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Cerebellar injury induced by cadmium via disrupting the heat-shock response

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Abstract

Cadmium (Cd) is a food contaminant that poses serious threats to animal health, including birds. It is also an air pollutant with well-known neurotoxic effects on humans. However, knowledge on the neurotoxic effects of chronic Cd exposure on chicken is limited. Thus, this study assessed the neurotoxic effects of chronic Cd on chicken cerebellum. Chicks were exposed to 0 (control), 35 (low), and 70 (high) mg/kg of Cd for 90 days, and the expression of genes related to the heat-shock response was investigated. The chickens showed clinical symptoms of ataxia, and histopathology revealed that Cd exposure decreased the number of Purkinje cells and induced degeneration of Purkinje cells with pyknosis, and some dendrites were missing. Moreover, Cd exposure increased the expression of heat-shock factors, HSF1, HSF2, and HSF3, and heat-shock proteins, HSP60, HSP70, HSP90, and HSP110. These changes indicate that HSPs improve the tolerance of the cerebellum to Cd. Conversely, the expressions of HSP10, HSP25, and HSP40 were decreased significantly, which indicated that Cd inhibits the expression of small heat-shock proteins. However, HSP27 and HSP47 were upregulated following low-dose Cd exposure, but downregulated under high-dose Cd exposure. This work sheds light on the toxic effects of Cd on the cerebellum, and it may provide evidence for health risks posed by Cd. Additionally, this work also identified a novel target of Cd exposure in that Cd induces cerebellar injury by disrupting the heat-shock response.

Graphical Abstract

Cd can be absorbed into chicken’s cerebellum through the food chain, which eventually caused cerebellar injury. This study provided a new insight that chronic Cd-induced neurotoxicity in the cerebellum is associated with alterations in heat-shock response–related genes, which indicated that Cd through disturbing heat-shock response induced cerebellar injury.

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Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Agarwal S, Ganesh S (2020): Perinuclear mitochondrial clustering, increased ROS levels, and HIF1 are required for the activation of HSF1 by heat stress. J Cell Sci 133, jcs245589

  • Al Olayan EM, Aloufi AS, AlAmri OD, El-Habit OH, Abdel Moneim AE (2020) Protocatechuic acid mitigates cadmium-induced neurotoxicity in rats: role of oxidative stress, inflammation and apoptosis. Sci Total Environ 723:137969

    Article  CAS  Google Scholar 

  • Barna J, Csermely P, Vellai T (2018) Roles of heat shock factor 1 beyond the heat shock response. Cell Mol Life Sci 75:2897–2916

    Article  CAS  Google Scholar 

  • Bekheet SH (2011) Comparative effects of repeated administration of cadmium chloride during pregnancy and lactation and selenium protection against cadmium toxicity on some organs in immature rats’ offsprings. Biol Trace Elem Res 144:1008–1023

    Article  CAS  Google Scholar 

  • Bi SS, Jin HT, Talukder M, Ge J, Zhang C, Lv MW, Yaqoob Ismail MA, Li JL (2021) The protective effect of nano-selenium against cadmium-induced cerebellar injury via the heat shock protein pathway in chicken. Food Chem Toxicol 154:112332

    Article  CAS  Google Scholar 

  • Bi SS, Talukder M, Jin HT, Lv MW, Ge J, Zhang C, Li JL (2022) Cadmium through disturbing MTF1-mediated metal response induced cerebellar injury. Neurotox Res 27:1–11

    Google Scholar 

  • Branca JJV, Fiorillo C, Carrino D, Paternostro F, Taddei N, Gulisano M, Pacini A, Becatti M (2020) Cadmium-induced oxidative stress: focus on the central nervous system. Antioxidants (basel) 9:492

    Article  CAS  Google Scholar 

  • Chow AM, Tang DW, Hanif A, Brown IR (2013) Induction of heat shock proteins in cerebral cortical cultures by celastrol. Cell Stress Chaperones 18:155–160

    Article  CAS  Google Scholar 

  • Cui JG, Zhao Y, Zhang H, Li XN, Li JL (2022) Lycopene regulates the mitochondrial unfolded protein response to prevent DEHP-induced cardiac mitochondrial damage in mice. Food Funct 13:4527–4536

    Article  CAS  Google Scholar 

  • Dai XY, Li XW, Zhu SY, Li MZ, Zhao Y, Talukder M, Li YH, Li JL (2021a) Lycopene ameliorates di(2-ethylhexyl) phthalate-induced pyroptosis in spleen via suppression of classic caspase-1/NLRP3 pathway. J Agric Food Chem 69:1291–1299

    Article  CAS  Google Scholar 

  • Dai XY, Zhao Y, Ge J, Zhu SY, Li MZ, Talukder M, Li JL (2021b) Lycopene attenuates di(2-ethylhexyl) phthalate-induced mitophagy in spleen by regulating the sirtuin3-mediated pathway. Food Funct 12:4582–4590

    Article  CAS  Google Scholar 

  • Dai XY, Zhu SY, Chen J, Li MZ, Talukder M, Li JL (2022a) Role of Toll-like receptor/MyD88 signaling in lycopene alleviated di-2-ethylhexyl phthalate (DEHP)-induced inflammatory response. J Agric Food Chem 70:10022–10030

    Article  CAS  Google Scholar 

  • Dai XY, Zhu SY, Chen J, Li MZ, Zhao Y, Talukder M, Li JL (2022b) Lycopene alleviates di(2-ethylhexyl) phthalate-induced splenic injury by activating P62-Keap1-NRF2 signaling. Food Chem Toxicol 168:113324

    Article  CAS  Google Scholar 

  • Fan G, Tu Y, Wu N, Xiao H (2020) The expression profiles and prognostic values of HSPs family members in head and neck cancer. Cancer Cell Int 20:220

    Article  CAS  Google Scholar 

  • Finicelli M, Squillaro T, Galderisi U, Peluso G (2020) Micro-RNAs: crossroads between the exposure to environmental particulate pollution and the obstructive pulmonary disease. Int J Mol Sci 21:7221

    Article  CAS  Google Scholar 

  • Forcella M, Lau P, Oldani M, Melchioretto P, Bogni A, Gribaldo L, Fusi P, Urani C (2020) Neuronal specific and non-specific responses to cadmium possibly involved in neurodegeneration: a toxicogenomics study in a human neuronal cell model. Neurotoxicology 76:162–173

    Article  CAS  Google Scholar 

  • Ge J, Guo K, Huang Y, Morse PD, Zhang C, Lv MW, Li JL (2022a) Comparison of antagonistic effects of nanoparticle-selenium, selenium-enriched yeast and sodium selenite against cadmium-induced cardiotoxicity via AHR/CAR/PXR/Nrf2 pathways activation. J Nutr Biochem 21:108992

    Article  Google Scholar 

  • Ge J, Guo K, Zhang C, Talukder M, Lv MW, Li JY, Li JL (2021a) Comparison of nanoparticle-selenium, selenium-enriched yeast and sodium selenite on the alleviation of cadmium-induced inflammation via NF-kB/IkappaB pathway in heart. Sci Total Environ 773:145442

    Article  CAS  Google Scholar 

  • Ge J, Huang Y, Lv M, Zhang C, Talukder M, Li JY, Li JL (2022b) Cadmium induced Fak-mediated anoikis activation in kidney via nuclear receptors (AHR/CAR/PXR)-mediated xenobiotic detoxification pathway. J Inorg Biochem 227:111682

    Article  CAS  Google Scholar 

  • Ge J, Liu LL, Cui ZG, Talukder M, Lv MW, Li JY, Li JL (2021b) Comparative study on protective effect of different selenium sources against cadmium-induced nephrotoxicity via regulating the transcriptions of selenoproteome. Ecotoxicol Environ Saf 215:112135

    Article  CAS  Google Scholar 

  • Ge J, Zhang C, Sun YC, Zhang Q, Lv MW, Guo K, Li JL (2019) Cadmium exposure triggers mitochondrial dysfunction and oxidative stress in chicken (Gallus gallus) kidney via mitochondrial UPR inhibition and Nrf2-mediated antioxidant defense activation. Sci Total Environ 689:1160–1171

    Article  CAS  Google Scholar 

  • Genchi G, Sinicropi MS, Lauria G, Carocci A, Catalano A (2020): The effects of cadmium toxicity. Int J Environ Res Public Health 17

  • Giri SS, Sen SS, Jun JW, Sukumaran V, Park SC (2016) Immunotoxicological effects of cadmium on Labeo rohita, with emphasis on the expression of HSP genes. Fish Shellfish Immunol 54:164–171

    Article  CAS  Google Scholar 

  • Guan TQ, Qiu BH, Nurmamedov H, Talukder M, Lv MW, Li JL (2022) Cadmium-induced splenic lymphocytes anoikis is not mitigated by activating Nrf2-mediated antioxidative defense response. J Inorg Biochem 234:111882

    Article  CAS  Google Scholar 

  • Guo JY, Lin J, Huang YQ, Talukder M, Yu L, Li JL (2021) AQP2 as a target of lycopene protects against atrazine-induced renal ionic homeostasis disturbance. Food Funct 12:4855–4863

    Article  CAS  Google Scholar 

  • Guo K, Ge J, Zhang C, Lv MW, Zhang Q, Talukder M, Li JL (2020) `Cadmium induced cardiac inflammation in chicken (Gallus gallus) via modulating cytochrome P450 systems and Nrf2 mediated antioxidant defense. Chemosphere 249:125858

    Article  CAS  Google Scholar 

  • Horiguchi H, Aoshima K, Oguma E, Sasaki S, Miyamoto K, Hosoi Y, Katoh T, Kayama F (2010) Latest status of cadmium accumulation and its effects on kidneys, bone, and erythropoiesis in inhabitants of the formerly cadmium-polluted Jinzu River Basin in Toyama, Japan, after restoration of rice paddies. Int Arch Occup Environ Health 83:953–970

    Article  CAS  Google Scholar 

  • Huang YQ, Tang YX, Qiu BH, Talukder M, Li XN, Li JL (2022) Di-2-ethylhexyl phthalate (DEHP) induced lipid metabolism disorder in liver via activating the LXR/SREBP-1c/PPARα/γ and NF-κB signaling pathway. Food Chem Toxicol 165:113119

    Article  CAS  Google Scholar 

  • Ibiwoye MO, Matthews Q, Travers K, Foster JD (2019) Association of acute, high-dose cadmium exposure with alterations in vascular endothelial barrier antigen expression and astrocyte morphology in the developing rat central nervous system. J Comp Pathol 172:37–47

    Article  CAS  Google Scholar 

  • Jiang FW, Yang ZY, Bian YF, Cui JG, Zhang H, Zhao Y, Li JL (2021) The novel role of the aquaporin water channel in lycopene preventing DEHP-induced renal ionic homeostasis disturbance in mice. Ecotoxicol Environ Saf 226:112836

    Article  CAS  Google Scholar 

  • Joshi T, Kumar V, Kaznacheyeva EV, Jana NR (2021) Withaferin A induces heat shock response and ameliorates disease progression in a mouse model of Huntington’s disease. Mol Neurobiol 58:3992–4006

    Article  CAS  Google Scholar 

  • Le Croizier G, Lacroix C, Artigaud S, Le Floch S, Munaron JM, Raffray J, Penicaud V, Rouget ML, Lae R, Tito De Morais L (2019) Metal subcellular partitioning determines excretion pathways and sensitivity to cadmium toxicity in two marine fish species. Chemosphere 217:754–762

    Article  Google Scholar 

  • Li MZ, Zhao Y, Wang HR, Talukder M, Li JL (2021) Lycopene preventing DEHP-induced renal cell damage is targeted by aryl hydrocarbon receptor. J Agric Food Chem 69:12853–12861

    Article  CAS  Google Scholar 

  • Li X, Mao L, Zhang Y, Wang X, Wang Y, Wu X (2020) Joint toxic impacts of cadmium and three pesticides on embryonic development of rare minnow (Gobiocypris rarus). Environ Sci Pollut Res Int 27:36596–36604

    Article  CAS  Google Scholar 

  • Mordes DA, Prudencio M, Goodman LD, Klim JR, Moccia R, Limone F, Pietilainen O, Chowdhary K, Dickson DW, Rademakers R, Bonini NM, Petrucelli L, Eggan K (2018) Dipeptide repeat proteins activate a heat shock response found in C9ORF72-ALS/FTLD patients. Acta Neuropathol Commun 6:55

    Article  Google Scholar 

  • Moyano P, Garcia JM, Lobo M, Anadon MJ, Sola E, Pelayo A, Garcia J, Frejo MT, Pino JD (2018) Cadmium alters heat shock protein pathways in SN56 cholinergic neurons, leading to Abeta and phosphorylated Tau protein generation and cell death. Food Chem Toxicol 121:297–308

    Article  CAS  Google Scholar 

  • Murakami T, Ohmori H, Katoh T, Abe T, Higashi K (1991) Cadmium causes increases of N-myc and multidrug-resistance gene mRNA in neuroblastoma cells. J UOEH 13:271–278

    Article  CAS  Google Scholar 

  • Naija A, Kestemont P, Chenais B, Haouas Z, Blust R, Helal AN, Marchand J (2017) Cadmium exposure exerts neurotoxic effects in peacock blennies Salaria pavo. Ecotoxicol Environ Saf 143:217–227

    Article  CAS  Google Scholar 

  • MM PM, Shahi MH, Tayyab M, Farheen S, Khanam N, Tabassum S, Ali A (2019) Cadmium-induced neurodegeneration and activation of noncanonical sonic hedgehog pathway in rat cerebellum. J Biochem Mol Toxicol. 33 e22274

  • Paithankar JG, Saini S, Dwivedi S, Sharma A, Chowdhuri DK (2021) Heavy metal associated health hazards: an interplay of oxidative stress and signal transduction. Chemosphere 262:128350

    Article  CAS  Google Scholar 

  • Pardinho RB, Vecchia PD, Alves C, Pimentel N, Gazzana D, Bolzan RC, Duarte FA, Bisognin DA, Flores EMM (2020) Ilex Paraguariensis exposition to As and Cd in a closed soilless system. Chemosphere 258:127284

    Article  CAS  Google Scholar 

  • Penke B, Bogar F, Crul T, Santha M, Toth ME, Vigh L (2018) Heat shock proteins and autophagy pathways in neuroprotection: from molecular bases to pharmacological interventions. Int J Mol Sci 19:325

    Article  Google Scholar 

  • Prince TL, Lang BJ, Guerrero-Gimenez ME, Fernandez-Munoz JM, Ackerman A, Calderwood SK (2020) HSF1: primary factor in molecular chaperone expression and a major contributor to cancer morbidity. Cells 9:1046

    Article  CAS  Google Scholar 

  • Sasaki T, Horiguchi H, Arakawa A, Oguma E, Komatsuda A, Sawada K, Murata K, Yokoyama K, Matsukawa T, Chiba M, Omori Y, Kamikomaki N (2019) Hospital-based screening to detect patients with cadmium nephropathy in cadmium-polluted areas in Japan. Environ Health Prev Med 24:8

    Article  Google Scholar 

  • Shinkawa T, Tan K, Fujimoto M, Hayashida N, Yamamoto K, Takaki E, Takii R, Prakasam R, Inouye S, Mezger V, Nakai A (2011) Heat shock factor 2 is required for maintaining proteostasis against febrile-range thermal stress and polyglutamine aggregation. Mol Biol Cell 22:3571–3583

    Article  CAS  Google Scholar 

  • Song G, Yuan S, Wen X, Xie Z, Lou L, Hu B, Cai Q, Xu B (2018) Transcriptome analysis of Cd-treated switchgrass root revealed novel transcripts and the importance of HSF/HSP network in switchgrass Cd tolerance. Plant Cell Rep 37:1485–1497

    Article  CAS  Google Scholar 

  • Steurer C, Eder N, Kerschbaum S, Wegrostek C, Gabriel S, Pardo N, Ortner V, Czerny T, Riegel E (2018) HSF1 mediated stress response of heavy metals. PLoS ONE 13:e0209077

    Article  CAS  Google Scholar 

  • Stoev SD, Grozeva N, Simeonov R, Borisov I, Hubenov H, Nikolov Y, Tsaneva M, Lazarova S (2003) Experimental cadmium poisoning in sheep. Exp Toxicol Pathol 55:309–314

    Article  CAS  Google Scholar 

  • Sudo K, Vand C, Miyamoto A, Shiraishi M (2019) Comparative analysis of in vitro neurotoxicity of methylmercury, mercury, cadmium, and hydrogen peroxide on SH-SY5Y cells. J Vet Med Sci. 81 828 837

  • Takii R, Fujimoto M, Matsuura Y, Wu F, Oshibe N, Takaki E, Katiyar A, Akashi H, Makino T, Kawata M, Nakai A (2017) HSF1 and HSF3 cooperatively regulate the heat shock response in lizards. PLoS ONE 12:e0180776

    Article  Google Scholar 

  • Talukder M, Bi SS, Jin HT, Ge J, Zhang C, Lv MW, Li JL (2021) Cadmium induced cerebral toxicity via modulating MTF1-MTs regulatory axis. Environ Pollut 285:117083

    Article  CAS  Google Scholar 

  • Tedesco B, Cristofani R, Ferrari V, Cozzi M, Rusmini P, Casarotto E, Chierichetti M, Mina F, Galbiati M, Piccolella M, Crippa V, Poletti A (2022) Insights on human small heat shock proteins and their alterations in diseases. Front Mol Biosci 9:842149

    Article  CAS  Google Scholar 

  • Urien N, Cooper S, Caron A, Sonnenberg H, Rozon-Ramilo L, Campbell PGC, Couture P (2018) Subcellular partitioning of metals and metalloids (As, Cd, Cu, Se and Zn) in liver and gonads of wild white suckers (Catostomus commersonii) collected downstream from a mining operation. Aquat Toxicol 202:105–116

    Article  CAS  Google Scholar 

  • Vennam S, Georgoulas S, Khawaja A, Chua S, Strouthidis NG, Foster PJ (2020) Heavy metal toxicity and the aetiology of glaucoma. Eye (lond) 34:129–137

    Article  Google Scholar 

  • Wang H, Abel GM, Storm DR, Xia Z (2019) Cadmium exposure impairs adult hippocampal neurogenesis. Toxicol Sci kfz152

  • Wang S, You M, Wang C, Zhang Y, Fan C, Yan S (2020a) Heat shock pretreatment induced cadmium resistance in the nematode Caenorhabditis elegans is depend on transcription factors DAF-16 and HSF-1. Environ Pollut 261:114081

    Article  CAS  Google Scholar 

  • Wang Y, Liu J, Chen R, Qi M, Tao D, Xu S (2020b) The antagonistic effects of selenium yeast (SeY) on cadmium-induced inflammatory factors and the heat shock protein expression levels in chicken livers. Biol Trace Elem Res 198:260–268

    Article  Google Scholar 

  • Wu L, Song J, Xue J, Xiao T, Wei Q, Zhang Z, Zhang Y, Li Z, Hu Y, Zhang G, Xia H, Li J, Yang X, Liu Q (2020) MircoRNA-143-3p regulating ARL6 is involved in the cadmium-induced inhibition of osteogenic differentiation in human bone marrow mesenchymal stem cells. Toxicol Lett 331:159–166

    Article  CAS  Google Scholar 

  • Zhang C, Ge J, Lv M, Zhang Q, Talukder M, Li JL (2020a) Selenium prevents cadmium-induced hepatotoxicity through modulation of endoplasmic reticulum-resident selenoproteins and attenuation of endoplasmic reticulum stress. Environ Pollut 260:113873

    Article  CAS  Google Scholar 

  • Zhang C, Huang Y, Talukder M, Ge J, Lv MW, Bi SS, Li JL (2020b) Selenium sources differ in their potential to alleviate the cadmium-induced testicular dysfunction. Environ Pollut 267:115610

    Article  CAS  Google Scholar 

  • Zhang C, Lin J, Ge J, Wang LL, Li N, Sun XT, Cao HB, Li JL (2017) Selenium triggers Nrf2-mediated protection against cadmium-induced chicken hepatocyte autophagy and apoptosis. Toxicol in Vitro 44:349–356

    Article  CAS  Google Scholar 

  • Zhang C, Wang LL, Cao CY, Li N, Talukder M, Li JL (2020c) Selenium mitigates cadmium-induced crosstalk between autophagy and endoplasmic reticulum stress via regulating calcium homeostasis in avian leghorn male hepatoma (LMH) cells. Environ Pollut 265:114613

    Article  CAS  Google Scholar 

  • Zhang H, Zhao Y, Cui JG, Li XN, Li JL (2022) DEHP-induced mitophagy and mitochondrial damage in the heart are associated with dysregulated mitochondrial biogenesis. Food Chem Toxicol 161:112818

    Article  CAS  Google Scholar 

  • Zhang Q, Zhang C, Ge J, Lv MW, Talukder M, Guo K, Li YH, Li JL (2020d) Ameliorative effects of resveratrol against cadmium-induced nephrotoxicity via modulating nuclear xenobiotic receptor response and PINK1/Parkin-mediated mitophagy. Food Funct 11:1856–1868

    Article  Google Scholar 

  • Zhao Y, Bao RK, Zhu SY, Talukder M, Cui JG, Zhang H, Li XN, Li JL (2021a) Lycopene prevents DEHP-induced hepatic oxidative stress damage by crosstalk between AHR-Nrf2 pathway. Environ Pollut 285:117080

    Article  CAS  Google Scholar 

  • Zhao Y, Cui JG, Zhang H, Li XN, Li MZ, Talukder M, Li JL (2021b) Role of mitochondria-endoplasmic reticulum coupling in lycopene preventing DEHP-induced hepatotoxicity. Food Funct 12:10741–10749

    Article  CAS  Google Scholar 

  • Zhao Y, Cui LG, Talukder M, Cui JG, Zhang H, Li JL (2021c) Lycopene prevents DEHP-induced testicular endoplasmic reticulum stress via regulating nuclear xenobiotic receptors and unfolded protein response in mice. Food Funct 12:12256–12264

    Article  CAS  Google Scholar 

  • Zhao Y, Ma DX, Wang HG, Li MZ, Talukder M, Wang HR, Li JL (2020a) Lycopene prevents DEHP-induced liver lipid metabolism disorder by inhibiting the HIF-1α-induced PPARα/PPARγ/FXR/LXR system. J Agric Food Chem 68:11468–11479

    Article  CAS  Google Scholar 

  • Zhao Y, Li HX, Luo Y, Cui JG, Talukder M, Li JL (2022a) Lycopene mitigates DEHP-induced hepatic mitochondrial quality control disorder via regulating SIRT1/PINK1/mitophagy axis and mitochondrial unfolded protein response. Environ Pollut 292:118390

    Article  CAS  Google Scholar 

  • Zhao Y, Li MZ, Talukder M, Luo Y, Shen Y, Wang HR, Li JL (2020b) Effect of mitochondrial quality control on the lycopene antagonizing DEHP-induced mitophagy in spermatogenic cells. Food Funct 11:5815–5826

    Article  CAS  Google Scholar 

  • Zhao Y, Li MZ, Shen Y, Lin J, Wang HR, Talukder M, Li JL (2020c) Lycopene prevents DEHP-induced Leydig cell damage with the Nrf2 antioxidant signaling pathway in mice. J Agric Food Chem 68:2031–2040

    Article  CAS  Google Scholar 

  • Zhao Y, Li XN, Zhang H, Cui JG, Wang JX, Chen MS, Li JL (2022b) Phthalate-induced testosterone/androgen receptor pathway disorder on spermatogenesis and antagonism of lycopene. J Hazard Mater 439:129689

    Article  CAS  Google Scholar 

  • Zhao Y, Lin J, Talukder M, Zhu SY, Li MZ, Wang HR, Li JL (2020d) Aryl hydrocarbon receptor as a target for lycopene preventing DEHP-induced spermatogenic disorders. J Agric Food Chem 68:4355–4366

    Article  CAS  Google Scholar 

  • Zhao YX, Tang YX, Sun XH, Zhu SY, Dai XY, Li XN, Li JL (2022c) Gap junction protein connexin 43 as a target is internalized in astrocyte neurotoxicity caused by di-(2-ethylhexyl) phthalate. J Agric Food Chem 70:5921–5931

    Article  CAS  Google Scholar 

  • Zhu SY, Guo JY, Li JY, Dai XY, Li XN, Li JL (2022) Lycopene ameliorates atrazine-induced pyroptosis in spleen by suppressing the Ox-mtDNA/Nlrp3 inflammasome pathway. Food Funct 13:3551–3560

    Article  CAS  Google Scholar 

  • Zhu SY, Liu LL, Huang YQ, Li XW, Talukder M, Dai XY, Li YH, Li JL (2021): In silico analysis of selenoprotein N (Gallus gallus): absence of EF-hand motif and the role of CUGS-helix domain in antioxidant protection. Metallomics 13, mfab004

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Funding

This study has received assistance from the National Natural Science Foundation of China (No. 32172932, 32102739), the Key Program of Natural Science Foundation of Heilongjiang Province of China (No. ZD2021C003), the China Agriculture Research System of MOF and MARA (No. CARS-35), the Distinguished Professor of Longjiang Scholars Support Project (No. T201908), High-level Talent Scientific Research start-up Foundation of Wanxi University (No. WGKQ2022031), the Heilongjiang Touyan Innovation Team Program and Postdoctoral Research Foundation of China (No. 2021M690925). The funder of the study had no role in study design, data collection, data analysis, data interpretation, or writing of the report.

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Author notes

  1. Shao-Shuai Bia, Milton Talukdera, and Xue-Tong Suna contributed equally to this study.

Authors and Affiliations

  1. College of Veterinary Medicine, Northeast Agricultural University, Harbin, 150030, People’s Republic of China

    Shao-Shuai Bi, Milton Talukder, Xue-Tong Sun, Mei-Wei Lv, Jing Ge, Cong Zhang & Jin-Long Li

  2. College of Biological and Pharmaceutical Engineering, West Anhui University, Lu’an, 237012, People’s Republic of China

    Shao-Shuai Bi

  3. Department of Physiology and Pharmacology, Faculty of Animal Science and Veterinary Medicine, Patuakhali Science and Technology University, Barishal, 8210, Bangladesh

    Milton Talukder

  4. College of Veterinary Medicine, Henan Agricultural University, Zhengzhou, 450046, People’s Republic of China

    Cong Zhang

  5. Key Laboratory of the Provincial Education, Department of Heilongjiang for Common Animal Disease Prevention and Treatment, Northeast Agricultural University, Harbin, 150030, People’s Republic of China

    Jin-Long Li

  6. Heilongjiang Key Laboratory for Laboratory Animals and Comparative Medicine, Northeast Agricultural University, Harbin, 150030, People’s Republic of China

    Jin-Long Li

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  1. Shao-Shuai Bi
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Contributions

SSB designed the study with contributions from MT, XTS, MWL, JG, CZ, JLL. SSB had a major role in the conception and design of the trial and managed the main trial and drafted the final manuscript. SSB authored and performed the statistical analyses. XTS and MT authored the cost-effectiveness analyses and with MWL, JG, and CZ performed the analysis. SSB contributed to the study design, statistical analyses, and the interpretation of the findings. JLL provided expertise to the study design and delivery. All authors read and approved the final manuscript.

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Correspondence to Jin-Long Li.

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Bi, SS., Talukder, M., Sun, XT. et al. Cerebellar injury induced by cadmium via disrupting the heat-shock response. Environ Sci Pollut Res 30, 22550–22559 (2023). https://doi.org/10.1007/s11356-022-23771-6

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