Regulation of GPCR-mediated smooth muscle contraction: Implications for asthma and pulmonary hypertension

Pulmonary Pharmacology and Therapeutics

Volumn 26, Issue 1, 2013, Pages 121-131

  Wright, D B ^a   Tripathi, S ^b   Sikarwar, A ^b   Santosh, K T ^b   Perez Zoghbi, J ^c   Ojo, O O ^a   Irechukwu, N ^a   Ward, J P T ^a   Schaafsma, D ^b,d  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF MANITOBA   (Canada)

^c TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^d CANADIAN INSTITUTES OF HEALTH RESEARCH   (Canada)

Author keywords

Ca2+ mobilization; Ca2+ sensitization; Calcium; CPI 17; Palmitoylation; ROCK

Indexed keywords

CALCIUM; G PROTEIN COUPLED RECEPTOR; PROTEIN KINASE C; RHO FACTOR;

ARTICLE; ASTHMA; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CALCIUM TRANSPORT; HUMAN; NITROSYLATION; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PULMONARY HYPERTENSION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE CONTRACTION; VASCULAR SMOOTH MUSCLE;

ANIMALS; ASTHMA; CALCIUM; HUMANS; HYPERTENSION, PULMONARY; MUSCLE CONTRACTION; MUSCLE, SMOOTH; MUSCLE, SMOOTH, VASCULAR; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84873176021     PISSN: 10945539     EISSN: 15229629     Source Type: Journal    
DOI: 10.1016/j.pupt.2012.06.005     Document Type: Article

References (186)

1. Rosenbaum D.M., Rasmussen S.G., Kobilka B.K. The structure and function of G-protein-coupled receptors. Nature 2009, 459:356-363.
2. King N., Hittinger C.T., Carroll S.B. Evolution of key cell signaling and adhesion protein families predates animal origins. Science 2003, 301:361-363.
3. Overington J.P., Al-Lazikani B., Hopkins A.L. How many drug targets are there?. Nat Rev Drug Discov 2006, 5:993-996.
4. Wettschureck N., Offermanns S. Mammalian G proteins and their cell type specific functions. Physiol Rev 2005, 85:1159-1204.
5. Cabrera-Vera T.M., Vanhauwe J., Thomas T.O., Medkova M., Preininger A., Mazzoni M.R., et al. Insights into G protein structure, function, and regulation. Endocr Rev 2003, 24:765-781.
6. Bourne H.R. How receptors talk to trimeric G proteins. Curr Opin Cell Biol 1997, 9:134-142.
7. Bohm A., Gaudet R., Sigler P.B. Structural aspects of heterotrimeric G-protein signaling. Curr Opin Biotechnol 1997, 8:480-487.
8. Iiri T., Farfel Z., Bourne H.R. G-protein diseases furnish a model for the turn-on switch. Nature 1998, 394:35-38.
9. Ford C.E., Skiba N.P., Bae H., Daaka Y., Reuveny E., Shekter L.R., et al. Molecular basis for interactions of G protein betagamma subunits with effectors. Science 1998, 280:1271-1274.
10. Berman D.M., Wilkie T.M., Gilman A.G. GAIP and RGS4 are GTPase-activating proteins for the Gi subfamily of G protein alpha subunits. Cell 1996, 86:445-452.
11. Guo Y., Li M., Lu M., Wen Z., Huang Z. Predicting G-protein coupled receptors-G-protein coupling specificity based on autocross-covariance transform. Proteins 2006, 65:55-60.
12. Gilman A.G. G proteins: transducers of receptor-generated signals. Annu Rev Biochem 1987, 56:615-649.
13. Clapham D.E., Neer E.J. G protein beta gamma subunits. Annu Rev Pharmacol Toxicol 1997, 37:167-203.
14. Dupre D.J., Robitaille M., Rebois R.V., Hebert T.E. The role of Gbetagamma subunits in the organization, assembly, and function of GPCR signaling complexes. Annu Rev Pharmacol Toxicol 2009, 49:31-56.
15. Akgoz M., Azpiazu I., Kalyanaraman V., Gautam N. Role of the G protein gamma subunit in beta gamma complex modulation of phospholipase Cbeta function. J Biol Chem 2002, 277:19573-19578.
16. Yevenes G.E., Peoples R.W., Tapia J.C., Parodi J., Soto X., Olate J., et al. Modulation of glycine-activated ion channel function by G-protein betagamma subunits. Nat Neurosci 2003, 6:819-824.
17. Downes G.B., Gautam N. The G protein subunit gene families. Genomics 1999, 62:544-552.
18. Kobilka B.K., Deupi X. Conformational complexity of G-protein-coupled receptors. Trends Pharmacol Sci 2007, 28:397-406.
19. Bokoch MP, Zou Y, Rasmussen SG, Liu CW, Nygaard R, Rosenbaum DM, et al. Ligand-specific regulation of the extracellular surface of a G-protein-coupled receptor. Nature. 463:108-112.
20. Scheer A., Fanelli F., Costa T., De Benedetti P.G., Cotecchia S. Constitutively active mutants of the alpha 1B-adrenergic receptor: role of highly conserved polar amino acids in receptor activation. EMBO J 1996, 15:3566-3578.
21. Gether U. Uncovering molecular mechanisms involved in activation of G protein-coupled receptors. Endocr Rev 2000, 21:90-113.
22. Lambert D.G. Drugs and receptors. Continuing education in anaesthesia. Crit Care & Pain 2004, 4:181-184.
23. Qanbar R., Bouvier M. Role of palmitoylation/depalmitoylation reactions in G-protein-coupled receptor function. Pharmacol Ther 2003, 97:1-33.
24. Resh M.D. Palmitoylation of ligands, receptors, and intracellular signaling molecules. Science's STKE Signal Transduction Knowledge Environment 2006, 2006:re14.
25. Kleuss C., Krause E. Galpha(s) is palmitoylated at the N-terminal glycine. The EMBO Journal 2003, 22:826-832.
26. Linder M.E., Deschenes R.J. Palmitoylation: policing protein stability and traffic. Nat Rev Mol Cell Biol 2007, 8:74-84.
27. Ohno Y., Kihara A., Sano T., Igarashi Y. Intracellular localization and tissue-specific distribution of human and yeast DHHC cysteine-rich domain-containing proteins. Biochim Biophys Acta 2006, 1761:474-483.
28. Korycka J., Lach A., Heger E., Boguslawska D.M., Wolny M., Toporkiewicz M., et al. Human DHHC proteins: a spotlight on the hidden player of palmitoylation. Eur J Cell Biology 2012, 91:107-117.
29. Probst W.C., Snyder L.A., Schuster D.I., Brosius J., Sealfon S.C. Sequence alignment of the G-protein coupled receptor superfamily. DNA Cell Biol 1992, 11:1-20.
30. Duncan J.A., Gilman A.G. A cytoplasmic acyl-protein thioesterase that removes palmitate from G protein alpha subunits and p21(RAS). J Biol Chem 1998, 273:15830-15837.
31. Reid H.M., Kinsella B.T. Palmitoylation of the TPbeta isoform of the human thromboxane A2 receptor. Modulation of G protein: effector coupling and modes of receptor internalization. Cell Signal 2007, 19:1056-1070.
32. Koshimizu T., Tsujimoto G., Ono K., Masaki T., Sakamoto A. Truncation of the receptor carboxyl terminus impairs membrane signaling but not ligand binding of human ETB endothelin receptor. Biochem Biophys Res Commun 1995, 217:354-362.
33. Cramer H., Schmenger K., Heinrich K., Horstmeyer A., Boning H., Breit A., et al. Coupling of endothelin receptors to the ERK/MAP kinase pathway. Roles of palmitoylation and G(alpha)q. Eur J Biochem 2001, 268:5449-5459.
34. Adams M.N., Christensen M.E., He Y., Waterhouse N.J., Hooper J.D. The role of palmitoylation in signalling, cellular trafficking and plasma membrane localization of protease-activated receptor-2. PLoS One 2011, 6:e28018.
35. Novotny J., Durchankova D., Ward R.J., Carrillo J.J., Svoboda P., Milligan G. Functional interactions between the alpha1b-adrenoceptor and Galpha11 are compromised by de-palmitoylation of the G protein but not of the receptor. Cell Signal 2006, 18:1244-1251.
36. Jones T.L., Gutkind J.S. Galpha12 requires acylation for its transforming activity. Biochemistry 1998, 37:3196-3202.
37. Bhattacharyya R., Wedegaertner P.B. Galpha 13 requires palmitoylation for plasma membrane localization, Rho-dependent signaling, and promotion of p115-RhoGEF membrane binding. J Biol Chem 2000, 275:14992-14999.
38. Percherancier Y., Planchenault T., Valenzuela-Fernandez A., Virelizier J.L., Arenzana-Seisdedos F., Bachelerie F. Palmitoylation-dependent control of degradation, life span, and membrane expression of the CCR5 receptor. J Biol Chem 2001, 276:31936-31944.
39. Fukushima Y., Saitoh T., Anai M., Ogihara T., Inukai K., Funaki M., et al. Palmitoylation of the canine histamine H2 receptor occurs at Cys(305) and is important for cell surface targeting. Biochim Biophys Acta 2001, 1539:181-191.
40. O'Dowd B.F., Hnatowich M., Caron M.G., Lefkowitz R.J., Bouvier M. Palmitoylation of the human beta 2-adrenergic receptor. Mutation of Cys341 in the carboxyl tail leads to an uncoupled nonpalmitoylated form of the receptor. J Biol Chem 1989, 264:7564-7569.
41. Gao Z., Ni Y., Szabo G., Linden J. Palmitoylation of the recombinant human A1 adenosine receptor: enhanced proteolysis of palmitoylation-deficient mutant receptors. Biochem J 1999, 342(Pt 2):387-395.
42. Ponimaskin E.G., Heine M., Joubert L., Sebben M., Bickmeyer U., Richter D.W., et al. The 5-hydroxytryptamine(4a) receptor is palmitoylated at two different sites, and acylation is critically involved in regulation of receptor constitutive activity. J Biol Chem 2002, 277:2534-2546.
43. Horstmeyer A., Cramer H., Sauer T., Muller-Esterl W., Schroeder C. Palmitoylation of endothelin receptor A. Differential modulation of signal transduction activity by post-translational modification. J Biol Chem 1996, 271:20811-20819.
44. Papoucheva E., Dumuis A., Sebben M., Richter D.W., Ponimaskin E.G. The 5-hydroxytryptamine(1A) receptor is stably palmitoylated, and acylation is critical for communication of receptor with Gi protein. J Biol Chem 2004, 279:3280-3291.
45. Wedegaertner P.B., Wilson P.T., Bourne H.R. Lipid modifications of trimeric G proteins. J Biol Chem 1995, 270:503-506.
46. Deshpande D.A., Penn R.B. Targeting G protein-coupled receptor signaling in asthma. Cell Signal 2006, 18:2105-2120.
47. Savoia C., Burger D., Nishigaki N., Montezano A., Touyz R.M. Angiotensin II and the vascular phenotype in hypertension. Expert Rev Mol Med 2011, 13:e11.
48. Burnstock G. Purinergic signaling and vascular cell proliferation and death. Arterioscler Thromb Vasc Biol 2002, 22:364-373.
49. Jones T.L. Role of palmitoylation in RGS protein function. Methods Enzymol 2004, 389:33-55.
50. Stoffel R.H., Inglese J., Macrae A.D., Lefkowitz R.J., Premont R.T. Palmitoylation increases the kinase activity of the G protein-coupled receptor kinase, GRK6. Biochemistry 1998, 37:16053-16059.
51. Mak J.C., Chan-Yeung M.M. Reactive oxidant species in asthma. Curr Opin Pulm Med 2006, 12:7-11.
52. Sylvester J.T., Shimoda L.A., Aaronson P.I., Ward J.P. Hypoxic pulmonary vasoconstriction. Physiol Rev 2012, 92:367-520.
53. Parat M.O., Stachowicz R.Z., Fox P.L. Oxidative stress inhibits caveolin-1 palmitoylation and trafficking in endothelial cells. Biochem J 2002, 361:681-688.
54. Burgoyne J.R., Haeussler D.J., Kumar V., Ji Y., Pimental D.R., Zee R.S., et al. Oxidation of HRas cysteine thiols by metabolic stress prevents palmitoylation in vivo and contributes to endothelial cell apoptosis. Faseb J 2011.
55. Clark K.L., Oelke A., Johnson M.E., Eilert K.D., Simpson P.C., Todd S.C. CD81 associates with 14-3-3 in a redox-regulated palmitoylation-dependent manner. J Biol Chem 2004, 279:19401-19406.
56. Adam L., Bouvier M., Jones T.L. Nitric oxide modulates beta(2)-adrenergic receptor palmitoylation and signaling. J Biol Chem 1999, 274:26337-26343.
57. Garcia-Cardena G., Oh P., Liu J., Schnitzer J.E., Sessa W.C. Targeting of nitric oxide synthase to endothelial cell caveolae via palmitoylation: implications for nitric oxide signaling. Proc Natl Acad Sci USA 1996, 93:6448-6453.
58. Navarro-Lerida I., Corvi M.M., Barrientos A.A., Gavilanes F., Berthiaume L.G., Rodriguez-Crespo I. Palmitoylation of inducible nitric-oxide synthase at Cys-3 is required for proper intracellular traffic and nitric oxide synthesis. J Biol Chem 2004, 279:55682-55689.
59. Stamler J.S., Simon D.I., Osborne J.A., Mullins M.E., Jaraki O., Michel T., et al. S-nitrosylation of proteins with nitric oxide: synthesis and characterization of biologically active compounds. Proc Natl Acad Sci USA 1992, 89:444-448.
60. Jennings B.C., Nadolski M.J., Ling Y., Baker M.B., Harrison M.L., Deschenes R.J., et al. 2-Bromopalmitate and 2-(2-hydroxy-5-nitro-benzylidene)-benzo[b]thiophen-3-one inhibit DHHC-mediated palmitoylation in vitro. J Lipid Res 2009, 50:233-242.
61. Daaka Y. S-nitrosylation-regulated GPCR signaling. Biochim Biophys Acta 2012, 1820:743-751.
62. Ushio-Fukai M. Vascular signaling through G protein-coupled receptors: new concepts. Curr Opin Nephrol Hypertens 2009, 18:153-159.
63. White T.A., Walseth T.F., Kannan M.S. Nitric oxide inhibits ADP-ribosyl cyclase through a cGMP-independent pathway in airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 2002, 283:L1065-L1071.
64. 2+ entry mediated by TRPC3/TRPC6 proteins in rat prostate smooth muscle (PS1) cell line. JCell Physiol 2005, 204:320-328.
65. Fill M., Copello J.A. Ryanodine receptor calcium release channels. Physiol Rev 2002, 82:893-922.
66. 2+ oscillations of porcine tracheal smooth muscle. Am J Physiol 1997, 272:L659-L664.
67. Lanner J.T., Georgiou D.K., Joshi A.D., Hamilton S.L. Ryanodine receptors: structure, expression, molecular details, and function in calcium release. Cold Spring Harb Perspect Biol 2010, 2:a003996.
68. 2+ release in smooth muscle cells. AmJPhysiol Cell Physiol 2004, 286:C538-C546.
69. 2+ signaling: regulation of endothelin-induced contraction in peritubular smooth muscle cells. FASEB J 2002, 16:697-705.
70. 2+ release by M1 muscarinic receptor activation in coronary arterial smooth muscle. JVascRes. 2003, 40:28-36.
71. Deshpande D.A., White T.A., Dogan S., Walseth T.F., Panettieri R.A., Kannan M.S. CD38/cyclic ADP-ribose signaling: role in the regulation of calcium homeostasis in airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 2005, 288:L773-L788.
72. Zheng J., Wenzhi B., Miao L., Hao Y., Zhang X., Yin W., et al. Ca(2+) release induced by cADP-ribose is mediated by FKBP12.6 proteins in mouse bladder smooth muscle. Cell Calcium 2010, 47:449-457.
73. Guedes A.G., Paulin J., Rivero-Nava L., Kita H., Lund F.E., Kannan M.S. CD38-deficient mice have reduced airway hyperresponsiveness following IL-13 challenge. Am J Physiol Lung Cell Mol Physiol 2006, 291:L1286-L1293.
74. Amrani Y., Krymskaya V., Maki C., Panettieri R.A. Mechanisms underlying TNF-alpha effects on agonist-mediated calcium homeostasis in human airway smooth muscle cells. Am J Physiol 1997, 273:L1020-L1028.
75. Hotta K., Emala C.W., Hirshman C.A. TNF-alpha upregulates Gialpha and Gqalpha protein expression and function in human airway smooth muscle cells. Am J Physiol 1999, 276:L405-L411.
76. Ammit A.J., Armour C.L., Black J.L. Smooth-muscle myosin light-chain kinase content is increased in human sensitized airways. Am J Respir Crit Care Med 2000, 161:257-263.
77. Mahn K., Ojo O.O., Chadwick G., Aaronson P.I., Ward J.P., Lee T.H. Ca(2+) homeostasis and structural and functional remodelling of airway smooth muscle in asthma. Thorax 2010, 65:547-552.
78. van Breemen C., Chen Q., Laher I. Superficial buffer barrier function of smooth muscle sarcoplasmic reticulum. Trends Pharmacol Sci 1995, 16:98-105.
79. Lewis R.S. The molecular choreography of a store-operated calcium channel. Nature 2007, 446:284-287.
80. Hewavitharana T., Deng X., Soboloff J., Gill D.L. Role of STIM and Orai proteins in the store-operated calcium signaling pathway. Cell Calcium 2007, 42:173-182.
81. Soboloff J., Spassova M.A., Tang X.D., Hewavitharana T., Xu W., Gill D.L. Orai1 and STIM reconstitute store-operated calcium channel function. J Biol Chem 2006, 281:20661-20665.
82. 2+ currents in canine bronchial smooth muscle: characterization and physiological roles. Am J Physiol 1997, 272:C1757-C1765.
83. 2+ activated K+ channels regulate human airway smooth muscle proliferation. Am J Respir Cell Mol Biol 2007, 37:525-531.
84. Kume H., Hall I.P., Washabau R.J., Takagi K., Kotlikoff M.I. Beta-adrenergic agonists regulate KCa channels in airway smooth muscle by cAMP-dependent and -independent mechanisms. J Clin Invest 1994, 93:371-379.
85. Wang Z.W., Kotlikoff M.I. Activation of KCa channels in airway smooth muscle cells by endogenous protein kinase A. Am J Physiol 1996, 271:L100-L105.
86. Semenov I., Wang B., Herlihy J.T., Brenner R. BK channel beta1 subunits regulate airway contraction secondary to M2 muscarinic acetylcholine receptor mediated depolarization. J Physiol 2011, 589:1803-1817.
87. Snetkov V.A., Hirst S.J., Twort C.H., Ward J.P. Potassium currents in human freshly isolated bronchial smooth muscle cells. Br J Pharmacol 1995, 115:1117-1125.
88. Mitchell C., Syed N.I., Gurney A.M., Kennedy C. A Ca(2+) -dependent chloride current and Ca(2+) influx via Ca(v) 1.2 ion channels play major roles in P2Y receptor-mediated pulmonary vasoconstriction. Br J Pharmacol 2012, 166:1503-1512.
89. Carafoli E., Garcia-Martin E., Guerini D. The plasma membrane calcium pump: recent developments and future perspectives. Experientia 1996, 52:1091-1100.
90. 2+ homeostasis of bladder smooth muscle: evidence from PMCA gene-ablated mice. Am J Physiol Cell Physiol 2007, 292:C423-C431.
91. Floyd R., Wray S. Calcium transporters and signalling in smooth muscles. Cell Calcium 2007, 42:467-476.
92. Penn R.B., Benovic J.L. Regulation of heterotrimeric G protein signaling in airway smooth muscle. Proc Am Thorac Soc 2008, 5:47-57.
93. 2+ oscillations by phosphorylation of Ins(1,4,5)P3 receptors. Biochem Soc Trans 2003, 31:954-957.
94. 2+ ATPase (SERCA) expression contributes to airway remodelling in bronchial asthma. Proc Natl Acad Sci USA 2009, 106:10775-10780.
95. Moffatt M.F., Kabesch M., Liang L., Dixon A.L., Strachan D., Heath S., et al. Genetic variants regulating ORMDL3 expression contribute to the risk of childhood asthma. Nature 2007, 448:470-473.
96. Cantero-Recasens G., Fandos C., Rubio-Moscardo F., Valverde M.A., Vicente R. The asthma-associated ORMDL3 gene product regulates endoplasmic reticulum-mediated calcium signaling and cellular stress. Hum Mol Genet 2010, 19:111-121.
97. Lodish H.F., Kong N. Perturbation of cellular calcium blocks exit of secretory proteins from the rough endoplasmic reticulum. J Biol Chem 1990, 265:10893-10899.
98. Yoo E., Tang L., Wu R., Torres T., Balitzer D., Dong H., et al. Cytokines induce human bronchial smooth muscle cell growth via an NCX1-dependent mechanism. Am J Respir Crit Care Med 2010, 181:A3604.
99. Rahman M., Inman M., Kiss L., Janssen L.J. Reverse-mode NCX-current in mouse airway smooth muscle: Na(+) - and voltage-dependence, contributions to Ca(2+) - influx and contraction, and altered expression in a model of allergen-induced hyperresponsiveness. Acta Physiol (Oxf) 2011.
100. Wang Y., Zhang S.Y., Wang X.L., Qian G.S. Expression of ryanodine receptor isoforms in airway smooth muscle cells of rats. Zhongguo Ying Yong Sheng Li Xue Za Zhi 2004, 20:181-184.
101. Karner L.C.H.S., Kanabar V., Mahn K., Simcock D.E., Gosling M., Ward J.P.T. Pro-asthmatic cytokines regulate multiple TRPC, TRPM and TRPV family genes expressed in human airway smooth muscle. Am J Respir Crit Care Med 2007, 175:A525.
102. Jude J.A., Solway J., Panettieri R.A., Walseth T.F., Kannan M.S. Differential induction of CD38 expression by TNF-{alpha} in asthmatic airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 2010, 299:L879-L890.
103. 2+ reuptake in human airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 2009, 297:L26-L34.
104. Ojo O.O., Lee T.H., Ward J.P.T. The long acting B2 agonist Formoterol and inflammatory cytokines Suppress SERCA-2 expression in human airway smooth muscle. Am J Respir Crit Care Med 2010, A5302.
105. Reuter H., Blaustein M.P., Haeusler G. Na-Ca exchange and tension development in arterial smooth muscle. Philos Trans R Soc Lond B Biol Sci 1973, 265:87-94.
106. 2+ exchanger impairs arteriolar myogenic reactivity. J Physiol 2008, 586:1669-1681.
107. White T.A., Xue A., Chini E.N., Thompson M., Sieck G.C., Wylam M.E. Role of transient receptor potential C3 in TNF-alpha-enhanced calcium influx in human airway myocytes. Am J Respir Cell Mol Biol 2006, 35:243-251.
108. Sathish V., Yang B., Meuchel L.W., VanOosten S.K., Ryu A.J., Thompson M.A., et al. Caveolin-1 and force regulation in porcine airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 2011, 300:L920-L929.
109. 2+ influx in human airway smooth muscle. Eur Respir J 2012.
110. Yu Y., Fantozzi I., Remillard C.V., Landsberg J.W., Kunichika N., Platoshyn O., et al. Enhanced expression of transient receptor potential channels in idiopathic pulmonary arterial hypertension. Proc Natl Acad Sci USA 2004, 101:13861-13866.
111. 2+ entry in pulmonary artery smooth muscle cells from patients with idiopathic pulmonary arterial hypertension. Am J Physiol Cell Physiol 2007, 292:C2297-C2305.
112. 2+ entry pathways activated by store-depletion or hypoxia in canine pulmonary arterial smooth muscle cells. Am J Physiol Cell Physiol 2008, 294:C313-C323.
113. Ann Twiss M., Harman E., Chesrown S., Hendeles L. Efficacy of calcium channel blockers as maintenance therapy for asthma. Br J Clin Pharmacol 2002, 53:243-249.
114. Ten Broeke R., Folkerts G., Leusink-Muis T., Van der Linde H.J., Villain M., Manion M.K., et al. Calcium sensors as new therapeutic targets for airway hyperresponsiveness and asthma. Faseb J 2001, 15:1831-1833.
115. Choi I.S. Gender-specific asthma treatment. Allergy Asthma Immunol Res 2011, 3:74-80.
116. Curl C.L., Delbridge L.M.D., Canny B.J., Wendt I.R. Testosterone modulates Cardiomyocyte Ca(2+) handling and contractile function. Physiol Res 2009, 58:293-297.
117. Golden K.L., Marsh J.D., Jiang Y., Brown T., Moulden J. Gonadectomy of adult male rats reduces contractility of isolated cardiac myocytes. Am J Physiol Endocrinol Metab 2003, 285:E449-E453.
118. Brozovich F.V. Rho signaling: agonist stimulation and depolarization come together. Circ Res 2003, 93:481-483.
119. Somlyo A.P., Himpens B. Cell calcium and its regulation in smooth muscle. FASEB J 1989, 3:2266-2276.
120. Somlyo A.P., Somlyo A.V. Signal transduction by G-proteins, rho-kinase and protein phosphatase to smooth muscle and non-muscle myosin II. J Physiol 2000, 522(Pt 2):177-185.
121. Wettschureck N., Offermanns S. Rho/Rho-kinase mediated signaling in physiology and pathophysiology. J Mol Med (Berl) 2002, 80:629-638.
122. 2+ sensitization of smooth muscle. J Biol Chem 1997, 272:10704-10709.
123. 2+ sensitization of tracheal smooth muscle. Am J Physiol 1998, 275:L748-L755.
124. Hilgers R.H., Webb R.C. Molecular aspects of arterial smooth muscle contraction: focus on Rho. Exp Biol Med (Maywood) 2005, 230:829-835.
125. Bourne H.R., Sanders D.A., McCormick F. The GTPase superfamily: a conserved switch for diverse cell functions. Nature 1990, 348:125-132.
126. Waiczies S., Bendix I., Prozorovski T., Ratner M., Nazarenko I., Pfueller C.F., et al. Geranylgeranylation but not GTP loading determines rho migratory function in T cells. J Immunol 2007, 179:6024-6032.
127. Li X., Liu L., Tupper J.C., Bannerman D.D., Winn R.K., Sebti S.M., et al. Inhibition of protein geranylgeranylation and RhoA/RhoA kinase pathway induces apoptosis in human endothelial cells. J Biol Chem 2002, 277:15309-15316.
128. Ren X.D., Kiosses W.B., Schwartz M.A. Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J 1999, 18:578-585.
129. Puetz S., Lubomirov L.T., Pfitzer G. Regulation of smooth muscle contraction by small GTPases. Physiology (Bethesda) 2009, 24:342-356.
130. Ito M., Nakano T., Erdodi F., Hartshorne D.J. Myosin phosphatase: structure, regulation and function. Mol Cell Biochem 2004, 259:197-209.
131. 2+ sensitization force of smooth muscle contraction. J Biol Chem 2009, 284:21569-21579.
132. 2+ sensitization: rho-associated kinase-mediated phosphorylation of MYPT1 at Thr-855, but not Thr-697. Biochem J 2005, 389:763-774.
133. 2+-sensitization of rat pulmonary artery. Cardiovasc Res 2008, 77:570-579.
134. 2+ sensitization in rabbit smooth muscle. J Physiol 2003, 546:879-889.
135. Ramachandran C., Patil R.V., Combrink K., Sharif N.A., Srinivas S.P. Rho-Rho kinase pathway in the actomyosin contraction and cell-matrix adhesion in immortalized human trabecular meshwork cells. Mol Vis 2011, 17:1877-1890.
136. Schaafsma D., Gosens R., Bos I.S., Meurs H., Zaagsma J., Nelemans S.A. Role of contractile prostaglandins and Rho-kinase in growth factor-induced airway smooth muscle contraction. Respir Res 2005, 6:85.
137. Gosens R., Schaafsma D., Grootte Bromhaar M.M., Vrugt B., Zaagsma J., Meurs H., et al. Growth factor-induced contraction of human bronchial smooth muscle is Rho-kinase-dependent. Eur J Pharmacol 2004, 494:73-76.
138. Schaafsma D., Boterman M., de Jong A.M., Hovens I., Penninks J.M., Nelemans S.A., et al. Differential Rho-kinase dependency of full and partial muscarinic receptor agonists in airway smooth muscle contraction. Br J Pharmacol 2006, 147:737-743.
139. Zhang W., Du L., Gunst S.J. The effects of the small GTPase RhoA on the muscarinic contraction of airway smooth muscle result from its role in regulating actin polymerization. Am J Physiol Cell Physiol 2010, 299:C298-C306.
140. Schaafsma D., Gosens R., Bos I.S., Meurs H., Zaagsma J., Nelemans S.A. Allergic sensitization enhances the contribution of Rho-kinase to airway smooth muscle contraction. Br J Pharmacol 2004, 143:477-484.
141. Schaafsma D., Zuidhof A.B., Nelemans S.A., Zaagsma J., Meurs H. Inhibition of Rho-kinase normalizes nonspecific hyperresponsiveness in passively sensitized airway smooth muscle preparations. Eur J Pharmacol 2006, 531:145-150.
142. 2+ sensitization of bronchial smooth muscle contraction in antigen-induced airway hyperresponsive rats. Br J Pharmacol 1999, 127:597-600.
143. 2+ sensitization in antigen-induced bronchial smooth muscle hyperresponsiveness in mice. Respir Res 2005, 6:4.
144. Iizuka K., Shimizu Y., Tsukagoshi H., Yoshii A., Harada T., Dobashi K., et al. Evaluation of Y-27632, a rho-kinase inhibitor, as a bronchodilator in guinea pigs. Eur J Pharmacol 2000, 406:273-279.
145. Schaafsma D., Bos I.S., Zuidhof A.B., Zaagsma J., Meurs H. Inhalation of the Rho-kinase inhibitor Y-27632 reverses allergen-induced airway hyperresponsiveness after the early and late asthmatic reaction. Respir Res 2006, 7:121.
146. Hashimoto K., Peebles R.S., Sheller J.R., Jarzecka K., Furlong J., Mitchell D.B., et al. Suppression of airway hyperresponsiveness induced by ovalbumin sensitisation and RSV infection with Y-27632, a Rho kinase inhibitor. Thorax 2002, 57:524-527.
147. Chiba Y., Misawa M. Increased expression of G12 and G13 proteins in bronchial smooth muscle of airway hyperresponsive rats. Inflamm Res 2001, 50:333-336.
148. 2+ sensitization in tracheal smooth muscle. Clin Exp Allergy 2008, 38:135-144.
149. Kume H., Ito S., Ito Y., Yamaki K. Role of lysophosphatidylcholine in the desensitization of beta-adrenergic receptors by Ca(2+) sensitization in tracheal smooth muscle. Am J Respir Cell Mol Biol 2001, 25:291-298.
150. 2+ sensitization in airway smooth muscle. Allergol Int 2012, 61:311-322.
151. Robertson T.P., Dipp M., Ward J.P., Aaronson P.I., Evans A.M. Inhibition of sustained hypoxic vasoconstriction by Y-27632 in isolated intrapulmonary arteries and perfused lung of the rat. Br J Pharmacol 2000, 131:5-9.
152. Ward J.P., McMurtry I.F. Mechanisms of hypoxic pulmonary vasoconstriction and their roles in pulmonary hypertension: new findings for an old problem. Curr Opin Pharmacol 2009, 9:287-296.
153. Fukumoto Y., Matoba T., Ito A., Tanaka H., Kishi T., Hayashidani S., et al. Acute vasodilator effects of a Rho-kinase inhibitor, fasudil, in patients with severe pulmonary hypertension. Heart 2005, 91:391-392.
154. Chatterjee M., Tejada M. Phorbol ester-induced contraction in chemically skinned vascular smooth muscle. Am J Physiol 1986, 251:C356-C361.
155. Walsh M.P., Andrea J.E., Allen B.G., Clement-Chomienne O., Collins E.M., Morgan K.G. Smooth muscle protein kinase C. Can J Physiol Pharmacol 1994, 72:1392-1399.
156. 2+ sensitization of myosin light chain phosphorylation in smooth muscle. Biochem J 1996, 318(Pt 2):469-475.
157. Eto M., Ohmori T., Suzuki M., Furuya K., Morita F. A novel protein phosphatase-1 inhibitory protein potentiated by protein kinase C. Isolation from porcine aorta media and characterization. J Biochem 1995, 118:1104-1107.
158. Woodsome T.P., Eto M., Everett A., Brautigan D.L., Kitazawa T. Expression of CPI-17 and myosin phosphatase correlates with Ca(2+) sensitivity of protein kinase C-induced contraction in rabbit smooth muscle. J Physiol 2001, 535:553-564.
159. Bhetwal B.P., An C.L., Fisher S.A., Perrino B.A. Regulation of basal LC20 phosphorylation by MYPT1 and CPI-17 in murine gastric antrum, gastric fundus, and proximal colon smooth muscles. Neurogastroenterol Motil 2011, 23:e425-e436.
160. Kim J.I., Young G.D., Jin L., Somlyo A.V., Eto M. Expression of CPI-17 in smooth muscle during embryonic development and in neointimal lesion formation. Histochem Cell Biol 2009, 132:191-198.
161. Sakai H., Chiba Y., Misawa M. Augmentation of endothelin-1-induced phosphorylation of CPI-17 and myosin light chain in bronchial smooth muscle from airway hyperresponsive rats. Biol Pharm Bull 2006, 29:1897-1899.
162. Eto M., Bock R., Brautigan D.L., Linden D.J. Cerebellar long-term synaptic depression requires PKC-mediated activation of CPI-17, a myosin/moesin phosphatase inhibitor. Neuron 2002, 36:1145-1158.
163. Zemlickova E., Johannes F.J., Aitken A., Dubois T. Association of CPI-17 with protein kinase C and casein kinase I. Biochem Biophys Res Commun 2004, 316:39-47.
164. 2+ in isolated contractile lymphatics. J Vis Exp 2011.
165. Watanabe Y., Ito M., Kataoka Y., Wada H., Koyama M., Feng J., et al. Protein kinase C-catalyzed phosphorylation of an inhibitory phosphoprotein of myosin phosphatase is involved in human platelet secretion. Blood 2001, 97:3798-3805.
166. 2+ sensitization in triton X-100-demembranated rabbit arterial smooth muscle. J Physiol 1999, 520(Pt 1):139-152.
167. Kitazawa T., Polzin A.N., Eto M. CPI-17-deficient smooth muscle of chicken. J Physiol 2004, 557:515-528.
168. Mukherjee SSP, Willis RE, Pressley T, Trice J, Perez-Zoghbi JF. Protein kinase C activation induces Ca2+ oscillations, Ca2+ sensitization and contraction in smooth muscle cells of small intrapulmonary airways. Manuscript in Preparation. 2012.
169. Dubois T., Howell S., Zemlickova E., Learmonth M., Cronshaw A., Aitken A. Novel in vitro and in vivo phosphorylation sites on protein phosphatase 1 inhibitor CPI-17. Biochem Biophys Res Commun 2003, 302:186-192.
170. Kitazawa T., Eto M., Woodsome T.P., Brautigan D.L. Agonists trigger G protein-mediated activation of the CPI-17 inhibitor phosphoprotein of myosin light chain phosphatase to enhance vascular smooth muscle contractility. J Biol Chem 2000, 275:9897-9900.
171. Koyama M., Ito M., Feng J., Seko T., Shiraki K., Takase K., et al. Phosphorylation of CPI-17, an inhibitory phosphoprotein of smooth muscle myosin phosphatase, by Rho-kinase. FEBS Lett 2000, 475:197-200.
172. Pang H., Guo Z., Su W., Xie Z., Eto M., Gong M.C. RhoA-Rho kinase pathway mediates thrombin- and U-46619-induced phosphorylation of a myosin phosphatase inhibitor, CPI-17, in vascular smooth muscle cells. Am J Physiol Cell Physiol 2005, 289:C352-C360.
173. Huang J., Mahavadi S., Sriwai W., Hu W., Murthy K.S. Gi-coupled receptors mediate phosphorylation of CPI-17 and MLC20 via preferential activation of the PI3K/ILK pathway. Biochem J 2006, 396:193-200.
174. Eto M., Kitazawa T., Yazawa M., Mukai H., Ono Y., Brautigan D.L. Histamine-induced vasoconstriction involves phosphorylation of a specific inhibitor protein for myosin phosphatase by protein kinase C alpha and delta isoforms. J Biol Chem 2001, 276:29072-29078.
175. Obara K., Ukai K., Ishikawa T. Mechanism of potentiation by tea epigallocatechin of contraction in porcine coronary artery: the role of protein kinase Cdelta-mediated CPI-17 phosphorylation. Eur J Pharmacol 2011, 668:414-418.
176. Obara K., Ito Y., Shimada H., Nakayama K. The relaxant effect of okadaic acid on canine basilar artery involves activation of PKCalpha and phosphorylation of the myosin light chain at Thr-9. Eur J Pharmacol 2008, 598:87-93.
177. 2+ sensitization of contraction in arterial smooth muscle. Circ Res 2007, 100:121-129.
178. Mauban J.R., Lamont C., Balke C.W., Wier W.G. Adrenergic stimulation of rat resistance arteries affects Ca(2+) sparks, Ca(2+) waves, and Ca(2+) oscillations. Am J Physiol Heart Circ Physiol 2001, 280:H2399-H2405.
179. 2+ sensitization. Am J Physiol Lung Cell Mol Physiol 2007, 293:L1000-L1011.
180. 2+ oscillations induced by 5-HT and KCl. J Gen Physiol 2005, 125:555-567.
181. Perez-Zoghbi J.F., Karner C., Ito S., Shepherd M., Alrashdan Y., Sanderson M.J. Ion channel regulation of intracellular calcium and airway smooth muscle function. Pulm Pharmacol Ther 2009, 22:388-397.
182. Perez J.F., Sanderson M.J. The frequency of calcium oscillations induced by 5-HT, ACH, and KCl determine the contraction of smooth muscle cells of intrapulmonary bronchioles. J Gen Physiol 2005, 125:535-553.
183. Eto M., Kitazawa T., Matsuzawa F., Aikawa S., Kirkbride J.A., Isozumi N., et al. Phosphorylation-induced conformational switching of CPI-17 produces a potent myosin phosphatase inhibitor. Structure 2007, 15:1591-1602.
184. Dakshinamurti S., Mellow L., Stephens N.L. Regulation of pulmonary arterial myosin phosphatase activity in neonatal circulatory transition and in hypoxic pulmonary hypertension: a role for CPI-17. Pediatr Pulmonol 2005, 40:398-407.
185. Goto K., Chiba Y., Sakai H., Misawa M. Glucocorticoids inhibited airway hyperresponsiveness through downregulation of CPI-17 in bronchial smooth muscle. Eur J Pharmacol 2008, 591:231-236.
186. Morin C., Fortin S., Cantin A.M., Rousseau E. Docosahexaenoic acid derivative prevents inflammation and hyperreactivity in lung: implication of PKC-potentiated inhibitory protein for heterotrimeric myosin light chain phosphatase of 17 kD in asthma. Am J Respir Cell Mol Biol 2011, 45:366-375.