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Epigallocatechin-3-gallate Alleviates Vanadium-Induced Reduction of Antioxidant Capacity via Keap1-Nrf2-sMaf Pathway in the Liver, Kidney, and Ovary of Laying Hens

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Abstract

This study evaluated the effect of epigallocatechin-3-gallate (EGCG) alleviating the reduction of antioxidant capacity induced by dietary vanadium (V) in the liver, kidney, and ovary of laying hens. Furthermore, Kelch-like ECH-associated protein 1(Keap1)-nuclear factor erythroid 2-related factor 2 (Nrf2)-small Maf proteins (sMaf) pathway was explored to reveal the molecular mechanism. A total of 768 40-week-old Hyline-Brown laying hens were randomly allocated to 4 groups with 8 pens per group and 24 hens per pen. The experimental groups were as follows: control (basal diet); V15, control + 15 mg/kg V; EGCG150, control + 150 mg/kg EGCG; V15 + EGCG150, V15 + 150 mg/kg EGCG. Our results revealed that dietary EGCG supplementation completely alleviated the V-induced reductions of hen-day egg production, average egg weight, Haugh unit, albumen height, eggshell strength, and eggshell thickness. Dietary EGCG supplementation completely prevented the V-induced reductions of serum follicle-stimulating hormone and luteinizing hormone levels. Besides, dietary EGCG supplementation reversed the V-induced increments of alanine aminotransferase (ALT), aspartate aminotransferase (AST), blood urea nitrogen (BUN), creatinine (Cr), and uric acid (UA). In addition, dietary EGCG supplementation partially alleviated the V-induced reductions of the enzyme activities and gene expressions of superoxidative dismutase (SOD), catalase (CAT), glutathione reductase (GR), and glutathione peroxidase (GSH-Px). Furthermore, dietary EGCG supplementation partially alleviated the V-induced reductions of Nrf2 and sMaf gene expressions, and the increments of Keap1 gene expression. In summary, EGCG partially alleviated V-induced reduction of antioxidant capacity through Keap1-Nrf2-sMaf pathway in the liver, kidney, and ovary of laying hens.

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References

  1. Domingo JL (2000) Vanadium and diabetes. What about vanadium toxicity? Mol Cell Biochem 203(1-2):185–187. https://doi.org/10.1023/a:1007067011338

    Article  CAS  PubMed  Google Scholar 

  2. Mukherjee B, Patra B, Mahapatra S, Banerjee P, Tiwari A, Chatterjee M (2004) Vanadium-an element of atypical biological significance. Toxicol Lett 150(2):135–143. https://doi.org/10.1016/j.toxlet.2004.01.009

    Article  CAS  PubMed  Google Scholar 

  3. Ma Y, Zhu MK, Miao LP, Zhang XY, Dong XY, Zou XT (2018) Mercuric chloride induced ovarian oxidative stress by suppressing Nrf2-Keap1 signal pathway and its downstream genes in laying hens. Biol Trace Elem Res 185(1):186–196. https://doi.org/10.1007/s12011-018-1244-y

    Article  CAS  Google Scholar 

  4. Scibior A, Zaporowska H, Ostrowski J, Banach A (2006) Combined effect of vanadium (V) and chromium (III) on lipid peroxidation in liver and kidney of rats. Chem Biol Interact 159(3):213–222. https://doi.org/10.1016/j.cbi.2005.11.008

    Article  CAS  PubMed  Google Scholar 

  5. Kurt O, Ozden TY, Ozsoy N, Tunail S, Can R, Akev N, Yanardag R (2011) Influence of vanadium supplementation on oxidative stress factors in the muscle of STZ-diabetic rats. BioMetals 24(5):943–949. https://doi.org/10.1007/s10534-011-9452-3

    Article  CAS  PubMed  Google Scholar 

  6. Storey KB (1996) Oxidative stress: animal adaptations in nature. Braz J Med Biol Res 29(12):1715–1733. https://doi.org/10.1006/bmme.1996.0088

    Article  CAS  PubMed  Google Scholar 

  7. Wu G, Fang Y, Yang S, Lupton JR, Turner ND (2004) Glutathione metabolism and its implications for health. J Nutr 134(3):489–492. https://doi.org/10.1093/jn/134.3.489

    Article  CAS  PubMed  Google Scholar 

  8. Wang J, Yuan Z, Zhang K, Ding X, Bai S, Zeng Q, Peng H, Celi P (2018) Epigallocatechin-3-gallate protected vanadium-induced eggshell depigmentation via P38MAPK-Nrf2/HO-1 signaling pathway in laying hens. Poult Sci 97(9):3109–3118. https://doi.org/10.3382/ps/pey165

    Article  CAS  PubMed  Google Scholar 

  9. Tiedge M, Lortz S, Drinkgern J, Lenzen S (1997) Relation between antioxidant enzyme gene expression and antioxidative defense status of insulin-producing cells. Diabetes 46(11):1733–1742. https://doi.org/10.2337/diabetes.46.11.1733

    Article  CAS  PubMed  Google Scholar 

  10. Kwak MK, Itoh K, Yamamoto M, Sutter T, Kensler TW (2001) Role of transcription factor Nrf2 in the induction of hepatic phase 2 and antioxidative enzymes in vivo by the cancer chemoprotective agent, 3H-1, 2-dithiole-3-thione. Mol Med 7(2):135–145. https://doi.org/10.1177/1532673X12437555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Zhang DD (2006) Mechanistic studies of the Nrf2-Keap1 signaling pathway. Drug Metab Rev 38(4):769–789. https://doi.org/10.1080/03602530600971974

    Article  CAS  PubMed  Google Scholar 

  12. Sriram N, Kalayarasan S, Sudhandiran G (2009) Epigallocatechin-3-gallate augments antioxidant activities and inhibits inflammation during bleomycin-induced experimental pulmonary fibrosis through Nrf2-Keap1 signaling. Pulm Pharmacol Ther 22(3):22–236. https://doi.org/10.1016/j.pupt.2008.12.010

    Article  CAS  Google Scholar 

  13. Caetano M, Padrino L, Gutiérrez H, Fernández AJ, Castillo J (1998) Trace level vanadium determination using thermal lens spectrophotometry. Mikrochim Acta 128:169–175. https://doi.org/10.1007/BF01243045

    Article  CAS  Google Scholar 

  14. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262

    Article  CAS  PubMed  Google Scholar 

  15. Domingo JL, Gomez M, Llobet JM, Corbella J, Keen CL (1991) Oral vanadium administration to streptozotocin-diabetic rats has marked negative side-effects which are independent of the form of vanadium used. Toxicology 66(3):279–287. https://doi.org/10.1016/0300-483X(91)90199-B

    Article  CAS  PubMed  Google Scholar 

  16. Crans DC, Smee JJ, Gaidamauskas E, Yang LQ (2004) The chemistry and biochemistry of vanadium and the biological activities exerted by vanadium compounds. Chem Rev 104(2):849–902. https://doi.org/10.1002/chin.200420288

    Article  CAS  PubMed  Google Scholar 

  17. Davis EG, Miles RD, Butcher GD, Comer CW (2002) Effects of dietary vanadium on performance and immune response of commercial egg-type laying hens. J Appl Anim Res 22(1):113–124. https://doi.org/10.1080/09712119.2002.9706386

    Article  CAS  Google Scholar 

  18. Yuan ZH, Zhang KY, Ding XM, Luo YH, Bai SP, Zeng QF, Wang JP (2016) Effect of tea polyphenols on production performance, egg quality, and hepatic antioxidant status of laying hens in vanadium-containing diets. Poult Sci 95(7):1709–1717. https://doi.org/10.3382/ps/pew097

    Article  CAS  PubMed  Google Scholar 

  19. Stevenson MJ, Uyeda KS, Harder NHO, Heffern MC (2019) Metal-dependent hormone function: the emerging interdisciplinary field of metalloendocrinology. Metallomics 11(1):85–110. https://doi.org/10.1039/C8MT00221E

    Article  CAS  PubMed  Google Scholar 

  20. Graham JD, Clarke CL (1997) Physiological action of progesterone in target tissues. Endocr Rev 18(4):502–519. https://doi.org/10.1210/edrv.18.4.0308

    Article  CAS  PubMed  Google Scholar 

  21. Petersen SL, Ottem EN, Carpenter CD (2003) Direct and indirect regulation of gonadotropin-releasing hormone neurons by estradiol. Biol Reprod 69(6):1771–1778. https://doi.org/10.1095/biolreprod.103.019745

    Article  CAS  PubMed  Google Scholar 

  22. Scibior A, Zaporowska H (2007) Effects of vanadium(V) and/or chromium(III) on L-ascorbic acid and glutathione as well as iron, zinc, and copper levels in rat liver and kidney. J Toxicol Environ Health Part A 70(8):696–704. https://doi.org/10.1080/15287390601187906

    Article  CAS  Google Scholar 

  23. Tipoe GL, Leung TM, Liong EC, Lau TYH, Fung ML, Nanji AA (2010) Epigallocatechin-3-gallate (EGCG) reduces liver inflammation, oxidative stress and fibrosis in carbon tetrachloride (CCl4)-induced liver injury in mice. Toxicology 273(1-3):45–52. https://doi.org/10.1016/j.tox.2010.04.014

    Article  CAS  PubMed  Google Scholar 

  24. Mielgo-Ayuso J, Barrenechea L, Alcorta P, Larrart E, Margareto J, Labayen I (2014) Effects of dietary supplementation with epigallocatechin-3-gallate on weight loss, energy homeostasis, cardiometabolic risk factors and liver function in obese women: randomised, double-blind, placebo-controlled clinical trial. Br J Nutr 111(7):1263–1271. https://doi.org/10.1017/S0007114513003784

    Article  CAS  PubMed  Google Scholar 

  25. Kakuta Y, Okumi M, Isaka Y, Tsutahara K, Abe T, Yazawa K, Ichimaru N, Matsumura K, Hyon SH, Takahara S, Nonomura N (2011) Epigallocatechin-3-gallate protects kidneys from ischemia reperfusion injury by HO-1 upregulation and inhibition of macrophage infiltration. Transpl Int 24(5):514–522. https://doi.org/10.1111/j.1432-2277.2011.01224.x

    Article  CAS  PubMed  Google Scholar 

  26. Imura H, Shimada A, Naota M, Morita T, Togawa M, Hasegawa T, Seko Y (2013) Vanadium toxicity in mice. Toxicol Pathol 41(6):842–856. https://doi.org/10.1177/0192623312467101

    Article  CAS  PubMed  Google Scholar 

  27. Na HK, Surh TJ (2008) Modulation of Nrf2-mediated antioxidant and detoxifying enzyme induction by the green tea polyphenol EGCG. Food Chem Toxicol 46(4):1271–1278. https://doi.org/10.1016/j.fct.2007.10.006

    Article  CAS  PubMed  Google Scholar 

  28. Cui X, Gong J, Han H, He L, Teng Y, Tetley T, Sinharay R, Chung KF, Islam T, Gillilang F, Grady S, Garshick E, Li Z, Zhang JJ (2018) Relationship between free and total malondialdehyde, a well-established marker of oxidative stress, in various types of human biospecimens. J Thorac Dis 10(5):3088–3097. https://doi.org/10.21037/jtd.2018.05.92

    Article  PubMed  PubMed Central  Google Scholar 

  29. Finkel T, Holbrook NJ (2018) Oxidants, oxidative stress and the biology of aging. Nature 408(6809):239–247. https://doi.org/10.1038/35041687

    Article  CAS  Google Scholar 

  30. Tuzcu M, Sahin N, Karatepe M, Cikim G, Kilinc U, Sahin K (2008) Epigallocatechin-3-gallate supplementation can improve antioxidant status in stressed quail. Br Poult Sci 49(5):643–648. https://doi.org/10.1080/00071660802298336

    Article  CAS  PubMed  Google Scholar 

  31. Kanna PS, Mahendrakumar CB, Chatterjee M, Hemalatha P, Datta S, Chakraborty P (2003) Vanadium inhibits placental glutathione S-transferase (GST-P) positive foci in 1, 2-dimethyl hydrazine induced rat colon carcinogenesis. J Biochem Mol Toxicol 17(6):357–365. https://doi.org/10.1002/jbt.10099

    Article  CAS  PubMed  Google Scholar 

  32. Sahin K, Orhan C, Tuzcu M, Ali S, Sahin N, Hayirli A (2010) Epigallocatechin-3-gallate prevents lipid peroxidation and enhances antioxidant defense system via modulating hepatic nuclear transcription factors in heat-stressed quails. Poult Sci 89(10):2251–2258. https://doi.org/10.3382/ps.2010-00749

    Article  CAS  PubMed  Google Scholar 

  33. Motohashi H, Yamamoto M (2004) Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol Med 10(11):549–557. https://doi.org/10.1016/j.molmed.2004.09.003

    Article  CAS  PubMed  Google Scholar 

  34. Tkachev VO, Menshchikova EB, Zenkov NK (2011) Mechanism of the Nrf2/Keap1/ARE signaling system. Biochemistry 76(4):407–422. https://doi.org/10.1134/S0006297911040031

    Article  CAS  PubMed  Google Scholar 

  35. Wang JP, He KR, Ding XM, Luo YH, Bai SP, Zeng QF, Su ZW, Xuan Y, Zhang KY (2016) Effect of dietary vanadium and vitamin C on egg quality and antioxidant status in laying hens. J Anim Physiol Anim Nutr 100(3):440–447. https://doi.org/10.1111/jpn.12377

    Article  CAS  Google Scholar 

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Funding

This study was supported by the Earmarked Fund for PhD Research Start-up Fund of Henan University of Science and Technology (No. 13480086).

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  1. College of Animal Science and Technology, Henan University of Science and Technology, Luoyang, 471003, China

    Yan Ma, Yizhen Shi, Qiujue Wu & Wenfeng Ma

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  1. Yan Ma
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Correspondence to Yan Ma.

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All process in the present study was approved by the Animal Ethics and Welfare Committee of Henan University of Science and Technology (Luoyang, China). The experiment was carried out according to the Guiding Principles in the Use of Animals in Toxicology, adopted by the Chinese Society of Toxicology.

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Ma, Y., Shi, Y., Wu, Q. et al. Epigallocatechin-3-gallate Alleviates Vanadium-Induced Reduction of Antioxidant Capacity via Keap1-Nrf2-sMaf Pathway in the Liver, Kidney, and Ovary of Laying Hens. Biol Trace Elem Res 199, 2707–2716 (2021). https://doi.org/10.1007/s12011-020-02398-z

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