Lactobacillus brevis MTCC 1750 enhances oxidative stress resistance and lifespan extension with improved physiological and functional capacity in Caenorhabditis elegans via the DAF-16 pathway

References

• Boisvert MM, Erikson GA, Shokhirev MN, et al. The aging astrocyte transcriptome from multiple regions of the mouse brain. Cell Rep. 2018;22(1):269–285.
   PubMed Web of Science ®Google Scholar
• Schaffer S, Gruber J, Ng LF, et al. The effect of dichloroacetate on health- and lifespan in C. elegans. Biogerontology. 2011;12(3):195–209.
   PubMed Web of Science ®Google Scholar
• Miller KN, Burhans MS, Clark JP, et al. Aging and caloric restriction impact adipose tissue, adiponectin, and circulating lipids. Aging Cell. 2017;16(3):497–507.
   PubMed Web of Science ®Google Scholar
• Harman D. The biologic clock: the mitochondria? J Am Geriatr Soc. 1972;20(4):145–147.
   PubMed Web of Science ®Google Scholar
• Beckman KB, Ames BN. The free radical theory of aging matures. Physiol Rev. 1998;78(2):547–581.
   PubMed Web of Science ®Google Scholar
• Andriollo-Sanchez M, Hininger-Favier I, Meunier N, et al. Age-related oxidative stress and antioxidant parameters in middle-aged and older European subjects: the ZENITH study. Eur J Clin Nutr. 2005;59(S2):s58–s62.
   PubMedGoogle Scholar
• Santiago KH, López ALL, Sánchez-Muñoz F, et al. Sleep deprivation induces oxidative stress in the liver and pancreas in young and aging rats. Heliyon. 2021;7(3):E06466.
   PubMed Web of Science ®Google Scholar
• Sohal RS, Weindruch R. Oxidative stress, caloric restriction, and aging. Science. 1996;273(5271):59–63.
   PubMed Web of Science ®Google Scholar
• Ziada AS, Smith MSR, Côté HCF. Updating the free radical theory of aging. Front Cell Dev Biol. 2020;8:575645.
   PubMed Web of Science ®Google Scholar
• El Assar M, Angulo J, Rodríguez-Mañas L. Frailty as a phenotypic manifestation of underlying oxidative stress. Free Radic Biol Med. 2020;149:72–77.
   PubMed Web of Science ®Google Scholar
• Viña J, Borrás C, Miquel J. Theories of ageing. IUBMB Life. 2007;59(4-5):249–254.
   PubMed Web of Science ®Google Scholar
• Muralidharan N, Bhat T, Kumari S. A study on effect of ageing on the levels of total antioxidant and lipid peroxidation. Int J Contemp Med Res. 2017;4(12):8–10.
   Google Scholar
• Ho S-T, Hsieh Y-T, Wang S-Y, et al. Improving effect of a probiotic mixture on memory and learning abilities in d-galactose–treated aging mice. J Dairy Sci. 2019;102(3):1901–1909.
   PubMed Web of Science ®Google Scholar
• Mohanty SK, Suchiang K. Triiodothyronine (T3) enhances lifespan and protects against oxidative stress via activation of klotho in Caenorhabditis elegans. Biogerontology. 2021;22(4):397–413.
   PubMed Web of Science ®Google Scholar
• Chen W, Rezaizadehnajafi L, Wink M. Influence of resveratrol on oxidative stress resistance and life span in Caenorhabditis elegans. J Pharm Pharmacol. 2013;65(5):682–688.
   PubMed Web of Science ®Google Scholar
• Miracle Uwa L. The anti-aging efficacy of antioxidants. CTBEB. 2017;7(4):2–4.
   Google Scholar
• Das D, Goyal A. Antioxidant activity and γ-aminobutyric acid (GABA) producing ability of probiotic Lactobacillus plantarum DM5 isolated from Marcha of Sikkim. LWT Food Sci Technol. 2015;61(1):263–268.
   Web of Science ®Google Scholar
• Al-Dhabi NA, Arasu MV, Vijayaraghavan P, et al. Probiotic and antioxidant potential of Lactobacillus reuteriLR12 and Lactobacillus lactisLL10 isolated from pineapple puree and quality analysis of pineapple-flavored goat milk yoghurt during storage. Microorganisms. 2020;8(10):1461–1415.
   PubMed Web of Science ®Google Scholar
• Tsai YC, Cheng LH, Liu YW, et al. Gerobiotics: probiotics targeting fundamental aging processes. Biosci Microbiota Food Health. 2021;40(1):1–11.
   PubMed Web of Science ®Google Scholar
• Kim H, Kim J-S, Kim Y, et al. Antioxidant and probiotic properties of lactobacilli and bifidobacteria of human origins. Biotechnol Bioproc E. 2020;25(3):421–430.
   Web of Science ®Google Scholar
• Lee J, Hwang K-T, Heo M-S, et al. Resistance of Lactobacillus plantarum KCTC 3099 from kimchi to oxidative stress. J Med Food. 2005;8(3):299–304.
   PubMed Web of Science ®Google Scholar
• Choi SS, Kim Y, Han KS, et al. Effects of lactobacillus strains on cancer cell proliferation and oxidative stress in vitro. Lett Appl Microbiol. 2006;42(5):452–458.
   PubMed Web of Science ®Google Scholar
• Grompone G, Martorell P, Llopis S, et al. Anti-inflammatory Lactobacillus rhamnosus CNCM I-3690 strain protects against oxidative stress and increases lifespan in Caenorhabditis elegans. PLoS One. 2012;7(12):e52493.
   PubMed Web of Science ®Google Scholar
• Zhang W, Zheng B, Deng N, et al. Effects of ethyl acetate fractional extract from portulaca oleracea L. (PO-EA) on lifespan and healthspan in Caenorhabditis elegans. J Food Sci. 2020;85(12):4367–4376.
   PubMed Web of Science ®Google Scholar
• Wilson MA, Shukitt-Hale B, Kalt W, et al. Blueberry polyphenols increase lifespan and thermotolerance in Caenorhabditis elegans. Aging Cell. 2006;5(1):59–68.
   PubMed Web of Science ®Google Scholar
• Yi L, Luo JF, Xie BB, et al. α7 nicotinic acetylcholine receptor is a novel mediator of sinomenine anti-inflammation effect in macrophages stimulated by lipopolysaccharide. Shock. 2015;44(2):188–195.
   PubMed Web of Science ®Google Scholar
• Fang Z, Xiao B, Jiang W, et al. The antioxidant capacity evaluation of polysaccharide hydrolyzates from pumpkin using Caenorhabditis elegans model. J Food Biochem. 2021;45(3):e13275.
   PubMed Web of Science ®Google Scholar
• Zhang J, Xiao Y, Guan Y, et al. An aqueous polyphenol extract from rosa rugosa tea has antiaging effects on Caenorhabditis elegans. J Food Biochem. 2019;43(4):e12796.
   PubMed Web of Science ®Google Scholar
• Poupet C, Chassard C, Nivoliez A, et al. Caenorhabditis elegans, a host to investigate the probiotic properties of beneficial microorganisms. Front Nutr. 2020;7:135.
   PubMed Web of Science ®Google Scholar
• Kenyon C. The first long-lived mutants: discovery of the insulin/IGF-1 pathway for ageing. Philos Trans R Soc Lond B Biol Sci. 2011;366(1561):9–16.
   PubMed Web of Science ®Google Scholar
• Zhao L, Zhao Y, Liu R, et al. The transcription factor DAF-16 is essential for increased longevity in C. elegans exposed to Bifidobacterium longum BB68. Sci Rep. 2017;7(1):1–7.
   PubMed Web of Science ®Google Scholar
• Stiernagle T. Maintenance of C. elegans. WormBook. 2006;1:11.
   Google Scholar
• Park MR, Ryu S, Maburutse BE, et al. Probiotic Lactobacillus fermentum strain JDFM216 stimulates the longevity and immune response of Caenorhabditis elegans through a nuclear hormone receptor. Sci Rep. 2018;8(1):7441.
   PubMed Web of Science ®Google Scholar
• Smolentseva C, Gusarov I, Gautier L, et al. Mechanism of biofilm-mediated stress resistance and lifespan extension in C. elegans. Sci Rep. 2017;7(1):1–6.
   Google Scholar
• Senchuk MM, Dues DJ, Van Raamsdonk JM. Measuring oxidative stress in Caenorhabditis elegans: paraquat and juglone sensitivity assays. Bio-protocol. 2017;7(1):e2086.
   Google Scholar
• Zanni E, Laudenzi C, Schifano E, et al. Impact of a complex food microbiota on energy metabolism in the model organism Caenorhabditis elegans. Biomed Res Int. 2015;2015:621709.
   PubMed Web of Science ®Google Scholar
• Kaplan EL, Meier P. Nonparametric estimation from incomplete observations. J American Stati Ass. 1958;53(282):457–481..
   Google Scholar
• Rangsinth P, Prasansuklab A, Duangjan C, et al. Leaf extract of caesalpinia mimosoides enhances oxidative stress resistance and prolongs lifespan in Caenorhabditis elegans. BMC Complement Altern Med. 2019;19(1):1–13.
   PubMedGoogle Scholar
• Lu M, Tan L, Zhou X-G, et al. Tectochrysin increases stress resistance and extends the lifespan of Caenorhabditis elegans via FOXO/DAF-16. Biogerontology. 2020;21(5):669–682.
   PubMed Web of Science ®Google Scholar
• Lee J, Kwon G, Lim Y-H. Elucidating the mechanism of Weissella -dependent lifespan extension in Caenorhabditis elegans. Sci Rep. 2015;5(1):1–14.
   Google Scholar
• Balaguer F, Enrique M, Llopis S, et al. Lipoteichoic acid from Bifidobacterium animalis subsp. lactis BPL1: a novel postbiotic that reduces fat deposition via IGF-1 pathway. Microb Biotechnol. 2022;15(3):805–816.
   PubMed Web of Science ®Google Scholar
• Kwon G, Lee J, Lim YH. Dairy propionibacterium extends the mean lifespan of Caenorhabditis elegans via activation of the innate immune system. Sci Rep. 2016;6(1):1–11.
   PubMedGoogle Scholar
• Eruslanov E, Kusmartsev S. Identification of ROS using oxidized DCFDA and flow-cytometry. Methods Mol Biol. 2010;594:57–72.
   PubMedGoogle Scholar
• Thakur BK, Saha P, Banik G, et al. Live and heat-killed probiotic Lactobacillus casei Lbs2 protects from experimental colitis through toll-like receptor 2-dependent induction of T-regulatory response. Int Immunopharmacol. 2016;36:39–50.
   PubMed Web of Science ®Google Scholar
• Ahrén IL, Xu J, Önning G, et al. Antihypertensive activity of blueberries fermented by Lactobacillus plantarum DSM 15313 and effects on the gut microbiota in healthy rats. Clin Nutr. 2015;34(4):719–726.
   PubMed Web of Science ®Google Scholar
• Kakimoto Y, Okada, C, Kawabe N, et al. Myocardial lipofuscin accumulation in ageing and sudden cardiac death. Sci Rep. 2019;9(1):91.
   PubMedGoogle Scholar
• Lee EB, Kim JH, An CW, et al. Longevity and stress resistant property of 6-Gingerol from Zingiber officinale roscoe in Caenorhabditis elegans. Biomol Ther. 2018;26(6):568–575.
   PubMed Web of Science ®Google Scholar
• Son HG, Altintas O, Kim EJE, et al. Age-dependent changes and biomarkers of aging in Caenorhabditis elegans. Aging Cell. 2019;18(2):e12853.
   PubMed Web of Science ®Google Scholar
• Trojanowski NF, Raizen DM, Fang-Yen C. Pharyngeal pumping in Caenorhabditis elegans depends on tonic and phasic signaling from the nervous system. Sci Rep. 2016;6(1):1–10.
   PubMedGoogle Scholar
• Sharma K, Pooranachithra M, Balamurugan K, et al. Multivariate analysis of increase in life span of Caenorhabditis elegans through intestinal colonization by indigenous probiotic strains. Probiotics Antimicrob Proteins. 2019;11(3):865–873.
   PubMed Web of Science ®Google Scholar
• Tullet JMA, Hertweck M, An JH, et al. Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans. Cell. 2008;132(6):1025–1038.
   PubMed Web of Science ®Google Scholar
• Zarse K, Schmeisser S, Groth M, et al. Impaired insulin/IGF1 signaling extends life span by promoting mitochondrial L-proline catabolism to induce a transient ROS signal. Cell Metab. 2012;15(4):451–465.
   PubMed Web of Science ®Google Scholar
• Henderson ST, Johnson TE. Daf-16 integrates developmental and environmental inputs to mediate aging in the nematode Caenorhabditis elegans. Curr Biol. 2001;11(24):1975–1980.
   PubMed Web of Science ®Google Scholar
• Davis RJ. Signal transduction by the JNK group of MAP kinases. Cell. 2000;103(2):239–252.
   PubMed Web of Science ®Google Scholar
• Oh SW, Mukhopadhyay A, Svrzikapa N, et al. JNK regulates lifespan in Caenorhabiditis elegans by modulating nuclear translocation of Forkhead transcription factor/DAF-16. Proc Natl Acad Sci U S A. 2005;102(12):4494–4499.
   PubMed Web of Science ®Google Scholar
• Palikaras K, Mari M, Petanidou B, et al. Ectopic fat deposition contributes to age-associated pathology in Caenorhabditis elegans. J Lipid Res. 2017;58(1):72–80.
   PubMed Web of Science ®Google Scholar
• Huang C, Xiong C, Kornfeld K. Measurements of age-related changes of physiological processes that predict lifespan of Caenorhabditis elegans. Proc Natl Acad Sci U S A. 2004;101(21):8084–8089.
   PubMed Web of Science ®Google Scholar
• Sawin ER, Ranganathan R, Horvitz HR. C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron. 2000;26(3):619–631.
   PubMed Web of Science ®Google Scholar
• Sharma R, Padwad Y. Probiotic bacteria as modulators of cellular senescence: emerging concepts and opportunities. Gut Microbes. 2020;11(3):335–349.
   PubMed Web of Science ®Google Scholar
• Czyż D. Exploiting Caenorhabditis elegans to discover human gut microbiota-mediated intervention strategies in protein conformational diseases. Neural Regen Res. 2022;17(10):2203–2204.
   PubMed Web of Science ®Google Scholar
• Inbaraj JJ, Chignell CF. Cytotoxic action of juglone and plumbagin: a mechanistic study using HaCaT keratinocytes. Chem Res Toxicol. 2004;17(1):55–62.
   PubMed Web of Science ®Google Scholar
• Kumar A, Joishy T, Das S, et al. A potential probiotic Lactobacillus plantarum JBC5 improves longevity and healthy aging by modulating antioxidative, innate immunity and serotonin-signaling pathways in Caenorhabditis elegans. Antioxidants. 2022;11(2):268.
   Web of Science ®Google Scholar
• Martorell P, Alvarez B, Llopis S, et al. Heat-treated bifidobacterium longum CECT-7347: a whole-cell postbiotic with antioxidant, anti-inflammatory, and gut-barrier protection properties. mdpi.com. 2021;10(4):536.
   Google Scholar
• Martorell P, Llopis S, González N, et al. Probiotic strain Bifidobacterium animalis subsp. lactis CECT 8145 reduces fat content and modulates lipid metabolism and antioxidant response in Caenorhabditis elegans. J Agric Food Chem. 2016;64(17):3462–3472.
   PubMed Web of Science ®Google Scholar
• Fontana L, Partridge L, Longo VD. Extending healthy life span–from yeast to humans. Science. 2010;328(5976):321–326.
   PubMed Web of Science ®Google Scholar
• Kondo M, Yanase S, Ishii T, et al. The p38 signal transduction pathway participates in the oxidative stress-mediated translocation of DAF-16 to Caenorhabditis elegans nuclei. Mech Ageing Dev. 2005;126(6-7):642–647.
   PubMed Web of Science ®Google Scholar
• An JH, Blackwell TK. SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress response. Genes Dev. 2003;17(15):1882–1893.
   PubMed Web of Science ®Google Scholar
• Kell A, Ventura N, Kahn N, et al. Activation of SKN-1 by novel kinases in Caenorhabditis elegans. Free Radic Biol Med. 2007;43(11):1560–1566.
   PubMed Web of Science ®Google Scholar
• Song B, Zheng B, Li T, et al. SKN-1 is involved in combination of apple peels and blueberry extracts synergistically protecting against oxidative stress in Caenorhabditis elegans. Food Funct. 2020;11(6):5409–5419.
   PubMed Web of Science ®Google Scholar
• Putker M, Madl T, Vos HR, et al. Redox-dependent control of FOXO/DAF-16 by transportin-1. Mol Cell. 2013;49(4):730–742.
   PubMed Web of Science ®Google Scholar
• Apfeld J, Kenyon C. Cell nonautonomy of C. elegans daf-2 function in the regulation of diapause and life span. Cell. 1998;95(2):199–210.
   PubMed Web of Science ®Google Scholar
• Katewa SD, Kapahi P. Dietary restriction and aging, 2009. Aging Cell. 2010;9(2):105–112.
   PubMed Web of Science ®Google Scholar
• Scholz M, Lynch DJ, Lee KS, et al. A scalable method for automatically measuring pharyngeal pumping in C. elegans. J Neurosci Methods. 2016;274:172–178.
   PubMed Web of Science ®Google Scholar
• Chow DK, Glenn CF, Johnston JL, et al. Sarcopenia in the Caenorhabditis elegans pharynx correlates with muscle contraction rate over lifespan. Exp Gerontol. 2006;41(3):252–260.
   PubMed Web of Science ®Google Scholar
• Nakagawa H, Shiozaki T, Kobatake E, et al. Effects and mechanisms of prolongevity induced by Lactobacillus gasseri SBT2055 in Caenorhabditis elegans. Aging Cell. 2016;15(2):227–236.
   PubMed Web of Science ®Google Scholar
• Sun T, Zhang J, Zhao Y. Lacticaseibacillus rhamnosus Probio-M9 extends the lifespan of Caenorhabditis elegans. Communications Bio. 2022;5(1):1–16.
   Google Scholar
• Dinic M, Herholz M, Kačarevic U, et al. Host–commensal interaction promotes health and lifespan in Caenorhabditis elegans through the activation of HLH-30/TFEB-mediated autophagy. Aging. 2021;13(6):8040–8054.
   PubMedGoogle Scholar
• Jo Aan G, Shahril Aszrin Zainudin M, Abdul Karim N, et al. Effect of the tocotrienol-rich fraction on the lifespan and oxidative biomarkers in Caenorhabditis elegans under oxidative stress. Clinics. 2013;68:599–604.
   Google Scholar
• Büchter C, Ackermann D, Havermann S, et al. Myricetin-mediated lifespan extension in Caenorhabditis elegans is modulated by DAF-16. Int J Mol Sci. 2013;14(6):11895–11914.
   PubMed Web of Science ®Google Scholar
• Desaka N, Ota C, Nishikawa H, et al. Streptococcus thermophilus extends lifespan through activation of DAF-16-mediated antioxidant pathway in Caenorhabditis elegans. J Clin Biochem Nutr. 2022;70(1):7–13.
   PubMed Web of Science ®Google Scholar
• Qin X, Wang W, Chu W. Antioxidant and reducing lipid accumulation effects of rutin in Caenorhabditis elegans. Biofactors. 2021;47(4):686–693.
   PubMed Web of Science ®Google Scholar
• Liu YJ, Gao AW, Smith RL, et al. Reduced ech-6 expression attenuates fat-induced lifespan shortening in C. elegans. Sci Rep. 2022;12(1):1–18.
   PubMed Web of Science ®Google Scholar
• Glenn CF, Chow DK, David L, et al. Behavioral deficits during early stages of aging in Caenorhabditis elegans result from locomotory deficits possibly linked to muscle frailty. J Gerontol A Biol Sci Med Sci. 2004;59(12):1251–1260.
   PubMed Web of Science ®Google Scholar
• Bolanowski MA, Russell RL, Jacobson LA. Quantitative measures of aging in the nematode Caenorhabditis elegans. I. Population and longitudinal studies of two behavioral parameters. Mech Ageing Dev. 1981;15(3):279–295.
   PubMed Web of Science ®Google Scholar
• Hahm JH, Kim S, Diloreto R, et al. C. elegans maximum velocity correlates with healthspan and is maintained in worms with an insulin receptor mutation. Nat Commun. 2015;6(1):1–7.
   Google Scholar
• Ayuda-Durán B, González-Manzano S, Miranda-Vizuete A, et al. Exploring target genes involved in the effect of quercetin on the response to oxidative stress in Caenorhabditis elegans. Antioxidants. 2019;8(12):585.
   Google Scholar
• Ma J, Xu X, Wang R, et al. Lipopolysaccharide exposure induces oxidative damage in Caenorhabditis elegans: protective effect of carnosine. Pharmacology and Toxicology. 2020;21(1):1–9.
   Google Scholar