Fecal microbiota manipulation prevents dysbiosis and alcohol-induced liver injury in mice

Journal of Hepatology

Volumn 66, Issue 4, 2017, Pages 806-815

  Ferrere, Gladys ^a,b   Wrzosek, Laura ^a,b   Cailleux, Frédéric ^a,b   Turpin, Williams ^c,d   Puchois, Virginie ^a,b   Spatz, Madeleine ^a,b   Ciocan, Dragos ^a,b   Rainteau, Dominique ^e,f,g,h   Humbert, Lydie ^e,f,g   Hugot, Cindy ^a,b   Gaudin, Françoise ^a,b   Noordine, Marie Louise ⁱ   Robert, Véronique ⁱ   Berrebi, Dominique ^a,j   Thomas, Muriel ⁱ   Naveau, Sylvie ^a,b,k   Perlemuter, Gabriel ^a,b,k   Cassard, Anne Marie ^a,b  

^a Universite Paris Sud   (France)

^b IPSIT   (France)

^c MOUNT SINAI HOSPITAL   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

^e SORBONNE UNIVERSITÉ   (France)

^f INSERM   (France)

^g CNRS   (France)

^h HÔPITAL SAINT ANTOINE   (France)

ⁱ AGROPARISTECH   (France)

^j HÔPITAL ROBERT DEBRÉ   (France)

^k HÔPITAL ANTOINE BÉCLÈRE   (France)

more..

Author keywords

Alcohol drinking; Bacteroides; Dysbiosis; Fatty liver; Fecal microbiota transplantation; Gastrointestinal microbiome; Liver diseases, alcoholic; Microbiota; Prebiotic

Indexed keywords

ALANINE AMINOTRANSFERASE; INTERLEUKIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; PREBIOTIC AGENT; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR; BILE ACID; PECTIN;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ALCOHOL LIVER CIRRHOSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTEROIDES; CONTROLLED STUDY; DYSBIOSIS; FATTY LIVER; FECAL MICROBIOTA TRANSPLANTATION; FEMALE; HEPATITIS; HOMEOSTASIS; INTESTINE; LIPID LIVER LEVEL; MOUSE; NONHUMAN; PRIORITY JOURNAL; ADMINISTRATION AND DOSAGE; ALCOHOL LIVER DISEASE; ANIMAL; C57BL MOUSE; DIETARY FIBER; DISEASE MODEL; DISEASE PREDISPOSITION; GENETICS; HUMAN; INTESTINE FLORA; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

ANIMALS; BACTEROIDES; BILE ACIDS AND SALTS; DIETARY FIBER; DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; DYSBIOSIS; FECAL MICROBIOTA TRANSPLANTATION; FEMALE; GASTROINTESTINAL MICROBIOME; HUMANS; LIVER DISEASES, ALCOHOLIC; MICE; MICE, INBRED C57BL; PECTINS; PREBIOTICS;

EID: 85009807664     PISSN: 01688278     EISSN: 16000641     Source Type: Journal    
DOI: 10.1016/j.jhep.2016.11.008     Document Type: Article

References (43)

1. [1] Teli, M.R., Day, C.P., Burt, A.D., Bennett, M.K., James, O.F., Determinants of progression to cirrhosis or fibrosis in pure alcoholic fatty liver. Lancet 346 (1995), 987–990.
2. [2] Henao-Mejia, J., Elinav, E., Thaiss, C.A., Flavell, R.A., The intestinal microbiota in chronic liver disease. Adv Immunol 117 (2013), 73–97.
3. [3] Lozupone, C.A., Stombaugh, J.I., Gordon, J.I., Jansson, J.K., Knight, R., Diversity, stability and resilience of the human gut microbiota. Nature 489 (2012), 220–230.
4. [4] Johansson, M.E., Sjovall, H., Hansson, G.C., The gastrointestinal mucus system in health and disease. Nat Rev Gastroenterol Hepatol 10 (2013), 352–361.
5. [5] Wrzosek, L., Miquel, S., Noordine, M.L., Bouet, S., Joncquel Chevalier-Curt, M., Robert, V., et al. Bacteroides thetaiotaomicron and Faecalibacterium prausnitzii influence the production of mucus glycans and the development of goblet cells in the colonic epithelium of a gnotobiotic model rodent. BMC Biol, 11, 2013, 61.
6. [6] Buffie, C.G., Pamer, E.G., Microbiota-mediated colonization resistance against intestinal pathogens. Nat Rev Immunol 13 (2013), 790–801.
7. [7] Rao, R., Endotoxemia and gut barrier dysfunction in alcoholic liver disease. Hepatology 50 (2009), 638–644.
8. [8] Chen, P., Starkel, P., Turner, J.R., Ho, S.B., Schnabl, B., Dysbiosis-induced intestinal inflammation activates TNFRI and mediates alcoholic liver disease in mice. Hepatology 61 (2015), 883–894.
9. [9] Keshavarzian, A., Farhadi, A., Forsyth, C.B., Rangan, J., Jakate, S., Shaikh, M., et al. Evidence that chronic alcohol exposure promotes intestinal oxidative stress, intestinal hyperpermeability and endotoxemia prior to development of alcoholic steatohepatitis in rats. J Hepatol 50 (2009), 538–547.
10. [10] Szabo, G., Gut-liver axis in alcoholic liver disease. Gastroenterology 148 (2015), 30–36.
11. [11] Bajaj, J.S., Heuman, D.M., Hylemon, P.B., Sanyal, A.J., White, M.B., Monteith, P., et al. Altered profile of human gut microbiome is associated with cirrhosis and its complications. J Hepatol 60 (2014), 940–947.
12. [12] Qin, N., Yang, F., Li, A., Prifti, E., Chen, Y., Shao, L., et al. Alterations of the human gut microbiome in liver cirrhosis. Nature 513 (2014), 59–64.
13. [13] Llopis, M., Cassard, A.M., Wrzosek, L., Boschat, L., Bruneau, A., Ferrere, G., et al. Intestinal microbiota contributes to individual susceptibility to alcoholic liver disease. Gut 65 (2016), 830–839.
14. [14] Bull-Otterson, L., Feng, W., Kirpich, I., Wang, Y., Qin, X., Liu, Y., et al. Metagenomic analyses of alcohol induced pathogenic alterations in the intestinal microbiome and the effect of Lactobacillus rhamnosus GG treatment. PLoS One, 8, 2013, e53028.
15. [15] Forsyth, C.B., Farhadi, A., Jakate, S.M., Tang, Y., Shaikh, M., Keshavarzian, A., Lactobacillus GG treatment ameliorates alcohol-induced intestinal oxidative stress, gut leakiness, and liver injury in a rat model of alcoholic steatohepatitis. Alcohol 43 (2009), 163–172.
16. [16] Yan, A.W., Fouts, D.E., Brandl, J., Starkel, P., Torralba, M., Schott, E., et al. Enteric dysbiosis associated with a mouse model of alcoholic liver disease. Hepatology 53 (2011), 96–105.
17. [17] Kirpich, I.A., Solovieva, N.V., Leikhter, S.N., Shidakova, N.A., Lebedeva, O.V., Sidorov, P.I., et al. Probiotics restore bowel flora and improve liver enzymes in human alcohol-induced liver injury: a pilot study. Alcohol 42 (2008), 675–682.
18. [18] Tomas, J., Langella, P., Cherbuy, C., The intestinal microbiota in the rat model: major breakthroughs from new technologies. Anim Health Res Rev 13 (2012), 54–63.
19. [19] Gustot, T., Lemmers, A., Moreno, C., Nagy, N., Quertinmont, E., Nicaise, C., et al. Differential liver sensitization to Toll-like receptor pathways in mice with alcoholic fatty liver. Hepatology 43 (2006), 989–1000.
20. [20] Ki, S.H., Park, O., Zheng, M., Morales-Ibanez, O., Kolls, J.K., Bataller, R., et al. Interleukin-22 treatment ameliorates alcoholic liver injury in a murine model of chronic-binge ethanol feeding: role of signal transducer and activator of transcription 3. Hepatology 52 (2010), 1291–1300.
21. [21] Xie, G., Zhong, W., Li, H., Li, Q., Qiu, Y., Zheng, X., et al. Alteration of bile acid metabolism in the rat induced by chronic ethanol consumption. FASEB J 27 (2013), 3583–3593.
22. [22] Manley, S., Ding, W., Role of farnesoid X receptor and bile acids in alcoholic liver disease. Acta Pharm Sin B 5 (2015), 158–167.
23. [23] Stenman, L.K., Holma, R., Eggert, A., Korpela, R., A novel mechanism for gut barrier dysfunction by dietary fat: epithelial disruption by hydrophobic bile acids. Am J Physiol Gastrointest Liver Physiol 304 (2013), G227–G234.
24. [24] Chen, P., Torralba, M., Tan, J., Embree, M., Zengler, K., Starkel, P., et al. Supplementation of saturated long-chain fatty acids maintains intestinal eubiosis and reduces ethanol-induced liver injury in mice. Gastroenterology, 148, 2015, e216.
25. [25] Yoseph, B.P., Breed, E., Overgaard, C.E., Ward, C.J., Liang, Z., Wagener, M.E., et al. Chronic alcohol ingestion increases mortality and organ injury in a murine model of septic peritonitis. PLoS One, 8, 2013, e62792.
26. [26] Zhong, W., Li, Q., Xie, G., Sun, X., Tan, X., Jia, W., et al. Dietary fat sources differentially modulate intestinal barrier and hepatic inflammation in alcohol-induced liver injury in rats. Am J Physiol Gastrointest Liver Physiol 305 (2013), G919–G932.
27. [27] Dongowski, G., Lorenz, A., Proll, J., The degree of methylation influences the degradation of pectin in the intestinal tract of rats and in vitro. J Nutr 132 (2002), 1935–1944.
28. [28] Willing, B.P., Vacharaksa, A., Croxen, M., Thanachayanont, T., Finlay, B.B., Altering host resistance to infections through microbial transplantation. PLoS One, 6, 2011, e26988.
29. [29] Gunness, P., Gidley, M.J., Mechanisms underlying the cholesterol-lowering properties of soluble dietary fibre polysaccharides. Food Funct 1 (2010), 149–155.
30. [30] Dongowski, G., Lorenz, A., Intestinal steroids in rats are influenced by the structural parameters of pectin. J Nutr Biochem 15 (2004), 196–205.
31. [31] Chen, Y., Yang, F., Lu, H., Wang, B., Lei, D., Wang, Y., et al. Characterization of fecal microbial communities in patients with liver cirrhosis. Hepatology 54 (2011), 562–572.
32. [32] Kakiyama, G., Pandak, W.M., Gillevet, P.M., Hylemon, P.B., Heuman, D.M., Daita, K., et al. Modulation of the fecal bile acid profile by gut microbiota in cirrhosis. J Hepatol 58 (2013), 949–955.
33. [33] Nelson, A.M., Elftman, M.D., Pinto, A.K., Baldridge, M., Hooper, P., Kuczynski, J., et al. Murine norovirus infection does not cause major disruptions in the murine intestinal microbiota. Microbiome, 1, 2013, 7.
34. [34] Johansson, M.E., Phillipson, M., Petersson, J., Velcich, A., Holm, L., Hansson, G.C., The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci U S A 105 (2008), 15064–15069.
35. [35] Grewal, R.K., Mahmood, A., Ethanol induced changes in glycosylation of mucins in rat intestine. Ann Gastroenterol, 22, 2009.
36. [36] Hartmann, P., Chen, P., Wang, H.J., Wang, L., McCole, D.F., Brandl, K., et al. Deficiency of intestinal mucin-2 ameliorates experimental alcoholic liver disease in mice. Hepatology 58 (2013), 108–119.
37. [37] Wang, L., Fouts, D.E., Starkel, P., Hartmann, P., Chen, P., Llorente, C., et al. Intestinal REG3 lectins protect against alcoholic steatohepatitis by reducing mucosa-associated microbiota and preventing bacterial translocation. Cell Host Microbe 19 (2016), 227–239.
38. [38] Le Chatelier, E., Nielsen, T., Qin, J., Prifti, E., Hildebrand, F., Falony, G., et al. Richness of human gut microbiome correlates with metabolic markers. Nature 500 (2013), 541–546.
39. [39] Manichanh, C., Rigottier-Gois, L., Bonnaud, E., Gloux, K., Pelletier, E., Frangeul, L., et al. Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut 55 (2006), 205–211.
40. [40] Shin, N.R., Whon, T.W., Bae, J.W., Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol 33 (2015), 496–503.
41. [41] Carvalho, F.A., Koren, O., Goodrich, J.K., Johansson, M.E., Nalbantoglu, I., Aitken, J.D., et al. Transient inability to manage proteobacteria promotes chronic gut inflammation in TLR5-deficient mice. Cell Host Microbe 12 (2012), 139–152.
42. [42] Neyrinck, A.M., Etxeberria, U., Taminiau, B., Daube, G., Van Hul, M., Everard, A., et al. Rhubarb extract prevents hepatic inflammation induced by acute alcohol intake, an effect related to the modulation of the gut microbiota. Mol Nutr Food Res, 2016.
43. [43] Machiels, K., Joossens, M., Sabino, J., De Preter, V., Arijs, I., Eeckhaut, V., et al. A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut 63 (2014), 1275–1283.