Oxidative stress modulates the expression of genes involved in cell survival in ΔF508 cystic fibrosis airway epithelial cells

Physiological Genomics

Volumn 46, Issue 17, 2014, Pages 634-646

  Voisin, Grégory ^a   Bouvet, Guillaume F ^b   Legendre, Pierre ^c   Dagenais, André ^b   Massé, Chantal ^b   Berthiaume, Yves ^b,c  

^a CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^b CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Apoptosis; Cystic fibrosis; Microarray; Oxidative stress; Twoway permutational multivariate analysis of variance; F508

Indexed keywords

2,3-DIMETHOXY-1,4-NAPHTHOQUINONE; CASPASE 3; CASPASE 7; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR DELTA F508; MESSENGER RNA; NAPHTHOQUINONE;

APOPTOSIS; CELL CULTURE; CELL LINE; CELL SURVIVAL; CYSTIC FIBROSIS; DOWN REGULATION; DRUG EFFECTS; EPITHELIUM CELL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE ONTOLOGY; GENETICS; HUMAN; INFLAMMATION; LUNG; METABOLISM; OXIDATIVE STRESS; PATHOLOGY; REPRODUCIBILITY; UPREGULATION;

APOPTOSIS; CASPASE 3; CASPASE 7; CELL LINE; CELL SURVIVAL; CELLS, CULTURED; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DOWN-REGULATION; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE ONTOLOGY; HUMANS; INFLAMMATION; LUNG; NAPHTHOQUINONES; OXIDATIVE STRESS; REPRODUCIBILITY OF RESULTS; RNA, MESSENGER; UP-REGULATION;

EID: 84906919893     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00003.2014     Document Type: Article

References (57)

1. Aldallal N, McNaughton EE, Manzel LJ, Richards AM, Zabner J, Ferkol TW, Look DC. Inflammatory response in airway epithelial cells isolated from patients with cystic fibrosis. Am J Respir Crit Care Med 166: 1248-1256, 2002.
2. Arsalane K, Dubois CM, Muanza T, Begin R, Boudreau F, Asselin C, Cantin AM. Transforming growth factor-beta1 is a potent inhibitor of glutathione synthesis in the lung epithelial cell line A549: transcriptional effect on the GSH rate-limiting enzyme gamma-glutamylcysteine synthetase. Am J Respir Cell Mol Biol 17: 599-607, 1997.
3. Barrett T, Troup DB, Wilhite SE, Ledoux P, Rudnev D, Evangelista C, Kim IF, Soboleva A, Tomashevsky M, Marshall KA, Phillippy KH, Sherman PM, Muertter RN, Edgar R. NCBI GEO: archive for highthroughput functional genomic data. Nucleic Acids Res 37: D885-D890, 2009.
4. Becker MN, Sauer MS, Muhlebach MS, Hirsh AJ, Wu Q, Verghese MW, Randell SH. Cytokine secretion by cystic fibrosis airway epithelial cells. Am J Respir Crit Care Med 169: 645-653, 2004.
5. Bensalem N, Ventura AP, Vallee B, Lipecka J, Tondelier D, Davezac N, Santos AD, Perretti M, Fajac A, Sermet-Gaudelus I, Renouil M, Lesure JF, Halgand F, Laprevote O, Edelman A. Down-regulation of the anti-inflammatory protein annexin A1 in cystic fibrosis knock-out mice and patients. Mol Cell Proteomics 4: 1591-1601, 2005.
6. Bezzerri V, Borgatti M, Nicolis E, Lampronti I, Dechecchi MC, Mancini I, Rizzotti P, Gambari R, Cabrini G. Transcription factor oligodeoxynucleotides to NF-kappaB inhibit transcription of IL-8 in bronchial cells. Am J Respir Cell Mol Biol 39: 86-96, 2008.
7. Bianchi ME. DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol 81: 1-5, 2007.
8. Bouvet GF, Voisin G, Berthiaume Y. Exploring epigenetic modulation in cystic fibrosis: relationship between DNA methylation and inflammatory gene expression in epithelial cells. Pediatr Pulmonol 278: A159, 2012.
9. Cantin AM, White TB, Cross CE, Forman HJ, Sokol RJ, Borowitz D. Antioxidants in cystic fibrosis. Conclusions from the CF antioxidant workshop, Bethesda, Maryland, November 11-12, 2003. Free Radic Biol Med 42: 15-31, 2007.
10. Coakley RD, Grubb BR, Paradiso AM, Gatzy JT, Johnson LG, Kreda SM, O'Neal WK, Boucher RC. Abnormal surface liquid pH regulation by cultured cystic fibrosis bronchial epithelium. Proc Natl Acad Sci USA 100: 16083-16088, 2003.
11. de la Rosa G, Yang D, Tewary P, Varadhachary A, Oppenheim JJ. Lactoferrin acts as an alarmin to promote the recruitment and activation of APCs and antigen-specific immune responses. J Immunol 180: 6868-6876, 2008.
12. Dechecchi MC, Nicolis E, Norez C, Bezzerri V, Borgatti M, Mancini I, Rizzotti P, Ribeiro CM, Gambari R, Becq F, Cabrini G. Antiinflammatory effect of miglustat in bronchial epithelial cells. J Cyst Fibros 7: 555-565, 2008.
13. Dimagno MJ, Lee SH, Hao Y, Zhou SY, McKenna BJ, Owyang C. A proinflammatory, antiapoptotic phenotype underlies the susceptibility to acute pancreatitis in cystic fibrosis transmembrane regulator (-/-) mice. Gastroenterology 129: 665-681, 2005.
14. Donaldson SH, Boucher RC. Update on pathogenesis of cystic fibrosis lung disease. Curr Opin Pulm Med 9: 486-491, 2003.
15. Falcon S, Gentleman R. Using GOstats to test gene lists for GO term association. Bioinformatics 23: 257-258, 2007.
16. Futschik ME, Carlisle B. Noise-robust soft clustering of gene expression time-course data. J Bioinform Comput Biol 3: 965-988, 2005.
17. Gambardella S, Biancolella M, D'Apice MR, Amati F, Sangiuolo F, Farcomeni A, Chillemi G, Bueno S, Desideri A, Novelli G. Gene expression profile study in CFTR mutated bronchial cell lines. Clin Exp Med 6: 157-165, 2006.
18. Gruenert DC, Willems M, Cassiman JJ, Frizzell RA. Established cell lines used in cystic fibrosis research. J Cyst Fibros 3: 191-196, 2004.
19. Guilbault C, Novak JP, Martin P, Boghdady ML, Saeed Z, Guiot MC, Hudson TJ, Radzioch D. Distinct pattern of lung gene expression in the Cftr-KO mice developing spontaneous lung disease compared with their littermate controls. Physiol Genomics 25: 179-193, 2006.
20. Hampton TH, Ballok AE, Bomberger JM, Rutkowski MR, Barnaby R, Coutermarsh B, Conejo-Garcia JR, O'Toole GA, Stanton BA. Does the F508-CFTR mutation induce a proinflammatory response in human airway epithelial cells? Am J Physiol Lung Cell Mol Physiol 303: L509-L518, 2012.
21. Hampton TH, Stanton BA. A novel approach to analyze gene expression data demonstrates that the DeltaF508 mutation in CFTR downregulates the antigen presentation pathway. Am J Physiol Lung Cell Mol Physiol 298: L473-L482, 2010.
22. Haraldsen G, Balogh J, Pollheimer J, Sponheim J, Küchler AM. Interleukin-33 - cytokine of dual function or novel alarmin? Trends Immunol 30: 227-233, 2009.
23. Haston CK, Cory S, Lafontaine L, Dorion G, Hallett MT. Straindependent pulmonary gene expression profiles of a cystic fibrosis mouse model. Physiol Genomics 25: 336-345, 2006.
24. He CH, Waxman AB, Lee CG, Link H, Rabach ME, Ma B, Chen Q, Zhu Z, Zhong M, Nakayama K, Nakayama KI, Homer R, Elias JA. Bcl-2-related protein A1 is an endogenous and cytokine-stimulated mediator of cytoprotection in hyperoxic acute lung injury. J Clin Invest 115: 1039-1048, 2005.
25. Irizarry RA. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31: 15e, 2003.
26. Jacquot J, Tabary O, Le RP, Clement A. Airway epithelial cell inflammatory signalling in cystic fibrosis. Int J Biochem Cell Biol 40: 1703-1715, 2008.
27. Jungas T, Motta I, Duffieux F, Fanen P, Stoven V, Ojcius DM. Glutathione levels and BAX activation during apoptosis due to oxidative stress in cells expressing wild-type and mutant cystic fibrosis transmembrane conductance regulator. J Biol Chem 277: 27912-27918, 2002.
28. Lagrange-Puget M, Durieu I, Ecochard R, Abbas-Chorfa F, Drai J, Steghens JP, Pacheco Y, Vital-Durand D, Bellon G. Longitudinal study of oxidative status in 312 cystic fibrosis patients in stable state and during bronchial exacerbation. Pediatr Pulmonol 38: 43-49, 2004.
29. Lee CG, Da Silva CA, Dela Cruz CS, Ahangari F, Ma B, Kang MJ, He CH, Takyar S, Elias JA. Role of chitin and chitinase/chitinase-like proteins in inflammation, tissue remodeling, and injury. Annu Rev Physiol 73: 479-501, 2011.
30. Legendre P, Anderson MJ. Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr 69: 1-24, 1999.
31. Legendre P, Legendre L. Numerical Ecology. Elsevier, 2012, p. 1006.
32. Luciani A, Villella VR, Esposito S, Brunetti-Pierri N, Medina D, Settembre C, Gavina M, Pulze L, Giardino I, Pettoello-Mantovani M, D'Apolito M, Guido S, Masliah E, Spencer B, Quaratino S, Raia V, Ballabio A, Maiuri L. Defective CFTR induces aggresome formation and lung inflammation in cystic fibrosis through ROS-mediated autophagy inhibition. Nat Cell Biol 12: 863-875, 2010.
33. Machen TE. Innate immune response in CF airway epithelia: hyperinflammatory? Am J Physiol Cell Physiol 291: C218-C230, 2006.
34. Martin C, Coolen N, Wu Y, Thevenot G, Touqui L, Prulière-Escabasse V, Papon JF, Coste A, Escudier E, Dusser DJ, Fajac I, Burgel PR. CFTR dysfunction induces vascular endothelial growth factor synthesis in airway epithelium. Eur Respir J 42: 1553-1562, 2013.
35. McColley SA, Stellmach V, Boas SR, Jain M, Crawford SE. Serum vascular endothelial growth factor is elevated in cystic fibrosis and decreases with treatment of acute pulmonary exacerbation. Am J Respir Crit Care Med 161: 1877-1880, 2000.
36. Norkina O, Kaur S, Ziemer D, De Lisle RC. Inflammation of the cystic fibrosis mouse small intestine. Am J Physiol Gastrointest Liver Physiol 286: G1032-G1041, 2004.
37. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, Ohara RB, Simpson GL, Solymos P, Stevens HH, Wagner H. vegan: Community Ecology Package. http://vegan.r-forge.r-project.org/2013.
38. Pavlidis P. Using ANOVA for gene selection from microarray studies of the nervous system. Methods 31: 282-289, 2003.
39. Raman M, Chen W, Cobb MH. Differential regulation and properties of MAPKs. Oncogene 26: 3100-3112, 2007.
40. Ratjen F, Doring G. Cystic fibrosis. Lancet 361: 681-689, 2003.
41. Rottner M, Tual-Chalot S, Mostefai HA, Andriantsitohaina R, Freyssinet JM, Martínez MC. Increased oxidative stress induces apoptosis in human cystic fibrosis cells. PLoS One 6: e24880, 2011.
42. Smyth GK. Limma: linear models for microarray data. In: Bioinformatics and Computational Biology Solutions Using R and Bioconductor, edited by Gentleman R, Carey V, Huber W, Irizarry R, Dudoit S. New York: Springer, 2005, p. 397-420.
43. Soleti R, Porro C, Martínez MC. Apoptotic process in cystic fibrosis cells. Apoptosis 18: 1029-1038, 2013.
44. Takeda K, Noguchi T, Naguro I, Ichijo H. Apoptosis signal-regulating kinase 1 in stress and immune response. Annu Rev Pharmacol Toxicol 48: 199-225, 2008.
45. Tamm C, Zhivotovsky B, Ceccatelli S. Caspase-2 activation in neural stem cells undergoing oxidative stress-induced apoptosis. Apoptosis 13: 354-363, 2008.
46. Tarran R, Button B, Boucher RC. Regulation of normal and cystic fibrosis airway surface liquid volume by phasic shear stress. Annu Rev Physiol 68: 543-561, 2006.
47. +channel activity control normal and cystic fibrosis bronchial epithelia repair. Am J Physiol Lung Cell Mol Physiol 295: L866-L880, 2008.
48. Valdivieso AG, Santa-Coloma TA. CFTR activity and mitochondrial function. Redox Biol 1: 190-202, 2013.
49. Vankeerberghen A, Cuppens H, Cassiman JJ. The cystic fibrosis transmembrane conductance regulator: an intriguing protein with pleiotropic functions. J Cyst Fibros 1: 13-29, 2002.
50. Verhaeghe C, Remouchamps C, Hennuy B, Vanderplasschen A, Chariot A, Tabruyn SP, Oury C, Bours V. Role of IKK and ERK pathways in intrinsic inflammation of cystic fibrosis airways. Biochem Pharmacol 73: 1982-1994, 2007.
51. Vogler M. BCL2A1: the underdog in the BCL2 family. Cell Death Differ 19: 67-74, 2012.
52. Wright JM, Merlo CA, Reynolds JB, Zeitlin PL, Garcia JGN, Guggino WB, Boyle MP. Respiratory epithelial gene expression in patients with mild and severe cystic fibrosis lung disease. Am J Respir Cell Mol Biol 35: 327-336, 2006.
53. Xu Y, Clark JC, Aronow BJ, Dey CR, Liu C, Wooldridge JL, Whitsett JA. Transcriptional adaptation to cystic fibrosis transmembrane conductance regulator deficiency. J Biol Chem 278: 7674-7682, 2003.
54. Yalçin E, Talim B, Ozçelik U, Doǧru D, Cobanoǧlu N, Pekcan S, Kiper N. Does defective apoptosis play a role in cystic fibrosis lung disease? Arch Med Res 40: 561-564, 2009.
55. Zabner J, Karp P, Seiler M, Phillips SL, Mitchell CJ, Saavedra M, Welsh M, Klingelhutz AJ. Development of cystic fibrosis and noncystic fibrosis airway cell lines. Am J Physiol Lung Cell Mol Physiol 284: L844-L854, 2003.
56. Zabner J, Scheetz TE, Almabrazi HG, Casavant TL, Huang J, Keshavjee S, McCray PB Jr. CFTR DeltaF508 mutation has minimal effect on the gene expression profile of differentiated human airway epithelia. Am J Physiol Lung Cell Mol Physiol 289: L545-L553, 2005.
57. Ziady AG, Hansen J. Redox balance in cystic fibrosis. Int J Biochem Cell Biology 52C: 113-123, 2014.