Rapid ionic modifications during the aequorin-detected calcium transient in a skinned canine cardiac Purkinje cell

A microprocessor-controlled system of microinjections and microaspirations has been developed to change, within approximately 1 ms, the [free Ca2+] at the outer surface of the sarcoplasmic reticulum (SR) wrapped around individual myofibrils (0.3-0.4 micron radius) of a skinned canine cardiac Purkinje cell (2.5-4.5 micron overall radius) at different phases of a Ca2+ transient. Simultaneously monitoring tension and aequorin bioluminescence provided two methods for estimating the peak myoplasmic [free Ca2+] reached during the spontaneous cyclic Ca2+ release from the SR obtained in the continuous presence of a bulk solution [free Ca2+] sufficiently high to overload the SR. These methods gave results in excellent agreement for the spontaneous Ca2+ release under a variety of conditions of pH and [free Mg2+], and of enhancement of Ca2+ release by calmodulin. Disagreement was observed, however, when the Ca2+ transient was modified during its ascending phase. The experiments also permitted quantification of the aequorin binding within the myofibrils and determination of its operational apparent affinity constant for Ca2+ at various [free Mg2+] levels. An increase of [free Ca2+] at the outer surface of the SR during the ascending phase of the Ca2+ transient induced further release of Ca2+. In contrast, an increase of [free Ca2+] during the descending phase of the Ca2+ transient did not cause further Ca2+ release. Varying [free H+], [free Mg2+], or the [Na+]/[K+] ratio had no significant effect on the Ca2+ transient during which the modification was applied, but it altered the subsequent Ca2+ transient. Therefore, Ca2+ appears to be the major, if not the only, ion controlling Ca2+ release from the SR rapidly enough to alter a Ca2+ transient during its course.

[1]  S. Street,et al.  Lateral transmission of tension in frog myofibers: A myofibrillar network and transverse cytoskeletal connections are possible transmitters , 1983, Journal of cellular physiology.

[2]  A. M. Gordon,et al.  Muscle calcium transient. Effect of post-stimulus length changes in single fibers , 1984, The Journal of general physiology.

[3]  P. Brandt,et al.  Can the binding of Ca2+ to two regulatory sites on troponin C determine the steep pCa/tension relationship of skeletal muscle? , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[4]  J. Illingworth.  A common source of error in pH measurements. , 1981, The Biochemical journal.

[5]  D. Allen,et al.  The effects of muscle length on intracellular calcium transients in mammalian cardiac muscle. , 1982, The Journal of physiology.

[6]  W. Wier.  Calcium transients during excitation-contraction coupling in mammalian heart: aequorin signals of canine Purkinje fibers. , 1980, Science.

[7]  G. Elliott.  Donnan and osmotic effects in muscle fibres without membranes. , 1973, Journal of mechanochemistry & cell motility.

[8]  W. Wier,et al.  Excitation-contraction coupling in cardiac Purkinje fibers. Effects of caffeine on the intracellular [Ca2+] transient, membrane currents, and contraction , 1984, The Journal of general physiology.

[9]  G. Lopaschuk,et al.  Characterization of calmodulin effects on calcium transport in cardiac microsomes enriched in sarcoplasmic reticulum. , 1980, Biochemistry.

[10]  E. Lakatta,et al.  Cellular calcium fluctuations in mammalian heart: direct evidence from noise analysis of aequorin signals in Purkinje fibers. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[11]  S. McLaughlin.  Electrostatic Potentials at Membrane-Solution Interfaces , 1977 .

[12]  A. Fabiato,et al.  Effects of magnesium on contractile activation of skinned cardiac cells. , 1975, The Journal of physiology.

[13]  A. Fabiato,et al.  Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. , 1983, The American journal of physiology.

[14]  D. Allen,et al.  The effects of changes of pH on intracellular calcium transients in mammalian cardiac muscle. , 1983, The Journal of physiology.

[15]  A. Fabiato,et al.  Myoplasmic free calcium concentration reached during the twitch of an intact isolated cardiac cell and during calcium-induced release of calcium from the sarcoplasmic reticulum of a skinned cardiac cell from the adult rat or rabbit ventricle , 1981, The Journal of general physiology.

[16]  D. Allen,et al.  Calcium transients in mammalian ventricular muscle. , 1980, European heart journal.

[17]  M. Kushmerick,et al.  Ionic Mobility in Muscle Cells , 1969, Science.

[18]  A. Fabiato,et al.  Calculator programs for computing the composition of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells. , 1979, Journal de physiologie.

[19]  A. Fabiato,et al.  Excitation‐Contraction Coupling of Isolated Cardiac Fibers with Disrupted or Closed Sarcolemmas: CALCIUM‐DEPENDENT CYCLIC AND TONIC CONTRACTIONS , 1972, Circulation research.

[20]  Fluorescence and differential light absorption recordings with calcium probes and potential-sensitive dyes in skinned cardiac cells. , 1982, Canadian journal of physiology and pharmacology.

[21]  E. W. Stephenson.  Activation of fast skeletal muscle: contributions of studies on skinned fibers. , 1981, The American journal of physiology.

[22]  C. Baumgarten,et al.  Potential and K+ activity in skinned muscle fibers. Evidence against a simple Donnan equilibrium. , 1984, Biophysical journal.

[23]  A. Fabiato,et al.  Excitation-Contraction Coupling of Isolated Cardiac Fibers with Disrupted or Closed Sarcolemmas , 1972 .

[24]  D. Stephenson,et al.  Calcium‐activated force responses in fast‐ and slow‐twitch skinned muscle fibres of the rat at different temperatures. , 1981, The Journal of physiology.

[25]  D. S. Wood,et al.  Chemically skinned mammalian skeletal muscle. I. The structure of skinned rabbit psoas. , 1979, Tissue & cell.

[26]  A. Fabiato,et al.  Myofilament-generated tension oscillations during partial calcium activation and activation dependence of the sarcomere length-tension relation of skinned cardiac cells , 1978, The Journal of general physiology.

[27]  J. Westwater,et al.  The Mathematics of Diffusion. , 1957 .

[28]  A. Fabiato,et al.  Use of aequorin for the appraisal of the hypothesis of the release of calcium from the sarcoplasmic reticulum induced by a change of pH in skinned cardiac cells. , 1985, Cell calcium.

[29]  H. Shuman,et al.  Calcium release and ionic changes in the sarcoplasmic reticulum of tetanized muscle: an electron-probe study , 1981, The Journal of cell biology.

[30]  C. Ashley,et al.  The effect of physiologically occurring cations upon aequorin light emission. Determination of the binding constants. , 1977, Biochimica et biophysica acta.

[31]  A. Hill.  The Combinations of Haemoglobin with Oxygen and with Carbon Monoxide. I. , 1913, The Biochemical journal.

[32]  G. Smith,et al.  EGTA purity and the buffering of calcium ions in physiological solutions. , 1984, The American journal of physiology.

[33]  A. M. Gordon,et al.  Hysteresis in the force-calcium relation in muscle. , 1983, Science.

[34]  I. Matsubara,et al.  X-ray diffraction studies on skinned single fibres of frog skeletal muscle. , 1972, Journal of molecular biology.

[35]  B. R. Jewell,et al.  [31] Practical aspects of the use of aequorin as a calcium indicator: Assay, preparation, microinjection, and interpretation of signals , 1978 .

[36]  D. Stephenson,et al.  Non-uniform ion distributions and electrical potentials in sarcoplasmic regions of skeletal muscle fibres , 1981, Nature.

[37]  A. Fabiato,et al.  Effects of pH on the myofilaments and the sarcoplasmic reticulum of skinned cells from cardiace and skeletal muscles. , 1978, The Journal of physiology.

[38]  J R Smith,et al.  Hydrogen ion buffers for biological research. , 1966, Analytical biochemistry.

[39]  W J Crozier,et al.  The Journal of General Physiology , 1919, Botanical Gazette.

[40]  J. Morgan,et al.  Intracellular Ca2+ transients in the cat papillary muscle. , 1982, Canadian journal of physiology and pharmacology.

[41]  P. M. Best,et al.  Characterization of the effects of Mg2+ on Ca2+- and Sr2+-activated tension generation of skinned rat cardiac fibers , 1978, The Journal of general physiology.

[42]  J. Potter,et al.  Studies on Phosphorylation of Canine Cardiac Sarcoplasmic Reticulum by Calmodulin‐Dependent Protein Kinase , 1981, Circulation research.

[43]  J S Shiner,et al.  Calcium Requirements for Cardiac Myofibrillar Activation , 1974, Circulation research.

[44]  D. Allen,et al.  Photoproteins as biological calcium indicators. , 1976, Pharmacological reviews.

[45]  Don Lancaster.  Active-Filter Cookbook , 1975 .

[46]  R. Godt.  A simple electrostatic model can explain the effect of pH upon the force-pCa relation of skinned frog skeletal muscle fibers. , 1981, Biophysical journal.

[47]  O. Shimomura,et al.  Calcium Binding, Quantum Yield, and Emitting Molecule in Aequorin Bioluminescence , 1970, Nature.

[48]  A. Fabiato,et al.  Time and calcium dependence of activation and inactivation of calcium- induced release of calcium from the sarcoplasmic reticulum of a skinned canine cardiac Purkinje cell , 1985, The Journal of general physiology.

[49]  J. Potter,et al.  A fluorescence stopped flow analysis of Ca2+ exchange with troponin C. , 1979, The Journal of biological chemistry.

[50]  A. Fabiato.  Simulated calcium current can both cause calcium loading in and trigger calcium release from the sarcoplasmic reticulum of a skinned canine cardiac Purkinje cell , 1985, The Journal of general physiology.

[51]  D. Allen,et al.  Calcium transients in aequorin-injected frog cardiac muscle , 1978, Nature.

[52]  A. Fabiato.  Calcium release in skinned cardiac cells: variations with species, tissues, and development. , 1982, Federation proceedings.

[53]  K. Mann,et al.  Chemical and physical properties of aequorin and the green fluorescent protein isolated from Aequorea forskålea. , 1978, Biochemistry.

[54]  A. Badran,et al.  On the ultrastructure of cardiac muscle. , 1969, The Journal of the Egyptian Medical Association.

[55]  J. Suko,et al.  Correlation between calmodulin-dependent increase in the rate of calcium transport and calmodulin-dependent phosphorylation of cardiac sarcoplasmic reticulum. Characterization of calmodulin-dependent phosphorylation. , 1983, European journal of biochemistry.

[56]  D. Allen,et al.  Aequorin luminescence: relation of light emission to calcium concentration--a calcium-independent component. , 1977, Science.