The Sarcoplasmic Reticulum of Skeletal Muscle: A Look from Inside

  • Pompeo Volpe
  • Adelina Martini
  • Alessandra Nori
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 311)


The sarcoplasmic reticulum (SR), the membrane-bound calcium store of skeletal muscle, controls the contraction-relaxation cycle by raising and lowering the myoplasmic free calcium concentration, and consists of two continuous yet distinct regions, the free or non-junctional SR and the junctional SR, i.e., the area of terminal cisternae (TC) directly facing the transverse tubules (Costello et al., 1986; Fleischer and Inui, 1989).


Sarcoplasmic Reticulum Calcium Binding Calcium Binding Protein Ryanodine Receptor Calcium Pump 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Blount, P. and L.J.P. Merlie, 1991, BiP associates with newly synthesized subunits of the mouse nicotinic receptor, J. Cell Biol.,113: 1125.PubMedCrossRefGoogle Scholar
  2. Bole, D.G., L.M. Hendershot and J.F. Kenney, 1986, Posttranslational association of immunoglobulin heavy chain binding proteins with nascent heavy chains in non secreting and secreting hybridomas. J. Cell Biol., 102: 1558.PubMedCrossRefGoogle Scholar
  3. Bole, D.G., R. Down, M. Doriaux and J.J. Jamieson, 1990, Immunocytochemical localization of BiP to the rough endoplasmic reticulum: evidence for protein sorting by selective retention. J. Histochem. Cytochem., 37: 1817.CrossRefGoogle Scholar
  4. Cala, S.E. and L.R. Jones, 1983, Rapid purification of calsequestrin from cardiac and skeletal muscle sarcoplasmic reticulum vesicles by Ca2+ -dependent elution from phenyl-Sepharose. J. Biol. Chem., 258: 11932.PubMedGoogle Scholar
  5. Cala, S.E. and L.R. Jones, 1991, Phosphorylation of cardiac and skeletal muscle calsequestrin isoforms by casein kinase II. J. Biol. Chem., 266: 391.PubMedGoogle Scholar
  6. Cala, S.E., B.T. Scott and L.R. Jones, 1990, Intraluminal sarcoplasmic reticulum Ca2+-binding proteins. Sem. Cell Biol., 1: 265.Google Scholar
  7. Chiesi, M. and E. Carafoli, 1982, The regulation of Ca2+ transport by rat skeletal muscle sarcoplasmic reticulum. Role of calmodulin and the 53,000 dalton glycoprotein. J. Biol. Chem., 257: 984PubMedGoogle Scholar
  8. Costello B., C. Chadwick, A. Saito, A. Chu, A. Maurer and S. Fleischer, 1986, Characterization of the junctional face membrane of terminal cisternae of sarcoplasmic reticulum. J. Cell Biol., 103: 741.PubMedCrossRefGoogle Scholar
  9. Damiani, E., and A. Margreth, 1990, Specific protein-protein interactions of calsequestrin with junctional sarcoplasmic reticulum of skeletal muscle. Biochem. Biophys. Res. Commun., 172: 1253.PubMedCrossRefGoogle Scholar
  10. Damiani, E. and A. Margreth, 1991, Subcellular fractionation to junctional sarcoplasmic reticulum and biochemical characterization of the 170 kDa Ca2+- and LDL-binding protein in rabbit skeletal muscle. Biochem. J., in press.Google Scholar
  11. Damiani, E., P. Volpe and A. Margreth, 1990, Coexpression of two isoforms of calsequestrin in rabbit slow-twitch muscle. J. Muscle Res. Cell Motil., 11: 522.PubMedCrossRefGoogle Scholar
  12. Earnshaw, W.C., 1987, Anionic regions in nuclear proteins. J. Cell Biol., 105:1479.PubMedCrossRefGoogle Scholar
  13. Ezerman, E.B. and H. Ishikawa, 1967, Differentiation of the sarcoplasmic reticulum and T-system in developing chick skeletal muscle in vitro. J. Cell Biol., 35: 405.PubMedCrossRefGoogle Scholar
  14. Fambrough, D.M. and P.N. Devreotes, 1978, Newly synthesized acetylcholine receptors are located in the Golgi apparatus. J. Cell Biol., 76: 237.PubMedCrossRefGoogle Scholar
  15. Fleischer, S. and M. Inui, 1989, Biochemistry and biophysics of excitation-contraction coupling. Annu. Rev. Piophys, Biophys, Chem., 18: 333.CrossRefGoogle Scholar
  16. Fliegel, L., K. Burns, M. Opas and M. Michalak, 1989a, The high-affinity calcium binding protein of sarcoplasmic reticulum. Tissue distribution and homology with calregulin. Biochim. Biophys. Acta. 982: 1.CrossRefGoogle Scholar
  17. Fliegel, L., E. Leberer, N.M. Green and D.H. MacLennan, 1989b, The fast-twitch muscle calsequestrin isoform predominates in rabbit slow-twitch soleus muscle. FEB3 Lett., 242: 297.CrossRefGoogle Scholar
  18. Fliegel, L., K. Burns, D.H. MacLennan, R.A.F. Reithmeier and M. Michalak, 1989c, Molecular cloning of the high affinity calcium binding protein (calreticulin) of skeletal muscle sarcoplasmic reticulum. J. Biol. Chem., 264: 21522.Google Scholar
  19. Fliegel, L., E. Newton, K. Burns and M. Michalak, 1990, Molecular cloning of cDNA encoding a 55-KDa multifunctional thyroid hormone binding protein of skeletal muscle sarcoplasmic reticulum. J. Biol. Chem., 265: 15496.PubMedGoogle Scholar
  20. Fliegel, L., M. Ohnishi, M.R. Carpenter, V.H. Khanna, A.F. Reinhart, R.A.F Reithmeier and D.H. MacLennan, 1987, Amino acid sequence of rabbit fast-twitch skeletal muscle calsequestrin deduced from cDNA and peptide sequencing. Proc. Natl. Acad. Sci. (USA), 84: 1167.CrossRefGoogle Scholar
  21. Franzini-Armstrong, C., L.J. Kenney and E. Varriano-Marston, 1987, The structure of calsequestrin in triads of vertebrate skeletal muscle: a deep-etch study. J. Cell Biol., 105: 49.PubMedCrossRefGoogle Scholar
  22. Gething, M.-J. and J. Sambrook, 1990, Transport and assembly processes in the endoplasmic reticulum. Sem. Cell Biol., 1: 65.Google Scholar
  23. Hofmann, S.L., M.S. Brown, E. Lee, R.K. Pathak, R.G.W. Anderson and J.L. Goldstein, 1989a, Purification of a sarcoplasmic reticulum protein that binds calcium and plasma lipoproteins. J. Biol. Chem., 264: 8260.Google Scholar
  24. Hofmann, S.L., J.L. Goldstein, K. Orth, C.R. Moorman, C.A. Slaughter and M.S. Brown, 1989b, Molecular cloning of histidine-rich calcium binding protein of sarcoplasmic reticulum that contains highly conserved repeated elements. J. Biol. Chem., 264: 18083.Google Scholar
  25. Ikemoto, N., M. Ronjat, L.G. Meszaros and M. Koshita, 1989, Postulated role of calsequestrin in the regulation of calcium release from sarcoplasmic reticulum. Biochemistry, 28: 6764.PubMedCrossRefGoogle Scholar
  26. Koch, G.L.E., 1987, Reticuloplasmins: a novel group of proteins in the endoplasmic reticulum. J. Cell Sci., 87: 491.PubMedGoogle Scholar
  27. Leberer, E., J.M.H Charuk, N.M. Green and D.H. MacLennan, 1989a, Molecular cloning and expression of cDNA encoding a lumenal calcium binding glycoprotein from sarcoplasmic reticulum. Proc. Natl. Acad. Sci., (USA). 86: 6047.CrossRefGoogle Scholar
  28. Leberer, E., J.M.H. Charuk, D.M. Clarke, N.M. Green, E. Zubrzycka-Gaarn and D.H. MacLennan, 1989b, Molecular cloning and expression of cDNA encoding the 53,000-dalton glycoprotein of rabbit skeletal muscle sarcoplasmic reticulum. J. Biol. Chem., 264: 3484.Google Scholar
  29. Leberer, E., B.G. Timms, K.P. Campbell and D.H. MacLennan, 1990, Purification, calcium binding properties, and ultrastructural localization of the 53,000 and 160,000 (sarcalumenin) dalton glycoproteins of sarcoplasmic reticulum. J. Biol. Chem., 265: 10118.PubMedGoogle Scholar
  30. Leonards, K.S. and H. Kutchai, 1985, Coupling of Ca2+ transport to ATP hydrolysis by the Ca2+-ATPase of sarcoplasmic reticulum. Potential role of the 53-Kilodalton glycoprotein. Biochemistry. 24: 4876.PubMedCrossRefGoogle Scholar
  31. Macer, D.R.J, and G.L.E. Koch, 1988, Identification of a set of calcium-binding proteins in reticuloplasm, the luminal content of the endoplasmic reticulum. J. Cell Sci., 91: 61.PubMedGoogle Scholar
  32. MacLennan, D.H. and P.T.S. Wong, 1971, Isolation of a calcium-sequestering protein from sarcoplasmic reticulum. Proc. Natl. Acad. Sci. (USA). 68: 1231.CrossRefGoogle Scholar
  33. MacLennan, D.H., C.J. Brandl, B. Korczak and N.M. Green, 1985, Amino acid sequence of a Ca2++Mg2+-dependent ATPase from rabbit muscle sarcoplasmic reticulum, deduced from its complementary DNA sequence. Nature (London). 316: 699.CrossRefGoogle Scholar
  34. MacLennan, D.H., K.P. Campbell and R.A.F Reithmeier, 1983, in: “Calcium and Cell Function:, Chung, W.Y. ed., Academic Press, New York, pp. 151–173.Google Scholar
  35. Maylie, J., M. Irving, N. Leung Sizto, G. Boyarsky and W.K Chandler, 1987, Calcium signals recorded from cut frog twitch fibers containing tetramethylmurexide. J. Gen. Physiol., 89: 145.PubMedCrossRefGoogle Scholar
  36. Mitchell, R.D., H.K.B. Simmerman and L.R. Jones, 1988, Calcium binding effects on protein conformation and protein interactions of canine cardiac calsequestrin. J. Biol. Chem., 263: 1376.PubMedGoogle Scholar
  37. Munro, S. and H.R.B. Pelham, 1987, A C-terminal signal prevents secretion of luminal ER proteins. Cell, 48: 899.PubMedCrossRefGoogle Scholar
  38. Nelson, T.E. and K. Nelson, 1990, Intra- and extraluminal sarcoplasmic reticulum membrane regulatory sites for Ca2+-induced Ca2+ release. FEBS Lett., 263: 292.PubMedCrossRefGoogle Scholar
  39. Ostwald, T.J. and D.H MacLennan, 1974, Isolation of a high affinity calcium-binding protein from sarcoplasmic reticulum. J. Biol. Chem., 249: 974.PubMedGoogle Scholar
  40. Porter, K.R. and G.E. Palade, 1957, Studies on the sarcoplasmic reticulum. III. Its form and distribution in striated muscle cells. J. Biophys. Biochem. Cytol., 3: 269.PubMedCrossRefGoogle Scholar
  41. Saito, A., S. Seiler, A. Chu and S. Fleischer, 1984, Preparation and morphology of terminal cisternae from rabbit skeletal muscle. J. Cell Biol., 99: 875.PubMedCrossRefGoogle Scholar
  42. Sambrook, J.F., 1990, The involvement of calcium in transport of secretory proteins from the endoplasmic reticulum. Cell, 61: 197.PubMedCrossRefGoogle Scholar
  43. Schiaffino, S. and A. Margreth, 1969, Coordinated development of the sarcoplasmic reticulum and T system during postnatal differentiation of rat skeletal muscle. J. Cell Biol., 41: 855.PubMedCrossRefGoogle Scholar
  44. Scott, B.T., H.K.B. Simmerman, J.H. Collins, B. Nadal-Ginard and LR. Jones, 1988, Complete amino acid sequence of canine cardiac calsequestrin deduced by cDNA cloning. J. Biol. Chem., 263: 8958.PubMedGoogle Scholar
  45. Smith, M.J. and Koch, G.L.E., 1989, Multiple zones in the sequence of calreticulin (CRP 55, calregulin, HACBP) a major calcium binding ER/SR protein. EMBO J., 8: 3581.PubMedGoogle Scholar
  46. Takeshima, H., S. Nishimura, T. Matsumoto, H. Ishida, K. Kangawa, N. Minamino, H. Matsuo, M. Ueda, M. Hanaoka, T. Hirose and S. Numa, 1989, Primary structure and expression from complementary DNA of skeletal muscle ryanodine receptor. Nature (London). 339: 439.CrossRefGoogle Scholar
  47. Thomas, K., J. Navarro, R.J.J. Benson, K.P. Campbell, R.L. Rotundo and R.E. Fine, 1989, Newly synthesized calsequestrin, destined for the sarcoplasmic reticulum, is contained in early/intermediate Golgi-derived clathrin-coated vesicles. J. Biol. Chem., 264: 3140.PubMedGoogle Scholar
  48. Tooze, J., M. Hollinshead, S.D. Fuller, S.A. Tooze and W.B. Huttner, 1989, Morphological and biochemical properties in AtT-20 cells and their growth cones. Eur. J. Cell Biol., 49: 259.PubMedGoogle Scholar
  49. Valdivia, C., H. Valdivia, J. Vilven and R. Coronado, 1989, Proton gating of calcium release channels in vesicles derived from junctional sarcoplasmic reticulum. Biophys. J., 55: 88a.Google Scholar
  50. Villa, A., P. Podini, D.O. Clegg, T. Pozzan and J. Meldolesi, 1991, Intracellular Ca2+ stores in chicken Purkinje neurons: differential distribution of the low affinity-high capacity calcium binding protein, calsequestrin, of Ca2+ ATPase and of the ER lumenal protein, BiP. J. Cell Biol., 113: 779.PubMedCrossRefGoogle Scholar
  51. Volpe, P., 1989, The unraveling architecture of the junctional sarcoplasmic reticulum. J. Bioenerg. Biomem., 21: 215.CrossRefGoogle Scholar
  52. Volpe, P. and B.J. Simon, 1991, The bulk of calcium released to the myoplasm is free in the sarcoplasmic reticulum and does not unbind from calsequestrin. FEBS Lett., 278: 274.PubMedCrossRefGoogle Scholar
  53. Volpe, P., H.E. Gutweniger and C. Montecucco, 1987, Photolabeling of integral proteins of skeletal muscle sarcoplasmic reticulum. Comparison of junctional and non-junctional membrane fractions. Arch. Biochem. Biophys., 253: 138.PubMedCrossRefGoogle Scholar
  54. Volpe, P., B.H. Alderson-Lang, L. Madeddu, E. Damiani, J.H. Collins and A. Margreth, 1990, Calsequestrin a component of the inositol 1,4,5-trisphosphate-sensitive Ca2+ store of chicken cerebellum. Neuron, 5: 713.PubMedCrossRefGoogle Scholar
  55. Waisman, D.M., B.P. Salimath and M.J. Anderson, 1985, Isolation and characterization of CAB-63, a novel calcium-binding protein. J. Biol. Chem., 260: 1652.PubMedGoogle Scholar
  56. Yuan, S., W. Arnold and A.O. Jorgensen, 1991, Biogenesis of transverse tubules and triads: immunolocalization of the 1,4-dihydropyridine receptor, TS28, and the ryanodine receptor in rabbit skeletal muscle developing in situ. J. Cell Biol., 112: 289.PubMedCrossRefGoogle Scholar
  57. Zorzato, F. and P. Volpe, 1988, Calcium binding proteins of junctional sarcoplasmic reticulum. Detection by Ca2+ ligand overlay. Arch. Biochem Biophys., 261: 324.PubMedCrossRefGoogle Scholar
  58. Zorzato, F., J. Fujii, K. Otsu, M. Phillips, N.M. Green, F.A. Lai, G. Meissner and D.H. MacLennan, 1990, Molecular cloning of cDNA encoding human and rabbit forms of the Ca2+ release channel (ryanodine receptor) of skeletal muscle sarcoplasmic reticulum. J. Biol. Chem., 265: 2244.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1992

Authors and Affiliations

  • Pompeo Volpe
    • 1
  • Adelina Martini
    • 1
  • Alessandra Nori
    • 1
  1. 1.Centro di Studio per la Biologia e Fisiopatologia Muscolare del CNR, Istituto di Patologia GeneraleUniversita’ degli Studi di PadovaPadovaItaly

Personalised recommendations