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Sadat Kamali, F., Shahrooz, R., Najafi, G., & Razi, M. (2019). Ameliorative effects of crocin on paraquat-induced oxidative stress in testis of adult mice: An experimental study. International Journal of Reproductive BioMedicine (IJRM), 17(10), 807–818. https://doi.org/10.18502/ijrm.v17i10.5490
https://doi.org/10.18502/ijrm.v17i10.5490
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Fahime Sadat Kamali
Fahime Sadat Kamali
Department of Histology and Embryology, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran
-
Rasoul Shahrooz
Rasoul Shahrooz
Department of Histology and Embryology, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran
-
Golamreza Najafi
Golamreza Najafi
Department of Anatomy and Embryology, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran
-
Mazdak Razi
Mazdak Razi
Department of Histology and Embryology, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran
Published Date
- Nov 28, 2019
Ameliorative effects of crocin on paraquat-induced oxidative stress in testis of adult mice: An experimental study
Abstract
Background: Paraquat (PQ), as a pyridine compound, is widely used worldwide to control annual weeds. The oxidative stress caused by PQ can cause deleterious changes in the testicular tissue.
Objective: An investigation on the protective effects of Crocin (CCN) against PQinduced oxidative damages and apoptotic indices in testicular tissue.
Materials and Methods: Twenty-eight adult male albino mice (20-25 gr) were divided into four groups (n = 7/each). The control group received 0.1 ml/day of normal saline by intraperitoneal injection (IP); sham-control group received PQ 5 mg/kg/day, IP, and the experimental groups received PQ (CCN+PQ) and CCN-sole (200 mg/kg/day, IP), respectively, for 35 continuous days. At the end of the treatment period, the testes were dissected out and used for biochemical, molecular, and histological analyses. The expressions of tumor suppressor p53, B-cell lymphoma 2 (bcl-2), and caspase-3 were considered as hallmark factors of mitochondria-dependent apoptosis. Moreover, the testicular superoxide dismutase (SOD) and malondialdehyde (MDA) were evaluated as key biomarkers for oxidative stress.
Results: The PQ significantly (p < 0.02, p < 0.01) diminished the spermatogenesis indices and SOD, increased MDA levels, and enhanced the apoptosis-related gene expression. However, the co-administration of CCN and PQ significantly (p < 0.01, p < 0.01, p < 0.02) ameliorated the spermatogenesis ratio, upregulated the SOD level as well as bcl-2 expression, and reduced the MDA content and apoptosis vs the PQ-sole group.
Conclusion: This study showed that the antioxidant properties of CCN enable to ameliorate the PQ-induced destructive effects by upregulating the testicular structure, antioxidant and apoptotic status.
Key words: Histology, Testis, Paraquat, Crocin, Mice.
References
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[15] Shokri F, Shokoohi M, Niazkar HR, Roudi Rasht Abadi A, Kalarestaghi H, Ahin M. Investigation the Spermatogenesis and Testis Structure in diabetic rats after treatment with galega officinalis extract. Crescent Journal of Medical and Biological Sciences 2019; 6: 31–36.
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[18] Elumalai P, Gunadharini DN, Senthilkumar K, Banudevi S, Arunkumar R, Benson C, et al. Induction of apoptosis in human breast cancer cells by nimbolide through extrinsic and intrinsic pathway. Toxicol Lett 2012; 215: 131–142.
[19] Zhang Z, Wang CZ, Wen XD, Shoyama Y, Yuan CS. Role of saffron and its constituents on cancer chemoprevention. Pharm Biol 2013; 51: 920–924.
[20] Dianat M, Esmaeilizadeh M, Badavi M, Samarbaf-zadeh AR, Naghizadeh B. Protective effects of crocin on ischemia-reperfusion induced oxidative stress in comparison with vitamin E in isolated rat hearts. Jundishapur J Nat Pharm Prod 2014; 9: e17187.
[21] Talaei A, Hassanpour Moghadam M, Sajadi Tabassi SA, Mohajeri SA. Crocin, the main active saffron constituent, as an adjunctive treatment in major depressive disorder: a randomized, double-blind, placebo-controlled, pilot clinical trial. J Affect Disord 2015; 174: 51–56.
[22] Amin A, Bajbouj K, Koch A, Gandesiri M, Schneider- Stock R. Defective autophagosome formation in p53-null colorectal cancer reinforces crocin-induced apoptosis. Int J Mol Sci 2015; 16: 1544–1561.
[23] Farshid AA, Tamaddonfard E. Histopathological and behavioral evaluations of the effects of crocin, safranal and insulin on diabetic peripheral neuropathy in rats. Avic J Phytomed 2015; 5: 469–478.
[24] Bakhtiary Z, Shahrooz R, Ahmadi A, Zarei L. Evaluation of antioxidant effects of crocin on sperm quality in cyclophosphamide treated adult mice. Vet Res Forum 2014; 5: 213–218.
[25] Bakhtiary Z, Shahrooz R, Ahmadi A, Malekinejad H, Mostafavi M. Study of protective effects of crocin on testicular histomorphometryand serological parameters incyclophosphamide on treated adult mice. The Journal of Urmia University of Medical Sciences 2014; 25: 663–673.
[26] Kuter K, Nowak P, Golembiowska K, Ossowska K. Increased reactive oxygen species production in the brain after repeated low-dose pesticide paraquat exposure in rats. A comparison with peripheral tissues. Neurochem Res 2010; 35: 1121–1130.
[27] Nagababu E, Rifkind JM, Boindala S, Nakka L. Assessment of antioxidant activity of eugenol in vitro and in vivo. Methods Mol Biol 2010; 610: 165–180.
[28] Seevaratnam R, Patel BP, Hamadeh MJ. Comparison of total protein concentration in skeletal muscle as measured by the Bradford and Lowry assays. J Biochem 2009; 145: 791–797.
[29] Faião-Flores F, Coelho PR, Toledo Arruda-Neto JD, Maria- Engler SS, Tiago M, Capelozzi VL, et al. Apoptosis through Bcl-2/Bax and cleaved caspase up-regulation in melanoma treated by boron neutron capture therapy. PLoS One 2013; 8: e59639.
[30] Shamsi-Gamchi N, Razi M, Behfar M. Testicular torsion and reperfusion: evidences for biochemical and molecular alterations. Cell Stress Chaperones 2018; 23: 429–439.
[31] Ko EY, Sabanegh ESJr, Agarwal A. Male infertility testing: reactive oxygen species and antioxidant capacity. Fertil Steril 2014; 102: 1518–1527.
[32] Tremellen K. Oxidative stress and male infertility-a clinical perspective. Hum Reprod Update 2008; 14: 243–258.
[33] Agarwal A, Sharma RK, Sharma R, Assidi M, Abuzenadah AM, Alshahrani S, et al. Characterizing semen parameters and their association with reactive oxygen species in infertile men. Reprod Biol Endocrinol 2014; 12: 33.
[34] Shokoohi M, Shoorei H, Soltani M, Abtahi−Eivari SH, Salimnejad R, Moghimian M. Protective effects of the hydroalcoholic extract of Fumaria parviflora on testicular injury induced by torsion/detorsion in adult rats. Andrologia 2018; 50: e13047.
[35] Shokoohi M, Olad Saheb Madarek E, Khaki A, Shoorei H, Khaki AA, Soltani M, Ainehchi N. Investigating the effects of onion juice on male fertility factors and pregnancy rate after testicular torsion/detorsion by intrauterine insemination method. Int J Women’s Health Reprod Sci 2018; 6: 499–505.
[36] Khosravanian N, Razi M, Farokhi F, Khosravanian H. Testosterone and vitamin E administration up-regulated varicocele-reduced Hsp70-2 protein expression and ameliorated biochemical alterations. J Assist Reprod Genet 2014; 31: 341–354.
[37] Schieber M, Chandel NS. ROS function in redox signaling and oxidative stress. Curr Biol 2014; 24: R453–R462.
[38] Tiwari S, Tiwari S, Singh M, Singh A, Prasad SM. Generation mechanisms of reactive oxygen species in the plant cell: Boon or Bane - Revisiting the Role of ROS. Reactive Oxygen Species in Plants. London: John Wiley & Sons Ltd.; 2017. Chapter 49; p.1–22.
[39] Weydert CJ, Cullen JJ. Measurement of superoxide dismutase, catalase and glutathione peroxidase in cultured cells and tissue. Nat Protoc 2010; 5: 51–66.
[40] Dar RA, Brahman PK, Khurana N, Wagay JA, Lone ZA, Ganaie MA, et al. Evaluation of antioxidant activity of crocin, podophyllotoxin and kaempferol by chemical, biochemical and electrochemical assays. Arabian Journal of Chemistry 2017; 10: S1119–S1128.
[41] Subramaniam SR, Chesselet MF. Mitochondrial dysfunction and oxidative stress in Parkinson’s disease. Prog Neurobiol 2013; 106: 17–32.
[42] Ola MS, Nawaz M, Ahsan H. Role of Bcl-2 family proteins and caspases in the regulation of apoptosis. Mol Cell Biochem 2011; 351: 41–58.
[43] Khavarimehr M, Nejati V, Razi M, Najafi G. Ameliorative effect of omega-3 on spermatogenesis, testicular antioxidant status and preimplantation embryo development in streptozotocin-induced diabetes in rats. Int Urol Nephrol 2017; 49: 1545–1560.
[44] Liu D, Ou L, Clemenson GD Jr, Chao C, Lutske ME, Zambetti GP, et al. Puma is required for p53-induced depletion of adult stem cells. Nat Cell Biol 2010; 12: 993–998.
[2] Senarathna L, Eddleston M, Wilks MF, Woollen BH, Tomenson JA, Roberts DM, et al. Prediction of outcome after paraquat poisoning by measurement of the plasma paraquat concentration. QJM 2009; 102: 251–259.
[3] Gunnell D, Eddleston M, Phillips MR, Konradsen F. The global distribution of fatal pesticide self-poisoning: systematic review. BMC Public Health 2007; 7: 357.
[4] Ashoka DKHM, De Silva WAJP. Mechanism of paraquat action shows interference in spermatogenesis and epididymal maturation of sperm in mice. J Biol 2013; 01: 66– 76.
[5] Agarwal A, Sharma RK, Desai NR, Prabakaran S, Tavares A, Sabanegh E. Role of oxidative stress in pathogenesis of varicocele and infertility. Urology 2009; 73: 461–469.
[6] Schiefer HB, Irvine DG, Buzik SC. Understanding toxicology: Chemicals, their benefits and risks. CRC Press: New York; 1997.
[7] Tanner CM, Kamel F, Ross GW, Hoppin JA, Goldman SM, Korell M, et al. Rotenone, paraquat, and Parkinson’s disease. Environment Health Perspect 2011; 119: 866–872.
[8] Ossowska K, Śmiałowska M, Kuter K, Wierońska J, Zięba B, Wardas J, et al. Degeneration of dopaminergic mesocortical neurons and activation of compensatory processes induced by a long-term paraquat administration in rats: implications for Parkinson’s disease. Neuroscience 2006; 141: 2155–2165.
[9] Bus JS, Gibson JE. Paraquat: model for oxidant-initiated toxicity. Environm Health Perspect 1984; 55: 37–46.
[10] Karaguzel E, Kadihasanoglu M, Kutlu O. Mechanisms of testicular torsion and potential protective agents. Nat Rev Urol 2014; 11: 391–399.
[11] Aitken RJ, Roman SD. Antioxidant systems and oxidative stress in the testes. Oxid Med Cell Longev 2008; 1: 15–24.
[12] Kutikov A, Casale P, White MA, Meyer WA, Chang A, Gosalbez R, et al. Testicular compartment syndrome: a new approach to conceptualizing and managing testicular torsion. Urology 2008; 72: 786–789.
[13] Moghimian M, Soltani M, Abtahi H, Shokoohi M. Effect of vitamin c on tissue damage and oxidative stress following tunica vaginalis flap coverage after testicular torsion. J Pediatr Surg 2017; 52: 1651–1655.
[14] Moghimian M, Abtahi-Evari SH, Shokoohi M, Amiri M, Soltani M. Effect of Syzygium aromaticum (clove) extract on seminiferous tubules and oxidative stress after testicular torsion in adult rats. Physiol Pharmacol 2017; 21: 343–350.
[15] Shokri F, Shokoohi M, Niazkar HR, Roudi Rasht Abadi A, Kalarestaghi H, Ahin M. Investigation the Spermatogenesis and Testis Structure in diabetic rats after treatment with galega officinalis extract. Crescent Journal of Medical and Biological Sciences 2019; 6: 31–36.
[16] Fathi N, Hossinipanah M, Hajihossini M, Ranjbar A. Effects of paraquat on testicular histomorphometry of male rats. Biol Forum 2015; 7: 573–575.
[17] D’Souza UJ, Narayana K, Zain A, Raju S, Nizam HM, Noriah O. Dermal exposure to the herbicide-paraquat results in genotoxic and cytotoxic damage to germ cells in the male rat. Folia Morphol 2006; 65: 6–10.
[18] Elumalai P, Gunadharini DN, Senthilkumar K, Banudevi S, Arunkumar R, Benson C, et al. Induction of apoptosis in human breast cancer cells by nimbolide through extrinsic and intrinsic pathway. Toxicol Lett 2012; 215: 131–142.
[19] Zhang Z, Wang CZ, Wen XD, Shoyama Y, Yuan CS. Role of saffron and its constituents on cancer chemoprevention. Pharm Biol 2013; 51: 920–924.
[20] Dianat M, Esmaeilizadeh M, Badavi M, Samarbaf-zadeh AR, Naghizadeh B. Protective effects of crocin on ischemia-reperfusion induced oxidative stress in comparison with vitamin E in isolated rat hearts. Jundishapur J Nat Pharm Prod 2014; 9: e17187.
[21] Talaei A, Hassanpour Moghadam M, Sajadi Tabassi SA, Mohajeri SA. Crocin, the main active saffron constituent, as an adjunctive treatment in major depressive disorder: a randomized, double-blind, placebo-controlled, pilot clinical trial. J Affect Disord 2015; 174: 51–56.
[22] Amin A, Bajbouj K, Koch A, Gandesiri M, Schneider- Stock R. Defective autophagosome formation in p53-null colorectal cancer reinforces crocin-induced apoptosis. Int J Mol Sci 2015; 16: 1544–1561.
[23] Farshid AA, Tamaddonfard E. Histopathological and behavioral evaluations of the effects of crocin, safranal and insulin on diabetic peripheral neuropathy in rats. Avic J Phytomed 2015; 5: 469–478.
[24] Bakhtiary Z, Shahrooz R, Ahmadi A, Zarei L. Evaluation of antioxidant effects of crocin on sperm quality in cyclophosphamide treated adult mice. Vet Res Forum 2014; 5: 213–218.
[25] Bakhtiary Z, Shahrooz R, Ahmadi A, Malekinejad H, Mostafavi M. Study of protective effects of crocin on testicular histomorphometryand serological parameters incyclophosphamide on treated adult mice. The Journal of Urmia University of Medical Sciences 2014; 25: 663–673.
[26] Kuter K, Nowak P, Golembiowska K, Ossowska K. Increased reactive oxygen species production in the brain after repeated low-dose pesticide paraquat exposure in rats. A comparison with peripheral tissues. Neurochem Res 2010; 35: 1121–1130.
[27] Nagababu E, Rifkind JM, Boindala S, Nakka L. Assessment of antioxidant activity of eugenol in vitro and in vivo. Methods Mol Biol 2010; 610: 165–180.
[28] Seevaratnam R, Patel BP, Hamadeh MJ. Comparison of total protein concentration in skeletal muscle as measured by the Bradford and Lowry assays. J Biochem 2009; 145: 791–797.
[29] Faião-Flores F, Coelho PR, Toledo Arruda-Neto JD, Maria- Engler SS, Tiago M, Capelozzi VL, et al. Apoptosis through Bcl-2/Bax and cleaved caspase up-regulation in melanoma treated by boron neutron capture therapy. PLoS One 2013; 8: e59639.
[30] Shamsi-Gamchi N, Razi M, Behfar M. Testicular torsion and reperfusion: evidences for biochemical and molecular alterations. Cell Stress Chaperones 2018; 23: 429–439.
[31] Ko EY, Sabanegh ESJr, Agarwal A. Male infertility testing: reactive oxygen species and antioxidant capacity. Fertil Steril 2014; 102: 1518–1527.
[32] Tremellen K. Oxidative stress and male infertility-a clinical perspective. Hum Reprod Update 2008; 14: 243–258.
[33] Agarwal A, Sharma RK, Sharma R, Assidi M, Abuzenadah AM, Alshahrani S, et al. Characterizing semen parameters and their association with reactive oxygen species in infertile men. Reprod Biol Endocrinol 2014; 12: 33.
[34] Shokoohi M, Shoorei H, Soltani M, Abtahi−Eivari SH, Salimnejad R, Moghimian M. Protective effects of the hydroalcoholic extract of Fumaria parviflora on testicular injury induced by torsion/detorsion in adult rats. Andrologia 2018; 50: e13047.
[35] Shokoohi M, Olad Saheb Madarek E, Khaki A, Shoorei H, Khaki AA, Soltani M, Ainehchi N. Investigating the effects of onion juice on male fertility factors and pregnancy rate after testicular torsion/detorsion by intrauterine insemination method. Int J Women’s Health Reprod Sci 2018; 6: 499–505.
[36] Khosravanian N, Razi M, Farokhi F, Khosravanian H. Testosterone and vitamin E administration up-regulated varicocele-reduced Hsp70-2 protein expression and ameliorated biochemical alterations. J Assist Reprod Genet 2014; 31: 341–354.
[37] Schieber M, Chandel NS. ROS function in redox signaling and oxidative stress. Curr Biol 2014; 24: R453–R462.
[38] Tiwari S, Tiwari S, Singh M, Singh A, Prasad SM. Generation mechanisms of reactive oxygen species in the plant cell: Boon or Bane - Revisiting the Role of ROS. Reactive Oxygen Species in Plants. London: John Wiley & Sons Ltd.; 2017. Chapter 49; p.1–22.
[39] Weydert CJ, Cullen JJ. Measurement of superoxide dismutase, catalase and glutathione peroxidase in cultured cells and tissue. Nat Protoc 2010; 5: 51–66.
[40] Dar RA, Brahman PK, Khurana N, Wagay JA, Lone ZA, Ganaie MA, et al. Evaluation of antioxidant activity of crocin, podophyllotoxin and kaempferol by chemical, biochemical and electrochemical assays. Arabian Journal of Chemistry 2017; 10: S1119–S1128.
[41] Subramaniam SR, Chesselet MF. Mitochondrial dysfunction and oxidative stress in Parkinson’s disease. Prog Neurobiol 2013; 106: 17–32.
[42] Ola MS, Nawaz M, Ahsan H. Role of Bcl-2 family proteins and caspases in the regulation of apoptosis. Mol Cell Biochem 2011; 351: 41–58.
[43] Khavarimehr M, Nejati V, Razi M, Najafi G. Ameliorative effect of omega-3 on spermatogenesis, testicular antioxidant status and preimplantation embryo development in streptozotocin-induced diabetes in rats. Int Urol Nephrol 2017; 49: 1545–1560.
[44] Liu D, Ou L, Clemenson GD Jr, Chao C, Lutske ME, Zambetti GP, et al. Puma is required for p53-induced depletion of adult stem cells. Nat Cell Biol 2010; 12: 993–998.