(R)-albuterol elicits antiinflammatory effects in human airway epithelial cells via iNOS

American Journal of Respiratory Cell and Molecular Biology

Volumn 34, Issue 1, 2006, Pages 119-127

  Chorley, Brian N ^b   Li, Yuehua ^b   Fang, Shijing ^b   Park, Jin Ah ^b   Adler, Kenneth B ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b NONE

Author keywords

Albuterol; Asthma; Cytokines; Epithelium; Inducible nitric oxide synthase

Indexed keywords

3 ISOPROPYLAMINO 1 (7 METHYL 4 INDANYLOXY) 2 BUTANOL; BETA 2 ADRENERGIC RECEPTOR BLOCKING AGENT; BETA 2 ADRENERGIC RECEPTOR STIMULATING AGENT; CALPHOSTIN C; CYTOKINE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; ISOPROTEIN; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN KINASE C EPSILON; PROTEIN KINASE C INHIBITOR; PROTEIN KINASE INHIBITOR; ROTTLERIN; SALBUTAMOL; SMALL INTERFERING RNA;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; BETA ADRENERGIC STIMULATION; CATECHOLAMINE RELEASE; CELL TYPE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENANTIOMER; HUMAN; HUMAN CELL; MEDIATOR RELEASE; RACEMIC MIXTURE; REGULATORY MECHANISM; RESPIRATORY EPITHELIUM; STEADY STATE;

ADRENERGIC BETA-AGONISTS; ALBUTEROL; ANTI-INFLAMMATORY AGENTS; CELLS, CULTURED; EPITHELIAL CELLS; GENE SILENCING; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; INTERFERON TYPE II; INTERLEUKIN-1; ISOENZYMES; MOLECULAR CONFORMATION; NITRIC OXIDE SYNTHASE TYPE II; PROTEIN KINASE C; RECEPTORS, ADRENERGIC, BETA-2; RESPIRATORY MUCOSA; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 29944439722     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2005-0338OC     Document Type: Article

References (52)

1. Yanaura S, Imamura N, Misawa M. Effects of beta-adrenoceptor stimulants on the canine tracheal ciliated cells. Jpn J Pharmacol 1981;31:951-956.
2. Frohock JI, Wijkstrom-Frei C, Salathe M. Effects of albuterol enantiomers on ciliary beat frequency in ovine tracheal epithelial cells. J Appl Physiol 2002;92:2396-2402.
3. Knowles M, Murray G, Shallal J, Askin F, Ranga V, Gatzy J, Boucher R. Bioelectric properties and ion flow across excised human bronchi. J Appl Physiol 1984;56:868-877.
4. Spurzem JR, Gupta J, Veys T, Kneifl KR, Rennard SI, Wyatt TA. Activation of protein kinase A accelerates bovine bronchial epithelial cell migration. Am J Physiol Lung Cell Mol Physiol 2002;282:L1108-1116.
5. Farmer P, Pugin J. Beta-adrenergic agonists exert their "anti-inflammatory" effects in monocytic cells through the IkappaB/NF-kappaB pathway. Am J Physiol Lung Cell Mol Physiol 2000;279:L675-L682.
6. Reid DW, Ward C, Wang N, Zheng L, Bish R, Orsida B, Walters EH. Possible anti-inflammatory effect of salmeterol against interleukin-8 and neutrophil activation in asthma in vivo. Eur Respir J 2003;21:994-999.
7. Hallsworth MP, Twort CH, Lee TH, Hirst SJ. beta(2)-adrenoceptor agonists inhibit release of eosinophil-activating cytokines from human airway smooth muscle cells. Br J Pharmacol 2001;132:729-741.
8. Oddera S, Silvestri M, Lantero S, Sacco O, Rossi GA. Downregulation of the expression of intercellular adhesion molecule (ICAM)-1 on bronchial epithelial cells by fenoterol, a beta2-adrenoceptor agonist. J Asthma 1998;35:401-408.
9. Korn SH, Jerre A, Brattsand R. Effects of formoterol and budesonide on GM-CSF and IL-8 secretion by triggered human bronchial epithelial cells. Eur Respir J 2001;17:1070-1077.
10. Guo FH, Erzurum SC. Characterization of inducible nitric oxide synthase expression in human airway epithelium. Environ Health Perspect 1998;106:1119-1124.
11. Liu HW, Anand A, Bloch K, Christiani D, Kradin R. Expression of inducible nitric oxide synthase by macrophages in rat lung. Am J Respir Crit Care Med 1997;156:223-228.
12. Robbins RA, Springall DR, Warren JB, Kwon OJ, Buttery LD, Wilson AJ, Adcock IM, Riveros-Moreno V, Moncada S, Polak J, et al. Inducible nitric oxide synthase is increased in murine lung epithelial cells by cytokine stimulation. Biochem Biophys Res Commun 1994;198:835-843.
13. Guo FH, Uetani K, Haque SJ, Williams BR, Dweik RA, Thunnissen FB, Calhoun W, Erzurum SC. Interferon gamma and interleukin 4 stimulate prolonged expression of inducible nitric oxide synthase in human airway epithelium through synthesis of soluble mediators. J Clin Invest 1997;100:829-838.
14. Warner RL, Paine R III, Christensen PJ, Marletta MA, Richards MK, Wilcoxen SE, Ward PA. Lung sources and cytokine requirements for in vivo expression of inducible nitric oxide synthase. Am J Respir Cell Mol Biol 1995;12:649-661.
15. Kenyon NJ, Gohil K, Last JA. Susceptibility to ovalbumin-induced airway inflammation and fibrosis in inducible nitric oxide synthetase-deficient mice: mechanisms and consequences. Toxicol Appl Pharmacol 2003;191:2-11.
16. Saleh D, Ernst P, Lim S, Barnes PJ, Giaid A. Increased formation of the potent oxidant peroxynitrite in the airways of asthmatic patients is associated with induction of nitric oxide synthase: effect of inhaled glucocorticoid. FASEB J 1998;12:929-937.
17. Muijsers RB, van der Veeken A, Habernickel J, Folkerts G, Postma DS, Nijkamp FP. Intra-luminal exposure of murine airways to peroxynitrite causes inflammation but not hyperresponsiveness. Inflamm Res 2002;51:33-37.
18. Eliseeva EV, Romanova NA, Maistrovskaya YV. Regulation of NO-producing function of the lungs with salmeterol. Bull Exp Biol Med 2001;132:709-712.
19. Tamaoki J, Kondo M, Takemura H, Chiyotani A, Yamawaki I, Konno K. Cyclic adenosine monophosphate-mediated release of nitric oxide from canine cultured tracheal epithelium. Am J Respir Crit Care Med 1995;152:1325-1330.
20. Sanders SP, Kim J, Connolly KR, Porter JD, Siekierski ES, Proud D. Nitric oxide inhibits rhinovirus-induced granulocyte macrophage colony-stimulating factor production in bronchial epithelial cells. Am J Respir Cell Mol Biol 2001;24:317-325.
21. Krunkosky TM, Fischer BM, Martin LD, Jones N, Akley NJ, Adler KB. Effects of TNF-α on expression of ICAM-1 in human airway epithelial cells in vitro: signaling pathways controlling surface and gene expression. Am J Respir Cell Mol Biol 2000;22:685-692.
22. Heid CA, Stevens J, Livak KJ, Williams PM. Real time quantitative PCR. Genome Res 1996;6:986-994.
23. Peirson SN, Butler JN, Foster RG. Experimental validation of novel and conventional approaches to quantitative real-time PCR data analysis. Nucleic Acids Res 2003;31:e73.
24. Chorley BN, Martin LD, Crews AR, Li Y, Adler KB. Differential effects of albuterol isomers on normal human bronchial epithelial cells in vitro. Am J Respir Crit Care Med 2003;167:A205. (Abstr.)
25. Choi SH, Shin KH, Kang SW, Chun YS, Chun BG. Guanosine 5′, 3′-cyclic monophosphate enhances lipopolysaccharide-induced nitric oxide synthase expression in mixed glial cell cultures of rat. Neurosci Lett 1999;276:29-32.
26. Dobashi K, Asayama K, Shirahata A. Differential effects of cyclic AMP on induction of nitric oxide synthase in 3T3-L1 cells and brown adipocytes. Free Radic Biol Med 2003;35:94-101.
27. Banan A, Farhadi A, Fields JZ, Zhang LJ, Shaikh M, Keshavarzian A. The delta-isoform of protein kinase C causes inducible nitric-oxide synthase and nitric oxide up-regulation: key mechanism for oxidant-induced carbonylation, nitration, and disassembly of the microtubule cytoskeleton and hyperpermeability of barrier of intestinal epithelia. J Pharmacol Exp Ther 2003;305:482-494.
28. Meja KK, Catley MC, Cambridge LM, Barnes PJ, Lum H, Newton R, Giembycz MA. Adenovirus-mediated delivery and expression of a cAMP-dependent protein kinase inhibitor gene to BEAS-2B epithelial cells abolishes the anti-inflammatory effects of rolipram, salbutamol, and prostaglandin E2: a comparison with H-89. J Pharmacol Exp Ther 2004;309:833-844.
29. Johnson M. Effects of beta2-agonists on resident and infiltrating inflammatory cells. J Allergy Clin Immunol 2002;110:S282-S290.
30. Butchers PR, Vardey CJ, Johnson M. Salmeterol: a potent and long-acting inhibitor of inflammatory mediator release from human lung. Br J Pharmacol 1991;104:672-676.
31. Park CS, Choi YS, Ki SY, Moon SH, Jeong SW, Uh ST, Kim YH. Granulocyte macrophage colony-stimulating factor is the main cytokine enhancing survival of eosinophils in asthmatic airways. Eur Respir J 1998;12:872-878.
32. Woolley KL, Adelroth E, Woolley MJ, Ellis R, Jordana M, O'Byrne PM. Effects of allergen challenge on eosinophils, eosinophil cationic protein, and granulocyte-macrophage colony-stimulating factor in mild asthma. Am J Respir Crit Care Med 1995;151:1915-1924.
33. Penn RB, Frielle T, McCullough JR, Aberg G, Benovic JL. Comparison of R-, S-, and RS-albuterol interaction with human beta 1- and beta 2-adrenergic receptors. Clin Rev Allergy Immunol 1996;14:37-45.
34. Templeton AG, Chapman ID, Chilvers ER, Morley J, Handley DA. Effects of S-salbutamol on human isolated bronchus. Pulm Pharmacol Ther 1998;11:1-6.
35. Cho SH, Hartleroad JY, Oh CK. (S)-albuterol increases the production of histamine and IL-4 in mast cells. Int Arch Allergy Immunol 2001;124:478-484.
36. Baramki D, Koester J, Anderson AJ, Borish L. Modulation of T-cell function by (R)- and (S)-isomers of albuterol: anti-inflammatory influences of (R)-isomers are negated in the presence of the (S)-isomer. J Allergy Clin Immunol 2002;109:449-454.
37. Ameredes BT, Gligonic WJ, Calhoun WJ. Enantiomers of beta-agonists exhibit differential effects in combination with dexamethasone on GM-CSF production in human airway smooth muscle cells. J Allergy Clin Immunol 2004;113:S190-S191.
38. Chorley BN, Adler KB. Inducible nitric oxide synthase/protein kinase G signaling pathway suppresses granulocyte macrophage colony stimulating factor transcription in normal human bronchial epithelial cells. Am J Respir Crit Care Med 2004;169:A241. (Abstr.)
39. Robbins RA, Barnes PJ, Springall DR, Warren JB, Kwon OJ, Buttery LD, Wilson AJ, Geller DA, Polak JM. Expression of inducible nitric oxide in human lung epithelial cells. Biochem Biophys Res Commun 1994;203:209-218.
40. Kwon S, Newcomb RL, George SC. Mechanisms of synergistic cytokine-induced nitric oxide production in human alveolar epithelial cells. Nitric Oxide 2001;5:534-546.
41. Xie QW, Kashiwabara Y, Nathan C. Role of transcription factor NF-kappa B/Rel in induction of nitric oxide synthase. J Biol Chem 1994;269:4705-4708.
42. Taylor BS, de Vera ME, Ganster RW, Wang Q, Shapiro RA, Morris SM Jr, Billiar TR, Geller DA. Multiple NF-kappaB enhancer elements regulate cytokine induction of the human inducible nitric oxide synthase gene. J Biol Chem 1998;273:15148-15156.
43. Daffern PJ, Jagels MA, Saad JJ, Fischer W, Hugli TE. Upper airway epithelial cells support eosinophil survival in vitro through production of GM-CSF and prostaglandin E2: regulation by glucocorticoids and TNF-alpha. Allergy Asthma Proc 1999;20:243-253.
44. Clarke DL, Belvisi MG, Catley MC, Yacoub MH, Newton R, Giembycz MA. Identification in human airway smooth muscle cells of the prostanoid receptor and signalling pathway through which PGE2 inhibits the release of GM-CSF. Br J Pharmacol 2004;141:1141-1150.
45. Jain B, Rubinstein I, Robbins RA, Leise KL, Sisson JH. Modulation of airway epithelial cell ciliary beat frequency by nitric oxide. Biochem Biophys Res Commun 1993;191:83-88.
46. Park J-A, He F, Martin LD, Li Y, Adler KB. Human neutrophil elastase induces hypersecretion of mucin from human bronchial epithelial cells in vitro via a PKCδ-mediated mechanism. Am J Pathol 2005;167:651-661.
47. Davies SP, Reddy H, Caivano M, Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 2000;351:95-105.
48. Carpenter L, Cordery D, Biden TJ. Protein kinase Cdelta activation by interleukin-1beta stabilizes inducible nitric-oxide synthase mRNA in pancreatic beta-cells. J Biol Chem 2001;276:5368-5374.
49. Liu WS, Heckman CA. The sevenfold way of PKC regulation. Cell Signal 1998;10:529-542.
50. Bergmann M, Barnes PJ, Newton R. Molecular regulation of granulocyte macrophage colony-stimulating factor in human lung epithelial cells by interleukin (IL)-1β, IL-4, and IL-13 involves both transcriptional and post-transcriptional mechanisms. Am J Respir Cell Mol Biol 2000;22:582-589.
51. Woolley KL, Adelroth E, Woolley MJ, Ellis R, Jordana M, O'Byrne PM. Granulocyte-macrophage colony-stimulating factor, eosinophils and eosinophil cationic protein in subjects with and without mild, stable, atopic asthma. Eur Respir J 1994;7:1576-1584.
52. Pedersen B, Dahl R, Venge P. The effect of salmeterol on the early and late phase reaction to bronchial hyperreactivity, blood eosinophils, and serum eosinophil cationic protein. Am Rev Respir Dis 1991;143:A649.