Document Type : Original Article

Authors

1 Department of Biology and Anatomical Sciences, Shahid Sadoughi University of Medical Sciences, Yazd, Iran

2 Department of Biology and Anatomical Sciences, Shahid Sadoughi University of Medical Sciences, Yazd, Iran Department of Reproductive Biology, Research and Clinical Center for Infertility, Shahid Sadoughi University of Medical Sciences, Yazd, Iran

Abstract

Background: The present study aimed to evaluate the sperm chromatin quality and rate of apoptosis in formaldehyde (FA)-exposed mice and the possible protective effects of curcumin (Cur) on the fertility potential of spermatozoa.
Methods: Twenty-four adult male NMRI mice were randomly divided into three groups: Group Ι (control), group ΙΙ (Sham) received Cur solvent (2 ml/day, intraperitoneal), group ΙΙΙ received FA (10 mg/kg, intraperitoneal), and group ΙV received FA+Cur (100 mg/kg, intraperitoneal). After 35 days, the spermatozoa from right cauda epididymis were analyzed using Chromomycin A3 (CMA3) and TUNEL staining.
Result: Regarding CMA3 and TUNEL tests, the data revealed a significant increase (p <0.05) in control and sham groups compared to the FA and FA+Cur groups. There was also a significant decrease in CMA3 tests and apoptosis in FA+Cur group compared to FA group (p <0.05).
Conclusion: Cur, as a potent antioxidant, can attenuate detrimental effects of FA on the chromatin quality and apoptosis in an experimental animal model.

Keywords

  1.  Sharpe RM, Irvine DS. How strong is the evidence of a link between environmental chemicals and adverse effects on human reproductive health? BMJ 2004; 328(7437):447-51. doi: 10.1136/bmj.328.7437.447.
  2. Sheiner EK, Sheiner E, Hammel RD, Potashnik G, Carel R. Effect of occupational exposures on male fertility: literature review. Ind Health 2003; 41(2):55-62. doi: 10.2486/indhealth.41.55.
  3. Working PK. Male reproductive toxicology: comparison of the human to animal models. Environ Health Perspect 1988; 77:37-44. doi: 10.1289/ehp.887737.
  4. Vaziri MH, Sadighi Gilani MA, Kavousi A, Firoozeh M, Khani Jazani R, Vosough Taqi Dizaj A, et al. The relationship between occupation and semen quality. Int J Fertil Steril 2011; 5(2):66-71.
  5. Ye X, Yan W, Xie H, Zhao M, Ying C. Cytogenetic analysis of nasal mucosa cells and lymphocytes from high-level long-term formaldehyde exposed workers and low-level short-term exposed waiters. Mutat Res 2005; 588(1):22-7. doi: 10.1016/j.mrgentox.2005.08.005.
  6. Gules O, Eren U. The effect of xylene and formaldehyde inhalation on testicular tissue in rats. Asian-Aust J Anim Sci 2010; 23(11):1412-20.
  7. WHO. Air quality guidelines for Europe. [cited 2020 Apr 17]: Available from: https://apps.who.int/iris/bitstream/handle/10665/107335/9789289013581-eng.pdf?sequence=1&isAllowed=y.
  8. Lu K, Boysen G, Gao L, Collins LB, Swenberg JA. Formaldehyde-induced histone modifications in vitro. Chem Res Toxicol 2008; 21(8):1586-93. doi: 10.1021/tx8000576.
  9. National Research Council. Review of the Environmental Protection Agency's Draft IRIS Assessment of Formaldehyde. Washington, DC: The National Academies Press; 2011.
  10. Zhou DX, Qiu SD, Zhang J, Tian H, Wang HX. The protective effect of vitamin E against oxidative damage caused by formaldehyde in the testes of adult rats. Asian J Androl 2006; 8(5):584-8. doi: 10.1111/j.1745-7262.2006.00198.x.
  11. Tan W, Deans AJ. Formaldehyde causes bone marrow failure linked to transcriptional reprogramming or metabolic deficiency. Mol Cell 2020; 80(6):935-7. doi: 10.1016/j.molcel.2020.11.042.
  12. Golalipour MJ, Azarhoush R, Ghafari S, Gharravi AM, Fazeli SA, Davarian A. Formaldehyde exposure induces histopathological and morphometric changes in the rat testis. Folia Morphol (Warsz) 2007; 66(3):167-71.
  13. Tang M, Xie Y, Yi Y, Wang W. Effects of formaldehyde on germ cells of male mice. Wei Sheng Yan Jiu 2003; 32(6):544-8. [In Chinese].
  14. Zhou DX, Qiu SD, Zhang J, Wang ZY. Reproductive toxicity of formaldehyde to adult male rats and the functional mechanism concerned. Sichuan Da Xue Xue Bao Yi Xue Ban 2006; 37(4):566-9. [In Chinese].
  15. Zare M, Haghpanah T, Shekari MA, Eftekhar-Vaghefi SH. The prophylactic effect of date palm (Phoenix dactylifera L.) fruit extract on testicular toxicity induced by formaldehyde: An experimental study. Int J Reprod Biomed 2020; 18(4):275-86. doi: 10.18502/ijrm.v13i4.6890.
  16. Manicardi GC, Tombacco A, Bizzaro D, Bianchi U, Bianchi PG, Sakkas D. DNA strand breaks in ejaculated human spermatozoa: comparison of susceptibility to the nick translation and terminal transferase assays. Histochem J 1998; 30(1):33-9. doi: 10.1023/a:1003214529185.
  17. Cortés-Gutiérrez E, Dávila-Rodríguez MI, López-Fernández C, Fernández JL, Gosálvez J. Evaluación del daño en el DNA espermático. Actas Urológicas Españolas 2007; 31(2):120-31. doi: 10.1016/S0210-4806(07)73609-4. [In Spanish].
  18. Ward WS. Deoxyribonucleic acid loop domain tertiary structure in mammalian spermatozoa. Biol Reprod 1993; 48(6):1193-201. doi: 10.1095/biolreprod48.6.1193.
  19. Balhorn R. A model for the structure of chromatin in mammalian sperm. J Cell Biol 1982; 93(2):298-305. doi: 10.1083/jcb.93.2.298.
  20. Ward WS, Coffey DS. DNA packaging and organization in mammalian spermatozoa: comparison with somatic cells. Biol Reprod 1991; 44(4):569-74. doi: 10.1095/biolreprod44.4.569.
  21. Amann RP. Can the fertility potential of a seminal sample be predicted accurately? J Androl 1989; 10(2):89-98. doi: 10.1002/j.1939-4640.1989.tb00066.x.
  22. Talebi AR, Fesahat F, Mangoli E, Ghasemzadeh J, Nayeri M, Sadeghian-Nodoshan F. Relationship between sperm protamine deficiency and apoptosis in couples with unexplained repeated spontaneous abortions. Int J Reprod Biomed 2016; 14(3):199-204.
  23. Sikka SC, Rajasekaran M, Hellstrom WJ. Role of oxidative stress and antioxidants in male infertility. J Androl 1995; 16(6):464-8.
  24. Sengupta P, Dutta S. Does SARS-CoV-2 infection cause sperm DNA fragmentation? Possible link with oxidative stress. Eur J Contracept Reprod Health Care 2020; 25(5):405-6. doi: 10.1080/13625187.2020.1787376.
  25. Dona G, Fiore C, Andrisani A, Ambrosini G, Brunati A, Ragazzi E, et al. Evaluation of correct endogenous reactive oxygen species content for human sperm capacitation and involvement of the NADPH oxidase system. Hum Reprod 2011; 26(12):3264-73. doi: 10.1093/humrep/der321.
  26. Oborna I, Malickova K, Fingerova H, Brezinova J, Horka P, Novotny J, et al. A randomized controlled trial of lycopene treatment on soluble receptor for advanced glycation end products in seminal and blood plasma of normospermic men. Am J Reprod Immunol 2011; 66(3):179-84. doi: 10.1111/j.1600-0897.2011.00984.x.
  27. Uz E, Söğüt S, Şahin Ş, Var A, Özyurt H, Güleç M, et al. The protective role of caffeic acid phenethyl ester (CAPE) on testicular tissue after testicular torsion and detorsion. World J Urol 2002; 20(4):264-70. doi: 10.1007/s00345-002-0259-2.
  28. Yurtçu M, Abasiyanik A, Avunduk MC, Muhtaroğlu S. Effects of melatonin on spermatogenesis and testicular ischemia-reperfusion injury after unilateral testicular torsion-detorsion. J Pediatr Surg 2008; 43(10):1873-8. doi: 10.1016/j.jpedsurg.2008.01.065.
  29. Can C, Töre F, Tunçel N, Uysal O, Gürer F, Ak D, et al. Protective effect of vasoactive intestinal peptide on testicular torsion-detorsion injury: association with heparin-containing mast cells. Urology 2004; 63(1):195-200. doi: 10.1016/j.urology.2003.08.010.
  30. Koc A, Narci A, Duru M, Gergerlioglu HS, Akaydin Y, Sogut S. The protective role of erdosteine on testicular tissue after testicular torsion and detorsion. Mol Cell Biochem 2005; 280(1-2):193-9. doi: 10.1007/s11010-005-8911-y.
  31. Ozturk A, Baltaci AK, Mogulkoc R, Ozturk B. The effect of prophylactic melatonin administration on reperfusion damage in experimental testis ischemia-reperfusion. Neuro Endocrinol Lett 2003; 24(3-4):170-2.
  32. Hamidian S, Talebi AR, Fesahat F, Bayat M, Mirjalili AM, Ashrafzadeh HR, et al. The effect of vitamin C on the gene expression profile of sperm protamines in the male partners of couples with recurrent pregnancy loss: A randomized clinical trial. Clin Exp Reprod Med 2020; 47(1): 68-76. doi: 10.5653/cerm.2019.03188.
  33. Jagetia GC. Radioprotection and radiosensitization by curcumin. Adv Exp Med Biol 2007; 595:301-20. doi: 10.1007/978-0-387-46401-5_13.
  34. Ammon HP, Wahl MA. Pharmacology of Curcuma longa. Planta Med 1991; 57(01):1-7. doi: 10.1055/s-2006-960004.
  35. Anand P, Sundaram C, Jhurani S, Kunnumakkara AB, Aggarwal BB. Curcumin and cancer: an “old-age” disease with an “age-old” solution. Cancer Lett 2008; 267(1):133-64.
  36. Sharma P, Singh R. Protective role of curcumin on lindane induced reproductive toxicity in male Wistar rats. Bull Environ Contam Toxicol 2010; 84(4):378-84. doi: 10.1007/s00128-010-9942-y.
  37. Giannessi F, Giambelluca MA, Grasso L, Scavuzzo MC, Ruffoli R. Curcumin protects Leydig cells of mice from damage induced by chronic alcohol administration. Med Sci Monit 2008; 14(11):BR237-42.
  38. Ilbey YO, Ozbek E, Cekmen M, Simsek A, Otunctemur A, Somay A. Protective effect of curcumin in cisplatin-induced oxidative injury in rat testis: mitogen-activated protein kinase and nuclear factor-kappa B signaling pathways. Hum Reprod 2009; 24(7):1717-25. doi: 10.1093/humrep/dep058.
  39. Verma RJ, Mathuria N. Effect of curcumin on aflatoxin-induced biochemical changes in testis of mice. Fertility and Sterility 2009; 91(2):597-601. doi: 10.1016/j.fertnstert.2007.11.053.
  40. El-Demerdash FM, Yousef MI, Radwan FM. Ameliorating effect of curcumin on sodium arsenite-induced oxidative damage and lipid peroxidation in different rat organs. Food Chem Toxicol 2009; 47(1):249-54. doi: 10.1016/j.fct.2008.11.013.
  41. Desai KR, Rajput DK, Patel PB, Highland HN. Ameliorative effects of curcumin on artesunate-induced subchronic toxicity in testis of Swiss albino male mice. Dose Response 2015; 13(2):1559325815592393. doi: 10.1177/1559325815592393.
  42. Tootian Z, Tajik P, Fazelipour S, Taghva M. Effect of Formaldehyde injection in mice on testis function. International Journal of Pharmacology 2007; 3:421-4. doi: 10.3923/ijp.2007.421.424.
  43. Momeni HR, Soleimani Mehranjani M, Eskandari N, Hemayatkhah Jahromi V. Protective effect of curcumin on testis histopathology in sodium arsenite-treated adult mice. Journal of Arak University of Medical Sciences 2014; 17(3):73-81. [In Persian].
  44. Kanter M, Aktas C, Erboga M. Curcumin attenuates testicular damage, apoptotic germ cell death, and oxidative stress in streptozotocin‐induced diabetic rats. Mol Nutr Food Res 2013; 57(9):1578-85. doi: 10.1002/mnfr.201200170.
  45. Bolt HM. Experimental toxicology of formaldehyde. J Cancer Res Clin Oncol 1987; 113(4):305-9. doi: 10.1007/BF00397713.
  46. Talebi A, Ghasemzadeh J, Khalili M, Halvaei I, Fesahat F. Sperm chromatin quality and DNA integrity in partial versus total globozoospermia. Andrologia 2018; 50(1). doi: 10.1111/and.12823.
  47. Khosrowbaki A. The role of oxidative stress in male infertility: A review. Journal of Arak University of Medical Sciences 2013; 15(9):94-103. [In Persian].
  48. Zhou D, Zhang J, Wang H. Assessment of the potential reproductive toxicity of long-term exposure of adult male rats to low-dose formaldehyde. Toxicol Ind Health 2011; 27(7):591-8. doi: 10.1177/0748233710393401.
  49. Wang HX, Zhou DX, Zheng LR, Zhang J, Huo YW, Tian H, et al. Effects of paternal occupation exposure to formaldehyde on reproductive outc. J Occup Environ Med 2012; 54(5):518-24. doi: 10.1097/JOM.0b013e31824e6937.
  50. Duong A, Steinmaus C, McHale CM, Vaughan CP, Zhang L. Reproductive and developmental toxicity of formaldehyde: a systematic review. Mutat Res 2011; 728(3):118-38. doi: 10.1016/j.mrrev.2011.07.003.
  51. Betancourt-Martínez ND, Jiménez-Villarreal J, Carranza-Rosales P, Guzmán-Delgado NE, Leyva Orasma C, Viveros Valdez E, et al. Sperm chromatin dispersion by formaldehyde in Wistar rats. Genet Mol Re 2015; 14(3):10816-26. doi: 10.4238/2015.September.9.20.
  52. Noorafshan A, Karbalay-Doust S, Valizadeh A, Aliabadi E. Ameliorative effects of curcumin on the structural parameters of seminiferous tubules and Leydig cells in metronidazole-treated mice: a stereological approach. Experimental and Toxicologic Pathology 2011; 63(7-8):627-33. doi: 10.1016/j.etp.2010.05.004.
  53. Rashid K, Sil PC. Curcumin ameliorates testicular damage in diabetic rats by suppressing cellular stress-mediated mitochondria and endoplasmic reticulum-dependent apoptotic death. Biochim Biophys Acta 2015; 1852(1):70-82. doi: 10.1016/j.bbadis.2014.11.007.
  54. Noorafshan A, Karbalay-Doust S, Valizadeh A, Aliabadi E, Mirkhani H. Ameliorative effects of curcumin on the seminiferous epithelium in metronidazole-treated mice: a stereological study. Toxicol Pathol 2010; 38(3):366-71. doi: 10.1177/0192623310362248.
  55. 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 2018:7468019. doi: 10.1155/2018/7468019.
  56. Karimi S, Khorsandi L, Nejaddehbashi F. Protective effects of Curcumin on testicular toxicity induced by titanium dioxide nanoparticles in mice. JBRA Assist Reprod 2019; 23(4):344-51. doi: 10.5935/1518-0557.20190031.
  57. Mahmoudi R, Honarmand Z, Karbalay-Doust S, Jafari-Barmak M, Nikseresht M, Noorafshan A. Using curcumin to prevent structural impairments of testicles in rats induced by sodium metabisulfite. EXCLI J 2017; 16:583-92. doi: 10.17179/excli2017-143.
  58. Cheraghi E, Golkar A, Roshanaei K, Alani B. Aluminium-induced oxidative stress, apoptosis and alterations in testicular tissue and sperm quality in Wistar rats: ameliorative effects of curcumin. Int J Fertil Steril 2017; 11(3):166-175. doi: 10.22074/ijfs.2017.4859.