A multifaceted evaluation of imatinib-induced cardiotoxicity in the rat

Toxicologic Pathology

Volumn 39, Issue 7, 2011, Pages 1091-1106

  Herman, Eugene H ^a   Knapton, Alan ^a   Rosen, Elliot ^a   Thompson, Karol ^a   Rosenzweig, Barry ^a   Estis, Joel ^b   Agee, Sara ^b   Lu, Quynh Anh ^b   Todd, John A ^b   Lipshultz, Steven ^c   Hasinoff, Brian ^d   Zhang, Jun ^a  

^a CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^b SINGULEX INC   (United States)

^c UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF MANITOBA   (Canada)

Author keywords

and Sprague Dawley rats; apoptosis; autophagy; cardiac troponin I; drug induced cardiotoxicity; LAMP 2; spontaneously hypertensive rats; tyrosine kinase inhibitors

Indexed keywords

ALPHA ACTININ; IMATINIB; LACTATE DEHYDROGENASE; TROPONIN I;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTERIAL PRESSURE; ARTICLE; AUTOPHAGY; CARDIOTOXICITY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION; HEART INJURY; HEART MUSCLE NECROSIS; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; RAT; SPONTANEOUSLY HYPERTENSIVE RAT; SPRAGUE DAWLEY RAT;

ANIMALS; APOPTOSIS; AUTOPHAGY; CARDIOTOXINS; HEART DISEASES; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 2; MALE; MUSCLE CELLS; MYOCARDIUM; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATION-REDUCTION; PIPERAZINES; PYRIMIDINES; RATS; RATS, INBRED SHR; RATS, SPRAGUE-DAWLEY; RAZOXANE; SARCOMERES; TROPONIN; WEIGHT GAIN;

EID: 82355169061     PISSN: 01926233     EISSN: 15331601     Source Type: Journal    
DOI: 10.1177/0192623311419524     Document Type: Article

References (61)

1. Adderly S. R., Fitzgerald D. J.. Oxidative damage of cardiomyocytes is limited by extracellular regulated kinases ½-mediated induction of cyclooxygenase-2. J Biol Chem. 1999 ; 274: 5038-46
2. Aguirre S. A., Heyen J. R., Cllette W., Bobrowski W., Blasi E. R.. Cardiovascular effects in rats following exposure to a receptor tyrosine kinase inhibitor. Toxicol Pathol. 2010 ; 38: 416-28
3. Atallah E., Durand J. B., Kantarjian H., Slade M. D.. Congestive heart failure is a rare event in patients receiving imatinib therapy. Blood. 2007 ; 110: 1233-37 (Pubitemid 47281421)
4. Bernabe N., Zastre J., Venkataram S., Hasinoff B. B.. Deferiprone protects against doxorubicin-induced myocyte cytotoxicity. Free Radic Biol Med. 2002 ; 33: 266-75 (Pubitemid 34775198)
5. Billingham M. E. Cardiovascular Pathology. M. D. Silver, ed. New York: Churchill Livingstone ; 1991: 1465-86.
6. Billingham M., Bristow M.. Evaluation of anthracycline cardiotoxicity: predictive ability and functional correlation of endomycardial biopsy. Cancer Treat Symp. 1984 ; 3: 71-76 (Pubitemid 15191720)
7. Cardinale D., Sandri M. T., Martinoni A., Tricca A., Civelli M., Lamantia G., Cinieri S., Martinelli G., Cipolla C.M., Fiorentini C.. Left ventricular dysfunction predicted by early troponin I release after high dose chemotherapy. J Am Coll Cardiol. 2000 ; 36: 517-22
8. Chu T. F., Rupnick M. A., Kerkela R., Dallabrida S. M., Zurakowski D., Nguyen L., Woulfe K., Prada E., Cassiola F., Desai J., George S., Morgan J. A., Harris D., Ismail N. S., Chen J.-H., Schoen F. J.. Cardiotoxicity associated with the tyrosine kinase inhibitor sunitinib. Lancet. 2007 ; 370: 2011-19 (Pubitemid 350236338)
9. Deininger M. W., OBrien S. G., Ford J. M., Drucker B. J.. Practical management of patients with chronic myeloid leukemia receiving imatinib. J Clin Oncol. 2003 ; 21: 1637-47 (Pubitemid 46594119)
10. Estabragh Z. R., Knight K., Watmough S. J., Lane S., Vinjamuri S., Hart G., Clark R. E.. A prospective evaluation of cardiac function in patients with chronic myeloid leukaemia treated with imatinib. Leuk Res. 2011 ; 35: 49-51
11. 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 H-D., Mangala L. S., Bankson J. A., Gelovani J., Samarel A., Bornmann W., Sood A. K., Lopez-Berestein G.. An anticancer C-kit kinase inhibitor reengineered to make it more active and less cardiotoxic. J Clin Invest. 2007 ; 117: 4044-54 (Pubitemid 350224113)
12. Force T., Krause D. S., van Etten R. A.. Molecular mechanisms of cardiotoxicity of tyrosine kinase inhibition. Nat Rev Cancer. 2007 ; 7: 332-44 (Pubitemid 46652481)
13. Freebern W. J., Fang H. S., Slade M. D., Wells S., Canale J., Megill J., Grubor B., Shi H., Fletcher A., Lombardo L., Levesque P., Lee F. Y., Sasseville V. G.. In vitro cardiotoxicity potential comparative assessments of chronic myelogenous leukemia tyrosine kinase inhibitor therapies: dasatinib, imatinib and nilotinib. Blood. 2007 ; 110: 4582
14. Gabizon A. A., Lyass O., Berry G. J., Wildgust M.. Cardiac safety of pegylated liposomal doxorubicin (Doxil/Caelyx) demonstrated be endomyocardial biopsy in patients with advanced malignancies. Cancer Invest. 2004 ; 22: 663-69 (Pubitemid 40064725)
15. Ganz W. I., Sridhar K. S., Ganz S. S., Gonzalez R., Chakko S., Serafini A.. Review of tests for monitoring doxorubicin-induced cardiomyopathy. Oncology. 1996 ; 53: 461-70 (Pubitemid 26388387)
16. Gotoh T., Terada K., Oyadomari S., Mori M.. hsp70-DnaJ chaperone pair prevents nitric oxide- and CHOP-induced apoptosis by inhibiting translocation of Bax to mitochondria. Cell Death Differ. 2004 ; 11: 390-402 (Pubitemid 38489417)
17. Hasinoff B. B.. Cardiotoxicity and myocyte damage caused by small molecule anticancer tyrosine kinase inhibitors is correlated with lack of target specificity. Toxicol Appl Pharmacol. 2010 ; 244: 190-95
18. Hasinoff B. B., Patel D., OHara K. A.. Mechanisms of myocyte toxicity induced by the multiple tyrosine receptor kinase inhibitor sunitinib. Mol Pharmacol. 2008 ; 74: 1722-28
19. Hasinoff B. B., Patel D., Wu X.. The cytotoxicity of celecoxib towards cardiac myocytes is cyclooxygenase-2 independent. Cardiovasc Toxicol. 2007 ; 7: 19-27 (Pubitemid 47338488)
20. Hasinoff B. B., Schroeder P. E., Patel D.. The metabolites of the cardioprotective drug dexrazoxane do not protect myocytes from doxorubicin-induced cytotoxicity. Mol Pharmacol. 2003 ; 64: 670-8 (Pubitemid 37048570)
21. Haskins K., Stewart S., Rosenzweig B., Mans D., Zhang J., Peters D., Colatasky T., Thompson K.L. Use of a quantitative immunohistochemical method for diagnosing phospholipidosis. 2011 :
22. Herman E. H., El-Hage A., Ferrans V. J.. Protective effect of ICRF-187 on doxorubicin-induced cardiac and renal toxicity in spontaneously hypertensive (SHR) and normotensive (WKY) rats. Toxicol Appl Pharmacol. 1988 ; 92: 42-53 (Pubitemid 18049689)
23. Herman E. H., El-Hage A. N., Ferrans V. J., Ardalan B.. Comparison of the severity of the chronic cardiotoxicity produced by doxorubicin in normotensive and hypertensive rats. Toxicol Appl Pharmacol. 1985 ; 78: 202-14 (Pubitemid 15081080)
24. Herman E. H., Ferrans V. J.. Preclinical animal models of cardiac protection from anthracycline-induced cardiotoxicity. Semin Oncol. 1998 ; 25 ((Suppl. 10)). 15-30
25. Herman E. H., Zhang J., Lipshultz S. E., Rifai N., Chadwick D., Takeda K., Yu Z.-X., Ferrans V. J.. Correlation between serum levels of cardiac troponin I and the severity of chronic cardiomyopathy induced by doxorubicin. J Clin Oncol. 1999 ; 17: 2237-43 (Pubitemid 29318858)
26. Kerkela R., Grazette L., Yacobi R., Illiescu C., Patten R., Beahm C., Walters B., Shevstoy S., Pesant S., Clubb F. J., Rosenzweig A., Salomon R. N., van Etten R. A., Alroy J., Durand J.-B., Force T.. Cardiotoxicity of the cancer chemotherapeutic agent imatinib mesylate. Nat Med. 2006 ; 12: 908-16 (Pubitemid 44175142)
27. 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 Transl Sci. 2009 ; 2: 15-25
28. Kooy N. W., Lewis S. J., Royall J. A., Ye Y. Z., Kelly D. R., Beckman J. S.. Extensive tyrosine nitration in human myocardial inflammation: evidence for the presence of peroxynitrite. Crit Care Med. 1997 ; 23: 812-19 (Pubitemid 27249159)
29. Kostin S.. Pathways of myocyte death: implication for development of clinical laboratory biomarkers. Adv Clin Chem. 2005 ; 40: 37-98 (Pubitemid 43588720)
30. Kostin S., Pool L., Elsasser A., Hein S., Drexler H. C., Amon E., Hayakawa Y., Zimmermann R., Bauer E., Klovekorm W-P., Schaper J.. Myocyte die by multiple mechanisms in failing human hearts. Circ Res. 2003 ; 92: 715-24 (Pubitemid 36457635)
31. Krause D. S., van Etten R. A.. Tyrosine kinases as targets for cancer therapy. N Engl J Med. 2005 ; 353: 172-87 (Pubitemid 41058349)
32. le Coutre P., Mologni L., Marchesi E., Buchdunger E., Giardini R., Formelli F., Gambacorti-Passerini C.. In vivo eradication of human BCR/ABL-positive leukemia cells with an ABL kinase inhibitor. J Natl Cancer Inst. 1999 ; 91: 102-103
33. Li F., Wang X., Capasso J. M., Gerdes A. M.. Rapid transition of cardiac myocytes from hyperplasia to hypertrophy during post natal development. J Mol Cell Cardiol. 1996 ; 28: 1737-46 (Pubitemid 26300573)
34. Lim C. C., Zuppinger C., Guo X., Kuster G. M., Helmes M., Eppenberger H. M., Suter T. M., Liao R., Sawyer D. B.. Anthracycluines induce calpain-dependent titin proteolysis and necrosis in cardiomyocytes. J Biol Chem. 2004 ; 279: 8290-99 (Pubitemid 38294721)
35. Lipshultz S. E., Rifai N., Sallan S. E., Lipsitz S. R., Dalton V., Sacks D. B., Olltinger M. E.. Predictive value of cardiac troponin T in pediatric patients at risk for myocardial myocardial injury. Circulation. 1997 ; 96: 2641-48 (Pubitemid 27451357)
36. Mehlhorn U., Krahwinkel A., Geissler H. G., LaRosse K., Fischer U. M., Klass O., Suedkamp M., Hekmat K., Tossios P., Block W.. Nitrotyrosine and 8-isoprostane formation indicate free radical-mediated injury in hearts of patients subjected to cardioplegia. J Thorac Cardiovasc Surg. 2003 ; 125: 178-83 (Pubitemid 36120285)
37. Minamino T., Kitakaze M.. ER stress in cardiovascular disease. J Mol Cell Cardiol. 2010 ; 48: 1105-10
38. Nakajima M., Togo W.. Tyrosine kinase inhibitor as a therapeutic drug for chronic myelogenous leukemia and gastrointestinal tumor. Nippon Yakurigaku Zasshi. 2003 ; 122: 482-90 (Pubitemid 38019940)
39. National Academy Press. DC: Washington ; 1996 :
40. Nishida K., Kyol S., Yamaguchi O., Sadoshima J., Otsu K.. The role of autophagy in the heart. Cell Death Differ. 2009 ; 16: 31-38
41. Nishida K., Yamaguchi O., Otsu K.. Crosstalk between autophagy and apoptosis in heart disease. Circ Res. 2008 ; 103: 343-51
42. OBrien S. G., Guilhot F., Larson R. A., Gathmann I., Baccarani M., Cervantes F., Cornelissen J. J., Fischer T., Hochhaus A., Hughes T., Lechner K., Nielsen J. L., Rousselot P., Reiffers J., Saglio G., Shepherd J., Simonsson B., Gratwohl A., Goldman J. M., Kantarjian H., Taylor K., Verhoef G., Bolton A. E., Capdeville R., Druker B. J.,. Imatinib compared with interferon and low-dose cytarabine for newly diagnosed chronic-phase chronic myeloid leukemia. N Engl J Med. 2003 ; 348: 994-1104
43. OMalley Y. Q., Reska K. J., Britigan B. E.. Direct oxidation of 2′7′-dichlorohydroflouroscein by procyanin and other redox-active compounds independent of reactive oxygen species production. Free Radic Biol Med. 2004 ; 36: 90-100 (Pubitemid 38068294)
44. Peng B., Hayes M., Resta D., Racine-Poon A., Druker B.J., Talpaz M., Sawyers C. L., Rosamilia M., Ford J., Lloyd P., Capdeville R.. Pharmacokinetics and pharmacodynamics of imatinib in a phase 1 trial with chronic myeloid leukemia patients. J Clin Oncol. 2004 ; 22: 935-42 (Pubitemid 41103606)
45. Perik P. J., Rikhof B., de Jong F. A., Verweij J., Gietema J. A., van der Graaf W. T. A.. Results of plasma N-terminal pro B-type natriuretic peptide and cardiac troponin monitoring in GIST patients do not support the existence of imatinib-induced cardiotoxicity. Ann Oncol. 2008 ; 19: 359-61 (Pubitemid 351201720)
46. Raines E. W.. PDGF and cardiovascular disease. Cytokine Growth Factor Rev. 2004 ; 15: 237-54 (Pubitemid 38781049)
47. Saad S. Y., Alkharty K. M., Arafah M. M.. Cardiotoxic effects of arsenic trioxide/imatinib mesilate combination in rats. J Pharm Pharmacol. 2006 ; 58: 567-73
48. Saftig P., Beertsen W., Eskelinen E.-L.. LAMP-2: a control step for phagosome and autophagosome maturation. Autophagy. 2008 ; 4: 510-12 (Pubitemid 351705148)
49. Sarvazyan N.. Visualization of doxorubicin-induced oxidative stress in isolated cardiac myocytes. Am J Physiol. 1996 ; 271: H2079-85
50. Sawyers C. L.. Opportunities and challenges in the development of kinase inhibitor therapy for cancer. Genes Dev. 2003 ; 17: 2998-3010 (Pubitemid 38040763)
51. Sawyer D. B., Peng X., Chen B., Pentassuglia L., Lim C. C.. Mechanisms of anthracycline cardiac injury: can we identify strategies for cardioprotection?. Prog Cardiovasc Dis. 2010 ; 53: 105-13
52. Telli M. L., Witteles R. M., Fischer G. A., Srinivas S.. Cardiotoxicity associated with the cancer chemotherapeutic agent sunitinib. Ann Oncol. 2008 ; 19: 1613-18
53. Thompson K., Rosenzweig B., Zhang J., Honchel R., Lipshultz S., Retief J., Sistare F., Herman E.. Early alterations in heart gene expression profiles associated with doxorubicin cardiotoxicity in rats. Cancer Chemother Pharmacol. 2010 ; 66: 303-14
54. Tiribelli M., Colatutto A., Marin L., Barbina G., Qualizza U., Damiani D., Toffoletti E., Medeot M., Candoni A., Tonutti E., Sala P., Fanin R.. Brain natriuretic peptide level as a marker of cardiac function in imatinib-treated chronic myeloid leukemia patients: no evidence of cardiotoxicity of imatinib therapy. Am J Hematol. 2008 ; 83: 517-18 (Pubitemid 351742806)
55. Trent J. C., Patel S. S., Zhang J., Araujo D. M., Plana J-C., Lenihan D. J., Fan D., Patel S. R., Benjamin R. S.. Rare incidence of congestive heart failure in gastrointestinal stromal tumor and other sarcoma patients receiving imatinib mesylate. Cancer. 2010 ; 116: 184-92
56. Verweij J., Casali P. G., Kotasek D., Le Cesne A., Reichard P., Judson I. R., Issels R., van Oosterom A. T., Van Glabbeke M., Blay J. Y.. Imatinib does not induce cardiac left ventricular failure in gastrointestinal stromal tumors patients: analysis of EORTC-ISG-GITG study 62005. Eur J Cancer. 2007 ; 43: 974-78 (Pubitemid 46505099)
57. von Hoff D. D., Layard M. V., Basa P., Davis H. L., von Hoff A. L., Rosencweig M., Muggia F. M.. Risk factors for doxorubicin-induced congestive heart failure. Ann Intern Med. 1979 ; 91: 710-77
58. Will Y., Dykens J. A., Nadanaciva S., Hirakawa B., Jameison J., Marroquin L. D., Hynes J., Patyna S., Jessen B. A.. Effect of multitargeted tyrosine kinase inhibitors imatinib, dasatinib, sunitinib and sorafenib on mitochondrial function in isolated rat heart mitochondria and H9c2 cells. Toxicol Sci. 2008 ; 106: 153-61
59. 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 G-J., Roth D. R., Trendelenburg C., Tsao J., Roman D.. Imitanib does not induce cardiotoxicity at clinically relevant concentrations in preclinical studies. Leuk Res. 2010 ; 34: 1180-88
60. Zhang J., Knapton A., Lipshultz S.E., Weaver J.L., Herman E. H.. Isoproterenol-induced cardiotoxicity in Sprague-Dawley rats: Correlation of reversible and irreversible myocardial injury with release of cardiac troponin T and roles of iNOS in myocardial injury. Toxicol Pathol. 2008 ; 36: 277-288 (Pubitemid 351534489)
61. Zhao Y., Xue T., Yang X., Zhu H., Ding X., Lou L., Lu W., Yang B., He Q.. Autophage plays an important role in sunitinib-mediated cell death in H9c2 cardiac muscle cells. Toxicol Appl Pharmacol. 2010 ; 248: 20-2