Abstract
Oxidative stress plays a detrimental role in gastrointestinal disorders. Although selenium-enriched probiotics have been shown to strengthen oxidation resistance and innate immunity, the potential mechanism remains unclear. Here, we focused on the biological function of our material, selenium-enriched Bacillus paralicheniformis SR14 (Se-BP), and investigated the antioxidative effects of Se-BP and its underlying molecular mechanism in porcine jejunum epithelial cells. First, we prepared Se-BP and quantified for its selenium and bacterial contents. Then, in vitro free radical scavenging activity was measured to evaluate the potential antioxidant effect of Se-BP. Third, to induce an appropriate oxidative stress model, we adopted different concentrations of H2O2 and determined the most suitable concentration by a methyl thiazolyl tetrazolium (MTT) assay. Regarding treatment with Se-BP and H2O2, we found that Se-BP increased cell viability and prevented lactate dehydrogenase release when administered prior to H2O2 exposure. Additionally, Se-BP markedly suppressed reactive oxygen species and malondialdehyde production in cells and effectively attenuated apoptosis. Compared with incubation with H2O2 alone, treatment with Se-BP significantly promoted phosphorylation of ERK and p38 MAPK signaling molecules. When administered with ERK and p38 MAPK inhibitors, Se-BP did not alleviate the decrease in cell viability. Our results suggest that Se-BP prevents H2O2-induced cell damage by activating the ERK/p38 MAPK signaling pathways.
Similar content being viewed by others
References
Aw TY (1999) Molecular and cellular responses to oxidative stress and changes in oxidation-reduction imbalance in the intestine. Am J Clin Nutr 70(4):557–565
Bakhshalinejad R, Akbari RMK, Zoidis E (2017) Effects of different dietary sources and levels of selenium supplements on growth performance, antioxidant status and immune parameters in Ross 308 broiler chickens. Br Poult Sci 59(1):81–91. https://doi.org/10.1080/00071668.2017.1380296
Balaban H, Naziroglu M, Demirci K, Ovey IS (2017) The protective role of selenium on scopolamine-induced memory impairment, oxidative stress, and apoptosis in aged rats: the involvement of TRPM2 and TRPV1 channels. Mol Neurobiol 54(4):2852–2868. https://doi.org/10.1007/s12035-016-9835-0
Bhattacharyya A, Chattopadhyay R, Mitra S, Crowe SE (2014) Oxidative stress: an essential factor in the pathogenesis of gastrointestinal mucosal diseases. Physiol Rev 94(2):329–354. https://doi.org/10.1152/physrev.00040.2012
Bhatti JS, Bhatti GK, Reddy PH (2017) Mitochondrial dysfunction and oxidative stress in metabolic disorders - a step towards mitochondria based therapeutic strategies. Bba-Mol Basis Dis 1863(5):1066–1077. https://doi.org/10.1016/j.bbadis.2016.11.010
Bidkar AP, Sanpui P, Ghosh SS (2017) Efficient induction of apoptosis in cancer cells by paclitaxel-loaded selenium nanoparticles. Nanomedicine 12(21):2641–2652. https://doi.org/10.2217/nnm-2017-0189
Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot-London 91(2):179–194. https://doi.org/10.1093/aob/mcf118
Borrás C, Gambini J, Gómez-Cabrera MC, Sastre J, Pallardó FV, Mann GE, Viña J (2005) 17β-oestradiol up-regulates longevity-related, antioxidant enzyme expression via the ERK1 and ERK2[MAPK]/NFκB cascade. Aging Cell 4(3):113–118. https://doi.org/10.1111/j.1474-9726.2005.00151.x
Chen L, Pan DD, Zhou J, Jiang YZ (2005) Protective effect of selenium-enriched lactobacillus on CCl4-induced liver injury in mice and its possible mechanisms. World J Gastroenterol 11(37):5795–5800. https://doi.org/10.3748/wjg.v11.i37.5795
Cheng YZ, Xiao X, Li XX, Song DG, Lu ZQ, Wang FQ, Wang YZ (2017) Characterization, antioxidant property and cytoprotection of exopolysaccharide-capped elemental selenium particles synthesized by Bacillus paralicheniformis SR14. Carbohydr Polym 178:18–26. https://doi.org/10.1016/j.carbpol.2017.08.124
Danesi F, Malaguti M, Di NM, Maranesi M, Biagi PL, Bordoni A (2006) Counteraction of adriamycin-induced oxidative damage in rat heart by selenium dietary supplementation. J Agric Food Chem 54(4):1203–1208. https://doi.org/10.1021/jf0518002
Feng C, Zhang Y, Yang M, Lan M, Liu H, Huang B, Zhou Y (2017) Oxygen-sensing Nox4 generates genotoxic ROS to induce premature senescence of nucleus pulposus cells through MAPK and NF-κB pathways. Oxidative Med Cell Longev 2017(1):7426458. https://doi.org/10.1155/2017/7426458
Gan F, Ren F, Chen XX, Lv CH, Pan CL, Ye GP, Shi J, Shi XL, Zhou H, Shituleni SA, Huang KH (2013) Effects of Selenium-enriched probiotics on heat shock protein mRNA levels in piglet under heat stress conditions. J Agric Food Chem 61(10):2385–2391. https://doi.org/10.1021/jf300249j
Gangadoo S, Dinev I, Chapman J, Hughes RJ, Van TTH, Moore RJ, Stanley D (2018) Selenium nanoparticles in poultry feed modify gut microbiota and increase abundance of Faecalibacterium prausnitzii. Appl Microbiol Biotechnol 102(3):1455–1466. https://doi.org/10.1007/s00253-017-8688-4
Gao D, Gao Z, Zhu G (2013) Antioxidant effects of Lactobacillus plantarum via activation of transcription factor Nrf2. Food Funct 4(6):982–989. https://doi.org/10.1039/c3fo30316k
Gao FP, Yuan Q, Gao L, Cai PJ, Zhu HR, Liu R, Wang YL, Wei YT, Huang GD, Liang J, Gao XY (2014) Cytotoxicity and therapeutic effect of irinotecan combined with selenium nanoparticles. Biomaterials 35(31):8854–8866. https://doi.org/10.1016/j.biomaterials.2014.07.004
Gaweł S, Wardas M, Niedworok E, Wardas P (2004) Dialdehyd malonowy (MDA) jako wskaznik procesow peroksydacji lipidow w organizmie[Malondialdehyde (MDA) as alipid peroxidation marker]. Wiad Lek 57(9-10):453–455
Grompone G, Martorell P, Llopis S, Gonzalez N, Genoves S, Mulet AP, Fernandez-Calero T, Tiscornia I, Bollati-Fogolin M, Chambaud I, Foligne B, Montserrat A, Ramon D (2012) Anti-inflammatory Lactobacillus rhamnosus CNCM I-3690 strain protects against oxidative stress and increases lifespan in Caenorhabditis elegans. PLoS One 7(12):e52493. https://doi.org/10.1371/journal.pone.0052493
Guan MC, Tang WH, Xu Z, Sun J (2014) Effects of selenium-enriched protein from ganoderma lucidum on the levels of IL-1 beta and TNF-alpha, oxidative stress, and NF-kappa B activation in ovalbumin-induced asthmatic mice. Evid-Based Compl Alt 2014:182817. https://doi.org/10.1155/2014/182817
Haddad JJ, Land SC (2002) Redox/ROS regulation of lipopolysaccharide-induced mitogen-activated protein kinase (MAPK) activation and MAPK-mediated TNF-alpha biosynthesis. Brit J Pharmacol 135(2):520–536. https://doi.org/10.1038/sj.bjp.0704467
Hall RJ, Gupta PL (1969) The determination of very small amounts of selenium in plant samples. Analyst 94(1117):292. https://doi.org/10.1039/an9699400292
Hatfield DL, Tsuji PA, Carlson BA, Gladyshev VN (2014) Selenium and selenocysteine: roles in cancer, health, and development. Trends Biochem Sci 39(3):112–120. https://doi.org/10.1016/j.tibs.2013.12.007
Je JY, Lee DB (2015) Nelumbo nucifera leaves protect hydrogen peroxide-induced hepatic damage via antioxidant enzymes and HO-1/Nrf2 activation. Food Funct 6(6):1911–1918. https://doi.org/10.1039/c5fo00201j
Liu XN, Zhou B, Lin RS, Jia L, Deng P, Fan KM, Wang GY, Wang L, Zhang JJ (2010) Extraction and antioxidant activities of intracellular polysaccharide from Pleurotus sp mycelium. Int J Biol Macromol 47(2):116–119. https://doi.org/10.1016/j.ijbiomac.2010.05.012
Liu HM, Bian WX, Liu SX, Huang KX (2012) Selenium protects bone marrow stromal cells against hydrogen peroxide-induced inhibition of osteoblastic differentiation by suppressing oxidative stress and ERK signaling pathway. Biol Trace Elem Res 150(1-3):441–450. https://doi.org/10.1007/s12011-012-9488-4
Maggini S, Wintergerst ES, Beveridge S, Hornig DH (2007) Selected vitamins and trace elements support immune function by strengthening epithelial barriers and cellular and humoral immune responses. Brit J Nutr 98 Suppl 1(S1):S29–S35. https://doi.org/10.1017/S0007114507832971
Mccready RG, Campbell JN, Payne JI (1966) Selenite reduction by Salmonella Heidelberg. Can J Microbiol 12(4):703–714. https://doi.org/10.1139/M66-097
Musa HH, Wu SL, Zhu CH, Seri HI, Zhu GQ (2009) The potential benefits of probiotics in animal production and health. J Anim Vet Adv 8(2):313–321
Nafees S, Rashid S, Ali N, Sultana S (2014) Rutin ameliorates cyclophosphamide induced oxidative stress and inflammation in wistar rats: role of NF kappa B/MAPK pathway. Free Radical Bio Med 76:S151–S151. https://doi.org/10.1016/j.freeradbiomed.2014.10.564
Nancharaiah YV, Lens PNL (2015) Ecology and biotechnology of selenium-respiring bacteria. Microbiol Mol Biol R 79(1):61–80. https://doi.org/10.1128/Mmbr.00037-14
Nathan C, Cunningham-Bussel A (2013) Beyond oxidative stress: an immunologist’s guide to reactive oxygen species. Nat Rev Immunol 13(5):349–361. https://doi.org/10.1038/nri3423
Nido SA, Shituleni SA, Mengistu BM, Liu YH, Khan AZ, Gan F, Kumbhar S, Huang KH (2016) Effects of selenium-enriched probiotics on lipid metabolism, antioxidative status, histopathological lesions, and related gene expression in mice fed a high-fat diet. Biol Trace Elem Res 171(2):399–409. https://doi.org/10.1007/s12011-015-0552-8
Patel B, Kumar P, Banerjee R, Basu M, Pal A, Samanta M, Das S (2016) Lactobacillus acidophilus attenuates Aeromonas hydrophila induced cytotoxicity in catla thymus macrophages by modulating oxidative stress and inflammation. Mol Immunol 75:69–83. https://doi.org/10.1016/j.molimm.2016.05.012
Pescuma M, Gomez-Gomez B, Perez-Corona T, Font G, Madrid Y, Mozzi F (2017) Food prospects of selenium enriched-Lactobacillus acidophilus CRL 636 and Lactobacillus reuteri CRL 1101. J Funct Foods 35:466–473. https://doi.org/10.1016/j.jff.2017.06.009
Raman M, Chen W, Cobb MH (2007) Differential regulation and properties of MAPKs. Oncogene 26(22):3100–3112. https://doi.org/10.1038/sj.onc.1210392
Ravn-Haren G, Bugel S, Krath BN, Hoac T, Stagsted J, Jorgensen K, Bresson JR, Larsen EH, Dragsted LO (2008) A short-term intervention trial with selenate, selenium-enriched yeast and selenium-enriched milk: effects on oxidative defence regulation. Brit J Nutr 99(4):883–892. https://doi.org/10.1017/S0007114507825153
Ray PD, Huang BW, Tsuji Y (2012) Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 24(5):981–990. https://doi.org/10.1016/j.cellsig.2012.01.008
Resta-Lenert SC, Valle AM, Barrett KE (2002) Probiotics prevent apoptosis of intestinal epithelial cells induced by enteroinvasive pathogens. Gastroenterology 122(4):A281–A281
Rezvanfar MA, Rezvanfar MA, Shahverdi AR, Ahmadi A, Baeeri M, Mohammadirad A, Abdollahi M (2013) Protection of cisplatin-induced spermatotoxicity, DNA damage and chromatin abnormality by selenium nano-particles. Toxicol Appl Pharmacol 266(3):356–365. https://doi.org/10.1016/j.taap.2012.11.025
Rui W, Guan L, Zhang F, Zhang W, Ding W (2015) PM2.5 -induced oxidative stress increases adhesion molecules expression in human endothelial cells through the ERK/AKT/NF- kappa B-dependent pathway. J Appl Toxicol 36(1):48–59. https://doi.org/10.1002/jat.3143
Song D, Cheng Y, Li X, Wang F, Lu Z, Xiao X, Wang Y (2017) Biogenic nanoselenium particles effectively attenuate oxidative stress-induced intestinal epithelial barrier injury by activating the Nrf2 antioxidant pathway. ACS Appl Mater Interfaces 9(17):14724–14740. https://doi.org/10.1021/acsami.7b03377
Xu J, Yang FM, An XX, Hu QH (2007) Anticarcinogenic activity of selenium-enriched green tea extracts in vivo. J Agric Food Chem 55(13):5349–5353. https://doi.org/10.1021/jf070568s
Yan F, Polk DB (2002) Probiotic bacterium prevents cytokine-induced apoptosis in intestinal epithelial cells. J Biol Chem 277(52):50959–50965. https://doi.org/10.1074/jbc.M207050200
Yang JJ, Huang KH, Qin SY, Wu XS, Zhao ZP, Chen F (2009) Antibacterial action of selenium-enriched probiotics against pathogenic Escherichia coli. Dig Dis Sci 54(2):246–254. https://doi.org/10.1007/s10620-008-0361-4
Yazdi MH, Mahdavi M, Setayesh N, Esfandyar M, Shahverdi AR (2013) Selenium nanoparticle-enriched Lactobacillus brevis causes more efficient immune responses in vivo and reduces the liver metastasis in metastatic form of mouse breast cancer. Daru 21:33. https://doi.org/10.1186/2008-2231-21-33
Zamani Moghaddam AK, Mehraei Hamzekolaei MH, Khajali F, Hassanpour H (2017) Role of selenium from different sources in prevention of pulmonary arterial hypertension syndrome in broiler chickens. Biol Trace Elem Res 180(1):164–170. https://doi.org/10.1007/s12011-017-0993-3
Zhang HB, Chen TF, Jiang J, Wong YS, Yang F, Zheng WJ (2011) Selenium-Containing Allophycocyanin purified from selenium-enriched spirulina platensis attenuates AAPH-induced oxidative stress in human erythrocytes through inhibition of ROS generation. J Agric Food Chem 59(16):8683–8690. https://doi.org/10.1021/jf2019769
Zhao Y, Wang Y, Jiang ZT, Li R (2017) Screening and evaluation of active compounds in polyphenol mixtures by HPLC coupled with chemical methodology and its application. Food Chem 227:187–193. https://doi.org/10.1016/j.foodchem.2017.01.085
Zou Y, Wang J, Peng J, Wei HK (2016) Oregano essential oil induces SOD1 and GSH expression through Nrf2 activation and alleviates hydrogen peroxide-induced oxidative damage in IPEC-J2 cells. Oxidative Med Cell Longev 5987183:1–13. https://doi.org/10.1155/2016/5987183
Acknowledgments
We thank the staff of the Electronic Microscopy Center and the Agricultural, Biological, and Environmental Test Center at Zhejiang University for their assistance with flow cytometry. We thank Prof. Yulong Yin for the gift of the IPEC-J2 cells.
Funding
This work was supported by grants from the Modern Agroindustry Technology Research System (No. CARS-35) and Zhejiang Province Key R & D Project (No. 2015C02022).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Ethics approval
The research performed did not involve human participants and/or animals.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(PDF 312 kb)
Rights and permissions
About this article
Cite this article
Xiao, X., Cheng, Y., Song, D. et al. Selenium-enriched Bacillus paralicheniformis SR14 attenuates H2O2-induced oxidative damage in porcine jejunum epithelial cells via the MAPK pathway. Appl Microbiol Biotechnol 103, 6231–6243 (2019). https://doi.org/10.1007/s00253-019-09922-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-019-09922-9