Skip to main content
SpringerLink
Log in

Alleviative effect of selenium on inflammatory damage caused by lead via inhibiting inflammatory factors and heat shock proteins in chicken testes

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

Abstract

The aim of this study was to investigate ameliorative effect of selenium (Se) on lead (Pb)-induced inflammatory damage in chicken testes. One hundred eighty 7-day-old male chickens were randomly assigned into the control group, the Se group, the Pb group, and the Pb/Se group. Lead acetate was added in drinking water (350 mg/L Pb). Sodium selenite was added in the standard commercial diet (1 mg/kg Se). On the 30th, 60th, and 90th days of the experiment, 15 chickens of each group were euthanized. Inductively coupled plasma mass spectrometry, hematoxylin and eosin staining, real-time quantitative PCR, and Western blot were used. The results indicated that excess Pb increased nitric oxide content; inducible nitric oxide synthase (iNOS) activity; nuclear factor-kappa B (NF-κB), tumor necrosis factor-α, cyclooxygenase-2, prostaglandin E synthases, and iNOS mRNA levels in a time-dependent manner; NF-κB, iNOS, heat shock protein (HSP) 60, HSP70, and HSP90 protein levels; and Pb concentration. Excess Pb decreased Se concentration and induced histological changes. Se-alleviated Pb caused all of the above changes. Se improved Pb-caused inflammatory damage by decreasing the expression of inflammatory factors and heat shock proteins in the chicken testes. Our results provided theoretical basis of an alleviative effect of Se on Pb-induced bird testis damage.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Abdel-Moneim AM (2014) Histopathological and ultrastructural perturbations in tilapia liver as potential indicators of pollution in Lake Al-Asfar, Saudi Arabia. Environ Sci Pollut R 21:4387–4396. doi:10.1007/s11356-013-2185-9

    Article  CAS  Google Scholar 

  • Agarwal S, Roy S, Ray A, Mazumder S, Bhattacharya S (2009) Arsenic trioxide and lead acetate induce apoptosis in adult rat hepatic stem cells. Cell Biol Toxicol 25:403–413. doi:10.1007/s10565-008-9094-6

    Article  CAS  Google Scholar 

  • Ahamed M, Siddiqui MK (2007) Environmental lead toxicity and nutritional factors. Clin Nutr 26:400–408. doi:10.1016/j.clnu.2007.03.010

    Article  CAS  Google Scholar 

  • Ansar S, Abudawood M, Hamed SS, Aleem MM (2016) Sodium selenite protects against silver nanoparticle-induced testicular toxicity and inflammation. Biol Trace Elem Res:1–8. doi:10.1007/s12011-016-0759-3

  • Ashry KM, El-Sayed YS, Khamiss RM, El-Ashmawy IM (2010) Oxidative stress and immunotoxic effects of lead and their amelioration with myrrh (Commiphora molmol) emulsion. Food Chem Toxicol 48:236–241. doi:10.1016/j.fct.2009.10.006

    Article  CAS  Google Scholar 

  • Assi MA, Hezmee MNM, Haron AW, Sabri MYM, Rajion MA (2016) The detrimental effects of lead on human and animal health. Vet World 9:660–671. doi:10.14202/vetworld.2016.660-671

    Article  Google Scholar 

  • Atreya I, Atreya R, Neurath MF (2008) NF-κB in inflammatory bowel disease. J Intern Med 263:591–596. doi:10.1111/j.1365-2796.2008.01953.x

    Article  CAS  Google Scholar 

  • Bernabò P, Rebecchi L, Jousson O, Martínez-Guitarte JL, Lencioni V (2011) Thermotolerance and hsp70 heat shock response in the cold-stenothermal chironomid Pseudodiamesa branickii (NE Italy). Cell Stress Chaperones 16:403–410. doi:10.1007/s12192-010-0251-5

    Article  Google Scholar 

  • Binkowski ŁJ, Sawicka-Kapusta K, Szarek J, Strzyżewska E, Felsmann M (2013) Histopathology of liver and kidneys of wild living Mallards Anas platyrhynchos and Coots Fulica atra with considerable concentrations of lead and cadmium. Sci Total Environ 468-469:326–333. doi:10.1016/j.scitotenv.2013.02.002

    Article  Google Scholar 

  • Boulanger D, Brouillette E, Jaspar F, Malouin F, Mainil J, Bureau F, Lekeux P (2007) Helenalin reduces Staphylococcus aureus infection in vitro and in vivo. Vet Microbioly 119:330–338. doi:10.1016/j.vetmic.2006.08.020

    Article  CAS  Google Scholar 

  • Cao HB, Gao FY, Xia B, Zhang MM, Liao YL, Yang Z, Hu GL, Zhang CY (2016a) Alterations in trace element levels and mRNA expression of Hsps and inflammatory cytokines in livers of duck exposed to molybdenum or/and cadmium. Ecotox Environ Saf. 125:93–101. doi:10.1016/j.ecoenv.2015.12.003

    Article  CAS  Google Scholar 

  • Cao HB, Gao FY, Xia B, Xiao QY, Guo XQ, Hu GL, Zhang CY (2016b) The co-induced effects of molybdenum and cadmium on the mRNA expression of inflammatory cytokines and trace element contents in duck kidneys. Ecotox Environ Saf 133:157–163. doi:10.1016/j.ecoenv.2016.07.007

    Article  CAS  Google Scholar 

  • Chapa-Vargas L, Mejía-Saavedra JJ, Karina M-S, Puebla-Olivares F (2010) Blood lead concentrations in wild birds from a polluted mining region at Villa de La Paz, San Luis Potosí. Mexico Environ Sci Heal A 45:90–98. doi:10.1080/10934520903389242

    Article  CAS  Google Scholar 

  • Chun KS, Cha HH, Shin JW, Na HK, Park KK, Chung WY, Surh YJ (2004) Nitric oxide induces expression of cyclooxygenase-2 in mouse skin through activation of NF-êB. Carcinogenesis 25:445–454. doi:10.1093/carcin/bgh021

    Article  CAS  Google Scholar 

  • Du Y, Zhu YH, Teng XJ, Zhang K, Teng XH, Li S (2015) Toxicological effect of manganese on NF-κB/iNOS-COX-2 signaling pathway in chicken testes. Biol Trace Elem Res 168:227–234. doi:10.1007/s12011-015-0340-5

    Article  CAS  Google Scholar 

  • El-Ashmawy IM, Ashry KM, El-Nahas AF, Salama OM (2006) Protection by turmeric and myrrh against liver oxidative damage and genotoxicity induced by lead acetate in mice. Basic Clin Pha Rmacol 98:32–37. doi:10.1111/j.1742-7843.2006.pto_228.x

    Article  CAS  Google Scholar 

  • El-Neweshy MS, El-Sayed YS (2011) Influence of vitamin C supplementation on lead-induce histopathological alterations in male rats. Exp Toxicol Pathol 63:221–227. doi:10.1016/j.etp.2009.12.003

    Article  Google Scholar 

  • El-Sayed YS, El-Neweshy MS (2010) Impact of lead toxicity on male rat reproduction at hormonal and histopathological levels. Toxico Enviro Chem 92:765–774. doi:10.1080/02772240902984453

    Article  CAS  Google Scholar 

  • Gao H, Liu CP, Song SQ, Fu J (2016) Effects of dietary selenium against lead toxicity on mRNA levels of twenty-five selenoprotein genes in the cartilage tissue of broiler chicken. Biol Trace Elem Res 172:234–241. doi:10.1007/s12011-015-0579-x

    Article  CAS  Google Scholar 

  • Govindarajan TR, Jadhav AL (2001) Levels of protein kinase C and nitric oxide synthase activity in rats exposed to sub chronic low level lead. Mol Cell Biochem 223:27–33. doi:10.1023/A:1017549003114

    Article  Google Scholar 

  • Guo Y, Zhao PP, Guo GY, Hu ZB, Tian L, Zhang KX, Sun Y, Zhang XG, Zhang W, Xing MW (2016) Effects of arsenic trioxide exposure on heat shock protein response in the immune organs of chickens. Biol Trace Elem Res 169:134–141. doi:10.1007/s12011-015- 0389-1

    Article  CAS  Google Scholar 

  • Hseu YC, Wu FY, Wu JJ, Chen JY, Chang WH, Lu FJ, Lai YC, Yang HL (2006) Anti-inflammatory potential of Antrodia camphorata through inhibition of iNOS, COX-2 and cytokines via the NF-κB pathway. Int Immunopharmacol 5:1914–1925. doi:10.1016/j.intimp.2005.06.013

    Article  Google Scholar 

  • Huang H, Liu Y, Daniluk J, Wang H, Ji B, Logsdon CD (2013) Elevated acinar cell NF-κB activity increases pancreatitis severity. Pancreatology 13:e9. doi:10.1016/j.pan.2012.12.085

    Google Scholar 

  • Ivanina AV, Cherkasov AS, Sokolova IM (2008) Effects of cadmium on cellular protein and glutathione synthesis and expression of stress proteins in eastern oysters, Crassostrea virginica Gmelin. J Exp Biol 211:577–586. doi:10.1242/jeb.011262

    Article  CAS  Google Scholar 

  • Jiang ZH, Khoso PA, Yao HD, Zhang ZW, Zhang XY, Xu SW (2015) SelW regulates inflammation-related cytokines in response to H2O2 in Se-deficient chicken liver. RSC Adv 5:37896–37905

    Article  CAS  Google Scholar 

  • Jin X, Liu CP, Teng XH, Fu J (2016) Effects of dietary selenium against lead toxicity are related to the ion profile in chicken muscle. Biol Trace Elem Res 172:496–503. doi:10.1007/s12011-015-0585-z

    Article  CAS  Google Scholar 

  • Kim BM, Rhee JS, Jeong CB, Seo JS, Park GS, Lee YM, Lee JS (2014) Heavy metals induce oxidative stress and trigger oxidative stress-mediated heat shock protein (hsp) modulation in the intertidal copepod Tigriopus japonicus. Comp Biochem Physc 166:65–74. doi:10.1016/j.cbpc.2014.07.005

    CAS  Google Scholar 

  • Klaassen CD, Watkins JB (2013) Casarett and Doull’s toxicology: the basic science of poisons. McGraw-Hill 35:477

    Google Scholar 

  • Köhler HR, Alberti G, Seniczak S, Seniczak A (2005) Lead-induced hsp70 and hsp60 pattern transformation and leg malformation during postembryonic development in the oribatid mite, Archegozetes longisetosus Aoki. Comp Biochem Physiol, Part C 141:398–405. doi:10.1016/j.cbpc.2005.09.003

    Google Scholar 

  • Li JL, Gao R, Li S, Wang JT, Tang ZX, Xu SW (2010) Testicular toxicity induced by dietary cadmium in cocks and ameliorative effect by selenium. Biometals 23:695–705. doi:10.1007/s10534-010-9334-0

    Article  CAS  Google Scholar 

  • Liu CM, Ma JQ, Sun YZ (2010) Quercetin protects the rat kidney against oxidative stress-mediated DNA damage and apoptosis induced by lead. Environ Toxicol Phar 30:264–271. doi:10.1016/j.etap.2010.07.002

    Article  CAS  Google Scholar 

  • 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 Chemical Toxicol 60:168–176. doi:10.1016/j.fct.2013.07.058

    Article  CAS  Google Scholar 

  • Liu G, Li ZF, Wang JQ, Wang H, Wang ZY, Wang L (2014) Puerarin protects against lead-induced cytotoxicity in cultured primary rat proximal tubular cells. Hum Exp Toxicol 33:1071–1080. doi:10.1177/0960327114521048

    Article  Google Scholar 

  • Liu CP, Fu J, Liu C, Li S (2015a) The role of nitric oxide and autophagy in liver injuries induced by selenium deficiency in chickens. RSC Adv 5:50549–50556. doi:10.1039/C5RA01030F

    Article  CAS  Google Scholar 

  • Liu LL, Yang BY, Cheng YP, Lin HJ (2015b) Ameliorative effects of selenium on cadmium-induced oxidative stress and endoplasmic reticulum stress in the chicken kidney. Biol Trace Elem Res 167:308–319. doi:10.1007/s12011-015-0314-7

    Article  CAS  Google Scholar 

  • Liu S, Xu FP, Fu J, Li S (2015c) Protective roles of selenium on nitric oxide and the gene expression of inflammatory cytokines induced by cadmium in chicken splenic lymphocytes. Biol Trace Elem Res 168:1–9. doi:10.1007/s12011-015-0354-z

    Article  Google Scholar 

  • Mabrouk A, Salah IBH, Chaieb W, Cheikh HB (2016) Protective effect of thymoquinone against lead-induced hepatic toxicity in rats. Environ Sci Pollut R 23:12206–12215. doi:10.1007/s11356-016-6419-5

    Article  Google Scholar 

  • Mahmood K, Jadoon S (2014) Synergistic effects of toxic elements on heat shock proteins. Biomed Res Int 2015:564136–564136. doi:10.1155/2014/564136

    Google Scholar 

  • Mao JS, Dong J, Graedel TE (2008) The multilevel cycle of anthropogenic lead: II. Results and discussion. Resour Conserv Recy 52:1050–1057. doi:10.1016/j.resconrec.2008.04.005

    Article  Google Scholar 

  • Naha N, Bhar RB, Mukherjee A, Chowdhury AR (2005) Structural alteration of spermatozoa in the persons employed in lead acid battery factory. Indian J Physiol Pharmacol 49:153–162

    CAS  Google Scholar 

  • Osickova J, Skochova H, Ondracek K, Kral J, Damkova V, Peckova L, Pohanka M, Vitula F, Bandouchova H, Pikula J (2012) Risk of single and combined exposure of birds to non-steroidal anti-inflammatory drugs and lead. Neuro Endocrinol Lett 33(Suppl 3):145–150

    CAS  Google Scholar 

  • Patrick L (2006) Lead toxicity part II: the role of free radical damage and the use of antioxidants in the pathology and treatment of lead toxicity. Altern Med Rev 11:114–127

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sharma JN, Al-omran A, Parvathy SS (2007) Role of nitric oxide in inflammatory diseases. Inflammopharmaco 15:252–259. doi:10.1007/s10787-007-0013-x

    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. doi:10.1007/s12011-015-0602-2

    Article  CAS  Google Scholar 

  • Vengris VE, Mare CJ (1974) Lead poisoning in chickens and the effect of lead on interferon and antibody production. Can J Comp Med 38:328–335

    CAS  Google Scholar 

  • Wang MZ, Jia XY (2009) Low levels of lead exposure induce oxidative damage and DNA damage in the testes of the frog Rana nigromaculata. Ecotoxicology 18:94–99. doi:10.1007/s10646-008-0262-5

    Article  Google Scholar 

  • Wang LL, Liu T, Wang C, Zhao FQ, Zhang ZW, Yao HD, Xing HJ, Xu SW (2013) Effects of atrazine and chlorpyrifos on the production of nitric oxide and expression of inducible nitric oxide synthase in the brain of common carp (Cyprinus carpio L.) Ecotoxicol Environ Saf 93:7–12. doi:10.1016/j.ecoenv.2013.03.007

    Article  CAS  Google Scholar 

  • Wang H, Li S, Teng XH (2015) 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. doi:10.1007/s12011-015-0532-z

    Article  Google Scholar 

  • Xia B, Chen H, Hu GL, Wang LQ, Cao HB, Zhang CY (2016) The co-induced effects of molybdenum and cadmium on the trace elements and the mRNA expression levels of CP and MT in duck testicles. Biol Trace Elem Res 169:331–340. doi:10.1007/s12011-015-0410-8

    Article  CAS  Google Scholar 

  • Xing HJ, Li S, Wang X, Gao XJ, Xu SW, Wang XL (2013) Effects of atrazine and chlorpyrifos on the mRNA levels of HSP70 and HSC70 in the liver, brain, kidney and gill of common carp (Cyprinus carpio L.) Chemosphere 90:910–916. doi:10.1016/j.chemosphere.2012.06.028

    Article  CAS  Google Scholar 

  • Xing MW, Zhao PP, Guo GY, Guo Y, Zhang KX, Tian L, He Y, Chai HL, Zhang W (2015) Inflammatory factor alterations in the gastrointestinal tract of cocks overexposed to arsenic trioxide. Biol Trace Elem Res 167:1–12. doi:10.1007/s12011-015-0305-8

    Article  Google Scholar 

  • Xu Z, Wang Z, Li JJ, Chen C, Zhang PC, Dong L, Chen JH, Chen Q, Zhang XT, Wang ZL (2013) Protective effects of selenium on oxidative damage and oxidative stress related gene expression in rat liver under chronic poisoning of arsenic. Food Chem Toxicol 58:1–7. doi:10.1016/j.fct.2013.03.048

    Article  CAS  Google Scholar 

  • Yang ZJ, Liu C, Zheng WJ, Teng XH, Li S (2015) The functions of antioxidants and heat shock proteins are altered in the immune organs of selenium-deficient broiler chickens. Biol Trace Elem Res 169:341–351. doi:10.1007/s12011-015-0407-3

    Article  Google Scholar 

  • Yao HD, Wu Q, Zhang ZW, Zhang JL, Li S, Huang JQ, Ren FZ, Xu SW, Wang XL, Lei XG (2013a) Gene expression of endoplasmic reticulum resident selenoproteins correlates with apoptosis in various muscles of Se-deficient chicks. J Nutr 143:613–619. doi:10.3945/jn.112.172395

    Article  CAS  Google Scholar 

  • Yao HD, Wu Q, Zhang ZW, Li S, Wang XL, Lei XG, Xu SW (2013b) Selenoprotein W serves as an antioxidant in chicken myoblasts. BBA-Biomembranes 1830:112–3120. doi:10.1016/j.bbagen.2013.01.007

    Google Scholar 

  • Zhao FQ, Zhang ZW, Wang C, Zhang B, Yao HD, Li S, Xu SW (2013) The role of heat shock proteins in inflammatory injury induced by cold stress in chicken hearts. Cell Stress Chaperon. 18:773–783. doi:10.1007/s12192-013-0429-8

    Article  CAS  Google Scholar 

  • Zhao FQ, Zhang ZW, Qu JP, Yao HD, Li M, Li S, Xu SW (2014a) Cold stress induces antioxidants and Hsps in chicken immune organs. Cell Stress Chaperon 19:635–648. doi:10.1007/s12192-013-0489-9

    Article  CAS  Google Scholar 

  • Zhao WC, Liu W, Chen X, Zhu YH, Zhang ZW, Yao HD, Xu SW (2014b) Four endoplasmic reticulum resident selenoproteins may be related to the protection of selenium against cadmium toxicity in chicken lymphocytes. Biol Trace Elem Res 161:328–333. doi:10.1007/s12011-014-0135-0

    Article  CAS  Google Scholar 

  • Zheng SF, Song HY, Gao H, Liu CP, Zhang ZW, Fu J (2016) The antagonistic effect of selenium on lead-induced inflammatory factors and heat shock protein mRNA level in chicken cartilage tissue. Biol Trace Elem Res 173:177–184. doi:10.1007/s12011-016-0630-6

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The work was supported by the Heilongjiang Province on Natural Fund Project of China (No. 41400172-4-14089), the Agricultural Science and Technology Innovation Program (ASTIP-IAS07), and the Key Special Project of National Key Research Program (2016YFD0500507) in Beijing, China.

Author information

Authors and Affiliations

  1. College of Animal Science and Technology, Northeast Agricultural University, Harbin, 150030, People’s Republic of China

    Yan Wang, Kexin Wang, He Huang & Xiaohua Teng

  2. Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, 100193, People’s Republic of China

    Xianhong Gu

Authors
  1. Yan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kexin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. He Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xianhong Gu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiaohua Teng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Xianhong Gu or Xiaohua Teng.

Ethics declarations

Informed consent was obtained from all individual participants included in the study.

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Responsible editor: Philippe Garrigues

All authors have read the manuscript and agreed to submit it in its current form for consideration for publication in Environmental Science and Pollution Research.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, Y., Wang, K., Huang, H. et al. 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 24, 13405–13413 (2017). https://doi.org/10.1007/s11356-017-8785-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-017-8785-z

Keywords

Search

Navigation