Effects of acute and chronic sunitinib treatment on cardiac function and calcium/calmodulin-dependent protein kinase II

British Journal of Pharmacology

Volumn 172, Issue 17, 2015, Pages 4342-4354

  Mooney, L ^a   Skinner, M ^b   Coker, S J ^a   Currie, S ^a  

^a UNIVERSITY OF STRATHCLYDE   (United Kingdom)

^b ASTRAZENECA   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; IMATINIB; ISOPRENALINE; RYANODINE RECEPTOR; SUNITINIB; TROPONIN I; VERAPAMIL; INDOLE DERIVATIVE; PYRROLE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOTOXICITY; CARDIOVASCULAR RESPONSE; CONTROLLED STUDY; DIASTOLIC BLOOD PRESSURE; DRUG EFFICACY; DRUG RESPONSE; ENZYME ACTIVITY; EXTRACELLULAR CALCIUM; HEART FUNCTION; HEART HEMODYNAMICS; HEART LEFT VENTRICLE; HEART MUSCLE CONTRACTILITY; HEART PERFORMANCE; HEART RATE; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SYSTOLIC BLOOD PRESSURE; TOXICITY TESTING; ANIMAL; BIOSYNTHESIS; BLOOD PRESSURE; CHEMICALLY INDUCED; DRUG ADMINISTRATION; DRUG EFFECTS; ENZYMOLOGY; GUINEA PIG; HEART DISEASE; MALE; PHYSIOLOGY; TREATMENT OUTCOME;

ANIMALS; BLOOD PRESSURE; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; DRUG ADMINISTRATION SCHEDULE; GUINEA PIGS; HEART DISEASES; HEART RATE; INDOLES; MALE; PYRROLES; TREATMENT OUTCOME;

EID: 84938738287     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.13213     Document Type: Article

References (50)

1. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, etal.; CGTP Collaborators (2013a). The Concise Guide to PHARMACOLOGY 2013/14: Enzymes. Br J Pharmacol 170: 1797-1867.
2. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Catterall WA, etal.; CGTP Collaborators (2013b). The Concise Guide to PHARMACOLOGY 2013/14: Ion Channels. Br J Pharmacol 170: 1607-1651.
3. Anderson ME, (2007). Multiple downstream proarrhythmic targets for CaMKII; moving beyond an ion channel-centric focus. Cardiovasc Res 73: 657-666.
4. Anderson ME, (2009). CaMKII and a failing strategy for growth in heart. J Clin Invest 119: 1082-1085.
5. C with sorcin indirectly modulates ryanodine receptor function in cardiac myocytes. J Mol Cell Cardiol 43: 492-503.
6. Barr LA, Makarewich CA, Berretta RM, Gao H, Truopes CD, Woitek F, etal. (2014). Imatinib activates pathological hypertrophy by altering myocyte calcium regulation. Clin Transl Sci 7: 360-367.
7. c interval in patients with advanced solid tumours: pharmacokinetic-pharmacodynamic evaluation of sunitinib. Clin Cancer Res 15: 7045-7052.
8. Blasi E, Heyen J, Patyna S, Hemkens M, Ramirez D, John-Baptiste A, etal. (2012). Sunitinib, a receptor tyrosine kinase inhibitor, increases blood pressure in rats without associated changes in cardiac structure and function. Cardiovasc Ther 30: 287-294.
9. Bosnjak ZJ, Marijic J, Roerig DL, Stowe DF, Murthy VS, Kampine JP, (1991). Chronic verapamil treatment depresses automaticity and contractility in isolated cardiac tissues. Anesth Analg 72: 462-468.
10. Cheng H, Force T, (2010). Why do kinase inhibitors cause cardiotoxicity and what can be done about it? Prog Cardiovasc Dis 53: 114-120.
11. Chu TF, Rupnick MA, Kerkela R, Dallabrida SM, Zurakowski D, Nguyen L, etal. (2007). Cardiotoxicity associated with the tyrosine kinase inhibitor sunitinib. Lancet 370: 2011-2019.
12. Curigliano G, Mayer EL, Burstein HJ, Winer EP, Goldhirsch A, (2010). Cardiac toxicity from systemic therapy: a comprehensive review. Prog Cardiovasc Dis 53: 94-104.
13. Currie S, Elliott EB, Smith GL, Loughrey CM, (2011). Two candidates at the heart of dysfunction: the ryanodine receptor and CaMKII as potential targets for therapeutic intervention-an in vivo perspective. Pharm Ther 131: 204-220.
14. Erickson JR, Joiner MA, Guan X, Kutschke W, Yang J, Oddis CV, etal. (2008). A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell 133: 462-474.
15. Force T, Kolaja KL, (2011). Cardiotoxicity of kinase inhibitors: the prediction and translation of preclinical models to clinical outcomes. Nat Rev Drug Discov 10: 111-126.
16. Freedman SB, Richmond DR, Ashley JJ, Kelly DT, (1981). Verapamil kinetics in normal subjects and patients with coronary artery spasm. Clin Pharmacol Ther 30: 644-652.
17. Friddle CJ, Koga T, Rubin EM, Bristow J, (2000). Expression profiling reveals distinct sets of genes altered during induction and regression of cardiac hypertrophy. Proc Natl Sci U S A 97: 6745-6750.
18. Ghoreschi K, Laurence A, O'Shea JJ, (2009). Selectivity and therapeutic inhibition of kinases: to be or not to be? Nat Immunol 10: 356-360.
19. Grimm M, Heller Brown J, (2010). β-Adrenergic receptor signalling in the heart: role of CaMKII. J Mol Cell Cardiol 48: 322-330.
20. Isobe T, Komatsu R, Honda M, Kuramoto S, Shindoh H, Tabo M, (2014). Estimating the clinical risk of hypertension from VEGF signal inhibitors by a non-clinical approach using telemetered rats. J Toxicol Sci 39: 237-242.
21. Joiner MA, Mei-Ling A, Koval OM, Li J, He BJ, Allamargot C, etal. (2012). CaMKII determines mitochondrial stress responses in heart. Nature 491: 269-273.
22. Kaurstad G, Alves MN, Keni OJ, Rolim N, Hoydal MA, Wisloff U, etal. (2012). Chronic CaMKII inhibition blunts the cardiac contractile response to exercise training. Eur J Appl Physiol 112: 579-588.
23. Kerkela R, Grazette L, Yacobi R, Iliescu C, Patten R, Beahm C, etal. (2006). Cardiotoxicity of the cancer therapeutic agent imatinib mesylate. Nat Med 12: 908-916.
24. Kerkela R, Woulfe KC, Durand JB, (2009). Sunitinib-induced cardiotoxicity is mediated by off-target inhibition of AMP-activated protein kinase. Clin Transl Sci 2: 15-25.
25. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, (2010). Animal research: Reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 160: 1577-1579.
26. Kitagawa D, Yokota K, Gouda M, Narumi Y, Ohmoto H, Nishiwaki E, etal. (2013). Activity-based kinase profiling of approved tyrosine kinase inhibitors. Genes Cells 18: 110-122.
27. Kitagawa Y, Tamura Y, Shimizu J, Nakajima-Takenaka C, Taniguchi S, Uesato S, etal. (1997). Effects of a novel histone deacetylase inhibitor, N-(2-aminophenyl) benzamide, on a reversible hypertrophy induced by isoproterenol in in situ rat hearts. J Pharmacol Sci 104: 167-175.
28. Kudej RK, Iwase M, Uechi M, Vatner DE, Oka N, Ishikawa Y, etal. (1997). Effects of chronic beta-adrenergic receptor stimulation in mice. J Mol Cell Cardiol 29: 2735-2746.
29. Maayah ZH, Ansari MA, El Gendy MA, Al-Arifi MN, Korashy HM, (2014). Development of cardiac hypertrophy by sunitinib in vivo and in vitro rat cardiomyocytes is influenced by the aryl hydrocarbon receptor signaling pathway. Arch Toxicol 88: 725-738.
30. Maisel AS, Motulsky HJ, Insel PA, (1987). Propranolol treatment externalizes beta-adrenergic receptors in guinea pig myocardium and prevents further externalization by ischemia. Circ Res 60: 108-112.
31. Markert M, Trautmann T, Groß M, Ege A, Mayer K, Guth B, (2012). Evaluation of a method to correct the contractility index LVdP/dt(max) for changes in heart rate. J Pharmacol Toxicol Methods 66: 90-105.
32. Marks L, Borland S, Philp K, Ewart L, Lainée P, Skinner M, etal. (2012). The role of the anaesthetised guinea-pig in the preclinical cardiac safety evaluation of drug candidate compounds. Toxicol Appl Pharmacol 263: 171-183.
33. Martin TP, Lawan A, Robinson E, Grieve DJ, Plevin R, Paul A, etal. (2014). Adult cardiac fibroblast proliferation is modulated by calcium/calmodulin-dependent protein kinase II in normal and hypertrophied hearts. Pflugers Arch Eur J Physiol 466: 319-330.
34. McGrath J, Drummond G, McLachlan E, Kilkenny C, Wainwright C, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
35. Mellor HR, Bell AR, Valentin J-P, Roberts RR, (2011). Cardiotoxicity associated with targeting kinase pathways in cancer. Toxicol Sci 120: 14-32.
36. Mooney L, (2012). Development of a small animal model for integrated assessment of cardiac contractility and calcium/calmodulin-dependent protein kinase II. PhD Thesis. University of Strathclyde.
37. Mooney L, Marks L, Philp KL, Skinner M, Coker SJ, Currie S, (2012). Optimising conditions for studying acute effects of drugs on indices of cardiac contractility and on haemodynamics in anaesthetised guinea pigs. J Pharmacol Toxicol Methods 66: 43-51.
38. Murphy MP, (2009). How mitochondria produce reactive oxygen species. Biochem J 417: 1-13.
39. Pawson AJ, Sharman JL, Benson HE, Faccenda E, Alexander SP, Buneman OP, etal.; NC-IUPHAR (2014). The IUPHAR/BPS Guide to PHARMACOLOGY: an expert-driven knowledge base of drug targets and their ligands. Nucl Acids Res 42 (Database Issue): D1098-D1106.
40. Stummann TC, Beilmann M, Duker G, Dumotier B, Fredriksson JM, Jones RL, etal. (2009). Report and recommendations of the workshop of the European Centre for the Validation of Alternative Methods for Drug-Induced Cardiotoxicity. Cardiovasc Toxicol 9: 107-125.
41. Takeshita D, Shimizu J, Kitagawa Y, Yamashita D, Tohne K, Nakajima-Takenaka C, etal. (2008). Isoproterenol-induced hypertrophied rat hearts: does short-term treatment correspond to long-term treatment? J Physiol Sci 58: 179-188.
42. Telli M, Witteles R, Fisher G, Srinivas S, (2008). Cardiotoxicity associated with the cancer therapeutic agent sunitinib malate. Ann Oncol 19: 1613-1618.
43. Wallace AG, Skinner NS, Mitchell JH, (1963). Hemodynamic determinants of the maximal rate of rise of left ventricular pressure. Am J Physiol 205: 30-36.
44. Wehrens XH, Lehnart SE, Reiken SR, Marks AR, (2004). CaMKII phosphorylation regulates the cardiac ryanodine receptor. Circ Res 94: e61-e70.
45. Wolf A, Couttet P, Dong M, Grenet O, Heron M, Junker U, etal. (2010). Imatinib does not induce cardiotoxicity at clinically relevant concentrations in preclinical studies. Leuk Res 34: 1180-1188.
46. Yoo B, Lemaire A, Mangmool S, WolF MJ, Curcio A, Mao L, etal. (2009). Beta 1 adrenergic receptors stimulate cardiac contractility and CaMKII activation in vivo and enhance cardiac dysfunction following myocardial infarction. Am J Physiol 297: H1377-H1386.
47. Zhang R, Khoo MS, Wu Y, Yang Y, Grueter CE, Ni G, etal. (2005). Calmodulin kinase II inhibition protects against structural heart disease. Nat Med 11: 409-417.
48. Zhang T, Maier LS, Dalton ND, Miyamoto S, Ross J, Bers DM, etal. (2003). The δC isoform of CaMKII is activated in cardiac hypertrophy and induces dilated cardiomyopathy and heart failure. Circ Res 92: 912-919.
49. Zhou J, (2010). Cardiac adaptation to chronic blockade of voltage-gated L-type calcium channels in the sarcolemma. Electronic Thesis and Dissertation Repository. Available at: http://ir.lib.uwo.ca/etd/54 (accessed 8/1/2012).
50. Zhuang G, Shu-yan H, Chen Y, Jun G, Li P, (2011). Mitochondrial reactive oxygen species in sunitinib induced cardiomyocytes apoptosis. Chin J Pharmacol Toxicol 25: 188-192.