Intestinal REG3 Lectins Protect against Alcoholic Steatohepatitis by Reducing Mucosa-Associated Microbiota and Preventing Bacterial Translocation

Approximately half of all deaths from liver cirrhosis, the tenth leading cause of mortality in the United States, are related to alcohol use. Chronic alcohol consumption is accompanied by intestinal dysbiosis and bacterial overgrowth, yet little is known about the factors that alter the microbial co...

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Published in	Cell host & microbe Vol. 19; no. 2; pp. 227 - 239
Main Authors	Wang, Lirui, Fouts, Derrick E., Stärkel, Peter, Hartmann, Phillipp, Chen, Peng, Llorente, Cristina, DePew, Jessica, Moncera, Kelvin, Ho, Samuel B., Brenner, David A., Hooper, Lora V., Schnabl, Bernd
Format	Journal Article
Language	English
Published	United States Elsevier Inc 10.02.2016
Subjects	Animals Bacteria - classification Bacteria - genetics Bacteria - isolation & purification Bacterial Translocation Ethanol - adverse effects Fatty Liver, Alcoholic - genetics Fatty Liver, Alcoholic - metabolism Fatty Liver, Alcoholic - microbiology Fatty Liver, Alcoholic - prevention & control Female Gastrointestinal Microbiome Humans Liver - microbiology Lymph Nodes - microbiology Mice Mice, Knockout Mucous Membrane - microbiology Pancreatitis-Associated Proteins Proteins - genetics Proteins - metabolism
Online Access	Get full text
ISSN	1931-3128 1934-6069 1934-6069
DOI	10.1016/j.chom.2016.01.003

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Abstract	Approximately half of all deaths from liver cirrhosis, the tenth leading cause of mortality in the United States, are related to alcohol use. Chronic alcohol consumption is accompanied by intestinal dysbiosis and bacterial overgrowth, yet little is known about the factors that alter the microbial composition or their contribution to liver disease. We previously associated chronic alcohol consumption with lower intestinal levels of the antimicrobial-regenerating islet-derived (REG)-3 lectins. Here, we demonstrate that intestinal deficiency in REG3B or REG3G increases numbers of mucosa-associated bacteria and enhances bacterial translocation to the mesenteric lymph nodes and liver, promoting the progression of ethanol-induced fatty liver disease toward steatohepatitis. Overexpression of Reg3g in intestinal epithelial cells restricts bacterial colonization of mucosal surfaces, reduces bacterial translocation, and protects mice from alcohol-induced steatohepatitis. Thus, alcohol appears to impair control of the mucosa-associated microbiota, and subsequent breach of the mucosal barrier facilitates progression of alcoholic liver disease. [Display omitted] •REG3 lectins restrict the access of bacteria to the intestinal epithelium•REG3 proteins reduce bacterial translocation associated with ethanol administration•Decreased bacterial translocation protects mice from alcohol-induced steatohepatitis•Mucosa-adherent bacteria are increased in the duodenum of alcohol-dependent patients The mechanism by which chronic alcohol consumption alters the microbial composition in the intestine is unknown. Wang et al. demonstrate that alcohol reduces intestinal expression of REG3 lectins, increasing the number of mucosa-associated bacteria. The subsequent translocation of bacteria to mesenteric lymph nodes and liver exacerbates alcoholic liver disease.
AbstractList	Approximately half of all deaths from liver cirrhosis, the tenth leading cause of mortality in the United States, are related to alcohol use. Chronic alcohol consumption is accompanied by intestinal dysbiosis and bacterial overgrowth, yet little is known about the factors that alter the microbial composition or their contribution to liver disease. We previously associated chronic alcohol consumption with lower intestinal levels of the antimicrobial-regenerating islet-derived (REG)-3 lectins. Here, we demonstrate that intestinal deficiency in REG3B or REG3G increases numbers of mucosa-associated bacteria and enhances bacterial translocation to the mesenteric lymph nodes and liver, promoting the progression of ethanol-induced fatty liver disease toward steatohepatitis. Overexpression of Reg3g in intestinal epithelial cells restricts bacterial colonization of mucosal surfaces, reduces bacterial translocation, and protects mice from alcohol-induced steatohepatitis. Thus, alcohol appears to impair control of the mucosa-associated microbiota, and subsequent breach of the mucosal barrier facilitates progression of alcoholic liver disease. [Display omitted] •REG3 lectins restrict the access of bacteria to the intestinal epithelium•REG3 proteins reduce bacterial translocation associated with ethanol administration•Decreased bacterial translocation protects mice from alcohol-induced steatohepatitis•Mucosa-adherent bacteria are increased in the duodenum of alcohol-dependent patients The mechanism by which chronic alcohol consumption alters the microbial composition in the intestine is unknown. Wang et al. demonstrate that alcohol reduces intestinal expression of REG3 lectins, increasing the number of mucosa-associated bacteria. The subsequent translocation of bacteria to mesenteric lymph nodes and liver exacerbates alcoholic liver disease. Approximately half of all deaths from liver cirrhosis, the tenth leading cause of mortality in the United States, are related to alcohol use. Chronic alcohol consumption is accompanied by intestinal dysbiosis and bacterial overgrowth, yet little is known about the factors that alter the microbial composition or their contribution to liver disease. We previously associated chronic alcohol consumption with lower intestinal levels of the antimicrobial-regenerating islet-derived (REG)-3 lectins. Here, we demonstrate that intestinal deficiency in REG3B or REG3G increases numbers of mucosa-associated bacteria and enhances bacterial translocation to the mesenteric lymph nodes and liver, promoting the progression of ethanol-induced fatty liver disease toward steatohepatitis. Overexpression of Reg3g in intestinal epithelial cells restricts bacterial colonization of mucosal surfaces, reduces bacterial translocation, and protects mice from alcohol-induced steatohepatitis. Thus, alcohol appears to impair control of the mucosa-associated microbiota, and subsequent breach of the mucosal barrier facilitates progression of alcoholic liver disease.Approximately half of all deaths from liver cirrhosis, the tenth leading cause of mortality in the United States, are related to alcohol use. Chronic alcohol consumption is accompanied by intestinal dysbiosis and bacterial overgrowth, yet little is known about the factors that alter the microbial composition or their contribution to liver disease. We previously associated chronic alcohol consumption with lower intestinal levels of the antimicrobial-regenerating islet-derived (REG)-3 lectins. Here, we demonstrate that intestinal deficiency in REG3B or REG3G increases numbers of mucosa-associated bacteria and enhances bacterial translocation to the mesenteric lymph nodes and liver, promoting the progression of ethanol-induced fatty liver disease toward steatohepatitis. Overexpression of Reg3g in intestinal epithelial cells restricts bacterial colonization of mucosal surfaces, reduces bacterial translocation, and protects mice from alcohol-induced steatohepatitis. Thus, alcohol appears to impair control of the mucosa-associated microbiota, and subsequent breach of the mucosal barrier facilitates progression of alcoholic liver disease. Approximately half of all deaths from liver cirrhosis, the tenth leading cause of mortality in the United States, are related to alcohol use. Chronic alcohol consumption is accompanied by intestinal dysbiosis and bacterial overgrowth, yet little is known about the factors that alter the microbial composition or their contribution to liver disease. We previously associated chronic alcohol consumption with lower intestinal levels of the antimicrobial-regenerating islet-derived (REG)-3 lectins. Here, we demonstrate that intestinal deficiency in REG3B or REG3G increases numbers of mucosa-associated bacteria and enhances bacterial translocation to the mesenteric lymph nodes and liver, promoting the progression of ethanol-induced fatty liver disease toward steatohepatitis. Overexpression of Reg3g in intestinal epithelial cells restricts bacterial colonization of mucosal surfaces, reduces bacterial translocation, and protects mice from alcohol-induced steatohepatitis. Thus, alcohol appears to impair control of the mucosa-associated microbiota, and subsequent breach of the mucosal barrier facilitates progression of alcoholic liver disease. Approximately half of all deaths from liver cirrhosis, the 10 th leading cause of mortality in the United States, are related to alcohol use. Chronic alcohol consumption is accompanied by intestinal dysbiosis and bacterial overgrowth, yet little is known about the factors that alter the microbial composition or their contribution to liver disease. We previously associated chronic alcohol consumption with lower intestinal levels of the antimicrobial-regenerating islet-derived (REG)-3 lectins. Here, we demonstrate that intestinal deficiency in REG3B or REG3G increases numbers of mucosa-associated bacteria and enhances bacterial translocation to the mesenteric lymph nodes and liver, promoting the progression of ethanol-induced fatty liver disease toward steatohepatitis. Overexpression of Reg3g in intestinal epithelial cells restricts bacterial colonization of mucosal surfaces, reduces bacterial translocation, and protects mice from alcohol-induced steatohepatitis. Thus, alcohol appears to impair control of the mucosa-associated microbiota, and subsequent breach of the mucosal barrier facilitates progression of alcoholic liver disease.
Author	DePew, Jessica Hartmann, Phillipp Moncera, Kelvin Ho, Samuel B. Schnabl, Bernd Hooper, Lora V. Chen, Peng Wang, Lirui Brenner, David A. Fouts, Derrick E. Llorente, Cristina Stärkel, Peter
AuthorAffiliation	1 Department of Medicine, University of California San Diego, La Jolla, CA 92093, USA 4 St. Luc University Hospital, Université Catholique de Louvain, Brussels B-1200, Belgium 2 Department of Medicine, VA San Diego Healthcare System, San Diego, CA 92161, USA 3 J. Craig Venter Institute, Rockville, MD 20850, USA 6 Department of Immunology, The University of Texas Southwestern Medical Center, Dallas, TX 75390, USA 5 Howard Hughes Medical Institute, The University of Texas Southwestern Medical Center, Dallas, TX 75390, USA
AuthorAffiliation_xml	– name: 3 J. Craig Venter Institute, Rockville, MD 20850, USA – name: 6 Department of Immunology, The University of Texas Southwestern Medical Center, Dallas, TX 75390, USA – name: 4 St. Luc University Hospital, Université Catholique de Louvain, Brussels B-1200, Belgium – name: 5 Howard Hughes Medical Institute, The University of Texas Southwestern Medical Center, Dallas, TX 75390, USA – name: 2 Department of Medicine, VA San Diego Healthcare System, San Diego, CA 92161, USA – name: 1 Department of Medicine, University of California San Diego, La Jolla, CA 92093, USA
Author_xml	– sequence: 1 givenname: Lirui surname: Wang fullname: Wang, Lirui organization: Department of Medicine, University of California San Diego, La Jolla, CA 92093, USA – sequence: 2 givenname: Derrick E. surname: Fouts fullname: Fouts, Derrick E. organization: J. Craig Venter Institute, Rockville, MD 20850, USA – sequence: 3 givenname: Peter surname: Stärkel fullname: Stärkel, Peter organization: St. Luc University Hospital, Université Catholique de Louvain, Brussels 1200, Belgium – sequence: 4 givenname: Phillipp surname: Hartmann fullname: Hartmann, Phillipp organization: Department of Medicine, University of California San Diego, La Jolla, CA 92093, USA – sequence: 5 givenname: Peng surname: Chen fullname: Chen, Peng organization: Department of Medicine, University of California San Diego, La Jolla, CA 92093, USA – sequence: 6 givenname: Cristina surname: Llorente fullname: Llorente, Cristina organization: Department of Medicine, University of California San Diego, La Jolla, CA 92093, USA – sequence: 7 givenname: Jessica surname: DePew fullname: DePew, Jessica organization: J. Craig Venter Institute, Rockville, MD 20850, USA – sequence: 8 givenname: Kelvin surname: Moncera fullname: Moncera, Kelvin organization: J. Craig Venter Institute, Rockville, MD 20850, USA – sequence: 9 givenname: Samuel B. surname: Ho fullname: Ho, Samuel B. organization: Department of Medicine, University of California San Diego, La Jolla, CA 92093, USA – sequence: 10 givenname: David A. surname: Brenner fullname: Brenner, David A. organization: Department of Medicine, University of California San Diego, La Jolla, CA 92093, USA – sequence: 11 givenname: Lora V. surname: Hooper fullname: Hooper, Lora V. organization: Howard Hughes Medical Institute – sequence: 12 givenname: Bernd surname: Schnabl fullname: Schnabl, Bernd email: beschnabl@ucsd.edu organization: Department of Medicine, University of California San Diego, La Jolla, CA 92093, USA
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/26867181$$D View this record in MEDLINE/PubMed
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Snippet	Approximately half of all deaths from liver cirrhosis, the tenth leading cause of mortality in the United States, are related to alcohol use. Chronic alcohol... Approximately half of all deaths from liver cirrhosis, the 10 th leading cause of mortality in the United States, are related to alcohol use. Chronic alcohol...
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SubjectTerms	Animals Bacteria - classification Bacteria - genetics Bacteria - isolation & purification Bacterial Translocation Ethanol - adverse effects Fatty Liver, Alcoholic - genetics Fatty Liver, Alcoholic - metabolism Fatty Liver, Alcoholic - microbiology Fatty Liver, Alcoholic - prevention & control Female Gastrointestinal Microbiome Humans Liver - microbiology Lymph Nodes - microbiology Mice Mice, Knockout Mucous Membrane - microbiology Pancreatitis-Associated Proteins Proteins - genetics Proteins - metabolism
Title	Intestinal REG3 Lectins Protect against Alcoholic Steatohepatitis by Reducing Mucosa-Associated Microbiota and Preventing Bacterial Translocation
URI	https://dx.doi.org/10.1016/j.chom.2016.01.003 https://www.ncbi.nlm.nih.gov/pubmed/26867181 https://www.proquest.com/docview/1765111892 https://pubmed.ncbi.nlm.nih.gov/PMC4786170
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