Supplementation of Saturated Long-Chain Fatty Acids Maintains Intestinal Eubiosis and Reduces Ethanol-induced Liver Injury in Mice
Alcoholic liver disease is a leading cause of mortality. Chronic alcohol consumption is accompanied by intestinal dysbiosis, and development of alcoholic liver disease requires gut-derived bacterial products. However, little is known about how alterations to the microbiome contribute to pathogenesis...
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| Published in | Gastroenterology (New York, N.Y. 1943) Vol. 148; no. 1; pp. 203 - 214.e16 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
01.01.2015
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| Subjects | |
| Online Access | Get full text |
| ISSN | 0016-5085 1528-0012 1528-0012 |
| DOI | 10.1053/j.gastro.2014.09.014 |
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| Abstract | Alcoholic liver disease is a leading cause of mortality. Chronic alcohol consumption is accompanied by intestinal dysbiosis, and development of alcoholic liver disease requires gut-derived bacterial products. However, little is known about how alterations to the microbiome contribute to pathogenesis of alcoholic liver disease.
We used the Tsukamoto-French mouse model, which involves continuous intragastric feeding of isocaloric diet or alcohol for 3 weeks. Bacterial DNA from the cecum was extracted for deep metagenomic sequencing. Targeted metabolomics assessed concentrations of saturated fatty acids in cecal contents. To maintain intestinal metabolic homeostasis, diets of ethanol-fed and control mice were supplemented with saturated long-chain fatty acids (LCFA). Bacterial genes involved in fatty acid biosynthesis, amounts of lactobacilli, and saturated LCFA were measured in fecal samples of nonalcoholic individuals and patients with active alcohol abuse.
Analyses of intestinal contents from mice revealed alcohol-associated changes to the intestinal metagenome and metabolome, characterized by reduced synthesis of saturated LCFA. Maintaining intestinal levels of saturated fatty acids in mice resulted in eubiosis, stabilized the intestinal gut barrier, and reduced ethanol-induced liver injury. Saturated LCFA are metabolized by commensal Lactobacillus and promote their growth. Proportions of bacterial genes involved in fatty acid biosynthesis were lower in feces from patients with active alcohol abuse than controls. Total levels of LCFA correlated with those of lactobacilli in fecal samples from patients with active alcohol abuse but not in controls.
In humans and mice, alcohol causes intestinal dysbiosis, reducing the capacity of the microbiome to synthesize saturated LCFA and the proportion of Lactobacillus species. Dietary approaches to restore levels of saturated fatty acids in the intestine might reduce ethanol-induced liver injury in patients with alcoholic liver disease. |
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| AbstractList | Alcoholic liver disease is a leading cause of mortality. Chronic alcohol consumption is accompanied by intestinal dysbiosis, and development of alcoholic liver disease requires gut-derived bacterial products. However, little is known about how alterations to the microbiome contribute to pathogenesis of alcoholic liver disease.
We used the Tsukamoto-French mouse model, which involves continuous intragastric feeding of isocaloric diet or alcohol for 3 weeks. Bacterial DNA from the cecum was extracted for deep metagenomic sequencing. Targeted metabolomics assessed concentrations of saturated fatty acids in cecal contents. To maintain intestinal metabolic homeostasis, diets of ethanol-fed and control mice were supplemented with saturated long-chain fatty acids (LCFA). Bacterial genes involved in fatty acid biosynthesis, amounts of lactobacilli, and saturated LCFA were measured in fecal samples of nonalcoholic individuals and patients with active alcohol abuse.
Analyses of intestinal contents from mice revealed alcohol-associated changes to the intestinal metagenome and metabolome, characterized by reduced synthesis of saturated LCFA. Maintaining intestinal levels of saturated fatty acids in mice resulted in eubiosis, stabilized the intestinal gut barrier, and reduced ethanol-induced liver injury. Saturated LCFA are metabolized by commensal Lactobacillus and promote their growth. Proportions of bacterial genes involved in fatty acid biosynthesis were lower in feces from patients with active alcohol abuse than controls. Total levels of LCFA correlated with those of lactobacilli in fecal samples from patients with active alcohol abuse but not in controls.
In humans and mice, alcohol causes intestinal dysbiosis, reducing the capacity of the microbiome to synthesize saturated LCFA and the proportion of Lactobacillus species. Dietary approaches to restore levels of saturated fatty acids in the intestine might reduce ethanol-induced liver injury in patients with alcoholic liver disease. Alcoholic liver disease is a leading cause of mortality. Chronic alcohol consumption is accompanied by intestinal dysbiosis, and development of alcoholic liver disease requires gut-derived bacterial products. However, little is known about how alterations to the microbiome contribute to pathogenesis of alcoholic liver disease.BACKGROUND & AIMSAlcoholic liver disease is a leading cause of mortality. Chronic alcohol consumption is accompanied by intestinal dysbiosis, and development of alcoholic liver disease requires gut-derived bacterial products. However, little is known about how alterations to the microbiome contribute to pathogenesis of alcoholic liver disease.We used the Tsukamoto-French mouse model, which involves continuous intragastric feeding of isocaloric diet or alcohol for 3 weeks. Bacterial DNA from the cecum was extracted for deep metagenomic sequencing. Targeted metabolomics assessed concentrations of saturated fatty acids in cecal contents. To maintain intestinal metabolic homeostasis, diets of ethanol-fed and control mice were supplemented with saturated long-chain fatty acids (LCFA). Bacterial genes involved in fatty acid biosynthesis, amounts of lactobacilli, and saturated LCFA were measured in fecal samples of nonalcoholic individuals and patients with active alcohol abuse.METHODSWe used the Tsukamoto-French mouse model, which involves continuous intragastric feeding of isocaloric diet or alcohol for 3 weeks. Bacterial DNA from the cecum was extracted for deep metagenomic sequencing. Targeted metabolomics assessed concentrations of saturated fatty acids in cecal contents. To maintain intestinal metabolic homeostasis, diets of ethanol-fed and control mice were supplemented with saturated long-chain fatty acids (LCFA). Bacterial genes involved in fatty acid biosynthesis, amounts of lactobacilli, and saturated LCFA were measured in fecal samples of nonalcoholic individuals and patients with active alcohol abuse.Analyses of intestinal contents from mice revealed alcohol-associated changes to the intestinal metagenome and metabolome, characterized by reduced synthesis of saturated LCFA. Maintaining intestinal levels of saturated fatty acids in mice resulted in eubiosis, stabilized the intestinal gut barrier, and reduced ethanol-induced liver injury. Saturated LCFA are metabolized by commensal Lactobacillus and promote their growth. Proportions of bacterial genes involved in fatty acid biosynthesis were lower in feces from patients with active alcohol abuse than controls. Total levels of LCFA correlated with those of lactobacilli in fecal samples from patients with active alcohol abuse but not in controls.RESULTSAnalyses of intestinal contents from mice revealed alcohol-associated changes to the intestinal metagenome and metabolome, characterized by reduced synthesis of saturated LCFA. Maintaining intestinal levels of saturated fatty acids in mice resulted in eubiosis, stabilized the intestinal gut barrier, and reduced ethanol-induced liver injury. Saturated LCFA are metabolized by commensal Lactobacillus and promote their growth. Proportions of bacterial genes involved in fatty acid biosynthesis were lower in feces from patients with active alcohol abuse than controls. Total levels of LCFA correlated with those of lactobacilli in fecal samples from patients with active alcohol abuse but not in controls.In humans and mice, alcohol causes intestinal dysbiosis, reducing the capacity of the microbiome to synthesize saturated LCFA and the proportion of Lactobacillus species. Dietary approaches to restore levels of saturated fatty acids in the intestine might reduce ethanol-induced liver injury in patients with alcoholic liver disease.CONCLUSIONSIn humans and mice, alcohol causes intestinal dysbiosis, reducing the capacity of the microbiome to synthesize saturated LCFA and the proportion of Lactobacillus species. Dietary approaches to restore levels of saturated fatty acids in the intestine might reduce ethanol-induced liver injury in patients with alcoholic liver disease. Alcoholic liver disease is a leading cause of mortality. Chronic alcohol consumption is accompanied by intestinal dysbiosis, and development of alcoholic liver disease requires gut-derived bacterial products. However, little is known about how alterations to the microbiome contribute to pathogenesis of alcoholic liver disease. We used the Tsukamoto-French mouse model, which involves continuous intragastric feeding of isocaloric diet or alcohol for 3 weeks. Bacterial DNA from the cecum was extracted for deep metagenomic sequencing. Targeted metabolomics assessed concentrations of saturated fatty acids in cecal contents. To maintain intestinal metabolic homeostasis, diets of ethanol-fed and control mice were supplemented with saturated long-chain fatty acids (LCFA). Bacterial genes involved in fatty acid biosynthesis, amounts of lactobacilli, and saturated LCFA were measured in fecal samples of nonalcoholic individuals and patients with active alcohol abuse. Analyses of intestinal contents from mice revealed alcohol-associated changes to the intestinal metagenome and metabolome, characterized by reduced synthesis of saturated LCFA. Maintaining intestinal levels of saturated fatty acids in mice resulted in eubiosis, stabilized the intestinal gut barrier, and reduced ethanol-induced liver injury. Saturated LCFA are metabolized by commensal Lactobacillus and promote their growth. Proportions of bacterial genes involved in fatty acid biosynthesis were lower in feces from patients with active alcohol abuse than controls. Total levels of LCFA correlated with those of lactobacilli in fecal samples from patients with active alcohol abuse but not in controls. In humans and mice, alcohol causes intestinal dysbiosis, reducing the capacity of the microbiome to synthesize saturated LCFA and the proportion of Lactobacillus species. Dietary approaches to restore levels of saturated fatty acids in the intestine might reduce ethanol-induced liver injury in patients with alcoholic liver disease. Background & Aims Alcoholic liver disease is a leading cause of mortality. Chronic alcohol consumption is accompanied by intestinal dysbiosis, and development of alcoholic liver disease requires gut-derived bacterial products. However, little is known about how alterations to the microbiome contribute to pathogenesis of alcoholic liver disease. Methods We used the Tsukamoto-French mouse model, which involves continuous intragastric feeding of isocaloric diet or alcohol for 3 weeks. Bacterial DNA from the cecum was extracted for deep metagenomic sequencing. Targeted metabolomics assessed concentrations of saturated fatty acids in cecal contents. To maintain intestinal metabolic homeostasis, diets of ethanol-fed and control mice were supplemented with saturated long-chain fatty acids (LCFA). Bacterial genes involved in fatty acid biosynthesis, amounts of lactobacilli, and saturated LCFA were measured in fecal samples of nonalcoholic individuals and patients with active alcohol abuse. Results Analyses of intestinal contents from mice revealed alcohol-associated changes to the intestinal metagenome and metabolome, characterized by reduced synthesis of saturated LCFA. Maintaining intestinal levels of saturated fatty acids in mice resulted in eubiosis, stabilized the intestinal gut barrier, and reduced ethanol-induced liver injury. Saturated LCFA are metabolized by commensal Lactobacillus and promote their growth. Proportions of bacterial genes involved in fatty acid biosynthesis were lower in feces from patients with active alcohol abuse than controls. Total levels of LCFA correlated with those of lactobacilli in fecal samples from patients with active alcohol abuse but not in controls. Conclusions In humans and mice, alcohol causes intestinal dysbiosis, reducing the capacity of the microbiome to synthesize saturated LCFA and the proportion of Lactobacillus species. Dietary approaches to restore levels of saturated fatty acids in the intestine might reduce ethanol-induced liver injury in patients with alcoholic liver disease. |
| Author | Zengler, Karsten DePew, Jessica Loomba, Rohit Tan, Justin Embree, Mallory Bajaj, Jasmohan S. van Pijkeren, Jan-Peter Fouts, Derrick E. Nelson, Karen E. Schnabl, Bernd Torralba, Manolito Chen, Peng Mutlu, Ece A. Ho, Samuel B. Tsukamoto, Hidekazu Keshavarzian, Ali Stärkel, Peter |
| AuthorAffiliation | 2 J. Craig Venter Institute, Rockville, MD 3 Department of Bioengineering, University of California San Diego, La Jolla, CA 5 Department of Food Science, University of Wisconsin-Madison, Madison, WI 6 Department of Medicine, VA San Diego Healthcare System, San Diego, CA 7 Division of Gastroenterology, Hepatology and Nutrition, Virginia Commonwealth University and McGuire VA Medical Center, Richmond, VA 8 Department of Medicine, Rush University Medical Center, Chicago, IL 9 Southern California Research Center for Alcoholic Liver and Pancreatic Diseases and Cirrhosis, Department of Pathology, Keck School of Medicine of the University of Southern California, Greater Los Angeles VA Healthcare System, Los Angeles, CA 1 Department of Medicine, University of California San Diego, La Jolla, CA 4 St. Luc University Hospital, Université Catholique de Louvain, Brussels, Belgium |
| AuthorAffiliation_xml | – name: 8 Department of Medicine, Rush University Medical Center, Chicago, IL – name: 9 Southern California Research Center for Alcoholic Liver and Pancreatic Diseases and Cirrhosis, Department of Pathology, Keck School of Medicine of the University of Southern California, Greater Los Angeles VA Healthcare System, Los Angeles, CA – name: 2 J. Craig Venter Institute, Rockville, MD – name: 3 Department of Bioengineering, University of California San Diego, La Jolla, CA – name: 5 Department of Food Science, University of Wisconsin-Madison, Madison, WI – name: 1 Department of Medicine, University of California San Diego, La Jolla, CA – name: 6 Department of Medicine, VA San Diego Healthcare System, San Diego, CA – name: 7 Division of Gastroenterology, Hepatology and Nutrition, Virginia Commonwealth University and McGuire VA Medical Center, Richmond, VA – name: 4 St. Luc University Hospital, Université Catholique de Louvain, Brussels, Belgium |
| Author_xml | – sequence: 1 givenname: Peng surname: Chen fullname: Chen, Peng organization: Department of Medicine, University of California San Diego, La Jolla, California – sequence: 2 givenname: Manolito surname: Torralba fullname: Torralba, Manolito organization: J. Craig Venter Institute, Rockville, Maryland – sequence: 3 givenname: Justin surname: Tan fullname: Tan, Justin organization: Department of Bioengineering, University of California San Diego, La Jolla, California – sequence: 4 givenname: Mallory surname: Embree fullname: Embree, Mallory organization: Department of Bioengineering, University of California San Diego, La Jolla, California – sequence: 5 givenname: Karsten surname: Zengler fullname: Zengler, Karsten organization: Department of Bioengineering, University of California San Diego, La Jolla, California – sequence: 6 givenname: Peter surname: Stärkel fullname: Stärkel, Peter organization: St Luc University Hospital, Université Catholique de Louvain, Brussels, Belgium – sequence: 7 givenname: Jan-Peter surname: van Pijkeren fullname: van Pijkeren, Jan-Peter organization: Department of Food Science, University of Wisconsin-Madison, Madison, Wisconsin – sequence: 8 givenname: Jessica surname: DePew fullname: DePew, Jessica organization: J. Craig Venter Institute, Rockville, Maryland – sequence: 9 givenname: Rohit surname: Loomba fullname: Loomba, Rohit organization: Department of Medicine, University of California San Diego, La Jolla, California – sequence: 10 givenname: Samuel B. surname: Ho fullname: Ho, Samuel B. organization: Department of Medicine, University of California San Diego, La Jolla, California – sequence: 11 givenname: Jasmohan S. surname: Bajaj fullname: Bajaj, Jasmohan S. organization: Division of Gastroenterology, Hepatology and Nutrition, Virginia Commonwealth University and McGuire VA Medical Center, Richmond, Virginia – sequence: 12 givenname: Ece A. surname: Mutlu fullname: Mutlu, Ece A. organization: Department of Medicine, Rush University Medical Center, Chicago, Illinois – sequence: 13 givenname: Ali surname: Keshavarzian fullname: Keshavarzian, Ali organization: Department of Medicine, Rush University Medical Center, Chicago, Illinois – sequence: 14 givenname: Hidekazu surname: Tsukamoto fullname: Tsukamoto, Hidekazu organization: Southern California Research Center for Alcoholic Liver and Pancreatic Diseases and Cirrhosis, Department of Pathology, Keck School of Medicine of the University of Southern California, Greater Los Angeles VA Healthcare System, Los Angeles, California – sequence: 15 givenname: Karen E. surname: Nelson fullname: Nelson, Karen E. organization: J. Craig Venter Institute, Rockville, Maryland – sequence: 16 givenname: Derrick E. surname: Fouts fullname: Fouts, Derrick E. organization: J. Craig Venter Institute, Rockville, Maryland – sequence: 17 givenname: Bernd surname: Schnabl fullname: Schnabl, Bernd email: beschnabl@ucsd.edu organization: Department of Medicine, University of California San Diego, La Jolla, California |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25239591$$D View this record in MEDLINE/PubMed |
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| Snippet | Alcoholic liver disease is a leading cause of mortality. Chronic alcohol consumption is accompanied by intestinal dysbiosis, and development of alcoholic liver... Background & Aims Alcoholic liver disease is a leading cause of mortality. Chronic alcohol consumption is accompanied by intestinal dysbiosis, and development... |
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| SubjectTerms | Animals Bacteria - classification Bacteria - isolation & purification Bacteria - metabolism Bacterial Translocation Dietary Supplements Disease Models, Animal Dysbiosis Ethanol Fatty Acids - administration & dosage Fatty Acids - biosynthesis Feces - chemistry Feces - microbiology Gastroenterology and Hepatology Host-Pathogen Interactions Intestinal Mucosa - metabolism Intestines - microbiology Lactobacillus - metabolism Liver Diseases, Alcoholic - etiology Liver Diseases, Alcoholic - metabolism Liver Diseases, Alcoholic - microbiology Liver Diseases, Alcoholic - prevention & control Male Metabolomics Metagenome Metagenomics Mice, Inbred C57BL Microbiome Microbiota Permeability Time Factors |
| Title | Supplementation of Saturated Long-Chain Fatty Acids Maintains Intestinal Eubiosis and Reduces Ethanol-induced Liver Injury in Mice |
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