Norepinephrine causes epigenetic repression of PKCε gene in rodent hearts by activating Nox1-dependent reactive oxygen species production

FASEB Journal

Volumn 26, Issue 7, 2012, Pages 2753-2763

  Xiong, Fuxia ^a   Xiao, Daliao ^a   Zhang, Lubo ^a  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Ischemic heart disease; Oxidative stress; Promoter methylation; Sympathetic activity

Indexed keywords

ACETYLCYSTEINE; APOCYNIN; DIPHENYLIODONIUM SALT; EARLY GROWTH RESPONSE FACTOR 1; MESSENGER RNA; NORADRENALIN; PREGNANCY SPECIFIC BETA1 GLYCOPROTEIN; PROTEIN KINASE C EPSILON; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CONTROLLED STUDY; DNA METHYLATION; EMBRYO CELL; EPIGENETICS; FETUS; FETUS HEART; GENE INTERACTION; GENE REPRESSION; GENE SILENCING; HEART MUSCLE CELL; HEART PROTECTION; HYPOTHESIS; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; OXIDATIVE STRESS; PARASYMPATHETIC TONE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RAT;

ANIMALS; BINDING SITES; CELL LINE; CPG ISLANDS; DNA METHYLATION; EARLY GROWTH RESPONSE PROTEIN 1; EPIGENESIS, GENETIC; FETAL HEART; GENE KNOCKDOWN TECHNIQUES; MODELS, CARDIOVASCULAR; MYOCYTES, CARDIAC; NADH, NADPH OXIDOREDUCTASES; NOREPINEPHRINE; PROMOTER REGIONS, GENETIC; PROTEIN KINASE C-EPSILON; RATS; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; RNA, SMALL INTERFERING; SP1 TRANSCRIPTION FACTOR;

RATTUS; RODENTIA;

EID: 84863206202     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-199422     Document Type: Article

References (38)

1. Lloyd-Jones, D., Adams, R. J., Brown, T. M., Carnethon, M., Dai, S., De Simone, G., Ferguson, T. B., Ford, E., Furie, K., Gillespie, C., Go, A., Greenlund, K., Haase, N., Hailpern, S., Ho, P. M., Howard, V., Kissela, B., Kittner, S., Lackland, D., Lisabeth, L., Marelli, A., McDermott, M. M., Meigs, J., Mozaffarian, D., Mussolino, M., Nichol, G., Roger, V. L., Rosamond, W., Sacco, R., Sorlie, P., Thom, T., Wasserthiel-Smoller, S., Wong, N. D., and Wylie-Rosett, J. (2010) Heart disease and stroke statistics-2010 update: a report from the American Heart Association. Circulation 121, e46-e215
2. Barker, D. J., and Osmond, C. (1986) Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 1, 1077-1081 (Pubitemid 16106274)
3. Bateson, P., Barker, D., Clutton-Brock, T., Deb, D., D'Udine, B., Foley, R. A., Gluckman, P., Godfrey, K., Kirkwood, T., Lahr, M. M., McNamara, J., Metcalfe, N. B., Monaghan, P., Spencer, H. G., and Sultan, S. E. (2004) Developmental plasticity and human health. Nature 430, 419-421 (Pubitemid 38987896)
4. Gluckman, P. D., Hanson, M. A., Cooper, C., and Thornburg, K. L. (2008) Effect of in utero and early-life conditions on adult health and disease. N. Engl. J. Med. 359, 61-73
5. McMillen, I. C., and Robinson, J. S. (2005) Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol. Rev. 85, 571-633 (Pubitemid 40404637)
6. Lawrence, J., Xiao, D., Xue, Q., Rejali, M., Yang, S., and Zhang, L. (2008) Prenatal nicotine exposure increases heart susceptibility to ischemia/reperfusion injury in adult offspring. J. Pharmacol. Exp. Ther. 324, 331-341 (Pubitemid 350294154)
7. Meyer, K., Zhang, H., and Zhang, L. (2009) Direct effect of cocaine on epigenetic regulation of PKCepsilon gene repression in the fetal rat heart. J. Mol. Cell. Cardiol. 47, 504-511
8. Zhang, H., Meyer, K. D., and Zhang, L. (2009) Fetal exposure to cocaine causes programming of Prkce gene repression in the left ventricle of adult rat offspring. Biol. Reprod. 80, 440-448
9. Meyer, K. D., Zhang, H., and Zhang, L. (2009) Prenatal cocaine exposure abolished ischemic preconditioning-induced protection in adult male rat hearts: role of PKCepsilon. Am. J. Physiol. Heart Circ. Physiol. 296, H1566-H1576
10. Xue, Q., and Zhang, L. (2009) Prenatal hypoxia causes a sex-dependent increase in heart susceptibility to ischemia and reperfusion injury in adult male offspring: role of protein kinase C epsilon. J. Pharmacol. Exp. Ther. 330, 624-632
11. Patterson, A. J., Chen, M., Xue, Q., Xiao, D., and Zhang, L. (2010) Chronic prenatal hypoxia induces epigenetic programming of PKCε gene repression in rat hearts. Circ. Res. 107, 365-373
12. Lawrence, J., Chen, M., Xiong, F., Xiao, D., Zhang, H., Buchholz, J. N., and Zhang, L. (2011) Foetal nicotine exposure causes PKCepsilon gene repression by promoter methylation in rat hearts. Cardiovasc. Res. 89, 89-97
13. Ping, P., Zhang, J., Pierce, W. M., Jr., and Bolli, R. (2001) Functional proteomic analysis of protein kinase C epsilon signaling complexes in the normal heart and during cardioprotection. Circ. Res. 88, 59-62 (Pubitemid 32064083)
14. Chen, L., Hahn, H., Wu, G., Chen, C. H., Liron, T., Schechtman, D., Cavallaro, G., Banci, L., Guo, Y., Bolli, R., Dorn, G. W., 2nd, and Mochly-Rosen, D. (2001) Opposing cardioprotective actions and parallel hypertrophic effects of delta PKC and epsilon PKC. Proc. Natl. Acad. Sci. U. S. A. 98, 11114-11119 (Pubitemid 32928691)
15. Murriel, C. L., and Mochly-Rosen, D. (2003) Opposing roles of delta and epsilonPKC in cardiac ischemia and reperfusion: targeting the apoptotic machinery. Arch. Biochem. Biophys. 420, 246-254 (Pubitemid 37491108)
16. Gray, M. O., Zhou, H. Z., Schafhalter-Zoppoth, I., Zhu, P., Mochly-Rosen, D., and Messing, R. O. (2004) Preservation of base-line hemodynamic function and loss of inducible cardioprotection in adult mice lacking protein kinase C epsilon. J. Biol. Chem. 279, 3596-3604 (Pubitemid 38140600)
17. Lim, S. O., Gu, J. M., Kim, M. S., Kim, H. S., Park, Y. N., Park, C. K., Cho, J. W., Park, Y. M., and Jung, G. (2008) Epigenetic changes induced by reactive oxygen species in hepatocellular carcinoma: methylation of the E-cadherin promoter. Gastroenterology 135, 2128-2140, 2140 e2121-2128
18. Liang, C., Rounds, N. K., Dong, E., Stevens, S. Y., Shite, J., and Qin, F. (2000) Alterations by norepinephrine of cardiac sympathetic nerve terminal function and myocardial beta-adrenergic receptor sensitivity in the ferret: normalization by antioxidant vitamins. Circulation 102, 96-103 (Pubitemid 30430559)
19. Murdoch, C. E., Zhang, M., Cave, A. C., and Shah, A. M. (2006) NADPH oxidase-dependent redox signalling in cardiac hypertrophy, remodelling and failure. Cardiovasc. Res. 71, 208 -215
20. Wang, H., and Joseph, J. A. (1999) Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader. Free Radic. Biol. Med. 27, 612-616 (Pubitemid 29408648)
21. Csont, T., Bereczki, E., Bencsik, P., Fodor, G., Gorbe, A., Zvara, A., Csonka, C., Puskas, L. G., Santha, M., and Ferdinandy, P. (2007) Hypercholesterolemia increases myocardial oxidative and nitrosative stress thereby leading to cardiac dysfunction in apoB-100 transgenic mice. Cardiovasc. Res. 76, 100-109 (Pubitemid 47362048)
22. Kuznetsov, A. V., Kehrer, I., Kozlov, A. V., Haller, M., Redl, H., Hermann, M., Grimm, M., and Troppmair, J. (2011) Mitochondrial ROS production under cellular stress: comparison of different detection methods. Anal. Bioanal. Chem. 400, 2383-2390
23. Patterson, A. J., Xiao, D., Xiong, F., Dixon, B., and Zhang, L. (2012) Hypoxia-derived oxidative stress mediates epigenetic repression of PKCε gene in foetal rat hearts. Cardiovasc. Res. 93, 302-310
24. Matsuno, K., Yamada, H., Iwata, K., Jin, D., Katsuyama, M., Matsuki, M., Takai, S., Yamanishi, K., Miyazaki, M., Matsubara, H., and Yabe-Nishimura, C. (2005) Nox1 is involved in angiotensin II-mediated hypertension: a study in Nox1-deficient mice. Circulation 112, 2677-2685 (Pubitemid 41532605)
25. Looi, Y. H., Grieve, D. J., Siva, A., Walker, S. J., Anilkumar, N., Cave, A. C., Marber, M., Monaghan, M. J., and Shah, A. M. (2008) Involvement of Nox2 NADPH oxidase in adverse cardiac remodeling after myocardial infarction. Hypertension 51, 319-325 (Pubitemid 351159945)
26. Kuroda, J., Ago, T., Matsushima, S., Zhai, P., Schneider, M. D., and Sadoshima, J. (2010) NADPH oxidase 4 (Nox4) is a major source of oxidative stress in the failing heart. Proc. Natl. Acad. Sci. U. S. A. 107, 15565-15570
27. Nisimoto, Y., Tsubouchi, R., Diebold, B. A., Qiao, S., Ogawa, H., Ohara, T., and Tamura, M. (2008) Activation of NADPH oxidase 1 in tumour colon epithelial cells. Biochem. J. 415, 57-65
28. Shinohara, M., Shang, W. H., Kubodera, M., Harada, S., Mitsushita, J., Kato, M., Miyazaki, H., Sumimoto, H., and Kamata, T. (2007) Nox1 redox signaling mediates oncogenic Ras-induced disruption of stress fibers and focal adhesions by down-regulating Rho. J. Biol. Chem. 282, 17640-17648 (Pubitemid 47100324)
29. Ago, T., Kuroda, J., Pain, J., Fu, C., Li, H., and Sadoshima, J. (2010) Upregulation of Nox4 by hypertrophic stimuli promotes apoptosis and mitochondrial dysfunction in cardiac myocytes. Circ. Res. 106, 1253-1264
30. Block, K., Gorin, Y., and Abboud, H. E. (2009) Subcellular localization of Nox4 and regulation in diabetes. Proc. Natl. Acad. Sci. U. S. A. 106, 14385-14390
31. Kuroda, J., Nakagawa, K., Yamasaki, T., Nakamura, K., Takeya, R., Kuribayashi, F., Imajoh-Ohmi, S., Igarashi, K., Shibata, Y., Sueishi, K., and Sumimoto, H. (2005) The superoxide-producing NAD(P)H oxidase Nox4 in the nucleus of human vascular endothelial cells. Genes Cells 10, 1139-1151 (Pubitemid 41830073)
32. Hilenski, L. L., Clempus, R. E., Quinn, M. T., Lambeth, J. D., and Griendling, K. K. (2004) Distinct subcellular localizations of Nox1 and Nox4 in vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 24, 677-683 (Pubitemid 38451603)
33. Lassegue, B., Sorescu, D., Szocs, K., Yin, Q., Akers, M., Zhang, Y., Grant, S. L., Lambeth, J. D., and Griendling, K. K. (2001) Novel gp91(phox) homologues in vascular smooth muscle cells: nox1 mediates angiotensin II-induced superoxide formation and redox-sensitive signaling pathways. Circ. Res. 88, 888-894 (Pubitemid 32441466)
34. Van Buul, J. D., Fernandez-Borja, M., Anthony, E. C., and Hordijk, P. L. (2005) Expression and localization of NOX2 and NOX4 in primary human endothelial cells. Antioxid. Redox Signal. 7, 308-317 (Pubitemid 40279800)
35. Ago, T., Kitazono, T., Ooboshi, H., Iyama, T., Han, Y. H., Takada, J., Wakisaka, M., Ibayashi, S., Utsumi, H., and Iida, M. (2004) Nox4 as the major catalytic component of an endothelial NAD(P)H oxidase. Circulation 109, 227-233 (Pubitemid 38114144)
36. Borchi, E., Parri, M., Papucci, L., Becatti, M., Nassi, N., Nassi, P., and Nediani, C. (2009) Role of NADPH oxidase in H9c2 cardiac muscle cells exposed to simulated ischaemia-reperfusion. J. Cell. Mol. Med. 13, 2724-2735
37. Skalnik, D. G., Strauss, E. C., and Orkin, S. H. (1991) CCAAT displacement protein as a repressor of the myelomonocytic-specific gp91-phox gene promoter. J. Biol. Chem. 266, 16736-16744 (Pubitemid 21907861)
38. Malpas, S. C. (2010) Sympathetic nervous system overactivity and its role in the development of cardiovascular disease. Physiol. Rev. 90, 513-557