Nox2 NADPH oxidase promotes pathologic cardiac remodeling associated with doxorubicin chemotherapy

Cancer Research

Volumn 70, Issue 22, 2010, Pages 9287-9297

  Zhao, Youyou ^a   McLaughlin, Declan ^a   Robinson, Emma ^a   Harvey, Adam P ^a   Hookham, Michelle B ^a   Shah, Ajay M ^b   McDermott, Barbara J ^a   Grieve, David J ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CONNECTIVE TISSUE GROWTH FACTOR; DOXORUBICIN; GELATINASE B; LOSARTAN; PROCOLLAGEN; PROCOLLAGEN III ALPHA I; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; TRANSFORMING GROWTH FACTOR BETA3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BLOOD PRESSURE; CANCER CHEMOTHERAPY; CARDIAC REMODELING; CARDIOTOXICITY; CONTROLLED STUDY; DIASTOLE; DISEASE ASSOCIATION; ECHOCARDIOGRAPHY; ENZYME ACTIVITY; FIBROSING ALVEOLITIS; GENE EXPRESSION; HEART CONTRACTILE DYSFUNCTION; HEART DISEASE; HEART EJECTION FRACTION; HEART LEFT VENTRICLE ENDDIASTOLIC PRESSURE; HEART LEFT VENTRICLE ENDSYSTOLIC VOLUME; HEART MUSCLE; HEART MUSCLE ATROPHY; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HEART MUSCLE FIBROSIS; HEART VENTRICLE PRESSURE; IMMUNOHISTOCHEMISTRY; MALE; MEAN ARTERIAL PRESSURE; MOUSE; MYOCARDIAL DISEASE; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SYSTOLE; WILD TYPE;

ANIMALS; ANTI-ARRHYTHMIA AGENTS; ANTIBIOTICS, ANTINEOPLASTIC; APOPTOSIS; CELLS, CULTURED; DOXORUBICIN; ECHOCARDIOGRAPHY; GATA4 TRANSCRIPTION FACTOR; GENE EXPRESSION; HEART; HELA CELLS; HUMANS; IN SITU NICK-END LABELING; LOSARTAN; MALE; MATRIX METALLOPROTEINASE 9; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDIAL CONTRACTION; MYOCARDIUM; MYOCYTES, CARDIAC; NADPH OXIDASE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; VENTRICULAR REMODELING;

EID: 78549271520     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-2664     Document Type: Article

References (50)

1. Wouters KA, Kremer LC, Miller TL, Herman EH, Lipshultz SE. Protecting against anthracycline-induced myocardial damage: a review of the most promising strategies. Br J Haematol 2005;131:561-78.
2. Floyd JD, Nguyen DT, Lobins RL, Bashir Q, Doll DC, Perry MC. Cardiotoxicity of cancer therapy. J Clin Oncol 2005;23:7685-96.
3. Swynghedauw B. Molecular mechanisms of myocardial remodeling. Physiol Rev 1999;79:215-62.
4. Wojnowski L, Kulle B, Schirmer M, et al. NAD(P)H oxidase and multidrug resistance protein genetic polymorphisms are associated with doxorubicin-induced cardiotoxicity. Circulation 2005;112:3754-62.
5. Spallarossa P, Altieri P, Garibaldi S, et al. Matrix metalloproteinase-2 and -9 are induced differently by doxorubicin in H9c2 cells: the role of MAP kinases and NAD(P)H oxidase. Cardiovasc Res 2006;69:736-45.
6. Mukhopadhyay P, Rajesh M, Batkai S, et al. Role of superoxide, nitric oxide, and peroxynitrite in doxorubicin-induced cell death in vivo and in vitro. Am J Physiol Heart Circ Physiol 2009;296:H1466-83.
7. Sun X, Zhou Z, Kang YJ. Attenuation of doxorubicin chronic toxicity in metallothionein-overexpressing transgenic mouse heart. Cancer Res 2001;61:3382-7.
8. Lipshultz SE, Rifai N, Dalton VM, et al. The effect of dexrazoxane on myocardial injury in doxorubicin-treated children with acute lymphoblastic leukemia. N Engl J Med 2004;351:145-53.
9. Siwik DA, Pagano PJ, Colucci WS. Oxidative stress regulates collagen synthesis and matrix metalloproteinase activity in cardiac fibroblasts. Am J Physiol Cell Physiol 2001;280:C53-60.
10. Grieve DJ, Byrne JA, Siva A, et al. Involvement of the nicotinamide adenosine dinucleotide phosphate oxidase isoform Nox2 in cardiac contractile dysfunction occurring in response to pressure overload. J Am Coll Cardiol 2006;47:817-26.
11. Qin F, Patel R, Yan C, Liu W. NADPH oxidase is involved in angiotensin II-induced apoptosis in H9C2 cardiac muscle cells: effects of apocynin. Free Radic Biol Med 2006;40:236-46.
12. Josephson RA, Silverman HS, Lakatta EG, Stern MD, Zweier JL. Study of the mechanisms of hydrogen peroxide and hydroxyl free radical-induced cellular injury and calcium overload in cardiac myocytes. J Biol Chem 1991;266:2354-61.
13. Gao WD, Liu Y, Marban E. Selective effects of oxygen free radicals on excitation-contraction coupling in ventricular muscle: implications for the mechanism of stunned myocardium. Circulation 1996;94:2597-604.
14. Cave AC, Brewer AC, Narayanapanicker A, et al. NADPH oxidases in cardiovascular health and disease. Antioxid Redox Signal 2006;8:691-728.
15. Byrne JA, Grieve DJ, Bendall JK, et al. Contrasting roles of NADPH oxidase isoforms in pressure-overload versus angiotensin II-induced cardiac hypertrophy. Circ Res 2003;93:802-5.
16. Looi YH, Grieve DJ, Siva A, et al. Involvement of Nox2 NADPH oxidase in adverse cardiac remodeling after myocardial infarction. Hypertension 2008;51:319-25.
17. Heymes C, Bendall JK, Ratajczak P, et al. Increased myocardial NADPH oxidase activity in human heart failure. J Am Coll Cardiol 2003;41:2164-71.
18. Bendall JK, Cave AC, Heymes C, Gall N, Shah AM. Pivotal role of a gp91phox-containing NADPH oxidase in angiotensin II-induced cardiac hypertrophy in mice. Circulation 2002;105:293-6.
19. Pacher P, Liaudet L, Bai P, et al. Potent metalloporphyrin peroxynitrite decomposition catalyst protects against the development of doxorubicin-induced cardiac dysfunction. Circulation 2003;107:896-904.
20. Mizutani H, Tada-Oikawa S, Hiraku Y, Kojima M, Kawanishi S. Mechanism of apoptosis induced by doxorubicin through the generation of hydrogen peroxide. Life Sci 2005;76:1439-53.
21. Toko H, Oka T, Zou Y, et al. Angiotensin II type 1a receptor mediates doxorubicin-induced cardiomyopathy. Hypertens Res 2002;25:597-603.
22. Pinto JT, Delman BN, Dutta P, Nisselbaum J. Adriamycin-induced increase in serum aldosterone levels: effects in riboflavin-sufficient and riboflavin-deficient rats. Endocrinology 1990;127:1495-501.
23. Sayed-Ahmed MM, Khattab MM, Gad MZ, Osman AM. Increased plasma endothelin-1 and cardiac nitric oxide during doxorubicin-induced cardiomyopathy. Pharmacol Toxicol 2001;89:140-4.
24. Deng S, Kruger A, Kleschyov AL, Kalinowski L, Daiber A, Wojnowski L. Gp91phox-containing NAD(P)H oxidase increases superoxide formation by doxorubicin and NADPH. Free Radic Biol Med 2007;42:466-73.
25. Pollock JD, Williams DA, Gifford MA, et al. Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production. Nat Genet 1995;9:202-9.
26. Xia H, Feng Y, Obr TD, Hickman PJ, Lazartigues E. Angiotensin II type 1 receptor-mediated reduction of angiotensin-converting enzyme 2 activity in the brain impairs baroreflex function in hypertensive mice. Hypertension 2009;53:210-6.
27. Georgakopoulos D, Mitzner WA, Chen CH, et al. In vivo murine left ventricular pressure-volume relations by miniaturized conductance micromanometry. Am J Physiol 1998;274:H1416-22.
28. Layland J, Grieve DJ, Cave AC, Sparks E, Solaro RJ, Shah AM. Essential role of troponin I in the positive inotropic response to isoprenaline in mouse hearts contracting auxotonically. J Physiol 2004;556:835-47.
29. Fukai T, Siegfried MR, Ushio-Fukai M, Griendling KK, Harrison DG. Modulation of extracellular superoxide dismutase expression by angiotensin II and hypertension. Circ Res 1999;85:23-8.
30. Zorov DB, Filburn CR, Klotz LO, Zweier JL, Sollott SJ. Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J Exp Med 2000;192:1001-14.
31. McNally JS, Davis ME, Giddens DP, et al. Role of xanthine oxidoreductase and NAD(P)H oxidase in endothelial superoxide production in response to oscillatory shear stress. Am J Physiol Heart Circ Physiol 2003;285:H2290-7.
32. Antoniades C, Shirodaria C, Warrick N, et al. 5-Methyltetrahydrofolate rapidly improves endothelial function and decreases superoxide production in human vessels: effects on vascular tetrahydrobiopterin availability and endothelial nitric oxide synthase coupling. Circulation 2006;114:1193-201.
33. Ide T, Tsutsui H, Hayashidani S, et al. Mitochondrial DNA damage and dysfunction associated with oxidative stress in failing hearts after myocardial infarction. Circ Res 2001;88:529-35.
34. Tu VC, Bahl JJ, Chen QM. Signals of oxidant-induced cardiomyocyte hypertrophy: key activation of p70 S6 kinase-1 and phosphoinositide 3-kinase. J Pharmacol Exp Ther 2002;300:1101-10.
35. Li L, Takemura G, Li Y, et al. Preventive effect of erythropoietin on cardiac dysfunction in doxorubicin-induced cardiomyopathy. Circulation 2006;113:535-43.
36. Zhu W, Soonpaa MH, Chen H, et al. Acute doxorubicin cardiotoxicity is associated with p53-induced inhibition of the mammalian target of rapamycin pathway. Circulation 2009;119:99-106.
37. Tea BS, Dam TV, Moreau P, Hamet P, deBlois D. Apoptosis during regression of cardiac hypertrophy in spontaneously hypertensive rats: temporal regulation and spatial heterogeneity. Hypertension 1999;34:229-35.
38. Zhang XP, Vatner SF, Shen YT, et al. Increased apoptosis and myocyte enlargement with decreased cardiac mass; distinctive features of the aging male, but not female, monkey heart. J Mol Cell Cardiol 2007;43:487-91.
39. Molkentin JD, Kalvakolanu DV, Markham BE. Transcription factor GATA-4 regulates cardiac muscle-specific expression of the α-myosin heavy-chain gene. Mol Cell Biol 1994;14:4947-57.
40. Murphy AM, Thompson WR, Peng LF, Jones L. Regulation of the rat cardiac troponin I gene by the transcription factor GATA-4. Biochem J 1997;322:393-401.
41. San Jose G, Bidegain J, Robador PA, Diez J, Fortuno A, Zalba G. Insulin-induced NADPH oxidase activation promotes proliferation and matrix metalloproteinase activation in monocytes/macrophages. Free Radic Biol Med 2009;46:1058-67.
42. Kizaki K, Ito R, Okada M, et al. Enhanced gene expression of myocardial matrix metalloproteinases 2 and 9 after acute treatment with doxorubicin in mice. Pharmacol Res 2006;53:341-6.
43. Guzik TJ, Hoch NE, Brown KA, et al. Role of the T cell in the genesis of angiotensin II induced hypertension and vascular dysfunction. J Exp Med 2007;204:2449-60.
44. Shiloh MU, MacMicking JD, Nicholson S, et al. Phenotype of mice and macrophages deficient in both phagocyte oxidase and inducible nitric oxide synthase. Immunity 1999;10:29-38.
45. Ostanin DV, Barlow S, Shukla D, Grisham MB. NADPH oxidase but not myeloperoxidase protects lymphopenic mice from spontaneous infections. Biochem Biophys Res Commun 2007;355:801-6.
46. Custodis F, Eberl M, Kilter H, Bohm M, Laufs U. Association of RhoGDIα with Rac1 GTPase mediates free radical production during myocardial hypertrophy. Cardiovasc Res 2006;71:342-51.
47. Riad A, Bien S, Westermann D, et al. Pretreatment with statin attenuates the cardiotoxicity of doxorubicin in mice. Cancer Res 2009;69:695-9.
48. Zhang M, Kho AL, Anilkumar N, et al. Glycated proteins stimulate reactive oxygen species production in cardiac myocytes: involvement of Nox2 (gp91phox)-containing NADPH oxidase. Circulation 2006;113:1235-43.
49. Bayer AL, Heidkamp MC, Howes AL, Heller Brown J, Byron KL, Samarel AM. Protein kinase Cε-dependent activation of proline-rich tyrosine kinase 2 in neonatal rat ventricular myocytes. J Mol Cell Cardiol 2003;35:1121-33.
50. 2+-sensitive tyrosine kinase Pyk2/CAK β-dependent signaling is essential for G-protein-coupled receptor agonist-induced hypertrophy. J Mol Cell Cardiol 2004;36:799-807.