Skip to main content
SpringerLink
Log in

Effects of Molybdenum or/and Cadmium on mRNA Expression Levels of Inflammatory Cytokines and HSPs in Duck Spleens

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Cadmium (Cd) and high dietary intake of molybdenum (Mo) can cause multiple-organ injury in animals, but the co-induced toxicity of Mo and Cd to spleen in ducks is not well understood. The aim of this study was to investigate the co-induced effects of Mo and Cd on the mRNA expression levels of inflammatory cytokines and heat shock proteins (HSPs) in duck spleens. Two hundred forty healthy 11-day-old ducks were randomly divided into six groups and treated with a commercial diet containing Mo or/and Cd. After being treated with Mo or/and Cd for 30, 60, 90, and 120 days, the mRNA expression levels of nuclear factor-kappa B (NF-κB), tumor necrosis factor-α (TNF-α), cyclooxygenase-2 (COX-2), HSP60, HSP70, and HSP90 were examined in duck spleens. Histopathology was examined in duck spleens at 120 days. The results indicated that the mRNA expression levels of HSPs were significantly upregulated in the co-induced groups (P < 0.01), while these decreased in the high dietary intake of Mo combined with Cd group at 120 days. Exposure to Mo or/and Cd upregulated the mRNA expression levels of NF-κB, COX-2, and TNF-α in the combination groups (P < 0.01). Furthermore, severe congestion, bleeding, splenic corpuscle structure fuzzy, wall thickness of sheath artery thickening, and oxyhematin were observed in the spleens of combination groups. Meanwhile, the organizational structure damage of the combined groups was more severe than that of the other groups. These results suggested that exposure to Mo or/and Cd might lead to tissue damage, and high expression of HSPs and inflammatory cytokines may play a role in the resistance of spleen toxicity induced by Mo or/and Cd. Interaction of Mo and Cd may have a synergistic effect on spleen toxicity.

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

Similar content being viewed by others

References

  1. McEwan AG, Ridge JP, McDevitt CA, Hugenholtz P (2002) The DMSO reductase family of microbial molybdenum enzymes; molecular properties and role in the dissimilatory reduction of toxic elements. Geomicrobiol J 19:3–21

    Article  CAS  Google Scholar 

  2. Kumchai J, Huang JZ, Lee CY, Chen FC, Chin SW (2013) Proline partially overcomes excess molybdenum toxicity in cabbage seedlings grown in vitro. Genet Mol Res 12:5589–5601. doi:10.4238/2013.November.18.8

    Article  CAS  PubMed  Google Scholar 

  3. Othman AR, Bakar NA, Halmi MI, Johari WL, Ahmad SA, Jirangon H, Syed MA, Shukor MY (2013) Kinetics of molybdenum reduction to molybdenum blue by Bacillus sp. strain A.rzi. Biomed Res Int. doi:10.1155/2013/371058

    Google Scholar 

  4. Aupperle H, Schoon HA, Frank A (2001) Experimental copper deficiency, chromium deficiency and additional molybdenum supplementation in goats—pathological findings. Acta Vet Scand 42:311–321

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  5. Bersenyi A, Berta E, Kadar I, Glavits R, Szilagyi M, Fekete SG (2008) Effects of high dietary molybdenum in rabbits. Acta Vet Hung 56:41–55. doi:10.1556/AVet.56.2008.1.5

    Article  CAS  PubMed  Google Scholar 

  6. Bulat ZP, Djukić-Cosić D, Malicević Z, Bulat P, Matović V (2008) Zinc or magnesium supplementation modulates Cd intoxication in blood, kidney, spleen, and bone of rabbits. Biol Trace Elem Res 124:110–117. doi:10.1007/s12011-008-8128-5

    Article  CAS  PubMed  Google Scholar 

  7. Suntararuks S, Yoopan N, Rangkadilok N, Worasuttayangkurn L, Nookabkaew S, Satayavivad J (2008) Immunomodulatory effects of cadmium and Gynostemma pentaphyllum herbal tea on rat splenocyte proliferation. J Agric Food Chem 56:9305–9311. doi:10.1021/jf801062z

    Article  CAS  PubMed  Google Scholar 

  8. Risso-de Faverney C, Orsini N, de Sousa G, Rahmani R (2004) Cadmium-induced apoptosis through the mitochondrial pathway in rainbow trout hepatocytes: involvement of oxidative stress. Aquat Toxicol 69:247–258

    Article  CAS  PubMed  Google Scholar 

  9. Pathak N, Khandelwal S (2007) Role of oxidative stress and apoptosis in cadmium induced thymic atrophy and splenomegaly in mice. Toxicol Lett 169:95–108

    Article  CAS  PubMed  Google Scholar 

  10. Holaskova I, Elliott M, Hanson ML, Schafer R, Barnett JB (2012) Prenatal cadmium exposure produces persistent changes to thymus and spleen cell phenotypic repertoire as well as the acquired immune response. Toxicol Appl Pharmacol 265:181–189. doi:10.1016/j.taap.2012.10.009

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  11. Suresh N (2009) Effect of cadmium chloride on liver, spleen and kidney melano macrophage centres in Tilapia mossambica. J Environ Biol 30:505–508

    CAS  PubMed  Google Scholar 

  12. Xia B, Cao H, Luo J, Liu P, Guo X, Hu G, Zhang C (2015) The co-induced effects of molybdenum and cadmium on antioxidants and heat shock proteins in duck kidneys. Biol Trace Elem Res. doi:10.1007/s12011-015-0348-x

    Google Scholar 

  13. Horiguchi H, Oguma E, Kayama F (2011) Cadmium induces anemia through interdependent progress of hemolysis, body iron accumulation, and insufficient erythropoietin production in rats. Toxicol Sci 122:198–210. doi:10.1093/toxsci/kfr100

    Article  CAS  PubMed  Google Scholar 

  14. Bozaykut P, Ozer NK, Karademir B (2014) Regulation of protein turnover by heat shock proteins. Free Radic Biol Med 77:195–209. doi:10.1016/j.freeradbiomed.2014.08.012

    Article  CAS  PubMed  Google Scholar 

  15. Al-Aqil A, Zulkifli I (2009) Changes in heat shock protein 70 expression and blood characteristics in transported broiler chickens as affected by housing and early age feed restriction. Poult Sci 88:1358–1364. doi:10.3382/ps.2008-00554

    Article  CAS  PubMed  Google Scholar 

  16. Zhang J, Liu B, Li J, Zhang L, Wang Y, Zheng H, Lu M, Chen J (2015) Hsf and Hsp gene families in Populus: genome-wide identification, organization and correlated expression during development and in stress responses. BMC Genomics. doi:10.1186/s12864-015-1398-3

    Google Scholar 

  17. Purandhar K, Jena PK, Prajapati B, Rajput P, Seshadri S (2014) Understanding the role of heat shock protein isoforms in male fertility, aging and apoptosis. World J Mens Health 32:123–132. doi:10.5534/wjmh.2014.32.3.123

    Article  PubMed Central  PubMed  Google Scholar 

  18. Ou JR, Tan MS, Xie AM, Yu JT, Tan L (2014) Heat shock protein 90 in Alzheimer’s disease. Biomed Res Int. doi:10.1155/2014/796869

    Google Scholar 

  19. Liu HH, He JY, Chi CF, Shao J (2014) Differential HSP70 expression in Mytilus coruscus under various stressors. Gene 543:166–173. doi:10.1016/j.gene.2014.04.008

    Article  CAS  PubMed  Google Scholar 

  20. Jimi S, Uchiyama M, Takaki AYA, Suzumiya J, Hara S (2004) Mechanisms of cell death induced by cadmium and arsenic. Ann N Y Acad Sci 1011:325–331

    Article  CAS  PubMed  Google Scholar 

  21. Lee E, Yin Z, Sidoryk-Wegrzynowicz M, Jiang H, Aschner M (2012) 15-Deoxy-Δ12,14-prostaglandin J2 modulates manganese-induced activation of the NF-κB, Nrf2, and PI3K pathways in astrocytes. Free Radic Biol Med 52:1067–1074. doi:10.1016/j.freeradbiomed.2011.12.016

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  22. Ferencz A, Juhasz R, Butnariu M, Deer AK, Varga IS, Nemcsok J (2012) Expression analysis of heat shock genes in the skin, spleen and blood of common carp (Cyprinus carpio) after cadmium exposure and hypothermia. Acta Biol Hung 63:15–25. doi:10.1556/ABiol.63.2012.1.2

    Article  PubMed  Google Scholar 

  23. Chen X, Zhu YH, Cheng XY, Zhang ZW, Xu SW (2012) The protection of selenium against cadmium-induced cytotoxicity via the heat shock protein pathway in chicken splenic lymphocytes. Molecules 17:14565–14572. doi:10.3390/molecules171214565

    Article  CAS  PubMed  Google Scholar 

  24. Voellmy R (2005) Dominant-positive and dominant-negative heat shock factors. Methods 35:199–207

    Article  CAS  PubMed  Google Scholar 

  25. Zhu J, Katz RJ, Quyyumi AA, Canos DA, Rott D, Csako G, Zalles-Ganley A, Ogunmakinwa J, Wasserman AG, Epstein SE (2004) Association of serum antibodies to heat-shock protein 65 with coronary calcification levels: suggestion of pathogen-triggered autoimmunity in early atherosclerosis. Circulation 109:36–41

    Article  CAS  PubMed  Google Scholar 

  26. Liu S, Wang X, Li Y, Xu L, Yu X, Ge L, Li J, Zhu Y, He S (2014) Necroptosis mediates TNF-induced toxicity of hippocampal neurons. Biomed Res Int. doi:10.1155/2014/290182

    Google Scholar 

  27. Xie J, Shaikh ZA (2006) Cadmium-induced apoptosis in rat kidney epithelial cells involves decrease in nuclear factor-kappa B activity. Toxicol Sci 91:299–308

    Article  CAS  PubMed  Google Scholar 

  28. Bonizzi G, Karin M (2004) The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol 25:280–288

    Article  CAS  PubMed  Google Scholar 

  29. Kim JH, Kim SJ (2014) Overexpression of microRNA-25 by withaferin a induces cyclooxygenase-2 expression in rabbit articular chondrocytes. J Pharmacol Sci 125:83–90

    Article  CAS  PubMed  Google Scholar 

  30. Park MH, Song HS, Kim KH, Son DJ, Lee SH, Yoon DY, Kim Y, Park IY, Song S, Hwang BY, Jung JK, Hong JT (2005) Cobrotoxin inhibits NF-kappa B activation and target gene expression through reaction with NF-kappa B signal molecules. Biochemistry 44:8326–8336

    Article  CAS  PubMed  Google Scholar 

  31. Asea A, Kraeft SK, Kurt-Jones EA, Stevenson MA, Chen LB, Finberg RW, Koo GC, Calderwood SK (2000) HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat Med 6:435–442

    Article  CAS  PubMed  Google Scholar 

  32. Chen L, Zhou J, Gao W, Jiang YZ (2003) Action of NO and TNF-α release of rats with cadmium loading in malfunction of multiple system organs. Sheng Li Xue Bao 55:535–540

    CAS  PubMed  Google Scholar 

  33. Du Y, Zhu Y, Teng X, Zhang K, Teng X, Li S (2015) Toxicological effect of manganese on NF-kappaB/iNOS-COX-2 signaling pathway in chicken testes. Biol Trace Elem Res. doi:10.1007/s12011-015-0340-5

    Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (No. 31260625, Beijing, People’s Republic of China) and the Training Plan for Young Scientists of Jiangxi Province (No. 2014BCB23040, Nanchang, People’s Republic of China). All authors thank all members of the team for their help in the experimental process in clinical veterinary medicine laboratory in the College of Animal Science and Technology, Jiangxi Agricultural University.

Conflict of Interest

The authors declare that they have no competing interests.

Author information

Authors and Affiliations

  1. Institute of Animal Population Health, College of Animal Science and Technology, Jiangxi Agricultural University, No. 1101 Zhimin Avenue, Economic and Technological Development District, Nanchang, 330045, Jiangxi, People’s Republic of China

    Huabin Cao, Mengmeng Zhang, Bing Xia, Jin Xiong, Yibo Zong, Guoliang Hu & Caiying Zhang

Authors
  1. Huabin Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mengmeng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bing Xia
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jin Xiong
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yibo Zong
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Guoliang Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Caiying Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Guoliang Hu or Caiying Zhang.

Additional information

All authors have read the manuscript and agreed to submit it in its current form for consideration for publication in the Journal.

Huabin Cao, Mengmeng Zhang, and Bing Xia are the first authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cao, H., Zhang, M., Xia, B. et al. Effects of Molybdenum or/and Cadmium on mRNA Expression Levels of Inflammatory Cytokines and HSPs in Duck Spleens. Biol Trace Elem Res 170, 237–244 (2016). https://doi.org/10.1007/s12011-015-0442-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-015-0442-0

Keywords

Search

Navigation