Estradiol mediates vasculoprotection via ERRα-dependent regulation of lipid and ROS metabolism in the endothelium

Journal of Molecular and Cellular Cardiology

Volumn 87, Issue , 2015, Pages 92-101

  Li, Huawen ^a   Liu, Zhaoyu ^b   Gou, Yulan ^c   Yu, Haibing ^a   Siminelakis, Stavros ^d   Wang, Shixuan ^b   Kong, Danli ^a   Zhou, Yikai ^e   Liu, Zhengxiang ^b   Ding, Yuanling ^a   Yao, Dachun ^a  

^a GUANGDONG MEDICAL UNIVERSITY   (China)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c WUHAN NO 1 HOSPITAL   (China)

^d UNIVERSITY OF IOANNINA   (Greece)

^e HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Estrogen receptor; Fatty acid metabolism; Mitochondria; Reactive oxygen species; Vascular function

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANGIOPOIETIN 2; ESTRADIOL; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ESTROGEN RELATED RECEPTOR ALPHA; INTERLEUKIN 8; LIPID; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE SYNTHASE; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR SP1; VASCULAR CELL ADHESION MOLECULE 1; VASCULOTROPIN; VASCULOTROPIN RECEPTOR; ERRALPHA ESTROGEN-RELATED RECEPTOR; ESTROGEN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL MODEL; AORTA ENDOTHELIUM; ARTICLE; BINDING KINETICS; BLOOD VESSEL INJURY; CELL FUNCTION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; FATTY ACID OXIDATION; FATTY ACID TRANSPORT; FEMALE; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INSULIN RESISTANCE; LIPID BLOOD LEVEL; MALE; MITOCHONDRIAL DNA REPLICATION; MITOCHONDRIAL DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTECTION; PROTEIN EXPRESSION; TRANSCRIPTION INITIATION; UPREGULATION; VASCULOPROTECTION; ANIMAL; AORTA; BIOSYNTHESIS; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIPID DIET; LIPID METABOLISM; METABOLISM; MITOCHONDRION; PATHOLOGY; VASCULAR ENDOTHELIUM;

ANIMALIA; LENTIVIRUS; MUS;

ANIMALS; AORTA; DIET, HIGH-FAT; ENDOTHELIUM, VASCULAR; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ESTROGENS; GENE EXPRESSION REGULATION; HUMANS; LIPID METABOLISM; MICE; MITOCHONDRIA; REACTIVE OXYGEN SPECIES; RECEPTORS, ESTROGEN;

EID: 84939642691     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2015.08.008     Document Type: Article

References (30)

1. Grodstein F., Stampfer M.J., Manson J.E., Colditz G.A., Willett W.C., Rosner B., Speizer F.E., Hennekens C.H. Postmenopausal estrogen and progestin use and the risk of cardiovascular disease. N. Engl. J. Med. 1996, 335(7):453-461.
2. Xing D., Nozell S., Chen Y.F., Hage F., Oparil S. Estrogen and mechanisms of vascular protection. Arterioscler. Thromb. Vasc. Biol. 2009, 29(3):289-295.
3. Giguere V., Yang N., Segui P., Evans R.M. Identification of a new class of steroid hormone receptors. Nature 1988, 331(6151):91-94.
4. Billon-Gales A., Fontaine C., Douin-Echinard V., Delpy L., Berges H., Calippe B., Lenfant F., Laurell H., Guery J.C., Gourdy P., Arnal J.F. Endothelial estrogen receptor-alpha plays a crucial role in the atheroprotective action of 17beta-estradiol in low-density lipoprotein receptor-deficient mice. Circulation 2009, 120(25):2567-2576.
5. Couse J.F., Korach K.S. Estrogen receptor null mice: what have we learned and where will they lead us?. Endocr. Rev. 1999, 20(3):358-417.
6. Villablanca A.C., Tenwolde A., Lee M., Huck M., Mumenthaler S., Rutledge J.C. 17beta-estradiol prevents early-stage atherosclerosis in estrogen receptor-alpha deficient female mice. J. Cardiovasc. Transl. Res. 2009, 2(3):289-299.
7. Ihionkhan C.E., Chambliss K.L., Gibson L.L., Hahner L.D., Mendelsohn M.E., Shaul P.W. Estrogen causes dynamic alterations in endothelial estrogen receptor expression. Circ. Res. 2002, 91(9):814-820.
8. Arnal J.F., Fontaine C., Billon-Gales A., Favre J., Laurell H., Lenfant F., Gourdy P. Estrogen receptors and endothelium. Arterioscler. Thromb. Vasc. Biol. 2010, 30(8):1506-1512.
9. Vanacker J.M., Pettersson K., Gustafsson J.A., Laudet V. Transcriptional targets shared by estrogen receptor- related receptors (ERRs) and estrogen receptor (ER) alpha, but not by ERbeta. EMBO J. 1999, 18(15):4270-4279.
10. Giguere V. Transcriptional control of energy homeostasis by the estrogen-related receptors. Endocr. Rev. 2008, 29(6):677-696.
11. St-Pierre J., Drori S., Uldry M., Silvaggi J.M., Rhee J., Jager S., Handschin C., Zheng K., Lin J., Yang W., Simon D.K., Bachoo R., Spiegelman B.M. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 2006, 127(2):397-408.
12. Schreiber S.N., Emter R., Hock M.B., Knutti D., Cardenas J., Podvinec M., Oakeley E.J., Kralli A. The estrogen-related receptor alpha (ERRalpha) functions in PPARgamma coactivator 1alpha (PGC-1alpha)-induced mitochondrial biogenesis. Proc. Natl. Acad. Sci. U. S. A. 2004, 101(17):6472-6477.
13. Huss J.M., Torra I.P., Staels B., Giguere V., Kelly D.P. Estrogen-related receptor alpha directs peroxisome proliferator-activated receptor alpha signaling in the transcriptional control of energy metabolism in cardiac and skeletal muscle. Mol. Cell. Biol. 2004, 24(20):9079-9091.
14. Nakajima H., Ishida T., Satomi-Kobayashi S., Mori K., Hara T., Sasaki N., Yasuda T., Toh R., Tanaka H., Kawai H., Hirata K. Endothelial lipase modulates pressure overload-induced heart failure through alternative pathway for fatty acid uptake. Hypertension 2013, 61(5):1002-1007.
15. Kelly D.P., Scarpulla R.C. Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev. 2004, 18(4):357-368.
16. Luo J., Sladek R., Carrier J., Bader J.A., Richard D., Giguere V. Reduced fat mass in mice lacking orphan nuclear receptor estrogen-related receptor alpha. Mol. Cell. Biol. 2003, 23(22):7947-7956.
17. Hu X., Xu X., Lu Z., Zhang P., Fassett J., Zhang Y., Xin Y., Hall J.L., Viollet B., Bache R.J., Huang Y., Chen Y. AMP activated protein kinase-alpha2 regulates expression of estrogen-related receptor-alpha, a metabolic transcription factor related to heart failure development. Hypertension 2011, 58(4):696-703.
18. Liu D., Zhang Z., Gladwell W., Teng C.T. Estrogen stimulates estrogen-related receptor alpha gene expression through conserved hormone response elements. Endocrinology 2003, 144(11):4894-4904.
19. Vanacker J.M., Bonnelye E., Chopin-Delannoy S., Delmarre C., Cavailles V., Laudet V. Transcriptional activities of the orphan nuclear receptor ERR alpha (estrogen receptor-related receptor-alpha). Mol. Endocrinol. 1999, 13(5):764-773.
20. Liu Z., Gou Y., Zhang H., Zuo H., Yao D. Estradiol improves cardiovascular function through up-regulation of SOD2 on vascular wall. Redox Biol. 2014, 3:88-99.
21. Mirebeau-Prunier D., Le Pennec S., Jacques C., Gueguen N., Poirier J., Malthiery Y., Savagner F. Estrogen-related receptor alpha and PGC-1-related coactivator constitute a novel complex mediating the biogenesis of functional mitochondria. FEBS J. 2010, 277(3):713-725.
22. O'Lone R., Frith M.C., Karlsson E.K., Hansen U. Genomic targets of nuclear estrogen receptors. Mol. Endocrinol. 2004, 18(8):1859-1875.
23. Carrier J.C., Deblois G., Champigny C., Levy E., Giguere V. Estrogen-related receptor alpha (ERRalpha) is a transcriptional regulator of apolipoprotein A-IV and controls lipid handling in the intestine. J. Biol. Chem. 2004, 279(50):52052-52058.
24. Favre J., Gao J., Henry J.P., Remy-Jouet I., Fourquaux I., Billon-Gales A., Thuillez C., Arnal J.F., Lenfant F., Richard V. Endothelial estrogen receptor {alpha} plays an essential role in the coronary and myocardial protective effects of estradiol in ischemia/reperfusion. Arterioscler. Thromb. Vasc. Biol. 2010, 30(12):2562-2567.
25. Theelen T.L., Lappalainen J.P., Sluimer J.C., Gurzeler E., Cleutjens J.P., Gijbels M.J., Biessen E.A., Daemen M.J., Alitalo K., Yla-Herttuala S. Angiopoietin-2 blocking antibodies reduce early atherosclerotic plaque development in mice. Atherosclerosis 2015, 241(2):297-304.
26. Sumi D., Ignarro L.J. Estrogen-related receptor alpha 1 up-regulates endothelial nitric oxide synthase expression. Proc. Natl. Acad. Sci. U. S. A. 2003, 100(24):14451-14456.
27. Zhu L., Brown W.C., Cai Q., Krust A., Chambon P., McGuinness O.P., Stafford J.M. Estrogen treatment after ovariectomy protects against fatty liver and may improve pathway-selective insulin resistance. Diabetes 2012, 62(2):424-434.
28. Esposito K., Marfella R., Ciotola M., Di Palo C., Giugliano F., Giugliano G., D'Armiento M., D'Andrea F., Giugliano D. Effect of a mediterranean-style diet on endothelial dysfunction and markers of vascular inflammation in the metabolic syndrome: a randomized trial. JAMA 2004, 292(12):1440-1446.
29. Al Suwaidi J., Higano S.T., Holmes D.R., Lennon R., Lerman A. Obesity is independently associated with coronary endothelial dysfunction in patients with normal or mildly diseased coronary arteries. J. Am. Coll. Cardiol. 2001, 37(6):1523-1528.
30. Sihag S., Cresci S., Li A.Y., Sucharov C.C., Lehman J.J. PGC-1alpha and ERRalpha target gene downregulation is a signature of the failing human heart. J. Mol. Cell. Cardiol. 2009, 46(2):201-212.