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

References

• Lucas KA., Pitari GM., Kazerounian S, Ruiz-Stewart I, Park J, Schulz S, Chepenik KP and Waldman SA. Guanylyl Cyclases and Signaling by Cyclic GMP. Pharmacol Rev 2000;52:375–413.
   PubMed Web of Science ®Google Scholar
• Roy B, Garthwaite J. Nitric oxide activation of guanylyl cyclase in cells revisited. Proc Natl Acad Sci USA 2006;103:12185–90.
   PubMed Web of Science ®Google Scholar
• Cary SP, Winger JA, Marletta MA. Tonic and acute nitric oxide signaling through soluble guanylate cyclase is mediated nonheme nitric oxide, ATP, and GTP. Proc Natl Acad Sci USA 2005;102:1306–69.
   PubMed Web of Science ®Google Scholar
• Papapetropoulos A, Simoes DC, Xanthou G, Roussos C, Gratziou C. Soluble guanylyl cyclase expression is reduced in allergic asthma. Am J Physiol Lung Cell Mol Physiol 2006;290:L179–L184.
   Web of Science ®Google Scholar
• Gupta G, Azam M, Yang L, Danziger RS. The β2 subunit inhibits stimulation of the alpha1/beta1 form of soluble guanylyl cyclase by nitric oxide. Potential relevance to regulation of blood pressure. J Clin Invest 1997;100:1488–92.
   PubMed Web of Science ®Google Scholar
• Sharina IG, Krumenacker JS, Martin E, Murad F. Genomic organization of α1 and β1 subunits of the mammalian soluble guanylyl cyclase genes. Proc Natl Acad Sci US 2000;97:10878–83.
   PubMed Web of Science ®Google Scholar
• Jiang Y, Stojilkovic SS. Molecular cloning and characterization of soluble of alpha1-soluble guanylyl cyclase gene promoter in rat pituitary cells J Mol Endocrinol 2006;37:503–15.
   PubMed Web of Science ®Google Scholar
• Pyriochou A, Papapetropoulos A. Soluble guanylyl cyclase: more secrets revealed. Cell Signal 2005;17:407–13.
   PubMed Web of Science ®Google Scholar
• Alfonzo MJ, Lippo de Becemberg L, Sanchez de Villarroel S, Napoleon de Herrera V, Misle AJ, Gonzalez de Alfonzo R. Two opposite transducing mechanisms regulate a G protein-coupled guanylyl cyclase. Arch Biochem Biophys 1998;350:19–25.
   PubMed Web of Science ®Google Scholar
• Bruges G., Borges A. Sánchez de Villarroel S, Lippo de Bécemberg I., Francis de Toba G., Pláceres F., González de Alfonzo R., Alfonzo MJ. 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
• Guerra de González L, Misle A, Pacheco G, Napoleón de Herrera V. González del Alfonzo R, Lippo de Becemberg I, Alfonzo MJ. Effects of 1H- [1,2,4]Oxadiazolo[4,3-]quinoxalin-1-one (ODQ) and N(6)-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
• Gonzalez de Alfonzo R, Lippo de Becemberg I, Alfonzo MJ. A Ca 2+/CAM protein kinase associated with Ca2+ transport in sarco(endo)plasmic vesicles from tracheal smooth muscle. Life Sci 1996;58:1403–12.
   PubMed Web of Science ®Google Scholar
• Lippo de Bécemberg I, Peña de Aguilar E, Camarillo I, González de Alfonzo R, Alfonzo MJ. Muscarinic agents modify kinetics properties of membrane-bound guanylyl cyclase activity. FEBS Lett 1989;253:16–22.
   PubMed Web of Science ®Google Scholar
• Hanoune J, Stengel D, Lacombe ML. Proteolytic activation and solubilization of adenylate and guanylate cyclases. Mol Cell Endocrinol 1983;31:21–41.
   PubMed Web of Science ®Google Scholar
• Serfass L, Carr HS, Aschenbrenner LM, Burstyn JN. Calcium ion downregulates soluble guanylyl cyclase activity: evidence for a two-metal ion catalytic mechanism. Arch Biochem Biophys 2001;387:47–56.
   PubMed Web of Science ®Google Scholar
• Tseng CM, Tabrizi-Fard MA, Fung HL. Differential sensitivity among nitric oxide donors toward ODQ-mediated inhibition of vascular relaxation. J Pharmacol Exp Ther 2000;292:737–42.
   PubMed Web of Science ®Google Scholar
• Lowry Oh, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265–75.
   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
• Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970;227:680–5.
   PubMed Web of Science ®Google Scholar
• Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 1979;76:4350−4.
   PubMed Web of Science ®Google Scholar
• Lippo de Bécemberg I, Herrera V, Pérez-Ayuso E, Alfonzo MJ. Effects of cholinergic agents on rat liver plasma membrane guanylate cyclase. FEBS Lett 1982;137:303–6.
   PubMed Web of Science ®Google Scholar
• Kaufmann SH, Ewing CM, Shaper JH. The erasable Western blot. Anal Biochem 1987;161:89–95.
   PubMed Web of Science ®Google Scholar
• Lippo de Becemberg I, Ponte-Sucre A, Alfonzo MJ. Biochemical and pharmacological characterization of octylglucoside-solubilized muscarinic receptors derived from bovine tracheal smooth muscle. Arch Venez Farmacol y Terap 1989;5:244–56.
   Google Scholar
• McIntosh H, Blazynshi C. Muscarnic receptor stimulated GTPase activity in synaptic membranes from bovine retina. J Neurochem 1992;29:210–5.
   Google Scholar
• Sankary RM, Jones CA, Madison JM, Brown JK. Muscarinic cholinergic inhibition of cyclic AMP accumulation in airway smooth muscle. Role of a pertussis toxin-sensitive protein. Am Rev Respir Dis 1988;138:145–50.
   PubMed Web of Science ®Google Scholar
• Roy B, Halvey EJ, Garthwaite J. An enzyme-linked receptor mechanism for nitric oxide-activated guanylyl cyclase. J Biol Chem. 2008;283:18841–51.
   PubMed Web of Science ®Google Scholar
• Misle AJ, Lippo de Bécemberg I, González 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
• Chinkers M, Garbers DL.Signal transduction by guanylyl cyclase Ann Rev Biochem. 1991;60:553–75.
   PubMed Web of Science ®Google Scholar
• Ding KH, Abdel-Latif AA. Actions of C-type natriuretic peptide and sodium nitroprusside on carbachol-stimulated inositol phosphate formation and contraction in ciliary and iris sphincter smooth muscles. Invest Opthalmol Vis Sci 1997;38:2629–38.
   PubMed Web of Science ®Google Scholar
• Garthwaite J, Southam E, Boulton CL, Nielsen EB, Schmidt K, Mayer B. Potent and selective inhibition of oxide nitric-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-α]quinoxalin-1-one. Mol Pharmacol 1995;48:84–8.
   Web of Science ®Google Scholar
• Krumenacker JS, Hanafy KA, Murad F. Regulation of nitric oxide and soluble guanylyl cyclase. Brain Res Bull 2004;62:505–51.
   PubMed Web of Science ®Google Scholar
• Levine SM, Steiner AL, Earp HS, Meissner G. Particulate guanylate cyclase of skeletal muscle: Effects of Ca2+ and other divalent cations on enzyme activity. Biochem Biophys Acta 1979;566:171–82.
   PubMedGoogle Scholar
• Sulakhe SJ, Leung NL, Sulakhe V. Interactions of divalent cations and nucleotides with solubilized cardic guanylate cyclase. Enzyme 1977;22:141–4.
   PubMedGoogle Scholar
• Zabel U, Weeger M, La M, Schmidt HH. Human soluble guanylate cyclase functional expression and revised isoenzyme family J Biochem 1998;1:51–7.
   Google Scholar
• Sharina IG, Krumenacker JS, Martin E, Murad F. Genomic organization of alpha1 and beta 1 subunits of the mammalian soluble guanylyl cyclase genes. Proc Natl Acad Sci USA 2000;97:10878–83.
   PubMed Web of Science ®Google Scholar
• Friebe A, Koesling D. Regulation of nitric oxide-sensitive guanylyl cyclase. Circ Res 2003;93:96–105.
   PubMed Web of Science ®Google Scholar
• Xia T, Dimitropoulou C, Zeng J, Antonova GN, Snead C, Venema RC, Fulton D, Qian S, Patterson C, Papapetropoulos A, Catravas JD. Chaperone-dependent E3 ligase CHIP ubiquitinates and mediates proteasomal degradation of soluble guanylyl cyclase. Am J Physiol Heart Circ Physiol 2007;293:H3080–H3087.
   Web of Science ®Google Scholar
• Meurer S. Pioch S, GrossS, Müller-Esterl W. Reactive oxygen species induce tyrosine phosphorylation of and Src kinase recruitment to NO-sensitive guanylyl cyclase. J Biol Chem 2005;280:33149–56.
   PubMed Web of Science ®Google Scholar
• Bellinghan M, Evans TJ. The α1β1 isoform of guanylyl cyclase mediates plasma membrane localized nitric oxide signaling. Cell Signal 2007;19:2183–93.
   PubMed Web of Science ®Google Scholar
• Russwurm M, Wittau N, Koesling D. Guanylyl cyclase/PSD-95 interaction targeting of the nitric oxide-sensitive alpha2beta1 guanylyl cyclase to synaptic membranes. J Biol Chem 2001;276:44647–52.
   PubMed Web of Science ®Google Scholar
• Feussner M, Richter H, Baum O, Gossrau R.Association of soluble guanylate cyclase with the sarcolemma of mammalian skeletal muscle fibers Acta Histochem 2001;103:265–77.
   PubMed Web of Science ®Google Scholar
• Jones JD, Carney ST, Vrana KE, Norford DC, Howlett AC. Cannabinoid receptor-mediated migration of NO-sensitive guanylyl cyclase and production of cyclic GMP in neuronal cells. Neuropharmacol 2008;54:23–30.
   PubMed Web of Science ®Google Scholar
• AgullóL, Garcia-Dorado D, Escalona N, Ruiz-Meana M, Mirabet M, Inserte J, Soler-Soler J. Membrane association of nitric oxide-sensitive guanylyl cyclase in cardiomyocytes. Cardiovasc Res 2005;68:65–74.
   PubMed Web of Science ®Google Scholar
• Zabel U, Kleinschnitz C, Oh P, Nedvetsky P, Smolenski A, Müller H, Kronich P, Kugler P, Walter U, Schnitzer JE, Schmidt HH. Calcium-dependent membrane association sensitizes soluble guanylyl cyclase to nitric oxide. Nat Cell Biol 2002;4:307–11.
   PubMed Web of Science ®Google Scholar
• Misle AJ, Lippo de Bécemberg I, González de Alfonzo R, Alfonzo MJ. Subcellular distribution and pharmacological characterization of muscarinic receptors in tracheal smooth muscle. Acta Cient Venez 1995;46:166–73.
   PubMedGoogle Scholar
• Guerra de González L, González del Alfonzo R, Lippo de Becemberg I, Alfonzo MJ. Cyclic nucleotide-dependent phosphodiesterases (PDEI) inhibition by muscarinic antagonists in bovine tracheal smooth muscle. Biochem Pharmacol 2004;68:651–58.
   PubMed Web of Science ®Google Scholar
• Guerra de González L, Lippo de Bécemberg I, González de Alfonzo R, Alfonzo MJ. La activación muscarínica del músculo liso de vías aéreas. Arch Venez Farmacol Terap 1995;15:20–4.
   Google Scholar
• Borges A, de Villarroel SS, Winand NJ, de Bécenberg IL, Alfonzo MJ, de Alfonzo RG. 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
• Michal P, El-Fakahany EE, Dolez V. Muscarinic M2 receptors directly activate Gq/11 and Gs G-proteins. J Pharmacol Exp Ther 2007;320:607–14.
   PubMed Web of Science ®Google Scholar
• Ashkenazi A, Winslow JW, Peralta EG, Peterson GL, Schimerlik MI, Capon DJ, Ramachandran J. An M2 muscarinic receptor subtype coupled to both adenylyl cyclase and phasphoinositide turnover. Science 1987;238:672–5.
   PubMed Web of Science ®Google Scholar
• Koesling D, Friebe A. Soluble guanylyl cyclase: structure and regulation. Rev Physiol Biochem Pharmacol 1999;135:41–65.
   PubMedGoogle Scholar
• Ma X, Sayed N, Baskaran P, Beuve A, Van den Akker F. PAS-mediated dimerization of soluble guanylyl cyclase revealed by signal transduction histidine kinase domain crystal structure. J Biol Chem 2008;283:1167–78.
   PubMed Web of Science ®Google Scholar