Selenium-Rich Yeast Protects Against Aluminum-Induced Renal Inflammation and Ionic Disturbances

Article

Abstract

The aim of this study was to evaluate the protective effects of SeY (selenium-rich yeast) against Al (aluminum)-induced inflammation and ionic imbalances. Male Kunming mice were treated with Al (10 mg/kg) and/or SeY (0.1 mg/kg) by oral gavage for 28 days. The degree of inflammation was assessed by mRNA expression of inflammatory biomarkers. Ionic disorders were assessed by determining the Na+, K+, and Ca2+ content, as well as the alteration in ATP-modifying enzymes (ATPases), including Na+K+-ATPase, Ca2+-ATPase, Mg2+-ATPase, Ca2+Mg2+-ATPase, and the mRNA levels of ATPase’s subunits in kidney. It was observed here that SeY exhibited a significant protective effect on the kidney against the Al-induced upregulation of pro-inflammatory and downregulation of anti-inflammatory cytokines. Furthermore, a significant effect of Al on the Na+, K+, Ca2+, and Mg2+ levels in kidney was observed, and Al was observed to decrease the activities of Na+K+-ATPase, Mg2+-ATPase, and Ca2+Mg2+-ATPase. The mRNA expression of the Na+K+-ATPase subunits and Ca2+-ATPase subunits was regulated significantly by Al. Notably, SeY modulated the Al-induced alterations of ion concentrations, ATPase activity, and mRNA expression of their subunits. These results suggest that SeY prevents renal toxicity caused by Al via regulation of inflammatory responses, ATPase activities, and transcription of their subunits.

Keywords

Aluminum Selenium-rich yeast Inflammation Ionic homeostasis Mouse kidney 

Notes

Compliance with Ethical Standards

All animal studies reported here were approved by the Institutional Animal Care and Use Committee of the Foshan University.

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

12011_2018_1324_MOESM1_ESM.doc (30 kb)
ESM 1 (DOC 30 kb)

References

  1. 1.
    Muselin F, Dumitrescu E, Cristina R, Doma A, Trif A (2015) Protective effect of melatonin on aluminum accumulation in some organs of rats. Istanbul Univ Vet Fak Dergisi 41:26–30Google Scholar
  2. 2.
    Nampoothiri M, John J, Kumar N et al (2015) Modulatory role of simvastatin against aluminium chloride-induced behavioural and biochemical changes in rats. Behav Neurol 2015:1–9CrossRefGoogle Scholar
  3. 3.
    Krewski D, Yokel RA, Nieboer E, Borchelt D, Cohen J, Harry J, Kacew S, Lindsay J, Mahfouz AM, Rondeau V (2007) Human health risk assessment for aluminium, aluminium oxide, and aluminium hydroxide. J Toxicol Environ Health B Crit Rev 10:1–269CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Maya S, Prakash T, Madhu KD, Goli D (2016) Multifaceted effects of aluminium in neurodegenerative diseases: a review. Biomed Pharmacother 83:746–754CrossRefPubMedGoogle Scholar
  5. 5.
    Umesalma SAS (2015) Protective effect of Centella asiatica against aluminium-induced neurotoxicity in cerebral cortex, striatum, hypothalamus and hippocampus of rat brain—histopathological, and biochemical approach. Journal of Molecular Biomarkers J & Diagnosis 6:1Google Scholar
  6. 6.
    Ligi D, Santi M, Croce L, Mannello F (2015) Aluminum induces inflammatory and proteolytic alterations in human monocytic cell line. J Inorg Biochem 152:190–198CrossRefPubMedGoogle Scholar
  7. 7.
    Lin J, Li HX, Qin L, du ZH, Xia J, Li JL (2016) A novel mechanism underlies atrazine toxicity in quails (Coturnix Coturnix coturnix): triggering ionic disorder via disruption of ATPases. Oncotarget 7:83880–83892PubMedPubMedCentralGoogle Scholar
  8. 8.
    Lin J, Zhao HS, Xiang LR, Xia J, Wang LL, Li XN, Li JL, Zhang Y (2016) Lycopene protects against atrazine-induced hepatic ionic homeostasis disturbance by modulating ion-transporting ATPases. J Nutr Biochem 27:249–256CrossRefPubMedGoogle Scholar
  9. 9.
    Bohuts’Ka KI, Iui PK, Nozdrenko DM (2014) The use of aluminum and its compounds for the biomedical purposes. Fiziol Zh 60:91–97CrossRefPubMedGoogle Scholar
  10. 10.
    Nozdrenko DM, Abramchuk OM, Soroca VM, Miroshnichenko NS (2015) Aluminum chloride effect on Ca2+, Mg(2+)-ATPase activity and dynamic parameters of skeletal muscle contraction. Ukr Biochem J 87:38–45CrossRefPubMedGoogle Scholar
  11. 11.
    Nilsen TO, Ebbesson LOE, Kverneland OG et al (2010) Effects of acidic water and aluminum exposure on gill Na+, K+-ATPase alpha -subunit isoforms, enzyme activity, physiology and return rates in Atlantic salmon (Salmo salar L.) Aquat Toxicol 97:250–259CrossRefPubMedGoogle Scholar
  12. 12.
    Liu J, Wang Q, Sun X, Yang X, Zhuang C, Xu F, Cao Z, Li Y (2016) The toxicity of aluminum chloride on kidney of rats. Biol Trace Elem Res 173:339–344CrossRefPubMedGoogle Scholar
  13. 13.
    Li X, Xing M, Chen M, Zhao J, Fan R, Zhao X, Cao C, Yang J, Zhang Z, Xu S (2017) Effects of selenium-lead interaction on the gene expression of inflammatory factors and selenoproteins in chicken neutrophils. Ecotoxicol Environ Saf 139:447–453CrossRefPubMedGoogle Scholar
  14. 14.
    Xing M, Jin X, Wang J, Shi Q, Cai J, Xu S (2017) The antagonistic effect of selenium on lead-induced immune dysfunction via recovery of cytokine and heat shock protein expression in chicken neutrophils. Biol Trace Elem Res 1:1–8Google Scholar
  15. 15.
    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 180:259–266CrossRefPubMedGoogle Scholar
  16. 16.
    Liu LL, Li CM, Zhang ZW, Zhang JL, Yao HD, Xu SW (2014) Protective effects of selenium on cadmium-induced brain damage in chickens. Biol Trace Elem Res 158:176–185CrossRefPubMedGoogle Scholar
  17. 17.
    Yao HD, Wu Q, Zhang ZW, Li S, Wang XL, Lei XG, Xu SW (2013) Selenoprotein W serves as an antioxidant in chicken myoblasts. Biochim Biophys Acta Gen Subj 1830:3112–3120CrossRefGoogle Scholar
  18. 18.
    Yao L, Du Q, Yao H et al (2015) Roles of oxidative stress and endoplasmic reticulum stress in selenium deficiency-induced apoptosis in chicken liver. Biometals 28:255–265CrossRefPubMedGoogle Scholar
  19. 19.
    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 17:14565–14572CrossRefPubMedGoogle Scholar
  20. 20.
    Iglesias P, Selgas R, Romero S, Díez JJ (2013) Selenium and kidney disease. J Nephrol 26:266–272CrossRefPubMedGoogle Scholar
  21. 21.
    Zhu SY, Li XN, Sun XC, Lin J, Li W, Zhang C, Li JL (2017) Biochemical characterization of the selenoproteome in Gallus gallus via bioinformatics analysis: structure-function relationships and interactions of binding molecules. Metallomics 9:124–131CrossRefPubMedGoogle Scholar
  22. 22.
    Kubachka K, Hanley T, Mantha M et al (2016) Evaluation of selenium in dietary supplements using elemental speciation. Food Chem 218:313–320CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Cao C, Zhao X, Fan R, Zhao J, Luan Y, Zhang Z, Xu S (2016) Dietary selenium increases the antioxidant levels and ATPase activity in the arteries and veins of poultry. Biol Trace Elem Res 172:222–227CrossRefPubMedGoogle Scholar
  24. 24.
    Cao C, Fan R, Chen M et al (2017) Inflammatory response occurs in veins of broiler chickens treated with a selenium deficiency diet. Biol Trace Elem Res 9:1–9Google Scholar
  25. 25.
    Guo CH, Hsu GS, Chuang CJ, Chen PC (2009) Aluminum accumulation induced testicular oxidative stress and altered selenium metabolism in mice. Environ Toxicol Pharmacol 27:176–181CrossRefPubMedGoogle Scholar
  26. 26.
    Krohn RM, Lemaire M, Negro Silva LF, Lemarié C, Bolt A, Mann KK, Smits JE (2016) High-selenium lentil diet protects against arsenic-induced atherosclerosis in a mouse model. J Nutr Biochem 27:9–15CrossRefPubMedGoogle Scholar
  27. 27.
    Mahieu S, Contini MC, Gonzã lM, Millen N (2009) Melatonin reduces oxidative damage induced by aluminium in rat kidney. Toxicol Lett 190:9–15CrossRefPubMedGoogle Scholar
  28. 28.
    Zhao HJ, Ning LI, Liu P (2011) Effect of deferiprone on activities of kidney ATPase and xanthine oxidase of aluminum induced mice. Food Drug 11:1Google Scholar
  29. 29.
    Vunta H, Davis F, Palempalli UD, Bhat D, Arner RJ, Thompson JT, Peterson DG, Reddy CC, Prabhu KS (2007) The anti-inflammatory effects of selenium are mediated through 15-deoxy-Delta12,14-prostaglandin J2 in macrophages. J Biol Chem 282:17964CrossRefPubMedGoogle Scholar
  30. 30.
    Bahmani F, Kia M, Soleimani A, Mohammadi AA, Asemi Z (2016) The effects of selenium supplementation on biomarkers of inflammation and oxidative stress in patients with diabetic nephropathy: a randomised, double-blind, placebo-controlled trial. Br J Nutr 116:1–7CrossRefGoogle Scholar
  31. 31.
    Zhu YZ, Liu DW, Liu ZY, Li YF (2013) Impact of aluminum exposure on the immune system: a mini review. Environ Toxicol Pharmacol 35:82–87CrossRefPubMedGoogle Scholar
  32. 32.
    Alexandrov PN, Kruck TP, Lukiw WJ (2015) Nanomolar aluminum induces expression of the inflammatory systemic biomarker C-reactive protein (CRP) in human brain microvessel endothelial cells (hBMECs). J Inorg Biochem 152:210–213CrossRefPubMedGoogle Scholar
  33. 33.
    Karabulutbulan O, Bayrak BB, Ardapirincci P et al (2015) Role of exogenous melatonin on cell proliferation and oxidant/antioxidant system in aluminum-induced renal toxicity. Biol Trace Elem Res 168:1–9CrossRefGoogle Scholar
  34. 34.
    Campbell A, Bondy SC (2000) Aluminum induced oxidative events and its relation to inflammation: a role for the metal in Alzheimer’s disease. Cell Mol Biol (Noisy-le-Grand, France) 46:721–730Google Scholar
  35. 35.
    Duntas LH (2009) Selenium and inflammation: underlying anti-inflammatory mechanisms. Horm Metab Res 41:443–447CrossRefPubMedGoogle Scholar
  36. 36.
    Speit G, Merk O (2002) Evaluation of mutagenic effects of formaldehyde in vitro: detection of crosslinks and mutations in mouse lymphoma cells. Mutagenesis 17:183–187CrossRefPubMedGoogle Scholar
  37. 37.
    Seven I, Turkozkan N, Cimen B (2005) The effects of nitric oxide synthesis on the Na+, K(+)-ATPase activity in guinea pig kidney exposed to lipopolysaccharides. Mol Cell Biochem 271:107–112CrossRefPubMedGoogle Scholar
  38. 38.
    Dogru PB, Daş EN, Ulusu NN, Bali M, Karasu C (2010) Effects of vitamin E on microsomal Ca(2+) -ATPase activity and calcium levels in streptozotocin-induced diabetic rat kidney. Cell Biochem Funct 21:177–182Google Scholar
  39. 39.
    Silva VS, Gonçalves PP (2014) Effect of lysine acetylsalicylate on aluminium accumulation and (Na+/K+) ATPase activity in rat brain cortex synaptosomes after aluminium ingestion. Toxicol Lett 232:167–174CrossRefPubMedGoogle Scholar
  40. 40.
    Sun X, Sun H, Yu K et al (2017) Aluminum chloride causes the dysfunction of testes through inhibiting the ATPase enzyme activities and gonadotropin receptor expression in rats. Biol Trace Elem Res 9:1–9Google Scholar

Copyright information

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

Authors and Affiliations

  1. 1.College of Life Science and EngineeringFoshan UniversityFoshanPeople’s Republic of China

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