Endogenous Gs-coupled receptors in smooth muscle exhibit differential susceptibility to GRK2/3-mediated desensitization

Biochemistry

Volumn 47, Issue 35, 2008, Pages 9279-9288

  Kok, Choi Kong ^a   Gandhi, Uma ^a   Martin, T J ^a   Anz, Candace B ^a   Yan, Huandong ^a   Misior, Anna M ^a   Pascual, Rodolfo M ^a   Deshpande, Deepak A ^a   Penn, Raymond B ^a  

^a WAKE FOREST UNIVERSITY HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR EXPRESSION; G PROTEIN-COUPLED RECEPTOR; PHYSIOLOGICAL CONDITIONS;

ADENOSINE 5' (N ETHYLCARBOXAMIDE); ADENOSINE A2 RECEPTOR; BETA 2 ADRENERGIC RECEPTOR; BETA 2 ADRENERGIC RECEPTOR STIMULATING AGENT; BUTAPROST; CYCLIC AMP; G PROTEIN COUPLED RECEPTOR KINASE; G PROTEIN COUPLED RECEPTOR KINASE 2; G PROTEIN COUPLED RECEPTOR KINASE 3; MESSENGER RNA; MITOGENIC AGENT; PROSTAGLANDIN E2; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; ADRBK1 PROTEIN, HUMAN; ADRBK2 PROTEIN, HUMAN; G PROTEIN COUPLED RECEPTOR; STIMULATORY GUANINE NUCLEOTIDE BINDING PROTEIN;

ARTICLE; BREATHING MUSCLE; CONTROLLED STUDY; DESENSITIZATION; ENZYME ACTIVATION; ENZYME ASSAY; ENZYME INHIBITION; HUMAN; HUMAN CELL; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; SMOOTH MUSCLE; CELL CULTURE; ENZYMOLOGY; GENETICS; METABOLISM;

CELLS, CULTURED; CYCLIC AMP; G-PROTEIN-COUPLED RECEPTOR KINASE 2; G-PROTEIN-COUPLED RECEPTOR KINASE 3; GTP-BINDING PROTEIN ALPHA SUBUNITS, GS; HUMANS; MUSCLE, SMOOTH; RECEPTORS, G-PROTEIN-COUPLED; RNA, MESSENGER; RNA, SMALL INTERFERING;

EID: 50849085454     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801056w     Document Type: Article

References (54)

1. Billington, C. K., and Penn, R. B. (2003) Signaling and regulation of G protein-coupled receptors in airway smooth muscle. Respir. Res. 4, 2.
2. Deshpande, D. A., and Penn, R. B. (2006) Targeting G protein-coupled receptor signaling in asthma. Cell. Signalling 18, 2105-2120.
3. Mundell, S. J., Olah, M. E., Panettieri, R. A., Benovic, J. L., and Penn, R. B. (2000) Regulation of G protein-coupled receptor-adenylyl cyclase responsiveness in human airway smooth muscle by exogenous and endogenous adenosine. Am. J. Respir. Cell Mol. Biol. 24, 155-163.
4. 2AR-adenylyl cyclase pathway in human airway smooth muscle. Am. J. Respir. Cell Mol. Biol. 19, 338-348.
5. Penn, R. B., Pascual, R. M., Kim, Y.-M., Mundell, S. J., Krymskaya, V. P., Panettieri, R. A., Jr., and Benovic, J. L. (2001) Arrestin specificity for G protein-coupled receptors in human airway smooth muscle. J. Biol. Chem. 276, 32648-32656.
6. Hirst, S. J., Martin, J. G., Bonacci, J. V., Chan, V., Fixman, E. D., Hamid, Q. A., Herszberg, B., Lavoie, J. P., McVicker, C. G., Moir, L. M., Nguyen, T. T., Peng, Q., Ramos-Barbon, D., and Stewart, A. G. (2004) Proliferative aspects of airway smooth muscle. J. Allergy Clin. Immunol. 114, 2-17.
7. Tomlinson, P. R., Wilson, J. W., and Stewart, A. G. (1995) Salbutamol inhibits the proliferation of human airway smooth muscle cells grown in culture: relationship to elevated cAMP levels. Biochem. Pharmacol. 49, 1809-1819.
8. Hua, X., Erikson, C. J., Chason, R. D., Rosebrock, C. N., Deshpande, D. A., Penn, R. B., and Tilley, S. L. (2007) Involvement of A1 adenosine receptors and neural pathways in adenosine-induced bronchoconstriction in mice. Am. J. Physiol. Lung Cell Mol. Physiol. 293, L25-L32.
9. Sheller, J. R., Mitchell, D., Meyrick, B., Oates, J., and Breyer, R. (2000) EP(2) receptor mediates bronchodilation by PGE(2) in mice. J. Appl. Physiol. 88, 2214-2218.
10. Tilley, S. L., Hartney, J. M., Erikson, C. J., Jania, C., Nguyen, M., Stock, J., McNeisch, J., Valancius, C., Panettieri, R. A., Jr., Penn, R. B., and Roller, B. H. (2003) Receptors and pathways mediating the effects of prostaglandin E2 on airway tone. Am. J. Physiol. Lung Cell Mol. Physiol. 284, 599-606.
11. Penn, R. B. and Benovic, J. L. (1998) Regulation of G Protein-Coupled Receptors, in Handbook of Physiology (Conn, P. M., Ed.) pp 125-164, Oxford University Press, New York.
12. Premont, R. T., and Gainetdinov, R. R. (2007) Physiological roles of G protein-coupled receptor kinases and arrestins. Annu. Rev. Physiol. 69, 511-534.
13. Ribas, C., Penela, P., Murga, C., Salcedo, A., Garcia-Hoz, C., Jurado-Pueyo, M., Aymerich, I., and Mayor, F., Jr. (2007) The G protein-coupled receptor kinase (GRR) interactome: role of GRRs in GPCR regulation and signaling. Biochim. Biophys. Acta 1768, 913-922.
14. Gainetdinov, R. R., Premont, R. T., Bohn, L. M., Lefkowitz, R. J., and Caron, M. G. (2004) Desensitization of G protein-coupled receptors and neuronal functions. Annu. Rev. Neurosci. 27, 107-144.
15. Roch, W. J. (2004) Genetic and phenotypic targeting of beta-adrenergic signaling in heart failure. Mol. Cell. Biochem. 263, 5-9.
16. Penn, R. B., Pronin, A. P., and Benovic, J. L. (2000) Regulation of G protein-coupled receptor kinases. Trends Cardiovasc. Med. 10, 81-89.
17. Roch, W. J., Rockman, H. A., Samama, P., Hamilton, R. A., Bond, R. A., Milano, C. A., and Lefkowitz, R. J. (1995) Cardiac function in mice overexpressing the beta-adrenergic receptor kinase or a beta ARR inhibitor. Science 268, 1350-1353.
18. Rockman, H. A., Chien, R. R., Choi, D. J., Iaccarino, G., Hunter, J. J., Ross, J., Jr., Lefkowitz, R. J., and Roch, W. J. (1998) Expression of a beta-adrenergic receptor kinase 1 inhibitor prevents the development of myocardial failure in gene-targeted mice. Proc. Natl. Acad. Sci. U.S.A. 95, 7000-7005.
19. Rockman, H. A., Choi, D. J., Akhter, S. A., Jaber, M., Giros, B., Lefkowitz, R. J., Caron, M. G., and Koch, W. J. (1998) Control of myocardial contractile function by the level of beta- adrenergic receptor kinase 1 in gene-targeted mice. J. Biol. Chem. 273, 18180-18184.
20. Green, S. A., Spasoff, A. P., Coleman, R. A., Johnson, M., and Liggett, S. A. (1996) Sustained activation of a G protein-coupled receptor via "anchored" agonist binding. J. Biol. Chem. 271, 24029-24035.
21. 2-adrenergic receptor desensitization, internalization, and phosphorylation in response to full and partial agonists. J. Biol. Chem. 272, 23871-23879.
22. January, B., Seibold, A., Allal, C., Whaley, B. S., Knoll, B. J., Moore, R. H., Dickey, B. F., Barber, R., and Clark, R. B. (1998) Salmeterol-induced desensitization, internalization and phosphorylation of the human beta2-adrenoceptor. Br. J. Pharmacol. 123, 701-711.
23. Penn, R. B. (2008) Embracing emerging pardigms of G protein-coupled receptor agonism and signaling to address airway smooth muscle pathobiology in asthma, Naunyn-Schmiedeberg's Arch. Pharmacol. 378, 149-169.
24. Kong, K. C., Billington, C. K., Gandhi, U., Panettieri, R. A., Jr., and Penn, R. B. (2006) Cooperative mitogenic signaling by G protein-coupled receptors and growth factors is dependent on G(q/11). FASEB J. 20, 1558-1560.
25. Misior, A. M., Yan, H., Pascual, R. M., Deshpande, D. A., Panettieri, R. A., Jr., and Penn, R. B. (2007) 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.
26. Carman, C. V., Barak, L. S., Chen, C., Liu-Chen, L., Onorato, J. J., Kennedy, S. P., Caron, M. C., and Benovic, J. L. (2000) Mutational analysis of Gbg and phospholipid interaction with G protein-coupled receptor kinase 2. J. Biol. Chem. 275, 10443-10452.
27. Carman, C. V., Parent, J. L., Day, P. W., Pronin, A. N., Sternweis, P. M., Wedegaertner, P. B., Gilman, A. G., Benovic, J. L., and Kozasa, T. (1999) Selective Regulation of Gq/11alpha by an RGS domain in the G protein-coupled receptor kinase GRR2. J. Biol. Chem. 274, 34483-34492.
28. 2-adrenergic receptor. J. Biol. Chem. 269, 13084-13087.
29. Billington, C. R., Rong, R. C., Bhattacharyya, R., Wedegaertner, P. B., Panettieri, R. A., 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.
30. Iwata, R., Luo, J., Penn, R. B., and Benovic, J. L. (2005) Bimodal regulation of the human H1 histamine receptor by G protein-coupled receptor kinase 2. J. Biol. Chem. 280, 2197-204.
31. Deshpande, D. A., Theriot, B. S., Penn, R. B., and Walker, J. R. (2008) (beta)-Arrestins specifically constrain {beta}2-adrenergic receptor signaling and function in airway smooth muscle. FASEB J. 22, 2134-2141.
32. 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 beta-2-adrenergic receptor responsiveness in airway smooth muscle via multiple PRA- and EP2 receptor-dependent mechanisms. Biochemistry 44, 13771-13782.
33. Deshpande, D. A., Pascual, R. M., Wang, S. W., Eckman, D. M., Riemer, E. C., Funk, C. D., and Penn, R. B. (2007) PRC-dependent regulation of the receptor locus dominates functional consequences of cysteinyl leukotriene type 1 receptor activation. FASEB J. 21, 2335-2342.
34. Kim, C. M., Dion, S. B., and Benovic, J. L. (1993) Mechanism of β-adrenergic receptor kinase activation by G proteins. J. Biol. Chem. 268, 15412-15418.
35. Pitcher, J. A., Inglese, J., Higgins, J. B., Arriza, J. L., Casey, P. J., Rim, C., Benovic, J. L., Rwatra, M. M., Caron, M. G., and Lefkowitz, R. J. (1992) Role of βγ subunits of G proteins in targeting the β-adrenergic receptor kinase to membrane-bound receptors. Science 257, 1264-1267.
36. Eckhart, A. D., Duncan, S. J., Penn, R. B., Benovic, J. L., Lefkowitz, R. J., and Koch, W. J. (2000) Hybrid transgenic mice reveal in vivo specificity of G protein-coupled receptor kinases in the heart. Circ. Res. 86, 43-50.
37. Wilson, R. J., Rhodes, S. A., Wood, R. L., Shield, V. J., Noel, L. S., Gray, D. W., and Giles, H. (2004) Functional pharmacology of human prostanoid EP2 and EP4 receptors. Eur. J. Pharmacol. 501, 49-58.
38. Pascual, R. M., Billington, C. K., Hall, I. P., Panettieri, R. A., Fish, J. E., Peters, S. P., and Penn, R. B. (2000) Comparison of chronic cytokine versus PGE2 pretreatment effects on G protein-coupled receptor (GPCR) signaling in human airway smooth muscle (HASM). Am. J. Respir. Cut. Care Med. A696.
39. Goncharova, E. A., Billington, C. K., Irani, C., Vorotnikov, A. V., Tkachuk, V. A., Penn, R. B., Krymskaya, V. P., and Panettieri, R. A., Jr. (2003) Cyclic AMP-Mobilizing Agents and Glucocorticoids Modulate Human Smooth Muscle Cell Migration. Am. J. Respir. Cell Mol. Biol. 31, 31.
40. Ammit, A. J., Hoffman, R. K., Amrani, Y., Lazaar, A. L., Hay, D. W. P., Torphy, T. J., Penn, R. B., and Panettieri, R. A. (2000) TNFα-induced secretion of RANTES and IL-6 from human airway smooth muscle cells: Modulation by cAMP. Am. J. Respir. Cell Mol. Biol. 23, 794-802.
41. Norel, X., Walch, L., Labat, C., Gascard, J. P., Dulmet, E., and Brink, C. (1999) Prostanoid receptors involved in the relaxation of human bronchial preparations. Br. J. Pharmacol. 126, 867-872.
42. McGraw, D. W., Mihlbachler, K. A., Schwarb, M. R., Rahman, F. F., Small, K. M., Almoosa, K. F., and Liggett, S. B. (2006) Airway smooth muscle prostaglandin-EP1 receptors directly modulate beta2-adrenergic receptors within a unique heterodimeric complex. J. Clin. Invest 116, 1400-1409.
43. Mundell, S. J., Benovic, J. L., and Kelly, E. (1997) A dominant negative mutant of the G protein-coupled receptor kinase 2 selectively attenuates adenosine A2 receptor desensitization. Mol. Pharmacol. 51, 991-998.
44. Wisler, J. W., DeWire, S. M., Whalen, E. J., Violin, J. D., Drake, M. T., Ahn, S., Shenoy, S. K., and Lefkowitz, R. J. (2007) A unique mechanism of beta-blocker action: Carvedilol stimulates beta-arrestin signaling. Proc. Natl. Acad. Sci. U.S.A 104, 16657-16662.
45. Clark, R. B., and Rich, T. C. (2003) Probing the roles of protein kinases in g-protein-coupled receptor desensitization. Mol. Pharmacol. 64, 1015-1017.
46. Tran, T. M., Friedman, J., Qunaibi, E., Baameur, F., Moore, R. H., and Clark, R. B. (2004) Characterization of agonist Stimulation of cAMP-dependent protein kinase and G protein-coupled receptor kinase phosphorylation of the beta2-adrenergic receptor using phosphoserine-specific antibodies. Mol. Pharmacol. 65, 196-206.
47. Xin, W., Tran, T. M., Richter, W., Clark, R. B., and Rich, T. C. (2008) Roles of GRK and PDE4 activities in the regulation of beta2 adrenergic signaling. J. Gen. Physiol 131, 349-364.
48. Jaber, M., Koch, W. J., Rockman, H., Smith, B., Bond, R. A., Sulik, K. K., Ross, J., Jr., Lefkowitz, R. J., Caron, M. G., and Giros, B. (1996) Essential role of beta-adrenergic receptor kinase 1 in cardiac development and function. Proc. Natl. Acad. Sci. U.S.A. 93, 12974-12979.
49. Abisheganaden, J., and Boushey, H. A. (1998) Long-acting inhaled beta 2-agonists and the loss of "bronchoprotective" efficacy. Am. J. Med. 104, 494-497; editorial; comment.
50. Bhagat, R., Kalra, S., Swystun, V. A., and Cockcroft, D. W. (1995) Rapid onset of tolerance to the bronchoprotective effect of salmeterol. Chest 108, 1235-1239.
51. Cheung, D., Timmers, M. C., Zwinderman, A. H., Bel, E. H., Dijkman, J. H., and Sterk, P. J. (1992) 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, 1198-1203; (see comments).
52. Peters, S. P., and Fish, J. E. (1999) Prior use of long-acting β-agonists: friend or foe in the emergency department? Am. J. Med. 107, 283-285.
53. Israel, E., Chinchilli, V. M., Ford, J. G., Boushey, H. A., Cherniack, R., Craig, T. J., Deykin, A., Fagan, J. K., Fahy, J. V., Fish, J., Kraft, M., Kunselman, S. J., Lazarus, S. C., Lemanske, R. F., Jr., Liggett, S. B., Martin, R. J., Mitra, N., Peters, S. P., Silverman, E., Sorkness, C. A., Szefler, S. J., Wechsler, M. E., Weiss, S. T., and Drazen, J. M. (2004) Use of regularly scheduled albuterol treatment in asthma: genotype-stratified, randomised, placebo-controlled cross-over trial. Lancet 364, 1505-1512.
54. Mak, J. C., Hisada, T., Salmon, M., Barnes, P. J., and Chung, K. F. (2002) Glucocorticoids reverse IL-1beta-induced impairment of beta-adrenoceptor-mediated relaxation and up-regulation of G-protein-coupled receptor kinases. Br. J. Pharmacol. 135, 987-996.