Female headstart in resistance to hyperoxia-induced oxidative stress in mice
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Increased oxygen concentration (hyperoxia) induces oxidative damage of tissues and organs. Oxygen toxicity in hyperoxia is controlled by factors such as sex, age, tissue, strain and hormones. In most species females show lower incidence of some age-related pathologies linked with oxidative stress, which has been attributed to a beneficial effect of ovarian hormones. In this study we found that hyperoxia induced hepatic oxidative damage exclusively in male CBA/H mice, followed by their decreased survival. Histopathological examination revealed that the observed differences in survival were not the consequence of acute lung injury induced by hyperoxia. Next, we observed that an increased Sirt1 protein level in hyperoxia-exposed female CBA/H mice correlated with their lower PPAR-γ and higher eNOS and Sod2 protein levels. In males, higher PPAR-γ and lower Sod2 protein levels were associated with unchanged Sirt1 expression. Although these results are of a correlative nature only, they clearly show that females show better survival, increased resistance to hyperoxia and have generally more efficient defense systems, which suggests that their headstart in resistance to hyperoxia could be a consequence of the beneficial effect of ovarian hormones.
- Alhazza I, Haffor ASA (2005) Effects of hyperoxia and aging on cholesterol levels in pigeon. JABS 1: 55-59.
- Almeida M, Ambrogini E, Han L, Manolagas SC, Jilka RL (2009) Increased lipid oxidation causes oxidative stress increased peroxisome proliferator-activated receptor-gamma expression and diminished pro-osteogenic Wnt signaling in the skeleton. J Biol Chem 284: 27438-27448.
- Boelsterli UA, Bedoucha M (2002) Toxicological consequences of altered peroxisome proliferator-activated receptor gamma (PPARgamma) expression in the liver: insights from models of obesity and type 2 diabetes. Biochem Pharmacol 63: 1-10 doi: 101016/S0006-2952(01)00817-6.
- Bordone L, Cohen D, Robinson A, Motta MC, van Veen E, Czopik A, Guarente L (2007) SIRT1 transgenic mice show phenotypes resembling calorie restriction. Aging Cell 6: 759-767.
- Chen YR, Lai YL, Lin SD, Li XT, Fu YC, Xu WC (2013) SIRT1 interacts with metabolic transcriptional factors in the pancreas of insulin-resistant and calorie-restricted rats. Mol Biol Rep 40: 3373-3380.
- Cheng HL, Mostoslavsky R, Saito S, Manis JP, Gu Y, Patel P, Chua KF (2003) Developmental defects and p53 hyperacetylation in Sir2 homolog (SIRT1)-deficient mice. Proc Natl Acad Sci USA 100: 10794-10799.
- Choudhary D, Jansson I, Schenkman JB, Sarfarazi M, Stoilov I (2003) Comparative expression profiling of 40 mouse cytochrome P450 genes in embryonic and adult tissues. Arch Biochem Biophys 414: 91-100 doi: 101016/S0003-9861(03)00174-7.
- Cross HR (2000) Trimetazidine: a novel protective role via maintenance of Na(+)/K(+)-ATPase activity? Cardiovasc Res 47: 637-639.
- Fagan JM, Sleczka BG, Sohar I (1999) Quantitation of oxidative damage to tissue proteins. Int J Biochem Cell Biol 31: 751-757.
- Festing MFW (1996) Are animal experiments in toxicological research the 'right' size? In: Statistics in Toxicology, Morgan BJT ed, pp 3-11. Oxford: Clarendon Press.
- Guarente L (2013) Calorie restriction and sirtuins revisited. Genes Dev 27: 2072-2085.
- Hayashi T, Matsui-Hirai H, Miyazaki-Akita A, Fukatsu A, Funami J, Ding QF, Iguchi A (2006) Endothelial cellular senescence is inhibited by nitric oxide: implications in atherosclerosis associated with menopause and diabetes. Proc Natl Acad Sci USA 103: 17018-17023.
- Kleinert H, Wallerath T, Euchenhofer C, Ihrig-Biedert I, Li H, Forstermann U (1998) Estrogens increase transcription of the human endothelial NO synthase gene: analysis of the transcription factors involved. Hypertension 31: 582-588.
- Kondrikov D, Fonseca FV, Elms S, Fulton D, Black SM, Block ER, Su Y (2010) Beta-actin association with endothelial nitric-oxide synthase modulates nitric oxide and superoxide generation from the enzyme. J Biol Chem 285: 4319-4327.
- Landis G N, Abdueva D, Skvortsov D, Yang J, Rabin BE, Carrick J, Tower J (2004) Similar gene expression patterns characterize aging and oxidative stress in Drosophila melanogaster. Proc Natl Acad Sci USA 101: 7663-7668.
- Lagranha CJ, Deschamps A, Aponte A, Steenbergen C, Murphy E (2010) Sex differences in the phosphorylation of mitochondrial proteins result in reduced production of reactive oxygen species and cardioprotection in females. Circ Res 106: 1681-1691.
- Lingappan K, Jiang W, Wang L, Couroucli XI, Barrios R, Moorthy B (2013) Sex-specific differences in hyperoxic lung injury in mice: implications for acute and chronic lung disease in humans. Toxicol Appl Pharmacol 272: 281-290.
- Mansure JJ, Nassim R, Kassouf W (2009) Peroxisome proliferator-activated receptor gamma in bladder cancer: a promising therapeutic target. Cancer Biol Ther 8: 6-15.
- Matute-Bello G, Downey G, Moore BB, Groshong SD, Matthay MA, Slutsky AS, Kuebler WM (2011) An official American Thoracic Society workshop report: features and measurements of experimental acute lung injury in animals. Am J Respir Cell Mol Biol 44: 725-738.
- Mikkola TS, Gissler M, Merikukka M, Tuomikoski P, Ylikorkala O (2013) Sex differences in age-related cardiovascular mortality. PLoS One 8: e63347.
- Moore RL, Faller DV (2013) SIRT1 represses estrogen-signaling, ligand-independent ERalpha-mediated transcription and cell proliferation in estrogen-responsive breast cells. J Endocrinol 216: 273-285.
- Muriel P (2009) Role of free radicals in liver diseases. Hepatol Int 3: 526-536.
- Nisoli E, Tonello C, Cardile A, Cozzi V, Bracale R, Tedesco L, Carruba MO (2005) Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 310: 314-317.
- Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95: 351-358.
- Pettinelli P, Videla LA (2011) Up-regulation of PPAR-gamma mRNA expression in the liver of obese patients: an additional reinforcing lipogenic mechanism to SREBP-1c induction. J Clin Endocrinol Metab 96: 1424-1430.
- Picard F, Kurtev M, Chung N, Topark-Ngarm A, Senawong T, Machado De Oliveira R, Guarente L (2004) Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma. Nature 429: 771-776.
- Rangwala SM, Lazar MA (2004) Peroxisome proliferator-activated receptor gamma in diabetes and metabolism. Trends Pharmacol Sci 25: 331-336.
- Reznick AZ, Packer L (1994) Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods Enzymol 233: 357-363.
- Sanz A, Gomez J, Caro P, Barja G (2006) Carbohydrate restriction does not change mitochondrial free radical generation and oxidative DNA damage. J Bioenerg Biomembr 38: 327-333.
- Singh NP, McCoy MT, Tice RR, Schneider EL (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 175: 184-191.
- Sobočanec S, Balog T, Šarić A, Šverko V, Žarković N, Gašparović A C, Marotti T (2010) Cyp4a14 overexpression induced by hyperoxia in female CBA mice as a possible contributor of increased resistance to oxidative stress. Free Radic Res 44: 181-190.
- Storer JB (1966) Longevity and gross pathology at death in 22 inbred mouse strains. J Gerontol 21: 404-409.
- Sumeray MS, Rees DD, Yellon DM (2000) Infarct size and nitric oxide synthase in murine myocardium. J Mol Cell Cardiol 32: 35-42.
- Šverko V, Sobočanec S, Balog T, Marotti T (2004) Age and gender differences in antioxidant enzyme activity: potential relationship to liver carcinogenesis in male mice. Biogerontology 5: 235-242.
- Tanno M, Kuno A, Yano T, Miura T, Hisahara S, Ishikawa S, Horio Y (2010) Induction of manganese superoxide dismutase by nuclear translocation and activation of SIRT1 promotes cell survival in chronic heart failure. J Biol Chem 285: 8375-8382.
- Tibbles PM, Edelsberg JS (1996) Hyperbaric-oxygen therapy. N Engl J Med 334: 1642-1648 doi: 101056/nejm199606203342506.
- Tice RR, Agurell E, Anderson D, Burlinson B, Hartmann A, Kobayashi H, Sasaki YF (2000) Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ Mol Mutagen 35: 206-221.
- Vina J, Borras C, Gambini J, Sastre J, Pallardo FV (2005) Why females live longer than males? Importance of the upregulation of longevity-associated genes by oestrogenic compounds. FEBS Lett 579: 2541-2545.
- Wang RH, Kim HS, Xiao C, Xu X, Gavrilova O, Deng CX (2011) Hepatic Sirt1 deficiency in mice impairs mTorc2/Akt signaling and results in hyperglycemia oxidative damage and insulin resistance. J Clin Invest 121: 4477-4490.
- Weaver LK, Hopkins RO, Chan KJ, Churchill S, Elliott CG, Clemmer TP, Morris AH (2002) Hyperbaric oxygen for acute carbon monoxide poisoning. N Engl J Med 347: 1057-1067.
- Yamamoto H, Schoonjans K, Auwerx J (2007) Sirtuin functions in health and disease. Mol Endocrinol 21: 1745-1755.
- Yao H, Chung S, Hwang JW, Rajendrasozhan S, Sundar IK, Dean DA, Rahman I (2012) SIRT1 protects against emphysema via FOXO3-mediated reduction of premature senescence in mice. J Clin Invest 122: 2032-2045.
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