Enteric dysbiosis associated with a mouse model of alcoholic liver disease
Open accessAbstract
The translocation of bacteria and bacterial products into the circulation contributes to alcoholic liver disease. Intestinal bacterial overgrowth is common in patients with alcoholic liver disease. The aims of our study were to investigate bacterial translocation, changes in the enteric microbiome, and its regulation by mucosal antimicrobial proteins in alcoholic liver disease. We used a mouse model of continuous intragastric feeding of alcohol or an isocaloric diet. Bacterial translocation occurred prior to changes observed in the microbiome. Quantitative changes in the intestinal microflora of these animals were assessed first using conventional culture techniques in the small and large intestine. Although we found no difference after 1 day or 1 week, intestinal bacterial overgrowth was observed in the gastrointestinal tract of mice fed alcohol for 3 weeks compared with control mice fed an isocaloric liquid diet. Because <20% of all gastrointestinal bacteria can be cultured using conventional methodologies, we performed massively parallel pyrosequencing to further assess the qualitative changes in the intestinal microbiome following alcohol exposure. Sequencing of 16S ribosomal RNA genes revealed a relative abundance of Bacteroidetes and Verrucomicrobia bacteria in mice fed alcohol compared with a relative predominance of Firmicutes bacteria in control mice. With respect to the host's transcriptome, alcohol feeding was associated with down-regulation in gene and protein expression of bactericidal c-type lectins Reg3b and Reg3g in the small intestine. Treatment with prebiotics partially restored Reg3g protein levels, reduced bacterial overgrowth, and lessened alcoholic steatohepatitis. Conclusion: Alcohol feeding is associated with intestinal bacterial overgrowth and enteric dysbiosis. Intestinal antimicrobial molecules are dysregulated following chronic alcohol feeding contributing to changes in the enteric microbiome and to alcoholic steatohepatitis. (Hepatology 2011)
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Increased blood lipopolysaccharide reflects gut leakiness and is accompanied by greater intestinal permeability to high molecular weight polyethylene glycol in alcoholic liver disease and to FITC-dextran in mouse models of alcoholic and biliary liver disease.
“Increases in blood LPS levels reflect gut leakiness and are mirrored by a number of other alterations such as increased intestinal permeability to high molecular weight polyethylene glycol in patients with ALD26 and to FITC-dextran in mouse models of alcoholic and biliary liver disease27,28.”
From The gut microbiome and liver cancer: mechanisms and clinical translation (2017) · cites this paper as [27]
Akkermansia, a mucus degrading bacteria, negatively correlates with obesity in patients and mice, although it is enriched in stool samples from alcohol-induced steatohepatitis in mice.
“The abundance of Akkermansia, a mucus degrading bacteria, has been described to negatively correlate with obesity in patients28 and mice29 although it is enriched in stool samples from alcohol-induced steatohepatitis in mice30.”
From Cholestasis induced by bile duct ligation promotes changes in the intestinal microbiome in mice (2019) · cites this paper as [30]
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Úbeda, M., Lario, M., Muñoz, L., Borrero, M.-J., Rodríguez-Serrano, M., Sánchez-Díaz, A.-M., del Campo, R., Lledó, L., Pastor, Ó., García-Bermejo, L., et al. (2016) · Journal of Hepatology · doi:10.1016/j.jhep.2015.12.010 · Cited by 178 · see citing works
The link between inflammation, bugs, the intestine and the brain in alcohol dependence
Leclercq, S., de Timary, P., Delzenne, N. M., & Stärkel, P. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.15 · Cited by 174 · see citing works
Self-citationMaccioni, L., Gao, B., Leclercq, S., Pirlot, B., Horsmans, Y., De Timary, P., Leclercq, I., Fouts, D., Schnabl, B., & Stärkel, P. (2020) · Gut Microbes · doi:10.1080/19490976.2020.1782157 · Cited by 174 · see citing works
Self-citationHu, J., Luo, H., Wang, J., Tang, W., Lu, J., Wu, S., Xiong, Z., Yang, G., Chen, Z., Lan, T., et al. (2017) · Experimental & Molecular Medicine · doi:10.1038/emm.2017.122 · Cited by 126 · see citing works
Chen, R.-C., Xu, L.-M., Du, S.-J., Huang, S.-S., Wu, H., Dong, J.-J., Huang, J.-R., Wang, X.-D., Feng, W.-K., & Chen, Y.-P. (2016) · Toxicology Letters · doi:10.1016/j.toxlet.2015.11.019 · Cited by 123 · see citing works
Alcoholic hepatitis: Translational approaches to develop targeted therapies
Mandrekar, P., Bataller, R., Tsukamoto, H., & Gao, B. (2016) · Hepatology · doi:10.1002/hep.28530 · Cited by 115 · see citing works
Self-citationMicrobiota, a key player in alcoholic liver disease
Cassard, A.-M., & Ciocan, D. (2018) · Clinical and Molecular Hepatology · doi:10.3350/cmh.2017.0067 · Cited by 100 · see citing works
Linking intestinal homeostasis and liver disease
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Self-citationCho, Y.-E., & Song, B.-J. (2018) · Redox Biology · doi:10.1016/j.redox.2018.07.012 · Cited by 78 · see citing works
Immunoglobulin A and liver diseases
Inamine, T., & Schnabl, B. (2018) · Journal of Gastroenterology · doi:10.1007/s00535-017-1400-8 · Cited by 76 · see citing works
Self-citationGut-liver axis: Recent concepts in pathophysiology in alcohol-associated liver disease
Raya Tonetti, F., Eguileor, A., Mrdjen, M., Pathak, V., Travers, J., Nagy, L. E., & Llorente, C. (2024) · Hepatology · doi:10.1097/hep.0000000000000924 · Cited by 78 · see citing works
Alcohol-associated bowel disease: new insights into pathogenesis
Maccioni, L., Fu, Y., Horsmans, Y., Leclercq, I., Stärkel, P., Kunos, G., & Gao, B. (2023) · eGastroenterology · doi:10.1136/egastro-2023-100013 · Cited by 69 · see citing works
Self-citationCholestasis induced by bile duct ligation promotes changes in the intestinal microbiome in mice
Cabrera-Rubio, R., Patterson, A. M., Cotter, P. D., & Beraza, N. (2019) · Scientific Reports · doi:10.1038/s41598-019-48784-z · Cited by 61 · see citing works
Murine Models of Acute Alcoholic Hepatitis and Their Relevance to Human Disease
Wilkin, R. J. W., Lalor, P. F., Parker, R., & Newsome, P. N. (2016) · The American Journal of Pathology · doi:10.1016/j.ajpath.2015.12.003 · Cited by 36 · see citing works
Recent insights into the pathogenesis and therapeutic targets of chronic liver diseases
Wen, Y., Ma, L., & Ju, C. (2023) · eGastroenterology · doi:10.1136/egastro-2023-100020 · Cited by 31 · see citing works
Host Factors in Dysregulation of the Gut Barrier Function during Alcohol-Associated Liver Disease
Maccioni, L., Leclercq, I. A., Schnabl, B., & Stärkel, P. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222312687 · Cited by 31 · see citing works
Self-citationPan, X.-Y., Wang, L., You, H.-M., Cheng, M., Yang, Y., Huang, C., & Li, J. (2021) · Laboratory Investigation · doi:10.1038/s41374-021-00531-7 · Cited by 26 · see citing works
Metabolic injury of hepatocytes promotes progression of NAFLD and AALD
Carvalho-Gontijo, R., Han, C., Zhang, L., Zhang, V., Hosseini, M., Mekeel, K., Schnabl, B., Loomba, R., Karin, M., Brenner, D. A., et al. (2022) · Seminars in Liver Disease · doi:10.1055/s-0042-1755316 · Cited by 23 · see citing works
Self-citation
- Authors
- Yan, A. W., Fouts, D. E., Brandl, J., Stärkel, P., Torralba, M., Schott, E., Tsukamoto, H., Nelson, K. E., Brenner, D. A., & Schnabl, B.
- Affiliations
- University of California San Diego (US)
- J. Craig Venter Institute (US)
- UCLouvain (BE)
- Charité – Universitätsmedizin Berlin (DE)
- Corresponding author
- Schnabl, Bernd
- ORCID
- Venue
- Hepatology
- Published
- 2011-01
- Volume
- 53
- Issue
- 1
- Pages
- 96-105
- ISSN
- 0270-9139 (ISSN-L)
- PMC
- PMC3059122
- OpenAlex
- W2027968599
- Cited by
- 791
- References
- 53
- Citations by year
- 2026: 23 · 2025: 45 · 2024: 77 · 2023: 58 · 2022: 70 · 2021: 81 · 2020: 79 · 2019: 58 · 2018: 62 · 2017: 60 · 2016: 38 · 2015: 49 · 2014: 34 · 2013: 23 · 2012: 19
- FWCI
- 7.17
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Hepatology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- DIAL (Catholic University of Leuven) (submittedVersion)
- Funders
- University of Southern California
- National Institutes of Health
- National Institute on Alcohol Abuse and Alcoholism (P50-AA11999, P50AA011999)
- National Institute of General Medical Sciences (R01GM041804)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK072237, K08DK081830)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Pathology and Forensic Medicine › Alcohol Consumption and Health Effects
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- alcoholic liver disease, alcoholic steatohepatitis, intestinal bacterial overgrowth, bacterial translocation, gut microbiota, Reg3b, Reg3g, C-type lectin, prebiotics, chronic alcohol feeding, Bacteroidetes, Verrucomicrobia, Firmicutes, 16S rRNA gene sequencing
- MeSH terms
- Pancreatitis-Associated Proteins, Animals, Disease Models, Animal, Fatty Liver, Alcoholic, Intestine, Small, Intestines, Liver Diseases, Alcoholic, Mice, Inbred C57BL, Proteins, RNA, Ribosomal, 16S, Bacterial Translocation, Mice
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