Abstract
The relative disposition of ryanodine receptors (RyRs) and L-type Ca(2+) channels was examined in body muscles from three arthropods. In all muscles the disposition of ryanodine receptors in the junctional gap between apposed SR and T tubule elements is highly ordered. By contrast, the junctional membrane of the T tubule is occupied by distinctive large particles that are clustered within the small junctional domain, but show no order in their arrangement. We propose that the large particles of the junctional T tubules represent L-type Ca(2+) channels involved in excitation-contraction (e-c) coupling, based on their similarity in size and location with the L-type Ca(2+) channels or dihydropyridine receptors (DHPRs) of skeletal and cardiac muscle. The random arrangement of DHPRs in arthropod body muscles indicates that there is no close link between them and RyRs. This matches the architecture of vertebrate cardiac muscle and is in keeping with the similarity in e-c coupling mechanisms in cardiac and invertebrate striated muscles.
Full Text
The Full Text of this article is available as a PDF (1.8 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Adams B. A., Tanabe T., Mikami A., Numa S., Beam K. G. Intramembrane charge movement restored in dysgenic skeletal muscle by injection of dihydropyridine receptor cDNAs. Nature. 1990 Aug 9;346(6284):569–572. doi: 10.1038/346569a0. [DOI] [PubMed] [Google Scholar]
- Araque A., Clarac F., Buño W. P-type Ca2+ channels mediate excitatory and inhibitory synaptic transmitter release in crayfish muscle. Proc Natl Acad Sci U S A. 1994 May 10;91(10):4224–4228. doi: 10.1073/pnas.91.10.4224. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bers D. M. Ca regulation in cardiac muscle. Med Sci Sports Exerc. 1991 Oct;23(10):1157–1162. [PubMed] [Google Scholar]
- 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]
- Branton D. Fracture faces of frozen membranes. Proc Natl Acad Sci U S A. 1966 May;55(5):1048–1056. doi: 10.1073/pnas.55.5.1048. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Carl S. L., Felix K., Caswell A. H., Brandt N. R., Brunschwig J. P., Meissner G., Ferguson D. G. Immunolocalization of triadin, DHP receptors, and ryanodine receptors in adult and developing skeletal muscle of rats. Muscle Nerve. 1995 Nov;18(11):1232–1243. doi: 10.1002/mus.880181104. [DOI] [PubMed] [Google Scholar]
- Castellote J., Araque A., Buño W. Sustained GABA-induced regulation of the L-type Ca2+ conductance in crustacean muscle fibers. Pflugers Arch. 1997 Jul;434(3):272–279. doi: 10.1007/s004240050396. [DOI] [PubMed] [Google Scholar]
- 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]
- Eastwood A. B., Franzini-Armstrong C., Peracchia C. Structure of membranes in crayfish muscle: comparison of phasic and tonic fibres. J Muscle Res Cell Motil. 1982 Sep;3(3):273–294. doi: 10.1007/BF00713038. [DOI] [PubMed] [Google Scholar]
- Ebashi S. Excitation-contraction coupling and the mechanism of muscle contraction. Annu Rev Physiol. 1991;53:1–16. doi: 10.1146/annurev.ph.53.030191.000245. [DOI] [PubMed] [Google Scholar]
- Erxleben C., Rathmayer W. A dihydropyridine-sensitive voltage-dependent calcium channel in the sarcolemmal membrane of crustacean muscle. J Gen Physiol. 1997 Mar;109(3):313–326. doi: 10.1085/jgp.109.3.313. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Flucher B. E., Andrews S. B., Fleischer S., Marks A. R., Caswell A., Powell J. A. Triad formation: organization and function of the sarcoplasmic reticulum calcium release channel and triadin in normal and dysgenic muscle in vitro. J Cell Biol. 1993 Dec;123(5):1161–1174. doi: 10.1083/jcb.123.5.1161. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Flucher B. E., Phillips J. L., Powell J. A. Dihydropyridine receptor alpha subunits in normal and dysgenic muscle in vitro: expression of alpha 1 is required for proper targeting and distribution of alpha 2. J Cell Biol. 1991 Dec;115(5):1345–1356. doi: 10.1083/jcb.115.5.1345. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Formelová J., Hurnák O., Novotová M., Zachar J. Ryanodine receptor purified from crayfish skeletal muscle. Gen Physiol Biophys. 1990 Oct;9(5):445–453. [PubMed] [Google Scholar]
- Franzini-Armstron C. Freeze fracture of skeletal muscle from the Tarantula spider. Structural differentiations of sarcoplasmic reticulum and transverse tubular system membranes. J Cell Biol. 1974 May;61(2):501–513. doi: 10.1083/jcb.61.2.501. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Franzini-Armstrong C., Eastwood A. B., Peachey L. D. Shape and disposition of clefts, tubules, and sarcoplasmic reticulum in long and short sarcomere fibers of crab and crayfish. Cell Tissue Res. 1986;244(1):9–19. doi: 10.1007/BF00218376. [DOI] [PubMed] [Google Scholar]
- Franzini-Armstrong C., Kish J. W. Alternate disposition of tetrads in peripheral couplings of skeletal muscle. J Muscle Res Cell Motil. 1995 Jun;16(3):319–324. doi: 10.1007/BF00121140. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Franzini-Armstrong C., Protasi F. Ryanodine receptors of striated muscles: a complex channel capable of multiple interactions. Physiol Rev. 1997 Jul;77(3):699–729. doi: 10.1152/physrev.1997.77.3.699. [DOI] [PubMed] [Google Scholar]
- Gathercole D. V., Colling D. J., Skepper J. N., Takagishi Y., Levi A. J., Severs N. J. Immunogold-labeled L-type calcium channels are clustered in the surface plasma membrane overlying junctional sarcoplasmic reticulum in guinea-pig myocytes-implications for excitation-contraction coupling in cardiac muscle. J Mol Cell Cardiol. 2000 Nov;32(11):1981–1994. doi: 10.1006/jmcc.2000.1230. [DOI] [PubMed] [Google Scholar]
- Gielow M. L., Gu G. G., Singh S. Resolution and pharmacological analysis of the voltage-dependent calcium channels of Drosophila larval muscles. J Neurosci. 1995 Sep;15(9):6085–6093. doi: 10.1523/JNEUROSCI.15-09-06085.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gilly W. F., Scheuer T. Contractile activation in scorpion striated muscle fibers. Dependence on voltage and external calcium. J Gen Physiol. 1984 Sep;84(3):321–345. doi: 10.1085/jgp.84.3.321. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grabner M., Bachmann A., Rosenthal F., Striessnig J., Schultz C., Tautz D., Glossmann H. Insect calcium channels. Molecular cloning of an alpha 1-subunit from housefly (Musca domestica) muscle. FEBS Lett. 1994 Feb 14;339(1-2):189–194. doi: 10.1016/0014-5793(94)80413-3. [DOI] [PubMed] [Google Scholar]
- Grabner M., Dirksen R. T., Suda N., Beam K. G. The II-III loop of the skeletal muscle dihydropyridine receptor is responsible for the Bi-directional coupling with the ryanodine receptor. J Biol Chem. 1999 Jul 30;274(31):21913–21919. doi: 10.1074/jbc.274.31.21913. [DOI] [PubMed] [Google Scholar]
- Györke S., Palade P. Ca(2+)-dependent negative control mechanism for Ca(2+)-induced Ca2+ release in crayfish muscle. J Physiol. 1994 Apr 15;476(2):315–322. doi: 10.1113/jphysiol.1994.sp020133. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Hasan G., Rosbash M. Drosophila homologs of two mammalian intracellular Ca(2+)-release channels: identification and expression patterns of the inositol 1,4,5-triphosphate and the ryanodine receptor genes. Development. 1992 Dec;116(4):967–975. doi: 10.1242/dev.116.4.967. [DOI] [PubMed] [Google Scholar]
- Hencek M., Zachar J. Calcium currents and conductances in the msucle membrane of the crayfish. J Physiol. 1977 Jun;268(1):51–71. doi: 10.1113/jphysiol.1977.sp011846. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hoyle G. Correlated physiological and ultrastructural studies on specialized muscles. 3b. Fine structure of the power-stroke muscle of the swimming leg of Portunus sanguinolentus. J Exp Zool. 1973 Jul;185(1):97–109. doi: 10.1002/jez.1401850110. [DOI] [PubMed] [Google Scholar]
- Huddart H., Oates K. Ultrastructure of stick insect and locust skeletal muscle in relation to excitation-contraction coupling. J Insect Physiol. 1970 Aug;16(8):1467–1483. doi: 10.1016/0022-1910(70)90247-7. [DOI] [PubMed] [Google Scholar]
- Hurnák O., Proks P., Krizanová O., Zachar J. DHP-sensitive Ca2+ channels from crayfish skeletal muscle T-tubules incorporated into planar lipid bilayers. Gen Physiol Biophys. 1990 Dec;9(6):643–646. [PubMed] [Google Scholar]
- Inagaki S., Kaku K., Dunlap D. Y., Matsumura F. Sequences of cDNAs encoding calmodulin, and partial structures of calmodulin kinase, and a calcium channel of kdr-resistant and -susceptible German cockroaches, Blattella germanica. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol. 1998 Aug;120(2):225–233. doi: 10.1016/s0742-8413(98)00044-9. [DOI] [PubMed] [Google Scholar]
- 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]
- Jeziorski M. C., Greenberg R. M., Anderson P. A. The molecular biology of invertebrate voltage-gated Ca(2+) channels. J Exp Biol. 2000 Mar;203(Pt 5):841–856. doi: 10.1242/jeb.203.5.841. [DOI] [PubMed] [Google Scholar]
- Jeziorski M. C., Greenberg R. M., Clark K. S., Anderson P. A. Cloning and functional expression of a voltage-gated calcium channel alpha1 subunit from jellyfish. J Biol Chem. 1998 Aug 28;273(35):22792–22799. doi: 10.1074/jbc.273.35.22792. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Kim Y. K., Valdivia H. H., Maryon E. B., Anderson P., Coronado R. High molecular weight proteins in the nematode C. elegans bind [3H]ryanodine and form a large conductance channel. Biophys J. 1992 Nov;63(5):1379–1384. doi: 10.1016/S0006-3495(92)81702-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Loesser K. E., Castellani L., Franzini-Armstrong C. Dispositions of junctional feet in muscles of invertebrates. J Muscle Res Cell Motil. 1992 Apr;13(2):161–173. doi: 10.1007/BF01874153. [DOI] [PubMed] [Google Scholar]
- McPherson P. S., Campbell K. P. The ryanodine receptor/Ca2+ release channel. J Biol Chem. 1993 Jul 5;268(19):13765–13768. [PubMed] [Google Scholar]
- 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]
- 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]
- Mounier Y., Goblet C. Role of the different calcium sources in the excitation-contraction coupling in crab muscle fibers. Can J Physiol Pharmacol. 1987 Apr;65(4):667–671. doi: 10.1139/y87-110. [DOI] [PubMed] [Google Scholar]
- Nakai J., Dirksen R. T., Nguyen H. T., Pessah I. N., Beam K. G., Allen P. D. Enhanced dihydropyridine receptor channel activity in the presence of ryanodine receptor. Nature. 1996 Mar 7;380(6569):72–75. doi: 10.1038/380072a0. [DOI] [PubMed] [Google Scholar]
- Protasi F., Franzini-Armstrong C., Allen P. D. Role of ryanodine receptors in the assembly of calcium release units in skeletal muscle. J Cell Biol. 1998 Feb 23;140(4):831–842. doi: 10.1083/jcb.140.4.831. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Protasi F., Franzini-Armstrong C., Flucher B. E. Coordinated incorporation of skeletal muscle dihydropyridine receptors and ryanodine receptors in peripheral couplings of BC3H1 cells. J Cell Biol. 1997 May 19;137(4):859–870. doi: 10.1083/jcb.137.4.859. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Protasi F., Sun X. H., Franzini-Armstrong C. Formation and maturation of the calcium release apparatus in developing and adult avian myocardium. Dev Biol. 1996 Jan 10;173(1):265–278. doi: 10.1006/dbio.1996.0022. [DOI] [PubMed] [Google Scholar]
- Protasi F., Takekura H., Wang Y., Chen S. R., Meissner G., Allen P. D., Franzini-Armstrong C. RYR1 and RYR3 have different roles in the assembly of calcium release units of skeletal muscle. Biophys J. 2000 Nov;79(5):2494–2508. doi: 10.1016/S0006-3495(00)76491-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rieger F., Pinçon-Raymond M., Tassin A. M., Garcia L., Romey G., Fosset M., Lazdunski M. Excitation-contraction uncoupling in the developing skeletal muscle of the muscular dysgenesis mouse embryo. Biochimie. 1987 Apr;69(4):411–417. doi: 10.1016/0300-9084(87)90033-2. [DOI] [PubMed] [Google Scholar]
- 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]
- Romey G., Rieger F., Renaud J. F., Pinçon-Raymond M., Lazdunski M. The electrophysiological expression of Ca2+ channels and of apamin sensitive Ca2+ activated K+ channels is abolished in skeletal muscle cells from mice with muscular dysgenesis. Biochem Biophys Res Commun. 1986 May 14;136(3):935–940. doi: 10.1016/0006-291x(86)90422-5. [DOI] [PubMed] [Google Scholar]
- Schneider M. F. Control of calcium release in functioning skeletal muscle fibers. Annu Rev Physiol. 1994;56:463–484. doi: 10.1146/annurev.ph.56.030194.002335. [DOI] [PubMed] [Google Scholar]
- Seok J. H., Xu L., Kramarcy N. R., Sealock R., Meissner G. The 30 S lobster skeletal muscle Ca2+ release channel (ryanodine receptor) has functional properties distinct from the mammalian channel proteins. J Biol Chem. 1992 Aug 5;267(22):15893–15901. [PubMed] [Google Scholar]
- Sherman R. G. Ultrastructural features of cardiac muscle cells in a tarantula spider. J Morphol. 1973 Jun;140(2):215–241. doi: 10.1002/jmor.1051400208. [DOI] [PubMed] [Google Scholar]
- Smith D. S. The organization and function of the sarcoplasmic reticulum and T-system of muscle cells. Prog Biophys Mol Biol. 1966;16:107–142. doi: 10.1016/0079-6107(66)90004-6. [DOI] [PubMed] [Google Scholar]
- Sun X. H., Protasi F., Takahashi M., Takeshima H., Ferguson D. G., Franzini-Armstrong C. Molecular architecture of membranes involved in excitation-contraction coupling of cardiac muscle. J Cell Biol. 1995 May;129(3):659–671. doi: 10.1083/jcb.129.3.659. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sutko J. L., Airey J. A. Ryanodine receptor Ca2+ release channels: does diversity in form equal diversity in function? Physiol Rev. 1996 Oct;76(4):1027–1071. doi: 10.1152/physrev.1996.76.4.1027. [DOI] [PubMed] [Google Scholar]
- 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]
- Tanabe T., Adams B. A., Numa S., Beam K. G. Repeat I of the dihydropyridine receptor is critical in determining calcium channel activation kinetics. Nature. 1991 Aug 29;352(6338):800–803. doi: 10.1038/352800a0. [DOI] [PubMed] [Google Scholar]
- 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]
- Wilkens C. M., Kasielke N., Flucher B. E., Beam K. G., Grabner M. Excitation-contraction coupling is unaffected by drastic alteration of the sequence surrounding residues L720-L764 of the alpha 1S II-III loop. Proc Natl Acad Sci U S A. 2001 Apr 24;98(10):5892–5897. doi: 10.1073/pnas.101618098. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Zacharová D., Zachar J. The effect of external calcium ions on the excitation-contraction coupling in single muscle fibres of the crayfish. Physiol Bohemoslov. 1967;16(3):191–207. [PubMed] [Google Scholar]
- Zahradník I., Zachar J. Calcium channels in crayfish muscle fibre fragments studied by means of the Vaseline gap technique. Gen Physiol Biophys. 1987 Apr;6(2):113–125. [PubMed] [Google Scholar]