Azithromycin reduces spontaneous and induced inflammation in ΔF508 cystic fibrosis mice

Respiratory Research

Volumn 7, Issue , 2006, Pages

  Legssyer, Rachida ^a   Huaux, François ^a   Lebacq, Jean ^b   Delos, Monique ^c   Marbaix, Etienne ^a   Lebecque, Patrick ^a   Lison, Dominique ^a   Scholte, Bob J ^d   Wallemacq, Pierre ^a   Leal, Teresinha ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b Uiversité Catholique de Louvain ^*  (Belgium)

^c UNIVERSITY HOSPITAL OF MONT GODINNE   (Belgium)

^d ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFLAMMATORY AGENT; AZITHROMYCIN; BACTERIUM LIPOPOLYSACCHARIDE; INTERLEUKIN 10; LACTATE DEHYDROGENASE; MACROPHAGE INFLAMMATORY PROTEIN 2; MYELOPEROXIDASE; TUMOR NECROSIS FACTOR ALPHA; CXCL2 CHEMOKINE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR DELTA F508; LIPOPOLYSACCHARIDE; MONOKINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ATTENUATION; CELL INFILTRATION; CONTROLLED STUDY; CYSTIC FIBROSIS; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DISEASE COURSE; DOSE RESPONSE; ENZYME ACTIVITY; FEMALE; HOMOZYGOSITY; LUNG FIBROSIS; MACROPHAGE; MOUSE; MUTATIONAL ANALYSIS; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PNEUMONIA; PSEUDOMONAS AERUGINOSA; UPREGULATION; ANIMAL; BIOSYNTHESIS; CHEMICALLY INDUCED; COMPLICATION; DRUG EFFECTS; GENETICS; LUNG; METABOLISM; MUTANT MOUSE STRAIN; PATHOLOGY;

ANIMALS; ANTI-INFLAMMATORY AGENTS; AZITHROMYCIN; CHEMOKINE CXCL2; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; INTERLEUKIN-10; LIPOPOLYSACCHARIDES; LUNG; MACROPHAGES; MICE; MICE, MUTANT STRAINS; MONOKINES; NEUTROPHIL INFILTRATION; PNEUMONIA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 33751177801     PISSN: 1465993X     EISSN: 1465993X     Source Type: Journal    
DOI: 10.1186/1465-9921-7-134     Document Type: Article

References (84)

1. Kerem B, Rommens JM, Buchanan JA, Markiewicz D, Cox TK, Chakravarti A, Buchwald M, Tsui LC: Identification of the cystic fibrosis gene: genetic analysis. Science 1989, 245:1073-1080.
2. Riordan JR, Rommens JM, Kerem B, Alon N, Rozmahel R, Grzelczak Z, Zielinski J, Lok S, Plavsic N, Chou JL: Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 1989, 245:1066-1073.
3. Stutts MJ, Rossier BC, Boucher RC: Cystic fibrosis transmembrane conductance regulator inverts protein kinase A-mediated regulation of epithelial sodium channel single channel kinetics. J Biol Chem 1997, 272:14307-14340.
4. Mohler PJ, Kreda SM, Boucher RC, Sudol M, Stutts MJ, Milgram SL: Yes-associated protein 65 localizes p62(cYes) to the apical compartment of airway epithelia by association with EBP50. J Cell Biol 1999, 147:879-890.
5. Ismailov II, Awayda MS, Jovov B, Berdiev BK, Fuller CM, Dedman JR, Kaetzel MA, Benos DJ: Regulation of epithelial sodium channels by the cystic fibrosis transmembrane conductance regulator. J Biol Chem 1996, 271:4725-4732.
6. Schwiebert EM, Morales MM, Devidas S, Egan ME, Guggino WB: Chloride channel and chloride conductance regulator domain of CFTR, the cystic fibrosis transmembrane conductance regulator. Proc Natl Acad Sci USA 1998, 95:2674-2679.
7. Lukacs GL, Mohamed A, Kartner N, Chang X-B, Riordan JR, Grinstein S: Conformational maturation of CFTR but not its mutant counterpart (ΔF508) occurs in the endoplasmic reticulum and requires ATP. EMBO J 1994, 13:6076-6086.
8. Stern RC: The diagnosis of cystic fibrosis. N Engl J Med 1997, 336:487-491.
9. Pamukcu A, Bush A, Buchdahal R: Effects of P. aeruginosa colonization on lung function and anthropomorphic variables in children with cystic fibrosis. Pediatr Pulmonol 1995, 19:10-15.
10. Henry RL, Mellis CM, Petrovic L: Mucoid Pseudomonas aeruginosa is a marker of poor survival in cystic fibrosis. Pediatr Pulmonol 1992, 12:158-161.
11. Chmiel JF, Konstan MW: Anti-inflammatory medications for cystic fibrosis lung disease: selecting the most appropriate agent. Treat Respir Med 2005, 4:255-273.
12. Dinwiddie R: Anti-inflammatory therapy in cystic fibrosis. J Cystic Fibrosis 2005, 4:45-48.
13. Jaffé A, Francis J, Rosenthal M, Bush A: Long-term azithromycin may improve lung function in children with cystic fibrosis. Lancet 1998, 351:420.
14. Wolter J, Seeney S, Bowler S, Masel P, McCornack J: Effect of long term treatment with azithromycin on disease parameters in cystic fibrosis: a randomised trial. Thorax 2002, 57:212-216.
15. Equi A, Balfour-Lynn IM, Bush A, Rosenthal M: Long term azithromycin in children with cystic fibrosis: a randomised, placebo-controlled crossover trial. Lancet 2002, 360:978-984.
16. Saiman L, Marshall BC, Mayer-Hamblett N, Burns JL, Quittner AL, Cibene DA, Coquillette S, Fieberg AY, Accurso FJ, Campbell PW 3rd, Macrolide Study Group: Azithromycin in patients with cystic fibrosis chronically infected with Pseudomonas aeruginosa: a randomised controlled trial. JAMA 2003, 290:1749-1756.
17. Gillis RI, Iglewski BH: Azithromycin retards Pseudomonas aeruginosa biofilm formation. J Clin Microbiol 2004, 42:5842-5845.
18. Kita MA, Sawari M, Oku D Hamuro A, Mikasa K, Konishi M, Emoto M, Takeuchi S, Narita N, Kashiba S: Suppression of virulence factors of Pseudomonas aeruginosa by erythromycin. J Antimicrob Chemother 1991, 27:273-284.
19. Tateda K, Ishii Y, Matsumoto T, Furuya N, Nagashima M, Matsunga T, Ohno A, Miyazaki S, Yamaguchi K: Direct evidence for antipseudomonal activity of macrolides: exposure dependent bactericidal activity and inhibition of protein synthesis by erythromycin, clarithromycin and azithromycin. Antimicrob Agents Chemother 1996, 40:2271-2275.
20. Imamura Y, Higashiyama Y, Tomono K, Izumikawa K, Yanagihara K, Ohno H, Miyazaki Y, Hirakata Y, Mizuta Y, Kadota J, Iglewski BH, Kohno S: Azithromycin exhibits bactericidal effects on Pseudomonas aeruginosa through interaction with outer membrane. Antimicrob Agents Chemother 2005, 49:1377-1380.
21. Pier G, Grout M, Zaidi TS: Cystic fibrosis transmembrane conductance regulator is an epithelial cell receptor for clearence of Pseudomonas aeruginosa from the lung. Proc Natl Acad Sci USA 1997, 94:12088-12093.
22. Schroeder TH, Lee MM, Yacono PW, Cannon CL, Gerçeker AA, Golan DE, Pier GB: CFTR is a pattern recognition molecule that extracts Pseudomonas aeruginosa LPS from the outer membrane into epithelial cells and activates NF-kB translocation. Proc Natl Acad Sci USA 2002, 99:6907-6912.
23. Pier GB: CFTR mutations and host susceptibility to Pseudomonas aeruginosa lung function. Curr Opin Microbiol 2002, 5:81-86.
24. van Doorninck JH, French PJ, Verbeek E, Peters RHPC, Morreau H, Bijman J, Scholte BJ: A mouse model for the cystic fibrosis ΔF508 mutation. EMBO J 1995, 14:4403-4411.
25. Nicklas W, Baneux P, Boot R, Decelle T, Deeny AA, Fumanelli M, Illgen-Wilcke B, FELASA (Federation of European Laboratory Animal Science Associations Working Group on Health Monitoring of Rodent and Rabbit Colonies: Recommendation for the health monitoring of rodent and rabbit colonies in breeding and experimental units. Lab Anim 2002, 36:20-42.
26. Huaux F, Liu T, McGarry B, Ullenbruch M, Phan SH: Dual roles of IL-4 in lung injury and fibrosis. J Immunol 2003, 170:2083-2092.
27. Arras M, Huaux F, Vink A, Delos M, Coutelier JP, Many MC, Barbarin V, Renauld JC, Lison D: Interleukin-9 reduces lung fibrosis and type 2 immune polarization induced by silica particles in a murine model. Am J Respir Cell Mol Biol 2001, 24:368-375.
28. Naito Y, Yoshikawa T, Matsuyama K, Yagi N, Arai M, Nakamura Y, Kaneko T, Yoshida N, Kondo M: Neutrophils, lipid peroxidation, and nitric oxide in gastric reperfusion injury in rats. Free Radic Biol Med 1998, 24:494-502.
29. Lasfargues G, Lardot C, Delos M, Lauwerys R, Lison D: The delayed lung responses to single and repeated intratracheal administration of pure cobalt and hard metal powder in the rat. Environ Res 1995, 69:108-21.
30. Hoiby H: Diffuse panbrochiolitis and cystic fibrosis: East meets West. Thorax 1994, 49:531-532.
31. Koyama H, Geddes DM: Erythromycin and diffuse panbronchiolitis. Thorax 1997, 52:915-918.
32. Jaffe A, Bush A: Anti-inflammatory effects of macrolides in lung disease. Pediatr Pulmonol 2001, 31:464-473.
33. Pradal U, Delmarco A, Morganti M, Cipolli M, Mini E, Cazzola G: Long-term azithromycin in cystic fibrosis: another possible mechanism of action? J Chemother 2005, 17:393-400.
34. Barker PM, Gillie DJ, Schechter MS, Rubin BK: Effect of macrolides on in vivo transport across cystic fibrosis nasal epithelium. Am J Respir Crit Care Med 2005, 1714:868-871.
35. Equi AC, Davies JC, Painter H, Hyde S, Bush A, Geddes DM, Alton EW: Exploring the mechanisms of macrolides in cystic fibrosis. Respir Med 2006, 100:687-697.
36. Snouwaert JN, Brigman KK, Latour AM, Malouf NN, Boucher RC, Smithies O, Koller BH: An animal model for cystic fibrosis made by gene targeting. Science 1992, 257:1083-1088.
37. Dorin JR, Dickinson P, Alton EW, Smith SN, Geddes DM, Stevenson BJ: Cystic fibrosis in the mouse by targeted insertional mutagenesis. Nature 1992, 359:211-215.
38. Delaney SJ, Alton EW, Smith SN, Lunn DP, Farley R, Lovelock PK, Thomson SA, Hume DA, Lamb D, Porteus DJ, Dorin JR, Wainwright BJ: Cystic fibrosis mice carrying the missense mutation G551D replicate human genotype-phenotype correlations. EMBO J 1996, 15:955-963.
39. Colledge WH, Abelia BS, Southern KW, Ratcliff R, Jiang C, Cheng SH, MacVinish LJ, Anderson JR, Cuthbert AW, Evans MJ: Generation and characterization of a delta F508 cystic fibrosis mouse model. Nat Genet 1995, 10:445-452.
40. Zeiher BG, Eichwald E, Zabner J, Smith JJ, Puga AP, McCray PB Jr, Capecchi MR, Welsh MJ, Thomas KR: A mouse model for the delta F508 allele of cystic fibrosis. J Clin Invest 1995, 96:2051-2064.
41. Durie PR, Kent G, Phillips MJ, Ackerley CA: Characteristic multi-organ pathology of cystic fibrosis in a long-living cystic fibrosis transmembrane regulator knockout murine model. Am J Pathol 2004, 164:1481-1493.
42. Kent G, Iles R, Bear CE, Huan L-J, Griesenbach U, McKerlie C, Frndova H, Ackerley C, Gosselin D, Radzioch D, O'Brodovich H, Tsui LC, Buchwald M, Tanswell AK: Lung disease in mice with cystic fibrosis. J Clin Invest 1997, 100:3060-3069.
43. Zahm JM, Gaillard D, Dupuit F, Hinnarasky J, Porteous D, Dorin JR, Puchelle E: Early alterations in airway mucociliary clearence and inflammation of the lamina propria in CF mice. Am J Physiol 1997, 272:C853-859.
44. 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 1997, 100:2810-2815.
45. Scholte BJ, Davidson DJ, Wilke M, De Jonge HR: Animal models of cystic fibrosis. J Cyst Fibros 2004, 3:183-190.
46. Grubb BR, Boucher RC: Pathophysiology of gene-targeted mouse models for cystic fibrosis. Physiol Rev 1999, 79:S193-S214.
47. van Heeckeren A, Schluchter MD, Xue W, Davis PB: Response to acute lung infection with mucoid Pseudomonas aeruginosa in cystic fibrosis mice. Am J Respir Crit Care Med 2006, 173:288-296.
48. Schroeder T, Reiniger N, Meluleni G, Grout M, Coleman FT, Pier GB: Transgenic cystic fibrosis mice exhibit reduced early clearence of Pseudomonas aeruginosa from the respiratory tract. J Immunol 2001, 166:7410-7418.
49. Coleman FT, Mueschenborn S, Meluleni G, Ray C, Carey VJ, Vargas SO, Canon CL, Ausubel FM, Pier GB: Hypersusceptibility of cystic fibrosis mice to chronic pseudomonas aeruginosa oropharyngeal colonization and lung infection. Proc Natl Acad Sci USA 2003, 100:1949-1954.
50. Yu H, Nasr SZ, Deretic V: Innate lung defenses and compromised Pseudomonas aeruginosa clearance in the malnourished mouse model of respiratory infections in cystic fibrosis. Infect Immun 2000, 68:2142-2147.
51. van Heeckeren AM, Schluchter M, Xue L, Alvarez J, Freedman S, St George J, Davis PB: Nutritional effects on host response to lung infections with mucoid Paseudomonas aeruginosa in mice. Infect Immun 2004, 72:1479-1489.
52. Khan TZ, Wagener JS, Bost T, Martinez J, Accurso FJ, Riches DW: Early pulmonary inflammation in infants with cystic fibrosis. Am J Respir Crit Care Med 1995, 151:1075-1082.
53. Balough KM, McCubbin M, Weinberger M, Smits W, Ahrens R, Fick R: The relationship between infection and inflammation in the early stages of lung disease from cystic fibrosis. Pediatr Pulmonol 1995, 20:63-70.
54. Noah TL, Black HR, Cheng PW, Wood RE, Leigh MW: Nasal and bronchoalveolar lavage fluid cytokines in early cystic fibrosis. J Infect Dis 1997, 175:638-647.
55. Tirouvanziam R, de Bentzmann S, Hubeau C, Hinnrasky J, Jacquot J, Péault B, Puchelle E: Inflammation and infection in naive human cystic fibrosis airway grafts. Am J Respir Cell Mol Biol 2000, 23:121-127.
56. Armstrong DS, Hook SM, Jamsen KM, Nixon GM, Carzino R, Carlin JB, Robertson CF, Grimwood K: Lower airway inflammation in infants with cystic fibrosis detected by newborn screening. Pediatr Pulmonol 2005, 40:500-510.
57. Konstan MW, Hilliard KA, Norvell TM, Berger M: Bronchoalveolar lavage findings in cystic fibrosis patients with stable, clinically mild lung disease suggest ongoing infection and inflammation. Am J Respir Crit Care Med 1994, 150:448-454.
58. Armstrong DS, Grimwood K, Carzino R, Carlin JB, Olinsky A, Phelan PD: Lower respiratory tract infection and inflammation in infants with newly diagnosed cystic fibrosis. BMJ 1995, 310:1571-1572.
59. Bonfield TL, Konstan MW, Berger M: Altered respiratory epithelial cell cytokine production in cystic fibrosis. J Allerg Clin Immunol 1999, 104:72-78.
60. Tabary O, Zahm JM, Hinnrasky J, Couétil JP, Cornillet P, Guenounou, Gaillard D, Puchelle E, Jacquot J: Selective up-regulation of chemokine IL-8 expression in cystic fibrosis bronchial gland cells in vivo and in vitro. Am J Pathol 1998, 153:921-930.
61. Kammouni W, Figarella C, Marchand S, Merten M: Altered cytokine production by cystic fibrosis tracheal gland serous cells. Infect Immun 1997, 65:5176-5183.
62. Corvol H, Fitting C, Chadelat K, Jacquot J, Tabary O, Boule M, Cavaillon JM, Clement A: Distinct cytokine production by lung and blood neutrophils from children with cystic fibrosis. Am J Physiol Lung Cell Mol Physiol 2003, 284:L997-1003.
63. Matheson NR, Wong PS, Travis J: Enzymatic inactivation of human alpha-1-antitripsin inhibitor by neutrophil myeloperoxidase. Biochem Biophys Res Commun 1979, 88:402-409.
64. Clark RA, Stone PJ, Hag AE, Calore JD, Franzblau C: Myeloperoxydase-catalysed inactivation of a1-proteinase inhibitor by human neutrophils. J Biol Chem 1981, 256:3348-3353.
65. Heinecke JW, Li W, Francis GA, Goldstein JA: Tyrosyl radical generated by myeloperoxidase catalyzes the oxidative crosslinking of proteins. J Clin Invest 1993, 91:2866-2872.
66. Garner HP, Phillips JR, Herron JG, Severson SJ, Mila CE, Regelman WE: Peroxidase activity within circulating neutrophils correlates with pulmonary phenotype in cystic fibrosis. J Lab Clin Med 2004, 144:127-133.
67. Koller DY, Gotz M, Wojnarowski C, Eichler I: Relationship between disease severity and inflammatory markers in cystic fibrosis. Arch Dis Child 1996, 75:498-501.
68. Johnson LG, Vanhook MK, Coyne CB, Haykal-Coates N, Gavett SH: Safety and efficiency of modulating paracellular permeability to enhance airway epithelial gene transfer in vivo. Hum Gene Ther 2003, 14:729-747.
69. Ferretti S, Bonneau O, Dubois G, Jones CE, Trifilieff A: IL-17, produced by lymphocytes and neutrophils, is necessary for lipopolysaccharide-induced airway neutrophilia: IL-15 as a possible trigger. J Immunol 2003, 170:2106-2112.
70. Freedman SD, Weinstein D, Blanco PG, Martinez-Clark P, Urman S, Zaman M, Morrow JD, Alvarez JG: Characterization of LPSinduced lung inflammation in cftr-/- mice and the effect of docosahexaenoic acid. J Appl Physiol 2002, 92:2169-2176.
71. Bonfield TL, Panuska JR, Konstan MW, Hilliard KA, Hilliard JB, Ghnaim H, Berger M: Inflammatory cytokines in cystic fibrosis lungs. Am J Respir Crit Care Med 1995, 152:2111-2118.
72. Bonfield TL, Konstan MW, Burfeind P, Panuska JR, Hilliard JB, Berger M: Normal bronchial epithelial cells constitutively produce the anti-inflammatory cytokine interleukin-10, which is downregulated in cystic fibrosis. Am J Respir Cell Mol Biol 1995, 13:257-261.
73. Saadane A, Soltys J, Berger M: Role of IL-10 deficiency in excessive nuclear factor-kppaB activation and lung inflammation in cystic fibrosis transmembrane conductance regulator knockout mice. J Allergy Clin Immunol 2005, 115:405-411.
74. Chmiel JF, Konstan MW, Knesebeck JE, Hilliard JB, Bonfield TL, Dawson DV, Berger M: IL-10 attenuates excessive inflammation in chronic Pseudomonas infection in mice. Am J Respir Crit Care Med 1999, 160:2040-2047.
75. Chmiel JF, Konstan MW, Saadane A, Krenicky JE, Kirchner HL, Berger M: Prolonged inflammatory response to acute Pseudomonas challenge in interleukin-10 knockout mice. Am J Respir Crit Care Med 2002, 165:1176-1181.
76. Saadane A, Soltys J, Berger M: Role of IL-10 deficiency in excessive nuclear factor-kappaB activation and lung inflammation in cystic fibrosis transmembrane conductance regulator knockout mice. J Allergy Clin Immunol 2005, 115:405-411.
77. Tabary O, Escotte S, Couétil JP, Hubert D, Dusser D, Puchelle E, Jacquot J: High susceptibility for cystic fibrosis human airway gland cells to produce IL-8 through the I.B kinase alpha pathway in response to extracellular NaCl content. J Immunol 2000, 164:3377-3384.
78. Barnes PJ, Karin M: Nuclear factor-kappaB: a pivotal transcription factor in chronic inflammatory diseases. N Engl J Med 1997, 336:1066-1071.
79. Wright JG, Christman JW: The role of nuclear factor kappa B in the pathogenesis of pulmonary diseases: implications for therapy. Am J Respir Med 2003, 2:211-219.
80. Beringer P, Huynh KM, Kriengkauykiat J, Bi L, Hoem N, Louie S, Han E, Nguyen T, Hsu D, Rao PA, Shapiro B, Gill M: Absolute bioavailability and intracellular pharmacokinetics of azithromycin in patients with cystic fibrosis. Antimicrob Agents Chemother 2005, 49:5013-5017.
81. Everard ML, Sly P, Brenan S, Ryan G: Macrolide antibiotics in diffuse panbronchiolitis and in cystic fibrosis. Eur Respir J 1997, 10:2926.
82. Tsai WC, Rodriguez ML, Young KS, Deng JC, Thannickal VJ, Tateda K, Hershenson MB, Standiford TJ: Azithromycin blocks neutrophil recruitment in Pseudomonas endobronchial infection. Am J Respir Crit Care Med 2004, 170:1331-1339.
83. Greenberger MJ, Strieter RM, Kunkel SL, Danforth JM, Goodman JM, Standiford : Neutralization of IL-10 increases survival in a murine model of Klebsiella pneumonia. J Immunol 1995, 155:722-729.
84. van der Poll T, Marchant A Keogh CV, Goldman M, Lowry SF: Interleukin-10 impairs host defense in murine pneumococcal pneumonia. J infect Dis 1996, 174:994-1000.