TCF21 and the environmental sensor aryl-hydrocarbon receptor cooperate to activate a pro-inflammatory gene expression program in coronary artery smooth muscle cells

PLoS Genetics

Volumn 13, Issue 5, 2017, Pages

  Kim, Juyong Brian ^a   Pjanic, Milos ^a   Nguyen, Trieu ^a   Miller, Clint L ^a   Iyer, Dharini ^a   Liu, Boxiang ^a   Wang, Ting ^a   Sazonova, Olga ^a   Carcamo Orive, Ivan ^a   Matic, Ljubica Perisic ^b   Maegdefessel, Lars ^b   Hedin, Ulf ^b   Quertermous, Thomas ^a  

^a STANFORD UNIVERSITY   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; CYTOCHROME P450 1A1; DIOXIN; INTERLEUKIN 1ALPHA; INTERSTITIAL COLLAGENASE; POLYCYCLIC AROMATIC HYDROCARBON; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TCF21; UNCLASSIFIED DRUG; AHR PROTEIN, HUMAN; ARNT PROTEIN, HUMAN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CYP1A1 PROTEIN, HUMAN; HYPOXIA INDUCIBLE FACTOR 1BETA; IL1A PROTEIN, HUMAN; MMP1 PROTEIN, HUMAN; PROTEIN BINDING; TCF21 PROTEIN, HUMAN;

AHR GENE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARNT GENE; ARTICLE; ATHEROSCLEROSIS; BINDING AFFINITY; BINDING SITE; CARDIOVASCULAR RISK; CONTROLLED STUDY; CORONARY ARTERY; CORONARY ARTERY DISEASE; CYP1A1 GENE; GENE; GENE EXPRESSION; GENE FUNCTION; GENE LOCUS; GENE TARGETING; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE ENVIRONMENT INTERACTION; HUMAN; HUMAN CELL; IL1A GENE; INNATE IMMUNITY; MMP1 GENE; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; QUANTITATIVE TRAIT LOCUS; REGULATORY MECHANISM; SINGLE NUCLEOTIDE POLYMORPHISM; SMOOTH MUSCLE CELL; TCF21 GENE; UPREGULATION; ANIMAL; C57BL MOUSE; CELL CULTURE; CORONARY BLOOD VESSEL; CYTOLOGY; GENETICS; HEK293 CELL LINE; METABOLISM;

ANIMALS; ARYL HYDROCARBON RECEPTOR NUCLEAR TRANSLOCATOR; ATHEROSCLEROSIS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELLS, CULTURED; CORONARY VESSELS; CYTOCHROME P-450 CYP1A1; HEK293 CELLS; HUMANS; INTERLEUKIN-1ALPHA; MATRIX METALLOPROTEINASE 1; MICE; MICE, INBRED C57BL; MYOCYTES, SMOOTH MUSCLE; PROTEIN BINDING; RECEPTORS, ARYL HYDROCARBON;

EID: 85020172478     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1006750     Document Type: Article

References (61)

1. Schunkert H, König I, Kathiresan S, Reilly M, Assimes T, Holm H, et al. Large-scale association analysis identifies 13 new susceptibility loci for coronary artery disease. Nat Genet. 2011;43(4):333–8. doi: 10.1038/ng.784 21378990
2. CARDIoGRAMplusC4D CDeloukas P, Kanoni S, Willenborg C, Farrall M, Assimes T, et al. Large-scale association analysis identifies new risk loci for coronary artery disease. Nat Genet. 2013;45(1):25–33. doi: 10.1038/ng.2480 23202125
3. Coronary Artery Disease Genetics CA genome-wide association study in Europeans and South Asians identifies five new loci for coronary artery disease. Nat Genet. 2011;43(4):339–44. doi: 10.1038/ng.782 21378988
4. Nikpay M, Goel A, Won HH, Hall LM, Willenborg C, Kanoni S, et al. A comprehensive 1,000 Genomes-based genome-wide association meta-analysis of coronary artery disease. Nat Genet. 2015;47(10):1121–30. PubMed Central PMCID: PMCPMC4589895. doi: 10.1038/ng.3396 26343387
5. Zuk O, Hechter E, Sunyaev SR, Lander ES, The mystery of missing heritability: Genetic interactions create phantom heritability. Proc Natl Acad Sci U S A. 2012;109(4):1193–8. Epub 2012/01/10. PubMed Central PMCID: PMC3268279. doi: 10.1073/pnas.1119675109 22223662
6. Franks PW, Pare G, Putting the Genome in Context: Gene-Environment Interactions in Type 2 Diabetes. Curr Diab Rep. 2016;16(7):57. doi: 10.1007/s11892-016-0758-y 27155607
7. Wang Y, Wang L, Liu X, Zhang Y, Yu L, Zhang F, et al. Genetic variants associated with myocardial infarction and the risk factors in Chinese population. PLoS One. 2014;9(1):e86332. PubMed Central PMCID: PMCPMC3903528. doi: 10.1371/journal.pone.0086332 24475106
8. Miller C, Anderson D, Kundu R, Raiesdana A, Nürnberg S, Diaz R, et al. Disease-related growth factor and embryonic signaling pathways modulate an enhancer of TCF21 expression at the 6q23.2 coronary heart disease locus. PLoS Genet. 2013;9(7):e1003652. doi: 10.1371/journal.pgen.1003652 23874238
9. Miller C, Haas U, Diaz R, Leeper N, Kundu R, Patlolla B, et al. Coronary heart disease-associated variation in TCF21 disrupts a miR-224 binding site and miRNA-mediated regulation. PLoS Genet. 2014;10(3):e1004263. doi: 10.1371/journal.pgen.1004263 24676100
10. Nurnberg S, Cheng K, Raiesdana A, Kundu R, Miller C, Kim J, et al. Coronary Artery Disease Associated Transcription Factor TCF21 Regulates Smooth Muscle Precursor Cells That Contribute to the Fibrous Cap. PLoS Genet. 2015;11(5):e1005155. doi: 10.1371/journal.pgen.1005155 26020946
11. Bennett MR, Sinha S, Owens GK, Vascular Smooth Muscle Cells in Atherosclerosis. Circ Res. 2016;118(4):692–702. PubMed Central PMCID: PMCPMC4762053. doi: 10.1161/CIRCRESAHA.115.306361 26892967
12. Sazonova O, Zhao Y, Nürnberg S, Miller C, Pjanic M, Castano V, et al. Characterization of TCF21 Downstream Target Regions Identifies a Transcriptional Network Linking Multiple Independent Coronary Artery Disease Loci. PLoS Genet. 2015;11(5):e1005202. doi: 10.1371/journal.pgen.1005202 26020271
13. Hollingshead BD, Beischlag TV, Dinatale BC, Ramadoss P, Perdew GH, Inflammatory signaling and aryl hydrocarbon receptor mediate synergistic induction of interleukin 6 in MCF-7 cells. Cancer research. 2008;68(10):3609–17. Epub 2008/05/17. PubMed Central PMCID: PMC2568985. doi: 10.1158/0008-5472.CAN-07-6168 18483242
14. Vondracek J, Umannova L, Machala M, Interactions of the aryl hydrocarbon receptor with inflammatory mediators: beyond CYP1A regulation. Current drug metabolism. 2011;12(2):89–103. Epub 2011/03/16. 21401513
15. Stockinger B, Hirota K, Duarte J, Veldhoen M, External influences on the immune system via activation of the aryl hydrocarbon receptor. Seminars in immunology. 2011;23(2):99–105. Epub 2011/02/04. doi: 10.1016/j.smim.2011.01.008 21288737
16. Shivanna B, Maity S, Zhang S, Patel A, Jiang W, Wang L, et al. Gene Expression Profiling Identifies Cell Proliferation and Inflammation as the Predominant Pathways Regulated by Aryl Hydrocarbon Receptor in Primary Human Fetal Lung Cells Exposed to Hyperoxia. Toxicol Sci. 2016;152(1):155–68. Epub 2016/04/23. PubMed Central PMCID: PMC4922543. doi: 10.1093/toxsci/kfw071 27103661
17. Vogel C, Khan E, Leung P, Gershwin M, Chang W, Wu D, et al. Cross-talk between aryl hydrocarbon receptor and the inflammatory response: a role for nuclear factor-κB. J Biol Chem. 2014;289(3):1866–75. doi: 10.1074/jbc.M113.505578 24302727
18. Beischlag TV, Luis Morales J, Hollingshead BD, Perdew GH, The aryl hydrocarbon receptor complex and the control of gene expression. Critical reviews in eukaryotic gene expression. 2008;18(3):207–50. Epub 2008/06/11. PubMed Central PMCID: PMC2583464. 18540824
19. Brandstatter O, Schanz O, Vorac J, Konig J, Mori T, Maruyama T, et al. Balancing intestinal and systemic inflammation through cell type-specific expression of the aryl hydrocarbon receptor repressor. Sci Rep. 2016;6:26091. Epub 2016/05/18. PubMed Central PMCID: PMC4869119. doi: 10.1038/srep26091 27184933
20. Carreira VS, Fan Y, Kurita H, Wang Q, Ko CI, Naticchioni M, et al. Disruption of Ah Receptor Signaling during Mouse Development Leads to Abnormal Cardiac Structure and Function in the Adult. PLoS One. 2015;10(11):e0142440. Epub 2015/11/12. PubMed Central PMCID: PMC4640841. doi: 10.1371/journal.pone.0142440 26555816
21. Carreira VS, Fan Y, Wang Q, Zhang X, Kurita H, Ko CI, et al. Ah Receptor Signaling Controls the Expression of Cardiac Development and Homeostasis Genes. Toxicol Sci. 2015;147(2):425–35. Epub 2015/07/04. PubMed Central PMCID: PMC4707199. doi: 10.1093/toxsci/kfv138 26139165
22. Kerley-Hamilton J, Trask H, Ridley C, Dufour E, Lesseur C, Ringelberg C, et al. Inherent and benzo[a]pyrene-induced differential aryl hydrocarbon receptor signaling greatly affects life span, atherosclerosis, cardiac gene expression, and body and heart growth in mice. Toxicol Sci. 2012;126(2):391–404. doi: 10.1093/toxsci/kfs002 22228805
23. Kitamura M, Kasai A, Cigarette smoke as a trigger for the dioxin receptor-mediated signaling pathway. Cancer Lett. 2007;252(2):184–94. doi: 10.1016/j.canlet.2006.11.015 17189671
24. Kim M, Pelloux V, Guyot E, Tordjman J, Bui L, Chevallier A, et al. Inflammatory pathway genes belong to major targets of persistent organic pollutants in adipose cells. Environ Health Perspect. 2012;120(4):508–14. doi: 10.1289/ehp.1104282 22262711
25. Bertazzi PA, Consonni D, Bachetti S, Rubagotti M, Baccarelli A, Zocchetti C, et al. Health effects of dioxin exposure: a 20-year mortality study. American journal of epidemiology. 2001;153(11):1031–44. Epub 2001/06/08. 11390319
26. Wu D, Nishimura N, Kuo V, Fiehn O, Shahbaz S, Van Winkle L, et al. Activation of aryl hydrocarbon receptor induces vascular inflammation and promotes atherosclerosis in apolipoprotein E-/- mice. Arterioscler Thromb Vasc Biol. 2011;31(6):1260–7. doi: 10.1161/ATVBAHA.110.220202 21441140
27. Huang S, Shui X, He Y, Xue Y, Li J, Li G, et al. AhR expression and polymorphisms are associated with risk of coronary arterial disease in Chinese population. Sci Rep. 2015;5:8022. doi: 10.1038/srep08022 25620626
28. Young MD, Wakefield MJ, Smyth GK, Oshlack A, Gene ontology analysis for RNA-seq: accounting for selection bias. Genome biology. 2010;11(2):R14. Epub 2010/02/06. PubMed Central PMCID: PMC2872874. doi: 10.1186/gb-2010-11-2-r14 20132535
29. van Dam S, Craig T, de Magalhaes JP, GeneFriends: a human RNA-seq-based gene and transcript co-expression database. Nucleic Acids Res. 2015;43(Database issue):D1124–32. Epub 2014/11/02. PubMed Central PMCID: PMC4383890. doi: 10.1093/nar/gku1042 25361971
30. Kerkvliet NI, Immunological effects of chlorinated dibenzo-p-dioxins. Environ Health Perspect. 1995;103Suppl 9:47–53. PubMed Central PMCID: PMCPMC1518816.
31. Ono Y, Torii K, Fritsche E, Shintani Y, Nishida E, Nakamura M, et al. Role of the aryl hydrocarbon receptor in tobacco smoke extract-induced matrix metalloproteinase-1 expression. Exp Dermatol. 2013;22(5):349–53. doi: 10.1111/exd.12148 23614742
32. Tsai MJ, Hsu YL, Wang TN, Wu LY, Lien CT, Hung CH, et al. Aryl hydrocarbon receptor (AhR) agonists increase airway epithelial matrix metalloproteinase activity. J Mol Med (Berl). 2014;92(6):615–28.
33. Miller CL, Pjanic M, Wang T, Nguyen T, Cohain A, Lee JD, et al. Integrative functional genomics identifies regulatory mechanisms at coronary artery disease loci. Nat Commun. 2016;7:12092. PubMed Central PMCID: PMCPMC4941121. doi: 10.1038/ncomms12092 27386823
34. Arab K, Smith LT, Gast A, Weichenhan D, Huang JP, Claus R, et al. Epigenetic deregulation of TCF21 inhibits metastasis suppressor KISS1 in metastatic melanoma. Carcinogenesis. 2011;32(10):1467–73. PubMed Central PMCID: PMCPMC3179423. doi: 10.1093/carcin/bgr138 21771727
35. Mathelier A, Zhao X, Zhang AW, Parcy F, Worsley-Hunt R, Arenillas DJ, et al. JASPAR 2014: an extensively expanded and updated open-access database of transcription factor binding profiles. Nucleic Acids Res. 2014;42(Database issue):D142-7. PubMed Central PMCID: PMCPMC3965086.
36. Arab K, Park YJ, Lindroth AM, Schafer A, Oakes C, Weichenhan D, et al. Long noncoding RNA TARID directs demethylation and activation of the tumor suppressor TCF21 via GADD45A. Molecular cell. 2014;55(4):604–14. Epub 2014/08/05. doi: 10.1016/j.molcel.2014.06.031 25087872
37. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, et al. Model-based analysis of ChIP-Seq (MACS). Genome biology. 2008;9(9):R137. Epub 2008/09/19. PubMed Central PMCID: PMC2592715. doi: 10.1186/gb-2008-9-9-r137 18798982
38. Sekiya T, Muthurajan UM, Luger K, Tulin AV, Zaret KS, Nucleosome-binding affinity as a primary determinant of the nuclear mobility of the pioneer transcription factor FoxA. Genes Dev. 2009;23(7):804–9.; PubMed Central PMCID: PMCPMC2666343. doi: 10.1101/gad.1775509 19339686
39. Gaffney DJ, McVicker G, Pai AA, Fondufe-Mittendorf YN, Lewellen N, Michelini K, et al. Controls of nucleosome positioning in the human genome. PLoS Genet. 2012;8(11):e1003036. PubMed Central PMCID: PMCPMC3499251. doi: 10.1371/journal.pgen.1003036 23166509
40. McLean CY, Bristor D, Hiller M, Clarke SL, Schaar BT, Lowe CB, et al. GREAT improves functional interpretation of cis-regulatory regions. Nature biotechnology. 2010;28(5):495–501. Epub 2010/05/04. PubMed Central PMCID: PMC4840234. doi: 10.1038/nbt.1630 20436461
41. Lo R, Matthews J, High-resolution genome-wide mapping of AHR and ARNT binding sites by ChIP-Seq. Toxicol Sci. 2012;130(2):349–61. Epub 2012/08/21. doi: 10.1093/toxsci/kfs253 22903824
42. Welter D, MacArthur J, Morales J, Burdett T, Hall P, Junkins H, et al. The NHGRI GWAS Catalog, a curated resource of SNP-trait associations. Nucleic Acids Res. 2014;42(Database issue):D1001–6. Epub 2013/12/10. PubMed Central PMCID: PMC3965119. doi: 10.1093/nar/gkt1229 24316577
43. McMillan B, Bradfield C, The aryl hydrocarbon receptor is activated by modified low-density lipoprotein. Proc Natl Acad Sci U S A. 2007;104(4):1412–7. doi: 10.1073/pnas.0607296104 17227852
44. Kerzee JK, Ramos KS, Activation of c-Ha-ras by benzo(a)pyrene in vascular smooth muscle cells involves redox stress and aryl hydrocarbon receptor. Molecular pharmacology. 2000;58(1):152–8. 10860937
45. Sasaki T, Kuzuya M, Nakamura K, Cheng XW, Shibata T, Sato K, et al. A simple method of plaque rupture induction in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2006;26(6):1304–9. Epub 2006/04/01. doi: 10.1161/01.ATV.0000219687.71607.f7 16574894
46. Perisic L, Aldi S, Sun Y, Folkersen L, Razuvaev A, Roy J, et al. Gene expression signatures, pathways and networks in carotid atherosclerosis. Journal of internal medicine. 2016;279(3):293–308. Epub 2015/12/02. doi: 10.1111/joim.12448 26620734
47. Moyer BJ, Rojas IY, Kerley-Hamilton JS, Hazlett HF, Nemani KV, Trask HW, et al. Inhibition of the aryl hydrocarbon receptor prevents Western diet-induced obesity. Model for AHR activation by kynurenine via oxidized-LDL, TLR2/4, TGFbeta, and IDO1. Toxicol Appl Pharmacol. 2016;300:13–24. PubMed Central PMCID: PMCPMC4851598. doi: 10.1016/j.taap.2016.03.011 27020609
48. Pjanic M, Pjanic P, Schmid C, Ambrosini G, Gaussin A, Plasari G, et al. Nuclear factor I revealed as family of promoter binding transcription activators. BMC Genomics. 2011;12:181. PubMed Central PMCID: PMCPMC3082249. doi: 10.1186/1471-2164-12-181 21473784
49. Pjanic M, Schmid CD, Gaussin A, Ambrosini G, Adamcik J, Pjanic P, et al. Nuclear Factor I genomic binding associates with chromatin boundaries. BMC Genomics. 2013;14:99. PubMed Central PMCID: PMCPMC3610271. doi: 10.1186/1471-2164-14-99 23402308
50. Smith NC, Matthews JM, Mechanisms of DNA-binding specificity and functional gene regulation by transcription factors. Current opinion in structural biology. 2016;38:68–74. Epub 2016/06/14. doi: 10.1016/j.sbi.2016.05.006 27295424
51. Sun F, Indran IR, Zhang ZW, Tan MH, Li Y, Lim ZL, et al. A novel prostate cancer therapeutic strategy using icaritin-activated arylhydrocarbon-receptor to co-target androgen receptor and its splice variants. Carcinogenesis. 2015;36(7):757–68. Epub 2015/04/25. PubMed Central PMCID: PMC4580537. doi: 10.1093/carcin/bgv040 25908644
52. Hong CY, Gong EY, Kim K, Suh JH, Ko HM, Lee HJ, et al. Modulation of the expression and transactivation of androgen receptor by the basic helix-loop-helix transcription factor Pod-1 through recruitment of histone deacetylase 1. Molecular endocrinology. 2005;19(9):2245–57. Epub 2005/05/28. doi: 10.1210/me.2004-0400 15919722
53. Carney SA, Chen J, Burns CG, Xiong KM, Peterson RE, Heideman W, Aryl hydrocarbon receptor activation produces heart-specific transcriptional and toxic responses in developing zebrafish. Molecular pharmacology. 2006;70(2):549–61. Epub 2006/05/23. doi: 10.1124/mol.106.025304 16714409
54. Plavicki J, Hofsteen P, Peterson RE, Heideman W, Dioxin inhibits zebrafish epicardium and proepicardium development. Toxicol Sci. 2013;131(2):558–67. Epub 2012/11/09. PubMed Central PMCID: PMC3551425. doi: 10.1093/toxsci/kfs301 23135548
55. Merki E, Zamora M, Raya A, Kawakami Y, Wang J, Zhang X, et al. Epicardial retinoid X receptor alpha is required for myocardial growth and coronary artery formation. Proc Natl Acad Sci U S A. 2005;102(51):18455–60. Epub 2005/12/15. PubMed Central PMCID: PMC1317903. doi: 10.1073/pnas.0504343102 16352730
56. Braitsch CM, Combs MD, Quaggin SE, Yutzey KE, Pod1/Tcf21 is regulated by retinoic acid signaling and inhibits differentiation of epicardium-derived cells into smooth muscle in the developing heart. Developmental biology. 2012;368(2):345–57. Epub 2012/06/13. PubMed Central PMCID: PMC3414197. doi: 10.1016/j.ydbio.2012.06.002 22687751
57. Jacobs H, Dennefeld C, Feret B, Viluksela M, Hakansson H, Mark M, et al. Retinoic acid drives aryl hydrocarbon receptor expression and is instrumental to dioxin-induced toxicity during palate development. Environ Health Perspect. 2011;119(11):1590–5. Epub 2011/08/03. PubMed Central PMCID: PMC3226489. doi: 10.1289/ehp.1003075 21807577
58. Murphy KA, Villano CM, Dorn R, White LA, Interaction between the aryl hydrocarbon receptor and retinoic acid pathways increases matrix metalloproteinase-1 expression in keratinocytes. J Biol Chem. 2004;279(24):25284–93. Epub 2004/04/13. doi: 10.1074/jbc.M402168200 15075337
59. Magne J, Gustafsson P, Jin H, Maegdefessel L, Hultenby K, Wernerson A, et al. ATG16L1 Expression in Carotid Atherosclerotic Plaques Is Associated With Plaque Vulnerability. Arterioscler Thromb Vasc Biol. 2015;35(5):1226–35. Epub 2015/03/15. doi: 10.1161/ATVBAHA.114.304840 25767270
60. Picelli S, Faridani OR, Bjorklund AK, Winberg G, Sagasser S, Sandberg R, Full-length RNA-seq from single cells using Smart-seq2. Nat Protoc. 2014;9(1):171–81. doi: 10.1038/nprot.2014.006 24385147
61. Branca RM, Orre LM, Johansson HJ, Granholm V, Huss M, Perez-Bercoff A, et al. HiRIEF LC-MS enables deep proteome coverage and unbiased proteogenomics. Nat Methods. 2014;11(1):59–62. doi: 10.1038/nmeth.2732 24240322