Chronic psychological stress disrupted the composition of the murine colonic microbiota and accelerated a murine model of inflammatory bowel disease

PLoS ONE

Volumn 11, Issue 3, 2016, Pages

  Watanabe, Yohei ^a   Arase, Sohei ^a   Nagaoka, Noriko ^a   Kawai, Mitsuhisa ^a   Matsumoto, Satoshi ^a  

^a YAKULT CENTRAL INSTITUTE FOR MICROBIOLOGICAL RESEARCH   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CLOSTRIDIUM TOXIN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; PHOSPHOLIPASE C; RNA 16S; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BAGG ALBINO MOUSE; C57BL 6 MOUSE; CELL COUNT; CHRONIC STRESS; CLOSTRIDIUM; CLOSTRIDIUM PERFRINGENS; COLON FLORA; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE EXACERBATION; DISEASE SEVERITY; DYSBIOSIS; GENE SEQUENCE; HISTOPATHOLOGY; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNOGLOBULIN PRODUCTION; INFLAMMATORY BOWEL DISEASE; KNOCKOUT MOUSE; MENTAL STRESS; MICROBIAL DIVERSITY; MOUSE; MUCOSAL IMMUNITY; MURINE MODEL; NEXT GENERATION SEQUENCING; NONHUMAN; PHYLOGENY; POPULATION ABUNDANCE; SPECIES COMPOSITION; SPECIES RICHNESS; STRAIN DIFFERENCE; T LYMPHOCYTE RECEPTOR ALPHA CHAIN GENE; T LYMPHOCYTE RECEPTOR GENE; ULCERATIVE COLITIS; ANIMAL; AVOIDANCE BEHAVIOR; BIOSYNTHESIS; COLON; DEFICIENCY; DISEASE MODEL; GENE INACTIVATION; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MICROFLORA; PHYSIOLOGY; PSYCHOLOGY;

ANIMALS; AVOIDANCE LEARNING; CLOSTRIDIUM; COLON; DISEASE MODELS, ANIMAL; GENE KNOCKOUT TECHNIQUES; IMMUNOGLOBULIN A; INFLAMMATORY BOWEL DISEASES; MICE; MICROBIOTA; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; STRESS, PSYCHOLOGICAL; TYPE C PHOSPHOLIPASES;

EID: 84961149490     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0150559     Document Type: Article

References (48)

1. Consortium THMP. Structure, function and diversity of the healthy human microbiome. Nature. 2012; 486: 207-214. doi: 10.1038/nature11234
2. O'Hara AM, Shanahan F. The gut flora as a forgotten organ. EMBO reports. 2006; 7: 688-693. doi: 10. 1038/sj.embor.7400731
3. Ahn J, Sinha R, Pei Z, Dominianni C, Wu J, Shi J, et al. Human Gut Microbiome and Risk of Colorectal Cancer. JNCI J Natl Cancer Inst. 2013; djt300. doi: 10.1093/jnci/djt300
4. Kostic AD, Gevers D, Siljander H, Vatanen T, Hyötyläinen T, Hämäläinen A-M, et al. The Dynamics of the Human Infant Gut Microbiome in Development and in Progression toward Type 1 Diabetes. Cell Host & Microbe. 2015; 17: 260-273. doi: 10.1016/j.chom.2015.01.001
5. Zhang H, DiBaise JK, Zuccolo A, Kudrna D, Braidotti M, Yu Y, et al. Human gut microbiota in obesity and after gastric bypass. PNAS. 2009; 106: 2365-2370. doi: 10.1073/pnas.0812600106
6. Frank DN, Robertson CE, Hamm CM, Kpadeh Z, Zhang T, Chen H, et al. Disease phenotype and genotype are associated with shifts in intestinal-Associated microbiota in inflammatory bowel diseases. Inflamm Bowel Dis. 2011; 17: 179-184. doi: 10.1002/ibd.21339
7. Baumgart DC, Bernstein CN, Abbas Z, Colombel JF, Day AS, D'Haens G, et al. IBD Around the world: comparing the epidemiology, diagnosis, and treatment: proceedings of the World Digestive Health Day 2010-Inflammatory Bowel Disease Task Force meeting. Inflamm Bowel Dis. 2011; 17: 639-644. doi: 10.1002/ibd.21409
8. Jawad N, Direkze N, Leedham SJ. Inflammatory Bowel Disease and Colon Cancer. In: Jankowski JAZ, editor. Inflammation and Gastrointestinal Cancers. Berlin, Heidelberg: Springer Berlin Heidelberg; 2011. pp. 99-115. Available: http://link.springer.com/10.1007/978-3-642-03503-6-6
9. Bernstein CN, Singh S, Graff LA, Walker JR, Miller N, Cheang M. A Prospective Population-Based Study of Triggers of Symptomatic Flares in IBD. Am J Gastroenterol. 2010; 105: 1994-2002. doi: 10. 1038/ajg.2010.140
10. Cryan JF, Dinan TG. Mind-Altering microorganisms: The impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci. 2012; 13: 701-712. doi: 10.1038/nrn3346
11. Galley JD, Nelson MC, Yu Z, Dowd SE, Walter J, Kumar PS, et al. Exposure to a social stressor disrupts the community structure of the colonic mucosa-Associated microbiota. BMC Microbiology. 2014; 14: 189. doi: 10.1186/1471-2180-14-189
12. Bailey MT, Dowd SE, Parry NMA, Galley JD, Schauer DB, Lyte M. Stressor Exposure Disrupts Commensal Microbial Populations in the Intestines and Leads to Increased Colonization by Citrobacter rodentium. Infect Immun. 2010; 78: 1509-1519. doi: 10.1128/IAI.00862-09
13. Bailey MT, Dowd SE, Galley JD, Hufnagle AR, Allen RG, Lyte M. Exposure to a social stressor alters the structure of the intestinal microbiota: Implications for stressor-induced immunomodulation. Brain, Behavior, and Immunity. 2011; 25: 397-407. doi: 10.1016/j.bbi.2010.10.023
14. Sun Y, Zhang M, Chen C, Gillilland M III, Sun X, El-Zaatari M, et al. Stress-Induced Corticotropin-Releasing Hormone-Mediated NLRP6 Inflammasome Inhibition and Transmissible Enteritis in Mice. Gastroenterology. 2013; 144: 1478-1487.e8. doi: 10.1053/j.gastro.2013.02.038
15. Leonard BE. The HPA and immune axes in stress: The involvement of the serotonergic system. European Psychiatry. 2005; 20, Supplement 3: S302-S306. doi: 10.1016/S0924-9338(05)80180-4
16. Mombaerts P, Mizoguchi E, Grusby MJ, Glimcher LH, Bhan AK, Tonegawa S. Spontaneous development of inflammatory bowel disease in T cell receptor mutant mice. Cell. 1993; 75: 275-282. doi: 10. 1016/0092-8674(93)80069-Q
17. Julio-Pieper M, O'Mahony CM, Clarke G, Bravo JA, Dinan TG, Cryan JF. Chronic stress-induced alterations in mouse colonic 5-HT and defecation responses are strain dependent. Stress. 2011; 15: 218-226. doi: 10.3109/10253890.2011.607524
18. Matsuki T, Watanabe K, Fujimoto J, Takada T, Tanaka R. Use of 16S rRNA Gene-Targeted Group-Specific Primers for Real-Time PCR Analysis of Predominant Bacteria in Human Feces. Appl Environ Microbiol. 2004; 70: 7220-7228. doi: 10.1128/AEM.70.12.7220-7228.2004
19. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, et al. Ultra-high-Throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 2012; 6: 1621-1624. doi: 10.1038/ismej.2012.8
20. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-Throughput community sequencing data. Nature Methods. 2010; 7: 335-336. doi: 10. 1038/nmeth.f.303
21. Aronesty E. Comparison of Sequencing Utility Programs. Open Bioinformatics Journal. 2013; 7: 1-8.
22. Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, et al. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Meth. 2013; 10: 57-59. doi: 10. 1038/nmeth.2276
23. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010; btq461. doi: 10.1093/bioinformatics/btq461
24. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011; 27: 2194-2200. doi: 10.1093/bioinformatics/btr381
25. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naïve Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy. Appl Environ Microbiol. 2007; 73: 5261-5267. doi: 10. 1128/AEM.00062-07
26. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, et al. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 2012; 6: 610-618. doi: 10.1038/ismej.2011.139
27. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R. PyNAST: A flexible tool for aligning sequences to a template alignment. Bioinformatics. 2010; 26: 266-267. doi: 10.1093/bioinformatics/btp636
28. Yarza P, Richter M, Peplies J, Euzeby J, Amann R, Schleifer K-H, et al. The All-Species Living Tree project: A 16S rRNA-based phylogenetic tree of all sequenced type strains. Systematic and Applied Microbiology. 2008; 31: 241-250. doi: 10.1016/j.syapm.2008.07.001
29. 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. doi: 10.1093/molbev/msp077
30. Lozupone C, Knight R. UniFrac: A New Phylogenetic Method for Comparing Microbial Communities. Appl Environ Microbiol. 2005; 71: 8228-8235. doi: 10.1128/AEM.71.12.8228-8235.2005
31. Nagpal R, Ogata K, Tsuji H, Matsuda K, Takahashi T, Nomoto K, et al. Sensitive quantification of Clostridium perfringens in human feces by quantitative real-Time PCR targeting alpha-Toxin and enterotoxin genes. BMC Microbiology. 2015; 15: 219. doi: 10.1186/s12866-015-0561-y
32. Watanabe Y, Nagai F, Morotomi M. Characterization of Phascolarctobacterium succinatutens sp. nov., an Asaccharolytic, Succinate-Utilizing Bacterium Isolated from Human Feces. Appl Environ Microbiol. 2012; 78: 511-518. doi: 10.1128/AEM.06035-11
33. Matsumoto S, Watanabe N, Imaoka A, Okabe Y. Preventive effects of Bifidobacterium-And Lactobacillus-fermented milk on the development of inflammatory bowel disease in senescence-Accelerated mouse P1/Yit strain mice. Digestion. 2001; 64: 92-99. 48846
34. Karasawa T, Wang X, Maegawa T, Michiwa Y, Kita H, Miwa K, et al. Clostridium sordellii Phospholipase C: Gene Cloning and Comparison of Enzymatic and Biological Activities with Those of Clostridium perfringens and Clostridium bifermentans Phospholipase C. Infect Immun. 2003; 71: 641-646. doi: 10. 1128/IAI.71.2.641-646.2003
35. Sakurai J, Nagahama M, Oda M. Clostridium perfringens Alpha-Toxin: Characterization and Mode of Action. J Biochem. 2004; 136: 569-574. doi: 10.1093/jb/mvh161
36. Kawamoto S, Maruya M, Kato LM, Suda W, Atarashi K, Doi Y, et al. Foxp3+ T Cells Regulate Immunoglobulin A Selection and Facilitate Diversification of Bacterial Species Responsible for Immune Homeostasis. Immunity. 2014; 41: 152-165. doi: 10.1016/j.immuni.2014.05.016
37. Bhan AK, Mizoguchi E, Smith RN, Mizoguchi A. Spontaneous chronic colitis in TCR alpha-mutant mice; an experimental model of human ulcerative colitis. Int Rev Immunol. 2000; 19: 123-138.
38. Kawamoto S, Tran TH, Maruya M, Suzuki K, Doi Y, Tsutsui Y, et al. The Inhibitory Receptor PD-1 Regulates IgA Selection and Bacterial Composition in the Gut. Science. 2012; 336: 485-489. doi: 10.1126/science.1217718
39. Ericsson AC, Davis JW, Spollen W, Bivens N, Givan S, Hagan CE, et al. Effects of Vendor and Genetic Background on the Composition of the Fecal Microbiota of Inbred Mice. PLoS ONE. 2015; 10: e0116704. doi: 10.1371/journal.pone.0116704
40. Krych L, Nielsen DS, Hansen AK, Hansen CHF. Gut microbial markers are associated with diabetes onset, regulatory imbalance, and IFN-γ level in NOD Mice. Gut Microbes. 2015; 6: 101-109. doi: 10. 1080/19490976.2015.1011876
41. Ravussin Y, Koren O, Spor A, LeDuc C, Gutman R, Stombaugh J, et al. Responses of Gut Microbiota to Diet Composition and Weight Loss in Lean and Obese Mice. Obesity. 2012; 20: 738-747. doi: 10. 1038/oby.2011.111
42. Berry D, Schwab C, Milinovich G, Reichert J, Mahfoudh KB, Decker T, et al. Phylotype-level 16S rRNA analysis reveals new bacterial indicators of health state in acute murine colitis. The ISME Journal. 2012; 6: 2091-2106. doi: 10.1038/ismej.2012.39
43. Nagy-Szakal D, Hollister EB, Luna RA, Szigeti R, Tatevian N, Smith CW, et al. Cellulose Supplementation Early in Life Ameliorates Colitis in Adult Mice. PLoS ONE. 2013; 8: e56685. doi: 10.1371/journal. pone.0056685
44. Perez-Muñoz ME, Bergstrom K, Peng V, Schmaltz R, Jimenez-Cardona R, Marsteller N, et al. Discordance between changes in the gut microbiota and pathogenicity in a mouse model of spontaneous colitis. Gut Microbes. 2014; 5: 286-485. doi: 10.4161/gmic.28622
45. Palm NW, de Zoete MR, Cullen TW, Barry NA, Stefanowski J, Hao L, et al. Immunoglobulin A Coating Identifies Colitogenic Bacteria in Inflammatory Bowel Disease. Cell. 2014; 158: 1000-1010. doi: 10. 1016/j.cell.2014.08.006
46. Titball RW. Bacterial phospholipases C. Microbiol Rev. 1993; 57: 347-366.
47. Bloom SM, Bijanki VN, Nava GM, Sun L, Malvin NP, Donermeyer DL, et al. Commensal Bacteroides Species Induce Colitis in Host-Genotype-Specific Fashion in a Mouse Model of Inflammatory Bowel Disease. Cell Host & Microbe. 2011; 9: 390-403. doi: 10.1016/j.chom.2011.04.009
48. Arthur JC, Perez-Chanona E, Möhlbauer M, Tomkovich S, Uronis JM, Fan T-J, et al. Intestinal Inflammation Targets Cancer-Inducing Activity of the Microbiota. Science. 2012; 338: 120-123. doi: 10.1126/science.1224820