Negatively charged amino acids within the intraluminal loop of ryanodine receptor are involved in the interaction with triadin - PubMed

Affiliations

• PMID: 14638677
• DOI: 10.1074/jbc.M312446200

Free article

Negatively charged amino acids within the intraluminal loop of ryanodine receptor are involved in the interaction with triadin

Jae Man Lee et al. J Biol Chem. 2004.

Free article

Abstract

In mammalian striated muscles, ryanodine receptor (RyR), triadin, junctin, and calsequestrin form a quaternary complex in the lumen of sarcoplasmic reticulum. Such intermolecular interactions contribute not only to the passive buffering of sarcoplasmic reticulum luminal Ca2+, but also to the active Ca2+ release process during excitation-contraction coupling. Here we tested the hypothesis that specific charged amino acids within the luminal portion of RyR mediate its direct interaction with triadin. Using in vitro binding assay and site-directed mutagenesis, we found that the second intraluminal loop of the skeletal muscle RyR1 (amino acids 4860-4917), but not the first intraluminal loop of RyR1 (amino acids 4581-4640) could bind triadin. Specifically, three negatively charged residues Asp4878, Asp4907, and Glu4908 appear to be critical for the association with triadin. Using deletional approaches, we showed that a KEKE motif of triadin (amino acids 200-232) is essential for the binding to RyR1. Because the second intraluminal loop of RyR has been previously shown to contain the ion-conducting pore as well as the selectivity filter of the Ca2+ release channel, and Asp4878, Asp4907, and Glu4908 residues are predicted to locate at the periphery of the pore assembly of the channel, our data suggest that a physical interaction between RyR1 and triadin could play an active role in the overall Ca2+ release process of excitation-contraction coupling in muscle cells.

Similar articles

• Triadin binding to the C-terminal luminal loop of the ryanodine receptor is important for skeletal muscle excitation contraction coupling.

  Goonasekera SA, Beard NA, Groom L, Kimura T, Lyfenko AD, Rosenfeld A, Marty I, Dulhunty AF, Dirksen RT. Goonasekera SA, et al. J Gen Physiol. 2007 Oct;130(4):365-78. doi: 10.1085/jgp.200709790. Epub 2007 Sep 10. J Gen Physiol. 2007. PMID: 17846166 Free PMC article.

• Three residues in the luminal domain of triadin impact on Trisk 95 activation of skeletal muscle ryanodine receptors.

  Wium E, Dulhunty AF, Beard NA. Wium E, et al. Pflugers Arch. 2016 Nov;468(11-12):1985-1994. doi: 10.1007/s00424-016-1869-7. Epub 2016 Sep 5. Pflugers Arch. 2016. PMID: 27595738

• Occurrence of atypical Ca2+ transients in triadin-binding deficient-RYR1 mutants.

  Lee EH, Song DW, Lee JM, Meissner G, Allen PD, Kim DH. Lee EH, et al. Biochem Biophys Res Commun. 2006 Dec 29;351(4):909-14. doi: 10.1016/j.bbrc.2006.10.115. Epub 2006 Nov 7. Biochem Biophys Res Commun. 2006. PMID: 17092484

• Calsequestrin and the calcium release channel of skeletal and cardiac muscle.

  Beard NA, Laver DR, Dulhunty AF. Beard NA, et al. Prog Biophys Mol Biol. 2004 May;85(1):33-69. doi: 10.1016/j.pbiomolbio.2003.07.001. Prog Biophys Mol Biol. 2004. PMID: 15050380 Review.

• Control of muscle ryanodine receptor calcium release channels by proteins in the sarcoplasmic reticulum lumen.

  Beard NA, Wei L, Dulhunty AF. Beard NA, et al. Clin Exp Pharmacol Physiol. 2009 Mar;36(3):340-5. doi: 10.1111/j.1440-1681.2008.05094.x. Clin Exp Pharmacol Physiol. 2009. PMID: 19278523 Review.

Cited by

• Absence of triadin, a protein of the calcium release complex, is responsible for cardiac arrhythmia with sudden death in human.

  Roux-Buisson N, Cacheux M, Fourest-Lieuvin A, Fauconnier J, Brocard J, Denjoy I, Durand P, Guicheney P, Kyndt F, Leenhardt A, Le Marec H, Lucet V, Mabo P, Probst V, Monnier N, Ray PF, Santoni E, Trémeaux P, Lacampagne A, Fauré J, Lunardi J, Marty I. Roux-Buisson N, et al. Hum Mol Genet. 2012 Jun 15;21(12):2759-67. doi: 10.1093/hmg/dds104. Epub 2012 Mar 14. Hum Mol Genet. 2012. PMID: 22422768 Free PMC article.

• Triadins are not triad-specific proteins: two new skeletal muscle triadins possibly involved in the architecture of sarcoplasmic reticulum.

  Vassilopoulos S, Thevenon D, Rezgui SS, Brocard J, Chapel A, Lacampagne A, Lunardi J, Dewaard M, Marty I. Vassilopoulos S, et al. J Biol Chem. 2005 Aug 5;280(31):28601-9. doi: 10.1074/jbc.M501484200. Epub 2005 May 31. J Biol Chem. 2005. PMID: 15927957 Free PMC article.

• Phylogenetic and biochemical analysis of calsequestrin structure and association of its variants with cardiac disorders.

  Wang Q, Paskevicius T, Filbert A, Qin W, Kim HJ, Chen XZ, Tang J, Dacks JB, Agellon LB, Michalak M. Wang Q, et al. Sci Rep. 2020 Oct 22;10(1):18115. doi: 10.1038/s41598-020-75097-3. Sci Rep. 2020. PMID: 33093545 Free PMC article.

• Altered stored calcium release in skeletal myotubes deficient of triadin and junctin.

  Wang Y, Li X, Duan H, Fulton TR, Eu JP, Meissner G. Wang Y, et al. Cell Calcium. 2009 Jan;45(1):29-37. doi: 10.1016/j.ceca.2008.05.006. Epub 2008 Jul 11. Cell Calcium. 2009. PMID: 18620751 Free PMC article.

• Junctin and triadin each activate skeletal ryanodine receptors but junctin alone mediates functional interactions with calsequestrin.

  Wei L, Gallant EM, Dulhunty AF, Beard NA. Wei L, et al. Int J Biochem Cell Biol. 2009 Nov;41(11):2214-24. doi: 10.1016/j.biocel.2009.04.017. Epub 2009 May 4. Int J Biochem Cell Biol. 2009. PMID: 19398037 Free PMC article.

Publication types

MeSH terms

Substances

LinkOut - more resources

• Full Text Sources

  • Elsevier Science

• Miscellaneous

  • NCI CPTAC Assay Portal