Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2016, Article ID 1687657, 12 pages
http://dx.doi.org/10.1155/2016/1687657
Research Article

Evaluation of Lasting Effects of Heat Stress on Sperm Profile and Oxidative Status of Ram Semen and Epididymal Sperm

1Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of Sao Paulo, Avenue Prof. Dr. Orlando Marques de Paiva 87, Cidade Universitária, 05508 270 Sao Paulo, SP, Brazil
2Department of Biochemistry and Molecular and Cell Biology, University of Zaragoza, Miguel Servet 177, 50013 Zaragoza, Spain

Received 25 September 2015; Revised 30 November 2015; Accepted 2 December 2015

Academic Editor: Paola Venditti

Copyright © 2016 Thais Rose dos Santos Hamilton 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. P. L. Senger, “The organization and function of the male reproductive system,” in Pathways to Pregnancy and Parturition, Pullman: Current Conceptions, pp. 44–79, 4th edition, 2003. View at Google Scholar
  2. R. J. Aitken and S. D. Roman, “Antioxidant systems and oxidative stress in the testes,” Oxidative Medicine and Cellular Longevity, vol. 1, no. 1, pp. 15–24, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. J. G. Reyes, J. G. Farias, S. Henríquez-Olavarrieta et al., “The hypoxic testicle: physiology and pathophysiology,” Oxidative Medicine and Cellular Longevity, vol. 2012, Article ID 929285, 15 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. W. Hou, Y. Dong, J. Zhang et al., “Hypoxia-induced deacetylation is required for tetraploid differentiation in response to testicular ischemia-reperfusion (IR) injury,” Journal of Andrology, vol. 33, no. 6, pp. 1379–1386, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Nichi, P. E. J. Bols, R. M. Züge et al., “Seasonal variation in semen quality in Bos indicus and Bos taurus bulls raised under tropical conditions,” Theriogenology, vol. 66, no. 4, pp. 822–828, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. J. S. Fleming, F. Yu, R. M. McDonald et al., “Effects of scrotal heating on sperm surface protein PH-20 expression in sheep,” Molecular Reproduction and Development, vol. 68, no. 1, pp. 103–114, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. C. Paul, S. Teng, and P. T. K. Saunders, “A single, mild, transient scrotal heat stress causes hypoxia and oxidative stress in mouse testes, which induces germ cell death,” Biology of Reproduction, vol. 80, no. 5, pp. 913–919, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. C. G. Blumer, R. M. Fariello, A. E. Restelli, D. M. Spaine, R. P. Bertolla, and A. P. Cedenho, “Sperm nuclear DNA fragmentation and mitochondrial activity in men with varicocele,” Fertility and Sterility, vol. 90, no. 5, pp. 1716–1722, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. B. Halliwell and J. M. C. Gutteridge, “Cellular responses to oxidative stress: adaptation, damage, repair, senescence and death,” in Free Radicals in Biology and Medicine, pp. 187–268, Oxford University Press, Oxford, UK, 4th edition, 2007. View at Google Scholar
  10. L. Schibler, D. Vaiman, A. Oustry, C. Giraud-Delville, and E. P. Cribiu, “Comparative gene mapping: a fine-scale survey of chromosome rearrangements between ruminants and humans,” Genome Research, vol. 8, no. 9, pp. 901–915, 1998. View at Google Scholar · View at Scopus
  11. P. Vernet, R. J. Aitken, and J. R. Drevet, “Antioxidant strategies in the epididymis,” Molecular and Cellular Endocrinology, vol. 216, no. 1, pp. 31–39, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. F. M. Flesch and B. M. Gadella, “Dynamics of the mammalian sperm plasma membrane in the process of fertilization,” Biochimica et Biophysica Acta—Reviews on Biomembranes, vol. 1469, no. 3, pp. 197–235, 2000. View at Publisher · View at Google Scholar · View at Scopus
  13. R. Jones and T. Mann, “Damage to ram spermatozoa by peroxidation of endogenous phospholipids,” Journal of Reproduction and Fertility, vol. 50, no. 2, pp. 261–268, 1977. View at Publisher · View at Google Scholar · View at Scopus
  14. A. J. Koppers, G. N. De Iuliis, J. M. Finnie, E. A. McLaughlin, and R. J. Aitken, “Significance of mitochondrial reactive oxygen species in the generation of oxidative stress in spermatozoa,” The Journal of Clinical Endocrinology and Metabolism, vol. 93, no. 8, pp. 3199–3207, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. R. Mahfouz, R. Sharma, A. Thiyagarajan et al., “Semen characteristics and sperm DNA fragmentation in infertile men with low and high levels of seminal reactive oxygen species,” Fertility and Sterility, vol. 94, no. 6, pp. 2141–2146, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. J. G. Alvarez and B. T. Storey, “Evidence for increased lipid peroxidative damage and loss of superoxide dismutase activity as a mode of sublethal cryodamage to human sperm during cryopreservation,” Journal of Andrology, vol. 13, no. 3, pp. 232–241, 1992. View at Google Scholar · View at Scopus
  17. S. P. Dandekar, G. D. Nadkarni, V. S. Kulkarni, and S. Punekar, “Lipid peroxidation and antioxidant enzymes in male infertility,” Journal of Postgraduate Medicine, vol. 48, no. 3, pp. 186–189, 2002. View at Google Scholar · View at Scopus
  18. R. J. Potts, T. Mjefferies, and L. J. Notarianni, “Antioxidant capacity of the epididymis,” Human Reproduction, vol. 14, no. 10, pp. 2513–2516, 1999. View at Publisher · View at Google Scholar · View at Scopus
  19. J. Djordjevic, A. Djordjevic, M. Adzic, A. Niciforovic, and M. B. Radojcic, “Chronic stress differentially affects antioxidant enzymes and modifies the acute stress response in liver of wistar rats,” Physiological Research, vol. 59, no. 5, pp. 729–736, 2010. View at Google Scholar · View at Scopus
  20. A. Rahal, A. Kumar, V. Singh et al., “Oxidative stress, prooxidants, and antioxidants: the interplay,” BioMed Research International, vol. 2014, Article ID 761264, 19 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. E. Blom, “The ultrastructure of some characteristic sperm defects and a proposal for a new classification of the bull spermiogram,” Nordisk Veterinaermedicin, vol. 25, no. 7-8, pp. 383–391, 1973. View at Google Scholar · View at Scopus
  22. A. Gomes, E. Fernandes, and J. L. F. C. Lima, “Fluorescence probes used for detection of reactive oxygen species,” Journal of Biochemical and Biophysical Methods, vol. 65, no. 2-3, pp. 45–80, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. S.-H. Kim, D.-H. Yu, and Y.-J. Kim, “Apoptosis-like change, ROS, and DNA status in cryopreserved canine sperm recovered by glass wool filtration and Percoll gradient centrifugation techniques,” Animal Reproduction Science, vol. 119, no. 1-2, pp. 106–114, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. J. I. Martí, E. Martí, J. A. Cebrián-Pérez, and T. Muiño-Blanco, “Survival rate and antioxidant enzyme activity of ram spermatozoa after dilution with different extenders or selection by a dextran swim-up procedure,” Theriogenology, vol. 60, no. 6, pp. 1025–1037, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. 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
  26. H. Ohkawa, N. Ohishi, and K. Yagi, “Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction,” Analytical Biochemistry, vol. 95, no. 2, pp. 351–358, 1979. View at Publisher · View at Google Scholar · View at Scopus
  27. R. Simões, W. B. Feitosa, A. F. P. Siqueira et al., “Influence of bovine sperm DNA fragmentation and oxidative stress on early embryo in vitro development outcome,” Reproduction, vol. 146, no. 5, pp. 433–441, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Nichi, I. G. F. Goovaerts, C. N. M. Cortada, V. H. Barnabe, J. B. P. De Clercq, and P. E. J. Bols, “Roles of lipid peroxidation and cytoplasmic droplets on in vitro fertilization capacity of sperm collected from bovine epididymides stored at 4 and 34°C,” Theriogenology, vol. 67, no. 2, pp. 334–340, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. C. N. Vaisberg, L. V. Jelezarsky, B. Dishlianova, and T. A. Chaushev, “Activity, substrate detection and immunolocalization of glutathione peroxidase (GPx) in bovine reproductive organs and semen,” Theriogenology, vol. 64, no. 2, pp. 416–428, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. J. R. Drevet, “The antioxidant glutathione peroxidase family and spermatozoa: a complex story,” Molecular and Cellular Endocrinology, vol. 250, no. 1-2, pp. 70–79, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Pérez-Crespo, B. Pintado, and A. Gutiérrez-Adán, “Scrotal heat stress effects on sperm viability, sperm DNA integrity, and the offspring sex ration in mice,” Molecular Reproduction and Development, vol. 75, no. 1, pp. 40–47, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. M. J. Fields, W. C. Burns, and A. C. Warnick, “Age, season and breed effects on testicular volume and semen traits in young beef bulls,” Journal of Animal Science, vol. 48, no. 6, pp. 1299–1304, 1979. View at Google Scholar · View at Scopus
  33. C. M. Barros, M. F. Pegorer, J. L. M. Vasconcelos, B. G. Eberhardt, and F. M. Monteiro, “Importance of sperm genotype (indicus versus taurus) for fertility and embryonic development at elevated temperatures,” Theriogenology, vol. 65, no. 1, pp. 210–218, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. M. B. Rahman, L. Vandaele, T. Rijsselaere et al., “Scrotal insulation and its relationship to abnormal morphology, chromatin protamination and nuclear shape of spermatozoa in Holstein-Friesian and Belgian Blue bulls,” Theriogenology, vol. 76, no. 7, pp. 1246–1257, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. P. Thonneau, L. Bujan, L. Multigner, and R. Mieusset, “Occupational heat exposure and male fertility: a review,” Human Reproduction, vol. 13, no. 8, pp. 2122–2125, 1998. View at Publisher · View at Google Scholar · View at Scopus
  36. J. K. Voglmayr, B. P. Setchell, and I. G. White, “The effects of heat on the metabolism and ultrastructure of ram testicular spermatozoa,” Journal of Reproduction and Fertility, vol. 24, no. 1, pp. 71–80, 1971. View at Publisher · View at Google Scholar · View at Scopus
  37. P. Williamson, “The fine structure of ejaculated ram spermatozoa following scrotal heating,” Journal of Reproduction and Fertility, vol. 40, no. 1, pp. 191–195, 1974. View at Publisher · View at Google Scholar · View at Scopus
  38. S. W. Byers, “Effect of scrotal insulation on the ability of ram testes to produce testosterone in vitro,” Journal of Reproduction and Fertility, vol. 71, no. 1, pp. 17–21, 1984. View at Publisher · View at Google Scholar · View at Scopus
  39. S. W. Byers and T. D. Glover, “Effect of scrotal insulation on the pituitary-testicular axis of the rat,” Journal of Reproduction and Fertility, vol. 71, no. 1, pp. 23–31, 1984. View at Publisher · View at Google Scholar · View at Scopus
  40. R. Walczak-Jedrzejowska, J. K. Wolski, and J. Slowikowska-Hilczer, “The role of oxidative stress and antioxidants in male fertility,” Central European Journal of Urology, vol. 66, no. 1, pp. 60–67, 2013. View at Google Scholar · View at Scopus
  41. S. A. Suleiman, M. Elamin Ali, Z. M. S. Zaki, E. M. A. El-Malik, and M. A. Nasr, “Lipid peroxidation and human sperm motility: protective role of vitamin E,” Journal of Andrology, vol. 17, no. 5, pp. 530–537, 1996. View at Google Scholar · View at Scopus
  42. S. I. Peris, J.-F. Bilodeau, M. Dufour, and J. L. Bailey, “Impact of cryopreservation and reactive oxygen species on DNA integrity, lipid peroxidation, and functional parameters in ram sperm,” Molecular Reproduction and Development, vol. 74, no. 7, pp. 878–892, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Ferramosca, S. P. Provenzano, D. D. Montagna, L. Coppola, and V. Zara, “Oxidative stress negatively affects human sperm mitochondrial respiration,” Urology, vol. 82, no. 1, pp. 78–83, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Agarwal, E. Tvrda, and R. Sharma, “Relationship amongst teratozoospermia, seminal oxidative stress and male infertility,” Reproductive Biology and Endocrinology, vol. 12, article 45, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. U. Ott, A. Aschoff, R. Fünfstück, G. Jirikowski, and G. Wolf, “DNA fragmentation in acute and chronic rejection after renal transplantation,” Transplantation Proceedings, vol. 39, no. 1, pp. 73–77, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. R. Mahfouz, R. Sharma, J. Lackner, N. Aziz, and A. Agarwal, “Evaluation of chemiluminescence and flow cytometry as tools in assessing production of hydrogen peroxide and superoxide anion in human spermatozoa,” Fertility and Sterility, vol. 92, no. 2, pp. 819–827, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. N. Aziz, J. Novotny, I. Oborna, H. Fingerova, J. Brezinova, and M. Svobodova, “Comparison of chemiluminescence and flow cytometry in the estimation of reactive oxygen and nitrogen species in human semen,” Fertility and Sterility, vol. 94, no. 7, pp. 2604–2608, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. J. B. Sharma, A. Sharma, A. Bahadur, N. Vimala, A. Satyam, and S. Mittal, “Oxidative stress markers and antioxidant levels in normal pregnancy and pre-eclampsia,” International Journal of Gynecology and Obstetrics, vol. 94, no. 1, pp. 23–27, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. I. Garaiová, J. Muchová, M. Šustrová et al., “The relationship between antioxidant systems and some markers of oxidative stress in persons with Down syndrome,” Biologia, vol. 59, no. 6, pp. 787–794, 2004. View at Google Scholar · View at Scopus
  50. R. P. Barcelos, M. A. Souza, G. P. Amaral et al., “Caffeine supplementation modulates oxidative stress markers in the liver of trained rats,” Life Sciences, vol. 96, no. 1-2, pp. 40–45, 2014. View at Publisher · View at Google Scholar · View at Scopus
  51. M. A. Bouzid, O. Hammouda, R. Matran, S. Robin, and C. Fabre, “Changes in oxidative stress markers and biological markers of muscle injury with aging at rest and in response to an exhaustive exercise,” PLoS ONE, vol. 9, no. 3, Article ID e90420, 2014. View at Publisher · View at Google Scholar · View at Scopus
  52. A. Giannattasio, M. De Rosa, R. Smeraglia et al., “Glutathione Peroxidase (GPX) activity in seminal plasma of healthy and infertile males,” Journal of Endocrinological Investigation, vol. 25, no. 11, pp. 983–986, 2002. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Maiorino, V. Bosello, F. Ursini et al., “Genetic variations of gpx-4 and male infertility in humans,” Biology of Reproduction, vol. 68, no. 4, pp. 1134–1141, 2003. View at Publisher · View at Google Scholar · View at Scopus
  54. N. Garrido, M. Meseguer, C. Simon, A. Pellicer, and J. Remohi, “Pro-oxidative and anti-oxidative imbalance in human semen and its relation with male fertility,” Asian Journal of Andrology, vol. 6, no. 1, pp. 59–65, 2004. View at Google Scholar · View at Scopus
  55. H. D. Guthrie, G. R. Welch, and J. A. Long, “Mitochondrial function and reactive oxygen species action in relation to boar motility,” Theriogenology, vol. 70, no. 8, pp. 1209–1215, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. A. L. Agarwal, K. Makker, and R. Sharma, “Clinical relevance of oxidative stress in male factor infertility: an update,” American Journal of Reproductive Immunology, vol. 59, no. 1, pp. 2–11, 2008. View at Publisher · View at Google Scholar · View at Scopus
  57. R. J. Aitken, J. S. Clarkson, and S. Fishel, “Generation of reactive oxygen species, lipid peroxidation, and human sperm function,” Biology of Reproduction, vol. 41, no. 1, pp. 183–197, 1989. View at Publisher · View at Google Scholar · View at Scopus
  58. R. J. Aitken and M. A. Baker, “Reactive oxygen species generation by human spermatozoa: a continuing enigma,” International Journal of Andrology, vol. 25, no. 4, pp. 191–194, 2002. View at Google Scholar · View at Scopus
  59. R. J. Aitken and J. S. Clarkson, “Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa,” Journal of Reproduction and Fertility, vol. 81, no. 2, pp. 459–469, 1987. View at Publisher · View at Google Scholar · View at Scopus
  60. K. Stephan, M. Chang, E. P. Brass, and C. L. Hoppel, “Decreased activities of ubiquinol: ferricytochrome c oxidoreductase (complex III) and ferrocytochrome c:oxygen oxidoreductase (complex IV) in liver mitochondria from rats with hydroxycobalamin[c-lactam]-induced methylmalonic aciduria,” The Journal of Biological Chemistry, vol. 266, no. 31, pp. 20998–21003, 1991. View at Google Scholar
  61. N. J. Waterhouse, J. C. Goldstein, O. Von Ahsen, M. Schuler, D. D. Newmeyer, and D. R. Green, “Cytochrome c maintains mitochondrial transmembrane potential and ATP generation after outer mitochondrial membrane permeabilization during the apoptotic process,” The Journal of Cell Biology, vol. 153, no. 2, pp. 319–328, 2001. View at Publisher · View at Google Scholar · View at Scopus
  62. P. Mahaboob Basha and S. M. Saumya, “Suppression of mitochondrial oxidative phosphorylation and TCA enzymes in discrete brain regions of mice exposed to high fluoride: amelioration by Panax ginseng (Ginseng) and Lagerstroemia speciosa (Banaba) extracts,” Cellular and Molecular Neurobiology, vol. 33, no. 3, pp. 453–464, 2013. View at Publisher · View at Google Scholar · View at Scopus