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. 1968 Jul 1;38(1):99–114. doi: 10.1083/jcb.38.1.99

THE ULTRASTRUCTURE OF FROG VENTRICULAR CARDIAC MUSCLE AND ITS RELATIONSHIP TO MECHANISMS OF EXCITATION-CONTRACTION COUPLING

Nancy A Staley 1, Ellis S Benson 1
PMCID: PMC2107467  PMID: 5691981

Abstract

Frog ventricular cardiac muscle has structural features which set it apart from frog and mammalian skeletal muscle and mammalian cardiac muscle. In describing these differences, our attention focused chiefly on the distribution of cellular membranes. Abundant inter cellular clefts, the absence of tranverse tubules, and the paucity of sarcotubules, together with exceedingly small cell diameters (less than 5 µ), support the suggestion that the mechanism of excitation-contraction coupling differs in these muscle cells from that now thought to be characteristic of striated muscle such as skeletal muscle and mammalian cardiac muscle. These structural dissimilarities also imply that the mechanism of relaxation in frog ventricular muscle differs from that considered typical of other striated muscles. Additional ultrastructural features of frog ventricular heart muscle include spherical electron-opaque bodies on thin filaments, inconstantly present, forming a rank across the I band about 150 mµ from the Z line, and membrane-bounded dense granules resembling neurosecretory granules. The functional significance of these features is not yet clear.

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Selected References

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  1. Aghajanian G. K., Bloom F. E. Electron-microscopic autoradiography of rat hypothalamus after intraventricular h3-norepinephrine. Science. 1966 Jul 15;153(3733):308–310. doi: 10.1126/science.153.3733.308. [DOI] [PubMed] [Google Scholar]
  2. BARR L., DEWEY M. M., BERGER W. PROPAGATION OF ACTION POTENTIALS AND THE STRUCTURE OF THE NEXUS IN CARDIAC MUSCLE. J Gen Physiol. 1965 May;48:797–823. doi: 10.1085/jgp.48.5.797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BIANCHI C. P., SHANES A. M. Calcium influx in skeletal muscle at rest, during activity, and during potassium contracture. J Gen Physiol. 1959 Mar 20;42(4):803–815. doi: 10.1085/jgp.42.4.803. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. BLOOM G. D. The fine structure of cyclostome cardiac muscle cells. Z Zellforsch Mikrosk Anat. 1962;57:213–239. doi: 10.1007/BF00319394. [DOI] [PubMed] [Google Scholar]
  5. Bloom F. E., Barrnett R. J. Fine structural localization of noradrenaline in vesicles of autonomic nerve endings. Nature. 1966 May 7;210(5036):599–601. doi: 10.1038/210599a0. [DOI] [PubMed] [Google Scholar]
  6. CAULFIELD J. B. Effects of varying the vehicle for OsO4 in tissue fixation. J Biophys Biochem Cytol. 1957 Sep 25;3(5):827–830. doi: 10.1083/jcb.3.5.827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Costantin L. L., Podolsky R. J. Calcium localization and the activation of striated muscle fibers. Fed Proc. 1965 Sep-Oct;24(5):1141–1145. [PubMed] [Google Scholar]
  8. Costantin L. L., Podolsky R. J. Evidence for depolarization of the internal membrane system in activation of frog semitendinosus muscle. Nature. 1966 Apr 30;210(5035):483–486. doi: 10.1038/210483a0. [DOI] [PubMed] [Google Scholar]
  9. EBASHI S. Calcium binding activity of vesicular relaxing factor. J Chir (Paris) 1961 Sep;82:236–244. doi: 10.1093/oxfordjournals.jbchem.a127439. [DOI] [PubMed] [Google Scholar]
  10. ELFVIN L. G. THE FINE STRUCTURE OF THE CELL SURFACE OF CHROMAFFIN CELLS IN THE RAT ADRENAL MEDULLA. J Ultrastruct Res. 1965 Apr;12:263–286. doi: 10.1016/s0022-5320(65)80099-5. [DOI] [PubMed] [Google Scholar]
  11. Edwards C., Lorkovic H. The roles of calcium in excitation-contraction coupling in various muscles of the frog, mouse, and barnacle. Am Zool. 1967 Aug;7(3):615–622. doi: 10.1093/icb/7.3.615. [DOI] [PubMed] [Google Scholar]
  12. FAWCETT D. W., SELBY C. C. Observations on the fine structure of the turtle atrium. J Biophys Biochem Cytol. 1958 Jan 25;4(1):63–72. doi: 10.1083/jcb.4.1.63. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. FRANZINIARMSTRONG C. SARCOLEMMAL INVAGINATIONS AND THE T-SYSTEM IN FISH SKELETAL MUSCLE. Nature. 1964 Apr 25;202:355–357. doi: 10.1038/202355a0. [DOI] [PubMed] [Google Scholar]
  14. GRIMLEY P. M., EDWARDS G. A. The ultrastructure of cardiac desnosomes in the toad and their relationship to the intercalated disc. J Biophys Biochem Cytol. 1960 Oct;8:305–318. doi: 10.1083/jcb.8.2.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gillis J. M., Page S. G. Localization of ATPase activity in striated muscle and probable sources of artifact. J Cell Sci. 1967 Mar;2(1):113–118. doi: 10.1242/jcs.2.1.113. [DOI] [PubMed] [Google Scholar]
  16. HILL A. V. The abrupt transition from rest to activity in muscle. Proc R Soc Lond B Biol Sci. 1949 Oct;136(884):399–420. doi: 10.1098/rspb.1949.0033. [DOI] [PubMed] [Google Scholar]
  17. HUXLEY A. F., TAYLOR R. E. Local activation of striated muscle fibres. J Physiol. 1958 Dec 30;144(3):426–441. doi: 10.1113/jphysiol.1958.sp006111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. HUXLEY H. E. EVIDENCE FOR CONTINUITY BETWEEN THE CENTRAL ELEMENTS OF THE TRIADS AND EXTRACELLULAR SPACE IN FROG SARTORIUS MUSCLE. Nature. 1964 Jun 13;202:1067–1071. doi: 10.1038/2021067b0. [DOI] [PubMed] [Google Scholar]
  19. INCHIOSA M. A., Jr ACTOMYOSIN CONTENT OF RABBIT HEART VENTRICLE. Am J Physiol. 1964 Mar;206:541–546. doi: 10.1152/ajplegacy.1964.206.3.541. [DOI] [PubMed] [Google Scholar]
  20. Irisawa A., Hama K. Some observations on the fine structure of the mantis shrimp heart. Z Zellforsch Mikrosk Anat. 1965 Dec 10;68(5):674–688. doi: 10.1007/BF00340093. [DOI] [PubMed] [Google Scholar]
  21. JAMIESON J. D., PALADE G. E. SPECIFIC GRANULES IN ATRIAL MUSCLE CELLS. J Cell Biol. 1964 Oct;23:151–172. doi: 10.1083/jcb.23.1.151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. KISCH B. Electronmicroscopy of the frog's heart. Exp Med Surg. 1961;19:104–142. [PubMed] [Google Scholar]
  23. Katz A. M., Repke D. I. Control of myocardial contraction: the sensitivity of cardiac actomyosin to calcium ion. Science. 1966 May 27;152(3726):1242–1243. doi: 10.1126/science.152.3726.1242. [DOI] [PubMed] [Google Scholar]
  24. Kisch B. The ultrastructure of the myocardium of fishes. Exp Med Surg. 1966;24(2):220–227. [PubMed] [Google Scholar]
  25. LUFT J. H. Improvements in epoxy resin embedding methods. J Biophys Biochem Cytol. 1961 Feb;9:409–414. doi: 10.1083/jcb.9.2.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Leak L. V. The ultrastructure of myofibers in a reptilian heart: the boa constrictor. Am J Anat. 1967 May;120(3):553–581. doi: 10.1002/aja.1001200308. [DOI] [PubMed] [Google Scholar]
  27. NAYLER W. G., MERRILLEES N. C. SOME OBSERVATIONS ON THE FINE STRUCTURE AND METABOLIC ACTIVITY OF NORMAL AND GLYCERINATED VENTRICULAR MUSCLE OF TOAD. J Cell Biol. 1964 Sep;22:533–550. doi: 10.1083/jcb.22.3.533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. NELSON D. A., BENSON E. S. On the structural continuities of the transverse tubular system of rabbit and human myocardial cells. J Cell Biol. 1963 Feb;16:297–313. doi: 10.1083/jcb.16.2.297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. NIEDERGERKE R. MOVEMENTS OF CA IN FROG HEART VENTRICLES AT REST AND DURING CONTRACTURES. J Physiol. 1963 Jul;167:515–550. doi: 10.1113/jphysiol.1963.sp007166. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. NIEDERGERKE R. Movements of Ca in beating ventricles of the frog heart. J Physiol. 1963 Jul;167:551–580. doi: 10.1113/jphysiol.1963.sp007167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. REYNOLDS E. S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 1963 Apr;17:208–212. doi: 10.1083/jcb.17.1.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Rayns D. G., Simpson F. O., Bertaud W. S. Transverse tubule apertures in mammalian myocardial cells: surface array. Science. 1967 May 5;156(3775):656–657. doi: 10.1126/science.156.3775.656. [DOI] [PubMed] [Google Scholar]
  33. SABATINI D. D., BENSCH K., BARRNETT R. J. Cytochemistry and electron microscopy. The preservation of cellular ultrastructure and enzymatic activity by aldehyde fixation. J Cell Biol. 1963 Apr;17:19–58. doi: 10.1083/jcb.17.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. SCHAFER D. E., JOHNSON J. A. PERMEABILITY OF MAMMALIAN HEART CAPILLARIES TO SUCROSE AND INULIN. Am J Physiol. 1964 May;206:985–991. doi: 10.1152/ajplegacy.1964.206.5.985. [DOI] [PubMed] [Google Scholar]
  35. SIMPSON F. O., OERTELIS S. J. The fine structure of sheep myocardial cells; sarcolemmal invaginations and the transverse tubular system. J Cell Biol. 1962 Jan;12:91–100. doi: 10.1083/jcb.12.1.91. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. SIMPSON F. O. THE TRANSVERSE TUBULAR SYSTEM IN MAMMALIAN MYOCARDIAL CELLS. Am J Anat. 1965 Jul;117:1–17. doi: 10.1002/aja.1001170102. [DOI] [PubMed] [Google Scholar]
  37. Sandow A. Excitation-contraction coupling in skeletal muscle. Pharmacol Rev. 1965 Sep;17(3):265–320. [PubMed] [Google Scholar]
  38. WEBER A., HERZ R., REISS I. On the mechanism of the relaxing effect of fragmented sarcoplasmic reticulum. J Gen Physiol. 1963 Mar;46:679–702. doi: 10.1085/jgp.46.4.679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. WEBER A., HERZ R., REISS I. THE REGULATION OF MYOFIBRILLAR ACTIVITY BY CALCIUM. Proc R Soc Lond B Biol Sci. 1964 Oct 27;160:489–501. doi: 10.1098/rspb.1964.0063. [DOI] [PubMed] [Google Scholar]
  40. WEBER A., HERZ R. The binding of calcium to actomyosin systems in relation to their biological activity. J Biol Chem. 1963 Feb;238:599–605. [PubMed] [Google Scholar]
  41. WINEGRAD S. The possible role of calcium in excitation-contraction coupling of heart muscle. Circulation. 1961;24:523–529. doi: 10.1161/01.cir.24.2.523. [DOI] [PubMed] [Google Scholar]

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