Skip to main content
Log in

NLRP3 inflammasome is involved in the mechanism of mitigative effect of selenium on lead-induced inflammatory damage in chicken kidneys

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Lead (Pb) is a kind of widespread toxic environmental pollutant which can cause harm to organisms. Selenium (Se) has the property of mitigating Pb toxicity through decreasing oxidative stress and inflammation caused by Pb. Nucleotide-binding domain, leucine-rich-containing family, and pyrin-domain containing-3 (NLRP3) inflammasome involve in inflammation process. However, the effect of NLRP3 inflammasome in heavy metal-caused animal damage remains unknown. This research aimed to explore the mechanism of mitigative role of Se on Pb-caused renal inflammatory injury in chickens. One-week-old male chickens were provided a standard diet and drinking water, a standard diet added with 1 mg kg−1 of Se and drinking water, a standard diet and drinking water added with 350 mg L−1 Pb, and a standard diet added with 1 mg kg−1 Se and drinking water added with 350 mg L−1 Pb. On the 4th, 8th, and 12th weeks, serum was used to measure creatinine (CREA) and uric acid (UA) contents, and kidneys were used to measure Se and Pb concentrations, histological structure, oxidative stress indicators, relative expressions of cytokines, and inflammatory factors. The results showed that Pb accumulated, Se concentration decreased, CREA and UA contents increased, and renal injury occurred in Pb-treated chicken kidneys. Excess Pb increased MDA content and the expressions of IL-1β, IL-6, IL-17, NLRP3, caspase-1, NF-κB, COX-2, TNF-α, and PTGEs and decreased GSH content, GPx and SOD activities, and IFN-γ expression in the chicken kidneys. Se administration alleviated the aforementioned changes. In addition, toxic effect of Pb on the chicken kidneys was time-dependent. NLRP3 inflammasome, caspase-1, and IL-1β may be sensitive indicators in Pb-induced chicken kidney inflammatory damage. In conclusion, NLRP3 inflammasome took part in antagonistic role of Se against Pb-caused inflammation via changing oxidative stress indicators, cytokines, and inflammation-related genes in the chicken kidneys.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

Not applicable.

References

  • Akhter N, Madhoun A, Arefanian H, Wilson A, Kochumon S, Thomas R, Shenouda S, Al-Mulla F, Ahmad R, Sindhu S (2019) Oxidative stress induces expression of the toll-like receptors (TLRs) 2 and 4 in the human peripheral blood mononuclear cells: implications for metabolic inflammation. Cellular Physiology and Biochemistry: International Journal of Experimental Cellular Physiology, Biochemistry, and Pharmacology 53:1–18

    CAS  Google Scholar 

  • An Y, Xing HJ, Zhang Y, Jia PC, Gu XH, Teng XH (2019) The evaluation of potential immunotoxicity induced by environmental pollutant ammonia in broilers. Poult Sci 98:3165–3175

    Article  CAS  Google Scholar 

  • Cao H, Gao F, Xia B, Zhang M, Liao Y, Yang Z, Hu G, Zhang C (2016) Alterations in trace element levels and mRNA expression of Hsps and inflammatory cytokines in livers of duck exposed to molybdenum or/and cadmium. Ecotoxicol Environ Saf 125:93–101

    Article  CAS  Google Scholar 

  • Cao Y, Wang D, Li Q, Liu H, Jin C, Yang J, Wu S, Lu X, Cai Y (2020) Activation of Nrf2 by lead sulfide nanoparticles induces impairment of learning and memory. Metallomics : integrated biometal science 12:34–41

    Article  CAS  Google Scholar 

  • Carlos D, Costa FR, Pereira CA, Rocha FA, Yaochite JN, Oliveira GG, Carneiro FS, Tostes RC, Ramos SG, Zamboni DS, Camara NO, Ryffel B, Silva JS (2017) Mitochondrial DNA activates the nlrp3 inflammasome and predisposes to type 1 diabetes in murine model. Front Immunol 8:164

    Article  CAS  Google Scholar 

  • Chen D, Miao Z, Peng M, Xing H, Zhang H, Teng X (2019a) The co-expression of circRNA and mRNA in the thymuses of chickens exposed to ammonia. Ecotoxicol Environ Saf 176:146–152

    Article  CAS  Google Scholar 

  • Chen JQ, Xu YM, Han Q, Yao YC, Xing HJ, Teng XH (2019b) Immunosuppression, oxidative stress, and glycometabolism disorder caused by cadmium in common carp (Cyprinus carpio L.): application of transcriptome analysis in risk assessment of environmental contaminant cadmium. J Hazard Mater 366:386–394

    Article  CAS  Google Scholar 

  • Chen D, Ning F, Zhang J, Tang Y, Teng X (2020a) NF-kappa B pathway took part in the development of apoptosis mediated by miR-15a and oxidative stress via mitochondrial pathway in ammonia-treated chicken splenic lymphocytes. Sci Total Environ 729:139017

    Article  CAS  Google Scholar 

  • Chen J, Zhang S, Tong J, Teng X, Zhang Z, Li S, Teng X (2020b) Whole transcriptome-based miRNA-mRNA network analysis revealed the mechanism of inflammation-immunosuppressive damage caused by cadmium in common carp spleens. Sci Total Environ 717:137081

    Article  CAS  Google Scholar 

  • Chibowska K, Baranowska-Bosiacka I, Falkowska A, Gutowska I, Goschorska M, Chlubek D (2016) Effect of lead (pb) on inflammatory processes in the brain. Int J Mol Sci 17:2140

    Article  CAS  Google Scholar 

  • Franchi L, Eigenbrod T, Munoz-Planillo R, Nunez G (2009) The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat Immunol 10:241–247

    Article  CAS  Google Scholar 

  • Gargouri M, Hamed H, Akrouti A, Christian M, Ksouri R, El Feki A (2017) Immunomodulatory and antioxidant protective effect of Sarcocornia perennis L. (swampfire) in lead intoxicated rat. Toxicol Mech Methods 27:697–706

    Article  CAS  Google Scholar 

  • Green RE, Pain DJ (2019) Risks to human health from ammunition-derived lead in Europe. Ambio 48:954–968

    Article  CAS  Google Scholar 

  • Han Q, Tong J, Sun Q, Teng X, Zhang H, Teng X (2020a) The involvement of miR-6615-5p/Smad7 axis and immune imbalance in ammonia-caused inflammatory injury via NF-κB pathway in broiler kidneys. Poultry science

  • Han Q, Zhang J, Sun Q, Xu Y, Teng X (2020b) Oxidative stress and mitochondrial dysfunction involved in ammonia-induced nephrocyte necroptosis in chickens. Ecotoxicol Environ Saf 203:110974

    Article  CAS  Google Scholar 

  • Hu X, Chi Q, Liu Q, Wang D, Zhang Y, Li S (2019) Atmospheric H2S triggers immune damage by activating the TLR-7/MyD88/NF-kappaB pathway and NLRP3 inflammasome in broiler thymus. Chemosphere 237:124427

    Article  CAS  Google Scholar 

  • Huang H, An Y, Jiao W, Wang J, Li S, Teng X (2018) CHOP/caspase-3 signal pathway involves in mitigative effect of selenium on lead-induced apoptosis via endoplasmic reticulum pathway in chicken testes. Environ Sci Pollut Res Int 25:18838–18845

    Article  CAS  Google Scholar 

  • Huang H, Jiao X, Xu Y, Han Q, Jiao W, Liu Y, Li S, Teng X (2019a) Dietary selenium supplementation alleviates immune toxicity in the hearts of chickens with lead-added drinking water. Avian Pathol 48:230–237

    Article  CAS  Google Scholar 

  • Huang H, Wang Y, An Y, Jiao W, Xu Y, Han Q, Teng X, Teng X (2019b) Selenium alleviates oxidative stress and autophagy in lead-treated chicken testes. Theriogenology 131:146–152

    Article  CAS  Google Scholar 

  • Huang H, Li XY, Wang ZM, Lin X, Tian YG, Zhao Q, Zheng P (2020) Anti-inflammatory effect of selenium on lead-induced testicular inflammation by inhibiting NLRP3 inflammasome activation in chickens. Theriogenology 155:139–149

    Article  CAS  Google Scholar 

  • Jiao X, Yang K, An Y, Teng X, Teng X (2017) Alleviation of lead-induced oxidative stress and immune damage by selenium in chicken bursa of Fabricius. Environ Sci Pollut Res Int 24:7555–7564

    Article  CAS  Google Scholar 

  • Jiao WY, Han Q, Xu YM, Jiang HJ, Xing HJ, Teng XH (2019) Impaired immune function and structural integrity in the gills of common carp (Cyprinus carpio L.) caused by chlorpyrifos exposure: Through oxidative stress and apoptosis. Fish Shellfish Immun 86:239–245

    Article  CAS  Google Scholar 

  • Jin X, Xu Z, Zhao X, Chen MH, Xu SW (2017) The antagonistic effect of selenium on lead-induced apoptosis via mitochondrial dynamics pathway in the chicken kidney. Chemosphere 180:259–266

    Article  CAS  Google Scholar 

  • Joshi D, Mittal DK, Shukla S, Srivastav AK, Srivastav SK (2014) N-acetyl cysteine and selenium protects mercuric chloride-induced oxidative stress and antioxidant defense system in liver and kidney of rats: a histopathological approach. Journal of trace elements in medicine and biology : organ of the Society for Minerals and Trace Elements 28:218–226

    Article  CAS  Google Scholar 

  • Kim JY, Park JH, Kim K, Jo J, Leem J, Park KK (2018) Pharmacological inhibition of caspase-1 ameliorates cisplatin-induced nephrotoxicity through suppression of apoptosis, oxidative stress, and inflammation in mice. Mediat Inflamm 2018:6571676

    Google Scholar 

  • Krishnan RK, Nolte H, Sun T, Kaur H, Sreenivasan K, Looso M, Offermanns S, Kruger M, Swiercz JM (2015) Quantitative analysis of the TNF-alpha-induced phosphoproteome reveals AEG-1/MTDH/LYRIC as an IKKbeta substrate. Nat Commun 6:6658

    Article  CAS  Google Scholar 

  • Li M, Gao J, Li X (2005) Antagonistic action of selenium against the toxicity of lead. Wei Sheng Yan Jiu 34:375–377

    CAS  Google Scholar 

  • Li QW, Fu WH, Yao JW, Ji Z, Wang YQ, Zhou ZS, Yan JN, Li WB (2014) Heme induces IL-1 beta secretion through activating NLRP3 in kidney inflammation. Cell Biochem Biophys 69:495–502

    Article  CAS  Google Scholar 

  • Liu CM, Sun YZ, Sun JM, Ma JQ, Cheng C (2012) Protective role of quercetin against lead-induced inflammatory response in rat kidney through the ROS-mediated MAPKs and NF-kappa B pathway. Bba-Gen Subjects 1820:1693–1703

    Article  CAS  Google Scholar 

  • Liu CM, Yang HX, Ma JQ, Yang W, Feng ZJ, Sun JM, Cheng C, Li J, Jiang H (2018) Role of AMPK pathway in lead-induced endoplasmic reticulum stress in kidney and in paeonol-induced protection in mice. Food and chemical toxicology: an international journal published for the British Industrial Biological Research Association 122:87–94

    Article  CAS  Google Scholar 

  • Liu QQ, Wang W, Zhang YM, Cui Y, Xu SW, Li S (2020) Bisphenol A regulates cytochrome P450 1B1 through miR-27b-3p and induces carp lymphocyte oxidative stress leading to apoptosis. Fish Shellfish Immun 102:489–498

    Article  CAS  Google Scholar 

  • Matovic V, Buha A, Dukic-Cosic D, Bulat Z (2015) Insight into the oxidative stress induced by lead and/or cadmium in blood, liver and kidneys. Food Chem Toxicol 78:130–140

    Article  CAS  Google Scholar 

  • Mohammadi M, Ghaznavi R, Keyhanmanesh R, Sadeghipour HR, Naderi R, Mohammadi H (2014) Caloric restriction prevents lead-induced oxidative stress and inflammation in rat liver. Sci World J 2014:821524

    Google Scholar 

  • Sanchez OF, Lee J, Yu King Hing N, Kim SE, Freeman JL, Yuan C (2017) Lead (Pb) exposure reduces global DNA methylation level by non-competitive inhibition and alteration of dnmt expression. Metallomics : integrated biometal science 9:149–160

    Article  CAS  Google Scholar 

  • Schroder K, Tschopp J (2010) The inflammasomes. Cell 140:821–832

    Article  CAS  Google Scholar 

  • Shah SWA, Chen J, Han Q, Xu Y, Ishfaq M, Teng X (2020a) Ammonia inhalation impaired immune function and mitochondrial integrity in the broilers bursa of fabricius: implication of oxidative stress and apoptosis. Ecotoxicol Environ Saf 190:110078

    Article  CAS  Google Scholar 

  • Shah SWA, Ishfaq M, Nasrullah M, Qayum A, Akhtar MU, Jo H, Hussain M, Teng XH (2020b) Ammonia inhalation-induced inflammation and structural impairment in the bursa of fabricius and thymus of broilers through NF-kappa B signaling pathway. Environ Sci Pollut R 27:11596–11607

    Article  CAS  Google Scholar 

  • Shan Q, Zheng Y, Lu J, Zhang Z, Wu D, Fan S, Hu B, Cai X, Cai H, Liu P, Liu F (2014) Purple sweet potato color ameliorates kidney damage via inhibiting oxidative stress mediated NLRP3 inflammasome activation in high fat diet mice. Food and chemical toxicology: an international journal published for the British Industrial Biological Research Association 69:339–346

    Article  CAS  Google Scholar 

  • Sun GX, Chen Y, Liu CP, Li S, Fu J (2016) Effect of selenium against lead-induced damage on the gene expression of heat shock proteins and inflammatory cytokines in peripheral blood lymphocytes of chickens. Biol Trace Elem Res 172:474–480

    Article  CAS  Google Scholar 

  • Sun JX, Wang SC, Cao YR, Wang ST, Li S (2020) Cadmium exposure induces apoptosis, inflammation and immunosuppression through CYPs activation and antioxidant dysfunction in common carp neutrophils. Fish Shellfish Immun 99:284–290

    Article  CAS  Google Scholar 

  • Vunta H, Belda BJ, Arner RJ, Channa Reddy C, Vanden Heuvel JP, Sandeep Prabhu K (2008) Selenium attenuates pro-inflammatory gene expression in macrophages. Mol Nutr Food Res 52:1316–1323

    Article  CAS  Google Scholar 

  • Wang H, Li S, Teng XH (2016) The antagonistic effect of selenium on lead-induced inflammatory factors and heat shock proteins mRNA expression in chicken livers. Biol Trace Elem Res 171:437–444

    Article  CAS  Google Scholar 

  • Wang Y, Wang K, Huang H, Gu X, Teng X (2017) Alleviative effect of selenium on inflammatory damage caused by lead via inhibiting inflammatory factors and heat shock proteins in chicken testes. Environ Sci Pollut Res Int 24:13405–13413

    Article  CAS  Google Scholar 

  • Wang W, Chen M, Jin X, Li X, Yang Z, Lin H, Xu S (2018a) H2S induces Th1/Th2 imbalance with triggered NF-kappa B pathway to exacerbate LPS-induce chicken pneumonia response. Chemosphere 208:241–246

    Article  CAS  Google Scholar 

  • Wang XY, An Y, Jiao WY, Zhang ZY, Han H, Gu XH, Teng XH (2018b) Selenium protects against lead-induced apoptosis via endoplasmic reticulum stress in chicken kidneys. Biol Trace Elem Res 182:354–363

    Article  CAS  Google Scholar 

  • Wang S, Chi Q, Hu X, Cong Y, Li S (2019) Hydrogen sulfide-induced oxidative stress leads to excessive mitochondrial fission to activate apoptosis in broiler myocardia. Ecotoxicol Environ Saf 183:109578

    Article  CAS  Google Scholar 

  • Wang L, Wang L, Shi X, Xu S (2020) Chlorpyrifos induces the apoptosis and necroptosis of L8824 cells through the ROS/PTEN/PI3K/AKT axis. J Hazard Mater 398:122905

    Article  CAS  Google Scholar 

  • Wei H, Zhang R, Su Y, Bi Y, Li X, Zhang X, Li J, Bao J (2018) Effects of acute cold stress after long-term cold stimulation on antioxidant status, heat shock proteins, inflammation and immune cytokines in broiler heart. Front Physiol 9:1589

    Article  Google Scholar 

  • Xin C, Guangliang S, Qing Z, Qingqing L, Hang Y, Yiming Z, Shu L (2020) Astilbin protects chicken peripheral blood lymphocytes from cadmium-induced necroptosis via oxidative stress and the PI3K/Akt pathway. Ecotoxicol Environ Saf 190:110064

    Article  CAS  Google Scholar 

  • Yiming Z, Qingqing L, Hang Y, Yahong M, Shu L (2020) Selenium deficiency causes immune damage by activating the DUSP1/NF-kappaB pathway and endoplasmic reticulum stress in chicken spleen. Food Funct 11:6467–6475

    Article  Google Scholar 

  • Zhang R, Liu Y, Xing L, Zhao N, Zheng Q, Li J, Bao J (2018) The protective role of selenium against cadmium-induced hepatotoxicity in laying hens: expression of Hsps and inflammation-related genes and modulation of elements homeostasis. Ecotoxicol Environ Saf 159:205–212

    Article  CAS  Google Scholar 

  • Zhuang Y, Yasinta M, Hu C, Zhao M, Ding G, Bai M, Yang L, Ni J, Wang R, Jia Z, Huang S, Zhang A (2015) Mitochondrial dysfunction confers albumin-induced NLRP3 inflammasome activation and renal tubular injury. Am J Physiol Ren Physiol 308:F857–F866

    Article  CAS  Google Scholar 

Download references

Funding

The study was supported by National Natural Science Foundation of China (No. 31972612), the Heilongjiang Province on Natural Fund Project of China (No. LH2019C026), Smart Agricultural Engineering Research Center of Jilin Province Foundation, and Digital Agriculture key discipline of Jilin Province Foundation.

Author information

Authors and Affiliations

Authors

Contributions

He Huang was responsible for the research design, the performance of whole experiment, analysis of the data, and drafting the manuscript. Jianqing Chen helped to perform the experiments and analyse the data. Qi Sun and Yuhao Liu made contribution to the sample collection and treatment. You Tang made contribution to the technical assistance. Xiaohua Teng contributed significantly to the manuscript preparation. All listed authors have made substantial contributions to the research and publication.

Corresponding authors

Correspondence to You Tang or Xiaohua Teng.

Ethics declarations

All procedures used in this experiment were approved by the Northeast Agricultural University’s Institutional Animal Care and Use Committee under the approved protocol number SRM-06. Date of approval: 1 January 2018.

Competing interests

The authors declare that they have no conflict of interest.

Consent to participate

Written informed consent for publication was obtained from all participants.

Consent to publish

All authors read and approved the final manuscript. They agreed with the publication and consented to submit. They obtained consent from the responsible authorities at the Northeast Agricultural University.

Additional information

Responsible Editor: Mohamed M. Abdel-Daim

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

He Huang and Jianqing Chen are co-first authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, H., Chen, J., Sun, Q. et al. NLRP3 inflammasome is involved in the mechanism of mitigative effect of selenium on lead-induced inflammatory damage in chicken kidneys. Environ Sci Pollut Res 28, 10898–10908 (2021). https://doi.org/10.1007/s11356-020-11322-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-11322-w

Keywords

Navigation