β-agonist-mediated relaxation of airway smooth muscle is protein kinase A-dependent

Journal of Biological Chemistry

Volumn 289, Issue 33, 2014, Pages 23065-23074

  Morgan, Sarah J ^a   Deshpande, Deepak A ^a   Tiegs, Brian C ^a   Misior, Anna M ^b   Yan, Huandong ^a   Hershfeld, Alena V ^a   Rich, Thomas C ^c   Panettieri, Reynold A ^d   An, Steven S ^e   Penn, Raymond B ^a,f  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b WAKE FOREST UNIVERSITY HEALTH SCIENCES   (United States)

^c UNIVERSITY OF SOUTH ALABAMA COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^f THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEINS;

AIRWAY SMOOTH MUSCLES; BRONCHOCONSTRICTION; EXCHANGE PROTEINS; INHIBITORY EFFECT; INTRACELLULAR CALCIUM; ISOPROTERENOL; PROTEIN KINASE; SMOOTH MUSCLES;

MUSCLE;

BETA ADRENERGIC RECEPTOR STIMULATING AGENT; CALCIUM; CELL PROTEIN; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; MLC 20 PROTEIN; PROTEIN KINASE INHIBITOR; REVAB PROTEIN; UNCLASSIFIED DRUG; GUANINE NUCLEOTIDE EXCHANGE FACTOR; ISOPRENALINE; RAPGEF3 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRONCHUS MUSCLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE CONTRACTION; SMOOTH MUSCLE RELAXATION; CELL LINE; CYTOLOGY; DRUG EFFECTS; METABOLISM; MUSCLE RELAXATION; RESPIRATORY SYSTEM; SMOOTH MUSCLE;

ADRENERGIC BETA-AGONISTS; CELL LINE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; ISOPROTERENOL; MUSCLE RELAXATION; MUSCLE, SMOOTH; RESPIRATORY SYSTEM;

EID: 84905987213     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.557652     Document Type: Article

References (47)

1. Newnham, D. M., McDevitt, D. G., and Lipworth, B. J. (1994) Bronchodilator subsensitivity after chronic dosing with eformoterol in patients with asthma. The American Journal of Medicine 97, 29-37 (Pubitemid 24223631)
2. Newnham, D. M., Grove, A., McDevitt, D. G., and Lipworth, B. J. (1995) Subsensitivity of bronchodilator and systemic β 2 adrenoceptor responses after regular twice daily treatment with eformoterol dry powder in asthmatic patients. Thorax 50, 497-504
3. Grove, A., and Lipworth, B. J. (1995) Bronchodilator subsensitivity to salbutamol after twice daily salmeterol in asthmatic patients. Lancet 346, 201-206
4. Sears, M. R. (2002) Adverse effects of b-agonists. J. Allergy Clin. Immunol. 110, S322-S328
5. Salpeter, S. R., Buckley, N. S., Ormiston, T. M., and Salpeter, E. E. (2006) Meta-analysis: effect of long-acting b-Agonists on severe asthma exacerbations and asthma-related deaths. Annals Intern. Med. 144, 904-912 (Pubitemid 46768131)
6. Deshpande, D. A., and Penn, R. B. (2006) Targeting G protein-coupled receptor signaling in asthma. Cell Signal. 18, 2105-2120 (Pubitemid 44636173)
7. Stolley, P. D., and Schinnar, R. (1978) Association between asthma mortality and isoproterenol aerosols: a review. Prev. Med. 7, 519-538 (Pubitemid 9113632)
8. Spitzer, W. O., Suissa, S., Ernst, P., Horwitz, R. I., Habbick, B., Cockcroft, D., Boivin, J. F., McNutt, M., Buist, A. S., and Rebuck, A. S. (1992) The use of b-agonists and the risk of death and near death from asthma. N. Engl. J. Med. 326, 501-506
9. Pearce, N., Beasley, R., Crane, J., Burgess, C., and Jackson, R. (1995) End of the New Zealand asthma mortality epidemic. Lancet 345, 41-44
10. Nelson, H. S., Weiss, S. T., Bleecker, E. R., Yancey, S. W., and Dorinsky, P. M. (2006) The salmeterol multicenter asthma research trial: a comparison of usual pharmacotherapy for asthma or usual pharmacotherapy plus salmeterol. Chest 129, 15-26 (Pubitemid 43265239)
11. Taylor, D. R. (2009) The b-agonist saga and its clinical relevance: on and on it goes. Am. J. Respir. Crit. Care Med. 179, 976-978
12. Ortega, V. E., and Peters, S. P. (2010) β-2 adrenergic agonists: focus on safety and benefits versus risks. Curr. Opin. Pharmacol. 10, 246-253
13. Walker, J. K., Penn, R. B., Hanania, N. A., Dickey, B. F., and Bond, R. A. (2011) New perspectives regarding b2-adrenoceptor ligands in the treatment of asthma. Br. J. Pharmacol. 163, 18-28
14. Penn, R. B., Parent, J. L., Pronin, A. N., Panettieri, R. A., Jr., and Benovic, J. L. (1999) Pharmacological inhibition of protein kinases in intact cells: antagonism of β adrenergic receptor ligand binding by H-89 reveals limitations of usefulness. J. Pharmacol. Exp. Ther. 288, 428-437 (Pubitemid 29119648)
15. Guo, M., Pascual, R. M., Wang, S., Fontana, M. F., Valancius, C. A., Panettieri, R. A., Jr., Tilley, S. L., and Penn, R. B. (2005) Cytokines regulate β-2-adrenergic receptor responsiveness in airway smooth muscle via multiple PKA- and EP2 receptor-dependent mechanisms. Biochemistry 44, 13771-13782 (Pubitemid 41507458)
16. Misior, A. M., Yan, H., Pascual, R. M., Deshpande, D. A., Panettieri, R. A., and Penn, R. B. (2008) Mitogenic effects of cytokines on smooth muscle are critically dependent on protein kinase A and are unmasked by steroids and cyclooxygenase inhibitors. Mol. Pharmacol. 73, 566-574 (Pubitemid 351159225)
17. Komalavilas, P., Penn, R. B., Flynn, C. R., Thresher, J., Lopes, L. B., Furnish, E. J., Guo, M., Pallero, M. A., Murphy-Ullrich, J. E., and Brophy, C. M. (2007) The small heat shock-related protein, HSP20, is a cAMP-dependent protein kinase substrate that is involved in airway smooth muscle relaxation. Am. J. Physiol. Lung Cell Mol. Physiol. 294, L69-L78 (Pubitemid 351380319)
18. Wang, Z. W., and Kotlikoff, M. I. (1996) Activation of KCa channels in airway smooth muscle cells by endogenous protein kinase A. Am. J. Physiol. 271, L100-L105
19. Kume, H., Hall, I. P., Washabau, R. J., Takagi, K., and Kotlikoff, M. I. (1994) b-Adrenergic agonists regulate KCa channels in airway smooth muscle by cAMP-dependent and -independent mechanisms. J. Clin. Invest. 93, 371-379
20. Roscioni, S. S., Maarsingh, H., Elzinga, C. R., Schuur, J., Menzen, M., Halayko, A. J., Meurs, H., and Schmidt, M. (2011) Epac as a novel effector of airway smooth muscle relaxation. J. Cell. Mol. Med. 15, 1551-1563
21. Zieba, B. J., Artamonov, M. V., Jin, L., Momotani, K., Ho, R., Franke, A. S., Neppl, R. L., Stevenson, A. S., Khromov, A. S., Chrzanowska-Wodnicka, M., and Somlyo, A. V. (2011) The cAMP-responsive Rap1 guanine nucleotide exchange factor, Epac, induces smooth muscle relaxation by down-regulation of RhoA activity. J. Biol. Chem. 286, 16681-16692
22. Kassel, K. M., Wyatt, T. A., Panettieri, R. A., Jr., and Toews, M. L. (2008) Inhibition of human airway smooth muscle cell proliferation by β 2-adrenergic receptors and cAMP is PKA independent: evidence for EPAC involvement. Am. J. Physiol. Lung Cell Mol. Physiol. 294, L131-L138 (Pubitemid 351380325)
23. Roscioni, S. S., Prins, A. G., Elzinga, C. R., Menzen, M. H., Dekkers, B. G., Halayko, A. J., Meurs, H., Maarsingh, H., and Schmidt, M. (2011) Protein kinase A and the exchange protein directly activated by cAMP (Epac) modulate phenotype plasticity in human airway smooth muscle. Br. J. Pharmacol. 164, 958-969
24. Roscioni, S. S., Dekkers, B. G., Prins, A. G., Menzen, M. H., Meurs, H., Schmidt, M., and Maarsingh, H. (2011) cAMP inhibits modulation of airway smooth muscle phenotype via the exchange protein activated by cAMP (Epac) and protein kinase A. Br. J. Pharmacol. 162, 193-209
25. Yan, H., Deshpande, D. A., Misior, A. M., Miles, M. C., Saxena, H., Riemer, E. C., Pascual, R. M., Panettieri, R. A., and Penn, R. B. (2011) Anti-mitogenic effects of β-agonists and PGE2 on airway smooth muscle are PKA dependent. FASEB J. 25, 389-397
26. q11. FASEB J. 20, 1558-1560
27. Saxena, H., Deshpande, D. A., Tiegs, B. C., Yan, H., Battafarano, R. J., Burrows, W. M., Damera, G., Panettieri, R. A., Dubose, T. D., Jr., An, S. S., and Penn, R. B. (2012) The GPCR OGR1 (GPR68) mediates diverse signalling and contraction of airway smooth muscle in response to small reductions in extracellular pH. Br. J. Pharmacol. 166, 981-990
28. Billington, C. K., Kong, K. C., Bhattacharyya, R., Wedegaertner, P. B., Panettieri, R. A., Jr., Chan, T. O., and Penn, R. B. (2005) Cooperative regulation of p70S6 kinase by receptor tyrosine kinases and G protein-coupled receptors augments airway smooth muscle growth. Biochemistry 44, 14595-14605 (Pubitemid 41567467)
29. Naik, S., Billington, C. K., Pascual, R. M., Deshpande, D. A., Stefano, F. P., Kohout, T. A., Eckman, D. M., Benovic, J. L., and Penn, R. B. (2005) Regulation of cysteinyl leukotriene type 1 receptor internalization and signaling. J. Biol. Chem. 280, 8722-8732 (Pubitemid 40409559)
30. An, S. S., Fabry, B., Trepat, X., Wang, N., and Fredberg, J. J. (2006) Do biophysical properties of the airway smooth muscle in culture predict airway hyperresponsiveness? Am. J. Respir. Cell Mol. Biol. 35, 55-64 (Pubitemid 43993154)
31. Fabry, B., Maksym, G. N., Butler, J. P., Glogauer, M., Navajas, D., and Fredberg, J. J. (2001) Scaling the microrheology of living cells. Phys. Rev. Lett. 87, 148102
32. Gavett, S. H., and Wills-Karp, M. (1993) Elevated lung G protein levels and muscarinic receptor affinity in a mouse model of airway hyperreactivity. Am. J. Physiol. Lung Cell. Mol. Physiol. 265, L493-L500
33. Freyer, A. M., Billington, C. K., Penn, R. B., and Hall, I. P. (2004) Extracellular matrix modulates β2-adrenergic receptor signalling in human airway smooth muscle cells. Am. J. Respir. Cell Mol. Biol. 31, 440-445 (Pubitemid 39330954)
34. Butt, E., Abel, K., Krieger, M., Palm, D., Hoppe, V., Hoppe, J., and Walter, U. (1994) cAMP- and cGMP-dependent protein kinase phosphorylation sites of the focal adhesion vasodilator-stimulated phosphoprotein (VASP) in vitro and in intact human platelets. J. Biol. Chem. 269, 14509-14517 (Pubitemid 24194005)
35. Billington, C. K., and Penn, R. B. (2003) Signaling and regulation of G protein-coupled receptors in airway smooth muscle. Respir. Res. 4, 2
36. Grandoch, M., Roscioni, S. S., and Schmidt, M. (2010) The role of Epac proteins, novel cAMP mediators, in the regulation of immune, lung and neuronal function. Br. J. Pharmacol. 159, 265-284
37. Penn, R. B. (2008) Embracing emerging paradigms of G protein-coupled receptor agonism and signaling to address airway smooth muscle pathobiology in asthma. Naunyn Schmiedebergs Arch. Pharmacol. 378, 149-169
38. Spicuzza, L., Belvisi, M. G., Birrell, M. A., Barnes, P. J., Hele, D. J., and Giembycz, M. A. (2001) Evidence that the anti-spasmogenic effect of the β-adrenoceptor agonist, isoprenaline, on guinea-pig trachealis is not mediated by cyclic AMP-dependent protein kinase. Br. J. Pharmacol. 133, 1201-1212 (Pubitemid 32783479)
39. Rehmann, H., Schwede, F., Døskeland, S. O., Wittinghofer, A., and Bos, J. L. (2003) Ligand-mediated activation of the cAMP-responsive guanine nucleotide exchange factor Epac. J. Biol. Chem. 278, 38548-38556 (Pubitemid 37221750)
40. Poppe, H., Rybalkin, S. D., Rehmann, H., Hinds, T. R., Tang, X. B., Christensen, A. E., Schwede, F., Genieser, H. G., Bos, J. L., Doskeland, S. O., Beavo, J. A., and Butt, E. (2008) Cyclic nucleotide analogs as probes of signaling pathways. Nat. Methods 5, 277-278 (Pubitemid 351455143)
41. Holz, G. G., Chepurny, O. G., and Schwede, F. (2008) Epac-selective cAMP analogs: new tools with which to evaluate the signal transduction properties of cAMP-regulated guanine nucleotide exchange factors. Cell. Signal. 20, 10-20 (Pubitemid 350138365)
42. Laxman, S., Riechers, A., Sadilek, M., Schwede, F., and Beavo, J. A. (2006) Hydrolysis products of cAMP analogs cause transformation of Trypanosoma brucei from slender to stumpy-like forms. Proc. Natl. Acad. Sci. 103, 19194-19199 (Pubitemid 350002849)
43. Altschuler, D. L., Peterson, S. N., Ostrowski, M. C., and Lapetina, E. G. (1995) Cyclic AMP-dependent activation of Rap1b. J. Biol. Chem. 270, 10373-10376
44. 2+ oscillations. J. Gen. Physiol. 135, 247-259
45. Carvajal, J. A., Germain, A. M., Huidobro-Toro, J. P., and Weiner, C. P. (2000) Molecular mechanism of cGMP-mediated smooth muscle relaxation. J. Cell Physiol. 184, 409-420 (Pubitemid 30625505)
46. White, R. E., Kryman, J. P., El-Mowafy, A. M., Han, G., and Carrier, G. O. (2000) cAMP-dependent vasodilators cross-activate the cGMP-dependent protein kinase to stimulate BKCa channel activity in coronary artery smooth muscle cells. Circ. Res. 86, 897-905 (Pubitemid 30246988)
47. Jiang, H., Colbran, J. L., Francis, S. H., and Corbin, J. D. (1992) Direct evidence for cross-activation of cGMP-dependent protein kinase by cAMP in pig coronary arteries. J. Biol. Chem. 267, 1015-1019