A novel preclinical strategy for identifying cardiotoxic kinase inhibitors and mechanisms of cardiotoxicity

Circulation Research

Volumn 109, Issue 12, 2011, Pages 1401-1409

  Cheng, Hui ^a   Kari, Gabor ^a   Dicker, Adam P ^a   Rodeck, Ulrich ^a   Koch, Walter J ^a   Force, Thomas ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Cancer; Cardiotoxicity; ERK; Kinase inhibitors; Zebrafish

Indexed keywords

ADENOVIRUS VECTOR; ALPHA ADRENERGIC RECEPTOR; GEFITINIB; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; PHOSPHOTRANSFERASE INHIBITOR; PRAZOSIN; RAF PROTEIN; SORAFENIB; SUNITINIB;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BRAIN VENTRICLE DILATATION; CARDIOTOXICITY; CELL DEATH; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; VIRAL GENE DELIVERY SYSTEM; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; BENZENESULFONATES; CARDIOTOXINS; CELL SURVIVAL; CELLS, CULTURED; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; INDOLES; MALE; MODELS, ANIMAL; MYOCYTES, CARDIAC; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS B-RAF; PROTO-ONCOGENE PROTEINS C-RAF; PYRIDINES; PYRROLES; QUINAZOLINES; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; ZEBRAFISH;

EID: 84856104973     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.111.255695     Document Type: Article

References (29)

1. Slamon DJ, Leyland-Jones B, Shak S, Fuchs H, Paton V, Bajamonde A, Fleming T, Eiermann W, Wolter J, Pegram M, Baselga J, Norton L. Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N Engl J Med. 2001;344:783-792. (Pubitemid 32222155)
2. Chu TF, Rupnick MA, Kerkela R, Dallabrida SM, Zurakowski D, Nguyen L, Woulfe K, Pravda E, Cassiola F, Desai J, George S, Morgan JA, Harris DM, Ismail NS, Chen JH, Schoen FJ, Van den Abbeele AD, Demetri GD, Force T, Chen MH. Cardiotoxicity associated with tyrosine kinase inhibitor sunitinib. Lancet. 2007;370:2011-2019. (Pubitemid 350236338)
3. Kerkela R, Woulfe KC, Durand JB, Vagnozzi R, Kramer D, Chu TF, Beahm C, Chen MH, Force T. Sunitinib-induced cardiotoxicity is mediated by off-target inhibition of AMP-activated protein kinase. Clin Transl Sci. 2009;2:1.
4. Dahme T, Katus HA, Rottbauer W. Fishing for the genetic basis of cardiovascular disease. Dis Model Mech. 2009;2:18-22.
5. Chico TJ, Ingham PW, Crossman DC. Modeling cardiovascular disease in the zebrafish. Trends Cardiovasc Med. 2008;18:150-155. (Pubitemid 351794544)
6. Rocke J, Lees J, Packham I, Chico T. The zebrafish as a novel tool for cardiovascular drug discovery. Recent Pat Cardiovasc Drug Discov. 2009;4:1-5.
7. Kari G, Rodeck U, Dicker AP. Zebrafish: an emerging model system for human disease and drug discovery. Clin Pharmacol Ther. 2007;82:70-80. (Pubitemid 46944200)
8. Langheinrich U. Zebrafish: a new model on the pharmaceutical catwalk. Bioessays. 2003;25:904-912. (Pubitemid 37081756)
9. Khakoo AY, Kassiotis CM, Tannir N, Plana JC, Halushka M, Bickford C, Trent J II, Champion JC, Durand JB, Lenihan DJ. Heart failure associated with sunitinib malate: a multitargeted receptor tyrosine kinase inhibitor. Cancer. 2008;112:2500-2508.
10. Schmidinger M, Zielinski CC, Vogl UM, Bojic A, Bojic M, Schukro C, Ruhsam M, Hejna M, Schmidinger H. Cardiac toxicity of sunitinib and sorafenib in patients with metastatic renal cell carcinoma. J Clin Oncol. 2008;26:5204-5212.
11. Tolcher AW, Appleman LJ, Shapiro GI, Mita AC, Cihon F, Mazzu A, Sundaresan PR. A phase I open-label study evaluating the cardiovascular safety of sorafenib in patients with advanced cancer. Cancer Chemother Pharmacol. 2010;67:751-764.
12. Strumberg D, Clark JW, Awada A, Moore MJ, Richly H, Hendlisz A, Hirte HW, Eder JP, Lenz HJ, Schwartz B. Safety, pharmacokinetics, and preliminary antitumor activity of sorafenib: a review of four phase I trials in patients with advanced refractory solid tumors. Oncologist. 2007;12:426-437. (Pubitemid 46698720)
13. Faivre S, Delbaldo C, Vera K, Robert C, Lozahic S, Lassau N, Bello C, Deprimo S, Brega N, Massimini G, Armand JP, Scigalla P, Raymond E. Safety, pharmacokinetic, and antitumor activity of SU11248, a novel oral multitarget tyrosine kinase inhibitor, in patients with cancer. J Clin Oncol. 2006;24:25-35. (Pubitemid 46630490)
14. Mendel DB, Laird AD, Xin X, Louie SG, Christensen JG, Li G, Schreck RE, Abrams YJ, Ngai TJ, Lee LB, Murray LJ, Carver J, Chan ED, Moss KG, Haznedar JO, Sukbuntherng J, Blake RA, Sun L, Tang C, Miller TA, Shirazian S, McMahon G, Cherrington JM. In vivo antitumor activity of SU11248, a novel tyrosine kinase inhibitor targeting vascular endothelial growth factor and platelet-derived growth factor receptors: determination of a pharmacokinetic/pharmacodynamic relationship. Clin Cancer Res. 2003;9:327-337. (Pubitemid 36109749)
15. Fiedler W, Serve H, Dohner H, Schwittay M, Ottmann OG, O'Farrell AM, Bello CL, Allred R, Manning WC, Cherrington JM, Louie SG, Hong W, Brega NM, Massimini G, Scigalla P, Berdel WE, Hossfeld DK. A phase 1 study of SU11248 in the treatment of patients with refractory or resistant acute myeloid leukemia (AML) or not amenable to conventional therapy for the disease. Blood. 2005;105:986-993. (Pubitemid 40170865)
16. Roskoski R Jr. Sunitinib: a VEGF and PDGF receptor protein kinase and angiogenesis inhibitor. Biochem Biophys Res Commun. 2007;356:323-328. (Pubitemid 46452568)
17. Parng C, Seng WL, Semino C, McGrath P. Zebrafish: a preclinical model for drug screening. Assay Drug Dev Technol. 2002;1 (1 Pt 1):41-48.
18. Tucker B, Lardelli M. A rapid apoptosis assay measuring relative acridine orange fluorescence in zebrafish embryos. Zebrafish. 2007;4:113-116. (Pubitemid 47325190)
19. Shepard JL, Stern HM, Pfaff KL, Amatruda JF. Analysis of the cell cycle in zebrafish embryos. Methods Cell Biol. 2004;76:109-125.
20. Karaman MW, Herrgard S, Treiber DK, Gallant P, Atteridge CE, Campbell BT, Chan KW, Ciceri P, Davis MI, Edeen PT, Faraoni R, Floyd M, Hunt JP, Lockhart DJ, Milanov ZV, Morrison MJ, Pallares G, Patel HK, Pritchard S, Wodicka LM, Zarrinkar PP. A quantitative analysis of kinase inhibitor selectivity. Nat Biotechnol. 2008;26:127-132.
21. Harris IS, Zhang S, Treskov I, Kovacs A, Weinheimer C, Muslin AJ. Raf-1 kinase is required for cardiac hypertrophy and cardiomyocyte survival in response to pressure overload. Circulation. 2004;110:718-723. (Pubitemid 39056272)
22. Rose BA, Force T, Wang Y. Mitogen-activated protein kinase signaling in the heart: angels versus demons in a heart-breaking tale. Physiol Rev. 2010;90:1507-1546.
23. Cheng H, Force T. Molecular mechanisms of cardiovascular toxicity of targeted cancer therapeutics. Circ Res. 2010;106:21-34.
24. Fernandez A, Sanguino A, Peng Z, Ozturk E, Chen J, Crespo A, Wulf S, Shavrin A, Qin C, Ma J, Trent J, Lin Y, Han HD, Mangala LS, Bankson JA, Gelovani J, Samarel A, Bornmann W, Sood AK, Lopez-Berestein G. An anticancer C-Kit kinase inhibitor is reengineered to make it more active and less cardiotoxic. J Clin Invest. 2007;117:4044-4054. (Pubitemid 350224113)
25. Kerkela R, Grazette L, Yacobi R, Iliescu C, Patten R, Beahm C, Walters B, Shevtsov S, Pesant S, Clubb FJ, Rosenzweig A, Salomon RN, Van Etten RA, Alroy J, Durand JB, Force T. Cardiotoxicity of the cancer therapeutic agent imatinib mesylate. Nat Med. 2006;12:908-916. (Pubitemid 44175142)
26. Wolf A, Couttet P, Dong M, Grenet O, Heron M, Junker U, Laengle U, Ledieu D, Marrer E, Nussher A, Persohn E, Pognan F, Riviere GJ, Roth DR, Trendelenburg C, Tsao J, Roman D. Imatinib does not induce cardiotoxicity at clinically relevant concentrations in preclinical studies. Leuk Res. 2010;34:1180-1188.
27. French KJ, Coatney RW, Renninger JP, Hu CX, Gales TL, Zhao S, Storck LM, Davis CB, McSurdy-Freed J, Chen E, Frazier KS. Differences in effects on myocardium and mitochondria by angiogenic inhibitors suggest separate mechanisms of cardiotoxicity. Toxicol Pathol. 2010;38:691-702.
28. Huang Y, Wright CD, Merkwan CL, Baye NL, Liang Q, Simpson PC, O'Connell TD. An alpha1A-adrenergic-extracellular signal-regulated kinase survival signaling pathway in cardiac myocytes. Circulation. 2007;115:763-772. (Pubitemid 46294744)
29. Kojima Y, Kubota Y, Sasaki S, Hayashi Y, Kohri K. Translational pharmacology in aging men with benign prostatic hyperplasia: molecular and clinical approaches to alpha1-adrenoceptors. Curr Aging Sci. 2009;2:223-239.