Normal CFTR Inhibits Epidermal Growth Factor Receptor-Dependent Pro-Inflammatory Chemokine Production in Human Airway Epithelial Cells

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Kim, Suil ^a,b   Beyer, Brittney A ^a   Lewis, Courtney ^c,d   Nadel, Jay A ^c,d  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CHLOROTRIANISENE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EPIDERMAL GROWTH FACTOR RECEPTOR; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 8; NEUTRALIZING ANTIBODY; SMALL INTERFERING RNA; 3-((3-TRIFLUOROMETHYL)PHENYL)-5-((3-CARBOXYPHENYL)METHYLENE)-2-THIOXO-4-THIAZOLIDINONE; ADAM PROTEIN; AUTACOID; BENZOIC ACID DERIVATIVE; MUTANT PROTEIN; THIAZOLIDINE DERIVATIVE; TUMOR NECROSIS FACTOR-ALPHA CONVERTASE;

ARTICLE; CONTROLLED STUDY; CYSTIC FIBROSIS; CYTOKINE PRODUCTION; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; LIGAND BINDING; NEUTROPHIL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN PHOSPHORYLATION; RESPIRATORY EPITHELIUM; SIGNAL TRANSDUCTION; SUPERNATANT; BIOLOGICAL MODEL; BIOSYNTHESIS; BRONCHUS; CELL LINE; DRUG EFFECTS; EPITHELIUM CELL; METABOLISM; PATHOLOGY; PHOSPHORYLATION;

ADAM PROTEINS; BENZOATES; BRONCHI; CELL LINE; CHEMOKINES; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EPITHELIAL CELLS; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-1ALPHA; INTERLEUKIN-8; MODELS, BIOLOGICAL; MUTANT PROTEINS; PHOSPHORYLATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, INTERLEUKIN-1; THIAZOLIDINES;

EID: 84881559756     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072981     Document Type: Article

References (65)

1. Baggiolini M, Walz A, Kunkel SL, (1989) Neutrophil-activating peptide-1/interleukin 8, a novel cytokine that activates neutrophils. J Clin Invest 84: 1045-1049.
2. Kerem B, Rommens JM, Buchanan JA, Markiewicz D, Cox TK, et al. (1989) Identification of the cystic fibrosis gene: genetic analysis. Science 245: 1073-1080.
3. Riordan JR, Rommens JM, Kerem B, Alon N, Rozmahel R, et al. (1989) Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245: 1066-1073.
4. Bonfield TL, Panuska JR, Konstan MW, Hilliard KA, Hilliard JB, et al. (1995) Inflammatory cytokines in cystic fibrosis lungs. Am J Respir Crit Care Med 152: 2111-2118.
5. Dean TP, Dai Y, Shute JK, Church MK, Warner JO, (1993) Interleukin-8 concentrations are elevated in bronchoalveolar lavage, sputum, and sera of children with cystic fibrosis. Pediatr Res 34: 159-161.
6. Salva PS, Doyle NA, Graham L, Eigen H, Doerschuk CM, (1996) TNF-alpha, IL-8, soluble ICAM-1, and neutrophils in sputum of cystic fibrosis patients. Pediatr Pulmonol 21: 11-19.
7. Davis PB, Drumm M, Konstan MW, (1996) Cystic fibrosis. Am J Respir Crit Care Med 154: 1229-1256.
8. Khan TZ, Wagener JS, Bost T, Martinez J, Accurso FJ, et al. (1995) Early pulmonary inflammation in infants with cystic fibrosis. Am J Respir Crit Care Med 151: 1075-1082.
9. Tirouvanziam R, Khazaal I, Peault B, (2002) Primary inflammation in human cystic fibrosis small airways. Am J Physiol Lung Cell Mol Physiol 283: L445-51.
10. DiMango E, Ratner AJ, Bryan R, Tabibi S, Prince A, (1998) Activation of NF-kappaB by adherent Pseudomonas aeruginosa in normal and cystic fibrosis respiratory epithelial cells. J Clin Invest 101: 2598-2605.
11. Kube D, Sontich U, Fletcher D, Davis PB, (2001) Proinflammatory cytokine responses to P. aeruginosa infection in human airway epithelial cell lines. Am J Physiol Lung Cell Mol Physiol 280: L493-502.
12. Li J, Johnson XD, Iazvovskaia S, Tan A, Lin A, et al. (2003) Signaling intermediates required for NF-kappa B activation and IL-8 expression in CF bronchial epithelial cells. Am J Physiol Lung Cell Mol Physiol 284: L307-15.
13. Stecenko AA, King G, Torii K, Breyer RM, Dworski R, et al. (2001) Dysregulated cytokine production in human cystic fibrosis bronchial epithelial cells. Inflammation 25: 145-155.
14. Tabary O, Zahm JM, Hinnrasky J, Couetil JP, Cornillet P, et al. (1998) Selective up-regulation of chemokine IL-8 expression in cystic fibrosis bronchial gland cells in vivo and in vitro. Am J Pathol 153: 921-930.
15. Eidelman O, Srivastava M, Zhang J, Leighton X, Murtie J, et al. (2001) Control of the proinflammatory state in cystic fibrosis lung epithelial cells by genes from the TNF-alphaR/NFkappaB pathway. Mol Med 7: 523-534.
16. Aldallal N, McNaughton EE, Manzel LJ, Richards AM, Zabner J, et al. (2002) Inflammatory response in airway epithelial cells isolated from patients with cystic fibrosis. Am J Respir Crit Care Med 166: 1248-1256.
17. Perez A, Issler AC, Cotton CU, Kelley TJ, Verkman AS, et al. (2007) CFTR inhibition mimics the cystic fibrosis inflammatory profile. Am J Physiol Lung Cell Mol Physiol 292: L383-95.
18. Vij N, Mazur S, Zeitlin PL, (2009) CFTR is a negative regulator of NFkappaB mediated innate immune response. PLoS One 4: e4664.
19. Hunter MJ, Treharne KJ, Winter AK, Cassidy DM, Land S, et al. (2010) Expression of wild-type CFTR suppresses NF-kappaB-driven inflammatory signalling. PLoS One 5: e11598.
20. Nakanaga T, Nadel JA, Ueki IF, Koff JL, Shao MX, (2007) Regulation of interleukin-8 via an airway epithelial signaling cascade. Am J Physiol Lung Cell Mol Physiol 292: L1289-96.
21. Richter A, O'Donnell RA, Powell RM, Sanders MW, Holgate ST, et al. (2002) Autocrine ligands for the epidermal growth factor receptor mediate interleukin-8 release from bronchial epithelial cells in response to cigarette smoke. Am J Respir Cell Mol Biol 27: 85-90.
22. Subauste MC, Proud D, (2001) Effects of tumor necrosis factor-alpha, epidermal growth factor and transforming growth factor-alpha on interleukin-8 production by, and human rhinovirus replication in, bronchial epithelial cells. Int Immunopharmacol 1: 1229-1234.
23. Takeyama K, Fahy JV, Nadel JA, (2001) Relationship of epidermal growth factor receptors to goblet cell production in human bronchi. Am J Respir Crit Care Med 163: 511-516.
24. Burgel PR, Montani D, Danel C, Dusser DJ, Nadel JA, (2007) A morphometric study of mucins and small airway plugging in cystic fibrosis. Thorax 62: 153-161.
25. Peschon JJ, Slack JL, Reddy P, Stocking KL, Sunnarborg SW, et al. (1998) An essential role for ectodomain shedding in mammalian development. Science 282: 1281-1284.
26. Shao MX, Ueki IF, Nadel JA, (2003) Tumor necrosis factor alpha-converting enzyme mediates MUC5AC mucin expression in cultured human airway epithelial cells. Proc Natl Acad Sci U S A 100: 11618-11623.
27. Kuwahara I, Lillehoj EP, Lu W, Singh IS, Isohama Y, et al. (2006) Neutrophil elastase induces IL-8 gene transcription and protein release through p38/NF-{kappa}B activation via EGFR transactivation in a lung epithelial cell line. Am J Physiol Lung Cell Mol Physiol 291: L407-16.
28. Liu K, Gualano RC, Hibbs ML, Anderson GP, Bozinovski S, (2008) Epidermal growth factor receptor signaling to Erk1/2 and STATs control the intensity of the epithelial inflammatory responses to rhinovirus infection. J Biol Chem 283: 9977-9985.
29. Koff JL, Shao MX, Ueki IF, Nadel JA, (2008) Multiple TLRs activate EGFR via a signaling cascade to produce innate immune responses in airway epithelium. Am J Physiol Lung Cell Mol Physiol 294: L1068-75.
30. Kim S, Lewis C, Nadel JA, (2011) Epidermal growth factor receptor reactivation induced by E-prostanoid-3 receptor- and tumor necrosis factor-alpha-converting enzyme-dependent feedback exaggerates interleukin-8 production in airway cancer (NCI-H292) cells. Exp Cell Res 317: 2650-2660.
31. Ma T, Thiagarajah JR, Yang H, Sonawane ND, Folli C, et al. (2002) Thiazolidinone CFTR inhibitor identified by high-throughput screening blocks cholera toxin-induced intestinal fluid secretion. J Clin Invest 110: 1651-1658.
32. Nagayama S, Kai H, Okiyoneda T, Horikawa S, Miyata T, (1999) Characterization of CFTR expression in a human pulmonary mucoepidermoid carcinoma cell line, NCI-H292 cells. FEBS Lett 455: 215-218.
33. Zeitlin PL, Lu L, Rhim J, Cutting G, Stetten G, et al. (1991) A cystic fibrosis bronchial epithelial cell line: immortalization by adeno-12-SV40 infection. Am J Respir Cell Mol Biol 4: 313-319.
34. Flotte TR, Afione SA, Solow R, Drumm ML, Markakis D, et al. (1993) Expression of the cystic fibrosis transmembrane conductance regulator from a novel adeno-associated virus promoter. J Biol Chem 268: 3781-3790.
35. Venkatakrishnan A, Stecenko AA, King G, Blackwell TR, Brigham KL, et al. (2000) Exaggerated activation of nuclear factor-kappaB and altered IkappaB-beta processing in cystic fibrosis bronchial epithelial cells. Am J Respir Cell Mol Biol 23: 396-403.
36. Bezzerri V, Borgatti M, Finotti A, Tamanini A, Gambari R, et al. (2011) Mapping the transcriptional machinery of the IL-8 gene in human bronchial epithelial cells. J Immunol 187: 6069-6081.
37. Bhattacharyya S, Balakathiresan NS, Dalgard C, Gutti U, Armistead D, et al. (2011) Elevated miR-155 promotes inflammation in cystic fibrosis by driving hyperexpression of interleukin-8. J Biol Chem 286: 11604-11615.
38. Banks-Schlegel SP, Gazdar AF, Harris CC, (1985) Intermediate filament and cross-linked envelope expression in human lung tumor cell lines. Cancer Res 45: 1187-1197.
39. Wong J, Korcheva V, Jacoby DB, Magun BE, (2007) Proinflammatory responses of human airway cells to ricin involve stress-activated protein kinases and NF-kappaB. Am J Physiol Lung Cell Mol Physiol 293: L1385-94.
40. Zhang Z, Oliver P, Lancaster JJ, Schwarzenberger PO, Joshi MS, et al. (2001) Reactive oxygen species mediate tumor necrosis factor alpha-converting, enzyme-dependent ectodomain shedding induced by phorbol myristate acetate. FASEB J 15: 303-305.
41. Verhaeghe C, Remouchamps C, Hennuy B, Vanderplasschen A, Chariot A, et al. (2007) Role of IKK and ERK pathways in intrinsic inflammation of cystic fibrosis airways. Biochem Pharmacol 73: 1982-1994.
42. Xu P, Derynck R, (2010) Direct activation of TACE-mediated ectodomain shedding by p38 MAP kinase regulates EGF receptor-dependent cell proliferation. Mol Cell 37: 551-566.
43. Hall KC, Blobel CP, (2012) Interleukin-1 stimulates ADAM17 through a mechanism independent of its cytoplasmic domain or phosphorylation at threonine 735. PLoS One 7: e31600.
44. Strieter RM, Kunkel SL, Showell HJ, Remick DG, Phan SH, et al. (1989) Endothelial cell gene expression of a neutrophil chemotactic factor by TNF-alpha, LPS, and IL-1 beta. Science 243: 1467-1469.
45. Hardie WD, Bejarano PA, Miller MA, Yankaskas JR, Ritter JH, et al. (1999) Immunolocalization of transforming growth factor alpha and epidermal growth factor receptor in lungs of patients with cystic fibrosis. Pediatr Dev Pathol 2: 415-423.
46. Maiuri L, Luciani A, Giardino I, Raia V, Villella VR, et al. (2008) Tissue transglutaminase activation modulates inflammation in cystic fibrosis via PPARgamma down-regulation. J Immunol 180: 7697-7705.
47. Kim S, Lewis C, Nadel JA, (2011) CCL20/CCR6 feedback exaggerates epidermal growth factor receptor-dependent MUC5AC mucin production in human airway epithelial (NCI-H292) cells. J Immunol 186: 3392-3400.
48. Tang A, Sharma A, Jen R, Hirschfeld AF, Chilvers MA, et al. (2012) Inflammasome-mediated IL-1beta production in humans with cystic fibrosis. PLoS One 7: e37689.
49. Olaru F, Jensen LE, (2010) Staphylococcus aureus stimulates neutrophil targeting chemokine expression in keratinocytes through an autocrine IL-1alpha signaling loop. J Invest Dermatol 130: 1866-1876.
50. Botelho FM, Bauer CM, Finch D, Nikota JK, Zavitz CC, et al. (2011) IL-1alpha/IL-1R1 expression in chronic obstructive pulmonary disease and mechanistic relevance to smoke-induced neutrophilia in mice. PLoS One 6: e28457.
51. Manzer R, Dinarello CA, McConville G, Mason RJ, (2008) Ozone exposure of macrophages induces an alveolar epithelial chemokine response through IL-1alpha. Am J Respir Cell Mol Biol 38: 318-323.
52. Veit G, Bossard F, Goepp J, Verkman AS, Galietta LJ, et al. (2012) Proinflammatory cytokine secretion is suppressed by TMEM16A or CFTR channel activity in human cystic fibrosis bronchial epithelia. Mol Biol Cell 23: 4188-4202.
53. Matsui H, Grubb BR, Tarran R, Randell SH, Gatzy JT, et al. (1998) Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airways disease. Cell 95: 1005-1015.
54. Stoltz DA, Meyerholz DK, Pezzulo AA, Ramachandran S, Rogan MP, et al. (2010) Cystic fibrosis pigs develop lung disease and exhibit defective bacterial eradication at birth. Sci Transl Med 2: 29ra31.
55. Kelly M, Trudel S, Brouillard F, Bouillaud F, Colas J, et al. (2010) Cystic fibrosis transmembrane regulator inhibitors CFTR(inh)-172 and GlyH-101 target mitochondrial functions, independently of chloride channel inhibition. J Pharmacol Exp Ther 333: 60-69.
56. Hybiske K, Fu Z, Schwarzer C, Tseng J, Do J, et al. (2007) Effects of cystic fibrosis transmembrane conductance regulator and DeltaF508CFTR on inflammatory response, ER stress, and Ca2+ of airway epithelia. Am J Physiol Lung Cell Mol Physiol 293: L1250-60.
57. Reiniger N, Ichikawa JK, Pier GB, (2005) Influence of cystic fibrosis transmembrane conductance regulator on gene expression in response to Pseudomonas aeruginosa infection of human bronchial epithelial cells. Infect Immun 73: 6822-6830.
58. John G, Yildirim AO, Rubin BK, Gruenert DC, Henke MO, (2010) TLR-4-mediated innate immunity is reduced in cystic fibrosis airway cells. Am J Respir Cell Mol Biol 42: 424-431.
59. Massengale AR, Quinn FJ, Yankaskas J, Weissman D, McClellan WT, et al. (1999) Reduced interleukin-8 production by cystic fibrosis airway epithelial cells. Am J Respir Cell Mol Biol 20: 1073-1080.
60. Black HR, Yankaskas JR, Johnson LG, Noah TL, (1998) Interleukin-8 production by cystic fibrosis nasal epithelial cells after tumor necrosis factor-alpha and respiratory syncytial virus stimulation. Am J Respir Cell Mol Biol 19: 210-215.
61. Ribeiro CM, Paradiso AM, Schwab U, Perez-Vilar J, Jones L, et al. (2005) Chronic airway infection/inflammation induces a Ca2+i-dependent hyperinflammatory response in human cystic fibrosis airway epithelia. J Biol Chem 280: 17798-17806.
62. Becker MN, Sauer MS, Muhlebach MS, Hirsh AJ, Wu Q, et al. (2004) Cytokine secretion by cystic fibrosis airway epithelial cells. Am J Respir Crit Care Med 169: 645-653.
63. Bartling TR, Drumm ML, (2009) Loss of CFTR results in reduction of histone deacetylase 2 in airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 297: L35-43.
64. Bjorge JD, Paterson AJ, Kudlow JE, (1989) Phorbol ester or epidermal growth factor (EGF) stimulates the concurrent accumulation of mRNA for the EGF receptor and its ligand transforming growth factor-alpha in a breast cancer cell line. J Biol Chem 264: 4021-4027.
65. Coffey RJJ, Derynck R, Wilcox JN, Bringman TS, Goustin AS, et al. (1987) Production and auto-induction of transforming growth factor-alpha in human keratinocytes. Nature 328: 817-820.