Home LiteratureArticle Details
PMID: 8245124 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Triad formation: organization and function of the sarcoplasmic reticulum calcium release channel and triadin in normal and dysgenic muscle in vitro.

The Journal of cell biology ·Vol. 123 ·No. 5 ·1993-12-00 ·Pages 1161-74

Flucher BE, Andrews SB, Fleischer S, Marks AR, Caswell A, Powell JA

Abstract

Excitation-contraction (E-C) coupling is thought to involve close interactions between the calcium release channel (ryanodine receptor; RyR) of the sarcoplasmic reticulum (SR) and the dihydropyridine receptor (DHPR) alpha 1 subunit in the T-tubule membrane. Triadin, a 95-kD protein isolated from heavy SR, binds both the RyR and DHPR and may thus participate in E-C coupling or in interactions responsible for the formation of SR/T-tubule junctions. Immunofluorescence labeling of normal mouse myotubes shows that the RyR and triadin co-aggregate with the DHPR in punctate clusters upon formation of functional junctions. Dysgenic myotubes with a deficiency in the alpha 1 subunit of the DHPR show reduced expression and clustering of RyR and triadin; however, both proteins are still capable of forming clusters and attaining mature cross-striated distributions. Thus, the molecular organization of the RyR and triadin in the terminal cisternae of SR as well as its association with the T-tubules are independent of interactions with the DHPR alpha 1 subunit. Analysis of calcium transients in dysgenic myotubes with fluorescent calcium indicators reveals spontaneous and caffeine-induced calcium release from intracellular stores similar to those of normal muscle; however, depolarization-induced calcium release is absent. Thus, characteristic calcium release properties of the RyR do not require interactions with the DHPR; neither do they require the normal organization of the RyR in the terminal SR cisternae. In hybrids of dysgenic myotubes fused with normal cells, both action potential-induced calcium transients and the normal clustered organization of the RyR are restored in regions expressing the DHPR alpha 1 subunit.

Related Genes
mdg
MeSH Terms
Amino Acid Sequence Animals Calcium/metabolism Calcium Channels/isolation & purification,metabolism Calcium Channels, L-Type Calcium-Transporting ATPases/isolation & purification,metabolism Carrier Proteins Cells, Cultured Fluorescent Antibody Technique Intracellular Signaling Peptides and Proteins Macromolecular Substances Mice Mice, Mutant Strains Microscopy, Fluorescence Microscopy, Phase-Contrast Microtubules/metabolism Molecular Sequence Data Muscle Proteins/isolation & purification,metabolism Muscles/cytology,embryology,metabolism Rats Rats, Sprague-Dawley Ryanodine Receptor Calcium Release Channel Sarcoplasmic Reticulum/metabolism,ultrastructure
Chemicals
Calcium Channels Calcium Channels, L-Type Carrier Proteins Intracellular Signaling Peptides and Proteins Macromolecular Substances Muscle Proteins Ryanodine Receptor Calcium Release Channel Trdn protein, mouse Trdn protein, rat triadin Calcium-Transporting ATPases Calcium
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Flucher B E
Laboratory of Neurobiology, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland 20892.
Andrews S B
Fleischer S
Marks A R
Caswell A
Powell J A
References (57)
57 references, click to expand
  1. Monoclonal antibody identifies a 200-kDa subunit of the dihydropyridine-sensitive calcium channel.
    J Biol Chem. 1987 Sep 5;262(25):11904-7 PMID: 2442152
  2. 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):135-47 PMID: 2545725
  3. Polypeptides of the Golgi apparatus of neurons from rat brain.
    J Neurochem. 1987 Nov;49(5):1498-506 PMID: 3668536
  4. Expression of fast and slow isoforms of the Ca2+-ATPase in developing chick skeletal muscle.
    Dev Biol. 1987 Dec;124(2):490-503 PMID: 2960578
  5. Purification and reconstitution of the calcium release channel from skeletal muscle.
    Nature. 1988 Jan 28;331(6154):315-9 PMID: 2448641
  6. Restoration of excitation-contraction coupling and slow calcium current in dysgenic muscle by dihydropyridine receptor complementary DNA.
    Nature. 1988 Nov 10;336(6195):134-9 PMID: 2903448
  7. 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):2587-600 PMID: 2849609
  8. Specific absence of the alpha 1 subunit of the dihydropyridine receptor in mice with muscular dysgenesis.
    J Biol Chem. 1989 Jan 25;264(3):1345-8 PMID: 2536362
  9. Three-dimensional architecture of the calcium channel/foot structure of sarcoplasmic reticulum.
    Nature. 1989 Mar 9;338(6211):167-70 PMID: 2537473
  10. The muscular dysgenesis mutation in mice leads to arrest of the genetic program for muscle differentiation.
    Dev Biol. 1989 Jun;133(2):456-67 PMID: 2731637
  11. Production and properties of site-specific antibodies to synthetic peptide antigens related to potential cell surface receptor sites for rhinovirus.
    Methods Enzymol. 1989;178:676-92 PMID: 2557528
  12. A novel calcium current in dysgenic skeletal muscle.
    J Gen Physiol. 1989 Sep;94(3):429-44 PMID: 2558151
  13. Restoration of dysgenic murine (mdg) myotube contraction after addition of Schwann cells from normal mice in vitro.
    Biol Cell. 1989;67(3):355-8 PMID: 2620167
  14. Rescue of excitation-contraction coupling in dysgenic muscle by addition of fibroblasts in vitro.
    Neuron. 1989 Apr;2(4):1341-50 PMID: 2560638
  15. Molecular interactions of the junctional foot protein and dihydropyridine receptor in skeletal muscle triads.
    J Membr Biol. 1990 Feb;113(3):237-51 PMID: 2159517
  16. A genetic model for the study of abnormal nerve-muscle interactions at the level of excitation-contraction coupling: the mutation muscular dysgenesis.
    J Physiol (Paris). 1990;84(1):82-7 PMID: 2193149
  17. Muscular dysgenesis in mice: a model system for studying excitation-contraction coupling.
    FASEB J. 1990 Jul;4(10):2809-16 PMID: 2165014
  18. Intramembrane charge movement restored in dysgenic skeletal muscle by injection of dihydropyridine receptor cDNAs.
    Nature. 1990 Aug 9;346(6284):569-72 PMID: 2165571
  19. Localization of the alpha 1 and alpha 2 subunits of the dihydropyridine receptor and ankyrin in skeletal muscle triads.
    Neuron. 1990 Sep;5(3):339-51 PMID: 2169270
  20. Isolation of a terminal cisterna protein which may link the dihydropyridine receptor to the junctional foot protein in skeletal muscle.
    Biochemistry. 1990 Oct 2;29(39):9281-9 PMID: 2176846
  21. 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 PMID: 1846372
  22. Biogenesis of transverse tubules in skeletal muscle in vitro.
    Dev Biol. 1991 May;145(1):77-90 PMID: 2019326
  23. The mechanical hypothesis of excitation-contraction (EC) coupling in skeletal muscle.
    J Muscle Res Cell Motil. 1991 Apr;12(2):127-35 PMID: 1648106
  24. 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):7507-13 PMID: 1649631
  25. Simultaneous maturation of transverse tubules and sarcoplasmic reticulum during muscle differentiation in the mouse.
    Dev Biol. 1991 Aug;146(2):353-63 PMID: 1864461
  26. Muscle fibers from dysgenic mouse in vivo lack a surface component of peripheral couplings.
    Dev Biol. 1991 Aug;146(2):364-76 PMID: 1650725
  27. The path of calcium in cytosolic calcium oscillations: a unifying hypothesis.
    Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9883-7 PMID: 1946414
  28. 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):1345-56 PMID: 1659576
  29. Coordinated development of myofibrils, sarcoplasmic reticulum and transverse tubules in normal and dysgenic mouse skeletal muscle, in vivo and in vitro.
    Dev Biol. 1992 Apr;150(2):266-80 PMID: 1551475
  30. Molecular mechanisms of intracellular calcium excitability in X. laevis oocytes.
    Cell. 1992 Apr 17;69(2):283-94 PMID: 1568248
  31. Structural analysis of muscle development: transverse tubules, sarcoplasmic reticulum, and the triad.
    Dev Biol. 1992 Dec;154(2):245-60 PMID: 1426638
  32. A single nucleotide deletion in the skeletal muscle-specific calcium channel transcript of muscular dysgenesis (mdg) mice.
    J Biol Chem. 1992 Dec 25;267(36):25636-9 PMID: 1281468
  33. Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate.
    Science. 1992 Dec 11;258(5089):1812-5 PMID: 1465619
  34. mRNA for cardiac calcium channel is expressed during development of skeletal muscle.
    Dev Biol. 1993 Feb;155(2):507-15 PMID: 8381753
  35. Characterization of spontaneous and action potential-induced calcium transients in developing myotubes in vitro.
    Cell Motil Cytoskeleton. 1993;25(2):143-57 PMID: 8324830
  36. DEVELOPMENTAL GENETICS OF A LETHAL MUTATION, MUSCULAR DYSGENESIS (MDG), IN THE MOUSE. I. GENETIC ANALYSIS AND GROSS MORPHOLOGY.
    Dev Biol. 1965 Feb;11:82-92 PMID: 14300095
  37. An in vitro study of normal and mutant myogenesis in the mouse.
    Dev Biol. 1972 Mar;27(3):351-64 PMID: 5019134
  38. Voltage dependent charge movement of skeletal muscle: a possible step in excitation-contraction coupling.
    Nature. 1973 Mar 23;242(5395):244-6 PMID: 4540479
  39. Isolation of sarcoplasmic reticulum by zonal centrifugation and purification of Ca 2+ -pump and Ca 2+ -binding proteins.
    Biochim Biophys Acta. 1973 Mar 16;298(2):246-69 PMID: 4268907
  40. Electrical properties of normal and dysgenic mouse skeletal muscle in culture.
    J Cell Physiol. 1973 Aug;82(1):21-38 PMID: 4738109
  41. Muscular dysgenesis in the mouse (mdg/mdg). I. Ultrastructural study of skeletal and cardiac muscle.
    J Neuropathol Exp Neurol. 1977 Jan;36(1):100-27 PMID: 137961
  42. 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):287-98 PMID: 141456
  43. [3H]nitrendipine receptors in skeletal muscle.
    J Biol Chem. 1983 May 25;258(10):6086-92 PMID: 6304026
  44. Evidence for dysfunction in the regulation of cytosolic Ca2+ in excitation-contraction uncoupled dysgenic muscle.
    Dev Biol. 1983 Sep;99(1):152-65 PMID: 6617998
  45. Ultrastructural localization of calsequestrin in rat skeletal muscle by immunoferritin labeling of ultrathin frozen sections.
    J Cell Biol. 1983 Nov;97(5 Pt 1):1573-81 PMID: 6355123
  46. Preparation and morphology of sarcoplasmic reticulum terminal cisternae from rabbit skeletal muscle.
    J Cell Biol. 1984 Sep;99(3):875-85 PMID: 6147356
  47. 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):14255-63 PMID: 2997201
  48. Abnormal transverse tubule system and abnormal amount of receptors for Ca2+ channel inhibitors of the dihydropyridine family in skeletal muscle from mice with embryonic muscular dysgenesis.
    Dev Biol. 1985 Dec;112(2):458-66 PMID: 2416618
  49. Purified calcium channels have three allosterically coupled drug receptors.
    FEBS Lett. 1986 Mar 3;197(1-2):204-10 PMID: 2419161
  50. A lethal mutation in mice eliminates the slow calcium current in skeletal muscle cells.
    Nature. 1986 Mar 13-19;320(6058):168-70 PMID: 2419767
  51. Purified dihydropyridine-binding site from skeletal muscle t-tubules is a functional calcium channel.
    Nature. 1986 Sep 4-10;323(6083):66-8 PMID: 2427959
  52. 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):1740-7 PMID: 3805051
  53. Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle.
    Nature. 1987 Feb 19-25;325(6106):717-20 PMID: 2434854
  54. Subunit structure of dihydropyridine-sensitive calcium channels from skeletal muscle.
    Proc Natl Acad Sci U S A. 1987 Aug;84(15):5478-82 PMID: 2440051
  55. Primary structure and expression from complementary DNA of skeletal muscle ryanodine receptor.
    Nature. 1989 Jun 8;339(6224):439-45 PMID: 2725677
  56. Biochemistry and biophysics of excitation-contraction coupling.
    Annu Rev Biophys Biophys Chem. 1989;18:333-64 PMID: 2660829
  57. Excitation-contraction uncoupling in the developing skeletal muscle of the muscular dysgenesis mouse embryo.
    Biochimie. 1987 Apr;69(4):411-7 PMID: 3115318
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
DOI
10.1083/jcb.123.5.1161
Published
1993-12-00
Pages
1161-74
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2119885
Subset
IM
Grants
NHLBI NIH HHS · HL32711 · United States
External Links
PubMed source DOI: 10.1083/jcb.123.5.1161 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2