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Effects of Excess Manganese on the Oxidative Status, and the Expression of Inflammatory Factors and Heat Shock Proteins in Cock Kidneys

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Abstract

Manganese (Mn) can have adverse effects on organisms as a result of heavy or chronic exposure, including neurological damage. This study examined the effects of chronic exposure to manganese chloride (MnCl2) on various biochemical indices of inflammatory cytokines, antioxidant enzymes, and heat shock proteins (HSPs) in the kidneys of Hy-line cocks. The exposures were carried out using 600, 900, or 1800 mg/kg doses of MnCl2 administered for periods of 30, 60, and 90 days. The exposure experiments indicated that Mn concentration in the kidneys increased over time and that Mn exposure potentially caused ultrastructural changes to the cells. Treatment with Mn was seen to increase the levels of various biomarkers, including protein carbonyl group content; DNA-protein cross-links (DPCs) and the mRNA expression of inflammatory factors such as tumor necrosis factor-α (TNF-α), nuclear factor-κB p50 (NF-κB p50), cyclooxygenase-2 (COX-2), and prostaglandin E synthase (PGES). The levels of other biomarkers were found to decrease as a result of Mn exposure, including the mRNA expression of oxidation indexes such as copper-zinc superoxide dismutase (CuZn–SOD), manganese superoxide dismutase (Mn-SOD), glutathione peroxidase (GSH-Px), and catalase (CAT). Accompanying the above changes, Mn exposure was seen to result in the relative mRNA and protein expression of HSPs 90, 70, 60, 40, and 27 increasing significantly. Thus, in cock kidneys, HSPs attenuated the biological changes caused by toxic exposure to Mn. This mechanism needs further exploration.

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References

  1. Krüger AL, Snyman R, Odendaal J (2019) The impact of urban pollution on metal contamination of selected forest pockets in Cape Town, South Africa. Environ Sci Pollut Res Int 26:12537–12549. https://doi.org/10.1007/s11356-019-04679-0

    Article  CAS  PubMed  Google Scholar 

  2. Iyare PU (2019) The effects of manganese exposure from drinking water on school-age children: a systematic review. Neurotoxicol 73:1–7. https://doi.org/10.1016/j.neuro.2019.02.013

    Article  CAS  Google Scholar 

  3. Zeng H, Yin C, Zhang J, Li D (2019) Start-up of a biofilter in a full-scale groundwater treatment plant for iron and manganese removal. Int J Environ Res Public Health 16(5):698. https://doi.org/10.3390/ijerph16050698

    Article  CAS  PubMed Central  Google Scholar 

  4. Li Z, Su H, Wang L, Hu D, Zhang L, Fang J, Jin M, Fiati Kenston SS, Song X, Shi H, Zhao J, Mao G (2018) Epidemiological study on metal pollution of Ningbo in China. Int J Environ Res Public Health 15(3):424–438. https://doi.org/10.3390/ijerph15030424

    Article  CAS  PubMed Central  Google Scholar 

  5. Ellingsen DG, Shvartsman G, Bast-Pettersen R, Chashchin M, Thomassen Y, Chashchin V (2019) Neurobehavioral performance of patients diagnosed with manganism and idiopathic Parkinson disease. Int Arch Occup Environ Health 92(3):383–394. https://doi.org/10.1007/s00420-019-01415-6

    Article  PubMed  Google Scholar 

  6. Nascimento S, Baierle M, Göethel G et al (2016) Associations among environmental exposure to manganese, neuropsychological performance, oxidative damage and kidney biomarkers in children. Environ Res 147:32–43. https://doi.org/10.1016/j.envres.2016.01.035

    Article  CAS  PubMed  Google Scholar 

  7. Dos Santos NR, Rodrigues JLG, Bandeira MJ, Anjos ALDS, Araújo CFS, Adan LFF, Menezes-Filho JA (2019) Manganese exposure and association with hormone imbalance in children living near a ferro-manganese alloy plant. Environ Res 172:166–174. https://doi.org/10.1016/j.envres.2019.02.021

    Article  CAS  PubMed  Google Scholar 

  8. Yan DY, Liu C, Tan X et al (2019) Mn-induced neurocytes injury and autophagy dysfunction in alpha-synuclein wild-type and knock-out mice: highlighting the role of alpha-synuclein, Neurotox Res. https://doi.org/10.1007/s12640-019-00016-y

  9. Ferraro PM, Gambaro G, Curhan GC, Taylor EN (2018) Intake of trace metals and the risk of incident kidney stones. J Urol 199(6):1534–1539. https://doi.org/10.1016/j.juro.2018.01.077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Oladipo OO, Ayo JO, Ambali SF et al (2017) Evaluation of hepatorenal impairments in Wistar rats coexposed to low-dose lead, cadmium and manganese: insights into oxidative stress mechanism. Drug Des Dev Ther 11:2605–2619. https://doi.org/10.1080/15376516.2016.1223242

    Article  CAS  Google Scholar 

  11. Jayawardena UA, Angunawela P, Wickramasinghe DD, Ratnasooriya WD, Udagama PV (2017) Heavy metal-induced toxicity in the Indian green frog: biochemical and histopathological alterations. Environ Toxicol Chem 36(10):2855–2867. https://doi.org/10.1002/etc.3848

    Article  CAS  PubMed  Google Scholar 

  12. Shi Q, Jin X, Fan R et al (2019) Cadmium-mediated miR-30a-GRP78 leads to JNK-dependent autophagy in chicken kidney. Chemosphere 215:710–715. https://doi.org/10.1016/j.chemosphere.2018.10.019

    Article  CAS  PubMed  Google Scholar 

  13. Song X-B, Liu G, Liu F, Yan ZG, Wang ZY, Liu ZP, Wang L (2017) Autophagy blockade and lysosomal membrane permeabilization contribute to lead-induced nephrotoxicity in primary rat proximal tubular cells. Cell Death Dis 8(6):e2863. https://doi.org/10.1038/cddis.2017.262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Zhang L, Sun D, Bao Y et al (2017) Nerolidol protects against lps-induced acute kidney injury via inhibiting TLR4/NF-κB signaling Phytother Res 31(3):459-465. https://doi.org/10.1002/ptr.5770

  15. Shi Y, Hua Q, Li N, Zhao M et al (2019) Protective effects of evodiamine against LPS-induced acute kidney injury through regulation of ROS-NF-B-mediated inflammation. Evid Based Complement Alternat Med. https://doi.org/10.1155/2019/2190847

  16. Peng X, Wang Y, Li H, Fan J, Shen J, Yu X, Zhou Y, Mao H (2019) ATG5-mediated autophagy suppresses NF-κB signaling to limit epithelial inflammatory response to kidney injury. Cell Death Dis 10(4). https://doi.org/10.1038/s41419-019-1483-7

  17. Wang Y, Jiang L, He J et al (2018) The adverse effects of Se toxicity on inflammatory and immune responses in chicken spleens. Biol Trace Elem Res 185(1):170–176. https://doi.org/10.1007/s12011-017-1224-7

    Article  CAS  PubMed  Google Scholar 

  18. Tewari P, Roy R, Mishra S et al (2015) Benzanthrone induced immunotoxicity via oxidative stress and inflammatory mediators in Balb/c mice. Immunobiology 220(3):369–381. https://doi.org/10.1016/j.imbio.2014.10.011

    Article  CAS  PubMed  Google Scholar 

  19. Yu W, Zhao H, Liu J et al (2018) Copper and arsenic-induced oxidative stress and immune imbalance areassociated with activation of heat shock proteins in chicken intestines. Int Immunopharmacol 60:64–75. https://doi.org/10.1016/j.intimp.2018.04.038

    Article  CAS  Google Scholar 

  20. Smuder AJ, Morton AB, Hall SE (2019) Effects of exercise preconditioning and HSP72 on diaphragm muscle function during mechanical ventilation. J Cachexia Sarcopenia Muscle. https://doi.org/10.1002/jcsm.12427

  21. Guo D, Ma J, Li T, Yan L (2018) Up-regulation of miR-122 protects against neuronal cell death in ischemic stroke through the heat shock protein 70-dependent NF-κB pathway by targeting FOXO3. Exp Cell Res 369(1):34–42. https://doi.org/10.1016/j.yexcr.2018.04.027

    Article  CAS  PubMed  Google Scholar 

  22. Song X, Li L, Wu Y et al (2017) Functional role of inflammation in the surgical injury induced vascular remodeling of male albino rats. Cell Mol Biol (Noisy-le-grand) 63(9):8–12. https://doi.org/10.14715/cmb/2017.63.9.2

    Article  CAS  Google Scholar 

  23. Liu XF, Zhang LM, Guan HN, Zhang ZW, Xu SW (2013) Effects of oxidative stress on apoptosis in manganese-induced testicular toxicity in cocks. Food Chem Toxicol 60:168–176. https://doi.org/10.1016/j.fct.2013.07.058

    Article  CAS  PubMed  Google Scholar 

  24. Liu X, Li Z, Han C, Zhang Z, Xu S (2012) Effects of dietary manganese on Cu, Fe, Zn, Ca, Se, IL-1β, and IL-2 changes of immune organs in cocks. Biol Trace Elem Res 148:336–344. https://doi.org/10.1007/s12011-012-9377-x

    Article  CAS  PubMed  Google Scholar 

  25. Wang X, Yang A, Jiao W et al (2017) Selenium protects against Lead-induced apoptosis via endoplasmic reticulum stress in chicken kidneys. Biol Trace Elem Res 182(4):354–363. https://doi.org/10.1007/s12011-017-1097-9

    Article  CAS  PubMed  Google Scholar 

  26. Sogut O, Percin F (2011) Trace elements in the kidney tissue of Bluefin Tuna (Thunnus thynnus L.1758) Turkish seas. Afr J Biotechnol 10(7):1252–1259. https://doi.org/10.5897/AJB10.1464

    Article  CAS  Google Scholar 

  27. Li CH, Li LY, Liu F, Ning X, Chen A, Zhang L, Wu H, Zhao J (2011) Alternation of Venerupis philippinarum Hsp40 gene expression in response to pathogen challenge and heavy metal exposure. Fish Shellfish Immunol 30(1):447–450. https://doi.org/10.1016/j.fsi.2010.10.023

    Article  CAS  PubMed  Google Scholar 

  28. Sun B, Wang R, Xu SW et al (2011) Dietary selenium affects selenoprotein W gene expression in the liver of chicken. Biol Trace Elem Res 143:1516–1523. https://doi.org/10.1007/s12011-011-8995-z

    Article  CAS  PubMed  Google Scholar 

  29. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29(9):e45. https://doi.org/10.1093/nar/29.9.e45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Xing H, Liu T, Zhang Z et al (2015) Acute and subchronic toxic effects of atrazine and chlorpyrifos on common carp (Cyprinus carpio L.): immunotoxicity assessments. Fish Shellfish Immunol 45:327–333. https://doi.org/10.1016/j.fsi.2015.04.016

    Article  CAS  PubMed  Google Scholar 

  31. Nkpaa KW, Onyeso GI, Kponee KZ (2019) Rutin abrogates manganese-induced striatal and hippocampal toxicity via inhibition of iron depletion, oxidative stress, inflammation and suppressing the NF-κB signaling pathway. J Trace Elem Med Biol. https://doi.org/10.1016/j.jtemb.2019.01.014

  32. Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278. https://doi.org/10.1146/annurev.physiol.68.040104.110001

    Article  CAS  PubMed  Google Scholar 

  33. Di Giulio RT, Washburn PC, Wenning RJ et al (1989) Biochemical responses in aquatic animal: a review of determinants of oxidative stress. Environ Toxicol Chem 8(1989):1103–1123

    Article  Google Scholar 

  34. Ma Y, Zheng YX, Dong XY, Zou XT (2018) Effect of mercury chloride on oxidative stress and nuclear factor erythroid 2-related factor 2 signalling molecule in liver and kidney of laying hens. J Anim Physiol Anim Nutr (Berl) 102(5):1199–1209. https://doi.org/10.1111/jpn.12920

    Article  CAS  Google Scholar 

  35. Guo Y, Zhao P, Guo G, Hu Z, Tian L, Zhang K, Zhang W, Xing M (2015) The role of oxidative stress in gastrointestinal tract tissues induced by arsenic toxicity in cocks. Biol Trace Elem Res 168(2):490–499. https://doi.org/10.1007/s12011-015-0357-9

    Article  CAS  PubMed  Google Scholar 

  36. Ziwei Z, Zheng Z, Jingzeng C (2017) Effect of cadmium on oxidative stress and immune function of common carp (Cyprinus carpio L.) by transcriptome analysis. Aquat Toxicol 192:171–177. https://doi.org/10.1016/j.aquatox.2017.09.022

    Article  CAS  Google Scholar 

  37. Chi Q, Liu T, Sun Z, Tan S, Li S, Li S (2017) Involvement of mitochondrial pathway in environmental metal pollutant lead-induced apoptosis of chicken liver: perspectives from oxidative stress and energy metabolism. Environ Sci Pollut Res 24(36):28121–28131. https://doi.org/10.1007/s11356-017-0411-6

    Article  CAS  Google Scholar 

  38. Yang T, Cao C, Yang J et al (2018) miR-200a-5p regulates myocardial necroptosis induced by se deficiency via targeting RNF11. Redox Biol 15:159e169

    Article  Google Scholar 

  39. Wang W, Chen M, Jin X (2018) H2S induces Th1/Th2 imbalance with triggered NF-κB pathway to exacerbate LPS-induce chicken pneumonia response. Chemosphere 208:241–246. https://doi.org/10.1016/j.chemosphere.2018.05.1

    Article  CAS  PubMed  Google Scholar 

  40. Guo Y, Zhao P, Guo G, Hu Z, Tian L, Zhang K, Sun Y, Zhang X, Zhang W, Xing M (2015) Effects of arsenic trioxide exposure on heat shock protein response in the immune organs of chickens. Biol Trace Elem Res 169(1):134–141. https://doi.org/10.1007/s12011-015-0389-1

    Article  CAS  PubMed  Google Scholar 

  41. Zhao P, Zhang K, Guo G, Sun X, Chai H, Zhang W, Xing M (2015) Heat shock protein alteration in the gastrointestinal tract tissues of chickens exposed to arsenic trioxide. Biol Trace Elem Res 170(1):224–236. https://doi.org/10.1007/s12011-015-0462-9

    Article  CAS  PubMed  Google Scholar 

  42. Zhao FQ, Zhang Z-W, Wang C et al (2013) The role of heat shock proteins in inflammatory injury induced by cold stress in chicken hearts. Cell Stress Chaperones 18(6):773–783. https://doi.org/10.1007/s12192.013.0429.8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

The present research has received strong support from the postdoctoral foundation of Heilongjiang province(LBH-Z15200), Habin University of Commerce level scientific research projects (17XN023), The National Science Foundation (No. 31301602 and 31201376), the key organization project of the Ministry of Science of China, and the research technology project organization of some provinces of Heilongjiang province.

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Liu, X., Song, J., Zheng, Z. et al. Effects of Excess Manganese on the Oxidative Status, and the Expression of Inflammatory Factors and Heat Shock Proteins in Cock Kidneys. Biol Trace Elem Res 197, 639–650 (2020). https://doi.org/10.1007/s12011-019-02003-y

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