اثر آستاگزانتین بر آسیب القاءشده توسط کلرید کادمیوم در بیضهء موش‌صحرایی نر بالغ نژاد ویستار
محورهای موضوعی : آسیب شناسی درمانگاهی دامپزشکیمهوش حافظ‌امینی 1 , اکرم عیدی 2 , سید پژمان مرتضوی 3 , فتاح ستوده نژاد نعمت الهی 4
1 - دانش‌آموخته دکتری تخصصی فیزیولوژی، گروه زیست‌شناسی، واحد علوم و تحقیقات، دانشگاه آزاد اسلامی، تهران، ایران.
2 - استاد گروه زیست شناسی، واحد علوم و تحقیقات، دانشگاه آزاد اسلامی، تهران، ایران.
3 - دانشیار گروه پاتولوژی، دانشکده دامپزشکی، واحدعلوم و تحقیقات، دانشگاه آزاد اسلامی، تهران، ایران.
4 - استادیار گروه زیست شناسی، واحدعلوم و تحقیقات، دانشگاه آزاد اسلامی، تهران، ایران
کلید واژه: آستاگزانتین, موش صحرایی, بیضه, آسیب, کلرید کادمیوم,
چکیده مقاله :
نقش حفاظتی آستاگزانتین بر سلامتی انسان، از جمله پیشگیری از بیماری‌های قلبی- عروقی و جلوگیری از روند پیرشدن سلول‌ها، اشاره به خاصیت آنتی‌اکسیدانی بسیار قوی این ماده دارد. کادمیوم یکی از آلاینده‌های موجود در اکوسیستم ها است. این فلز سنگین به عنوان یک توکسین بر سیستم تولیدمثل اثر گذاشته و سبب تخریب روند اسپرماتوژنز در بافت بیضه می شود. هدف مطالعه حاضر، بررسی تأثیر آستاگزانتین بر آسیب بیضه ای القاءشده توسط کلرید کادمیوم در موش صحرایی بود. بدین منظور، تعداد ۴۵ سر موش صحرایی نر بالغ نژاد ویستار به صورت تصادفی به ۹ گروه تقسیم شدند. گروه کنترل سالم هیچ گونه تیماری دریافت نکرد. گروه شاهد، سرم فیزیولوژی، گروه کنترل نابارور، کلرید کادمیوم (به میزان 1 میلی گرم بر کیلوگرم وزن) به صورت تزریق درون صفاقی، 3 گروه آستاگزانتین را با دوزهای 5، ۱۰ و ۲۰ میلی گرم بر کیلوگرم وزن و 3 گروه هم همزمان کلرید کادمیوم و آستاگزانتین را با دوزهای 5، ۱۰ و ۲۰ میلی گرم بر کیلوگرم به صورت گاواژ دریافت کردند. از هموژنات بافت بیضه جهت سنجش پارامترهای استرس اکسیداتیو، به عنوان نمونه‌های آزمون استفاده شد. پارامترهای مورد نظر به روش فتومتریک با دستگاه الایزا ریدر و میکروپلیت ریدر بررسی شد. آستاگزانتین با مقادیر 10 و 20 میلی‌گرم بر کیلوگرم وزن، موجب افزایش آنزیم های آنتی اکسیدانی سوپراکسید دیسموتاز، گلوتاتیون پراکسیداز و کاتالاز و همچنین کاهش میزان مالون‌دی‌آلدئید شد (001/0p). بنابراین، آستاگزانتین احتمالاً به عنوان یک آنتی اکسیدان در محافظت از بیضه موش صحرایی در برابر استرس اکسیداتیو ناشی از کلرید کادمیوم عمل می کند.
چکیده انگلیسی:
The protective role of astaxanthin on human health, including the prevention of cardiovascular disease, prevention of cell aging, refers to the very strong antioxidant properties of this substance. Cadmium is one of the pollutants in ecosystems. This heavy metal acts as a toxin on the reproductive system and destroys the process of spermatogenesis in testicular tissue. The aim of this study was to evaluate the effect of astaxanthin on cadmium chloride induced testicular damage in adult male Wistar rats. In this study, 45 rats were randomly divided into 9 groups. The healthy control group did not receive any treatment. Control group, physiological serum, infertile control group, cadmium chloride (1 mg / kg body weight) by intraperitoneal injection, astaxanthin receiving groups (5, 10 and 20 mg / kg body weight) by gavage and groups They received cadmium chloride and astaxanthin (5, 10 and 20 mg / kg) at the same time. Test samples from testicular tissue homogenates were used to measure oxidative stress parameters. The parameters were analyzed by photometric method with ELISA reader and microplate reader. The results showed that astaxanthin (10 and 20 mg / kg body weight) increased the antioxidant enzymes SOD, GPX and CAT and astaxanthin (10 mg / kg body weight) decreased MDA. Thus, astaxanthin may act as an antioxidant in protecting the rat testis against oxidative stress induced by cadmium chloride.
منابع و مأخذ:
Ahmadi, Z. and Ashrafizadeh, M. (2018). Downregulation of osteocalcin gene in chickens treated with lead acetate II. International Biological and Biomedical Journal, 4(4): 177-182.
Acosta, I.B., Junior, A.S.V., EF, E.S., Cardoso, T.F., Caldas, J.S., Jardim, R.D., et al. (2016). Effects of exposure to cadmium in sperm cells of zebrafish. Toxicology Reports, 3(1): 696-700.
Agarwal, A., Prabakaran, S. and Said, T. (2005). Prevention of oxidative stress injury to sperm. Journal of Andrology, 26(6): 654-660.
Agarwal, A., Virk, G., Ong, C. and Du Plessis, S. (2014). Effect of oxidative stress on male The World Journal of Men's Health, 32(1): 1-17.
Aitken, R.J. (1997). Molecular mechanisms regulating human sperm function. Molecular Human Reproduction, 3(3): 169-173.
Andrisani, A., Dona, G., Tibaldi, E., Maria Brunati, A., Sabbadin, C.H., Armanini, D., et al. (2015). Astaxanthin improves human sperm capacitation by inducing lyn displacement and activation. Marine Drugs, 13(9): 5533-5551.
Alkhedaide, A., Alshehri, Z.S., Sabry, A., Abdel-Ghaffar, T., Soliman, M.M. and Attia. H. (2016). Protective effect of grape seed extract against cadmium-induced testicular dysfunction. Molecular Medicine Reports, 13(4): 3101-3109.
Alvarez, J.G., Touchtone, J., Touchstone J.C., Blasco, L. and Storey, B. (1987). Spontaneous lipid peroxidation and production of hydrogen peroxide and superoxide in human spermatozoa superoxide dismutase as major enzyme protectant against oxygen toxicity. Journal of Andrology, 8(5): 338-348.
Amara, S., Abdelmelek, H., Garrel, C., Guiraud, P., Douki, T., Ravanat, J.L., et al. (2008). Preventive effect of zinc against cadmium-induced oxidative stress in the rat testis. Development & Reproduction, 54(2): 129-134.
Aprioku, J.S., (2013). Pharmacology of free radicals and the impact of reactive oxygen species on the testis. Journal of Reproduction and Infertility, 14(4): 158-172.
Asadi, N. (2017). The impact of oxidative stress on testicular function and the role of antioxidants in improving it: a review. Journal of Clinical and Diagnostic Research: JCDR, 11(5): 1-5.
Asghari, M.H., Moloudizargari, M., Bahadar, H. and Abdollahi, M. (2016). A review of the protective effect of melatonin in pesticide-induced toxicity. Expert Opinion on Drug Metabolism and Toxicology, 13(5): 545-554.
Ashrafizadeh, M. and Ahmadi, Z. (2019). Effect of Astaxanthin treatment on the sperm quality of the mice treated with nicotine. Reviews in Clinical Medicine, 6(1): 1-5.
Bahmanzadeh, M., Vahidnia, A., Mahdinejadiani, S.H., Shokri, S. and Alizadeh, Z. (2016). Dietary supplementation with astaxanthin may ameliorate sperm parameters and DNA integrity in streptozotocin-induced diabetic rats. Clinical and Experimental Reproductive Medicine, 43(2): 90-96.
Baninameh, Z., Moloudizargari, M., Ghasemnejad Berenji, H., Rezaie Chamani, S., Hassanzadeh, V., Ferrante, M., et al. (2016). Urtica dioica attenuate effect of doxorubicin-induced changes on sperm parameters in the International Journal of Medical Research and Health Sciences, 5(11): 116-121.
Bauer, R., Demeter, I., Hasemann, V. and Johansen, J.T. (1980). Structural properties of the zinc site in Cu,Znsuperoxide dismutase; perturbed angular correlation of gamma ray spectroscopy on the Cu, 111Cd-superoxide dismutase derivative. Biochemical and Biophysical Research Communications, 94(4): 1296-1302.
Borowitzka, M.A. (1999). Commercial production of microalgae: ponds, tanks, tubes and fermentors. Journal of Biotechnology, 70(1): 313-321.
Caslino, E., Sblano, C. and Landriscina, C. (1997). Enzyme activity alteration by cadmium administration to rats: the possibility of iron involuement in lipid peroxidation. Archives of Biochemistry and Biophysics, 346(2): 171-179.
Dhankhar, J., Kadiad, S. and Sharma, A. (2012). Astaxanthin: A potential carotenoid. International Journal of Pharmaceutical Sciences and Research, 3(5): 1246.
Dokumacioglu, E., Iskender, H., Yenice, , Kapakin, K.A.T., Sevim, C., Hayirli, A., et al. (2018). Effects of astaxanthin on biochemical and histopathological parameters related to oxidative stress on testes of rats on high fructose regime. Andrologia, 50(7): 1-10.
Farhangdoost, F., JafariBarmak, M., Hemayatkhah Jahromi, V., Azizi, A., Mahmoodi, R., et al. (2013). Aloe vera extract effect on sperm quality and testicular tissue of rats induced by cadmium chloride. Armaghane-Danesh, 19(1): 47-55.
Fatahian Dehkordi, R., Alijani, M.R., Rahimi Junqani, R. and Bahadoran, Sh. (2020). The effects of pomegranate skin extract and powder on renal tissue structure following experimental cadmium poisoning in Japanese quail. Veterinary Clinical Pathology, 14(53): 37-50. [In Persian]
Fukuzawa, K. (2000). Singlet oxygen scavenging in phospholipid membranes. Methods in Enzymology, 319(10): 101-110.
Gharagozloo, P. and Aitken, R.J. (2011). The role of sperm oxidative stress in male infertility and the significance of oral antioxidant therapy. Human Reproduction, 26(7): 1628-1640.
Ghavidel Aghdam, E., Narimani Rad, M. and Lotfi, A. (2016). Effects of silver nanoparticles synthesized through chemical reduction on plasma superoxide dismutase and glutathione peroxidase enzymes in rat model. Journal of Veterinary Clinical Pathology, 10(37): 69-80. [In Persian]
Gil-Guzman, E., Ollero, M., Lopez, M.C., Sharma, R.K., Alvarez, J.G., Thomas, Jr, A.J., et al. (2001). Differential production of reactive oxygen species by subsets of human spermatozoa at different stages of maturation. Human Reproduction, 16(9): 1922-1930.
Goto, S., Kogure, K., Abe, K., Kimata, Y., Kitahama, K., Yamashita, E., et al. (2001). Efficient radical trapping at the surface and inside the phospholipid membrane is responsible for highly potent antiperoxidative activity of the carotenoid Biochemical and Biophysical Acta (BBA)-Biomembranes, 1512(2): 251-258.
Hassanpour, H., Bigham Sadegh, A., Karimi, I., Heidari Khoei, H., Karimi, A., Edalati Shaarbaf, P., et al. (2017). Comparative expression analysis of HSP70, HSP90, IL-4, TNF, KITLG and KIT-receptor gene between varicocele-induced and non-varicocele testes of International Journal of Fertility and Sterility, 11(3): 148-155.
Heidari Khoei, H., Fakhri, S., Parvardeh, S., Shams Mofarahe, Z., Baninameh, Z. and Vardiani, M. (2018a). Astaxanthin prevents the methotrexateinduced reproductive toxicity by targeting oxidative stress in male mice. Toxin Reviews, 38(4): 1-7.
Heidari Khoei, H., Fakhri, S., Parvardeh, S., Shams Mofarahe, Z., Ghasemnejad-Berenji, H., Nazarian, H., et al. (2018b). Testicular toxicity and reproductive performance of streptozotocin-induced diabetic male rats: the ameliorating role of silymarin as an antioxidant. Toxin Reviews, 38(3): 223-233.
Ibrahim, S.F., Osman, K., Das, S, Mazni Othman, A., Abdul Majid, N. and Abdul Rahman, M.P. (2008). A study of the antioxidant effect of alpha lipoic acids on sperm quality. Clinics (Sao Paulo), 63(4): 545-550.
Jamalan, M., Ghaffari, M.A., Hoseinzadeh, P., Hashemitabar, M. and Zeinali, M. (2016). Human sperm quality and metal toxicants: protective effects of some flavonoids on male reproductive function. International Journal of Fertility and Sterility, 10(2): 215-223.
Jamshidi, N., Asghari, A., Neshat, M. and Mortazavi, P. (2016). Effects of magnesium sulfate administration on ischemia-reperfusion kidney in rat. Veterinary Journal (Pajouhesh & Sazandegi), 115(1): 63-75.
Jiang, X., Chen, L., Shen, L., Chen, Z., Xu, L., Zhang, J. and Yu, X. (2016). Trans-astaxanthin attenuates lipopolysaccharide-induced neuroinflammation and depressive-like behavior in mice. Brain Research Journal, 1649(1): 30-37.
Kadivar, A., Heidari Khoei, H., Hassanpour, H., Ghanaei, H., Golestanfar, A., Mehraban, H., et al. (2016). Peroxisome proliferator-activated receptors (PPARa, PPARc and PPARb/d) gene expression profile on ram spermatozoa and their relation to the sperm Veterinary Research Forum, 7(1): 27-34.
Kara, H., Cevik, A., Konar, V., Dayangac, A. and Yilmaz, M. (2007). Protective effects of antioxidants against cadmium-induced oxidative damage in rat testes. Biological Trace Element Research, 120(1-3): 205-211.
Kidd, P. (2011). Astaxanthin, cell membrane nutrient with diverse clinical benefits and anti-aging potential. Alternative Medicine Review, 16 (4): 355-364.
Koyuturk, M., Yanardag, R., Bolkent, S. and Tunali, S. (2006). Influence of combined antioxidants against cadmium induced testicular damage. Environmental Toxicology and Pharmacology, 21(3): 235-240.
Li, Y., Wu, J., Zhou, W. and Gao, J. (2016). Association between environmental exposure to cadmium and human semen quality. International Journal of Environmental Health Research, 26(2): 175-186.
Mansour, N., McNiven, M.A. and Richardson, G.F. (2006). The effect of dietary supplementation with blueberry, alpha-tocopherol or astaxanthin on oxidative stability of Arctic char (Salvelinus Alpinus) semen. Theriogenology, 66(2): 373-382.
Massanyi, P., Weis, J., Lukac, N., Trandzik, J. and Bystricka, J. (2008). Cadmium, zinc, copper, sodium and potassium concentrations in rooster and turkey semen and their correlation. Journal of Environmental Science and Health, 43(5): 563-565.
Mohammadi Roushandeh, A., Salehi, I. and Mortazavi, M. (2015). Protective Effects of Restricted Diet and Antioxidants on Testis Tissue in Rats Fed with High-Fat Diet. Iranian Biomedical Journal, 19(2): 96-101.
Mohammadnejad, D., Soleimani rad, J. and Mohammadi-roshandeh, A. (2013). Preventive effects of Cetrorelix on the changes induced by Cisplatin on spermatogenic and myoid cells and basal lamina of seminiferous ducts in the testis of Balb/C mouse. Journal of Veterinary Clinical Pathology, 6(4): 1665-1674. [In Persian]
Mortazavi, M., Salehi, I., Alizadeh, Z., Vahabian,M. and Mohammadi Roushandeh, A. (2014). Protective Effects of Antioxidants on Sperm Parameters and Seminiferous Tubules Epithelium in High Fat-fed Rats. Journal of Reproduction & Infertility, 15(1): 22-28.
Naguib, Y.M. (2000). Antioxidant activities of astaxanthin and related carotenoids. Journal of agricultural and Food Chemistry, 48(4): 1150-1154.
Ognjanovic_c, B. I., Markovi_c, S.D., ĐorCevi_c, N.Z., Trbojevi_c, I.S., Stajn, A.S. and Sai_ci_c, Z.S. (2010). Cadmium-induced lipid peroxidation and changes in antioxidant defense system in the rat testes: protective role of coenzyme Q 10 and Vitamin E. Reproductive Toxicology, 29(2): 191-197.
Orisakwe, O. (2014). Lead and cadmium in public health in Nigeria: physicians neglect and pitfall in patient management. North American Journal of Medicine and Science, 6(2): 61-71.
Rafiei, H. and Ashrafizadeh, M. (2018). Expression of Collagen Type II and Osteocalcin Genes in Mesenchymal Stem Cells from Rats Treated with Lead acetate II. Iranian Journal of Toxicology, 12(5): 35-40.
Rasulifar, M.H. and Zargari F. (2015). The effect of aqueous extract of white tea on serum levels of antioxidant enzymes in mice Field exposed to arsenic. Journal of Veterinary Clinical Pathology, 9(2): 153-161. [In Persian]
Sen Gupta, R., Sen Gupta, E., Dhakal, B.K. and Thakur Ahnn, J. (2004). Vitamin C and vitamin E protect the rat testes from cadmium-induced reactive oxygen species. Molecules and Cells, 17(1): 132-139.
Siu, E.R., Mruk, D.D., Porto, C.S. and Cheng, C.Y. (2009). Cadmium-induced testicular injury. Toxicology and Applied Pharmacology, 238(3): 240-249.
Sayed, M.M., Hassanein, K.M.A. and Senosy, W. (2014). Protective effects of thymoquinone and l-cysteine on cadmium-induced reproductive toxicity in rats. Reproductive Toxicology Journal, 13(1): 612-620.
Tandon, S. K., Singh, S., Prasad, S., Khandekar, K., Dwivedi, V.K., Chatterjee, M., et al. (2003). Reversal of cadmium induced oxidative stress by chelating agent, antioxidant or their combination in rat. Toxicology Letters Journal, 145(3): 211-217.
Thompson, J. and Bannigan, J. (2008). Cadmium: toxic effects on the reproductive system and the embryo. Reproductive Toxicology Journal, 25(3): 304-315.
Tripathi, D.N. and Jena, G.B. (2008). Astaxanthin inhibits cytotoxic and genotoxic effects of cyclophosphamidein mice germ cells. Toxicology, 248(2-3): 96-103.
Tvrda, E., Knazicka, Z. and Lukac, N. (2012). Selected heavy metals versus antioxidant parameters in bull seminal plasma - a comparative study. Journal of Environmental Science and Health, 47(9): 1261-1266.
Tvrda, E., Knazicka, Z., Lukacova, J., Schneidgenova, M., Goc, Z., Gren, A., et al. (2013). The impact of lead and cadmium on selected motility, prooxidant and antioxidant parameters of bovine seminal plasma and spermatozoa. Journal of Environmental Science and Health, 48(10): 1292-1300.
Vahidinia, A., Rahbar, A.R. and Shakoori Mahmoodabadi, M.M. (2017). Effect of astaxanthin, vitamin E, and vitamin C in combination with calorie restriction on sperm quality and quantity in male rats. Journal of Dietary Supplements, 14(3): 252-263.
Verbost, P.M., Flik, G., Look, R.A. and Wendelaar, B.S. (1988). Cadmium inhibits plasma membrane calcium transport. The Journal of Membrane Biology, 102(2): 97-104.
Wang, J.Y., Lee, Y.J., Chou, M.C., Chang, R., Chiu, C.H., Liang, Y.J., et al. (2015(. Astaxanthin protects steroidogenesis from hydrogen peroxide-induced oxidative stress in mouse leydig cells. Marine Drugs, 13(3): 1375-1388.
Waisberg, M., Joseph, P., Hale, B. and Beyersmann, D. (2003). Molecular and cellular mechanisms of cadmium carcinogenesis: a review. Toxicology, 192(2-3): 95-117.
Wolf, A.M., Asoh, S., Hiranuma, H., Ohsawa, I., Iio, K., Satou, A., et al. (2010). Astaxanthin protects mitochondrial redox state and functional integrity against oxidative The Journal of Nutritional Biochemistry, 21(5): 381-389.
Wu, J., Hua, Y., Keep, R.F., Schallert, T., Hoff, J.T., and Xi, G. (2002). Oxidative brain injury from extravasated erythrocytes after intracerebral hemorrhage. Brain Research, 953(1-2): 45-52.
Yan, T., Zhao, Y., Zhang, X. and Lin, X. (2016). Astaxanthin inhibits acetaldehyde-induced cytotoxicity in SH-SY5Y cells by modulating Akt/CREB and p38MAPK/ERK signaling pathways. Marine Drugs, 14(3): 56-68.
Yang, S.H., Long, M., Yu, L.H., Li, L., Li, P., Zhang, Y., et al. (2016). Sulforaphane prevents testicular damage in Kunming mice exposed to cadmium via activation of Nrf2/ARE signaling pathways. International Journal of Molecular, 17(10): 1703-1713.
Zalata, A., Hafez, T. and Comhaire, F. (1995). Evaluation of the role of reactive oxygen species in male infertility. Human Reproduction, 10(6): 1444-1451.
Zhang, L.,Li, Q., Zheng, G., Chen, Y., Huang, M., Zhang, L., et al. (2017). Protective effect of Lyciumbarbarum polysaccharides against cadmium-induced testicular toxicity in male mice. Food & Function Journal, 8(6): 2322-2330.
Zhou, X.Y., Zhang, F., Hu, X.T., Chen, J., Tang, R.X., Zheng, K.Y., et al. (2017). Depression can be prevented by astaxanthin through inhibition of hippocampal inflammation in diabetic mice. Brain Research, 1657(1): 262-268.
_||_
Ahmadi, Z. and Ashrafizadeh, M. (2018). Downregulation of osteocalcin gene in chickens treated with lead acetate II. International Biological and Biomedical Journal, 4(4): 177-182.
Acosta, I.B., Junior, A.S.V., EF, E.S., Cardoso, T.F., Caldas, J.S., Jardim, R.D., et al. (2016). Effects of exposure to cadmium in sperm cells of zebrafish. Toxicology Reports, 3(1): 696-700.
Agarwal, A., Prabakaran, S. and Said, T. (2005). Prevention of oxidative stress injury to sperm. Journal of Andrology, 26(6): 654-660.
Agarwal, A., Virk, G., Ong, C. and Du Plessis, S. (2014). Effect of oxidative stress on male The World Journal of Men's Health, 32(1): 1-17.
Aitken, R.J. (1997). Molecular mechanisms regulating human sperm function. Molecular Human Reproduction, 3(3): 169-173.
Andrisani, A., Dona, G., Tibaldi, E., Maria Brunati, A., Sabbadin, C.H., Armanini, D., et al. (2015). Astaxanthin improves human sperm capacitation by inducing lyn displacement and activation. Marine Drugs, 13(9): 5533-5551.
Alkhedaide, A., Alshehri, Z.S., Sabry, A., Abdel-Ghaffar, T., Soliman, M.M. and Attia. H. (2016). Protective effect of grape seed extract against cadmium-induced testicular dysfunction. Molecular Medicine Reports, 13(4): 3101-3109.
Alvarez, J.G., Touchtone, J., Touchstone J.C., Blasco, L. and Storey, B. (1987). Spontaneous lipid peroxidation and production of hydrogen peroxide and superoxide in human spermatozoa superoxide dismutase as major enzyme protectant against oxygen toxicity. Journal of Andrology, 8(5): 338-348.
Amara, S., Abdelmelek, H., Garrel, C., Guiraud, P., Douki, T., Ravanat, J.L., et al. (2008). Preventive effect of zinc against cadmium-induced oxidative stress in the rat testis. Development & Reproduction, 54(2): 129-134.
Aprioku, J.S., (2013). Pharmacology of free radicals and the impact of reactive oxygen species on the testis. Journal of Reproduction and Infertility, 14(4): 158-172.
Asadi, N. (2017). The impact of oxidative stress on testicular function and the role of antioxidants in improving it: a review. Journal of Clinical and Diagnostic Research: JCDR, 11(5): 1-5.
Asghari, M.H., Moloudizargari, M., Bahadar, H. and Abdollahi, M. (2016). A review of the protective effect of melatonin in pesticide-induced toxicity. Expert Opinion on Drug Metabolism and Toxicology, 13(5): 545-554.
Ashrafizadeh, M. and Ahmadi, Z. (2019). Effect of Astaxanthin treatment on the sperm quality of the mice treated with nicotine. Reviews in Clinical Medicine, 6(1): 1-5.
Bahmanzadeh, M., Vahidnia, A., Mahdinejadiani, S.H., Shokri, S. and Alizadeh, Z. (2016). Dietary supplementation with astaxanthin may ameliorate sperm parameters and DNA integrity in streptozotocin-induced diabetic rats. Clinical and Experimental Reproductive Medicine, 43(2): 90-96.
Baninameh, Z., Moloudizargari, M., Ghasemnejad Berenji, H., Rezaie Chamani, S., Hassanzadeh, V., Ferrante, M., et al. (2016). Urtica dioica attenuate effect of doxorubicin-induced changes on sperm parameters in the International Journal of Medical Research and Health Sciences, 5(11): 116-121.
Bauer, R., Demeter, I., Hasemann, V. and Johansen, J.T. (1980). Structural properties of the zinc site in Cu,Znsuperoxide dismutase; perturbed angular correlation of gamma ray spectroscopy on the Cu, 111Cd-superoxide dismutase derivative. Biochemical and Biophysical Research Communications, 94(4): 1296-1302.
Borowitzka, M.A. (1999). Commercial production of microalgae: ponds, tanks, tubes and fermentors. Journal of Biotechnology, 70(1): 313-321.
Caslino, E., Sblano, C. and Landriscina, C. (1997). Enzyme activity alteration by cadmium administration to rats: the possibility of iron involuement in lipid peroxidation. Archives of Biochemistry and Biophysics, 346(2): 171-179.
Dhankhar, J., Kadiad, S. and Sharma, A. (2012). Astaxanthin: A potential carotenoid. International Journal of Pharmaceutical Sciences and Research, 3(5): 1246.
Dokumacioglu, E., Iskender, H., Yenice, , Kapakin, K.A.T., Sevim, C., Hayirli, A., et al. (2018). Effects of astaxanthin on biochemical and histopathological parameters related to oxidative stress on testes of rats on high fructose regime. Andrologia, 50(7): 1-10.
Farhangdoost, F., JafariBarmak, M., Hemayatkhah Jahromi, V., Azizi, A., Mahmoodi, R., et al. (2013). Aloe vera extract effect on sperm quality and testicular tissue of rats induced by cadmium chloride. Armaghane-Danesh, 19(1): 47-55.
Fatahian Dehkordi, R., Alijani, M.R., Rahimi Junqani, R. and Bahadoran, Sh. (2020). The effects of pomegranate skin extract and powder on renal tissue structure following experimental cadmium poisoning in Japanese quail. Veterinary Clinical Pathology, 14(53): 37-50. [In Persian]
Fukuzawa, K. (2000). Singlet oxygen scavenging in phospholipid membranes. Methods in Enzymology, 319(10): 101-110.
Gharagozloo, P. and Aitken, R.J. (2011). The role of sperm oxidative stress in male infertility and the significance of oral antioxidant therapy. Human Reproduction, 26(7): 1628-1640.
Ghavidel Aghdam, E., Narimani Rad, M. and Lotfi, A. (2016). Effects of silver nanoparticles synthesized through chemical reduction on plasma superoxide dismutase and glutathione peroxidase enzymes in rat model. Journal of Veterinary Clinical Pathology, 10(37): 69-80. [In Persian]
Gil-Guzman, E., Ollero, M., Lopez, M.C., Sharma, R.K., Alvarez, J.G., Thomas, Jr, A.J., et al. (2001). Differential production of reactive oxygen species by subsets of human spermatozoa at different stages of maturation. Human Reproduction, 16(9): 1922-1930.
Goto, S., Kogure, K., Abe, K., Kimata, Y., Kitahama, K., Yamashita, E., et al. (2001). Efficient radical trapping at the surface and inside the phospholipid membrane is responsible for highly potent antiperoxidative activity of the carotenoid Biochemical and Biophysical Acta (BBA)-Biomembranes, 1512(2): 251-258.
Hassanpour, H., Bigham Sadegh, A., Karimi, I., Heidari Khoei, H., Karimi, A., Edalati Shaarbaf, P., et al. (2017). Comparative expression analysis of HSP70, HSP90, IL-4, TNF, KITLG and KIT-receptor gene between varicocele-induced and non-varicocele testes of International Journal of Fertility and Sterility, 11(3): 148-155.
Heidari Khoei, H., Fakhri, S., Parvardeh, S., Shams Mofarahe, Z., Baninameh, Z. and Vardiani, M. (2018a). Astaxanthin prevents the methotrexateinduced reproductive toxicity by targeting oxidative stress in male mice. Toxin Reviews, 38(4): 1-7.
Heidari Khoei, H., Fakhri, S., Parvardeh, S., Shams Mofarahe, Z., Ghasemnejad-Berenji, H., Nazarian, H., et al. (2018b). Testicular toxicity and reproductive performance of streptozotocin-induced diabetic male rats: the ameliorating role of silymarin as an antioxidant. Toxin Reviews, 38(3): 223-233.
Ibrahim, S.F., Osman, K., Das, S, Mazni Othman, A., Abdul Majid, N. and Abdul Rahman, M.P. (2008). A study of the antioxidant effect of alpha lipoic acids on sperm quality. Clinics (Sao Paulo), 63(4): 545-550.
Jamalan, M., Ghaffari, M.A., Hoseinzadeh, P., Hashemitabar, M. and Zeinali, M. (2016). Human sperm quality and metal toxicants: protective effects of some flavonoids on male reproductive function. International Journal of Fertility and Sterility, 10(2): 215-223.
Jamshidi, N., Asghari, A., Neshat, M. and Mortazavi, P. (2016). Effects of magnesium sulfate administration on ischemia-reperfusion kidney in rat. Veterinary Journal (Pajouhesh & Sazandegi), 115(1): 63-75.
Jiang, X., Chen, L., Shen, L., Chen, Z., Xu, L., Zhang, J. and Yu, X. (2016). Trans-astaxanthin attenuates lipopolysaccharide-induced neuroinflammation and depressive-like behavior in mice. Brain Research Journal, 1649(1): 30-37.
Kadivar, A., Heidari Khoei, H., Hassanpour, H., Ghanaei, H., Golestanfar, A., Mehraban, H., et al. (2016). Peroxisome proliferator-activated receptors (PPARa, PPARc and PPARb/d) gene expression profile on ram spermatozoa and their relation to the sperm Veterinary Research Forum, 7(1): 27-34.
Kara, H., Cevik, A., Konar, V., Dayangac, A. and Yilmaz, M. (2007). Protective effects of antioxidants against cadmium-induced oxidative damage in rat testes. Biological Trace Element Research, 120(1-3): 205-211.
Kidd, P. (2011). Astaxanthin, cell membrane nutrient with diverse clinical benefits and anti-aging potential. Alternative Medicine Review, 16 (4): 355-364.
Koyuturk, M., Yanardag, R., Bolkent, S. and Tunali, S. (2006). Influence of combined antioxidants against cadmium induced testicular damage. Environmental Toxicology and Pharmacology, 21(3): 235-240.
Li, Y., Wu, J., Zhou, W. and Gao, J. (2016). Association between environmental exposure to cadmium and human semen quality. International Journal of Environmental Health Research, 26(2): 175-186.
Mansour, N., McNiven, M.A. and Richardson, G.F. (2006). The effect of dietary supplementation with blueberry, alpha-tocopherol or astaxanthin on oxidative stability of Arctic char (Salvelinus Alpinus) semen. Theriogenology, 66(2): 373-382.
Massanyi, P., Weis, J., Lukac, N., Trandzik, J. and Bystricka, J. (2008). Cadmium, zinc, copper, sodium and potassium concentrations in rooster and turkey semen and their correlation. Journal of Environmental Science and Health, 43(5): 563-565.
Mohammadi Roushandeh, A., Salehi, I. and Mortazavi, M. (2015). Protective Effects of Restricted Diet and Antioxidants on Testis Tissue in Rats Fed with High-Fat Diet. Iranian Biomedical Journal, 19(2): 96-101.
Mohammadnejad, D., Soleimani rad, J. and Mohammadi-roshandeh, A. (2013). Preventive effects of Cetrorelix on the changes induced by Cisplatin on spermatogenic and myoid cells and basal lamina of seminiferous ducts in the testis of Balb/C mouse. Journal of Veterinary Clinical Pathology, 6(4): 1665-1674. [In Persian]
Mortazavi, M., Salehi, I., Alizadeh, Z., Vahabian,M. and Mohammadi Roushandeh, A. (2014). Protective Effects of Antioxidants on Sperm Parameters and Seminiferous Tubules Epithelium in High Fat-fed Rats. Journal of Reproduction & Infertility, 15(1): 22-28.
Naguib, Y.M. (2000). Antioxidant activities of astaxanthin and related carotenoids. Journal of agricultural and Food Chemistry, 48(4): 1150-1154.
Ognjanovic_c, B. I., Markovi_c, S.D., ĐorCevi_c, N.Z., Trbojevi_c, I.S., Stajn, A.S. and Sai_ci_c, Z.S. (2010). Cadmium-induced lipid peroxidation and changes in antioxidant defense system in the rat testes: protective role of coenzyme Q 10 and Vitamin E. Reproductive Toxicology, 29(2): 191-197.
Orisakwe, O. (2014). Lead and cadmium in public health in Nigeria: physicians neglect and pitfall in patient management. North American Journal of Medicine and Science, 6(2): 61-71.
Rafiei, H. and Ashrafizadeh, M. (2018). Expression of Collagen Type II and Osteocalcin Genes in Mesenchymal Stem Cells from Rats Treated with Lead acetate II. Iranian Journal of Toxicology, 12(5): 35-40.
Rasulifar, M.H. and Zargari F. (2015). The effect of aqueous extract of white tea on serum levels of antioxidant enzymes in mice Field exposed to arsenic. Journal of Veterinary Clinical Pathology, 9(2): 153-161. [In Persian]
Sen Gupta, R., Sen Gupta, E., Dhakal, B.K. and Thakur Ahnn, J. (2004). Vitamin C and vitamin E protect the rat testes from cadmium-induced reactive oxygen species. Molecules and Cells, 17(1): 132-139.
Siu, E.R., Mruk, D.D., Porto, C.S. and Cheng, C.Y. (2009). Cadmium-induced testicular injury. Toxicology and Applied Pharmacology, 238(3): 240-249.
Sayed, M.M., Hassanein, K.M.A. and Senosy, W. (2014). Protective effects of thymoquinone and l-cysteine on cadmium-induced reproductive toxicity in rats. Reproductive Toxicology Journal, 13(1): 612-620.
Tandon, S. K., Singh, S., Prasad, S., Khandekar, K., Dwivedi, V.K., Chatterjee, M., et al. (2003). Reversal of cadmium induced oxidative stress by chelating agent, antioxidant or their combination in rat. Toxicology Letters Journal, 145(3): 211-217.
Thompson, J. and Bannigan, J. (2008). Cadmium: toxic effects on the reproductive system and the embryo. Reproductive Toxicology Journal, 25(3): 304-315.
Tripathi, D.N. and Jena, G.B. (2008). Astaxanthin inhibits cytotoxic and genotoxic effects of cyclophosphamidein mice germ cells. Toxicology, 248(2-3): 96-103.
Tvrda, E., Knazicka, Z. and Lukac, N. (2012). Selected heavy metals versus antioxidant parameters in bull seminal plasma - a comparative study. Journal of Environmental Science and Health, 47(9): 1261-1266.
Tvrda, E., Knazicka, Z., Lukacova, J., Schneidgenova, M., Goc, Z., Gren, A., et al. (2013). The impact of lead and cadmium on selected motility, prooxidant and antioxidant parameters of bovine seminal plasma and spermatozoa. Journal of Environmental Science and Health, 48(10): 1292-1300.
Vahidinia, A., Rahbar, A.R. and Shakoori Mahmoodabadi, M.M. (2017). Effect of astaxanthin, vitamin E, and vitamin C in combination with calorie restriction on sperm quality and quantity in male rats. Journal of Dietary Supplements, 14(3): 252-263.
Verbost, P.M., Flik, G., Look, R.A. and Wendelaar, B.S. (1988). Cadmium inhibits plasma membrane calcium transport. The Journal of Membrane Biology, 102(2): 97-104.
Wang, J.Y., Lee, Y.J., Chou, M.C., Chang, R., Chiu, C.H., Liang, Y.J., et al. (2015(. Astaxanthin protects steroidogenesis from hydrogen peroxide-induced oxidative stress in mouse leydig cells. Marine Drugs, 13(3): 1375-1388.
Waisberg, M., Joseph, P., Hale, B. and Beyersmann, D. (2003). Molecular and cellular mechanisms of cadmium carcinogenesis: a review. Toxicology, 192(2-3): 95-117.
Wolf, A.M., Asoh, S., Hiranuma, H., Ohsawa, I., Iio, K., Satou, A., et al. (2010). Astaxanthin protects mitochondrial redox state and functional integrity against oxidative The Journal of Nutritional Biochemistry, 21(5): 381-389.
Wu, J., Hua, Y., Keep, R.F., Schallert, T., Hoff, J.T., and Xi, G. (2002). Oxidative brain injury from extravasated erythrocytes after intracerebral hemorrhage. Brain Research, 953(1-2): 45-52.
Yan, T., Zhao, Y., Zhang, X. and Lin, X. (2016). Astaxanthin inhibits acetaldehyde-induced cytotoxicity in SH-SY5Y cells by modulating Akt/CREB and p38MAPK/ERK signaling pathways. Marine Drugs, 14(3): 56-68.
Yang, S.H., Long, M., Yu, L.H., Li, L., Li, P., Zhang, Y., et al. (2016). Sulforaphane prevents testicular damage in Kunming mice exposed to cadmium via activation of Nrf2/ARE signaling pathways. International Journal of Molecular, 17(10): 1703-1713.
Zalata, A., Hafez, T. and Comhaire, F. (1995). Evaluation of the role of reactive oxygen species in male infertility. Human Reproduction, 10(6): 1444-1451.
Zhang, L.,Li, Q., Zheng, G., Chen, Y., Huang, M., Zhang, L., et al. (2017). Protective effect of Lyciumbarbarum polysaccharides against cadmium-induced testicular toxicity in male mice. Food & Function Journal, 8(6): 2322-2330.
Zhou, X.Y., Zhang, F., Hu, X.T., Chen, J., Tang, R.X., Zheng, K.Y., et al. (2017). Depression can be prevented by astaxanthin through inhibition of hippocampal inflammation in diabetic mice. Brain Research, 1657(1): 262-268.
_||_