Muscarinic drugs regulate the PKG-II-dependent phosphorylation of M₃ muscarinic acetylcholine receptors at plasma membranes from airway smooth muscle

References

• Mak JC, Barnes PJ. Autoradiographic visualization of muscarinic receptor subtypes in human and guinea pig lung. Am Rev Respir Dis 1990;141:1559–68
   PubMed Web of Science ®Google Scholar
• Lucchesi PA, Scheid CR, Romano FD, et al. Ligand binding and G protein coupling of muscarinic receptors in airway smooth muscle. Am J Physiol 1990;258:C730–8
   PubMed Web of Science ®Google Scholar
• Haddad EB, Landry Y, Gies JP. Muscarinic receptor subtypes in guinea pig airways. Am J Physiol 1991;261:L327–33
   PubMed Web of Science ®Google Scholar
• Murad F, Kimura H. Cyclic nucleotide levels in incubations of guinea pig trachea. Biochim Biophys Acta 1974;343:275–86
   PubMed Web of Science ®Google Scholar
• Katsuki S, Murad F. Regulation of adenosine cyclic 3′, 5′-monophosphate and guanosine cyclic 3′,5′-monophosphate levels and contractility in bovine tracheal smooth muscle. Mol Pharmacol 1977;13:330–41
   PubMed Web of Science ®Google Scholar
• Guerra de González L, Misle A, Pacheco G, et al. Effects of 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one (ODQ) and N omega (ω)-nitro-L-arginine methyl ester (NAME) on cyclic GMP levels during muscarinic activation of tracheal smooth muscle. Biochem Pharmacol 1999;58:563–9
   PubMed Web of Science ®Google Scholar
• Alfonzo MJ, Placeres-Uray F, Hassan-Soto W, et al. Two guanylylcyclases regulated the muscarinic activation of airway smooth muscle. In: Sugi H, ed. Current basic and pathological approaches to the function of muscle cells and tissues-from molecules to humans. Croatia: InTech; 2012:113–32
   Google Scholar
• Uray FP, de Alfonzo RG, de Becemberg IL, Alfonzo MJ. Muscarinic agonists acting through M2 acetylcholine receptors stimulate the migration of an NO-sensitive guanylyl cyclase to the plasma membrane of bovine tracheal smooth muscle. J Recept Signal Transduct Res 2010;30:10–23
   PubMed Web of Science ®Google Scholar
• Alfonzo MJ, Becemberg IL, Villaroel SS, et al. Two opposite signal transducing mechanisms regulate a G-protein-coupled guanylyl cyclase. Arch Biochem Biophys 1998;350:19–25
   PubMed Web of Science ®Google Scholar
• Alfonzo MJ, Guerra de González L, Villaroel SS, et al. Signal transduction pathways through mammalian guanylyl cyclases. New Adv Cardiovasc Physiol Pharmacol 1998;1184:147–72
   Google Scholar
• Borges A, Villarroel SS, Winand NJ, et al. Molecular and biochemical characterization of a CNP-sensitive guanylyl cyclase in bovine tracheal smooth muscle. Am J Respir Cell Mol Biol 2001;25:98–103
   PubMed Web of Science ®Google Scholar
• Bruges G, Borges A, Villarroel SS, et al. Coupling of M3 acetylcholine receptor to Gq16 activates a natriuretic peptide receptor guanylyl cyclase. J Recept Signal Transduct Res 2007;27:189–216
   PubMed Web of Science ®Google Scholar
• Misle AJ, Lippo de Becemberg I, Gonzalez de Alfonzo R, Alfonzo MJ. Methoctramine binding sites sensitive to alkylation on muscarinic receptors from tracheal smooth muscle. Biochem Pharmacol 1994;48:191–5
   PubMed Web of Science ®Google Scholar
• Alfonzo MJ, González de Alfonzo R, Alfonzo-González MA, Lippo de Bécemberg I. Cyclic GMP regulates M3AChR activity at plasma membranes from airway smooth muscle. Mol Membrane Biol 2013;30:403–17
   PubMed Web of Science ®Google Scholar
• González de Alfonzo R, Bécemberg IL, Alfonzo MJ. A Ca2+/Ca M dependent protein kinase associated with Ca2+ transport in sarco(endo)plasmic vesicles from tracheal smooth muscle. Life Sci 1996;58:18–24
   Web of Science ®Google Scholar
• Fields JZ, Roeske WR, Morkin E, Yamamura HI. Cardiac muscarinic cholinergic receptors. Biochemical identification and characterization. J Biol Chem 1978;253:3251–8
   PubMed Web of Science ®Google Scholar
• Bennett JP Jr, Yamamura HI. Neurotransmitter, hormone, or drug receptor binding methods. In: Yamamura HI, Enna SJ, Kuhar MJ, eds. Neurotransmitter receptor binding. New York: Raven Press; 1985:61–90
   Google Scholar
• Corbin JD, Reissman EM. Assay of cyclic AMP-dependent protein kinases. Meth Enzymol 1974;38:287–90
   PubMedGoogle Scholar
• Vardanis A. A unique cyclic nucleotide-dependent protein kinase. J Biol Chem 1980;255:7238–43
   PubMed Web of Science ®Google Scholar
• Clausen T. Measurement of 32P activity in a liquid scintillation counter without the use of scintillator. Anal Biochem 1968;22:70–3
   PubMed Web of Science ®Google Scholar
• Peterson GL, Schimerlik MI. Large scale preparation and characterization of membrane-bound and detergent-solubilized muscarinic acetylcholine receptor from pig atria. Prep Biochem 1984;14:33–74
   PubMed Web of Science ®Google Scholar
• Bensadoun A, Weinstein D. Assay of proteins in the presence of interfering materials. Anal Biochem 1976;70:241–50
   PubMed Web of Science ®Google Scholar
• Perez-Zoghbi JF, Bai Y, Sanderson MJ. Nitric oxide induces airway smooth muscle cell relaxation by decreasing the frequency of agonist-induced Ca2+ oscillations. J Gen Physiol 2010;135:247–59
   PubMed Web of Science ®Google Scholar
• Butt E, Pöhler D, Genieser HG, et al. Inhibition of cyclic GMP-dependent protein kinase-mediated effects by (Rp)-8-bromo-PET-cyclic GMPS. Br J Pharmacol 1995;116:3110–16
   PubMed Web of Science ®Google Scholar
• Butt E, Nolte C, Schulz S, et al. Analysis of the functional role of cGMP-dependent protein kinase in intact human platelets using a specific activator 8-para-chlorophenylthio-cGMP. Biochem Pharmacol 1992;43:2591–600
   PubMed Web of Science ®Google Scholar
• Gamm DM, Francis SH, Angelotti TP, et al. The type II isoform of cGMP-dependent protein kinase is dimeric and possesses regulatory and catalytic properties distinct from the type I isoforms. J Biol Chem 1995;270:27380–8
   PubMed Web of Science ®Google Scholar
• Vaandrager AB, Edixhoven M, Bot AG, et al. Endogenous type II cGMP-dependent protein kinase exists as a dimer in membranes and can be functionally distinguished from the type I isoforms. J Biol Chem 1997;272:11816–23
   PubMed Web of Science ®Google Scholar
• Caulfield MP, Birdsall NJ. International Union of Pharmacology. XVII. Classification of muscarinic acetylcholine receptors. Pharmacol Rev 1998;50:279–90
   PubMed Web of Science ®Google Scholar
• Eller M, Jarv J. Two-step isomerization of quinuclidinyl benzilate-muscarinic receptor complex. Neurochem Int 1998;12:285–9
   Google Scholar
• Jakubik J, El-Fakahany EE, Tucek S. Evidence for a tandem two-site model of ligand binding to muscarinic acetylcholine receptors. J Biol Chem 2000;275:18836–44
   PubMed Web of Science ®Google Scholar
• Zeng Y, Wess J. Identification and molecular characterization of m3 muscarinic receptor dimmers. J Biol Chem 1999;274:19487–97
   PubMed Web of Science ®Google Scholar
• Palczewski K. Oligomeric forms of G-protein coupled receptors (GPCRs). Trends Biochem Sci 2010;35:595–600
   PubMed Web of Science ®Google Scholar
• Alvarez-Curto E, Ward RJ, Pediani JD, Milligan G. Ligand regulation of the quaternary organization of cell surface M3 muscarinic acetylcholine receptors analyzed by fluorescence resonance energy transfer (FRET) imaging and homogeneous time-resolved FRET. J Biol Chem 2010;285:23318–30
   PubMedGoogle Scholar
• McMillin, SM, Heusel, M, Liu T, et al. Structural basis of M3 muscarinic receptor dimer/oligomer formation. J Biol Chem 2011;286:28584–98
   PubMed Web of Science ®Google Scholar
• Francis SH, Busch JL, Jackie D, Corbin JD. cGMP-dependent protein kinases and cGMP phosphodiesterases in nitric oxide and cGMP action. Pharmacol Rev 2010;62:525–63
   PubMed Web of Science ®Google Scholar
• Burgoyne RD. The loss of muscarinic acetylcholine receptors in synaptic membranes under phosphorylating conditions is dependent on calmodulin. FEBS Lett 1981;127:144–8
   PubMed Web of Science ®Google Scholar
• Sibley DR, Strasser RH, Benovic JL, et al. Phosphorylation/dephosphorylation of the beta-adrenergic receptor regulates its functional coupling to adenylate cyclase and subcellular distribution. Proc Natl Acad Sci USA 1986;83:9408–12
   PubMed Web of Science ®Google Scholar
• Bundey RA, Nahorski SR. Homologous and heterologous uncoupling of muscarinic M3 and 1B adrenoceptors to G q/11 in SH-SY5Y human neuroblastoma cells. Br J Pharmacol 2001;134:257–64
   PubMed Web of Science ®Google Scholar
• Butcher AJ, Kong KC, Prihandoko R, Tobin AB. Physiological role of G-protein coupled receptor phosphorylation. Handb Exp Pharmacol 2012;208:79–94
   PubMedGoogle Scholar
• Tobin AB. G-protein-coupled receptor phosphorylation: where, when and by whom. Br J Pharmacol 2008;153:S167–76
   PubMed Web of Science ®Google Scholar
• Hosey MM, Benovic JL, DebBurman SK, Richardson RM. Multiple mechanisms involving protein phosphorylation are linked to desensitization of muscarinic receptors. Life Sci 1995;56:951–5
   PubMed Web of Science ®Google Scholar
• Jiansong L, Busillo JM, Benovic JL. M3 muscarinic acetylcholine receptor-mediated signaling is regulated by distinct mechanisms. Mol Pharmacol 2008;74:338–47
   PubMed Web of Science ®Google Scholar
• Hosey MM. Diversity of structure, signaling and regulation within the family of muscarinic cholinergic receptors. FASEB J 1992;6:845–52
   PubMed Web of Science ®Google Scholar
• Kennelly PJ, Krebs EG. Consensus sequences as substrate specificity determinants for protein kinases and protein phosphatases. J Biol Chem 1991;266:15555–8
   PubMed Web of Science ®Google Scholar
• Kemp BE, Pearson RB. Protein kinase recognition sequence motifs. Trends Biochem Sci 1990;16:342–6
   Google Scholar
• Rovati GE, Nicosia S. Lower efficacy: interaction with an inhibitory or partial agonism? TIPS 1994;15:140–4
   PubMed Web of Science ®Google Scholar
• Michel AD, Stefanich E, Whiting RL. Direct labeling of rat M3-muscarinic receptors by [3H]-4DAMP. Eur J Pharmacol 1989;166:459–66
   PubMed Web of Science ®Google Scholar
• Dowling MR, Willets JM, Budd DC, et al. A single point mutation (N514Y) in the human M3 muscarinic acetylcholine receptor reveals differences in the properties of antagonists: evidence for differential inverse agonism. JPET 2006;317:1134–42
   PubMed Web of Science ®Google Scholar
• Cohen P. The structure and regulation of protein phosphatases. Annu Rev Biochem 1989;58:453–508
   PubMed Web of Science ®Google Scholar
• Bialojan C, Takai A. Inhibitory effect of a marine-sponge toxin, okadaic acid, on protein phosphatases: specificity and kinetics. Biochem J 1988;256:283–90
   PubMed Web of Science ®Google Scholar
• Krause M, Pedarzani P. A protein phosphatase is involved in the cholinergic suppression of the Ca2+-activated K+ current sIAHP in hippocampal pyramidal neurons. Neuropharmacology 2000;39:1274–83
   PubMed Web of Science ®Google Scholar
• Herzig S, Meier A, Pfeiffer M, Neumann J. Stimulation of protein phosphatases as a mechanism of the muscarinic-receptor-mediated inhibition of cardiac L-type Ca2+ channels. Plugers Arch 1995;429:531–8
   PubMed Web of Science ®Google Scholar
• Wu G, Bogatkevich GS, Mukhin YV, et al. Identification of G binding sites in the third intracellular loop of the M3-muscarinic receptor and their role in receptor regulation. J Biol Chem 2000;275:9026–34
   PubMed Web of Science ®Google Scholar
• Simon V, Guidry J, Gettys TW, et al. The proto-oncogene SET interacts with muscarinic receptors and attenuates receptor signaling. J Biol Chem 2006;281:40310–20
   PubMed Web of Science ®Google Scholar
• Borroto-Escuela DO, Correia PA, Romero-Fernandez W, et al. Muscarinic receptor family interacting proteins: role in receptor function. J Neurosci Methods 2011;195:161–9
   PubMed Web of Science ®Google Scholar
• Pitcher JA, Payne ES, Csortos C, et al. The G-protein-coupled receptor phosphatase: a protein phosphatase type 2A with a distinct subcellular distribution and substrate specificity. Proc Natl Acad Sci USA 1995;92:8343–7
   PubMed Web of Science ®Google Scholar
• Simon V, Oner SS, Cohen-Tannoudji J, et al. Influence of the accessory protein SET on M3 muscarinic receptor phosphorylation and G protein coupling. Mol Pharmacol 2012;82:17–26
   PubMed Web of Science ®Google Scholar
• Schmidt C, Li B, Bloodworth L, et al. Random mutagenesis of the M3 muscarinic acetylcholine receptor expressed in yeast: identification of point mutations that “silence” a constitutively active mutant M3 receptor and greatly impair receptor/G protein coupling. J Biol Chem 2003;278:30248–60
   PubMed Web of Science ®Google Scholar
• Kistemaker LE, Oenema TA, Meurs H, Gosens R. Regulation of airway inflammation and remodeling by muscarinic receptors: perspectives on anticholinergic therapy in asthma and COPD. Life Sci 2012;91:1126–33
   PubMed Web of Science ®Google Scholar