Holdemanella biformis improves glucose tolerance and regulates GLP-1 signaling in obese mice.
Animals
Blood Glucose
/ metabolism
Diabetes Mellitus, Type 2
/ metabolism
Disease Models, Animal
Firmicutes
/ physiology
Glucagon-Like Peptide 1
/ metabolism
Gluconeogenesis
/ physiology
Glucose
/ metabolism
Glucose Tolerance Test
/ methods
Hyperglycemia
/ metabolism
Insulin
/ metabolism
Mice
Mice, Inbred C57BL
Mice, Obese
/ metabolism
Obesity
/ metabolism
Holdemanella biformis
glucagon-like peptide 1
gut microbiota
obesity
type 2 diabetes
vagal afferent neurons
Journal
FASEB journal : official publication of the Federation of American Societies for Experimental Biology
ISSN: 1530-6860
Titre abrégé: FASEB J
Pays: United States
ID NLM: 8804484
Informations de publication
Date de publication:
07 2021
07 2021
Historique:
revised:
04
05
2021
received:
25
01
2021
accepted:
01
06
2021
entrez:
18
6
2021
pubmed:
19
6
2021
medline:
17
7
2021
Statut:
ppublish
Résumé
Impaired glucose homeostasis in obesity is mitigated by enhancing the glucoregulatory actions of glucagon-like peptide 1 (GLP-1), and thus, strategies that improve GLP-1 sensitivity and secretion have therapeutic potential for the treatment of type 2 diabetes. This study shows that Holdemanella biformis, isolated from the feces of a metabolically healthy volunteer, ameliorates hyperglycemia, improves oral glucose tolerance and restores gluconeogenesis and insulin signaling in the liver of obese mice. These effects were associated with the ability of H. biformis to restore GLP-1 levels, enhancing GLP-1 neural signaling in the proximal and distal small intestine and GLP-1 sensitivity of vagal sensory neurons, and to modify the cecal abundance of unsaturated fatty acids and the bacterial species associated with metabolic health. Our findings overall suggest the potential use of H biformis in the management of type 2 diabetes in obesity to optimize the sensitivity and function of the GLP-1 system, through direct and indirect mechanisms.
Identifiants
pubmed: 34143451
doi: 10.1096/fj.202100126R
doi:
Substances chimiques
Blood Glucose
0
Insulin
0
Glucagon-Like Peptide 1
89750-14-1
Glucose
IY9XDZ35W2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e21734Informations de copyright
© 2021 The Authors. The FASEB Journal published by Wiley Periodicals LLC on behalf of Federation of American Societies for Experimental Biology.
Références
Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444:1022-1023.
Turnbaugh PJ, Hamady M, Yatsunenko T, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457:480-484.
Ridaura VK, Faith JJ, Rey FE, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science. 2013;341:1241214.
Carmody RN, Gerber GK, Luevano JM, et al. Diet dominates host genotype in shaping the murine gut microbiota. Cell Host Microbe. 2015;17:72-84.
David LA, Maurice CF, Carmody RN, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505:559-563.
Fung TC, Olson CA, Hsiao EY. Interactions between the microbiota, immune and nervous systems in health and disease. Nat Neurosci. 2017;20:145-155.
Martin CR, Osadchiy V, Kalani A, Mayer EA. The brain-gut-microbiome axis. Cell Mol Gastroenterol Hepatol. 2018;6:133-148.
Christ A, Lauterbach M, Latz E. Western diet and the immune system: an inflammatory connection. Immunity. 2019;51:794-811.
Garidou L, Pomié C, Klopp P, et al. The gut microbiota regulates intestinal CD4 T cells expressing RORγt and controls metabolic disease. Cell Metab. 2015;22:100-112.
Grasset E, Puel A, Charpentier J, et al. A specific gut microbiota dysbiosis of Type 2 diabetic mice induces GLP-1 resistance through an enteric NO-dependent and gut-brain axis mechanism. Cell Metab. 2017;25:1075-1090.e5.
Wollam J, Riopel M, Xu Y-J, et al. Microbiota-produced N-formyl peptide fMLF promotes obesity-induced glucose intolerance. Diabetes. 2019;68:1415-1426.
Drucker DJ. Mechanisms of action and therapeutic application of glucagon-like peptide-1. Cell Metab. 2018;27:740-756.
Krieger J-P, Arnold M, Pettersen KG, Lossel P, Langhans W, Lee SJ. Knockdown of GLP-1 receptors in vagal afferents affects normal food intake and glycemia. Diabetes. 2016;65:34-43.
Sandoval DA, Bagnol D, Woods SC, D’Alessio DA, Seeley RJ. Arcuate glucagon-like peptide 1 receptors regulate glucose homeostasis but not food intake. Diabetes. 2008;57:2046-2054.
Breton J, Tennoune N, Lucas N, et al. Gut commensal E coli proteins activate host satiety pathways following nutrient-induced bacterial growth. Cell Metab. 2016;23:324-334.
Chimerel C, Emery E, Summers DK, Keyser U, Gribble FM, Reimann F. Bacterial metabolite indole modulates incretin secretion from intestinal enteroendocrine L cells. Cell Rep. 2014;9:1202-1208.
Natividad JM, Agus A, Planchais J, et al. Impaired aryl hydrocarbon receptor ligand production by the gut microbiota is a key factor in metabolic syndrome. Cell Metab. 2018;28:737-749.e4.
Claus SP. Will gut microbiota help design the next generation of GLP-1-based therapies for Type 2 diabetes? Cell Metab. 2017;26:6-7.
O’Toole PW, Paoli M. The contribution of microbial biotechnology to sustainable development goals: microbiome therapies. Microb Biotechnol. 2017;10:1066-1069.
Romaní-Pérez M, Agusti A, Sanz Y. Innovation in microbiome-based strategies for promoting metabolic health. Curr Opin Clin Nutr Metab Care. 2017;20:484-491.
Tsai Y-L, Lin T-L, Chang C-J, et al. Probiotics, prebiotics and amelioration of diseases. J Biomed Sci. 2019;26:3.
Depommier C, Everard A, Druart C, et al. Supplementation with Akkermansia muciniphila in overweight and obese human volunteers: a proof-of-concept exploratory study. Nat Med. 2019;25:1096-1103.
Everard A, Belzer C, Geurts L, et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci USA. 2013;110:9066-9071.
Gauffin Cano P, Santacruz A, Moya Á, Sanz Y. Bacteroides uniformis CECT 7771 ameliorates metabolic and immunological dysfunction in mice with high-fat-diet induced obesity. PLoS One. 2012;7:e41079.
Plovier H, Everard A, Druart C, et al. A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice. Nat Med. 2017;23:107-113.
Rastelli M, Cani PD, Knauf C. The gut microbiome influences host endocrine functions. Endocr Rev. 2019;40:1271-1284.
Modasia A, Parker A, Jones E, et al. Regulation of enteroendocrine cell networks by the major human gut symbiont Bacteroides thetaiotaomicron. Front Microbiol. 2020;11. https://doi.org/10.3389/fmicb.2020.575595
Collins MD, Lawson PA, Willems A, et al. The phylogeny of the genus clostridium: proposal of five new genera and eleven new species combinations. Int J Syst Evol Microbiol. 1994;44:812-826.
De Maesschalck C, Van Immerseel F, Eeckhaut V, et al. 1977), Eubacterium biforme (Eggerth 1935) and Eubacterium cylindroides (Cato et al. 1974) as Faecalicoccus pleomorphus comb. nov., Holdemanella biformis gen. nov., comb. nov. and Faecalitalea cylindroides gen. nov., comb. nov., respectively, within the family Erysipelotrichaceae. Int J Syst Evol Microbiol. 2014;64:3877-3884.
Zagato E, Pozzi C, Bertocchi A, et al. Endogenous murine microbiota member Faecalibaculum rodentium and its human homologue protect from intestinal tumour growth. Nat Microbiol. 2020;5:511-524.
Pujo J, Petitfils C, Faouder PL, et al. Bacteria-derived long chain fatty acid exhibits anti-inflammatory properties in colitis. Gut. 2021;70(6):1088-1097. https://doi.org/10.1136/gutjnl-2020-321173
Tolhurst G, Heffron H, Lam YS, et al. Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2. Diabetes. 2012;61:364-371.
Hirasawa A, Tsumaya K, Awaji T, et al. Free fatty acids regulate gut incretin glucagon-like peptide-1 secretion through GPR120. Nat Med. 2005;11:90-94.
Liebisch G, Ecker J, Roth S, et al. Quantification of fecal short chain fatty acids by liquid chromatography tandem mass spectrometry-investigation of pre-analytic stability. Biomolecules. 2019;9(4):121. https://doi.org/10.3390/biom9040121
Ecker J, Scherer M, Schmitz G, Liebisch G. A rapid GC-MS method for quantification of positional and geometric isomers of fatty acid methyl esters. J Chromatogr B Analyt Technol Biomed Life Sci. 2012;897:98-104.
Klindworth A, Pruesse E, Schweer T, et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 2013;41:e1.
Magoč T, Salzberg SL. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinforma Oxf Engl. 2011;27:2957-2963.
Caporaso JG, Kuczynski J, Stombaugh J, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335-336.
Schloss PD, Westcott SL, Ryabin T, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75:7537-7541.
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinforma Oxf Engl. 2011;27:2194-2200.
Quast C, Pruesse E, Yilmaz P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590-596.
Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinforma Oxf Engl. 2010;26:2460-2461.
Pruesse E, Peplies J, Glöckner FO. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinforma Oxf Engl. 2012;28:1823-1829.
Price MN, Dehal PS, Arkin AP. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol. 2009;26:1641-1650.
Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 2019;47:W256-W259.
Cadaveira-Mosquera A, Pérez M, Reboreda A, Rivas-Ramírez P, Fernández-Fernández D, Lamas JA. Expression of K2P channels in sensory and motor neurons of the autonomic nervous system. J Mol Neurosci MN. 2012;48:86-96.
Segata N, Izard J, Waldron L, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:R60.
Yang M, Wang J, Wu S, et al. Duodenal GLP-1 signaling regulates hepatic glucose production through a PKC-δ-dependent neurocircuitry. Cell Death Dis. 2017;8:e2609.
Lewis JE, Miedzybrodzka EL, Foreman RE, et al. Selective stimulation of colonic L cells improves metabolic outcomes in mice. Diabetologia. 2020;63:1396-1407.
Brubaker PL. Glucagon-like peptide-2 and the regulation of intestinal growth and function. Compr Physiol. 2018;8:1185-1210.
Iakoubov R, Ahmed A, Lauffer LM, Bazinet RP, Brubaker PL. Essential role for protein kinase Cζ in oleic acid-induced glucagon-like peptide-1 secretion in vivo in the rat. Endocrinology. 2011;152:1244-1252.
Rocca AS, LaGreca J, Kalitsky J, Brubaker PL. Monounsaturated fatty acid diets improve glycemic tolerance through increased secretion of glucagon-like peptide-1. Endocrinology. 2001;142:1148-1155.
Duca FA, Sakar Y, Covasa M. The modulatory role of high fat feeding on gastrointestinal signals in obesity. J Nutr Biochem. 2013;24:1663-1677.
Boets E, Gomand SV, Deroover L, et al. Systemic availability and metabolism of colonic-derived short-chain fatty acids in healthy subjects: a stable isotope study. J Physiol. 2017;595:541-555.
Lauffer LM, Iakoubov R, Brubaker PL. GPR119 is essential for oleoylethanolamide-induced glucagon-like peptide-1 secretion from the intestinal enteroendocrine L-cell. Diabetes. 2009;58:1058-1066.
Cheng Y-H, Ho M-S, Huang W-T, Chou Y-T, King K. Modulation of glucagon-like peptide-1 (GLP-1) potency by endocannabinoid-like lipids represents a novel mode of regulating GLP-1 receptor signaling. J Biol Chem. 2015;290:14302-14313.
Cani PD, Possemiers S, Van de Wiele T, et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut. 2009;58:1091-1103.
Duca FA, Waise TMZ, Peppler WT, Lam TKT. The metabolic impact of small intestinal nutrient sensing. Nat Commun. 2021;12:903.
Bauer PV, Duca FA, Waise TMZ, et al. Lactobacillus gasseri in the upper small intestine impacts an ACSL3-dependent fatty acid-sensing pathway regulating whole-body glucose homeostasis. Cell Metab. 2018;27:572-587.e6.
Sandoval D, Sisley SR. Brain GLP-1 and insulin sensitivity. Mol Cell Endocrinol. 2015;418(Pt 1):27-32.