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The Intestinal Microbiota in Metabolic Disease

Anni Woting, Michael Blaut

Nutrients · 2016 · Review · CC BY

doi:10.3390/nu8040202

Abstract

Gut bacteria exert beneficial and harmful effects in metabolic diseases as deduced from the comparison of germfree and conventional mice and from fecal transplantation studies. Compositional microbial changes in diseased subjects have been linked to adiposity, type 2 diabetes and dyslipidemia. Promotion of an increased expression of intestinal nutrient transporters or a modified lipid and bile acid metabolism by the intestinal microbiota could result in an increased nutrient absorption by the host. The degradation of dietary fiber and the subsequent fermentation of monosaccharides to short-chain fatty acids (SCFA) is one of the most controversially discussed mechanisms of how gut bacteria impact host physiology. Fibers reduce the energy density of the diet, and the resulting SCFA promote intestinal gluconeogenesis, incretin formation and subsequently satiety. However, SCFA also deliver energy to the host and support liponeogenesis. Thus far, there is little knowledge on bacterial species that promote or prevent metabolic disease. Clostridium ramosum and Enterococcus cloacae were demonstrated to promote obesity in gnotobiotic mouse models, whereas bifidobacteria and Akkermansia muciniphila were associated with favorable phenotypes in conventional mice, especially when oligofructose was fed. How diet modulates the gut microbiota towards a beneficial or harmful composition needs further research. Gnotobiotic animals are a valuable tool to elucidate mechanisms underlying diet–host–microbe interactions.

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    Amar J., Burcelin R., Ruidavets J.B., Cani P.D., Fauvel J., Alessi M.C., Chamontin B., Ferrieres J. Energy intake is associated with endotoxemia in apparently healthy men. Am. J. Clin. Nutr. 2008;87:1219-1223.

    Not in our library10.1093/ajcn/87.5.1219

  88. 88.

    Kitchens R.L., Thompson P.A. Modulatory effects of sCD14 and LBP on LPS-host cell interactions. J. Endotoxin Res. 2005;11:225-229.

    Not in our library10.1177/09680519050110040701

  89. 89.

    Hersoug L.G., Moller P., Loft S. Gut microbiota-derived lipopolysaccharide uptake and trafficking to adipose tissue: Implications for inflammation and obesity. Obes. Rev. 2016;17:297-312.

    Not in our library10.1111/obr.12370

  90. 90.
    High Fat Diet-Induced Gut Microbiota Exacerbates Inflammation and Obesity in Mice via the TLR4 Signaling Pathway · 2012
    No notice
  91. 91.

    Liu J., Batkai S., Pacher P., Harvey-White J., Wagner J.A., Cravatt B.F., Gao B., Kunos G. Lipopolysaccharide induces anandamide synthesis in macrophages via CD14/MAPK/phosphoinositide 3-kinase/NF-kappaB independently of platelet-activating factor. J. Biol. Chem. 2003;278:45034-45039.

    Not in our library10.1074/jbc.m306062200

  92. 92.

    Muccioli G.G., Naslain D., Backhed F., Reigstad C.S., Lambert D.M., Delzenne N.M., Cani P.D. The endocannabinoid system links gut microbiota to adipogenesis. Mol. Syst. Biol. 2010;6:392.

    Not in our library10.1038/msb.2010.46

  93. 93.

    Kless C., Muller V.M., Schuppel V.L., Lichtenegger M., Rychlik M., Daniel H., Klingenspor M., Haller D. Diet-induced obesity causes metabolic impairment independent of alterations in gut barrier integrity. Mol. Nutr. Food Res. 2015;59:968-978.

    Not in our library10.1002/mnfr.201400840

  94. 94.

    Johnson R.J., Rivard C., Lanaspa M.A., Otabachian-Smith S., Ishimoto T., Cicerchi C., Cheeke P.R., Macintosh B., Hess T. Fructokinase, fructans, intestinal permeability, and metabolic syndrome: An equine connection? J. Equine Vet. Sci. 2013;33:120-126.

    Not in our library10.1016/j.jevs.2012.05.004

  95. 95.

    Ferrer M., Ruiz A., Lanza F., Haange S.B., Oberbach A., Till H., Bargiela R., Campoy C., Segura M.T., Richter M., et al. Microbiota from the distal guts of lean and obese adolescents exhibit partial functional redundancy besides clear differences in community structure. Environ. Microbiol. 2013;15:211-226.

    Not in our library10.1111/j.1462-2920.2012.02845.x

  96. 96.

    Karlsson F.H., Tremaroli V., Nookaew I., Bergstrom G., Behre C.J., Fagerberg B., Nielsen J., Backhed F. Gut metagenome in european women with normal, impaired and diabetic glucose control. Nature. 2013;498:99-103.

    Not in our library10.1038/nature12198

  97. 97.

    Le Chatelier E., Nielsen T., Qin J., Prifti E., Hildebrand F., Falony G., Almeida M., Arumugam M., Batto J.M., Kennedy S., et al. Richness of human gut microbiome correlates with metabolic markers. Nature. 2013;500:541-546.

    Not in our library10.1038/nature12506

  98. 98.

    Fei N., Zhao L. An opportunistic pathogen isolated from the gut of an obese human causes obesity in germfree mice. ISME J. 2013;7:880-884.

    Not in our library10.1038/ismej.2012.153

  99. 99.

    Faith J.J., Ahern P.P., Ridaura V.K., Cheng J., Gordon J.I. Identifying gut microbe-host phenotype relationships using combinatorial communities in gnotobiotic mice. Sci. Transl. Med. 2014;6:220ra211.

    Not in our library10.1126/scitranslmed.3008051

  100. 100.

    Everard A., Belzer C., Geurts L., Ouwerkerk J.P., Druart C., Bindels L.B., Guiot Y., Derrien M., Muccioli G.G., Delzenne N.M., et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc. Natl. Acad. Sci. USA. 2013;110:9066-9071.

    Not in our library10.1073/pnas.1219451110

  101. 101.

    Roopchand D.E., Carmody R.N., Kuhn P., Moskal K., Rojas-Silva P., Turnbaugh P.J., Raskin I. Dietary polyphenols promote growth of the gut bacterium Akkermansia muciniphila and attenuate high fat diet-induced metabolic syndrome. Diabetes. 2015;64:2847-2858.

    Not in our library10.2337/db14-1916

  102. 102.

    Dao M.C., Everard A., Aron-Wisnewsky J., Sokolovska N., Prifti E., Verger E.O., Kayser B.D., Levenez F., Chilloux J., Hoyles L., et al. Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: Relationship with gut microbiome richness and ecology. Gut. 2016;65:426-436.

    Not in our library10.1136/gutjnl-2014-308778

  103. 103.

    Shin N.R., Lee J.C., Lee H.Y., Kim M.S., Whon T.W., Lee M.S., Bae J.W. An increase in the Akkermansia spp. Population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice. Gut. 2014;63:727-735.

    Not in our library10.1136/gutjnl-2012-303839

  104. 104.

    Behnsen J., Deriu E., Sassone-Corsi M., Raffatellu M. Probiotics: Properties, examples, and specific applications. Cold Spring Harb. Perspect. Med. 2013;3:a010074.

    Not in our library10.1101/cshperspect.a010074

  105. 105.

    Million M., Angelakis E., Paul M., Armougom F., Leibovici L., Raoult D. Comparative meta-analysis of the effect of lactobacillus species on weight gain in humans and animals. Microb. Pathog. 2012;53:100-108.

    Not in our library10.1016/j.micpath.2012.05.007

  106. 106.
    Supplementation of Lactobacillus curvatus HY7601 and Lactobacillus plantarum KY1032 in Diet-Induced Obese Mice Is Associated with Gut Microbial Changes and Reduction in Obesity · 2013
    No notice
  107. 107.

    Wu C.C., Weng W.L., Lai W.L., Tsai H.P., Liu W.H., Lee M.H., Tsai Y.C. Effect of Lactobacillus plantarum strain K21 on high-fat diet-fed obese mice. Evid. Based Complement. Altern. Med. 2015;2015:391767.

    Not in our library10.1155/2015/391767

  108. 108.

    Kadooka Y., Sato M., Ogawa A., Miyoshi M., Uenishi H., Ogawa H., Ikuyama K., Kagoshima M., Tsuchida T. Effect of Lactobacillus gasseri SBT2055 in fermented milk on abdominal adiposity in adults in a randomised controlled trial. Br. J. Nutr. 2013;110:1696-1703.

    Not in our library10.1017/s0007114513001037

  109. 109.

    Collado M.C., Isolauri E., Laitinen K., Salminen S. Distinct composition of gut microbiota during pregnancy in overweight and normal-weight women. Am. J. Clin. Nutr. 2008;88:894-899.

    Not in our library10.1093/ajcn/88.4.894

  110. 110.

    Kalliomaki M., Collado M.C., Salminen S., Isolauri E. Early differences in fecal microbiota composition in children may predict overweight. Am. J. Clin. Nutr. 2008;87:534-538.

    Not in our library10.1093/ajcn/87.3.534

  111. 111.

    Wu X., Ma C., Han L., Nawaz M., Gao F., Zhang X., Yu P., Zhao C., Li L., Zhou A., et al. Molecular characterisation of the faecal microbiota in patients with type II diabetes. Curr. Microbiol. 2010;61:69-78.

    Not in our library10.1007/s00284-010-9582-9

  112. 112.

    Cani P.D., Neyrinck A.M., Fava F., Knauf C., Burcelin R.G., Tuohy K.M., Gibson G.R., Delzenne N.M. Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia. 2007;50:2374-2383.

    Not in our library10.1007/s00125-007-0791-0

  113. 113.

    Cani P.D., Knauf C., Iglesias M.A., Drucker D.J., Delzenne N.M., Burcelin R. Improvement of glucose tolerance and hepatic insulin sensitivity by oligofructose requires a functional glucagon-like peptide 1 receptor. Diabetes. 2006;55:1484-1490.

    Not in our library10.2337/db05-1360

  114. 114.

    Woting A., Pfeiffer N., Hanske L., Loh G., Klaus S., Blaut M. Alleviation of high fat diet-induced obesity by oligofructose in gnotobiotic mice is independent of presence of bifidobacterium longum. Mol. Nutr. Food Res. 2015;59:2267-2278.

    Not in our library10.1002/mnfr.201500249

  115. 115.

    Kondo S., Xiao J.Z., Satoh T., Odamaki T., Takahashi S., Sugahara H., Yaeshima T., Iwatsuki K., Kamei A., Abe K. Antiobesity effects of Bifidobacterium breve strain B-3 supplementation in a mouse model with high-fat diet-induced obesity. Biosci. Biotechnol. Biochem. 2010;74:1656-1661.

    Not in our library10.1271/bbb.100267

  116. 116.

    Stenman L.K., Waget A., Garret C., Klopp P., Burcelin R., Lahtinen S. Potential probiotic Bifidobacterium animalis ssp. lactis 420 prevents weight gain and glucose intolerance in diet-induced obese mice. Benef. Microbes. 2014;5:437-445.

    Not in our library10.3920/bm2014.0014

  117. 117.

    Minami J., Kondo S., Yanagisawa N., Odamaki T., Xiao J.Z., Abe F., Nakajima S., Hamamoto Y., Saitoh S., Shimoda T. Oral administration of Bifidobacterium breve B-3 modifies metabolic functions in adults with obese tendencies in a randomised controlled trial. J. Nutr. Sci. 2015;4:e17.

    Not in our library10.1017/jns.2015.5

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