Azithromycin increases chloride efflux from cystic fibrosis airway epithelial cells

Experimental Lung Research

Volumn 35, Issue 3, 2009, Pages 210-221

  Oliynyk, Igor ^a,b,f   Varelogianni, Georgia ^a   Schalling, Martin ^c,d   Asplund, Monika Stenkvist ^e   Roomans, Godfried M ^a   Johannesson, Marie ^e  

^a UPPSALA UNIVERSITY   (Sweden)

^b ÖREBRO UNIVERSITY   (Sweden)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^d Department of Molecular Medicine and Surgery ^*  (Sweden)

^e UPPSALA UNIVERSITY HOSPITAL   (Sweden)

^f ÖREBRO UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Azithromycin; Chloride transport; Cystic fibrosis; Cystic fibrosis transmembrane conductance regulator; Lung function; Multidrug resistance

Indexed keywords

AZITHROMYCIN; AZITROMAX; BLOCKING AGENT; CHLORIDE CHANNEL; CHLORIDE CHANNEL BLOCKING AGENT; CHLORIDE ION; GADOLINIUM CHLORIDE; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN; THIAZOLIDONE; TRANSMEMBRANE CONDUCTANCE REGULATOR; UNCLASSIFIED DRUG; CHLORIDE;

ADULT; ARTICLE; CHLORIDE TRANSPORT; CLINICAL ARTICLE; COMPARATIVE STUDY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYSTIC FIBROSIS; DISEASE EXACERBATION; DOSE RESPONSE; EPITHELIUM CELL; FEMALE; FORCED EXPIRATORY VOLUME; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN SITU HYBRIDIZATION; INHIBITION KINETICS; MALE; NASAL BIOPSY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY EPITHELIUM; TREATMENT DURATION; UPREGULATION; VITAL CAPACITY; CASE CONTROL STUDY; CELL LINE; CLINICAL TRIAL; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; ION TRANSPORT; LUNG FUNCTION TEST; METABOLISM; PATHOLOGY; RESPIRATORY SYSTEM; TREATMENT OUTCOME;

AZITHROMYCIN; CASE-CONTROL STUDIES; CELL LINE; CHLORIDE CHANNELS; CHLORIDES; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DOSE-RESPONSE RELATIONSHIP, DRUG; EPITHELIAL CELLS; FEMALE; HUMANS; ION TRANSPORT; MALE; RESPIRATORY FUNCTION TESTS; RESPIRATORY SYSTEM; RNA, MESSENGER; TREATMENT OUTCOME; YOUNG ADULT;

EID: 67149144260     PISSN: 01902148     EISSN: 15210499     Source Type: Journal    
DOI: 10.1080/01902140802534967     Document Type: Article

References (42)

1. Tarran R, Button B, Picher M, Paradiso AM, Ribeiro CM, Lazarowski ER, Zhang L, Collins PL, Pickles RJ, Fredberg JJ, Boucher RC: Normal and cystic fibrosis airway surface liquid homeostasis. The effects of phasic shear stress and viral infections. J Biol Chem. 2005;280:35751-35759.
2. Clunes MT, Boucher RC: Cystic fibrosis: the mechanisms of pathogenesis of an inherited lung disorder. Drug Discov Today Dis Mech. 2007;4:63-72.
3. Wang X, Kim J, McWilliams R, Cutting GR: Increased prevalence of chronic rhinosinusitis in carriers of a cystic fibrosis mutation. Arch Otolaryngol Head Neck Surg. 2005;131:237-240.
4. Saiman L: The use of macrolide antibiotics in patients with cystic fibrosis. Curr Opin Pulm Med. 2004;10:515-523.
5. Southern KW, Barker PM: Azithromycin for cystic fibrosis. Eur Respir J. 2004;24:834-838.
6. Amsden GW: Anti-inflammatory effects of macrolides - an underappreciated benefit in the treatment of community-acquired respiratory tract infections and chronic inflammatory pulmonary conditions? J Antimicrob Chemother. 2005;55:10-21.
7. Labro MT, Abdelghaffar H: Immunomodulation by macrolide antibiotics. J Chemother. 2001;13:3-8.
8. Asgrimsson V, Gudjonsson T, Gudmundsson GH, Baldursson O: Novel effects of azithromycin on tight junction proteins in human airway epithelia. Antimicrob Agents Chemother. 2006;50:1805-1812.
9. Labro MT, Babin-Chevaye C, Mergey M: Accumulation of azithromycin and roxithromycin in tra-cheal epithelial fetal cell lines expressing wild type or mutated cystic fibrosis transmembrane conductance regulator protein (CFTR). J Chemother. 2005;17:385-392.
10. Gant TW, O'Connor CK, Corbitt R, Thorgeirsson U, Thorgeirsson SS: In vivo induction of liver P-glycoprotein expression by xenobiotics in monkeys. Toxicol Appl Pharmacol. 1995;133:269-276.
11. Ambudkar SV, Dey S, Hrycyna CA, Ramachandra M, Pastan I, Gottesman MM: Biochemical, cellular, and pharmacological aspects of the multidrug transporter. Annu Rev Pharmacol Toxicol. 1999;39:361-398.
12. Klein I, Sarkadi B, Varadi A: An inventory of the human ABC proteins. Biochim Biophys Acta. 1999;1461:237-262.
13. Sarkadi B, Homolya L, Szakacs G, Varadi A: Human multidrug resistance ABCB and ABCG transporters: participation in a chemoimmunity defense system. Physiol Rev. 2006;86:1179-1236.
14. Lallemand JY, Stoven V, Annereau JP, Boucher J, Blanquet S, Barthe J, Lenoir G: Induction by anti-tumoral drugs of proteins that functionally complement CFTR: a novel therapy for cystic fibrosis? Lancet. 1997;350:711-712.
15. Barker PM, Gillie DJ, Schechter MS, Rubin BK: Effect of macrolides on in vivo ion transport across cystic fibrosis nasal epithelium. Am J Respir Crit Care Med. 2005;171:868-871.
16. 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.
17. 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.
18. Munkonge F, Alton EW, Andersson C, Davidson H, Dragomir A, Edelman A, Farley R, Hjelte L, McLachlan G, Stern M, Roomans GM: Measurement of halide efflux from cultured and primary airway epithelial cells using fluorescence indicators. J Cyst Fibros. 2004;3(Suppl 2):171-176.
19. Ma T, Thiagarajah JR, Yang H, Sonawane ND, Folli C, Galietta LJ, Verkman AS: Thiazolidinone CFTR inhibitor identified by high-throughput screening blocks cholera toxin-induced intestinal fluid secretion. J Clin Invest. 2002;110:1651-1658.
20. 2+ entry mechanism in rat A7r5 smooth muscle cells stimulated with low concentrations of vasopressin. J Physiol. 1999;517( Pt 1):121-134.
21. Jentsch TJ, Stein V, Weinreich F, Zdebik AA: Molecular structure and physiological function of chloride channels. Physiol Rev. 2002;82:503-568.
22. Schalling M, Franco-Cereceda A, Hemsen A, Dagerlind A, Seroogy K, Persson H, Hokfelt T, Lund-berg JM: Neuropeptide Y and catecholamine synthesizing enzymes and their mRNAs in rat sympathetic neurons and adrenal glands: studies on expression, synthesis and axonal transport after pharmacological and experimental manipulations using hybridization techniques and radioim-munoassay. Neuroscience. 1991;41:753-766.
23. Schalling M: In situ hybridisation and immunohistochemical methods in study of regulatory molecules. Methods Neurosci. 1992;1:231-255.
24. Hudson VM: New insights into the pathogenesis of cystic fibrosis: pivotal role of glutathione system dysfunction and implications for therapy. Treat Respir Med. 2004;3:353-363.
25. Wang X, Venable J, LaPointe P, Hutt DM, Koulov AV, Coppinger J, Gurkan C, Kellner W, Matteson J, Plutner H, Riordan JR, Kelly JW, Yates JR 3rd, Balch WE: Hsp90 cochaperone Aha1 downregulation rescues misfolding of CFTR in cystic fibrosis. Cell. 2006;127:803-815.
26. Tateda K, Ishii Y, Matsumoto T, Kobayashi T, Miyazaki S, Yamaguchi K: Potential of macrolide antibiotics to inhibit protein synthesis of Pseudomonas aeruginosa: suppression of virulence factors and stress response. J Infect Chemother. 2000;6:1-7.
27. Berquand A, Fa N, Dufrene YF, Mingeot-Leclercq MP: Interaction of the macrolide antibiotic azithromycin with lipid bilayers: effect on membrane organization, fluidity, and permeability. Pharm Res. 2005;22:465-475.
28. 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 the outer membrane. Antimicrob Agents Chemother. 2005;49:1377-1380.
29. Berquand A, Mingeot-Leclercq MP, Dufrene YF: Real-time imaging of drug-membrane interactions by atomic force microscopy. Biochim Biophys Acta. 2004;1664:198-205.
30. Fa N, Lins L, Courtoy PJ, Dufrene Y, Van Der Smissen P, Brasseur R, Tyteca D, Mingeot-Leclercq MP: Decrease of elastic moduli of DOPC bilayers induced by a macrolide antibiotic, azithromycin. Biochim Biophys Acta. 2007;1768:1830-1838.
31. Kerem E: Pharmacologic therapy for stop mutations: how much CFTR activity is enough? Curr Opin Pulm Med. 2004;10:547-552.
32. Saiman L, Mayer-Hamblett N, Campbell P, Marshall BC: Heterogeneity of treatment response to azithromycin in patients with cystic fibrosis. Am J Respir Crit Care Med. 2005;172:1008-1012.
33. Wolter J, Seeney S, Bell S, Bowler S, Masel P, McCormack J: Effect of long term treatment with azithromycin on disease parameters in cystic fibrosis: a randomised trial. Thorax. 2002;57:212-216.
34. Pirzada OM, McGaw J, Taylor CJ, Everard ML: Improved lung function and body mass index associated with long-term use of Macrolide antibiotics. J Cyst Fibros. 2003;2:69-71.
35. Hansen CR, Pressler T, Koch C, Hoiby N: Long-term azitromycin treatment of cystic fibrosis patients with chronic Pseudomonas aeruginosa infection; an observational cohort study. J Cyst Fibros. 2005;4:35-40.
36. Cigana C, Nicolis E, Pasetto M, Assael BM, Melotti P: Effects of azithromycin on the expression of ATP binding cassette transporters in epithelial cells from the airways of cystic fibrosis patients. J Chemother. 2007;19:643-649.
37. Gillis RJ, Iglewski BH: Azithromycin retards Pseudomonas aeruginosa biofilm formation. J Clin Mi-crobiol. 2004;42:5842-5845.
38. Clement A, Tamalet A, Leroux E, Ravilly S, Fauroux B, Jais JP: Long term effects of azithromycin in patients with cystic fibrosis: a double blind, placebo controlled trial. Thorax. 2006;61:895-902.
39. Culic O, Erakovic V, Parnham MJ: Anti-inflammatory effects of macrolide antibiotics. Eur J Pharmacol. 2001;429:209-229.
40. Culic O, Erakovic V, Cepelak I, Barisic K, Brajsa K, Ferencic Z, Galovic R, Glojnaric I, Manojlovic Z, Munic V, Novak-Mircetic R, Pavicic-Beljak V, Sucic M, Veljaca M, Zanic-Grubisic T, Parnham MJ: Azithromycin modulates neutrophil function and circulating inflammatory mediators in healthy human subjects. Eur J Pharmacol. 2002;450:277-289.
41. Legssyer R, Huaux F, Lebacq J, Delos M, Marbaix E, Lebecque P, Lison D, Scholte BJ, Wallemacq P, Leal T: Azithromycin reduces spontaneous and induced inflammation in DeltaF508 cystic fibrosis mice. Respir Res. 2006;7:134.
42. Daenas C, Hatziefthimiou AA, Gourgoulianis KI, Molyvdas PA: Azithromycin has a direct relaxant effect on precontracted airway smooth muscle. Eur J Pharmacol. 2006;553:280-287.