Left ventricular diastolic dysfunction in Nrf2 knock out mice is associated with cardiac hypertrophy, decreased expression of SERCA2a, and preserved endothelial function

Free Radical Biology and Medicine

Volumn 89, Issue , 2015, Pages 906-917

  Erkens, Ralf ^a   Kramer, Christian M ^a   Lückstädt, Wiebke ^a   Panknin, Christina ^a   Krause, Lisann ^a   Weidenbach, Mathias ^a   Dirzka, Jennifer ^a   Krenz, Thomas ^a   Mergia, Evanthia ^b   Suvorava, Tatsiana ^a   Kelm, Malte ^a   Cortese Krott, Miriam M ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Echocardiography; eNOS; Flow mediated dilation; High resolution ultrasound; Nrf2 KO; Translational research

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; ISOPRENALINE; NITROPRUSSIDE SODIUM; OUABAIN; PHENYLEPHRINE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE 2A; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; NFE2L2 PROTEIN, MOUSE;

ANIMAL MODEL; AORTA; ARTICLE; BETA ADRENERGIC STIMULATION; BLOOD PRESSURE; BLOOD VESSEL REACTIVITY; CARDIOVASCULAR SYSTEM; CELL FUNCTION; CONTROLLED STUDY; DECELERATION; DIASTOLE; ECHOCARDIOGRAPHY; EX VIVO STUDY; HEART; HEART HEMODYNAMICS; HEART INDEX; HEART MUSCLE; HEART MUSCLE RELAXATION; HEART PERFORMANCE; HEART VENTRICLE HYPERTROPHY; HUMAN; HUMAN CELL; IN VIVO STUDY; LEFT VENTRICULAR DIASTOLIC DYSFUNCTION; MALE; MOUSE; MYOCARDIAL PERFORMANCE INDEX; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; RELAXATION TIME; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULAR ENDOTHELIUM; VASCULARIZATION; VASODILATATION; ANIMAL; C57BL MOUSE; CARDIOMEGALY; CARDIOMYOPATHIES; CELL CULTURE; CELL PROLIFERATION; ENZYME IMMUNOASSAY; FEMALE; HEART LEFT VENTRICLE FUNCTION; HEART VENTRICLE REMODELING; HEMODYNAMICS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGY; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CARDIOMEGALY; CARDIOMYOPATHIES; CELL PROLIFERATION; CELLS, CULTURED; ECHOCARDIOGRAPHY; ENDOTHELIUM, VASCULAR; FEMALE; HEMODYNAMICS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; IMMUNOENZYME TECHNIQUES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-E2-RELATED FACTOR 2; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; VENTRICULAR DYSFUNCTION, LEFT; VENTRICULAR REMODELING;

EID: 84946111638     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2015.10.409     Document Type: Article

References (54)

1. T. Suzuki, and M. Yamamoto Molecular basis of the Keap1-Nrf2 system Free Radic. Biol. Med. 2015
2. K. Itoh, T. Chiba, S. Takahashi, T. Ishii, K. Igarashi, Y. Katoh, T. Oyake, N. Hayashi, K. Satoh, I. Hatayama, M. Yamamoto, and Y. Nabeshima An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements Biochem. Biophys. Res. Commun. 236 1997 313 322
3. A. Enomoto, K. Itoh, E. Nagayoshi, J. Haruta, T. Kimura, T. O'Connor, T. Harada, and M. Yamamoto High sensitivity of Nrf2 knockout mice to acetaminophen hepatotoxicity associated with decreased expression of ARE-regulated drug metabolizing enzymes and antioxidant genes Tox. Sci 59 2001 169 177
4. H. Sies Oxidative stress: a concept in redox biology and medicine Redox biol 2015
5. M. Seddon, Y.H. Looi, and A.M. Shah Oxidative stress and redox signalling in cardiac hypertrophy and heart failure Heart 93 2007 903 907
6. E. Kansanen, S.M. Kuosmanen, H. Leinonen, and A.-L. Levonen The Keap1-Nrf2 pathway: Mechanisms of activation and dysregulation in cancer Redox biol 1 2013 45 49
7. L. Gan, and J.A. Johnson Oxidative damage and the Nrf2-ARE pathway in neurodegenerative diseases Biochim. Biophys. Acta 1842 2014 1208 1218
8. J. Pi, L. Leung, P. Xue, W. Wang, Y. Hou, D. Liu, E. Yehuda-Shnaidman, C. Lee, J. Lau, T.W. Kurtz, and J.Y. Chan Deficiency in the nuclear factor E2-related factor-2 transcription factor results in impaired adipogenesis and protects against diet-induced obesity J. Biol. Chem. 285 2010 9292 9300
9. A. Alfieri, S. Srivastava, R.C. Siow, M. Modo, P.A. Fraser, and G.E. Mann Targeting the Nrf2-Keap1 antioxidant defence pathway for neurovascular protection in stroke J. Physiol. 589 2011 4125 4136
10. A. Uruno, Y. Yagishita, and M. Yamamoto The Keap1-Nrf2 system and diabetes mellitus Arch. Biochem. Biophys. 566 2015 76 84
11. H. Zhang, K.J. Davies, and H.J. Forman Oxidative stress response and Nrf2 signaling in aging Free Radic. Biol. Med. 2015
12. M.M. Cortese-Krott, C.V. Suschek, W. Wetzel, K.-D. Kröncke, and V. Kolb-Bachofen Nitric oxide-mediated protection of endothelial cells from hydrogen peroxide is mediated by intracellular zinc and glutathione Am. J. Physiol.- Cell. Ph 296 2009 C811 C820
13. M.M. Cortese, C.V. Suschek, W. Wetzel, K.-D. Kröncke, and V. Kolb-Bachofen Zinc protects endothelial cells from hydrogen peroxide via Nrf2-dependent stimulation of glutathione biosynthesis Free Radic. Biol. Med. 44 2008 2002 2012
14. H. Zhu, Z. Jia, B.R. Misra, L. Zhang, Z. Cao, M. Yamamoto, M.A. Trush, H.P. Misra, and Y. Li Nuclear factor E2-related factor 2-dependent myocardiac cytoprotection against oxidative and electrophilic stress Cardiovasc. Toxicol. 8 2008 71 85
15. A.C. Brewer, T.V. Murray, M. Arno, M. Zhang, N.P. Anilkumar, G.E. Mann, and A.M. Shah Nox4 regulates Nrf2 and glutathione redox in cardiomyocytes in vivo Free Radic. Biol. Med. 51 2011 205 215
16. J.W. Calvert, S. Jha, S. Gundewar, J.W. Elrod, A. Ramachandran, C.B. Pattillo, C.G. Kevil, and D.J. Lefer Hydrogen sulfide mediates cardioprotection through Nrf2 signaling Circ. Res. 105 2009 365 374
17. B. Xu, J. Zhang, J. Strom, S. Lee, and Q.M. Chen Myocardial ischemic reperfusion induces de novo Nrf2 protein translation Biochim. Biophys. Acta 1842 2014 1638 1647
18. M. Kelm Flow-mediated dilatation in human circulation: diagnostic and therapeutic aspects Am. J. Physiol: Heart and Circ. Physiol 282 2002 H1 H5
19. T. Gori, S. Dragoni, M. Lisi, G. Di Stolfo, S. Sonnati, M. Fineschi, and J.D. Parker Conduit artery constriction mediated by low flow a novel noninvasive method for the assessment of vascular function J. Am. Coll. Cardiol. 51 2008 1953 1958
20. A. Gödecke, U.K. Decking, Z. Ding, J. Hirchenhain, H.-J. Bidmon, S. Gödecke, and J. Schrader Coronary hemodynamics in endothelial NO synthase knockout mice Circ. Res. 82 1998 186 194
21. K.C. Wood, M.M. Cortese-Krott, J.C. Kovacic, A. Noguchi, V.B. Liu, X. Wang, N. Raghavachari, M. Boehm, G.J. Kato, and M. Kelm Circulating blood endothelial nitric oxide synthase contributes to the regulation of systemic blood pressure and nitrite homeostasis Arterioscler. Thromb. Vasc. Biol. 33 2013 1861 1871
22. C. Tei, R.A. Nishimura, J.B. Seward, and A.J. Tajik Noninvasive Doppler-derived myocardial performance index: correlation with simultaneous measurements of cardiac catheterization measurements J. Am. Soc. Echocard 10 1997 169 178
23. J. Ärnlöv, E. Ingelsson, U. Risérus, B. Andrén, and L. Lind Myocardial performance index, a Doppler-derived index of global left ventricular function, predicts congestive heart failure in elderly men Eur. Heart J. 25 2004 2220 2225
24. D. Schuler, R. Sansone, T. Freudenberger, A. Rodriguez-Mateos, G. Weber, T.Y. Momma, C. Goy, J. Altschmied, J. Haendeler, J.W. Fischer, M. Kelm, and C. Heiss Measurement of endothelium-dependent vasodilation in mice - Brief Report Arterioscler. Thromb. Vasc. Biol. 34 2014 2651 2657
25. C. Rammos, U.B. Hendgen-Cotta, R. Deenen, J. Pohl, P. Stock, C. Hinzmann, M. Kelm, and T. Rassaf Age-related vascular gene expression profiling in mice Mech. Ageing Dev. 135 2014 15 23
26. T. Suvorava, N. Lauer, S. Kumpf, R. Jacob, W. Meyer, and G. Kojda Endogenous vascular hydrogen peroxide regulates arteriolar tension in vivo Circulation 112 2005 2487 2495
27. U. Flögel, U.K. Decking, A. Gödecke, and J. Schrader Contribution of NO to ischemia-reperfusion injury in the saline-perfused heart: a study in endothelial NO synthase knockout mice J. Mol. Cell. Cardiol. 31 1999 827 836
28. P. Pacher, T. Nagayama, P. Mukhopadhyay, S. Bátkai, and D.A. Kass Measurement of cardiac function using pressure-volume conductance catheter technique in mice and rats Nat. Protoc. 3 2008 1422 1434
29. E. Mergia, A. Friebe, O. Dangel, M. Russwurm, and D. Koesling Spare guanylyl cyclase NO receptors ensure high NO sensitivity in the vascular system J. Clin. Invest. 116 2006 1731 1737
30. T. Rassaf, N.S. Bryan, M. Kelm, and M. Feelisch Concomitant presence of N-nitroso and S-nitroso proteins in human plasma Free Radic. Biol. Med. 33 2002 1590 1596
31. X. He, and Q. Ma Redox regulation by nuclear factor erythroid 2-related factor 2: gatekeeping for the basal and diabetes-induced expression of thioredoxin-interacting protein Mol. Pharmacol. 82 2012 887 897
32. J. Li, T. Ichikawa, L. Villacorta, J.S. Janicki, G.L. Brower, M. Yamamoto, and T. Cui Nrf2 protects against maladaptive cardiac responses to hemodynamic stress Arterioscler. Thromb. Vasc. Biol. 29 2009 1843 1850
33. Lacher, S.E.; Lee, J.S.; Wang, X.; Campbell, M.R.; Bell, D.A.; Slattery, M. Beyond antioxidant genes in the ancient Nrf2 regulatory network. Free Radical Biol. Med.
34. E.H. Heiss, D. Schachner, E.R. Werner, and V.M. Dirsch Active NF-E2-related factor (Nrf2) contributes to keep endothelial NO synthase (eNOS) in the coupled state role of reactive oxygen species (ROS), eNOS, and heme oxygenase (HO-1) levels J. Biol. Chem. 284 2009 31579 31586
35. C.X. Santos, N. Anilkumar, M. Zhang, A.C. Brewer, and A.M. Shah Redox signaling in cardiac myocytes Free Radic. Biol. Med. 50 2011 777 793
36. Y. Ding, B. Zhang, K. Zhou, M. Chen, M. Wang, Y. Jia, Y. Song, Y. Li, and A. Wen Dietary ellagic acid improves oxidant-induced endothelial dysfunction and atherosclerosis: role of Nrf2 activation Int. J. Cardiol. 175 2014 508 514
37. M. Buelna-Chontal, J.-G. Guevara-Chávez, A. Silva-Palacios, O.-N. Medina-Campos, J. Pedraza-Chaverri, and C. Zazueta Nrf2-regulated antioxidant response is activated by protein kinase C in postconditioned rat hearts Free Rad. Biol. Med 74 2014 145 156
38. H. Tsutsui, S. Kinugawa, and S. Matsushima Oxidative stress and heart failure Am. J. Physiol. Heart Circ. Physiol 301 2011 H2181 H2190
39. L. Cominacini, C. Mozzini, U. Garbin, A. Pasini, C. Stranieri, E. Solani, P. Vallerio, I.A. Tinelli, and A. Fratta Pasini Endoplasmic reticulum stress and Nrf2 signaling in cardiovascular diseases Free Radic. Biol. Med. 2015
40. P. Giannuzzi, A. Imparato, P.L. Temporelli, F. de Vito, P.L. Silva, F. Scapellato, and A. Giordano Doppler-derived mitral deceleration time of early filling as a strong predictor of pulmonary capillary wedge pressure in postinfarction patients with left ventricular systolic dysfunction J. Am. Coll. Cardiol. 23 1994 1630 1637
41. M.J. García, L. Rodríguez, M. Ares, B.P. Griffin, J.D. Thomas, and A.L. Klein Differentiation of constrictive pericarditis from restrictive cardiomyopathy: assessment of left ventricular diastolic velocities in longitudinal axis by Doppler tissue imaging J. Am. Coll. Cardiol. 27 1996 108 114
42. J.-M. Lee, A.Y. Shih, T.H. Murphy, and J.A. Johnson NF-E2-related factor-2 mediates neuroprotection against mitochondrial complex I inhibitors and increased concentrations of intracellular calcium in primary cortical neurons J. Biol. Chem. 278 2003 37948 37956
43. M.A. Shareef, L.A. Anwer, and C. Poizat Cardiac SERCA2a/b: therapeutic targets for heart failure Eur J. Pharmacol. 724 2014 1 8
44. C.T. Tsai, C.K. Wu, J.K. Lee, S.N. Chang, Y.M. Kuo, Y.C. Wang, L.P. Lai, F.T. Chiang, J.J. Hwang, and J.L. Lin TNF-alpha down-regulates sarcoplasmic reticulum Ca(2)(+) ATPase expression and leads to left ventricular diastolic dysfunction through binding of NF-kappaB to promoter response element Cardiovasc. Res. 105 2015 318 329
45. K. Yoh, K. Itoh, A. Enomoto, A. Hirayama, N. Yamaguchi, M. Kobayashi, N. Morito, A. Koyama, M. Yamamoto, and S. Takahashi Nrf2-deficient female mice develop lupus-like autoimmune nephritis Kidney Int. 60 2001 1343 1353
46. H. Li, S. Horke, and U. Forstermann Vascular oxidative stress, nitric oxide and atherosclerosis Atherosclerosis 237 2014 208 219
47. P. Kleinbongard, A. Dejam, T. Lauer, T. Jax, S. Kerber, P. Gharini, J. Balzer, R.B. Zotz, R.E. Scharf, R. Willers, A.N. Schechter, M. Feelisch, and M. Kelm Plasma nitrite concentrations reflect the degree of endothelial dysfunction in humans Free Radic. Biol. Med. 40 2006 295 302
48. T. Suvorava, N. Nagy, S. Pick, O. Lieven, U. Ruther, V.T. Dao, J.W. Fischer, M. Weber, and G. Kojda Impact of eNOS-Dependent Oxidative Stress on Endothelial Function and Neointima Formation Antioxid. Redox Signal. 23 2015 711 723
49. H.K. Jyrkkanen, E. Kansanen, M. Inkala, A.M. Kivela, H. Hurttila, S.E. Heinonen, G. Goldsteins, S. Jauhiainen, S. Tiainen, H. Makkonen, O. Oskolkova, T. Afonyushkin, J. Koistinaho, M. Yamamoto, V.N. Bochkov, S. Yla-Herttuala, and A.L. Levonen Nrf2 regulates antioxidant gene expression evoked by oxidized phospholipids in endothelial cells and murine arteries in vivo Circ. Res. 103 2008 e1-9
50. J.-L. Balligand, O. Feron, and C. Dessy eNOS activation by physical forces: from short-term regulation of contraction to chronic remodeling of cardiovascular tissues Physiol. Rev. 89 2009 481 534
51. J.B. Laursen, M. Somers, S. Kurz, L. McCann, A. Warnholtz, B.A. Freeman, M. Tarpey, T. Fukai, and D.G. Harrison Endothelial regulation of vasomotion in apoE-deficient mice: implications for interactions between peroxynitrite and tetrahydrobiopterin Circulation 103 2001 1282 1288
52. P. Massion, and J.-L. Balligand Modulation of cardiac contraction, relaxation and rate by the endothelial nitric oxide synthase (eNOS): lessons from genetically modified mice J. Physiol. 546 2003 63 75
53. T. Suvorava, and G. Kojda Reactive oxygen species as cardiovascular mediators: lessons from endothelial-specific protein overexpression mouse models Biochim. Biophys. Acta 1787 2009 802 810
54. T.E. Owan, D.O. Hodge, R.M. Herges, S.J. Jacobsen, V.L. Roger, and M.M. Redfield Trends in prevalence and outcome of heart failure with preserved ejection fraction N. Engl. J. Med. 355 2006 251 259