Azithromycin inhibits macrophage interleukin-1β production through inhibition of activator protein-1 in lipopolysaccharide-induced murine pulmonary neutrophilia

International Immunopharmacology

Volumn 11, Issue 4, 2011, Pages 424-434

  Bosnar, Martina ^a,b   Čužić, Snježana ^a,b   Bošnjak, Berislav ^a,c   Nujić, Krunoslav ^a,b   Ergović, Gabrijela ^a,b   Marjanović, Nikola ^a,b   Pašalić, Ivanka ^a,b   Hrvačić, Boška ^a,b   Polančec, Denis ^a,b   Glojnarić, Ines ^a,b   Haber, Vesna Eraković ^a,b  

^a GLAXOSMITHKLINE   (United Kingdom)

^b Galapagos Istraživački Centar Doo ^*  (Croatia)

^c Universitatsklinik fur Dermatologie   (Austria)

Author keywords

Activator protein 1; Azithromycin; Interleukin 1 ; Lipopolysaccharide induced pulmonary; neutrophilia

Indexed keywords

AZITHROMYCIN; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; TRANSCRIPTION FACTOR AP 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME LOCALIZATION; ENZYME REGULATION; IMMUNOHISTOCHEMISTRY; LUNG ALVEOLUS MACROPHAGE; LUNG HOMOGENATE; MALE; MOUSE; NEUTROPHILIA; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS INHIBITION;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; AZITHROMYCIN; BRONCHOALVEOLAR LAVAGE FLUID; CELL LINE; ENZYME-LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; LUNG; MACROPHAGES; MALE; MICE; MICE, INBRED BALB C; NEUTROPHIL INFILTRATION; NF-KAPPA B; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTOR AP-1;

EID: 79952739861     PISSN: 15675769     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.intimp.2010.12.010     Document Type: Article

References (49)

1. Whitman MS, Tunkel AR. Azithromycin and clarithromycin: overview and comparison with erythromycin. Infect Control Hosp Epidemiol 1992;13:357-68.
2. Zuckerman JM, Qamar F, Bono BR. Macrolides, ketolides, and glycylcyclines: azithromycin, clarithromycin, telithromycin, tigecycline. Infect Dis Clin North Am 2009;23:997-1026.
3. Kudoh S, Azuma A, Yamamoto M, Izumi T, Ando M. Improvement of survival in patients with diffuse panbronchiolitis treated with low-dose erythromycin. Am J Respir Crit Care Med 1998;157:1829-32.
4. Crosbie PA, Woodhead MA. Long-term macrolide therapy in chronic inflammatory airway diseases. Eur Respir J 2009;33:171-81.
5. Culic O, Erakovic V, Parnham MJ. Anti-inflammatory effects of macrolide antibiotics. Eur J Pharmacol 2001;429:209-29. (Pubitemid 33043997)
6. Giamarellos-Bourboulis EJ. Macrolides beyond the conventional antimicrobials: a class of potent immunomodulators. Int J Antimicrob Agents 2008;31:12-20. (Pubitemid 350236720)
7. Murphy DM, Forrest IA, Curran D, Ward C. Macrolide antibiotics and the airway: antibiotic or non-antibiotic effects? Expert Opin Investig Drugs 2010;19:401-14.
8. Shinkai M, Henke MO, Rubin BK. Macrolide antibiotics as immunomodulatory medications: proposed mechanisms of action. Pharmacol Ther 2008;117:393-405.
9. Bosnar M, Bosnjak B, Cuzic S, Hrvacic B, Marjanovic N, Glojnaric I, et al. Azithromycin and clarithromycin inhibit lipopolysaccharide-induced murine pulmonary neutrophilia mainly through effects on macrophage-derived granulocyte- macrophage colony-stimulating factor and interleukin-1beta. J Pharmacol Exp Ther 2009;331:104-13.
10. Ivetic TV, Bosnjak B, Hrvacic B, Bosnar M, Marjanovic N, Ferencic Z, et al. Antiinflammatory activity of azithromycin attenuates the effects of lipopolysaccharide administration in mice. Eur J Pharmacol 2006;539:131-8. (Pubitemid 44208808)
11. Kadota J, Sakito O, Kohno S, Sawa H, Mukae H, Oda H, et al. A mechanism of erythromycin treatment in patients with diffuse panbronchiolitis. Am Rev Respir Dis 1993;147:153-9. (Pubitemid 23025932)
12. Leiva M, Ruiz-Bravo A, Jimenez-Valera M. Effects of telithromycin in in vitro and in vivo models of lipopolysaccharide-induced airway inflammation. Chest 2008;134: 20-9. (Pubitemid 352008759)
13. Ou XM, Feng YL, Wen FQ, Wang K, Yang J, Deng ZP, et al. Macrolides attenuate mucus hypersecretion in rat airways through inactivation of NF-kappaB. Respirology 2008;13:63-72.
14. Sanz MJ, Nabah YN, Cerda-Nicolas M, O'Connor JE, Issekutz AC, Cortijo J, et al. Erythromycin exerts in vivo anti-inflammatory activity downregulating cell adhesion molecule expression. Br J Pharmacol 2005;144:190-201. (Pubitemid 40216117)
15. Tamaoki J, Tagaya E, Yamawaki I, Sakai N, Nagai A, Konno K. Effect of erythromycin on endotoxin-induced microvascular leakage in the rat trachea and lungs. Am J Respir Crit Care Med 1995;151:1582-8.
16. Cigana C, Nicolis E, Pasetto M, Assael BM, Melotti P. Anti-inflammatory effects of azithromycin in cystic fibrosis airway epithelial cells. Biochem Biophys Res Commun 2006;350:977-82. (Pubitemid 44584188)
17. Ichiyama T, Nishikawa M, Yoshitomi T, Hasegawa S, Matsubara T, Hayashi T, et al. Clarithromycin inhibits NF-kappaB activation in human peripheral blood mononuclear cells and pulmonary epithelial cells. Antimicrob Agents Chemother 2001;45:44-7. (Pubitemid 32039091)
18. Kikuchi T, Hagiwara K, Honda Y, Gomi K, Kobayashi T, Takahashi H, et al. Clarithromycin suppresses lipopolysaccharide-induced interleukin-8 production by humanmonocytes through AP-1 and NF-kappa B transcription factors. J Antimicrob Chemother 2002;49:745-55. (Pubitemid 34537634)
19. Shinkai M, Foster GH, Rubin BK. Macrolide antibiotics modulate ERK phosphorylation and IL-8 and GM-CSF production by human bronchial epithelial cells. Am J Physiol Lung Cell Mol Physiol 2006;290:L75-85.
20. Barnes PJ, Stockley RA. COPD: current therapeutic interventions and future approaches. Eur Respir J 2005;25:1084-106. (Pubitemid 40823786)
21. Fitzgerald MF, Fox JC. Emerging trends in the therapy of COPD: novel antiinflammatory agents in clinical development. Drug Discov Today 2007;12: 479-86. (Pubitemid 46795591)
22. Dinarello CA. Biologic basis for interleukin-1 in disease. Blood 1996;87:2095-147. (Pubitemid 26086851)
23. Carroll TP, Greene CM, Taggart CC, McElvaney NG, O'Neill OJ. Interleukin-1, neutrophil elastase, and lipopolysaccharide: key pro-inflammatory stimuli regulating inflammation in cystic fibrosis. Curr Respir Med Rev 2005;1:43-67.
24. Chung KF. Cytokines in chronic obstructive pulmonary disease. Eur Respir J Suppl 2001;34:50s-9s.
25. Ekberg-Jansson A, Andersson B, Bake B, Boijsen M, Enanden I, Rosengren A, et al. Neutrophil-associated activation markers in healthy smokers relates to a fall in DL (CO) and to emphysematous changes on high resolution CT. Respir Med 2001;95: 363-73. (Pubitemid 32624481)
26. Ulich TR, Watson LR, Yin SM, Guo KZ, Wang P, Thang H, et al. The intratracheal administration of endotoxin and cytokines. I. Characterization of LPS-induced IL-1 and TNF mRNA expression and the LPS-, IL-1-, and TNF-induced inflammatory infiltrate. Am J Pathol 1991;138:1485-96.
27. Lappalainen U, Whitsett JA, Wert SE, Tichelaar JW, Bry K. Interleukin-1beta causes pulmonary inflammation, emphysema, and airway remodeling in the adult murine lung. Am J Respir Cell Mol Biol 2005;32:311-8. (Pubitemid 40478306)
28. Castro P, Legora-Machado A, Cardilo-Reis L, Valenca S, Porto LC, Walker C, et al. Inhibition of interleukin-1beta reduces mouse lung inflammation induced by exposure to cigarette smoke. Eur J Pharmacol 2004;498:279-86. (Pubitemid 39208090)
29. Churg A, Zhou S, Wang X, Wang R, Wright JL. The role of interleukin-1beta in murine cigarette smoke-induced emphysema and small airway remodeling. Am J Respir Cell Mol Biol 2009;40:482-90.
30. Elazar S, Gonen E, Livneh-Kol A, Rosenshine I, Shpigel NY. Neutrophil recruitment in endotoxin-induced murine mastitis is strictly dependent on mammary alveolar macrophages. Vet Res 2010;41:10.
31. Hodge S, Hodge G, Jersmann H, Matthews G, Ahern J, Holmes M, et al. Azithromycin improves macrophage phagocytic function and expression of mannose receptor in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2008;178:139-48. (Pubitemid 351957772)
32. Kadota J, Matsubara Y, Ishimatsu Y, Ashida M, Abe K, Shirai R, et al. Significance of IL-1beta and IL-1 receptor antagonist (IL-1Ra) in bronchoalveolar lavage fluid (BALF) in patients with diffuse panbronchiolitis (DPB). Clin Exp Immunol 1996;103: 461-6.
33. Sakito O, Kadota J, Kohno S, Abe K, Shirai R, Hara K. Interleukin 1 beta, tumor necrosis factor alpha, and interleukin 8 in bronchoalveolar lavage fluid of patients with diffuse panbronchiolitis: a potential mechanism of macrolide therapy. Respiration 1996;63:42-8. (Pubitemid 26039586)
34. Cogswell JP, Godlevski MM, Wisely GB, Clay WC, Leesnitzer LM, Ways JP, et al. NF-kappa B regulates IL-1 beta transcription through a consensus NF-kappa B binding site and a nonconsensus CRE-like site. J Immunol 1994;153:712-23.
35. Serkkola E, Hurme M. Synergism between protein-kinase C and cAMP-dependent pathways in the expression of the interleukin-1 beta gene is mediated via the activator-protein-1 (AP-1) enhancer activity. Eur J Biochem 1993;213:243-9. (Pubitemid 23106052)
36. Shirakawa F, Saito K, Bonagura CA, Galson DL, Fenton MJ, Webb AC, et al. The human prointerleukin 1 beta gene requires DNA sequences both proximal and distal to the transcription start site for tissue-specific induction. Mol Cell Biol 1993;13:1332-44. (Pubitemid 23068068)
37. Iles KE, Forman HJ. Macrophage signaling and respiratory burst. Immunol Res 2002;26:95-105. (Pubitemid 35177488)
38. Karin M. The regulation of AP-1 activity by mitogen-activated protein kinases. J Biol Chem 1995;270:16483-6.
39. Saperstein S, Huyck H, Kimball E, Johnston C, Finkelstein J, Pryhuber G. The effects of interleukin-1beta in tumor necrosis factor-alpha-induced acute pulmonary inflammation in mice. Mediat Inflamm 2009;2009:958658.
40. Murugan V, Peck MJ. Signal transduction pathways linking the activation of alveolar macrophages with the recruitment of neutrophils to lungs in chronic obstructive pulmonary disease. Exp Lung Res 2009;35:439-85.
41. Yamauchi K, Shibata Y, Kimura T, Abe S, Inoue S, Osaka D, et al. Azithromycin suppresses interleukin-12p40 expression in lipopolysaccharide and interferongamma stimulated macrophages. Int J Biol Sci 2009;5:667-78.
42. Ikegaya S, Inai K, Iwasaki H, Naiki H, Ueda T. Azithromycin reduces tumor necrosis factor-alpha production in lipopolysaccharide-stimulated THP-1 monocytic cells by modification of stress response and p38 MAPK pathway. J Chemother 2009;21: 396-402.
43. Cheung PS, Si EC, Hosseini K. Anti-inflammatory activity of azithromycin as measured by its NF-kappaB, inhibitory activity. Ocul Immunol Inflamm 2010;18: 32-7.
44. Aghai ZH, Kode A, Saslow JG, Nakhla T, Farhath S, Stahl GE, et al. Azithromycin suppresses activation of nuclear factor-kappa B and synthesis of pro-inflammatory cytokines in tracheal aspirate cells from premature infants. Pediatr Res 2007;62: 483-8. (Pubitemid 47476210)
45. Araki N, Yanagihara K, Morinaga Y, Yamada K, Nakamura S, Yamada Y, et al. Azithromycin inhibits nontypeable Haemophilus influenzae-induced MUC5AC expression and secretion via inhibition of activator protein-1 in human airway epithelial cells. Eur J Pharmacol 2010;644:209-14.
46. Morinaga Y, Yanagihara K, Miyashita N, Seki M, Izumikawa K, Kakeya H, et al. Azithromycin, clarithromycin and telithromycin inhibit MUC5AC induction by Chlamydophila pneumoniae in airway epithelial cells. Pulm Pharmacol Ther 2009;22: 580-6.
47. Blau H, Klein K, Shalit I, Halperin D, Fabian I. Moxifloxacin but not ciprofloxacin or azithromycin selectively inhibits IL-8, IL-6, ERK1/2, JNK, and NF-kappaB activation in a cystic fibrosis epithelial cell line. Am J Physiol Lung Cell Mol Physiol 2007;292: L343-52.
48. Cigana C, Assael BM, Melotti P. Azithromycin selectively reduces tumor necrosis factor alpha levels in cystic fibrosis airway epithelial cells. Antimicrob Agents Chemother 2007;51:975-81. (Pubitemid 46355283)
49. Suzaki H, Asano K, Ohki S, Kanai K, Mizutani T, Hisamitsu T. Suppressive activity of a macrolide antibiotic, roxithromycin, on pro-inflammatory cytokine production in vitro and in vivo. Mediat Inflamm 1999;8:199-204. (Pubitemid 30019329)