Aging negatively affects estrogens-mediated effects on nitric oxide bioavailability by shifting ERα/ERβ balance in female mice

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Novensà, Laura ^a,b   Novella, Susana ^c,d   Medina, Pascual ^c,d   Segarra, Gloria ^c,d   Castillo, Nadia ^a,b   Heras, Magda ^a,b   Hermenegildo, Carlos ^c,d   Dantas, Ana Paula ^a,b  

^a INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^b HOSPITAL CLÍNIC   (Spain)

^c UNIVERSITY OF VALENCIA   (Spain)

^d HOSPITAL CLÍNICO UNIVERSITARIO   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; NITRATE; NITRIC OXIDE; NITRITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; ESTROGEN RECEPTOR;

AGING; ANIMAL EXPERIMENT; ARTICLE; CATABOLISM; CONTROLLED STUDY; DNA METHYLATION; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; UPREGULATION; ANIMAL; DRUG EFFECT; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

MUS;

AGING; ANIMALS; BLOTTING, WESTERN; DNA METHYLATION; ESTROGENS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; MICE; NADPH OXIDASE; NITRIC OXIDE; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, ESTROGEN;

EID: 80053059329     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0025335     Document Type: Article

References (41)

1. Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, et al. (2002) Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results From the Women's Health Initiative randomized controlled trial. JAMA 288: 321-333.
2. Hulley S, Grady D, Bush T, Furberg C, Herrington D, et al. (1998) Randomized trial of estrogen plus progestin for secondary prevention of coronary heart disease in postmenopausal women. Heart and Estrogen/progestin Replacement Study (HERS) Research Group. JAMA 280: 605-613.
3. Ferrari AU, Radaelli A, Centola M, (2003) Invited review: aging and the cardiovascular system. J Applied Physiol 95: 2591-2597.
4. Lakatta EG, (2003) Arterial and cardiac aging: major shareholders in cardiovascular disease enterprises: Part III: cellular and molecular clues to heart and arterial aging. Circulation 107: 490-497.
5. Lakatta EG, Levy D, (2003) Arterial and cardiac aging: major shareholders in cardiovascular disease enterprises: Part I: aging arteries: a "set up" for vascular disease. Circulation 107: 139-146.
6. Rossouw JE, Prentice RL, Manson JE, Wu L, Barad D, et al. (2007) Postmenopausal hormone therapy and risk of cardiovascular disease by age and years since menopause. JAMA 297: 1465-1477.
7. Prentice RL, Manson JE, Langer RD, Anderson GL, Pettinger M, et al. (2009) Benefits and risks of postmenopausal hormone therapy when it is initiated soon after menopause. Am J Epidemiol 170: 12-23.
8. Grodstein F, Manson JE, Stampfer MJ, (2006) Hormone therapy and coronary heart disease: the role of time since menopause and age at hormone initiation. J Womens Health (Larchmt) 15: 35-44.
9. Harman SM, (2006) Estrogen replacement in menopausal women: recent and current prospective studies, the WHI and the KEEPS. Gend Med 3: 254-269.
10. Wynne FL, Payne JA, Cain AE, Reckelhoff JF, Khalil RA, (2004) Age-related reduction in estrogen receptor-mediated mechanisms of vascular relaxation in female spontaneously hypertensive rats. Hypertension 43: 405-412.
11. LeBlanc AJ, Reyes R, Kang LS, Dailey RA, Stallone JN, et al. (2009) Estrogen replacement restores flow-induced vasodilation in coronary arterioles of aged and ovariectomized rats. Am J Physiol Regul Integr Comp Physiol 297: R1713-1723.
12. Lekontseva O, Rueda-Clausen C, Morton J, Davidge S, (2010) Ovariectomy in aged versus young rats augments matrix metalloproteinase-mediated vasoconstriction in mesenteric arteries. Menopause 17: 516-523.
13. Manson JE, Allison MA, Rossouw JE, Carr JJ, Langer RD, et al. (2007) Estrogen therapy and coronary-artery calcification. N Engl J Med 356: 2591-2602.
14. Sherwood A, Bower JK, McFetridge-Durdle J, Blumenthal JA, Newby LK, et al. (2007) Age moderates the short-term effects of transdermal 17beta-estradiol on endothelium-dependent vascular function in postmenopausal women. Arterioscler Thromb Vasc Biol 27: 1782-1787.
15. Novella S, Dantas AP, Segarra G, Novensa L, Bueno C, et al. (2010) Gathering of aging and estrogen withdrawal in vascular dysfunction of senescent accelerated mice. Exp Gerontol 45: 868-874.
16. Onetti Y J-AF, Vila E, Dantas AP, (2010) Aortic changes in senescence-accelerated female mice. Hypertension 56: 1172-1172.
17. Riazi S, Maric C, Ecelbarger CA, (2006) 17-beta Estradiol attenuates streptozotocin-induced diabetes and regulates the expression of renal sodium transporters. Kidney Int 69: 471-480.
18. Chen Y, Gill PS, Welch WJ, (2005) Oxygen availability limits renal NADPH-dependent superoxide production. Am J Physiol- Renal Physiology 289: F749-753.
19. Novensa L, Selent J, Pastor M, Sandberg K, Heras M, et al. (2010) Equine estrogens impair nitric oxide production and endothelial nitric oxide synthase transcription in human endothelial cells compared with the natural 17{beta}-estradiol. Hypertension 56: 405-411.
20. Fujiwara H, Ito M, (2002) Nonisotopic cytosine extension assay: a highly sensitive method to evaluate CpG island methylation in the whole genome. Anal Biochem 307: 386-389.
21. Oakes CC, La Salle S, Robaire B, Trasler JM, (2006) Evaluation of a quantitative DNA methylation analysis technique using methylation-sensitive/dependent restriction enzymes and real-time PCR. Epigenetics 1: 146-152.
22. Harrison DG, (1997) Endothelial function and oxidant stress. Clin Cardiol 20: II-11-17.
23. Jaenisch R, Bird A, (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33 Suppl pp. 245-254.
24. Fortepiani LA, Zhang H, Racusen L, Roberts LJ II, Reckelhoff JF, (2003) Characterization of an Animal Model of Postmenopausal Hypertension in Spontaneously Hypertensive Rats. Hypertension 41: 640-645.
25. Wynne FL, Payne JA, Cain AE, Reckelhoff JF, Khalil RA, (2004) Age-Related Reduction in Estrogen Receptor-Mediated Mechanisms of Vascular Relaxation in Female Spontaneously Hypertensive Rats. Hypertension 43: 405-412.
26. Moien-Afshari F, Kenyon E, Choy JC, Battistini B, McManus BM, et al. (2003) Long-term effects of ovariectomy and estrogen replacement treatment on endothelial function in mature rats. Maturitas 45: 213-223.
27. Virdis A, Ghiadoni L, Pinto S, Lombardo M, Petraglia F, et al. (2000) Mechanisms responsible for endothelial dysfunction associated with acute estrogen deprivation in normotensive women. Circulation 101: 2258-2263.
28. Miller VM, Duckles SP, (2008) Vascular actions of estrogens: functional implications. Pharmacol Rev 60: 210-241.
29. Yuan M, Wen-Xia Z, Cheng JP, Zhang YX, (2005) Related changes in the oestrous cycle and reproductive hormones in senescence-accelerated mouse. Reprod Fert Dev 17: 507-512.
30. Seals DR, Jablonski KL, Donato AJ, (2011) Aging and vascular endothelial function in humans. Clin Sci (Lond) 120: 357-375.
31. Meyer MR, Barton M, (2009) ERalpha, ERbeta, and gpER: novel aspects of oestrogen receptor signalling in atherosclerosis. Cardiovasc Res 83: 605-610.
32. Sumi D, Ignarro LJ, (2003) Estrogen-related receptor alpha 1 up-regulates endothelial nitric oxide synthase expression. Proc Nat Acad Sci U S A 100: 14451-14456.
33. Zhang QG, Raz L, Wang R, Han D, De Sevilla L, et al. (2009) Estrogen attenuates ischemic oxidative damage via an estrogen receptor alpha-mediated inhibition of NADPH oxidase activation. J Neurosci 29: 13823-13836.
34. Stirone C, Duckles SP, Krause DN, Procaccio V, (2005) Estrogen increases mitochondrial efficiency and reduces oxidative stress in cerebral blood vessels. Mol Pharmacol 68: 959-965.
35. Rubanyi GM, Freay AD, Kauser K, Sukovich D, Burton G, et al. (1997) Vascular estrogen receptors and endothelium-derived nitric oxide production in the mouse aorta. Gender difference and effect of estrogen receptor gene disruption. J Clin Invest 99: 2429-2437.
36. Darblade B, Pendaries C, Krust A, Dupont S, Fouque MJ, et al. (2002) Estradiol alters nitric oxide production in the mouse aorta through the alpha-, but not beta-, estrogen receptor. Circ Res 90: 413-419.
37. Miro AM, Sastre-Serra J, Pons DG, Valle A, Roca P, et al. (2011) 17beta-Estradiol regulates oxidative stress in prostate cancer cell lines according to ERalpha/ERbeta ratio. J Steroid Biochem Mol Biol 123: 133-139.
38. Matthews J, Gustafsson JA, (2003) Estrogen signaling: a subtle balance between ER alpha and ER beta. Mol Interv 3: 281-292.
39. Bhavnani BR, Tam SP, Lu X, (2008) Structure Activity Relationships and Differential Interactions and Functional Activity of Various Equine Estrogens Mediated via Estrogen Receptors (ERs) ER{alpha} and ER{beta}. Endocrinology 149: 4857-4870.
40. Issa JP, (2000) CpG-island methylation in aging and cancer. Curr Top Microbiol Immunol 249: 101-118.
41. Post WS, Goldschmidt-Clermont PJ, Wilhide CC, Heldman AW, Sussman MS, et al. (1999) Methylation of the estrogen receptor gene is associated with aging and atherosclerosis in the cardiovascular system. Cardiovasc Res 43: 985-991.