Genetic regulation of human adipose microRNA expression and its consequences for metabolic traits
The genetics of messenger RNA (mRNA) expression has been extensively studied in humans and other organisms, but little is known about genetic factors contributing to microRNA (miRNA) expression. We examined natural variation of miRNA expression in adipose tissue in a population of 200 men who have b...
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| Published in | Human molecular genetics Vol. 22; no. 15; pp. 3023 - 3037 |
|---|---|
| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
Oxford University Press
01.08.2013
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| Subjects | |
| Online Access | Get full text |
| ISSN | 0964-6906 1460-2083 1460-2083 |
| DOI | 10.1093/hmg/ddt159 |
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| Abstract | The genetics of messenger RNA (mRNA) expression has been extensively studied in humans and other organisms, but little is known about genetic factors contributing to microRNA (miRNA) expression. We examined natural variation of miRNA expression in adipose tissue in a population of 200 men who have been carefully characterized for metabolic syndrome (MetSyn) phenotypes as part of the Metabolic Syndrome in Men (METSIM) study. We genotyped the subjects using high-density single-nucleotide polymorphism microarrays and quantified the mRNA abundance using genome-wide expression arrays and miRNA abundance using next-generation sequencing. We reliably quantified 356 miRNA species that were expressed in human adipose tissue, a limited number of which made up most of the expressed miRNAs. We mapped the miRNA abundance as an expression quantitative trait and determined cis regulation of expression for nine of the miRNAs and of the processing of one miRNA (miR-28). The degree of genetic variation of miRNA expression was substantially less than that of mRNAs. For the majority of the miRNAs, genetic regulation of expression was independent of the expression of mRNA from which the miRNA is transcribed. We also showed that for 108 miRNAs, mapped reads displayed widespread variation from the canonical sequence. We found a total of 24 miRNAs to be significantly associated with MetSyn traits. We suggest a regulatory role for miR-204-5p which was predicted to inhibit acetyl coenzyme A carboxylase β, a key fatty acid oxidation enzyme that has been shown to play a role in regulating body fat and insulin resistance in adipose tissue. |
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| AbstractList | The genetics of messenger RNA (mRNA) expression has been extensively studied in humans and other organisms, but little is known about genetic factors contributing to microRNA (miRNA) expression. We examined natural variation of miRNA expression in adipose tissue in a population of 200 men who have been carefully characterized for metabolic syndrome (MetSyn) phenotypes as part of the Metabolic Syndrome in Men (METSIM) study. We genotyped the subjects using high-density single-nucleotide polymorphism microarrays and quantified the mRNA abundance using genome-wide expression arrays and miRNA abundance using next-generation sequencing. We reliably quantified 356 miRNA species that were expressed in human adipose tissue, a limited number of which made up most of the expressed miRNAs. We mapped the miRNA abundance as an expression quantitative trait and determined
cis
regulation of expression for nine of the miRNAs and of the processing of one miRNA (miR-28). The degree of genetic variation of miRNA expression was substantially less than that of mRNAs. For the majority of the miRNAs, genetic regulation of expression was independent of the expression of mRNA from which the miRNA is transcribed. We also showed that for 108 miRNAs, mapped reads displayed widespread variation from the canonical sequence. We found a total of 24 miRNAs to be significantly associated with MetSyn traits. We suggest a regulatory role for miR-204-5p which was predicted to inhibit acetyl coenzyme A carboxylase β, a key fatty acid oxidation enzyme that has been shown to play a role in regulating body fat and insulin resistance in adipose tissue. The genetics of messenger RNA (mRNA) expression has been extensively studied in humans and other organisms, but little is known about genetic factors contributing to microRNA (miRNA) expression. We examined natural variation of miRNA expression in adipose tissue in a population of 200 men who have been carefully characterized for metabolic syndrome (MetSyn) phenotypes as part of the Metabolic Syndrome in Men (METSIM) study. We genotyped the subjects using high-density single-nucleotide polymorphism microarrays and quantified the mRNA abundance using genome-wide expression arrays and miRNA abundance using next-generation sequencing. We reliably quantified 356 miRNA species that were expressed in human adipose tissue, a limited number of which made up most of the expressed miRNAs. We mapped the miRNA abundance as an expression quantitative trait and determined cis regulation of expression for nine of the miRNAs and of the processing of one miRNA (miR-28). The degree of genetic variation of miRNA expression was substantially less than that of mRNAs. For the majority of the miRNAs, genetic regulation of expression was independent of the expression of mRNA from which the miRNA is transcribed. We also showed that for 108 miRNAs, mapped reads displayed widespread variation from the canonical sequence. We found a total of 24 miRNAs to be significantly associated with MetSyn traits. We suggest a regulatory role for miR-204-5p which was predicted to inhibit acetyl coenzyme A carboxylase β, a key fatty acid oxidation enzyme that has been shown to play a role in regulating body fat and insulin resistance in adipose tissue.The genetics of messenger RNA (mRNA) expression has been extensively studied in humans and other organisms, but little is known about genetic factors contributing to microRNA (miRNA) expression. We examined natural variation of miRNA expression in adipose tissue in a population of 200 men who have been carefully characterized for metabolic syndrome (MetSyn) phenotypes as part of the Metabolic Syndrome in Men (METSIM) study. We genotyped the subjects using high-density single-nucleotide polymorphism microarrays and quantified the mRNA abundance using genome-wide expression arrays and miRNA abundance using next-generation sequencing. We reliably quantified 356 miRNA species that were expressed in human adipose tissue, a limited number of which made up most of the expressed miRNAs. We mapped the miRNA abundance as an expression quantitative trait and determined cis regulation of expression for nine of the miRNAs and of the processing of one miRNA (miR-28). The degree of genetic variation of miRNA expression was substantially less than that of mRNAs. For the majority of the miRNAs, genetic regulation of expression was independent of the expression of mRNA from which the miRNA is transcribed. We also showed that for 108 miRNAs, mapped reads displayed widespread variation from the canonical sequence. We found a total of 24 miRNAs to be significantly associated with MetSyn traits. We suggest a regulatory role for miR-204-5p which was predicted to inhibit acetyl coenzyme A carboxylase β, a key fatty acid oxidation enzyme that has been shown to play a role in regulating body fat and insulin resistance in adipose tissue. The genetics of messenger RNA (mRNA) expression has been extensively studied in humans and other organisms, but little is known about genetic factors contributing to microRNA (miRNA) expression. We examined natural variation of miRNA expression in adipose tissue in a population of 200 men who have been carefully characterized for metabolic syndrome (MetSyn) phenotypes as part of the Metabolic Syndrome in Men (METSIM) study. We genotyped the subjects using high-density single-nucleotide polymorphism microarrays and quantified the mRNA abundance using genome-wide expression arrays and miRNA abundance using next-generation sequencing. We reliably quantified 356 miRNA species that were expressed in human adipose tissue, a limited number of which made up most of the expressed miRNAs. We mapped the miRNA abundance as an expression quantitative trait and determined cis regulation of expression for nine of the miRNAs and of the processing of one miRNA (miR-28). The degree of genetic variation of miRNA expression was substantially less than that of mRNAs. For the majority of the miRNAs, genetic regulation of expression was independent of the expression of mRNA from which the miRNA is transcribed. We also showed that for 108 miRNAs, mapped reads displayed widespread variation from the canonical sequence. We found a total of 24 miRNAs to be significantly associated with MetSyn traits. We suggest a regulatory role for miR-204-5p which was predicted to inhibit acetyl coenzyme A carboxylase beta , a key fatty acid oxidation enzyme that has been shown to play a role in regulating body fat and insulin resistance in adipose tissue. The genetics of messenger RNA (mRNA) expression has been extensively studied in humans and other organisms, but little is known about genetic factors contributing to microRNA (miRNA) expression. We examined natural variation of miRNA expression in adipose tissue in a population of 200 men who have been carefully characterized for metabolic syndrome (MetSyn) phenotypes as part of the Metabolic Syndrome in Men (METSIM) study. We genotyped the subjects using high-density single-nucleotide polymorphism microarrays and quantified the mRNA abundance using genome-wide expression arrays and miRNA abundance using next-generation sequencing. We reliably quantified 356 miRNA species that were expressed in human adipose tissue, a limited number of which made up most of the expressed miRNAs. We mapped the miRNA abundance as an expression quantitative trait and determined cis regulation of expression for nine of the miRNAs and of the processing of one miRNA (miR-28). The degree of genetic variation of miRNA expression was substantially less than that of mRNAs. For the majority of the miRNAs, genetic regulation of expression was independent of the expression of mRNA from which the miRNA is transcribed. We also showed that for 108 miRNAs, mapped reads displayed widespread variation from the canonical sequence. We found a total of 24 miRNAs to be significantly associated with MetSyn traits. We suggest a regulatory role for miR-204-5p which was predicted to inhibit acetyl coenzyme A carboxylase β, a key fatty acid oxidation enzyme that has been shown to play a role in regulating body fat and insulin resistance in adipose tissue. |
| Author | Kuusisto, Johanna Yang, Wen-pin Civelek, Mete Hagopian, Raffi Che, Nam Cederberg, Henna Saleem, Niyas K. Pan, Calvin Gargalovic, Peter S. Kirchgessner, Todd G. Lusis, Aldons J. Laakso, Markku Kayne, Paul S. |
| AuthorAffiliation | 4 Department of Applied Genomics 2 Department of Human Genetics and 5 Department of Cardiovascular Drug Discovery , Bristol-Myers Squibb , Pennington, NJ 08534 , USA and 6 Department of Medicine , University of Eastern Finland and Kuopio University Hospital , Kuopio , Finland 3 Department of Microbiology, Immunology and Molecular Genetics , University of California , Los Angeles, CA 90095 , USA 1 Department of Medicine |
| AuthorAffiliation_xml | – name: 1 Department of Medicine – name: 4 Department of Applied Genomics – name: 3 Department of Microbiology, Immunology and Molecular Genetics , University of California , Los Angeles, CA 90095 , USA – name: 6 Department of Medicine , University of Eastern Finland and Kuopio University Hospital , Kuopio , Finland – name: 2 Department of Human Genetics and – name: 5 Department of Cardiovascular Drug Discovery , Bristol-Myers Squibb , Pennington, NJ 08534 , USA and |
| Author_xml | – sequence: 1 givenname: Mete surname: Civelek fullname: Civelek, Mete – sequence: 2 givenname: Raffi surname: Hagopian fullname: Hagopian, Raffi – sequence: 3 givenname: Calvin surname: Pan fullname: Pan, Calvin – sequence: 4 givenname: Nam surname: Che fullname: Che, Nam – sequence: 5 givenname: Wen-pin surname: Yang fullname: Yang, Wen-pin – sequence: 6 givenname: Paul S. surname: Kayne fullname: Kayne, Paul S. – sequence: 7 givenname: Niyas K. surname: Saleem fullname: Saleem, Niyas K. – sequence: 8 givenname: Henna surname: Cederberg fullname: Cederberg, Henna – sequence: 9 givenname: Johanna surname: Kuusisto fullname: Kuusisto, Johanna – sequence: 10 givenname: Peter S. surname: Gargalovic fullname: Gargalovic, Peter S. – sequence: 11 givenname: Todd G. surname: Kirchgessner fullname: Kirchgessner, Todd G. – sequence: 12 givenname: Markku surname: Laakso fullname: Laakso, Markku – sequence: 13 givenname: Aldons J. surname: Lusis fullname: Lusis, Aldons J. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23562819$$D View this record in MEDLINE/PubMed |
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| SubjectTerms | Adipose Tissue - metabolism Gene Expression Regulation Genetic Association Studies Humans Metabolic Syndrome - genetics Metabolic Syndrome - metabolism MicroRNAs - genetics Phenotype Polymorphism, Single Nucleotide Quantitative Trait Loci Quantitative Trait, Heritable RNA Interference RNA Processing, Post-Transcriptional Transcription, Genetic Transcriptome |
| Title | Genetic regulation of human adipose microRNA expression and its consequences for metabolic traits |
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