Toxoplasma gondii: A Possible Inducer of Oxidative Stress in Reproductive System of Male Rats
Abstract
Background: Toxoplasmosis is suspected to have adverse effects on the male reproductive system. We aimed to determine the possible role of Toxoplasma gondii in oxidative stress in reproductive system of male rats. Methods: This study was performed from 2018 until 2019 at the Parasitology Re-search Laboratory of Hamadan University of Medical Sciences, Hamadan, Iran. Eighty male Wistar rats were randomly divided to control and test groups. The ani-mals in the test group were inoculated by 107 T. gondii RH strain tachyzoites and the control group were injected by 0.2 ml of phosphate-buffered saline. The both groups were following every 10 days until day 80 post inoculation. Oxidative stress markers (OSMs) including antioxidant enzymes such as superoxide dismutase (SOD), catalase (CAT) and non-enzymatic markers including malondialdehyde (MDA), reduced glutathione (GSH) and total antioxidant capacity (TAC) were as-sessed in testis and serum of T. gondii infected rats. Results: After post inoculation, the variations of the OSMs in the testis tissue of infected rats were as follows: a significant decrease of SOD on day 80 (P=0.03), and CAT activity were detected on day 60 and 80 (P=0.04 and P=0.01) respectively. In addition, GSH (P =0.01) and TAC (P =0.03) concentration were significantly re-duced on day 80. On the contrary, the concentration of MDA (P =0.01) was in-creased 70 days after infection. In addition, consistent changes with the tissue testis were observed in the serum OSMs of infected rats. Conclusion: T. gondii infection caused oxidative stress in testis tissue. Thus, the adverse effects of oxidative stress may affect the male rat reproductive system.
1. Elmore SA, Jones JL, Conrad PA, et al. Toxoplasma gondii: epidemiology, feline clinical aspects, and prevention. Trends Parasitol. 2010;26(4):190-6.
2. Xu X, He L, Zhang A, et al. Toxoplasma gondii isolate with genotype Chinese 1 triggers trophoblast apoptosis through oxidative stress and mitochondrial dysfunction in mice. Exp Parasitol. 2015;154:51-61.
3. Dubey JP. Toxoplasmosis of animals and humans: CRC press; 2016; https://doi.org/10.1201/9781420092370
4. Olariu TR, Press C, Talucod J, et al. ongenital toxoplasmosis in the United States: clinical and serologic findings in infants born to mothers treated during pregnancy. Parasite. 2019;26:13.
5. Ghasemi H, Khodadadi I, Fattahi A, et al. Polymorphisms of DNA repair genes XRCC1 and LIG4 and idiopathic male infertility. Syst Biol Reprod Med. 2017;63(6):382-90.
6. Agarwal A, Mulgund A, Hamada A, et al. A unique view on male infertility around the globe. Reprod Biol Endocrin. 2015;13:37.
7. Komijani M, Ghasemi SM, Shaykh-Baygloo N, et al. A systematic review on the role of infectious agents in female and male infertility. Urmia Medical Journal. 2018;29(4):295-304.
8. Zhou Y-H, Lu Y-J, Wang R-B, et al. Survey of infection of Toxoplasma gondii in infertile couples in Suzhou countryside. Zhonghua Nan Ke Xue. 2002;8(5):350-2.
9. Qi R, Su X, Gao X, et al. [Toxoplasma infection in males with sterility in Shenyang, China]. Zhonghua Nan Ke Xue. 2005;11(7):503-4.
10. Terpsidis KI, Papazahariadou MG, Taitzoglou IA, et al. Toxoplasma gondii: reproductive parameters in experimentally infected male rats. Exp Parasitol. 2009;121(3):238-41.
11. Lopes WDZ, Rodriguez JDA, Souza FA, et al. Sexual transmission of Toxoplasma gondii in sheep. Vet Parasitol. 2013;195(1-2):47-56.
12. Bahrami S, Shahriari A, Tavalla M, et al. Blood levels of oxidant/antioxidant parameters in rats infected with Toxoplasma gondii. Oxid Med Cell Longev. 2016;2016:8045969.
13. Al-Kennany E. Pathological study on the capability of Toxoplasma gondii to induce oxidative stress and initiation a primary lesion of atherosclerosis experimentally in broiler chickens. J Anim Vet Adv. 2007;6:938-42.
14. Silva F, Marques A, Chaveiro A. Reactive oxygen species: a double-edged sword in reproduction. Open Vet Sci J. 2010;4:127-33.
15. Nayak J, Jena SR, Samanta L. Oxidative Stress and Sperm Dysfunction: An Insight Into Dynamics of Semen Proteome. Oxidants, Antioxidants and Impact of the Oxidative Status in Male Reproduction: Elsevier; 2019;261-75.
16. Dubey J, Shen S, Kwok O, et al. Infection and immunity with the RH strain of Toxoplasma gondii in rats and mice. J Parasitol. 1999;85(4):657-62.
17. Erel O. A new automated colorimetric method for measuring total oxidant status. Clin Biochem. 2005;38(12):1103-11.
18. Riddles PW, Andrews RK, Blakeley RL, et al. Jack bean urease VI. Determination of thiol and disulfide content: reversible inactivation of the enzyme by the blocking of the unique cysteine residue. Biochim Biophys Acta. 1983;743(1):115-20.
19. Mohseni R, Sadeghabadi ZA, Goodarzi MT, et al. Evaluation of Mn-superoxide dismutase and catalase gene expression in childhood obesity: its association with insulin resistance. J Pediatr Endocrinol Metab. 2018;31(7):727-32.
20. Rostampour F, Ghasemi H, Mousavi-Bahar SH, et al. Total antioxidant capacity , lipid peroxidation, thiol group and catalase activity in patients with kidney stone. Avicenna J Med Biochem. 2017;5(2):60-4.
21. Motavalli M, Khodadadi I, Fallah M, et al. Effect of oxidative stress on vital indicators of Acanthamoeba castellanii (T4 genotype). Parasitol Res. 2018;117(9):2957-62.
22. Atmaca N, Cinar M, Güner B, et al. Evaluation of oxidative stress, hematological and biochemical parameters during Toxoplasma gondii infection in gerbils. Ankara Üniv Vet Fak Derg. 2015;62:165-70.
23. Bosch SS, Kronenberger T, Meissner KA, et al. Oxidative stress control by apicomplexan parasites. Biomed Res Int. 2015;2015:351289.
24. Abd Ellah MR. Involvement of free radicals in parasitic infestations. J Appl Anim Res. 2013;41(1):69-76.
25. Alscher RG, Erturk N, Heath LS. Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot. 2002;53(372):1331-41.
26. Sato K, Akaike T, Kohno M, et al. Hydroxyl radical production by H2O2 plus Cu, Zn-superoxide dismutase reflects the activity of free copper released from the oxidatively damaged enzyme. J Biol Chem. 1992;267(35):25371-7.
27. Alajmi RA, AL-Megrin WA, Metwally D, et al. Anti-Toxoplasma activity of silver nanoparticles green synthesized with Phoenix dactylifera and Ziziphus spina-christi extracts which inhibits inflammation through liver regulation of cytokines in Balb/c mice. Biosci Rep. 2019;39(5):BSR20190379.
28. Xuandong X, Ke O, Chongxing N. Determination of SOD activity and SOD isoenzymes in mice with experimental acute toxoplasmosis. Zhongguo Ren Shou Gong Huan Bing Za Zhi. 1998;3.
29. Kwok LY, Schlüter D, Clayton C, et al. The antioxidant systems in Toxoplasma gondii and the role of cytosolic catalase in defence against oxidative injury. Mol Microbiol. 2004;51(1):47-61.
30. Moreira-Souza ACA, Almeida-da-Silva CLC, Rangel TP, et al. The P2X7 receptor mediates Toxoplasma gondii control in macrophages through canonical NLRP3 inflammasome activation and reactive oxygen species production. Front Immunol. 2017;8:1257.
31. Kim JH, Lee J, Bae S-J, et al. NADPH oxidase 4 is required for the generation of macrophage migration inhibitory factor and host defense against Toxoplasma gondii infection. Sci Rep. 2017;7(1):6361.
32. Ríos J, Blasco B, Cervilla L, et al. Production and detoxification of H2O2 in lettuce plants exposed to selenium. Ann Appl Biol. 2008;154(1):107-16.
33. Dincel GC, Atmaca HT. Role of oxidative stress in the pathophysiology of Toxoplasma gondii infection. Int J Immunopathol Pharmacol. 2016;29(2):226-40.
34. Nagalakshmi N, Prasad M. Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Sci. 2001;160(2):291-9.
35. Karaman U, Celik T, Kiran TR, et al. Malondialdehyde, glutathione, and nitric oxide levels in Toxoplasma gondii seropositive patients. Korean J Parasitol. 2008;46(4):293-5.
36. Maryam Salehi M, Shirbazou S, Talebi-Meymand F. Evaluation of gender-related differences in response to oxidative stress in Toxoplasma gondii positive serum. AMHSR. 2014;12(2):64-9.
37. Ali WK, Umar FH, Aziz BN. Effect of Toxoplasma gondii Infestation on lipid peroxidation and certain antioxidants in pregnant women in Mosul City. AREJ. 2006;17(10):16-25.
38. Kratz E, Piwowar A. Melatonin, advanced oxidation protein products and total antioxidant capacity as seminal parameters of prooxidant-antioxidant balance and their connection with expression of metalloproteinases in context of male fertility. J Physiol Pharmacol 2017;68(5):659-68.
39. Lim A, Kumar V, Hari Dass SA, et al. Toxoplasma gondii infection enhances testicular steroidogenesis in rats. Mol Ecol. 2013;22(1):102-10.
40. Engin AB, Dogruman-Al F, Ercin U, et al. Oxidative stress and tryptophan degradation pattern of acute Toxoplasma gondii infection in mice. Parasitol Res. 2012;111(4):1725-30.
41. Zhang H-b, Shen Q-K, Wang H, et al. Synthesis and evaluation of novel arctigenin derivatives as potential anti-Toxoplasma gondii agents. Eur J Med Chem. 2018;158:414-27.
42. Dubey J. Pathogenicity and infectivity of Toxoplasma gondii oocysts for rats. J Parasitol. 1996;82(6):951-6.
43. Frenkel J. Pathogenesis of toxoplasmosis and of infections with organisms resembling Toxoplasma. Ann Ny Acad Sci. 1956;64(2):215-51.
44. Lewis WP, Markell EK. Acquisition of immunity to toxoplasmosis by the newborn rat. Exp Parasitol. 1958;7(5):463-7.
45. De Champs C, Pelloux H, Dechelotte P, et al. Toxoplasma gondii infection in rats by the RH strain: inoculum and age effects. Parasite. 1998;5(3):215-8.
2. Xu X, He L, Zhang A, et al. Toxoplasma gondii isolate with genotype Chinese 1 triggers trophoblast apoptosis through oxidative stress and mitochondrial dysfunction in mice. Exp Parasitol. 2015;154:51-61.
3. Dubey JP. Toxoplasmosis of animals and humans: CRC press; 2016; https://doi.org/10.1201/9781420092370
4. Olariu TR, Press C, Talucod J, et al. ongenital toxoplasmosis in the United States: clinical and serologic findings in infants born to mothers treated during pregnancy. Parasite. 2019;26:13.
5. Ghasemi H, Khodadadi I, Fattahi A, et al. Polymorphisms of DNA repair genes XRCC1 and LIG4 and idiopathic male infertility. Syst Biol Reprod Med. 2017;63(6):382-90.
6. Agarwal A, Mulgund A, Hamada A, et al. A unique view on male infertility around the globe. Reprod Biol Endocrin. 2015;13:37.
7. Komijani M, Ghasemi SM, Shaykh-Baygloo N, et al. A systematic review on the role of infectious agents in female and male infertility. Urmia Medical Journal. 2018;29(4):295-304.
8. Zhou Y-H, Lu Y-J, Wang R-B, et al. Survey of infection of Toxoplasma gondii in infertile couples in Suzhou countryside. Zhonghua Nan Ke Xue. 2002;8(5):350-2.
9. Qi R, Su X, Gao X, et al. [Toxoplasma infection in males with sterility in Shenyang, China]. Zhonghua Nan Ke Xue. 2005;11(7):503-4.
10. Terpsidis KI, Papazahariadou MG, Taitzoglou IA, et al. Toxoplasma gondii: reproductive parameters in experimentally infected male rats. Exp Parasitol. 2009;121(3):238-41.
11. Lopes WDZ, Rodriguez JDA, Souza FA, et al. Sexual transmission of Toxoplasma gondii in sheep. Vet Parasitol. 2013;195(1-2):47-56.
12. Bahrami S, Shahriari A, Tavalla M, et al. Blood levels of oxidant/antioxidant parameters in rats infected with Toxoplasma gondii. Oxid Med Cell Longev. 2016;2016:8045969.
13. Al-Kennany E. Pathological study on the capability of Toxoplasma gondii to induce oxidative stress and initiation a primary lesion of atherosclerosis experimentally in broiler chickens. J Anim Vet Adv. 2007;6:938-42.
14. Silva F, Marques A, Chaveiro A. Reactive oxygen species: a double-edged sword in reproduction. Open Vet Sci J. 2010;4:127-33.
15. Nayak J, Jena SR, Samanta L. Oxidative Stress and Sperm Dysfunction: An Insight Into Dynamics of Semen Proteome. Oxidants, Antioxidants and Impact of the Oxidative Status in Male Reproduction: Elsevier; 2019;261-75.
16. Dubey J, Shen S, Kwok O, et al. Infection and immunity with the RH strain of Toxoplasma gondii in rats and mice. J Parasitol. 1999;85(4):657-62.
17. Erel O. A new automated colorimetric method for measuring total oxidant status. Clin Biochem. 2005;38(12):1103-11.
18. Riddles PW, Andrews RK, Blakeley RL, et al. Jack bean urease VI. Determination of thiol and disulfide content: reversible inactivation of the enzyme by the blocking of the unique cysteine residue. Biochim Biophys Acta. 1983;743(1):115-20.
19. Mohseni R, Sadeghabadi ZA, Goodarzi MT, et al. Evaluation of Mn-superoxide dismutase and catalase gene expression in childhood obesity: its association with insulin resistance. J Pediatr Endocrinol Metab. 2018;31(7):727-32.
20. Rostampour F, Ghasemi H, Mousavi-Bahar SH, et al. Total antioxidant capacity , lipid peroxidation, thiol group and catalase activity in patients with kidney stone. Avicenna J Med Biochem. 2017;5(2):60-4.
21. Motavalli M, Khodadadi I, Fallah M, et al. Effect of oxidative stress on vital indicators of Acanthamoeba castellanii (T4 genotype). Parasitol Res. 2018;117(9):2957-62.
22. Atmaca N, Cinar M, Güner B, et al. Evaluation of oxidative stress, hematological and biochemical parameters during Toxoplasma gondii infection in gerbils. Ankara Üniv Vet Fak Derg. 2015;62:165-70.
23. Bosch SS, Kronenberger T, Meissner KA, et al. Oxidative stress control by apicomplexan parasites. Biomed Res Int. 2015;2015:351289.
24. Abd Ellah MR. Involvement of free radicals in parasitic infestations. J Appl Anim Res. 2013;41(1):69-76.
25. Alscher RG, Erturk N, Heath LS. Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot. 2002;53(372):1331-41.
26. Sato K, Akaike T, Kohno M, et al. Hydroxyl radical production by H2O2 plus Cu, Zn-superoxide dismutase reflects the activity of free copper released from the oxidatively damaged enzyme. J Biol Chem. 1992;267(35):25371-7.
27. Alajmi RA, AL-Megrin WA, Metwally D, et al. Anti-Toxoplasma activity of silver nanoparticles green synthesized with Phoenix dactylifera and Ziziphus spina-christi extracts which inhibits inflammation through liver regulation of cytokines in Balb/c mice. Biosci Rep. 2019;39(5):BSR20190379.
28. Xuandong X, Ke O, Chongxing N. Determination of SOD activity and SOD isoenzymes in mice with experimental acute toxoplasmosis. Zhongguo Ren Shou Gong Huan Bing Za Zhi. 1998;3.
29. Kwok LY, Schlüter D, Clayton C, et al. The antioxidant systems in Toxoplasma gondii and the role of cytosolic catalase in defence against oxidative injury. Mol Microbiol. 2004;51(1):47-61.
30. Moreira-Souza ACA, Almeida-da-Silva CLC, Rangel TP, et al. The P2X7 receptor mediates Toxoplasma gondii control in macrophages through canonical NLRP3 inflammasome activation and reactive oxygen species production. Front Immunol. 2017;8:1257.
31. Kim JH, Lee J, Bae S-J, et al. NADPH oxidase 4 is required for the generation of macrophage migration inhibitory factor and host defense against Toxoplasma gondii infection. Sci Rep. 2017;7(1):6361.
32. Ríos J, Blasco B, Cervilla L, et al. Production and detoxification of H2O2 in lettuce plants exposed to selenium. Ann Appl Biol. 2008;154(1):107-16.
33. Dincel GC, Atmaca HT. Role of oxidative stress in the pathophysiology of Toxoplasma gondii infection. Int J Immunopathol Pharmacol. 2016;29(2):226-40.
34. Nagalakshmi N, Prasad M. Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Sci. 2001;160(2):291-9.
35. Karaman U, Celik T, Kiran TR, et al. Malondialdehyde, glutathione, and nitric oxide levels in Toxoplasma gondii seropositive patients. Korean J Parasitol. 2008;46(4):293-5.
36. Maryam Salehi M, Shirbazou S, Talebi-Meymand F. Evaluation of gender-related differences in response to oxidative stress in Toxoplasma gondii positive serum. AMHSR. 2014;12(2):64-9.
37. Ali WK, Umar FH, Aziz BN. Effect of Toxoplasma gondii Infestation on lipid peroxidation and certain antioxidants in pregnant women in Mosul City. AREJ. 2006;17(10):16-25.
38. Kratz E, Piwowar A. Melatonin, advanced oxidation protein products and total antioxidant capacity as seminal parameters of prooxidant-antioxidant balance and their connection with expression of metalloproteinases in context of male fertility. J Physiol Pharmacol 2017;68(5):659-68.
39. Lim A, Kumar V, Hari Dass SA, et al. Toxoplasma gondii infection enhances testicular steroidogenesis in rats. Mol Ecol. 2013;22(1):102-10.
40. Engin AB, Dogruman-Al F, Ercin U, et al. Oxidative stress and tryptophan degradation pattern of acute Toxoplasma gondii infection in mice. Parasitol Res. 2012;111(4):1725-30.
41. Zhang H-b, Shen Q-K, Wang H, et al. Synthesis and evaluation of novel arctigenin derivatives as potential anti-Toxoplasma gondii agents. Eur J Med Chem. 2018;158:414-27.
42. Dubey J. Pathogenicity and infectivity of Toxoplasma gondii oocysts for rats. J Parasitol. 1996;82(6):951-6.
43. Frenkel J. Pathogenesis of toxoplasmosis and of infections with organisms resembling Toxoplasma. Ann Ny Acad Sci. 1956;64(2):215-51.
44. Lewis WP, Markell EK. Acquisition of immunity to toxoplasmosis by the newborn rat. Exp Parasitol. 1958;7(5):463-7.
45. De Champs C, Pelloux H, Dechelotte P, et al. Toxoplasma gondii infection in rats by the RH strain: inoculum and age effects. Parasite. 1998;5(3):215-8.
| Files | ||
| Issue | Vol 15 No 4 (2020) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijpa.v15i4.4857 | |
| Keywords | ||
| Toxoplasmosis Rat Oxidative Stress Superoxide dismutase Catalase Malondialdehyde Glutathione | ||
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How to Cite
1.
HOSEINY ASL NAZARLU Z, MATINI M, BAHMANZADEH M, FOROUGHI-PARVAR F. Toxoplasma gondii: A Possible Inducer of Oxidative Stress in Reproductive System of Male Rats. Iran J Parasitol. 2020;15(4):521-529.
