Advertisement

Biological Trace Element Research

, Volume 187, Issue 1, pp 281–290 | Cite as

Protective Effect of Ganoderma Triterpenoids on Cadmium-Induced Testicular Toxicity in Chickens

  • Hongmei Wang
  • Ruili Zhang
  • Yangyang Song
  • Tianqi Li
  • Ming GeEmail author
Article
  • 109 Downloads

Abstract

Studies have shown that cadmium can cause chicken testicular damage, but a protective effect of Ganoderma triterpenoids on cadmium-induced testicular damage in chickens has not yet been reported. The present study was designed to research the protective effect of Ganoderma triterpenoids on cadmium-induced testicular damage in chicken. Eighty healthy 7-day-old Hyline egg laying chickens were randomly divided into four groups with 20 in each group. The control group was fed with normal full-fodder, the model group was fed with normal full-fodder with 140 mg/kg of CdCl2, the Ganoderma triterpenoid treatment group was fed with a full-fodder diet containing 140 mg/kg of CdCl2 and 0.5 mL of Ganoderma triterpenoid solution (20 mg/mL), and the Ganoderma triterpenoid group was fed normal full-fodder and 0.5 mL of Ganoderma triterpenoid solution (20 mg/mL) gavage. The chickens were euthanized at 20, 40, and 60 days, respectively, and the testes were harvested. The changes of cadmium contents, the antioxidant enzymes (superoxide dismutase (SOD), glutathione peroxidase (GSH-Px)), peroxide (malondialdehyde (MDA)), inflammatory factors (interleukin (IL)-1β, IL-6, and tumor necrosis factor alpha (TNF-α)), and apoptosis-related proteins (Bax, Bcl-2, and Caspase-3) were detected. The pathological sections of the testes were made at the same time. The results suggested that Ganoderma triterpenoids could reduce the accumulation of cadmium in testis tissue; reduce the content of IL-1β, IL-6, and TNF-α in cadmium poisoning testis; significantly increase the activity of SOD and GSH-Px; decrease the content of MDA; regulate the expression of Bax, Caspase-3, and Bcl-2; and reduce the damage of testicular tissue. The results showed that Ganoderma triterpenoids have a protective effect on cadmium-induced testicular injury in chicken.

Keywords

Ganoderma triterpenoids Cadmium Chicken testis Antioxidation Inflammatory factors Apoptosis 

Notes

Acknowledgments

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

Funding Information

This work was supported by the National Key R&D Program of China (Project No. 2017YFD0502200).

Compliance with Ethical Standards

All procedures used in this study were approved by the Institutional Animal Care and Use Committee of Northeast Agricultural University.

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Satofuka H, Amano S, Atomi H, Takagi M, Hirata K, Miyamoto K, Imanaka T (1999) Rapid method for detection and detoxification of heavy metal ions in water environments using phytochelation. J Biosci Bioeng 88(3):287–292PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Angle CR, Thomas DJ, Swanson SA (1993) Osteotoxicity of cadmium and lead in HOS TE 85 and ROS 17/2.8 cells: relation to metallothionein induction and mitochondrial binding. Biometals 6(3):179–184PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Xiao C, Zhu G, Jin T, Zhou Z, Gu S, Jing Q, Xiao H (2012) Cadmium stimulates the osteoclastic differentiation of RAW264.7 cells in presence of osteoblasts. Biol Trace Elem Res 146(3):349–353PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Siu ER, Mruk DD, Porto CS, Cheng CY (2009) Cadmium-induced testicular injury. Toxicol Appl Pharmacol 238(3):240PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Marettová E, Maretta M, Legáth J (2015) Toxic effects of cadmium on testis of birds and mammals: a review. Anim Reprod Sci 155:1–10PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Chen A, Kim SS, Ethan C, Dietrich KN (2013) Thyroid hormones in relation to lead, mercury, and cadmium exposure in the National Health and Nutrition Examination Survey, 2007–2008. Environ Health Perspect 121(2):181–186PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Wu SM, Tsai PJ, Chou MY, Wang WD (2013) Effects of maternal cadmium exposure on female reproductive functions, gamete quality, and offspring development in zebrafish (Danio rerio). Arch Environ Contam Toxicol 65(3):521–536PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Kim JY, Mi SJ, Mi KP, Lee MK, Seo SJ (2014) Time-dependent progression from the acute to chronic phases in atopic dermatitis induced by epicutaneous allergen stimulation in NC/Nga mice. Exp Dermatol 23(1):53–57PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Jin X, Xu Z, Zhao X, Chen M, Xu S (2017) The antagonistic effect of selenium on lead-induced apoptosis via mitochondrial dynamics pathway in the chicken kidney. Chemosphere 180:259–266PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Angenard G, Muczynski V, Coffigny H, Pairault C, Duquenne C, Frydman R, Habert R, Rouillerfabre V, Livera G (2010) Cadmium increases human fetal germ cell apoptosis. Environ Health Perspect 118(3):331–337PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Modi HR, Patil N, Katyare SS (2008) Effect of treatment with cadmium on kinetic properties of Na+, K+-ATPase and glucose-6-phosphatase activity in rat liver microsomes: a correlative study on influence of lipid/phospholipid make-up. Toxicology 254(1–2):29–41PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Olgun O (2015) The effect of dietary cadmium supplementation on performance, egg quality, tibia biomechanical properties and eggshell and bone mineralisation in laying quails. Animal 9(8):1298–1303PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Zhao P, Guo Y, Zhang W, Chai H, Xing H, Xing M (2016) Neurotoxicity induced by arsenic in Gallus Gallus: regulation of oxidative stress and heat shock protein response. Chemosphere 166:238PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Chen M, Li X, Fan R, Yang J, Jin X, Hamid S, Xu S (2017) Cadmium induces BNIP3-dependent autophagy in chicken spleen by modulating miR-33-AMPK axis. Chemosphere 194:396PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Sun X, Li J, Zhao H, Wang Y, Liu J, Shao Y, Xue Y, Xing M (2018) Synergistic effect of copper and arsenic upon oxidative stress, inflammation and autophagy alterations in brain tissues of Gallus gallus. J Inorg Biochem 178:54–62PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Li S, Zhao H, Wang Y, Shao Y, Li J, Liu J, Xing M (2017) The inflammatory responses in Cu-mediated elemental imbalance is associated with mitochondrial fission and intrinsic apoptosis in Gallus gallus heart. Chemosphere 189:489–497PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Kukongviriyapan U, Pannangpetch P, Kukongviriyapan V, Donpunha W, Sompamit K, Surawattanawan P (2014) Curcumin protects against cadmium-induced vascular dysfunction, hypertension and tissue cadmium accumulation in mice. Nutrients 6(3):1194–1208PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Takiguchi M, Yoshihara S (2006) New aspects of cadmium as endocrine disruptor. Environ Sci Int J Environ Physiol Toxicol 13(2):107Google Scholar
  19. 19.
    Sadik NA (2008) Effects of diallyl sulfide and zinc on testicular steroidogenesis in cadmium-treated male rats. J Biochem Mol Toxicol 22(5):345–353PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Wong CH, Mruk DD, Lui WY, Cheng CY (2004) Regulation of blood-testis barrier dynamics: an in vivo study. J Cell Sci 117(Pt 5):783PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Blanco A, Moyano R, Vivo J, Flores-Acuña R, Molina A, Blanco C, Agüera E, Monterde JG (2007) Quantitative changes in the testicular structure in mice exposed to low doses of cadmium. Environ Toxicol Pharmacol 23(1):96–101PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Sant’Ana MG, Moraes R, Bernardi MM (2005) Toxicity of cadmium in Japanese quail: evaluation of body weight, hepatic and renal function, and cellular immune response. Environ Res 99(2):273–277PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    De Coninck DI, Asselman J, Glaholt S, Janssen CR, Colbourne JK, Shaw JR, De Schamphelaere KA (2014) Genome-wide transcription profiles reveal genotype-dependent responses of biological pathways and gene-families in Daphnia exposed to single and mixed stressors. Environ Sci Technol 48(6):3513PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Faurskov B, Bjerregaard HF (1997) Effect of cadmium on active ion transport and cytotoxicity in cultured renal epithelial cells (A6). Toxicol In Vitro Int J Publ Assoc Bibra 11(5):717CrossRefGoogle Scholar
  25. 25.
    Wachtel-Galor S, Tomlinson B, Benzie IF (2004) Ganoderma lucidum (“Lingzhi”), a Chinese medicinal mushroom: biomarker responses in a controlled human supplementation study. Br J Nutr 91(2):263–269PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Bao XF, Wang XS, Dong Q, Fang JN, Li XY (2002) Structural features of immunologically active polysaccharides from Ganoderma lucidum. Phytochemistry 59(2):175PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Lull C, Wichers HJ, Savelkoul HF (2005) Antiinflammatory and immunomodulating properties of fungal metabolites. Mediat Inflamm 2005(2):63CrossRefGoogle Scholar
  28. 28.
    Liu Z, Xing J, Zheng S, Bo R, Luo L, Huang Y, Niu Y, Li Z, Wang D, Hu Y (2016) Ganoderma lucidum polysaccharides encapsulated in liposome as an adjuvant to promote Th1-bias immune response. Carbohydr Polym 142:141PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Kubota T, Asaka Y, Miura I, Mori H (1982) Structures of ganoderic acid a and B, two new lanostane type bitter triterpenes from Ganoderma lucidum (FR.) KARST. Helv Chim Acta 65(65):611–619CrossRefGoogle Scholar
  30. 30.
    Luo J, Zhao YY, Li ZB (2002) A new lanostane-type triterpene from the fruiting bodies of Ganoderma lucidum. J Asian Nat Prod Res 4(2):129PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Hu LL, Ma QY, Huang SZ, Guo ZK, Ma HX, Guo JC, Dai HF, Zhao YX (2016) Three new lanostanoid triterpenes from the fruiting bodies of Ganoderma tropicum. J Asian Nat Prod Res 52(4):656–659Google Scholar
  32. 32.
    Sun J, He H, Xie BJ (2004) Novel antioxidant peptides from fermented mushroom Ganoderma lucidum. J Agric Food Chem 52(21):6646–6652PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Chu QP, Wang LE, Cui XY, Fu HZ, Lin ZB, Lin SQ, Zhang YH (2007) Extract of Ganoderma lucidum potentiates pentobarbital-induced sleep via a GABAergic mechanism. Pharmacol Biochem Behav 86(4):693–698PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Wang MF, Chan YC, Wu CL, Wong YC, Hosoda K, Yamamoto S (2004) Effects of Ganoderma on aging and learning and memory ability in senescence accelerated mice. Int Congr 1260(03):399–404CrossRefGoogle Scholar
  35. 35.
    Tung NT, Cuong TD, Hung TM, Lee JH, Woo MH, Choi JS, Kim J, Ryu SH, Min BS (2013) Inhibitory effect on NO production of triterpenes from the fruiting bodies of Ganoderma lucidum. Bioorg Med Chem Lett 23(5):1428–1432PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Hu X, Zhang R, Xie Y, Wang H, Ge M (2016) The protective effects of polysaccharides from Agaricus blazei Murill against cadmium-induced oxidant stress and inflammatory damage in chicken livers. Biol Trace Elem Res 1–10Google Scholar
  37. 37.
    Pant N, Upadhyay G, Pandey S, Mathur N, Saxena DK, Srivastava SP (2003) Lead and cadmium concentration in the seminal plasma of men in the general population: correlation with sperm quality. Reprod Toxicol 17(4):447–450PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Razinger J, Dermastia M, Koce JD, Zrimec A (2008) Oxidative stress in duckweed (Lemna minor L.) caused by short-term cadmium exposure. Environ Pollut 153(3):687PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Fujiwara Y, Lee JY, Tokumoto M, Satoh M (2012) Cadmium renal toxicity via apoptotic pathways. Biol Pharm Bull 35(11):1892–1897PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Heleno SA, Barros L, Martins A, Mjrp Q, Santosbuelga C, Icfr F (2012) Fruiting body, spores and in vitro produced mycelium of Ganoderma lucidum from Northeast Portugal: a comparative study of the antioxidant potential of phenolic and polysaccharidic extracts. Food Res Int 46(1):135–140CrossRefGoogle Scholar
  41. 41.
    Jiao Y, Xie T, Zou LH, Wei Q, Qiu L, Chen LX (2016) Lanostane triterpenoids from Ganoderma curtisii and their NO production inhibitory activities of LPS-induced microglia. Bioorg Med Chem Lett 26(15):3556–3561PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Tremellen K (2012) Oxidative stress and male infertility: a clinical perspective. Humana PressGoogle Scholar
  43. 43.
    Pathak N, Khandelwal S (2006) Oxidative stress and apoptotic changes in murine splenocytes exposed to cadmium. Toxicology 220(1):26–36PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Kumar DV, Anuj B, Manu C (2012) Protective role of ceftriaxone plus sulbactam with VRP1034 on oxidative stress, hematological and enzymatic parameters in cadmium toxicity induced rat model. Interdiscip Toxicol 5(4):192CrossRefGoogle Scholar
  45. 45.
    Mau JL, Tsai SY, Tseng YH, Huang SJ (2005) Antioxidant properties of methanolic extracts from Ganoderma tsugae. Food Chem 39(7):707–716Google Scholar
  46. 46.
    Lin KW, Maitraie D, Huang AM, Wang JP, Lin CN (2016) Triterpenoids and an alkamide from Ganoderma tsugae. Fitoterapia 108:73–80PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Liu L, Tao R, Huang J, He X, Qu L, Jin Y, Zhang S, Fu Z (2015) Hepatic oxidative stress and inflammatory responses with cadmium exposure in male mice. Environ Toxicol Pharmacol 39(1):229–236PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Taofiq O, Martins A, Barreiro MF, Ferreira ICFR (2016) Anti-inflammatory potential of mushroom extracts and isolated metabolites. Trends Food Sci Technol 50:193–210CrossRefGoogle Scholar
  49. 49.
    Yan JJ, Jung JS, Hong YJ, Moon YS, Suh HW, Kim YH, Yun-Choi HS, Song DK (2004) Protective effect of protocatechuic acid isopropyl ester against murine models of sepsis: inhibition of TNF-alpha and nitric oxide production and augmentation of IL-10. Biol Pharm Bull 27(12):2024–2027PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Krecic SM, Shepard D, Mullet D, Apseloff G, Weisbrode S, Gerber N (1999) Gallium nitrate suppresses the production of nitric oxide and liver damage in a murine model of LPS-induced septic shock. Life Sci 65(13):1359–1371CrossRefGoogle Scholar
  51. 51.
    Verstrepen L, Bekaert T, Chau TL, Tavernier J, Chariot A, Beyaert R (2008) TLR-4, IL-1R and TNF-R signaling to NF-kappaB: variations on a common theme. Cell Mol Life Sci Cmls 65(19):2964–2978PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Shen X-s, Hai-bo J-c, Ming-hui F-d, Meng Z, Yue-lang (2013) Emodin induces human T cell apoptosis in vitro by ROS-mediated endoplasmic reticulum stress and mitochondrial dysfunction. Chin J Pharmacol 34(9):1217–1228Google Scholar
  53. 53.
    Wang L, Cao J, Chen D, Liu X, Lu H, Liu Z (2009) Role of oxidative stress, apoptosis, and intracellular homeostasis in primary cultures of rat proximal tubular cells exposed to cadmium. Biol Trace Elem Res 127(1):53PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Tsujimoto Y, Shimizu S (2000) Bcl-2 family: life-or-death switch. FEBS Lett 466(1):6–10PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Siddiqui WA, Ahad A, Ahsan H (2015) The mystery of BCL2 family: Bcl-2 proteins and apoptosis: an update. Arch Toxicol 89(3):289–317PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Larsen BD, Rampalli S, Burns LE, Brunette S, Dilworth FJ, Megeney LA (2010) Caspase 3/caspase-activated DNase promote cell differentiation by inducing DNA strand breaks. Proc Natl Acad Sci U S A 107(9):4230–4235PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    (2015) Non-apoptotic role of caspase-3 in synapse refinement. Sci Found China (1):33Google Scholar
  58. 58.
    Yuan G, Dai S, Yin Z, Lu H, Jia R, Xu J, Song X, Li L, Shu Y, Zhao X (2014) Sub-chronic lead and cadmium co-induce apoptosis protein expression in liver and kidney of rats. Int J Clin Exp Pathol 7(6):2905–2914PubMedPubMedCentralGoogle Scholar
  59. 59.
    Chen C, Li P, Li Y, Yao G, Xu JH (2016) Antitumor effects and mechanisms of Ganoderma extracts and spores oil. Oncol Lett 12(5):3571PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Wu X, Zeng J, Hu J, Liao Q, Zhou R, Zhang P, Chen Z (2013) Hepatoprotective effects of aqueous extract from Lingzhi or Reishi medicinal mushroom Ganoderma lucidum (higher basidiomycetes) on α-amanitin-induced liver injury in mice. Int J Med Mushrooms 15(4):383PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Adamkovicova M, Toman R, Cabaj M, Massanyi P, Martiniakova M, Omelka R, Krajcovicova V, Duranova H (2014) Effects of subchronic exposure to cadmium and diazinon on testis and epididymis in rats. ScientificWorldJournal 2014(3):632581PubMedPubMedCentralGoogle Scholar
  62. 62.
    Sakr SA, Nooh HZ (2013) Effect of Ocimum basilicum extract on cadmium-induced testicular histomorphometric and immunohistochemical alterations in albino rats. Anat Cell Biol 46(2):122–130PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Pu DB, Zheng X, Gao JB, Zhang XJ, Qi Y, Li XS, Wang YM, Li XN, Li XL, Wan CP (2017) Highly oxygenated lanostane-type triterpenoids and their bioactivity from the fruiting body of Ganoderma gibbosum. Fitoterapia 119:1PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Barbieri A, Quagliariello V, Del VV, Falco M, Luciano A, Amruthraj NJ, Nasti G, Ottaiano A, Berretta M, Iaffaioli RV (2017) Anticancer and anti-inflammatory properties of Ganoderma lucidum extract effects on melanoma and triple-negative breast cancer treatment. Nutrients 9(3):210CrossRefGoogle Scholar
  65. 65.
    Dabrio M, Rodríguez AR, Bordin G, Bebianno MJ, De LM, Sestáková I, Vasák M, Nordberg M (2002) Recent developments in quantification methods for metallothionein. J Inorg Biochem 88(2):123PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Toriumi S, Saito T, Hosokawa T, Takahashi Y, Numata T, Kurasaki M (2005) Metal binding ability of metallothionein-3 expressed in Escherichia coli. Basic Clin Pharmacol Toxicol 96(4):295–301PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Radtke F, Heuchel R, Georgiev O, Hergersberg M, Gariglio M, Dembic Z, Schaffner W (1993) Cloned transcription factor MTF-1 activates the mouse metallothionein I promoter. EMBO J 12(4):1355–1362PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Hongmei Wang
    • 1
    • 2
  • Ruili Zhang
    • 1
    • 2
  • Yangyang Song
    • 1
    • 2
  • Tianqi Li
    • 1
    • 2
  • Ming Ge
    • 1
    • 2
    Email author
  1. 1.College of Veterinary MedicineNortheast Agricultural UniversityHarbinChina
  2. 2.Key Laboratory of the Provincial Education Department of Heilongjiang for Common Animal Disease Prevention and TreatmentNortheast Agricultural UniversityHarbinChina

Personalised recommendations