Mechanism of glucocorticoid protection of airway smooth muscle from proasthmatic effects of long-acting β2-adrenoceptor agonist exposure

Journal of Allergy and Clinical Immunology

Volumn 125, Issue 5, 2010, Pages 1020-1027

  Nino, Gustavo ^a   Hu, Aihua ^a   Grunstein, Judith S ^a   Grunstein, Michael M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

airway smooth muscle; Asthma; ERK1 2 phosphorylation; homologous 2 adrenergic receptor desensitization; MAPK phosphatase 1; phosphodiesterase; salmeterol; siRNA

Indexed keywords

BETA 2 ADRENERGIC RECEPTOR STIMULATING AGENT; DEXAMETHASONE; GLUCOCORTICOID; LONG ACTING DRUG; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 1; PHOSPHODIESTERASE IV; SALMETEROL;

AIRWAY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTHMA; CONTROLLED STUDY; DESENSITIZATION; DRUG ACTIVITY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; LONG TERM EXPOSURE; NONHUMAN; PHARMACODYNAMICS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE; UPREGULATION;

ADRENERGIC BETA-AGONISTS; ALBUTEROL; ANIMALS; ASTHMA; CELLS, CULTURED; DEXAMETHASONE; DUAL SPECIFICITY PHOSPHATASE 1; GLUCOCORTICOIDS; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASE 3; MUSCLE, SMOOTH; RABBITS; RESPIRATORY SYSTEM; UP-REGULATION;

EID: 77951665607     PISSN: 00916749     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jaci.2010.02.007     Document Type: Article

References (42)

1. Beasley R., Pearce N., Crane J., and Burgess C. Beta-agonists: what is the evidence that their use increases the risk of asthma morbidity and mortality?. J Allergy Clin Immunol 104 (1999) S18-S30
2. Cheung D., Timmers M.C., Zwinderman A.H., Bel E.H., Dijkman J.H., and Sterk P.J. Long-term effects of a long-acting beta 2-adrenoceptor agonist, salmeterol, on airway hyperresponsiveness in patients with mild asthma. N Engl J Med 327 (1992) 1198-1203
3. Nelson H.S., Weiss S.T., Bleecker E.R., Yancey S.W., and Dorinsky P.M. The Salmeterol Multicenter Asthma Research Trial: a comparison of usual pharmacotherapy for asthma or usual pharmacotherapy plus salmeterol. Chest 129 (2006) 15-26
4. Giembycz M.A., and Newton R. Beyond the dogma: novel beta2-adrenoceptor signalling in the airways. Eur Respir J 27 (2006) 1286-1306
5. Woolcock A., Lundback B., Ringdahl N., and Jaques L.A. Comparison of addition of salmeterol to inhaled steroids with doubling of the dose of inhaled steroids. Am J Respir Crit Care Med 153 (1996) 1481-1488
6. Pauwels R.A., Lofdahl C.G., Postma D.S., Tattersfield A.E., O'Byrne P., Barnes P.J., et al. Effect of inhaled formoterol and budesonide on exacerbations of asthma. N Engl J Med 337 (1997) 1405-1411
7. Kips J., O'Connor B., Inman M., Svensson K., Pauwels R.A., and O'Byrne P.M. A long-term study of the anti-inflammatory effect of low-dose budesonide plus formoterol versus high-dose budesonide in asthma. Am J Respir Crit Care Med 161 (2000) 996-1001
8. Bateman E., Nelson H., Bousquet J., Kral K., Sutton L., Ortega H., et al. Meta-analysis: effects of adding salmeterol to inhaled corticosteroids on serious asthma-related events. Ann Int Med 149 (2008) 33-42
9. Ni Chroinin M., Lasserson T.J., Greenstone I., and Ducharme F.M. Addition of long-acting beta-agonists to inhaled corticosteroids for chronic asthma in children. Cochrane Database Syst Rev 3 (2009) CD007949
10. Giembycz M.A., Kaur M., Leigh R., and Newton R. A Holy Grail of asthma management: toward understanding how long-acting beta(2)-adrenoceptor agonists enhance the clinical efficacy of inhaled corticosteroids. Br J Pharmacol 153 (2008) 1090-1104
11. Hauck R.W., Harth M., Schulz C., Prauer H., Bohm M., and Schomig A. Effects of β2-agonist- and dexamethasone-treatment on relaxation and regulation of β-adrenoceptors in human bronchi and lung tissue. Br J Pharmacol 121 (1997) 1523-1530
12. Cooper P.R., and Panettieri Jr. R.A. Steroids completely reverse albuterol-induced β2-adrenergic receptor tolerance in human small airways. J Allergy Clin Immunol 122 (2008) 734-740
13. Nino G., Hu A., Grunstein J.S., and Grunstein M.M. Mechanism regulating proasthmatic effects of prolonged homologous β2-adrenergic receptor desensitization in airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 297 (2009) L746-L757
14. Hu A., Nino G., Grunstein J.S., Fatma S., and Grunstein M.M. Prolonged heterologous β2-adrenoceptor desensitization promotes proasthmatic airway smooth muscle function via PKA/ERK1/2-mediated phosphodiesterase-4 induction. Am J Physiol Lung Cell Mol Physiol 294 (2008) L1055-L1067
15. Billington C.K., Le Jeune I.R., Young K.W., and Hall I.P. A major functional role for phosphodiesterase 4D5 in human airway smooth muscle cells. Am J Respir Cell Mol Biol 38 (2008) 1-7
16. Abraham S.M., and Clark A.R. Dual-specificity phosphatase 1: a critical regulator of innate immune responses. Biochem Soc Trans 34 (2006) 1018-1023
17. Issa R., Xie S., Khorasani N., Sukkar M., Adcock I.M., Lee K.Y., et al. Corticosteroid inhibition of growth-related oncogene protein-alpha via mitogen-activated kinase phosphatase-1 in airway smooth muscle cells. J Immunol 178 (2007) 7366-7375
18. Kang B.N., Jude J.A., Panettieri Jr. R.A., Walseth T.F., and Kannan M.S. Glucocorticoid regulation of CD38 expression in human airway smooth muscle cells: role of dual specificity phosphatase 1. Am J Physiol Lung Cell Mol Physiol 295 (2008) L186-L193
19. Beltman J., McCormick F., and Cook S.J. The selective protein kinase C inhibitor, Ro-31-8220, inhibits mitogen-activated protein kinase phosphatase-1 (MKP-1) expression, induces c-Jun expression, and activates Jun N-terminal kinase. J Biol Chem 271 (1996) 27018-27024
20. Penn R.B., Panettieri Jr. R.A., and Benovic J.L. Mechanisms of acute desensitization of the β2AR-adenylyl cyclase pathway in human airway smooth muscle. Am J Respir Cell Mol Biol 19 (1998) 338-348
21. Shore S.A., and Moore P.E. Regulation of β-adrenergic responses in airway smooth muscle. Respir Physiol Neurobiol 137 (2003) 179-195
22. Mak J.C., Hisada T., Salmon M., Barnes P.J., and Chung K.F. Glucocorticoids reverse IL-1β-induced impairment of β-adrenoceptor-mediated relaxation and up-regulation of G-protein-coupled receptor kinases. Br J Pharmacol 135 (2002) 987-996
23. Mehats C., Jin S.L., Wahlstrom J., Law E., Umetsu D.T., and Conti M. PDE4D plays a critical role in the control of airway smooth muscle contraction. FASEB J 17 (2003) 1831-1841
24. van Schalkwyk E., Strydom K., Williams Z., Venter L., Leichtl S., Schmid-Wirlitsch C., et al. Roflumilast, an oral, once-daily phosphodiesterase 4 inhibitor, attenuates allergen-induced asthmatic reactions. J Allergy Clin Immunol 116 (2005) 292-298
25. Hansen G., Jin S., Umetsu D.T., and Conti M. Absence of muscarinic cholinergic airway responses in mice deficient in the cyclic nucleotide phosphodiesterase PDE4D. Proc Natl Acad Sci U S A 97 (2000) 6751-6756
26. Kanehiro A., Ikemura T., Makela M.J., Lahn M., Joetham A., Dakhama A., et al. Inhibition of phosphodiesterase 4 attenuates airway hyperresponsiveness and airway inflammation in a model of secondary allergen challenge. Am J Respir Crit Care Med 163 (2001) 173-184
27. Tang H.F., Song Y.H., Chen J.C., Chen J.Q., and Wang P. Upregulation of phosphodiesterase-4 in the lung of allergic rats. Am J Respir Crit Care Med 171 (2005) 823-828
28. Sun J.G., Deng Y.M., Wu X., Tang H.F., Deng J.F., Chen J.Q., et al. Inhibition of phosphodiesterase activity, airway inflammation and hyperresponsiveness by PDE4 inhibitor and glucocorticoid in a murine model of allergic asthma. Life Sci 79 (2006) 2077-2085
29. Chapman R.W., House A., Jones H., Richard J., Celly C., Prelusky D., et al. Effect of inhaled roflumilast on the prevention and resolution of allergen-induced late phase airflow obstruction in Brown Norway rats. Eur J Pharmacol 571 (2007) 215-221
30. Hirst S.J., and Lee T.H. Airway smooth muscle as a target of glucocorticoid action in the treatment of asthma. Am J Respir Crit Care Med 158 (1998) S201-S206
31. Panettieri Jr. R.A. Effects of corticosteroids on structural cells in asthma and chronic obstructive pulmonary disease. Proc Am Thorac Soc 1 (2004) 231-234
32. Barnes P.J. Antiinfammatory action of glucocorticoids: molecular mechanisms. Clin Sci 94 (1998) 557-572
33. Hakonarson H., Halapi E., Whelan R., Gulcher J., Stefansson K., and Grunstein M.M. Association between IL-1β/TNF-α-induced glucocorticoid-sensitive changes in multiple gene expression and altered responsiveness in airway smooth muscle. Am J Respir Cell Mol Biol 6 (2001) 761-771
34. Noguchi T., Metz R., Chen L., Mattéi M.-G., Carrasco D., and Bravo R. Structure, mapping and expression of erp, a growth factor-inducible gene encoding a nontransmembrane protein tyrosine phosphase and effect of erp on cell growth. Mol Cell Biol 13 (1993) 5195-5205
35. Burgess J.K., Lee J.H., Ge Q., Ramsay E.E., Poniris M.H., Parmentier J., et al. Dual ERK and phosphatidylinositol 3-kinase pathways control airway smooth muscle proliferation: differences in asthma. J Cell Physiol 216 (2008) 673-679
36. Liu H., Palmer D., Jimmo S.L., Tilley D.G., Dunkerley H.A., Pang S.C., et al. Expression of phosphodiesterase 4D (PDE4D) is regulated by both the cyclic AMP-dependent protein kinase and mitogen-activated protein kinase signaling pathways: a potential mechanism allowing for the coordinated regulation of PDE4D activity and expression in cells. J Biol Chem 275 (2000) 26615-26624
37. Houslay M.D., and Baillie G.S. The role of ERK2 docking and phosphorylation of PDE4 cAMP phosphodiesterase isoforms in mediating cross-talk between the cAMP and ERK signalling pathways. Biochem Soc Trans 31 (2003) 1186-1190
38. Duan W., Chan J.H., Wong C.H., Leung B.P., and Wong W.S. Anti-inflammatory effects of mitogen-activated protein kinase kinase inhibitor U0126 in an asthma mouse model. J Immunol 172 (2004) 7053-7059
39. Ohnishi H., Takeda K., Domenico J., Lucas J.J., Miyahara N., Swasey C.H., et al. Mitogen-activated protein kinase/extracellular signal-regulated kinase 1/2-dependent pathways are essential for CD8+ T cell-mediated airway hyperresponsiveness and inflammation. J Allergy Clin Immunol 123 (2009) 249-257
40. Grunstein M.M., Veler H., Shan X., Larson J., Grunstein J.S., and Chuang S. Proasthmatic effects and mechanisms of action of the dust mite allergen, Der p 1, in airway smooth muscle. J Allergy Clin Immunol 116 (2005) 94-101
41. Shan X., Hu A., Veler H., Fatma S., Grunstein J.S., Chuang S., et al. Regulation of toll-like receptor 4-induced pro-asthmatic changes in airway smooth muscle function by opposing actions of ERK1/2 and p38 MAPK signaling. Am J Physiol Lung Cell Mol Physiol 291 (2006) L324-L333
42. Kassel O., Sancono A., Kratzschmar J., Kreft B., Stassen M., and Cato A.C. Glucocorticoids inhibit MAP kinase via increased expression and decreased degradation of MKP-1. EMBO J 20 (2001) 7108-7116