Energy-dense diet triggers changes in gut microbiota, reorganization of gut-brain vagal communication and increases body fat accumulation

Alexandra C. Vaughn, Erin M. Cooper, Patricia M. Dilorenzo, Levi J. O’Loughlin, Michael E. Konkel, James H. Peters, Andras Hajnal, Tanusree Sen, Sun Hye Lee, Claire B. de La Serre, Krzysztof Czaja

Research output: Contribution to journalArticle

56 Scopus citations

Abstract

Obesity is associated with consumption of energy-dense diets and development of systemic inflammation. Gut microbiota play a role in energy harvest and inflammation and can influence the change from lean to obese phenotypes. The nucleus of the solitary tract (NTS) is a brain target for gastrointestinal signals modulating satiety and alterations in gut-brain vagal pathway may promote overeating and obesity. Therefore, we tested the hypothesis that high-fat diet-induced changes in gut microbiota alter vagal gut-brain communication associated with increased body fat accumulation. Sprague-Dawley rats consumed a low energy-dense rodent diet (LFD; 3.1 kcal/g) or high energy-dense diet (HFD, 5.24 kcal/g). Minocycline was used to manipulate gut microbiota composition. 16S Sequencing was used to determine microbiota composition. Immunofluorescence against IB4 and Iba1 was used to determine NTS reorganization and microglia activation. Nodose ganglia from LFD rats were isolated and co-cultured with different bacteria strains to determine neurotoxicity. HFD altered gut microbiota with increases in Firmicutes/Bacteriodetes ratio and in pro-inflammatory Proteobacteria proliferation. HFD triggered reorganization of vagal afferents and microglia activation in the NTS, associated with weight gain. Minocycline-treated HFD rats exhibited microbiota profile comparable to LFD animals. Minocycline suppressed HFD-induced reorganization of vagal afferents and microglia activation in the NTS, and reduced body fat accumulation. Proteobacteria isolated from cecum of HFD rats were toxic to vagal afferent neurons in culture. Our findings show that diet-induced shift in gut microbiome may disrupt vagal gut-brain communication resulting in microglia activation and increased body fat accumulation.

Original languageEnglish (US)
Pages (from-to)18-30
Number of pages13
JournalActa neurobiologiae experimentalis
Volume77
Issue number1
DOIs
StatePublished - 2017

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)

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    Vaughn, A. C., Cooper, E. M., Dilorenzo, P. M., O’Loughlin, L. J., Konkel, M. E., Peters, J. H., Hajnal, A., Sen, T., Lee, S. H., de La Serre, C. B., & Czaja, K. (2017). Energy-dense diet triggers changes in gut microbiota, reorganization of gut-brain vagal communication and increases body fat accumulation. Acta neurobiologiae experimentalis, 77(1), 18-30. https://doi.org/10.21307/ane-2017-033