Gut microbiome remodeling induces depressive-like behaviors through a pathway mediated by the host's metabolism

Molecular Psychiatry

Volumn 21, Issue 6, 2016, Pages 786-796

  Zheng, P ^a,b   Zeng, B ^c   Zhou, C ^a,b   Liu, M ^a,b   Fang, Z ^a,b   Xu, X ^a,b   Zeng, L ^a,b   Chen, J ^a,b   Fan, S ^a,b   Du, X ^a,b   Zhang, X ^a,b   Yang, D ^a   Yang, Y ^a,b   Meng, H ^a   Li, W ^c   Melgiri, N D ^a,b   Licinio, J ^d   Wei, H ^c   Xie, P ^a,b  

^a CHONGQING MEDICAL UNIVERSITY   (China)

^b CHONGQING KEY LABORATORY OF NEUROBIOLOGY   (China)

^c THIRD MILITARY MEDICAL UNIVERSITY   (China)

^d FLINDERS UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CARBOHYDRATE; GENOMIC DNA; RNA 16S;

ACTINOBACTERIA; ADULT; AGED; AMINO ACID METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTEROIDETES; CARBOHYDRATE METABOLISM; COMPARATIVE STUDY; CONTROLLED STUDY; DYSBIOSIS; FIRMICUTES; FORCED SWIM TEST; HUMAN; IMMOBILITY; INTESTINE FLORA; MAJOR CLINICAL STUDY; MAJOR DEPRESSION; MALE; METABOLISM; METAGENOMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; RNA SEQUENCE; TAIL SUSPENSION TEST; Y-MAZE TEST; ANIMAL; DEPRESSION; GENOTYPE ENVIRONMENT INTERACTION; MICROBIOLOGY; MICROFLORA; PHYSIOLOGY; PSYCHOLOGY;

ANIMALS; DEPRESSION; DEPRESSIVE DISORDER, MAJOR; DYSBIOSIS; GASTROINTESTINAL MICROBIOME; GENE-ENVIRONMENT INTERACTION; HUMANS; MICE; MICROBIOTA;

EID: 84963547235     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2016.44     Document Type: Article

References (71)

1. Mitchell AJ, Chan M, Bhatti H, Halton M, Grassi L, Johansen C, et al. Prevalence of depression, anxiety, and adjustment disorder in oncological, haematological, and palliative-care settings: a meta-Analysis of 94 interview-based studies. Lancet Oncol 2011; 12: 160-174
2. Simon GE. Social and economic burden of mood disorders. Biol Psychiatry 2003; 54: 208-215
3. Luscher B, Shen Q, Sahir N. The GABAergic deficit hypothesis of major depressive disorder. Mol Psychiatry 2011; 16: 383-406
4. Guilloux J-P, Douillard-Guilloux G, Kota R, Wang X, Gardier A, Martinowich K, et al. Molecular evidence for BDNF-And GABA-related dysfunctions in the amygdala of female subjects with major depression. Mol Psychiatry 2012; 17: 1130-1142
5. Müller N, Schwarz M. The immune-mediated alteration of serotonin and glutamate: towards an integrated view of depression. Mol Psychiatry 2007; 12: 988-1000
6. Schlösser RG, Wagner G, Koch K, Dahnke R, Reichenbach JR, Sauer H. Fronto-cingulate effective connectivity in major depression: a study with fMRI and dynamic causal modeling. Neuroimage 2008; 43: 645-655
7. Zheng P, Gao HC, Li Q, Shao WH, Zhang ML, Cheng K, et al. Plasma metabonomics as a novel diagnostic approach for major depressive disorder. J Proteome Res 2012; 11: 1741-1748
8. Zheng P, Chen J-J, Huang T, Wang M-J, Wang Y, Dong M-X, et al. A novel urinary metabolite signature for diagnosing major depressive disorder. J Proteome Res 2013; 12: 5904-5911
9. Zheng P, Wang Y, Chen L, Yang D, Meng H, Zhou D, et al. Identification and validation of urinary metabolite biomarkers for major depressive disorder. Mol Cell Proteomics 2013; 12: 207-214
10. Chen J-J, Zhou C-J, Liu Z, Fu Y-Y, Zheng P, Yang D-Y, et al. Divergent urinary metabolic phenotypes between major depressive disorder and bipolar disorder identified by a combined GC-MS and NMR spectroscopic metabonomic approach. J Proteome Res 2015; 14: 3382-3389
11. Naseribafrouei A, Hestad K, Avershina E, Sekelja M, Linløkken A, Wilson R, et al. Correlation between the human fecal microbiota and depression. Neurogastroenterol Motil 2014; 26: 1155-1162
12. Jiang H, Ling Z, Zhang Y, Mao H, Ma Z, Yin Y, et al. Altered fecal microbiota composition in patients with major depressive disorder. Brain Behav Immun 2015; 48: 186-194
13. Park A, Collins J, Blennerhassett P, Ghia J, Verdu E, Bercik P, et al. Altered colonic function and microbiota profile in a mouse model of chronic depression. Neurogastroenterol Motil 2013; 25: 733-e575
14. Clemente JC, Ursell LK, Parfrey LW, Knight R. The impact of the gut microbiota on human health: an integrative view. Cell 2012; 148: 1258-1270
15. Henao-Mejia J, Elinav E, Jin C, Hao L, Mehal WZ, Strowig T, et al. Inflammasomemediated dysbiosis regulates progression of NAFLD and obesity. Nature 2012; 482: 179-185
16. Koren O, Goodrich JK, Cullender TC, Spor A, Laitinen K, Bäckhed HK, et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 2012; 150: 470-480
17. Konstantinov SR, Peppelenbosch MP. Fecal microbiota transfer may increase irritable bowel syndrome and inflammatory bowel diseases-Associated bacteria. Gastroenterology 2013; 144: e19-e20
18. Wen L, Ley RE, Volchkov PY, Stranges PB, Avanesyan L, Stonebraker AC, et al. Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature 2008; 455: 1109-1113
19. Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 2013; 341: 1241214
20. Bercik P, Denou E, Collins J, Jackson W, Lu J, Jury J, et al. The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology 2011; 141: 599-609.e593
21. Clarke G, Grenham S, Scully P, Fitzgerald P, Moloney R, Shanahan F, et al. The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Mol Psychiatry 2013; 18: 666-673
22. Heijtz RD, Wang S, Anuar F, Qian Y, Björkholm B, Samuelsson A, et al. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci USA 2011; 108: 3047-3052
23. Neufeld K, Kang N, Bienenstock J, Foster J. Reduced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterol Motil 2011; 23: 255-e119
24. Cryan JF, Dinan TG. Mind-Altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 2012; 13: 701-712
25. Gareau MG, Wine E, Rodrigues DM, Cho JH, Whary MT, Philpott DJ, et al. Bacterial infection causes stress-induced memory dysfunction in mice. Gut 2010; 60: 307-317, gut. 2009.202515
26. Desbonnet L, Clarke G, Shanahan F, Dinan T, Cryan J. Microbiota is essential for social development in the mouse. Mol Psychiatry 2014; 19: 146
27. Hsiao EY, McBride SW, Hsien S, Sharon G, Hyde ER, McCue T, et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 2013; 155: 1451-1463
28. Yang D, Li Q, Fang L, Cheng K, Zhang R, Zheng P, et al. Reduced neurogenesis and pre-synaptic dysfunction in the olfactory bulb of a rat model of depression. Neuroscience 2011; 192: 609-618
29. Kim CS, Chang PY, Johnston D. Enhancement of dorsal hippocampal activity by knockdown of HCN1 channels leads to anxiolytic-And antidepressant-like behaviors. Neuron 2012; 75: 503-516
30. Sadakata T, Shinoda Y, Oka M, Sekine Y, Sato Y, Saruta C, et al. Reduced axonal localization of a Caps2 splice variant impairs axonal release of BDNF and causes autistic-like behavior in mice. Proc Natl Acad Sci USA 2012; 109: 21104-21109
31. Crupi R, Cambiaghi M, Spatz L, Hen R, Thorn M, Friedman E, et al. Reduced adult neurogenesis and altered emotional behaviors in autoimmune-prone B-cell activating factor transgenic mice. Biol Psychiatry 2010; 67: 558-566
32. Oury F, Khrimian L, Denny CA, Gardin A, Chamouni A, Goeden N, et al. Maternal and offspring pools of osteocalcin influence brain development and functions. Cell 2013; 155: 228-241
33. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders (Text Revision). American Psychiatric Association: Washington, DC, USA, 2000
34. Potts MK, Daniels M, Burnam MA, Wells KB. A structured interview version of the Hamilton Depression Rating Scale: evidence of reliability and versatility of administration. J Psychiatr Res 1990; 24: 335-350
35. Tamaki H, Wright CL, Li X, Lin Q, Hwang C, Wang S, et al. Analysis of 16 S rRNA amplicon sequencing options on the Roche/454 next-generation titanium sequencing platform. PloS One 2011; 6: e25263
36. Bruce-Keller AJ, Salbaum JM, Luo M, Blanchard E, Taylor CM, Welsh DA, et al. Obese-Type gut microbiota induce neurobehavioral changes in the absence of obesity. Biol Psychiatry 2015; 77: 607-615
37. Yang S, Liebner S, Alawi M, Ebenhöh O, Wagner D. Taxonomic database and cut-off value for processing mcrA gene 454 pyrosequencing data by MOTHUR. J Microbiol Methods 2014; 103: 3-5
38. Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, et al. Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 2013; 42: D633-D642, gkt1244
39. Keylock C. Simpson diversity and the Shannon-Wiener index as special cases of a generalized entropy. Oikos 2005; 109: 203-207
40. Faith DP. Conservation evaluation and phylogenetic diversity. Biological Conservation 1992; 61: 1-10
41. Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 2005; 71: 8228-8235
42. 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
43. Breiman L. Random forests. Machine Learning 2001; 45: 5-32
44. Xu X-J, Zheng P, Ren G-P, Liu M-L, Mu J, Guo J, et al. 2, 4-Dihydroxypyrimidine is a potential urinary metabolite biomarker for diagnosing bipolar disorder. Mol Biosyst 2014; 10: 813-819
45. Worley B, Halouska S, Powers R. Utilities for quantifying separation in PCA/PLS-DA scores plots. Anal Biochem 2013; 433: 102-104
46. Chen T, Xie G, Wang X, Fan J, Qiu Y, Zheng X, et al. Serum and urine metabolite profiling reveals potential biomarkers of human hepatocellular carcinoma. Mol Cell Proteomics 2011; 10: M110.004945
47. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30: 2114-2120, btu170
48. Cock PJ, Fields CJ, Goto N, Heuer ML, Rice PM. The Sanger FASTQ file format for sequences with quality scores, and the Solexa/Illumina FASTQ variants. Nucleic Acids Res 2010; 38: 1767-1771
49. Segata N, Waldron L, Ballarini A, Narasimhan V, Jousson O, Huttenhower C. Metagenomic microbial community profiling using unique clade-specific marker genes. Nat Methods 2012; 9: 811-814
50. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9: 357-359
51. Peng Y, Leung HC, Yiu S-M, Chin FY. IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 2012; 28: 1420-1428
52. Hyatt D, Chen G-L, LoCascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 2010; 11: 119
53. Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 2012; 490: 55-60
54. Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res 2014; 42: D199-D205
55. Zhang D, Jing X, Yang J. Biometric image discrimination technologies. IGI Global 2011; 60: 307-317
56. Bangsgaard Bendtsen KM, Krych L, Sørensen DB, Pang W, Nielsen DS, Josefsen K, et al. Gut microbiota composition is correlated to grid floor induced stress and behavior in the BALB/c mouse. PLoS One 2012; 7: e46231
57. Li W, Dowd SE, Scurlock B, Acosta-Martinez V, Lyte M. Memory and learning behavior in mice is temporally associated with diet-induced alterations in gut bacteria. Physiol Behav 2009; 96: 557-567
58. Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, et al. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci USA 2011; 108: 16050-16055
59. Goodrich JK, Di Rienzi SC, Poole AC, Koren O, Walters WA, Caporaso JG, et al. Conducting a microbiome study. Cell 2014; 158: 250-262
60. Pollack MH. Comorbid anxiety and depression. J Clin Psychiatry 2004; 66: 22-29
61. MacQueen G, Frodl T. The hippocampus in major depression: evidence for the convergence of the bench and bedside in psychiatric research&quest. Mol Psychiatry 2011; 16: 252-264
62. Foster JA, Neufeld K-AM. Gut-brain axis: how the microbiome influences anxiety and depression. Trends Neurosci 2013; 36: 305-312
63. Arseneault-Bréard J, Rondeau I, Gilbert K, Girard S-A, Tompkins TA, Godbout R, et al. Combination of Lactobacillus helveticus R0052 and Bifidobacterium longum R0175 reduces post-myocardial infarction depression symptoms and restores intestinal permeability in a rat model. Br J Nutr 2012; 107: 1793-1799
64. Desbonnet L, Garrett L, Clarke G, Bienenstock J, Dinan TG. The probiotic Bifidobacteria infantis: an assessment of potential antidepressant properties in the rat. J Psychiatr Res 2008; 43: 164-174
65. Desbonnet L, Garrett L, Clarke G, Kiely B, Cryan J, Dinan T. Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression. Neuroscience 2010; 170: 1179-1188
66. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, et al. Human gut microbiome viewed across age and geography. Nature 2012; 486: 222-227
67. Consortium HMP. Structure, function and diversity of the healthy human microbiome. Nature 2012; 486: 207-214
68. Martins-de-Souza D, Guest P, Harris L, Vanattou-Saifoudine N, Webster M, Rahmoune H, et al. Identification of proteomic signatures associated with depression and psychotic depression in post-mortem brains from major depression patients. Transl Psychiatry 2012; 2: e87
69. Chen G, Yang D, Yang Y, Li J, Cheng K, Tang G, et al. Amino acid metabolic dysfunction revealed in the prefrontal cortex of a rat model of depression. Behav Brain Res 2015; 278: 286-292
70. Mayoral-Mariles A, Cruz-Revilla C, Vega-Manriquez X, Aguirre-Hernández R, Severiano-Pérez P, Aburto-Arciniega E, et al. Plasma amino acid levels discriminate between control subjects and mildly depressed elderly women. Arch Med Res 2012; 43: 375-382
71. Wong M-L, Inserra A, Lewis MD, Mastronardi CA, Kentish S, Leong L, et al. Inflammasome signaling affects anxiety-And depressive-like behavior and gut microbiome composition. Mol Psychiatry 2016 (in press