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. 1984 Aug 1;99(2):558–568. doi: 10.1083/jcb.99.2.558

Calcium and magnesium contents and volume of the terminal cisternae in caffeine-treated skeletal muscle

PMCID: PMC2113262  PMID: 6611338

Abstract

(a) The effects of caffeine on the composition and volume of the terminal cisternae (TC) of the sarcoplasmic reticulum (SR) in frog skeletal muscle were determined with rapid freezing, electron microscopy, and electron probe analysis. (b) Caffeine (5 mM) released approximately 65% of the Ca content of the TC in 1 min and 84% after 3 min. The release of Ca from the TC was associated with a highly significant increase in its Mg content. This increase in Mg was not reduced by valinomycin. There was also a small increase in the K content of the TC at 1 min, although not after 3 min of caffeine contracture. (c) On the basis of the increase in Mg content during caffeine contracture and during tetanus (Somlyo, A. V., H. Gonzalez- Serratos, H. Shuman, G. McClellan, and A. P. Somlyo, 1981, J. Cell Biol., 90:577-594), we suggest that both mechanisms of Ca release are associated with an increase in the Ca and Mg permeability of the SR membranes, the two ions possibly moving through a common channel. (d) There was a significant increase in the P content of the TC during caffeine contracture, while in tetanized muscle (see reference above) there was no increase in the P content of the TC. (e) Mitochondrial Ca content was significantly increased (at 1 and at 3 min) during caffeine contracture. Valinomycin (5 microM) blocked this mitochondrial Ca uptake. (f) The sustained Ca release caused by caffeine in situ contrasts with the transient Ca release observed in studies of fragmented SR preparations, and could be explained by mediation of the caffeine-induced Ca release by a second messenger produced more readily in intact muscle than in isolated SR. (g) The TC were not swollen in rapidly frozen, caffeine-treated muscles, in contrast to the swelling of the TC observed in conventionally fixed, caffeine-treated preparation, the latter finding being in agreement with previous studies. (h) The fractional volume of the TC in rapidly frozen control (resting) frog semitendinosus muscles (approximately 2.1%) was less than the volume (approximately 2.5%) after glutaraldehyde-osmium fixation.

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Selected References

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  1. ADRIAN R. H. The effect of internal and external potassium concentration on the membrane potential of frog muscle. J Physiol. 1956 Sep 27;133(3):631–658. doi: 10.1113/jphysiol.1956.sp005615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. AXELSSON J., THESLEFF S. Activation of the contractile mechanism in striated muscle. Acta Physiol Scand. 1958 Oct 28;44(1):55–66. doi: 10.1111/j.1748-1716.1958.tb01608.x. [DOI] [PubMed] [Google Scholar]
  3. Baylor S. M., Chandler W. K., Marshall M. W. Sarcoplasmic reticulum calcium release in frog skeletal muscle fibres estimated from Arsenazo III calcium transients. J Physiol. 1983 Nov;344:625–666. doi: 10.1113/jphysiol.1983.sp014959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bianchi C. P. The Effect of Caffeine on Radiocalcium Movement in Frog Sartorius. J Gen Physiol. 1961 May 1;44(5):845–858. doi: 10.1085/jgp.44.5.845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Birks R. I., Davey D. F. An analysis of volume changes in the T-tubes of frog skeletal muscle exposed to sucrose. J Physiol. 1972 Apr;222(1):95–111. doi: 10.1113/jphysiol.1972.sp009789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Borys H. K., Karler R. Effects of caffeine on the intracellular distribution of calcium in frog sartorius muscle. J Cell Physiol. 1971 Dec;78(3):387–404. doi: 10.1002/jcp.1040780308. [DOI] [PubMed] [Google Scholar]
  7. Brown L. M., Hill L. Mercuric chloride in alcohol and chloroform used as a rapidly acting fixative for contracting muscle fibres. J Microsc. 1982 Mar;125(Pt 3):319–336. doi: 10.1111/j.1365-2818.1982.tb00348.x. [DOI] [PubMed] [Google Scholar]
  8. Burt C. T., Glonek T., Bárány M. Analysis of living tissue by phosphorus-31 magnetic resonance. Science. 1977 Jan 14;195(4274):145–149. doi: 10.1126/science.188132. [DOI] [PubMed] [Google Scholar]
  9. Caputo C. The effect of caffeine and tetracaine on the time course of potassium contractures of single muscle fibres. J Physiol. 1976 Feb;255(1):191–207. doi: 10.1113/jphysiol.1976.sp011275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chiarandini D. J., Reuben J. P., Brandt P. W., Grundfest H. Effects of caffeine on crayfish muscle fibers. I. Activation of contraction and induction of Ca spike electrogenesis. J Gen Physiol. 1970 May;55(5):640–664. doi: 10.1085/jgp.55.5.640. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chiesi M., Ho M. M., Inesi G., Somlyo A. V., Somlyo A. P. Primary role of sarcoplasmic reticulum in phasic contractile activation of cardiac myocytes with shunted myolemma. J Cell Biol. 1981 Dec;91(3 Pt 1):728–742. doi: 10.1083/jcb.91.3.728. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. DYDYNSKA M., WILKIE D. R. THE OSMOTIC PROPERTIES OF STRIATED MUSCLE FIBERS IN HYPERTONIC SOLUTIONS. J Physiol. 1963 Nov;169:312–329. doi: 10.1113/jphysiol.1963.sp007258. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Davey D. F., O'Brien G. M. The sarcoplasmic reticulum and T-system of rat extensor digitorum longus muscles exposed to hypertonic solutions. Aust J Exp Biol Med Sci. 1978 Aug;56(4):409–419. doi: 10.1038/icb.1978.46. [DOI] [PubMed] [Google Scholar]
  14. Eisenberg B. R., Eisenberg R. S. The T-SR junction in contracting single skeletal muscle fibers. J Gen Physiol. 1982 Jan;79(1):1–19. doi: 10.1085/jgp.79.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Eisenberg B. R., Gilai A. Structural changes in single muscle fibers after stimulation at a low frequency. J Gen Physiol. 1979 Jul;74(1):1–16. doi: 10.1085/jgp.74.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Eisenberg B. R., Kuda A. M., Peter J. B. Stereological analysis of mammalian skeletal muscle. I. Soleus muscle of the adult guinea pig. J Cell Biol. 1974 Mar;60(3):732–754. doi: 10.1083/jcb.60.3.732. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Eisenberg B. R., Mobley B. A. Size changes in single muscle fibers during fixation and embedding. Tissue Cell. 1975;7(2):383–387. doi: 10.1016/0040-8166(75)90013-0. [DOI] [PubMed] [Google Scholar]
  18. Endo M. Calcium release from the sarcoplasmic reticulum. Physiol Rev. 1977 Jan;57(1):71–108. doi: 10.1152/physrev.1977.57.1.71. [DOI] [PubMed] [Google Scholar]
  19. Endo M., Tanaka M., Ogawa Y. Calcium induced release of calcium from the sarcoplasmic reticulum of skinned skeletal muscle fibres. Nature. 1970 Oct 3;228(5266):34–36. doi: 10.1038/228034a0. [DOI] [PubMed] [Google Scholar]
  20. Fabiato A., Fabiato F. Calcium release from the sarcoplasmic reticulum. Circ Res. 1977 Feb;40(2):119–129. doi: 10.1161/01.res.40.2.119. [DOI] [PubMed] [Google Scholar]
  21. Fabiato A., Fabiato F. Effects of pH on the myofilaments and the sarcoplasmic reticulum of skinned cells from cardiace and skeletal muscles. J Physiol. 1978 Mar;276:233–255. doi: 10.1113/jphysiol.1978.sp012231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Fairhurst A. S., Hasselbach W. Calcium efflux from a heavy sarcotubular fraction. Effects of ryanodine, caffeine and magnesium. Eur J Biochem. 1970 Apr;13(3):504–509. doi: 10.1111/j.1432-1033.1970.tb00953.x. [DOI] [PubMed] [Google Scholar]
  23. Franzini-Armstrong C., Heuser J. E., Reese T. S., Somlyo A. P., Somlyo A. V. T-tubule swelling in hypertonic solutions: a freeze substitution study. J Physiol. 1978 Oct;283:133–140. doi: 10.1113/jphysiol.1978.sp012492. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Franzini-Armstrong C. STUDIES OF THE TRIAD : I. Structure of the Junction in Frog Twitch Fibers. J Cell Biol. 1970 Nov 1;47(2):488–499. doi: 10.1083/jcb.47.2.488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Franzini-Armstrong C. Structure of sarcoplasmic reticulum. Fed Proc. 1980 May 15;39(7):2403–2409. [PubMed] [Google Scholar]
  26. Franzini-Armstrong C. Studies of the triad. II. Penetration of tracers into the junctional gap. J Cell Biol. 1971 Apr;49(1):196–203. doi: 10.1083/jcb.49.1.196. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Gonzalez-Serratos H., Somlyo A. V., McClellan G., Shuman H., Borrero L. M., Somlyo A. P. Composition of vacuoles and sarcoplasmic reticulum in fatigued muscle: electron probe analysis. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1329–1333. doi: 10.1073/pnas.75.3.1329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hasselbach W., Oetliker H. Energetics and electrogenicity of the sarcoplasmic reticulum calcium pump. Annu Rev Physiol. 1983;45:325–339. doi: 10.1146/annurev.ph.45.030183.001545. [DOI] [PubMed] [Google Scholar]
  29. Ikemoto N., Bhatnagar G. M., Nagy B., Gergely J. Interaction of divalent cations with the 55,000-dalton protein component of the sarcoplasmic reticulum. Studies of fluorescence and circular dichroism. J Biol Chem. 1972 Dec 10;247(23):7835–7837. [PubMed] [Google Scholar]
  30. Jones A. W., Somlyo A. P., Somlyo A. V. Potassium accumulation in smooth muscle and associated ultrastructural changes. J Physiol. 1973 Jul;232(2):247–273. doi: 10.1113/jphysiol.1973.sp010268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Jorgensen A. O., Kalnins V., MacLennan D. H. Localization of sarcoplasmic reticulum proteins in rat skeletal muscle by immunofluorescence. J Cell Biol. 1979 Feb;80(2):372–384. doi: 10.1083/jcb.80.2.372. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Julian F. J., Sollins M. R., Moss R. L. Sarcomere length non-uniformity in relation to tetanic responses of stretched skeletal muscle fibres. Proc R Soc Lond B Biol Sci. 1978 Jan 24;200(1138):109–116. doi: 10.1098/rspb.1978.0009. [DOI] [PubMed] [Google Scholar]
  33. Karp R. D., Silcox J. C., Somlyo A. V. Cryoultramicrotomy: evidence against melting and the use of a low temperature cement for specimen orientation. J Microsc. 1982 Feb;125(Pt 2):157–165. doi: 10.1111/j.1365-2818.1982.tb00333.x. [DOI] [PubMed] [Google Scholar]
  34. Kasai M., Miyamoto H. Depolarization induced calcium release from sarcoplasmic reticulum membrane fragments by changing ionic environment. FEBS Lett. 1973 Aug 15;34(2):299–301. doi: 10.1016/0014-5793(73)80816-6. [DOI] [PubMed] [Google Scholar]
  35. Kitazawa T., Shuman H., Somlyo A. P. Calcium and magnesium binding to thin and thick filaments in skinned muscle fibres: electron probe analysis. J Muscle Res Cell Motil. 1982 Dec;3(4):437–454. doi: 10.1007/BF00712093. [DOI] [PubMed] [Google Scholar]
  36. Kitazawa T., Somlyo A. P., Somlyo A. V. The effects of valinomycin on ion movements across the sarcoplasmic reticulum in frog muscle. J Physiol. 1984 May;350:253–268. doi: 10.1113/jphysiol.1984.sp015199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Kovács L., Szücs G. Effect of caffeine on intramembrane charge movement and calcium transients in cut skeletal muscle fibres of the frog. J Physiol. 1983 Aug;341:559–578. doi: 10.1113/jphysiol.1983.sp014824. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Kumbaraci N. M., Nastuk W. L. Action of caffeine in excitation-contraction coupling of frog skeletal muscle fibres. J Physiol. 1982 Apr;325:195–211. doi: 10.1113/jphysiol.1982.sp014145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Loud A. V. A quantitative stereological description of the ultrastructure of normal rat liver parenchymal cells. J Cell Biol. 1968 Apr;37(1):27–46. doi: 10.1083/jcb.37.1.27. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Miyamoto H., Racker E. Mechanism of calcium release from skeletal sarcoplasmic reticulum. J Membr Biol. 1982;66(3):193–201. doi: 10.1007/BF01868494. [DOI] [PubMed] [Google Scholar]
  41. Mobley B. A., Eisenberg B. R. Sizes of components in frog skeletal muscle measured by methods of stereology. J Gen Physiol. 1975 Jul;66(1):31–45. doi: 10.1085/jgp.66.1.31. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Moisescu D. G., Thieleczek R. Calcium and strontium concentration changes within skinned muscle preparations following a change in the external bathing solution. J Physiol. 1978 Feb;275:241–262. doi: 10.1113/jphysiol.1978.sp012188. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Oetliker H. An appraisal of the evidence for a sarcoplasmic reticulum membrane potential and its relation to calcium release in skeletal muscle. J Muscle Res Cell Motil. 1982 Sep;3(3):247–272. doi: 10.1007/BF00713037. [DOI] [PubMed] [Google Scholar]
  44. Ogawa Y., Ebashi S. Ca-releasing action of beta, gamma-methylene adenosine triphosphate on fragmented sarcoplasmic reticulum. J Biochem. 1976 Nov;80(5):1149–1157. doi: 10.1093/oxfordjournals.jbchem.a131370. [DOI] [PubMed] [Google Scholar]
  45. Ogawa Y. Some properties of fragmented frog sarcoplasmic reticulum with particular reference to its response to caffeine. J Biochem. 1970 May;67(5):667–683. doi: 10.1093/oxfordjournals.jbchem.a129295. [DOI] [PubMed] [Google Scholar]
  46. PAGE S. G., HUXLEY H. E. FILAMENT LENGTHS IN STRIATED MUSCLE. J Cell Biol. 1963 Nov;19:369–390. doi: 10.1083/jcb.19.2.369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Peachey L. D. The sarcoplasmic reticulum and transverse tubules of the frog's sartorius. J Cell Biol. 1965 Jun;25(3 Suppl):209–231. doi: 10.1083/jcb.25.3.209. [DOI] [PubMed] [Google Scholar]
  48. Sakai T., Geffner E. S., Sandow A. Caffeine contracture in muscle with disrupted transverse tubules. Am J Physiol. 1971 Mar;220(3):712–717. doi: 10.1152/ajplegacy.1971.220.3.712. [DOI] [PubMed] [Google Scholar]
  49. Sakai T., Yoshioka T. Studies on rapid cooling contracture of frog toe mucle immersed in hypertonic and hypotonic solutions. Jpn J Physiol. 1973 Apr;23(2):135–147. doi: 10.2170/jjphysiol.23.135. [DOI] [PubMed] [Google Scholar]
  50. Shuman H., Somlyo A. V., Somlyo A. P. Quantitative electron probe microanalysis of biological thin sections: methods and validity. Ultramicroscopy. 1976 Sep-Oct;1(4):317–339. doi: 10.1016/0304-3991(76)90049-8. [DOI] [PubMed] [Google Scholar]
  51. Somlyo A. P., Somlyo A. V., Shuman H. Electron probe analysis of vascular smooth muscle. Composition of mitochondria, nuclei, and cytoplasm. J Cell Biol. 1979 May;81(2):316–335. doi: 10.1083/jcb.81.2.316. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Somlyo A. P., Somlyo A. V., Shuman H., Endo M. Calcium and monovalent ions in smooth muscle. Fed Proc. 1982 Oct;41(12):2883–2890. [PubMed] [Google Scholar]
  53. Somlyo A. V. Bridging structures spanning the junctioning gap at the triad of skeletal muscle. J Cell Biol. 1979 Mar;80(3):743–750. doi: 10.1083/jcb.80.3.743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Somlyo A. V., Gonzalez-Serratos H. G., Shuman H., McClellan G., Somlyo A. P. Calcium release and ionic changes in the sarcoplasmic reticulum of tetanized muscle: an electron-probe study. J Cell Biol. 1981 Sep;90(3):577–594. doi: 10.1083/jcb.90.3.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Somlyo A. V., Shuman H., Somlyo A. P. Elemental distribution in striated muscle and the effects of hypertonicity. Electron probe analysis of cryo sections. J Cell Biol. 1977 Sep;74(3):828–857. doi: 10.1083/jcb.74.3.828. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Spurr A. R. A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res. 1969 Jan;26(1):31–43. doi: 10.1016/s0022-5320(69)90033-1. [DOI] [PubMed] [Google Scholar]
  57. Stephenson E. W. Ca2+ dependence of stimulated 45Ca efflux in skinned muscle fibers. J Gen Physiol. 1981 Apr;77(4):419–443. doi: 10.1085/jgp.77.4.419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Stephenson E. W. Properties of chloride-stimulated 45Ca flux in skinned muscle fibers. J Gen Physiol. 1978 Apr;71(4):411–430. doi: 10.1085/jgp.71.4.411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Su J. Y., Hasselbach W. Caffeine-induced calcium release from isolated sarcoplasmic reticulum of rabbit skeletal muscle. Pflugers Arch. 1984 Jan;400(1):14–21. doi: 10.1007/BF00670530. [DOI] [PubMed] [Google Scholar]
  60. Suarez-Kurtz G. Caffeine and quinine increase the release of sarcoplasmic enzymes from frog skeletal muscles. Braz J Med Biol Res. 1982 Apr;15(1):61–64. [PubMed] [Google Scholar]
  61. Uhrík B., Zacharová D. Recovery of ultrastructural changes accompanying caffeine contractures in isolated muscle fibres of the crayfish. Pflugers Arch. 1976 Jul 30;364(2):183–190. doi: 10.1007/BF00585188. [DOI] [PubMed] [Google Scholar]
  62. VANHARREVELD A., CROWELL J. ELECTRON MICROSCOPY AFTER RAPID FREEZING ON A METAL SURFACE AND SUBSTITUTION FIXATION. Anat Rec. 1964 Jul;149:381–385. doi: 10.1002/ar.1091490307. [DOI] [PubMed] [Google Scholar]
  63. VANHARREVELD A., CROWELL J., MALHOTRA S. K. A STUDY OF EXTRACELLULAR SPACE IN CENTRAL NERVOUS TISSUE BY FREEZE-SUBSTITUTION. J Cell Biol. 1965 Apr;25:117–137. doi: 10.1083/jcb.25.1.117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Weber A., Herz R. The relationship between caffeine contracture of intact muscle and the effect of caffeine on reticulum. J Gen Physiol. 1968 Nov;52(5):750–759. doi: 10.1085/jgp.52.5.750. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Weber A. The mechanism of the action of caffeine on sarcoplasmic reticulum. J Gen Physiol. 1968 Nov;52(5):760–772. doi: 10.1085/jgp.52.5.760. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Weibel E. R. A stereological method for estimating volume and surface of sarcoplasmic reticulum. J Microsc. 1972 Apr;95(2):229–242. doi: 10.1111/j.1365-2818.1972.tb03722.x. [DOI] [PubMed] [Google Scholar]
  67. Yoshioka T., Ohmori K., Sakai T. Ultrastructural features of the sarcoplasmic reticulum during rapid cooling contracture and tetanus in frog skeletal muscle. Jpn J Physiol. 1981;31(1):29–42. doi: 10.2170/jjphysiol.31.29. [DOI] [PubMed] [Google Scholar]
  68. Yoshioka T. Width of the junctional gap of the triad of various sarcomere lengths in frog skeletal muscle. Jpn J Physiol. 1982;32(3):475–479. doi: 10.2170/jjphysiol.32.475. [DOI] [PubMed] [Google Scholar]

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