Abstract
The control of force by [Ca2+] was investigated in rat cardiac trabeculae loaded with fura-2 salt. At sarcomere lengths of 2.1-2.3 microns, the steady state force-[Ca2+]i relationship during tetanization in the presence of ryanodine was half maximally activated at a [Ca2+]i of 0.65 +/- 0.19 microM with a Hill coefficient of 5.2 +/- 1.2 (mean +/- SD, n = 9), and the maximal stress produced at saturating [Ca2+]i equalled 121 +/- 35 mN/mm2 (n = 9). The dependence of steady state force on [Ca2+]i was identical in muscles tetanized in the presence of the Ca(2+)-ATPase inhibitor cyclopiazonic acid (CPA). The force-[Ca2+]i relationship during the relaxation of twitches in the presence of CPA coincided exactly to that measured at steady state during tetani, suggesting that CPA slows the decay rate of [Ca2+]i sufficiently to allow the force to come into a steady state with the [Ca2+]i. In contrast, the relationship of force to [Ca2+]i during the relaxation phase of control twitches was shifted leftward relative to the steady state relationship, establishing that relaxation is limited by the contractile system itself, not by Ca2+ removal from the cytosol. Under control conditions the force-[Ca2+]i relationship, quantified at the time of peak twitch force (i.e., dF/dt = 0), coincided fairly well with steady state measurements in some trabeculae (i.e., three of seven). However, the force-[Ca2+]i relationship at peak force did not correspond to the steady state measurements after the application of 5 mM 2,3-butanedione monoxime (BDM) (to accelerate cross-bridge kinetics) or 100 microM CPA (to slow the relaxation of the [Ca2+]i transient). Therefore, we conclude that the relationship of force to [Ca2+]i during physiological twitch contractions cannot be used to predict the steady state relationship.
MeSH Terms
Animals
Calcium/metabolism,physiology
Calcium-Transporting ATPases/antagonists & inhibitors
Cytosol/drug effects,metabolism
Female
Fura-2
Heart/drug effects,physiology
In Vitro Techniques
Indoles/pharmacology
Male
Muscle Fibers, Skeletal/physiology,ultrastructure
Myocardial Contraction/drug effects,physiology
Myocardium/metabolism,ultrastructure
Papillary Muscles/drug effects,metabolism
Rats
Rats, Inbred Strains
Ryanodine/pharmacology
Sarcomeres/physiology,ultrastructure
Spectrometry, Fluorescence
Chemicals
Indoles
Ryanodine
Calcium-Transporting ATPases
Calcium
Fura-2
cyclopiazonic acid
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Backx P H
Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205, USA.
Gao W D
Azan-Backx M D
Marban E
References (33)
33 references, click to expand
-
Intracellular calcium transients underlying the short-term force-interval relationship in ferret ventricular myocardium.
J Physiol. 1986 Jul;376:507-30
PMID: 2432238
-
The force-frequency relationship in rat myocardium. The influence of muscle dimensions.
Pflugers Arch. 1986 Jul;407(1):14-7
PMID: 3737379
-
Ryanodine modifies conductance and gating behavior of single Ca2+ release channel.
Am J Physiol. 1987 Sep;253(3 Pt 1):C364-8
PMID: 2443015
-
Quantitation of intracellular free calcium in single adult cardiomyocytes by fura-2 fluorescence microscopy: calibration of fura-2 ratios.
Biochem Biophys Res Commun. 1987 Aug 31;147(1):120-6
PMID: 3115258
-
Effect of rigor and cycling cross-bridges on the structure of troponin C and on the Ca2+ affinity of the Ca2+-specific regulatory sites in skinned rabbit psoas fibers.
J Biol Chem. 1987 Oct 5;262(28):13627-35
PMID: 3654633
-
Evidence for a force-dependent component of calcium binding to cardiac troponin C.
Am J Physiol. 1987 Oct;253(4 Pt 1):C541-6
PMID: 3499084
-
Fluorescence and bioluminescence measurement of cytoplasmic free calcium.
Biochem J. 1987 Dec 1;248(2):313-28
PMID: 3325037
-
Hysteresis and the length dependence of calcium sensitivity in chemically skinned rat cardiac muscle.
J Physiol. 1988 Jul;401:115-43
PMID: 3171985
-
Influence of temperature on the calcium sensitivity of the myofilaments of skinned ventricular muscle from the rabbit.
J Gen Physiol. 1989 Mar;93(3):411-28
PMID: 2703821
-
Correction of proton and Ca association constants of EGTA for temperature and ionic strength.
Am J Physiol. 1989 Jun;256(6 Pt 1):C1250-6
PMID: 2544095
-
Fura-2 calcium transients in frog skeletal muscle fibres.
J Physiol. 1988 Sep;403:151-92
PMID: 3267019
-
Butanedione monoxime suppresses contraction and ATPase activity of rabbit skeletal muscle.
J Biochem. 1989 Apr;105(4):638-43
PMID: 2527229
-
Modulation of Ca2+ transients and contractile properties by beta-adrenoceptor stimulation in ferret ventricular muscles.
J Physiol. 1990 Apr;423:221-40
PMID: 1696985
-
Relation between steady-state force and intracellular [Ca2+] in intact human myocardium. Index of myofibrillar responsiveness to Ca2+.
Circulation. 1990 Oct;82(4):1266-78
PMID: 2205417
-
Ca2+ and activation mechanisms in skeletal muscle.
Q Rev Biophys. 1991 Feb;24(1):1-73
PMID: 2047521
-
Ca2+ regulation of mechanical properties of striated muscle. Mechanistic studies using extraction and replacement of regulatory proteins.
Circ Res. 1992 May;70(5):865-84
PMID: 1348975
-
Theoretical model for the cooperative equilibrium binding of myosin subfragment 1 to the actin-troponin-tropomyosin complex.
Proc Natl Acad Sci U S A. 1980 Jun;77(6):3186-90
PMID: 10627230
-
Effects of magnesium on contractile activation of skinned cardiac cells.
J Physiol. 1975 Aug;249(3):497-517
PMID: 1177102
-
The calcium and magnesium binding sites on cardiac troponin and their role in the regulation of myofibrillar adenosine triphosphatase.
J Biol Chem. 1980 Dec 25;255(24):11688-93
PMID: 6449512
-
Calcium transients in mammalian ventricular muscle.
Eur Heart J. 1980;Suppl A:5-15
PMID: 7274230
-
Influence of osmotic compression on calcium activation and tension in skinned muscle fibers of the rabbit.
Pflugers Arch. 1981 Oct;391(4):334-7
PMID: 7312568
-
Cytosolic calcium and myofilaments in single rat cardiac myocytes achieve a dynamic equilibrium during twitch relaxation.
J Physiol. 1992 Feb;447:83-102
PMID: 1593465
-
Effect of 2,3-butanedione monoxime on myosin and myofibrillar ATPases. An example of an uncompetitive inhibitor.
Biochemistry. 1992 Dec 8;31(48):12227-32
PMID: 1457420
-
The effect of the lattice spacing change on cross-bridge kinetics in chemically skinned rabbit psoas muscle fibers. II. Elementary steps affected by the spacing change.
Biophys J. 1993 Jan;64(1):197-210
PMID: 7679297
-
Fluorescent properties of rat cardiac trabeculae microinjected with fura-2 salt.
Am J Physiol. 1993 Apr;264(4 Pt 2):H1098-110
PMID: 8476086
-
Effect of cross-bridge kinetics on apparent Ca2+ sensitivity.
J Gen Physiol. 1982 Jun;79(6):997-1016
PMID: 6980967
-
The effects of muscle length on intracellular calcium transients in mammalian cardiac muscle.
J Physiol. 1982 Jun;327:79-94
PMID: 7120151
-
Measurement of Ca2+ concentrations in living cells.
Prog Biophys Mol Biol. 1982;40(1-2):1-114
PMID: 6758036
-
The inhibitory effects of monovalent ions on force development in detergent-skinned ventricular muscle from guinea-pig.
J Physiol. 1984 Jul;352:353-74
PMID: 6747893
-
A new generation of Ca2+ indicators with greatly improved fluorescence properties.
J Biol Chem. 1985 Mar 25;260(6):3440-50
PMID: 3838314
-
Rapid ionic modifications during the aequorin-detected calcium transient in a skinned canine cardiac Purkinje cell.
J Gen Physiol. 1985 Feb;85(2):189-246
PMID: 3981128
-
Relationship between force and intracellular [Ca2+] in tetanized mammalian heart muscle.
J Gen Physiol. 1986 Feb;87(2):223-42
PMID: 2419483
-
Intracellular [Ca2+] related to rate of force development in twitch contraction of heart.
Am J Physiol. 1987 Apr;252(4 Pt 2):H760-70
PMID: 3565592