Home»
Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia.
Accès à distance ? S'identifier sur le proxy UCLouvain
Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia.
AIMS/HYPOTHESIS: Recent evidence suggests that a particular gut microbial community may favour occurrence of the metabolic diseases. Recently, we reported that high-fat (HF) feeding was associated with higher endotoxaemia and lower Bifidobacterium species (spp.) caecal content in mice. We therefore tested whether restoration of the quantity of caecal Bifidobacterium spp. could modulate metabolic endotoxaemia, the inflammatory tone and the development of diabetes. METHODS: Since bifidobacteria have been reported to reduce intestinal endotoxin levels and improve mucosal barrier function, we specifically increased the gut bifidobacterial content of HF-diet-fed mice through the use of a prebiotic (oligofructose [OFS]). RESULTS: Compared with normal chow-fed control mice, HF feeding significantly reduced intestinal Gram-negative and Gram-positive bacteria including levels of bifidobacteria, a dominant member of the intestinal microbiota, which is seen as physiologically positive. As expected, HF-OFS-fed mice had totally restored quantities of bifidobacteria. HF-feeding significantly increased endotoxaemia, which was normalised to control levels in HF-OFS-treated mice. Multiple-correlation analyses showed that endotoxaemia significantly and negatively correlated with Bifidobacterium spp., but no relationship was seen between endotoxaemia and any other bacterial group. Finally, in HF-OFS-treated-mice, Bifidobacterium spp. significantly and positively correlated with improved glucose tolerance, glucose-induced insulin secretion and normalised inflammatory tone (decreased endotoxaemia, plasma and adipose tissue proinflammatory cytokines). CONCLUSIONS/INTERPRETATION: Together, these findings suggest that the gut microbiota contribute towards the pathophysiological regulation of endotoxaemia and set the tone of inflammation for occurrence of diabetes and/or obesity. Thus, it would be useful to develop specific strategies for modifying gut microbiota in favour of bifidobacteria to prevent the deleterious effect of HF-diet-induced metabolic diseases.
Hotamisligil GS, Shargill NS, Spiegelman BM (1993) Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 259:87–91
Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW, Jr (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112:1796–1808
Hotamisligil GS, Peraldi P, Budavari A, Ellis R, White MF, Spiegelman BM (1996) IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha- and obesity-induced insulin resistance. Science 271:665–668
Plomgaard P, Bouzakri K, Krogh-Madsen R, Mittendorfer B, Zierath JR, Pedersen BK (2005) Tumor necrosis factor-alpha induces skeletal muscle insulin resistance in healthy human subjects via inhibition of Akt substrate 160 phosphorylation. Diabetes 54:2939–2945
Backhed F, Ding H, Wang T et al (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 101:15718–15723
Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI (2005) Host–bacterial mutualism in the human intestine. Science 307:1915–1920
Backhed F, Manchester JK, Semenkovich CF, Gordon JI (2007) Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc Natl Acad Sci USA 104:979–984
Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci USA 102:11070–11075
Ley RE, Turnbaugh PJ, Klein S, Gordon JI (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444:1022–1023
Cani PD, Amar J, Iglesias MA et al (2007) Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56:1761–1772
Griffiths EA, Duffy LC, Schanbacher FL et al (2004) In vivo effects of bifidobacteria and lactoferrin on gut endotoxin concentration and mucosal immunity in Balb/c mice. Dig Dis Sci 49:579–589
Wang Z, Xiao G, Yao Y, Guo S, Lu K, Sheng Z (2006) The role of bifidobacteria in gut barrier function after thermal injury in rats. J Trauma 61:650–657
Wang Zhong-Tang, Risk factors of development of gut-derived bacterial translocation in thermally injured rats, 10.3748/wjg.v10.i11.1619
Tuohy KM, Rouzaud GC, Bruck WM, Gibson GR (2005) Modulation of the human gut microflora towards improved health using prebiotics—assessment of efficacy. Curr Pharm Des 11:75–90
Cani PD, Dewever C, Delzenne NM (2004) Inulin-type fructans modulate gastrointestinal peptides involved in appetite regulation (glucagon-like peptide-1 and ghrelin) in rats. Br J Nutr 92:521–526
Cani PD, Knauf C, Iglesias MA, Drucker DJ, Delzenne NM, Burcelin R (2006) Improvement of glucose tolerance and hepatic insulin sensitivity by oligofructose requires a functional glucagon-like peptide 1 receptor. Diabetes 55:1484–1490
Franks AH, Harmsen HJ, Raangs GC, Jansen GJ, Schut F, Welling GW (1998) Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes. Appl Environ Microbiol 64:3336–3345
Harmsen HJ, Wildeboer-Veloo AC, Raangs GC et al (2000) Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J Pediatr Gastroenterol Nutr 30:61–67
Langendijk PS, Schut F, Jansen GJ et al (1995) Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in fecal samples. Appl Environ Microbiol 61:3069–3075
Manz W, Amann R, Ludwig W, Vancanneyt M, Schleifer KH (1996) Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum cytophaga–flavobacter–bacteroides in the natural environment. Microbiology 142:1097–1106
Salzman Nita H., Bos Nicolaas A., Paterson Yvonne, de Jong Hendrik, Welling Gjalt W., Harmsen Hermie J. M., Analysis of 16S libraries of mouse gastrointestinal microflora reveals a large new group of mouse intestinal bacteria b, 10.1099/00221287-148-11-3651
Devereux R, Mundfrom GW (1994) A phylogenetic tree of 16S rRNA sequences from sulfate-reducing bacteria in a sandy marine sediment. Appl Environ Microbiol 60:3437–3439
Ootsubo M, Shimizu T, Tanaka R et al (2002) Oligonucleotide probe for detecting Enterobacteriaceae by in situ hybridization. J Appl Microbiol 93:60–68
Knauf C, Rieusset J, Foretz M et al (2006) Peroxisome proliferator-activated receptor-alpha-null mice have increased white adipose tissue glucose utilization, GLUT4, and fat mass: role in liver and brain. Endocrinology 147:4067–4078
Cani PD, Neyrinck AM, Maton N, Delzenne NM (2005) Oligofructose promotes satiety in rats fed a high-fat diet: involvement of glucagon-like peptide-1. Obes Res 13:1000–1007
Cani PD, Daubioul CA, Reusens B, Remacle C, Catillon G, Delzenne NM (2005) Involvement of endogenous glucagon-like peptide-1(7-36) amide on glycaemia-lowering effect of oligofructose in streptozotocin-treated rats. J Endocrinol 185:457–465
Cani PD, Hoste S, Guiot Y, Delzenne NM (2007) Dietary non-digestible carbohydrates promote L-cell differentiation in the proximal colon of rats. Br J Nutr 98:32–37
Brun P, Castagliuolo I, Leo VD et al (2007) Increased intestinal permeability in obese mice: new evidence in the pathogenesis of nonalcoholic steatohepatitis. Am J Physiol Gastrointest Liver Physiol 292:G518–G525
Caplan MS, Miller-Catchpole R, Kaup S et al (1999) Bifidobacterial supplementation reduces the incidence of necrotizing enterocolitis in a neonatal rat model. Gastroenterology 117:577–583
Commane DM, Shortt CT, Silvi S, Cresci A, Hughes RM, Rowland IR (2005) Effects of fermentation products of pro- and prebiotics on trans-epithelial electrical resistance in an in vitro model of the colon. Nutr Cancer 51:102–109
Spindler-Vesel A, Bengmark S, Vovk I, Cerovic O, Kompan L (2007) Synbiotics, prebiotics, glutamine, or peptide in early enteral nutrition: a randomized study in trauma patients. JPEN J Parenter Enteral Nutr 31:119–126
Guarner F (2005) Inulin and oligofructose: impact on intestinal diseases and disorders. Br J Nutr 93(Suppl 1):S61–S65
Mariadason JM, Barkla DH, Gibson PR (1997) Effect of short-chain fatty acids on paracellular permeability in Caco-2 intestinal epithelium model. Am J Physiol 272:G705–G712
Brugman S, Klatter FA, Visser JT et al (2006) Antibiotic treatment partially protects against type 1 diabetes in the Bio-Breeding diabetes-prone rat. Is the gut flora involved in the development of type 1 diabetes? Diabetologia 49:2105–2108
Gibson GR, Willems A, Reading S, Collins MD (1996) Fermentation of non-digestible oligosaccharides by human colonic bacteria. Proc Nutr Soc 55:899–912
Gibson GR (1998) Dietary modulation of the human gut microflora using prebiotics. Br J Nutr 80:S209–S212
Gibson GR (1999) Dietary modulation of the human gut microflora using the prebiotics oligofructose and inulin. J Nutr 129:1438S–1441S
Gibson GR, Roberfroid MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125:1401–1412
Scholz-Ahrens KE, Ade P, Marten B et al (2007) Prebiotics, probiotics, and synbiotics affect mineral absorption, bone mineral content, and bone structure. J Nutr 137:838S–846S
Cani PD, Joly E, Horsmans Y, Delzenne NM (2006) Oligofructose promotes satiety in healthy human: a pilot study. Eur J Clin Nutr 60:567–572
Daubioul CA, Horsmans Y, Lambert P, Danse E, Delzenne NM (2005) Effects of oligofructose on glucose and lipid metabolism in patients with nonalcoholic steatohepatitis: results of a pilot study. Eur J Clin Nutr 59:723–726
Letexier D, Diraison F, Beylot M (2003) Addition of inulin to a moderately high-carbohydrate diet reduces hepatic lipogenesis and plasma triacylglycerol concentrations in humans. Am J Clin Nutr 77:559–564
Bibliographic reference
Cani, Patrice D. ; Neyrinck, Audrey M. ; Fava, F ; Knauf, Claude ; Burcelin, Rémy G. ; et. al. Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia.. In: Diabetologia : clinical and experimental diabetes and metabolism, Vol. 50, no. 11, p. 2374-2383 (2007)