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Mediators of Inflammation
Volume 2018, Article ID 6136075, 10 pages
https://doi.org/10.1155/2018/6136075
Research Article

Downregulation of DJ-1 Fails to Protect Mitochondrial Complex I Subunit NDUFS3 in the Testes and Contributes to the Asthenozoospermia

1National Key Research Laboratory of Natural and Biomimetic Drugs, Peking University, Beijing 100191, China
2Department of Molecular and Cellular Pharmacology, School of Pharmaceutical Sciences, Peking University, Beijing 100191, China
3Department of Urology, Peking University Third Hospital, Beijing 100191, China

Correspondence should be addressed to Yi Sun; nc.ude.umjb@iynus, Hui Jiang; moc.361@55iuhgnaij, and Xiaoping Pu; nc.ude.umjb@321pxp

Received 1 November 2017; Revised 29 December 2017; Accepted 14 January 2018; Published 3 April 2018

Academic Editor: Cheng Xiao

Copyright © 2018 Yupeng Wang 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. S. M. Curi, J. I. Ariagno, P. H. Chenlo et al., “Asthenozoospermia: analysis of a large population,” Archives of Andrology, vol. 49, no. 5, pp. 343–349, 2003. View at Publisher · View at Google Scholar
  2. A. Jungwirth, A. Giwercman, H. Tournaye et al., “European Association of Urology guidelines on male infertility: the 2012 update,” European Urology, vol. 62, no. 2, pp. 324–332, 2012. View at Publisher · View at Google Scholar · View at Scopus
  3. A. Fathy, S. J. Chen, N. Novak, H. C. Schuppe, G. Haidl, and J. P. Allam, “Differential leucocyte detection by flow cytometry improves the diagnosis of genital tract inflammation and identifies macrophages as proinflammatory cytokine-producing cells in human semen,” Andrologia, vol. 46, no. 9, pp. 1004–1012, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. J. S. Armstrong, M. Rajasekaran, W. Chamulitrat, P. Gatti, W. J. Hellstrom, and S. C. Sikka, “Characterization of reactive oxygen species induced effects on human spermatozoa movement and energy metabolism,” Free Radical Biology & Medicine, vol. 26, no. 7-8, pp. 869–880, 1999. View at Publisher · View at Google Scholar · View at Scopus
  5. 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
  6. A. J. Mundy, T. A. Ryder, and D. K. Edmonds, “Asthenozoospermia and the human sperm mid-piece,” Human Reproduction, vol. 10, no. 1, pp. 116–119, 1995. View at Publisher · View at Google Scholar · View at Scopus
  7. E. Ruiz-Pesini, C. Diez, A. C. Lapena et al., “Correlation of sperm motility with mitochondrial enzymatic activities,” Clinical Chemistry, vol. 44, no. 8, Part 1, pp. 1616–1620, 1998. View at Google Scholar
  8. E. Ruiz-Pesini, A. C. Lapena, C. Diez, E. Alvarez, J. A. Enriquez, and M. J. Lopez-Perez, “Seminal quality correlates with mitochondrial functionality,” Clinica Chimica Acta, vol. 300, no. 1-2, pp. 97–105, 2000. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Amaral, J. Ramalho-Santos, and J. C. St John, “The expression of polymerase gamma and mitochondrial transcription factor A and the regulation of mitochondrial DNA content in mature human sperm,” Human Reproduction, vol. 22, no. 6, pp. 1585–1596, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. D. Martinvalet, D. M. Dykxhoorn, R. Ferrini, and J. Lieberman, “Granzyme A cleaves a mitochondrial complex I protein to initiate caspase-independent cell death,” Cell, vol. 133, no. 4, pp. 681–692, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. T. Hayashi, C. Ishimori, K. Takahashi-Niki et al., “DJ-1 binds to mitochondrial complex I and maintains its activity,” Biochemical and Biophysical Research Communications, vol. 390, no. 3, pp. 667–672, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Inden, T. Taira, Y. Kitamura et al., “PARK7 DJ-1 protects against degeneration of nigral dopaminergic neurons in Parkinson’s disease rat model,” Neurobiology of Disease, vol. 24, no. 1, pp. 144–158, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. E. Andres-Mateos, C. Perier, L. Zhang et al., “DJ-1 gene deletion reveals that DJ-1 is an atypical peroxiredoxin-like peroxidase,” Proceedings of the National Academy of Sciences, vol. 104, no. 37, pp. 14807–14812, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. J. M. Kim, H. J. Jang, S. Y. Choi et al., “DJ-1 contributes to adipogenesis and obesity-induced inflammation,” Scientific Reports, vol. 4, no. 1, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. L. Chen, M. Luo, X. Sun et al., “DJ-1 deficiency attenuates expansion of liver progenitor cells through modulating the inflammatory and fibrogenic niches,” Cell Death & Disease, vol. 7, no. 6, article e2257, 2016. View at Publisher · View at Google Scholar · View at Scopus
  16. G. R. Klinefelter, J. W. Laskey, J. Ferrell, J. D. Suarez, and N. L. Roberts, “Discriminant analysis indicates a single sperm protein (SP22) is predictive of fertility following exposure to epididymal toxicants,” Journal of Andrology, vol. 18, no. 2, pp. 139–150, 1997. View at Google Scholar
  17. A. Wagenfeld, C. H. Yeung, K. Strupat, and T. G. Cooper, “Shedding of a rat epididymal sperm protein associated with infertility induced by ornidazole and alpha-chlorohydrin,” Biology of Reproduction, vol. 58, no. 5, pp. 1257–1265, 1998. View at Publisher · View at Google Scholar · View at Scopus
  18. J. E. Welch, R. R. Barbee, N. L. Roberts, J. D. Suarez, and G. R. Klinefelter, “SP22: a novel fertility protein from a highly conserved gene family,” Journal of Andrology, vol. 19, no. 4, pp. 385–393, 1998. View at Google Scholar
  19. C. N. An, H. Jiang, Q. Wang et al., “Down-regulation of DJ-1 protein in the ejaculated spermatozoa from Chinese asthenozoospermia patients,” Fertility and Sterility, vol. 96, no. 1, pp. 19–23.e2, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. Y. Sun, W. J. Zhang, X. Zhao, R. P. Yuan, H. Jiang, and X. P. Pu, “PARK7 protein translocating into spermatozoa mitochondria in Chinese asthenozoospermia,” Reproduction, vol. 148, no. 3, pp. 249–257, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. R. M. McClain and J. C. Downing, “Reproduction studies in rats treated with ornidazole,” Toxicology and Applied Pharmacology, vol. 92, no. 3, pp. 480–487, 1988. View at Publisher · View at Google Scholar · View at Scopus
  22. W. Bone, N. G. Jones, G. Kamp, C. H. Yeung, and T. G. Cooper, “Effect of ornidazole on fertility of male rats: inhibition of a glycolysis-related motility pattern and zona binding required for fertilization in vitro,” Journal of Reproduction and Fertility, vol. 118, no. 1, pp. 127–135, 2000. View at Google Scholar
  23. World Health Organization, WHO laboratory manual for the examination and processing of human semen, World Health Organization, Geneva, Switzerland, 2010.
  24. G. Oberlander, C. H. Yeung, and T. G. Cooper, “Induction of reversible infertility in male rats by oral ornidazole and its effects on sperm motility and epididymal secretions,” Journal of Reproduction and Fertility, vol. 100, no. 2, pp. 551–559, 1994. View at Publisher · View at Google Scholar · View at Scopus
  25. D. A. Rizzetti, C. S. Martinez, A. G. Escobar et al., “Egg white-derived peptides prevent male reproductive dysfunction induced by mercury in rats,” Food and Chemical Toxicology, vol. 100, pp. 253–264, 2017. View at Publisher · View at Google Scholar · View at Scopus
  26. K. Chenniappan and K. Murugan, “Therapeutic and fertility restoration effects of ionidium suffruticosumon sub-fertile male albino Wistar rats: effects on testis and caudal spermatozoa,” Pharmaceutical Biology, vol. 55, no. 1, pp. 946–957, 2017. View at Publisher · View at Google Scholar · View at Scopus
  27. Y.-N. Wang, B. Wang, M. Liang et al., “Down-regulation of CatSper1 channel in epididymal spermatozoa contributes to the pathogenesis of asthenozoospermia, whereas up-regulation of the channel by Sheng-Jing-San treatment improves the sperm motility of asthenozoospermia in rats,” Fertility and Sterility, vol. 99, no. 2, pp. 579–587, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Benoff, K. Auborn, J. L. Marmar, and I. R. Hurley, “Link between low-dose environmentally relevant cadmium exposures and asthenozoospermia in a rat model,” Fertility and Sterility, vol. 89, no. 2, pp. e73–e79, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. C. Ortega, G. Verheyen, D. Raick, M. Camus, P. Devroey, and H. Tournaye, “Absolute asthenozoospermia and ICSI: what are the options?” Human Reproduction Update, vol. 17, no. 5, pp. 684–692, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. P. Piomboni, R. Focarelli, A. Stendardi, A. Ferramosca, and V. Zara, “The role of mitochondria in energy production for human sperm motility,” International Journal of Andrology, vol. 35, no. 2, pp. 109–124, 2012. View at Publisher · View at Google Scholar · View at Scopus
  31. X. Li, M. Tian, G. Zhang et al., “Spatially dependent fluorescent probe for detecting different situations of mitochondrial membrane potential conveniently and efficiently,” Analytical Chemistry, vol. 89, no. 6, pp. 3335–3344, 2017. View at Publisher · View at Google Scholar · View at Scopus
  32. D. P. Evenson, Z. Darzynkiewicz, and M. R. Melamed, “Simultaneous measurement by flow cytometry of sperm cell viability and mitochondrial membrane potential related to cell motility,” Journal of Histochemistry & Cytochemistry, vol. 30, no. 3, pp. 279-280, 1982. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Ferramosca, R. Focarelli, P. Piomboni, L. Coppola, and V. Zara, “Oxygen uptake by mitochondria in demembranated human spermatozoa: a reliable tool for the evaluation of sperm respiratory efficiency,” International Journal of Andrology, vol. 31, no. 3, pp. 337–345, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. F. Pelliccione, A. Micillo, G. Cordeschi et al., “Altered ultrastructure of mitochondrial membranes is strongly associated with unexplained asthenozoospermia,” Fertility and Sterility, vol. 95, no. 2, pp. 641–646, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. Z. Li, Y. Zhou, R. Liu et al., “Effects of semen processing on the generation of reactive oxygen species and mitochondrial membrane potential of human spermatozoa,” Andrologia, vol. 44, no. 3, pp. 157–163, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. J. Y. Chan and S. H. Chan, “Activation of endogenous antioxidants as a common therapeutic strategy against cancer, neurodegeneration and cardiovascular diseases: a lesson learnt from DJ-1,” Pharmacology & Therapeutics, vol. 156, pp. 69–74, 2015. View at Publisher · View at Google Scholar · View at Scopus
  37. D. Nagakubo, T. Taira, H. Kitaura et al., “DJ-1, a novel oncogene which transforms mouse NIH3T3 cells in cooperation with ras,” Biochemical and Biophysical Research Communications, vol. 231, no. 2, pp. 509–513, 1997. View at Publisher · View at Google Scholar · View at Scopus
  38. A. Wagenfeld, J. Gromoll, and T. G. Cooper, “Molecular cloning and expression of rat contraception associated protein 1 (CAP1), a protein putatively involved in fertilization,” Biochemical and Biophysical Research Communications, vol. 251, no. 2, pp. 545–549, 1998. View at Publisher · View at Google Scholar · View at Scopus
  39. G. R. Klinefelter, “Saga of a sperm fertility biomarker,” Animal Reproduction Science, vol. 105, no. 1-2, pp. 90–103, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. S. Shen, J. Wang, J. Liang, and D. He, “Comparative proteomic study between human normal motility sperm and idiopathic asthenozoospermia,” World Journal of Urology, vol. 31, no. 6, pp. 1395–1401, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. R. O. Vogel, C. E. Dieteren, L. P. van den Heuvel et al., “Identification of mitochondrial complex I assembly intermediates by tracing tagged NDUFS3 demonstrates the entry point of mitochondrial subunits,” The Journal of Biological Chemistry, vol. 282, no. 10, pp. 7582–7590, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. E. Ruizpesini, A. C. Lapeña, C. Díez, E. Alvarez, J. A. Enríquez, and M. J. Lópezpérez, “Seminal quality correlates with mitochondrial functionality,” Clinica Chimica Acta, vol. 300, no. 1-2, pp. 97–105, 2000. View at Publisher · View at Google Scholar · View at Scopus
  43. S. Lucken-Ardjomande and J. C. Martinou, “Granzyme A, a stealth killer in the mitochondrion,” Cell, vol. 133, no. 4, pp. 568–570, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Rajender, P. Rahul, and A. A. Mahdi, “Mitochondria, spermatogenesis and male infertility,” Mitochondrion, vol. 10, no. 5, pp. 419–428, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. L. Zhang, M. Shimoji, B. Thomas et al., “Mitochondrial localization of the Parkinson’s disease related protein DJ-1: implications for pathogenesis,” Human Molecular Genetics, vol. 14, no. 14, pp. 2063–2073, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. A. P. Joselin, S. J. Hewitt, S. M. Callaghan et al., “ROS-dependent regulation of Parkin and DJ-1 localization during oxidative stress in neurons,” Human Molecular Genetics, vol. 21, no. 22, pp. 4888–4903, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. R. M. Canet-Aviles, M. A. Wilson, D. W. Miller et al., “The Parkinson’s disease protein DJ-1 is neuroprotective due to cysteine-sulfinic acid-driven mitochondrial localization,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 24, pp. 9103–9108, 2004. View at Publisher · View at Google Scholar · View at Scopus
  48. P. McGonigle and B. Ruggeri, “Animal models of human disease: challenges in enabling translation,” Biochemical Pharmacology, vol. 87, no. 1, pp. 162–171, 2014. View at Publisher · View at Google Scholar · View at Scopus