys Rev

Publisher Springer

Specialty Biophysics

Date 2017 May 17

PMID 28509964

Citations 71

Authors

Juan C Calderon

Pura Bolanos

Carlo Caputo

Affiliations

Soon will be listed here.

Abstract

First coined by Alexander Sandow in 1952, the term excitation-contraction coupling (ECC) describes the rapid communication between electrical events occurring in the plasma membrane of skeletal muscle fibres and Ca release from the SR, which leads to contraction. The sequence of events in twitch skeletal muscle involves: (1) initiation and propagation of an action potential along the plasma membrane, (2) spread of the potential throughout the transverse tubule system (T-tubule system), (3) dihydropyridine receptors (DHPR)-mediated detection of changes in membrane potential, (4) allosteric interaction between DHPR and sarcoplasmic reticulum (SR) ryanodine receptors (RyR), (5) release of Ca from the SR and transient increase of Ca concentration in the myoplasm, (6) activation of the myoplasmic Ca buffering system and the contractile apparatus, followed by (7) Ca disappearance from the myoplasm mediated mainly by its reuptake by the SR through the SR Ca adenosine triphosphatase (SERCA), and under several conditions movement to the mitochondria and extrusion by the Na/Ca exchanger (NCX). In this text, we review the basics of ECC in skeletal muscle and the techniques used to study it. Moreover, we highlight some recent advances and point out gaps in knowledge on particular issues related to ECC such as (1) DHPR-RyR molecular interaction, (2) differences regarding fibre types, (3) its alteration during muscle fatigue, (4) the role of mitochondria and store-operated Ca entry in the general ECC sequence, (5) contractile potentiators, and (6) Ca sparks.

Citing Articles

Immature Skeletal Myotubes Are an Effective Source for Improving the Terminal Differentiation of Skeletal Muscle.

Jeong S, Choi J, Allen P, Lee E Cells. 2025; 13(24.

PMID: 39768224 PMC: 11674136. DOI: 10.3390/cells13242136.

Metabolic acidosis and sudden infant death syndrome: overlooked data provides insight into SIDS pathogenesis.

Goldwater P, Gebien D World J Pediatr. 2024; 21(1):29-40.

PMID: 39656413 PMC: 11814015. DOI: 10.1007/s12519-024-00860-9.

Sorafenib induces cachexia by impeding transcriptional signaling of the SET1/MLL complex on muscle-specific genes.

Khan B, Lanzuolo C, Rosti V, Santarelli P, Pich A, Kraft T iScience. 2024; 27(10):110913.

PMID: 39386761 PMC: 11462028. DOI: 10.1016/j.isci.2024.110913.

A comprehensive review on physiological and biological activities of carnosine: turning from preclinical facts to potential clinical applications.

Kumar A, Suryakumar G, Singh S, Rathor R Naunyn Schmiedebergs Arch Pharmacol. 2024; 398(2):1341-1366.

PMID: 39302423 DOI: 10.1007/s00210-024-03427-7.

Constitutive, Muscle-Specific Knockout Results in the Incomplete Assembly of Ca Entry Units and a Reduction in the Age-Dependent Formation of Tubular Aggregates.

Di Fonso A, Serano M, He M, Leigh J, Rastelli G, Dirksen R Biomedicines. 2024; 12(8).

PMID: 39200116 PMC: 11351919. DOI: 10.3390/biomedicines12081651.

References

Ebashi S . Regulatory mechanism of muscle contraction with special reference to the Ca-troponin-tropomyosin system. Essays Biochem. 1974; 10:1-36. View

Franzini-Armstrong C, Boncompagni S . The evolution of the mitochondria-to-calcium release units relationship in vertebrate skeletal muscles. J Biomed Biotechnol. 2011; 2011:830573. PMC: 3196067. DOI: 10.1155/2011/830573. View

HODGKIN A, Horowicz P . The influence of potassium and chloride ions on the membrane potential of single muscle fibres. J Physiol. 1959; 148:127-60. PMC: 1363113. DOI: 10.1113/jphysiol.1959.sp006278. View

Weber A, HERZ R . The relationship between caffeine contracture of intact muscle and the effect of caffeine on reticulum. J Gen Physiol. 1968; 52(5):750-9. PMC: 2225844. DOI: 10.1085/jgp.52.5.750. View

GAUTHIER G, PADYKULA H . Cytological studies of fiber types in skeletal muscle. A comparative study of the mammalian diaphragm. J Cell Biol. 1966; 28(2):333-54. PMC: 2106931. DOI: 10.1083/jcb.28.2.333. View

Martins de Brito O, Scorrano L . Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature. 2008; 456(7222):605-10. DOI: 10.1038/nature07534. View

Raju B, Murphy E, LEVY L, Hall R, London R . A fluorescent indicator for measuring cytosolic free magnesium. Am J Physiol. 1989; 256(3 Pt 1):C540-8. DOI: 10.1152/ajpcell.1989.256.3.C540. View

Kirichok Y, Krapivinsky G, Clapham D . The mitochondrial calcium uniporter is a highly selective ion channel. Nature. 2004; 427(6972):360-4. DOI: 10.1038/nature02246. View

Serysheva I, Chiu W, Ludtke S . Single-particle electron cryomicroscopy of the ion channels in the excitation-contraction coupling junction. Methods Cell Biol. 2007; 79:407-35. DOI: 10.1016/S0091-679X(06)79016-1. View

10.

Parekh A, Putney Jr J . Store-operated calcium channels. Physiol Rev. 2005; 85(2):757-810. DOI: 10.1152/physrev.00057.2003. View

11.

Hille B, Campbell D . An improved vaseline gap voltage clamp for skeletal muscle fibers. J Gen Physiol. 1976; 67(3):265-93. PMC: 2214972. DOI: 10.1085/jgp.67.3.265. View

12.

Launikonis B, Zhou J, Royer L, R Shannon T, Brum G, Rios E . Confocal imaging of [Ca2+] in cellular organelles by SEER, shifted excitation and emission ratioing of fluorescence. J Physiol. 2005; 567(Pt 2):523-43. PMC: 1474212. DOI: 10.1113/jphysiol.2005.087973. View

13.

Wium E, Dulhunty A, Beard N . A skeletal muscle ryanodine receptor interaction domain in triadin. PLoS One. 2012; 7(8):e43817. PMC: 3427183. DOI: 10.1371/journal.pone.0043817. View

14.

Moopanar T, Allen D . Reactive oxygen species reduce myofibrillar Ca2+ sensitivity in fatiguing mouse skeletal muscle at 37 degrees C. J Physiol. 2005; 564(Pt 1):189-99. PMC: 1456045. DOI: 10.1113/jphysiol.2005.083519. View

15.

Franzini-Armstrong C, Jorgensen A . Structure and development of E-C coupling units in skeletal muscle. Annu Rev Physiol. 1994; 56:509-34. DOI: 10.1146/annurev.ph.56.030194.002453. View

16.

Calderon J, Bolanos P, Caputo C . Kinetic changes in tetanic Ca²⁺ transients in enzymatically dissociated muscle fibres under repetitive stimulation. J Physiol. 2011; 589(Pt 21):5269-83. PMC: 3225679. DOI: 10.1113/jphysiol.2011.213314. View

17.

Baylor S, Hollingworth S . Calcium indicators and calcium signalling in skeletal muscle fibres during excitation-contraction coupling. Prog Biophys Mol Biol. 2010; 105(3):162-79. PMC: 2974769. DOI: 10.1016/j.pbiomolbio.2010.06.001. View

18.

Parekh A . Store-operated Ca2+ entry: dynamic interplay between endoplasmic reticulum, mitochondria and plasma membrane. J Physiol. 2003; 547(Pt 2):333-48. PMC: 2342659. DOI: 10.1113/jphysiol.2002.034140. View

19.

Samso M, Wagenknecht T, Allen P . Internal structure and visualization of transmembrane domains of the RyR1 calcium release channel by cryo-EM. Nat Struct Mol Biol. 2005; 12(6):539-44. PMC: 1925259. DOI: 10.1038/nsmb938. View

20.

Westerblad H, Allen D, Lannergren J . Muscle fatigue: lactic acid or inorganic phosphate the major cause?. News Physiol Sci. 2002; 17:17-21. DOI: 10.1152/physiologyonline.2002.17.1.17. View