NF-E2-related factor 2, a key inducer of antioxidant defenses, negatively regulates the CFTR transcription

Cellular and Molecular Life Sciences

Volumn 67, Issue 13, 2010, Pages 2297-2309

  René, Céline ^a,b,c   Lopez, Estelle ^a,b   Claustres, Mireille ^a,b,c   Taulan, Magali ^a,b,c   Romey Chatelain, Marie Catherine ^a,b  

^a INSERM   (France)

^b UNIV MONTPELLIER   (France)

^c HÔPITAL ARNAUD DE VILLENEUVE   (France)

Author keywords

CFTR; Cystic fibrosis; Nrf2; Oxidative stress; Transcription; YY1

Indexed keywords

ANTIOXIDANT; TRANSCRIPTION FACTOR NRF2; TRANSCRIPTION FACTOR YY1; TRANSMEMBRANE CONDUCTANCE REGULATOR; CURCUMIN; YY1 PROTEIN, HUMAN;

ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; GENE REPRESSION; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; TRANSCRIPTION REGULATION; CELL LINE; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY;

ANTIOXIDANTS; BASE SEQUENCE; CELL LINE; CHROMATIN IMMUNOPRECIPITATION; CURCUMIN; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; GENE EXPRESSION REGULATION; HUMANS; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PROMOTER REGIONS, GENETIC; TRANSCRIPTION, GENETIC; YY1 TRANSCRIPTION FACTOR;

EID: 77954068742     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-010-0336-4     Document Type: Article

References (50)

1. Mouchel N, Henstra SA, McCarthy VA, Williams SH, Phylactides M, Harris A (2004) HNF1alpha is involved in tissue-specific regulation of CFTR gene expression. Biochem J 378:909-918
2. Paul T, Li S, Khurana S, Leleiko NS, Walsh MJ (2007) The epigenetic signature of CFTR expression is co-ordinated via chromatin acetylation through a complex intronic element. Biochem J 408:317-326
3. Blackledge NP, Carter EJ, Evans JR, Lawson V, Rowntree RK, Harris A (2007) CTCF mediates insulator function at the CFTR locus. Biochem J 408:267-275
4. Blackledge N, Ott C, Gillen A, Harris A (2009) An insulator element 3' to the CFTR gene binds CTCF and reveals an active chromatin hub in primary cells. Nucleic Acids Res 37:1086-1094
5. René C, Taulan M, Iral F, Doudement J, L'Honoré A, Gerbon C, Demaille J, Claustres M, Romey MC (2005) 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 33:5271-5290
6. Taulan M, Lopez E, Guittard C, René C, Baux D, Altieri JP, DesGeorges M, Claustres M, Romey MC (2007) First functional polymorphism in CFTR promoter that results in decreased transcriptional activity and Sp1/USF binding. Biochem Biophys Res Commun 361:775-781
7. Kreindler JL, Jackson AD, Kemp PA, Bridges RJ, Danahay H (2005) Inhibition of chloride secretion in human bronchial epithelial cells by cigarette smoke extract. Am J Physiol Lung Cell Mol Physiol 288:L894-L902
8. Cantin AM, Hanrahan JW, Bilodeau G, Ellis L, Dupuis A, Liao J, Zielenski J, Durie P (2006) Cystic fibrosis transmembrane conductance regulator function is suppressed in cigarette smokers. Am J Respir Crit Care Med 173:1139-1144
9. Schwarzer C, Fischer H, Kim EJ, Barber KJ, Mills AD, Kurth MJ, Gruenert DC, Suh JH, Machen TE, Illek B (2008) Oxidative stress caused by pyocyanin impairs CFTR Cl (-) transport in human bronchial epithelial cells. Free Radic Biol Med 45:1653-1662
10. Cantin AM, Bilodeau G, Ouellet C, Liao J, Hanrahan JW (2006) Oxidant stress suppresses CFTR expression. Am J Physiol Cell Physiol 290:C262-C270
11. Qu F, Qin XQ, Cui YR, Xiang Y, Tan YR, Liu HJ, Peng LH, Zhou XY, Liu C, Zhu XL (2008) Ozone stress down-regulates the expression of cystic fibrosis transmembrane conductance regulator in human bronchial epithelial cells. Chem Biol Interact 179(2-3):219-226
12. Nguyen T, Yang CS, Pickett CB (2004) The pathways and molecular mechanisms regulating Nrf2 activation in response to chemical stress. Free Radic Biol Med 37:433-441
13. Nguyen T, Huang HC, Pickett CB (2000) Transcriptional regulation of the antioxidant response element. Activation by Nrf2 and repression by MafK. J Biol Chem 275:15466-15473
14. Hayes JD, McMahon M(2001) Molecular basis for the contribution of the antioxidant responsive element to cancer chemoprevention. Cancer Lett 174:103-113
15. Copple IM, Goldring CE, Kitteringham NR, Park BK (2008) The Nrf2-Keap1 defence pathway: role in protection against druginduced toxicity. Toxicology 246:24-33
16. Itoh K, Wakabayashi N, Katoh Y, Ishii T, O'Connor T, Yamamoto M (2003) Keap1 regulates both cytoplasmic-nuclear shuttling and degradation of Nrf2 in response to electrophiles. Genes Cells 8:379-391
17. Cho HY, Reddy SP, Yamamoto M, Kleeberger SR (2004) The transcription factor NRF2 protects against pulmonary fibrosis. FASEB J 18:1258-1260
18. Goven D, Boutten A, Leçon-Malas V, Marchal-Sommé J, Amara N, Crestani B, Fournier M, Lesèche G, Soler P, Boczkowski J, Bonay M (2008) Altered Nrf2/Keap1-Bach1 equilibrium in pulmonary emphysema. Thorax 63:916-924
19. Adachi T, Nakagawa H, Chung I, Hagiya Y, Hoshijima K, Noguchi N, Kuo MT, Ishikawa T (2007) Nrf2-dependent and-independent induction of ABC transporters ABCC1, ABCC2, and ABCG2 in HepG2 cells under oxidative stress. J Exp Ther Oncol 6:335-348
20. Vollrath V, Wielandt AM, Iruretagoyena M, Chianale J (2006) Role of Nrf2 in the regulation of the Mrp2 (ABCC2) gene. Biochem J 395:599-609
21. Wang X, Tomso D, Chorley B, Cho H, Cheung V, Kleeberger S, Bell D (2007) Identification of polymorphic antioxidant response elements in the human genome. Hum Mol Genet 16:1188-1200
22. Romey MC, Pallares-Ruiz N, Mange A, Mettling C, Peytavi R, Demaille J, Claustres M (2000) A naturally occurring sequence variation that creates a YY1 element is associated with increased cystic fibrosis transmembrane conductance regulator gene expression. J Biol Chem 275:3561-3567
23. Pearson M, Carbone R, Sebastiani C, Cioce M, Fagioli M, Saito S, Higashimoto Y, Appella E, Minucci S, Pandolfi PP, Pelicci PG (2000) PML regulates p53 acetylation and premature senescence induced by oncogenic Ras. Nature 406:207-210
24. Balogun E, Hoque M, Gong P, Killeen E, Green CJ, Foresti R, Alam J, Motterlini R (2003) Curcumin activates the heme oxygenase-1 gene via regulation of Nrf2 and the antioxidantresponsive element. Biochem J 371:887-895
25. Dhakshinamoorthy S, Jain AK, Bloom DA, Jaiswal AK (2005) Bach1 competes with Nrf2 leading to negative regulation of the antioxidant response element (ARE)-mediated NAD(P)H:quinone oxidoreductase 1 gene expression and induction in response to antioxidants. J Biol Chem 280:16891-16900
26. Bloom D, Dhakshinamoorthy S, Jaiswal AK (2002) Site-directed mutagenesis of cysteine to serine in the DNA binding region of Nrf2 decreases its capacity to upregulate antioxidant response element-mediated expression and antioxidant induction of NAD(P)H:quinone oxidoreductase1 gene. Oncogene 21:2191-2200
27. Kang KW, Lee SJ, Park JW, Kim SG (2002) Phosphatidylinositol 3-kinase regulates nuclear translocation of NF-E2-related factor 2 through actin rearrangement in response to oxidative stress. Mol Pharmacol 62:1001-1010
28. Dhakshinamoorthy S, Jaiswal AK (2002) c-Maf negatively regulates ARE-mediated detoxifying enzyme genes expression and anti-oxidant induction. Oncogene 21:5301-5312
29. Lee JM, Moehlenkamp JD, Hanson JM, Johnson JA (2001) Nrf2-dependent activation of the antioxidant responsive element by tert-butylhydroquinone is independent of oxidative stress in IMR-32 human neuroblastoma cells. Biochem Biophys Res Commun 280:286-292
30. Shen G, Xu C, Hu R, Jain MR, Gopalkrishnan A, Nair S, Huang MT, Chan JY, Kong AN (2006) Modulation of nuclear factor E2-related factor 2-mediated gene expression in mice liver and small intestine by cancer chemopreventive agent curcumin. Mol Cancer Ther 5:39-51
31. Chou JL, Rozmahel R, Tsui LC (1991) Characterization of the promoter region of the cystic fibrosis transmembrane conductance regulator gene. J Biol Chem 266:24471-24476
32. Erickson AM, Nevarea Z, Gipp JJ, Mulcahy RT (2002) Identification of a variant antioxidant response element in the promoter of the human glutamate-cysteine ligase modifier subunit gene. Revision of the ARE consensus sequence. J Biol Chem 277:30730-30737
33. Alam J, Stewart D, Touchard C, Boinapally S, Choi AM, Cook JL (1999) Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J Biol Chem 274:26071-26078
34. Itoh K, Chiba T, Takahashi S, Ishii T, Igarashi K, Katoh Y, Oyake T, Hayashi N, Satoh K, Hatayama I, Yamamoto M, Nabeshima Y (1997) An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun 236:313-322
35. Nioi P, McMahon M, Itoh K, Yamamoto M, Hayes JD (2003) Identification of a novel Nrf2-regulated antioxidant response element (ARE) in the mouse NAD(P)H: quinone oxidoreductase 1 gene: reassessment of the ARE consensus sequence. Biochem J 374:337-348
36. Breslin MB, Vedeckis WV (1998) The human glucocorticoid receptor promoter upstream sequences contain binding sites for the ubiquitous transcription factor, Yin Yang 1. J Steroid Biochem Mol Biol 67:369-381
37. Jaiswal AK (2004) Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radic Biol Med 36:1199-1207
38. Jain AK, Bloom DA, Jaiswal AK (2005) Nuclear import and export signals in control of Nrf2. J Biol Chem 280:29158-29168
39. Favot L, Hall SM, Haworth SG, Kemp PR (2005) Cytoplasmic YY1 is associated with increased smooth muscle-specific gene expression: implications for neonatal pulmonary hypertension. Am J Pathol 167:1497-1509
40. Kobayashi M, Li L, Iwamoto N, Nakajima-Takagi Y, Kaneko H, Nakayama Y, Eguchi M, Wada Y, Kumagai Y, Yamamoto M (2009) The antioxidant defense system Keap1-Nrf2 comprises a multiple sensing mechanism for responding to a wide range of chemical compounds. Mol Cell Biol 29:493-502
41. Baudouin-Legros M, Brouillard F, Tondelier D, Hinzpeter A, Edelman A (2003) Effect of ouabain on CFTR gene expression in human Calu-3 cells. Am J Physiol Cell Physiol 284:C620-C626
42. Venugopal R, Jaiswal AK (1996) Nrf1 and Nrf2 positively and c-Fos and Fra1 negatively regulate the human antioxidant response element-mediated expression of NAD(P)H:quinone oxidoreductase1 gene. Proc Natl Acad Sci USA 93:14960-14965
43. Wang W, Kwok AM, Chan JY (2007) The p65 isoform of Nrf1 is a dominant negative inhibitor of ARE-mediated transcription. J Biol Chem 282:24670-24678
44. Pittman N, Shue G, LeLeiko NS, Walsh MJ (1995) Transcription of cystic fibrosis transmembrane conductance regulator requires a CCAAT-like element for both basal and cAMP-mediated regulation. J Biol Chem 270:28848-28857
45. Ikeda H, Omoteyama K, Yoshida K, Nishi S, Sakai M (2006) CCAAT enhancer-binding protein alpha suppresses the rat placental glutathione S-transferase gene in normal liver. J Biol Chem 281:6734-6741
46. Walters DM, Cho HY, Kleeberger SR (2008) Oxidative stress and antioxidants in the pathogenesis of pulmonary fibrosis: a potential role for Nrf2. Antioxid Redox Signal 10:321-332
47. Rahman I (2008) Antioxidant therapeutic advances in COPD. Ther Adv Respir Dis 2:351-374
48. Linsdell P, Hanrahan JW (1998) Glutathione permeability of CFTR. Am J Physiol 275:C323-C326
49. - secretion in airway epithelia. J Biol Chem 277:43041-43049
50. 2 and inflammatory cytokine production. PLoS ONE 3:e3367