Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1982 Jun 1;93(3):883–892. doi: 10.1083/jcb.93.3.883

Localization of Ca2+ + Mg2+-ATPase of the sarcoplasmic reticulum in adult rat papillary muscle

PMCID: PMC2112148  PMID: 6749864

Abstract

Localization of the Ca2+ + Mg2+-ATPase of the sarcoplasmic reticulum in rat papillary muscle was determined by indirect immunofluorescence and immunoferritin labeling of cryostat and ultracryotomy sections, respectively. The Ca2+ + Mg2+-ATPase was found to be rather uniformly distributed in the free sarcoplasmic reticulum membrane but to be absent from both peripheral and interior junctional sarcoplasmic reticulum membrane, transverse tubules, sarcolemma, and mitochondria. This suggests that the Ca2+ + Mg2+-ATPase of the sarcoplasmic reticulum is antigenically unrelated to the Ca2+ + Mg2+-ATPase of the sarcolemma. These results are in agreement with the idea that the sites of interior and peripheral coupling between sarcoplasmic reticulum membrane and transverse tubules and between sarcoplasmic reticulum and sarcolemmal membranes play the same functional role in the excitation-contraction coupling in cardiac muscle.

Full Text

The Full Text of this article is available as a PDF (1.3 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson P. A., Manring A., Sommer J. R., Johnson E. A. Cardiac muscle: an attempt to relate structure to function. J Mol Cell Cardiol. 1976 Feb;8(2):123–143. doi: 10.1016/0022-2828(76)90025-0. [DOI] [PubMed] [Google Scholar]
  2. Caroni P., Carafoli E. An ATP-dependent Ca2+-pumping system in dog heart sarcolemma. Nature. 1980 Feb 21;283(5749):765–767. doi: 10.1038/283765a0. [DOI] [PubMed] [Google Scholar]
  3. Caroni P., Carafoli E. The Ca2+-pumping ATPase of heart sarcolemma. Characterization, calmodulin dependence, and partial purification. J Biol Chem. 1981 Apr 10;256(7):3263–3270. [PubMed] [Google Scholar]
  4. DeFoor P. H., Levitsky D., Biryukova T., Fleischer S. Immunological dissimilarity of the calcium pump protein of skeletal and cardiac muscle sarcoplasmic reticulum. Arch Biochem Biophys. 1980 Mar;200(1):196–205. doi: 10.1016/0003-9861(80)90346-x. [DOI] [PubMed] [Google Scholar]
  5. Dhalla N. S., Anand M. B., Harrow J. A. Calcium binding and ATPase activities of heart sarcolemma. J Biochem. 1976 Jun;79(6):1345–1350. doi: 10.1093/oxfordjournals.jbchem.a131188. [DOI] [PubMed] [Google Scholar]
  6. Fabiato A., Fabiato F. Calcium and cardiac excitation-contraction coupling. Annu Rev Physiol. 1979;41:473–484. doi: 10.1146/annurev.ph.41.030179.002353. [DOI] [PubMed] [Google Scholar]
  7. Fawcett D. W., McNutt N. S. The ultrastructure of the cat myocardium. I. Ventricular papillary muscle. J Cell Biol. 1969 Jul;42(1):1–45. doi: 10.1083/jcb.42.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fozzard H. A. Heart: excitation-contraction coupling. Annu Rev Physiol. 1977;39:201–220. doi: 10.1146/annurev.ph.39.030177.001221. [DOI] [PubMed] [Google Scholar]
  9. Harigaya S., Schwartz A. Rate of calcium binding and uptake in normal animal and failing human cardiac muscle. Membrane vesicles (relaxing system) and mitochondria. Circ Res. 1969 Dec;25(6):781–794. doi: 10.1161/01.res.25.6.781. [DOI] [PubMed] [Google Scholar]
  10. Holland P. C. Biosynthesis of the Ca2+- and Mg2+-dependent adenosine triphosphatase of sarcoplasmic reticulum in cell cultures of embryonic chick heart. J Biol Chem. 1979 Aug 25;254(16):7604–7610. [PubMed] [Google Scholar]
  11. Holland P. C., MacLennan D. H. Assembly of the sarcoplasmic reticulum. Biosynthesis of the adenosine triphosphatase in rat skeletal muscle cell culture. J Biol Chem. 1976 Apr 10;251(7):2030–2036. [PubMed] [Google Scholar]
  12. Hui C. W., Drummond M., Drummond G. I. Calcium accumulation and cyclic AMP-stimulated phosphorylation in plasma membrane-enriched preparations of myocardium. Arch Biochem Biophys. 1976 Apr;173(2):415–427. doi: 10.1016/0003-9861(76)90279-4. [DOI] [PubMed] [Google Scholar]
  13. Jones L. R., Besch H. R., Jr, Fleming J. W., McConnaughey M. M., Watanabe A. M. Separation of vesicles of cardiac sarcolemma from vesicles of cardiac sarcoplasmic reticulum. Comparative biochemical analysis of component activities. J Biol Chem. 1979 Jan 25;254(2):530–539. [PubMed] [Google Scholar]
  14. Jones L. R., Besch H. R., Jr, Watanabe A. M. Monovalent cation stimulation of Ca2+ uptake by cardiac membrane vesicles. J Biol Chem. 1977 May 25;252(10):3315–3323. [PubMed] [Google Scholar]
  15. Jorgensen A. O., Kalnins V. I., Zubrzycka E., MacLennan D. H. Assembly of the sarcoplasmic reticulum. Localization by immunofluorescence of sarcoplasmic reticulum proteins in differentiating rat skeletal muscle cell cultures. J Cell Biol. 1977 Jul;74(1):287–298. doi: 10.1083/jcb.74.1.287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Jorgensen A. O., Shen A. C., MacLennan D. H., Tokuyasu K. T. Ultrastructural localization of the Ca2+ + Mg2+-dependent ATPase of sarcoplasmic reticulum in rat skeletal muscle by immunoferritin labeling of ultrathin frozen sections. J Cell Biol. 1982 Feb;92(2):409–416. doi: 10.1083/jcb.92.2.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Jorgensen A. O., Subrahmanyan L., Turnbull C., Kalnins V. I. Localization of the neurofilament protein in neuroblastoma cells by immunofluorescent staining. Proc Natl Acad Sci U S A. 1976 Sep;73(9):3192–3196. doi: 10.1073/pnas.73.9.3192. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kishida Y., Olsen B. R., Berg R. A., Prockop D. J. Two improved methods for preparing ferritin-protein conjugates for electron microscopy. J Cell Biol. 1975 Feb;64(2):331–339. doi: 10.1083/jcb.64.2.331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  21. Langer G. A., Frank J. S., Brady A. J. The myocardium. Int Rev Physiol. 1976;9:191–237. [PubMed] [Google Scholar]
  22. Le Peuch C. J., Haiech J., Demaille J. G. Concerted regulation of cardiac sarcoplasmic reticulum calcium transport by cyclic adenosine monophosphate dependent and calcium--calmodulin-dependent phosphorylations. Biochemistry. 1979 Nov 13;18(23):5150–5157. doi: 10.1021/bi00590a019. [DOI] [PubMed] [Google Scholar]
  23. Levitsky D. O., Aliev M. K., Kuzmin A. V., Levchenko T. S., Smirnov V. N., Chazov E. I. Isolation of calcium pump system and purification of calcium ion-dependent ATPase from heart muscle. Biochim Biophys Acta. 1976 Sep 7;443(3):468–484. doi: 10.1016/0005-2736(76)90466-1. [DOI] [PubMed] [Google Scholar]
  24. Lopaschuk G., Richter B., Katz S. Characterization of calmodulin effects on calcium transport in cardiac microsomes enriched in sarcoplasmic reticulum. Biochemistry. 1980 Nov 25;19(24):5603–5607. doi: 10.1021/bi00565a022. [DOI] [PubMed] [Google Scholar]
  25. MacLennan D. H. Purification and properties of an adenosine triphosphatase from sarcoplasmic reticulum. J Biol Chem. 1970 Sep 10;245(17):4508–4518. [PubMed] [Google Scholar]
  26. McNutt N. S., Fawcett D. W. The ultrastructure of the cat myocardium. II. Atrial muscle. J Cell Biol. 1969 Jul;42(1):46–67. doi: 10.1083/jcb.42.1.46. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Meissner G. Isolation and characterization of two types of sarcoplasmic reticulum vesicles. Biochim Biophys Acta. 1975 Apr 21;389(1):51–68. doi: 10.1016/0005-2736(75)90385-5. [DOI] [PubMed] [Google Scholar]
  28. Morcos N. C., Drummond G. I. (Ca2+ + Mg2+)-ATPase in enriched sarcolemma from dog heart. Biochim Biophys Acta. 1980 May 8;598(1):27–39. doi: 10.1016/0005-2736(80)90263-1. [DOI] [PubMed] [Google Scholar]
  29. PORTER K. R., PALADE G. E. Studies on the endoplasmic reticulum. III. Its form and distribution in striated muscle cells. J Biophys Biochem Cytol. 1957 Mar 25;3(2):269–300. doi: 10.1083/jcb.3.2.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Page E., Surdyk-Droske M. Distribution, surface density, and membrane area of diadic junctional contacts between plasma membrane and terminal cisterns in mammalian ventricle. Circ Res. 1979 Aug;45(2):260–267. doi: 10.1161/01.res.45.2.260. [DOI] [PubMed] [Google Scholar]
  31. Solaro R. J., Briggs F. N. Estimating the functional capabilities of sarcoplasmic reticulum in cardiac muscle. Calcium binding. Circ Res. 1974 Apr;34(4):531–540. doi: 10.1161/01.res.34.4.531. [DOI] [PubMed] [Google Scholar]
  32. Sommer J. R., Waugh R. A. The ultrastructure of the mammalian cardiac muscle cell--with special emphasis on the tubular membrane systems. A review. Am J Pathol. 1976 Jan;82(1):192–232. [PMC free article] [PubMed] [Google Scholar]
  33. St Louis P. J., Sulakhe P. V. Adenosine triphosphate - dependent calcium binding and accumulation by guinea pig cardiac sarcolemma. Can J Biochem. 1976 Nov;54(11):946–956. doi: 10.1139/o76-137. [DOI] [PubMed] [Google Scholar]
  34. Tada M., Yamamoto T., Tonomura Y. Molecular mechanism of active calcium transport by sarcoplasmic reticulum. Physiol Rev. 1978 Jan;58(1):1–79. doi: 10.1152/physrev.1978.58.1.1. [DOI] [PubMed] [Google Scholar]
  35. Tokuyasu K. T. A study of positive staining of ultrathin frozen sections. J Ultrastruct Res. 1978 Jun;63(3):287–307. doi: 10.1016/s0022-5320(78)80053-7. [DOI] [PubMed] [Google Scholar]
  36. Tokuyasu K. T. A technique for ultracryotomy of cell suspensions and tissues. J Cell Biol. 1973 May;57(2):551–565. doi: 10.1083/jcb.57.2.551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Tokuyasu K. T. Immunochemistry on ultrathin frozen sections. Histochem J. 1980 Jul;12(4):381–403. doi: 10.1007/BF01011956. [DOI] [PubMed] [Google Scholar]
  38. Tokuyasu K. T., Singer S. J. Improved procedures for immunoferritin labeling of ultrathin frozen sections. J Cell Biol. 1976 Dec;71(3):894–906. doi: 10.1083/jcb.71.3.894. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Van Winkle W. B., Entman M. L. Comparative aspects of cardiac and skeletal muscle sarcoplasmic reticulum. Life Sci. 1979 Oct 1;25(14):1189–1200. doi: 10.1016/0024-3205(79)90460-0. [DOI] [PubMed] [Google Scholar]
  41. Van Winkle W. B., Pitts B. J., Entman M. L. Rapid purification of canine cardiac sarcoplasmic reticulum Ca2+-ATPase. J Biol Chem. 1978 Dec 25;253(24):8671–8673. [PubMed] [Google Scholar]
  42. Van Winkle W. B. The fenestrated collar of mammalian cardiac sarcoplasmic reticulum: a freeze-fracture study. Am J Anat. 1977 Jun;149(2):277–282. doi: 10.1002/aja.1001490210. [DOI] [PubMed] [Google Scholar]
  43. Wang T., Tsai L. I., Solaro R. J., Grassi de Gende A. O., Schwartz A. Effects of potassium on vanadate inhibition of sarcoplasmic reticulum Ca2+-ATPase from dog cardiac and rabbit skeletal muscle. Biochem Biophys Res Commun. 1979 Nov 14;91(1):356–361. doi: 10.1016/0006-291x(79)90626-0. [DOI] [PubMed] [Google Scholar]
  44. Wendt-Gallitelli M. F., Stöhr P., Wolburg H., Schlote W. Cryoultramicrotomy, electron probe microanalysis and STEM of myocardial tissue. Scan Electron Microsc. 1980;(Pt 2):499–509. [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES