Early biomarkers of doxorubicin-induced heart injury in a mouse model

Toxicology and Applied Pharmacology

Volumn 281, Issue 2, 2014, Pages 221-229

  Desai, Varsha G ^a   C Kwekel, Joshua ^a   Vijay, Vikrant ^a   Moland, Carrie L ^a   Herman, Eugene H ^b   Lee, Taewon ^c   Han, Tao ^a   Lewis, Sherry M ^a   Davis, Kelly J ^a   Muskhelishvili, Levan ^a   Kerr, Susan ^d   Fuscoe, James C ^a  

^a NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c Korea University   (South Korea)

^d ARKANSAS HEART HOSPITAL   (United States)

Author keywords

Biomarker; Doxorubicin; Heart; MicroRNA profiling; Mouse

Indexed keywords

BIOLOGICAL MARKER; DOXORUBICIN; MICRORNA; MICRORNA 34A; SODIUM CHLORIDE; TROPONIN; TROPONIN T; ANTINEOPLASTIC ANTIBIOTIC; GAMMA-H2AX PROTEIN, MOUSE; GENETIC MARKER; HISTONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARDIOMYOPATHY; CARDIOTOXICITY; CONTROLLED STUDY; DNA DAMAGE; DOSE RESPONSE; DOWN REGULATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; HEART HYPERTROPHY; HEART INJURY; HEART MUSCLE CELL; MALE; MICROSCOPY; MOUSE; MOUSE MODEL; NONHUMAN; TREATMENT DURATION; UPREGULATION; ANIMAL; BLOOD; CHEMICALLY INDUCED; DISEASE MODEL; DOUBLE STRANDED DNA BREAK; GENE EXPRESSION REGULATION; GENETIC MARKER; GENETICS; HEART DISEASE; HEART MUSCLE; METABOLISM; PATHOLOGY; TIME;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; APOPTOSIS; DISEASE MODELS, ANIMAL; DNA BREAKS, DOUBLE-STRANDED; DOXORUBICIN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC MARKERS; HEART DISEASES; HISTONES; MALE; MICE; MICRORNAS; MYOCARDIUM; TIME FACTORS; TROPONIN T;

EID: 84912071171     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2014.10.006     Document Type: Article

References (63)

1. Ambros V. The functions of animal microRNAs. Nature 2004, 431:350-355.
2. Bagchi D., Sen C.K., Ray S.D., Das D.K., Bagchi M., Preuss H.G., Vinson J.A. Molecular mechanisms of cardioprotection by a novel grape seed proanthocyanidin extract. Mutat. Res. 2003, 523-524:87-97.
3. Bang C., Fiedler J., Thum T. Cardiovascular importance of the microRNA-23/27/24 family. Microcirculation 2012, 19:208-214.
4. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
5. Bernaba B.N., Chan J.B., Lai C.K., Fishbein M.C. Pathology of late-onset anthracycline cardiomyopathy. Cardiovasc. Pathol. 2010, 19:308-311.
6. Bernardo B.C., Gao X.M., Winbanks C.E., Boey E.J., Tham Y.K., Kiriazis H., Gregorevic P., Obad S., Kauppinen S., Du X.J., Lin R.C., McMullen J.R. Therapeutic inhibition of the miR-34 family attenuates pathological cardiac remodeling and improves heart function. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:17615-17620.
7. Bertinchant J.P., Polge A., Juan J.M., Oliva-Lauraire M.C., Giuliani I., Marty-Double C., Burdy J.Y., Fabbro-Peray P., Laprade M., Bali J.P., Granier C., de la Coussaye J.E., Dauzat M. Evaluation of cardiac troponin I and T levels as markers of myocardial damage in doxorubicin-induced cardiomyopathy rats, and their relationship with echocardiographic and histological findings. Clin. Chim. Acta 2003, 329:39-51.
8. Boon R.A., Iekushi K., Lechner S., Seeger T., Fischer A., Heydt S., Kaluza D., Treguer K., Carmona G., Bonauer A., Horrevoets A.J., Didier N., Girmatsion Z., Biliczki P., Ehrlich J.R., Katus H.A., Muller O.J., Potente M., Zeiher A.M., Hermeking H., Dimmeler S. MicroRNA-34a regulates cardiac ageing and function. Nature 2013, 495:107-110.
9. Chang T.C., Wentzel E.A., Kent O.A., Ramachandran K., Mullendore M., Lee K.H., Feldmann G., Yamakuchi M., Ferlito M., Lowenstein C.J., Arking D.E., Beer M.A., Maitra A., Mendell J.T. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol. Cell 2007, 26:745-752.
10. Corsten M.F., Dennert R., Jochems S., Kuznetsova T., Devaux Y., Hofstra L., Wagner D.R., Staessen J.A., Heymans S., Schroen B. Circulating MicroRNA-208b and MicroRNA-499 reflect myocardial damage in cardiovascular disease. Circ. Cardiovasc. Genet. 2010, 3:499-506.
11. Creemers E.E., Pinto Y.M. Molecular mechanisms that control interstitial fibrosis in the pressure-overloaded heart. Cardiovasc. Res. 2011, 89:265-272.
12. D'Alessandra Y., Devanna P., Limana F., Straino S., Di Carlo A., Brambilla P.G., Rubino M., Carena M.C., Spazzafumo L., De Simone M., Micheli B., Biglioli P., Achilli F., Martelli F., Maggiolini S., Marenzi G., Pompilio G., Capogrossi M.C. Circulating microRNAs are new and sensitive biomarkers of myocardial infarction. Eur. Heart J. 2010, 31:2765-2773.
13. Desai V.G., Herman E.H., Moland C.L., Branham W.S., Lewis S.M., Davis K.J., George N.I., Lee T., Kerr S., Fuscoe J.C. Development of doxorubicin-induced chronic cardiotoxicity in the B6C3F1 mouse model. Toxicol. Appl. Pharmacol. 2013, 266:109-121.
14. Divakaran V., Mann D.L. The emerging role of microRNAs in cardiac remodeling and heart failure. Circ. Res. 2008, 103:1072-1083.
15. Dorn G.W. miR-34a and the cardiomyopathy of senescence: SALT PNUTS, SALT PNUTS!. Cell Metab. 2013, 17:629-630.
16. Elzenaar I., Pinto Y.M., van Oort R.J. MicroRNAs in heart failure: new targets in disease management. Clin. Pharmacol. Ther. 2013, 94:480-489.
17. Emanueli C., Thum T. miRNAGE-34 induces cardiac damAGE. Cell Res. 2013, 23:866-867.
18. Fang H., Harris S.C., Su Z., Chen M., Qian F., Shi L., Perkins R., Tong W. ArrayTrack: an FDA and public genomic tool. Methods Mol. Biol. 2009, 563:379-398.
19. From A.M., Maleszewski J.J., Rihal C.S. Current status of endomyocardial biopsy. Mayo Clin. Proc. 2011, 86:1095-1102.
20. Gharib M.I., Burnett A.K. Chemotherapy-induced cardiotoxicity: current practice and prospects of prophylaxis. Eur. J. Heart Fail. 2002, 4:235-242.
21. Gidlof O., Smith J.G., Miyazu K., Gilje P., Spencer A., Blomquist S., Erlinge D. Circulating cardio-enriched microRNAs are associated with long-term prognosis following myocardial infarction. BMC Cardiovasc. Disord. 2013, 13:12.
22. Greco S., Fasanaro P., Castelvecchio S., D'Alessandra Y., Arcelli D., Di Donato M., Malavazos A., Capogrossi M.C., Menicanti L., Martelli F. MicroRNA dysregulation in diabetic ischemic heart failure patients. Diabetes 2012, 61:1633-1641.
23. Green P.S., Leeuwenburgh C. Mitochondrial dysfunction is an early indicator of doxorubicin-induced apoptosis. Biochim. Biophys. Acta 2002, 1588:94-101.
24. He L., He X., Lim L.P., de Stanchina E., Xuan Z., Liang Y., Xue W., Zender L., Magnus J., Ridzon D., Jackson A.L., Linsley P.S., Chen C., Lowe S.W., Cleary M.A., Hannon G.J. A microRNA component of the p53 tumour suppressor network. Nature 2007, 447:1130-1134.
25. Herman E.H., Lipshultz S.E., Rifai N., Zhang J., Papoian T., Yu Z.X., Takeda K., Ferrans V.J. Use of cardiac troponin T levels as an indicator of doxorubicin-induced cardiotoxicity. Cancer Res. 1998, 58:195-197.
26. 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-T and the severity of the chronic cardiomyopathy induced by doxorubicin. J. Clin. Oncol. 1999, 17:2237-2243.
27. Ikeda S., Kong S.W., Lu J., Bisping E., Zhang H., Allen P.D., Golub T.R., Pieske B., Pu W.T. Altered microRNA expression in human heart disease. Physiol. Genomics 2007, 31:367-373.
28. Imondi A.R., Della Torre P., Mazué G., Sullivan T.M., Robbins T.L., Hagerman L.M., Podestà A., Pinciroli G. Dose-response relationship of dexrazoxane for prevention of doxorubicin-induced cardiotoxicity in mice, rats, and dogs. Cancer Res. 1996, 56:4200-4204.
29. Karagiannis T.C., Lin A.J., Ververis K., Chang L., Tang M.M., Okabe J., El-Osta A. Trichostatin A accentuates doxorubicin-induced hypertrophy in cardiac myocytes. Aging (Albany NY) 2010, 2:659-668.
30. Kavela S., Shinde S.R., Ratheesh R., Viswakalyan K., Bashyam M.D., Gowrishankar S., Vamsy M., Pattnaik S., Rao S., Sastry R.A., Srinivasulu M., Chen J., Maddika S. PNUTS functions as a proto-oncogene by sequestering PTEN. Cancer Res. 2013, 73:205-214.
31. Kluza J., Marchetti P., Gallego M.A., Lancel S., Fournier C., Loyens A., Beauvillain J.C., Bailly C. Mitochondrial proliferation during apoptosis induced by anticancer agents: effects of doxorubicin and mitoxantrone on cancer and cardiac cells. Oncogene 2004, 23:7018-7030.
32. Kuo L.J., Yang L-X. Gamma-H2AX - A novel biomarker for DNA double-strand breaks. In Vivo 2008, 22:305-310.
33. Lebrecht D., Geist A., Ketelsen U.P., Haberstroh J., Setzer B., Walker U.A. Dexrazoxane prevents doxorubicin-induced long-term cardiotoxicity and protects myocardial mitochondria from genetic and functional lesions in rats. Br. J. Pharmacol. 2007, 151:771-778.
34. Lin R.C., Weeks K.L., Gao X.M., Williams R.B., Bernardo B.C., Kiriazis H., Matthews V.B., Woodcock E.A., Bouwman R.D., Mollica J.P., Speirs H.J., Dawes I.W., Daly R.J., Shioi T., Izumo S., Febbraio M.A., Du X.J., McMullen J.R. PI3K(p110 alpha) protects against myocardial infarction-induced heart failure: identification of PI3K-regulated miRNA and mRNA. Arterioscler. Thromb. Vasc. Biol. 2010, 30:724-732.
35. Lipshultz S.E., Colan S.D., Gelber R.D., Perez-Atayde A.R., Sallan S.E., Sanders S.P. Late cardiac effects of doxorubicin therapy for acute lymphoblastic leukemia in childhood. N. Engl. J. Med. 1991, 324:808-815.
36. Lipshultz S.E., Rifai N., Sallan S.E., Lipsitz S.R., Dalton V., Sacks D.B., Ottlinger M.E. Predictive value of cardiac troponin T in pediatric patients at risk for myocardial injury. Circulation 1997, 96:2641-2648.
37. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 2001, 25:402-408.
38. MacLellan W.R., Schneider M.D. Death by design. Programmed cell death in cardiovascular biology and disease. Circ. Res. 1997, 81:137-144.
39. Matsumoto S., Sakata Y., Suna S., Nakatani D., Usami M., Hara M., Kitamura T., Hamasaki T., Nanto S., Kawahara Y., Komuro I. Circulating p53-responsive microRNAs are predictive indicators of heart failure after acute myocardial infarction. Circ. Res. 2013, 113:322-326.
40. Minotti G., Menna P., Salvatorelli E., Cairo G., Gianni L. Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity. Pharmacol. Rev. 2004, 56:185-229.
41. Nag A.C. Study of non-muscle cells of the adult mammalian heart: a fine structural analysis and distribution. Cytobios 1980, 28:41-61.
42. Narula J., Haider N., Virmani R., DiSalvo T.G., Kolodgie F.D., Hajjar R.J., Schmidt U., Semigran M.J., Dec G.W., Khaw B.A. Apoptosis in myocytes in end-stage heart failure. N. Engl. J. Med. 1996, 335:1182-1189.
43. Olivetti G., Abbi R., Quaini F., Kajstura J., Cheng W., Nitahara J.A., Quaini E., Di Loreto C., Beltrami C.A., Krajewski S., Reed J.C., Anversa P. Apoptosis in the failing human heart. N. Engl. J. Med. 1997, 336:1131-1141.
44. Olson R.D., Mushlin P.S. Doxorubicin cardiotoxicity: analysis of prevailing hypotheses. FASEB J. 1990, 4:3076-3086.
45. Rao P.K., Toyama Y., Chiang H.R., Gupta S., Bauer M., Medvid R., Reinhardt F., Liao R., Krieger M., Jaenisch R., Lodish H.F., Blelloch R. Loss of cardiac microRNA-mediated regulation leads to dilated cardiomyopathy and heart failure. Circ. Res. 2009, 105:585-594.
46. Raver-Shapira N., Marciano E., Meiri E., Spector Y., Rosenfeld N., Moskovits N., Bentwich Z., Oren M. Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol. Cell 2007, 26:731-743.
47. Sayed D., Hong C., Chen I.Y., Lypowy J., Abdellatif M. MicroRNAs play an essential role in the development of cardiac hypertrophy. Circ. Res. 2007, 100:416-424.
48. Sethi G.K., Copeland J.G. Routine surveillance endomyocardial biopsy. Ann. Thorac. Surg. 1997, 64:1230.
49. Singal P.K., Iliskovic N. Doxorubicin-induced cardiomyopathy. N. Engl. J. Med. 1998, 339:900-905.
50. Singal P.K., Iliskovic N., Li T., Kumar D. Adriamycin cardiomyopathy: pathophysiology and prevention. FASEB J. 1997, 11:931-936.
51. Small E.M., Frost R.J., Olson E.N. MicroRNAs add a new dimension to cardiovascular disease. Circulation 2010, 121:1022-1032.
52. Sun X., Zhou Z., Kang Y.J. Attenuation of doxorubicin chronic toxicity in metallothionein-overexpressing transgenic mouse heart. Cancer Res. 2001, 61:3382-3387.
53. Tewey K.M., Rowe T.C., Yang L., Halligan B.D., Liu L.F. Adriamycin-induced DNA damage mediated by mammalian DNA topoisomerase II. Science 1984, 226:466-468.
54. Thum T., Galuppo P., Wolf C., Fiedler J., Kneitz S., van Laake L.W., Doevendans P.A., Mummery C.L., Borlak J., Haverich A., Gross C., Engelhardt S., Ertl G., Bauersachs J. MicroRNAs in the human heart: a clue to fetal gene reprogramming in heart failure. Circulation 2007, 116:258-267.
55. Thum T., Gross C., Fiedler J., Fischer T., Kissler S., Bussen M., Galuppo P., Just S., Rottbauer W., Frantz S., Castoldi M., Soutschek J., Koteliansky V., Rosenwald A., Basson M.A., Licht J.D., Pena J.T., Rouhanifard S.H., Muckenthaler M.U., Tuschl T., Martin G.R., Bauersachs J., Engelhardt S. MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature 2008, 456:980-984.
56. Tong W., Cao X., Harris S., Sun H., Fang H., Fuscoe J., Harris A., Hong H., Xie Q., Perkins R., Shi L., Casciano D. ArrayTrack-supporting toxicogenomic research at the U.S. Food and Drug Administration National Center for Toxicological Research. Environ. Health Perspect. 2003, 111:1819-1826.
57. Vacchi-Suzzi C., Bauer Y., Berridge B.R., Bongiovanni S., Gerrish K., Hamadeh H.K., Letzkus M., Lyon J., Moggs J., Paules R.S., Pognan F., Staedtler F., Vidgeon-Hart M.P., Grenet O., Couttet P. Perturbation of microRNAs in rat heart during chronic doxorubicin treatment. PLoS One 2012, 7:e40395.
58. van Rooij E., Sutherland L.B., Liu N., Williams A.H., McAnally J., Gerard R.D., Richardson J.A., Olson E.N. A signature pattern of stress-responsive microRNAs that can evoke cardiac hypertrophy and heart failure. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:18255-18260.
59. van Rooij E., Marshall W.S., Olson E.N. Toward microRNA-based therapeutics for heart disease: the sense in antisense. Circ. Res. 2008, 103:919-928.
60. Wallace K.B., Hausner E., Herman E., Holt G.D., MacGregor J.T., Metz A.L., Murphy E., Rosenblum I.Y., Sistare F.D., York M.J. Serum troponins as biomarkers of drug-induced cardiac toxicity. Toxicol. Pathol. 2004, 32:106-121.
61. Xiao J., Chen Y.H. MicroRNAs: novel regulators of the heart. J. Thorac. Dis. 2010, 2:43-47.
62. Yamakuchi M., Lowenstein C.J. MiR-34, SIRT1 and p53: the feedback loop. Cell Cycle 2009, 8:712-715.
63. Zak R. Development and proliferative capacity of cardiac muscle cells. Circ. Res. 1974, 35:17-26.