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The effect of manganese nanoparticles on performance, redox reactions and epigenetic changes in turkey tissues

Published online by Cambridge University Press:  31 October 2018

K. Ognik Open the ORCID record for K. Ognik [Opens in a new window] ,
K. Kozłowski ,
A. Stępniowska ,
R. Szlązak ,
K. Tutaj ,
Z. Zduńczyk  and
J. Jankowski
K. Ognik*
Affiliation:
Department of Biochemistry and Toxicology, Faculty of Biology, Animal Sciences and Bioeconomy, University of Life Sciences in Lublin, Akademicka 13, 20-950 Lublin, Poland
K. Kozłowski
Affiliation:
Department of Poultry Science, Faculty of Animal Bioengineering, University of Warmia and Mazury, Oczapowskiego 5, 10-719 Olsztyn, Poland
A. Stępniowska
Affiliation:
Department of Biochemistry and Toxicology, Faculty of Biology, Animal Sciences and Bioeconomy, University of Life Sciences in Lublin, Akademicka 13, 20-950 Lublin, Poland
R. Szlązak
Affiliation:
Institute of Agrophysics, Polish Academy of Sciences, Doświadczalna 4, 20-290 Lublin, Poland
K. Tutaj
Affiliation:
Centre for Innovative Research in Medical and Natural Sciences, Faculty of Medicine, University of Rzeszów, Warzywna 1a, 35-310 Rzeszów, Poland
Z. Zduńczyk
Affiliation:
Institute of Animal Reproduction and Food Research, Polish Academy of Sciences, Tuwima 10, 10–748 Olsztyn, Poland
J. Jankowski
Affiliation:
Department of Poultry Science, Faculty of Animal Bioengineering, University of Warmia and Mazury, Oczapowskiego 5, 10-719 Olsztyn, Poland
*
†E-mail: kasiaognik@poczta.fm
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Abstract

The hypothesis of the research was the assumption, that manganese nanoparticles can affect the body in the same way as macromolecules. Their smaller size and greater biological reactivity will potentially allow the Mn addition to the diet to be reduced and, consequently, less excretion of this element into the environment. The aim of the study was to determine whether the use of Mn nanoparticles would make it possible to reduce the level of this micronutrient added to turkey diets without adversely affecting redox reactions in cells and epigenetic changes. The experiment was conducted on six groups with 10 replications, in a two-factor design with three dosages of manganese: 100, 50 and 10 mg/kg, and two sources: manganese oxide (MnO) and manganese nanoparticles (NP-Mn2O3). Markers of oxidative stress determined in the blood, that is, the concentration of lipid hydroperoxides, malondialdehyde, protein carbonyl derivatives, 3-nitrotyrosine, 8-hydroxydeoxyguanosine, total glutathione, superoxide dismutase, glutathione peroxidase, catalase, ceruloplasmin, total antioxidant status, albumin and vitamin C content. The level of epigenetic changes in the blood was determined by analysing global DNA methylation. In the experiment, in which the diet of turkeys was supplemented with two forms of Mn (MnO or NP-Mn2O3) at three dosages: 100, 50 and 10 mg/kg, the 10 mg/kg dose, especially in the form of NP-Mn2O3, induced lipid oxidation reactions to the greatest extent. Irrespective of the dosage of Mn in the turkey diet, Mn in the form of NP-Mn2O3 was found to reduce protein nitration more than Mn in the form of MnO. Reducing the Mn dosage in the diet from 100 to 50 mg/kg and then to 10 mg/kg is unfavourable because proportionally increases protein and DNA oxidation in cells, decreases the activity of antioxidant enzymes, and increases the level of glutathione. Reducing the dosage from 100 to 10 mg/kg increases global DNA methylation. The reduction of the Mn level, regardless of the form used, is disadvantageous, because it weakens the defense of the antioxidant system, which consequently can induce oxidative processes in the cells. Although Mn in the form of NP-Mn2O3 reduce protein nitration better than in MnO form, the use of manganese nanoparticles in turkey feeding (even in lower doses) requires further study.

Keywords

poultrynanomanganeserearingoxidationDNA methylation

Information

Type
Research Article
Information
animal , Volume 13 , Issue 6 , June 2019 , pp. 1137 - 1144
Copyright
© The Animal Consortium 2018 

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References

Asaikkuttia, A, Bhavana, PS, Vimalab, K, Karthika, M and Cheruparambathc, P 2016. Dietary supplementation of green synthesized manganese-oxide nanoparticles and its effect on growth performance, muscle composition and digestive enzyme activities of the giant freshwater prawn Macrobrachium rosenbergii . Journal of Trace Elements in Medicine and Biology 35, 7–17.Google Scholar
Bartesaghi, S, Herrera, D, Martinez, DM, Petruk, A, Demicheli, V, Trujillo, M, Marti, MA, Estrin, DA and Radi, R 2017. Tyrosine oxidation and nitration in transmembrane peptides is connected to lipid peroxidation. Archives of Biochemistry and Biophysics 622, 9–25.Google Scholar
Bartesaghi, S, Wenzel, J, Trujillo, M, Lopez, M, Joseph, J, Kalyanaraman, B and Radi, R 2010. Lipid peroxyl radicals mediate tyrosine dimerization and nitration in membranes. Chemical Research in Toxicology 23, 821–835.Google Scholar
Bertechini, A.G and Hossain, SM 1992. Requirements and bioavailability of manganese from inorganic sources. Poultry Science 71 (suppl. 1), 32–40.Google Scholar
Bozkurt, Z, Bulbul, T, Bozkurt, MF, Bulbul, A, Maralcan, G and Qeukeloglu, K 2015. Effects of organic and inorganic manganese supplementation on bone characteristics, immune response to vaccine and oxidative stress status in broiler reared under high stocking density. Kafkas Universitesi Veteriner Fakultesi Dergisi 21, 623–630.Google Scholar
Brenneman, KA, Cattley, RC, Ali, SF and Dorman, DC 1999. Manganese-induced developmental neurotoxicity in the CD rat: is oxidative damage a mechanism of action? Neurotoxicology 20, 477–487.Google Scholar
Campos, ACE, Molognoni, F, Melo, FHM, Galdieri, LC, Carneiro, CRW, D’Almeiday, V, Correa, M and Jasiulionis, MG. 2007. Oxidative stress modulates DNA methylation during melanocyte anchorage blockade associated with malignant transformation. Neoplasia 9, 1111–1121.Google Scholar
Costanzoa, M, Scolarob, L, Berlierc, G, Marengob, A, Grecchia, S, Zancanaroa, C, Malatestaa, M and Arpiccob, S 2016. Cell uptake and intracellular fate of phospholipidic manganese-based nanoparticles. International Journal of Pharmaceutics 508, 83–91.Google Scholar
Dalle-Donne, I, Scaloni, A, Giustarini, D, Cavarra, E, Tell, G, Lungarella, G, Colombo, R, Rossi, R and Milzani, A 2005. Protein as biomarkers of oxidative/ nitrosative stress in diseases: the contribution of redox proteomics. Mass Spectrometry Reviews 24, 55–99.Google Scholar
De Prins, S, Koppen, G, Jacobs, G, Dons, E, Van de Mieroop, E, Nelen, F, Fierens, V, Int Panis, L, De Boever, P, Cox, B, Nawrot, TS and Schoeters, G 2013. Influence of ambient air pollution on global DNA methylation in healthy adults: a seasonal follow-up. Environment International 59, 418–424.Google Scholar
Dotan, Y, Lichtenberg, D and Pinchuk, I 2004. Lipid peroxidation cannot be used as a universal criterion of oxidative stress. Progress in Lipid Research 43, 20–27.Google Scholar
Fu, PP, Xia, Q, Hwang, HM, Ray, PC and Yu, H 2014. Mechanisms of nanotoxicity: generation of reactive oxygen species. Journal of Food and Drug Analysis 22, 64–75.Google Scholar
Heinlaan, M, Muna, M, Juganson, K, Oriekhova, O, Stoll, S, Kahru, A and Slaveykova, VI 2017. Exposure to sublethal concentrations of Co3O4 and Mn2O3 nanoparticles induced elevated metal body burden in Daphnia magna. Aquatic Toxicology 189, 123–133.Google Scholar
Horning, KJ, Caito, SW, Tipps, KG, Bowman, AB and Aschner, M 2015. Manganese is essential for neuronal health. Annual Review of Nutrition 35, 71–108.Google Scholar
Jaenisch, R and Bird, A 2003. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nature Genetics 33, 245–254.Google Scholar
Lebovitz, RM, Zhang, H, Vogel, H, Cartwright, J, Dionne, L, Lu, N, Huang, S and Matzuk, MM 1996. Neurodegeneration, myocardial injury, and perinatal death in mitochondrial superoxide dismutase-deficient mice. Proceedings of the National Academy of Sciences of the United States of America 93, 9782–9787.Google Scholar
Li, N, Xia, T and Nel, AE 2008. The role of oxidative stress in ambient particulatematter-induced lung diseases and its implications in the toxicity of engineered nanoparticles. Free Radical Biology and Medicine 44, 1689–1699.Google Scholar
Liao, HY, Chung, YT, Lai, CH, Wang, SL, Chiang, HC, Li, LA, Tsou, TC, Li, WF, Lee, HL, Wu, WT, Lin, MH, Hsu, JH, Ho, JJ, Chen, CJ, Shih, TS, Lin, CC and Liou, SH 2014. Six-month follow-up study of health markers of nanomaterials amongworkers handling engineered nanomaterials. Nanotoxicology 8, 100–110.Google Scholar
Liou, SH, Wua, WT, Liaoa, HY, Chenb, CY, Tsaib, CY, Jungb, WT and Leeb, HL 2017. Global DNA methylation and oxidative stress biomarkers in workers exposed to metal oxide nanoparticles. Journal of Hazardous Materials 331, 329–335.Google Scholar
Lu, L, Luo, XG, Ji, C, Liu, B and Yu, SX 2007. Effect of manganese supplementation and source on carcass traits, meat quality, and lipid oxidation in broilers. Journal of Animal Science 85, 812–822.Google Scholar
Luo, XG, Su, Q, Huang, JC and Liu, JX 1992. Effects of manganese (Mn) deficiency on tissue Mn-containing superoxide dismutase (MnSOD) activity and its mitochondrial ultrastructures of broiler chicks fed a practical diet. China Journal of Animal and Veterinary Science 23, 97–101.Google Scholar
Miriyala, S, Spasojevic, I, Tovmasyan, A, Salvemini, D, Vujaskovic, Z, St Clair, D and Batinic-Haberle, I 2012. Manganese superoxide dismutase, MnSOD and its mimics. Biochimica et Biophysica Acta 1822, 794–814.Google Scholar
National Research Council (NRC) 1994. Nutrient requirements of poultry, 9th revised edition. The National Academies Press, Washington, DC, USA.Google Scholar
Ognik, K and Krauze, M 2016. The potential for using enzymatic assays to assess the health of turkeys. World’s Poultry Science Journal 72, 535–550.Google Scholar
Olgun, O 2017. Manganese in poultry nutrition and its effect on performance and eggshell quality. World’s Poultry Science Journal 73, 45–56.Google Scholar
Pelclova, D, Barosova, H, Kukutschova, J, Zdimal, V, Navratil, T, Fenclova, Z, Vlckova, S, Schwarz, J, Zikova, N, Kacer, P, Komarc, M, Belacek, J and Raman, SZ 2015. Microspectroscopy of exhaled breath condensate and urine in work ersexposed to fine and nano TiO2 particles: a cross-sectional study. Journal of Breath Research 9, 036008.Google Scholar
Powers, W and Angel, R 2008. A review of the capacity for nutritional strategies to address environmental challenges in poultry production. Poultry Science 87, 1929–1938.Google Scholar
Purdel, NC, Margina, D and Ilie, M 2014. Current methods used in the protein carbonyl assay. Annual Research and Review in Biology 4, 2015–2026.Google Scholar
Souza, JM, Peluffo, G and Radi, R 2008. Protein tyrosine nitration--functional alteration or just a biomarker. Free Radical Biology and Medicine 45, 357–366.Google Scholar
Strassburger, M, Bloch, W, Sulyok, S, Schuller, J, Keist, AF, Schmidt, A, Wenk, J, Peters, T, Wlaschek, M, Lenart, J, Krieg, T, Hafner, M, Kumin, A, Werner, S, Muller, W and Scharffetter-Kochanek, K 2005. Heterozygous deficiency of manganese superoxide dismutase results in severe lipid peroxidation and spontaneous apoptosis in murine myocardium in vivo. Free Radical Biology and Medicine 38, 1458–1470.Google Scholar
Sunder, GS, Panda, AK, Gopinalth, NCS, Mantena, VLN, Savaram, RR and Chalasani, VK 2006. Effect of supplemental manganese on mineral uptake by tissue and immune response in broiler chickens. The Journal of Poultry Science 43, 371–377.Google Scholar
Vaidya, S, Thaplyal, PAK and Ganguli, A 2011. Enhanced functionalization of Mn2O3@SiO2 core-shell nanostructures. Nanoscale Research Letters 169, 1–6.Google Scholar
Van Remmen, H, Ikeno, Y, Hamilton, M, Pahlavani, M, Wolf, N, Thorpe, SR, Alderson, NL, Baynes, JW, Epstein, CJ, Huang, TT, Nelson, J, Strong, R and Richardson, A 2003. Life-long reduction in MnSOD activity results in increased DNA damage and higher incidence of cancer but does not accelerate aging. Physiological Genomics 16, 29–37.Google Scholar
Venza, M, Visalli, M, Beninati, C, De Gaetano, GV, Teti, D and Venza, I 2015. Cellular mechanisms of oxidative stress and action in melanoma. Oxidative Medicine and Cellular Longevity 2015, 1–11.Google Scholar
Wang, Z, Cerrate, S, Yan, F, Sacakli, P and Waldroup, PW 2008. Comparison of different concentrations of inorganic trace minerals in broiler diets on live performance and mineral excretion. International Journal of Poultry Science 7, 625–629.Google Scholar