Skip to main content
PMC home page
Biochemical Journal logoLink to Biochemical Journal
. 1998 Nov 1;335(Pt 3):541–547. doi: 10.1042/bj3350541

Identification of 30 kDa calsequestrin-binding protein, which regulates calcium release from sarcoplasmic reticulum of rabbit skeletal muscle.

N Yamaguchi 1, M Kasai 1
PMCID: PMC1219814  PMID: 9794793

Abstract

In a previous study [Yamaguchi, Kawasaki and Kasai (1995) Biochem. Biophys. Res. Commun. 210, 648-653], we showed that the stilbene derivative 4,4'-di-isothiocyanostilbene-2,2'-disulphonic acid activates the Ca2+ channel in the sarcoplasmic reticulum (SR) in rabbit skeletal muscle, and it does not bind to the channel protein itself but to the SR 30 kDa protein. Furthermore, the 30 kDa protein was shown to bind to calsequestrin (CSQ), which is one of the regulators of the Ca2+ release channel in the SR. In the present study, we determined the partial amino acid sequence of the CSQ-binding 30 kDa protein and, consequently, this protein was proved to be highly similar to ADP/ATP translocase (AAT) expressed in the mitochondria in a variety of cells. By Western-blotting analysis, the CSQ-binding 30 kDa protein was recognized by the antibody raised against bovine cardiac AAT and, furthermore, depolarization-induced Ca2+ release monitored in the rabbit skeletal muscle triads was significantly activated by the antibody. As a result of cloning and sequencing of the cDNA encoding AAT of the rabbit skeletal muscle, the amino acid sequence was found to be the same as that of the CSQ-binding 30 kDa protein determined above. Furthermore, the expressed product of the cDNA encoding AAT in Escherichia coli was proved to bind to CSQ. These results suggest that AAT itself is expressed in the rabbit skeletal muscle SR and regulates the Ca2+ release from the SR; that is, excitation-contraction coupling of the skeletal muscle cell.

Full Text

The Full Text of this article is available as a PDF (478.0 KB).

Selected References

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

  1. Brandolin G., Le Saux A., Trezeguet V., Lauquin G. J., Vignais P. V. Chemical, immunological, enzymatic, and genetic approaches to studying the arrangement of the peptide chain of the ADP/ATP carrier in the mitochondrial membrane. J Bioenerg Biomembr. 1993 Oct;25(5):459–472. doi: 10.1007/BF01108403. [DOI] [PubMed] [Google Scholar]
  2. Brandt N. R., Caswell A. H., Wen S. R., Talvenheimo J. A. Molecular interactions of the junctional foot protein and dihydropyridine receptor in skeletal muscle triads. J Membr Biol. 1990 Feb;113(3):237–251. doi: 10.1007/BF01870075. [DOI] [PubMed] [Google Scholar]
  3. Brillantes A. B., Ondrias K., Scott A., Kobrinsky E., Ondriasová E., Moschella M. C., Jayaraman T., Landers M., Ehrlich B. E., Marks A. R. Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell. 1994 May 20;77(4):513–523. doi: 10.1016/0092-8674(94)90214-3. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  6. Costello B., Chadwick C., Fleischer S. Isolation of the junctional face membrane of sarcoplasmic reticulum. Methods Enzymol. 1988;157:46–50. doi: 10.1016/0076-6879(88)57067-2. [DOI] [PubMed] [Google Scholar]
  7. Damiani E., Margreth A. Specific protein-protein interactions of calsequestrin with junctional sarcoplasmic reticulum of skeletal muscle. Biochem Biophys Res Commun. 1990 Nov 15;172(3):1253–1259. doi: 10.1016/0006-291x(90)91584-f. [DOI] [PubMed] [Google Scholar]
  8. Donoso P., Prieto H., Hidalgo C. Luminal calcium regulates calcium release in triads isolated from frog and rabbit skeletal muscle. Biophys J. 1995 Feb;68(2):507–515. doi: 10.1016/S0006-3495(95)80212-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fan H., Brandt N. R., Caswell A. H. Disulfide bonds, N-glycosylation and transmembrane topology of skeletal muscle triadin. Biochemistry. 1995 Nov 14;34(45):14902–14908. doi: 10.1021/bi00045a035. [DOI] [PubMed] [Google Scholar]
  10. Fan H., Brandt N. R., Peng M., Schwartz A., Caswell A. H. Binding sites of monoclonal antibodies and dihydropyridine receptor alpha 1 subunit cytoplasmic II-III loop on skeletal muscle triadin fusion peptides. Biochemistry. 1995 Nov 14;34(45):14893–14901. doi: 10.1021/bi00045a034. [DOI] [PubMed] [Google Scholar]
  11. Frohman M. A., Dush M. K., Martin G. R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. doi: 10.1073/pnas.85.23.8998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gilchrist J. S., Belcastro A. N., Katz S. Intraluminal Ca2+ dependence of Ca2+ and ryanodine-mediated regulation of skeletal muscle sarcoplasmic reticulum Ca2+ release. J Biol Chem. 1992 Oct 15;267(29):20850–20856. [PubMed] [Google Scholar]
  13. Guo W., Campbell K. P. Association of triadin with the ryanodine receptor and calsequestrin in the lumen of the sarcoplasmic reticulum. J Biol Chem. 1995 Apr 21;270(16):9027–9030. doi: 10.1074/jbc.270.16.9027. [DOI] [PubMed] [Google Scholar]
  14. Jones L. R., Zhang L., Sanborn K., Jorgensen A. O., Kelley J. Purification, primary structure, and immunological characterization of the 26-kDa calsequestrin binding protein (junctin) from cardiac junctional sarcoplasmic reticulum. J Biol Chem. 1995 Dec 22;270(51):30787–30796. doi: 10.1074/jbc.270.51.30787. [DOI] [PubMed] [Google Scholar]
  15. Kagari T., Yamaguchi N., Kasai M. Biochemical characterization of calsequestrin-binding 30-kDa protein in sarcoplasmic reticulum of skeletal muscle. Biochem Biophys Res Commun. 1996 Oct 23;227(3):700–706. doi: 10.1006/bbrc.1996.1572. [DOI] [PubMed] [Google Scholar]
  16. Kasai M., Kawasaki T., Yamamoto K. Permeation of neutral molecules through calcium channel in sarcoplasmic reticulum vesicles. J Biochem. 1992 Aug;112(2):197–203. doi: 10.1093/oxfordjournals.jbchem.a123877. [DOI] [PubMed] [Google Scholar]
  17. Kawasaki T., Kasai M. Disulfonic stilbene derivatives open the Ca2+ release channel of sarcoplasmic reticulum. J Biochem. 1989 Sep;106(3):401–405. doi: 10.1093/oxfordjournals.jbchem.a122865. [DOI] [PubMed] [Google Scholar]
  18. Kawasaki T., Kasai M. Regulation of calcium channel in sarcoplasmic reticulum by calsequestrin. Biochem Biophys Res Commun. 1994 Mar 30;199(3):1120–1127. doi: 10.1006/bbrc.1994.1347. [DOI] [PubMed] [Google Scholar]
  19. Kim K. C., Caswell A. H., Talvenheimo J. A., Brandt N. R. 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):9281–9289. doi: 10.1021/bi00491a025. [DOI] [PubMed] [Google Scholar]
  20. Knudson C. M., Stang K. K., Moomaw C. R., Slaughter C. A., Campbell K. P. Primary structure and topological analysis of a skeletal muscle-specific junctional sarcoplasmic reticulum glycoprotein (triadin). J Biol Chem. 1993 Jun 15;268(17):12646–12654. [PubMed] [Google Scholar]
  21. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. 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]
  24. Melzer W., Herrmann-Frank A., Lüttgau H. C. The role of Ca2+ ions in excitation-contraction coupling of skeletal muscle fibres. Biochim Biophys Acta. 1995 May 8;1241(1):59–116. doi: 10.1016/0304-4157(94)00014-5. [DOI] [PubMed] [Google Scholar]
  25. Mitchell R. D., Simmerman H. K., Jones L. R. Ca2+ binding effects on protein conformation and protein interactions of canine cardiac calsequestrin. J Biol Chem. 1988 Jan 25;263(3):1376–1381. [PubMed] [Google Scholar]
  26. Oba T., Koshita M., Van Helden D. F. Modulation of frog skeletal muscle Ca2+ release channel gating by anion channel blockers. Am J Physiol. 1996 Sep;271(3 Pt 1):C819–C824. doi: 10.1152/ajpcell.1996.271.3.C819. [DOI] [PubMed] [Google Scholar]
  27. Powell S. J., Medd S. M., Runswick M. J., Walker J. E. Two bovine genes for mitochondrial ADP/ATP translocase expressed differences in various tissues. Biochemistry. 1989 Jan 24;28(2):866–873. doi: 10.1021/bi00428a069. [DOI] [PubMed] [Google Scholar]
  28. Shoshan-Barmatz V., Hadad N., Feng W., Shafir I., Orr I., Varsanyi M., Heilmeyer L. M. VDAC/porin is present in sarcoplasmic reticulum from skeletal muscle. FEBS Lett. 1996 May 20;386(2-3):205–210. doi: 10.1016/0014-5793(96)00442-5. [DOI] [PubMed] [Google Scholar]
  29. Storrie B., Madden E. A. Isolation of subcellular organelles. Methods Enzymol. 1990;182:203–225. doi: 10.1016/0076-6879(90)82018-w. [DOI] [PubMed] [Google Scholar]
  30. Timerman A. P., Ogunbumni E., Freund E., Wiederrecht G., Marks A. R., Fleischer S. The calcium release channel of sarcoplasmic reticulum is modulated by FK-506-binding protein. Dissociation and reconstitution of FKBP-12 to the calcium release channel of skeletal muscle sarcoplasmic reticulum. J Biol Chem. 1993 Nov 5;268(31):22992–22999. [PubMed] [Google Scholar]
  31. Watanabe K., Fujii Y., Nakayama K., Ohkubo H., Kuramitsu S., Kagamiyama H., Nakanishi S., Hayaishi O. Structural similarity of bovine lung prostaglandin F synthase to lens epsilon-crystallin of the European common frog. Proc Natl Acad Sci U S A. 1988 Jan;85(1):11–15. doi: 10.1073/pnas.85.1.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Wistow G. J., Mulders J. W., de Jong W. W. The enzyme lactate dehydrogenase as a structural protein in avian and crocodilian lenses. Nature. 1987 Apr 9;326(6113):622–624. doi: 10.1038/326622a0. [DOI] [PubMed] [Google Scholar]
  33. Yamaguchi N., Igami K., Kasai M. Kinetics of depolarization-induced calcium release from skeletal muscle triads in vitro. J Biochem. 1997 Mar;121(3):432–439. doi: 10.1093/oxfordjournals.jbchem.a021607. [DOI] [PubMed] [Google Scholar]
  34. Yamaguchi N., Kasai M. Potentiation of depolarization-induced calcium release from skeletal muscle triads by cyclic ADP-ribose and inositol 1,4,5-trisphosphate. Biochem Biophys Res Commun. 1997 Nov 26;240(3):772–777. doi: 10.1006/bbrc.1997.7583. [DOI] [PubMed] [Google Scholar]
  35. Yamaguchi N., Kawasaki T., Kasai M. DIDS binding 30-kDa protein regulates the calcium release channel in the sarcoplasmic reticulum. Biochem Biophys Res Commun. 1995 May 25;210(3):648–653. doi: 10.1006/bbrc.1995.1709. [DOI] [PubMed] [Google Scholar]
  36. Zahradníková A., Zahradník I. Modification of cardiac Ca2+ release channel gating by DIDS. Pflugers Arch. 1993 Dec;425(5-6):555–557. doi: 10.1007/BF00374886. [DOI] [PubMed] [Google Scholar]
  37. Zhang L., Kelley J., Schmeisser G., Kobayashi Y. M., Jones L. R. Complex formation between junctin, triadin, calsequestrin, and the ryanodine receptor. Proteins of the cardiac junctional sarcoplasmic reticulum membrane. J Biol Chem. 1997 Sep 12;272(37):23389–23397. doi: 10.1074/jbc.272.37.23389. [DOI] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES