Molecular architecture of membranes involved in excitation-contraction coupling of cardiac muscle (original) (raw)

Abstract

Peripheral couplings are junctions between the sarcoplasmic reticulum (SR) and the surface membrane (SM). Feet occupy the SR/SM junctional gap and are identified as the SR calcium release channels, or ryanodine receptors (RyRs). In cardiac muscle, the activation of RyRs during excitation-contraction (e-c) coupling is initiated by surface membrane depolarization, followed by the opening of surface membrane calcium channels, the dihydropyridine receptors (DHPRs). We have studied the disposition of DHPRs and RyRs, and the structure of peripheral couplings in chick myocardium, a muscle that has no transverse tubules. Immunolabeling shows colocalization of RyRs and DHPRs in clusters at the fiber's periphery. The positions of DHPR and RyR clusters change coincidentally during development. Freeze-fracture of the surface membrane reveals the presence of domains (junctional domains) occupied by clusters of large particles. Junctional domains in the surface membrane and arrays of feet in the junctional gap have similar sizes and corresponding positions during development, suggesting that both are components of peripheral couplings. As opposed to skeletal muscle, membrane particles in junctional domains of cardiac muscle do not form tetrads. Thus, despite their proximity to the feet, they do not appear to be specifically associated with them. Two observations establish the identify of the structurally identified feet arrays/junctional domain complexes with the immunocytochemically defined RyRs/DHPRs coclusters: the concomitant changes during development and the identification of feet as the cytoplasmic domains of RyRs. We suggest that the large particles in junctional domains of the surface membrane represent DHPRs. These observations have two important functional consequences. First, the apposition of DHPRs and RyRs indicates that most of the inward calcium current flows into the restricted space where feet are located. Secondly, contrary to skeletal muscle, presumptive DHPRs do not show a specific association with the feet, which is consistent with a less direct role of charge movement in cardiac than in skeletal e-c coupling.

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Selected References

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  1. Airey J. A., Beck C. F., Murakami K., Tanksley S. J., Deerinck T. J., Ellisman M. H., Sutko J. L. Identification and localization of two triad junctional foot protein isoforms in mature avian fast twitch skeletal muscle. J Biol Chem. 1990 Aug 25;265(24):14187–14194. [PubMed] [Google Scholar]
  2. Anderson K., Lai F. A., Liu Q. Y., Rousseau E., Erickson H. P., Meissner G. Structural and functional characterization of the purified cardiac ryanodine receptor-Ca2+ release channel complex. J Biol Chem. 1989 Jan 15;264(2):1329–1335. [PubMed] [Google Scholar]
  3. Bers D. M., Stiffel V. M. Ratio of ryanodine to dihydropyridine receptors in cardiac and skeletal muscle and implications for E-C coupling. Am J Physiol. 1993 Jun;264(6 Pt 1):C1587–C1593. doi: 10.1152/ajpcell.1993.264.6.C1587. [DOI] [PubMed] [Google Scholar]
  4. Block B. A., Imagawa T., Campbell K. P., Franzini-Armstrong C. Structural evidence for direct interaction between the molecular components of the transverse tubule/sarcoplasmic reticulum junction in skeletal muscle. J Cell Biol. 1988 Dec;107(6 Pt 2):2587–2600. doi: 10.1083/jcb.107.6.2587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bossen E. H., Sommer J. R., Waugh R. A. Comparative stereology of the mouse and finch left ventricle. Tissue Cell. 1978;10(4):773–784. doi: 10.1016/0040-8166(78)90062-9. [DOI] [PubMed] [Google Scholar]
  6. Brandt N. R., Caswell A. H., Carl S. A., Ferguson D. G., Brandt T., Brunschwig J. P., Bassett A. L. Detection and localization of triadin in rat ventricular muscle. J Membr Biol. 1993 Feb;131(3):219–228. doi: 10.1007/BF02260110. [DOI] [PubMed] [Google Scholar]
  7. Cannell M. B., Cheng H., Lederer W. J. Spatial non-uniformities in [Ca2+]i during excitation-contraction coupling in cardiac myocytes. Biophys J. 1994 Nov;67(5):1942–1956. doi: 10.1016/S0006-3495(94)80677-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Carl S. L., Felix K., Caswell A. H., Brandt N. R., Ball W. J., Jr, Vaghy P. L., Meissner G., Ferguson D. G. Immunolocalization of sarcolemmal dihydropyridine receptor and sarcoplasmic reticular triadin and ryanodine receptor in rabbit ventricle and atrium. J Cell Biol. 1995 May;129(3):673–682. doi: 10.1083/jcb.129.3.673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Caswell A. H., Brandt N. R., Brunschwig J. P., Purkerson S. Localization and partial characterization of the oligomeric disulfide-linked molecular weight 95,000 protein (triadin) which binds the ryanodine and dihydropyridine receptors in skeletal muscle triadic vesicles. Biochemistry. 1991 Jul 30;30(30):7507–7513. doi: 10.1021/bi00244a020. [DOI] [PubMed] [Google Scholar]
  10. Coronado R., Morrissette J., Sukhareva M., Vaughan D. M. Structure and function of ryanodine receptors. Am J Physiol. 1994 Jun;266(6 Pt 1):C1485–C1504. doi: 10.1152/ajpcell.1994.266.6.C1485. [DOI] [PubMed] [Google Scholar]
  11. De Jongh K. S., Merrick D. K., Catterall W. A. Subunits of purified calcium channels: a 212-kDa form of alpha 1 and partial amino acid sequence of a phosphorylation site of an independent beta subunit. Proc Natl Acad Sci U S A. 1989 Nov;86(21):8585–8589. doi: 10.1073/pnas.86.21.8585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dolber P. C., Sommer J. R. Corbular sarcoplasmic reticulum of rabbit cardiac muscle. J Ultrastruct Res. 1984 May;87(2):190–196. doi: 10.1016/s0022-5320(84)80078-7. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Fleischer S., Inui M. Biochemistry and biophysics of excitation-contraction coupling. Annu Rev Biophys Biophys Chem. 1989;18:333–364. doi: 10.1146/annurev.bb.18.060189.002001. [DOI] [PubMed] [Google Scholar]
  15. Flucher B. E., Morton M. E., Froehner S. C., Daniels M. P. Localization of the alpha 1 and alpha 2 subunits of the dihydropyridine receptor and ankyrin in skeletal muscle triads. Neuron. 1990 Sep;5(3):339–351. doi: 10.1016/0896-6273(90)90170-k. [DOI] [PubMed] [Google Scholar]
  16. Franzini-Armstrong C., Jorgensen A. O. Structure and development of E-C coupling units in skeletal muscle. Annu Rev Physiol. 1994;56:509–534. doi: 10.1146/annurev.ph.56.030194.002453. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Franzini-Armstrong C., Pincon-Raymond M., Rieger F. Muscle fibers from dysgenic mouse in vivo lack a surface component of peripheral couplings. Dev Biol. 1991 Aug;146(2):364–376. doi: 10.1016/0012-1606(91)90238-x. [DOI] [PubMed] [Google Scholar]
  19. Györke S., Palade P. Role of local Ca2+ domains in activation of Ca(2+)-induced Ca2+ release in crayfish muscle fibers. Am J Physiol. 1993 Jun;264(6 Pt 1):C1505–C1512. doi: 10.1152/ajpcell.1993.264.6.C1505. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. Jewett P. H., Sommer J. R., Johnson E. A. Cardiac muscle. Its ultrastructure in the finch and hummingbird with special reference to the sarcoplasmic reticulum. J Cell Biol. 1971 Apr;49(1):50–65. doi: 10.1083/jcb.49.1.50. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Jorgensen A. O., Broderick R., Somlyo A. P., Somlyo A. V. Two structurally distinct calcium storage sites in rat cardiac sarcoplasmic reticulum: an electron microprobe analysis study. Circ Res. 1988 Dec;63(6):1060–1069. doi: 10.1161/01.res.63.6.1060. [DOI] [PubMed] [Google Scholar]
  24. Jorgensen A. O., Shen A. C., Arnold W., Leung A. T., Campbell K. P. Subcellular distribution of the 1,4-dihydropyridine receptor in rabbit skeletal muscle in situ: an immunofluorescence and immunocolloidal gold-labeling study. J Cell Biol. 1989 Jul;109(1):135–147. doi: 10.1083/jcb.109.1.135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Jorgensen A. O., Shen A. C., Arnold W., McPherson P. S., Campbell K. P. The Ca2+-release channel/ryanodine receptor is localized in junctional and corbular sarcoplasmic reticulum in cardiac muscle. J Cell Biol. 1993 Feb;120(4):969–980. doi: 10.1083/jcb.120.4.969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Junker J., Sommer J. R., Sar M., Meissner G. Extended junctional sarcoplasmic reticulum of avian cardiac muscle contains functional ryanodine receptors. J Biol Chem. 1994 Jan 21;269(3):1627–1634. [PubMed] [Google Scholar]
  27. 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]
  28. 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]
  29. Meissner G. Ryanodine receptor/Ca2+ release channels and their regulation by endogenous effectors. Annu Rev Physiol. 1994;56:485–508. doi: 10.1146/annurev.ph.56.030194.002413. [DOI] [PubMed] [Google Scholar]
  30. Niedergerke R., Page S. Receptor-controlled calcium discharge in frog heart cells. Q J Exp Physiol. 1989 Dec;74(7):987–1002. doi: 10.1113/expphysiol.1989.sp003374. [DOI] [PubMed] [Google Scholar]
  31. Näbauer M., Callewaert G., Cleemann L., Morad M. Regulation of calcium release is gated by calcium current, not gating charge, in cardiac myocytes. Science. 1989 May 19;244(4906):800–803. doi: 10.1126/science.2543067. [DOI] [PubMed] [Google Scholar]
  32. Ogawa Y. Role of ryanodine receptors. Crit Rev Biochem Mol Biol. 1994;29(4):229–274. doi: 10.3109/10409239409083482. [DOI] [PubMed] [Google Scholar]
  33. Pozzan T., Rizzuto R., Volpe P., Meldolesi J. Molecular and cellular physiology of intracellular calcium stores. Physiol Rev. 1994 Jul;74(3):595–636. doi: 10.1152/physrev.1994.74.3.595. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Ríos E., Ma J. J., González A. The mechanical hypothesis of excitation-contraction (EC) coupling in skeletal muscle. J Muscle Res Cell Motil. 1991 Apr;12(2):127–135. doi: 10.1007/BF01774031. [DOI] [PubMed] [Google Scholar]
  36. Schneider M. F., Chandler W. K. Voltage dependent charge movement of skeletal muscle: a possible step in excitation-contraction coupling. Nature. 1973 Mar 23;242(5395):244–246. doi: 10.1038/242244a0. [DOI] [PubMed] [Google Scholar]
  37. Sorrentino V., Volpe P. Ryanodine receptors: how many, where and why? Trends Pharmacol Sci. 1993 Mar;14(3):98–103. doi: 10.1016/0165-6147(93)90072-r. [DOI] [PubMed] [Google Scholar]
  38. Stern M. D., Lakatta E. G. Excitation-contraction coupling in the heart: the state of the question. FASEB J. 1992 Sep;6(12):3092–3100. doi: 10.1096/fasebj.6.12.1325933. [DOI] [PubMed] [Google Scholar]
  39. Takahashi M., Catterall W. A. Dihydropyridine-sensitive calcium channels in cardiac and skeletal muscle membranes: studies with antibodies against the alpha subunits. Biochemistry. 1987 Aug 25;26(17):5518–5526. doi: 10.1021/bi00391a046. [DOI] [PubMed] [Google Scholar]
  40. Takekura H., Bennett L., Tanabe T., Beam K. G., Franzini-Armstrong C. Restoration of junctional tetrads in dysgenic myotubes by dihydropyridine receptor cDNA. Biophys J. 1994 Aug;67(2):793–803. doi: 10.1016/S0006-3495(94)80539-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Takekura H., Sun X., Franzini-Armstrong C. Development of the excitation-contraction coupling apparatus in skeletal muscle: peripheral and internal calcium release units are formed sequentially. J Muscle Res Cell Motil. 1994 Apr;15(2):102–118. doi: 10.1007/BF00130422. [DOI] [PubMed] [Google Scholar]
  42. Tanabe T., Beam K. G., Powell J. A., Numa S. Restoration of excitation-contraction coupling and slow calcium current in dysgenic muscle by dihydropyridine receptor complementary DNA. Nature. 1988 Nov 10;336(6195):134–139. doi: 10.1038/336134a0. [DOI] [PubMed] [Google Scholar]
  43. Yoshida A., Takahashi M., Nishimura S., Takeshima H., Kokubun S. Cyclic AMP-dependent phosphorylation and regulation of the cardiac dihydropyridine-sensitive Ca channel. FEBS Lett. 1992 Sep 14;309(3):343–349. doi: 10.1016/0014-5793(92)80804-p. [DOI] [PubMed] [Google Scholar]
  44. Yuan S. H., Arnold W., Jorgensen A. O. 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. 1991 Jan;112(2):289–301. doi: 10.1083/jcb.112.2.289. [DOI] [PMC free article] [PubMed] [Google Scholar]