The Interaction between Zinc and Cadmium from Antioxidant and Anti-Inflammatory Perspectives. Is Zinc a Natural Protector?

Year 2023, Volume: 13 Issue: 2, 215 - 234, 31.12.2023

Fatih Çağlar Çelikezen

https://doi.org/10.17678/beuscitech.1372319

Abstract

Cadmium is known as a toxicant for animals and human beings. Despite of its toxic properties it is used in many industrial branches. Thus, people are likely to be exposed to cadmium due to professional and environmental reasons. The underlying mechanisms of cadmium toxication are oxidative stress, oxidative stress-related inflammation and interaction with bio-elements. Many studies have reported a protective role of zinc against cadmium toxication in animals and at cellular levels. Thus, this review revealed the protective effect of zinc from antioxidant and anti-inflammatory perspectives. In this study, documents analyzing the interaction between Zn and Cd in metabolism were examined.

Keywords

Cadmium, Zinc, antioxidant, anti-inflammatory, toxicity, oxidative stress

References

• [1] P.C. Nagajyoti, K.D. Lee, and T.V.M. Sreekanth, “Heavy metals, occurrence and toxicity for plants: a review,” Environ. Chem. Lett., vol.8, pp. 199–216, 2010.
• [2] S. Banik, K.C. Das, M.S. Islam, and M. Salimullah, “Recent advancements and challenges in microbial bioremediation of heavy metals contamination,” JSM Biotechnol. Bioeng., vol.2, no. 1,1035, 2014.
• [3] A.T. Jan, M. Azam, K. Siddiqui, A. Ali, I. Choi, and Q.M.R. Haq, “Heavy metals and human health: mechanistic insight into toxicity and counter defense system and antioxidants,” Int. J. Mol. Sci., vol.16, pp. 29592–29630, 2015.
• [4] S. Honey, R. Neetu, B.M. Blessy, “The characteristics, toxicity and e_ects of cadmium,” Int. J. Nanosci.,vol.3, pp. 1–9, 2015.
• [5] Agency for Toxic Substances and Disease Registry (ATSDR) (1998) U.S. Public Health Service. Toxicological Profile for Cadmium. Atlanta, GA
• [6] W.M. Hayes, CRC Handbook of Chemistry and Physics. CRC Press, Boca Raton, 2016
• [7] H. Zhang, and M. Reynolds, “Cadmium exposure in living organisms: a short review,” Sci. Total. Environ., vol.678, pp. 761–767, 2019.
• [8] G.G. Schwartz, and I.M. Reis, “Is cadmium a cause of human pancreatic cancer?,” Cancer Epidemiol. Biomark. Prev., vol. 9, pp.139–145, 2000.
• [9] G. Bjørklund, G. Crisponi, V.M. Nurchi, R. Cappai, A. Buha Djordjevic, J. Aaseth (2019) “A review on coordination properties of thiolcontaining chelating agents towards mercury, cadmium, and lead,” Molecules, vol. 24, no. 18, https://doi.org/10.3390/molecules24183247.
• [10] A. Buha, V. Matovic, B. Antonijevic, Z. Bulat, M. Curcic, E.A. Renieri, A.M. Tsatsakis, A. Schweitzer, and D. Wallace, “Overview of cadmium thyroid disrupting effects and mechanisms,” Int. J. Mol. Sci., vol. 17;19, no. 5, 1501 https://doi.org/10.3390/ijms19051501.
• [11] S. Sarkar, P. Yadav, R. Trivedi, A.K. Bansal, and D. Bhatnager, “Cadmium-induced lipid peroxidation and the status antioxidant system in rat tissues,” J. Trace Elem. Med. Biol., vol. 9, pp. 144–149, 1995.
• [12] A.A. Tinkov, T. Filippini, O.P. Ajsuvakova, J. Aaseth, Y.G. Gluhcheva, J.M. Ivanova, G. Bjørklund, M.G. Skalnaya, E.R. Gatiatulina, E.V. Popova, O.N. Nemereshina, M. Vinceti, and A.V. Skalny, “The role of cadmium in obesity and diabetes,” Sci. Total Environ., vol. 601, pp. 741-755, 2017.
• [13] M. Tellez-Plaza, A. Navas-Acien, K.L Caldwell, A. Menke, P. Muntner, and E. Guallar, “Reduction in cadmium exposure in the United States population 1988-2008: the contribution of declining smoking rates,” Environ. Health Perspect., vol.120, no.2, pp. 204-209, 2012.
• [14] J.Y. Min, and K.B. Min, “Blood cadmium levels and Alzheimer's disease mortality risk in older US adults,” Environ. Health-Glob., vol.5, no:1, pp. 69, 2016.
• [15] M.P. Waalkes, “Cadmium carcinogenesis,” Mutat. Res., vol. 533, pp. 107–120, 2003.
• [16] A.N. Sarkar, G.E. Ravindran, and V.I. Krishnamurthy, “A brief review on the effect of cadmium toxicity: from cellular to organ level,” Int. J. Bio. Technol. Res., vol.3, pp.17–36, 2013.
• [17] S.C. Gupta, A. Sharma, M. Mishra, R.K. Mishra, and D.K. Chowdhur, “Heat shock proteins in toxicology: How close and how far,” Life Sci., vol. 86, pp. 377–384, 2010.
• [18] J. Demenesku, I. Mirkov, M. Ninkov, A.P. Aleksandrov, L. Zolotarevski, D. Kataranovski, and M. Kataranovski, “Acute cadmium administration to rats exerts both immunosuppressive and proinflammatory effects in spleen,” Toxicology, pp. 96-108, 2014.
• [19] Z. Zhao, J.S. Hyun, H. Satsu, S. Kakuta, and M. Shimizu, “Oral exposure to cadmium chloride triggers an acute inflammatory response in the intestines of mice, initiated by the over-expression of tissue macrophage inflammatory protein-2 mRNA,” Toxicol. Lett., vol.164, pp. 144–154, 2006.
• [20] A. Winiarska-Mieczan, “Protective effect of tea against lead and cadmium-induced oxidative stress-a review,” Biometals, vol. 31,no. 6. pp. 909–926, 2018.
• [21] R.S. Almeer, G.I. AlBasher, S. Alarifi, S.Alkahtani, D.Ali, and A.E. Abdel Moneim, “Royal jelly attenuates cadmium-induced nephrotoxicity in male mice,” Sci. Rep., vol.9, no.1, pp. 5825, 2019.
• [22] E.M. Al Olayan, A.S. Aloufi, O.D. Al Amri, O.H. El-Habit, A.E. “Abdel Moneim Protocatechuic acid mitigates cadmium-induced neurotoxicity in rats: Role of oxidative stress, inflammation and apoptosis,” Sci. Total Env., vol.723, 137969, 2020.
• [23] R. Marchan, C. Cadenas, and H.M. Bolt, “Zinc as a multipurpose trace element,” Arch. Toxicol., vol. 86, pp.519-520, 2012.
• [24] M. Stefanidou, C. Maravelias, A. Dona, and C. Spiliopoulou “ Zinc: a multipurpose trace element,” Arch. Toxicol., vol.80, pp.1-9, 2006.
• [25] P.I. Oteiza, V.N. Adonaylo, and C.L. Keen, “Cadmium-induced testes oxidative damage in rats can be influenced by dietary zinc intake,” Toxicology, vol. 137, pp.13–22, 1999.
• [26] M. Brzoska, and J. Moniuszko-Jakoniuk, “Interactions between cadmium and zinc in the organism,” Food Chem. Toxicol., vol. 39, pp. 967–980, 2000.
• [27] I.M. Olsson, I. Bensryd, T. Lundh, H. Ottosson, S. Skerfving, and A. Oskarsson “ Cadmium in blood and urine–impact of sex, age, dietary intake, iron status, and former smoking–association of renal effects,” Environ. Health Perspect., vol. 110, pp. 1185–1190, 2002.
• [28] S. Willers, L. Gerhardsson, and T. Lundh, “Environmental tobacco smoke (ETS) exposure in children with asthma relation between lead and cadmium, and cotinine concentrations in urine,” Respir. Med., vol. 99, pp. 1521–1527, 2005.
• [29] M. Arora, J. Weuve, J. Schwartz, and R.O. Wright, “Association of environmental cadmium exposure with pediatric dental caries,” Environ. Health Perspect., vol.116, pp. 821–825, 2008.
• [30] M. Vahter, M. Berglund, S. Slorach, L. Friberg, M. Sarić, X.Q. Zheng, and M. Fujita, “ Methods for integrated exposure monitoring of lead and cadmium,” Environ. Res., vol. 56, pp.78–89, 1991.
• [31] H.H. Rahman, D. Niemann, and S.H. Munson-McGee, “Association between environmental toxic metals, arsenic and polycyclic aromatic hydrocarbons and chronic obstructive pulmonary disease in the US adult population,” Environ. Sci. Pollut. Res. Int., vol. 29, no. 36, pp. 54507-54517, 2022.
• [32] S. Ma, J. Zhang, C. Xu, M. Da, Y. Xu, Y. Chen, and X. Mo, “Increased serum levels of cadmium are associated with an elevated risk of cardiovascular disease in adults,” Environ. Sci. Pollut. Res. Int., vol. 29, no. 2, pp. 1836-1844, 2022.
• [33] P.Rosales-Cruz, M. Domínguez-Pérez, E. Reyes-Zárate, O. Bello-Monroy, C. Enriquez Cortina, R. Miranda-Labra, L.Bucio, L. E. Gomez-Quiroz, E.Rojaz-Del Castillo, M. C. Gutierrez-Ruiz, and V. Souza-Arroyo, “ Cadmium exposure exacerbates hyperlipidemia in cholesterol overloaded hepatocytes via autophagy dysregulation, ”Toxicology, 398-399, pp. 41-51,2018.
• [34]Y.Zhu,Y.Zhao,X.X.Chai,J.Zhou,M.J.Shi,Y.Zhao,Y.Tian,X.M.Wang,T.X.Ying,Q.Feng,J.Sheng,and C.Luo, “Chronic exposure to low-dose cadmium facilitated nonalcoholic steatohepatitis in mice by suppressing fatty acid desaturation,” Ecotoxicol. Environ. Saf., vol.15, 233, 113306, 2022
• [35] FAO/WHO (1993) Evaluation of Certain Food Additives and Contaminants: Forty-first Report of the Joint FAO/WHO Expert Committee on Food Additives. WHO Technical Report Series No. 837. WHO, Geneva.
• [36] FAO/WHO (2010) Seventy-third Meeting, Geneva, 8e17 June 2010. Summary and Conclusions. JECFA/73/SC. Food and Agriculture Organization of the United Nations; World Health Organization, Geneva, Switzerland.
• [37] EFSA, “Statement on tolerable weekly intake for cadmium,” EFSA J., vol.9, 1975 (pp. 1-19), 2011.
• [38] EFSA, “Cadmium dietary exposure in the European population,” EFSA J., vol.10, 2551(pp. 1-36), 2012.
• [39] A.E. Sahmoun, L.D. Case, S.A. Jackson, and G.G. Schwartz, “Cadmium and prostate cancer: a critical epidemiologic analysis,” Cancer Investig. vol.23, pp. 256–263, 2005.
• [40] K. Martinez-Flores, V. Souza Arroyo, L. Bucio Ortiz, L.E. Gomez-Quiroz, M.C. Gutierrez-Ruiz, “Cadmio: efectos sobre la salud. Respuesta celular y molecular,” Acta Toxicol. Argent., vol. 21, no.1, pp. 33–49, 2013.
• [41] A.L. Koons, and V. Rajasurya, “Cadmium Toxicity,” Stat Pearls. Stat Pearls Publishing, Treasure Island (FL), pp. 2018–2019, 2018.
• [42] International Agency for Research on Cancer (IARC). “Cadmium and cadmium compounds. In: Arsenic, metals, fibres and dusts. A review of human carcinogens,” IARC Monographs 100C, IARC, Lyon, pp 121–145, 2012.
• [43] L. Järup, A. Rogenfelt, C.G. Elinder, K. Nogawa, and T. Kjellström, “Biological half-time of cadmium in the blood of workers after cessation of exposure,” Scand. J Work Environ. Health, vol.9, pp.327–331, 1983.
• [44] L. Jarup, and A. Akesson, “Current status of cadmium as an environmental health problem,” Toxicol. Appl. Pharmacol., vol. 238, pp. 201–208, 2009.
• [45] E.R. Siu, D.D. Mruk, C.S. Porto, C.Y. Cheng, “Cadmium-induced tes- ticular injury,” Toxicol. Appl. Pharmacol., vol. 238, pp. 240–249, 2009.
• [46] D.M. Templeton, and Y. Liu, “Multiple roles of cadmium in cell death and survival,” Chem. Biol. Interact., vol.188, pp. 267–275, 2010.
• [47] C. Fasanyaodewumi, L.M. Latinwo, C.O. Ikediobi, L. Giliard, G. Sponholtz, J. Nwoga, F. Stino, N. Hamilton, and G.V. Erdos, “The genotox- icity and cytotoxicity of dermally-administered cadmium: effects of dermal cadmium administration,” Int. J. Mol. Med., vol. 1, pp. 1001–1006, 1998.
• [48] S. Klimova, and E. Misurova, “Effects of cadmium and ionizing radiation on histones in rat testes,” Acta Vet. Brno., vol. 73, pp. 483–489, 2004.
• [49] P. Joseph, “Mechanisms of cadmium carcinogenesis,” Tox. and App. Pharm., vol. 238, pp. 272–279, 2009.
• [50] S.H. Gavett, and G. Oberdörster, “Cadmium chloride and cadmium metallothionein-induced pulmonary injury and recruitment of polymorphonuclear leukocytes,” Exp. Lung Res., vol. 20, pp. 517-37, 1994.
• [51] F. Kayama, T. Yoshida, M.R. Elwell, and M.I. Luster, “Cadmium-induced renal damage and proinflammatory cytokines: possible role of IL-6 in tubular epithelial cell regeneration,” Toxicol. Appl. Pharmacol., vol. 134, pp. 26-34, 1995.
• [52] F. Kayama, T. Yoshida, M.R. Elwell and M.I. Luster, “Role of tumor necrosis factor alpha in cadmium induced hepatotoxicity,” Toxicol. Appl. Pharmacol., vol. 131, pp. 224 234, 1995.
• [53] U.N. Das, 2011. Inflammation. In: Das UN (ed) Molecular Basis of Health and Disease. Springer Science+Business Media BV, London, pp 15–100.
• [54] M. Knoflach, B. Messner, Y.H. Shen, S. Frotschnig, G. Liu, K. Pfaller, X. Wang, B. Matosevic, J. Willeit, S. Kiechl, G, Laufer, and D. Bernhard, “Non-toxic cadmium concentrations induce vascular inflammation and promote atherosclerosis,” Circ. J., vol. 75, pp. 2491–2495, 2011.
• [55] K.E. Wellen, and G.S. Hotamisligil, “Inflammation, stress, and diabetes,” J Cli. Inv., vol. 5, pp. 1111-1119, 2005.
• [56] L.M. Coussens, and Z. Werb,“ Inflammation and cancer,” Nature, vol. 420, pp. 860–867, 2002.
• [57] M. Valko, H. Morris, and M.T.D. Cronin, “ Metals, toxicity and oxidative stress,” Curr. Med. Chem., vol.12, pp. 1161–1208, 2005.
• [58] Y.M. Go, M. Orr, and D.P. Jones, “Increased nuclear thioredoxin-1 potentiates cadmium-induced cytotoxicity,” Toxicol. Sci., vol.131, no.1, pp. 84-94, 2012.
• [59] J. Lee, and K.T. Lim, “Preventive effect of phytoglycoprotein (27 kDa) on inflammatory factors at liver injury in cadmium chloride-exposed ICR mice,” J. Cell Biochem., vol 112, pp. 694–703, 2011.
• [60] V. Souza, C. Escobar Md Mdel, L. Gómez-Quiroz, L. Bucio, E. Hernández, E.C. Cossio, and M.C. Gutiérrez-Ruiz, “Acute cadmium exposure enhances AP-1 DNA binding and induces cytokines expression and heat shock protein 70 in HepG2 cells,” Toxicology, vol.197, pp. 213–228, 2004.
• [61] M. Lag, D. Rodionov, J. Ovrevik, O. Bakke, P.E. Schwarze, and M. Refsnes, “Cadmium-induced inflammatory responses in cells relevant for lung toxicity: Expression and release of cytokines in fibroblasts, epithelial cells and macrophages,” Toxicol. Lett., vol. 193, pp. 252–260, 2010.
• [62] Kataranovski M, Mirkov I, Belij S, Nikolic M, Zolotarevski L, Ciric D, and Kataranovski D “ Lungs: remote inflammatory target of systemic cadmium administration in rats,” Environ. Toxicol. Pharmacol., vol. 28, pp. 225–231, 2009.
• [63] K.J. Tracey, “The inflammatory reflex,” Nature, vol. 420, pp.853–859, 2002.
• [64] M. Freitas, and E. Fernandes, “ Zinc, cadmium and nickel increase the activation of NF-κB and the release of cytokines from THP-1 monocytic cells,” Metallomics, vol. 3, pp.1238–1243, 2011.
• [65] E. Cormet-Boyaka, K. Jolivette, A. Bonnegarde-Bernard, J. Rennolds, F. Hassan, P Mehta, S. Tridandapani, J. Webster-Marketon, and P.N. Boyaka, “An NF-κB–independent and Erk1/2-dependent mechanism controls CXCL8/IL-8 responses of airway epithelial cells to cadmium,” Toxicol. Sci., vol. 125, pp. 418–429, 2012.
• [66] A. Cuypers, M. Plusquin, T. Remans, M. Jozefczak, E. Keunen, H. Gielen, K. Opdenakker, A.R. Nair, E. Munters, T.J. Artois, T. Nawrot, J. Vangronsveld, and K. Smeets, “ Cadmium stress: an oxidative challenge,” Biometals, vol. 23, pp. 927–940, 2010.
• [67] J. Ivanova, Y. Gluhcheva, D. Tsanova, A. Piskova, R. Djaleva, S. Mokresheva, D. Kamenova, and M. Mitewa, “On the effect of chelating agents and antioxidants on Cd induced organ toxicity An overview,” Eur. J. Chem., vol.4, pp. 74–84, 2013.
• [68] A.S. El-Sharaky, A.A. Newairy, M.M. Badreldeen, S.M. Eweda, and S.A. Sheweita, “Protective role of selenium against renal toxicity induced by cadmium in rats,” Toxicology, vol. 235, pp.185–193, 2007.
• [69] M. Jurczuk, M.M. Brzoska, J. Moniuszko-Jakoniuk, M. Galazyn-Sidorczuk, and E. Kulikowska- Karpinska, “Antioxidant enzymes activity and lipid peroxidation in liver and kidney of rats exposed to cadmium and ethanol,” Food Chem. Toxicol. vol. 42, pp. 429–438, 2004.
• [70] D. Nigam, G.S. Shukla, and A.K. Agarwal, “Glutathione depletion and oxidative damage in mitochondria following exposure to cadmium in rat liver and kidney,” Toxicol. Lett., vol. 106, pp.151–157, 1999.
• [71] V.L. Badisa, L.M. Latinwo, C.O. Odewumi, C.O. Ikediobi, R.B. Badisa, A. Brooks-Walter, A.T. Lambert, and J. Nwoga, “Cytotoxicity and stress gene microarray analysis in cadmium-exposed CRL-1439 normal rat liver cells,” Int. J. Mol. Med., vol. 22, pp. 213–219, 2008.
• [72] S. Nemmiche, D. Chabane-Sari, P. Guiraud, “Role of alpha-tocopherol in cadmiuminduced oxidative stress in Wistar rat's blood, liver and brain,” Chem. Biol. Interact., vol.170, no. 3, pp. 221–230, 2007.
• [73] M. Taşdemir, F.Ç. Çelikezen, G. Oto, and F. Özbey, “The effects of pretreatment with lithium metaborate dihydrate on lipid peroxidation and Ca, Fe, Mg, and K levels in serum of wistar albino male rats exposed to Cd,” Env. Sci. and Poll. Res., vol. 27, pp. 7702–7711, 2020.
• [74] K. Athmounia, D. Belhaja, A. El Feki, and H. Ayadi, “Optimization, antioxidant properties and GC–MS analysis of Periploca angustifolia polysaccharides and chelation therapy on cadmium-induced toxicity in human HepG2 cells line and rat liver,” Int. J. Biol. Macromol., vol.108, pp. 853–862, 2018.
• [75] M. Ahmada, G.M. Abu Taweel, and S. Hidayathulla, “Nano-composites chitosan-curcumin synergistically inhibits the oxidative stress induced by toxic metal cadmium,” Int. J. Biol. Macromol., vol. 108, pp. 591–597, 2018.
• [76] J. Xie, Z.A. Shaikh, “Cadmium-induced apoptosis in rat kidney epithelial cells involves decrease in nuclear factor-kappa B activity,” Toxicol. Sci., vol. 91, pp. 299–308, 2006.
• [77] M. Hettiarachchi, C. Liyanage, R. Wickremasinghe, D.C. Hilmers, and S.A. Abrams, “The efficacy of micronutrient supplementation in reducing the prevalence of anaemia and deficiencies of zinc and iron among adolescents in Sri Lanka,” Eur. J. Clin. Nutr., vol. 62, pp. 856–65, 2008.
• [78] I.J. Griffin, S.C. Kim, P.D. Hicks, L.K. Liang, and S.A. Abrams, “Zinc metabolism in adolescents with Crohn’s disease,” Pediatr. Res., vol. 56, pp. 235–239, 2004.
• [79] S.A. Abrams, “Assessing mineral metabolism in children using stable isotopes,” Pediatr. Blood Can., vol. 50, pp. 438–41, 2008.
• [80] S.L. Sensi, and J.M. Jeng, “Rethinking the excitotoxic ionic milieu: the emerging role of Zn(2+) in ischemic neuronal injury,” Curr. Mol. Med. vol. 4, pp. 87–111, 2004.
• [81] I. Korichneva, B. Hoyos, R. Chua, E. Levi, and U. Hammerling, “Zinc release from protein kinase C as the common event during activation by lipid second messenger or reactive oxygen,” J. Biol. Chem., vol. 277, pp. 44327–44331, 2002.
• [82] I. Korichneva, “Zinc dynamics in the myocardial redox signaling network,” Antioxid Redox Signal., vol. 8, pp. 1707–1721, 2006.
• [83] R.D. Palmiter, and S.D. Findley, “Cloning and functional characterization of a mammalian zinc transporter that confers resistance to zinc,” EMBO J., vol. 14, pp. 639–649, 1995.
• [84] S.L. Sensi, D. Ton-That, and J.H. Weiss, “Mitochondrial sequestration and Ca(2+)-dependent release of cytosolic Zn(2+) loads in cortical neurons,” Neurobiol. Dis., vol. 10, pp. 100–108, 2002.
• [85] S.R. Powell, L. Aiuto, D. Hall, and A.J. Tortolani, “Zinc supplementation enhances the effectiveness of St. Thomas’ Hospital No. 2 cardioplegic solution in an in vitro model of hypothermic cardiac arrest,” J. Thorac. Cardiovasc. Surg., vol. 110, pp.1642–1648, 1995.
• [86] A.S. Prasad, “Zinc is an antioxidant and anti-inflammatory agent: its role in human health,” Front. Nutr., vol. 1, pp. 1-14, 2014.
• [87] B.L. Vallee, and D.S. Auld, “Zinc coordination, function, and structure of zinc enzymes and other proteins,” Biochemistry, vol. 29, pp. 5647–5659, 1990.
• [88] F. Chimienti, M. Seve, S. Richard, J. Mathieu, and A. Favier, “Role of cellular zinc in programmed cell death: temporal relationship between zinc depletion, activation of caspases, and cleavage of Sp family transcription factors,” Biochem. Pharmacol., vol. 62, pp. 51–62, 2001.
• [89] J. Lemire, R. Mailloux, and V.D. Appanna, “Zinc toxicity alters mitochondrial metabolism and leads to decrease ATP production in hepatocytes,” J. Appl. Toxicol., vol. 28, pp. 175–182, 2008.
• [90] M.O. Parat, M.J. Richard, J.C. Beani, and A. Favier, “Involvement of zinc in intracellular oxidant/antioxidant balance,” Bio. Trace Elem. Res., vol. 60, pp.187–204, 1997.
• [91] A. Meister, M.E. Anderson, “Glutathione,” Annu Rev. Biochem., vol. 52, pp. 711–760, 1983.
• [92] S.R. Powell, “Antioxidant properties of zinc,” J. Nutr., vol. 130, pp.1447–1454, 2000.
• [93] M. Bicer, M. Günay, A.K. Baltacı, K. Uney, R. Mogulkoc, and M. Akil, “Effect of zinc supplementation on lipid peroxidation and lactate levels in rats with diabetes induced by streptozotocin and subjected to acute swimming exercise,” Bratisl. Lek. Listy., vol.113, pp.199–205, 2012.
• [94] M. Dżugan, M.W. Lis, M. Droba, and J.W. Niedziółka, “Protective effect of zinc on cadmium embryotoxicity and antioxidant status of blood plasma in newly hatched chicks,” Environ. Lett., vol. 47, pp. 1288–1293, 2012.
• [95] F.T. Celino, S. Yamaguchi, C. Miura, T. Ohta, Y. Tozawa, T. Iwai, T. Miura “Tolerance of spermatogonia to oxidative stress is due to high levels of Zn and Cu/Zn superoxide dismutase,” PLoS One, vol. 6, no.2, e16938, 2011.
• [96] B. Bao, A. Ahmad, A. Azmi, Y. Li, A. Prasad, and F.H. Sarkar, “The biological significance of zinc in inflammation and aging. In: Rahman I, Bagchi D (eds). Inflammation, advancing age and nutrition. Academic Press, San Diego, pp 15-27, 2014.
• [97] Y. Sheng, I.A. Abreu, D.E. Cabelli, M.J. Maroney, A.F. Miller, M. Teixeira, and J.S. Valentine, “Superoxide dismutases and superoxide reductases,” Chem. Rev., vol.114, pp. 3854–3918, 2014.
• [98] Z.E. Suntres, and E.M. Lui, “Biochemical mechanism of metallothionein –carbon tetrachloride interaction in vitro,” Biochem. Pharmacol., vol. 39, no.5, pp. 833-840, 1990.
• [99] M. Cabre, J. Camps, N. Ferre, J.L. Paternain, and J. Joven, “The antioxidant and hepatoprotective effects of zinc are related to hepatic cytochrome P450 depression and metallothionein induction in rats with experimental cirrhosis,” Int. J. Vitam. Nutr. Res., vol. 71, pp. 229-236, 2001.
• [100] H.T. Abul, T.C. Mathew, F. Abul, H. Al-Sayer, and H.M. Dashti, “Antioxidant enzyme level in the testes of cirrhotic rats,” Nutr., vol.18, pp. 56-59, 2002.
• [101] A. Kojima-Yuasa, T. Ohkita, K. Yukami, H. Ichikawa, N. Takami, T. Nakatani, D.O. Kennedy, S. Nishiguchi, and I. Matsui-Yuasa, “Involvement of intracellular glutathione in zinc deficiency induced activation of hepatic stellate cells,” Chem. Biol. Interact., vol. 146, pp. 89-99, 2003.
• [102] K. Jomova and M. Valko, “Advances in metal-induced oxidative stress and human disease,” Toxicology, vol. 283, pp. 65–87, 2011.
• [103] P. Coyle, J.C. Philcox, L.C. Carey, and A.M. Rofe, “Metallothionein: the multipurpose protein,” Cell. Mol. Life Sci., vol.59, pp. 627–647, 2002.
• [104] G.K. Andrews, “Regulation of metallothionein gene expression by oxidative stress and metal ions,” Biochem. Pharmacol., vol.59, pp. 95–104, 2000.
• [105] R.J. Cousins, and L.M. Lee-Ambrose, “Nuclear zinc uptake and interactions andmetallothionein gene expression are influenced by dietary zinc in rats,” J. Nutr., vol. 122, pp. 56–64, 1992.
• [106] S. Bodiga, and M.N. Krishnapillai, “Concurrent repletion of iron and zinc reduces intestinal oxidative damage in iron- and zinc-deficient rats,” World J. Gastroenterol, vol. 13, pp. 5707–5717, 2007.
• [107] S.R. Davis, and R.J. Cousins, “Metallothionein expression in animals: a physiological perspective on function,” J. Nutr., vol.130, pp. 1085–1088, 2000.
• [108] C.D. Klaassen, J. Liu, and S. Choudhuri, “Metallothionein: an intracellular protein to protect against Cadmium Toxicity,” Annu Rev. Pharmacol. Toxicol., vol.39, pp. 267-294, 1999.
• [109] M.P. Waalkes, “Cadmium carcinogenesis,” Mutat. Res., vol. 533, pp. 107–120, 2003.
• [110] A.M. Sandbichler, and M. Hockner, “Cadmium protection strategiesea hidden trade-off,” Int. J. Mol. Sci., vol.17, no.1, pp. 139, 2016.
• [111] N. Babaknejad, A.A. Moshtaghie, H. Nayeri, M. Hani, S. Bahrami, “ Protective role of zinc and magnesium against cadmium nephrotoxicity in male wistar rats,” Biol. Trace. Elem. Res. vol.174, no.1, pp.112-120, 2016.
• [112] L. Said, M. Banni, A. Kerkeni, K. Said, and I. Messaoudi, “ Influence of combined treatment with zinc and selenium on cadmium induced testicular pathophysiology in rat,” Food Chem. Toxicol., vol. 48, no. 10, pp. 2759-2765, 2010.
• [113] V. Souza, C. Escobar Mdel, L. Bucio, E. Hernandez, and M.C. Gutierrez-Ruiz, “Zinc pretreatment prevents hepatic stellate cells from cadmium-produced oxidative damage,” Cell Biol. Toxicol., vol. 20, pp. 241–251, 2004.
• [114] M.G. Sidorczuk, M.M. Brzóska, J. Rogalska, A. Roszczenko, and M. Jurczuk, “Effect of zinc supplementation on glutathione peroxidase activity and selenium concentration in the serum, liver and kidney of rats chronically exposed to cadmium,” J. Trace Elem.Med. Bio., vol. 26, pp. 46– 52, 2012.
• [115] I. Messaoudi, M. Banni, L. Saïd, K. Saïd, and A. Kerkeni, “Evaluation of involvement of testicular metallothionein gene expression in the protective effect of zinc against cadmium-induced testicular pathophysiology in rat,” Reprod. Toxicol., vol.29, pp. 339–345, 2010.
• [116] Md.M. Rahman, K.F. Binte Hossain, S. Banik, Md.T. Sikder, M. Akter, S.E. Corpus Bondad, Md.S. Rahaman, T. Hosokawa, T. Saito, and M. Kurasaki, “Selenium and zinc protections against metal-(loids)-induced toxicity and disease manifestations: A review,” Ecotox. and Env. Safety, vol. 168,pp. 146–163, 2019.
• [117] I. Messaoudia, F. Hammoudab, J. Ji El Heni, T. Baati, K. Said, and A. Kerkeni, “Reversal of cadmium-induced oxidative stress in rat erythrocytes by selenium, zinc or their combination,” Exp. Tox. Path., vol. 62, pp. 281–288, 2010.
• [118] H. Jemai, H.A. Lachkar, I. Messaoudi, and A. Kerkeni, “Effects of zinc pre-treatment on blood glutathione, serum zinc and kidney histological organisation in male rats exposed to cadmium,” J Trace Elem. Med. Bio., vol. 24, pp. 277–282, 2010.
• [119] E.H. Jihen, H. Fatima, A. Nouha, T. Baati, M. Imed, and K. Abdelhamid, “Cadmium retention increase: A probable key mechanism of the protective effect of zinc on cadmium-induced toxicity in the kidney,” Toxicol. Lett., vol. 196, pp. 104–109, 2010.
• [120] E.H. Jihen, S. Sonia, H. Fatima, M.S. Tahar, and K. Abdelhamid, “Interrelationships between cadmium, zinc and antioxidants in the liver of the rat exposed orally to relatively high doses of cadmium and zinc,” Ecotoxic and Env. Safety, vol. 74, pp. 2099–2104, 2011.
• [121] M.M. Brzóska, and J. Rogalska, “Protective effect of zinc supplementation against cadmium-induced oxidative stress and the RANK/RANKL/OPG system imbalance in the bone tissue of rats,” Tox. App. Pharm., vol. 272, no. 208–220, 2013.
• [122] H. Ebaid, I. Hassan, S. Bashandy, N.A. Taha, A. Mahmood, S. Alomar, I. Alhazza, A. Mashaly, and A. Rady, “Zinc improves the immune function and the proliferation of lymphocytes in cadmium-treated rats. Experimental immunology,” Centr. Eur. J. Immunol., vol. 39, no. 4, pp. 441-448, 2014.
• [123] S.B. Mimouna, S. Boughammoura, M. Chemek, Z. Haouas, M. Banni, I. Messaoudi, “Disruption of the zinc metabolism in rat foetal brain after prenatal exposure to cadmium,” Chem. Bio. Int., vol. 286, pp. 88–95, 2018.
• [124] S.A.M. Bashandy, E.A.A. Omara, H. Ebaid, M.M. Amin, and M.S. Soliman, “Role of zinc as an antioxidant and anti-inflammatory to relieve cadmium oxidative stress induced testicular damage in rats,” Asian Pac. J. Trop Biomed., vol. 6, no.12, pp.1056–1064, 2016.
• [125] J. Rogalska, B.P. Marcinkiewicz, and M.M. Brzoska, “Protective effect of zinc against cadmium hepatotoxicity depends on this bioelement intake and level of cadmium exposure: A study in a rat model,” Chem. Bio. Interac., vol. 193, pp. 191–203, 2011.