Ascorbic acid supplementation suppresses cadmium-derived alterations in the fission yeast Schizosaccharomyces pombe

Authors

  • Marek Kovár Slovak University of Agriculture, Faculty of Agrobiology and Food Resources, Department of Plant Physiology, Trieda A. Hlinku 2, 949 76 Nitra, Slovakia, Tel.: +421376414440 https://orcid.org/0000-0002-1478-8383
  • Alica Navrátilová Slovak University of Agriculture, Faculty of Agrobiology and Food Resources, Department of Genetics and Breeding Biology, Trieda A. Hlinku 2, 949 76 Nitra, Slovakia, Tel.: +421376414296 https://orcid.org/0000-0002-8447-5016
  • Anna Trakovická Slovak University of Agriculture, Faculty of Agrobiology and Food Resources, Department of Genetics and Breeding Biology, Trieda A. Hlinku 2, 949 76 Nitra, Slovakia, Tel.: +421376414285 https://orcid.org/0000-0002-6708-2384
  • Miroslava Požgajová Slovak University of Agriculture, AgroBioTech Research Center, Trieda A. Hlinku 2, 949 76 Nitra, Slovakia, Tel.: +421376414919 https://orcid.org/0000-0003-3713-0717

DOI:

https://doi.org/10.5219/1618

Keywords:

cell, cadmium, ascorbic acid, oxidative stress, contamination

Abstract

Cadmium (Cd) a highly toxic environmental pollutant, that does not have any physiological function in the organism, represents a great concern for human health as it can be easily transported from its environmental sources to the food chain. Food, water, and air are the major sources of Cd exposure to the population. Cd-mediated impairments of the basic cellular properties largely depend on its ability to enhance the formation of reactive oxygen species (ROS) and thus triggers oxidative stress to the cell. With the use of fission yeast Schizosaccharomyces pombe (S. pombe) as the model organism, we have analyzed the impact of Cd on the cell growth intensity, as it represents the fundamental feature of all living organisms. Cells were incubated with different Cd concentrations for 3, 6, and 9 hours to investigate the effect of Cd on cell growth in a time and dose-dependent manner. Further possible Cd-derived alterations, as the peroxidation of membrane lipids or the functional impairment of the enzymatic antioxidant protection mechanisms, were investigated by determination of the MDA content and via catalase (CAT) activity detection. Moreover, ascorbic acid (AsA) pre-treatment was subjected to investigate the assumed positive effect of AsA against Cd toxicity. We show here on one hand that cells suffer under the influence of Cd, but on the other hand, they substantially profit from AsA supplementation. Because S. pombe is known to shares many molecular, and biochemical similarities with higher organisms, the effect of AsA in cadmium toxicity elimination might be expected to a similar extent also in other cell types.

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References

Abedi, T., Mojiri, A. 2020. Cadmium Uptake by Wheat (Triticum aestivum L.): An Overview. Plants, vol. 9, no. 4, 14 p. https://doi.org/10.3390/plants9040500

Aebi, H. 1984. Catalase in vitro. Methods in Enzymology, vol. 105, p. 121-126. https://doi.org/10.1016/S0076-6879(84)05016-3

Awan, A. R., Manfredo, A., Pleiss, J. A. 2013. Lariat sequencing in a unicellular yeast identifies regulated alternative splicing of exons that are evolutionarily conserved with humans. Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 31, p. 12762-12767. https://doi.org/10.1073/pnas.1218353110

Boudebbouz, A., Boudalia, S., Bousbia, A., Habila, S., Boussadia, M. I., Gueroui, Y. 2021. Heavy metals levels in raw cow milk and health risk assessment across the globe: A systematic review. Science of The Total Environment, vol. 751, 15 p. https://doi.org/10.1016/j.scitotenv.2020.141830

Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, vol. 72, no. 1-2, p. 248-254. https://doi.org/10.1016/0003-2697(76)90527-3

Chen, N., Su, P., Wang, M., Li, Y. M. 2018. Ascorbic acid inhibits cadmium-induced disruption of the blood-testis barrier by regulating oxidative stress-mediated p38 MAPK pathways. Environmental Science and Pollution Research, vol. 25, p. 21713-21720. https://doi.org/10.1007/s11356-018-2138-4

Chiocchetti, G. M., Latorre, T., Clemente, M. J., Jadán-Piedra, C., Devesa, V., Vélez, D. 2020. Toxic trace elements in dried mushrooms: Effects of cooking and gastrointestinal digestion on food safety. Food Chemistry, vol. 306, 7 p. https://doi.org/10.1016/j.foodchem.2019.125478

Chunhabundit, R. 2016. Cadmium Exposure and Potential Health Risk from Foods in Contaminated Area, Thailand. Toxicological Research, vol. 32, no. 1, p. 65-72. https://doi.org/10.5487/TR.2016.32.1.065

Ćwieląg-Drabek, M., Piekut, A., Gut, K., Grabowski, M. 2020. Risk of cadmium, lead and zinc exposure from consumption of vegetables produced in areas with mining and smelting past. Scientific Reports, vol. 10, no. 1, 9 p. https://doi.org/10.1038/s41598-020-60386-8

Darwish, W. S., Chiba, H., Elhelaly, A. E., Hui, S. P. 2019. Estimation of cadmium content in Egyptian foodstuffs: Health risk assessment, biological responses of human HepG2 cells to food-relevant concentrations of cadmium, and protection trials using rosmarinic and ascorbic acids. Environmental Science and Pollution Research, vol. 26, no. 15, p. 15443-15457. https://doi.org/10.1007/s11356-019-04852-5

Erdogan, Z., Erdogan, S., Celik, S., Unlu, A. 2005. Effects of ascorbic acid on cadmium-induced oxidative stress and performance of broilers. Biological Trace Element Research, vol. 104, no. 1, p. 19-31. https://doi.org/10.1385/BTER:104:1:019

Fatima, G., Raza, A. M., Hadi, N., Nigam, N., Mahdi, A. A. 2019. Cadmium in Human Diseases: It’s More than Just a Mere Metal. Indian Journal of Clinical Biochemistry, vol. 34, no. 4, p. 371-378. https://doi.org/10.1007/s12291-019-00839-8

Fawcett, J. A., Iida, T., Takuno, S., Sugino, R. P., Kado, T., Kugou, K., Mura, S., Kobayashi, T., Ohta, K., Nakayama, J., Innan, H. 2014. Population Genomics of the Fission Yeast Schizosaccharomyces pombe. PLOS ONE, vol. 9, no. 8, 12 p. https://doi.org/10.1371/journal.pone.0104241

Forsburg, S. L., Rhind, N. 2006. Basic methods for fission yeast. Yeast, vol. 23, no. 3, p. 173-183. https://doi.org/10.1002/yea.1347

Ganguly, K., Levänen, B., Palmberg, L., Åkesson, A., Lindén, A. 2018. Cadmium in tobacco smokers: A neglected link to lung disease? European Respiratory Review, vol. 27, 8 p. https://doi.org/10.1183/16000617.0122-2017

Garre, E., Raginel, F., Palacios, A., Julien, A., Matallana, E. 2010. Oxidative stress responses and lipid peroxidation damage are induced during dehydration in the production of dry active wine yeasts. International Journal of Food Microbiology, vol. 136, no. 3 p. 295-303. https://doi.org/10.1016/j.ijfoodmicro.2009.10.018

Genchi, G., Sinicropi, M. S., Lauria, G., Carocci, A., Catalano, A. 2020. The Effects of Cadmium Toxicity. International Journal of Environmental Research and Public Health, vol. 17, no. 11, 24 p. https://doi.org/10.3390/ijerph17113782

Hamid, Y., Tang, L., Sohail, M. I., Cao, X., Hussain, B., Aziz, M. Z., Usman, M., He, Z., Yang, X. 2019. An explanation of soil amendments to reduce cadmium phytoavailability and transfer to food chain. Science of The Total Environment, vol. 660, p. 80-96. https://doi.org/10.1016/j.scitotenv.2018.12.419

Huang, Y., He, C., Shen, C., Guo, J., Mubeen, S., Yuan, J., Yang, Z. 2017. Toxicity of cadmium and its health risks from leafy vegetable consumption. Food & Function, vol. 8. no. 4, p. 1373-1401. https://doi.org/10.1039/C6FO01580H

Jarosz‐Krzemińska, E., Mikołajczyk, N., Adamiec, E. 2020. Content of toxic metals and As in marine and freshwater fish species available for sale in EU supermarkets and health risk associated with its consumption. Journal of the Science of Food and Agriculture, vol. 101, no. 7, p. 2818-2827. https://doi.org/10.1002/jsfa.10911

Jung, H. I., Lee, B. R., Chae M. J., Lee, E. J., Lee, T. G., Jung, G. B., Kim, M. S., Lee, J. 2020. Ascorbate-mediated modulation of cadmium stress responses: reactive oxygen species and redox status in Brassica napus. Frontiers in Plant Science, vol. 11, 15 p. https://doi.org/10.3389/fpls.2020.586547

Khojastehfar, A., Aghaei, M., Gharagozloo, M., Panjehpour, M. 2015. Cadmium induces reactive oxygen species-dependent apoptosis in MCF-7 human breast cancer cell line. Toxicology Mechanisms and Methods, vol. 25, no. 1, p. 48-55. https://doi.org/10.3109/15376516.2014.985353

Kippler, M., Bakhtiar Hossain, M., Lindh, C., Moore, S. E., Kabir, I., Vahter, M., Broberg, K. 2012. Early life low-level cadmium exposure is positively associated with increased oxidative stress. Environmental Research, vol. 112, p. 164-170. https://doi.org/10.1016/j.envres.2011.11.012

Kosečková, P., Zvěřina, O., Pruša, T., Coufalík, P., Hrežová, E. 2020. Estimation of cadmium load from soybeans and soy-based foods for vegetarians. Environmental Monitoring and Assessment, vol. 192, no. 2, 7 p. https://doi.org/10.1007/s10661-019-8034-7

Kubová, J., Tulinská, J., Štolcová, E., Mošaťová, A., Ginter, E. 1993. The influence of ascorbic acid on selected parameters of cell immunity in guinea pigs exposed to cadmium. Zeitschrift Fur Ernahrungswissenschaft, vol. 32, no. 2, p. 113-120. https://doi.org/10.1007/BF01614754

Li, Q., Wang, G., Wang, Y., Yang, D., Guan, C., Ji, J. 2019. Foliar application of salicylic acid alleviate the cadmium toxicity by modulation the reactive oxygen species in potato. Ecotoxicology and Environmental Safety, vol. 172, p. 317-325. https://doi.org/10.1016/j.ecoenv.2019.01.078

Lin, L., Zhou, W., Dai, H., Cao, F., Zhang, G., Wu, F. 2012. Selenium reduces cadmium uptake and mitigates cadmium toxicity in rice. Journal of Hazardous Materials, vol. 235-236, p. 343-351. https://doi.org/10.1016/j.jhazmat.2012.08.012

Liu, J., Qu, W., Kadiiska, M. B. 2009. Role of oxidative stress in cadmium toxicity and carcinogenesis. Toxicology and Applied Pharmacology, vol. 238, no. 3, p. 209-214. https://doi.org/10.1016/j.taap.2009.01.029

Liu, L., Han, J., Xu, X., Xu, Z., Abeysinghe, K. S., Atapattu, A. J., De Silva, P. M. C. S., Lu, Q., Qiu, G. 2020. Dietary exposure assessment of cadmium, arsenic, and lead in market rice from Sri Lanka. Environmental Science and Pollution Research, vol. 27, no. 34, p. 42704-42712. https://doi.org/10.1007/s11356-020-10209-0

Liu, Z., Ding, Y., Wang, F., Ye, Y., Zhu, C. 2016. Role of salicylic acid in resistance to cadmium stress in plants. Plant Cell Reports, vol. 35, no. 4, p. 719-731. https://doi.org/10.1007/s00299-015-1925-3

Modareszadeh, M., Bahmani, R., Kim, D., Hwang, S. 2021. CAX3 (cation/proton exchanger) mediates a Cd tolerance by decreasing ROS through Ca elevation in Arabidopsis. Plant Molecular Biology, vol. 105, no. 1, 115-132. https://doi.org/10.1007/s11103-020-01072-1

Nagyova, A., Galbavy, S., Ginter, E. 1994. Histopathological evidence of vitamin C protection against Cd-nephrotoxicity in guinea pigs. Experimental and Toxicologic Pathology, vol. 46, no. 1, p. 11-14. https://doi.org/10.1016/S0940-2993(11)80005-9

Okereafor, U., Makhatha, M., Mekuto, L., Uche-Okereafor, N., Sebola, T., Mavumengwana, V. 2020. Toxic Metal Implications on Agricultural Soils, Plants, Animals, Aquatic life and Human Health. International Journal of Environmental Research and Public Health, vol. 17, no. 7, 24 p. https://doi.org/10.3390/ijerph17072204

Pekmez, M., Arda, N., Hamad, İ., Kiğ, C., Temizkan, G. 2008. Hydrogen peroxide-induced oxidative damages in Schizosaccharomyces pombe. Biologia, vol. 63, no. 2, p. 151-155. https://doi.org/10.2478/s11756-008-0040-0

Quest Graph™ IC50 Calculator. AAT Bioquest, Inc, [online] [cit.2021-04-30], Available at: https://www.aatbio.com/tools/ic50-calculator

Requena, J. R., Fu, M. X., Ahmed, M. U., Jenkins, A. J., Lyons, T. J., Thorpe, S. R. 1996. Lipoxidation products as biomarkers of oxidative damage to proteins during lipid peroxidation reactions. Nephrology Dialysis Transplantation, vol. 11, no. 5, p. 48-53. https://doi.org/10.1093/ndt/11.supp5.48

Sandalio, L. M., Dalurzo, H. C., Gómez, M., Romero‐Puertas, M. C., del Río, L. A. 2001. Cadmium‐induced changes in the growth and oxidative metabolism of pea plants. Journal of Experimental Botany, vol. 52, no. 364, p. 2115-2126. https://doi.org/10.1093/jexbot/52.364.2115

Satapathy, S., Panda, C. R., Jena, B. S. 2019. Risk-based prediction of metal toxicity in sediment and impact on human health due to consumption of seafood (Saccostrea cucullata) found in two highly industrialised coastal estuarine regions of Eastern India: A food safety issue. Environmental Geochemistry and Health, vol. 41, no. 5, p. 1967-1985. https://doi.org/10.1007/s10653-019-00251-4

Singh, S., Singh, A., Srivastava, P. K., Prasad, S. M. 2018. Cadmium toxicity and its amelioration by kinetin in tomato seedlings vis-à-vis ascorbate-glutathione cycle. Journal of Photochemistry and Photobiology B: Biology, vol. 178, p. 76-84. https://doi.org/10.1016/j.jphotobiol.2017.10.025

Suwatvitayakorn, P., Ko, M. S., Kim, K. W., Chanpiwat, P. 2019. Human health risk assessment of cadmium exposure through rice consumption in cadmium-contaminated areas of the Mae Tao sub-district, Tak, Thailand. Environmental Geochemistry and Health, vol. 42, p. 2331-2344. https://doi.org/10.1007/s10653-019-00410-7

Tang, H., Liu, Y., Gong, X., Zeng, G., Zheng, B., Wang, D., Sun, Z., Zhou, L., Zeng, X. 2015. Effects of selenium and silicon on enhancing antioxidative capacity in ramie (Boehmeria nivea (L.) Gaud.) under cadmium stress. Environmental Science and Pollution Research, vol. 22. no. 13, p. 9999-10008. https://doi.org/10.1007/s11356-015-4187-2

Tinkov, A. A., Gritsenko, V. A., Skalnaya, M. G., Cherkasov, S. V., Aaseth, J., Skalny, A. V. 2018. Gut as a target for cadmium toxicity. Environmental Pollution, vol. 235, p. 429-434. https://doi.org/10.1016/j.envpol.2017.12.114

Venkatesh, J., Park, S. W. 2014. Role of L-ascorbate in alleviating abiotic stresses in crop plants. Botanical Studies, vol. 55, no. 1, 19 p. https://doi.org/10.1186/1999-3110-55-38

Wang, Q. W., Wang, Y., Wang, T., Zhang, K. B., Yuan, Y., Bian, J. C., Liu, X. Z., Gu, J. H., Zhu, J. Q., Liu, Z. P. 2015. Cadmium-induced autophagy is mediated by oxidative signaling in PC-12 cells and is associated with cytoprotection. Molecular Medicine Reports, vol. 12, no 3, p. 4448-4454. https://doi.org/10.3892/mmr.2015.3907

Wang, X., Wang, T., Pan, T., Huang, M., Ren, W., Xu, G., Amin, H. K., Kassab, R. B., Abdel Moneim, A. E. 2020. Senna alexandrina extract supplementation reverses hepatic oxidative, inflammatory, and apoptotic effects of cadmium chloride administration in rats. Environmental Science and Pollution Research, vol. 27, no. 6, 5981-5992. https://doi.org/10.1007/s11356-019-07117-3

Wang, Y., Yang, R., Zheng, J., Shen, Z., Xu, X. 2019. Exogenous foliar application of fulvic acid alleviate cadmium toxicity in lettuce (Lactuca sativa L.). Ecotoxicology and Environmental Safety, vol. 167, p. 10-19. https://doi.org/10.1016/j.ecoenv.2018.08.064

Wu, H., Liao, Q., Chillrud, S. N., Yang, Q., Huang, L., Bi, J., Yan, B. 2016. Environmental Exposure to Cadmium: Health Risk Assessment and its Associations with Hypertension and Impaired Kidney Function. Scientific Reports, vol. 6, no. 1, 9 p. https://doi.org/10.1038/srep29989

Xu, P., Guo, H., Wang, H., Lee, S. C., Liu, M., Pan, Y., Zheng, J., Zheng, K., Wang, H., Xie, Y., Bai, X., Liu, Y., Zhao, M., Wang, L. 2019. Downregulations of placental fatty acid transporters during cadmium-induced fetal growth restriction. Toxicology, vol. 423, p. 112-122. https://doi.org/10.1016/j.tox.2019.05.013

Yamada, H., Uenishi, R., Suzuki, K., Koizumi, S. 2009. Cadmium-induced alterations of gene expression in human cells. Environmental Toxicology and Pharmacology, vol. 28, no. 1, p. 61-69. https://doi.org/10.1016/j.etap.2009.02.007

Zhang, K., Wang, G., Bao, M., Wang, L., Xie, X. 2019. Exogenous application of ascorbic acid mitigates cadmium toxicity and uptake in Maize (Zea mays L.). Environmental Science and Pollution Research, vol. 26, no. 19, p. 19261-19271. https://doi.org/10.1007/s11356-019-05265-0

Zhuang, J., Nie, G., Yang, F., Dai, X., Cao, H., Xing, C., Hu, G., Zhang, C. 2019. Cadmium induces cytotoxicity through oxidative stress-mediated apoptosis pathway in duck renal tubular epithelial cells. Toxicology in Vitro, vol. 61, 10 p. https://doi.org/10.1016/j.tiv.2019.104625

Published

2021-05-28

How to Cite

Kovár, M., Navrátilová, A., Trakovická, A., & Požgajová, M. (2021). Ascorbic acid supplementation suppresses cadmium-derived alterations in the fission yeast Schizosaccharomyces pombe. Potravinarstvo Slovak Journal of Food Sciences, 15, 423–432. https://doi.org/10.5219/1618