Abstract
Cr(VI) is a heavy metal environmental pollutant and carcinogen. Excessive Cr(VI) exposure injures kidneys. This study aimed to investigate mitophagy induced by mitochondrial function damage in chicken kidney exposed to Cr(VI). To explore the mechanism involved, we randomly divided 40 one-day-old Hy-line Brown cockerels into four groups, with each group exposed to different concentrations of Cr(VI), i.e., 0, 10, 30 and 50 mg kg−1, which were orally administered daily for 45 days. Excessive Cr(VI) increased tumor necrosis factor-α (TNF-α), interleukin-6 (IL-6) and chemokine (C-X-C motif) ligand 1(CXCL1) expression and decreased Ca2+-adenosine triphosphatase (Ca2+-ATPase), Mg2+-ATPase and Na+/k+-ATPase activities in chicken kidney. Furthermore, Cr(VI) significantly increased reactive oxygen species (ROS) production and induced mitochondrial membrane potential (MMP) collapse and typical autophagosome formation. With the increase of Cr(VI) concentration, the Parkin translocation, value of LC3-II increased and decreased the content of p62/SQSTM1 and the translocase of outer mitochondrial membrane 20 (TOMM20). In summary, our findings explicated that mitochondrial function damage and mitophagy-related indicators were related to Cr(VI) concentration in chicken kidney.
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Kotyzova D, Hodková A, Bludovská M, Eybl V (2015) Effect of chromium (VI) exposure on antioxidant defense status and trace element homeostasis in acute experiment in rat. Toxicol Ind Health 31(11):1044–1050. https://doi.org/10.1177/0748233713487244
De Flora S, D'Agostini F, Balansky R, Micale R, Baluce B, Izzotti A (2008) Lack of genotoxic effects in hematopoietic and gastrointestinal cells of mice receiving chromium(VI) with the drinking water. Mutat Res 659(1–2):60–67. https://doi.org/10.1016/j.mrrev.2007.11.005
Thatoi H, Das S, Mishra J, Rath BP, Das N (2014) Bacterial chromate reductase, a potential enzyme for bioremediation of hexavalent chromium: a review. J Environ Manag 146:383–399. https://doi.org/10.1016/j.jenvman.2014.07.014
Roy RV, Pratheeshkumar P, Son YO, Wang L, Hitron JA, Divya SP, Zhang Z, Shi X (2016) Different roles of ROS and Nrf2 in Cr(VI)-induced inflammatory responses in normal and Cr(VI)-transformed cells. Toxicol Appl Pharmacol 307:81–90. https://doi.org/10.1016/j.taap.2016.07.016
Lag M, Rodionov D, Ovrevik J, Bakke O, Schwarze PE, Refsnes M (2010) Cadmium-induced inflammatory responses in cells relevant for lung toxicity: expression and release of cytokines in fibroblasts, epithelial cells and macrophages. Toxicol Lett 193(3):252–260. https://doi.org/10.1016/j.toxlet.2010.01.015
Dong GH, Zhang YH, Zheng L, Liang ZF, Jin YH, He QC (2012) Subchronic effects of perfluorooctanesulfonate exposure on inflammation in adult male C57BL/6 mice. Environ Toxicol 27(5):285–296. https://doi.org/10.1002/tox.20642
Park EJ, Park K (2009) Oxidative stress and pro-inflammatory responses induced by silica nanoparticles in vivo and in vitro. Toxicol Lett 184(1):18–25. https://doi.org/10.1016/j.toxlet.2008.10.012
Liu SQ, Wang LY, Liu GH, Tang DZ, Fan XX, Zhao JP, Jiao HC, Wang XJ, Sun SH, Lin H (2018) Leucine alters immunoglobulin a secretion and inflammatory cytokine expression induced by lipopolysaccharide via the nuclear factor-kappaB pathway in intestine of chicken embryos. Animal 12(9):1903–1911. https://doi.org/10.1017/s1751731117003342
Kim JH, Kang JC (2016) The toxic effects on the stress and immune responses in juvenile rockfish, Sebastes schlegelii exposed to hexavalent chromium. Environ Toxicol Pharmacol 43:128–133. https://doi.org/10.1016/j.etap.2016.03.008
Liang Q, Zhang Y, Zeng M, Guan L, Xiao Y, Xiao F (2018) The role of IP3R-SOCCs in Cr(vi)-induced cytosolic Ca(2+) overload and apoptosis in L-02 hepatocytes. Toxicol Res (Camb) 7(3):521–528. https://doi.org/10.1039/c8tx00029h
Huang C, Jiao H, Song Z, Zhao J, Wang X, Lin H (2015) Heat stress impairs mitochondria functions and induces oxidative injury in broiler chickens. J Anim Sci 93(5):2144–2153. https://doi.org/10.2527/jas.2014-8739
Song Z, Zhao T, Liu L, Jiao H, Lin H (2011) Effect of copper on antioxidant ability and nutrient metabolism in broiler chickens stimulated by lipopolysaccharides. Arch Anim Nutr 65(5):366–375. https://doi.org/10.1080/1745039x.2011.609753
Barhoma RAE (2019) The role of eugenol in the prevention of chromium-induced acute kidney injury in male albino rats. Alexandria J Med 54(4):711–715. https://doi.org/10.1016/j.ajme.2018.05.006
Figgitt M, Newson R, Leslie IJ, Fisher J, Ingham E, Case CP (2010) The genotoxicity of physiological concentrations of chromium (Cr(III) and Cr(VI)) and cobalt (Co(II)): an in vitro study. Mutat Res 688(1–2):53–61. https://doi.org/10.1016/j.mrfmmm.2010.03.008
Welling R, Beaumont JJ, Petersen SJ, Alexeeff GV, Steinmaus C (2015) Chromium VI and stomach cancer: a meta-analysis of the current epidemiological evidence. Occup Environ Med 72(2):151-159. https://doi.org/10.1136/oemed-2014-102178
Wang Y, Liu Y, Wan H, Zhu Y, Chen P, Hao P, Cheng Z, Liu J (2017) Moderate selenium dosing inhibited chromium (VI) toxicity in chicken liver. J Biochem Mol Toxicol 31(8). https://doi.org/10.1002/jbt.21916
De Flora S, Camoirano A, Bagnasco M, Bennicelli C, Corbett GE, Kerger BD (1997) Estimates of the chromium(VI) reducing capacity in human body compartments as a mechanism for attenuating its potential toxicity and carcinogenicity. Carcinogenesis 18(3):531–537. https://doi.org/10.1093/carcin/18.3.531
Wan H, Zhu Y, Chen P, Wang Y, Hao P, Cheng Z, Liu Y, Liu J (2017) Effect of various selenium doses on chromium(IV)-induced nephrotoxicity in a male chicken model. Chemosphere 174:306–314. https://doi.org/10.1016/j.chemosphere.2017.01.143
Ceriello A, Assaloni R, Da Ros R, Maier A, Piconi L, Quagliaro L, Esposito K, Giugliano D (2005) Effect of atorvastatin and irbesartan, alone and in combination, on postprandial endothelial dysfunction, oxidative stress, and inflammation in type 2 diabetic patients. Circulation 111(19):2518–2524. https://doi.org/10.1161/01.Cir.0000165070.46111.9f
Shi JX, Wang QJ, Li H, Huang Q (2016) Silencing of USP22 suppresses high glucose-induced apoptosis, ROS production and inflammation in podocytes. Mol BioSyst 12(5):1445–1456. https://doi.org/10.1039/c5mb00722d
Sridharan S, Jain K, Basu A (2011) Regulation of autophagy by kinases. Cancers (Basel) 3(2):2630–2654. https://doi.org/10.3390/cancers3022630
Wu D, Luo N, Wang L, Zhao Z, Bu H, Xu G, Yan Y, Che X, Jiao Z, Zhao T, Chen J, Ji A, Li Y, Lee GD (2017) Hydrogen sulfide ameliorates chronic renal failure in rats by inhibiting apoptosis and inflammation through ROS/MAPK and NF-kappaB signaling pathways. Sci Rep 7(1):455. https://doi.org/10.1038/s41598-017-00557-2
Yang G, Chang CC, Yang Y, Yuan L, Xu L, Ho CT, Li S (2018) Resveratrol alleviates rheumatoid arthritis via reducing ROS and inflammation, inhibiting MAPK signaling pathways, and suppressing angiogenesis. J Agric Food Chem 66(49):12953–12960. https://doi.org/10.1021/acs.jafc.8b05047
Niu Y, Sun Q, Zhang G, Liu X, Shang Y, Xiao Y, Liu S (2018) Fowl adenovirus serotype 4-induced apoptosis, autophagy, and a severe inflammatory response in liver. Vet Microbiol 223:34–41. https://doi.org/10.1016/j.vetmic.2018.07.014
Jin Y, Liu Z, Liu F, Ye Y, Peng T, Fu Z (2015) Embryonic exposure to cadmium (II) and chromium (VI) induce behavioral alterations, oxidative stress and immunotoxicity in zebrafish (Danio rerio). Neurotoxicol Teratol 48:9–17. https://doi.org/10.1016/j.ntt.2015.01.002
al-Harbi MM, Osman AM, al-Gharably NM, al-Bekairi AM, al-Shabanah OA, Sabah DM, Raza M (1995) Effect of desferrioxamine on cisplatin-induced nephrotoxicity in normal rats. Chemotherapy 41(6):448–454. https://doi.org/10.1159/000239381
Lu J, Liu K, Qi M, Geng H, Hao J, Wang R, Zhao X, Liu Y, Liu J (2019) Effects of Cr(VI) exposure on electrocardiogram, myocardial enzyme parameters, inflammatory factors, oxidative kinase, and ATPase of the heart in Chinese rural dogs. Environ Sci Pollut Res Int 26(29):30444–30451. https://doi.org/10.1007/s11356-019-06253-0
Molina-Jijon E, Zarco-Marquez G, Medina-Campos ON, Zatarain-Barron ZL, Hernandez-Pando R, Pinzon E, Zavaleta RM, Tapia E, Pedraza-Chaverri J (2012) Deferoxamine pretreatment prevents Cr(VI)-induced nephrotoxicity and oxidant stress: role of Cr(VI) chelation. Toxicology 291(1–3):93–101. https://doi.org/10.1016/j.tox.2011.11.003
Dai H, Deng Y, Zhang J, Han H, Zhao M, Li Y, Zhang C, Tian J, Bing G, Zhao L (2015) PINK1/Parkin-mediated mitophagy alleviates chlorpyrifos-induced apoptosis in SH-SY5Y cells. Toxicology 334:72–80. https://doi.org/10.1016/j.tox.2015.06.003
Gao F, Chen D, Si J, Hu Q, Qin Z, Fang M, Wang G (2015) The mitochondrial protein BNIP3L is the substrate of PARK2 and mediates mitophagy in PINK1/PARK2 pathway. Hum Mol Genet 24(9):2528–2538. https://doi.org/10.1093/hmg/ddv017
Zhang HT, Mi L, Wang T, Yuan L, Li XH, Dong LS, Zhao P, Fu JL, Yao BY, Zhou ZC (2016) PINK1/Parkin-mediated mitophagy play a protective role in manganese induced apoptosis in SH-SY5Y cells. Toxicol in Vitro 34:212–219. https://doi.org/10.1016/j.tiv.2016.04.006
Yin F, Yan J, Zhao Y, Guo KJ, Zhang ZL, Li AP, Meng CY, Guo L (2019) Bone marrow mesenchymal stem cells repair Cr (VI)- injured kidney by regulating mitochondria-mediated apoptosis and mitophagy mediated via the MAPK signaling pathway. Ecotoxicol Environ Saf 176:234–241. https://doi.org/10.1016/j.ecoenv.2019.03.093
Eiyama A, Okamoto K (2015) PINK1/Parkin-mediated mitophagy in mammalian cells. Curr Opin Cell Biol 33:95–101. https://doi.org/10.1016/j.ceb.2015.01.002
Fujimaki M, Saiki S, Sasazawa Y, Ishikawa KI, Imamichi Y, Sumiyoshi K, Hattori N (2018) Immunocytochemical monitoring of PINK1/Parkin-mediated mitophagy in cultured cells. Methods Mol Biol 1759:19–27. https://doi.org/10.1007/7651_2017_20
Geisler S, Holmstrom KM, Skujat D, Fiesel FC, Rothfuss OC, Kahle PJ, Springer W (2010) PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat Cell Biol 12(2):119–131. https://doi.org/10.1038/ncb2012
Yang F, Zhao L, Mei D, Jiang L, Geng C, Li Q, Yao X, Liu Y, Kong Y, Cao J (2017) HMGA2 plays an important role in Cr (VI)-induced autophagy. Int J Cancer 141(5):986–997. https://doi.org/10.1002/ijc.30789
Huang C, Andres AM, Ratliff EP, Hernandez G, Lee P, Gottlieb RA (2011) Preconditioning involves selective mitophagy mediated by Parkin and p62/SQSTM1. PLoS One 6(6):e20975. https://doi.org/10.1371/journal.pone.0020975
Strappazzon F, Nazio F, Corrado M, Cianfanelli V, Romagnoli A, Fimia GM, Campello S, Nardacci R, Piacentini M, Campanella M, Cecconi F (2015) AMBRA1 is able to induce mitophagy via LC3 binding, regardless of PARKIN and p62/SQSTM1. Cell Death Differ 22(3):517. https://doi.org/10.1038/cdd.2014.190
Kawajiri S, Saiki S, Sato S, Sato F, Hatano T, Eguchi H, Hattori N (2010) PINK1 is recruited to mitochondria with parkin and associates with LC3 in mitophagy. FEBS Lett 584(6):1073–1079. https://doi.org/10.1016/j.febslet.2010.02.016
Lan R, Wu JT, Wu T, Ma YZ, Wang BQ, Zheng HZ, Li YN, Wang Y, Gu CQ, Zhang Y (2018) Mitophagy is activated in brain damage induced by cerebral ischemia and reperfusion via the PINK1/Parkin/p62 signalling pathway. Brain Res Bull 142:63–77. https://doi.org/10.1016/j.brainresbull.2018.06.018
Zha Z, Wang J, Wang X, Lu M, Guo Y (2017) Involvement of PINK1/Parkin-mediated mitophagy in AGE-induced cardiomyocyte aging. Int J Cardiol 227:201–208. https://doi.org/10.1016/j.ijcard.2016.11.161
Wu L, Maimaitirexiati X, Jiang Y, Liu L (2016) Parkin regulates mitochondrial autophagy after myocardial infarction in rats. Med Sci Monit 22:1553–1559. https://doi.org/10.12659/msm.898722
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The project was supported by the National Nature Science Foundation of China (No. 31872535), Shandong Natural Science Foundation of China (ZR2018MC027), Shandong Key R&D Program (GG201809160113), China Postdoctoral Science Foundation (2018M632704, 2019T120601), and Funds of Shandong “Double Tops” Program.
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Wang, Y., Wang, X., Wang, L. et al. Mitophagy Induced by Mitochondrial Function Damage in Chicken Kidney Exposed to Cr(VI). Biol Trace Elem Res 199, 703–711 (2021). https://doi.org/10.1007/s12011-020-02176-x
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DOI: https://doi.org/10.1007/s12011-020-02176-x