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Oxidative Medicine and Cellular Longevity
Volume 2017, Article ID 2172981, 12 pages
https://doi.org/10.1155/2017/2172981
Research Article

Chrysin Administration Protects against Oxidative Damage in Varicocele-Induced Adult Rats

1Department of Morphology, Institute of Biosciences, São Paulo State University (UNESP), Botucatu, SP, Brazil
2Graduate Program in Cell and Structural Biology, University of Campinas (UNICAMP), Campinas, SP, Brazil
3Department of Clinical Analyses, Toxicology and Food Sciences, School of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil

Correspondence should be addressed to Gabriela Missassi; moc.liamtoh@issassim_ybbag

Received 20 June 2017; Revised 23 October 2017; Accepted 15 November 2017; Published 19 December 2017

Academic Editor: Tiziana Persichini

Copyright © 2017 Gabriela Missassi 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. R. Smith, H. Kaune, D. Parodi et al., “Increased sperm DNA damage in patients with varicocele: relationship with seminal oxidative stress,” Human Reproduction, vol. 21, no. 4, pp. 986–993, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. World Health Organization, “The influence of varicocele on parameters of fertility in a large group of men presenting to infertility clinics,” Fertility and Sterility, vol. 57, no. 6, pp. 1289–1293, 1992. View at Publisher · View at Google Scholar
  3. Y. Gat, G. N. Bachar, Z. Zukerman, A. Belenky, and M. Gornish, “Varicocele: a bilateral disease,” Fertility and Sterility, vol. 81, no. 2, pp. 424–429, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. M. A. Witt and L. I. Lipshultz, “Varicocele: a progressive or static lesion?” Urology, vol. 42, no. 5, pp. 541–543, 1993. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Gokce, M. Davarci, F. R. Yalcinkaya et al., “Hereditary behavior of varicocele,” Journal of Andrology, vol. 31, no. 3, pp. 288–290, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. J. L. Marmar, “Varicocele and male infertility: part II: the pathophysiology of varicoceles in the light of current molecular and genetic information,” Human Reproduction Update, vol. 7, no. 5, pp. 461–472, 2001. View at Publisher · View at Google Scholar · View at Scopus
  7. C. L. Cho, S. C. Esteves, and A. Agarwal, “Novel insights into the pathophysiology of varicocele and its association with reactive oxygen species and sperm DNA fragmentation,” Asian Journal of Andrology, vol. 18, no. 2, pp. 186–193, 2016. View at Publisher · View at Google Scholar · View at Scopus
  8. T. Mostafa, T. H. Anis, A. El-Nashar, H. Imam, and I. A. Othman, “Varicocelectomy reduces reactive oxygen species levels and increases antioxidant activity of seminal plasma from infertile men with varicocele,” International Journal of Andrology, vol. 24, no. 5, pp. 261–265, 2001. View at Publisher · View at Google Scholar · View at Scopus
  9. W. Hsiao, J. S. Rosoff, J. R. Pale, J. L. Powell, and M. Goldstein, “Varicocelectomy is associated with increases in serum testosterone independent of clinical grade,” Urology, vol. 81, no. 6, pp. 1213–1218, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. T. A. Abdel-Meguid, H. M. Farsi, A. Al-Sayyad, A. Tayib, H. A. Mosli, and A. H. Halawani, “Effects of varicocele on serum testosterone and changes of testosterone after varicocelectomy: a prospective controlled study,” Urology, vol. 84, no. 5, pp. 1081–1087, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. E. C. Schatte, S. J. Hirshberg, M. L. Fallick, L. I. Lipschultz, and E. D. Kim, “Varicocelectomy improves sperm strict morphology and motility,” The Journal of Urology, vol. 160, no. 4, pp. 1338–1340, 1998. View at Publisher · View at Google Scholar · View at Scopus
  12. P. Masson and R. E. Brannigan, “The varicocele,” The Urologic Clinics of North America, vol. 41, no. 1, pp. 129–144, 2014. View at Publisher · View at Google Scholar · View at Scopus
  13. F. K. Al-Rubiey, “Effect of L-carnitine and meloxicam treatment on testicular Leydig cell numbers of varicocelized rats,” Middle East Fertility Society Journal, vol. 17, no. 1, pp. 47–53, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. S. Sohrabipour, A. Jafari, M. Kamalinejad, A. Sarrafnejd, T. Shahrestany, and H. R. Sadeghipour, “The role of flaxseed and vitamin E on oxidative stress in prepubertal rats with experimental varicocele: an experimental study,” Iranian Journal of Reproductive Medicine, vol. 11, no. 6, pp. 459–466, 2013. View at Google Scholar
  15. T. B. Mendes, C. C. Paccola, F. M. de Oliveira Neves et al., “Resveratrol improves reproductive parameters of adult rats varicocelized in peripuberty,” Reproduction, vol. 152, no. 1, pp. 23–35, 2016. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Kellis and L. Vickery, “Inhibition of human estrogen synthetase (aromatase) by flavones,” Science, vol. 225, no. 4666, pp. 1032–1034, 1984. View at Publisher · View at Google Scholar
  17. J. T. Sanderson, J. Hordijk, M. S. Denison, M. F. Springsteel, M. H. Nantz, and M. van den Berg, “Induction and inhibition of aromatase (CYP19) activity by natural and synthetic flavonoid compounds in H295R human adrenocortical carcinoma cells,” Toxicological Sciences, vol. 82, no. 1, pp. 70–79, 2004. View at Publisher · View at Google Scholar · View at Scopus
  18. E. R. Kasala, L. N. Bodduluru, R. M. Madana, A. K. V, R. Gogoi, and C. C. Barua, “Chemopreventive and therapeutic potential of chrysin in cancer: mechanistic perspectives,” Toxicology Letters, vol. 233, no. 2, pp. 214–225, 2015. View at Publisher · View at Google Scholar · View at Scopus
  19. H. A. Darwish, H. H. Arab, and R. M. Abdelsalam, “Chrysin alleviates testicular dysfunction in adjuvant arthritic rats via suppression of inflammation and apoptosis: comparison with celecoxib,” Toxicology and Applied Pharmacology, vol. 279, no. 2, pp. 129–140, 2014. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Rauf, R. Khan, M. Raza et al., “Suppression of inflammatory response by chrysin, a flavone isolated from Potentilla evestita Th. Wolf. In silico predictive study on its mechanistic effect,” Fitoterapia, vol. 103, pp. 129–135, 2015. View at Publisher · View at Google Scholar · View at Scopus
  21. I. C. Villar, R. Jimenez, M. Galisteo, M. F. Garcia-Saura, A. Zarzuelo, and J. Duarte, “Effects of chronic chrysin treatment in spontaneously hypertensive rats,” Planta Medica, vol. 68, no. 9, pp. 847–850, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. L. C. Souza, M. S. Antunes, C. B. Filho, L. Del Fabbro, and M. G. de Gomes, “Flavonoid chrysin prevents age-related cognitive decline via attenuation of oxidative stress and modulation of BDNF levels in aged mouse brain,” Pharmacology, Biochemistry, and Behavior, vol. 134, pp. 22–30, 2015. View at Publisher · View at Google Scholar · View at Scopus
  23. K. Dhawan, S. Kumar, and A. Sharma, “Beneficial effects of chrysin and benzoflavone on virility in 2-year-old male rats,” Journal of Medicinal Food, vol. 5, no. 1, pp. 43–48, 2002. View at Publisher · View at Google Scholar
  24. O. Ciftci, I. Ozdemir, M. Aydin, and A. Beytur, “Beneficial effects of chrysin on the reproductive system of adult male rats,” Andrologia, vol. 44, no. 3, pp. 181–186, 2012. View at Publisher · View at Google Scholar · View at Scopus
  25. K. Jana, X. Yin, R. B. Schiffer et al., “Chrysin, a natural flavonoid enhances steroidogenesis and steroidogenic acute regulatory protein gene expression in mouse Leydig cells,” The Journal of Endocrinology, vol. 197, no. 2, pp. 315–323, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. N. Ali, S. Rashid, S. Nafees, S. K. Hasan, and S. Sultana, “Beneficial effects of chrysin against methotrexate-induced hepatotoxicity via attenuation of oxidative stress and apoptosis,” Molecular and Cellular Biochemistry, vol. 385, no. 1-2, pp. 215–223, 2014. View at Publisher · View at Google Scholar · View at Scopus
  27. E. S. Manzolli, J. M. Serpeloni, D. Grotto et al., “Protective effects of the flavonoid chrysin against methylmercury-induced genotoxicity and alterations of antioxidant status, in vivo,” Oxidative Medicine and Cellular Longevity, vol. 2015, Article ID 602360, 7 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  28. L. D. Russell, R. A. Ettlin, A. P. Sinha Hikim, and E. D. Clegg, Histological and Histopathological Evaluation of the Testis, Cache River Press, Montreal, 1990.
  29. M. U. Rehman, N. Ali, S. Rashid et al., “Alleviation of hepatic injury by chrysin in cisplatin administered rats: probable role of oxidative and inflammatory markers,” Pharmacological Reports, vol. 66, no. 6, pp. 1050–1059, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. R. Khan, A. Q. Khan, W. Qamar et al., “Chrysin protects against cisplatin-induced colon. toxicity via amelioration of oxidative stress and apoptosis: probable role of p38MAPK and p53,” Toxicology and Applied Pharmacology, vol. 258, no. 3, pp. 315–329, 2012. View at Publisher · View at Google Scholar · View at Scopus
  31. T. T. Turner, “The study of varicocele through the use of animal models,” Human Reproduction Update, vol. 7, no. 1, pp. 78–84, 2001. View at Publisher · View at Google Scholar · View at Scopus
  32. J. Seed, R. E. Chapin, E. D. Clegg et al., “Methods for assessing sperm motility, morphology, and counts in the rat, rabbit, and dog: a consensus report,” Reproductive Toxicology, vol. 10, no. 3, pp. 237–244, 1996. View at Publisher · View at Google Scholar
  33. R. Filler, “Methods for evaluation of rats epididymal sperm morphology,” in Male Reproductive Toxicology, R. E. Chapin and J. J. Heindel, Eds., pp. 334–343, Academic Press, San Diego, CA, USA, 1993. View at Google Scholar
  34. A. M. Codrington, B. F. Hales, and B. Robaire, “Spermiogenic germ cell phase—specific DNA damage following cyclophosphamide exposure,” Journal of Andrology, vol. 25, no. 3, pp. 354–362, 2004. View at Publisher · View at Google Scholar
  35. G. W. Robb, R. P. Amann, and G. J. Killian, “Daily sperm production and epididymal sperm reserves of pubertal and adult rats,” Journal of Reproduction and Fertility, vol. 54, no. 1, pp. 103–107, 1978. View at Publisher · View at Google Scholar
  36. C. D. B. Fernandez, E. M. Porto, A. C. Arena, and W. G. Kempinas, “Effects of altered epididymal sperm transit time on sperm quality,” International Journal of Andrology, vol. 31, no. 4, pp. 427–437, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. G. S. A. Fernandes, A. C. Arena, C. D. B. Fernandez, A. Mercadante, L. F. Barbisan, and W. G. Kempinas, “Reproductive effects in male rats exposed to diuron,” Reproductive Toxicology, vol. 23, no. 1, pp. 106–112, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Ahlenius and K. Larsson, “Apomorphine and haloperidol-induced effects on male rat sexual behavior: no evidence for actions due to stimulation of central dopamine autoreceptors,” Pharmacology, Biochemistry, and Behavior, vol. 21, no. 3, pp. 463–466, 1984. View at Publisher · View at Google Scholar
  39. A. Agmo, “Male rat sexual behavior,” Brain Research Protocols, vol. 1, no. 2, pp. 203–209, 1997. View at Publisher · View at Google Scholar · View at Scopus
  40. 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
  41. H. H. Draper and M. Hadley, “[43] Malondialdehyde determination as index of lipid peroxidation,” Methods in Enzymology, vol. 186, pp. 421–431, 1990. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Ayala, M. F. Munoz, and S. Arguelles, “Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal,” Oxidative Medicine and Cellular Longevity, vol. 2014, Article ID 360438, 31 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Agarwal, R. K. Sharma, N. R. Desai, S. Prabakaran, A. Tavares, and E. Sabanegh, “Role of oxidative stress in pathogenesis of varicocele and infertility,” Urology, vol. 73, no. 3, pp. 461–469, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. B. Rao, J. C. Soufir, M. Martin, and G. David, “Lipid peroxidation in human spermatozoa as relatd to midpiece abnormalities and motility,” Gamete Research, vol. 24, no. 2, pp. 127–134, 1989. View at Publisher · View at Google Scholar · View at Scopus
  45. M. A. Abd-Elmoaty, R. Saleh, R. Sharma, and A. Agarwal, “Increased levels of oxidants and reduced antioxidants in semen of infertile men with varicocele,” Fertility and Sterility, vol. 94, no. 4, pp. 1531–1534, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. I. T. Koksal, A. Tefekli, M. Usta, H. Erol, S. Abbasoglu, and A. Kadioglu, “The role of reactive oxygen species in testicular dysfunction associated with varicocele,” BJU International, vol. 86, no. 4, pp. 549–552, 2000. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Gholirad, M. Razi, and H. Hassani Bafrani, “Tracing of zinc and iron in experimentally induced varicocele: correlation with oxidative, nitrosative and carbonyl stress,” Andrologia, vol. 49, no. 6, article e12687, 2017. View at Publisher · View at Google Scholar · View at Scopus
  48. H. Ozturk, B. Tander, A. Aydin, Z. Okumus, and S. Cetinkursun, “The effects of chemical sympathectomy on testicular injury in varicocele,” BJU International, vol. 87, no. 3, pp. 232–234, 2001. View at Publisher · View at Google Scholar · View at Scopus
  49. E. H. Aksu, M. Ozkaraca, F. M. Kandemir et al., “Mitigation of paracetamol-induced reproductive damage by chrysin in male rats via reducing oxidative stress,” Andrologia, vol. 48, no. 10, pp. 1145–1154, 2016. View at Publisher · View at Google Scholar · View at Scopus
  50. G. Pushpavalli, P. Kalaiarasi, C. Veeramani, and K. V. Pugalendi, “Effect of chrysin on hepatoprotective and antioxidant status in d-galactosamine-induced hepatitis in rats,” European Journal of Pharmacology, vol. 631, no. 1–3, pp. 36–41, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. S. Sultana, K. Verma, and R. Khan, “Nephroprotective efficacy of chrysin against cisplatin-induced toxicity via attenuation of oxidative stress,” The Journal of Pharmacy and Pharmacology, vol. 64, no. 6, pp. 872–881, 2012. View at Publisher · View at Google Scholar · View at Scopus
  52. I. U. Schraufstatter, D. B. Hinshaw, P. A. Hyslop, R. G. Spragg, and C. G. Cochrane, “Oxidant injury of cells. DNA strand-breaks activate polyadenosine diphosphate-ribose polymerase and lead to depletion of nicotinamide adenine dinucleotide,” The Journal of Clinical Investigation, vol. 77, no. 4, pp. 1312–1320, 1986. View at Publisher · View at Google Scholar
  53. R. K. Sharma and A. Agarwal, “Role of reactive oxygen species in male infertility,” Urology, vol. 48, no. 6, pp. 835–850, 1996. View at Publisher · View at Google Scholar · View at Scopus
  54. R. J. Aitken, T. B. Smith, M. S. Jobling, M. A. Baker, and G. N. De Iuliis, “Oxidative stress and male reproductive health,” Asian Journal of Andrology, vol. 16, no. 1, pp. 31–38, 2014. View at Publisher · View at Google Scholar · View at Scopus
  55. C. K. Naughton, A. K. Nangia, and A. Agarwal, “Varicocele and male infertility: part II: pathophysiology of varicoceles in male infertility,” Human Reproduction Update, vol. 7, no. 5, pp. 473–481, 2001. View at Publisher · View at Google Scholar · View at Scopus
  56. R. A. Saleh, A. Agarwal, R. K. Sharma, T. M. Said, S. C. Sikka, and A. J. Thomas Jr., “Evaluation of nuclear DNA damage in spermatozoa from infertile men with varicocele,” Fertility and Sterility, vol. 80, no. 6, pp. 1431–1436, 2003. View at Publisher · View at Google Scholar · View at Scopus
  57. C. Thompson, “Apoptosis in the pathogenesis and treatment of disease,” Science, vol. 267, no. 5203, pp. 1456–1462, 1995. View at Publisher · View at Google Scholar
  58. M. R. Goren, F. Kilinc, F. Kayaselcuk, C. Ozer, I. Oguzulgen, and E. Hasirci, “Effects of experimental left varicocele repair on hypoxia-inducible factor-1α and vascular endothelial growth factor expressions and angiogenesis in rat testis,” Andrologia, vol. 49, no. 2, 2017. View at Publisher · View at Google Scholar · View at Scopus
  59. N. A. Bayomy, N. I. Sarhan, and K. M. Abdel-Razek, “Effect of an experimental left varicocele on the bilateral testes of adult rats: a histological and immunohistochemical study,” The Egyptian Journal of Histology, vol. 35, no. 3, pp. 509–519, 2012. View at Publisher · View at Google Scholar · View at Scopus
  60. Y. S. Oh, N. H. Jo, J. K. Park, and M. C. Gye, “Changes in inflammatory cytokines accompany deregulation of claudin-11, resulting in inter-sertoli tight junctions in varicocele rat testes,” The Journal of Urology, vol. 196, no. 4, pp. 1303–1312, 2016. View at Publisher · View at Google Scholar · View at Scopus
  61. A. E. El-Sisi, M. E. El-Sayad, and N. M. Abdelsalam, “Protective effects of mirtazapine and chrysin on experimentally induced testicular damage in rats,” Biomedicine & Pharmacotherapy, vol. 95, pp. 1059–1066, 2017. View at Publisher · View at Google Scholar
  62. B. Kurowicka, G. J. Dietrich, and G. Kotwica, “Effect of neonatal or adult heat acclimation on testicular and epididymal morphometry and sperm production in rats,” Reproductive Biology, vol. 15, no. 1, pp. 1–8, 2015. View at Publisher · View at Google Scholar · View at Scopus
  63. S. Cayan, A. Kadioglu, I. Orhan, E. Kandirali, A. Tefekli, and S. Tellaloglu, “The effect of microsurgical varicocelectomy on serum follicle stimulating hormone, testosterone and free testosterone levels in infertile men with varicocele,” BJU International, vol. 84, no. 9, pp. 1046–1049, 1999. View at Google Scholar
  64. J. Damsgaard, U. N. Joensen, E. Carlsen et al., “Varicocele is associated with impaired semen quality and reproductive hormone levels: a study of 7035 healthy young men from six European countries,” European Urology, vol. 70, no. 6, pp. 1019–1029, 2016. View at Publisher · View at Google Scholar · View at Scopus
  65. J. Rajfer, T. T. Turner, F. Rivera, S. S. Howards, and S. C. Sikka, “Inhibition of testicular testosterone biosynthesis following experimental varicocele in rats,” Biology of Reproduction, vol. 36, no. 4, pp. 933–937, 1987. View at Publisher · View at Google Scholar
  66. Y. Zheng, X. Zhang, J. Zhou, F. Cheng, and B. Zhou, “Effects on the ipsilateral testis during progression of experimental varicocele in rat,” Medical Science Monitor, vol. 14, no. 6, pp. BR122–BR126, 2008. View at Google Scholar
  67. A. Hamada, R. Sharma, S. S. du Plessis et al., “Two-dimensional differential in-gel electrophoresis–based proteomics of male gametes in relation to oxidative stress,” Fertility and Sterility, vol. 99, no. 5, pp. 1216–1226.e2, 2013. View at Publisher · View at Google Scholar · View at Scopus
  68. A. Agarwal, R. Sharma, L. Samanta, D. Durairajanayagam, and E. Sabanegh, “Proteomic signatures of infertile men with clinical varicocele and their validation studies reveal mitochondrial dysfunction leading to infertility,” Asian Journal of Andrology, vol. 18, no. 2, pp. 282–291, 2016. View at Publisher · View at Google Scholar · View at Scopus
  69. N. Sofikitis, C. Takahashi, I. Nakamura, S. Hirakawa, and I. Miyagawa, “Surgical repair of secondary right varicocele in rats with primary left varicocele: effects on fertility, testicular temperature, spermatogenesis, and sperm maturation,” Archives of Andrology, vol. 28, no. 1, pp. 43–52, 1992. View at Publisher · View at Google Scholar · View at Scopus
  70. R. Heidari, R. Alizadeh, N. Abbasi et al., “Do Pilea microphylla improve sperm DNA fragmentation and sperm parameters in varicocelized rats?” Acta Medica Iranica, vol. 53, no. 9, pp. 547–554, 2015. View at Google Scholar
  71. R. Amann, “Use of animal models for detecting specific alterations in reproduction,” Fundamental and Applied Toxicology, vol. 2, no. 1, pp. 13–26, 1982. View at Publisher · View at Google Scholar · View at Scopus
  72. W. D. G. Kempinas and G. R. Klinefelter, “The epididymis as a target for toxicants,” in Comprehensive Toxicology, C. A. McQueen, Ed., pp. 149–166, Academic Press, Oxford, 2014. View at Google Scholar