Sex-specific divergence of antioxidant pathways in fetal brain, liver, and skeletal muscles

Free Radical Research

Volumn 50, Issue 3, 2016, Pages 366-373

  Al Gubory, Kaïs H ^a   Garrel, Catherine ^b  

^a INRA Institut National de la Recherche Agronomique   (France)

^b GRENOBLE UNIVERSITY HOSPITAL   (France)

Author keywords

Antioxidant pathways; fetal organs; opposite sex twin; pregnancy; sex dimorphism

Indexed keywords

CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; GLUTATHIONE; GLUTATHIONE DISULFIDE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; MALONALDEHYDE; MANGANESE SUPEROXIDE DISMUTASE; OXIDOREDUCTASE; ANTIOXIDANT; SUPEROXIDE DISMUTASE;

ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; ENZYME ACTIVITY; FEMALE; FETAL BRAIN; FETUS; FETUS DEVELOPMENT; KIDNEY PARENCHYMA; LIPID PEROXIDATION; LIVER; LUNG PARENCHYMA; MALE; NONHUMAN; ORGANOGENESIS; OXIDATIVE STRESS; SEX DIFFERENCE; SHEEP; SKELETAL MUSCLE; TWIN PREGNANCY; ANIMAL; ANTIBODY SPECIFICITY; BRAIN; EMBRYOLOGY; GENE EXPRESSION; GENETICS; METABOLISM;

ANIMALS; ANTIOXIDANTS; BRAIN; CATALASE; FEMALE; GENE EXPRESSION; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; LIPID PEROXIDATION; LIVER; MALE; MUSCLE, SKELETAL; ORGAN SPECIFICITY; OXIDATIVE STRESS; SEX FACTORS; SHEEP; SUPEROXIDE DISMUTASE;

EID: 84955675224     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.3109/10715762.2015.1130224     Document Type: Article

References (38)

1. Clayton JA, Joseph S. Why research sex differences and similarities? Med Phys 2013;40:040403. doi: 10.1118/1.4789532.
2. Clayton JA, Collins FS. Policy: NIH to balance sex in cell and animal studies. Nature 2014;509:282-283.
3. Luo ZC, Fraser WD, Julien P, Deal CL, Audibert F, Smith GN, et al. Tracing the origins of "fetal origins" of adult diseases: programming by oxidative stress? Med Hypotheses 2006;66:38-44.
4. Jakovljevic B, Novakov-Mikic A, Brkic S, Bogavac MA, Tomic S, Miler V. Lipid peroxidation in the first trimester of pregnancy. J Matern Fetal Neonatal Med 2012;25:1316-1318.
5. Agarwal A, Allamaneni SSR. Role of free radicals in female reproductive diseases and assisted reproduction. Reprod Biomed Online 2004;9:338-437.
6. Csapo AI, Pulkkinen MO, Wiest WG. Effects of luteectomy and progesterone replacement therapy in early pregnant patients. Am J Obstet Gynecol 1973;115:759-765.
7. Al-Gubory KH, Solari A, Mirman B. Effects of luteectomy on the maintenance of pregnancy, circulating progesterone concentrations and lambing performance in sheep. Reprod Fertil Dev 1999;11:317-322.
8. Roselli CE, Resko JA, Stormshak F. Expression of steroid hormone receptors in the fetal sheep brain during the critical period for sexual differentiation. Brain Res 2006;1110:76-80.
9. Lowry OH, Rosebrough NJ, Farr AL, Randall RF. Protein measurement with folin phenol reagent. J Biol Chem 1951;193:265-275.
10. Marklund S, Marklund G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 1974;47:469-474.
11. Al-Gubory KH, Ceballos-Picot I, Nicole A, Bolifraud P, Germain G, Michaud M, et al. Changes in activities of superoxide dismutase, nitric oxide synthase, glutathionedependent enzymes and the incidence of apoptosis in sheep corpus luteum during the estrous cycle. Biochim Biophys Acta 2005;1725:348-357.
12. Garrel C, Ceballos-Picot I, Germain G, Al-Gubory KH. Oxidative stress-inducible antioxidant adaptive response during prostaglandin F2alpha-induced luteal cell death in vivo. Free Radic Res 2007;41:251-259.
13. Garrel C, Fowler PA, Al-Gubory KH. Developmental changes in antioxidant enzymatic defences against oxidative stress in sheep placentomes. J Endocrinol 2010;205:107-116.
14. Al-Gubory KH, Garrel C. Antioxidative signalling pathways regulate the level of reactive oxygen species at the endometrial-extraembryonic membranes interface during early pregnancy. Int J Biochem Cell Biol 2012;44:1511-1518.
15. Jin ZQ, Zhou HZ, Cecchini G, Gray MO, Karliner JS. MnSOD in mouse heart: acute responses to ischemic preconditioning and ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 2005;288:H2986-H2994.
16. Nzengue Y, Steiman R, Garrel C, Lefèbvre E, Guiraud P. Oxidative stress and DNA damage induced by cadmium in the human keratinocyte HaCaT cell line: role of glutathione in the resistance to cadmium. Toxicology 2008;243:193-206.
17. Akerboom TP, Sies H. Assay of glutathione, glutathione disulfide, and glutathione mixed disulfides in biological samples. Meth Enzymol 1981;77:373-382.
18. Londero D, Lo Greco P. Automated high-performance liquid chromatographic separation with spectrofluorometric detection of a malondialdehyde-thiobarbituric acid adduct in plasma. J Chromatogr A 1996;729:207-210.
19. Halliwell B, Chirico S. Lipid peroxidation: its mechanism, measurement, and significance. Am J Clin Nutr 1993;57:715S-724S.
20. Del RD, Stewart AJ, Pellegrini N. A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutr Metab Cardio Vasc Dis 2005;15:316-328.
21. Georgieff MK. Nutrition and the developing brain: nutrient priorities and measurement. Am J Clin Nutr 2007;85:614S-620S.
22. Tuzun F, Kumral A, Ozbal S, Dilek M, Tugyan K, Duman N, Ozkan H. Maternal prenatal omega-3 fatty acid supplementation attenuates hyperoxia-induced apoptosis in the developing rat brain. Int J Dev Neurosci 2012;30:315-323.
23. Ikonomidou C, Kaindl AM. Neuronal death and oxidative stress in the developing brain. Antioxid Redox Signal 2011;14:1535-1550.
24. Al-Gubory KH. Mitochondria: omega-3 in the route of mitochondrial reactive oxygen species. Int J Biochem Cell Biol 2012;4:1569-1573.
25. Delivoria-Papadopoulos M, Mishra OP. Mechanisms of perinatal cerebral injury in fetus and newborn. Ann NY Acad Sci 2000;900:159-168.
26. McCord I, Fridovich JM. Superoxide dismutase. An enzymatic function for erythrocuprein. J Biol Chem 1969;244:6049-6055.
27. Weisiger RA, Fridovich I. Mitochondrial superoxide dismutase. Site of synthesis and intramitochondrial localisation. J Biol Chem 1973;248:4791-4793.
28. Minotti G, Aust SD. Redox cycling of iron and lipid peroxidation. Lipids 1992;27:219-226.
29. Kehrer JP. The Haber-Weiss reaction and mechanisms of toxicity. Toxicology 2000;149:43-50.
30. Beckman JS, Koppenol WH. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol 1996;271:C1424-C1437.
31. Schafer FQ, Buettner GR. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 2001;30:1191-1212.
32. Bellingham M, Fiandanese N, Byers A, Cotinot C, Evans NP, Pocar P, et al. Effects of exposure to environmental chemicals during pregnancy on the development of the male and female reproductive axes. Reprod Domest Anim 2012;47:15-22.
33. Al-Gubory KH. Environmental pollutants and lifestyle factors induce oxidative stress and poor prenatal development. Reprod Biomed Online 2014;29:17-31.
34. Kabuto H, Amakawa M, Shishibori T. Exposure to bisphenol A during embryonic/fetal life and infancy increases oxidative injury and causes underdevelopment of the brain and testis in mice. Life Sci 2004;74:2931-2940.
35. Palanza P, Gioiosa L, vom Saal FS, Parmigiani S. Effects of developmental exposure to bisphenol A on brain and behavior in mice. Environ Res 2008;108:150-157.
36. Li Y, Wang H. In utero exposure to tobacco and alcohol modifies neurobehavioral development in mice offspring: consideration a role of oxidative stress. Pharmacol Res 2004;49:467-473.
37. Jedrychowski WA, Perera FP, Maugeri U, Mroz E, Klimaszewska-Rembiasz M, Flak E, et al. Effect of prenatal exposure to fine particulate matter on ventilatory lung function of preschool children of non-smoking mothers. Paediatr Perinat Epidemiol 2010;24:492-501.
38. Anblagan D, Jones NW, Costigan C, Parker AJ, Allcock K, Aleong R, et al. Maternal smoking during pregnancy and fetal organ growth: a magnetic resonance imaging study. PLoS One 2013;8:e67223.