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Cell Stress and Chaperones

, Volume 23, Issue 3, pp 429–439 | Cite as

Testicular torsion and reperfusion: evidences for biochemical and molecular alterations

  • Naeimeh Shamsi-Gamchi
  • Mazdak Razi
  • Mehdi Behfar
Original Paper
  • 86 Downloads

Abstract

This study was done in order to determine the molecular and biochemical alterations following testicular torsion (TT) and torsion-reperfusion (TR). For this purpose, 54 male Wistar rats were divided into five groups as control group (n = 6) and experimental group subjected to 1, 2, 4, and 8 h unilateral left torsion induction (n = 12 in each group). After induction of TT, testicular samples were collected from each group (n = 6), and the other six rats of each group underwent the same period of reperfusion after TT and then were sampled. Histological changes, the mRNA and protein expression of heat shock protein-70 (Hsp70), and caspase-3 were examined using reverse transcriptase-PCR (RT-PCR) and immunohistochemistry, respectively. Testicular total antioxidant capacity (TAC), glutathione peroxidase (GSH-px), and malondialdehyde (MDA) levels were evaluated. The mRNA damage and DNA fragmentation were assessed. The TT and TR significantly reduced differentiation and spermiogenesis indices (p < 0.05). The TT- and TR-induced groups exhibited a severe reduction in Hsp70 expression as well as remarkable enhancement in caspase-3 expression. The TAC and GSH-px levels were decreased and the MDA content was increased in TT- and TR-induced groups. Finally, the TT and TR enhanced mRNA damage and DNA fragmentation. The TT- and TR-induced damaging oxidative stress, diminished Hsp70 expression, and enhanced caspase-3 mRNA and protein levels result in apoptosis following 1, 2, and 4 h. Whereas, following 8 h, TT and TR initiate the necrosis by inducing energy depletion as well as severe mRNA damage.

Keywords

Torsion-reperfusion Hsp70 Caspase-3 Apoptosis Necrosis Rat 

Notes

Acknowledgments

Authors wish to thank departments of Comparative Histology and Embryology and Surgery and Diagnostic Imaging, Faculty of Veterinary Medicine, Urmia University.

Funding information

The current manuscript is from thesis NO: 2D-337, which was funded by Urmia University. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

References

  1. Adibnia E, Razi M, Malekinejad H (2016) Zearalenone and 17 beta-estradiol induced damages in male rats reproduction potential; evidence for ERalpha and ERbeta receptors expression and steroidogenesis. Toxicon 120:133–146.  https://doi.org/10.1016/j.toxicon.2016.08.009 CrossRefPubMedGoogle Scholar
  2. Agarwal A, Makker K, Sharma R (2008) Clinical relevance of oxidative stress in male factor infertility: an update. Am J Reprod Immunol 59:2–11.  https://doi.org/10.1111/j.1600-0897.2007.00559.x CrossRefPubMedGoogle Scholar
  3. Comish PB et al (2015) Increasing testicular temperature by exposure to elevated ambient temperatures restores spermatogenesis in adult Utp14b (jsd) mutant (jsd) mice. Andrology 3:376–384.  https://doi.org/10.1111/andr.287 CrossRefPubMedGoogle Scholar
  4. Dada R, Gupta N, Kucheria K (2002) Spermatogenic alterations in men with high testiculo epididymal temperatures. Indian J Human Genetics 8:20–25Google Scholar
  5. Dun MD, Aitken RJ, Nixon B (2012) The role of molecular chaperones in spermatogenesis and the post-testicular maturation of mammalian spermatozoa. Hum Reprod Update 18:420–435.  https://doi.org/10.1093/humupd/dms009 CrossRefPubMedGoogle Scholar
  6. Ekici S, Dogan Ekici AI, Ozturk G, Benli Aksungar F, Sinanoglu O, Turan G, Luleci N (2012) Comparison of melatonin and ozone in the prevention of reperfusion injury following unilateral testicular torsion in rats. Urology 80:899–906.  https://doi.org/10.1016/j.urology.2012.06.049 CrossRefPubMedGoogle Scholar
  7. Filho DW, Torres MA, Bordin AL, Crezcynski-Pasa TB, Boveris A (2004) Spermatic cord torsion, reactive oxygen and nitrogen species and ischemia-reperfusion injury. Mol Asp Med 25:199–210.  https://doi.org/10.1016/j.mam.2004.02.020 CrossRefGoogle Scholar
  8. Forlenza MJ, Miller GE (2006) Increased serum levels of 8-hydroxy-2′-deoxyguanosine in clinical depression. Psychosom Med 68:1–7.  https://doi.org/10.1097/01.psy.0000195780.37277.2a CrossRefPubMedGoogle Scholar
  9. Gholirad S, Razi M, Hassani Bafrani H (2016) Tracing of zinc and iron in experimentally induced varicocele: correlation with oxidative, nitrosative and carbonyl stress. Andrologia 49(6).  https://doi.org/10.1111/and.12687
  10. Gladden JD et al (2011) Novel insights into interactions between mitochondria and xanthine oxidase in acute cardiac volume overload. Free Radic Biol Med 51:1975–1984.  https://doi.org/10.1016/j.freeradbiomed.2011.08.022 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Gunther C, Neumann H, Neurath MF, Becker C (2013) Apoptosis, necrosis and necroptosis: cell death regulation in the intestinal epithelium. Gut 62:1062–1071.  https://doi.org/10.1136/gutjnl-2011-301364 CrossRefPubMedGoogle Scholar
  12. Khosravanian N, Razi M, Farokhi F, Khosravanian H (2014) Testosterone and vitamin E administration up-regulated varicocele-reduced Hsp70-2 protein expression and ameliorated biochemical alterations. J Assist Reprod Genet 31:341–354.  https://doi.org/10.1007/s10815-013-0165-0 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Kwon YK, Hecht NB (1991) Cytoplasmic protein binding to highly conserved sequences in the 3′ untranslated region of mouse protamine 2 mRNA, a translationally regulated transcript of male germ cells. Proc Natl Acad Sci U S A 88:3584–3588CrossRefPubMedPubMedCentralGoogle Scholar
  14. Lorenzini F, Tambara Filho R, Gomes RP, Martino-Andrade AJ, Erdmann TR, Matias JE (2012) Long-term effects of the testicular torsion on the spermatogenesis of the contralateral testis and the preventive value of the twisted testis orchiepididymectomy. Acta Cir Bras 27:388–395CrossRefPubMedGoogle Scholar
  15. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275PubMedGoogle Scholar
  16. McIlwain DR, Berger T, Mak TW (2013) Caspase functions in cell death and disease. Cold Spring Harb Perspect Biol 5:a008656.  https://doi.org/10.1101/cshperspect.a008656 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Molavi M, Razi M, Malekinejad H, Amniattalab A, Rezaie H (2014) Vitamin E improved cypermethrin-induced damages in the ovary of rats; evidence for angiogenesis and p53 involvement. Pestic Biochem Physiol 110:27–35.  https://doi.org/10.1016/j.pestbp.2014.02.004 CrossRefPubMedGoogle Scholar
  18. Nagakannan P, Shivasharan BD, Thippeswamy BS, Veerapur VP (2012) Effect of tramadol on behavioral alterations and lipid peroxidation after transient forebrain ischemia in rats. Toxicol Mech Methods 22:674–678.  https://doi.org/10.3109/15376516.2012.716092 CrossRefPubMedGoogle Scholar
  19. Niehaus WG Jr, Samuelsson B (1968) Formation of malonaldehyde from phospholipid arachidonate during microsomal lipid peroxidation. Eur J Biochem 6:126–130CrossRefPubMedGoogle Scholar
  20. Oberst A et al (2011) Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis. Nature 471:363–367.  https://doi.org/10.1038/nature09852 CrossRefPubMedPubMedCentralGoogle Scholar
  21. O'Donnell L (2014) Mechanisms of spermiogenesis and spermiation and how they are disturbed. Spermatogenesis 4:e979623.  https://doi.org/10.4161/21565562.2014.979623 CrossRefPubMedGoogle Scholar
  22. Okorie CO (2011) Unilateral testicular torsion with necrotic outcome: dilemmas of surgical timing. Urology 78:1232–1234.  https://doi.org/10.1016/j.urology.2011.08.059 CrossRefPubMedGoogle Scholar
  23. Pant N, Srivastava SP (2003) Testicular and spermatotoxic effects of quinalphos in rats. J Appl Toxicol 23:271–274.  https://doi.org/10.1002/jat.919 CrossRefPubMedGoogle Scholar
  24. Rerole AL, Jego G, Garrido C (2011) Hsp70: anti-apoptotic and tumorigenic protein. Methods Mol Biol 787:205–230.  https://doi.org/10.1007/978-1-61779-295-3_16 CrossRefPubMedGoogle Scholar
  25. Rezazadeh-Reyhani Z, Razi M, Malekinejad H, Sadrkhanlou R (2015) Cytotoxic effect of nanosilver particles on testicular tissue: evidence for biochemical stress and Hsp70-2 protein expression. Environ Toxicol Pharmacol 40:626–638.  https://doi.org/10.1016/j.etap.2015.08.024 CrossRefPubMedGoogle Scholar
  26. Sakai W, Sugasawa K (2014) FANCD2 is a target for caspase 3 during DNA damage-induced apoptosis. FEBS Lett 588:3778–3785.  https://doi.org/10.1016/j.febslet.2014.08.027 CrossRefPubMedGoogle Scholar
  27. Sarge KD, Cullen KE (1997) Regulation of hsp expression during rodent spermatogenesis. Cell Mol Life Sci 53:191–197CrossRefPubMedGoogle Scholar
  28. Shen S, Kepp O, Kroemer G (2012) The end of autophagic cell death? Autophagy 8:1–3.  https://doi.org/10.4161/auto.8.1.16618 CrossRefPubMedGoogle Scholar
  29. Takhtfooladi MA, Asghari A, Takhtfooladi HA, Shabani S (2015) The protective role of curcumin on testicular tissue after hindlimb ischemia reperfusion in rats. Int Urol Nephrol 47:1605–1610.  https://doi.org/10.1007/s11255-015-1101-2 CrossRefPubMedGoogle Scholar
  30. Turner TT, Brown KJ (1993) Spermatic cord torsion: loss of spermatogenesis despite return of blood flow. Biol Reprod 49:401–407CrossRefPubMedGoogle Scholar
  31. Turner TT, Bang HJ, Lysiak JJ (2005) Experimental testicular torsion: reperfusion blood flow and subsequent testicular venous plasma testosterone concentrations. Urology 65:390–394.  https://doi.org/10.1016/j.urology.2004.09.033 CrossRefPubMedGoogle Scholar
  32. Vigueras RM, Reyes G, Rojas-Castaneda J, Rojas P, Hernandez R (2004) Testicular torsion and its effects on the spermatogenic cycle in the contralateral testis of the rat. Lab Anim 38:313–320.  https://doi.org/10.3201/eid0905.020609 CrossRefPubMedGoogle Scholar
  33. Yurtcu M, Abasiyanik A, Avunduk MC, Muhtaroglu S (2008) Effects of melatonin on spermatogenesis and testicular ischemia-reperfusion injury after unilateral testicular torsion-detorsion. J Pediatr Surg 43:1873–1878.  https://doi.org/10.1016/j.jpedsurg.2008.01.065 CrossRefPubMedGoogle Scholar
  34. Zeiss CJ (2003) The apoptosis-necrosis continuum: insights from genetically altered mice. Vet Pathol 40:481–495CrossRefPubMedGoogle Scholar
  35. Zhang JQ, Hu XP, Kong XZ, Huang ML, Gou JM, Liu JH, Zhang XD (2009) Testis necrosis following repeated misdiagnosis of testicular torsion: a case report and literature review. Zhonghua Nan Ke Xue 15:445–448PubMedGoogle Scholar

Copyright information

© Cell Stress Society International 2017

Authors and Affiliations

  1. 1.Department of Basic Sciences, Faculty of Veterinary MedicineUrmia UniversityUrmiaIran
  2. 2.Department of Surgery and Diagnostic Imaging, Faculty of Veterinary MedicineUrmia UniversityUrmiaIran

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