Gut-Microbiota-Metabolite Axis in Early Renal Function Decline
Several circulating metabolites derived from bacterial protein fermentation have been found to be inversely associated with renal function but the timing and disease severity is unclear. The aim of this study is to explore the relationship between indoxyl-sulfate, p-cresyl-sulfate, phenylacetylgluta...
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| creator | Barrios, Clara Beaumont, Michelle Pallister, Tess Villar, Judith Goodrich, Julia K Clark, Andrew Pascual, Julio Ley, Ruth E Spector, Tim D Bell, Jordana T Menni, Cristina |
| description | Several circulating metabolites derived from bacterial protein fermentation have been found to be inversely associated with renal function but the timing and disease severity is unclear. The aim of this study is to explore the relationship between indoxyl-sulfate, p-cresyl-sulfate, phenylacetylglutamine and gut-microbial profiles in early renal function decline.
Indoxyl-sulfate (Beta(SE) = -2.74(0.24); P = 8.8x10-29), p-cresyl-sulfate (-1.99(0.24), P = 4.6x10-16), and phenylacetylglutamine(-2.73 (0.25), P = 1.2x10-25) were inversely associated with eGFR in a large population base cohort (TwinsUK, n = 4439) with minimal renal function decline. In a sub-sample of 855 individuals, we analysed metabolite associations with 16S gut microbiome profiles (909 profiles, QIIME 1.7.0). Three Operational Taxonomic Units (OTUs) were significantly associated with indoxyl-sulfate and 52 with phenylacetylglutamine after multiple testing; while one OTU was nominally associated with p-cresyl sulfate. All 56 microbial members belong to the order Clostridiales and are represented by anaerobic Gram-positive families Christensenellaceae, Ruminococcaceae and Lachnospiraceae. Within these, three microbes were also associated with eGFR.
Our data suggest that indoxyl-sulfate, p-cresyl-sulfate and phenylacetylglutamine are early markers of renal function decline. Changes in the intestinal flora associated with these metabolites are detectable in early kidney disease. Future efforts should dissect this relationship to improve early diagnostics and therapeutics strategies. |
| doi_str_mv | 10.1371/journal.pone.0134311 |
| format | Article |
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Indoxyl-sulfate (Beta(SE) = -2.74(0.24); P = 8.8x10-29), p-cresyl-sulfate (-1.99(0.24), P = 4.6x10-16), and phenylacetylglutamine(-2.73 (0.25), P = 1.2x10-25) were inversely associated with eGFR in a large population base cohort (TwinsUK, n = 4439) with minimal renal function decline. In a sub-sample of 855 individuals, we analysed metabolite associations with 16S gut microbiome profiles (909 profiles, QIIME 1.7.0). Three Operational Taxonomic Units (OTUs) were significantly associated with indoxyl-sulfate and 52 with phenylacetylglutamine after multiple testing; while one OTU was nominally associated with p-cresyl sulfate. All 56 microbial members belong to the order Clostridiales and are represented by anaerobic Gram-positive families Christensenellaceae, Ruminococcaceae and Lachnospiraceae. Within these, three microbes were also associated with eGFR.
Our data suggest that indoxyl-sulfate, p-cresyl-sulfate and phenylacetylglutamine are early markers of renal function decline. Changes in the intestinal flora associated with these metabolites are detectable in early kidney disease. Future efforts should dissect this relationship to improve early diagnostics and therapeutics strategies.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0134311</identifier><identifier>PMID: 26241311</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adult ; Aged ; Aged, 80 and over ; Anaerobic microorganisms ; Body Mass Index ; Cardiovascular disease ; Clostridiales ; Clostridiales - classification ; Clostridiales - isolation & purification ; Clostridiales - metabolism ; Cresols - blood ; Cross-Sectional Studies ; Diabetes ; Diabetes Mellitus, Type 2 - blood ; Diabetes Mellitus, Type 2 - genetics ; Diabetes Mellitus, Type 2 - microbiology ; Diabetic Nephropathies - blood ; Diabetic Nephropathies - genetics ; Diabetic Nephropathies - microbiology ; Digestive system ; Digestive tract ; Diseases in Twins - blood ; Diseases in Twins - genetics ; Diseases in Twins - microbiology ; Epidemiology ; Epidermal growth factor receptors ; Feces - microbiology ; Female ; Fermentation ; Flora ; Gastrointestinal Microbiome - physiology ; Gastrointestinal tract ; Genetics ; Glomerular Filtration Rate ; Glutamine - analogs & derivatives ; Glutamine - blood ; Health aspects ; Hospitals ; Humans ; Indican - blood ; Infectious diseases ; Intestinal microflora ; Intestine ; Kidney diseases ; Kidney Diseases - blood ; Kidney Diseases - genetics ; Kidney Diseases - microbiology ; Male ; Metabolism ; Metabolites ; Metabolome ; Microbiomes ; Microbiota ; Microbiota (Symbiotic organisms) ; Microorganisms ; Middle Aged ; Molecular biology ; Nephrology ; Physiological aspects ; Population ; Proteins ; Renal function ; Ribotyping ; Studies ; Sulfates ; Sulfuric Acid Esters - blood ; Taxonomy</subject><ispartof>PloS one, 2015-08, Vol.10 (8), p.e0134311-e0134311</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Barrios et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2015 Barrios et al 2015 Barrios et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c791t-2e8892d5372dfb4b10c3b5fa80127f5c74cc71436686ffbad1d7c092cf53f83d3</citedby><cites>FETCH-LOGICAL-c791t-2e8892d5372dfb4b10c3b5fa80127f5c74cc71436686ffbad1d7c092cf53f83d3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4524635/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4524635/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,725,778,782,862,883,2098,2917,23849,27907,27908,53774,53776,79351,79352</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26241311$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Remuzzi, Giuseppe</contributor><creatorcontrib>Barrios, Clara</creatorcontrib><creatorcontrib>Beaumont, Michelle</creatorcontrib><creatorcontrib>Pallister, Tess</creatorcontrib><creatorcontrib>Villar, Judith</creatorcontrib><creatorcontrib>Goodrich, Julia K</creatorcontrib><creatorcontrib>Clark, Andrew</creatorcontrib><creatorcontrib>Pascual, Julio</creatorcontrib><creatorcontrib>Ley, Ruth E</creatorcontrib><creatorcontrib>Spector, Tim D</creatorcontrib><creatorcontrib>Bell, Jordana T</creatorcontrib><creatorcontrib>Menni, Cristina</creatorcontrib><title>Gut-Microbiota-Metabolite Axis in Early Renal Function Decline</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Several circulating metabolites derived from bacterial protein fermentation have been found to be inversely associated with renal function but the timing and disease severity is unclear. The aim of this study is to explore the relationship between indoxyl-sulfate, p-cresyl-sulfate, phenylacetylglutamine and gut-microbial profiles in early renal function decline.
Indoxyl-sulfate (Beta(SE) = -2.74(0.24); P = 8.8x10-29), p-cresyl-sulfate (-1.99(0.24), P = 4.6x10-16), and phenylacetylglutamine(-2.73 (0.25), P = 1.2x10-25) were inversely associated with eGFR in a large population base cohort (TwinsUK, n = 4439) with minimal renal function decline. In a sub-sample of 855 individuals, we analysed metabolite associations with 16S gut microbiome profiles (909 profiles, QIIME 1.7.0). Three Operational Taxonomic Units (OTUs) were significantly associated with indoxyl-sulfate and 52 with phenylacetylglutamine after multiple testing; while one OTU was nominally associated with p-cresyl sulfate. All 56 microbial members belong to the order Clostridiales and are represented by anaerobic Gram-positive families Christensenellaceae, Ruminococcaceae and Lachnospiraceae. Within these, three microbes were also associated with eGFR.
Our data suggest that indoxyl-sulfate, p-cresyl-sulfate and phenylacetylglutamine are early markers of renal function decline. Changes in the intestinal flora associated with these metabolites are detectable in early kidney disease. Future efforts should dissect this relationship to improve early diagnostics and therapeutics strategies.</description><subject>Adult</subject><subject>Aged</subject><subject>Aged, 80 and over</subject><subject>Anaerobic microorganisms</subject><subject>Body Mass Index</subject><subject>Cardiovascular disease</subject><subject>Clostridiales</subject><subject>Clostridiales - classification</subject><subject>Clostridiales - isolation & purification</subject><subject>Clostridiales - metabolism</subject><subject>Cresols - blood</subject><subject>Cross-Sectional Studies</subject><subject>Diabetes</subject><subject>Diabetes Mellitus, Type 2 - blood</subject><subject>Diabetes Mellitus, Type 2 - genetics</subject><subject>Diabetes Mellitus, Type 2 - microbiology</subject><subject>Diabetic Nephropathies - blood</subject><subject>Diabetic Nephropathies - genetics</subject><subject>Diabetic Nephropathies - microbiology</subject><subject>Digestive system</subject><subject>Digestive tract</subject><subject>Diseases in Twins - blood</subject><subject>Diseases in Twins - genetics</subject><subject>Diseases in Twins - microbiology</subject><subject>Epidemiology</subject><subject>Epidermal growth factor receptors</subject><subject>Feces - microbiology</subject><subject>Female</subject><subject>Fermentation</subject><subject>Flora</subject><subject>Gastrointestinal Microbiome - physiology</subject><subject>Gastrointestinal tract</subject><subject>Genetics</subject><subject>Glomerular Filtration Rate</subject><subject>Glutamine - analogs & derivatives</subject><subject>Glutamine - blood</subject><subject>Health aspects</subject><subject>Hospitals</subject><subject>Humans</subject><subject>Indican - blood</subject><subject>Infectious diseases</subject><subject>Intestinal microflora</subject><subject>Intestine</subject><subject>Kidney diseases</subject><subject>Kidney Diseases - blood</subject><subject>Kidney Diseases - genetics</subject><subject>Kidney Diseases - microbiology</subject><subject>Male</subject><subject>Metabolism</subject><subject>Metabolites</subject><subject>Metabolome</subject><subject>Microbiomes</subject><subject>Microbiota</subject><subject>Microbiota (Symbiotic organisms)</subject><subject>Microorganisms</subject><subject>Middle Aged</subject><subject>Molecular biology</subject><subject>Nephrology</subject><subject>Physiological aspects</subject><subject>Population</subject><subject>Proteins</subject><subject>Renal function</subject><subject>Ribotyping</subject><subject>Studies</subject><subject>Sulfates</subject><subject>Sulfuric Acid Esters - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Barrios, Clara</au><au>Beaumont, Michelle</au><au>Pallister, Tess</au><au>Villar, Judith</au><au>Goodrich, Julia K</au><au>Clark, Andrew</au><au>Pascual, Julio</au><au>Ley, Ruth E</au><au>Spector, Tim D</au><au>Bell, Jordana T</au><au>Menni, Cristina</au><au>Remuzzi, Giuseppe</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Gut-Microbiota-Metabolite Axis in Early Renal Function Decline</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-08-04</date><risdate>2015</risdate><volume>10</volume><issue>8</issue><spage>e0134311</spage><epage>e0134311</epage><pages>e0134311-e0134311</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Several circulating metabolites derived from bacterial protein fermentation have been found to be inversely associated with renal function but the timing and disease severity is unclear. The aim of this study is to explore the relationship between indoxyl-sulfate, p-cresyl-sulfate, phenylacetylglutamine and gut-microbial profiles in early renal function decline.
Indoxyl-sulfate (Beta(SE) = -2.74(0.24); P = 8.8x10-29), p-cresyl-sulfate (-1.99(0.24), P = 4.6x10-16), and phenylacetylglutamine(-2.73 (0.25), P = 1.2x10-25) were inversely associated with eGFR in a large population base cohort (TwinsUK, n = 4439) with minimal renal function decline. In a sub-sample of 855 individuals, we analysed metabolite associations with 16S gut microbiome profiles (909 profiles, QIIME 1.7.0). Three Operational Taxonomic Units (OTUs) were significantly associated with indoxyl-sulfate and 52 with phenylacetylglutamine after multiple testing; while one OTU was nominally associated with p-cresyl sulfate. All 56 microbial members belong to the order Clostridiales and are represented by anaerobic Gram-positive families Christensenellaceae, Ruminococcaceae and Lachnospiraceae. Within these, three microbes were also associated with eGFR.
Our data suggest that indoxyl-sulfate, p-cresyl-sulfate and phenylacetylglutamine are early markers of renal function decline. Changes in the intestinal flora associated with these metabolites are detectable in early kidney disease. Future efforts should dissect this relationship to improve early diagnostics and therapeutics strategies.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26241311</pmid><doi>10.1371/journal.pone.0134311</doi><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2015-08, Vol.10 (8), p.e0134311-e0134311 |
| issn | 1932-6203 1932-6203 |
| language | eng |
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| subjects | Adult Aged Aged, 80 and over Anaerobic microorganisms Body Mass Index Cardiovascular disease Clostridiales Clostridiales - classification Clostridiales - isolation & purification Clostridiales - metabolism Cresols - blood Cross-Sectional Studies Diabetes Diabetes Mellitus, Type 2 - blood Diabetes Mellitus, Type 2 - genetics Diabetes Mellitus, Type 2 - microbiology Diabetic Nephropathies - blood Diabetic Nephropathies - genetics Diabetic Nephropathies - microbiology Digestive system Digestive tract Diseases in Twins - blood Diseases in Twins - genetics Diseases in Twins - microbiology Epidemiology Epidermal growth factor receptors Feces - microbiology Female Fermentation Flora Gastrointestinal Microbiome - physiology Gastrointestinal tract Genetics Glomerular Filtration Rate Glutamine - analogs & derivatives Glutamine - blood Health aspects Hospitals Humans Indican - blood Infectious diseases Intestinal microflora Intestine Kidney diseases Kidney Diseases - blood Kidney Diseases - genetics Kidney Diseases - microbiology Male Metabolism Metabolites Metabolome Microbiomes Microbiota Microbiota (Symbiotic organisms) Microorganisms Middle Aged Molecular biology Nephrology Physiological aspects Population Proteins Renal function Ribotyping Studies Sulfates Sulfuric Acid Esters - blood Taxonomy |
| title | Gut-Microbiota-Metabolite Axis in Early Renal Function Decline |
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