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Research Articles

Panax ginseng ameliorate toxic effects of cadmium on germ cell apoptosis, sperm quality, and oxidative stress in male Wistar rats

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Pages 389-401 | Received 25 Jul 2020, Accepted 28 Jan 2021, Published online: 22 Feb 2021

References

  • Abdel-Wahhab, M.A. and Ahmed, H.H., 2004. Protective effect of Korean Panax ginseng against chromium VI toxicity and free radicals generation in rats. Journal of ginseng research, 28, 11–17.
  • Abolhassani, M., et al., 2019. Organochlorine and organophosphorous pesticides may induce colorectal cancer; a case-control study. Ecotoxicology and environmental safety, 178, 168–177.
  • Acharya, U.R., et al., 2008. Effect of vitamins C and E on spermatogenesis in mice exposed to cadmium. Reproductive toxicology, 25 (1), 84–88.
  • Adamkovicova, M., et al., 2016. Sperm motility and morphology changes in rats exposed to cadmium and diazinon. Reproductive biology and endocrinology, 14 (1), 42.
  • Adebayo, A., Oke, B., and Akinloye, A., 2009. Characterizing the gonadosomatic index and its relationship with age in greater cane rat (Thryonomys swinderianus, Temminck). Journal of veterinary anatomy, 2 (2), 53–59.
  • Babaknejad, N., et al., 2018. Cadmium testicular toxicity in male Wistar rats: protective roles of zinc and magnesium. Biological trace element research, 185 (1), 106–115.
  • Benoff, S., et al., 2009. Cadmium concentrations in blood and seminal plasma: correlations with sperm number and motility in three male populations (infertility patients, artificial insemination donors, and unselected volunteers). Molecular medicine, 15 (7–8), 248–262.
  • Benzie, I.F. and Strain, J.J., 1996. The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Analytical biochemistry, 239 (1), 70–76.
  • Birben, E., et al., 2012. Oxidative stress and antioxidant defense. World allergy organization journal, 5, 9–19.
  • Casalino, E., et al., 2002. Molecular inhibitory mechanisms of antioxidant enzymes in rat liver and kidney by cadmium. Toxicology, 179 (1–2), 37–50.
  • Chemek, M., et al., 2018. Involvement of testicular DAAM1 expression in zinc protection against cadmium-induced male rat reproductive toxicity. Journal of cellular physiology, 233 (1), 630–640.
  • Chen, F. and Huang, G., 2019. Antioxidant activity of polysaccharides from different sources of ginseng. International journal of biological macromolecules, 125, 906–908.
  • Chung, N.P. and Cheng, C.Y., 2001. Is cadmium chloride-induced inter-Sertoli tight junction permeability barrier disruption a suitable in vitro model to study the events of junction disassembly during spermatogenesis in the rat testis? Endocrinology, 142 (5), 1878–1888.
  • Cupertino, M.C., et al., 2017. Differential susceptibility of germ and leydig cells to cadmium-mediated toxicity: impact on testis structure, adiponectin levels, and steroidogenesis. Oxidative medicine and cellular longevity, 2017, 1–11.
  • Cuypers, A., et al., 2010. Cadmium stress: an oxidative challenge. Biometals: an international journal on the role of metal ions in biology, biochemistry, and medicine, 23 (5), 927–940.
  • El-Demerdash, F.M., et al., 2004. Cadmium-induced changes in lipid peroxidation, blood hematology, biochemical parameters and semen quality of male rats: protective role of vitamin E and β-carotene. Food and chemical toxicology, 42 (10), 1563–1571.
  • El-Shahat, A.E.-R., et al., 2009. Altered testicular morphology and oxidative stress induced by cadmium in experimental rats and protective effect of simultaneous green tea extract. International journal of morphology, 27 (3), 757–764.
  • Erboga, M., et al., 2016. Anti-apoptotic and anti-oxidant effects of caffeic acid phenethyl ester on cadmium-induced testicular toxicity in rats. Biological trace element research, 171 (1), 176–184.
  • Eskandari, M., et al., 2016. Ameliorating effect of ginseng on epididymo-orchitis inducing alterations in sperm quality and spermatogenic cells apoptosis following infection by uropathogenic Escherichia coli in rats. Cell journal, 18, 446.
  • Farjad, E. and Momeni, H.R., 2018. Silymarin ameliorates oxidative stress and enhances antioxidant defense system capacity in cadmium-treated mice. Cell journal, 20, 422.
  • Fowler, B.A., 2009. Monitoring of human populations for early markers of cadmium toxicity: a review. Toxicology and applied pharmacology, 238 (3), 294–300.
  • Friberg, L., 2018. Cadmium in the environment. Boca Raton (FL): CRC press.
  • Genchi, G., et al., 2020. The effects of cadmium toxicity. International journal of environmental research and public health, 17 (11), 3782.
  • Ghanbari, E., Nejati, V., and Khazaei, M., 2016. Antioxidant and protective effects of Royal jelly on histopathological changes in testis of diabetic rats. International journal of reproductive biomedicine, 14, 519.
  • Godt, J., et al., 2006. The toxicity of cadmium and resulting hazards for human health. Journal of occupational medicine and toxicology, 1, 22.
  • Goyer, R.A., Liu, J., and Waalkes, M.P., 2004. Cadmium and cancer of prostate and testis. Biometals: an international journal on the role of metal ions in biology, biochemistry, and medicine, 17 (5), 555–558.
  • Hakemi, S.G., et al., 2019. The effects of olive leaf extract on the testis, sperm quality and testicular germ cell apoptosis in male rats exposed to busulfan. International journal of fertility & sterility, 13, 57.
  • Harborne, J., 1973. Textbook of phytochemical methods. 1st ed. London, UK: Champraan and Hall Ltd., 110–113.
  • He, L., et al., 2018. Protective effects of proanthocyanidins against cadmium-induced testicular injury through the modification of Nrf2-Keap1 signal path in rats. Environmental toxicology and pharmacology, 57, 1–8.
  • Ji, Y.L., et al., 2012. Melatonin alleviates cadmium-induced cellular stress and germ cell apoptosis in testes. Journal of pineal research, 52 (1), 71–79.
  • Ji, Y.-L., et al., 2013. N-acetylcysteine protects against cadmium-induced germ cell apoptosis by inhibiting endoplasmic reticulum stress in testes. Asian Journal of andrology, 15 (2), 290–296.
  • Karadeniz, A., Cemek, M., and Simsek, N., 2009. The effects of Panax ginseng and Spirulina platensis on hepatotoxicity induced by cadmium in rats. Ecotoxicology and environmental safety, 72 (1), 231–235.
  • Khafaga, A.F., et al., 2019. The potential modulatory role of herbal additives against Cd toxicity in human, animal, and poultry: a review. Environmental science and pollution research international, 26 (5), 4588–4604.
  • Kim, J.-S., 2016. Investigation of phenolic, flavonoid, and vitamin contents in different parts of Korean Ginseng (Panax ginseng CA Meyer). Preventive nutrition and food science, 21 (3), 263–270.
  • Kim, Y.K., Guo, Q., and Packer, L., 2002. Free radical scavenging activity of red ginseng aqueous extracts. Toxicology, 172 (2), 149–156.
  • Kim, S., et al., 2005. Effects of Panax ginseng extract on exercise-induced oxidative stress. Journal of sports medicine and physical fitness, 45, 178.
  • Kim, H.-G., et al., 2011. Antioxidant effects of Panax ginseng CA Meyer in healthy subjects: a randomized, placebo-controlled clinical trial. Food and chemical toxicology, 49 (9), 2229–2235.
  • Lee, Y.-M., et al., 2017. Implications of red Panax ginseng in oxidative stress associated chronic diseases. Journal of ginseng research, 41 (2), 113–119.
  • Leung, K.W. and Wong, A.S., 2013. Ginseng and male reproductive function. Spermatogenesis, 3 (3), e26391.
  • Li, H. and Li, H., 2019. Ginsenoside-Rg5 inhibits growth and metastasis of ovarian carcinoma via suppressing expression of fibroblast growth factor-8b (FGF8b). Journal of King Saud University-science, 32 (1), 1162–1167.
  • Liu, Q., et al., 2013. Effect of cadmium on rat Leydig cell testosterone production and DNA integrity in vitro. Biomedical and environmental sciences, 26, 769.
  • Liu, J., Qu, W., and Kadiiska, M.B., 2009. Role of oxidative stress in cadmium toxicity and carcinogenesis. Toxicology and applied pharmacology, 238 (3), 209–214.
  • Li, X.-H., et al., 2010. Effects of cadmium on testis spermatocyte apoptosis and epididymis mature spermatozoa quality of mice. Chinese journal of applied ecology, 4, 987–992.
  • Ma, D., et al., 2013. Oxidative damages and ultrastructural changes in the sperm of freshwater crab Sinopotamon henanense exposed to cadmium. Ecotoxicology and environmental safety, 98, 244–249.
  • Mandegary, A., et al., 2012. Anticonvulsant activity of the essential oil and methanolic extract of Bunium persicum (Boiss). B. Fedtsch. Journal of ethnopharmacology, 140 (2), 447–451.
  • Meeker, J.D., et al., 2008. Cadmium, lead, and other metals in relation to semen quality: human evidence for molybdenum as a male reproductive toxicant. Environmental health perspectives, 116 (11), 1473–1479.
  • Mehraein, F. and Negahdar, F., 2011. Morphometric evaluation of seminiferous tubules in aged mice testes after melatonin administration. Cell journal, 13, 1.
  • Menkveld, R., 2010. Clinical significance of the low normal sperm morphology value as proposed in the fifth edition of the WHO Laboratory Manual for the examination and processing of human semen. Asian journal of andrology, 12 (1), 47–58.
  • Mitra, E., et al., 2012. Protective effect of aqueous curry leaf (Murraya koenigii) extract against cadmium-induced oxidative stress in rat heart. Food and chemical toxicology: an international journal published for the British Industrial Biological Research Association, 50 (5), 1340–1353.
  • Mortazavi, N., et al., 2019. Organochlorine and organophosphorus pesticides and bladder cancer: a case‐control study. Journal of cellular biochemistry, 120 (9), 14847–14859.
  • Mouro, V.G., et al., 2019. Subacute testicular toxicity to cadmium exposure Intraperitoneally and orally. Oxidative medicine and cellular longevity, 2019, 1–14.
  • Mouro, V.G.S., et al., 2020. Cadmium-induced testicular toxicity in mice: subacute and subchronic route-dependent effects. Biological trace element research, 193 (2), 466–482.
  • Murphy, C.J. and Richburg, J.H., 2014. Implications of Sertoli cell induced germ cell apoptosis to testicular pathology. Spermatogenesis, 4 (2), e979110.
  • Nemmiche, S., 2017. Oxidative signaling response to cadmium exposure. Toxicological sciences, 156 (1), 4–10.
  • Niknafs, B., Salehnia, M., and Kamkar, M., 2015. Induction and determination of apoptotic and necrotic cell death by cadmium chloride in testis tissue of mouse. Journal of reproduction & infertility, 16 (1), 24–29.
  • Ognjanovic, B., et al., 2003. Protective influence of vitamin E on antioxidant defense system in the blood of rats treated with cadmium. Physiological research, 52, 563–570.
  • Ok, S., Kang, J.S., and Kim, K.M., 2016. Testicular antioxidant mechanism of cultivated wild ginseng extracts. Molecular & cellular toxicology, 12 (2), 149–158.
  • Ola-Mudathir, K.F., et al., 2008. Protective roles of onion and garlic extracts on cadmium-induced changes in sperm characteristics and testicular oxidative damage in rats. Food and chemical toxicology, 46 (12), 3604–3611.
  • Olaniyi, K.S., et al., 2020. Protective role of glutamine against cadmium-induced testicular dysfunction in Wistar rats: involvement of G6PD activity. Life sciences, 242, 117250.
  • Oliveira, H., et al., 2009. Adverse effects of cadmium exposure on mouse sperm. Reproductive toxicology, 28 (4), 550–555.
  • Ong, W.-Y., et al., 2015. Protective effects of ginseng on neurological disorders. Frontiers in aging neuroscience, 7, 129.
  • Pařízek, J., 1964. Vascular changes at sites of oestrogen biosynthesis produced by parenteral injection of cadmium salts: the destruction of placenta by cadmium salts. Reproduction, 7, 263–265.
  • Park, S.J., et al., 2013. Protective effects of Korean red ginseng extract on cadmium-induced hepatic toxicity in rats. Journal of ginseng research , 37 (1), 37–44.
  • Paydar, P., et al., 2018. The role of acetylcholinesterase, paraoxonase, and oxidative stress in breast tumors. International journal of cancer management, 11 (11), e83370.
  • Rajendar, B., et al., 2011. Protective effect of an aphrodisiac herb Tribulus terrestris Linn on cadmium-induced testicular damage. Indian journal of pharmacology, 43 (5), 568–573.
  • Rajeshkumar, S., Mini, J., and Munuswamy, N., 2013. Effects of heavy metals on antioxidants and expression of HSP70 in different tissues of Milk fish (Chanos chanos) of Kaattuppalli Island, Chennai, India. Ecotoxicology and environmental safety, 98, 8–18.
  • Ramesh, T., et al., 2012. Panax ginseng reduces oxidative stress and restores antioxidant capacity in aged rats. Nutrition research, 32 (9), 718–726.
  • Rinaldi, M., et al., 2017. Cadmium, organ toxicity and therapeutic approaches: a review on brain, kidney and testis damage. Current medicinal chemistry, 24 (35), 3879–3893.
  • Saddein, E., et al., 2019. Preventative effects of vitamin E on testicular damage and sperm parameters in the first-generation mice pups due to pre-and postnatal mancozeb exposure. Journal of toxicology, 2019, 4763684.
  • Salari, S., et al., 2016. Evaluation of antifungal activity of standardized extract of Salvia rhytidea Benth. (Lamiaceae) against various Candida isolates. Journal de mycologie medicale, 26 (4), 323–330.
  • Sarhadynejad, Z., et al., 2016. Pharmacological safety evaluation of a traditional herbal medicine “Zereshk-e-Saghir” and assessment of its hepatoprotective effects on carbon tetrachloride induced hepatic damage in rats. Journal of ethnopharmacology, 190, 387–395.
  • Shao, J.-W., et al., 2019. Therapeutic potential of ginsenosides on diabetes: from hypoglycemic mechanism to clinical trials. Journal of functional foods, 64, 103630.
  • Sharififar, F., et al., 2012. Essential oil and methanolic extract of Zataria multiflora Boiss with anticholinesterase effect. Pakistan journal of biological sciences, 15 (1), 49–53.
  • Siu, E.R., et al., 2009. Cadmium-induced testicular injury. Toxicology and applied pharmacology, 238 (3), 240–249.
  • Skipper, A., et al., 2016. Cadmium chloride induces DNA damage and apoptosis of human liver carcinoma cells via oxidative stress. International journal of environmental research and public health, 13 (1), 88.
  • Tvrdá, E., 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, part A, 48 (10), 1292–1300.
  • Valenzuela, A., 1991. The biological significance of malondialdehyde determination in the assessment of tissue oxidative stress. Life sciences, 48 (4), 301–309.
  • Valko, M., Morris, H., and Cronin, M., 2005. Metals, toxicity and oxidative stress. Current medicinal chemistry, 12 (10), 1161–1208.
  • Wang, B., et al., 2013. Ginsenoside Rd maintains adult neural stem cell proliferation during lead-impaired neurogenesis. Neurological sciences, 34 (7), 1181–1188.
  • Wang, Y., et al., 2017. Role of autophagy in cadmium-induced testicular injury. Human & experimental toxicology, 36 (10), 1039–1048.
  • Worek, F., et al., 1999. Improved determination of acetylcholinesterase activity in human whole blood. Clinica chimica acta, 288 (1–2), 73–90.
  • Wu, X., et al., 2017. A brief exposure to cadmium impairs Leydig cell regeneration in the adult rat testis. Scientific reports, 7, 1–11.
  • Zare, M., et al., 2020. The prophylactic effect of date palm (Phoenix dactylifera L.) fruit extract on testicular toxicity induced by formaldehyde: an experimental study. International journal of reproductive biomedicine, 18, 275.
  • Zhang, Y., Li, S., and Li, S., 2019. Relationship between cadmium content in semen and male infertility: a meta-analysis. Environmental science and pollution research, 26 (2), 1947–1953.
  • Zhang, Q.H., et al., 2008. Protective effects of total saponins from stem and leaf of Panax ginseng against cyclophosphamide-induced genotoxicity and apoptosis in mouse bone marrow cells and peripheral lymphocyte cells. Food and chemical toxicology: an international journal published for the British Industrial Biological Research Association, 46 (1), 293–302.
  • Zhao, L.-L., et al., 2017. Reproductive effects of cadmium on sperm function and early embryonic development in vitro. PLoS one, 12 (11): e0186727.
  • Zhu, Q., Li, X., and Ge, R.-S., 2020. Toxicological effects of cadmium on mammalian testis. Frontiers in genetics, 11, 527.
  • Zongping, L., 2013. Oxidative stress and mitogen-activated protein kinase pathways involved in cadmium-induced BRL 3A cell apoptosis. Oxidative medicine and cellular longevity, 2013, 516051.

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