Ranolazine protects from doxorubicin-induced oxidative stress and cardiac dysfunction

European Journal of Heart Failure

Volumn 16, Issue 4, 2014, Pages 358-366

  Tocchetti, Carlo G ^a   Carpi, Andrea ^b   Coppola, Carmela ^c   Quintavalle, Cristina ^d   Rea, Domenica ^c   Campesan, Marika ^b   Arcari, Antonella ^e   Piscopo, Giovanna ^c   Cipresso, Clemente ^c   Monti, Maria Gaia ^d   De Lorenzo, Claudia ^d   Arra, Claudio ^c   Condorelli, Gerolama ^d   Di Lisa, Fabio ^b   Maurea, Nicola ^c  

^a Clinica Montevergine   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c NATIONAL CANCER INSTITUTE   (Italy)

^d UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^e IRCCS NEUROMED   (Italy)

Author keywords

Doxorubicin cardiotoxicity Ranolazine Heart failure Oxidative stress Na+

Indexed keywords

2 [2 [4 (4 NITROBENZYLOXY)PHENYL]ETHYL]ISOTHIOUREA METHANESULFONATE; ATRIAL NATRIURETIC FACTOR; BRAIN NATRIURETIC PEPTIDE; CASPASE 3; CONNECTIVE TISSUE GROWTH FACTOR; DOXORUBICIN; GELATINASE A; HYDROGEN PEROXIDE; MESSENGER RNA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; RANOLAZINE; ACETANILIDE DERIVATIVE; ANTINEOPLASTIC ANTIBIOTIC; ENZYME INHIBITOR; PIPERAZINE DERIVATIVE; REACTIVE OXYGEN METABOLITE; SODIUM;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CARDIOTOXICITY; CELL DEATH; CONTROLLED STUDY; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; HEART DISEASE; HEART MUSCLE CELL; HEART PROTECTION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; ANIMAL; BLOOD; C57BL MOUSE; CHEMICALLY INDUCED; CYTOLOGY; DRUG EFFECTS; ECHOGRAPHY; GENETICS; HEART LEFT VENTRICLE FUNCTION; METABOLISM; PREVENTION AND CONTROL; PROCEDURES; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ACETANILIDES; ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; ATRIAL NATRIURETIC FACTOR; BLOTTING, WESTERN; CARDIOTOXICITY; CONNECTIVE TISSUE GROWTH FACTOR; DOXORUBICIN; ENZYME INHIBITORS; MATRIX METALLOPROTEINASE 2; MICE; MICE, INBRED C57BL; MYOCYTES, CARDIAC; NATRIURETIC PEPTIDE, BRAIN; OXIDATIVE STRESS; PIPERAZINES; POLY(ADP-RIBOSE) POLYMERASES; REACTIVE OXYGEN SPECIES; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SODIUM; VENTRICULAR DYSFUNCTION, LEFT;

EID: 84906070648     PISSN: 13889842     EISSN: 18790844     Source Type: Journal    
DOI: 10.1002/ejhf.50     Document Type: Article

References (41)

1. Khouri MG, Douglas PS, Mackey JR, Martin M, Scott JM, Scherrer-Crosbie M, Jones LW,. Cancer therapy-induced cardiac toxicity in early breast cancer: addressing the unresolved issues. Circulation 2012; 126: 2749-2763.
2. Eschenhagen T, Force T, Ewer MS, de Keulenaer GW, Suter TM, Anker SD, Avkiran M, de Azambuja E, Balligand JL, Brutsaert DL, Condorelli G, Hansen A, Heymans S, Hill JA, Hirsch E, Hilfiker-Kleiner D, Janssens S, de Jong S, Neubauer G, Pieske B, Ponikowski P, Pirmohamed M, Rauchhaus M, Sawyer D, Sugden PH, Wojta J, Zannad F, Shah AM,. Cardiovascular side effects of cancer therapies: a position statement from the Heart Failure Association of the European Society of Cardiology. Eur J Heart Fail 2011; 13: 1-10.
3. Tocchetti CG, Ragone G, Coppola C, Rea D, Piscopo G, Scala S, De Lorenzo C, Iaffaioli RV, Arra C, Maurea N,. Detection, monitoring, and management of trastuzumab-induced left ventricular dysfunction: an actual challenge. Eur J Heart Fail 2012; 14: 130-137.
4. Authors/Task Force Members, McMurray JJ, Adamopoulos S, Anker SD, Auricchio A, Böhm M, Dickstein K, Falk V, Filippatos G, Fonseca C, Gomez-Sanchez MA, Jaarsma T, Køber L, Lip GY, Maggioni AP, Parkhomenko A, Pieske BM, Popescu BA, Rønnevik PK, Rutten FH, Schwitter J, Seferovic P, Stepinska J, Trindade PT, Voors AA, Zannad F, Zeiher A,; ESC Committee for Practice Guidelines (CPG), Bax JJ, Baumgartner H, Ceconi C, Dean V, Deaton C, Fagard R, Funck-Brentano C, Hasdai D, Hoes A, Kirchhof P, Knuuti J, Kolh P, McDonagh T, Moulin C, Popescu BA, Reiner Z, Sechtem U, Sirnes PA, Tendera M, Torbicki A, Vahanian A, Windecker S,;, Document Reviewers, McDonagh T, Sechtem U, Bonet LA, Avraamides P, Ben Lamin HA, Brignole M, Coca A, Cowburn P, Dargie H, Elliott P, Flachskampf FA, Guida GF, Hardman S, Iung B, Merkely B, Mueller C, Nanas JN, Nielsen OW, Orn S, Parissis JT, Ponikowski P, ESC Guidelines for the diagnosis and treatment of acute and chronic heart failure 2012: the Task Force for the Diagnosis and Treatment of Acute and Chronic Heart Failure 2012 of the European Society of Cardiology. Developed in collaboration with the Heart Failure Association (HFA) of the ESC. Eur J Heart Fail 2012; 14: 803-869.
5. Octavia Y, Tocchetti CG, Gabrielson KL, Janssens S, Crijns HJ, Moens AL,. Doxorubicin-induced cardiomyopathy: from molecular mechanisms to therapeutic strategies. J Mol Cell Cardiol 2012; 52: 1213-1225.
6. Bers DM,. Excitation-Contraction Coupling and Cardiac Contractile Force, 2nd ed. Dordrecht: Kluwer Academic Publishers; 2001.
7. Pieske B, Houser SR,. [Na+]i handling in the failing human heart. Cardiovasc Res 2003; 57: 874-886.
8. Sossalla S, Maier LS,. Role of ranolazine in angina, heart failure, arrhythmias, and diabetes. Pharmacol Ther 2012; 133: 311-323.
9. + increases mitochondrial formation of reactive oxygen species in failing cardiac myocytes. Circulation 2010; 121: 1606-1613.
10. Hwang H, Arcidi JM Jr, Hale SL, Simkhovich BZ, Belardinelli L, Dhalla AK, Shryock JC, Kloner RA,. Ranolazine as a cardioplegia additive improves recovery of diastolic function in isolated rat hearts. Circulation 2009; 120: S16-S21.
11. Wu Y, Song Y, Belardinelli L, Shryock JC,. The late Na-‰+-‰current (INa) inhibitor ranolazine attenuates effects of palmitoyl- l -carnitine to increase late INa and cause ventricular diastolic dysfunction. J Pharmacol Exp Ther 2009; 330: 550-557.
12. Sabbah HN, Chandler MP, Mishima T, Suzuki G, Chaudhry P, Nass O, Biesiadecki BJ, Blackburn B, Wolff A, Stanley WC,. Ranolazine, a partial fatty acid oxidation (pFOX) inhibitor, improves left ventricular function in dogs with chronic heart failure. J Card Fail 2002; 8: 416-422.
13. Rastogi S, Sharov VG, Mishra S, Gupta RC, Blackburn B, Belardinelli L, Stanley WC, Sabbah HN,. Ranolazine combined with enalapril or metoprolol prevents progressive LV dysfunction and remodeling in dogs with moderate heart failure. Am J Physiol Heart Circ Physiol 2008; 295: H2149-H2155.
14. Morrow DA, Scirica BM, Sabatine MS, de Lemos JA, Murphy SA, Jarolim P, Theroux P, Bode C, Braunwald E,. B-type natriuretic peptide and the effect of ranolazine in patients with non-ST-segment elevation acute coronary syndromes: observations from the MERLIN-TIMI 36 (Metabolic Efficiency With Ranolazine for Less Ischemia in Non-ST Elevation Acute Coronary-Thrombolysis In Myocardial Infarction 36) trial. J Am Coll Cardiol 2010; 55: 1189-1196.
15. Fedele C, Riccio G, Coppola C, Barbieri A, Monti MG, Arra C, Tocchetti CG, D'Alessio G, Maurea N, De Lorenzo C,. Comparison of preclinical cardiotoxic effects of different ErbB2 inhibitors. Breast Cancer Res Treat 2012; 133: 511-521.
16. Reagan-Shaw S, Nihal M, Ahmad N,. Dose translation from animal to human studies revisited. FASEB J 2008; 22: 659-661.
17. Livak KJ, Schmittgen TD,. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25: 402-408.
18. Claycomb WC, Lanson NA Jr, Stallworth BS, Egeland DB, Delcarpio JB, Bahinski A, Izzo NJ Jr,. HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte. Proc Natl Acad Sci USA 1998; 95: 2979-2984.
19. Sapia L, Palomeque J, Mattiazzi A, Petroff MV,. Na+/K-‰+-‰-ATPase inhibition by ouabain induces CaMKII-dependent apoptosis in adult rat cardiac myocytes. J Mol Cell Cardiol 2010; 49: 459-468.
20. Bergmeyer HU, Bernt E,. Lactate dehydrogenase. In:, Bergmeyer HU, ed. Methods of Enzymatic Analysis. Weinheim: Verlag Chemie; 1974. p607- 612.
21. Kaludercic N, Carpi A, Nagayama T, Sivakumaran V, Zhu G, Lai EW, Bedja D, De Mario A, Chen K, Gabrielson KL, Lindsey ML, Pacak K, Takimoto E, Shih JC, Kass DA, Di Lisa F, Paolocci N,. Monoamine oxidase B prompts mitochondrial and cardiac dysfunction in pressure overloaded hearts. Antioxid Redox Signal 2013; in press.
22. Canton M, Neverova I, Menabò R, Van Eyk JE, Di Lisa F,. Evidence of myofibrillar protein oxidation induced by postischemic reperfusion in isolated rat hearts. Am J Physiol Heart Circ Physiol 2004; 286: H870-H877.
23. Di Lisa F, Kaludercic N, Carpi A, Menabò R, Giorgio M,. Mitochondrial pathways for ROS formation and myocardial injury: the relevance of p66(Shc) and monoamine oxidase. Basic Res Cardiol 2009; 104: 131-139.
24. Zhang Y, Tocchetti CG, Krieg T, Moens AL,. Oxidative and nitrosative stress in the maintenance of myocardial function. Free Radic Biol Med 2012; 53: 1531-1540.
25. Minotti G, Menna P, Salvatorelli E, Cairo G, Gianni L,. Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity. Pharmacol Rev 2004; 56: 185-229.
26. Kalivendi SV, Konorev EA, Cunningham S, Vanamala SK, Kaji EH, Joseph J, Kalyanaraman B,. Doxorubicin activates nuclear factor of activated T-lymphocytes and Fas ligand transcription: role of mitochondrial reactive oxygen species and calcium. Biochem J 2005; 389: 527-539.
27. Zhang S, Liu X, Bawa-Khalfe T, Lu LS, Lyu YL, Liu LF, Yeh ET,. Identification of the molecular basis of doxorubicin-induced cardiotoxicity. Nat Med 2012; 18: 1639-1642.
28. Andreadou I, Sigala F, Iliodromitis EK, Papaefthimiou M, Sigalas C, Aligiannis N, Savvari P, Gorgoulis V, Papalabros E,. Kremastinos DT Acute doxorubicin cardiotoxicity is successfully treated with the phytochemical oleuropein through suppression of oxidative and nitrosative stress. J Mol Cell Cardiol 2007; 42: 549-558.
29. Mukhopadhyay P, Rajesh M, Bátkai S, Kashiwaya Y, Haskõ G, Liaudet L, Szabõ C, Pacher P,. Role of superoxide, nitric oxide, and peroxynitrite in doxorubicin-induced cell death in vivo and in vitro. Am J Physiol Heart Circ Physiol 2009; 296: H1466-H1483.
30. Sun X, Zhou Z, Kang YJ,. Attenuation of doxorubicin chronic toxicity in metallothionein-overexpressing transgenic mouse heart. Cancer Res. 2001; 61: 3382-3387.
31. Suter TM, Ewer MS,. Cancer drugs and the heart: importance and management. Eur Heart J 2013; 34: 1102-1111.
32. 2+ uptake during excitation-contraction coupling and impairs energetic adaptation in cardiac myocytes. Circ Res 2006; 99: 172-182.
33. Erickson JR, Joiner ML, Guan X, Kutschke W, Yang J, Oddis CV, Bartlett RK, Lowe JS, O'Donnell SE, Aykin-Burns N, Zimmerman MC, Zimmerman K, Ham AJ, Weiss RM, Spitz DR, Shea MA, Colbran RJ, Mohler PJ, Anderson ME,. A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell 2008; 133: 462-474.
34. Song Y, Shryock JC, Wagner S, Maier LS, Belardinelli L,. Blocking late sodium current reduces hydrogen peroxide-induced arrhythmogenic activity and contractile dysfunction. J Pharmacol Exp Ther 2006; 318: 214-222.
35. + channels. J Clin Invest 2006; 116: 3127-3138.
36. Zeitz O, Maass AE, Van Nguyen P, Hensmann G, Kögler H, Möller K, Hasenfuss G, Janssen PM,. Hydroxyl radical-induced acute diastolic dysfunction is due to calcium overload via reverse-mode Na(+)-Ca(2+) exchange. Circ Res 2002; 90: 988-995.
37. Murphy E, Eisner DA,. Regulation of intracellular and mitochondrial sodium in health and disease. Circ Res 2009; 104: 292-303.
38. Zacharowski K, Blackburn B, Thiemermann C,. Ranolazine, a partial fatty acid oxidation inhibitor, reduces myocardial infarct size and cardiac troponin T release in the rat. Eur J Pharmacol 2001; 418: 105-110.
39. Zhao Y, McLaughlin D, Robinson E, Harvey AP, Hookham MB, Shah AM, McDermott BJ, Grieve DJ,. Nox2 NADPH oxidase promotes pathologic cardiac remodeling associated with Doxorubicin chemotherapy. Cancer Res 2010; 70: 9287-9297.
40. Kandasamy AD, Chow AK, Ali MA, Schulz R,. Matrix metalloproteinase-2 and myocardial oxidative stress injury: beyond the matrix. Cardiovasc Res 2010; 85: 413-423.
41. Minotti G,. Pharmacology at work for cardio-oncology: ranolazine to treat early cardiotoxicity induced by antitumor drugs. J Pharmacol Exp Ther 2013; 346: 343-349.