RNA-Seq in 296 phased trios provides a high-resolution map of genomic imprinting

Background: Identification of imprinted genes, demonstrating a consistent preference towards the paternal or maternal allelic expression, is important for the understanding of gene expression regulation during embryonic development and of the molecular basis of developmental disorders with a parent-...

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Main Authors: Jadhav, B., Monajemi, R., Gagalova, Kristina, Ho, D., Draisma, H.H.M., Van De Wiel, M.A., Franke, L., Heijmans, B.T., Van Meurs, J., Jansen, R., T'Hoen, P.A.C., Sharp, A.J., Kiełbasa, S.M.
Format: Journal Article
Language:English
Published: 2019
Subjects:
Online Access:http://hdl.handle.net/20.500.11937/96873
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author Jadhav, B.
Monajemi, R.
Gagalova, Kristina
Ho, D.
Draisma, H.H.M.
Van De Wiel, M.A.
Franke, L.
Heijmans, B.T.
Van Meurs, J.
Jansen, R.
T'Hoen, P.A.C.
Sharp, A.J.
Kiełbasa, S.M.
author_facet Jadhav, B.
Monajemi, R.
Gagalova, Kristina
Ho, D.
Draisma, H.H.M.
Van De Wiel, M.A.
Franke, L.
Heijmans, B.T.
Van Meurs, J.
Jansen, R.
T'Hoen, P.A.C.
Sharp, A.J.
Kiełbasa, S.M.
author_sort Jadhav, B.
building Curtin Institutional Repository
collection Online Access
description Background: Identification of imprinted genes, demonstrating a consistent preference towards the paternal or maternal allelic expression, is important for the understanding of gene expression regulation during embryonic development and of the molecular basis of developmental disorders with a parent-of-origin effect. Combining allelic analysis of RNA-Seq data with phased genotypes in family trios provides a powerful method to detect parent-of-origin biases in gene expression. Results: We report findings in 296 family trios from two large studies: 165 lymphoblastoid cell lines from the 1000 Genomes Project and 131 blood samples from the Genome of the Netherlands (GoNL) participants. Based on parental haplotypes, we identified > 2.8 million transcribed heterozygous SNVs phased for parental origin and developed a robust statistical framework for measuring allelic expression. We identified a total of 45 imprinted genes and one imprinted unannotated transcript, including multiple imprinted transcripts showing incomplete parental expression bias that was located adjacent to strongly imprinted genes. For example, PXDC1, a gene which lies adjacent to the paternally expressed gene FAM50B, shows a 2:1 paternal expression bias. Other imprinted genes had promoter regions that coincide with sites of parentally biased DNA methylation identified in the blood from uniparental disomy (UPD) samples, thus providing independent validation of our results. Using the stranded nature of the RNA-Seq data in lymphoblastoid cell lines, we identified multiple loci with overlapping sense/antisense transcripts, of which one is expressed paternally and the other maternally. Using a sliding window approach, we searched for imprinted expression across the entire genome, identifying a novel imprinted putative lncRNA in 13q21.2. Overall, we identified 7 transcripts showing parental bias in gene expression which were not reported in 4 other recent RNA-Seq studies of imprinting. Conclusions: Our methods and data provide a robust and high-resolution map of imprinted gene expression in the human genome.
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institution Curtin University Malaysia
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spelling curtin-20.500.11937-968732025-02-13T00:37:14Z RNA-Seq in 296 phased trios provides a high-resolution map of genomic imprinting Jadhav, B. Monajemi, R. Gagalova, Kristina Ho, D. Draisma, H.H.M. Van De Wiel, M.A. Franke, L. Heijmans, B.T. Van Meurs, J. Jansen, R. T'Hoen, P.A.C. Sharp, A.J. Kiełbasa, S.M. Allele-specific expression Bayesian analysis Imprinting Parent-of-origin Phased genotypes Alleles Blood Chemical Analysis Cell Line Gene Expression Genomic Imprinting Haplotypes Humans Sequence Analysis, RNA GoNL Consortium BIOS Consortium Cell Line Humans Blood Chemical Analysis Sequence Analysis, RNA Gene Expression Genomic Imprinting Haplotypes Alleles Background: Identification of imprinted genes, demonstrating a consistent preference towards the paternal or maternal allelic expression, is important for the understanding of gene expression regulation during embryonic development and of the molecular basis of developmental disorders with a parent-of-origin effect. Combining allelic analysis of RNA-Seq data with phased genotypes in family trios provides a powerful method to detect parent-of-origin biases in gene expression. Results: We report findings in 296 family trios from two large studies: 165 lymphoblastoid cell lines from the 1000 Genomes Project and 131 blood samples from the Genome of the Netherlands (GoNL) participants. Based on parental haplotypes, we identified > 2.8 million transcribed heterozygous SNVs phased for parental origin and developed a robust statistical framework for measuring allelic expression. We identified a total of 45 imprinted genes and one imprinted unannotated transcript, including multiple imprinted transcripts showing incomplete parental expression bias that was located adjacent to strongly imprinted genes. For example, PXDC1, a gene which lies adjacent to the paternally expressed gene FAM50B, shows a 2:1 paternal expression bias. Other imprinted genes had promoter regions that coincide with sites of parentally biased DNA methylation identified in the blood from uniparental disomy (UPD) samples, thus providing independent validation of our results. Using the stranded nature of the RNA-Seq data in lymphoblastoid cell lines, we identified multiple loci with overlapping sense/antisense transcripts, of which one is expressed paternally and the other maternally. Using a sliding window approach, we searched for imprinted expression across the entire genome, identifying a novel imprinted putative lncRNA in 13q21.2. Overall, we identified 7 transcripts showing parental bias in gene expression which were not reported in 4 other recent RNA-Seq studies of imprinting. Conclusions: Our methods and data provide a robust and high-resolution map of imprinted gene expression in the human genome. 2019 Journal Article http://hdl.handle.net/20.500.11937/96873 10.1186/s12915-019-0674-0 eng http://creativecommons.org/licenses/by/4.0/ fulltext
spellingShingle Allele-specific expression
Bayesian analysis
Imprinting
Parent-of-origin
Phased genotypes
Alleles
Blood Chemical Analysis
Cell Line
Gene Expression
Genomic Imprinting
Haplotypes
Humans
Sequence Analysis, RNA
GoNL Consortium
BIOS Consortium
Cell Line
Humans
Blood Chemical Analysis
Sequence Analysis, RNA
Gene Expression
Genomic Imprinting
Haplotypes
Alleles
Jadhav, B.
Monajemi, R.
Gagalova, Kristina
Ho, D.
Draisma, H.H.M.
Van De Wiel, M.A.
Franke, L.
Heijmans, B.T.
Van Meurs, J.
Jansen, R.
T'Hoen, P.A.C.
Sharp, A.J.
Kiełbasa, S.M.
RNA-Seq in 296 phased trios provides a high-resolution map of genomic imprinting
title RNA-Seq in 296 phased trios provides a high-resolution map of genomic imprinting
title_full RNA-Seq in 296 phased trios provides a high-resolution map of genomic imprinting
title_fullStr RNA-Seq in 296 phased trios provides a high-resolution map of genomic imprinting
title_full_unstemmed RNA-Seq in 296 phased trios provides a high-resolution map of genomic imprinting
title_short RNA-Seq in 296 phased trios provides a high-resolution map of genomic imprinting
title_sort rna-seq in 296 phased trios provides a high-resolution map of genomic imprinting
topic Allele-specific expression
Bayesian analysis
Imprinting
Parent-of-origin
Phased genotypes
Alleles
Blood Chemical Analysis
Cell Line
Gene Expression
Genomic Imprinting
Haplotypes
Humans
Sequence Analysis, RNA
GoNL Consortium
BIOS Consortium
Cell Line
Humans
Blood Chemical Analysis
Sequence Analysis, RNA
Gene Expression
Genomic Imprinting
Haplotypes
Alleles
url http://hdl.handle.net/20.500.11937/96873