Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1988 Dec 1;107(6):2587–2600. doi: 10.1083/jcb.107.6.2587

Structural evidence for direct interaction between the molecular components of the transverse tubule/sarcoplasmic reticulum junction in skeletal muscle

PMCID: PMC2115675  PMID: 2849609

Abstract

The architecture of the junctional sarcoplasmic reticulum (SR) and transverse tubule (T tubule) membranes and the morphology of the two major proteins isolated from these membranes, the ryanodine receptor (or foot protein) and the dihydropyridine receptor, have been examined in detail. Evidence for a direct interaction between the foot protein and a protein component of the junctional T tubule membrane is presented. Comparisons between freeze-fracture images of the junctional SR and rotary-shadowed images of isolated triads and of the isolated foot protein, show that the foot protein has two domains. One is the large hydrophilic foot which spans the junctional gap and is composed of four subunits. The other is a hydrophobic domain which presumably forms the SR Ca2+-release channel and which also has a fourfold symmetry. Freeze-fracture images of the junctional T tubule membranes demonstrate the presence of diamond-shaped clusters of particles that correspond exactly in position to the subunits of the feet protein. These results suggest the presence of a large junctional complex spanning the two junctional membranes and intervening gap. This junctional complex is an ideal candidate for a mechanical coupling hypothesis of excitation-contraction coupling at the triadic junction.

Full Text

The Full Text of this article is available as a PDF (7.0 MB).

Selected References

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

  1. Borsotto M., Barhanin J., Fosset M., Lazdunski M. The 1,4-dihydropyridine receptor associated with the skeletal muscle voltage-dependent Ca2+ channel. Purification and subunit composition. J Biol Chem. 1985 Nov 15;260(26):14255–14263. [PubMed] [Google Scholar]
  2. Brandt N. R., Kawamoto R. M., Caswell A. H. Dihydropyridine binding sites on transverse tubules isolated from triads of rabbit skeletal muscle. J Recept Res. 1985;5(2-3):155–170. doi: 10.3109/10799898509041877. [DOI] [PubMed] [Google Scholar]
  3. Campbell K. P., Knudson C. M., Imagawa T., Leung A. T., Sutko J. L., Kahl S. D., Raab C. R., Madson L. Identification and characterization of the high affinity [3H]ryanodine receptor of the junctional sarcoplasmic reticulum Ca2+ release channel. J Biol Chem. 1987 May 15;262(14):6460–6463. [PubMed] [Google Scholar]
  4. Curtis B. M., Catterall W. A. Purification of the calcium antagonist receptor of the voltage-sensitive calcium channel from skeletal muscle transverse tubules. Biochemistry. 1984 May 8;23(10):2113–2118. doi: 10.1021/bi00305a001. [DOI] [PubMed] [Google Scholar]
  5. Fabiato A. Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am J Physiol. 1983 Jul;245(1):C1–14. doi: 10.1152/ajpcell.1983.245.1.C1. [DOI] [PubMed] [Google Scholar]
  6. Ferguson D. G., Schwartz H. W., Franzini-Armstrong C. Subunit structure of junctional feet in triads of skeletal muscle: a freeze-drying, rotary-shadowing study. J Cell Biol. 1984 Nov;99(5):1735–1742. doi: 10.1083/jcb.99.5.1735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fleischer S., Ogunbunmi E. M., Dixon M. C., Fleer E. A. Localization of Ca2+ release channels with ryanodine in junctional terminal cisternae of sarcoplasmic reticulum of fast skeletal muscle. Proc Natl Acad Sci U S A. 1985 Nov;82(21):7256–7259. doi: 10.1073/pnas.82.21.7256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Flockerzi V., Oeken H. J., Hofmann F. Purification of a functional receptor for calcium-channel blockers from rabbit skeletal-muscle microsomes. Eur J Biochem. 1986 Nov 17;161(1):217–224. doi: 10.1111/j.1432-1033.1986.tb10145.x. [DOI] [PubMed] [Google Scholar]
  9. Fosset M., Jaimovich E., Delpont E., Lazdunski M. [3H]nitrendipine receptors in skeletal muscle. J Biol Chem. 1983 May 25;258(10):6086–6092. [PubMed] [Google Scholar]
  10. Franzini-Armstrong C. Freeze-fracture of frog slow tonic fibers. Structure of surface and internal membranes. Tissue Cell. 1984;16(4):647–664. doi: 10.1016/0040-8166(84)90038-7. [DOI] [PubMed] [Google Scholar]
  11. Franzini-Armstrong C., Nunzi G. Junctional feet and particles in the triads of a fast-twitch muscle fibre. J Muscle Res Cell Motil. 1983 Apr;4(2):233–252. doi: 10.1007/BF00712033. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Heuser J. E., Reese T. S., Dennis M. J., Jan Y., Jan L., Evans L. Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release. J Cell Biol. 1979 May;81(2):275–300. doi: 10.1083/jcb.81.2.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hymel L., Inui M., Fleischer S., Schindler H. Purified ryanodine receptor of skeletal muscle sarcoplasmic reticulum forms Ca2+-activated oligomeric Ca2+ channels in planar bilayers. Proc Natl Acad Sci U S A. 1988 Jan;85(2):441–445. doi: 10.1073/pnas.85.2.441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Imagawa T., Smith J. S., Coronado R., Campbell K. P. Purified ryanodine receptor from skeletal muscle sarcoplasmic reticulum is the Ca2+-permeable pore of the calcium release channel. J Biol Chem. 1987 Dec 5;262(34):16636–16643. [PubMed] [Google Scholar]
  16. Inui M., Saito A., Fleischer S. Isolation of the ryanodine receptor from cardiac sarcoplasmic reticulum and identity with the feet structures. J Biol Chem. 1987 Nov 15;262(32):15637–15642. [PubMed] [Google Scholar]
  17. Inui M., Saito A., Fleischer S. Purification of the ryanodine receptor and identity with feet structures of junctional terminal cisternae of sarcoplasmic reticulum from fast skeletal muscle. J Biol Chem. 1987 Feb 5;262(4):1740–1747. [PubMed] [Google Scholar]
  18. Jenden D. J., Fairhurst A. S. The pharmacology of ryanodine. Pharmacol Rev. 1969 Mar;21(1):1–25. [PubMed] [Google Scholar]
  19. Kawamoto R. M., Brunschwig J. P., Kim K. C., Caswell A. H. Isolation, characterization, and localization of the spanning protein from skeletal muscle triads. J Cell Biol. 1986 Oct;103(4):1405–1414. doi: 10.1083/jcb.103.4.1405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kelly D. E., Kuda A. M. Subunits of the triadic junction in fast skeletal muscle as revealed by freeze-fracture. J Ultrastruct Res. 1979 Aug;68(2):220–233. doi: 10.1016/s0022-5320(79)90156-4. [DOI] [PubMed] [Google Scholar]
  21. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  22. Lai F. A., Erickson H. P., Rousseau E., Liu Q. Y., Meissner G. Purification and reconstitution of the calcium release channel from skeletal muscle. Nature. 1988 Jan 28;331(6154):315–319. doi: 10.1038/331315a0. [DOI] [PubMed] [Google Scholar]
  23. Lai F. A., Erickson H., Block B. A., Meissner G. Evidence for a junctional feet-ryanodine receptor complex from sarcoplasmic reticulum. Biochem Biophys Res Commun. 1987 Mar 13;143(2):704–709. doi: 10.1016/0006-291x(87)91411-2. [DOI] [PubMed] [Google Scholar]
  24. Lattanzio F. A., Jr, Schlatterer R. G., Nicar M., Campbell K. P., Sutko J. L. The effects of ryanodine on passive calcium fluxes across sarcoplasmic reticulum membranes. J Biol Chem. 1987 Feb 25;262(6):2711–2718. [PubMed] [Google Scholar]
  25. Leung A. T., Imagawa T., Block B., Franzini-Armstrong C., Campbell K. P. Biochemical and ultrastructural characterization of the 1,4-dihydropyridine receptor from rabbit skeletal muscle. Evidence for a 52,000 Da subunit. J Biol Chem. 1988 Jan 15;263(2):994–1001. [PubMed] [Google Scholar]
  26. Leung A. T., Imagawa T., Campbell K. P. Structural characterization of the 1,4-dihydropyridine receptor of the voltage-dependent Ca2+ channel from rabbit skeletal muscle. Evidence for two distinct high molecular weight subunits. J Biol Chem. 1987 Jun 15;262(17):7943–7946. [PubMed] [Google Scholar]
  27. Meissner G. Ryanodine activation and inhibition of the Ca2+ release channel of sarcoplasmic reticulum. J Biol Chem. 1986 May 15;261(14):6300–6306. [PubMed] [Google Scholar]
  28. Mitchell R. D., Palade P., Fleischer S. Purification of morphologically intact triad structures from skeletal muscle. J Cell Biol. 1983 Apr;96(4):1008–1016. doi: 10.1083/jcb.96.4.1008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Pessah I. N., Francini A. O., Scales D. J., Waterhouse A. L., Casida J. E. Calcium-ryanodine receptor complex. Solubilization and partial characterization from skeletal muscle junctional sarcoplasmic reticulum vesicles. J Biol Chem. 1986 Jul 5;261(19):8643–8648. [PubMed] [Google Scholar]
  31. Peterson G. L. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem. 1977 Dec;83(2):346–356. doi: 10.1016/0003-2697(77)90043-4. [DOI] [PubMed] [Google Scholar]
  32. Rios E., Brum G. Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle. Nature. 1987 Feb 19;325(6106):717–720. doi: 10.1038/325717a0. [DOI] [PubMed] [Google Scholar]
  33. Rousseau E., Smith J. S., Meissner G. Ryanodine modifies conductance and gating behavior of single Ca2+ release channel. Am J Physiol. 1987 Sep;253(3 Pt 1):C364–C368. doi: 10.1152/ajpcell.1987.253.3.C364. [DOI] [PubMed] [Google Scholar]
  34. Saito A., Inui M., Radermacher M., Frank J., Fleischer S. Ultrastructure of the calcium release channel of sarcoplasmic reticulum. J Cell Biol. 1988 Jul;107(1):211–219. doi: 10.1083/jcb.107.1.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Schneider M. F. Membrane charge movement and depolarization-contraction coupling. Annu Rev Physiol. 1981;43:507–517. doi: 10.1146/annurev.ph.43.030181.002451. [DOI] [PubMed] [Google Scholar]
  36. Schwartz L. M., McCleskey E. W., Almers W. Dihydropyridine receptors in muscle are voltage-dependent but most are not functional calcium channels. 1985 Apr 25-May 1Nature. 314(6013):747–751. doi: 10.1038/314747a0. [DOI] [PubMed] [Google Scholar]
  37. Sharp A. H., Imagawa T., Leung A. T., Campbell K. P. Identification and characterization of the dihydropyridine-binding subunit of the skeletal muscle dihydropyridine receptor. J Biol Chem. 1987 Sep 5;262(25):12309–12315. [PubMed] [Google Scholar]
  38. Smith J. S., Coronado R., Meissner G. Single channel measurements of the calcium release channel from skeletal muscle sarcoplasmic reticulum. Activation by Ca2+ and ATP and modulation by Mg2+. J Gen Physiol. 1986 Nov;88(5):573–588. doi: 10.1085/jgp.88.5.573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Smith J. S., Imagawa T., Ma J., Fill M., Campbell K. P., Coronado R. Purified ryanodine receptor from rabbit skeletal muscle is the calcium-release channel of sarcoplasmic reticulum. J Gen Physiol. 1988 Jul;92(1):1–26. doi: 10.1085/jgp.92.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sutko J. L., Ito K., Kenyon J. L. Ryanodine: a modifier of sarcoplasmic reticulum calcium release in striated muscle. Fed Proc. 1985 Dec;44(15):2984–2988. [PubMed] [Google Scholar]
  41. Tanabe T., Takeshima H., Mikami A., Flockerzi V., Takahashi H., Kangawa K., Kojima M., Matsuo H., Hirose T., Numa S. Primary structure of the receptor for calcium channel blockers from skeletal muscle. Nature. 1987 Jul 23;328(6128):313–318. doi: 10.1038/328313a0. [DOI] [PubMed] [Google Scholar]
  42. Unwin N. Is there a common design for cell membrane channels? Nature. 1986 Sep 4;323(6083):12–13. doi: 10.1038/323012a0. [DOI] [PubMed] [Google Scholar]
  43. Vergara J., Tsien R. Y., Delay M. Inositol 1,4,5-trisphosphate: a possible chemical link in excitation-contraction coupling in muscle. Proc Natl Acad Sci U S A. 1985 Sep;82(18):6352–6356. doi: 10.1073/pnas.82.18.6352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Zorzato F., Margreth A., Volpe P. Direct photoaffinity labeling of junctional sarcoplasmic reticulum with [14C]doxorubicin. J Biol Chem. 1986 Oct 5;261(28):13252–13257. [PubMed] [Google Scholar]

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

RESOURCES