Ryanodine receptor modification and regulation by intracellular Ca2+ and Mg2+ in healthy and failing human hearts

Journal of Molecular and Cellular Cardiology - Tập 104 - Trang 53-62 - 2017
K. Walweel1, P. Molenaar2, M.S. Imtiaz3, A. Denniss4, C. dos Remedios5, D.F. van Helden1, A.F. Dulhunty6, D.R. Laver1, N.A. Beard4,6
1School of Biomedical Sciences and Pharmacy, University of Newcastle and Hunter Medical Research Institute, Callaghan, NSW, 2308, Australia
2Biomedical Sciences, Queensland University of Technology, Brisbane, QLD, 4000, Northside Clinical School, School of Clinical Medicine, University of Queensland and Critical Care Research Group, The Prince Charles Hospital, Chermside, QLD, 4032, Australia
3Victor Chang Cardiac Research Institute, Darlinghurst, New South Wales 2010, Australia
4Health Research Institute, Faculty of Education Science and Mathematics, University of Canberra, Bruce, ACT 2617, Australia
5Bosch Institute, Discipline of Anatomy, University of Sydney, Sydney, New South Wales 2006, Australia
6John Curtin School of Medical Research, Australian National University, Canberra, ACT, 0200, Australia

Tài liệu tham khảo

Bers, 2006, Altered cardiac myocyte Ca2+ regulation in heart failure, Physiology (Bethesda), 21, 380, 10.1152/physiol.00019.2006 George, 2008, Sarcoplasmic reticulum Ca2+ leak in heart failure: mere observation or functional relevance?, Cardiovasc. Res., 77, 302, 10.1093/cvr/cvm006 Zima, 2013, Sarcoplasmic reticulum Ca2+ homeostasis and heart failure, 5 Belevych, 2011, The relationship between arrhythmogenesis and impaired contractility in heart failure: role of altered ryanodine receptor function, Cardiovasc. Res., 90, 493, 10.1093/cvr/cvr025 Bers, 2002, Calcium and cardiac rhythms: physiological and pathophysiological, Circ. Res., 90, 14, 10.1161/res.90.1.14 Hu, 2010, Altered intracellular Ca2+ regulation in chronic rat heart failure, J. Physiol. Sci., 60, 85, 10.1007/s12576-009-0070-6 Respress, 2012, Role of RyR2 phosphorylation at S2814 during heart failure progression, Circ. Res., 110, 1474, 10.1161/CIRCRESAHA.112.268094 Shannon, 2002, Quantitative assessment of the SR Ca2+ leak-load relationship, Circ. Res., 91, 594, 10.1161/01.RES.0000036914.12686.28 Kushnir, 2010, The ryanodine receptor in cardiac physiology and disease, Adv. Pharm., 59, 1, 10.1016/S1054-3589(10)59001-X Walweel, 2014, Differences in the regulation of RyR2 from human, sheep, and rat by Ca2+ and Mg2+ in the cytoplasm and in the lumen of the sarcoplasmic reticulum, J. Gen. Physiol., 144, 263, 10.1085/jgp.201311157 Blayney, 2009, Ryanodine receptor-mediated arrhythmias and sudden cardiac death, Pharmacol. Ther., 123, 151, 10.1016/j.pharmthera.2009.03.006 Roux-Buisson, 2012, Absence of triadin, a protein of the calcium release complex, is responsible for cardiac arrhythmia with sudden death in human, Hum. Mol. Genet., 21, 2759, 10.1093/hmg/dds104 Dobrev, 2014, Role of RyR2 phosphorylation in heart failure and arrhythmias: controversies around ryanodine receptor phosphorylation in cardiac disease, Circ. Res., 114, 1311, 10.1161/CIRCRESAHA.114.300568 Jiang, 2002, Abnormal Ca2+ release, but normal ryanodine receptors, in canine and human heart failure, Circ. Res., 91, 1015, 10.1161/01.RES.0000043663.08689.05 Marx, 2000, PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts, Cell, 101, 365, 10.1016/S0092-8674(00)80847-8 Houser, 2010, Does protein kinase a-mediated phosphorylation of the cardiac ryanodine receptor play any role in adrenergic regulation of calcium handling in health and disease?, Circ. Res., 106, 1672, 10.1161/CIRCRESAHA.110.221853 Bers, 2012, Ryanodine receptor S2808 phosphorylation in heart failure: smoking gun or red herring, Circ. Res., 110, 796, 10.1161/CIRCRESAHA.112.265579 Cuadrado-Godia, 2010, Heart failure in acute ischemic stroke, Curr. Cardiol. Rev., 6, 202, 10.2174/157340310791658776 Maron, 2006, Circulation, 113, 1807, 10.1161/CIRCULATIONAHA.106.174287 Brown, 2008, Investigating the pathology of Emery-Dreifuss muscular dystrophy, Biochem. Soc. Trans., 36, 1335, 10.1042/BST0361335 Azibani, 2014, Striated muscle laminopathies, Semin. Cell Dev. Biol., 29, 107, 10.1016/j.semcdb.2014.01.001 Bright-Thomas, 2002, The heart in cystic fibrosis, J. R. Soc. Med., 95, 2 Burghuber, 1988, Right ventricular contractility is preserved in patients with cystic fibrosis and pulmonary artery hypertension, Scand. J. Gastroenterol. Suppl., 143, 93, 10.3109/00365528809090225 Florea, 2000, Right ventricular dysfunction in adult severe cystic fibrosis, Chest, 118, 1063, 10.1378/chest.118.4.1063 Weitzenblum, 1994, The pulmonary circulation and the heart in chronic lung disease, Monaldi Arch. Chest Dis., 49, 231 Sellers, 2013, Left ventricular and aortic dysfunction in cystic fibrosis mice, J. Cyst. Fibros., 12, 517, 10.1016/j.jcf.2012.11.012 Jacobstein, 1981, Ventricular interdependence in severe cystic fibrosis. A two-dimensional echocardiographic study, Chest, 80, 399, 10.1378/chest.80.4.399 Johnson, 1991, Changes in left ventricular diastolic filling patterns by Doppler echocardiography in cystic fibrosis, Chest, 99, 646, 10.1378/chest.99.3.646 Kuzumoto, 2008, Simulation analysis of intracellular Na+ and Cl− homeostasis during β 1-adrenergic stimulation of cardiac myocyte, Prog. Biophys. Mol. Biol., 96, 171, 10.1016/j.pbiomolbio.2007.07.005 Sellers, 2010, Cardiomyocytes with disrupted CFTR function require CaMKII and Ca2+-activated Cl− channel activity to maintain contraction rate, J. Physiol., 588, 2417, 10.1113/jphysiol.2010.188334 Sellers, 2012, MRP4 and CFTR in the regulation of cAMP and beta-adrenergic contraction in cardiac myocytes, Eur. J. Pharmacol., 681, 80, 10.1016/j.ejphar.2012.02.018 Wehrens, 2004, Protection from cardiac arrhythmia through ryanodine receptor-stabilizing protein calstabin2, Science, 304, 292, 10.1126/science.1094301 Reiken, 2003, Protein kinase A phosphorylation of the cardiac calcium release channel (ryanodine receptor) in normal and failing hearts. Role of phosphatases and response to isoproterenol, J. Biol. Chem., 278, 444, 10.1074/jbc.M207028200 Terentyev, 2008, Redox modification of ryanodine receptors contributes to sarcoplasmic reticulum Ca2+ leak in chronic heart failure, Circ. Res., 103, 1466, 10.1161/CIRCRESAHA.108.184457 Laver, 2013, Termination of calcium-induced calcium release by induction decay: an emergent property of stochastic channel gating and molecular scale architecture, J. Mol. Cell. Cardiol., 54, 98, 10.1016/j.yjmcc.2012.10.009 Laver, 2008, Luminal Mg2+, a key factor controlling RyR2-mediated Ca2+ release: cytoplasmic and luminal regulation modeled in a tetrameric channel, J. Gen. Physiol., 132, 429, 10.1085/jgp.200810001 Go, 1995, Differential regulation of two types of intracellular calcium release channels during end-stage heart failure, J. Clin. Invest., 95, 888, 10.1172/JCI117739 Zissimopoulos, 2012, Disparities in the association of the ryanodine receptor and the FK506-binding proteins in mammalian heart, J. Cell Sci., 125, 1759, 10.1242/jcs.098012 Belevych, 2009, Redox modification of ryanodine receptors underlies calcium alternans in a canine model of sudden cardiac death, Cardiovasc. Res., 84, 387, 10.1093/cvr/cvp246 Marks, 2013, Calcium cycling proteins and heart failure: mechanisms and therapeutics, J. Clin. Invest., 123, 46, 10.1172/JCI62834 Yano, 2005, Correction of defective interdomain interaction within ryanodine receptor by antioxidant is a new therapeutic strategy against heart failure, Circulation, 112, 3633, 10.1161/CIRCULATIONAHA.105.555623 Oda, 2005, Defective regulation of interdomain interactions within the ryanodine receptor plays a key role in the pathogenesis of heart failure, Circulation, 111, 3400, 10.1161/CIRCULATIONAHA.104.507921 Huttlin, 2010, A tissue-specific atlas of mouse protein phosphorylation and expression, Cell, 143, 1174, 10.1016/j.cell.2010.12.001 Yano, 2000, Altered stoichiometry of FKBP12.6 versus ryanodine receptor as a cause of abnormal Ca2+ leak through ryanodine receptor in heart failure, Circulation, 102, 2131, 10.1161/01.CIR.102.17.2131 Shan, 2010, Role of chronic ryanodine receptor phosphorylation in heart failure and β-adrenergic receptor blockade in mice, J. Clin. Invest., 120, 4375, 10.1172/JCI37649 Marx, 2001, Phosphorylation-dependent regulation of ryanodine receptors. A novel role for leucine/isoleucine zippers, J. Cell Biol., 153, 699, 10.1083/jcb.153.4.699 Wehrens, 2003, FKBP12.6 deficiency and defective calcium release channel (ryanodine receptor) function linked to exercise-induced sudden cardiac death, Cell, 113, 829, 10.1016/S0092-8674(03)00434-3 Galfre, 2012, FKBP12 activates the cardiac ryanodine receptor Ca2+-release channel and is antagonised by FKBP12.6, PLoS One, 7, 10.1371/journal.pone.0031956 Guo, 2010, Kinetics of FKBP12.6 binding to ryanodine receptors in permeabilized cardiac myocytes and effects on Ca2+ sparks, Circ. Res., 106, 1743, 10.1161/CIRCRESAHA.110.219816 Copello, 1997, Heterogeneity of Ca2+ gating of skeletal muscle and cardiac ryanodine receptors, Biophys. J., 73, 141, 10.1016/S0006-3495(97)78055-X Laver, 1995, Cytoplasmic Ca2+ inhibits the ryanodine receptor from cardiac muscle, J. Membr. Biol., 147, 7, 10.1007/BF00235394 Li, 2013, Beta-adrenergic stimulation increases RyR2 activity via intracellular Ca2+ and Mg2+ regulation, PLoS One, 8 Samso, 2006, Structural characterization of the RyR1-FKBP12 interaction, J. Mol. Biol., 356, 917, 10.1016/j.jmb.2005.12.023 Xu, 1998, Activation of the cardiac calcium release channel (ryanodine receptor) by poly-S-nitrosylation, Science, 279, 234, 10.1126/science.279.5348.234 Sun, 2001, Cysteine-3635 is responsible for skeletal muscle ryanodine receptor modulation by NO, Proc. Natl. Acad. Sci. U. S. A., 98, 11158, 10.1073/pnas.201289098 Crossman, 2011, Changes in the organization of excitation-contraction coupling structures in failing human heart, PLoS One, 6, 10.1371/annotation/061613ea-0f01-420f-bc3f-af36e5c35790 Murphy, 2013, Ca2+-dependent proteolysis of junctophilin-1 and junctophilin-2 in skeletal and cardiac muscle, J. Physiol., 591, 719, 10.1113/jphysiol.2012.243279 Pedrozo, 1802, Calpains and proteasomes mediate degradation of ryanodine receptors in a model of cardiac ischemic reperfusion, Biochim. Biophys. Acta, 2010, 356