A complex intronic enhancer regulates expression of the CFTR gene by direct interaction with the promoter

Journal of Cellular and Molecular Medicine

Volumn 13, Issue 4, 2009, Pages 680-692

  Ott, Christopher J ^a   Suszko, Magdalena ^a   Blackledge, Neil P ^a   Wright, Jane E ^a   Crawford, Gregory E ^b   Harris, Ann ^a,c  

^a NORTHWESTERN UNIVERSITY   (United States)

^b DUKE UNIVERSITY   (United States)

^c Box 211 ^*  (United States)

Author keywords

CFTR; Enhancer promoter interaction; HNF1; Intronic enhancer

Indexed keywords

DEOXYRIBONUCLEASE I; HEPATOCYTE NUCLEAR FACTOR 1; TRANSCRIPTION FACTOR; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ANTIBODY SPECIFICITY; ARTICLE; BASE PAIRING; BINDING SITE; CELL LINE; DNA FOOTPRINTING; ENHANCER REGION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; GENETICS; HUMAN; INTRON; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN BINDING; REPORTER GENE;

BASE PAIRING; BASE SEQUENCE; BINDING SITES; CELL LINE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DEOXYRIBONUCLEASE I; DNA FOOTPRINTING; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION; GENES, REPORTER; HEPATOCYTE NUCLEAR FACTOR 1; HUMANS; INTRONS; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION;

EID: 65249131931     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2008.00621.x     Document Type: Article

References (50)

1. The ENCODE Project Consortium. The ENCODE (ENCyclopedia Of DNA Elements) Project. Science. 2004 306 : 636 40.
2. Blackledge NP, Carter EJ, Evans JR, Lawson V, Rowntree RK, Harris A. CTCF mediates insulator function at the CFTR locus. Biochem J. 2007 408 : 267 75.
3. Nuthall HN, Moulin DS, Huxley C, Harris A. Analysis of DNase-I-hypersensitive sites at the 3′ end of the cystic fibrosis trans-membrane conductance regulator gene (CFTR). Biochem J. 1999 341 : 601 11.
4. Phylactides M, Rowntree R, Nuthall H, Ussery D, Wheeler A, Harris A. Evaluation of potential regulatory elements identified as DNase I hypersensitive sites in the CFTR gene. Eur J Biochem. 2002 269 : 553 9.
5. Smith AN, Wardle CJ, Harris A. Characterization of DNASE I hypersensitive sites in the 120 kb 5′ to the CFTR gene. Biochem Biophys Res Commun. 1995 211 : 274 81.
6. Smith DJ, Nuthall HN, Majetti ME, Harris A. Multiple potential intragenic regulatory elements in the CFTR gene. Genomics. 2000 64 : 90 6.
7. Crawford GE, Davis S, Scacheri PC, Renaud G, Halawi MJ, Erdos MR, Green R, Meltzer PS, Wolfsberg TG, Collins FS. DNase-chip: a high-resolution method to identify DNase I hypersensitive sites using tiled microarrays. Nat Methods. 2006 : 3 : 503 9.
8. Rowntree RK, Vassaux G, McDowell TL, Howe S, McGuigan A, Phylactides M, Huxley C, Harris A. An element in intron 1 of the CFTR gene augments intestinal expression in vivo. Hum Mol Genet. 2001 10 : 1455 64.
9. Smith AN, Barth ML, McDowell TL, Moulin DS, Nuthall HN, Hollingsworth MA, Harris A. A regulatory element in intron 1 of the cystic fibrosis transmem-brane conductance regulator gene. J Biol Chem. 1996 271 : 9947 54.
10. Mogayzel PJ, Ashlock MA. CFTR intron 1 increases luciferase expression driven by CFTR 5′-flanking DNA in a yeast artificial chromosome. Genomics. 2000 64 : 211 5.
11. Mouchel N, Henstra SA, McCarthy VA, Williams SH, Phylactides M, Harris A. HNF1alpha is involved in tissue-specific regulation of CFTR gene expression. Biochem J. 2003 378 : 909 18.
12. Fogh J, Wright WC, Loveless JD. Absence of HeLa cell contamination in 169 cell lines derived from human tumors. J Natl Cancer Inst. 1977 58 : 209 14.
13. Huet C, Sahuquillo-Merino C, Coudrier E, Louvard D. Absorbtive and mucus-secreting subclones isolated from a multipotent intestinal cell line (HT-29) provide new models for cell polarity and terminal differentiation. J Cell Biol. 1987 105 : 345 57.
14. Cozens AL, Yezzi MJ, Kunzelmann K, Ohrui T, Chin L, Eng K, Finkbeiner WE, Widdicombe JH, Gruenert DC. CFTR expression and chloride secretion in polarized immortal human bronchial epithelial cells. Am J Respir Cell Mol Biol. 1994 10 : 38 47.
15. Simmons NL. A cultured human renal epithelioid cell line responsive to vasoac-tive intestinal peptide. Exp Physiol. 1990 75 : 309 19.
16. Scacheri PC, Crawford GE, Davis S. Statistics for ChIP-chip and DNase hyper-sensitivity experiments on NimbleGen arrays. Meth Enzymol. 2006 411 : 270 82.
17. Harris A, Chalkley G, Goodman S, Coleman L. Expression of the cystic fibro-sis gene in human development. Development. 1991 113 : 305 10.
18. Dekker J, Rippe K, Dekker M, Kleckner N. Capturing chromosome conformation. Science. 2002 295 : 1306 11.
19. Hagège H, Klous P, Braem C, Splinter E, Dekker J, Cathala G, de Laat W, Forné T. Quantitative analysis of chromosome conformation capture assays (3C-qPCR). Nat Prot. 2007 2 : 1722 33.
20. de Laat W, Grosveld F. Spatial organization of gene expression: the active chro-matin hub. Chromosome Res. 2003 11 : 447 59.
21. Drissen R, Palstra RJ, Gillemans N, Splinter E, Grosveld F, Philipsen S, de Laat W. The active spatial organization of the beta-globin locus requires the transcription factor EKLF. Genes Dev. 2004 18 : 2485 90.
22. Palstra RJ, Tolhuis B, Splinter E, Nijmeijer R, Grosveld F, de Laat W. The beta-globin nuclear compartment in development and erythroid differentiation. Nat Genet. 2003 35 : 190 4.
23. Ryffel GU. Mutations in the human genes encoding the transcription factors of the hepatocyte nuclear factor (HNF)1 and HNF4 families: functional and pathological consequences. J Mol Endocrinol. 2001 27 : 11 29.
24. Courtois G, Morgan JG, Campbell LA, Fourel G, Crabtree GR. Interaction of a liver-specific nuclear factor with the fib-rinogen and alpha 1-antitrypsin promoters. Science. 1987 238 : 688 92.
25. Hu C, Perlmutter DH. Regulation of alpha1-antitrypsin gene expression in human intestinal epithelial cell line Caco-2 by HNF-1alpha and HNF-4. Am J Physiol. 1999 276 : 1181 94.
26. Cai S, Lee CC, Kohwi-Shigematsu T. SATB1 packages densely looped, tran-scriptionally active chromatin for coordinated expression of cytokine genes. Nat Genet. 2006 38 : 1278 88.
27. Jing H, Vakoc CR, Ying L, Mandat S, Wang H, Zheng X, Blobel GA. Exchange of GATA factors mediates transitions in looped chromatin organization at a devel-opmentally regulated gene locus. Mol Cell. 2008 29 : 232 42.
28. Song SH, Hou C, Dean A. A positive role for NLI/Ldb1 in long-range beta-globin locus control region function. Mol Cell. 2007 28 : 810 22.
29. Spilianakis CG, Lalioti MD, Town T, Lee GR, Flavell RA. Interchromosomal associations between alternatively expressed loci. Nature. 2005 435 : 637 45.
30. Splinter E, Heath H, Kooren J, Palstra RJ, Klous P, Grosveld F, Galjart N, de Laat W. CTCF mediates long-range chro-matin looping and local histone modification in the beta-globin locus. Genes Dev. 2006 20 : 2349 54.
31. Vernimmen D, Gobbi MD, Sloane-Stanley JA, Wood WG, Higgs DR. Long-range chromosomal interactions regulate the timing of the transition between poised and active gene expression. EMBO J. 2007 26 : 2041 51.
32. Crawford I, Maloney PC, Zeitlin PL, Guggino WB, Hyde SC, Turley H, Gatter KC, Harris A, Higgins CF. Immunocytochemical localization of the cystic fibrosis gene product CFTR. Proc Natl Acad Sci USA. 1991 88 : 9262 6.
33. Engelhardt JF, Zepeda M, Cohn JA, Yankaskas JR, Wilson JM. Expression of the cystic fibrosis gene in adult human lung. J Clin Invest. 1994 93 : 737 49.
34. Hyde K, Reid CJ, Tebbutt SJ, Weide L, Hollingsworth MA, Harris A. The cystic fibrosis transmembrane conductance regulator as a marker of human pancreatic duct development. Gastroenterology. 1997 113 : 914 9.
35. Strong TV, Boehm K, Collins FS. Localization of cystic fibrosis transmem-brane conductance regulator mRNA in the human gastrointestinal tract by in situ hybridization. J Clin Invest. 1994 93 : 347 54.
36. Chou JL, Rozmahel R, Tsui LC. Characterization of the promoter region of the cystic fibrosis transmembrane conductance regulator gene. J Biol Chem. 1991 266 : 24471 6.
37. Koh J, Sferra TJ, Collins FS. Characterization of the cystic fibrosis transmembrane conductance regulator promoter region: chromatin context and tissue-specificity. J Biol Chem. 1993 268 : 15912 21.
38. Yoshimura K, Nakamura H, Trapnell BC, Dalemans W, Pavirani A, Lecocq JP, Crystal RG. The cystic fibrosis gene has a "housekeeping"-type promoter and is expressed at low levels in cells of epithelial origin. J Biol Chem. 1991 266 : 9140 4.
39. Matthews RP, McKnight GS. Characterization of the cAMP response element of the cystic fibrosis transmem-brane conductance regulator gene promoter. J Biol Chem. 1996 271 : 31869 77.
40. McDonald RA, Matthews RP, Idzerda RL, McKnight GS. Basal expression of the cystic fibrosis transmembrane conductance regulator gene is dependent on protein kinase A activity. Proc Natl Acad Sci USA. 1995 92 : 7560 4.
41. Pittman N, Shue G, LeLeiko NS, Walsh MJ. Transcription of cystic fibrosis trans-membrane conductance regulator requires a CCAAT-like element for both basal and cAMP-mediated regulation. J Biol Chem. 1995 270 : 28848 57.
42. Cafferata EG, Guerrico AM, Pivetta OH, Santa-Coloma TA. NF-kappaB activation is involved in regulation of cystic fibrosis transmembrane conductance regulator (CFTR) by interleukin-1beta. J Biol Chem. 2001 276 : 15441 4.
43. René C, Taulan M, Iral F, Doudement J, L'Honoré A, Gerbon C, Demaille J, Claustres M, Romey MC. Binding of serum response factor to cystic fibrosis transmembrane conductance regulator CArG-like elements, as a new potential CFTR transcriptional regulation pathway. Nucl Acids Res. 2005 33 : 5271 90.
44. Gregori C, Porteu A, Lopez S, Kahn A, Pichard AL. Characterization of the aldolase B intronic enhancer. J Biol Chem. 1998 273 : 25237 43.
45. Shah RN, Ibbitt JC, Alitalo K, Hurst HC. FGFR4 overexpression in pancreatic cancer is mediated by an intronic enhancer activated by HNF1alpha. Oncogene. 2002 21 : 8251 61.
46. Su JS, Tsai TF, Chang HM, Chao KM, Su TS, Tsai SF. Distant HNF1 site as a master control for the human class I alcohol dehy-drogenase gene expression. J Biol Chem. 2006 281 : 19809 21.
47. Rey-Campos J, Chouard T, Yaniv M, Cereghini S. vHNF1 is a homeoprotein that activates transcription and forms het-erodimers with HNF1. EMBO J. 1991 10 : 1445 57.
48. Pontoglio M, Faust DM, Doyen A, Yaniv M, Weiss MC. Hepatocyte nuclear factor 1alpha gene inactivation impairs chro-matin remodeling and demethylation of the phenylalanine hydroxylase gene. Mol Cell Biol. 1997 17 : 4948 56.
49. Soutoglou E, Viollet B, Vaxillaire M, Yaniv M, Pontoglio M, Talianidis I. Transcription factor-dependent regulation of CBP and P/CAF histone acetyltransferase activity. EMBO J. 2001 20 : 1984 92.
50. Paul T, Li S, Khurana S, Leleiko NS, Walsh MJ. The epigenetic signature of CFTR expression is coordinated via chro-matin acetylation through a complex intronic element. Biochem J. 2007 408 : 317 26.