Log in

Protective Effect of Agaricus blazei Polysaccharide Against Cadmium-Induced Damage on the Testis of Chicken

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

Abstract

Cadmium (Cd) exposure can cause reproductive toxicity through oxidative stress and inflammatory response. A polysaccharide extract of the edible mushroom Agaricus blazei Murill has been isolated and exhibits antioxidant activity and immunoregulatory effect. The aim of this study was to investigate the protective role of Agaricus blazei polysaccharide (ABP) against Cd-induced damage in chicken testis through enhancing antioxidant activity and alleviating inflammatory response. One hundred twenty healthy 7-day-old Hy-Line male chickens (Harbin, China) were randomly divided into four groups, and each group consisted of 30 chickens: Normal control was fed daily with full feed and 0.2 mL distilled water per day via oral gavage; Cd-treated group was fed daily with full feed that contained 140 mg/kg CdCl2 and 0.2 mL distilled water per day by gavage; Polysaccharide-treated group was fed daily with full feed with 0.2 mL ABP(30 mg/ml) solution per day via oral gavage; Cd/polysaccharide-treated group was fed daily with full feed containing 140 mg/kg CdCl2 and 0.2 mL ABP(30 mg/ml) solution per day by gavage. On the 20, 40, and 60 days, the testis was immediately removed. The contents of Cd in the testis, activities of superoxide dismutase (SOD) and glutathione peroxidase (GSH-Px), malondialdehyde (MDA) production, messenger RNA (m RNA) levels of tumor necrosis factor-alpha (TNF-α), interleukin-1 beta (IL-1β), and interleukin-6 (IL-6), protein expressions of heat shock proteins (HSPs) (HSP60, HSP70, and HSP90), and the histopathological changes of the testis were determined. The results indicated that ABP improved Cd-caused testicular tissue damage by increasing the SOD and GSH-Px activities: decreasing the Cd accumulation and MDA content, mRNA levels of TNF-α, IL-1β, and IL-6, and protein expressions of HSP60, HSP70, and HSP90. Results suggest that ABP for the mitigation of damage induced by cadmium in chicken testis through enhancing antioxidant activity and alleviating Inflammatory response.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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
Fig. 6

Similar content being viewed by others

References

  1. ** Y, Zhang S, Tao R, Huang J, He X, Qu L, Fu Z (2016) Oral exposure of mice to cadmium (II), chromium (VI) and their mixture induce oxidative- and endoplasmic reticulum-stress mediated apoptosis in the livers. Environ Toxicol 31(6):693–705

    Article  CAS  PubMed  Google Scholar 

  2. Phuc HD, Kido T, Oanh NTP, Manh HD, Anh LT, Oyama Y, Okamoto R, Ichimori A, Nogawa K, Suwazono Y, Nakagawa H (2017) Effects of aging on cadmium concentrations and renal dysfunction in inhabitants in cadmium-polluted regions in Japan. Journal of applied toxicology : JAT 37(9):1046–1052

    Article  CAS  PubMed  Google Scholar 

  3. Ronchetti SA, Novack GV, Bianchi MS, Crocco MC, Duvilanski BH, Cabilla JP (2016) In vivo xenoestrogenic actions of cadmium and arsenic in anterior pituitary and uterus. Reproduction (Cambridge, England) 152(1):1–10

    Article  CAS  Google Scholar 

  4. Siu ER, Mruk DD, Porto CS, Cheng CY (2009) Cadmium-induced testicular injury. Toxicol Appl Pharmacol 238(3):240–249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Wang YJ, Yan J, Zou XL, Guo KJ, Zhao Y, Meng CY, Yin F, Guo L (2017) Bone marrow mesenchymal stem cells repair cadmium-induced rat testis injury by inhibiting mitochondrial apoptosis. Chem Biol Interact 271:39–47

    Article  CAS  PubMed  Google Scholar 

  6. Li JL, Gao R, Li S, Wang JT, Tang ZX, SW X (2010) Testicular toxicity induced by dietary cadmium in cocks and ameliorative effect by selenium. Biometals 23(4):695–705

    Article  CAS  PubMed  Google Scholar 

  7. Sadek KM, Lebda MA, Abouzed TK, Nasr SM, Shoukry M (2017) Neuro- and nephrotoxicity of subchronic cadmium chloride exposure and the potential chemoprotective effects of selenium nanoparticles. Metab Brain Dis 32(5):1659–1673

    Article  CAS  PubMed  Google Scholar 

  8. Liu S, FP X, Yang ZJ, Li M, Min YH, Li S (2014) Cadmium-induced injury and the ameliorative effects of selenium on chicken splenic lymphocytes: mechanisms of oxidative stress and apoptosis. Biol Trace Elem Res 160(3):340–351

    Article  CAS  PubMed  Google Scholar 

  9. Abdel-Rahim EA, Abdel-Mobdy YE, Ali RF, Mahmoud HA (2014) Hepatoprotective effects of Solanum nigrum Linn fruits against cadmium chloride toxicity in albino rats. Biol Trace Elem Res 160(3):400–408

    Article  CAS  PubMed  Google Scholar 

  10. Olszowski T, Baranowska-Bosiacka I, Gutowska I, Chlubek D (2012) Pro-inflammatory properties of cadmium. Acta Biochim Pol 59(4):475–482

    Article  CAS  PubMed  Google Scholar 

  11. Kim SJ, Um JY, Kim SH, Hong SH (2013) Protective effect of rosmarinic acid is through regulation of inflammatory cytokine in cadmium-induced ototoxicity. Am J Chin Med 41(2):391–404

    Article  CAS  PubMed  Google Scholar 

  12. Zivkovic L, Borozan S, Cabarkapa A, Topalovic D, Ciptasari U, Bajic V, Spremo-Potparevic B (2017) Antigenotoxic properties of Agaricus blazei against hydrogen peroxide in human peripheral blood cells. Oxidative Med Cell Longev 2017:8759764

    Article  CAS  Google Scholar 

  13. Liu XR, Wang YY, Fan HR, CJ W, Kumar A, Yang LG (2016) Preventive effects of beta-cryptoxanthin against cadmium-induced oxidative stress in the rat testis. Asian J Androl 18(6):920–924

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Merra E, Calzaretti G, Bobba A, Storelli MM, Casalino E (2014) Antioxidant role of hydroxytyrosol on oxidative stress in cadmium-intoxicated rats: different effect in spleen and testes. Drug Chem Toxicol 37(4):420–426

    Article  CAS  PubMed  Google Scholar 

  15. Jahan S, Zahra A, Irum U, Iftikhar N, Ullah H (2014) Protective effects of different antioxidants against cadmium induced oxidative damage in rat testis and prostate tissues. Syst Biol Reprod Med 60(4):199–205

    Article  CAS  PubMed  Google Scholar 

  16. Zhang C, Li S, Zhang J, Hu C, Che G, Zhou M, Jia L (2016) Antioxidant and hepatoprotective activities of intracellular polysaccharide from Pleurotus eryngii SI-04. Int J Biol Macromol 91:568–577

    Article  CAS  PubMed  Google Scholar 

  17. Amamou F, Nemmiche S, Meziane RK, Didi A, Yazit SM, Chabane-Sari D (2015) Protective effect of olive oil and colocynth oil against cadmium-induced oxidative stress in the liver of Wistar rats. Food and chemical toxicology : an international journal published for the British Industrial Biological Research Association 78:177–184

    Article  CAS  Google Scholar 

  18. de Souza Predes F, da Silva Diamante MA, Foglio MA, Camargo Cde A, Aoyama H, Miranda SC, Cruz B, Gomes Marcondes MC, Dolder H (2014) Hepatoprotective effect of Arctium lappa root extract on cadmium toxicity in adult Wistar rats. Biol Trace Elem Res 160(2):250–257

    Article  PubMed  CAS  Google Scholar 

  19. Wu S, Li F, Jia S, Ren H, Gong G, Wang Y, Lv Z, Liu Y (2014) Drying effects on the antioxidant properties of polysaccharides obtained from Agaricus blazei Murrill. Carbohydr Polym 103:414–417

    Article  CAS  PubMed  Google Scholar 

  20. da Silva de Souza AC, Correa VG, Goncalves GA, Soares AA, Bracht A, Peralta RM (2017) Agaricus blazei bioactive compounds and their effects on human health: benefits and controversies. Curr Pharm Des 23(19):2807–2834

    Article  PubMed  CAS  Google Scholar 

  21. Wang P, Li XT, Sun L, Shen L (2013) Anti-inflammatory activity of water-soluble polysaccharide of Agaricus blazei Murill on ovariectomized osteopenic rats. Evid Based Complement Alternat Med: eCAM 2013:164817

    PubMed  PubMed Central  Google Scholar 

  22. Ni WY, MF W, Liao NC, Yeh MY, HF L, Hsueh SC, Liu JY, Huang YP, Chang CH, Chung JG (2013) Extract of medicinal mushroom Agaricus blazei Murill enhances the non-specific and adaptive immune activities in BALB/c mice. In vivo (Athens, Greece) 27(6):779–786

    CAS  Google Scholar 

  23. Spiazzi CC, Manfredini V, Barcellos da Silva FE, Flores EM, Izaguirry AP, Vargas LM, Soares MB, Santos FW (2013) Gamma-Oryzanol protects against acute cadmium-induced oxidative damage in mice testes. Food Chem Toxicol 55:526–532

    Article  CAS  PubMed  Google Scholar 

  24. Chemek M, Mimouna SB, Boughammoura S, Delbes G, Messaoudi I (2016) Protective role of zinc against the toxicity induced by exposure to cadmium during gestation and lactation on testis development. Reprod Toxicol (Elmsford, NY) 63:151–160

    Article  CAS  Google Scholar 

  25. Marettova E, Maretta M, Legath J (2015) Toxic effects of cadmium on testis of birds and mammals: a review. Anim Reprod Sci 155:1–10

    Article  CAS  PubMed  Google Scholar 

  26. Liu Y, Zhang L, Zhu X, Wang Y, Liu W, Gong W (2015) Polysaccharide Agaricus blazei Murill stimulates myeloid derived suppressor cell differentiation from M2 to M1 type, which mediates inhibition of tumour immune-evasion via the toll-like receptor 2 pathway. Immunology 146(3):379–391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Li X, Zhao X, Wang H, Han J, Liu L (2014) A polysaccharide from the fruiting bodies of Agaricus blazei Murill induces caspase-dependent apoptosis in human leukemia HL-60 cells. Tumour biology : the journal of the International Society for Oncodevelopmental Biology and Medicine 35(9):8963–8968

    Article  CAS  Google Scholar 

  28. Hu X, Zhang R, **e Y, Wang H, Ge M (2017) The protective effects of polysaccharides from Agaricus blazei Murill against cadmium-induced oxidant stress and inflammatory damage in chicken livers. Biol Trace Elem Res 178(1):117–126

    Article  CAS  PubMed  Google Scholar 

  29. Yang SH, Long M, LH Y, Li L, Li P, Zhang Y, Guo Y, Gao F, Liu MD, He JB (2016) Sulforaphane prevents testicular damage in Kunming mice exposed to cadmium via activation of Nrf2/ARE signaling pathways. Int J Mol Sci 17(10)

    Article  PubMed Central  CAS  Google Scholar 

  30. Sivaprakasam C, Nachiappan V (2016) Modulatory effect of cadmium on the expression of phospholipase A2 and proinflammatory genes in rat testis. Environ Toxicol 31(10):1176–1184

    Article  CAS  PubMed  Google Scholar 

  31. Verçosa Junior D, Oliveira NJFD, Duarte ER, Bastos GA, Soares ACM, Cassali GD, Sotoblanco B, Melo MM (2016) Serum hepatic biochemistry and electrophoretic protein profile of healthy and Ehrlich tumor-bearing mice treated with extracts of Agaricus blazei Murill. Semina Ciencias Agrarias 37(2):763

    Article  CAS  Google Scholar 

  32. de Sa-Nakanishi AB, Soares AA, Natali MR, Comar JF, Peralta RM, Bracht A (2014) Effects of the continuous administration of an Agaricus blazei extract to rats on oxidative parameters of the brain and liver during aging. Molecules (Basel, Switzerland) 19(11):18590–18603

    Article  CAS  Google Scholar 

  33. Elmallah MIY, Elkhadragy MF, Al-Olayan EM, Abdel Moneim AE (2017) Protective effect of Fragaria ananassa crude extract on cadmium-induced lipid peroxidation, antioxidant enzymes suppression, and apoptosis in rat testes. Int J Mol Sci 18(5)

    Article  PubMed Central  CAS  Google Scholar 

  34. Abdelrazek HM, Helmy SA, Elsayed DH, Ebaid HM, Mohamed RM (2016) Ameliorating effects of green tea extract on cadmium induced reproductive injury in male Wistar rats with respect to androgen receptors and caspase-3. Reprod Biol 16(4):300–308

    Article  PubMed  Google Scholar 

  35. Cilenk KT, Ozturk I, Sonmez MF (2016) Ameliorative effect of propolis on the cadmium-induced reproductive toxicity in male albino rats. Exp Mol Pathol 101(2):207–213

    Article  CAS  PubMed  Google Scholar 

  36. Kheradmand A, Alirezaei M, Dezfoulian O (2013) Cadmium-induced oxidative stress in the rat testes: protective effects of betaine. Int J Pept Res Ther 19(4):337–344

    Article  CAS  Google Scholar 

  37. Varoni MV, Gadau SD, Pasciu V, Baralla E, Serra E, Palomba D, Demontis MP (2017) Investigation of the effects of Lycium barbarum polysaccharides against cadmium induced damage in testis. Exp Mol Pathol 103(1):26–32

    Article  CAS  PubMed  Google Scholar 

  38. Jia S, Li F, Liu Y, Ren H, Gong G, Wang Y, Wu S (2013) Effects of extraction methods on the antioxidant activities of polysaccharides from Agaricus blazei Murrill. Int J Biol Macromol 62:66–69

    Article  CAS  PubMed  Google Scholar 

  39. Yurkiv B, Wasser SP, Nevo E, Sybirna NO (2015) Antioxidant effects of medicinal mushrooms Agaricus brasiliensis and Ganoderma lucidum (higher Basidiomycetes): evidence from animal studies. Int J Med Mushrooms 17(10):943–955

    Article  PubMed  Google Scholar 

  40. de Sa-Nakanishi AB, Soares AA, de Oliveira AL, Comar JF, Peralta RM, Bracht A (2014) Effects of treating old rats with an aqueous Agaricus blazei extract on oxidative and functional parameters of the brain tissue and brain mitochondria. Oxidative Med Cell Longev 2014:563179

  41. Li R, Luo X, Li L, Peng Q, Yang Y, Zhao L, Ma M, Hou Z (2016) The protective effects of melatonin against oxidative stress and inflammation induced by acute cadmium exposure in mice testis. Biol Trace Elem Res 170(1):152–164

    Article  CAS  PubMed  Google Scholar 

  42. de Freitas ML, Dalmolin L, Oliveira LP, da Rosa Moreira L, Roman SS, Soares FA, Bresolin L, Duarte MM, Brandao R (2012) Effects of butane-2,3-dione thiosemicarbazone oxime on testicular damage induced by cadmium in mice. J Toxicol Sci 37(5):899–910

    Article  PubMed  Google Scholar 

  43. Djuric A, Djukic M, Begic A, Djukic-Cosic D, Stevanovic I, Ninkovic M (2014) Disulfiram reduces lipid peroxidation in testes of rat subchronically exposed to ethanol and cadmium. 14th ISANH Congress on Oxidative Stress Reduction, Redox Homeostasis and Antioxidants, Paris

  44. Kheradmand A, Alirezaei M, Dezfoulian O (2013) Cadmium-induced oxidative stress in the rat testes: protective effects of betaine. International Journal of Peptide Research & Therapeutics 19(4):337–344

    Article  CAS  Google Scholar 

  45. Hoek JB, Pastorino JG (2002) Ethanol, oxidative stress, and cytokine-induced liver cell injury. Alcohol (Fayetteville, NY) 27(1):63–68

    Article  CAS  Google Scholar 

  46. Chen CY, Huang YL, Lin TH (1998) Association between oxidative stress and cytokine production in nickel-treated rats. Arch Biochem Biophys 356(2):127–132

    Article  CAS  PubMed  Google Scholar 

  47. Martins PR, de Campos Soares AMV, Silva Pinto d, Domeneghini AV, Golim MA, Kaneno R (2017) Agaricus brasiliensis polysaccharides stimulate human monocytes to capture Candida albicans, express toll-like receptors 2 and 4, and produce pro-inflammatory cytokines. J Venom Anim Toxins Incl Trop Dis 23:17

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Sun X, Li S, He Y, Zhao H, Wang Y, Zeng X, **ng M (2017) Arsenic-induced testicular toxicity in Gallus gallus: expressions of inflammatory cytokines and heat shock proteins. Poult Sci 96(9):3399–3406

    Article  CAS  PubMed  Google Scholar 

  49. Chen XM, Guo GL, Sun L, Yang QS, Wang GQ, Zhang DM (2017) Modulatory role of L-carnitine against microcystin-LR-induced immunotoxicity and oxidative stress in common carp. Fish Physiol Biochem 43(4):1081–1093

    Article  CAS  PubMed  Google Scholar 

  50. Wang H, Li S, Teng X (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(2):437–444

    Article  CAS  PubMed  Google Scholar 

  51. Kusakabe T, Nakajima K, Nakazato K, Suzuki K, Takada H, Satoh T, Oikawa M, Arakawa K, Nagamine T (2008) Changes of heavy metal, metallothionein and heat shock proteins in Sertoli cells induced by cadmium exposure. Toxicology in vitro : an international journal published in association with BIBRA 22(6):1469–1475

    Article  CAS  Google Scholar 

  52. Cao H, Gao F, **a 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  PubMed  Google Scholar 

  53. Chen X, Zhu YH, Cheng XY, Zhang ZW, SW X (2012) The protection of selenium against cadmium-induced cytotoxicity via the heat shock protein pathway in chicken splenic lymphocytes. Molecules (Basel, Switzerland) 17(12):14565–14572

    Article  CAS  Google Scholar 

  54. Wang B, Du Y (2013) Cadmium and its neurotoxic effects. Oxidative Med Cell Longev 2013:898034

    Google Scholar 

  55. Zhu X, Hu S, Zhu L, Ding J, Zhou Y, Li G (2015) Effects of Lycium barbarum polysaccharides on oxidative stress in hyperlipidemic mice following chronic composite psychological stress intervention. Mol Med Rep 11(5):3445–3450

    Article  CAS  PubMed  Google Scholar 

  56. Xu D, Li W, Huang Y, He J, Tian Y (2014) The effect of selenium and polysaccharide of Atractylodes macrocephala Koidz. (PAMK) on immune response in chicken spleen under heat stress. Biol Trace Elem Res 160(2):232–237

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the members of the Traditional Chinese Veterinary Medicine Laboratory in the College of Veterinary Medicine, Northeast Agricultural University.

Funding

This work was supported by the National Science Foundation of China (Grant No. 31272533).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ge Ming.

Ethics declarations

All procedures in this study have been approved by the Institutional Animal Care and Use Committee of Northeast Agricultural University in China.

Conflict of Interest

The authors declare that they have no conflicts of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Song, Y., Zhang, R., Wang, H. et al. Protective Effect of Agaricus blazei Polysaccharide Against Cadmium-Induced Damage on the Testis of Chicken. Biol Trace Elem Res 184, 491–500 (2018). https://doi.org/10.1007/s12011-017-1196-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-017-1196-7

Keywords

Navigation