Ca2+-regulated-cAMP/PKA signaling in cardiac pacemaker cells links ATP supply to demand

Journal of Molecular and Cellular Cardiology

Volumn 51, Issue 5, 2011, Pages 740-748

  Yaniv, Yael ^a   Juhaszova, Magdalena ^a   Lyashkov, Alexey E ^a   Spurgeon, Harold A ^a   Sollott, Steven J ^a   Lakatta, Edward G ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

Bioenergetics; Calcium activated adenylyl cyclase; Constitutive basal PKA dependent phosphorylation; Pacemaker automaticity; Respiration

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; CYCLIC AMP DEPENDENT PROTEIN KINASE; FLAVOPROTEIN; OXYGEN; ADENYLATE CYCLASE; CALCIUM; CYCLIC AMP; ENZYME INHIBITOR; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL STIMULATION; CONTROLLED STUDY; FEEDBACK SYSTEM; FLUORESCENCE ANALYSIS; GLYCOLYSIS; HEART CONTRACTION; HEART MITOCHONDRION; HEART MUSCLE CELL; HEART MUSCLE OXYGEN CONSUMPTION; HEART VENTRICLE WALL; METABOLIC REGULATION; NONHUMAN; PRIORITY JOURNAL; SINUS NODE; SINUS NODE CELL; ACTION POTENTIAL; ANIMAL; BIOSYNTHESIS; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; HEART RATE; HEART VENTRICLE; METABOLISM; MITOCHONDRION; OXYGEN CONSUMPTION; PERIODICITY; PHOSPHORYLATION; PHYSIOLOGY; RABBIT; SARCOPLASMIC RETICULUM;

ORYCTOLAGUS CUNICULUS;

ACTION POTENTIALS; ADENOSINE TRIPHOSPHATE; ADENYLATE CYCLASE; ANIMALS; CALCIUM; CALCIUM SIGNALING; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENZYME INHIBITORS; FEEDBACK, PHYSIOLOGICAL; GLYCOLYSIS; HEART RATE; HEART VENTRICLES; MITOCHONDRIA; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; MYOCYTES, CARDIAC; OXYGEN CONSUMPTION; PERIODICITY; PHOSPHORYLATION; RABBITS; SARCOPLASMIC RETICULUM; SINOATRIAL NODE;

EID: 80053222653     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2011.07.018     Document Type: Article

References (33)

1. Bogdanov K.Y., Vinogradova T.M., Lakatta E.G. Sinoatrial nodal cell ryanodine receptor and Na(+)-Ca(2+) exchanger: molecular partners in pacemaker regulation. Circ Res 2001, 88(12):1254-1258.
2. Gao Z., Chen B., Joiner M.L., Wu Y., Guan X., Koval O.M., et al. I(f) and SR Ca(2+) release both contribute to pacemaker activity in canine sinoatrial node cells. J Mol Cell Cardiol 2010, 49(1):33-40.
3. Younes A., Lyashkov A.E., Graham D., Sheydina A., Volkova M.V., Mitsak M., et al. Ca(2+) -stimulated basal adenylyl cyclase activity localization in membrane lipid microdomains of cardiac sinoatrial nodal pacemaker cells. J Biol Chem 2008, 283(21):14461-14468.
4. Mattick P., Parrington J., Odia E., Simpson A., Collins T., Terrar D. Ca2+-stimulated adenylyl cyclase isoform AC1 is preferentially expressed in guinea-pig sino-atrial node cells and modulates the I(f) pacemaker current. J Physiol 2007, 582(Pt 3):1195-1203.
5. Vinogradova T.M., Sirenko S., Lyashkov A.E., Younes A., Li Y., Zhu W., et al. Constitutive phosphodiesterase activity restricts spontaneous beating rate of cardiac pacemaker cells by suppressing local Ca2+ releases. Circ Res 2008, 102(7):761-769.
6. Vinogradova T.M., Lyashkov A.E., Zhu W., Ruknudin A.M., Sirenko S., Yang D., et al. High basal protein kinase A-dependent phosphorylation drives rhythmic internal Ca2+ store oscillations and spontaneous beating of cardiac pacemaker cells. Circ Res 2006, 98(4):505-514.
7. Ju Y.K., Allen D.G. Early effects of metabolic inhibition on intracellular Ca2+ in toad pacemaker cells: involvement of Ca2+ stores. Am J Physiol Heart Circ Physiol 2003, 284(4):H1087-H1094.
8. Balaban R.S., Kantor H.L., Katz L.A., Briggs R.W. Relation between work and phosphate metabolite in the in vivo paced mammalian heart. Science 1986, 232(4754):1121-1123.
9. 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(4):659-673.
10. Nett M.P., Vassalle M. Obligatory role of diastolic voltage oscillations in sino-atrial node discharge. J Mol Cell Cardiol 2003, 35(10):1257-1276.
11. Ju Y.K., Allen D.G. How does beta-adrenergic stimulation increase the heart rate? The role of intracellular Ca2+ release in amphibian pacemaker cells. J Physiol 1999, 516(Pt 3):793-804.
12. DiFrancesco D., Tortora P. Direct activation of cardiac pacemaker channels by intracellular cyclic AMP. Nature 1991, 351(6322):145-147.
13. van Borren M.M., Verkerk A.O., Wilders R., Hajji N., Zegers J.G., Bourier J., et al. Effects of muscarinic receptor stimulation on Ca2+ transient, cAMP production and pacemaker frequency of rabbit sinoatrial node cells. Basic Res Cardiol 2010, 105(1):73-87.
14. Lyashkov A.E., Vinogradova T.M., Zahanich I., Li Y., Younes A., Nuss H.B., et al. Cholinergic receptor signaling modulates spontaneous firing of sinoatrial nodal cells via integrated effects on PKA-dependent Ca(2+) cycling and I(KACh). Am J Physiol Heart Circ Physiol 2009, 297(3):H949-H959.
15. Boyett M.R., Honjo H., Kodama I. The sinoatrial node, a heterogeneous pacemaker structure. Cardiovasc Res 2000, 47(4):658-687.
16. Senges J., Brachmann J., Pelzer D., Rizos I., Kubler W. Effect of glycolytic inhibitors on the sinoatrial node, atrium and atrioventricular node in the rabbit heart. J Mol Cell Cardiol 1981, 13(9):811-821.
17. Liu T., O'Rourke B. Enhancing mitochondrial Ca2+ uptake in myocytes from failing hearts restores energy supply and demand matching. Circ Res 2008, 103(3):279-288.
18. Miyata H., Silverman H.S., Sollott S.J., Lakatta E.G., Stern M.D., Hansford R.G. Measurement of mitochondrial free Ca2+ concentration in living single rat cardiac myocytes. Am J Physiol 1991, 261(4 Pt 2):H1123-H1134.
19. Harris D.A., Das A.M. Control of mitochondrial ATP synthesis in the heart. Biochem J 1991, 280(Pt 3):561-573.
20. Bleeker W.K., Mackaay A.J., Masson-Pevet M., Bouman L.N., Becker A.E. Functional and morphological organization of the rabbit sinus node. Circ Res 1980, 46(1):11-22.
21. Bouman L.N., Jongsma H.J. Structure and function of the sino-atrial node: a review. Eur Heart J 1986, 7(2):94-104.
22. Masson-Pevet M., Bleeker W.K., Mackaay A.J., Bouman L.N., Houtkooper J.M. Sinus node and atrium cells from the rabbit heart: a quantitative electron microscopic description after electrophysiological localization. J Mol Cell Cardiol 1979, 11(6):555-568.
23. Katz L.A., Swain J.A., Portman M.A., Balaban R.S. Relation between phosphate metabolites and oxygen consumption of heart in vivo. Am J Physiol 1989, 256(1 Pt 2):H265-H274.
24. Yaniv Y., Juhaszova M., Nuss H.B., Wang S., Zorov D.B., Lakatta E.G., et al. Matching ATP supply and demand in mammalian heart. Ann N Y Acad Sci 2010, 1188:133-142.
25. Cortassa S., O'Rourke B., Winslow R.L., Aon M.A. Control and regulation of mitochondrial energetics in an integrated model of cardiomyocyte function. Biophys J 2009, 96(6):2466-2478.
26. Bera A.K., Ghosh S., Das S. Mitochondrial VDAC can be phosphorylated by cyclic AMP-dependent protein kinase. Biochem Biophys Res Commun 1995, 209(1):213-217.
27. Sardanelli A.M., Technikova-Dobrova Z., Speranza F., Mazzocca A., Scacco S., Papa S. Topology of the mitochondrial cAMP-dependent protein kinase and its substrates. FEBS Lett 1996, 396(2-3):276-278.
28. Papa S., Sardanelli A.M., Scacco S., Technikova-Dobrova Z. cAMP-dependent protein kinase and phosphoproteins in mammalian mitochondria. An extension of the cAMP-mediated intracellular signal transduction. FEBS Lett 1999, 444(2-3):245-249.
29. Signorile A., Sardanelli A.M., Nuzzi R., Papa S. Serine (threonine) phosphatase(s) acting on cAMP-dependent phosphoproteins in mammalian mitochondria. FEBS Lett 2002, 512(1-3):91-94.
30. Helling S., Vogt S., Rhiel A., Ramzan R., Wen L., Marcus K., et al. Phosphorylation and kinetics of mammalian cytochrome c oxidase. Mol Cell Proteomics 2008, 7(9):1714-1724.
31. Feliciello A., Gottesman M.E., Avvedimento E.V. cAMP-PKA signaling to the mitochondria: protein scaffolds, mRNA and phosphatases. Cell Signal 2005, 17(3):279-287.
32. Martin M.C., Allan L.A., Lickrish M., Sampson C., Morrice N., Clarke P.R. Protein kinase A regulates caspase-9 activation by Apaf-1 downstream of cytochrome c. J Biol Chem 2005, 280(15):15449-15455.
33. Acin-Perez R., Salazar E., Kamenetsky M., Buck J., Levin L.R., Manfredi G. Cyclic AMP produced inside mitochondria regulates oxidative phosphorylation. Cell Metab 2009, 9(3):265-276.