Compartmentalized phosphodiesterase-2 activity blunts β-adrenergic cardiac inotropy via an NO/cGMP-dependent pathway

Circulation Research

Volumn 98, Issue 2, 2006, Pages 226-234

  Mongillo, Marco ^a,b   Tocchetti, Carlo G ^c   Terrin, Anna ^a,b   Lissandron, Valentina ^a,b   Cheung, York Fong ^d   Dostmann, Wolfgang R ^e   Pozzan, Tullio ^b,f   Kass, David A ^c   Paolocci, Nazareno ^c   Houslay, Miles D ^d   Zaccolo, Manuela ^a,b  

^a DULBECCO TELETHON INSTITUTE   (Italy)

^b VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

^c DEPARTMENT OF PATHOLOGY   (United States)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

^e UNIVERSITY OF VERMONT   (United States)

^f UNIVERSITY OF PADOVA   (Italy)

Author keywords

cAMP; Cardiomyocytes; Compartmentalization; Fluorescence resonance energy transfer; PDE2

Indexed keywords

ADENYLATE CYCLASE; BETA 1 ADRENERGIC RECEPTOR; BETA 2 ADRENERGIC RECEPTOR; BETA 3 ADRENERGIC RECEPTOR; BETA ADRENERGIC RECEPTOR; CATECHOLAMINE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC GMP; CYCLIC NUCLEOTIDE; NITRIC OXIDE; PHOSPHODIESTERASE; SPLEEN EXONUCLEASE; 9 (2 HYDROXY 3 NONYL)ADENINE; 9-(2-HYDROXY-3-NONYL)ADENINE; ADENINE; CALCIUM; DRUG DERIVATIVE; ISOPRENALINE; NORADRENALIN; PDE2 PHOSPHODIESTERASE;

ADRENERGIC SYSTEM; ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CELL COMPARTMENTALIZATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME LOCALIZATION; FEEDBACK SYSTEM; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; INOTROPISM; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; DRUG EFFECT; ENZYMOLOGY; HEART CONTRACTION; METABOLISM; MOUSE; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ADENINE; ANIMALS; CALCIUM; CELLS, CULTURED; CYCLIC AMP; CYCLIC GMP; ENZYME ACTIVATION; ISOPROTERENOL; MICE; MICE, INBRED C57BL; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; NITRIC OXIDE; NOREPINEPHRINE; PHOSPHORIC DIESTER HYDROLASES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADRENERGIC, BETA; SIGNAL TRANSDUCTION;

EID: 33644865929     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000200178.34179.93     Document Type: Article

References (44)

1. Zaccolo M, Magalhaes P, Pozzan T. Compartmentalisation of cAMP and Ca(2+) signals. Curr Opin Cell Biol. 2002;14:160-166.
2. Tasken K, Aandahl EM. Localized effects of cAMP mediated by distinct routes of protein kinase A. Physiol Rev. 2004;84:137-167.
3. Rybin VO, Xu X, Lisanti MP, Steinberg SF. Differential targeting of beta-adrenergic receptor subtypes and adenylyl cyclase to cardiomyocyte caveolae. A mechanism to functionally regulate the cAMP signaling pathway. J Biol Chem. 2000;275:41447-41457.
4. Colledge M, Scott JD. AKAPs: from structure to function. Trends Cell Biol. 1999;9:216-221.
5. Kapiloff MS. Contributions of protein kinase A anchoring proteins to compartmentation of cAMP signaling in the heart. Mol Pharmacol. 2002;62:193-199.
6. Buxton IL, Brunton LL. Compartments of cyclic AMP and protein kinase in mammalian cardiomyocytes. J Biol Chem. 1983;258:10233-10239.
7. Jurevicius J, Fischmeister R. cAMP compartmentation is responsible for a local activation of cardiac Ca2+ channels by beta-adrenergic agonists. Proc Natl Acad Sci U S A. 1996;93:295-299.
8. Zaccolo M, Pozzan T. Discrete microdomains with high concentration of cAMP in stimulated rat neonatal cardiac myocytes. Science. 2002;295:1711-1715.
9. Beavo JA, Brunton LL. Cyclic nucleotide research - still expanding after half a century. Nat Rev Mol Cell Biol. 2002;3:710-718.
10. Houslay MD, Milligan G. Tailoring cAMP-signalling responses through isoform multiplicity. Trends Biochem Sci. 1997;22:217-224.
11. Mongillo M, McSorley T, Evellin S, Sood A, Lissandron V, Terrin A, Huston E, Hannawacker A, Lohse MJ, Pozzan T, Houslay MD, Zaccolo M. Fluorescence resonance energy transfer-based analysis of cAMP dynamics in live neonatal rat cardiac myocytes reveals distinct functions of compartmentalized phosphodiesterases. Circ Res. 2004;95:67-75.
12. Han X, Kobzik L, Balligand JL, Kelly RA, Smith TW. Nitric oxide synthase (NOS3)-mediated cholinergic modulation of Ca2+ current in adult rabbit atrioventricular nodal cells. Circ Res. 1996;78:998-1008.
13. Han X, Shimoni Y, Giles WR. A cellular mechanism for nitric oxide-mediated cholinergic control of mammalian heart rate. J Gen Physiol. 1995;106:45-65.
14. Mery PF, Pavoine C, Belhassen L, Pecker F, Fischmeister R. Nitric oxide regulates cardiac Ca2+ current. Involvement of cGMP-inhibited and cGMP-stimulated phosphodiesterases through guanylyl cyclase activation. J Biol Chem. 1993;268:26286-26295.
15. Rivet-Bastide M, Vandecasteele G, Hatem S, Verde I, Benardeau A, Mercadier JJ, Fischmeister R. cGMP-stimulated cyclic nucleotide phosphodiesterase regulates the basal calcium current in human atrial myocytes. J Clin Invest. 1997;99:2710-2718.
16. Mery PF, Lohmann SM, Walter U, Fischmeister R. Ca2+ current is regulated by cyclic GMP-dependent protein kinase in mammalian cardiac myocytes. Proc Natl Acad Sci U S A. 1991;88:1197-1201.
17. Zaccolo M. Use of chimeric fluorescent proteins and fluorescence resonance energy transfer to monitor cellular responses. Circ Res. 2004;94:866-873.
18. Zaccolo M, De Giorgi F, Cho CY, Feng L, Knapp T, Negulescu PA, Taylor SS, Tsien RY, Pozzan T. A genetically encoded, fluorescent indicator for cyclic AMP in living cells. Nat Cell Biol. 2000;2:25-29.
19. Zocchi C, Ongini E, Conti A, Monopoli A, Negretti A, Baraldi PG, Dionisotti S. The non-xanthine heterocyclic compound SCH 58261 is a new potent and selective A2a adenosine receptor antagonist. J Pharmacol Exp Ther. 1996;276:398-404.
20. Pyne NJ, Cooper ME, Houslay MD. Identification and characterization of both the cytosolic and particulate forms of cyclic GMP-stimulated cyclic AMP phosphodiesterase from rat liver. Biochem J. 1986;234:325-334.
21. Manganiello VC, Degerman E. Cyclic nucleotide phosphodiesterases (PDEs): diverse regulators of cyclic nucleotide signals and inviting molecular targets for novel therapeutic agents. Thromb Haemost. 1999;82:407-411.
22. Houslay MD, Adams DR. PDE4 cAMP phosphodiesterases: modular enzymes that orchestrate signalling cross-talk, desensitization and compartmentalization. Biochem J. 2003;370:1-18.
23. Martinez SE, Beavo JA, Hol WG. GAF Domains: two-billion-year-old molecular switches that bind cyclic nucleotides. Mol Interv. 2002;2:317-323.
24. Michie AM, Lobban M, Muller T, Harnett MM, Houslay MD. Rapid regulation of PDE-2 and PDE-4 cyclic AMP phosphodiesterase activity following ligation of the T cell antigen receptor on thymocytes: analysis using the selective inhibitors erythro-9-(2-hydroxy-3-nonyl)-adenine (EHNA) and rolipram. Cell Signal. 1996;8:97-110.
25. Paolocci N, Ekelund UE, Isoda T, Ozaki M, Vandegaer K, Georgakopoulos D, Harrison RW, Kass DA, Hare JM. cGMP-independent inotropic effects of nitric oxide and peroxynitrite donors: potential role for nitrosylation. Am J Physiol Heart Circ Physiol. 2000;279:H1982-H1988.
26. Gauthier C, Leblais V, Kobzik L, Trochu JN, Khandoudi N, Bril A, Balligand JL, Le Marec H. The negative inotropic effect of beta3-adrenoceptor stimulation is mediated by activation of a nitric oxide synthase pathway in human ventricle. J Clin Invest. 1998;102:1377-1384.
27. Honda A, Adams SR, Sawyer CL, Lev-Ram V, Tsien RY, Dostmann WR. Spatiotemporal dynamics of guanosine 3′,5′-cyclic monophosphate revealed by a genetically encoded, fluorescent indicator. Proc Natl Acad Sci U S A. 2001;98:2437-2442.
28. Brini M, Marsault R, Bastianutto C, Alvarez J, Pozzan T, Rizzuto R. Transfected aequorin in the measurement of cytosolic Ca2+ concentration ([Ca2+]c). A critical evaluation. J Biol Chem. 1995;270:9896-9903.
29. Shesely EG, Maeda N, Kim HS, Desai KM, Krege JH, Laubach VE, Sherman PA, Sessa WC, Smithies O. Elevated blood pressures in mice lacking endothelial nitric oxide synthase. Proc Natl Acad Sci U S A. 1996;93:13176-13181.
30. Godecke A, Heinicke T, Kamkin A, Kiseleva I, Strasser RH, Decking UK, Stumpe T, Isenberg G, Schrader J. Inotropic response to beta-adrenergic receptor stimulation and anti-adrenergic effect of ACh in endothelial NO synthase-deficient mouse hearts. J Physiol. 2001;532:195-204.
31. Takimoto E, Champion HC, Belardi D, Moslehi J, Mongillo M, Mergia E, Montrose DC, Isoda T, Aufiero K, Zaccolo M, Dostmann WR, Smith CJ, Kass DA. cGMP catabolism by phosphodiesterase 5A regulates cardiac adrenergic stimulation by NOS3-dependent mechanism. Circ Res. 2005;96:100-109.
32. Rochais F, Vandecasteele G, Lefebvre F, Lugnier C, Lum H, Mazet JL, Cooper DM, Fischmeister R. Negative feedback exerted by PKA and cAMP phosphodiesterase on subsarcolemmal cAMP signals in intact cardiac myocytes. An in vivo study using adenovirus-mediated expression of CNG channels. J Biol Chem. 2004;279:52095-52105.
33. Baillie GS, Sood A, McPhee I, Gall I, Perry SJ, Lefkowitz RJ, Houslay MD. beta-Arrestin-mediated PDE4 cAMP phosphodiesterase recruitment regulates beta-adrenoceptor switching from Gs to Gi. Proc Natl Acad Sci U S A. 2003;100:940-945.
34. Noyama K, Maekawa S. Localization of cyclic nucleotide phosphodiesterase 2 in the brain-derived Triton-insoluble low-density fraction (raft). Neurosci Res. 2003;45:141-148.
35. Ostrom RS, Bundey RA, Insel PA. Nitric oxide inhibition of adenylyl cyclase type 6 activity is dependent upon lipid rafts and caveolin signaling complexes. J Biol Chem. 2004;279:19846-19853.
36. Kohout TA, Takaoka H, McDonald PH, Perry SJ, Mao L, Lefkowitz RJ, Rockman HA. Augmentation of cardiac contractility mediated by the human beta(3)-adrenergic receptor overexpressed in the hearts of transgenic mice. Circulation. 2001;104:2485-2491.
37. Soeder KJ, Snedden SK, Cao W, Della Rocca GJ, Daniel KW, Luttrell LM, Collins S. The beta3-adrenergic receptor activates mitogen-activated protein kinase in adipocytes through a Gi-dependent mechanism. J Biol Chem. 1999;274:12017-12022.
38. Barouch LA, Harrison RW, Skaf MW, Rosas GO, Cappola TP, Kobeissi ZA, Hobai IA, Lemmon CA, Bumett AL, O'Rourke B, Rodriguez ER, Huang PL, Lima JA, Berkowitz DE, Hare JM. Nitric oxide regulates the heart by spatial confinement of nitric oxide synthase isoforms. Nature. 2002;416:337-339.
39. Vandecasteele G, Eschenhagen T, Scholz H, Stein B, Verde I, Fischmeister R. Muscarinic and beta-adrenergic regulation of heart rate, force of contraction and calcium current is preserved in mice lacking endothelial nitric oxide synthase. Nat Med. 1999;5:331-334.
40. Heubach JF, Rau T, Eschenhagen T, Ravens U, Kaumann AJ. Physiological antagonism between ventricular beta 1-adrenoceptors and alpha 1-adrenoceptors but no evidence for beta 2- and beta 3-adrenoceptor function in murine heart. Br J Pharmacol. 2002;136:217-229.
41. Brodde OE. Beta-adrenoceptors in cardiac disease. Pharmacol Ther. 1993;60:405-430.
42. Moniotte S, Kobzik L, Feron O, Trochu JN, Gauthier C, Balligand JL. Upregulation of beta(3)-adrenoceptors and altered contractile response to inotropic amines in human failing myocardium. Circulation. 2001;103:1649-1655.
43. Thomas RF, Holt BD, Schwinn DA, Liggett SB. Long-term agonist exposure induces upregulation of beta 3-adrenergic receptor expression via multiple cAMP response elements. Proc Natl Acad Sci U S A. 1992;89:4490-4494.
44. Yanaka N, Kurosawa Y, Minami K, Kawai E, Omori K. cGMP-phosphodiesterase activity is upregulated in response to pressure overload of rat ventricles. Biosci Biotechnol Biochem. 2003;67:973-979.