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Pediococcus acidilactici Promotes the Longevity of C. elegans by Regulating the Insulin/IGF-1 and JNK/MAPK Signaling, Fat Accumulation and Chloride Ion.

ABSTRACT: Probiotics are known to contribute to the anti-oxidation, immunoregulation, and aging delay. Here, we investigated the extension of lifespan by fermented pickles-origin Pediococcus acidilactici (PA) in Caenorhabditis elegans (C. elegans), and found that PA promoted a significantly extended longevity of wild-type C. elegans. The further results revealed that PA regulated the longevity via promoting the insulin/IGF-1 signaling, JNK/MAPK signaling but not TOR signaling in C. elegans, and that PA reduced the reactive oxygen species (ROS) levels and modulated expression of genes involved in fatty acids uptake and lipolysis, thus reducing the fat accumulation in C. elegans. Moreover, this study identified the nrfl-1 as the key regulator of the PA-mediated longevity, and the nrfl-1/daf-18 signaling might be activated. Further, we highlighted the roles of one chloride ion exchanger gene sulp-6 in the survival of C. elegans and other two chloride ion channel genes clh-1 and clh-4 in the prolonged lifespan by PA-feeding through the modulating expression of genes involved in inflammation. Therefore, these findings reveal the detailed and novel molecular mechanisms on the longevity of C. elegans promoted by PA.

SUBMITTER: Hu R

PROVIDER: S-EPMC9010657 | biostudies-literature | 2022

REPOSITORIES: biostudies-literature

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Pediococcus acidilactici Promotes the Longevity of C. elegans by Regulating the Insulin/IGF-1 and JNK/MAPK Signaling, Fat Accumulation and Chloride Ion.

Hu Rui R Zhang Yong Y Qian Weiyi W Leng Yan Y Long Yan Y Liu Xinjie X Li Jinping J Wan Xiangyuan X Wei Xun X

Frontiers in nutrition 20220401

Probiotics are known to contribute to the anti-oxidation, immunoregulation, and aging delay. Here, we investigated the extension of lifespan by fermented pickles-origin Pediococcus acidilactici (PA) in Caenorhabditis elegans (C. elegans), and found that PA promoted a significantly extended longevity of wild-type C. elegans. The further results revealed that PA regulated the longevity via promoting the insulin/IGF-1 signaling, JNK/MAPK signaling but not TOR signaling i ...[more]

PMID: 35433778

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Project description:Aims/hypothesisModulation of gut microbiota has emerged as a promising strategy to treat or prevent the development of different metabolic diseases, including type 2 diabetes and obesity. Previous data from our group suggest that the strain Pediococcus acidilactici CECT9879 (pA1c) could be an effective probiotic for regulating glucose metabolism. Hence, the objectives of this study were to verify the effectiveness of pA1c on glycaemic regulation in diet-induced obese mice and to evaluate whether the combination of pA1c with other normoglycaemic ingredients, such as chromium picolinate (PC) and oat β-glucans (BGC), could increase the efficacy of this probiotic on the regulation of glucose and lipid metabolism.MethodsCaenorhabditis elegans was used as a screening model to describe the potential synbiotic activities, together with the underlying mechanisms of action. In addition, 4-week-old male C57BL/6J mice were fed with a high-fat/high-sucrose diet (HFS) for 6 weeks to induce hyperglycaemia and obesity. Mice were then divided into eight groups (n=12 mice/group) according to dietary supplementation: control-diet group; HFS group; pA1c group (1010 colony-forming units/day); PC; BGC; pA1c+PC+BGC; pA1c+PC; and pA1c+BGC. Supplementations were maintained for 10 weeks. Fasting blood glucose was determined and an IPGTT was performed prior to euthanasia. Fat depots, liver and other organs were weighed, and serum biochemical variables were analysed. Gene expression analyses were conducted by real-time quantitative PCR. Sequencing of the V3-V4 region of the 16S rRNA gene from faecal samples of each group was performed, and differential abundance for family, genera and species was analysed by ALDEx2R package.ResultsSupplementation with the synbiotic (pA1c+PC+BGC) counteracted the effect of the high glucose by modulating the insulin-IGF-1 signalling pathway in C. elegans, through the reversal of the glucose nuclear localisation of daf-16. In diet-induced obese mice, all groups supplemented with the probiotic significantly ameliorated glucose tolerance after an IPGTT, demonstrating the glycaemia-regulating effect of pA1c. Further, mice supplemented with pA1c+PC+BGC exhibited lower fasting blood glucose, a reduced proportion of visceral adiposity and a higher proportion of muscle tissue, together with an improvement in the brown adipose tissue in comparison with the HFS group. Besides, the effect of the HFS diet on steatosis and liver damage was normalised by the synbiotic. Gene expression analyses demonstrated that the synbiotic activity was mediated not only by modulation of the insulin-IGF-1 signalling pathway, through the overexpression of GLUT-1 and GLUT-4 mediators, but also by a decreased expression of proinflammatory cytokines such as monocyte chemotactic protein-1. 16S metagenomics demonstrated that the synbiotic combinations allowed an increase in the concentration of P. acidilactici, together with improvements in the intestinal microbiota such as a reduction in Prevotella and an increase in Akkermansia muciniphila.Conclusions/interpretationOur data suggest that the combination of pA1c with PC and BGC could be a potential synbiotic for blood glucose regulation and may help to fight insulin resistance, diabetes and obesity.

Dataset Information

Pediococcus acidilactici Promotes the Longevity of C. elegans by Regulating the Insulin/IGF-1 and JNK/MAPK Signaling, Fat Accumulation and Chloride Ion.

Publications

<i>Pediococcus acidilactici</i> Promotes the Longevity of <i>C. elegans</i> by Regulating the Insulin/IGF-1 and JNK/MAPK Signaling, Fat Accumulation and Chloride Ion.

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