Nucleosome mapping across the CFTR locus identifies novel regulatory factors

Nucleic Acids Research

Volumn 41, Issue 5, 2013, Pages 2857-2868

  Yigit, Erbay ^c   Bischof, Jared M ^a,b   Zhang, Zhaolin ^a,b   Ott, Christopher J ^a,b,d   Kerschner, Jenny L ^a,b   Leir, Shih Hsing ^a,b   Buitrago Delgado, Elsy ^c   Zhang, Quanwei ^c   Wang, Ji Ping Z ^c   Widom, Jonathan ^c   Harris, Ann ^a,b  

^a CHILDREN S MEMORIAL RESEARCH CENTER   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BARRIER TO AUTOINTEGRATION FACTOR; CIS ACTING ELEMENT; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; GLUCOCORTICOID RECEPTOR; HEPATOCYTE NUCLEAR FACTOR 1; HEPATOCYTE NUCLEAR FACTOR 3ALPHA; TRANS ACTING FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CTCF;

ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; BINDING SITE; CELL TYPE; GENE LOCUS; GENE MAPPING; HUMAN; HUMAN CELL; HYBRIDIZATION; IN VIVO STUDY; NUCLEOSOME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REGULATORY MECHANISM; TISSUE SPECIFICITY;

BINDING SITES; CACO-2 CELLS; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME MAPPING; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DEXAMETHASONE; GENE SILENCING; GENETIC LOCI; GLUCOCORTICOIDS; HEPATOCYTE NUCLEAR FACTOR 3-ALPHA; HUMANS; NUCLEOSOMES; PROTEIN BINDING; RECEPTORS, GLUCOCORTICOID; REPRESSOR PROTEINS; RESPONSE ELEMENTS; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION FACTORS;

BACTERIA (MICROORGANISMS);

EID: 84876392496     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks1462     Document Type: Article

References (41)

1. Boyle, A.P., Davis, S., Shulha, H.P., Meltzer, P., Margulies, E.H., Weng, Z., Furey, T.S. and Crawford, G.E. (2008) High-resolution mapping and characterization of open chromatin across the genome. Cell, 132, 311-322.
2. Giresi, P.G., Kim, J., McDaniell, R.M., Iyer, V.R. and Lieb, J.D. (2007) FAIRE (Formaldehyde-Assisted Isolation of Regulatory Elements) isolates active regulatory elements from human chromatin. Genome Res., 17, 877-885.
3. Boyle, A.P., Song, L., Lee, B.K., London, D., Keefe, D., Birney, E., Iyer, V.R., Crawford, G.E. and Furey, T.S. (2011) High-resolution genome-wide in vivo footprinting of diverse transcription factors in human cells. Genome Res., 21, 456-464.
4. He, H.H., Meyer, C.A., Chen, M.W., Jordan, V.C., Brown, M. and Liu, X.S. (2012) Differential DNase I hypersensitivity reveals factor-dependent chromatin dynamics. Genome Res., 22, 1015-1025.
5. Reddy, T.E., Gertz, J., Pauli, F., Kucera, K.S., Varley, K.E., Newberry, K.M., Marinov, G.K., Mortazavi, A., Williams, B.A., Song, L. et al. (2012) Effects of sequence variation on differential allelic transcription factor occupancy and gene expression. Genome Res., 22, 860-869.
6. Segal, E. and Widom, J. (2009) From DNA sequence to transcriptional behaviour: a quantitative approach. Nat. Rev. Genet., 10, 443-456.
7. Valouev, A., Johnson, S.M., Boyd, S.D., Smith, C.L., Fire, A.Z. and Sidow, A. (2011) Determinants of nucleosome organization in primary human cells. Nature, 474, 516-520.
8. Moyle-Heyrman, G., Tims, H.S. and Widom, J. (2011) Structural constraints in collaborative competition of transcription factors against the nucleosome. J. Mol. Biol., 412, 634-646.
9. Tims, H.S., Gurunathan, K., Levitus, M. and Widom, J. (2011) Dynamics of nucleosome invasion by DNA binding proteins. J. Mol. Biol., 411, 430-448.
10. Andreu-Vieyra, C., Lai, J., Berman, B.P., Frenkel, B., Jia, L., Jones, P.A. and Coetzee, G.A. (2011) Dynamic nucleosome-depleted regions at androgen receptor enhancers in the absence of ligand in prostate cancer cells. Mol. Cell Biol., 31, 4648-4662.
11. Rommens, J.M., Iannuzzi, M.C., Kerem, B., Drumm, M.L., Melmer, G., Dean, M., Rozmahel, R., Cole, J.L., Kennedy, D., Hidaka, N. et al. (1989) Identification of the cystic fibrosis gene: chromosome walking and jumping. Science, 245, 1059-1065.
12. Gillen, A.E. and Harris, A. (2012) Transcriptional regulation of CFTR gene expression. Front. Biosci. (Elite Ed.), 4, 587-592.
13. Kotzamanis, G., Abdulrazzak, H., Gifford-Garner, J., Haussecker, P., Cheung, W., Harris, A., Kotsinas, A., Gorgoulis, V. and Huxley, C. (2009) CFTR expression from a BAC carrying the complete human gene and associated regulatory elements. J. Cell Mol. Med., 13, 2938-2948.
14. Ott, C.J., Blackledge, N.P., Leir, S.H. and Harris, A. (2009) Novel regulatory mechanisms for the CFTR gene. Biochem. Soc. Trans., 37, 843-848.
15. Ott, C.J., Blackledge, N.P., Kerschner, J.L., Leir, S.H., Crawford, G.E., Cotton, C.U. and Harris, A. (2009) Intronic enhancers coordinate epithelial-specific looping of the active CFTR locus. Proc. Natl Acad. Sci. USA, 106, 19934-19939.
16. Zhang, Z., Ott, C.J., Lewandowska, M.A., Leir, S.H. and Harris, A. (2012) Molecular mechanisms controlling CFTR gene expression in the airway. J. Cell Mol. Med., 16, 1321-1330.
17. Ott, C.J., Bischof, J.M., Unti, K.M., Gillen, A.E., Leir, S.H. and Harris, A. (2012) Nucleosome occupancy reveals regulatory elements of the CFTR promoter. Nucleic Acids Res., 40, 625-637.
18. Fogh, J., Wright, W.C. and Loveless, J.D. (1977) Absence of HeLa cell contamination in 169 cell lines derived from human tumors. J. Natl Cancer. Inst., 58, 209-214.
19. Cozens, A.L., Yezzi, M.J., Kunzelmann, K., Ohrui, T., Chin, L., Eng, K., Finkbeiner, W.E., Widdicombe, J.H. and Gruenert, D.C. (1994) CFTR expression and chloride secretion in polarized immortal human bronchial epithelial cells. Am. J. Respir. Cell Mol. Biol., 10, 38-47.
20. Harris, A. and Coleman, L. (1989) Ductal epithelial cells cultured from human foetal epididymis and vas deferens: relevance to sterility in cystic fibrosis. J. Cell Sci., 92, Pt 4, 687-690.
21. Mouchel, N., Henstra, S.A., McCarthy, V.A., Williams, S.H., Phylactides, M. and Harris, A. (2004) HNF1alpha is involved in regulation of expression of the CFTR gene. Biochem. J., 378, 909-918.
22. Bashiardes, S., Veile, R., Helms, C., Mardis, E.R., Bowcock, A.M. and Lovett, M. (2005) Direct genomic selection. Nat. Methods, 2, 63-69.
23. Robinson, M.D., McCarthy, D.J. and Smyth, G.K. (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26, 139-140.
24. Frith, M.C., Fu, Y., Yu, L., Chen, J.F., Hansen, U. and Weng, Z. (2004) Detection of functional DNA motifs via statistical over-representation. Nucleic Acids Res., 32, 1372-1381.
25. Smith, A.N., Barth, M.L., McDowell, T.L., Moulin, D.S., Nuthall, H.N., Hollingsworth, M.A. and Harris, A. (1996) A regulatory element in intron 1 of the cystic fibrosis transmembrane conductance regulator gene. J. Biol. Chem., 271, 9947-9954.
26. Ott, C.J., Suszko, M., Blackledge, N.P., Wright, J.E., Crawford, G.E. and Harris, A. (2009) A complex intronic enhancer regulates expression of the CFTR gene by direct interaction with the promoter. J. Cell Mol. Med., 13, 680-692.
27. Gheldof, N., Smith, E.M., Tabuchi, T.M., Koch, C.M., Dunham, I., Stamatoyannopoulos, J.A. and Dekker, J. (2010) Cell-type-specific long-range looping interactions identify distant regulatory elements of the CFTR gene. Nucleic Acids Res., 38, 4325-4336.
28. Kerschner, J.L. and Harris, A. (2012) Transcriptional networks driving enhancer function in the CFTR gene. Biochem. J., 446, 203-212.
29. Parelho, V., Hadjur, S., Spivakov, M., Leleu, M., Sauer, S., Gregson, H.C., Jarmuz, A., Canzonetta, C., Webster, Z., Nesterova, T. et al. (2008) Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell, 132, 422-433.
30. Wendt, K.S., Yoshida, K., Itoh, T., Bando, M., Koch, B., Schirghuber, E., Tsutsumi, S., Nagae, G., Ishihara, K., Mishiro, T. et al. (2008) Cohesin mediates transcriptional insulation by CCCT C-binding factor. Nature, 451, 796-801.
31. Nuthall, H., Vassaux, G., Huxley, C. and Harris, A. (1999) Analysis of a DNAse I hypersensitve site located 20.9 kb upstream of the CFTR gene. Eur. J. Biochem., 266, 431-443.
32. Blackledge, N.P., Carter, E.J., Evans, J.R., Lawson, V., Rowntree, R.K. and Harris, A. (2007) CTCF mediates insulator function at the CFTR locus. Biochem. J., 408, 267-275.
33. Blackledge, N.P., Ott, C.J., Gillen, A.E. and Harris, A. (2009) An insulator element 30 to the CFTR gene binds CTCF and reveals an active chromatin hub in primary cells. Nucleic Acids Res., 37, 1086-1094.
34. Nuthall, H.N., Moulin, D.S., Huxley, C. and Harris, A. (1999) Analysis of DNase I hypersensitive sites at the 30 end of the cystic fibrosis transmembrane conductance regulator gene. Biochem. J., 341, 601-611.
35. Sekiya, T., Muthurajan, U.M., Luger, K., Tulin, A.V. and Zaret, K.S. (2009) Nucleosome-binding affinity as a primary determinant of the nuclear mobility of the pioneer transcription factor FoxA. Genes Dev., 23, 804-809.
36. Chung, H.R., Dunkel, I., Heise, F., Linke, C., Krobitsch, S., Ehrenhofer-Murray, A.E., Sperling, S.R. and Vingron, M. (2010) The effect of micrococcal nuclease digestion on nucleosome positioning data. PLoS One, 5, e15754.
37. Brogaard, K., Xi, L., Wang, J.P. and Widom, J. (2012) A map of nucleosome positions in yeast at base-pair resolution. Nature, 486, 496-501.
38. Rochwerger, L., Dho, S., Parker, L., Foskett, J.K. and Buchwald, M. (1994) Estrogen-dependent expression of the cystic fibrosis transmembrane regulator gene in a novel uterine epithelial cell line. J. Cell Sci., 107, Pt 9, 2439-2448.
39. Laube, M. and Thome, U.H. (2011) CFTR is negatively regulated by glucocorticoids in alveolar epithelial cells. Pediatr. Res., 70, 522-522.
40. Santos, G.M., Fairall, L. and Schwabe, J.W. (2011) Negative regulation by nuclear receptors: a plethora of mechanisms. Trends Endocrinol. Metab., 22, 87-93.
41. Giard, D.J., Aaronson, S.A., Todaro, G.J., Arnstein, P., Kersey, J.H., Dosik, H. and Parks, W.P. (1973) In vitro cultivation of human tumors: establishment of cell lines derived from a series of solid tumors. J. Natl Cancer Inst., 51, 1417-1423.