Heme-induced contractile dysfunction in Human cardiomyocytes caused by oxidant damage to thick filament proteins

Free Radical Biology and Medicine - Tập 89 - Trang 248-262 - 2015
Gerardo Alvarado1,2, Viktória Jeney2,3, Attila Tóth1, Éva Csősz4, Gergő Kalló4, An T. Huynh1, Csaba Hajnal1, Judit Kalász1, Enikő T. Pásztor1, István Édes1, Magnus Gram5, Bo Akerström5, Ann Smith6, John W. Eaton7, György Balla3,8, Zoltán Papp1, József Balla2,3
1Division of Clinical Physiology, Institute of Cardiology, Faculty of Medicine, University of Debrecen, H-4032 Debrecen, Hungary
2Department of Nephrology, Institute of Internal Medicine, Faculty of Medicine, University of Debrecen, H-4032 Debrecen, Hungary
3MTA-DE Vascular Biology, Thrombosis and Hemostasis Research Group, Hungarian Academy of Sciences, H-4032 Debrecen, Hungary
4Department of Biochemistry and Molecular Biology, Faculty of Medicine, University of Debrecen, H-4032 Debrecen, Hungary
5Department of Clinical Sciences, Division of Infection Medicine, Lund University, Lund, Sweden
6School of Biological Sciences, University of Missouri-Kansas City, MO, USA
7Molecular Targets Program, James Graham Brown Cancer Center, University of Louisville, Louisville, KY 40059, USA
8Institute of Pediatrics, Faculty of Medicine, University of Debrecen, H-4032 Debrecen, Hungary

Tài liệu tham khảo

Sumandea, 2011, Redox signaling and cardiac sarcomeres, The Journal of biological chemistry, 286, 9921, 10.1074/jbc.R110.175489 Tsutsui, 2011, Oxidative stress and heart failure, American journal of physiology. Heart and circulatory physiology, 301, H2181, 10.1152/ajpheart.00554.2011 Hamdani, 2008, Sarcomeric dysfunction in heart failure, Cardiovascular research, 77, 649, 10.1093/cvr/cvm079 Hausenloy, 2013, Myocardial ischemia-reperfusion injury: a neglected therapeutic target, The Journal of clinical investigation, 123, 92, 10.1172/JCI62874 Gladwin, 2012, Cardiovascular abnormalities in sickle cell disease, Journal of the American College of Cardiology, 59, 1123, 10.1016/j.jacc.2011.10.900 Sachdev, 2007, Diastolic dysfunction is an independent risk factor for death in patients with sickle cell disease, Journal of the American College of Cardiology, 49, 472, 10.1016/j.jacc.2006.09.038 Dickinson, 2011, Chemistry and biology of reactive oxygen species in signaling or stress responses, Nature chemical biology, 7, 504, 10.1038/nchembio.607 Chung, 2013, Cysteine oxidative posttranslational modifications: emerging regulation in the cardiovascular system, Circulation research, 112, 382, 10.1161/CIRCRESAHA.112.268680 Ponka, 1999, Cell biology of heme, The American journal of the medical sciences, 318, 241, 10.1016/S0002-9629(15)40628-7 Palmer, 2004, Effect of cardiac myosin binding protein-C on mechanoenergetics in mouse myocardium, Circulation research, 94, 1615, 10.1161/01.RES.0000132744.08754.f2 Balla, 1993, Endothelial-cell heme uptake from heme proteins: induction of sensitization and desensitization to oxidant damage, Proceedings of the National Academy of Sciences of the United States of America, 90, 9285, 10.1073/pnas.90.20.9285 Tracz, 2007, Physiology and pathophysiology of heme: implications for kidney disease, Journal of the American Society of Nephrology: JASN, 18, 414, 10.1681/ASN.2006080894 Balla, 1991, Hemin: a possible physiological mediator of low density lipoprotein oxidation and endothelial injury, Arterioscler Thromb, 11, 1700, 10.1161/01.ATV.11.6.1700 Rose, 1985, Heme transfer between phospholipid membranes and uptake by apohemoglobin, The Journal of biological chemistry, 260, 6632, 10.1016/S0021-9258(18)88828-7 Solar, 1989, Serum proteins as mediators of hemin efflux from red cell membranes: specificity of hemopexin, FEBS letters, 256, 225, 10.1016/0014-5793(89)81753-3 Balla, 1991, Exposure of endothelial cells to free heme potentiates damage mediated by granulocytes and toxic oxygen species, Lab Invest, 64, 648 Ryter, 2000, The heme synthesis and degradation pathways: role in oxidant sensitivity. Heme oxygenase has both pro- and antioxidant properties, Free radical biology & medicine, 28, 289, 10.1016/S0891-5849(99)00223-3 Khechaduri, 2013, Heme levels are increased in human failing hearts, Journal of the American College of Cardiology, 61, 1884, 10.1016/j.jacc.2013.02.012 Bhoite-Solomon, 1993, Myocyte injury by hemin, In vitro cellular & developmental biology. Animal, 29A, 636, 10.1007/BF02634552 Bhoite-Solomon, 1990, Association of iron-protoporphyrin-IX (hemin) with myosins, FEBS letters, 266, 9, 10.1016/0014-5793(90)81493-8 Lund, 2008, Oxidation of myosin by haem proteins generates myosin radicals and protein cross-links, The Biochemical journal, 410, 565, 10.1042/BJ20071107 Avissar, 1984, The interaction of hemin with skeletal muscle actin, Biochimica et biophysica acta, 786, 179, 10.1016/0167-4838(84)90087-6 Kobayashi, 2005, Calcium, thin filaments, and the integrative biology of cardiac contractility, Annu Rev Physiol, 67, 39, 10.1146/annurev.physiol.67.040403.114025 Vigoreaux, 1994, The muscle Z band: lessons in stress management, J Muscle Res Cell Motil, 15, 237, 10.1007/BF00123477 Frank, 2011, Cardiac Z-disc signaling network, The Journal of biological chemistry, 286, 9897, 10.1074/jbc.R110.174268 Solaro, 2011, Regulation of Cardiac Contractility, 10.4199/C00030ED1V01Y201104ISP018 Linke, 1994, Passive and active tension in single cardiac myofibrils, Biophysical journal, 67, 782, 10.1016/S0006-3495(94)80538-7 Labeit, 1995, Titins: giant proteins in charge of muscle ultrastructure and elasticity, Science, 270, 293, 10.1126/science.270.5234.293 Granzier, 1995, Passive tension in cardiac muscle: contribution of collagen, titin, microtubules, and intermediate filaments, Biophysical journal, 68, 1027, 10.1016/S0006-3495(95)80278-X Palmer, 2005, Thick filament proteins and performance in human heart failure, Heart Fail Rev, 10, 187, 10.1007/s10741-005-5249-1 Fukuda, 2001, Length dependence of tension generation in rat skinned cardiac muscle: role of titin in the Frank-Starling mechanism of the heart, Circulation, 104, 1639, 10.1161/hc3901.095898 Stoyanova, 2012, Evidence for a novel mechanism independent of myocardial iron in beta-thalassemia cardiac pathogenesis, PLoS One, 7, e52128, 10.1371/journal.pone.0052128 Vinchi, 2013, Hemopexin therapy improves cardiovascular function by preventing heme-induced endothelial toxicity in mouse models of hemolytic diseases, Circulation, 127, 1317, 10.1161/CIRCULATIONAHA.112.130179 Papp, 2002, The mechanism of the force enhancement by MgADP under simulated ischaemic conditions in rat cardiac myocytes, The Journal of physiology, 543, 177, 10.1113/jphysiol.2002.022145 van Der Velden, 2001, Effects of calcium, inorganic phosphate, and pH on isometric force in single skinned cardiomyocytes from donor and failing human hearts, Circulation, 104, 1140, 10.1161/hc3501.095485 Fan, 1997, Decreased myocyte tension development and calcium responsiveness in rat right ventricular pressure overload, Circulation, 95, 2312, 10.1161/01.CIR.95.9.2312 Fabiato, 1979, Calculator programs for computing the composition of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells, Journal de physiologie, 75, 463 Szilagyi, 2004, The effects of levosimendan and OR-1896 on isolated hearts, myocyte-sized preparations and phosphodiesterase enzymes of the guinea pig, European journal of pharmacology, 486, 67, 10.1016/j.ejphar.2003.12.005 Olsson, 2011, Up-regulation of A1M/alpha1-microglobulin in skin by heme and reactive oxygen species gives protection from oxidative damage, PLoS One, 6, e27505, 10.1371/journal.pone.0027505 Kwasek, 2007, Production of recombinant human alpha1-microglobulin and mutant forms involved in chromophore formation, Protein expression and purification, 53, 145, 10.1016/j.pep.2006.10.023 Riddles, 1983, Reassessment of Ellman’s reagent, Methods in enzymology, 91, 49, 10.1016/S0076-6879(83)91010-8 Jones, 2011, Heme conjugated magnetic beads to isolate heme-binding proteins from complex mixtures, Protein expression and purification, 76, 79, 10.1016/j.pep.2010.10.001 Qian, 2011, Simple synthesis of 1,3-cyclopentanedione derived probes for labeling sulfenic acid proteins, Chem Commun (Camb), 47, 9203, 10.1039/c1cc12127h Phumala, 2003, Hemin: a possible cause of oxidative stress in blood circulation of beta-thalassemia/hemoglobin E disease, Free radical research, 37, 129, 10.1080/1071576031000060607 Hertelendi, 2008, Oxidation of myofilament protein sulfhydryl groups reduces the contractile force and its Ca2+ sensitivity in human cardiomyocytes, Antioxidants & redox signaling, 10, 1175, 10.1089/ars.2007.2014 Winterbourn, 2008, Thiol chemistry and specificity in redox signaling, Free radical biology & medicine, 45, 549, 10.1016/j.freeradbiomed.2008.05.004 Chen, 2002, Hydrogen peroxide enhances iron-induced injury in isolated heart and ventricular cardiomyocyte in rats, Molecular and cellular biochemistry, 231, 61, 10.1023/A:1014484907291 Catalano, 1989, Reactions of the protein radical in peroxide-treated myoglobin. Formation of a heme-protein cross-link, The Journal of biological chemistry, 264, 10534, 10.1016/S0021-9258(18)81654-4 Sugiyama, 1997, Hydrogen peroxide-mediated alteration of the heme prosthetic group of metmyoglobin to an iron chlorin product: evidence for a novel oxidative pathway, Proceedings of the National Academy of Sciences of the United States of America, 94, 796, 10.1073/pnas.94.3.796 Goto, 1995, Synthesis of a Stable Arenesulfenic Acid Bearing a Bowl-Shaped Macrobicyclic Cyclophane Skeleton, Angewandte Chemie International Edition in English, 34, 1124, 10.1002/anie.199511241 Lo Conte, 2013, The redox biochemistry of protein sulfenylation and sulfinylation, The Journal of biological chemistry, 288, 26480, 10.1074/jbc.R113.467738 Collino, 2013, Beneficial effect of prolonged heme oxygenase 1 activation in a rat model of chronic heart failure, Dis Model Mech, 6, 1012, 10.1242/dmm.011528 Tolosano, 2010, Heme scavenging and the other facets of hemopexin, Antioxidants & redox signaling, 12, 305, 10.1089/ars.2009.2787 Smith, 2015, Hemopexin and haptoglobin: allies against heme toxicity from hemoglobin not contenders, Frontiers in Physiology, 6, 10.3389/fphys.2015.00187 Muller-Eberhard, 1993, Bioactivity of heme and its containment, Am J Hematol, 42, 59, 10.1002/ajh.2830420112 Fujita, 2012, Filamin C plays an essential role in the maintenance of the structural integrity of cardiac and skeletal muscles, revealed by the medaka mutant zacro, Dev Biol, 361, 79, 10.1016/j.ydbio.2011.10.008 Borbely, 2005, Peroxynitrite-induced alpha-actinin nitration and contractile alterations in isolated human myocardial cells, Cardiovascular research, 67, 225, 10.1016/j.cardiores.2005.03.025 Hein, 2000, The role of the cytoskeleton in heart failure, Cardiovascular research, 45, 273, 10.1016/S0008-6363(99)00268-0 Calaghan, 2004, Cytoskeletal modulation of electrical and mechanical activity in cardiac myocytes, Prog Biophys Mol Biol, 84, 29, 10.1016/S0079-6107(03)00057-9 Previs, 2014, Molecular modulation of actomyosin function by cardiac myosin-binding protein C, Pflugers Arch, 466, 439, 10.1007/s00424-013-1433-7 Steinberg, 2013, Oxidative stress and sarcomeric proteins, Circulation research, 112, 393, 10.1161/CIRCRESAHA.111.300496 Tiago, 2010, Peroxynitrite-mediated oxidative modifications of myosin and implications on structure and function, Free radical research, 44, 1317, 10.3109/10715762.2010.502170 Kanski, 2005, Proteomic identification of 3-nitrotyrosine-containing rat cardiac proteins: effects of biological aging, American journal of physiology. Heart and circulatory physiology, 288, H371, 10.1152/ajpheart.01030.2003 Hernandez, 2007, Myosin essential light chain in health and disease, American journal of physiology. Heart and circulatory physiology, 292, H1643, 10.1152/ajpheart.00931.2006 Muthu, 2011, Structural and functional aspects of the myosin essential light chain in cardiac muscle contraction, FASEB J, 25, 4394, 10.1096/fj.11-191973 Borbely, 2005, Cardiomyocyte stiffness in diastolic heart failure, Circulation, 111, 774, 10.1161/01.CIR.0000155257.33485.6D Porter, 2009, Pathophysiology of transfusional iron overload: contrasting patterns in thalassemia major and sickle cell disease, Hemoglobin, 33, S37, 10.3109/03630260903346627 Tong, 2014, Cardiac myosin-binding protein-C is a critical mediator of diastolic function, Pflugers Arch, 466, 451, 10.1007/s00424-014-1442-1 Barefield, 2010, Phosphorylation and function of cardiac myosin binding protein-C in health and disease, Journal of molecular and cellular cardiology, 48, 866, 10.1016/j.yjmcc.2009.11.014 Yamasaki, 2001, Titin-actin interaction in mouse myocardium: passive tension modulation and its regulation by calcium/S100A1, Biophysical journal, 81, 2297, 10.1016/S0006-3495(01)75876-6 Larsen, 2012, Heme cytotoxicity and the pathogenesis of immune-mediated inflammatory diseases, Frontiers in pharmacology, 3, 77, 10.3389/fphar.2012.00077 Kuster, 2014, Release kinetics of circulating cardiac myosin binding protein-C following cardiac injury, American journal of physiology. Heart and circulatory physiology, 306, H547, 10.1152/ajpheart.00846.2013