Protein carbonylation causes sarcoplasmic reticulum Ca

Ca2+ signaling Heart Methylglyoxal Na+ homeostasis Na+ pump Na+/Ca2+ exchanger Sarcoplasmic reticulum

Journal

Pflugers Archiv : European journal of physiology
ISSN: 1432-2013
Titre abrégé: Pflugers Arch
Pays: Germany
ID NLM: 0154720

Informations de publication

Date de publication:
20 May 2024
Historique:
received: 26 02 2024
accepted: 15 05 2024
revised: 22 04 2024
medline: 21 5 2024
pubmed: 21 5 2024
entrez: 20 5 2024
Statut: aheadofprint

Résumé

Diabetes is commonly associated with an elevated level of reactive carbonyl species due to alteration of glucose and fatty acid metabolism. These metabolic changes cause an abnormality in cardiac Ca

Identifiants

DOI: 10.1007/s00424-024-02972-7 PMID: 38769127
pubmed: 38769127
doi: 10.1007/s00424-024-02972-7
pii: 10.1007/s00424-024-02972-7
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NIH HHS
ID : R01 HL092321
Pays : United States
Organisme : NIH HHS
ID : R01HL151990
Pays : United States

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Références

Ai X, Curran JW, Shannon TR, Bers DM, Pogwizd SM (2005) Ca2+/calmodulin-dependent protein kinase modulates cardiac ryanodine receptor phosphorylation and sarcoplasmic reticulum Ca2+ leak in heart failure. Circ Res 97:1314–1322. https://doi.org/10.1161/01.RES.0000194329.41863.89
doi: 10.1161/01.RES.0000194329.41863.89 pubmed: 16269653
Armoundas AA, Rose J, Aggarwal R, Stuyvers BD, O’Rourke B, Kass DA, Marban E, Shorofsky SR, Tomaselli GF, William Balke C (2007) Cellular and molecular determinants of altered Ca2+ handling in the failing rabbit heart: primary defects in SR Ca2+ uptake and release mechanisms. Am J Physiol Heart Circ Physiol 292:H1607-1618. https://doi.org/10.1152/ajpheart.00525.2006
doi: 10.1152/ajpheart.00525.2006 pubmed: 17122195
Baginski ES, Foa PP, Zak B (1967) Determnation of rat liver microsomal glucose-6-phosphatase activity: study of citrate and G-6-P inhibition. Anal Biochem 21:201–207. https://doi.org/10.1016/0003-2697(67)90181-9
doi: 10.1016/0003-2697(67)90181-9 pubmed: 4295432
Bassani JW, Bassani RA, Bers DM (1994) Relaxation in rabbit and rat cardiac cells: species-dependent differences in cellular mechanisms. J Physiol 476:279–293
doi: 10.1113/jphysiol.1994.sp020130 pubmed: 8046643 pmcid: 1160440
Belevych AE, Terentyev D, Viatchenko-Karpinski S, Terentyeva R, Sridhar A, Nishijima Y, Wilson LD, Cardounel AJ, Laurita KR, Carnes CA, Billman GE, Gyorke S (2009) Redox modification of ryanodine receptors underlies calcium alternans in a canine model of sudden cardiac death. Cardiovasc Res 84:387–395. https://doi.org/10.1093/cvr/cvp246
doi: 10.1093/cvr/cvp246 pubmed: 19617226 pmcid: 2777950
Bers DM (2002) Cardiac excitation-contraction coupling. Nature 415:198–205. https://doi.org/10.1038/415198a
doi: 10.1038/415198a pubmed: 11805843
Bovo E, Dvornikov AV, Mazurek SR, de Tombe PP, Zima AV (2013) Mechanisms of Ca(2)+ handling in zebrafish ventricular myocytes. Pflugers Arch 465:1775–1784. https://doi.org/10.1007/s00424-013-1312-2
doi: 10.1007/s00424-013-1312-2 pubmed: 23821298 pmcid: 4138713
Bovo E, Lipsius SL, Zima AV (2012) Reactive oxygen species contribute to the development of arrhythmogenic Ca(2)(+) waves during beta-adrenergic receptor stimulation in rabbit cardiomyocytes. J Physiol 590:3291–3304. https://doi.org/10.1113/jphysiol.2012.230748
doi: 10.1113/jphysiol.2012.230748 pubmed: 22586224 pmcid: 3459043
Bovo E, Mazurek SR, Zima AV (2018) Oxidation of ryanodine receptor after ischemia-reperfusion increases propensity of Ca(2+) waves during beta-adrenergic receptor stimulation. Am J Physiol Heart Circ Physiol 315:H1032–H1040. https://doi.org/10.1152/ajpheart.00334.2018
doi: 10.1152/ajpheart.00334.2018 pubmed: 30028204 pmcid: 6230903
Bovo E, Nikolaienko R, Bhayani S, Kahn D, Cao Q, Martin JL, Kuo IY, Robia SL, Zima AV (2019) Novel approach for quantification of endoplasmic reticulum Ca(2+) transport. Am J Physiol Heart Circ Physiol 316:H1323–H1331. https://doi.org/10.1152/ajpheart.00031.2019
doi: 10.1152/ajpheart.00031.2019 pubmed: 30901276 pmcid: 6620677
Brette F, Luxan G, Cros C, Dixey H, Wilson C, Shiels HA (2008) Characterization of isolated ventricular myocytes from adult zebrafish (Danio rerio). Biochem Biophys Res Commun 374:143–146. https://doi.org/10.1016/j.bbrc.2008.06.109
doi: 10.1016/j.bbrc.2008.06.109 pubmed: 18602892 pmcid: 2581121
Brownlee M, Cerami A, Vlassara H (1988) Advanced products of nonenzymatic glycosylation and the pathogenesis of diabetic vascular disease. Diabetes Metab Rev 4:437–451. https://doi.org/10.1002/dmr.5610040503
doi: 10.1002/dmr.5610040503 pubmed: 2850143
Cutler MJ, Plummer BN, Wan X, Sun QA, Hess D, Liu H, Deschenes I, Rosenbaum DS, Stamler JS, Laurita KR (2012) Aberrant S-nitrosylation mediates calcium-triggered ventricular arrhythmia in the intact heart. Proc Natl Acad Sci USA 109:18186–18191. https://doi.org/10.1073/pnas.1210565109
doi: 10.1073/pnas.1210565109 pubmed: 23071315 pmcid: 3497770
Despa S, Islam MA, Weber CR, Pogwizd SM, Bers DM (2002) Intracellular Na(+) concentration is elevated in heart failure but Na/K pump function is unchanged. Circulation 105:2543–2548. https://doi.org/10.1161/01.cir.0000016701.85760.97
doi: 10.1161/01.cir.0000016701.85760.97 pubmed: 12034663
DiNello E, Bovo E, Thuo P, Martin TG, Kirk JA, Zima AV, Cao Q, Kuo IY (2020) Deletion of cardiac polycystin 2/PC2 results in increased SR calcium release and blunted adrenergic reserve. Am J Physiol Heart Circ Physiol 319:H1021–H1035. https://doi.org/10.1152/ajpheart.00302.2020
doi: 10.1152/ajpheart.00302.2020 pubmed: 32946258 pmcid: 7789970
El-Armouche A, Eschenhagen T (2009) Beta-adrenergic stimulation and myocardial function in the failing heart. Heart Fail Rev 14:225–241. https://doi.org/10.1007/s10741-008-9132-8
doi: 10.1007/s10741-008-9132-8 pubmed: 19110970
Gaber EM, Jayaprakash P, Qureshi MA, Parekh K, Oz M, Adrian TE, Howarth FC (2014) Effects of a sucrose-enriched diet on the pattern of gene expression, contraction and Ca(2+) transport in Goto-Kakizaki type 2 diabetic rat heart. Exp Physiol 99:881–893. https://doi.org/10.1113/expphysiol.2013.077594
doi: 10.1113/expphysiol.2013.077594 pubmed: 24681897
Galderisi M (2006) Diastolic dysfunction and diabetic cardiomyopathy: evaluation by Doppler echocardiography. J Am Coll Cardiol 48:1548–1551. https://doi.org/10.1016/j.jacc.2006.07.033
doi: 10.1016/j.jacc.2006.07.033 pubmed: 17045886
Gheorghiade M, Adams KF Jr, Colucci WS (2004) Digoxin in the management of cardiovascular disorders. Circulation 109:2959–2964. https://doi.org/10.1161/01.CIR.0000132482.95686.87
doi: 10.1161/01.CIR.0000132482.95686.87 pubmed: 15210613
Grisanti LA (2018) Diabetes and Arrhythmias: Pathophysiology, Mechanisms and Therapeutic Outcomes. Front Physiol 9:1669. https://doi.org/10.3389/fphys.2018.01669
doi: 10.3389/fphys.2018.01669 pubmed: 30534081 pmcid: 6275303
Guide for the Care and Use of Laboratory Animals (2011) NBK54050 [bookaccession]. https://doi.org/10.17226/12910
Horvath B, Bers DM (2014) The late sodium current in heart failure: pathophysiology and clinical relevance. ESC Heart Fail 1:26–40. https://doi.org/10.1002/ehf2.12003
doi: 10.1002/ehf2.12003 pubmed: 28834665
Horvath B, Szentandrassy N, Almassy J, Dienes C, Kovacs ZM, Nanasi PP, Banyasz T (2022) Late Sodium Current of the Heart: Where Do We Stand and Where Are We Going? Pharmaceuticals (Basel) 15. https://doi.org/10.3390/ph15020231
Imahashi K, Kusuoka H, Hashimoto K, Yoshioka J, Yamaguchi H, Nishimura T (1999) Intracellular sodium accumulation during ischemia as the substrate for reperfusion injury. Circ Res 84:1401–1406. https://doi.org/10.1161/01.res.84.12.1401
doi: 10.1161/01.res.84.12.1401 pubmed: 10381892
Jelicks LA, Siri FM (1995) Effects of hypertrophy and heart failure on [Na+]i in pressure-overloaded guinea pig heart. Am J Hypertens 8:934–943. https://doi.org/10.1016/0895-7061(95)00219-F
doi: 10.1016/0895-7061(95)00219-F pubmed: 8541010
Jorgensen PL (1988) Purification of Na+, K+-ATPase: enzyme sources, preparative problems, and preparation from mammalian kidney. Methods Enzymol 156:29–43. https://doi.org/10.1016/0076-6879(88)56005-6
doi: 10.1016/0076-6879(88)56005-6 pubmed: 2835612
Kim HW, Ch YS, Lee HR, Park SY, Kim YH (2001) Diabetic alterations in cardiac sarcoplasmic reticulum Ca2+-ATPase and phospholamban protein expression. Life Sci 70:367–379. https://doi.org/10.1016/s0024-3205(01)01483-7
doi: 10.1016/s0024-3205(01)01483-7 pubmed: 11798007
Miki T, Yuda S, Kouzu H, Miura T (2013) Diabetic cardiomyopathy: pathophysiology and clinical features. Heart Fail Rev 18:149–166. https://doi.org/10.1007/s10741-012-9313-3
doi: 10.1007/s10741-012-9313-3 pubmed: 22453289
Papadaki M, Kampaengsri T, Barrick SK, Campbell SG, von Lewinski D, Rainer PP, Harris SP, Greenberg MJ, Kirk JA (2022) Myofilament glycation in diabetes reduces contractility by inhibiting tropomyosin movement, is rescued by cMyBPC domains. J Mol Cell Cardiol 162:1–9. https://doi.org/10.1016/j.yjmcc.2021.08.012
doi: 10.1016/j.yjmcc.2021.08.012 pubmed: 34487755
Picht E, Zima AV, Blatter LA, Bers DM (2007) SparkMaster: automated calcium spark analysis with ImageJ. Am J Physiol Cell Physiol 293:C1073-1081. https://doi.org/10.1152/ajpcell.00586.2006
doi: 10.1152/ajpcell.00586.2006 pubmed: 17376815
Semchyshyn HM (2014) Reactive carbonyl species in vivo: generation and dual biological effects. Sci World J 2014:417842. https://doi.org/10.1155/2014/417842
doi: 10.1155/2014/417842
Shao CH, Capek HL, Patel KP, Wang M, Tang K, DeSouza C, Nagai R, Mayhan W, Periasamy M, Bidasee KR (2011) Carbonylation contributes to SERCA2a activity loss and diastolic dysfunction in a rat model of type 1 diabetes. Diabetes 60:947–959. https://doi.org/10.2337/db10-1145
doi: 10.2337/db10-1145 pubmed: 21300842 pmcid: 3046856
Shao CH, Tian C, Ouyang S, Moore CJ, Alomar F, Nemet I, D’Souza A, Nagai R, Kutty S, Rozanski GJ, Ramanadham S, Singh J, Bidasee KR (2012) Carbonylation induces heterogeneity in cardiac ryanodine receptor function in diabetes mellitus. Mol Pharmacol 82:383–399. https://doi.org/10.1124/mol.112.078352
doi: 10.1124/mol.112.078352 pubmed: 22648972 pmcid: 3422706
Shao CH, Wehrens XH, Wyatt TA, Parbhu S, Rozanski GJ, Patel KP (1985) Bidasee KR (2009) Exercise training during diabetes attenuates cardiac ryanodine receptor dysregulation. J Appl Physiol 106:1280–1292. https://doi.org/10.1152/japplphysiol.91280.2008
doi: 10.1152/japplphysiol.91280.2008
Sweadner KJ (1989) Isozymes of the Na+/K+-ATPase. Biochim Biophys Acta 988:185–220. https://doi.org/10.1016/0304-4157(89)90019-1
doi: 10.1016/0304-4157(89)90019-1 pubmed: 2541792
Tian CJ, Zhen Z (2019) Reactive Carbonyl Species: Diabetic Complication in the Heart and Lungs. Trends Endocrinol Metab 30:546–556. https://doi.org/10.1016/j.tem.2019.05.005
doi: 10.1016/j.tem.2019.05.005 pubmed: 31253519
Undrovinas AI, Fleidervish IA, Makielski JC (1992) Inward sodium current at resting potentials in single cardiac myocytes induced by the ischemic metabolite lysophosphatidylcholine. Circ Res 71:1231–1241. https://doi.org/10.1161/01.res.71.5.1231
doi: 10.1161/01.res.71.5.1231 pubmed: 1327577
Undrovinas AI, Maltsev VA, Sabbah HN (1999) Repolarization abnormalities in cardiomyocytes of dogs with chronic heart failure: role of sustained inward current. Cell Mol Life Sci 55:494–505. https://doi.org/10.1007/s000180050306
doi: 10.1007/s000180050306 pubmed: 10228563
Undrovinas AI, Shander GS, Makielski JC (1995) Cytoskeleton modulates gating of voltage-dependent sodium channel in heart. Am J Physiol 269:H203-214. https://doi.org/10.1152/ajpheart.1995.269.1.H203
doi: 10.1152/ajpheart.1995.269.1.H203 pubmed: 7631850
West JW, Numann R, Murphy BJ, Scheuer T, Catterall WA (1991) A phosphorylation site in the Na+ channel required for modulation by protein kinase C. Science 254:866–868. https://doi.org/10.1126/science.1658937
doi: 10.1126/science.1658937 pubmed: 1658937
Wold LE, Dutta K, Mason MM, Ren J, Cala SE, Schwanke ML, Davidoff AJ (2005) Impaired SERCA function contributes to cardiomyocyte dysfunction in insulin resistant rats. J Mol Cell Cardiol 39:297–307. https://doi.org/10.1016/j.yjmcc.2005.03.014
doi: 10.1016/j.yjmcc.2005.03.014 pubmed: 15878173
Yan Y, Shapiro AP, Mopidevi BR, Chaudhry MA, Maxwell K, Haller ST, Drummond CA, Kennedy DJ, Tian J, Malhotra D, Xie ZJ, Shapiro JI, Liu J (2016) Protein Carbonylation of an Amino Acid Residue of the Na/K-ATPase alpha1 Subunit Determines Na/K-ATPase Signaling and Sodium Transport in Renal Proximal Tubular Cells. J Am Heart Assoc 5. https://doi.org/10.1161/JAHA.116.003675
Zima AV, Bovo E, Bers DM, Blatter LA (2010) Ca(2)+ spark-dependent and -independent sarcoplasmic reticulum Ca(2)+ leak in normal and failing rabbit ventricular myocytes. J Physiol 588:4743–4757. https://doi.org/10.1113/jphysiol.2010.197913
doi: 10.1113/jphysiol.2010.197913 pubmed: 20962003 pmcid: 3010143
Zima AV, Bovo E, Mazurek SR, Rochira JA, Li W, Terentyev D (2014) Ca handling during excitation-contraction coupling in heart failure. Pflugers Arch 466:1129–1137. https://doi.org/10.1007/s00424-014-1469-3
doi: 10.1007/s00424-014-1469-3 pubmed: 24515294 pmcid: 5370565
Zima AV, Copello JA, Blatter LA (2004) Effects of cytosolic NADH/NAD(+) levels on sarcoplasmic reticulum Ca(2+) release in permeabilized rat ventricular myocytes. J Physiol 555:727–741. https://doi.org/10.1113/jphysiol.2003.055848
doi: 10.1113/jphysiol.2003.055848 pubmed: 14724208 pmcid: 1664876
Zima AV, Kockskamper J, Mejia-Alvarez R, Blatter LA (2003) Pyruvate modulates cardiac sarcoplasmic reticulum Ca2+ release in rats via mitochondria-dependent and -independent mechanisms. J Physiol 550:765–783. https://doi.org/10.1113/jphysiol.2003.040345
doi: 10.1113/jphysiol.2003.040345 pubmed: 12824454 pmcid: 2343083
Zima AV, Picht E, Bers DM, Blatter LA (2008) Termination of cardiac Ca2+ sparks: role of intra-SR [Ca2+], release flux, and intra-SR Ca2+ diffusion. Circ Res 103:e105-115. https://doi.org/10.1161/CIRCRESAHA.107.183236
doi: 10.1161/CIRCRESAHA.107.183236 pubmed: 18787194 pmcid: 2678058

Auteurs

Elisa Bovo (E)

Department of Cell & Molecular Physiology, Stritch School of Medicine, Loyola University Chicago, 2160 South First Avenue, Maywood, IL, 60153, USA.

Jaroslava Seflova (J)

Department of Cell & Molecular Physiology, Stritch School of Medicine, Loyola University Chicago, 2160 South First Avenue, Maywood, IL, 60153, USA.

Seth L Robia (SL)

Department of Cell & Molecular Physiology, Stritch School of Medicine, Loyola University Chicago, 2160 South First Avenue, Maywood, IL, 60153, USA.

Aleksey V Zima (AV)

Department of Cell & Molecular Physiology, Stritch School of Medicine, Loyola University Chicago, 2160 South First Avenue, Maywood, IL, 60153, USA. azima@luc.edu.

Classifications MeSH