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Mechanism Underlying the Protective Effect of Selenium on NO-Induced Oxidative Damage in Bovine Mammary Epithelial Cells

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Abstract

This experiment was conducted to investigate the effects and mechanism of selenium (Se) on antioxidant and immune function of bovine mammary epithelial cells (BMEC) damaged by nitric oxide (NO). The third-generation BMEC was randomly divided into eight treatments with six replicates. The BMEC in the control group was cultured in the medium without Se and diethylenetriamine/NO (DETA/NO) for 30 h. For the DETA/NO group and Se protection group BMEC were exposed to different concentrations of Se (0, 10, 20, 50, 100, 150, and 200 nmol/L) for 24 h, followed by treatment with DETA/NO (1000 μmol/L) for 6 h. Compared with the control group, DETA/NO decreased proliferation rate and activity of thioredoxin reductase (TrxR; P < 0.05). Additionally, DETA/NO decreased the gene expression of both nuclear factor-E2-related factor 2 (Nrf2) and TrxR, as well as the protein expression level of TrxR. However, the activity, and expression levels of inducible nitric oxide synthase (iNOS), as well as the concentration and gene expression level of interleukin-1β (IL-1β) and the concentration of NO significantly increased (P < 0.05). The gene expression levels of indexes related to the mitogen-activated protein kinase (MAPK) signaling pathway showed similar changes. Treatment of BMEC with Se significantly reversed DETA/NO-induced changes in a linear or quadratic dose-dependent manner (P < 0.05), with greatest benefit at 50 nmol/L. These data suggests that Se improves the antioxidant function of BMEC, and protects cells from DETA/NO-induced oxidative damage, primarily by enhancing the activity of TrxR and decreasing the concentration of NO through modulation of Nrf2 and MAPK signaling pathways.

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References

  1. Sordillo LM, Aitken SL (2009) Impact of oxidative stress on the health and immune function of dairy cattle. Vet Immunol Immunopathol 128:104–109

    Article  CAS  PubMed  Google Scholar 

  2. Gong J, Ni L, Wang D, Shi BL, Yan SM (2014) Effect of dietary organic selenium on milk selenium concentration and antioxidant and immune status in midlactation dairy cows. Livest Sci 170:84–90

    Article  Google Scholar 

  3. Guo YM, Yan SM, Gong J, Jin L, Shi BL (2017) The protective effect of selenium on bovine mammary epithelial cell injury caused by depression of thioredoxin reductase. Biol Trace Elem Res 2017:1–8

    Google Scholar 

  4. Guo YM, Zhang BQ, Shi HY, Yan SM, Shi BL, Guo XY (2016) Establishment of oxidative damage model of bovine mammary epithelial cells induced by diethylenetriamine/nitric oxide adduct. J Anim Sci 28:2378–2384 In Chinese

    Google Scholar 

  5. Obata T, Brown GE, Yaffe MB (2000) MAP kinase pathways activated by stress: the p38 MAPK pathway. Crit Care Med 28:N67–N77

    Article  CAS  PubMed  Google Scholar 

  6. Cheng AWM, Stabler TV, Bolognesi M, Kraus VB (2009) Selenomethionine inhibits IL-1β inducible nitric oxide synthase (iNOS) and cyclooxygenase 2 (COX2) expression in primary human chondrocytes. Osteoarthr Cartil 17:118–125

    Article  Google Scholar 

  7. Ferret PJ, Soum E, Negre O, Wollman EE, Fradelizi D (2000) Protective effect of thioredoxin upon NO-mediated cell injury in THP1 monocytic human cells. Biochem J 346:759–765

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Soga M, Matsuzawa A, Ichijo H (2012) Oxidative stress-induced diseases via the ASK1 signaling pathway. Int J Cell B 2012:439587

    Google Scholar 

  9. Sakurai A, Nishimoto M, Himeno S, Imura N, Tsujimoto M, Kunimoto M, Hara S (2005) Transcriptional regulation of thioredoxin reductase 1 expression by cadmium in vascular endothelial cells: role of NF-E2-related factor-2. J Cell Physiol 203:529–537

    Article  CAS  PubMed  Google Scholar 

  10. Choi EO, Jeong JW, Park C, Hong SH, Kim GY, Hwang HG, Cho EJ, Choi TH (2016) Baicalein protects C6 glial cells against hydrogen peroxide-induced oxidative stress and apoptosis through regulation of the Nrf2 signaling pathway. Int J Mol Med 37:798–806

    Article  CAS  PubMed  Google Scholar 

  11. Keefer LK, Nims RW, Davies KM, Wink DA (1996) “NONOates” (1-substituted diazen-1-ium-1,2-diolates) as nitric oxide donors: convenient nitric oxide dosage forms. Methods Enzymol 268:281

    Article  CAS  PubMed  Google Scholar 

  12. Mo C, Wang L, Zhang J, Numazawa S, Tang H, Tang XQ, Han XJ, Li JH, Yang M, Wang Z, Wei DD, Xiao HG (2014) The crosstalk between Nrf2 and AMPK signal pathways is important for the anti-inflammatory effect of berberine in LPS-stimulated macrophages and endotoxin-shocked mice. Antioxid Redox Signal 20:574–588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Kunz A, Dirnagl U, Mergenthaler P (2010) Acute pathophysiological processes after ischaemic and traumatic brain injury. Best Pract Res Clin Anaesthesiol 24:495–509

    Article  CAS  PubMed  Google Scholar 

  14. Pacher P, Beckman JS, Liaudet L (2007) Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87:315–424

    Article  CAS  PubMed  Google Scholar 

  15. Wissel J, Kaňovský P, Růžička E, Bares M, Hortova H, Streitova H, Jech R, Roth J, Brenneis C, Müller J, Schnider P, Auff E, Richardson A, Poewe W (2012) Efficacy and safety of standardised 500 unit dose of dysport (Clostridium botulinum toxin type a haemaglutinin compplex) in a heterogenous cervical dystonia popupation: results of a prospective, multicentre, randomised, double-blind, placebo-controlled, parallel group study. Antioxid Redox Signal 17:992–1012

    Article  CAS  Google Scholar 

  16. Jin X, Jia T, Liu R, Xu S (2018) The antagonistic effect of selenium on cadmium-induced apoptosis via PPAR-γ/PI3K/Akt pathway in chicken pancreas. J Hazard Mater 357:355–362

    Article  CAS  PubMed  Google Scholar 

  17. Yu J, Yao H, Gao X, Zhang Z, Wang JF, Xu SW (2015) The role of nitric oxide and oxidative stress in intestinal damage induced by selenium deficiency in chickens. Biol Trace Elem Res 163(1–2):144–153

    Article  CAS  PubMed  Google Scholar 

  18. Liu T, Yang T, Xu Z, Tan S, Pan T, Wan N, Li S (2018) MicroRNA-193b-3p regulates hepatocyte apoptosis in selenium-deficient broilers by targeting MAML1. J Inorg Biochem 186:235–245

    Article  CAS  PubMed  Google Scholar 

  19. Hua WB, Zhang YK, Wu XH, Kang L, Tu J, Zhao KC, Li S, Wang K, Song Y, Luo RJ, Shao ZW, Yang SH, Yang C (2017) Icariin attenuates interleukin-1β-induced inflammatory response in human nucleus pulposus cells. Curr Pharm Des 23

  20. Kim SH, Johnson VJ, Shin TY, Shin TY, Sharma RP (2004) Selenium attenuates lipopolysaccharide-induced oxidative stress responses through modulation of p38 MAPK and NF-kappaB signaling pathways. Exp Biol Med 229:203–213

    Article  CAS  Google Scholar 

  21. Korbecki J, Baranowskabosiacka I, Gutowska I, Chlubek D (2013) The effect of reactive oxygen species on the synthesis of prostanoids from arachidonic acid. J Physiol Pharmacol 64:409

    CAS  PubMed  Google Scholar 

  22. Karrasch T, Jobin C (2008) NF-kappaB and the intestine: friend or foe? Inflamm Bowel Dis 14:114–124

    Article  PubMed  Google Scholar 

  23. Xu LK, Wang XM, Tan XM, Xing XF, Tang QF, Luo JB (2017) Ephedra-cinnamomi attenuates cerebral ischemia-induced memory deficits via TLR4/MyD88/p38 MAPK pathway. Biomed Res 28:8309–8315

    CAS  Google Scholar 

  24. Wang H, Wang Z, Chen J, Wu J (2007) Apoptosis induced by NO via phosphorylation of p38 MAPK that stimulates NF-κB, p53 and caspase-3 activation in rabbit articular chondrocytes. Cell Biol Int 31:1027–1035

    Article  CAS  PubMed  Google Scholar 

  25. Zhang W, Zhang R, Wang T, Jiang H, Guo M, Zhou E, Yong S, Yang Z, Xu S, Cao Y, Zhang N (2014) Selenium inhibits LPS-induced pro-inflammatory gene expression by modulating MAPK and NF-κB signaling pathways in mouse mammary epithelial cells in primary culture. Inflammation 37(2):478–485

    Article  CAS  PubMed  Google Scholar 

  26. Lee SE, Son GW, Park HR, Jin YH, Park CS, Park YS (2015) Induction of thioredoxin reductase 1 by crotonaldehyde as an adaptive mechanism in human endothelial cells. Mol Cell Toxicol 11:433–439

    Article  CAS  Google Scholar 

  27. Wang YC, Jiang L, Li YF, Luo XG, He J (2016) Effect of different selenium supplementation levels on oxidative stress, cytokines, and immunotoxicity in chicken thymus. Biol Trace Elem Res 172:488–495

    Article  CAS  PubMed  Google Scholar 

  28. Spallholz JE, Hoffman DJ (2002) Selenium toxicity: cause and effects in aquatic birds. Aquat Toxicol 57:27–37

    Article  CAS  PubMed  Google Scholar 

  29. Silva MAOD, Andrade SALD, Mazzafera P, Arruda MAZ (2011) Evaluation of sunflower metabolism from zinc and selenium addition to the culture: a comparative metallomic study. Int J Mass Spectrom 307:55–60

    Article  CAS  Google Scholar 

  30. Schrauzer GN (2000) Selenomethionine: a review of its nutritional significance, metabolism and toxicity. J Nutr 130(7):1653–1656

    Article  CAS  PubMed  Google Scholar 

  31. Hauser-Davis RA, Silva JAN, Rocha RCC, Pierre TS, Ziolli RL, Arruda MAZ (2015) Acute selenium selenite exposure effects on oxidative stress biomarkers and essential metals and trace-elements in the model organism zebrafish (Danio rerio). J Trace Elem Med Biol 33:68

    Article  CAS  PubMed  Google Scholar 

  32. Tuzen M, Pekiner OZ (2015) Ultrasound-assisted ionic liquid dispersive liquid-liquid microextraction combined with graphite furnace atomic absorption spectrometric for selenium speciation in foods and beverages. Food Chem 188:619–624

    Article  CAS  PubMed  Google Scholar 

  33. Hafla A (2015) Micro-Minerals: selenium. Agri-King Web. https://www.agriking.com/micro-minerals-selenium/. Accessed 8 January 2015

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Acknowledgments

Yongmei Guo and Xiaoyu Guo contributed equally to this article. The authors are also grateful to Boqi Zhang for his assistance during the experiments and to Dr. Christine Rosser for her modification to this manuscript.

Funding

The authors acknowledge the support of the National Natural Science Foundation of China (Project No. 31560650).

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Authors and Affiliations

  1. College of Animal Science, Inner Mongolia Agricultural University, Hohhot, 010018, China

    Yongmei Guo, Xiaoyu Guo, Sumei Yan, Boqi Zhang & Binlin Shi

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  1. Yongmei Guo
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  2. Xiaoyu Guo
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  3. Sumei Yan
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Correspondence to Sumei Yan.

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Guo, Y., Guo, X., Yan, S. et al. Mechanism Underlying the Protective Effect of Selenium on NO-Induced Oxidative Damage in Bovine Mammary Epithelial Cells. Biol Trace Elem Res 191, 104–114 (2019). https://doi.org/10.1007/s12011-018-1603-8

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