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Protecting Effect of Bacillus coagulans T242 on HT-29 Cells Against AAPH-Induced Oxidative Damage

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Abstract

The aim of the present study was to investigate the in vitro antioxidant potential of Bacillus coagulans T242. B. coagulans T242 showed better antioxidant activities, including the 2,2′-azino-bis (3-ethylbenzothiazoline-6-sulfonic acid) (ABTS) free radical scavenging ability, lipid peroxidation inhibiting ability and reducing ability, than those exerted by Lactobacillus rhamnosus GG (LGG). B. coagulans T242 positively regulated the expression of the nuclear factor erythroid 2-relatedfactor 2/Kelch-like ECH-associated protein-1 (Nrf2/Keap1) pathway-related proteins (Nrf2, Keap1, heine oxygenase-1 (HO-1)); increased antioxidant enzymes (glutathione peroxidase (GSH-Px), catalase (CAT), superoxide dismutase (SOD)); reduced the content of malondialdehyde (MDA) level; decreased the expression of inflammatory-related cytokines interleukin-6 (IL-6), interleukin-8 (IL-8), and tumor necrosis factor-α (TNF-α); and thus increased the survival rate in 2,2′-azobis (2-methylpropionamidine) dihydrochloride (AAPH)-damaged HT-29 cells. This study proved that B. coagulans T242 exerted antioxidative effects by quenching oxygen free radicals and activating the Nrf2 signaling pathway in HT-29 cells.

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Data Availability

The datasets generated or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Wang L, Ding L, Yu Z, Zhang T, Ma S, Liu J (2016) Intracellular ROS scavenging and antioxidant enzyme regulating capacities of corn gluten meal-derived antioxidant peptides in HepG2 cells. Food Res Int 90:33–41. https://doi.org/10.1016/j.foodres.2016.10.023

    Article  CAS  PubMed  Google Scholar 

  2. Ji K, Cho YS, Kim YT (2018) Tyrosinase inhibitory and anti-oxidative effects of lactic acid bacteria isolated from dairy cow feces. Probiotics Antimicrob Proteins 10(1):43–55. https://doi.org/10.1007/s12602-017-9274-x

    Article  CAS  PubMed  Google Scholar 

  3. Liu Z, Ren Z, Zhang J, Chuang CC, Kandaswamy E, Zhou T, Zuo L (2018) Role of ROS and nutritional antioxidants in human diseases. Front Physiol 9:477. https://doi.org/10.3389/fphys.2018.00477

    Article  PubMed  PubMed Central  Google Scholar 

  4. Zhang J, Wang X, Vikash V, Ye Q, Wu D, Liu Y, Dong W (2016) ROS and ROS-mediated cellular signaling. Oxid Med Cell Longev 2016:4350965. https://doi.org/10.1155/2016/4350965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Cabello-Verrugio C, Vilos C, Rodrigues-Diez R, Estrada L (2018) Oxidative stress in disease and aging: mechanisms and therapies 2018. Oxid Med Cell Longev 2018:2835189. https://doi.org/10.1155/2018/2835189

    Article  PubMed  PubMed Central  Google Scholar 

  6. Dixon SJ, Stockwell BR (2014) The role of iron and reactive oxygen species in cell death. Nat Chem Biol 10(1):9–17. https://doi.org/10.1038/nchembio.1416

    Article  CAS  PubMed  Google Scholar 

  7. Tsang AH, Chung KK (2009) Oxidative and nitrosative stress in Parkinson’s disease. Biochim Biophys Acta 1792(7):643–650. https://doi.org/10.1016/j.bbadis.2008.12.006

    Article  CAS  PubMed  Google Scholar 

  8. Yu X, Li Y, Wu Q, Shah NP, Wei H, Xu F (2020) Genomic analysis for antioxidant property of Lactobacillus plantarum FLPL05 from Chinese longevity people. Probiotics Antimicrob Proteins 12(4):1451–1458. https://doi.org/10.1007/s12602-020-09704-0

    Article  CAS  PubMed  Google Scholar 

  9. Finamore A, Ambra R, Nobili F, Garaguso I, Raguzzini A, Serafini M (2018) Redox Role of Lactobacillus casei Shirota Against the Cellular Damage Induced by 2,2’-Azobis (2-Amidinopropane) Dihydrochloride-Induced Oxidative and Inflammatory Stress in Enterocytes-Like Epithelial Cells. Front Immunol 9:1131. https://doi.org/10.3389/fimmu.2018.01131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Mishra V, Shah C, Mokashe N, Chavan R, Yadav H, Prajapati J (2015) probiotics as potential antioxidants: a systematic review. J Agric Food Chem 63(14):3615–3626. https://doi.org/10.1021/jf506326t

    Article  CAS  PubMed  Google Scholar 

  11. Elsayed Azab A, Adwas A, Ibrahim Elsayed AS, Adwas A, Ibrahim Elsayed AS, Quwaydir FA (2019) Oxidative stress and antioxidant mechanisms in human body. J Biotechnol Bioeng 6(1):43–47. https://doi.org/10.15406/jabb.2019.06.00173

  12. Wang Y, Wu Y, Wang Y, Xu H, Mei X, Yu D, Wang Y, Li W (2017) Antioxidant properties of probiotic bacteria. Nutrients 9(5). https://doi.org/10.3390/nu9050521

  13. Rajoka MSR, Mehwish HM, Hayat HF, Hussain N, Sarwar S, Aslam H, Nadeem A, Shi J (2019) Characterization, the Antioxidant and Antimicrobial Activity of Exopolysaccharide Isolated from Poultry Origin Lactobacilli. Probiotics Antimicrob Proteins 11(4):1132–1142. https://doi.org/10.1007/s12602-018-9494-8

    Article  CAS  PubMed  Google Scholar 

  14. Mu G, Gao Y, Tuo Y, Li H, Zhang Y, Qian F, Jiang S (2018) Assessing and comparing antioxidant activities of lactobacilli strains by using different chemical and cellular antioxidant methods. J Dairy Sci 101(12):10792–10806. https://doi.org/10.3168/jds.2018-14989

    Article  CAS  PubMed  Google Scholar 

  15. Persichetti E, De Michele A, Codini M, Traina G (2014) Antioxidative capacity of Lactobacillus fermentum LF31 evaluated in vitro by oxygen radical absorbance capacity assay. Nutrition 30(7–8):936–938. https://doi.org/10.1016/j.nut.2013.12.009

    Article  CAS  PubMed  Google Scholar 

  16. Shen Q, Shang N, Li P (2011) In vitro and in vivo antioxidant activity of Bifidobacterium animalis 01 isolated from centenarians. Curr Microbiol 62(4):1097–1103. https://doi.org/10.1007/s00284-010-9827-7

    Article  CAS  PubMed  Google Scholar 

  17. Hu Y, Dun Y, Li S, Zhao S, Peng N, Liang Y (2014) Effects of Bacillus subtilis KN-42 on growth performance, diarrhea and faecal bacterial flora of weaned piglets. Asian-Australas J Anim Sci 27(8):1131–1140. https://doi.org/10.5713/ajas.2013.13737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Hong HA, le Duc H, Cutting SM (2005) The use of bacterial spore formers as probiotics. FEMS Microbiol Rev 29(4):813–835. https://doi.org/10.1016/j.femsre.2004.12.001

    Article  CAS  PubMed  Google Scholar 

  19. Safronova LS, Skorochod IA, Ilyash VM (2021) Antioxidant and antiradical properties of probiotic strains Bacillus amyloliquefaciens ssp. plantarum. Probiotics Antimicrob Proteins 13 (6):1585–1597. https://doi.org/10.1007/s12602-021-09827-y

  20. Jemil N, Ben Ayed H, Manresa A, Nasri M, Hmidet N (2017) Antioxidant properties, antimicrobial and anti-adhesive activities of DCS1 lipopeptides from Bacillus methylotrophicus DCS1. BMC Microbiol 17(1):144. https://doi.org/10.1186/s12866-017-1050-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Majlesi M, Shekarforoush SS, Ghaisari HR, Nazifi S, Sajedianfard J, Eskandari MH (2017) Effect of Probiotic Bacillus Coagulans and Lactobacillus Plantarum on alleviation of mercury toxicity in rat. Probiotics Antimicrob Proteins 9(3):300–309. https://doi.org/10.1007/s12602-016-9250-x

    Article  CAS  PubMed  Google Scholar 

  22. Li LY, Lei K, Xu X, Rajput IR, Yu DY, Li WF (2013) Protective effect of Bacillus subtilis B10 against hydrogen peroxide-induced oxidative stress in a murine macrophage cell line. Int J Agric Biol 15(5)

  23. Wang Y, Wu Y, Wang Y, Fu A, Gong L, Li W, Li Y (2017) Bacillus amyloliquefaciens SC06 alleviates the oxidative stress of IPEC-1 via modulating Nrf2/Keap1 signaling pathway and decreasing ROS production. Appl Microbiol Biotechnol 101(7):3015–3026. https://doi.org/10.1007/s00253-016-8032-4

    Article  CAS  PubMed  Google Scholar 

  24. Kobatake E, Nakagawa H, Seki T, Miyazaki T (2017) Protective effects and functional mechanisms of Lactobacillus gasseri SBT2055 against oxidative stress. PLoS ONE 12(5):e0177106. https://doi.org/10.1371/journal.pone.0177106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Cutting SM (2011) Bacillus probiotics. Food Microbiol 28(2):214–220. https://doi.org/10.1016/j.fm.2010.03.007

    Article  PubMed  Google Scholar 

  26. Elshaghabee FMF, Rokana N, Gulhane RD, Sharma C, Panwar H (2017) Bacillus as potential probiotics: status, concerns, and future perspectives. Front Microbiol 8:1490. https://doi.org/10.3389/fmicb.2017.01490

    Article  PubMed  PubMed Central  Google Scholar 

  27. Sui L, Zhu X, Wu D, Ma T, Tuo Y, Jiang S, Qian F, Mu G (2020) In vitro assessment of probiotic and functional properties of Bacillus coagulans T242. Food Biosci 36. https://doi.org/10.1016/j.fbio.2020.100675

  28. Li C, Huang Q, Fu X, Yue XJ, Liu RH, You LJ (2015) Characterization, antioxidant and immunomodulatory activities of polysaccharides from Prunella vulgaris Linn. Int J Biol Macromol 75:298–305. https://doi.org/10.1016/j.ijbiomac.2015.01.010

    Article  CAS  PubMed  Google Scholar 

  29. Tang W, **ng Z, Li C, Wang J, Wang Y (2017) Molecular mechanisms and in vitro antioxidant effects of Lactobacillus plantarum MA2. Food Chem 221:1642–1649. https://doi.org/10.1016/j.foodchem.2016.10.124

    Article  CAS  PubMed  Google Scholar 

  30. Stinco CM, Baroni MV, Di Paola Naranjo RD, Wunderlin DA, Heredia FJ, Meléndez-Martínez AJ, Vicario IM (2015) Hydrophilic antioxidant compounds in orange juice from different fruit cultivars: Composition and antioxidant activity evaluated by chemical and cellular based (Saccharomyces cerevisiae) assays. J Food Compos Anal 37:1–10. https://doi.org/10.1016/j.jfca.2014.09.006

    Article  CAS  Google Scholar 

  31. Felice DL, Sun J, Liu RH (2009) A modified methylene blue assay for accurate cell counting. Journal of Functional Foods 1(1):109–118. https://doi.org/10.1016/j.jff.2008.09.014

    Article  Google Scholar 

  32. Mu G, Li H, Tuo Y, Gao Y, Zhang Y (2019) Antioxidative effect of Lactobacillus plantarum Y44 on 2,2’-azobis(2-methylpropionamidine) dihydrochloride (ABAP)-damaged Caco-2 cells. J Dairy Sci 102(8):6863–6875. https://doi.org/10.3168/jds.2019-16447

    Article  CAS  PubMed  Google Scholar 

  33. Zainodini N, Hassanshahi G, Hajizadeh M, Khanamani Falahati-Pour S, Mahmoodi M, Mirzaei MR (2018) Nisin induces cytotoxicity and apoptosis in human asterocytoma cell line (SW1088). Asian Pac J Cancer Prev 19(8):2217–2222. https://doi.org/10.22034/APJCP.2018.19.8.2217

  34. De Giani A, Bovio F, Forcella M, Fusi P, Sello G, Di Gennaro P (2019) Identification of a bacteriocin-like compound from Lactobacillus plantarum with antimicrobial activity and effects on normal and cancerogenic human intestinal cells. AMB Express 9(1):88. https://doi.org/10.1186/s13568-019-0813-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Molska M, Regula J (2019) Potential mechanisms of probiotics action in the prevention and treatment of colorectal cancer. Nutrients 11(10). https://doi.org/10.3390/nu11102453

  36. Park JM, Lee JS, Song JE, Sim YC, Ha SJ, Hong EK (2015) Cytoprotective effect of hispidin against palmitate-induced lipotoxicity in C2C12 myotubes. Molecules 20(4):5456–5467. https://doi.org/10.3390/molecules20045456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Jaramillo MC, Zhang DD (2013) The emerging role of the Nrf2-Keap1 signaling pathway in cancer. Genes Dev 27(20):2179–2191. https://doi.org/10.1101/gad.225680.113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Yang Y, Tian Z, Ding Y, Li X, Zhang Z, Yang L, Zhao F, Ren F, Guo R (2018) EGFR-targeted immunotoxin exerts antitumor effects on esophageal cancers by increasing ROS accumulation and inducing apoptosis via inhibition of the Nrf2-Keap1 pathway. J Immunol Res 2018:1090287. https://doi.org/10.1155/2018/1090287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Saw CLL, Wu Q, Kong AN (2010) Anti-cancer and potential chemopreventive actions of ginseng by activating Nrf2 (NFE2L2) anti-oxidative stress/anti-inflammatory pathways. Chin Med-UK 5(1):1–7. https://doi.org/10.1186/1749-8546-5-37

    Article  Google Scholar 

  40. Jiang CS, Zhuang CL, Zhu K, Zhang J, Muehlmann LA, Figueiro Longo JP, Azevedo RB, Zhang W, Meng N, Zhang H (2018) Identification of a novel small-molecule Keap1-Nrf2 PPI inhibitor with cytoprotective effects on LPS-induced cardiomyopathy. J Enzyme Inhib Med Chem 33(1):833–841. https://doi.org/10.1080/14756366.2018.1461856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Paloczi J, Varga ZV, Hasko G, Pacher P (2018) Neuroprotection in oxidative stress-related neurodegenerative diseases: role of endocannabinoid system modulation. Antioxid Redox Signal 29(1):75–108. https://doi.org/10.1089/ars.2017.7144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Wu J, **a S, Kalionis B, Wan W, Sun T (2014) The role of oxidative stress and inflammation in cardiovascular aging. Biomed Res Int 2014:615312. https://doi.org/10.1155/2014/615312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Amaretti A, di Nunzio M, Pompei A, Raimondi S, Rossi M, Bordoni A (2013) Antioxidant properties of potentially probiotic bacteria: in vitro and in vivo activities. Appl Microbiol Biotechnol 97(2):809–817. https://doi.org/10.1007/s00253-012-4241-7

    Article  CAS  PubMed  Google Scholar 

  44. Gu SB, Zhao LN, Wu Y, Li SC, Sun JR, Huang JF, Li DD (2015) Potential probiotic attributes of a new strain of Bacillus coagulans CGMCC 9951 isolated from healthy piglet feces. World J Microbiol Biotechnol 31(6):851–863. https://doi.org/10.1007/s11274-015-1838-x

    Article  CAS  PubMed  Google Scholar 

  45. Yu HS, Lee NK, Choi AJ, Choe JS, Bae CH, Paik HD (2019) Antagonistic and antioxidant effect of probiotic Weissella cibaria JW15. Food Sci Biotechnol 28(3):851–855. https://doi.org/10.1007/s10068-018-0519-6

    Article  CAS  PubMed  Google Scholar 

  46. Mateos R, Lecumberri E, Ramos S, Goya L, Bravo L (2005) Determination of malondialdehyde (MDA) by high-performance liquid chromatography in serum and liver as a biomarker for oxidative stress. Application to a rat model for hypercholesterolemia and evaluation of the effect of diets rich in phenolic antioxidants from fruits. J Chromatogr B Analyt Technol Biomed Life Sci 827(1):76–82. https://doi.org/10.1016/j.jchromb.2005.06.035

  47. Ighodaro OM, Akinloye OA (2019) First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid. Alexandria Journal of Medicine 54(4):287–293. https://doi.org/10.1016/j.ajme.2017.09.001

    Article  Google Scholar 

  48. Guerin P, El Mouatassim S, Menezo Y (2001) Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum reprod update 7(2):175–189. https://doi.org/10.1093/humupd/7.2.175

    Article  CAS  PubMed  Google Scholar 

  49. Ho YS, **ong Y, Ma W, Spector A, Ho DS (2004) Mice lacking catalase develop normally but show differential sensitivity to oxidant tissue injury. J Biol Chem 279(31):32804–32812. https://doi.org/10.1074/jbc.M404800200

    Article  CAS  PubMed  Google Scholar 

  50. Achuthan AA, Duary RK, Madathil A, Panwar H, Kumar H, Batish VK, Grover S (2012) Antioxidative potential of lactobacilli isolated from the gut of Indian people. Mol Biol Rep 39(8):7887–7897. https://doi.org/10.1007/s11033-012-1633-9

    Article  CAS  PubMed  Google Scholar 

  51. Wu T, Zhang Y, Lv Y, Li P, Yi D, Wang L, Zhao D, Chen H, Gong J, Hou Y (2018) Beneficial impact and molecular mechanism of Bacillus coagulans on piglets’ intestine. Int J Mol Sci 19 (7). https://doi.org/10.3390/ijms19072084

  52. Suzuki T, Yamamoto M (2017) Stress-sensing mechanisms and the physiological roles of the Keap1-Nrf2 system during cellular stress. J Biol Chem 292(41):16817–16824. https://doi.org/10.1074/jbc.R117.800169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Itoh K, Tong KI, Yamamoto M (2004) Molecular mechanism activating Nrf2-Keap1 pathway in regulation of adaptive response to electrophiles. Free Radic Biol Med 36(10):1208–1213. https://doi.org/10.1016/j.freeradbiomed.2004.02.075

    Article  CAS  PubMed  Google Scholar 

  54. Li C, Cheng L, Wu H, He P, Zhang Y, Yang Y, Chen J, Chen M (2018) Activation of the KEAP1NRF2ARE signaling pathway reduces oxidative stress in Hep2 cells. Mol Med Rep 18(3):2541–2550. https://doi.org/10.3892/mmr.2018.9288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Rahman MS, Hee Choi Y, Seok Choi Y, Alam MB, Han Lee S, Cheol Yoo J (2018) A novel antioxidant peptide, purified from Bacillus amyloliquefaciens, showed strong antioxidant potential via Nrf-2 mediated heme oxygenase-1 expression. Food Chem 239:502–510. https://doi.org/10.1016/j.foodchem.2017.06.106

    Article  CAS  PubMed  Google Scholar 

  56. Kobayashi M, Li L, Iwamoto N, Nakajima-Takagi Y, Kaneko H, Nakayama Y, Eguchi M, Wada Y, Kumagai Y, Yamamoto M (2009) The antioxidant defense system Keap1-Nrf2 comprises a multiple sensing mechanism for responding to a wide range of chemical compounds. Mol Cell Biol 29(2):493–502. https://doi.org/10.1128/MCB.01080-08

    Article  CAS  PubMed  Google Scholar 

  57. 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

    Article  CAS  PubMed  Google Scholar 

  58. Wang LX, Liu K, Gao DW, Hao JK (2013) Protective effects of two Lactobacillus plantarum strains in hyperlipidemic mice. World J Gastroenterol 19(20):3150–3156. https://doi.org/10.3748/wjg.v19.i20.3150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Lindqvist D, Dhabhar FS, James SJ, Hough CM, Jain FA, Bersani FS, Reus VI, Verhoeven JE, Epel ES, Mahan L, Rosser R, Wolkowitz OM, Mellon SH (2017) Oxidative stress, inflammation and treatment response in major depression. Psychoneuroendocrinology 76:197–205. https://doi.org/10.1016/j.psyneuen.2016.11.031

    Article  CAS  PubMed  Google Scholar 

  60. Biswas SK (2016) Does the interdependence between oxidative stress and inflammation explain the antioxidant paradox? Oxid Med Cell Longev 2016:5698931. https://doi.org/10.1155/2016/5698931

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Xu LQ, **e YL, Gui SH, Zhang X, Mo ZZ, Sun CY, Li CL, Luo DD, Zhang ZB, Su ZR, **e JH (2016) Polydatin attenuates d-galactose-induced liver and brain damage through its anti-oxidative, anti-inflammatory and anti-apoptotic effects in mice. Food Funct 7(11):4545–4555. https://doi.org/10.1039/c6fo01057a

    Article  CAS  PubMed  Google Scholar 

  62. Yang G, Shen K, Yu R, Wu Q, Yan Q, Chen W, Ding L, Kumar V, Wen C, Peng M (2020) Probiotic (Bacillus cereus) enhanced growth of Pengze crucian carp concurrent with modulating the antioxidant defense response and exerting beneficial impacts on inflammatory response via Nrf2 activation. Aquaculture 529. https://doi.org/10.1016/j.aquaculture.2020.735691

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Acknowledgements

This research was supported by Liaoning Province Natural Science Foundation of China (2020-MZLH-39), scientific research fund project of Liaoning Provincial Department of Education (J2019017).

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**aoxi Gao and Yuhong Zhang performed the experiments and wrote the manuscript. Yunpeng Xu, **nmiao Wang checked the logicality and language of this manuscript. Fang Qian, Yanfeng Tuo and Guangqing Mu conceived and designed the study. Fang Qian was responsible for overall study coordination of this manuscript.

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Correspondence to Yanfeng Tuo or Fang Qian.

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Gao, X., Zhang, Y., Mu, G. et al. Protecting Effect of Bacillus coagulans T242 on HT-29 Cells Against AAPH-Induced Oxidative Damage. Probiotics & Antimicro. Prot. 14, 741–750 (2022). https://doi.org/10.1007/s12602-022-09917-5

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