Regulator of G-protein signaling 6 (RGS6) in cardiology and oncology
2015; Elsevier BV; Volume: 187; Linguagem: Inglês
10.1016/j.ijcard.2015.03.278
ISSN1874-1754
Autores Tópico(s)Cardiac electrophysiology and arrhythmias
ResumoAcetylcholine (ACh) [ 1 Daliry A. Caldas I.S. de Figueiredo Diniz L. Torres R.M. Talvani A. Bahia M.T. de Carvalho A.C. Anti-adrenergic and muscarinic receptor autoantibodies in a canine model of Chagas disease and their modulation by benznidazole. Int. J. Cardiol. Jan 1 2014; 170: e66-e67 Abstract Full Text Full Text PDF PubMed Scopus (10) Google Scholar , 2 Tsai W.C. Lee T.I. Chen Y.C. Kao Y.H. Lu Y.Y. Lin Y.K. Chen S.A. Chen Y.J. Testosterone replacement increases aged pulmonary vein and left atrium arrhythmogenesis with enhanced adrenergic activity. Int. J. Cardiol. Sep 2014; 176: 110-118 Abstract Full Text Full Text PDF PubMed Scopus (27) Google Scholar , 3 Hishikari K. Kuwahara T. Takahashi A. Isobe M. Severe coronary artery spasm during radiofrequency ablation for atrial fibrillation. Int. J. Cardiol. Apr 1 2014; 172: e513-e515 Abstract Full Text Full Text PDF PubMed Scopus (14) Google Scholar , 4 Petersen J.W. Mehta P.K. Kenkre T.S. Anderson R.D. Johnson B.D. Shufelt C. 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Aug 20 2014; 175: 446-450 Abstract Full Text Full Text PDF PubMed Scopus (26) Google Scholar ] is an important neurotransmitter expressed in the central and peripheral nervous systems, in several non-neuronal cell types and also in most common cancer cells where it has been reported that the growth of tumor cells was accelerated via activation of muscarinic-acetylcholine receptors (mAChRs) [ [16] Song P. Sekhon H.S. Lu A. Arredondo J. Sauer D. Gravett C. Mark G.P. Grando S.A. Spindel E.R. M3 muscarinic receptor antagonists inhibit small cell lung carcinoma growth and mitogen activated protein kinase phosphorylation induced by acetylcholine secretion. Cancer Res. Apr 15 2007; 67: 3936-3944 Crossref PubMed Scopus (117) Google Scholar ]. Muscarinic receptors are G protein-coupled receptors (GPCRs), and as such they activate heterotrimeric G proteins by catalyzing GDP dissociation from the Gα subunit and consequently promoting GTP binding [ 17 Tuomi J.M. Chidiac P. Jones D.L. Evidence for enhanced M3 muscarinic receptor function and sensitivity to atrial arrhythmia in the RGS2-deficient mouse. Am. J. Physiol. Heart Circ. Physiol. Feb 2010; 298: H554-H561 Crossref PubMed Scopus (43) Google Scholar , 18 Lyu J.H. Park D.W. Huang B. Kang S.H. Lee S.J. Lee C. Bae Y.S. Lee J.G. Baek S.H. RGS2 suppresses breast cancer cell growth via a MCPIP1-dependent pathway. J. Cell. Biochem. Sep 2014; 4 Crossref Scopus (50) Google Scholar ]. Regulator of G-protein signaling 6 (RGS6) is a member of a large family of proteins that all regulate signaling through GPCRs by accelerating guanosine triphosphatase (GTPase) [ 19 Li J. Zhang D.S. Ye J.C. Li C.M. Qi M. Liang D.D. Xu X.R. Xu L. Liu Y. Zhang H. Zhang Y.Y. Deng F.F. Feng J. Shi D. Chen J.J. Li L. Chen G. Sun Y.F. Peng L.Y. Chen Y.H. Dynamin-2 mediates heart failure by modulating Ca2+-dependent cardiomyocyte apoptosis. Int. J. Cardiol. 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Fisher R.A. RGS proteins in heart: brakes on the vagus. Front. Physiol. Apr 13 2012; 3: 95 Crossref PubMed Scopus (29) Google Scholar ] and it is involved in parasympathetic control of the heart and IKACh signaling [ [23] Yang J. Huang J. Maity B. Gao Z. Lorca R.A. Gudmundsson H. Li J. Stewart A. Swaminathan P.D. Ibeawuchi S.R. Shepherd A. Chen C.K. Kutschke W. Mohler P.J. Mohapatra D.P. Anderson M.E. Fisher R.A. RGS6, a modulator of parasympathetic activation in heart. Circ. Res. Nov 26 2010; 107: 1345-1349 Crossref PubMed Scopus (89) Google Scholar ] having an essential role in desensitization and rapid deactivation of G protein-coupled inwardly rectifying K(+) (GIRK)-mediated IKACh in atrial myocytes serving as a GTPase Activating protein (GAP) for heterotrimeric G(i/o) proteins. Several recent studies have indicated that the duration of G protein signaling from the m2AChRs to the IKACh plays a critical role in determining the extent of the parasympathetic heart rate inhibition being RGS proteins the negative regulators of m2AChRs-IKACh signaling [ [24] Posokhova E. Ng D. Opel A. Masuho I. Tinker A. Biesecker L.G. Wickman K. Martemyanov K.A. Essential role of the m2R-RGS6-IKACh pathway in controlling intrinsic heart rate variability. PLoS One. Oct 29 2013; 8: e76973 Crossref PubMed Scopus (33) Google Scholar ]. Delayed deactivation of IKACh in RGS6-deficient atrial pacemaker cells slows channel closing, prolonging membrane hyperpolarization leading to dramatic increase in ACh-induced bradycardia, to enhanced inhibition of spontaneous action potential firing in SAN cells [ [23] Yang J. Huang J. Maity B. Gao Z. Lorca R.A. Gudmundsson H. Li J. Stewart A. Swaminathan P.D. Ibeawuchi S.R. Shepherd A. Chen C.K. Kutschke W. Mohler P.J. Mohapatra D.P. Anderson M.E. Fisher R.A. RGS6, a modulator of parasympathetic activation in heart. Circ. Res. Nov 26 2010; 107: 1345-1349 Crossref PubMed Scopus (89) Google Scholar ] and to, in turn, increase fluctuation in timing between individual depolarization events, manifesting as elevated heart rare variability (HRV) [ [23] Yang J. Huang J. Maity B. Gao Z. Lorca R.A. Gudmundsson H. Li J. Stewart A. Swaminathan P.D. Ibeawuchi S.R. Shepherd A. Chen C.K. Kutschke W. Mohler P.J. Mohapatra D.P. Anderson M.E. Fisher R.A. RGS6, a modulator of parasympathetic activation in heart. Circ. Res. Nov 26 2010; 107: 1345-1349 Crossref PubMed Scopus (89) Google Scholar ] and susceptibility to atrial fibrillation [ [24] Posokhova E. Ng D. Opel A. Masuho I. Tinker A. Biesecker L.G. Wickman K. Martemyanov K.A. Essential role of the m2R-RGS6-IKACh pathway in controlling intrinsic heart rate variability. PLoS One. Oct 29 2013; 8: e76973 Crossref PubMed Scopus (33) Google Scholar ]. Thus, the Rgs6-IKACh mechanism has an essential role in controlling the regularity of the rhythm, in addition to preventing severe bradycardia [ [23] Yang J. Huang J. Maity B. Gao Z. Lorca R.A. Gudmundsson H. Li J. Stewart A. Swaminathan P.D. Ibeawuchi S.R. Shepherd A. Chen C.K. Kutschke W. Mohler P.J. Mohapatra D.P. Anderson M.E. Fisher R.A. RGS6, a modulator of parasympathetic activation in heart. Circ. Res. Nov 26 2010; 107: 1345-1349 Crossref PubMed Scopus (89) Google Scholar ], increased HRV and susceptibility to atrial fibrillation [ [24] Posokhova E. Ng D. Opel A. Masuho I. Tinker A. Biesecker L.G. Wickman K. Martemyanov K.A. Essential role of the m2R-RGS6-IKACh pathway in controlling intrinsic heart rate variability. PLoS One. Oct 29 2013; 8: e76973 Crossref PubMed Scopus (33) Google Scholar ]. Activation of m2AChRs, in addition to opening IKACh, results also in the reduction of cAMP concentration which would inhibit HCN and Cav1.3 channels [ 24 Posokhova E. Ng D. Opel A. Masuho I. Tinker A. Biesecker L.G. Wickman K. Martemyanov K.A. Essential role of the m2R-RGS6-IKACh pathway in controlling intrinsic heart rate variability. PLoS One. Oct 29 2013; 8: e76973 Crossref PubMed Scopus (33) Google Scholar , 25 Lakatta E.G. Maltsev V.A. Vinogradova T.M. A coupled SYSTEM of intracellular Ca2+ clocks and surface membrane voltage clocks controls the timekeeping mechanism of the heart's pacemaker. Circ. Res. 2010; 106: 659-673 Crossref PubMed Scopus (461) Google Scholar , 26 Mangoni M.E. Nargeot J. Genesis and regulation of the heart automaticity. Physiol. Rev. 2008; 88: 919-982 Crossref PubMed Scopus (429) Google Scholar ] and in this function RGS6 has also an essential "membrane voltage clock" adjusting role in IKACh rhythm controlling. Members of the R7 subfamily of regulator of G protein signaling (R7 RGS) proteins (RGS6, RGS7, RGS9, and RGS11) exist as heterodimers with the G protein beta-subunit Gβ5 [ [27] Slepak V.Z. Structure, function, and localization of Gβ5-RGS complexes. Prog. Mol. Biol. Transl. Sci. 2009; 86: 157-203 Crossref PubMed Scopus (27) Google Scholar ] having an essential role in other several processes [ [28] Anderson G.R. Posokhova E. Martemyanov K.A. The R7 RGS protein family: multi-subunit regulators of neuronal G protein signaling. Cell Biochem. Biophys. 2009; 54: 33-46 Crossref PubMed Scopus (109) Google Scholar ]. R7 RGS proteins consist of three functional modules. The N-terminal DEP (Disheveled, EGL-10, Pleckstrin) and DHEX (DEP helical extension) domains mediate binding to the membrane anchors R7BP and R9AP. The central GGL (G Protein gamma-like) domain forms a complex with the Gβ5 (G protein β subunit, type 5). The C-terminal RGS (regulator of G protein signaling) domain mediates transient association with Gα-GTP subunits, during which GTP hydrolysis is stimulated. Gβ5 also associates with the DEP/DHEX module [ [28] Anderson G.R. Posokhova E. Martemyanov K.A. The R7 RGS protein family: multi-subunit regulators of neuronal G protein signaling. Cell Biochem. Biophys. 2009; 54: 33-46 Crossref PubMed Scopus (109) Google Scholar ]. Rgs6 interacts both with the Gβ5 and with the R7 binding protein (R7BP) in the central nervous system (CNS) [ [29] Posokhova E. Wydeven N. Allen K.L. Wickman K. Martemyanov K.A. RGS6/Gβ5 complex accelerates IKACh gating kinetics in atrial myocytes and modulates parasympathetic regulation of heart rate. Circ. Res. Nov 26 2010; 107: 1350-1354 Crossref PubMed Scopus (76) Google Scholar ] while in the mouse heart only Gβ5 interacts with Rgs6. RGS6–Gβ5 has been reported as the primary parasympathetic HR regulation and SAN M2AChRs-IKACh signaling modulator in mice [ [30] Wydeven N. Posokhova E. Xia Z. Martemyanov K.A. Wickman K. RGS6, but not RGS4, is the dominant regulator of G protein signaling (RGS) modulator of the parasympathetic regulation of mouse heart rate. J. Biol. Chem. 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