Transcription factors and miRNAs that regulate fetal to adult CFTR expression change are new targets for cystic fibrosis

European Respiratory Journal

Volumn 45, Issue 1, 2015, Pages 116-128

  Viart, Victoria ^a,b,c   Bergougnoux, Anne ^a,c   Bonini, Jennifer ^a,b   Varilh, Jessica ^a,c   Chiron, Raphaël ^c   Tabary, Olivier ^d,e   Molinari, Nicolas ^c,f   Claustres, Mireille ^a,b,c   Taulan Cadars, Magali ^a,b  

^a INSERM   (France)

^b UNIV MONTPELLIER   (France)

^c MONTPELLIER UNIVERSITY HOSPITAL   (France)

^d CENTRE DE RECHERCHE SAINT ANTOINE   (France)

^e SORBONNE UNIVERSITÉ   (France)

^f UMR 729 MISTEA   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN ALPHA; CCAAT ENHANCER BINDING PROTEIN BETA; HEPATOCYTE NUCLEAR FACTOR 3ALPHA; HEPATOCYTE NUCLEAR FACTOR 3BETA; MICRORNA; MICRORNA 101; MICRORNA 145; MICRORNA 384; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXA; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; CFTR PROTEIN, HUMAN; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; MIRN101 MICRORNA, HUMAN; MIRN145 MICRORNA, HUMAN; OLIGONUCLEOTIDE;

3' UNTRANSLATED REGION; ARTICLE; BINDING AFFINITY; BINDING SITE; CFTR GENE; CONTROLLED STUDY; CYSTIC FIBROSIS; DOWN REGULATION; GENE; GENE CONTROL; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE MUTATION; GENE OVEREXPRESSION; HOMOZYGOSITY; HUMAN; HUMAN CELL; LUNG ALVEOLUS CELL; PROTEIN BINDING; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION; UPREGULATION; ADULT; ANIMAL; BRONCHUS; CELL LINE; CHEMISTRY; CHROMATIN IMMUNOPRECIPITATION; FEMALE; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; MOUSE; MUTAGENESIS; MUTATION; REPORTER GENE; TUMOR CELL LINE;

3' UNTRANSLATED REGIONS; ADULT; ANIMALS; BINDING SITES; BRONCHI; CELL LINE; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, REPORTER; HUMANS; MALE; MICE; MICRORNAS; MUTAGENESIS; MUTATION; OLIGONUCLEOTIDES; TRANSCRIPTION FACTORS;

EID: 84920610349     PISSN: 09031936     EISSN: 13993003     Source Type: Journal    
DOI: 10.1183/09031936.00113214     Document Type: Article

References (53)

1. Higgs DR, Vernimmen D, Hughes J, et al. Using genomics to study how chromatin influences gene expression. Annu Rev Genomics Hum Genet 2007; 8: 299-325.
2. Martinez NJ, Walhout AJ. The interplay between transcription factors and microRNAs in genome-scale regulatory networks. Bioessays 2009; 31: 435-445.
3. Shalgi R, Brosh R, Oren M, et al. Coupling transcriptional and post-transcriptional miRNA regulation in the control of cell fate. Aging (Albany NY) 2009; 1: 762-770.
4. Krol J, Loedige I, Filipowicz W, et al. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 2010; 11: 597-610.
5. Dong J, Jiang G, Asmann YW, et al. MicroRNA networks in mouse lung organogenesis. PLoS One 2010; 5: e10854.
6. Chou JL, Rozmahel R, Tsui LC, et al. Characterization of the promoter region of the cystic fibrosis transmembrane conductance regulator gene. J Biol Chem 1991; 266: 24471-24476.
7. Yoshimura K, Nakamura H, Trapnell BC, et al. 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: 9140-9144.
8. 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: 15912-15921.
9. White NL, Higgins CF, Trezise AE. Tissue-specific in vivo transcription start sites of the human and murine cystic fibrosis genes. Hum Mol Genet 1998; 7: 363-369.
10. Harris A, Chalkley G, Goodman S, et al. Expression of the cystic fibrosis gene in human development. Development 1991; 113: 305-310.
11. McCray PB Jr, Reenstra WW, Louie E, et al. Expression of CFTR and presence of cAMP-mediated fluid secretion in human fetal lung. Am J Physiol 1992; 262: L472-L481.
12. Trezise AE, Chambers JA, Wardle CJ, et al. Expression of the cystic fibrosis gene in human foetal tissues. Hum Mol Genet 1993; 2: 213-218.
13. Tizzano EF, O'Brodovich H, Chitayat D, et al. Regional expression of CFTR in developing human respiratory tissues. Am J Respir Cell Mol Biol 1994; 10: 355-362.
14. Marcorelles P, Montier T, Gillet D, et al. Evolution of CFTR protein distribution in lung tissue from normal and CF human fetuses. Pediatr Pulmonol 2007; 42: 1032-1040.
15. Cohen JC, Larson JE, Killeen E, et al. CFTR and Wnt/beta-catenin signaling in lung development. BMC Dev Biol 2008; 8: 70.
16. Pittman N, Shue G, LeLeiko NS, et al. Transcription of cystic fibrosis transmembrane conductance regulator requires a CCAAT-like element for both basal and cAMP-mediated regulation. J Biol Chem 1995; 270: 28848-28857.
17. Rene C, Taulan M, Iral F, et al. Binding of serum response factor to cystic fibrosis transmembrane conductance regulator CArG-like elements, as a new potential CFTR transcriptional regulation pathway. Nucleic Acids Res 2005; 33: 5271-5290.
18. Taulan M, Lopez E, Guittard C, et al. First functional polymorphism in CFTR promoter that results in decreased transcriptional activity and Sp1/USF binding. Biochem Biophys Res Commun 2007; 361: 775-781.
19. Lopez E, Viart V, Guittard C, et al. Variants in CFTR untranslated regions are associated with congenital bilateral absence of the vas deferens. J Med Genet 2011; 48: 152-159.
20. Zheng W, Kuhlicke J, Jackel K, et al. Hypoxia inducible factor-1 (HIF-1)-mediated repression of cystic fibrosis transmembrane conductance regulator (CFTR) in the intestinal epithelium. FASEB J 2009; 23: 204-213.
21. Burnight ER, Wang G, McCray PB Jr, et al. Transcriptional targeting in the airway using novel gene regulatory elements. Am J Respir Cell Mol Biol 2012; 47: 227-233.
22. Zhang Z, Leir SH, Harris AImmune mediators regulate CFTR expression through a bifunctional airway-selective enhancer. Mol Cell Biol 2013; 33: 2843-2853.
23. Nuthall HN, Vassaux G, Huxley C, et al. Analysis of a DNase I hypersensitive site located -20.9 kb upstream of the CFTR gene. Eur J Biochem 1999; 266: 431-443.
24. Viart VVJ, Lopez E, René C, et al. Phosphorylated C/EBPβ influences a complex network involving YY1 and USF2 in lung epithelial cells. PLoS One 2013:8: e60211.
25. Gheldof N, Smith EM, Tabuchi TM, et al. Cell-type-specific long-range looping interactions identify distant regulatory elements of the CFTR gene. Nucleic Acids Res 2010; 38: 4325-4336.
26. Blackledge NP, Ott CJ, Gillen AE, et al. An insulator element 3′ to the CFTR gene binds CTCF and reveals an active chromatin hub in primary cells. Nucleic Acids Res 2009; 37: 1086-1094.
27. Kerschner JL, Harris A. Transcriptional networks driving enhancer function in the CFTR gene. Biochem J 2012; 446: 203-212.
28. Yigit E, Bischof JM, Zhang Z, et al. Nucleosome mapping across the CFTR locus identifies novel regulatory factors. Nucleic Acids Res 2013; 41: 2857-2868.
29. Kerschner JL, Gosalia N, Leir SH, et al. Chromatin remodeling mediated by the FOXA1/A2 transcription factors activates CFTR expression in intestinal epithelial cells. Epigenetics 2014; 9: 557-565.
30. Gillen AE, Gosalia N, Leir SH, et al. MicroRNA regulation of expression of the cystic fibrosis transmembrane conductance regulator gene. Biochem J 2011; 438: 25-32.
31. Megiorni F, Cialfi S, Dominici C, et al. Synergistic post-transcriptional regulation of the Cystic Fibrosis Transmembrane conductance Regulator (CFTR) by miR-101 and miR-494 specific binding. PLoS One 2011; 6: e26601.
32. Ramachandran S, Karp PH, Jiang P, et al. A microRNA network regulates expression and biosynthesis of wild-type and DeltaF508 mutant cystic fibrosis transmembrane conductance regulator. Proc Natl Acad Sci USA 2012; 109: 13362-13367.
33. Oglesby IK, Chotirmall SH, McElvaney NG, et al. Regulation of cystic fibrosis transmembrane conductance regulator by microRNA-145, -223, and -494 is altered in DeltaF508 cystic fibrosis airway epithelium. J Immunol 2013; 190: 3354-3362.
34. Ramachandran S, Karp PH, Osterhaus SR, et al. Post-transcriptional regulation of CFTR expression and function by microRNAs. Am J Respir Cell Mol Biol 2013; 49: 544-551.
35. Romey MC, Pallares-Ruiz N, Mange A, et al. A naturally occurring sequence variation that creates a YY1 element is associated with increased cystic fibrosis transmembrane conductance regulator gene expression. J Biol Chem 2000; 275: 3561-3567.
36. Saint-Criq V, Ruffin M, Rebeyrol C, et al. Azithromycin fails to reduce inflammation in cystic fibrosis airway epithelial cells. Eur J Pharmacol 2012; 674: 1-6.
37. Gras D, Bourdin A, Vachier I, et al. An ex vivo model of severe asthma using reconstituted human bronchial epithelium. J Allergy Clin Immunol 2012; 129: 1259-1266.
38. Viart V, Des Georges M, Claustres M, et al. Functional analysis of a promoter variant identified in the CFTR gene in cis of a frameshift mutation. Eur J Hum Genet 2012; 20: 180-184.
39. Riordan JR, Rommens JM, Kerem B, et al. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 1989; 245: 1066-1073.
40. Maeda Y, Dave V, Whitsett JA. Transcriptional control of lung morphogenesis. Physiol Rev 2007; 87: 219-244.
41. Baudouin-Legros M, Hinzpeter A, Jaulmes A, et al. Cell-specific posttranscriptional regulation of CFTR gene expression via influence of MAPK cascades on 3′UTR part of transcripts. Am J Physiol Cell Physiol 2005; 289: C1240-C1250.
42. Jing Q, Huang S, Guth S, et al. Involvement of microRNA in AU-rich element-mediated mRNA instability. Cell 2005; 120: 623-634.
43. Sun G, Li H, Rossi JJ. Sequence context outside the target region influences the effectiveness of miR-223 target sites in the RhoB 3′UTR. Nucleic Acids Res 2010; 38: 239-252.
44. Glorian V, Maillot G, Poles S, et al. HuR-dependent loading of miRNA RISC to the mRNA encoding the Ras-related small GTPase RhoB controls its translation during UV-induced apoptosis. Cell Death Differ 2011; 18: 1692-1701.
45. Broackes-Carter FC, Mouchel N, Gill D, et al. Temporal regulation of CFTR expression during ovine lung development: implications for CF gene therapy. Hum Mol Genet 2002; 11: 125-131.
46. Romey MC, Guittard C, Carles S, et al. First putative sequence alterations in the minimal CFTR promoter region. J Med Genet 1999; 36: 263-264.
47. Sinn PL, Anthony RM, McCray PB Jr. Genetic therapies for cystic fibrosis lung disease. Hum Mol Genet 2011; 20: R79-R86.
48. Hutt DM, Herman D, Rodrigues AP, et al. Reduced histone deacetylase 7 activity restores function to misfolded CFTR in cystic fibrosis. Nat Chem Biol 2010; 6: 25-33.
49. Ramsey BW, Davies J, McElvaney NG, et al. A CFTR potentiator in patients with cystic fibrosis and the G551D mutation. N Engl J Med 2011; 365: 1663-1672.
50. Clancy JP, Rowe SM, Accurso FJ, et al. Results of a phase IIa study of VX-809, an investigational CFTR corrector compound, in subjects with cystic fibrosis homozygous for the F508del-CFTR mutation. Thorax 2012; 67: 12-18.
51. Van Goor F, Hadida S, Grootenhuis PD, et al. Correction of the F508del-CFTR protein processing defect in vitro by the investigational drug VX-809. Proc Natl Acad Sci USA 2011; 108: 18843-18848.
52. Varambally S, Cao Q, Mani RS, et al. Genomic loss of microRNA-101 leads to overexpression of histone methyltransferase EZH2 in cancer. Science 2008; 322: 1695-1699.
53. Guan P, Yin Z, Li X, et al. Meta-analysis of human lung cancer microRNA expression profiling studies comparing cancer tissues with normal tissues. J Exp Clin Cancer Res 2012; 31: 54