Effects of cystic fibrosis transmembrane conductance regulator and ΔF508CFTR on inflammatory response, ER stress, and Ca2+ of airway epithelia

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 293, Issue 5, 2007, Pages

  Hybiske, Kevin ^a   Fu, Zhu ^a   Schwarzer, Christian ^a   Tseng, Jill ^a   Do, Jiun ^a   Huang, Natalie ^a   Machen, Terry E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adenovirus; Endoplasmic reticulum stress; Inflammation; Interleukin 8; Ire1 ; Nuclear factor B

Indexed keywords

ADENOSINE TRIPHOSPHATE; BETA GALACTOSIDASE; CALCIUM ION; FLAGELLIN; FORSKOLIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; THAPSIGARGIN; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ARTICLE; CELL CULTURE; CELL LINE; CONTROLLED STUDY; CYSTIC FIBROSIS; CYTOKINE RELEASE; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HUMAN; HUMAN CELL; INFLAMMATION; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSEUDOMONAS AERUGINOSA; RESPIRATORY EPITHELIUM; VIRUS INFECTION;

BRONCHI; CALCIUM; CALCIUM SIGNALING; CELLS, CULTURED; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; ENDOPLASMIC RETICULUM; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLAGELLIN; HUMANS; INFLAMMATION; INTERLEUKIN-8; MICROSCOPY, CONFOCAL; MUTATION; NF-KAPPA B; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; RESPIRATORY MUCOSA;

EID: 36348955754     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00231.2007     Document Type: Article

References (65)

1. Adamo R, Sokol S, Soong G, Gomez MI, Prince A. Pseudomonas aeruginosa flagella activate airway epithelial cells through asialoGM1 and toll-like receptor 2 as well as toll-like receptor 5. Am J Respir Cell Mol Biol 30: 627-634, 2004.
2. 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: 1248-156, 2002.
3. Back SH, Lee K, Vink E, Kaufman RJ. Cytoplasmic IRE1alpha-mediated XBP1 mRNA splicing in the absence of nuclear processing and endoplasmic reticulum stress. J Biol Chem 281: 18691-18706, 2006.
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: 645-53, 2004.
5. Bonfield TL, Konstan MW, Berger M. Altered respiratory epithelial cell cytokine production in cystic fibrosis. J Allergy Clin Immunol 104: 72-78, 1999.
6. Bryan R, Kube D, Perez A, Davis PB, Prince A. Overproduction of the CFTR R-domain leads to increased levels of asialoGM1 and increased P. aeruginosa binding by epithelial cells. Am J Respir Cell Mol Biol 19: 269-277, 1998.
7. Carrabino S, Carpani D, Livraghi A, Di Cicco M, Costantini D, Copreni E, Colombo C, Conese M. Dysregulated interleukin-8 secretion and NF-kappaB activity in human cystic fibrosis nasal epithelial cells. J Cyst Fibros 5: 113-9, 2006.
8. Coyne MJ Jr, Russell KS, Coyle CL, Goldberg JB. The Pseudomonas aeruginosa algC gene encodes phosphoglucomutase, required for the synthesis of a complete lipopolysaccharide core. J Bacteriol 176: 3500-3507, 1994.
9. Cuzick A, Stirling FR, Lindsay SL, Evans TJ. The type III pseudomonal exotoxin U activates the c-Jun NH2-terminal kinase pathway and increases human epithelial interleukin-8 production. Infect Immun 74: 4104-4113, 2006.
10. Dakin CJ, Numa AH, Wang H, Morton JR, Vertzyas CC, Henry RL. Inflammation, infection, and pulmonary function in infants and young children with cystic fibrosis. Am J Respir Crit Care Med 165: 904-910, 2002.
11. DiMango E, Ratner AJ, Bryan R, Tabibi S, Prince A. Activation of NF-kappaB by adherent Pseudomonas aeruginosa in normal and cystic fibrosis respiratory epithelial cells. J Clin Invest 101: 2598-2605, 1998.
12. Eidelman O, Srivastava M, Zhang J, Leighton X, Murtie J, Jozwik C, Jacobson K, Weinstein DL, Metcalf EL, Pollard HB. Control of the proinflammatory state in cystic fibrosis lung epithelial cells by genes from the TNF-alphaR/NFkappaB pathway. Mol Med 7: 523-534, 2001.
13. 2+ in responses of airway epithelia to P. aeruginosa, flagellin, ATP and thapsigargin. Am J Physiol Lung Cell Mol Physiol 292: L353-L364, 2007.
14. Grynkiewicz G, Poenie M, Tsien RY. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440-3450, 1985.
15. Hallows KR, Fitch AC, Richardson CA, Reynolds PR, Clancy JP, Dagher PC, Witters LA, Kolls JK, Pilewski JM. Up-regulation of AMP-activated kinase by dysfunctional cystic fibrosis transmembrane conductance regulator in cystic fibrosis airway epithelial cells mitigates excessive inflammation. J Biol Chem 281: 4231-4241, 2006.
16. Hanna SL, Sherman NE, Kinter MT, Goldberg JB. Comparison of proteins expressed by Pseudomonas aeruginosa strains representing initial and chronic isolates from a cystic fibrosis patient: an analysis by 2-D gel electrophoresis and capillary column liquid chromatography-tandem mass spectrometry. Microbiology 146: 2495-2508, 2000.
17. Hybiske K, Ichikawa J, Huang V, Lory SJ, Machen TE. Cystic fibrosis airway epithelial cell polarity and bacterial flagellin determine host response to P. aeruginosa, Cell Micro 6: 49-62, 2004.
18. 3 secretion through CFTR in human airway epithelia. Am J Physiol Lung Cell Mol Physiol 272: L752-L761, 1997.
19. Imundo L, Barasch J, Prince A, Al-Awqati Q. Cystic fibrosis epithelial cells have a receptor for pathogenic bacteria on their apical surface. Proc Nat Acad Sci USA 92: 3019-3012, 1995.
20. 2+ concentration in airway epithelial cells by Pseudomonas aeruginosa. Infect Immun 70: 6399-6408, 2002.
21. Jefferson DM, Valentich JD, Marini FC, Grubman SA, Iannuzzi MC, Dorkin HL, Li M, Klinger KW, Welsh MJ. Expression of normal and cystic fibrosis phenotypes by continuous airway epithelial cell lines. Am J Physiol Lung Cell Mol Physiol 259: L496-L505, 1990.
22. Joo NS, Irokawa T, Wu JV, Robbins RC, Whyte RI, Wine JJ. Absent secretion to vasoactive intestinal peptide in cystic fibrosis airway glands. J Biol Chem 277: 50710-50715, 2002.
23. Kopito RR. Biosynthesis and degradation of CFTR. Physiol Rev 79: S167-S173, 1999.
24. Kube D, Sontic U, Fletcher D, Davis PB. Proinflammatory cytokine responses to P. aeruginosa infection in human airway epithelial cell lines. Am J Physiol Lung Cell Mol Physiol 280: L493-L502, 2001.
25. Kunzelmann K, Scheidt K, Scharf B, Ousingsawat J, Schreiber R, Wainwright B, McMorran B. Flagellin of Pseudomonas aeruginosa inhibits Na+ transport in airway epithelia. FASEB J 20: 545-546, 2006.
26. Lee A, Chow D, Tseng W, Haus B, Evans D, Fleiszig S, Chandy G, Machen TE. Airway epithelial tight junctions and binding and cytotoxicity of Pseudomonas aeruginosa. Am J Physiol Lung Cell Mol Physiol 277: L204-L217, 1999.
27. Lee MC, Penland CM, Widdicombe JH, Wine JJ. Evidence that Calu-3 human airway cells secrete bicarbonate. Am J Physiol Lung Cell Mol Physiol 274: L450-L453, 1998.
28. Machen TE. Innate immune response in CF airway epithelia: hyperinflammatory? Am J Physiol Cell Physiol 291: C218-C230, 2006.
29. Massengale AR, Quinn F, Yankaskas J, Weissman D, McClellan WT, Cuff C, Aronoff SC. Reduced interleukin-8 production by cystic fibrosis airway epithelial cells. Am J Respir Cell Mol Biol 20: 1073-1080, 1999.
30. Matsui H, Grubb BR, Tarran R, Randell SH, Gatzy JT, Davis CW, Boucher RC. Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airways disease. Cell 95: 1005-1015, 1998.
31. McNamara N, Gallup M, Sucher A, Maltseva I, McKemy D, Basbaum C. AsialoGM1 and TLR5 cooperate in flagellin-induced nucleotide signaling to activate ERK1/2. Am J Respir Cell Mol Biol 34: 653-60, 2006.
32. Minguet S, Huber M, Rosenkranz L, Schamel WW, Reth M, Brummer T. Adenosine and cAMP are potent inhibitors of the NF-kappa B pathway downstream of immunoreceptors. Eur J Immunol 35: 31-41, 2005.
33. Muhlebach MS, Stewart PW, Leigh MW, Noah TL. Quantification of inflammatory responses to bacteria in young cystic fibrosis and control patients. Am J Respir Crit Care Med 160: 186-191, 1999.
34. Perez A, Davis PB. Gene profile changes after Pseudomonas aeruginosa exposure in immortalized airway epithelial cells. J Struct Funct Genomics 5: 179-94, 2004.
35. Perez A, Issler AC, Cotton CU, Kelley TJ, Verkman AS, Davis PB. CFTR inhibition mimics the cystic fibrosis inflammatory profile. Am J Physiol Lung Cell Mol Physiol 292: L383-L395, 2007.
36. Pizurki L, Morris MA, Chanson M, Solomon M, Pavirani A, Bouchardy I, Suter S. Cystic fibrosis transmembrane conductance regulator does not affect neutrophil migration across cystic fibrosis airway epithelial monolayers. Am J Pathol 156: 1407-1416, 2000.
37. Rab A, Bartoszewski R, Jurkuvenaite A, Wakefield J, Collawn JF, Bebok Z. Endoplasmic reticulum stress and the unfolded protein response regulate genomic cystic fibrosis transmembrane conductance regulator expression. Am J Physiol Cell Physiol 292: C756-C766, 2007.
38. Ratner AJ, Bryan R, Weber A, Nguyen S, Barnes D, Pitt A, Gelber S, Cheung A, Prince A. Cystic fibrosis pathogens activate Ca2+-dependent mitogen-activated protein kinase signaling pathways in airway epithelial cells. J Biol Chem 276: 19267-19275, 2001.
39. Reddy MM, Quinton PM. Effect of anion transport blockers on C.FTR in the human sweat duct. J Membr Biol 189: 15-25, 2002.
40. Reiniger N, Ichikawa JK, Pier GB. 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, 2005.
41. 2+i-dependent hyperinflammatory response in human cystic fibrosis airway epithelia. J Biol Chem 280: 17798-17806, 2005.
42. Riordan JR, Chang XB. CFTR, a channel with the structure of a transporter. Biochim Biophys Acta 110: 221-222, 1992.
43. Rogers GB, Carroll MP, Serisier DJ, Hockey PM, Kehagia V, Jones GR, Bruce KD. Bacterial activity in cystic fibrosis lung infections (Abstract). Respir Res 6: 49, 2005.
44. Rogers GB, Carroll MP, Serisier DJ, Hockey PM, Jones G, Bruce KD. Characterization of bacterial community diversity in cystic fibrosis lung infections by use of 16s ribosomal DNA terminal restriction fragment length polymorphism profiling. J Clin Microbiol 42: 5176-5178, 2004.
45. Sachs LA, Finkbeiner WE, Widdicombe JH. Effects of media on differentiation of cultured human tracheal epithelium. In Vitro Cell Dev Biol Animal 39: 56-62, 2003.
46. Saiman L, Prince A. Pseudomonas aeruginosa pili bind to asialoGM1 which is increased on the surface of cystic fibrosis epithelial cells. J Clin Invest 92: 1875-1880, 1993.
47. Sanlioglu S, Williams CM, Samavati L, Butler NS, Wang G, McCray PB Jr, Ritchie TC, Hunninghake GW, Zandi E, Engelhardt JF. Lipopolysaccharide induces Rac1-dependent reactive oxygen species formation and coordinates tumor necrosis factor-alpha secretion through IKK regulation of NF-kappa B. J Biol Chem 276: 30188-30198, 2001.
48. Schwarzer C, Illek B, Remington SJ, Fischer H, Machen TE. Organelle redox of CF and CFTR-corrected airway epithelia measured with roGFP1. Free Rad Biol Med 43: 300-316, 2007.
49. Schwiebert LM, Estell K, Propst SM. Chemokine expression in CF epithelia: implications for the role of CFTR in RANTES expression. Am J Physiol Cell Physiol 276: C700-C710, 1999.
50. Srivastava M, Eidelman O, Pollard HB. Pharmacogenomics of the cystic fibrosis transmembrane conductance regulator (CFTR) and the cystic fibrosis drug CPX using genome microarray analysis. Mol Med 5: 753-767, 2001.
51. Tirouvanziam R, de Bentzmann S, Hubeau C, Hinnrasky J, Jacquot J, Peault B, Puchelle E. Inflammation and infection in naive human cystic fibrosis airway grafts. Am J Respir Cell Mol Biol 23: 121-127, 2000.
52. Tseng J, Do J, Widdicombe JH, Machen TE. Innate immune responses of human tracheal epithelium to Pseudomonas aeruginosa flagellin, TNF-α, and IL-1β. Am J Physiol Cell Physiol 290: C678-C690, 2006.
53. Ulrich M, Herbert S, Berger J, Bellon G, Louis D, Munker G, Doring G. Localization of Staphylococcus aureus in infected airways of patients with cystic fibrosis and in a cell culture model of S. aureus adherence Am J Respir Cell Mol Biol 19: 83-91, 1998.
54. Vais H, Gao GP, Yang M, Tran P, Louboutin JP, Somanathan S, Wilson JM, Reenstra WW. Novel adenoviral vectors coding for GFP-tagged wtCFTR and deltaF508-CFTR: characterization of expression and electrophysiological properties in A549 cells. Pflugers Arch 449: 278-287, 2004.
55. Van Heeckeren A, Walenga R, Konstan MW, Bonfield T, Davis PB, Ferkol T. Excessive inflammatory response of cystic fibrosis mice to bronchopulmonary infection with Pseudomonas aeruginosa. J Clin Invest 100: 2810-2815, 1997.
56. van Heeckeren AM, Schluchter MD. Murine models of chronic Pseudomonas aeruginosa lung infection. Lab Anim 36: 291-312, 2002.
57. Van Heeckeren AM, Schluchter MD, Drumm ML, Davis PB. Cftr genotype in the response to chronic Pseudomonas aeruginosa lung infection in mice. Am J Physiol Lung Cell Mol Physiol 287: L944-L952, 2004.
58. Verkman AS, Song Y, Thiagarajah JR. Role of airway surface liquid and submucosal glands in cystic fibrosis lung disease. Am J Physiol Cell Physiol 284: C2-C15, 2003.
59. Weber AJ, Soong G, Bryan R, Saba S, Prince A. Activation of NF-kappaB in airway epithelial cells is dependent on CFTR trafficking and Cl channel function. Am J Physiol Lung Cell Mol Physiol 281: L71-L78, 2001.
60. Widdicombe JH, Sachs LA, Morrow JL, Finkbeiner WE. Expansion of cultures of human tracheal epithelium with maintenance of differentiated structure and function. Biotechniques 39: 249-255, 2005.
61. Willumsen NJ, Boucher RC. Shunt resistance and ion permeabilities in normal and cystic fibrosis airway epithelia. Am J Physiol Cell Physiol 256: C1054-C1063, 1989.
62. Wu J, Kaufman RJ. From acute ER stress to physiological roles of the Unfolded Protein Response. Cell Death Differ 13: 374-384, 2006.
63. Xu C, Bailly-Maitre B, Reed JC. Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest 115: 2656-2664, 2005.
64. 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.
65. Zhang Z, Louboutin JP, Weiner DJ, Goldberg JB, Wilson JM. Human airway epithelial cells sense Pseudomonas aeruginosa infection via recognition of flagellin by Toll-like receptor 5. Infect Immun 73: 7151-7160, 2005.