DOI QR코드

DOI QR Code

Protective effects of curcumin on chromatin quality, sperm parameters, and apoptosis following testicular torsion-detorsion in mice

  • Shahedi, Abbas (Department of Biology and Anatomical Sciences, Research and Clinical Center for Infertility, Shahid Sadoughi University of Medical Sciences) ;
  • Talebi, Ali Reza (Department of Biology and Anatomical Sciences, Research and Clinical Center for Infertility, Shahid Sadoughi University of Medical Sciences) ;
  • Mirjalili, Aghdas (Department of Biology and Anatomical Sciences, Research and Clinical Center for Infertility, Shahid Sadoughi University of Medical Sciences) ;
  • Pourentezari, Majid (Department of Biology and Anatomical Sciences, Research and Clinical Center for Infertility, Shahid Sadoughi University of Medical Sciences)
  • Received : 2020.05.27
  • Accepted : 2020.09.15
  • Published : 2021.03.31

Abstract

Objective: The chief outcome of testicular torsion in clinical and experimental contexts is testicular ischemia. Curcumin, a compound with anti-inflammatory and antioxidant properties, has fascinated researchers and clinicians for its promise in the treatment of fertility diseases. Methods: Thirty-five fully grown male mice were randomly classified into five groups: control, sham, testicular torsion, treatment group 1 (testicular torsion+short-term curcumin), and treatment group 2 (testicular torsion+long-term curcumin). Thirty-five days later, spermatozoa from the right cauda epididymis were analyzed with regard to count and motility. Toluidine blue (TB), aniline blue (AB), and chromomycin A3 (CMA3) staining assays were used to evaluate the sperm chromatin integrity. In addition, the terminal deoxynucleotidyl transferase-mediated deoxyuridine triphosphate nick-end labeling (TUNEL) test was used to assess apoptosis. Results: Treatment group 1 exhibited a remarkably elevated sperm count compared to the testicular torsion group. Additionally, notably lower sperm motility was found in the testicular torsion group compared to the control, treatment 1, and treatment 2 groups. Staining (CMA3, AB, and TB) and the TUNEL test indicated significantly greater testicular torsion in the torsion group compared to the control group (p<0.05). The data also revealed notably lower results of all sperm chromatin assays and lower apoptosis in both treatment groups relative to the testicular torsion group (p<0.05). Significantly elevated (p<0.05) AB and TB results were noted in treatment group 1 compared to treatment group 2. Conclusion: Curcumin can compensate for the harmful effects of testicular ischemia and improve sperm chromatin quality in mice.

Keywords

References

  1. Schilling K, Toth B, Rosner S, Strowitzki T, Wischmann T. Prevalence of behaviour-related fertility disorders in a clinical sample: results of a pilot study. Arch Gynecol Obstet 2012;286:1307-14. https://doi.org/10.1007/s00404-012-2436-x
  2. Azizollahi S, Aflatoonian R, Sadighi Gilani MA, Behnam B, Tajik N, Asghari-Jafarabadi M, et al. Alteration of spermatogenesis following spermatogonial stem cells transplantation in testicular torsion-detorsion mice. J Assist Reprod Genet 2016;33:771-81. https://doi.org/10.1007/s10815-016-0708-2
  3. Yousefi-Manesh H, Shirooie S, Hemati S, Shokrian-Zeini M, Zarei N, Raoufi M, et al. Protective effects of modafinil administration on testicular torsion/detorsion damage in rats. Exp Mol Pathol 2019;111:104305. https://doi.org/10.1016/j.yexmp.2019.104305
  4. Anderson JB, Williamson RC. Testicular torsion in Bristol: a 25-year review. Br J Surg 1988;75:988-92. https://doi.org/10.1002/bjs.1800751015
  5. Turner TT, Lysiak JJ, Shannon JD, Nguyen QA, Bazemore-Walker CR. Testicular torsion alters the presence of specific proteins in the mouse testis as well as the phosphorylation status of specific proteins. J Androl 2006;27:285-93. https://doi.org/10.2164/jandrol.05134
  6. Nguyen L, Lievano G, Ghosh L, Radhakrishnan J, Fornell L, John E. Effect of unilateral testicular torsion on blood flow and histology of contralateral testes. J Pediatr Surg 1999;34:680-3. https://doi.org/10.1016/S0022-3468(99)90355-X
  7. Mellick LB, Sinex JE, Gibson RW, Mears K. A systematic review of testicle survival time after a torsion event. Pediatr Emerg Care 2019;35:821-5. https://doi.org/10.1097/pec.0000000000001287
  8. Wampler SM, Llanes M. Common scrotal and testicular problems. Prim Care 2010;37:613-26. https://doi.org/10.1016/j.pop.2010.04.009
  9. Shimizu S, Tsounapi P, Dimitriadis F, Higashi Y, Shimizu T, Saito M. Testicular torsion-detorsion and potential therapeutic treatments: a possible role for ischemic postconditioning. Int J Urol 2016; 23:454-63. https://doi.org/10.1111/iju.13110
  10. Filho DW, Torres MA, Bordin AL, Crezcynski-Pasa TB, Boveris A. Spermatic cord torsion, reactive oxygen and nitrogen species and ischemia-reperfusion injury. Mol Aspects Med 2004;25:199-210. https://doi.org/10.1016/j.mam.2004.02.020
  11. MacLeod J. The role of oxygen in the metabolism and motility of human spermatozoa. Am J Physiol Legacy Content 1943;138: 512-8. https://doi.org/10.1152/ajplegacy.1943.138.3.512
  12. Wagner H, Cheng JW, Ko EY. Role of reactive oxygen species in male infertility: an updated review of literature. Arab J Urol 2017;16:35-43. https://doi.org/10.1016/j.aju.2017.11.001
  13. Soleimanzadeh A, Saberivand A. Effect of curcumin on rat sperm morphology after the freeze-thawing process. Vet Res Forum 2013;4:185-9.
  14. Lee WH, Loo CY, Bebawy M, Luk F, Mason RS, Rohanizadeh R. Curcumin and its derivatives: their application in neuropharmacology and neuroscience in the 21st century. Curr Neuropharmacol 2013;11:338-78. https://doi.org/10.2174/1570159X11311040002
  15. Wal P, Saraswat N, Pal RS, Wal A, Chaubey M. A detailed insight of the anti-inflammatory effects of curcumin with the assessment of parameters, sources of ROS and associated mechanisms. Open Med J 2019;6:64-76. https://doi.org/10.2174/1874220301906010064
  16. Wei SM, Yan ZZ, Zhou J. Curcumin attenuates ischemia-reperfusion injury in rat testis. Fertil Steril 2009;91:271-7. https://doi.org/10.1016/j.fertnstert.2007.10.082
  17. Masuda T, Maekawa T, Hidaka K, Bando H, Takeda Y, Yamaguchi H. Chemical studies on antioxidant mechanism of curcumin: analysis of oxidative coupling products from curcumin and linoleate. J Agric Food Chem 2001;49:2539-47. https://doi.org/10.1021/jf001442x
  18. Kazemizadeh A, Zare Shahneh A, Zeinoaldini S, Yousefi AR, Mehrabani Yeganeh H, Ansari Pirsaraei Z, et al. Effects of dietary curcumin supplementation on seminal quality indices and fertility rate in broiler breeder roosters. Br Poult Sci 2019;60:256-64. https://doi.org/10.1080/00071668.2019.1571165
  19. Zhang L, Diao RY, Duan YG, Yi TH, Cai ZM. In vitro antioxidant effect of curcumin on human sperm quality in leucocytospermia. Andrologia 2017;49:e12760. https://doi.org/10.1111/and.12760
  20. Naz RK. Can curcumin provide an ideal contraceptive? Mol Reprod Dev 2011;78:116-23. https://doi.org/10.1002/mrd.21276
  21. Xia X, Cai H, Qin S, Xu C. Histone acetylase inhibitor curcumin impairs mouse spermiogenesis: an in vitro study. PLoS One 2012;7: e48673. https://doi.org/10.1371/journal.pone.0048673
  22. Ray D, Pitts PB, Hogarth CA, Whitmore LS, Griswold MD, Ye P. Computer simulations of the mouse spermatogenic cycle. Biol Open 2014;4:1-12. https://doi.org/10.1242/bio.20149068
  23. Sharma P, Aslam Khan I, Singh R. Curcumin and quercetin ameliorated cypermethrin and deltamethrin-induced reproductive system impairment in male Wistar rats by upregulating the activity of pituitary-gonadal hormones and steroidogenic enzymes. Int J Fertil Steril 2018;12:72-80. https://doi.org/10.22074/ijfs.2018.5160
  24. Pourentezari M, Talebi AR, Mangoli E, Anvari M, Rahimipour M. Additional deleterious effects of alcohol consumption on sperm parameters and DNA integrity in diabetic mice. Andrologia 2016; 48:564-9. https://doi.org/10.1111/and.12481
  25. Talebi AR, Sarcheshmeh AA, Khalili MA, Tabibnejad N. Effects of ethanol consumption on chromatin condensation and DNA integrity of epididymal spermatozoa in rat. Alcohol 2011;45:403-9. https://doi.org/10.1016/j.alcohol.2010.10.005
  26. Pourmasumi S, Khoradmehr A, Rahiminia T, Sabeti P, Talebi AR, Ghasemzadeh J. Evaluation of sperm chromatin integrity using aniline blue and toluidine blue staining in infertile and normozoospermic men. J Reprod Infertil 2019;20:95-101.
  27. Rahiminia T, Yazd EF, Fesahat F, Moein MR, Mirjalili AM, Talebi AR. Sperm chromatin and DNA integrity, methyltransferase mRNA levels, and global DNA methylation in oligoasthenoteratozoospermia. Clin Exp Reprod Med 2018;45:17-24. https://doi.org/10.5653/cerm.2018.45.1.17
  28. Kucuk N. Sperm DNA and detection of DNA fragmentations in sperm. Turk J Urol 2018;44:1-5. https://doi.org/10.5152/tud.2018.49321
  29. Petersen CG, Mauri AL, Vagnini LD, Renzi A, Petersen B, Mattila M, et al. The effects of male age on sperm DNA damage: an evaluation of 2,178 semen samples. JBRA Assist Reprod 2018;22:323-30.
  30. Kostakis ID, Zavras N, Damaskos C, Sakellariou S, Korkolopoulou P, Misiakos EP, et al. Erythropoietin and sildenafil protect against ischemia/reperfusion injury following testicular torsion in adult rats. Exp Ther Med 2017;13:3341-7. https://doi.org/10.3892/etm.2017.4441
  31. Ghasemnejad-Berenji M, Ghazi-Khansari M, Pashapour S, Jafari A, Yazdani I, Ghasemnejad-Berenji H, et al. Synergistic effect of rapamycin and metformin against germ cell apoptosis and oxidative stress after testicular torsion/detorsion-induced ischemia/reperfusion in rats. Biomed Pharmacother 2018;105:645-51. https://doi.org/10.1016/j.biopha.2018.06.012
  32. Ikebuaso AD, Yama OE, Duru FI, Oyebadejo SA. Experimental testicular torsion in a rat model: effects of treatment with Pausinystalia macroceras on testis functions. J Reprod Infertil 2012; 13:218-24.
  33. Agarwal A, Cho CL, Esteves SC, Majzoub A. Reactive oxygen species and sperm DNA fragmentation. Transl Androl Urol 2017; 6(Suppl 4):S695-6. https://doi.org/10.21037/tau.2017.05.40
  34. DaJusta DG, Granberg CF, Villanueva C, Baker LA. Contemporary review of testicular torsion: new concepts, emerging technologies and potential therapeutics. J Pediatr Urol 2013;9(6 Pt A):723-30. https://doi.org/10.1016/j.jpurol.2012.08.012
  35. Granger DN, Kvietys PR. Reperfusion injury and reactive oxygen species: the evolution of a concept. Redox Biol 2015;6:524-51. https://doi.org/10.1016/j.redox.2015.08.020
  36. Kim SM, Kim SK, Jee BC, Kim SH. Effect of sperm DNA fragmentation on embryo quality in normal responder women in in vitro fertilization and intracytoplasmic sperm injection. Yonsei Med J 2019;60:461-6. https://doi.org/10.3349/ymj.2019.60.5.461
  37. Aparnak P, Saberivand A. Effects of curcumin on canine semen parameters and expression of NOX5 gene in cryopreserved spermatozoa. Vet Res Forum 2019;10:221-6.
  38. Singh S, Aggarwal BB. Activation of transcription factor NF-kappa B is suppressed by curcumin (diferuloylmethane) [corrected]. J Biol Chem 1995;270:24995-5000. https://doi.org/10.1074/jbc.270.42.24995
  39. Khalaji N, Namyari M, Rasmi Y, Pourjabali M, Chodari L. Protective effect of curcumin on fertility of rats after exposure to compact fluorescent lamps: an experimental study. Int J Reprod Biomed 2018;16:447-54. https://doi.org/10.29252/ijrm.16.7.447
  40. Zha W, Bai Y, Xu L, Liu Y, Yang Z, Gao H, et al. Curcumin attenuates testicular injury in rats with streptozotocin-induced diabetes. Biomed Res Int 2018;2018:7468019. https://doi.org/10.1155/2018/7468019

Cited by

  1. The Role of Selected Natural Biomolecules in Sperm Production and Functionality vol.26, pp.17, 2021, https://doi.org/10.3390/molecules26175196
  2. Curcumin nanocrystals attenuate cyclophosphamide-induced testicular toxicity in mice vol.433, 2021, https://doi.org/10.1016/j.taap.2021.115772