Altered heart rate and sinoatrial node function in mice lacking the cAMP regulator phosphoinositide 3-kinase-γ

Circulation Research

Volumn 101, Issue 12, 2007, Pages 1274-1282

  Rose, Robert A ^a,b   Kabir, M Golam ^a   Backx, Peter H ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

Action potentials; Arrhythmia; Electrophysiology; Ion channels

Indexed keywords

ATROPINE; CALCIUM CHANNEL L TYPE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE INHIBITOR; CYCLIC AMP DERIVATIVE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE GAMMA; PROPRANOLOL; RYANODINE; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANESTHESIA; ANIMAL EXPERIMENT; ARTICLE; CALCIUM CURRENT; CALCIUM TRANSPORT; CELL ISOLATION; DIALYSIS; HEART ATRIUM; HEART MUSCLE; HEART RATE VARIABILITY; HYPERPOLARIZATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SARCOPLASMIC RETICULUM; SINUS NODE; SINUS NODE MEMBRANE POTENTIAL; VOLTAGE CLAMP; WILD TYPE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ACTION POTENTIALS; ANIMALS; CYCLIC AMP; HEART RATE; ISOENZYMES; MALE; MICE; MICE, KNOCKOUT; MYOCYTES, CARDIAC; SINOATRIAL NODE;

EID: 37349027301     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.107.158428     Document Type: Article

References (49)

1. Alloatti G, Marcantoni A, Levi R, Gallo MP, Del Sorbo L, Patrucco E, Barberis L, Malan D, Azzolino O, Wymann M, Hirsch E, Montrucchio G. Phosphoinositide 3-kinase γ controls autonomic regulation of the mouse heart through Gi-independent downregulation of cAMP level. FEBS Lett. 2005;579:133-140.
2. Crackower MA, Oudit GY, Kozieradzki I, Sarao R, Sun H, Sasaki T, Hirsch E, Suzuki A, Shioi T, Irie-Sasaki J, Sah R, Cheng HY, Rybin VO, Lembo G, Fratta L, Oliveira-dos-Santos AJ, Benovic JL, Kahn CR, Izumo S, Steinberg SF, Wymann MP, Backx PH, Penninger JM. Regulation of myocardial contractility and cell size by distinct PI3K-PTEN signaling pathways. Cell. 2002;110:737-749.
3. Patrucco E, Notte A, Barberis L, Selvetella G, Maffei A, Brancaccio M, Marengo S, Russo G, Azzolino O, Rybalkin SD, Silengo L, Altruda F, Wetzker R, Wymann MP, Lembo G, Hirsch E. PI3Kγ modulates the cardiac response to chronic pressure overload by distinct kinase-dependent and -independent effects. Cell. 2004;118:375-387.
4. Kerfant BG, Gidrewicz D, Sun H, Oudit GY, Penninger JM, Backx PH. Cardiac sarcoplasmic reticulum calcium release and load are enhanced by subcellular cAMP elevations in PI3Kγ-deficient mice. Circ Res. 2005;96:1079-1086.
5. Kerfant BG, Zhao D, Lorenzen-Schmidt I, Wilson LS, Cai S, Chen SR, Maurice DH, Backx PH. PI3Kγ is required for PDE4, not PDE3, activity in subcellular microdomains containing the sarcoplasmic reticular calcium ATPase in cardiomyocytes. Circ Res. 2007;101:400-408.
6. 2+ currents via increased PI3Kα/PKB signaling. Circ Res. 2006;98:1390-1397.
7. Kerfant BG, Rose RA, Sun H, Backx PH. Phosphoinositide 3-kinase γ regulates cardiac contractility by locally controlling cyclic adenosine monophosphate levels. Trends Cardiovasc Med. 2006;16:250-256.
8. DiFrancesco D. Pacemaker mechanisms in cardiac tissue. Annu Rev Physiol. 1993;55:455-472.
9. Irisawa H, Brown HF, Giles W. Cardiac pacemaking in the sinoatrial node. Physiol Rev. 1993;73:197-227.
10. Accili EA, Proenza C, Baruscotti M, DiFrancesco D. From funny current to HCN channels: 20 years of excitation. News Physiol Sci. 2002;17:32-37.
11. Cho HS, Takano M, Noma A. The electrophysiological properties of spontaneously beating pacemaker cells isolated from mouse sinoatrial node. J Physiol. 2003;550:169-180.
12. + current regulates pacemaker activity in adult mouse sinoatrial node cells. Am J Physiol. 2004;286:H1757- H1766.
13. Rigg L, Terrar DA. Possible role of calcium release from the sarcoplasmic reticulum in pacemaking in guinea-pig sino-atrial node. Exp Physiol. 1996;81:877-880.
14. 2+ oscillations drive sinoatrial nodal cell pacemaker function to make the heart tick. Ann N Y Acad Sci. 2005;1047:138-156.
15. Rose RA, Kabir MG, Backx PH. Phosphoinositide-3-kinase γ regulates heart rate in vivo and modulates membrane currents in isolated mouse sinoatrial node cells. Circulation. 2006;114(suppl II):II-291 Abstract.
16. Sasaki T, Irie-Sasaki J, Jones RG, Oliveira-dos-Santos AJ, Stanford WL, Bolon B, Wakeham A, Itie A, Bouchard D, Kozieradzki I, Joza N, Mak TW, Ohashi PS, Suzuki A, Penninger JM. Function of PI3Kγ in thymocyte development, T cell activation, and neutrophil migration. Science. 2000;287:1040-1046.
17. + current in adult mouse atria. Br J Pharmacol. 2003;140:576-584.
18. f) in isolated mouse sino-atrial cells. Cardiovasc Res. 2001;52:51-64.
19. Rose RA, Lomax AE, Kondo CS, Anand-Srivastava MB, Giles WR. Effects of C-type natriuretic peptide on ionic currents in mouse sinoatrial node: a role for the NPR-C receptor. Am J Physiol. 2004;286:H1970-H1977.
20. Rothermel JD, Parker Botelho LH. A mechanistic and kinetic analysis of the interactions of the diastereoisomers of adenosine 3′,5′-(cyclic) phosphorothioate with purified cyclic AMP-dependent protein kinase. Biochem J. 1988;251:757-762.
21. 2+ channels in cardiac pacemaker activity. Proc Natl Acad Sci U S A. 2003;100:5543-5548.
22. 1D) calcium channel in sinoatrial nodes: insight gained using gene-targeted null mutant mice. Circ Res. 2002;90:981-987.
23. 1D) calcium channels in atria: insights gained from gene-targeted null mutant mice. Circulation. 2005;112:1936-1944.
24. Bois P, Renaudon B, Baruscotti M, Lenfant J, DiFrancesco D. Activation of f-channels by cAMP analogues in macropatches from rabbit sino-atrial node myocytes. J Physiol. 1997;501:565-571.
25. DiFrancesco D, Tortora P. Direct activation of cardiac pacemaker channels by intracellular cyclic AMP. Nature. 1991;351:145-147.
26. 2+ store oscillations and spontaneous beating of cardiac pacemaker cells. Circ Res. 2006;98:505-514.
27. 2+ exchanger: molecular partners in pacemaker regulation. Circ Res. 2001;88:1254-1258.
28. f- dependent modulation of pacemaker rate mediated by cAMP in the presence of ryanodine in rabbit sino-atrial node cells. J Mol Cell Cardiol. 2003;35:905-913.
29. Wickman K, Clapham DE. Ion channel regulation by G proteins. Physiol Rev. 1995;75:865-885.
30. Dobrzynski H, Boyett MR, Anderson RH. New insights into pacemaker activity: promoting understanding of sick sinus syndrome. Circulation. 2007;115:1921-1932.
31. de Marneffe M, Gregoire JM, Waterschoot P, Kestemont MP. The sinus node and the autonomic nervous system in normals and in sick sinus patients. Acta Cardiol. 1995;50:291-308.
32. Gehrmann J, Hammer PE, Maguire CT, Wakimoto H, Triedman JK, Berul CI. Phenotypic screening for heart rate variability in the mouse. Am J Physiol. 2000;279:H733-H740.
33. Jumrussirikul P, Dinerman J, Dawson TM, Dawson VL, Ekelund U, Georgakopoulos D, Schramm LP, Calkins H, Snyder SH, Hare JM, Berger RD. Interaction between neuronal nitric oxide synthase and inhibitory G protein activity in heart rate regulation in conscious mice. J Clin Invest. 1998;102:1279-1285.
34. Just A, Faulhaber J, Ehmke H. Autonomic cardiovascular control in conscious mice. Am J Physiol. 2000;279:R2214-R2221.
35. McDonald TF, Pelzer S, Trautwein W, Pelzer DJ. Regulation and modulation of calcium channels in cardiac, skeletal, and smooth muscle cells. Physiol Rev. 1994;74:365-507.
36. v1.3) L-type Ca channel by protein kinase A. Am J Physiol. 2005;288:H2123-H2130.
37. De Simone A, De Pasquale M, De Matteis C, Canciello M, Manzo M, Sabino L, Alfano F, Di Mauro M, Campana A, De Fabrizio G, Vitale DF, Turco P, Stabile G. Verapamil plus antiarrhythmic drugs reduce atrial fibrillation recurrences after an electrical cardioversion (VEPARAF Study). Eur Heart J. 2003;24:1425-1429.
38. Liu J, Dobrzynski H, Yanni J, Boyett MR, Lei M. Organisation of the mouse sinoatrial node: structure and expression of HCN channels. Cardiovasc Res. 2007;73:729-738.
39. Azene EM, Xue T, Marban E, Tomaselli GF, Li RA. Non-equilibrium behavior of HCN channels: insights into the role of HCN channels in native and engineered pacemakers. Cardiovasc Res. 2005;67:263-273.
40. Mannikko R, Pandey S, Larsson HP, Elinder F. Hysteresis in the voltage dependence of HCN channels: conversion between two modes affects pacemaker properties. J Gen Physiol. 2005;125:305-326.
41. f) by cAMP gating and phosphatase inhibition in rabbit sino-atrial node myocytes. J Physiol. 1997;500(pt 3):643-651.
42. f. J Physiol. 1991;440:367-384.
43. Kaupp UB, Seifert R. Molecular diversity of pacemaker ion channels. Annu Rev Physiol. 2001;63:235-257.
44. 2+ releases in rabbit sinoatrial nodal cells impart an exponential phase to the late diastolic depolarization that controls their chronotropic state. Circ Res. 2006;99:979-987.
45. Baillie GS, Scott JD, Houslay MD. Compartmentalisation of phosphodiesterases and protein kinase A: opposites attract. FEBS Lett. 2005;579:3264-3270.
46. Steinberg SF, Brunton LL. Compartmentation of G protein-coupled signaling pathways in cardiac myocytes. Annu Rev Pharmacol Toxicol. 2001;41:751-773.
47. Wong W, Scott JD. AKAP signalling complexes: focal points in space and time. Nat Rev Mol Cell Biol. 2004;5:959-970.
48. Jones SA, Boyett MR, Lancaster MK. Declining into failure: the agedependent loss of the L-type calcium channel within the sinoatrial node. Circulation. 2007;115:1183-1190.
49. Naga Prasad SV, Perrino C, Rockman HA. Role of phosphoinositide 3-kinase in cardiac function and heart failure. Trends Cardiovasc Med. 2003;13:206-212.