Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2016, Article ID 3837623, 13 pages
http://dx.doi.org/10.1155/2016/3837623
Research Article

Regular and Moderate Exercise Counteracts the Decline of Antioxidant Protection but Not Methylglyoxal-Dependent Glycative Burden in the Ovary of Reproductively Aging Mice

1Department of Life, Health and Environmental Sciences, University of L’Aquila, L’Aquila, Italy
2Department of Microbiology and Immunology, Albert Einstein College of Medicine, Bronx, NY, USA
3Department of Biomedical Sciences, “G. d’Annunzio” University, Via dei Vestini, Chieti Scalo, Italy
4Institute of Translational Pharmacology (IFT), National Research Council (CNR), L’Aquila, Italy

Received 9 October 2016; Revised 17 November 2016; Accepted 7 December 2016

Academic Editor: Mauricio Krause

Copyright © 2016 S. Falone et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. E. R. Te Velde and P. L. Pearson, “The variability of female reproductive ageing,” Human Reproduction Update, vol. 8, no. 2, pp. 141–154, 2002. View at Publisher · View at Google Scholar · View at Scopus
  2. C. Tatone, F. Amicarelli, M. C. Carbone et al., “Cellular and molecular aspects of ovarian follicle ageing,” Human Reproduction Update, vol. 14, no. 2, pp. 131–142, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. S. M. Briley, S. Jasti, J. M. McCracken et al., “Reproductive age-associated fibrosis in the stroma of the mammalian ovary,” Reproduction, vol. 152, no. 3, pp. 245–260, 2016. View at Publisher · View at Google Scholar
  4. S. M. Nelson, E. E. Telfer, and R. A. Anderson, “The ageing ovary and uterus: new biological insights,” Human Reproduction Update, vol. 19, no. 1, pp. 67–83, 2013. View at Publisher · View at Google Scholar · View at Scopus
  5. K. M. Desai, T. Chang, H. Wang et al., “Oxidative stress and aging: is methylglyoxal the hidden enemy?” Canadian Journal of Physiology and Pharmacology, vol. 88, no. 3, pp. 273–284, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. N. Rabbani and P. J. Thornalley, “Dicarbonyl stress in cell and tissue dysfunction contributing to ageing and disease,” Biochemical and Biophysical Research Communications, vol. 458, no. 2, pp. 221–226, 2015. View at Publisher · View at Google Scholar · View at Scopus
  7. M. C. Carbone, C. Tatone, S. Delle Monache et al., “Antioxidant enzymatic defences in human follicular fluid: characterization and age-dependent changes,” Molecular Human Reproduction, vol. 9, no. 11, pp. 639–643, 2003. View at Publisher · View at Google Scholar · View at Scopus
  8. C. Tatone, M. C. Carbone, S. Falone et al., “Age-dependent changes in the expression of superoxide dismutases and catalase are associated with ultrastructural modifications in human granulosa cells,” Molecular Human Reproduction, vol. 12, no. 11, pp. 655–660, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. J. Lim and U. Luderer, “Oxidative damage increases and antioxidant gene expression decreases with aging in the mouse ovary,” Biology of Reproduction, vol. 84, no. 4, pp. 775–782, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. C. Tatone and F. Amicarelli, “The aging ovary—the poor granulosa cells,” Fertility and Sterility, vol. 99, no. 1, pp. 12–17, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. C. Tatone, U. Eichenlaub-Ritter, and F. Amicarelli, “Dicarbonyl stress and glyoxalases in ovarian function,” Biochemical Society Transactions, vol. 42, no. 2, pp. 433–438, 2014. View at Publisher · View at Google Scholar · View at Scopus
  12. J. Lim, B. N. Nakamura, I. Mohar, T. J. Kavanagh, and U. Luderer, “Glutamate cysteine ligase modifier subunit (Gclm) null mice have increased ovarian oxidative stress and accelerated age-related ovarian failure,” Endocrinology, vol. 156, no. 9, pp. 3329–3343, 2015. View at Publisher · View at Google Scholar · View at Scopus
  13. A. R. Hipkiss, “Energy metabolism, altered proteins, sirtuins and ageing: converging mechanisms?” Biogerontology, vol. 9, no. 1, pp. 49–55, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Pertynska-Marczewska, E. Diamanti-Kandarakis, J. Zhang, and Z. Merhi, “Advanced glycation end products: a link between metabolic and endothelial dysfunction in polycystic ovary syndrome?” Metabolism: Clinical and Experimental, vol. 64, no. 11, pp. 1564–1573, 2015. View at Publisher · View at Google Scholar · View at Scopus
  15. L. D. Homa, L. L. Burger, A. J. Cuttitta, D. E. Michele, and S. M. Moenter, “Voluntary exercise improves estrous cyclicity in prenatally androgenized female mice despite programming decreased voluntary exercise: implications for polycystic ovary syndrome (PCOS),” Endocrinology, vol. 156, no. 12, pp. 4618–4628, 2015. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Falone, A. D'Alessandro, A. Mirabilio et al., “Late-onset running biphasically improves redox balance, energy- and methylglyoxal-related status, as well as SIRT1 expression in mouse hippocampus,” PLOS ONE, vol. 7, no. 10, Article ID e48334, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Falone, A. D'Alessandro, A. Mirabilio et al., “Long term running biphasically improves methylglyoxal-related metabolism, redox homeostasis and neurotrophic support within adult mouse brain cortex,” PLoS ONE, vol. 7, no. 2, Article ID e31401, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. G. G. Long, “Apparent mesonephric duct (rete anlage) origin for cysts and proliferative epithelial lesions in the mouse ovary,” Toxicologic Pathology, vol. 30, no. 5, pp. 592–598, 2002. View at Publisher · View at Google Scholar · View at Scopus
  19. M. E. Kevenaar, M. F. Meerasahib, P. Kramer et al., “Serum anti-Müllerian hormone levels reflect the size of the primordial follicle pool in mice,” Endocrinology, vol. 147, no. 7, pp. 3228–3234, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. J. A. Merriman, P. C. Jennings, E. A. McLaughlin, and K. T. Jones, “Effect of aging on superovulation efficiency, aneuploidy rates, and sister chromatid cohesion in mice aged up to 15 months,” Biology of Reproduction, vol. 86, no. 2, article 49, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. D.-F. Du, X.-L. Li, F. Fang, and M.-R. Du, “Expression of anti-Müllerian hormone in letrozole rat model of polycystic ovary syndrome,” Gynecological Endocrinology, vol. 30, no. 12, pp. 885–889, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. W. L. Ledger, “Clinical utility of measurement of anti-müllerian hormone in reproductive endocrinology,” Journal of Clinical Endocrinology & Metabolism, vol. 95, no. 12, pp. 5144–5154, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Di Loreto, S. Falone, A. D'Alessandro et al., “Regular and moderate exercise initiated in middle age prevents age-related amyloidogenesis and preserves synaptic and neuroprotective signaling in mouse brain cortex,” Experimental Gerontology, vol. 57, pp. 57–65, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. P. Fernando, A. Bonen, and L. Hoffman-Goetz, “Predicting submaximal oxygen consumption during treadmill running in mice,” Canadian Journal of Physiology and Pharmacology, vol. 71, no. 10-11, pp. 854–857, 1993. View at Publisher · View at Google Scholar · View at Scopus
  25. M. Szczodry, J. Zhang, C. Lim et al., “Treadmill running exercise results in the presence of numerous myofibroblasts in mouse patellar tendons,” Journal of Orthopaedic Research, vol. 27, no. 10, pp. 1373–1378, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. A. A. de Almeida, S. Gomes da Silva, J. Fernandes et al., “Differential effects of exercise intensities in hippocampal BDNF, inflammatory cytokines and cell proliferation in rats during the postnatal brain development,” Neuroscience Letters, vol. 553, pp. 1–6, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. M. M. Bradford, “A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding,” Analytical Biochemistry, vol. 72, no. 1-2, pp. 248–254, 1976. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Sun and S. Zigman, “An improved spectrophotometric assay for superoxide dismutase based on epinephrine autoxidation,” Analytical Biochemistry, vol. 90, no. 1, pp. 81–89, 1978. View at Publisher · View at Google Scholar · View at Scopus
  29. H. Aebi, “[13] Catalase in vitro,” Methods in Enzymology, vol. 105, no. C, pp. 121–126, 1984. View at Publisher · View at Google Scholar · View at Scopus
  30. D. E. Paglia and W. N. Valentine, “Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase,” The Journal of Laboratory and Clinical Medicine, vol. 70, no. 1, pp. 158–169, 1967. View at Google Scholar · View at Scopus
  31. B. Mannervik, A. C. Aronsson, E. Marmstål, and G. Tibbelin, “Glyoxalase I (rat liver),” Methods in Enzymology, vol. 77, pp. 297–301, 1981. View at Publisher · View at Google Scholar
  32. M. K. Guha, D. L. Vander Jagt, and D. J. Creighton, “Diffusion-dependent rates for the hydrolysis reaction catalyzed by glyoxalase II from rat erythrocytes,” Biochemistry, vol. 27, no. 24, pp. 8818–8822, 1988. View at Publisher · View at Google Scholar · View at Scopus
  33. M. A. Baker, G. J. Cerniglia, and A. Zaman, “Microtiter plate assay for the measurement of glutathione and glutathione disulfide in large numbers of biological samples,” Analytical Biochemistry, vol. 190, no. 2, pp. 360–365, 1990. View at Publisher · View at Google Scholar · View at Scopus
  34. M. M. Jack, J. M. Ryals, and D. E. Wright, “Characterisation of glyoxalase I in a streptozocin-induced mouse model of diabetes with painful and insensate neuropathy,” Diabetologia, vol. 54, no. 8, pp. 2174–2182, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. K. J. Livak and T. D. Schmittgen, “Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method,” Methods, vol. 25, no. 4, pp. 402–408, 2001. View at Publisher · View at Google Scholar · View at Scopus
  36. U. K. Laemmli, “Cleavage of structural proteins during the assembly of the head of bacteriophage T4,” Nature, vol. 227, no. 5259, pp. 680–685, 1970. View at Publisher · View at Google Scholar · View at Scopus
  37. H. Towbin, T. Staehelin, and J. Gordon, “Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications,” Proceedings of the National Academy of Sciences of the United States of America, vol. 76, no. 9, pp. 4350–4354, 1979. View at Publisher · View at Google Scholar · View at Scopus
  38. R. L. Levine, J. A. Williams, E. R. Stadtman, and E. Shacter, “Carbonyl assays for determination of oxidatively modified proteins,” Methods in Enzymology, vol. 233, pp. 346–357, 1994. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Hellemans, G. Mortier, A. De Paepe, F. Speleman, and J. Vandesompele, “qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data,” Genome Biology, vol. 8, no. 2, p. R19, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Bonfigli, S. Colafarina, S. Falone, C. Di Giulio, C. Di Ilio, and F. Amicarelli, “High levels of antioxidant enzymatic defence assure good protection against hypoxic stress in spontaneously diabetic rats,” International Journal of Biochemistry and Cell Biology, vol. 38, no. 12, pp. 2196–2208, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. E.-M. Park, N. Ramnath, G. Y. Yang et al., “High superoxide dismutase and low glutathione peroxidase activities in red blood cells predict susceptibility of lung cancer patients to radiation pneumonitis,” Free Radical Biology & Medicine, vol. 42, no. 2, pp. 280–287, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. National Institute of Health, NIH publication no. 11-7737, October 2011, https://www.nia.nih.gov/sites/default/files/global_health_and_aging.pdf.
  43. United Nations, “World Population Aging 2013,” New York, 2013.
  44. C. E. Finch, “The menopause and aging, a comparative perspective,” The Journal of Steroid Biochemistry and Molecular Biology, vol. 142, pp. 132–141, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. S. M. Somani, K. Husain, and E. C. Schlorff, “Response of antioxidant system to physical and chemical stress,” in Oxidant, Antioxidants and Free Radicals, S. I. Baskin and H. Salem, Eds., pp. 125–141, Taylor & Francis, London, UK, 1997. View at Google Scholar
  46. S. K. Powers and C. K. Sen, “Physiological antioxidants and exercise training,” in Handbook of Oxidants and Antioxidants in Exercise, C. K. Sen, L. Packer, and O. Hanninen, Eds., Elsevier Science B.V., Amsterdam, The Netherlands, 2000. View at Google Scholar
  47. S. Das, R. Chattopadhyay, S. Ghosh et al., “Reactive oxygen species level in follicular fluid—embryo quality marker in IVF?” Human Reproduction, vol. 21, no. 9, pp. 2403–2407, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. Z. Wiener-Megnazi, L. Vardi, A. Lissak et al., “Oxidative stress indices in follicular fluid as measured by the thermochemiluminescence assay correlate with outcome parameters in in vitro fertilization,” Fertility and Sterility, vol. 82, no. 3, pp. 1171–1176, 2004. View at Publisher · View at Google Scholar · View at Scopus
  49. F. A. V. Seixas, M. R. da Silva, M. T. Murakami, P. Tosqui, and M. F. Colombo, “The water effect on the kinetics of the bovine liver catalase,” Protein & Peptide Letters, vol. 18, no. 9, pp. 879–885, 2011. View at Publisher · View at Google Scholar · View at Scopus
  50. R. Masella, R. Di Benedetto, R. Varì, C. Filesi, and C. Giovannini, “Novel mechanisms of natural antioxidant compounds in biological systems: involvement of glutathione and glutathione-related enzymes,” The Journal of Nutritional Biochemistry, vol. 16, no. 10, pp. 577–586, 2005. View at Publisher · View at Google Scholar · View at Scopus
  51. Q. Gu, B. Wang, X.-F. Zhang, Y.-P. Ma, J.-D. Liu, and X.-Z. Wang, “Contribution of receptor for advanced glycation end products to vasculature-protecting effects of exercise training in aged rats,” European Journal of Pharmacology, vol. 741, pp. 186–194, 2014. View at Publisher · View at Google Scholar · View at Scopus
  52. J. Liu, M. Liu, X. Ye et al., “Delay in oocyte aging in mice by the antioxidant N-acetyl-l-cysteine (NAC),” Human Reproduction, vol. 27, no. 5, pp. 1411–1420, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. A. Ahangarpour, Z. Lamoochi, H. Fathi Moghaddam, and S. M. Mansouri, “Effects of Portulaca oleracea ethanolic extract on reproductive system of aging female mice,” International Journal of Reproductive BioMedicine, vol. 14, no. 3, pp. 205–212, 2016. View at Google Scholar
  54. M. Mahmoodi, M. Soleimani Mehranjani, S. M. A. Shariatzadeh, H. Eimani, and A. Shahverdi, “N-acetylcysteine improves function and follicular survival in mice ovarian grafts through inhibition of oxidative stress,” Reproductive BioMedicine Online, vol. 30, no. 1, pp. 101–110, 2015. View at Publisher · View at Google Scholar · View at Scopus
  55. D. Bae, J. B. Park, J. U. Yang, and T. H. Lee, “Purification and characterization of glyoxylase II from bovine liver,” Korean Journal of Biochemistry, vol. 27, pp. 99–103, 1995. View at Google Scholar
  56. S. Falone, S. Jr Santini, S. di Loreto et al., “Improved mitochondrial and methylglyoxal-related metabolisms support hyperproliferation induced by 50 Hz magnetic field in neuroblastoma cells,” Journal of Cellular Physiology, vol. 231, no. 9, pp. 2014–2025, 2016. View at Publisher · View at Google Scholar · View at Scopus