Genetic Drivers of Epigenetic and Transcriptional Variation in Human Immune Cells.

PubWeight™: 1.10‹?› | Rank: Top 10%

🔗 View Article (PMID 27863251)

Published in Cell on November 17, 2016

Authors

Lu Chen1, Bing Ge2, Francesco Paolo Casale3, Louella Vasquez4, Tony Kwan2, Diego Garrido-Martín5, Stephen Watt4, Ying Yan4, Kousik Kundu1, Simone Ecker6, Avik Datta7, David Richardson7, Frances Burden8, Daniel Mead4, Alice L Mann4, Jose Maria Fernandez9, Sophia Rowlston8, Steven P Wilder10, Samantha Farrow8, Xiaojian Shao2, John J Lambourne11, Adriana Redensek2, Cornelis A Albers12, Vyacheslav Amstislavskiy13, Sofie Ashford8, Kim Berentsen14, Lorenzo Bomba4, Guillaume Bourque2, David Bujold2, Stephan Busche2, Maxime Caron2, Shu-Huang Chen2, Warren Cheung2, Oliver Delaneau15, Emmanouil T Dermitzakis15, Heather Elding4, Irina Colgiu16, Frederik O Bagger17, Paul Flicek7, Ehsan Habibi14, Valentina Iotchkova18, Eva Janssen-Megens14, Bowon Kim14, Hans Lehrach13, Ernesto Lowy7, Amit Mandoli14, Filomena Matarese14, Matthew T Maurano19, John A Morris2, Vera Pancaldi9, Farzin Pourfarzad20, Karola Rehnstrom8, Augusto Rendon21, Thomas Risch13, Nilofar Sharifi14, Marie-Michelle Simon2, Marc Sultan13, Alfonso Valencia9, Klaudia Walter4, Shuang-Yin Wang14, Mattia Frontini22, Stylianos E Antonarakis15, Laura Clarke7, Marie-Laure Yaspo13, Stephan Beck23, Roderic Guigo24, Daniel Rico25, Joost H A Martens14, Willem H Ouwehand26, Taco W Kuijpers27, Dirk S Paul28, Hendrik G Stunnenberg14, Oliver Stegle3, Kate Downes8, Tomi Pastinen29, Nicole Soranzo30

Author Affiliations

1: Department of Human Genetics, The Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1HH, UK; Department of Haematology, University of Cambridge, Cambridge Biomedical Campus, Long Road, Cambridge CB2 0PT, UK.
2: Human Genetics, McGill University, 740 Dr. Penfield, Montreal, QC H3A 0G1, Canada.
3: European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SD, UK.
4: Department of Human Genetics, The Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1HH, UK.
5: Bioinformatics and Genomics, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Carrer del Dr. Aiguader, 88, Barcelona 8003, Spain; Department of Experimental and Health Sciences, Universitat Pompeu Fabra (UPF), Plaça de la Mercè, 10- 12, Barcelona 8002, Spain.
6: Structural Biology and Biocomputing Programme, Spanish National Cancer Research Centre (CNIO), Melchor Fernandez Almagro, 3, Madrid 28029, Spain; UCL Cancer Institute, University College London, 72 Huntley Street, London WC1E 6BT, UK.
7: Vertebrate Genomics, European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK.
8: Department of Haematology, University of Cambridge, Cambridge Biomedical Campus, Long Road, Cambridge CB2 0PT, UK; National Health Service (NHS) Blood and Transplant, Cambridge Biomedical Campus, Long Road, Cambridge CB2 0PT, UK.
9: Structural Biology and Biocomputing Programme, Spanish National Cancer Research Centre (CNIO), Melchor Fernandez Almagro, 3, Madrid 28029, Spain.
10: Genome Analysis, European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK.
11: Human Genetics, McGill University, 740 Dr. Penfield, Montreal, QC H3A 0G1, Canada; Department of Haematology, University of Cambridge, Cambridge Biomedical Campus, Long Road, Cambridge CB2 0PT, UK; National Health Service (NHS) Blood and Transplant, Cambridge Biomedical Campus, Long Road, Cambridge CB2 0PT, UK.
12: Human Genetics, Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Centre, P.O. Box 9101, Nijmegen 6500 HB, the Netherlands; Molecular Developmental Biology, Radboud Institute for Life Sciences, Radboud University, P.O. Box 9101, Nijmegen 6500 HB, the Netherlands.
13: Department of Vertebrate Genomics, Max Planck Institute for Molecular Genetics, Ihnestr. 63/73, Berlin 14195, Germany.
14: Department of Molecular Biology, Faculty of Science, Radboud University, Nijmegen 6525GA, the Netherlands.
15: Genetic Medicine and Development, University of Geneva Medical School-CMU, 1 Rue Michel-Servet, Geneva 1211, Switzerland.
16: Human Genetics Informatics, The Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1HH, UK.
17: Department of Haematology, University of Cambridge, Cambridge Biomedical Campus, Long Road, Cambridge CB2 0PT, UK; European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SD, UK; National Health Service (NHS) Blood and Transplant, Cambridge Biomedical Campus, Long Road, Cambridge CB2 0PT, UK.
18: Department of Human Genetics, The Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1HH, UK; European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK.
19: Institute for Systems Genetics, New York University Langone Medical Center, ACLS West, Room 511, 430 East 29(th) Street, New York, NY 10016, USA.
20: Blood Cell Research, Sanquin Research and Landsteiner Laboratory, Plesmanlaan 125, Amsterdam 1066CX, the Netherlands.
21: Department of Haematology, University of Cambridge, Cambridge Biomedical Campus, Long Road, Cambridge CB2 0PT, UK; Bioinformatics, Genomics England, Charterhouse Square, London EC1M 6BQ, UK.
22: Department of Haematology, University of Cambridge, Cambridge Biomedical Campus, Long Road, Cambridge CB2 0PT, UK; National Health Service (NHS) Blood and Transplant, Cambridge Biomedical Campus, Long Road, Cambridge CB2 0PT, UK; British Heart Foundation Centre of Excellence, Division of Cardiovascular Medicine, Addenbrooke's Hospital, Hills Road, Cambridge CB2 0QQ, UK.
23: UCL Cancer Institute, University College London, 72 Huntley Street, London WC1E 6BT, UK.
24: Bioinformatics and Genomics, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Carrer del Dr. Aiguader, 88, Barcelona 8003, Spain; Department of Experimental and Health Sciences, Universitat Pompeu Fabra (UPF), Plaça de la Mercè, 10- 12, Barcelona 8002, Spain; Computational Genomics, Institut Hospital del Mar d'Investigacions Mediques (IMIM), Carrer del Dr. Aiguader, 88, Barcelona 8003, Spain.
25: Structural Biology and Biocomputing Programme, Spanish National Cancer Research Centre (CNIO), Melchor Fernandez Almagro, 3, Madrid 28029, Spain; Institute of Cellular Medicine, Newcastle University, Framlington Place, Newcastle upon Tyne NE2 4HH, UK.
26: Department of Human Genetics, The Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1HH, UK; Department of Haematology, University of Cambridge, Cambridge Biomedical Campus, Long Road, Cambridge CB2 0PT, UK; National Health Service (NHS) Blood and Transplant, Cambridge Biomedical Campus, Long Road, Cambridge CB2 0PT, UK; British Heart Foundation Centre of Excellence, Division of Cardiovascular Medicine, Addenbrooke's Hospital, Hills Road, Cambridge CB2 0QQ, UK; The National Institute for Health Research Blood and Transplant Unit (NIHR BTRU) in Donor Health and Genomics at the University of Cambridge, Strangeways Research Laboratory, University of Cambridge, Wort's Causeway, Cambridge CB1 8RN, UK.
27: Department of Haematology, University of Cambridge, Cambridge Biomedical Campus, Long Road, Cambridge CB2 0PT, UK; Blood Cell Research, Sanquin Research and Landsteiner Laboratory, Plesmanlaan 125, Amsterdam 1066CX, the Netherlands; Emma Children's Hospital, Academic Medical Center (AMC), University of Amsterdam, Location H7-230, Meibergdreef 9, Amsterdam 1105AZ, the Netherlands.
28: UCL Cancer Institute, University College London, 72 Huntley Street, London WC1E 6BT, UK; Cardiovascular Epidemiology Unit, Department of Public Health and Primary Care, Strangeways Research Laboratory, University of Cambridge, Wort's Causeway, Cambridge CB1 8RN, UK.
29: Human Genetics, McGill University, 740 Dr. Penfield, Montreal, QC H3A 0G1, Canada. Electronic address: tomi.pastinen@mcgill.ca.
30: Department of Human Genetics, The Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1HH, UK; Department of Haematology, University of Cambridge, Cambridge Biomedical Campus, Long Road, Cambridge CB2 0PT, UK; British Heart Foundation Centre of Excellence, Division of Cardiovascular Medicine, Addenbrooke's Hospital, Hills Road, Cambridge CB2 0QQ, UK; The National Institute for Health Research Blood and Transplant Unit (NIHR BTRU) in Donor Health and Genomics at the University of Cambridge, Strangeways Research Laboratory, University of Cambridge, Wort's Causeway, Cambridge CB1 8RN, UK. Electronic address: ns6@sanger.ac.uk.

Articles cited by this

PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet (2007) 209.92

Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics (2009) 190.94

Statistical significance for genomewide studies. Proc Natl Acad Sci U S A (2003) 88.64

Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol (2010) 75.21

A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet (2011) 59.36

Potential etiologic and functional implications of genome-wide association loci for human diseases and traits. Proc Natl Acad Sci U S A (2009) 54.68

Model-based analysis of ChIP-Seq (MACS). Genome Biol (2008) 51.63

Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol (2014) 27.48

STAR: ultrafast universal RNA-seq aligner. Bioinformatics (2012) 25.21

Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am J Hum Genet (2007) 24.68

Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics (2006) 22.61

GCTA: a tool for genome-wide complex trait analysis. Am J Hum Genet (2010) 20.73

GENCODE: the reference human genome annotation for The ENCODE Project. Genome Res (2012) 19.19

Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature (2012) 16.13

The NHGRI GWAS Catalog, a curated resource of SNP-trait associations. Nucleic Acids Res (2013) 14.23

Efficient control of population structure in model organism association mapping. Genetics (2008) 12.32

Large-scale association analysis provides insights into the genetic architecture and pathophysiology of type 2 diabetes. Nat Genet (2012) 11.09

Integrative analysis of 111 reference human epigenomes. Nature (2015) 10.32

A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics (2011) 8.19

Meta-analysis identifies 29 additional ulcerative colitis risk loci, increasing the number of confirmed associations to 47. Nat Genet (2011) 7.98

ChromHMM: automating chromatin-state discovery and characterization. Nat Methods (2012) 7.66

DNA methylation age of human tissues and cell types. Genome Biol (2013) 7.48

Multiple common variants for celiac disease influencing immune gene expression. Nat Genet (2010) 6.90

Genetics of rheumatoid arthritis contributes to biology and drug discovery. Nature (2013) 6.57

The architecture of gene regulatory variation across multiple human tissues: the MuTHER study. PLoS Genet (2011) 5.95

Minfi: a flexible and comprehensive Bioconductor package for the analysis of Infinium DNA methylation microarrays. Bioinformatics (2014) 5.93

Genetic and epigenetic fine mapping of causal autoimmune disease variants. Nature (2014) 5.22

SWAN: Subset-quantile within array normalization for illumina infinium HumanMethylation450 BeadChips. Genome Biol (2012) 4.99

Global patterns of cis variation in human cells revealed by high-density allelic expression analysis. Nat Genet (2009) 4.72

Analysis of immune-related loci identifies 48 new susceptibility variants for multiple sclerosis. Nat Genet (2013) 4.62

The sva package for removing batch effects and other unwanted variation in high-throughput experiments. Bioinformatics (2012) 4.48

Accurate discovery of expression quantitative trait loci under confounding from spurious and genuine regulatory hotspots. Genetics (2008) 3.66

Innate immune activity conditions the effect of regulatory variants upon monocyte gene expression. Science (2014) 3.16

The African Genome Variation Project shapes medical genetics in Africa. Nature (2014) 3.11

Removing batch effects in analysis of expression microarray data: an evaluation of six batch adjustment methods. PLoS One (2011) 2.89

Characterizing the genetic basis of transcriptome diversity through RNA-sequencing of 922 individuals. Genome Res (2013) 2.77

Passive and active DNA methylation and the interplay with genetic variation in gene regulation. Elife (2013) 2.70

Genome-wide allele-specific analysis: insights into regulatory variation. Nat Rev Genet (2010) 2.68

Association analyses identify 38 susceptibility loci for inflammatory bowel disease and highlight shared genetic risk across populations. Nat Genet (2015) 2.59

Low-level processing of Illumina Infinium DNA Methylation BeadArrays. Nucleic Acids Res (2013) 2.19

Using probabilistic estimation of expression residuals (PEER) to obtain increased power and interpretability of gene expression analyses. Nat Protoc (2012) 2.14

Genetic Control of Chromatin States in Humans Involves Local and Distal Chromosomal Interactions. Cell (2015) 2.11

Orchestrated intron retention regulates normal granulocyte differentiation. Cell (2013) 2.06

Fine mapping of type 1 diabetes susceptibility loci and evidence for colocalization of causal variants with lymphoid gene enhancers. Nat Genet (2015) 2.04

From expression QTLs to personalized transcriptomics. Nat Rev Genet (2011) 1.94

Transcriptional diversity during lineage commitment of human blood progenitors. Science (2014) 1.93

Population Variation and Genetic Control of Modular Chromatin Architecture in Humans. Cell (2015) 1.85

Bayesian test for colocalisation between pairs of genetic association studies using summary statistics. PLoS Genet (2014) 1.71

RNA splicing is a primary link between genetic variation and disease. Science (2016) 1.61

Genome-wide signatures of differential DNA methylation in pediatric acute lymphoblastic leukemia. Genome Biol (2013) 1.57

ASTALAVISTA: dynamic and flexible analysis of alternative splicing events in custom gene datasets. Nucleic Acids Res (2007) 1.52

WASP: allele-specific software for robust molecular quantitative trait locus discovery. Nat Methods (2015) 1.45

Genetic association analyses implicate aberrant regulation of innate and adaptive immunity genes in the pathogenesis of systemic lupus erythematosus. Nat Genet (2015) 1.42

Detection and interpretation of shared genetic influences on 42 human traits. Nat Genet (2016) 1.32

Using the realized relationship matrix to disentangle confounding factors for the estimation of genetic variance components of complex traits. Genet Sel Evol (2010) 1.27

Enhancers: emerging roles in cell fate specification. EMBO Rep (2012) 1.23

Identification of genetic variants associated with alternative splicing using sQTLseekeR. Nat Commun (2014) 1.08

Characterization of functional methylomes by next-generation capture sequencing identifies novel disease-associated variants. Nat Commun (2015) 1.03

The role of Tec family kinases in myeloid cells. Int Arch Allergy Immunol (2004) 1.00

Fine-mapping cellular QTLs with RASQUAL and ATAC-seq. Nat Genet (2015) 0.98

AHT-ChIP-seq: a completely automated robotic protocol for high-throughput chromatin immunoprecipitation. Genome Biol (2013) 0.96

Efficient set tests for the genetic analysis of correlated traits. Nat Methods (2015) 0.95

Essential roles for the Tec family kinases Tec and Btk in M-CSF receptor signaling pathways that regulate macrophage survival. J Immunol (2008) 0.92

Genomic modulators of gene expression in human neutrophils. Nat Commun (2015) 0.91

Allelic expression mapping across cellular lineages to establish impact of non-coding SNPs. Mol Syst Biol (2014) 0.86

Statistical comparison of methods to estimate the error probability in short-read Illumina sequencing. J Bioinform Comput Biol (2010) 0.84