Differences in Anxiety Levels of Various Murine Models in Relation to the Gut Microbiota Composition
Abstract
:1. Introduction
2. Experimental Section
2.1. Bacterial Strains and Culture Conditions
2.2. Animal Experiments
2.3. Elevated Plus Maze Test
2.4. Fecal Microbiota Analysis
2.5. Analysis of Short-Chain Fatty Acids (SCFA) Using Gas Chromatography
2.6. Statistical Analysis
3. Results
3.1. Initial Anxiety and Gut Microbiota Composition of Substrains of C57BL/6 Mice
3.2. Initial Anxiety and Gut Microbiota Composition of Different Species of Mice
3.3. Microbiota Modulation through Probiotics Can Alter the Anxiety Levels, Microbiota Composition and Production of SCFAs
3.4. Microbiota Modulation through an Antibiotic Cocktail Can Alter the Anxiety and Microbiota Composition
3.5. Fecal Microbiota Transplantation Can Reverse the Anxiety and Production of SCFAs
4. Discussion
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
- Gerritsen, J.; Smidt, H.; Rijkers, G.T.; De Vos, W.M. Intestinal microbiota in human health and disease: The impact of probiotics. Genes Nutr. 2011, 6, 209–240. [Google Scholar] [CrossRef]
- Bäckhed, F.; Ley, R.E.; Sonnenburg, J.E.; Peterson, D.A.; Gordon, J.I. Host-bacterial mutualism in the human intestine. Science 2005, 307, 1915–1920. [Google Scholar] [CrossRef] [PubMed]
- Eckburg, P.B.; Bik, E.M.; Bernstein, C.N.; Purdon, E.; Dethlefsen, L.; Sargent, M.; Gill, S.R.; Nelson, K.E.; Relman, D.A. Diversity of the human intestinal microbial flora. Science 2005, 308, 1635–1638. [Google Scholar] [CrossRef] [PubMed]
- Sokol, H.; Pigneur, B.; Watterlot, L.; Lakhdari, O.; Bermudez-Humaran, L.G.; Gratadoux, J.-J.; Blugeon, S.; Bridonneau, C.; Furet, J.-P.; Corthier, G.; et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Nat. Acad. Sci. USA 2008, 105, 16731–16736. [Google Scholar] [CrossRef] [PubMed]
- Willing, B.P.; Dicksved, J.; Halfvarson, J.; Andersson, A.F.; Lucio, M.; Zheng, Z.; Järnerot, G.; Tysk, C.; Jansson, J.K.; Engstrand, L. A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology 2010, 139, 1844.e1–1854.e1. [Google Scholar] [CrossRef] [PubMed]
- Ley, R.E.; Turnbaugh, P.J.; Klein, S.; Gordon, J.I. Microbial ecology: Human gut microbes associated with obesity. Nature 2006, 444, 1022–1023. [Google Scholar] [CrossRef]
- Turnbaugh, P.J.; Ley, R.E.; Mahowald, M.A.; Magrini, V.; Mardis, E.R.; Gordon, J.I. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006, 444, 1027–1031. [Google Scholar] [CrossRef] [PubMed]
- Qin, J.; Li, Y.; Cai, Z.; Li, S.; Zhu, J.; Zhang, F.; Liang, S.; Zhang, W.; Guan, Y.; Shen, D.; et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 2012, 490, 55–60. [Google Scholar] [CrossRef] [PubMed]
- Karlsson, F.H.; Tremaroli, V.; Nookaew, I.; Bergström, G.; Behre, C.J.; Fagerberg, B.; Nielsen, J.; Bäckhed, F. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature 2013, 498, 99–103. [Google Scholar] [CrossRef] [PubMed]
- Wang, T.; Cai, G.; Qiu, Y.; Fei, N.; Zhang, M.; Pang, X.; Jia, W.; Cai, S.; Zhao, L. Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. ISME J. 2011, 6, 320–329. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Foster, J.A.; Rinaman, L.; Cryan, J.F. Stress & the gut-brain axis: Regulation by the microbiome. Neurobiol. Stress 2017, 7, 124–136. [Google Scholar] [PubMed]
- Clapp, M.; Aurora, N.; Herrera, L.; Bhatia, M.; Wilen, E.; Wakefield, S. Gut microbiota’s effect on mental health: The gut-brain axis. Clin. Pract. 2017, 7, 987. [Google Scholar] [CrossRef] [PubMed]
- Lyte, M. Microbial endocrinology: Host-microbiota neuroendocrine interactions influencing brain and behavior. Gut Microbes 2014, 5, 381–389. [Google Scholar] [CrossRef]
- Bourassa, M.W.; Alim, I.; Bultman, S.J.; Ratan, R.R. Butyrate, neuroepigenetics and the gut microbiome: Can a high fiber diet improve brain health? Neurosci. Lett. 2016, 625, 56–63. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ussar, S.; Fujisaka, S.; Kahn, C.R. Interactions between host genetics and gut microbiome in diabetes and metabolic syndrome. Mol. Metab. 2016, 5, 795–803. [Google Scholar] [CrossRef]
- Mekada, K.; Abe, K.; Murakami, A.; Nakamura, S.; Nakata, H.; Moriwaki, K.; Obata, Y.; Yoshiki, A. Genetic differences among C57BL/6 substrains. Exp. Anim. 2009, 58, 141–149. [Google Scholar] [CrossRef]
- Ivanov, I.I.; Atarashi, K.; Manel, N.; Brodie, E.L.; Shima, T.; Karaoz, U.; Wei, D.; Goldfarb, K.C.; Santee, C.A.; Lynch, S.V.; et al. Induction of Intestinal Th17 Cells by Segmented Filamentous Bacteria. Cell 2009, 139, 485–498. [Google Scholar] [CrossRef] [Green Version]
- Reikvam, D.H.; Erofeev, A.; Sandvik, A.; Grcic, V.; Jahnsen, F.L.; Gaustad, P.; McCoy, K.D.; Macpherson, A.J.; Meza-Zepeda, L.A.; Johansen, F.-E. Depletion of Murine Intestinal Microbiota: Effects on Gut Mucosa and Epithelial Gene Expression. PLoS ONE 2011, 6, e17996. [Google Scholar] [CrossRef] [Green Version]
- Seekatz, A.M.; Aas, J.; Gessert, C.E.; Rubin, T.A.; Saman, D.M.; Bakken, J.S.; Young, V.B. Recovery of the Gut Microbiome following Fecal Microbiota Transplantation. mBio 2014, 5, e00893-14. [Google Scholar] [CrossRef]
- Walf, A.A.; Frye, C.A. The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat. Protoc. 2007, 2, 322–328. [Google Scholar] [CrossRef] [Green Version]
- Bergström, A.; Licht, T.R.; Wilcks, A.; Andersen, J.B.; Schmidt, L.R.; Grønlund, H.A.; Vigsnaes, L.K.; Michaelsen, K.F.; Bahl, M.I. Introducing GUt Low-Density Array (GULDA)—A validated approach for qPCR-based intestinal microbial community analysis. FEMS Microbiol. Lett. 2012, 337, 38–47. [Google Scholar] [CrossRef] [PubMed]
- Schwiertz, A.; Taras, D.; Schäfer, K.; Beijer, S.; Bos, N.A.; Donus, C.; Hardt, P.D. Microbiota and SCFA in lean and overweight healthy subjects. Obesity 2009, 18, 190–195. [Google Scholar] [CrossRef] [PubMed]
- Strati, F.; Cavalieri, D.; Albanese, D.; De Felice, C.; Donati, C.; Hayek, J.; Jousson, O.; Leoncini, S.; Renzi, D.; Calabrò, A.; et al. New evidences on the altered gut microbiota in autism spectrum disorders. Microbiome 2017, 5, 24. [Google Scholar] [CrossRef] [PubMed]
- Huang, R.; Wang, K.; Hu, J. Effect of Probiotics on Depression: A Systematic Review and Meta-Analysis of Randomized Controlled Trials. Nutrients 2016, 8, E483. [Google Scholar] [CrossRef] [PubMed]
- Huang, R.; Ning, H.; Yang, L.; Jia, C.; Yang, F.; Xu, G.; Tan, H. Efficacy of Probiotics on Anxiety: A Meta-analysis of Randomized Controlled Trials. Neuropsychiatry 2017, 7, 862–871. [Google Scholar] [CrossRef]
- Dąbrowska, K.; Witkiewicz, W. Correlations of Host Genetics and Gut Microbiome Composition. Front. Microbiol. 2016, 7, 1357. [Google Scholar] [CrossRef]
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Huang, E.; Kang, S.; Park, H.; Park, S.; Ji, Y.; Holzapfel, W.H. Differences in Anxiety Levels of Various Murine Models in Relation to the Gut Microbiota Composition. Biomedicines 2018, 6, 113. https://doi.org/10.3390/biomedicines6040113
Huang E, Kang S, Park H, Park S, Ji Y, Holzapfel WH. Differences in Anxiety Levels of Various Murine Models in Relation to the Gut Microbiota Composition. Biomedicines. 2018; 6(4):113. https://doi.org/10.3390/biomedicines6040113
Chicago/Turabian StyleHuang, Eunchong, Shinwon Kang, Haryung Park, Soyoung Park, Yosep Ji, and Wilhelm H. Holzapfel. 2018. "Differences in Anxiety Levels of Various Murine Models in Relation to the Gut Microbiota Composition" Biomedicines 6, no. 4: 113. https://doi.org/10.3390/biomedicines6040113
APA StyleHuang, E., Kang, S., Park, H., Park, S., Ji, Y., & Holzapfel, W. H. (2018). Differences in Anxiety Levels of Various Murine Models in Relation to the Gut Microbiota Composition. Biomedicines, 6(4), 113. https://doi.org/10.3390/biomedicines6040113