Systematic differences in discovery of genetic effects on gene expression and complex traits

被引:97
作者
Mostafavi, Hakhamanesh [1 ]
Spence, Jeffrey P. [1 ]
Naqvi, Sahin [1 ,2 ]
Pritchard, Jonathan K. [1 ,3 ]
机构
[1] Stanford Univ, Dept Genet, Stanford, CA 94305 USA
[2] Stanford Univ, Dept Chem & Syst Biol, Stanford, CA USA
[3] Stanford Univ, Dept Biol, Stanford, CA 94305 USA
基金
美国国家卫生研究院;
关键词
PARTITIONING HERITABILITY; VARIANTS; TRANSCRIPTION; EQTL; COLOCALIZATION; INTEGRATION; THOUSANDS; NETWORK; LOCI; GWAS;
D O I
10.1038/s41588-023-01529-1
中图分类号
Q3 [遗传学];
学科分类号
071007 ; 090102 ;
摘要
Most signals in genome-wide association studies (GWAS) of complex traits implicate noncoding genetic variants with putative gene regulatory effects. However, currently identified regulatory variants, notably expression quantitative trait loci (eQTLs), explain only a small fraction of GWAS signals. Here, we show that GWAS and cis-eQTL hits are systematically different: eQTLs cluster strongly near transcription start sites, whereas GWAS hits do not. Genes near GWAS hits are enriched in key functional annotations, are under strong selective constraint and have complex regulatory landscapes across different tissue/cell types, whereas genes near eQTLs are depleted of most functional annotations, show relaxed constraint, and have simpler regulatory landscapes. We describe a model to understand these observations, including how natural selection on complex traits hinders discovery of functionally relevant eQTLs. Our results imply that GWAS and eQTL studies are systematically biased toward different types of variant, and support the use of complementary functional approaches alongside the next generation of eQTL studies.
引用
收藏
页码:1866 / +
页数:27
相关论文
共 84 条
[1]   Multiple causal variants underlie genetic associations in humans [J].
Abell, Nathan S. ;
DeGorter, Marianne K. ;
Gloudemans, Michael J. ;
Greenwald, Emily ;
Smith, Kevin S. ;
He, Zihuai ;
Montgomery, Stephen B. .
SCIENCE, 2022, 375 (6586) :1247-+
[2]   Relating pathogenic loss-of-function mutations in humans to their evolutionary fitness costs [J].
Agarwal, Ipsita ;
Fuller, Zachary L. ;
Myers, Simon R. ;
Przeworski, Molly .
ELIFE, 2023, 12
[3]   The GTEx Consortium atlas of genetic regulatory effects across human tissues [J].
Aguet, Francois ;
Barbeira, Alvaro N. ;
Bonazzola, Rodrigo ;
Brown, Andrew ;
Castel, Stephane E. ;
Jo, Brian ;
Kasela, Silva ;
Kim-Hellmuth, Sarah ;
Liang, Yanyu ;
Parsana, Princy ;
Flynn, Elise ;
Fresard, Laure ;
Gamazon, Eric R. ;
Hamel, Andrew R. ;
He, Yuan ;
Hormozdiari, Farhad ;
Mohammadi, Pejman ;
Munoz-Aguirre, Manuel ;
Ardlie, Kristin G. ;
Battle, Alexis ;
Bonazzola, Rodrigo ;
Brown, Christopher D. ;
Cox, Nancy ;
Dermitzakis, Emmanouil T. ;
Engelhardt, Barbara E. ;
Garrido-Martin, Diego ;
Gay, Nicole R. ;
Getz, Gad ;
Guigo, Roderic ;
Hamel, Andrew R. ;
Handsaker, Robert E. ;
He, Yuan ;
Hoffman, Paul J. ;
Hormozdiari, Farhad ;
Im, Hae Kyung ;
Jo, Brian ;
Kasela, Silva ;
Kashin, Seva ;
Kim-Hellmuth, Sarah ;
Kwong, Alan ;
Lappalainen, Tuuli ;
Li, Xiao ;
Liang, Yanyu ;
MacArthur, Daniel G. ;
Mohammadi, Pejman ;
Montgomery, Stephen B. ;
Munoz-Aguirre, Manuel ;
Rouhana, John M. ;
Hormozdiari, Farhad ;
Im, Hae Kyung .
SCIENCE, 2020, 369 (6509) :1318-1330
[4]   Genetic effects on gene expression across human tissues [J].
Aguet, Francois ;
Brown, Andrew A. ;
Castel, Stephane E. ;
Davis, Joe R. ;
He, Yuan ;
Jo, Brian ;
Mohammadi, Pejman ;
Park, Yoson ;
Parsana, Princy ;
Segre, Ayellet V. ;
Strober, Benjamin J. ;
Zappala, Zachary ;
Cummings, Beryl B. ;
Gelfand, Ellen T. ;
Hadley, Kane ;
Huang, Katherine H. ;
Lek, Monkol ;
Li, Xiao ;
Nedzel, Jared L. ;
Nguyen, Duyen Y. ;
Noble, Michael S. ;
Sullivan, Timothy J. ;
Tukiainen, Taru ;
MacArthur, Daniel G. ;
Getz, Gad ;
Management, Nih Program ;
Addington, Anjene ;
Guan, Ping ;
Koester, Susan ;
Little, A. Roger ;
Lockhart, Nicole C. ;
Moore, Helen M. ;
Rao, Abhi ;
Struewing, Jeffery P. ;
Volpi, Simona ;
Collection, Biospecimen ;
Brigham, Lori E. ;
Hasz, Richard ;
Hunter, Marcus ;
Johns, Christopher ;
Johnson, Mark ;
Kopen, Gene ;
Leinweber, William F. ;
Lonsdale, John T. ;
McDonald, Alisa ;
Mestichelli, Bernadette ;
Myer, Kevin ;
Roe, Bryan ;
Salvatore, Michael ;
Shad, Saboor .
NATURE, 2017, 550 (7675) :204-+
[5]  
Alexa A., 2020, topGO: Enrichment analysis for gene ontology
[6]   The Genotype-Tissue Expression (GTEx) pilot analysis: Multitissue gene regulation in humans [J].
Ardlie, Kristin G. ;
DeLuca, David S. ;
Segre, Ayellet V. ;
Sullivan, Timothy J. ;
Young, Taylor R. ;
Gelfand, Ellen T. ;
Trowbridge, Casandra A. ;
Maller, Julian B. ;
Tukiainen, Taru ;
Lek, Monkol ;
Ward, Lucas D. ;
Kheradpour, Pouya ;
Iriarte, Benjamin ;
Meng, Yan ;
Palmer, Cameron D. ;
Esko, Tonu ;
Winckler, Wendy ;
Hirschhorn, Joel N. ;
Kellis, Manolis ;
MacArthur, Daniel G. ;
Getz, Gad ;
Shabalin, Andrey A. ;
Li, Gen ;
Zhou, Yi-Hui ;
Nobel, Andrew B. ;
Rusyn, Ivan ;
Wright, Fred A. ;
Lappalainen, Tuuli ;
Ferreira, Pedro G. ;
Ongen, Halit ;
Rivas, Manuel A. ;
Battle, Alexis ;
Mostafavi, Sara ;
Monlong, Jean ;
Sammeth, Michael ;
Mele, Marta ;
Reverter, Ferran ;
Goldmann, Jakob M. ;
Koller, Daphne ;
Guigo, Roderic ;
McCarthy, Mark I. ;
Dermitzakis, Emmanouil T. ;
Gamazon, Eric R. ;
Im, Hae Kyung ;
Konkashbaev, Anuar ;
Nicolae, Dan L. ;
Cox, Nancy J. ;
Flutre, Timothee ;
Wen, Xiaoquan ;
Stephens, Matthew .
SCIENCE, 2015, 348 (6235) :648-660
[7]   Effective gene expression prediction from sequence by integrating long-range interactions [J].
Avsec, Ziga ;
Agarwal, Vikram ;
Visentin, Daniel ;
Ledsam, Joseph R. ;
Grabska-Barwinska, Agnieszka ;
Taylor, Kyle R. ;
Assael, Yannis ;
Jumper, John ;
Kohli, Pushmeet ;
Kelley, David R. .
NATURE METHODS, 2021, 18 (10) :1196-+
[8]   Brain-trait-associated variants impact cell-type-specific gene regulation during neurogenesis [J].
Aygun, Nil ;
Elwell, Angela L. ;
Liang, Dan ;
Lafferty, Michael J. ;
Cheek, Kerry E. ;
Courtney, Kenan P. ;
Mory, Jessica ;
Hadden-Ford, Ellie ;
Krupa, Oleh ;
de la Torre-Ubieta, Luis ;
Geschwind, Daniel H. ;
Love, Michael, I ;
Stein, Jason L. .
AMERICAN JOURNAL OF HUMAN GENETICS, 2021, 108 (09) :1647-1668
[9]   Characterizing the genetic basis of transcriptome diversity through RNA-sequencing of 922 individuals [J].
Battle, Alexis ;
Mostafavi, Sara ;
Zhu, Xiaowei ;
Potash, James B. ;
Weissman, Myrna M. ;
McCormick, Courtney ;
Haudenschild, Christian D. ;
Beckman, Kenneth B. ;
Shi, Jianxin ;
Mei, Rui ;
Urban, Alexander E. ;
Montgomery, Stephen B. ;
Levinson, Douglas F. ;
Koller, Daphne .
GENOME RESEARCH, 2014, 24 (01) :14-24
[10]   Approximately independent linkage disequilibrium blocks in human populations [J].
Berisa, Tomaz ;
Pickrell, Joseph K. .
BIOINFORMATICS, 2016, 32 (02) :283-285