Allelic expression mapping across cellular lineages to establish impact of non-coding SNPs

Molecular Systems Biology

Volumn 10, Issue 10, 2014, Pages

  Adoue, Veronique ^a   Schiavi, Alicia ^b   Light, Nicholas ^b   Almlöf, Jonas Carlsson ^c   Lundmark, Per ^c   Ge, Bing ^b   Kwan, Tony ^b   Caron, Maxime ^b   Rönnblom, Lars ^c   Wang, Chuan ^c   Chen, Shu Huang ^b   Goodall, Alison H ^d,e,f   Cambien, Francois ^a,f   Deloukas, Panos ^f,g   Ouwehand, Willem H ^f,h,i   Syvänen, Ann Christine ^c   Pastinen, Tomi ^b  

^a INSERM   (France)

^b MCGILL UNIVERSITY   (Canada)

^c UPPSALA UNIVERSITY   (Sweden)

^d UNIVERSITY OF LEICESTER   (United Kingdom)

^e GLENFIELD HOSPITAL   (United Kingdom)

^f Cardiogenics Consortium ^*  (United Kingdom)

^g WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^h UNIVERSITY OF CAMBRIDGE   (United Kingdom)

ⁱ NHS BLOOD AND TRANSPLANT   (United Kingdom)

Author keywords

Allelic expression; Cis rSNPs; Complex disease; Nf b; Repressor

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TRANSCRIPTION FACTOR;

ALLELE; ARTICLE; CAUCASIAN; CELL LINEAGE; CELL POPULATION; CONTROLLED STUDY; FIBROBLAST CULTURE; GENE EXPRESSION REGULATION; GENE MAPPING; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; HAPLOTYPE MAP; HUMAN; HUMAN CELL; LYMPHOBLASTOID CELL LINE; MONOCYTE; PROTEIN ANALYSIS; PROTEIN INTERACTION; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSCRIPTION REGULATION; BLACK PERSON; CELL LINE; CHROMOSOMAL MAPPING; DNA FOOTPRINTING; GENETIC VARIATION; GENETICS; PROCEDURES; QUANTITATIVE TRAIT LOCUS; REGULATOR GENE; REPRODUCIBILITY;

AFRICAN CONTINENTAL ANCESTRY GROUP; ALLELES; CELL LINE; CHROMOSOME MAPPING; DNA FOOTPRINTING; EUROPEAN CONTINENTAL ANCESTRY GROUP; GENES, REGULATOR; GENETIC VARIATION; HUMANS; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI; REPRODUCIBILITY OF RESULTS; TRANSCRIPTION FACTORS;

EID: 84910086797     PISSN: None     EISSN: 17444292     Source Type: Journal    
DOI: 10.15252/msb.20145114     Document Type: Article

References (67)

1. Almlof JC, Lundmark P, Lundmark A, Ge B, Maouche S, Goring HH, Liljedahl U, Enstrom C, Brocheton J, Proust C, Godefroy T, Sambrook JG, Jolley J, Crisp-Hihn A, Foad N, Lloyd-Jones H, Stephens J, Gwilliam R, Rice CM, Hengstenberg C et al (2012) Powerful identification of cis-regulatory SNPs in human primary monocytes using allele-specific gene expression. PLoS ONE 7: e52260
2. Battle A, Mostafavi S, Zhu X, Potash JB, Weissman MM, McCormick C, Haudenschild CD, Beckman KB, Shi J, Mei R, Urban AE, Montgomery SB, Levinson DF, Koller D (2014) Characterizing the genetic basis of transcriptome diversity through RNA-sequencing of 922 individuals. Genome Res 24: 14-24
3. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114-2120
4. Boyle AP, Hong EL, Hariharan M, Cheng Y, Schaub MA, Kasowski M, Karczewski KJ, Park J, Hitz BC, Weng S, Cherry JM, Snyder M (2012) Annotation of functional variation in personal genomes using RegulomeDB. Genome Res 22: 1790-1797
5. Catz SD, Johnson JL (2001) Transcriptional regulation of bcl-2 by nuclear factor kappa B and its significance in prostate cancer. Oncogene 20: 7342-7351
6. Chong JA, Tapia-Ramirez J, Kim S, Toledo-Aral JJ, Zheng Y, Boutros MC, Altshuller YM, Frohman MA, Kraner SD, Mandel G (1995 ) REST: a mammalian silencer protein that restricts sodium channel gene expression to neurons. Cell 80: 949-957
7. Cirulli ET, Goldstein DB (2007) In vitro assays fail to predict in vivo effects of regulatory polymorphisms. Hum Mol Genet 16: 1931-1939
8. Cotsapas C, Voight BF, Rossin E, Lage K, Neale BM, Wallace C, Abecasis GR, Barrett JC, Behrens T, Cho J, De Jager PL, Elder JT, Graham RR, Gregersen P, Klareskog L, Siminovitch KA, van Heel DA, Wijmenga C, Worthington J, Todd JA et al, Consortia FONo (2011) Pervasive sharing of genetic effects in autoimmune disease. PLoS Genet 7: e1002254
9. Degner JF, Pai AA, Pique-Regi R, Veyrieras JB, Gaffney DJ, Pickrell JK, De Leon S, Michelini K, Lewellen N, Crawford GE, Stephens M, Gilad Y, Pritchard JK (2012) DNase I sensitivity QTLs are a major determinant of human expression variation. Nature 482: 390-394
10. Dimas AS, Deutsch S, Stranger BE, Montgomery SB, Borel C, Attar-Cohen H, Ingle C, Beazley C, Gutierrez Arcelus M, Sekowska M, Gagnebin M, Nisbett J, Deloukas P, Dermitzakis ET, Antonarakis SE (2009) Common regulatory variation impacts gene expression in a cell type-dependent manner. Science 325: 1246-1250.
11. Ding J, Gudjonsson JE, Liang L, Stuart PE, Li Y, Chen W, Weichenthal M, Ellinghaus E, Franke A, Cookson W, Nair RP, Elder JT, Abecasis GR (2010) Gene expression in skin and lymphoblastoid cells: Refined statistical method reveals extensive overlap in cis-eQTL signals. Am J Hum Genet 87: 779-789
12. Emilsson V, Thorleifsson G, Zhang B, Leonardson AS, Zink F, Zhu J, Carlson S, Helgason A, Walters GB, Gunnarsdottir S, Mouy M, Steinthorsdottir V, Eiriksdottir GH, Bjornsdottir G, Reynisdottir I, Gudbjartsson D, Helgadottir A, Jonasdottir A, Jonasdottir A, Styrkarsdottir U et al (2008) Genetics of gene expression and its effect on disease. Nature 452: 423-428
13. Ernst J, Kheradpour P, Mikkelsen TS, Shoresh N, Ward LD, Epstein CB, Zhang X, Wang L, Issner R, Coyne M, Ku M, Durham T, Kellis M, Bernstein BE (2011) Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473: 43-49
14. Fairfax BP, Makino S, Radhakrishnan J, Plant K, Leslie S, Dilthey A, Ellis P, Langford C, Vannberg FO, Knight JC (2012) Genetics of gene expression in primary immune cells identifies cell type-specific master regulators and roles of HLA alleles. Nat Genet 44: 502-510
15. Fazio G, Palmi C, Rolink A, Biondi A, Cazzaniga G (2008) PAX5/TEL acts as a transcriptional repressor causing down-modulation of CD19, enhances migration to CXCL12, and confers survival advantage in pre-BI cells. Cancer Res 68: 181-189
16. Feng J, Liu T, Qin B, Zhang Y, Liu XS (2012) Identifying ChIP-seq enrichment using MACS. Nat Protoc 7: 1728-1740
17. Garnier S, Truong V, Brocheton J, Zeller T, Rovital M, Wild PS, Ziegler A, Munzel T, Tiret L, Blankenberg S, Deloukas P, Erdmann J, Hengstenberg C, Samani NJ, Schunkert H, Ouwehand WH, Goodall AH, Cambien F, Tregouet DA (2013) Genome-wide haplotype analysis of cis expression quantitative trait loci in monocytes. PLoS Genet 9: e1003240
18. Ge B, Pokholok DK, Kwan T, Grundberg E, Morcos L, Verlaan DJ, Le J, Koka V, Lam KC, Gagne V, Dias J, Hoberman R, Montpetit A, Joly MM, Harvey EJ, Sinnett D, Beaulieu P, Hamon R, Graziani A, Dewar K et al (2009) Global patterns of cis variation in human cells revealed by high-density allelic expression analysis. Nat Genet 41: 1216-1222
19. Grant CE, Bailey TL, Noble WS (2011) FIMO: scanning for occurrences of a given motif. Bioinformatics 27: 1017-1018
20. Grundberg E, Adoue V, Kwan T, Ge B, Duan QL, Lam KC, Koka V, Kindmark A, Weiss ST, Tantisira K, Mallmin H, Raby BA, Nilsson O, Pastinen T (2011) Global analysis of the impact of environmental perturbation on cis-regulation of gene expression. PLoS Genet 7: e1001279
21. Grundberg E, Small KS, Hedman AK, Nica AC, Buil A, Keildson S, Bell JT, Yang TP, Meduri E, Barrett A, Nisbett J, Sekowska M, Wilk A, Shin SY, Glass D, Travers M, Min JL, Ring S, Ho K, Thorleifsson G et al (2012) Mapping cis- and trans-regulatory effects across multiple tissues in twins. Nat Genet 44: 1084-1089
22. Hendriks JJ, Teunissen CE, de Vries HE, Dijkstra CD (2005) Macrophages and neurodegeneration. Brain Res Brain Res Rev 48: 185-195
23. Hess A, Iyer H (2007) Fisher's combined p-value for detecting differentially expressed genes using Affymetrix expression arrays. BMC Genomics 8: 96
24. Hiscott J, Marois J, Garoufalis J, D'Addario M, Roulston A, Kwan I, Pepin N, Lacoste J, Nguyen H, Bensi G, Fenton M (1993) Characterization of a functional NF-kappa B site in the human interleukin 1 beta promoter: evidence for a positive autoregulatory loop. Mol Cell Biol 13: 6231-6240
25. Hoggatt AM, Kriegel AM, Smith AF, Herring BP (2000) Hepatocyte nuclear factor-3 homologue 1 (HFH-1) represses transcription of smooth muscle-specific genes. J Biol Chem 275: 31162-31170
26. Howie BN, Donnelly P, Marchini J (2009) A flexible and accurate genotype imputation method for the next generation of genome-wide association studies. PLoS Genet 5: e1000529
27. International Multiple Sclerosis Genetics C, Wellcome Trust Case Control C, Sawcer S, Hellenthal G, Pirinen M, Spencer CC, Patsopoulos NA, Moutsianas L, Dilthey A, Su Z, Freeman C, Hunt SE, Edkins S, Gray E, Booth DR, Potter SC, Goris A, Band G, Oturai AB, Strange A et al (2011) Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature 476: 214-219.
28. Ito T, Nishiyama C, Nakano N, Nishiyama M, Usui Y, Takeda K, Kanada S, Fukuyama K, Akiba H, Tokura T, Hara M, Tsuboi R, Ogawa H, Okumura K (2009) Roles of PU.1 in monocyte- and mast cell-specific gene regulation: PU.1 transactivates CIITA pIV in cooperation with IFN-gamma. Int Immunol 21: 803-816
29. Kang HB, Kim YE, Kwon HJ, Sok DE, Lee Y (2007) Enhancement of NF-kappaB expression and activity upon differentiation of human embryonic stem cell line SNUhES3. Stem Cells Dev 16: 615-623
30. Karczewski KJ, Dudley JT, Kukurba KR, Chen R, Butte AJ, Montgomery SB, Snyder M (2013) Systematic functional regulatory assessment of disease-associated variants. Proc Natl Acad Sci USA 110: 9607-9612
31. Kempe S, Kestler H, Lasar A, Wirth T (2005) NF-kappaB controls the global pro-inflammatory response in endothelial cells: evidence for the regulation of a pro-atherogenic program. Nucleic Acids Res 33: 5308-5319
32. Kraft P (2008) Curses-winner's and otherwise-in genetic epidemiology. Epidemiology 19: 649-651; discussion 657-648
33. Kueh HY, Champhekhar A, Nutt SL, Elowitz MB, Rothenberg EV (2013) Positive feedback between PU. 1 and the cell cycle controls myeloid differentiation. Science 341: 670-673
34. Kwan T, Benovoy D, Dias C, Gurd S, Provencher C, Beaulieu P, Hudson TJ, Sladek R, Majewski J (2008) Genome-wide analysis of transcript isoform variation in humans. Nat Genet 40: 225-231
35. Lappalainen T, Sammeth M, Friedlander MR, 't Hoen PA, Monlong J, Rivas MA, Gonzalez-Porta M, Kurbatova N, Griebel T, Ferreira PG, Barann M, Wieland T, Greger L, van Iterson M, Almlof J, Ribeca P, Pulyakhina I, Esser D, Giger T, Tikhonov A et al (2013) Transcriptome and genome sequencing uncovers functional variation in humans. Nature 501: 506-511
36. Light N, Adoue V, Ge B, Chen SH, Kwan T, Pastinen T (2014) Interrogation of allelic chromatin states in human cells by high-density ChIP-genotyping. Epigenetics 9: 1238-1251
37. Lyss G, Knorre A, Schmidt TJ, Pahl HL, Merfort I (1998) The anti-inflammatory sesquiterpene lactone helenalin inhibits the transcription factor NF-kappaB by directly targeting p65. J Biol Chem 273: 33508-33516
38. Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ, McCarthy MI, Ramos EM, Cardon LR, Chakravarti A, Cho JH, Guttmacher AE, Kong A, Kruglyak L, Mardis E, Rotimi CN, Slatkin M, Valle D, Whittemore AS, Boehnke M et al (2009) Finding the missing heritability of complex diseases. Nature 461: 747-753
39. Maurano MT, Humbert R, Rynes E, Thurman RE, Haugen E, Wang H, Reynolds AP, Sandstrom R, Qu H, Brody J, Shafer A, Neri F, Lee K, Kutyavin T, Stehling-Sun S, Johnson AK, Canfield TK, Giste E, Diegel M, Bates D et al (2012) Systematic localization of common disease-associated variation in regulatory DNA. Science 337: 1190-1195
40. Mendenhall EM, Williamson KE, Reyon D, Zou JY, Ram O, Joung JK, Bernstein BE (2013) Locus-specific editing of histone modifications at endogenous enhancers. Nat Biotechnol 31: 1133-1136
41. Montgomery SB, Sammeth M, Gutierrez-Arcelus M, Lach RP, Ingle C, Nisbett J, Guigo R, Dermitzakis ET (2010) Transcriptome genetics using second generation sequencing in a Caucasian population. Nature 464: 773-777
42. Mori N, Prager D (1996) Transactivation of the interleukin-1alpha promoter by human T-cell leukemia virus type I and type II Tax proteins. Blood 87: 3410-3417
43. Myatt SS, Lam EW (2007) The emerging roles of forkhead box (Fox) proteins in cancer. Nat Rev Cancer 7: 847-859
44. Neph S, Vierstra J, Stergachis AB, Reynolds AP, Haugen E, Vernot B, Thurman RE, John S, Sandstrom R, Johnson AK, Maurano MT, Humbert R, Rynes E, Wang H, Vong S, Lee K, Bates D, Diegel M, Roach V, Dunn D et al (2012) An expansive human regulatory lexicon encoded in transcription factor footprints. Nature 489: 83-90
45. Nica AC, Parts L, Glass D, Nisbet J, Barrett A, Sekowska M, Travers M, Potter S, Grundberg E, Small K, Hedman AK, Bataille V, Tzenova Bell J, Surdulescu G, Dimas AS, Ingle C, Nestle FO, di Meglio P, Min JL, Wilk A et al (2011) The architecture of gene regulatory variation across multiple human tissues: the MuTHER study. PLoS Genet 7: e1002003.
46. Pastinen T (2010) Genome-wide allele-specific analysis: insights into regulatory variation. Nat Rev Genet 11: 533-538
47. Pavlidis P, Noble WS (2003) Matrix2png: a utility for visualizing matrix data. Bioinformatics 19: 295-296
48. Pickrell JK, Marioni JC, Pai AA, Degner JF, Engelhardt BE, Nkadori E, Veyrieras JB, Stephens M, Gilad Y, Pritchard JK (2010) Understanding mechanisms underlying human gene expression variation with RNA sequencing. Nature 464: 768-772
49. Ruiz C, Oeggerli M, Germann M, Gluderer S, Stocker H, Andreozzi M, Thalmann GN, Cecchini MG, Zellweger T, Sturm S, Koivisto PA, Helin HJ, Gelmann EP, Glass AG, Gasser TC, Terracciano LM, Bachmann A, Wyler S, Bubendorf L, Rentsch CA (2012) High NRBP1 expression in prostate cancer is linked with poor clinical outcomes and increased cancer cell growth. Prostate 72: 1678-1687
50. Sanseau P, Agarwal P, Barnes MR, Pastinen T, Richards JB, Cardon LR, Mooser V (2012) Use of genome-wide association studies for drug repositioning. Nat Biotechnol 30: 317-320
51. Schadt EE, Monks SA, Drake TA, Lusis AJ, Che N, Colinayo V, Ruff TG, Milligan SB, Lamb JR, Cavet G, Linsley PS, Mao M, Stoughton RB, Friend SH (2003) Genetics of gene expression surveyed in maize, mouse and man. Nature 422: 297-302
52. Schoenherr CJ, Anderson DJ (1995) The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuron-specific genes. Science 267: 1360-1363
53. Sehnert B, Burkhardt H, Wessels JT, Schroder A, May MJ, Vestweber D, Zwerina J, Warnatz K, Nimmerjahn F, Schett G, Dubel S, Voll RE (2013) NF-kappaB inhibitor targeted to activated endothelium demonstrates a critical role of endothelial NF-kappaB in immune-mediated diseases. Proc Natl Acad Sci USA 110: 16556-16561
54. Son YH, Jeong YT, Lee KA, Choi KH, Kim SM, Rhim BY, Kim K (2008) Roles of MAPK and NF-kappaB in interleukin-6 induction by lipopolysaccharide in vascular smooth muscle cells. J Cardiovasc Pharmacol 51: 71-77
55. Stolk L, Perry JR, Chasman DI, He C, Mangino M, Sulem P, Barbalic M, Broer L, Byrne EM, Ernst F, Esko T, Franceschini N, Gudbjartsson DF, Hottenga JJ, Kraft P, McArdle PF, Porcu E, Shin SY, Smith AV, van Wingerden S et al (2012) Meta-analyses identify 13 loci associated with age at menopause and highlight DNA repair and immune pathways. Nat Genet 44: 260-268
56. Suzuki S, Singhirunnusorn P, Nakano H, Doi T, Saiki I, Sakurai H (2006) Identification of TNF-alpha-responsive NF-kappaB p65-binding element in the distal promoter of the mouse serine protease inhibitor SerpinE2. FEBS Lett 580: 3257-3262.
57. Takegawa S, Jin Z, Nakayama T, Oyama T, Hieshima K, Nagakubo D, Shirakawa AK, Tsuzuki T, Nakamura S, Yoshie O (2008) Expression of CCL17 and CCL22 by latent membrane protein 1-positive tumor cells in age-related Epstein-Barr virus-associated B-cell lymphoproliferative disorder. Cancer Sci 99: 296-302
58. The ENCODE Project Consortium (2012) An integrated encyclopedia of DNA elements in the human genome. Nature 489: 57-74
59. Thurman RE, Rynes E, Humbert R, Vierstra J, Maurano MT, Haugen E, Sheffield NC, Stergachis AB, Wang H, Vernot B, Garg K, John S, Sandstrom R, Bates D, Boatman L, Canfield TK, Diegel M, Dunn D, Ebersol AK, Frum T et al (2012) The accessible chromatin landscape of the human genome. Nature 489: 75-82
60. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511-515
61. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7: 562-578
62. Vaquerizas JM, Kummerfeld SK, Teichmann SA, Luscombe NM (2009) A census of human transcription factors: function, expression and evolution. Nat Rev Genet 10: 252-263
63. Verlaan DJ, Berlivet S, Hunninghake GM, Madore AM, Lariviere M, Moussette S, Grundberg E, Kwan T, Ouimet M, Ge B, Hoberman R, Swiatek M, Dias J, Lam KC, Koka V, Harmsen E, Soto-Quiros M, Avila L, Celedon JC, Weiss ST et al (2009) Allele-specific chromatin remodeling in the ZPBP2/GSDMB/ORMDL3 locus associated with the risk of asthma and autoimmune disease. Am J Hum Genet 85: 377-393
64. Wagner JR, Busche S, Ge B, Kwan T, Pastinen T, Blanchette M (2014) The relationship between DNA methylation, genetic and expression inter-individual variation in untransformed human fibroblasts. Genome Biol 15: R37
65. Wang Y, Zhou Y, Graves DT (2014) FOXO transcription factors: their clinical significance and regulation. BioMed Res Int 2014: 925350
66. Wilson MD, Barbosa-Morais NL, Schmidt D, Conboy CM, Vanes L, Tybulewicz VL, Fisher EM, Tavare S, Odom DT (2008) Species-specific transcription in mice carrying human chromosome 21. Science 322: 434-438
67. Zhang W, Duan S, Kistner EO, Bleibel WK, Huang RS, Clark TA, Chen TX, Schweitzer AC, Blume JE, Cox NJ, Dolan ME (2008) Evaluation of genetic variation contributing to differences in gene expression between populations. Am J Hum Genet 82: 631-640