Genomic and non-genomic regulation of PGC1 isoforms by estrogen to increase cerebral vascular mitochondrial biogenesis and reactive oxygen species protection

European Journal of Pharmacology

Volumn 723, Issue 1, 2014, Pages 322-329

  Kemper, Martin F ^a   Stirone, Chris ^a   Krause, Diana N ^a   Duckles, Sue P ^a   Procaccio, Vincent ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cerebral blood vessels; Estrogen; Glutamate cysteine ligase; Glutathione; Mitochondria; Peroxisome proliferator activated receptor gamma coactivator 1 (PGC 1)

Indexed keywords

CEREBRAL BLOOD VESSELS; ESTROGEN; GLUTAMATE-CYSTEINE LIGASE; GLUTATHIONE; MITOCHONDRIA; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR-GAMMA COACTIVATOR-1 (PGC-1);

ADENOSINE TRIPHOSPHATE; ANIMALS; BRAIN; ESTRADIOL; ESTROGENS; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENOMICS; GLUTAMATE-CYSTEINE LIGASE; GLUTATHIONE; MITOCHONDRIA; NERVE TISSUE PROTEINS; NF-E2-RELATED FACTOR 1; OVARIECTOMY; PROTEIN ISOFORMS; RATS; RATS, INBRED F344; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; TRANSCRIPTION FACTORS;

EID: 84893817128     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2013.11.009     Document Type: Article

References (44)

1. A. Arduini, G. Serviddio, J. Escobar, A.M. Tormos, F. Bellanti, J. Vina, M. Monsalve, and J. Sastre Mitochondrial biogenesis fails in secondary biliary cirrhosis in rats leading to mitochondrial DNA depletion and deletions Am. J. Physiol. Gastrointest. Liver Physiol. 301 2011 G119 G127
2. G. Benard, B. Faustin, E. Passerieux, A. Galinier, C. Rocher, N. Bellance, J.P. Delage, L. Casteilla, T. Letellier, and R. Rossignol Physiological diversity of mitochondrial oxidative phosphorylation Am. J. Physiol. Cell Physiol. 291 2006 C1172 C1182
3. C.L. Bethea, and A.P. Reddy Ovarian steroids increase glutamatergic related gene expression in serotonin neurons of macaques Mol. Cell. Neurosci. 49 2012 251 262
4. S.A. Cook, T. Matsui, L. Li, and A. Rosenzweig Transcriptional effects of chronic Akt activation in the heart J. Biol. Chem. 277 2002 22528 22533 (Pubitemid 34967227)
5. H. Daitoku, K. Yamagata, H. Matsuzaki, M. Hatta, and A. Fukamizu Regulation of PGC-1 promoter activity by protein kinase B and the forkhead transcription factor FKHR Diabetes 52 2003 642 649 (Pubitemid 36323569)
6. S.M. Davidson, and M.R. Duchen Endothelial mitochondria: contributing to vascular function and disease Circ. Res. 100 2007 1128 1141 (Pubitemid 46684126)
7. S.P. Duckles, D.N. Krause, C. Stirone, and V. Procaccio Estrogen and mitochondria: a new paradigm for vascular protection? Mol. Interv. 6 2006 26 35 (Pubitemid 43327520)
8. G.G. Geary, D.N. Krause, and S.P. Duckles Estrogen reduces myogenic tone through a nitric oxide-dependent mechanism in rat cerebral arteries Am. J. Physiol. 275 1998 H292 H300
9. C. Handschin, and B.M. Spiegelman Peroxisome proliferator-activated receptor gamma coactivator 1 coactivators, energy homeostasis, and metabolism Endocr. Rev. 27 2006 728 735 (Pubitemid 44936056)
10. T. Hong, J. Ning, X. Yang, H.Y. Liu, J. Han, Z. Liu, and W. Cao Fine-tuned regulation of the PGC-1alpha gene transcription by different intracellular signaling pathways Am. J. Physiol. Endocrinol. Metab. 300 2011 E500 E507
11. D. Kang, S.H. Kim, and N. Hamasaki Mitochondrial transcription factor A (TFAM): roles in maintenance of mtDNA and cellular functions Mitochondrion 7 2007 39 44 (Pubitemid 46351974)
12. D.P. Kelly, and R.C. Scarpulla Transcriptional regulatory circuits controlling mitochondrial biogenesis and function Genes Dev. 18 2004 357 368 (Pubitemid 38316342)
13. M.F. Kemper, Y.Z. Zhao, S.P. Duckles, and D.N. Krause Endogenous ovarian hormones affect mitochondrial efficiency in cerebral endothelium via distinct regulation of PGC-1 isoforms J. Cereb. Blood Flow Metab. 33 2013 122 128
14. D. Kressler, M.B. Hock, and A. Kralli Coactivators PGC-1beta and SRC-1 interact functionally to promote the agonist activity of the selective estrogen receptor modulator tamoxifen J. Biol. Chem. 282 2007 26897 26907 (Pubitemid 47501898)
15. D. Kressler, S.N. Schreiber, D. Knutti, and A. Kralli The PGC-1-related protein PERC is a selective coactivator of estrogen receptor alpha J. Biol. Chem. 277 2002 13918 13925 (Pubitemid 34967998)
16. S.R. Lee, S.H. Kim, H.W. Lee, Y.H. Kim, H.D. Chae, C.H. Kim, and B.M. Kang Increased expression of glutathione by estradiol, tumor necrosis factor-alpha, and interleukin 1-beta in endometrial stromal cells Am. J. Reprod. Immunol. 62 2009 352 356
17. H. Liang, and W.F. Ward PGC-1alpha: a key regulator of energy metabolism Adv. Physiol. Educ. 30 2006 145 151 (Pubitemid 44749372)
18. J. Lin, C. Handschin, and B.M. Spiegelman Metabolic control through the PGC-1 family of transcription coactivators Cell. Metab. 1 2005 361 370 (Pubitemid 43960626)
19. J. Lin, P.T. Tarr, R. Yang, J. Rhee, P. Puigserver, C.B. Newgard, and B.M. Spiegelman PGC-1beta in the regulation of hepatic glucose and energy metabolism J. Biol. Chem. 278 2003 30843 30848 (Pubitemid 36994593)
20. V.A. Lira, D.L. Brown, A.K. Lira, A.N. Kavazis, Q.A. Soltow, E.H. Zeanah, and D.S. Criswell Nitric oxide and AMPK cooperatively regulate PGC-1 in skeletal muscle cells J. Physiol. 588 2010 3551 3566
21. K.J. Livak, and T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method Methods 25 2001 402 408 (Pubitemid 34164012)
22. S.C. Lu Regulation of glutathione synthesis Mol. Asp. Med. 30 2009 42 59
23. N.R. Madamanchi, Z.S. Hakim, and M.S. Runge Oxidative stress in atherogenesis and arterial thrombosis: the disconnect between cellular studies and clinical outcomes J. Thromb. Haemost. 3 2005 254 267 (Pubitemid 41623612)
24. K.A. Mattingly, M.M. Ivanova, K.A. Riggs, N.S. Wickramasinghe, M.J. Barch, and C.M. Klinge Estradiol stimulates transcription of nuclear respiratory factor-1 and increases mitochondrial biogenesis Mol. Endocrinol. 22 2008 609 622 (Pubitemid 351397789)
25. A.M. McNeill, C. Zhang, F.Z. Stanczyk, S.P. Duckles, and D.N. Krause Estrogen increases endothelial nitric oxide synthase via estrogen receptors in rat cerebral blood vessels: effect preserved after concurrent treatment with medroxyprogesterone acetate or progesterone Stroke 33 2002 1685 1691 (Pubitemid 34619979)
26. D.M. Medeiros Assessing mitochondria biogenesis Methods 46 2008 288 294
27. M.M. Montano, H. Deng, M. Liu, X. Sun, and R. Singal Transcriptional regulation by the estrogen receptor of antioxidative stress enzymes and its functional implications Oncogene 23 2004 2442 2453 (Pubitemid 38520742)
28. P.I. Moreira, J.B. Custodio, E. Nunes, P.J. Oliveira, A. Moreno, R. Seica, C.R. Oliveira, and M.S. Santos Mitochondria from distinct tissues are differently affected by 17beta-estradiol and tamoxifen J. Steroid Biochem. Mol. Biol. 123 2011 8 16
29. E. Nisoli, E. Clementi, S. Moncada, and M.O. Carruba Mitochondrial biogenesis as a cellular signaling framework Biochem. Pharmacol. 67 2004 1 15 (Pubitemid 37518530)
30. E. Nisoli, E. Clementi, C. Paolucci, V. Cozzi, C. Tonello, C. Sciorati, R. Bracale, A. Valerio, M. Francolini, S. Moncada, and M.O. Carruba Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide Science 299 2003 896 899 (Pubitemid 36182449)
31. J.A. Ospina, H.N. Brevig, D.N. Krause, and S.P. Duckles Estrogen suppresses IL-1beta-mediated induction of COX-2 pathway in rat cerebral blood vessels Am. J. Physiol. Heart Circ. Physiol. 286 2004 H2010 H2019
32. A. Ramachandran, A.L. Levonen, P.S. Brookes, E. Ceaser, S. Shiva, M.C. Barone, and V. Darley-Usmar Mitochondria, nitric oxide, and cardiovascular dysfunction Free Radic. Biol. Med. 33 2002 1465 1474 (Pubitemid 35351589)
33. A. Razmara, L. Sunday, C. Stirone, X.B. Wang, D.N. Krause, S.P. Duckles, and V. Procaccio Mitochondrial effects of estrogen are mediated by estrogen receptor alpha in brain endothelial cells J. Pharmacol. Exp. Ther. 325 2008 782 790 (Pubitemid 351724313)
34. R.C. Scarpulla Nuclear control of respiratory chain expression by nuclear respiratory factors and PGC-1-related coactivator Ann. N. Y. Acad. Sci. 1147 2008 321 334
35. R.C. Scarpulla Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network Biochim. Biophys. Acta 1813 2011 1269 1278
36. J. Sonoda, I.R. Mehl, L.W. Chong, R.R. Nofsinger, and R.M. Evans PGC-1beta controls mitochondrial metabolism to modulate circadian activity, adaptive thermogenesis, and hepatic steatosis Proc. Natl. Acad. Sci. USA 104 2007 5223 5228 (Pubitemid 47186203)
37. J. St-Pierre, J. Lin, S. Krauss, P.T. Tarr, R. Yang, C.B. Newgard, and B.M. Spiegelman Bioenergetic analysis of peroxisome proliferator-activated receptor gamma coactivators 1alpha and 1beta (PGC-1alpha and PGC-1beta) in muscle cells J. Biol. Chem. 278 2003 26597 26603 (Pubitemid 36876804)
38. C. Stirone, A. Boroujerdi, S.P. Duckles, and D.N. Krause Estrogen receptor activation of phosphoinositide-3 kinase, akt, and nitric oxide signaling in cerebral blood vessels: rapid and long-term effects Mol. Pharmacol. 67 2005 105 113 (Pubitemid 40069970)
39. C. Stirone, Y. Chu, L. Sunday, S.P. Duckles, and D.N. Krause 17 Beta-estradiol increases endothelial nitric oxide synthase mRNA copy number in cerebral blood vessels: quantification by real-time polymerase chain reaction Eur. J. Pharmacol. 478 2003 35 38 (Pubitemid 38366072)
40. C. Stirone, S.P. Duckles, D.N. Krause, and V. Procaccio Estrogen increases mitochondrial efficiency and reduces oxidative stress in cerebral blood vessels Mol. Pharmacol. 68 2005 959 965 (Pubitemid 41345787)
41. S.A. Thompson, C.C. White, C.M. Krejsa, D. Diaz, J.S. Woods, D.L. Eaton, and T.J. Kavanagh Induction of glutamate-cysteine ligase (gamma-glutamylcysteine synthetase) in the brains of adult female mice subchronically exposed to methylmercury Toxicol. Lett. 110 1999 1 9 (Pubitemid 29502421)
42. M. Tsai-Turton, and U. Luderer Gonadotropin regulation of glutamate cysteine ligase catalytic and modifier subunit expression in rat ovary is subunit and follicle stage specific Am. J. Physiol. Endocrinol. Metab. 289 2005 E391 E402
43. C.C. White, H. Viernes, C.M. Krejsa, D. Botta, and T.J. Kavanagh Fluorescence-based microtiter plate assay for glutamate-cysteine ligase activity Anal. Biochem. 318 2003 175 180 (Pubitemid 36694107)
44. E. Yu, J. Mercer, and M. Bennett Mitochondria in vascular disease Cardiovasc. Res. 95 2012 173 182