Total fecal microbiota transplantation alleviates high-fat diet-induced steatohepatitis in mice via beneficial regulation of gut microbiota

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Zhou, Da ^a   Pan, Qin ^a   Shen, Feng ^a   Cao, Hai Xia ^a   Ding, Wen Jin ^a   Chen, Yuan Wen ^a   Fan, Jian Gao ^a  

^a XINHUA HOSPITAL AFFILIATED TO SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOTRANSFERASE; BUTYRIC ACID;

ADIPOSE TISSUE; ANIMAL; BLOOD; BODY WEIGHT; C57BL MOUSE; CECUM; ENDOTOXEMIA; EPIDIDYMIS; FECAL MICROBIOTA TRANSPLANTATION; IMMUNOLOGY; INFLAMMATION; INJURIES; INSULIN RESISTANCE; INTESTINE FLORA; LIPID DIET; LIVER; MALE; METABOLISM; MICROBIOLOGY; NONALCOHOLIC FATTY LIVER; OBESITY; PATHOLOGY; SMALL INTESTINE; TIGHT JUNCTION;

ADIPOSE TISSUE; ANIMALS; BODY WEIGHT; BUTYRIC ACID; CECUM; DIET, HIGH-FAT; ENDOTOXEMIA; EPIDIDYMIS; FECAL MICROBIOTA TRANSPLANTATION; GASTROINTESTINAL MICROBIOME; INFLAMMATION; INSULIN RESISTANCE; INTESTINE, SMALL; LIVER; MALE; MICE, INBRED C57BL; NON-ALCOHOLIC FATTY LIVER DISEASE; OBESITY; TIGHT JUNCTIONS; TRANSAMINASES;

EID: 85019222164     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-01751-y     Document Type: Article

References (51)

1. Rinella, M. E. Nonalcoholic Fatty Liver Disease. Jama 313(2263), 5370-73, doi: 10.1001/jama.2015.5370 (2015).
2. Gkolfakis, P., Dimitriadis, G. & Triantafyllou, K. Gut microbiota and non-alcoholic fatty liver disease. Hepatobiliary & Pancreatic Diseases International 14, 572-581 (2015).
3. Marchesi, J. R. et al. The gut microbiota and host health: a new clinical frontier. Gut 65, 330-339, doi: 10.1136/gutjnl-2015-309990 (2016).
4. Compare, D. et al. Gut-liver axis: The impact of gut microbiota on non alcoholic fatty liver disease. Nutrition, Metabolism and Cardiovascular Diseases 22, 471-476, doi: 10.1016/j.numecd.2012.02.007 (2012).
5. Smits, L. P., Bouter, K. E. C., de Vos, W. M., Borody, T. J. & Nieuwdorp, M. Therapeutic Potential of Fecal Microbiota Transplantation. Gastroenterology 145, 946-953, doi: 10.1053/j.gastro.2013.08.058 (2013).
6. Gao, X., Zhu, Y., Wen, Y., Liu, G. & Wan, C. Efficacy of probiotics in nonalcoholic fatty liver disease in adult and children: A meta-analysis of randomized controlled trials. Hepatology Research 46, 1226-1233, doi: 10.1111/hepr.v46.12 (2016).
7. Das, S. K. & Balakrishnan, V. Role of Cytokines in the Pathogenesis of Non-Alcoholic Fatty Liver Disease. Indian Journal of Clinical Biochemistry 26, 202-209, doi: 10.1007/s12291-011-0121-7 (2011).
8. Hooper, L. V., Littman, D. R. & Macpherson, A. J. Interactions Between the Microbiota and the Immune System. Science 336, 1268-1273, doi: 10.1126/science.1223490 (2012).
9. Maynard, C. L., Elson, C. O., Hatton, R. D. & Weaver, C. T. Reciprocal interactions of the intestinal microbiota and immune system. Nature 489, 231-241, doi: 10.1038/nature11551 (2012).
10. Wu, H.-J. & Wu, E. The role of gut microbiota in immune homeostasis and autoimmunity. Gut Microbes 3, 4-14, doi: 10.4161/gmic.19320 (2014).
11. Suez, J. et al. Artificial sweeteners induce glucose intolerance by altering the gut microbiota. Nature 514, 181-186, doi: 10.1038/nature13793 (2014).
12. Schloss, P. D. et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75, 7537-7541, doi: 10.1128/AEM.01541-09 (2009).
13. Noval Rivas, M. et al. A microbiota signature associated with experimental food allergy promotes allergic sensitization and anaphylaxis. J Allergy Clin Immunol 131, 201-212, doi: 10.1016/j.jaci.2012.10.026 (2013).
14. Jiang, X. T. et al. Illumina sequencing of 16S rRNA tag revealed spatial variations of bacterial communities in a mangrove wetland. Microb Ecol 66, 96-104, doi: 10.1007/s00248-013-0238-8 (2013).
15. Segata, N. et al. Metagenomic biomarker discovery and explanation. Genome Biol 12, R60, doi: 10.1186/gb-2011-12-6-r60 (2011).
16. Lynch, S. V., Phimister, E. G. & Pedersen, O. The Human Intestinal Microbiome in Health and Disease. New England Journal of Medicine 375, 2369-2379, doi: 10.1056/NEJMra1600266 (2016).
17. Brandt, L. J. & Aroniadis, O. C. An overview of fecal microbiota transplantation: techniques, indications, and outcomes. Gastrointestinal Endoscopy 78, 240-249, doi: 10.1016/j.gie.2013.03.1329 (2013).
18. Vrieze, A. et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 143, 913-916 e917, doi: 10.1053/j.gastro.2012.06.031 (2012).
19. Li, J. et al. Probiotics modulated gut microbiota suppresses hepatocellular carcinoma growth in mice. Proc Natl Acad Sci USA 113, E1306-1315, doi: 10.1073/pnas.1518189113 (2016).
20. Berni Canani, R. et al. Lactobacillus rhamnosus GG-supplemented formula expands butyrate-producing bacterial strains in food allergic infants. ISME J 10, 742-750, doi: 10.1038/ismej.2015.151 (2016).
21. Le Chatelier, E. et al. Richness of human gut microbiome correlates with metabolic markers. Nature 500, 541-546, doi: 10.1038/nature12506 (2013).
22. Macfarlane, S. & Macfarlane, G. T. Regulation of short-chain fatty acid production. Proceedings of the Nutrition Society 62, 67-72, doi: 10.1079/PNS2002207 (2007).
23. Guilloteau, P. et al. From the gut to the peripheral tissues: the multiple effects of butyrate. Nutrition Research Reviews 23, 366-384, doi: 10.1017/S0954422410000247 (2010).
24. Plöger, S. et al. Microbial butyrate and its role for barrier function in the gastrointestinal tract. Annals of the New York Academy of Sciences 1258, 52-59, doi: 10.1111/j.1749-6632.2012.06553.x (2012).
25. Engen, P. A. et al. The Potential Role of Gut-Derived Inflammation in Multiple System Atrophy. Journal of Parkinson's Disease. 1-16, doi: 10.3233/JPD-160991 (2017).
26. Nova, E., Perez de Heredia, F., Gomez-Martinez, S. & Marcos, A. The Role of Probiotics on the Microbiota: Effect on Obesity. Nutr Clin Pract 31, 387-400, doi: 10.1177/0884533615620350 (2016).
27. Mishra, A. K., Dubey, V. & Ghosh, A. R. Obesity: An overview of possible role(s) of gut hormones, lipid sensing and gut microbiota. Metabolism 65, 48-65, doi: 10.1016/j.metabol.2015.10.008 (2016).
28. Cho, S.-Y. et al. Modulation of gut microbiota and delayed immunosenescence as a result of syringaresinol consumption in middle-aged mice. Scientific Reports 6, 39026, doi: 10.1038/srep39026 (2016).
29. Roberts, J. et al. An Exploratory Investigation of Endotoxin Levels in Novice Long Distance Triathletes, and the Effects of a Multi-Strain Probiotic/Prebiotic, Antioxidant Intervention. Nutrients 8, 733, doi: 10.3390/nu8110733 (2016).
30. Choi, S.-Y. et al. The role of Toll-like receptor 4 in high-glucose-induced inflammatory and fibrosis markers in human peritoneal mesothelial cells. International Urology and Nephrology 49, 171-181, doi: 10.1007/s11255-016-1430-9 (2016).
31. Khan, S. & Jena, G. Sodium butyrate, a HDAC inhibitor ameliorates eNOS, iNOS and TGF-beta1-induced fibrogenesis, apoptosis and DNA damage in the kidney of juvenile diabetic rats. Food Chem Toxicol 73, 127-139, doi: 10.1016/j.fct.2014.08.010 (2014).
32. Bulow, R. et al. Antifibrogenic effects of histone deacetylase inhibitors on pancreatic stellate cells. Biochem Pharmacol 74, 1747-1757, doi: 10.1016/j.bcp.2007.08.023 (2007).
33. Stenman, L. K., Burcelin, R. & Lahtinen, S. Establishing a causal link between gut microbes, body weight gain and glucose metabolism in humans - towards treatment with probiotics. Beneficial Microbes, 1-12 (2015).
34. Goodrich, Julia, K. et al. Human Genetics Shape the Gut Microbiome. Cell 159, 789-799, doi: 10.1016/j.cell.2014.09.053 (2014).
35. Jung, M.-J. et al. Chronic Repression of mTOR Complex 2 Induces Changes in the Gut Microbiota of Diet-induced Obese Mice. Scientific Reports 6, 30887, doi: 10.1038/srep30887 (2016).
36. Wang, J. et al. Modulation of gut microbiota during probiotic-mediated attenuation of metabolic syndrome in high fat diet-fed mice. The ISME Journal 9, 1-15, doi: 10.1038/ismej.2014.99 (2014).
37. Sommer, F. & Bäckhed, F. The gut microbiota - masters of host development and physiology. Nature Reviews Microbiology 11, 227-238, doi: 10.1038/nrmicro2974 (2013).
38. Nati, M. et al. The role of immune cells in metabolism-related liver inflammation and development of non-alcoholic steatohepatitis (NASH). Rev Endocr Metab Disord 17, 29-39, doi: 10.1007/s11154-016-9339-2 (2016).
39. Park, J.-S., Lee, E.-J., Lee, J.-C., Kim, W.-K. & Kim, H.-S. Anti-inflammatory effects of short chain fatty acids in IFN-γ-stimulated RAW 264.7 murine macrophage cells: Involvement of NF-κB and ERK signaling pathways. International Immunopharmacology 7, 70-77, doi: 10.1016/j.intimp.2006.08.015 (2007).
40. Smith, P. M. et al. The Microbial Metabolites, Short-Chain Fatty Acids, Regulate Colonic Treg Cell Homeostasis. Science 341, 569-573, doi: 10.1126/science.1241165 (2013).
41. Jin, C. J., Sellmann, C., Engstler, A. J., Ziegenhardt, D. & Bergheim, I. Supplementation of sodium butyrate protects mice from the development of non-alcoholic steatohepatitis (NASH). British Journal of Nutrition 114, 1745-1755, doi: 10.1017/S0007114515003621 (2015).
42. Olefsky, J. M. & Glass, C. K. Macrophages, Inflammation, and Insulin Resistance. Annual Review of Physiology 72, 219-246, doi: 10.1146/annurev-physiol-021909-135846 (2010).
43. Kelly, D. et al. Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shuttling of PPAR-gamma and RelA. Nat Immunol 5, 104-112, doi: 10.1038/ni1018 (2004).
44. Liu, Y. et al. 3, 3′-Diindolylmethane alleviates steatosis and the progression of NASH partly through shifting the imbalance of Treg/Th17 cells to Treg dominance. Int Immunopharmacol 23, 489-498, doi: 10.1016/j.intimp.2014.09.024 (2014).
45. Rolla, S. et al. The balance between IL-17 and IL-22 produced by liver-infiltrating T-helper cells critically controls NASH development in mice. Clin Sci (Lond) 130, 193-203, doi: 10.1042/CS20150405 (2016).
46. Sell, H., Habich, C. & Eckel, J. Adaptive immunity in obesity and insulin resistance. Nat Rev Endocrinol 8, 709-716, doi: 10.1038/nrendo.2012.114 (2012).
47. Ma, X. et al. A high-fat diet and regulatory T cells influence susceptibility to endotoxin-induced liver injury. Hepatology 46, 1519-1529, doi: 10.1002/hep.21823 (2007).
48. Ferreyra Solari, N. E. et al. The role of innate cells is coupled to a Th1-polarized immune response in pediatric nonalcoholic steatohepatitis. J Clin Immunol 32, 611-621, doi: 10.1007/s10875-011-9635-2 (2012).
49. Tang, Y. et al. Interleukin-17 exacerbates hepatic steatosis and inflammation in non-alcoholic fatty liver disease. Clin Exp Immunol 166, 281-290, doi: 10.1111/j.1365-2249.2011.04471.x (2011).
50. Xu, R., Tao, A., Zhang, S. & Zhang, M. Neutralization of interleukin-17 attenuates high fat diet-induced non-alcoholic fatty liver disease in mice. Acta Biochim Biophys Sin (Shanghai) 45, 726-733, doi: 10.1093/abbs/gmt065 (2013).
51. Saalim, M. et al. IL-22: a promising candidate to inhibit viral-induced liver disease progression and hepatocellular carcinoma. Tumour Biol 37, 105-114, doi: 10.1007/s13277-015-4294-1 (2016).