Use of human stem cell derived cardiomyocytes to examine sunitinib mediated cardiotoxicity and electrophysiological alterations

Toxicology and Applied Pharmacology

Volumn 257, Issue 1, 2011, Pages 74-83

  Cohen, J D ^a   Babiarz, J E ^a   Abrams, R M ^a   Guo, L ^a   Kameoka, S ^a   Chiao, E ^a   Taunton, J ^b   Kolaja, K L ^a  

^a HOFFMANN LA ROCHE INC   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

AMPK; Cardiotoxicity; Human stem cell derived cardiomyocytes; Induced pluripotent stem cells; RSK; Sunitinib

Indexed keywords

ADENOSINE TRIPHOSPHATE; GLUTATHIONE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; S6 KINASE; SUNITINIB;

APOPTOSIS; ARTICLE; CARDIOTOXICITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; HEART ELECTROPHYSIOLOGY; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING;

BLOTTING, WESTERN; CELL SURVIVAL; ELECTROPHYSIOLOGICAL PHENOMENA; ENZYME ACTIVATION; HUMANS; INDOLES; INDUCED PLURIPOTENT STEM CELLS; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; PROTEIN KINASES; PYRROLES; RECEPTOR PROTEIN-TYROSINE KINASES; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA;

RODENTIA;

EID: 81255142147     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2011.08.020     Document Type: Article

References (58)

1. Ahmad F., Arad M., Musi N., He H., Wolf C., Branco D., Perez-Atayde A.R., Stapleton D., Bali D., Xing Y., Tian R., Goodyear L.J., Berul C.I., Ingwall J.S., Seidman C.E., Seidman J.G. Increased alpha2 subunit-associated AMPK activity and PRKAG2 cardiomyopathy. Circulation 2005, 112:3140-3148.
2. Anjum R., Blenis J. The RSK family of kinases: emerging roles in cellular signalling. Nat. Rev. Mol. Cell. Biol. 2008, 9:747-758.
3. Anson B.D., Kolaja K.L., Kamp T.J. Opportunities for use of human iPS cells in predictive toxicology. Clin. Pharmacol. Ther. 2011, 89:754-758.
4. Arad M., Moskowitz I.P., Patel V.V., Ahmad F., Perez-Atayde A.R., Sawyer D.B., Walter M., Li G.H., Burgon P.G., Maguire C.T., Stapleton D., Schmitt J.P., Guo X.X., Pizard A., Kupershmidt S., Roden D.M., Berul C.I., Seidman C.E., Seidman J.G. Transgenic mice overexpressing mutant PRKAG2 define the cause of Wolff-Parkinson-White syndrome in glycogen storage cardiomyopathy. Circulation 2003, 107:2850-2856.
5. Bantscheff M., Eberhard D., Abraham Y., Bastuck S., Boesche M., Hobson S., Mathieson T., Perrin J., Raida M., Rau C., Reader V., Sweetman G., Bauer A., Bouwmeester T., Hopf C., Kruse U., Neubauer G., Ramsden N., Rick J., Kuster B., Drewes G. Quantitative chemical proteomics reveals mechanisms of action of clinical ABL kinase inhibitors. Nat. Biotechnol. 2007, 25:1035-1044.
6. Bello C.L., Mulay M., Huang X., Patyna S., Dinolfo M., Levine S., Van Vugt A., Toh M., Baum C., Rosen L. Electrocardiographic characterization of the QTc interval in patients with advanced solid tumors: pharmacokinetic-pharmacodynamic evaluation of sunitinib. Clin. Cancer. Res. 2009, 15:7045-7052.
7. Bistola V., Nikolopoulou M., Derventzi A., Kataki A., Sfyras N., Nikou N., Toutouza M., Toutouzas P., Stefanadis C., Konstadoulakis M.M. Long-term primary cultures of human adult atrial cardiac myocytes: cell viability, structural properties and BNP secretion in vitro. Int. J. Cardiol. 2008, 131:113-122.
8. Blair E., Redwood C., Ashrafian H., Oliveira M., Broxholme J., Kerr B., Salmon A., Ostman-Smith I., Watkins H. Mutations in the gamma(2) subunit of AMP-activated protein kinase cause familial hypertrophic cardiomyopathy: evidence for the central role of energy compromise in disease pathogenesis. Hum. Mol. Genet. 2001, 10:1215-1220.
9. Brouillette J., Clark R.B., Giles W.R., Fiset C. Functional properties of K+currents in adult mouse ventricular myocytes. J. Physiol. 2004, 559:777-798.
10. 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., Chen M.H. Cardiotoxicity associated with tyrosine kinase inhibitor sunitinib. Lancet 2007, 370:2011-2019.
11. Cohen M.S., Zhang C., Shokat K.M., Taunton J. Structural bioinformatics-based design of selective, irreversible kinase inhibitors. Science 2005, 308:1318-1321.
12. Cohen M.S., Hadjivassiliou H., Taunton J. A clickable inhibitor reveals context-dependent autoactivation of p90 RSK. Nat. Chem. Biol. 2007, 3:156-160.
13. Corton J.M., Gillespie J.G., Hawley S.A., Hardie D.G. 5-aminoimidazole-4-carboxamide ribonucleoside. A specific method for activating AMP-activated protein kinase in intact cells?. Eur. J. Biochem. 1995, 229:558-565.
14. Davidson M.M., Nesti C., Palenzuela L., Walker W.F., Hernandez E., Protas L., Hirano M., Isaac N.D. Novel cell lines derived from adult human ventricular cardiomyocytes. J. Mol. Cell. Cardiol. 2005, 39:133-147.
15. Davies S.P., Sim A.T., Hardie D.G. Location and function of three sites phosphorylated on rat acetyl-CoA carboxylase by the AMP-activated protein kinase. Eur. J. Biochem. 1990, 187:183-190.
16. Deeks E.D., Keating G.M. Sunitinib. Drugs 2006, 66:2255-2266. discussion 2267-2258.
17. Di Lorenzo G., Autorino R., Bruni G., Carteni G., Ricevuto E., Tudini M., Ficorella C., Romano C., Aieta M., Giordano A., Giuliano M., Gonnella A., De Nunzio C., Rizzo M., Montesarchio V., Ewer M., De Placido S. Cardiovascular toxicity following sunitinib therapy in metastatic renal cell carcinoma: a multicenter analysis. Ann. Oncol. 2009, 20:1535-1542.
18. Dyck J.R., Lopaschuk G.D. AMPK alterations in cardiac physiology and pathology: enemy or ally?. J. Physiol. 2006, 574:95-112.
19. Fabian M.A., Biggs W.H., Treiber D.K., Atteridge C.E., Azimioara M.D., Benedetti M.G., Carter T.A., Ciceri P., Edeen P.T., Floyd M., Ford J.M., Galvin M., Gerlach J.L., Grotzfeld R.M., Herrgard S., Insko D.E., Insko M.A., Lai A.G., Lelias J.M., Mehta S.A., Milanov Z.V., Velasco A.M., Wodicka L.M., Patel H.K., Zarrinkar P.P., Lockhart D.J. A small molecule-kinase interaction map for clinical kinase inhibitors. Nat. Biotechnol. 2005, 23:329-336.
20. Faivre S., Delbaldo C., Vera K., Robert C., Lozahic S., Lassau N., Bello C., Deprimo S., Brega N., Massimini G., Armand J.P., 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.
21. Faivre S., Demetri G., Sargent W., Raymond E. Molecular basis for sunitinib efficacy and future clinical development. Nat. Rev. 2007, 6:734-745.
22. Field L.J. Atrial natriuretic factor-SV40 T antigen transgenes produce tumors and cardiac arrhythmias in mice. Science 1988, 239:1029-1033.
23. Force T., Kolaja K.L. Cardiotoxicity of kinase inhibitors: the prediction and translation of preclinical models to clinical outcomes. Nat. Rev. 2011, 10:111-126.
24. Force T., Krause D.S., Van Etten R.A. Molecular mechanisms of cardiotoxicity of tyrosine kinase inhibition. Nat. Rev. Cancer. 2007, 7:332-344.
25. Guo L., Guthrie H. Automated electrophysiology in the preclinical evaluation of drugs for potential QT prolongation. J. Pharmacol. Toxicol. Methods 2005, 52:123-135.
26. Guo L., Abrams R.M., Babiarz J.E., Cohen J.D., Kameoka S., Sanders M.J., Chiao E., Kolaja K.L. Estimating the risk of drug-induced proarrhythmia using human induced pluripotent stem cell-derived cardiomyocytes. Toxicol. Sci. 2011, 123:281-289.
27. Gussak I., Chaitman B.R., Kopecky S.L., Nerbonne J.M. Rapid ventricular repolarization in rodents: electrocardiographic manifestations, molecular mechanisms, and clinical insights. J. Electrocardiol. 2000, 33:159-170.
28. Hardie D.G. Minireview: the AMP-activated protein kinase cascade: the key sensor of cellular energy status. Endocrinology 2003, 144:5179-5183.
29. Hardie D.G. The AMP-activated protein kinase pathway-new players upstream and downstream. J. Cell. Sci. 2004, 117:5479-5487.
30. Hasinoff B.B. The cardiotoxicity and myocyte damage caused by small molecule anticancer tyrosine kinase inhibitors is correlated with lack of target specificity. Toxicol. Appl. Pharmacol. 2010, 244:190-195.
31. Hasinoff B.B., Patel D. The lack of target specificity of small molecule anticancer kinase inhibitors is correlated with their ability to damage myocytes in vitro. Toxicol. Appl. Pharmacol. 2010, 249:132-139.
32. Hasinoff B.B., Patel D., O'Hara K.A. Mechanisms of myocyte cytotoxicity induced by the multiple receptor tyrosine kinase inhibitor sunitinib. Mol. Pharmacol. 2008, 74:1722-1728.
33. Hickson-Bick D.L., Buja L.M., McMillin J.B. Palmitate-mediated alterations in the fatty acid metabolism of rat neonatal cardiac myocytes. J. Mol. Cell. Cardiol. 2000, 32:511-519.
34. Karaman M.W., Herrgard S., Treiber D.K., Gallant P., Atteridge C.E., Campbell B.T., Chan K.W., Ciceri P., Davis M.I., Edeen P.T., Faraoni R., Floyd M., Hunt J.P., Lockhart D.J., Milanov Z.V., Morrison M.J., Pallares G., Patel H.K., Pritchard S., Wodicka L.M., Zarrinkar P.P. A quantitative analysis of kinase inhibitor selectivity. Nat. Biotechnol. 2008, 26:127-132.
35. Kattman S.J., Koonce C.H., Swanson B.J., Anson B.D. Stem cells and their derivatives: a renaissance in cardiovascular translational research. J. Cardiovasc. Transl. Res. 2011, 4:66-72.
36. Kerkela R., Woulfe K.C., Durand J.B., Vagnozzi R., Kramer D., Chu T.F., Beahm C., Chen M.H., Force T. Sunitinib-induced cardiotoxicity is mediated by off-target inhibition of AMP-activated protein kinase. Clin. Trans. Sci. 2009, 2:15-25.
37. Khouri E.M., Gregg D.E., Rayford C.R. Effect of exercise on cardiac output, left coronary flow and myocardial metabolism in the unanesthetized dog. Circ. Res. 1965, 17:427-437.
38. Kimes B.W., Brandt B.L. Properties of a clonal muscle cell line from rat heart. Exp. Cell. Res. 1976, 98:367-381.
39. Kudo N., Barr A.J., Barr R.L., Desai S., Lopaschuk G.D. High rates of fatty acid oxidation during reperfusion of ischemic hearts are associated with a decrease in malonyl-CoA levels due to an increase in 5'-AMP-activated protein kinase inhibition of acetyl-CoA carboxylase. J. Biol. Chem. 1995, 270:17513-17520.
40. Kudo N., Gillespie J.G., Kung L., Witters L.A., Schulz R., Clanachan A.S., Lopaschuk G.D. Characterization of 5'AMP-activated protein kinase activity in the heart and its role in inhibiting acetyl-CoA carboxylase during reperfusion following ischemia. Biochim. Biophys. Acta. 1996, 1301:67-75.
41. Maier L.S., Bers D.M. Calcium, calmodulin, and calcium-calmodulin kinase II: heartbeat to heartbeat and beyond. J. Mol. Cell. Cardiol. 2002, 34:919-939.
42. Meissner K., Heydrich B., Jedlitschky G., Meyer Zu Schwabedissen H., Mosyagin I., Dazert P., Eckel L., Vogelgesang S., Warzok R.W., Bohm M., Lehmann C., Wendt M., Cascorbi I., Kroemer H.K. The ATP-binding cassette transporter ABCG2 (BCRP), a marker for side population stem cells, is expressed in human heart. J. Histochem. Cytochem. 2006, 54:215-221.
43. Menna P., Salvatorelli E., Minotti G. Cardiotoxicity of antitumor drugs. Chem. Res. Toxicol. 2008, 21:978-989.
44. Motzer R.J., Hutson T.E., Tomczak P., Michaelson M.D., Bukowski R.M., Rixe O., Oudard S., Negrier S., Szczylik C., Kim S.T., Chen I., Bycott P.W., Baum C.M., Figlin R.A. Sunitinib versus interferon alfa in metastatic renal-cell carcinoma. N. Engl. J. Med. 2007, 356:115-124.
45. Oliveira S.M., Ehtisham J., Redwood C.S., Ostman-Smith I., Blair E.M., Watkins H. Mutation analysis of AMP-activated protein kinase subunits in inherited cardiomyopathies: implications for kinase function and disease pathogenesis. J. Mol. Cell. Cardiol. 2003, 35:1251-1255.
46. Orphanos G.S., Ioannidis G.N., Ardavanis A.G. Cardiotoxicity induced by tyrosine kinase inhibitors. Acta. Oncol. 2009, 48:964-970.
47. Russell R.R., Li J., Coven D.L., Pypaert M., Zechner C., Palmeri M., Giordano F.J., Mu J., Birnbaum M.J., Young L.H. AMP-activated protein kinase mediates ischemic glucose uptake and prevents postischemic cardiac dysfunction, apoptosis, and injury. J. Clin. Invest. 2004, 114:495-503.
48. Shen J.B., Jiang B., Pappano A.J. Comparison of L-type calcium channel blockade by nifedipine and/or cadmium in guinea pig ventricular myocytes. J. Pharmacol. Exp. Ther. 2000, 294:562-570.
49. Shibata R., Sato K., Pimentel D.R., Takemura Y., Kihara S., Ohashi K., Funahashi T., Ouchi N., Walsh K. Adiponectin protects against myocardial ischemia-reperfusion injury through AMPK- and COX-2-dependent mechanisms. Nat. Med. 2005, 11:1096-1103.
50. Simpson P., Savion S. Differentiation of rat myocytes in single cell cultures with and without proliferating nonmyocardial cells. Cross-striations, ultrastructure, and chronotropic response to isoproterenol. Circ. Res. 1982, 50:101-116.
51. Spector N.L., Yarden Y., Smith B., Lyass L., Trusk P., Pry K., Hill J.E., Xia W., Seger R., Bacus S.S. Activation of AMP-activated protein kinase by human EGF receptor 2/EGF receptor tyrosine kinase inhibitor protects cardiac cells. Proc. Natl. Acad. Sci. USA 2007, 104:10607-10612.
52. Telli M.L., Witteles R.M., Fisher G.A., Srinivas S. Cardiotoxicity associated with the cancer therapeutic agent sunitinib malate. Ann. Oncol. 2008, 19:1613-1618.
53. Terai K., Hiramoto Y., Masaki M., Sugiyama S., Kuroda T., Hori M., Kawase I., Hirota H. AMP-activated protein kinase protects cardiomyocytes against hypoxic injury through attenuation of endoplasmic reticulum stress. Mol. Cell. Biol. 2005, 25:9554-9575.
54. Topol E.J. Cariac Trauma. Textbook of Cardiovascular Medicine 2007, Lippincott Williams & Wilkins, Philadelphia. R.M. Califf, J.D. Thomas, P.D. Thompson (Eds.).
55. Towler M.C., Hardie D.G. AMP-activated protein kinase in metabolic control and insulin signaling. Circ. Res. 2007, 100:328-341.
56. White S.M., Constantin P.E., Claycomb W.C. Cardiac physiology at the cellular level: use of cultured HL-1 cardiomyocytes for studies of cardiac muscle cell structure and function. Am. J. Physiol. Heart. Circ. Physiol. 2004, 286:H823-H829.
57. Zhang P., Hu X., Xu X., Fassett J., Zhu G., Viollet B., Xu W., Wiczer B., Bernlohr D.A., Bache R.J., Chen Y. AMP activated protein kinase-alpha2 deficiency exacerbates pressure-overload-induced left ventricular hypertrophy and dysfunction in mice. Hypertension 2008, 52:918-924.
58. Zhang Y., Nuglozeh E., Toure F., Schmidt A.M., Vunjak-Novakovic G. Controllable expansion of primary cardiomyocytes by reversible immortalization. Hum. Gene. Ther. 2009, 20:1687-1696.