Gut microbiome populations are associated with structure-specific changes in white matter architecture

Translational Psychiatry

Volumn 8, Issue 1, 2018, Pages

  Ong, Irene M ^a,b   Gonzalez, Jose G ^c   McIlwain, Sean J ^a,b   Sawin, Emily A ^a   Schoen, Andrew J ^d   Adluru, Nagesh ^e   Alexander, Andrew L ^a,c,e   Yu, John Paul J ^a,c,f  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN   (United States)

^c University of Wisconsin Health   (United States)

^d University of Wisconsin Madison   (United States)

^e UNIVERSITY OF WISCONSIN MADISON   (United States)

^f University of Wisconsin Madison   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; BRAIN FUNCTION; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; GLOBAL CHANGE; IMAGE ANALYSIS; INTESTINE FLORA; LIPID DIET; MALE; METAGENOMICS; NERVOUS TISSUE; NONHUMAN; RANDOM FOREST; RAT; RNA SEQUENCE; TISSUE STRUCTURE; WHITE MATTER; ANIMAL; BACTERIUM; CLASSIFICATION; DIAGNOSTIC IMAGING; DIET; GENETICS; PATHOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; BACTERIA; DIET; DIFFUSION TENSOR IMAGING; GASTROINTESTINAL MICROBIOME; MALE; RATS; RATS, SPRAGUE-DAWLEY; RNA, RIBOSOMAL, 16S; WHITE MATTER;

EID: 85040520040     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/s41398-017-0022-5     Document Type: Article

References (47)

1. Gevers, D. et al. The treatment-naive microbiome in new-onset Crohn's disease. Cell Host Microbe 15, 382-392 (2014).
2. Hsiao, E. Y. et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 155, 1451-1463 (2013).
3. Tillisch, K. et al. Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology 144, 1394-401 (2013).
4. Heijtz, R. D. et al. Normal gut microbiota modulates brain development and behavior. Proc. Natl. Acad. Sci. 108, 3047-3052 (2011).
5. Whitehead, W. E., Palsson, O. & Jones, K. R. Systematic review of the comorbidity of irritable bowel syndrome with other disorders: what are the causes and implications? Gastroenterology 122, 1140-1156 (2002).
6. Liu, Z. et al. High-fat diet induces hepatic insulin resistance and impairment of synaptic plasticity. PLoS. ONE 10, e0128274 (2015).
7. Kaptan, Z. et al. Long termconsequences on spatial learning-memory of lowcalorie diet during adolescence in female rats; hippocampal and prefrontal cortex BDNF level, expression of NeuN and cell proliferation in dentate gyrus. Brain Res. 1618, 194-204 (2015).
8. Buffington, S. A. et al. Microbial reconstitution reverses maternal diet-induced social and synaptic deficits in offspring. Cell 165, 1762-1775 (2016).
9. Schafer, D. P. & Stevens, B. Phagocytic glial cells: Sculpting synaptic circuits in the developing nervous system. Curr. Opin. Neurobiol. 23, 1034-1040 (2013).
10. Rogers, G. B. et al. From gut dysbiosis to altered brain function and mental illness: mechanisms and pathways. Mol. Psychiatr. 21, 1-11 (2016).
11. David, L. A. et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559-63 (2014).
12. Jenkinson, M., Bannister, P., Brady, M. & Smith, S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17, 825-841 (2002).
13. Leemans, A. & Jones, D. K. The B-matrix must be rotated when correcting for subject motion in DTI data. Magn. Reson. Med. 61, 1336-1349 (2009).
14. Zhang, H., Yushkevich, P. A., Alexander, D. C. & Gee, J. C. Deformable registration of diffusion tensor MR images with explicit orientation optimization. Med. Image Anal. 10, 764-785 (2006).
15. Keihaninejad, S. et al. The importance of group-wise registration in tract based spatial statistics study of neurodegeneration: a simulation study in Alzheimer's disease. PLoS. ONE 7, e45996 (2012).
16. Wang, Y. et al. DTI registration in atlas based fiber analysis of infantile Krabbe disease. Neuroimage 55, 1577-1586 (2011).
17. Bach, M. et al. Methodological considerations on tract-based spatial statistics (TBSS). Neuroimage 100, 358-369 (2014).
18. Smith, S. M. & Nichols, T. E. Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 44, 83-98 (2009).
19. Rumple, A. et al. 3-dimensional diffusion tensor imaging (DTI) atlas of the rat brain. PLoS. ONE 8, e67334 (2013).
20. Avants, B. B. et al. A reproducible evaluation of ANTs similarity metric performance in brain image registration. Neuroimage 54, 2033-2044 (2011).
21. Klindworth, A. et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 41, e1 (2013).
22. Jiang, H., Lei, R., Ding, S.-W. & Zhu, S. Skewer: a fast and accurate adapter trimmer for next-generation sequencing paired-end reads. BMC Bioinforma. 15, 182 (2014).
23. Magoč, T. & Salzberg, S. L. FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957-2963 (2011).
24. Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-6 (2010).
25. Liaw, A. & Wiener, M. Classification and regression by random Forest. R. News 2, 18-22 (2002).
26. Breiman, L. Random forests. Mach. Learn. 45, 5-32 (2001).
27. Gu, Z., Gu, L., Eils, R., Schlesner,M. & Brors, B. Circlize Implements and enhances circular visualization in R. Bioinformatics 30, 2811-2812 (2014).
28. Lozupone, C. & Knight, R. UniFrac: A new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71, 8228-8235 (2005).
29. David, L. A. et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559-63 (2014).
30. R Development Core Team R. R: A language and environment for statistical computing. R found. Stat. Comput. 1, 409 (2011).
31. Nohr, M. K. et al. Expression of the short chain fatty acid receptor GPR41/FFAR3 in autonomic and somatic sensory ganglia. Neuroscience 290, 126-137 (2015).
32. Barrett, E., Ross, R. P., O'Toole, P. W., Fitzgerald, G. F. & Stanton, C. Gammaaminobutyric acid production by culturable bacteria from the human intestine. J. Appl. Microbiol. 113, 411-417 (2012).
33. Fernandez-Real, J. M. et al. Gut microbiota interacts with brain microstructure and function. J. Clin. Endocrinol. Metab. 100, 4505-4513 (2015).
34. Pasolli, E., Truong, D. T., Malik, F., Waldron, L. & Segata, N. Machine learning meta-analysis of large metagenomic datasets: Tools and biological insights. PLoS. Comput. Biol. 12, e1004977 (2016).
35. Tang, A. T. et al. Endothelial TLR4 and the microbiome drive cerebral cavernous malformations. Nature 545, 305-310 (2017).
36. Gacias, M. et al. Microbiota-driven transcriptional changes in prefrontal cortex override genetic differences in social behavior. Elife 5, e13442 (2016).
37. Hoban, A. E. et al. Regulation of prefrontal cortex myelination by the microbiota. Transl. Psychiatr. 6, e774 (2016).
38. Hoeft, F. et al. More is not always better: increased fractional anisotropy of superior longitudinal fasciculus associated with poor visuospatial abilities in Williams syndrome. J. Neurosci. 27, 11960-11965 (2007).
39. Mayer, A. R. et al. A prospective diffusion tensor imaging study in mild traumatic brain injury. Neurology 74, 643-650 (2010).
40. Metwalli, N. S. et al. Utility of axial and radial diffusivity from diffusion tensor MRI as markers of neurodegeneration in amyotrophic lateral sclerosis. Brain Res. 1348, 156-164 (2010).
41. Wheeler-Kingshott, C. A. M. & Cercignani, M. About 'axial' and 'radial' diffusivities. Magn. Reson. Med. 61, 1255-1260 (2009).
42. Uhlmann, A. et al. White matter microstructure and impulsivity in methamphetamine dependence with and without a history of psychosis. Hum. Brain Mapp. 37, 2055-2067 (2016).
43. Alexander, A. L., Lee, J. E., Lazar, M. & Field, A. S. Diffusion tensor imaging of the brain. Neurotherapeutics 4, 316-329 (2007).
44. Li, L. et al. Gut microbes in correlation with mood: case study in a closed experimental human life support system. Neurogastroenterol. Motil. 28, 1233-1240 (2016).
45. Paterson, C. et al. Temporal, diagnostic, and tissue-specific regulation of NRG3 isoform expression in human brain development and affective disorders. Am. J. Psychiatr. 174(3), 256-265 (2016).
46. Stappenbeck, T. S. & Virgin, H. W. Accounting for reciprocal host-microbiome interactions in experimental science. Nature 534, 191-199 (2016).
47. Thompson, P. M. et al. ENIGMA and the individual: Predicting factors that affect the brain in 35 countries worldwide. Neuroimage 145, 389-408 (2017).