Abstract
Selenium (Se) is a vital element which leads to strong antioxidation in animals and humans. However, the mechanism underlying natural cereal Se–induced biological changes is not well understood. This study intended to explore the gene differential expression in naturally aged mice exposed to selenium by RNA-Seq technique. A total spectrum of 53 differentially expressed genes was quantified in mice heart tissues treated with Se-rich and general rice. The GO functional annotation of differentially expressed genes disclosed the enrichment of cellular process, ionic binding, biological regulation, and catalytic activity. One hundred twenty-three differential pathways (cardiovascular diseases, immune system, transport and catabolism, longevity regulating, and PI3K-AKT signaling) were identified according to KEGG metabolic terms. Afterwards, the effect of Se-rich rice on the antioxidant activity was assessed. The selenium-rich diet increased the total antioxidant capacity (T-AOC), superoxide dismutase (SOD), and glutathione peroxidase (GSH-Px) in mice serum and livers while significantly reduces methane dicarboxylic aldehyde (MDA) contents. FOXO1 and FOXO3 genes, which acted as the regulators of apoptosis and the antioxidant enzyme, were significantly enhanced in mice when fed with Se-rich rice. In short, the present findings disclosed the alluring insights of organic and inorganic selenium sources on certain biological processes and antioxidant activity of living bodies. However, long-term trials are still required to draw a definitive conclusion, including risks and benefit analysis for various management strategies.
Similar content being viewed by others
References
Baar MP, Brandt RMC, Putavet DA, Klein JDD, Derks KWJ, Bourgeois BRM, Stryeck S, Rijksen Y, van Willigenburg H, Feijtel DA, van der Pluijm I, Essers J, van Cappellen WA, van IJcken WF, Houtsmuller AB, Pothof J, de Bruin RWF, Madl T, Hoeijmakers JHJ, Campisi J, de Keizer PLJ (2017) Targeted apoptosis of senescent cells restores tissue homeostasis in response to chemotoxicity and aging. Cell 169:132–147. e16. https://doi.org/10.1016/j.cell.2017.02.031
Bao R, Zheng S, Wang X (2017) Selenium protects against cadmium-induced kidney apoptosis in chickens by activating the PI3K/AKT/Bcl-2 signaling pathway. Environ Sci Pollut Res 24:20342–20353. https://doi.org/10.1007/s11356-017-9422-6
Bartholomeusz C, Gonzalez-Angulo AM (2012) Targeting the PI3K signaling pathway in cancer therapy. Expert Opin Ther Targets 26:121–130. https://doi.org/10.1517/14728222.2011.644788
Boreddy SR, Pramanik KC, Srivastava SK (2011) Pancreatic tumor suppression by benzyl isothiocyanate is associated with inhibition of PI3K/AKT/FOXO pathway. Clin Cancer Res 17:1784–1795. https://doi.org/10.1158/1078-0432.CCR-10-1891
Brozmanová J, Mániková D, Vlčková V, Chovanec M (2010) Selenium: a double-edged sword for defense and offence in cancer. Arch Toxicol 84:919–938. https://doi.org/10.1007/s00204-010-0595-8
Carey AM, Scheckel KG, Lombi E et al (2012) Grain accumulation of selenium species in rice (Oryza sativa L.). Environ Sci Technol 46:5557–5564. https://doi.org/10.1021/es203871j
Cashman KD, Kiely M (2013) EURRECA - estimating vitamin D requirements for deriving dietary reference values. Crit Rev Food Sci Nutr 53:1097–1109
Castellano JM, Mosher KI, Abbey RJ et al (2017) Human umbilical cord plasma proteins revitalize hippocampal function in aged mice. Nature 544:488–492. https://doi.org/10.1038/nature22067
Chun F, Bing Y, Daiwen C (2009) Effects of different sources and levels of selenium on performance, thyroid function and antioxidant status in stressed broiler chickens. Int J Poult Sci 8:583–587. https://doi.org/10.3923/ijps.2009.583.587
Doeing DC, Borowicz JL, Crockett ET (2003) Gender dimorphism in differential peripheral blood leukocyte counts in mice using cardiac, tail, foot, and saphenous vein puncture methods. BMC Clin Pathol 3:1–6. https://doi.org/10.1186/1472-6890-3-1
Eijkelenboom A, Burgering BMT (2013) FOXOs: Signalling integrators for homeostasis maintenance. Nat Rev Mol Cell Biol 14:83–97. https://doi.org/10.1038/nrm3507
Engelman JA (2009) Targeting PI3K signalling in cancer: opportunities, challenges and limitations. Nat Rev Cancer 9:550–562. https://doi.org/10.1038/nrc2664
Farooq MU, Zhichen T, Zeng R, et al. (2019) Accumulation, mobilization and transformation of selenium in rice grain provided with foliar sodium selenite. J Sci Food Agric 99:2892-2900. https://doi.org/10.1002/jsfa.9502
Gajčević Z, Kralik G, Has-Schön E, Pavić V (2009) Effects of organic selenium supplemented to layer diet on table egg freshness and selenium content. Ital J Anim Sci 8:189–199. https://doi.org/10.4081/ijas.2009.189
Giacosa A, Faliva MA, Perna S et al (2014) Selenium fortification of an Italian rice cultivar via foliar fertilization with sodium selenate and its effects on human serum selenium levels and on erythrocyte glutathione peroxidase activity. Nutrients 6:1251–1261. https://doi.org/10.3390/nu6031251
Greer EL, Brunet A (2005) FOXO transcription factors at the interface between longevity and tumor suppression. Oncogene 24:7410–7425. https://doi.org/10.1038/sj.onc.1209086
Hassan S (1990) Influence of dietary sodium selenite and barley selenium on the performance of laying hens and their subsequent progeny. Acta Agric Scand 40:267–278. https://doi.org/10.1080/00015129009438561
Houédé N, Pourquier P (2015) Targeting the genetic alterations of the PI3K-AKT-mTOR pathway: its potential use in the treatment of bladder cancers. Pharmacol Ther 145:1–18. https://doi.org/10.1016/j.pharmthera.2014.06.004
Hruszkewycz AM, Bergtold DS (1988) Oxygen radicals, lipid peroxidation and DNA damage in mitochondria. In: Oxygen radicals in biology and medicine. Basic Life Sciences 49:449–456. https://doi.org/10.1007/978-1-4684-5568-7_69
Janku F, Tsimberidou AM, Garrido-laguna I et al (2011) PIK3CA mutations in patients with advanced cancers treated with PI3K/AKT/mTOR axis inhibitors. Mol Cancer Ther 10:558–565. https://doi.org/10.1158/1535-7163.MCT-10-0994
Jing CL, Dong XF, Wang ZM et al (2015) Comparative study of DL-selenomethionine vs sodium selenite and seleno-yeast on antioxidant activity and selenium status in laying hens. Poult Sci 94:965–975. https://doi.org/10.3382/ps/pev045
Jomova K, Jenisova Z, Feszterova M et al (2011) Arsenic: toxicity, oxidative stress and human disease. J Appl Toxicol 31:95–107. https://doi.org/10.1002/jat.1649
Kalinsky K, Jacks LM, Heguy A et al (2009) PIK3CA mutation associates with improved outcome in breast cancer. Clin Cancer Res 15:5049–5059. https://doi.org/10.1158/1078-0432.CCR-09-0632
Klein E a, Goodman PJ, Lucia MS et al (2009) Effect of selenium and vitamin E on risk of prostate cancer and other cancers: the Selenium and Vitamin E Cancer Prevention Trial (SELECT). JAMA 301:39–51
Kryukov GV, Castellano S, Novoselov SV et al (2003) Characterization of mammalian selenoproteomes. Science (80- ) 300:1439–1443. https://doi.org/10.1126/science.1083516
Labunskyy VM, Hatfield DL, Gladyshev VN (2014) Selenoproteins: molecular pathways and physiological roles. Physiol Rev 94:739–777. https://doi.org/10.1152/physrev.00039.2013
Lam EWF, Brosens JJ, Gomes AR, Koo CY (2013) Forkhead box proteins: tuning forks for transcriptional harmony. Nat Rev Cancer 13:482–495. https://doi.org/10.1038/nrc3539
Lee JW, Soung YH, Kim SY et al (2005) PIK3CA gene is frequently mutated in breast carcinomas and hepatocellular carcinomas. Oncogene 24:1477–1480. https://doi.org/10.1038/sj.onc.1208304
Lemly AD (1997) Environmental implications of excessive selenium: a review. Biomed Environ Sci 435:415–435. https://doi.org/10.1016/S0147-6513(03)00095-2
Liang Y, Farooq MU, Hu Y et al (2018a) Study on stability and antioxidant activity of red anthocyanidin glucoside rich hybrid rice, its nutritional and physicochemical characteristics. Food Sci Technol Res 24:687–696. https://doi.org/10.3136/fstr.24.687
Liang Y, Farooq MU, Zeng R, et al. (2018b) Breeding of selenium rich red glutinous rice, protein extraction and analysis of the distribution of selenium in grain. Int J Agric Biol 20:1005–1011. https://doi.org/10.17957/IJAB/15.0592
Liao C, Booker RC, Morrison SJ, Le LQ (2017) Identification of hair shaft progenitors that create a niche for hair pigmentation. Genes Dev 31:1–13. https://doi.org/10.1101/gad.298703.117
Liu A, Ma Y, Zhu Z (2009) Protective effect of selenoarginine against oxidative stress in D-galactose-induced aging mice. Biosci Biotechnol Biochem 73:1461–1464. https://doi.org/10.1271/bbb.80558
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Luo H, Yang Y, Huang F et al (2012) Selenite induces apoptosis in colorectal cancer cells via AKT-mediated inhibition of β-catenin survival axis. Cancer Lett 315:78–85. https://doi.org/10.1016/j.canlet.2011.10.014
Luo H, Yang Y, Duan J et al (2013) PTEN-regulated AKT/FoxO3a/Bim signaling contributes to reactive oxygen species-mediated apoptosis in selenite-treated colorectal cancer cells. Cell Death Dis 4:481. https://doi.org/10.1038/cddis.2013.3
Mahmoud KZ, Edens FW (2003) Influence of selenium sources on age-related and mild heat stress-related changes of blood and liver glutathione redox cycle in broiler chickens (Gallus domesticus). Comp Biochem Physiol B Biochem Mol Biol 136:921–934. https://doi.org/10.1016/S1096-4959(03)00288-4
Mansour ATE, Goda AA, Omar EA et al (2017) Dietary supplementation of organic selenium improves growth, survival, antioxidant and immune status of meagre, Argyrosomus regius, juveniles. Fish Shellfish Immunol 68:516–524. https://doi.org/10.1016/j.fsi.2017.07.060
Martins R, Lithgow GJ, Link W (2016) Long live FOXO: unraveling the role of FOXO proteins in aging and longevity. Aging Cell 15:196–207. https://doi.org/10.1111/acel.12427
Mateo RD, Spallholz JE, Elder R et al (2007) Efficacy of dietary selenium sources on growth and carcass characteristics of growing-finishing pigs fed diets containing high endogenous selenium. J Anim Sci 85:1177–1183. https://doi.org/10.2527/jas.2006-067
Messarah M, Klibet F, Boumendjel A et al (2012) Hepatoprotective role and antioxidant capacity of selenium on arsenic-induced liver injury in rats. Exp Toxicol Pathol 64:167–174. https://doi.org/10.1016/j.etp.2010.08.002
Moore KL, Schroder M, Wu Z et al (2011) High-resolution secondary ion mass spectrometry reveals the contrasting subcellular distribution of arsenic and silicon in rice roots. Plant Physiol 156:913–924. https://doi.org/10.1104/pp.111.173088
Nicolau-neto P, Meireles N, Costa D et al (2018) Esophageal squamous cell carcinoma transcriptome reveals the effect of FOXM1 on patient outcome through novel PIK3R3 mediated activation of PI3K signaling pathway. Oncotarget 9:16634–16647
Oo SM, Misu H, Saito Y et al (2018) Serum selenoprotein P, but not selenium, predicts future hyperglycemia in a general Japanese population. Sci Rep 8:1–10. https://doi.org/10.1038/s41598-018-35067-2
Ošťádalová I, Charvátová Z, Wilhelm J (2010) Lipofuscin-like pigments in the rat heart during early postnatal development: effect of selenium supplementation. Physiol Res 59:881–886
Peters KM, Carlson BA, Gladyshev VN, Tsuji PA (2018) Selenoproteins in colon cancer. Free Radic Biol Med 127:14–25. https://doi.org/10.1016/j.freeradbiomed.2018.05.075
Pilarczyk B, Jankowiak D, Tomza-Marciniak A et al (2012) Selenium concentration and glutathione peroxidase (GSH-Px) activity in serum of cows at different stages of lactation. Biol Trace Elem Res 147:91–96. https://doi.org/10.1007/s12011-011-9271-y
Qin S, Gao J, Huang K (2007) Effects of different selenium sources on tissue selenium concentrations, blood GSH-Px activities and plasma interleukin levels in finishing lambs. Biol Trace Elem Res 116:91–102. https://doi.org/10.1007/s12011-007-9019-x
Radwan NL, Salah Eldin TA, El-Zaiat AA, Mostafa MASA (2015) Effect of dietary nano-selenium supplementation on selenium content and oxidative stability in table eggs and productive performance of laying hens. Int J Poult Sci 14:161–176. https://doi.org/10.3923/ijps.2015.161.176
Ravn-Haren G, Krath BN, Overvad K et al (2008) Effect of long-term selenium yeast intervention on activity and gene expression of antioxidant and xenobiotic metabolising enzymes in healthy elderly volunteers from the Danish Prevention of Cancer by Intervention by Selenium (PRECISE) Pilot Study. Br J Nutr 99:1190–1198. https://doi.org/10.1017/S0007114507882948
Rayman MP (2012) Selenium and human health. Lancet 379:1256–1268. https://doi.org/10.1016/S0140-6736(11)61452-9
Rotruck JT, Pope AL, Ganther HE et al (1973) Selenium: biochemical role as a component of glutathione peroxidase. Science (80- ) 179:588–590. https://doi.org/10.1126/science.179.4073.588
Schiavon M, Pilon-Smits EAH (2017) Selenium biofortification and phytoremediation phytotechnologies: a review. J Environ Qual 46:10. https://doi.org/10.2134/jeq2016.09.0342
Shao JF, Xia J, Yamaji N et al (2018) Effective reduction of cadmium accumulation in rice grain by expressing OsHMA3 under the control of the OsHMA2 promoter. J Exp Bot 69:2743–2752. https://doi.org/10.1093/jxb/ery107
Shen Q, Zhang B, Xu R et al (2010) Antioxidant activity in vitro of the selenium-contained protein from the Se-enriched Bifidobacterium animalis 01. Anaerobe 16:380–386. https://doi.org/10.1016/j.anaerobe.2010.06.006
Steinbrenner H, Speckmann B, Klotz LO (2016) Selenoproteins: antioxidant selenoenzymes and beyond. Arch Biochem Biophys 595:113–119. https://doi.org/10.1016/j.abb.2015.06.024
Tapiero H, Townsend DM, Tew KD (2003) The antioxidant role of selenium and seleno-compounds. Biomed Pharmacother 57:134–144. https://doi.org/10.1016/S0753-3322(03)00035-0
Tsuji PA, Carlson BA, Yoo MH et al (2015) The 15kDa selenoprotein and thioredoxin reductase 1 promote colon cancer by different pathways. PLoS One 10:1–18. https://doi.org/10.1371/journal.pone.0124487
Tzivion G, Dobson M, Ramakrishnan G (2011) FoxO transcription factors; regulation by AKT and 14-3-3 proteins. Biochim Biophys Acta - Mol Cell Res 1813:1938–1945. https://doi.org/10.1016/j.bbamcr.2011.06.002
Ursini F, Maiorino M, Gregolin C (1985) The selenoenzyme phospholipid hydroperoxide glutathione peroxidase. BBA - Gen Subj 839:62–70. https://doi.org/10.1016/0304-4165(85)90182-5
V WSA, GD (1987) Alterations in free radical tissue defense mechanisms in streptozotocin-induced diabetes in the rat: effects of insulin treatment. Diabetes 36:1014–1018. https://doi.org/10.2337/diab.36.9.1014
Van Gorp AGM, Pomeranz KM, Birkenkamp KU et al (2006) Chronic protein kinase B (PKB/c-akt) activation leads to apoptosis induced by oxidative stress-mediated Foxo3a transcriptional up-regulation. Cancer Res 66:10760–10769. https://doi.org/10.1158/0008-5472.CAN-06-1111
Vinceti M, Crespi CM, Bonvicini F et al (2013) The need for a reassessment of the safe upper limit of selenium in drinking water. Sci Total Environ 443:633–642. https://doi.org/10.1016/j.scitotenv.2012.11.025
Vinceti M, Filippini T, C DG et al (2018) Selenium for preventing cancer. Cochrane Database Syst Rev 1:CD005195. https://doi.org/10.1002/14651858.CD005195.pub4.
Vinceti M, Filippini T, Rothman KJ (2018) Selenium exposure and the risk of type 2 diabetes: a systematic review and meta-analysis. Eur J Epidemiol 33:789–810. https://doi.org/10.1007/s10654-018-0422-8
Wang YB, Xu BH (2008) Effect of different selenium source (sodium selenite and selenium yeast) on broiler chickens. Anim Feed Sci Technol 144:306–314. https://doi.org/10.1016/j.anifeedsci.2007.10.012
White PJ (2016) Selenium accumulation by plants. Ann Bot 117:217–235. https://doi.org/10.1093/aob/mcv180
Wilber CG (1980) Toxicology of selenium: a review. Clin Toxicol 17:171–230. https://doi.org/10.3109/15563658008985076
World Health Organization. (2009). Global health risks : mortality and burden of disease attributable to selected major risks. World Health Organization. http://www.who.int/iris/handle/10665/44203
Xia Y, Hill KE, Byrne DW, et al. (2005) Effectiveness of selenium supplements in a low selenium area of China. Am J Clin Nutr 81:829–834. https://doi.org/10.1093/ajcn/81.4.829
Yoon I, Werner TM, Butler JM (2007) Effect of source and concentration of selenium on growth performance and selenium retention in broiler chickens. Poult Sci 86:727–730. https://doi.org/10.1093/ps/86.4.727
You BR, Park WH (2012) Arsenic trioxide induces human pulmonary fibroblast cell death via increasing ROS levels and GSH depletion. Oncol Rep 28:749–757. https://doi.org/10.3892/or.2012.1852
Zhang H, Zhu NX, Huang K et al (2016) ITRAQ-based quantitative proteomic comparison of early- and late-passage human dermal papilla cell secretome in relation to inducing hair follicle regeneration. PLoS One 11:1–19. https://doi.org/10.1371/journal.pone.0167474
Zheng MZ, Li G, Sun GX et al (2013) Differential toxicity and accumulation of inorganic and methylated arsenic in rice. Plant Soil 365:227–238. https://doi.org/10.1007/s11104-012-1376-3
Zhu YG, Pilon-Smits EAH, Zhao FJ et al (2009) Selenium in higher plants: understanding mechanisms for biofortification and phytoremediation. Trends Plant Sci 14:436–442. https://doi.org/10.1016/j.tplants.2009.06.006
Acknowledgments
We thank Lu Tang for the assistance with the experiments.
Funding
This study was supported by the International Cooperation and Exchanges Research Program of the Department of S&T of Sichuan Province (2015HH0028) and Technology R&D Program of Sichuan Province (2016NZ0106).
Author information
Authors and Affiliations
Contributions
JZ and YL conceived the project and designed the experiments; YL, MUF, ZT, YZ, TZ, HLA, YS, XY, XJ, and RZ performed the experiments; YL and RZ analyzed the data; YL and MUF finalized the manuscript; all authors discussed the results and reviewed the manuscript.
Corresponding author
Ethics declarations
The animal study protocol (MICE2016022, 10/22/2016) was performed and approved by the Research Animal Care Committee of Sichuan Agricultural University (Chengdu, China), which confirmed to the national laws and policies and World Health Organization (WHO) definition. Animals were treated humanely, using approved procedures in accordance with the guidelines of the Institutional Animal Care and Use Committee at Sichuan Agricultural University.
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible editor: Philippe Garrigues
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Zeng, R., Liang, Y., Farooq, M.U. et al. Alterations in transcriptome and antioxidant activity of naturally aged mice exposed to selenium-rich rice. Environ Sci Pollut Res 26, 17834–17844 (2019). https://doi.org/10.1007/s11356-019-05226-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-019-05226-7