Genome-wide comparison of allele-specific gene expression between African and European populations

Human Molecular Genetics

Volumn 27, Issue 6, 2018, Pages 1067-1077

  Tian, Lei ^a,b   Khan, Asifullah ^a,c   Ning, Zhilin ^a,b   Yuan, Kai ^a,b   Zhang, Chao ^a,b   Lou, Haiyi ^a   Yuan, Yuan ^a   Xu, Shuhua ^a,b,d,e  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c ABDUL WALI KHAN UNIVERSITY   (Pakistan)

^d SHANGHAITECH UNIVERSITY   (China)

^e FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; DNAJC15 PROTEIN, HUMAN; HEAT SHOCK PROTEIN 40; TRANSCRIPTOME;

AFRICAN; ALLELE; ARTICLE; EUROPEAN; GENE EXPRESSION; GENETIC HETEROGENEITY; GENETIC TRAIT; GENETIC VARIABILITY; HAPLOTYPE; HAPLOTYPE MAP; HUMAN; HUMAN GENOME; HUMAN GENOME PROJECT; PHENOTYPIC VARIATION; PRIORITY JOURNAL; RNA SEQUENCE; SINGLE NUCLEOTIDE POLYMORPHISM; BLACK PERSON; CAUCASIAN; GENE EXPRESSION REGULATION; GENE FREQUENCY; GENETIC VARIATION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; PROCEDURES; QUANTITATIVE TRAIT LOCUS; SEQUENCE ANALYSIS;

AFRICAN CONTINENTAL ANCESTRY GROUP; EUROPEAN CONTINENTAL ANCESTRY GROUP; GENE EXPRESSION REGULATION; GENE FREQUENCY; GENETIC VARIATION; GENOME-WIDE ASSOCIATION STUDY; HAPLOTYPES; HSP40 HEAT-SHOCK PROTEINS; HUMANS; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME;

EID: 85043308904     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddy027     Document Type: Article

References (58)

1. Jobling, M.A. (2012) The impact of recent events on human genetic diversity. Philos. Trans. R. Soc. Lond. B Biol. Sci., 367, 793-799.
2. Balaresque, P.L., Ballereau, S.J. and Jobling, M.A. (2007) Challenges in human genetic diversity: demographic history and adaptation. Hum. Mol. Genet., 16, R134-R139.
3. Pala, M., Zappala, Z., Marongiu, M., Li, X., Davis, J.R., Cusano, R., Crobu, F., Kukurba, K.R., Gloudemans, M.J. and Reinier, F. (2017) Population- and individual-specific regulatory variation in Sardinia. Nat. Genet, 49, 700-707.
4. Walker, E.J., Zhang, C., Castelo-Branco, P., Hawkins, C., Wilson, W., Zhukova, N., Alon, N., Novokmet, A., Baskin, B., Ray, P. et al. (2012) Monoallelic expression determines oncogenic progression and outcome in benign and malignant brain tumors. Cancer Res., 72, 636-644.
5. Milani, L., Lundmark, A., Nordlund, J., Kiialainen, A., Flaegstad, T., Jonmundsson, G., Kanerva, J., Schmiegelow, K., Gunderson, K.L. and Lönnerholm, G.A.-C.S. (2009) Allele-specific gene expression patterns in primary leukemic cells reveal regulation of gene expression by CpG site methylation. Genome Res., 19, 1-11.
6. Gimelbrant, A., Hutchinson, J.N., Thompson, B.R. and Chess, A. (2007) Widespread monoallelic expression on human autosomes. Science, 318, 1136-1140.
7. Lappalainen, T., Sammeth, M., Friedländer, M.R., 't Hoen, P.A.C., Monlong, J., Rivas, M.A., Gonzàlez-Porta, M., Kurbatova, N., Griebel, T., Ferreira, P.G. et al. (2013) Transcriptome and genome sequencing uncovers functional variation in humans. Nature, 501, 506-511.
8. Warburton, A., Breen, G., Bubb, V.J. and Quinn, J.P. (2016) A GWAS SNP for schizophrenia is linked to the internal MIR137 promoter and supports differential allele-specific expression. Schizophr. Bull., 42, 1003-1008.
9. Ballantyne, R.L., Zhang, X., Nunez, S., Xue, C., Zhao, W., Reed, E., Salaheen, D., Foulkes, A.S., Li, M. and Reilly, M.P. Genome-wide interrogation reveals hundreds of long intergenic noncoding RNAs that associate with cardiometabolic traits. Hum. Mol. Genet., 25, 3125-3141.
10. Conde, L., Bracci, P.M., Richardson, R., Montgomery, S.B. and Skibola, C.F. (2013) Integrating GWAS and expression data for functional characterization of disease-associated SNPs: an application to follicular lymphoma. Am. J. Hum. Genet., 92, 126-130.
11. Buckland, P.R. (2004) Allele-specific gene expression differences in humans. Hum. Mol. Genet., 13, R255-R260.
12. Storey, J.D., Madeoy, J., Strout, J.L., Wurfel, M., Ronald, J. and Akey, J.M. (2007) Gene-expression variation within and among human populations. Am. J. Hum. Genet., 80, 502-509.
13. Zhang, W., Duan, S., Kistner, E.O., Bleibel, W.K., Huang, R.S., Clark, T.A., Chen, T.X., Schweitzer, A.C., Blume, J.E. and Cox, N.J. (2008) Evaluation of genetic variation contributing to differences in gene expression between populations. Am. J. Hum. Genet., 82, 631-640.
14. Kabza, M., Kubiak, M.R., Danek, A., Rosikiewicz, W., Deorowicz, S., Polanşki, A., Makałowska, I. and Gojobori, T. (2015) Inter-population differences in retrogene loss and expression in humans. PLoS Genet., 11, e1005579.
15. Halit Ongen, E.T.D. (2015) Alternative Splicing QTLs in European and African Populations. Am. J. Hum. Genet., 97, 567-575.
16. Mozhui, K., Smith, A.K. and Tylavsky, F.A. (2015) Ancestry dependent DNA methylation and influence of maternal nutrition. PLoS One, 10, e0118466.
17. Fraser, H., Lam, L., Neumann, S. and Kobor, M. (2012) Population-specificity of human DNA methylation. Genome Biol., 13, R8.
18. Light, N., Adoue, V., Ge, B., Chen, S.-H., Kwan, T. and Pastinen, T.T.P. (2014) Interrogation of allelic chromatin states in human cells by high density ChIP genotyping. Epigenetics, 9, 1238-1251.
19. Castel, S.E., Levy-Moonshine, A., Mohammadi, P., Banks, E. and Lappalainen, T. (2015) Tools and best practices for data processing in allelic expression analysis. Genome Biol., 16, 195.
20. Chen, J., Rozowsky, J., Galeev, T.R., Harmanci, A., Kitchen, R., Bedford, J., Abyzov, A., Kong, Y., Regan, L. and Gerstein, M. (2016) A uniform survey of allele-specific binding and expression over 1000-Genomes-Project individuals. Nat. Commun., 48, 829-834.
21. McLaren, W., Gil, L., Hunt, S.E., Riat, H.S., Ritchie, G.R.S., Thormann, A., Flicek, P. and Cunningham, F. (2016) The ensembl variant effect predictor. Genome Biol., 17, 122.
22. The NHGRI GWAS Catalog, a curated resource of SNP-trait associations (2014) Nucleic Acids Res., 42, D1001-D1006.
23. Deng, X., Sabino, E.C., Cunha-Neto, E., Ribeiro, A.L., Ianni, B., Mady, C., Busch, M.P., Seielstad, M., Component, I. and Tanowitz, H.B. (2013) Genome wide association study (GWAS) of chagas cardiomyopathy in Trypanosoma cruzi seropositive subjects. PLoS One, 8, e79629.
24. Song, M.Y., Kim, H.E., Kim, S., Choi, I.H. and Lee, J.K. (2012) SNP-based large-scale identification of allele-specific gene expression in human B cells. Gene, 493, 211-218.
25. Graham, R.R., Kyogoku, C., Sigurdsson, S., Vlasova, I.A., Davies, L.R.L., Baechler, E.C., Plenge, R.M., Koeuth, T., Ortmann, W.A., Hom, G. et al. (2007) Three functional variants of IFN regulatory factor 5 (IRF5) define risk and protective haplotypes for human lupus. Proc Natl Acad Sci U S A, 104, 6758-6763.
26. Battle, A., Mostafavi, S., Zhu, X., Potash, J.B., Weissman, M.M., McCormick, C., Haudenschild, C.D., Beckman, K.B., Shi, J., Mei, R. et al. (2014) Characterizing the genetic basis of transcriptome diversity through RNA-sequencing of 922 individuals. Genome Res., 24, 14-24.
27. Zhang, K., Li, J.B., Gao, Y., Egli, D., Xie, B., Deng, J., Li, Z., Lee, J.-H., Aach, J., Leproust, E.M., Eggan, K. and Church, G.M. (2009) Digital RNA allelotyping reveals tissue-specific and allele-specific gene expression in human. Nat. Methods, 6, 613-618.
28. Hombach, D., Schwarz, J.M., Robinson, P.N., Schuelke, M. and Seelow, D. (2016) A systematic, large-scale comparison of transcription factor binding site models. BMC Genomics, 17, 388.
29. Boyle, A.P., Hong, E.L., Hariharan, M., Cheng, Y., Schaub, M.A., Kasowski, M., Karczewski, K.J., Park, J., Hitz, B.C. and Weng, S. (2012) Annotation of functional variation in personal genomes using Regulome DB. Genome Res., 22, 1790-1797.
30. Serre, D., Gurd, S., Ge, B., Sladek, R., Sinnett, D., Harmsen, E., Bibikova, M., Chudin, E., Barker, D.L., Dickinson, T. et al. (2008) Differential allelic expression in the human genome: a robust approach to identify genetic and epigenetic Cis-acting mechanisms regulating gene expression. PLoS Genet., 4, e1000006.
31. Schadt, E.E., Monks, S.A., Drake, T.A., Lusis, A.J., Che, N., Colinayo, V., Ruff, T.G., Milligan, S.B., Lamb, J.R., Cavet, G. et al. (2003) Genetics of gene expression surveyed in maize, mouse and man. Nature, 422, 297-302.
32. Shuen Lo, H., Wang, Z., Hu, Y., Yang, H.H., Gere, S. and Buetow, K.H. and Lee, M.P. (2003) Allelic Variation in Gene Expression Is Common in the Human Genome. Genome Res., 13, 1855-1862.
33. Xing, J., Watkins, W.S., Witherspoon, D.J., Zhang, Y., Guthery, S.L., Thara, R., Mowry, B.J., Bulayeva, K., Weiss, R.B. and Jorde, L.B. (2009) Fine-scaled human genetic structure revealed by SNP microarrays. Genome Res., 19, 815-825.
34. Hasin-Brumshtein, Y., Hormozdiari, F., Martin, L., van Nas, A., Eskin, E., Lusis, A.J. and Drake, T.A. (2014) Allele-specific expression and eQTL analysis in mouse adipose tissue. BMC Genomics, 15, 471.
35. Kang, E.Y., Martin, L.J., Mangul, S., Isvilanonda, W., Zou, J., Ben-David, E., Han, B., Lusis, A.J., Shifman, S. and Eskin, E. (2016) Discovering single nucleotide polymorphisms regulating human gene expression using allele specific expression from RNA-seq data. Genetics, 204, 1057-1064.
36. HU, Y.-J., SUN, W., TZENG, J.-Y. and PEROU, C.M. (2015) Proper use of allele-specific expression improves statistical power for cis-eQTL mapping with RNA-seq data. J. Am. Stat. Assoc., 110, 962-974.
37. Sun, W. (2012) A statistical framework for eQTL mapping using RNA-seq data. Biometrics, 68, 1-11.
38. Khan, A., Tian, L., Zhang, C., Yuan, K. and Xu, S. (2016) Genetic diversity and natural selection footprints of the glycine amidinotransferase gene in various human populations. Sci. Rep., 6, 18755.
39. Zhang, C., Li, J., Tian, L., Lu, D., Yuan, K., Yuan, Y. and Xu, S. (2015) Differential natural selection of human zinc transporter genes between african and non-African populations. Sci. Rep., 5, 9658.
40. Li, J., Lao, X., Zhang, C., Tian, L., Lu, D. and Xu, S. (2014) Increased genetic diversity of ADME genes in African Americans compared with their putative ancestral source populations and implications for Pharmacogenomics. BMC Genet., 15, 52.
41. Josephs, E.B., Lee, Y.W., Stinchcombe, J.R. and Wright, S.I. (2015) Association mapping reveals the role of purifying selection in the maintenance of genomic variation in gene expression. Proc. Natl. Acad. Sci. U S A, 112, 15390-15395.
42. Sato, M.P., Makino, T., Kawata, M., Carroll, S., Wray, G., Wray, G., McDonald, J., Kreitman, M., Haygood, R. and Fedrigo, O. (2016) Natural selection in a population of Drosophila melanogaster explained by changes in gene expression caused by sequence variation in core promoter regions. BMC Evol. Biol., 16, 35.
43. Navasa, N., Martin-Ruiz, I., Atondo, E., Sutherland, J.D., Angel Pascual-Itoiz, M., Carreras-González, A., Izadi, H., Tomás-Cortázar, J., Ayaz, F., Martin-Martin, N. et al. (2015) Ikaros mediates the DNA methylation-independent silencing of MCJ/DNAJC15 gene expression in macrophages. Sci. Rep., 5, 14692.
44. Navasa, N., Martín, I., Iglesias-Pedraz, J.M., Beraza, N., Atondo, E., Izadi, H., Ayaz, F., Fernández-Alvarez, S., Hatle, K. and Som, A. (2015) Regulation of oxidative stress by methylation-controlled j protein controls macrophage responses to inflammatory insults. J. Infect. Dis., 211, 135-145.
45. Vatsiou, A.I., Bazin, E. and Gaggiotti, O.E. (2016) Changes in selective pressures associated with human population expansion may explain metabolic and immune related pathways enriched for signatures of positive selection. BMC Genomics, 17, 1-11.
46. Voight, B.F., Kudaravalli, S., Wen, X., Pritchard, J.K. and Hurst, L. (2006) A map of recent positive selection in the human genome. PLoS Biol., 4, e72.
47. 1000 Genomes Project Consortium (2015) A global reference for human genetic variation. Nature, 526, 68-74.
48. Martin, A.R., Costa, H.A., Lappalainen, T., Henn, B.M., Kidd, J.M., Yee, M.C., Grubert, F., Cann, H.M., Snyder, M., Montgomery, S.B. et al. (2014) Transcriptome sequencing from diverse human populations reveals differentiated regulatory architecture. PLoS Genet., 10, e1004549.
49. Stranger, B.E., Montgomery, S.B., Dimas, A.S., Parts, L., Stegle, O., Ingle, C.E., Sekowska, M., Smith, G.D., Evans, D., Gutierrez-Arcelus, M. et al. (2012) Patterns of Cis regulatory variation in diverse human populations. PLoS Genet, 8, e1002639.
50. Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M.A.R., Bender, D., Maller, J., Sklar, P., de Bakker, P.I.W., Daly, M.J. and Sham, P.C. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses Shaun. Am. J. Hum. Genet., 81, 559-575.
51. Price, A.L., patterson, N.j., plenge, R.m., weinblatt, M.e. and shadick, N.a. (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat. Genet., 38, 904-909.
52. Patterson, N., Price, A.L. and Reich, D. (2006) Population structure and eigenanalysis. PLoS Genet., 2, 2074-2093.
53. Shabalin, A.A. (2012) Matrix eQTL: ultra fast eQTL analysis via large matrix operations. Bioinformatics, 28, 1353-1358.
54. R Core Team (2017) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.
55. Lonsdale, J., Thomas, J., Salvatore, M., Phillips, R., Lo, E., Shad, S., Hasz, R., Walters, G., Garcia, F. and Young, N. (2013) The genotype-tissue expression (GTEx) project. Nat. Genet. 45, 580-585.
56. Weir, B.S. and Hill, W.G. (2002) Estimating F-Statistics. Annu. Rev. Genet. 36, 721-750.
57. Gautier, M. and Vitalis, R. (2012) rehh: an R package to detect footprints of selection in genome-wide SNP data from haplotype structure. Bioinformatics, 28, 1176-1177.
58. Barrett, J.C., Fry, B., Maller, J. and Daly, M.J. (2005) Haploview: Analysis and visualization of LD and haplotype maps. Bioinformatics. 21, 263-265.