Abstract
Oxidative stress (OS) is a phenomenon induced by excessive production and accumulation of reactive oxygen species (ROS) in living cells. These increased ROS productions connected, coupled with many neurological and physiological diseases. Several antioxidants were utilized recently to combat OS, and lactic acid bacteria have a potent radical-scavenging activity to minimize OS. The present work was designed to find out the protective effects of Lactobacillus brevis MG000874 (L. brevis MG000874) against oxidative injuries induced by D-galactose (D-gal) in vivo and to explore the gene expression of OS-related gene mice. Sixty male mice were randomly split into six groups. The first four groups were different control groups as no treatment (N), positive (G), probiotic (B), and ascorbic acid (A); the remaining two groups were treatment groups such as probiotic treatment (BG) and ascorbic acid treatment (AG). L. brevis MG000874 (0.2 ml of 1010 CFU/ml) and ascorbic acid (0.2 ml of 25 mg/ml) were administered orally daily for 5 weeks. It was revealed that these significantly affect the weight of treated mice: 40.22 ± 1.5 and 33.0 ± 0.57 g on days 0 and 36, respectively. D-gal induction in mice declined the levels of SOD and CAT determined by spectrophotometer. Administration of L. brevis MG000874 improved the antioxidant status of the stress mice and recovered the antioxidant activities of SOD and CAT enzymes. In addition, L. brevis MG000874–altered gene expression of OS marker at the messenger RNA (mRNA) levels was determined by RT-PCR in the mouse model. L. brevis MG000874 significantly improved the GST, GPX, SOD, CAT, and ß-actin levels in the kidney and the liver of the D-gal-induced mice (p < 0.05). Moreover, the histological investigation indicated that L. brevis MG000874 mitigated damage to the kidney and liver effectively in mice induced by D-gal. Therefore, it could be concluded from the current results that L. brevis MG000874 may act as a powerful antioxidant agent, and this study can provide the baseline data for drug development against OS-linked diseases.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included in this published article.
References
Almaghrabi OA (2015) Molecular and biochemical investigations on the effect of quercetin on oxidative stress induced by cisplatin in rat kidney. Saudi J Biol Sci 22:227–231. https://doi.org/10.1016/j.sjbs.2014.12.008
Arya A, Chahal R, Rao R, Rahman MH, Kaushik D, Akhtar MF, Saleem A, Khalifa SM, El-Seedi HR, Kamel M, Mittal V (2021) Acetylcholinesterase inhibitory potential of various sesquiterpene analogues for Alzheimer’s disease therapy. Biomolecules 11:350. https://doi.org/10.3390/biom11030350
Asan Ö, Meltem, Gunyakti A (2022). Investigation of a new Lactobacillus delbrueckii strain from human milk as a probiotic candidate. J Food Saf Food Qual-Archiv fur lebensmittelhygiene 73(2). https://doi.org/10.2376/0003-925X-73-58
Brown RA, Epis MR, Horsham JL, Kabir TD, Richardson KL, Leedman PJ (2018) Total RNA extraction from tissues for microRNA and target gene expression analysis: not all kits are created equal. BMC Biotechnol 18:1–11. https://doi.org/10.1186/s12896-018-0421-6
Chen Z, Xiao J, Liu H, Yao K, Hou X, Cao Y, Liu X (2020) Astaxanthin attenuates oxidative stress and immune impairment in D-galactose-induced aging in rats by activating the Nrf2/Keap1 pathway and suppressing the NF-κB pathway. Food Funct 11:8099–8111. https://doi.org/10.1039/D0FO01663B
Claiborne AL (2018) Catalase activity. In: Greenwald RA (ed) CRC handbook of methods for oxygen radical research. CRC Press, Boca Raton, FL, pp 283–284
Di Meo S, Reed TT, Venditti P, Victor VM (2016) Role of ROS and RNS sources in physiological and pathological conditions. Oxid Med Cell Longev 2016:1–44. https://doi.org/10.1155/2016/1245049
Eissa N, Hussein H, Wang H, Rabbi MF, Bernstein CN, Ghia JE (2016) Stability of reference genes for messenger RNA quantification by real-time PCR in mouse dextran sodium sulfate experimental colitis. PloS One 11:e0156289. https://doi.org/10.1371/journal.pone.0156289
El-Sayed A, Aleya L, Kamel M (2021) Microbiota’s role in health and diseases. Environ Sci Pollut Res 28:36967–36983. https://doi.org/10.1007/s11356-021-14593-z
Fanzo J, Covic N, Dobermann A, Henson S, Herrero M, Pingali P, Staal S (2020) A research vision for food systems in the 2020s: defying the status quo. Glob food Sec 26:100397. https://doi.org/10.1016/j.gfs.2020.100397
Feng Y, Yu YH, Wang ST, Ren J, Camer D, Hua YZ, Zhang Q, Huang J, Xue DL, Zhang XF, Huang XF (2016) Chlorogenic acid protects D-galactose-induced liver and kidney injury via antioxidation and anti-inflammation effects in mice. Pharm Biol 54:1027–1034. https://doi.org/10.3109/13880209.2015.1093510
Ge Q, Yang B, Liu R, Jiang D, Yu H, Wu M, Zhang W (2021) Antioxidant activity of Lactobacillus plantarum NJAU-01 in an animal model of aging. BMC Microbiol 21:1–9. https://doi.org/10.1186/s12866-021-02248-5
Germoush MO, Fouda M, Kamel M, Abdel-Daim MM (2022) Spirulina platensis protects against microcystin-LR-induced toxicity in rats. Environ Sci Pollut Res 29:11320–11331. https://doi.org/10.1007/s11356-021-16481-y
Ghazi S, Diab AM, Khalafalla MM, Mohamed RA (2022) Synergistic effects of selenium and zinc oxide nanoparticles on growth performance, hemato-biochemical profile, immune and oxidative stress responses, and intestinal morphometry of Nile tilapia (Oreochromis niloticus). Biol Trace Elem Res 200(1):364–374
Hart P, Mao M, de Abreu A, Fricano K, Ekoue D, Minshall R, Diamond A, Bonini M (2015) MnSOD/SOD2 upregulation sustains the Warburg effect via mitochondrial ROS and AMPK-dependent signaling in cancer. The FASEB J 29:884–962. https://doi.org/10.1038/ncomms7053
Hassani S, Maqbool F, Salek-Maghsoudi A, Rahmani S, Shadboorestan A, Nili-Ahmadabadi A, Amini M, Norouzi P, Abdollahi M (2018) Alteration of hepatocellular antioxidant gene expression pattern and biomarkers of oxidative damage in diazinon-induced acute toxicity in Wistar rat: a time-course mechanistic study. EXCLI J 17:57. https://doi.org/10.17179/excli2017-760
Iqbal N, Zubair HM, Almutairi MH, Abbas M, Akhtar MF, Aleya L, Kamel M, Saleem A, Jabeen Q, Noreen S, Abdel-Daim MM (2022) Hepatoprotective effect of Cordia rothii extract against CCl4-induced oxidative stress via Nrf2–NFκB pathways. Biomed Pharmacother 156:113840. https://doi.org/10.1016/j.biopha.2022.113840
Landete JM, Gaya P, Rodríguez E, Langa S, Peirotén Á, Medina M, Arqués JL (2017) Probiotic bacteria for healthier aging: immunomodulation and metabolism of phytoestrogens. BioMed Res Int 2017:1–14. https://doi.org/10.1155/2017/5939818
Li JJ, Zhu Q, Lu YP, Zhao P, Feng ZB, Qian ZM, Zhu L (2015) Ligustilide prevents cognitive impairment and attenuates neurotoxicity in D-galactose induced aging mice brain. Brain Res 1595:19–28. https://doi.org/10.1016/j.brainres.2014.10.012
Li F, Huang G, Tan F, Yi R, Zhou X, Mu J, Zhao X (2020) Lactobacillus plantarum KSFY06 on d-galactose-induced oxidation and aging in Kunming mice. Food Sci Nutr 8:379–389. https://doi.org/10.1002/fsn3.1318
Li W, Huang W, Ma Y, Muhammad I, Hanif A, Ding Z, Guo X (2022) Antioxidant properties of lactic acid bacteria isolated from traditional fermented yak milk and their probiotic effects on the oxidative senescence of Caenorhabditis elegans. Food Funct 13:3690–3703. https://doi.org/10.1039/D1FO03538J
Liguori I, Russo G, Curcio F, Bulli G, Aran L, Della-Morte D, Gargiulo G, Testa G, Cacciatore F, Bonaduce D, Abete P (2018) Oxidative stress, aging, and diseases. Clin Interv Aging 13:757. https://doi.org/10.2147/CIA.S158513
Lin X, Xia Y, Wang G, Xiong Z, Zhang H, Lai F, Ai L (2018) Lactobacillus plantarum AR501 alleviates the oxidative stress of D-galactose-induced aging mice liver by upregulation of Nrf2-mediated antioxidant enzyme expression. J Food Sci 83:1990–1998. https://doi.org/10.1111/1750-3841.14200
Motataianu A, Serban G, Barcutean L, Balasa R (2022) Oxidative stress in amyotrophic lateral sclerosis: synergy of genetic and environmental factors. Int J Mol Sci 23:9339
Noureen S, Riaz A, Arshad M, Arshad N (2019) In vitro selection and in vivo confirmation of the antioxidant ability of Lactobacillus brevis MG 000874. J Appl Microbio 126:1221–1232. https://doi.org/10.1111/jam.14189
Qian YU, Zhang J, Zhou X, Yi R, Mu J, Long X, Pan Y, Zhao X, Liu W (2018) Lactobacillus plantarum CQPC11 isolated from sichuan pickled cabbages antagonizes d-galactose-induced oxidation and aging in mice. Molecules 23(11):3026. https://doi.org/10.3390/molecules23113026
Qiu Y, Ai PF, Song JJ, Liu C, Li ZW (2017) Total flavonoid extract from Abelmoschus manihot (L.) medic flowers attenuates d-galactose-induced oxidative stress in mouse liver through the Nrf2 pathway. J Med Food 20:557–567. https://doi.org/10.1089/jmf.2016.3870
Ramos OY, Basualdo M, Libonatti C, Vega MF (2020) Current status and application of lactic acid bacteria in animal production systems with a focus on bacteria from honey bee colonies. J Appl Microbiol 128:248–1260. https://doi.org/10.1111/jam.14469
Rehman FU, Farid A, Shah SU, Dar MJ, Rehman AU, Ahmed N, ... Shah KU (2022) Self-emulsifying drug delivery systems (SEDDS): measuring energy dynamics to determine thermodynamic and kinetic stability. Pharmaceuticals 15(9):1064. https://doi.org/10.3390/ph15091064
Rezaei M, Noori N, Shariatifar N, Gandomi H, Basti AA, Khaneghah AM (2020) Isolation of lactic acid probiotic strains from Iranian camel milk: technological and antioxidant properties. LWT 132:109823–109831. https://doi.org/10.1016/j.lwt.2020.109823
Sang Y, Zhang F, Wang H, Yao J, Chen R, Zhou Z, Yang K, Xie Y, Wan T, Ding H (2017) Apigenin exhibits protective effects in a mouse model of d-galactose-induced aging via activating the Nrf2 pathway. Food Funct 8:2331–2340. https://doi.org/10.1016/j.jff.2020.103957
Selvaratnam JS, Robaire B (2016) Effects of aging and oxidative stress on spermatozoa of superoxide-dismutase 1-and catalase-null mice. Biol Reprod 95:60–61. https://doi.org/10.1095/biolreprod.116.141671
Sharma VK, Singh TG, Garg N, Dhiman S, Gupta S, Rahman MH, ... Abdel-Daim MM (2021) Dysbiosis and Alzheimer’s disease: a role for chronic stress?. Biomolecules 11(05):678. https://doi.org/10.3390/biom11050678
Shen Q, Shang N, Li P (2011) In vitro and in vivo antioxidant activity of Bifidobacterium animalis 01 isolated from centenarians. Curr Microbiol 62:1097–1103. https://doi.org/10.1007/s00284-010-9827-7
Shen M, Zhao DK, Qiao Q, Liu L, Wang JL, Cao GH, ... Zhao ZW (2015) Identification of glutathione S-transferase (GST) genes from a dark septate endophytic fungus (Exophiala pisciphila) and their expression patterns under varied metals stress. PloS one 10(4):e0123418. https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0123418
Shwe T, Pratchayasakul W, Chattipakorn N, Chattipakorn SC (2018) Role of D-galactose-induced brain aging and its potential used for therapeutic interventions. Exp Gerontol 101:13–36. https://doi.org/10.1016/j.exger.2017.10.029
Stroustrup N (2018) Measuring and modeling interventions in aging. Curr Opin Cell Biol 55:129–138. https://doi.org/10.1016/j.ceb.2018.07.004
Unban K, Chaichana W, Baipong S, Abdullahi AD, Kanpiengjai A, Shetty K, Khanongnuch C (2021) Probiotic and antioxidant properties of lactic acid bacteria isolated from indigenous fermented tea leaves (Miang) of north thailand and promising application in synbiotic formulation. Fermentation 7:195. https://doi.org/10.3390/fermentation7030195
Wells JC, Sawaya AL, Wibaek R, Mwangome M, Poullas MS, Yajnik CS, Demaio A (2020) The double burden of malnutrition: aetiological pathways and consequences for health. The Lancet 395:75–88. https://doi.org/10.1016/S0140-6736(19)32472-9
Woo JY, Gu W, Kim KA, Jang SE, Han MJ, Kim DH (2014) Lactobacillus pentosus var. plantarum C29 ameliorates memory impairment and inflammaging in a D-galactose-induced accelerated aging mouse model. Anaerobe 27:22–26. https://doi.org/10.1016/j.anaerobe.2014.03.003
Xu LQ, Xie YL, Gui SH, Zhang X, Mo ZZ, Sun CY, Li CL, Luo DD, Zhang ZB, Su ZR, Xie 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 7:4545–4555. https://doi.org/10.1039/c6fo01057a
Xu C, Li E, Suo Y, Su Y, Lu M, Zhao Q, Qin JG, Chen L (2018) Histological and transcriptomic responses of two immune organs, the spleen and head kidney, in Nile tilapia (Oreochromis niloticus) to long-term hypersaline stress. Fish Shellfish Immunol 76:48–57. https://doi.org/10.1016/j.fsi.2018.02.041
Yadav R, Khan SH, Mada SB, Meena S, Kapila R, Kapila S (2019) Consumption of probiotic Lactobacillus fermentum MTCC: 5898-fermented milk attenuates dyslipidemia, oxidative stress, and inflammation in male rats fed on cholesterol-enriched diet. Probiotics Antimicrob Prot 11:509–518. https://doi.org/10.1007/s12602-018-9429-4
Zhao J, Tian F, Yan S, Zhai Q, Zhang H, Chen W (2018) Lactobacillus plantarum CCFM10 alleviating oxidative stress and restoring the gut microbiota in d-galactose-induced aging mice. Food Funct 1:917–924. https://doi.org/10.1039/C7FO01574G
Zheng G, Xu X, Zheng J, Liu A (2016) Protective effect of seleno-β-lactoglobulin (Se-β-lg) against oxidative stress in D-galactose-induced aging mice. J Funct Foods 27:310–318. https://doi.org/10.1016/j.jff.2016.09.015
Funding
This research was funded by the NAHE Higher Education Commission of Pakistan through grant no. 532/IPFP-II (Batch-I) /SRGP/NAHE/HEC/2020/130.
Author information
Authors and Affiliations
Contributions
S. N: conceptualization, methodology, analysis, data curation, and writing — original draft; T. H: Analysis; A. N: reviewing and editing; A. E. A: reviewing and editing.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
The protocol for these experiments was approved by the Animal Ethics Committee of the Virtual University of Pakistan.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Mohamed M. Abdel-Daim
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Noureen, S., Hussain, T., Noureen, A. et al. Effect of Lactobacillus brevis (MG000874) on antioxidant-related gene expression of the liver and kidney in D-galactose-induced oxidative stress mice model. Environ Sci Pollut Res 30, 84099–84109 (2023). https://doi.org/10.1007/s11356-023-28203-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-023-28203-7