Abstract
Excitation–contraction coupling, as the name implies, was originally defined to include the events from the sarcolemma action potential to the contraction of the muscle. But with the rapidly increasing knowledge concerning the mechanisms of muscle activation, sub-disciplines developed. Now excitation-contraction coupling usually is defined in a more limited way as the events that link surface membrane depolarization to the release of Ca2+ from the sarcoplasmic reticulum in muscle cells (Paolini et al. 2004). The contraction part of excitation-contraction coupling is more likely now to be called regulation of contraction in striated muscle (Gordon et al. 2000).
…despite the identification of the key players in skeletal EC coupling, the same mechanistic questions facing investigators 15 years ago persist today. (Beam and Bannister 2010. With permission Rockefeller University Press)
K. G. Beam and R. Bannister (2010)
There is little doubt that the amphiphilic helix H3(I) works as a molecular switch that transmits the initial signal of Ca 2+ binding to the N lobe of TnC to the other components in the thin filament, and thus has a central role in initial steps of troponin-tropomyosin based regulation. (Takeda et al. 2003. With permission Nature Publishing Group)
Takeda et al. (2003)
The data can be interpreted in terms of a model in which strong cross-bridges activate the thin filament, this activation being modulated by Ca 2+ binding to troponin. (Millar and Homsher 1990. With permission American Society for Biochemistry and Molecular Biology)
N. C. Millar and E. Homsher (1990)
We can now say that the mechanism of active transport by SERCA1a is roughly understood, as crystal structures of most of the intermediates in the reaction cycle have been determined… (Toyoshima and Cornelius 2013. With permission Elsevier)
C. Toyoshima and F. Cornelius (2013)
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Notes
- 1.
Kurt G. Beam received a Ph.D. from the University of Washington in 1976 with Charles F. Stevens and did postdoctoral training at Yale University with Paul Greengard who would later win the Nobel Prize in 2000. His first faculty position was at the University of Iowa in the late 1970s from which he moved to Colorado State University and eventually to the University of Colorado. His research has concentrated on elucidation of the mechanism of excitation-contraction in skeletal muscle. Beam was elected to the National Academy of Sciences in 2012.
- 2.
Shosaku Numa (1929–1992) received his M.D. degree from Kyoto University in 1952. He did postdoctoral training at Harvard University and at the Max-Planck Institute in Munich. Numa returned to Kyoto University in 1961 and was appointed professor in the department of medical chemistry in 1968 where he remained throughout his research career. He was a pioneer of molecular neurobiology and he and his group were responsible for cloning the genes and studying the function of a large number of membrane proteins (receptors, ion channels and ion pumps, see text). Because of his outstanding achievements, he received many prizes and honors, including the Japan Academy Prize and nomination as a Person of Cultural Merit of Japan. He was a foreign member of the Royal Society and a foreign associate of the National Academy of Sciences. He died prematurely of colon cancer at the age of 63 at the height of his spectacular research career (Imura 1995).
- 3.
In order to clone the gene coding for the skeletal muscle voltage-gated Ca2+ channel, the following procedure was employed: (1) Rabbit skeletal muscle DHPR was purified, (2) Photoaffinity labeling of DHPR with dihydropyridine 3H-azidopine showed that the ligand was specifically incorporated into the 170 kDa polypeptide, (3) 170 kDa polypeptide was purified, (4) 170 kDa polypeptide was digested with trypsin and the resulting peptides were fractionated, (5) Amino acid sequences of peptides were determined, (6) Synthetic oligodeoxyribonucleotides for one of the peptides were prepared, (7) Then used as a specific primer for reverse transcription and as a probe for selecting the resulting cDNA clones, (8) The initial DNA clone thus isolated was used to probe for cloning longer cDNA sequences (Tanabe et al. 1987).
- 4.
What then is the function of the DHPR Ca2+ calcium current in skeletal muscle excitation-contraction coupling? In short, no one knows. It has been speculated that the Ca2+ current through the DHPR may act to ensure long-term Ca2+ replenishment of the SR (Tanabe et al. 1987).
- 5.
FKBP12 is a member of the immunophilin family. It was originally discovered based on its ability to bind and mediate the immunosuppressive effects of the drug FK506. It is named according to its ability to bind to FK506 and its molecular mass of 12 kDa (Marks 1996).
- 6.
Roger Yongjian Tsien (1952–) received a Ph.D. in physiology from the University of Cambridge in 1978. After a faculty position in physiology at the University of California, Berkeley, he moved to the University of California, San Diego in 1989 where he has remained throughout his research career. Worrying that he might become “trapped” in a career imaging inorganic ions, Tsien (2008) began a career exploring macromolecular interactions with fluorescent proteins. His laboratory is best known for designing and building molecules that either report or perturb signal transduction inside living cells. This work led to the discovery and development of the green fluorescent protein for which he shared the Nobel Prize in 2008.
- 7.
Names are derived from the first four letters of the chemical name of the chromophore or most prominent substituent. The following numeral indicates the chronological order of introduction. For example, 1,2-bis(o-aminophenoxy)ethane-N,N,-N′,N′-tetraacetic acid was called BAPTA.
- 8.
There are complications in using Ca2+ indicators to accurately track [Ca2+]i. All of the Ca2+ indicators bind to intracellular proteins to a greater or lesser extent and this binding changes their kinetic properties. Furthermore in order to minimize any artifacts due to muscle movement during contraction, Baylor and Hollingworth (2011) perform experiments on fibers stretched to sarcomere lengths of 3.5–4 μm. This condition eliminates the possibility of examining the relationship of the calcium transient to various mechanical responses.
- 9.
Muttaiya Sundaralingam (1931–2004) and his wife died tragically in the tsunami that hit the coast of Sri Lanka on December 26, 2004 following the submarine earthquake which had occurred a couple of hours earlier off the coast of Sumatra (Westhof 2005).
- 10.
During the latter part of the twentieth century investigators in the protein structure and function group in the department of biochemistry at the University of Alberta made major contributions to the understanding of protein-protein interactions in troponin and the structure of troponin C. The main investigators included: Lawrence B. Smillie and Robert S. Hodges (biochemistry of troponin and its subunits), Michael N. G. James (crystal structures of troponin C) and Brian D. Sykes (NMR solution structures of troponin C).
- 11.
The Hill equation is expressed as: F = Fo [Ca2+]n/(Kn + [Ca2+]n) or in the more usual form: F = Fo/(1 + 10n(pCa50−pCa)] where n (or nH, the Hill coefficient) is a measure of the steepness of the force versus pCa relationship and an indicator of the extent of cooperativity and pCa50 is a measure of the calcium concentration giving 50 % of maximum force and an indicator of calcium sensitivity of force of contraction (Gordon et al. 2000).
- 12.
The Hill coefficient, nH, is the most variable parameter in the force versus pCa relationship. The values of nH can vary from ~2 to 6 depending on experimental conditions and technical aspects of the measurement.
- 13.
Unlike skeletal muscle, phosphorylation of the myosin regulatory light chain is obligatory for contraction in smooth muscle. See Kamm and Stull (1985) for a review.
- 14.
Sarcolipin (SLN), originally characterized and named by Wawrzynow et al. (1992) has been shown to uncouple ATP hydrolysis from Ca2+ transport by the Ca2+-ATPase of the sarcoplasmic reticulum of skeletal muscle (SERCA) (Smith et al. 2002). Interestingly it was also shown to be necessary for muscle-based non-shivering thermogenesis. When challenged to acute cold, SLN knockout mice were not able to maintain their core body temperature and developed hypothermia. Over-expression of SLN in the SLN-null background fully restored muscle-based thermogenesis, suggesting that SLN is the basis for SERCA-mediated heat production. Ryanodine receptor 1 (Ryr1)-mediated Ca2+ leak was shown to be an important mechanism for SERCA-activated heat generation. It was suggested that SLN can continue to interact with SERCA in the presence of Ca2+ and can promote uncoupling of the SERCA pump and cause futile cycling and heat production (Bal et al. 2012).
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Rall, J.A. (2014). Excitation-Contraction Coupling and Regulation of Contraction in Skeletal Muscle: The Modern Synthesis. In: Mechanism of Muscular Contraction. Perspectives in Physiology. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-2007-5_8
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