Altered cytosolic Ca2+ dynamics in cultured Guinea pig cardiomyocytes as an in vitro model to identify potential cardiotoxicants

Toxicology in Vitro

Volumn 24, Issue 3, 2010, Pages 960-972

  Qian, Jian Yong ^a   Guo, Liang ^a  

^a Non Clinical Safety   (United States)

Author keywords

Arrhythmia; Calcium imaging; Cardiomyopathy; Cardiotoxicant; Cultured cardiomyocyte; Drug safety assessment; Guinea pig; Safety pharmacology

Indexed keywords

1 [2 (6 METHYL 2 PYRIDYL)ETHYL] 4 (4 METHYLSULFONYLAMINOBENZOYL)PIPERIDINE; ACETYLSALICYLIC ACID; ACONITINE; AMIODARONE; AMOXICILLIN; CALCIUM CHANNEL L TYPE; CISAPRIDE; DOFETILIDE; DOXORUBICIN; EPIRUBICIN; IMATINIB; ISOPRENALINE; OUABAIN; PENTAMIDINE; POTASSIUM CHANNEL HERG; SUNITINIB; TERFENADINE; ANTINEOPLASTIC AGENT; CALCIUM; FLUORESCENT DYE; FURA 2; ION CHANNEL;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM CURRENT; CALCIUM SIGNALING; CALCIUM TRANSPORT; CARDIOMYOPATHY; CARDIOTOXICITY; CHANNEL GATING; CONTROLLED STUDY; DRUG SAFETY; GUINEA PIG; HEART MUSCLE CELL; IN VITRO STUDY; NONHUMAN; SARCOPLASMIC RETICULUM; TORSADE DES POINTES; ANIMAL; CELL CULTURE; CHEMICALLY INDUCED DISORDER; CYTOSOL; DOSE RESPONSE; DRUG EFFECT; HEART CONTRACTION; HEART DISEASE; METABOLISM; PATHOLOGY; STATISTICAL ANALYSIS;

CAVIA; STROPHANTHUS GRATUS;

ANIMALS; ANTINEOPLASTIC AGENTS; CALCIUM; CALCIUM SIGNALING; CELLS, CULTURED; CYTOSOL; DATA INTERPRETATION, STATISTICAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FLUORESCENT DYES; FURA-2; GUINEA PIGS; HEART DISEASES; ION CHANNELS; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; TORSADES DE POINTES;

EID: 77649191413     PISSN: 08872333     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tiv.2009.12.027     Document Type: Article

References (84)

1. Aktas M.K., Shah A.H., and Akiyama T. Dofetilide-induced long QT and torsades de pointes. Ann. Noninvasive Electrocardiol. 12 (2007) 197-202
2. Anderson M.E. QT interval prolongation and arrhythmia: an unbreakable connection?. J. Intern. Med. 259 (2006) 81-90
3. ASHP, 2009. AHFS Drug Information, 2009, p. 2099.
4. Balasubramaniam R., Chawla S., Grace A.A., and Huang C.L. Caffeine-induced arrhythmias in murine hearts parallel changes in cellular Ca(2+) homeostasis. Am. J. Physiol. Heart Circ. Physiol. 289 (2005) H1584-H1593
5. Bers D.M., and Despa S. Cardiac myocytes Ca2+ and Na+ regulation in normal and failing hearts. J. Pharmacol. Sci. 100 (2006) 315-322
6. Bronner U., Gustafsson L.L., Doua F., Ericsson O., Miezan T., Rais M., and Rombo L. Pharmacokinetics and adverse reactions after a single dose of pentamidine in patients with Trypanosoma gambiense sleeping sickness. Br. J. Clin. Pharmacol. 39 (1995) 289-295
7. Brown K.A., Blow A.J., Weiss R.M., and Stewart J.A. Acute effects of doxorubicin on human left ventricular systolic and diastolic function. Am. Heart J. 118 (1989) 979-982
8. Caspi O., Itzhaki I., Arbel G., Kehat I., Gepstien A., Huber I., Satin J., and Gepstein L. In vitro electrophysiological drug testing using human embryonic stem cell derived cardiomyocytes. Stem Cells Dev. 18 (2009) 161-172
9. Cataldi M., Gaudino A., Lariccia V., Russo M., Amoroso S., di R.G., and Annunziato L. Imatinib-mesylate blocks recombinant T-type calcium channels expressed in human embryonic kidney-293 cells by a protein tyrosine kinase-independent mechanism. J. Pharmacol. Exp. Ther. 309 (2004) 208-215
10. Catterall W.A. Neurotoxins that act on voltage-sensitive sodium channels in excitable membranes. Ann. Rev. Pharmacol. Toxicol. 20 (1980) 15-43
11. Chiang C.E., Wang T.M., and Luk H.N. Inhibition of L-type Ca(2+) current in Guinea pig ventricular myocytes by cisapride. J. Biomed. Sci. 11 (2004) 303-314
12. Choi B.R., Burton F., and Salama G. Cytosolic Ca2+ triggers early afterdepolarizations and Torsade de Pointes in rabbit hearts with type 2 long QT syndrome. J. Physiol. 543 (2002) 615-631
13. Chu T.F., Rupnick M.A., Kerkela R., Dallabrida S.M., Zurakowski D., Nguyen L., Woulfe K., Pravda E., Cassiola F., Desai J., George S., Morgan J.A., Harris D.M., Ismail N.S., Chen J.H., Schoen F.J., Van den Abbeele A.D., Demetri G.D., Force T., and Chen M.H. Cardiotoxicity associated with tyrosine kinase inhibitor sunitinib. Lancet 370 (2007) 2011-2019
14. Couch R.D., Loh K.K., and Sugino J. Sudden cardiac death following adriamycin therapy. Cancer 48 (1981) 38-39
15. Crumb W., Llorca P.M., Lancon C., Thomas G.P., Garay R.P., and Hameg A. Effects of cyamemazine on hERG, INa, ICa, Ito, Isus and IK1 channel currents, and on the QTc interval in Guinea pigs. Eur. J. Pharmacol. 532 (2006) 270-278
16. Delpon E., Valenzuela C., and Tamargo J. Blockade of cardiac potassium and other channels by antihistamines. Drug Saf. 21 Suppl. 1 (1999) 11-18
17. Dhalla N.S., Yates J.C., and Proveda V. Calcium-linked changes in myocardial metabolism in the isolated perfused rat heart. Can. J. Physiol. Pharmacol. 55 (1977) 925-933
18. Distler J.H., and Distler O. Cardiotoxicity of imatinib mesylate: an extremely rare phenomenon or a major side effect?. Ann. Rheum. Dis. 66 (2007) 836
19. Eisenhauer M.D., Eliasson A.H., Taylor A.J., Coyne Jr. P.E., and Wortham D.C. Incidence of cardiac arrhythmias during intravenous pentamidine therapy in HIV-infected patients. Chest 105 (1994) 389-395
20. FDA Label, 1999. .
21. First DataBank I, 2008. Ellence-Drug Description.
22. Fu M., Li R.X., Fan L., He G.W., Thornburg K.L., and Wang Z. Sarcoplasmic reticulum Ca2+ release channel ryanodine receptor (RyR2) plays a crucial role in aconitine-induced arrhythmias. Biochem. Pharmacol. 75 (2008) 2147-2156
23. Galetta F., Franzoni F., Cervetti G., Cecconi N., Carpi A., Petrini M., and Santoro G. Effect of epirubicin-based chemotherapy and dexrazoxane supplementation on QT dispersion in non-Hodgkin lymphoma patients. Biomed. Pharmacother. 59 (2005) 541-544
24. Gan T.E., Ellims P.H., Tong N., Barned J.M., and Van der Weyden M.B. Doxorubicin-associated delayed ventricular fibrillation in acute promyelocytic leukemia. Acta Haematol. 69 (1983) 52-55
25. Gianni L., Herman E.H., Lipshultz S.E., Minotti G., Sarvazyan N., and Sawyer D.B. Anthracycline cardiotoxicity: from bench to bedside. J. Clin. Oncol. 26 (2008) 3777-3784
26. GlaxoSmithKline, 2008. Amoxicillin-Priscribing information.
27. Guo L., Dong Z., and Guthrie H. Validation of guinea pig Langendorff heart model for assessing potential cardiovascular liability of drug candidates. J. Pharmacol. Toxicol. Methods 60 (2009) 130-151
28. Guo L., and Guthrie H. Automated electrophysiology in the preclinical evaluation of drugs for potential QT prolongation. J. Pharmacol. Toxicol. Methods 52 (2005) 123-135
29. Gwathmey J.K., Tsaioun K., and Hajjar R.J. Cardionomics: a new integrative approach for screening cardiotoxicity of drug candidates. Exp. Opin. Drug Metab. Toxicol. 5 (2009) 647-660
30. Hashitani H., Hayase M., and Suzuki H. Effects of imatinib mesylate on spontaneous electrical and mechanical activity in smooth muscle of the Guinea-pig stomach. Br. J. Pharmacol. 154 (2008) 451-459
31. Hoffmann P., and Warner B. Are hERG channel inhibition and QT interval prolongation all there is in drug-induced torsadogenesis? A review of emerging trends. J. Pharmacol. Toxicol. Methods 53 (2006) 87-105
32. Hondeghem L.M. QT and TdP. QT: an unreliable predictor of proarrhythmia. Acta Cardiol. 63 (2008) 1-7
33. Horackova M., and Byczko Z. Differences in the structural characteristics of adult Guinea pig and rat cardiomyocytes during their adaptation and maintenance in long-term cultures: confocal microscopy study. Exp. Cell Res. 237 (1997) 158-175
34. Hove-Madsen L., Llach A., Molina C.E., Prat-Vidal C., Farre J., Roura S., and Cinca J. The proarrhythmic antihistaminic drug terfenadine increases spontaneous calcium release in human atrial myocytes. Eur. J. Pharmacol. 553 (2006) 215-221
35. Hussain M., and Orchard C.H. Sarcoplasmic reticulum Ca2+ content, L-type Ca2+ current and the Ca2+ transient in rat myocytes during beta-adrenergic stimulation. J. Physiol. 505 Pt 2 (1997) 385-402
36. Janse M.J. Electrophysiological changes in heart failure and their relationship to arrhythmogenesis. Cardiovasc. Res. 61 (2004) 208-217
37. January C.T., and Riddle J.M. Early after depolarizations: mechanism of induction and block. A role for L-type Ca2+ current. Circ. Res. 64 (1989) 977-990
38. Jiang J., Temma K., and Akera T. Doxorubicin-induced changes in intracellular Ca2+ transients observed in cardiac myocytes isolated from Guinea-pig heart. Can. J. Physiol. Pharmacol. 72 (1994) 622-631
39. Jo S.H., Choi S.Y., Kim K.T., and Lee C.O. Effects of polychlorinated biphenyl 19 (2, 2′, 6-trichlorobiphenyl) on contraction, Ca2+ transient, and Ca2+ current of cardiac myocytes. J. Cardiovasc. Pharmacol. 38 (2001) 11-20
40. Katritsis D., Morgan J., Brachmann J., Bygrave A., O'Farrell D., Rowland E., and Camm A.J. Electrophysiological effects of E 4031, a drug with selective class III properties, in man. Pacing Clin. Electrophysiol. 20 (1997) 930-937
41. Kerkela R., Grazette L., Yacobi R., Iliescu C., Patten R., Beahm C., Walters B., Shevtsov S., Pesant S., Clubb F.J., Rosenzweig A., Salomon R.N., Van Etten R.A., Alroy J., Durand J.B., and Force T. Cardiotoxicity of the cancer therapeutic agent imatinib mesylate. Nat. Med. 12 (2006) 908-916
42. Kilickap S., Akgul E., Aksoy S., Aytemir K., and Barista I. Doxorubicin-induced second degree and complete atrioventricular block. Europace 7 (2005) 227-230
43. Kirsch G.E., Trepakova E.S., Brimecombe J.C., Sidach S.S., Erickson H.D., Kochan M.C., Shyjka L.M., Lacerda A.E., and Brown A.M. Variability in the measurement of hERG potassium channel inhibition: effects of temperature and stimulus pattern. J. Pharmacol. Toxicol. Methods 50 (2004) 93-101
44. Kodama I., Kamiya K., and Toyama J. Cellular electropharmacology of amiodarone. Cardiovasc. Res. 35 (1997) 13-29
45. Kubota Y., Biers S.M., Kohri K., and Brading A.F. Effects of imatinib mesylate (Glivec) as a c-kit tyrosine kinase inhibitor in the guinea-pig urinary bladder. Neurourl. Urodyn. 25 (2006) 205-210
46. Kuryshev Y.A., Ficker E., Wang L., Hawryluk P., Dennis A.T., Wible B.A., Brown A.M., Kang J., Chen X.L., Sawamura K., Reynolds W., and Rampe D. Pentamidine-induced long QT syndrome and block of hERG trafficking. J. Pharmacol. Exp. Ther. 312 (2005) 316-323
47. Laurita K.R., and Rosenbaum D.S. Cellular mechanisms of arrhythmogenic cardiac alternans. Prog. Biophys. Mol. Biol. 97 (2008) 332-347
48. Lei M., and Brown H.F. Two components of the delayed rectifier potassium current, IK, in rabbit sino-atrial node cells. Exp. Physiol. 81 (1996) 725-741
49. Lewis L.K., Yandle T.G., Lewis J.G., Richards A.M., Pidgeon G.B., Kaaja R.J., and Nicholls M.G. Ouabain is not detectable in human plasma. Hypertension 24 (1994) 549-555
50. Marban E., Robinson S.W., and Wier W.G. Mechanisms of arrhythmogenic delayed and early afterdepolarizations in ferret ventricular muscle. J. Clin. Invest. 78 (1986) 1185-1192
51. Menna P., Salvatorelli E., and Minotti G. Cardiotoxicity of antitumor drugs. Chem. Res. Toxicol. 21 (2008) 978-989
52. Michael G., Dempster J., Kane K.A., and Coker S.J. Potentiation of E-4031-induced torsade de pointes by HMR1556 or ATX-II is not predicted by action potential short-term variability or triangulation. Br. J. Pharmacol. 152 (2007) 1215-1227
53. Mitcheson J.S., Hancox J.C., and Levi A.J. Cultured adult rabbit myocytes: effect of adding supplements to the medium, and response to isoprenaline. J. Cardiovasc. Electrophysiol. 8 (1997) 1020-1030
54. Olson R.D., Gambliel H.A., Vestal R.E., Shadle S.E., Charlier Jr. H.A., and Cusack B.J. Doxorubicin cardiac dysfunction: effects on calcium regulatory proteins, sarcoplasmic reticulum, and triiodothyronine. Cardiovasc. Toxicol. 5 (2005) 269-283
55. Peng B., Hayes M., Resta D., Racine-Poon A., Druker B.J., Talpaz M., Sawyers C.L., Rosamilia M., Ford J., Lloyd P., and Capdeville R. Pharmacokinetics and pharmacodynamics of imatinib in a phase I trial with chronic myeloid leukemia patients. J. Clin. Oncol. 22 (2004) 935-942
56. Pfizer, 2008. Sutent-highlights for prescribing information.
57. Pharmacia & Upjohn Company, 2003. Doxorubicin Hydrochloride for Injection, USP.
58. Plomp T.A., van Rossum J.M., Robles de Medina E.O., van L.T., and Maes R.A. Pharmacokinetics and body distribution of amiodarone in man. Arzneimittelforschung 34 (1984) 513-520
59. Redfern W.S., Carlsson L., Davis A.S., Lynch W.G., MacKenzie I., Palethorpe S., Siegl P.K., Strang I., Sullivan A.T., Wallis R., Camm A.J., and Hammond T.G. Relationships between preclinical cardiac electrophysiology, clinical QT interval prolongation and torsade de pointes for a broad range of drugs: evidence for a provisional safety margin in drug development. Cardiovasc. Res. 58 (2003) 32-45
60. Ribeiro A.L., Marcolino M.S., Bittencourt H.N., Barbosa M.M., Nunes M.D., Xavier V.F., and Clementino N.C. An evaluation of the cardiotoxicity of imatinib mesylate. Leuk Res. 32 (2008) 1809-1814
61. Rosati B., Dong M., Cheng L., Liou S.R., Yan Q., Park J.Y., Shiang E., Sanguinetti M., Wang H.S., and McKinnon D. Evolution of ventricular myocyte electrophysiology. Physiol. Genomics 5 (2008) 262-272
62. Rudzinski T., Ciesielczyk M., Religa W., Bednarkiewicz Z., and Krzeminska-Pakula M. Doxorubicin-induced ventricular arrhythmia treated by implantation of an automatic cardioverter-defibrillator. Europace 9 (2007) 278-280
63. Sarubbi B., Orditura M., Ducceschi V., De V.F., Santangelo L., Ciaramella F., Catalano G., and Iacono A. Ventricular repolarization time indexes following anthracycline treatment. Heart Vessels 12 (1997) 262-266
64. Schiller L.R., and Johnson D.A. Balancing drug risk and benefit: toward refining the process of FDA decisions affecting patient care. Am. J. Gastroenterol. 103 (2008) 815-819
65. Schimmel K.J., Richel D.J., van den Brink R.B., and Guchelaar H.J. Cardiotoxicity of cytotoxic drugs. Cancer Treat Rev. 30 (2004) 181-191
66. Schmidinger M., Zielinski C.C., Vogl U.M., Bojic A., Bojic M., Schukro C., Ruhsam M., Hejna M., and Schmidinger H. Cardiac toxicity of sunitinib and sorafenib in patients with metastatic renal cell carcinoma. J. Clin. Oncol. 26 (2008) 5204-5212
67. Shah R.R. Can pharmacogenetics help rescue drugs withdrawn from the market?. Pharmacogenomics 7 (2006) 889-908
68. Sham J.S., Hatem S.N., and Morad M. Species differences in the activity of the Na(+)-Ca2+ exchanger in mammalian cardiac myocytes. J. Physiol. 488 (1995) 623-631
69. Solem L.E., Henry T.R., and Wallace K.B. Disruption of mitochondrial calcium homeostasis following chronic doxorubicin administration. Toxicol. Appl. Pharmacol. 129 (1994) 214-222
70. Strevel E.L., Ing D.J., and Siu L.L. Molecularly targeted oncology therapeutics and prolongation of the QT interval. J. Clin. Oncol. 25 (2007) 3362-3371
71. SUTENT Web file. .
72. Tai Y.T., But P.P., Young K., and Lau C.P. Cardiotoxicity after accidental herb-induced aconite poisoning. Lancet 340 (1992) 1254-1256
73. Takahashi S., Denvir M.A., Harder L., Miller D.J., Cobbe S.M., Kawakami M., MacFarlane N.G., and Okabe E. Effects of in vitro and in vivo exposure to doxorubicin (adriamycin) on caffeine-induced Ca2+ release from sarcoplasmic reticulum and contractile protein function in 'chemically-skinned' rabbit ventricular trabeculae. Jpn. J. Pharmacol. 76 (1998) 405-413
74. Tazawa T., Zhao H.Q., Li Y., Meselhy M.R., Nakamura N., Akao T., and Hattori M. A new enzyme immunoassay for aconitine and its application to quantitative determination of aconitine levels in plasma. Biol. Pharm. Bull. 26 (2003) 1289-1294
75. Telli M.L., Witteles R.M., Fisher G.A., and Srinivas S. Cardiotoxicity associated with the cancer therapeutic agent sunitinib malate. Ann. Oncol. 19 (2008) 1613-1618
76. Thomas G.P. Studies on the protective effect of azepexole on ouabain-induced cardiac arrhythmias and lethality in Guinea-pig. Eur. J. Pharmacol. 276 (1995) 215-221
77. Timolati F., Ott D., Pentassuglia L., Giraud M.N., Perriard J.C., Suter T.M., and Zuppinger C. Neuregulin-1 beta attenuates doxorubicin-induced alterations of excitation-contraction coupling and reduces oxidative stress in adult rat cardiomyocytes. J. Mol. Cell. Cardiol. 41 (2006) 845-854
78. Tokuno T., Muraki K., Watanabe M., and Imaizumi Y. Effects of K+ channel modulators on the relationship between action potential duration and Ca2+ transients in single ventricular myocytes of the Guinea pig. Jpn. J. Pharmacol. 80 (1999) 243-253
79. Tomaselli G.F., and Marban E. Electrophysiological remodeling in hypertrophy and heart failure. Cardiovasc. Res. 42 (1999) 270-283
80. Vassallo D.V., Lima E.Q., Campagnaro P., Stefanon I., Leite C.M., and Mill J.G. Effects of isoproterenol on the mechanical activity of isolated papillary muscles and perfused rat hearts in various calcium concentrations. Pharmacol. Res. 29 (1994) 251-260
81. Verheijck E.E., van Ginneken A.C., Bourier J., and Bouman L.N. Effects of delayed rectifier current blockade by E-4031 on impulse generation in single sinoatrial nodal myocytes of the rabbit. Circ. Res. 76 (1995) 607-615
82. Wasserstrom J.A., and Aistrup G.L. Digitalis: new actions for an old drug. Am. J. Physiol. Heart Circ. Physiol. 289 (2005) H1781-H1793
83. Will Y., Dykens J.A., Nadanaciva S., Hirakawa B., Jamieson J., Marroquin L.D., Hynes J., Patyna S., and Jessen B.A. Effect of the multitargeted tyrosine kinase inhibitors imatinib, dasatinib, sunitinib, and sorafenib on mitochondrial function in isolated rat heart mitochondria and H9c2 cells. Toxicol. Sci. 106 (2008) 153-161
84. Wu D.M., Lu J.Y., and Wu B.W. Class III anti-arrhythmia drug E-4031 potentiates Na+/Ca2+ exchange current in rat ventricular myocytes. Acta Pharmacol. Sin. 21 (2000) 249-252