Cyclic AMP synthesis and hydrolysis in the normal and failing heart

Pflugers Archiv European Journal of Physiology

Volumn 466, Issue 6, 2014, Pages 1163-1175

  Guellich, Aziz ^a,b   Mehel, Hind ^a,b   Fischmeister, Rodolphe ^a,b  

^a Universite Paris Sud   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Adenylyl cyclase; Compartmentation; Cyclic AMP; Heart failure; Phosphodiesterases

Indexed keywords

ADENYLATE CYCLASE; BETA ADRENERGIC RECEPTOR; CYCLIC AMP; FORSKOLIN; PHOSPHODIESTERASE; PHOSPHODIESTERASE I; PHOSPHODIESTERASE III; PHOSPHODIESTERASE IV; SPLEEN EXONUCLEASE; ISOPROTEIN;

ENZYME DEGRADATION; ENZYME STRUCTURE; HEART FAILURE; HEART VENTRICLE HYPERTROPHY; HUMAN; HYDROLYSIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SYNTHESIS; REVIEW; ANIMAL; BIOSYNTHESIS; CHEMISTRY; GENETICS; METABOLISM;

ADENYLATE CYCLASE; ANIMALS; CYCLIC AMP; HEART FAILURE; HUMANS; HYDROLYSIS; PHOSPHORIC DIESTER HYDROLASES; PROTEIN ISOFORMS;

EID: 84901929552     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-014-1515-1     Document Type: Review

References (153)

1. Abi-Gerges A, Richter W, Lefebvre F, Matéo P, Varin A, Heymes C, Samuel J-L, Lugnier C, Conti M, Fischmeister R, Vandecasteele G (2009) Decreased expression and activity of cAMP phosphodiesterases in cardiac hypertrophy and its impact on β-adrenergic cAMP signals. Circ Res 105:784-792
2. Acin-Perez R, Salazar E, Kamenetsky M, Buck J, Levin LR, Manfredi G (2009) Cyclic AMP produced inside mitochondria regulates oxidative phosphorylation. Cell Metab 9:265-276
3. Ai X, Curran JW, Shannon TR, Bers DM, Pogwizd SM (2005) Ca2+/calmodulin-dependent protein kinase modulates cardiac ryanodine receptor phosphorylation and sarcoplasmic reticulum Ca2+ leak in heart failure. Circ Res 97:1314-1322
4. Antos CL, Frey N, Marx SO, Reiken S, Gaburjakova M, Richardson JA, Marks AR, Olson EN (2001) Dilated cardiomyopathy and sudden death resulting from constitutive activation of protein kinase A. Circ Res 89:997-1004 (Pubitemid 34640866)
5. Baillie GS, MacKenzie SJ, McPhee I, Houslay MD (2000) Subfamily selective actions in the ability of Erk2 MAP kinase to phosphorylate and regulate the activity of PDE4 cyclic AMP-specific phosphodiesterases. Br J Pharmacol 131:811-819
6. Baillie GS, Sood A, McPhee I, Gall I, Perry SJ, Lefkowitz RJ, Houslay MD (2003) β-Arrestin-mediated PDE4 cAMP phosphodiesterase recruitment regulates β-adrenoceptor switching from Gs to Gi. Proc Natl Acad Sci U S A 100:941-945
7. Beavo JA, Francis SH, Houslay MD (2007) Cyclic nucleotide phosphodiesterases in health and disease. CRC Press, Taylor & Francis Group, Boca Raton, Florida, USA, pp 1-713
8. Beazely MA, Watts VJ (2006) Regulatory properties of adenylate cyclases type 5 and 6: a progress report. Eur J Pharmacol 535:1-12
9. Beca S, Ahmad F, Shen W, Liu J, Makary S, Polidovitch N, Sun J, Hockman S, Chung YW, Murphy E, Manganiello VC, Backx PH (2013) PDE3A regulates basal myocardial contractility through interacting with SERCA2a-signaling complexes in mouse heart. Circ Res 112:289-297
10. Bender AT, Beavo JA (2006) Cyclic nucleotide phosphodiesterases: from molecular regulation to clinical use. Pharmacol Rev 58:488-520 (Pubitemid 44394910)
11. Bers DM (2002) Cardiac excitation-contraction coupling. Nature 415:198-205
12. Bode DC, Kanter JR, Brunton LL (1991) Cellular distribution of phosphodiesterase isoforms in rat cardiac tissue. Circ Res 68:1070-1079
13. Boluyt MO, Oneill L, Meredith AL, Bing OHL, Brooks WW, Conrad CH, Crow MT, Lakatta EG (1994) Alterations in cardiac gene expression during the transition from stable hypertrophy to heart failure - marked upregulation of genes encoding extracellular matrix components. Circ Res 75:23-32 (Pubitemid 24187732)
14. Braeunig JH, Schweda F, Han PL, Seifert R (2013) Similarly potent inhibition of adenylyl cyclase by P-site inhibitors in hearts from wild type and AC5 knockout mice. PLoS One 8:e68009
15. Brand CS, Hocker HJ, Gorfe AA, Cavasotto CN, Dessauer CW (2013) Isoform selectivity of adenylyl cyclase inhibitors: characterization of known and novel compounds. J Pharmacol Exp Ther 347:265-275
16. Chen-Goodspeed M, Lukan AN, Dessauer CW (2005) Modeling of Gαs and Gαi regulation of human type Vand VI adenylyl cyclase. J Biol Chem 280:1808-1816
17. Chen J, Levin LR, Buck J (2012) Role of soluble adenylyl cyclase in the heart. Am J Physiol Heart Circ Physiol 302:H538-H543
18. Conti M, Beavo JA (2007) Biochemistry and physiology of cyclic nucleotide phosphodiesterases: essential components in cyclic nucleotide signaling. Ann Rev Biochem 76:481-511
19. De Arcangelis V, Liu R, Soto D, Xiang Y (2009) Differential association of phosphodiesterase 4D isoforms with β2-adrenoceptor in cardiac myocytes. J Biol Chem 284:33824-33832
20. Dessauer CW (2009) Adenylyl cyclase - A-kinase anchoring protein complexes: the next dimension in cAMP signaling. Mol Pharmacol 76:935-941
21. Di Benedetto G, Pendin D, Greotti E, Pizzo P, Pozzan T (2014) Ca2+ and cAMP cross-talk in mitochondria. J Physiol 592:305-312
22. Di Benedetto G, Scalzotto E, Mongillo M, Pozzan T (2013) Mitochondrial Ca2+ uptake induces cyclic AMP generation in the matrix andmodulates organelle ATP levels. Cell Metab 17:965-975
23. Ding B, Abe J, Wei H, Huang Q, Walsh RA, Molina CA, Zhao A, Sadoshima J, Blaxall BC, Berk BC, Yan C (2005) Functional role of phosphodiesterase 3 in cardiomyocyte apoptosis: implication in heart failure. Circulation 111:2469-2476 (Pubitemid 40696135)
24. Ding B, Abe J, Wei H, Xu H, Che W, Aizawa T, Liu W, Molina CA, Sadoshima J, Blaxall BC, Berk BC, Yan C (2005) A positive feedback loop of phosphodiesterase 3 (PDE3) and inducible cAMP early repressor (ICER) leads to cardiomyocyte apoptosis. Proc Natl Acad Sci U S A 102:14771-14776 (Pubitemid 41457131)
25. Dodge-Kafka KL, Langeberg L, Scott JD (2006) Compartmentation of cyclic nucleotide signaling in the heart: the role of A-kinase anchoring proteins. Circ Res 98:993-1001
26. Dodge-Kafka KL, Soughayer J, Pare GC, Carlisle Michel JJ, Langeberg LK, Kapiloff MS, Scott JD (2005) The protein kinase A anchoring protein mAKAP co-ordinates two integrated cAMP effector pathways. Nature 437:574-578 (Pubitemid 41613557)
27. Dodge KL, Khouangsathiene S, Kapiloff MS, Mouton R, Hill EV, Houslay MD, Langeberg LK, Scott JD (2001) mAKAP assembles a protein kinase A/PDE4 phosphodiesterase cAMP signalingmodule. EMBO J 20:1921-1930 (Pubitemid 32397394)
28. Efendiev R, Samelson BK, Nguyen BT, Phatarpekar PV, Baameur F, Scott JD, Dessauer CW (2010) AKAP79 interacts with multiple adenylyl cyclase (AC) isoforms and scaffolds AC5 and -6 to alpha-amino-3-hydroxyl-5-methyl-4-isoxazole- propionate (AMPA) receptors. J Biol Chem 285:14450-14458
29. Engelhardt S, Hein L, Wiesmann F, Lohse MJ (1999) Progressive hypertrophy and heart failure in beta1-adrenergic receptor transgenic mice. Proc Natl Acad Sci U S A 96:7059-7064 (Pubitemid 29275009)
30. Enns LC, Morton JF, Treuting PR, Emond MJ, Wolf NS, McKnight GS, Rabinovitch PS, Ladiges WC (2009) Disruption of protein kinase A in mice enhances healthy aging. PLoS One 4:e5963
31. Espinasse I, Iourgenko V, Defer N, Samson F, Hanoune J, Mercadier JJ (1995) Type V, but not type VI, adenylyl cyclase mRNA accumulates in the rat heart during ontogenic development. Correlation with increased global adenylyl cyclase activity. J Mol Cell Cardiol 27:1789-1795
32. Esposito G, Perrino C, Ozaki T, Takaoka H, Defer N, Petretta MP, De Angelis MC, Mao L, Hanoune J, Rockman HA, Chiariello M (2008) Increased myocardial contractility and enhanced exercise function in transgenic mice overexpressing either adenylyl cyclase 5 or 8. Basic Res Cardiol 103:22-30 (Pubitemid 50005149)
33. Fan GC, Chu G, Mitton B, Song Q, Yuan Q, Kranias EG (2004) Small heat-shock protein Hsp20 phosphorylation inhibits beta-agonist-induced cardiac apoptosis. Circ Res 94:1474-1482 (Pubitemid 38780320)
34. Fischmeister R, Castro L, Abi-Gerges A, Rochais F, Vandecasteele G (2005) Species-and tissue-dependent effects of NO and cyclic GMP on cardiac ion channels. Comp Biochem Physiol A Mol Integr Physiol 142:136-143 (Pubitemid 41443573)
35. Fischmeister R, Castro LRV, Abi-Gerges A, Rochais F, Jurevièius J, Leroy J, Vandecasteele G (2006) Compartmentation of cyclic nucleotide signaling in the heart: the role of cyclic nucleotide phosphodiesterases. Circ Res 99:816-828 (Pubitemid 44556380)
36. Francis SH, Blount MA, Corbin JD (2011) Mammalian cyclic nucleotide phosphodiesterases: molecular mechanisms and physiological functions. Physiol Rev 91:651-690
37. Gao MH, Lai NC, Roth DM, Zhou J, Zhu J, Anzai T, Dalton N, Hammond HK (1999) Adenylylcyclase increases responsiveness to catecholamine stimulation in transgenic mice. Circulation 99:1618-1622 (Pubitemid 29152931)
38. Gao MH, Lai NC, Tang T, Guo T, Tang R, Chun BJ, Wang H, Dalton NN, Suarez J, Dillmann WH, Hammond HK (2013) Preserved Cardiac Function despite Marked Impairment of cAMP Generation. PLoS One 8:e72151
39. Gao MH, Tang T, Guo T, Miyanohara A, Yajima T, Pestonjamasp K, Feramisco JR, Hammond HK (2008) Adenylyl cyclase type VI increases Akt activity and phospholamban phosphorylation in cardiac myocytes. J Biol Chem 283:33527-33535
40. Gao MH, Tang T, Lai NC, Miyanohara A, Guo T, Tang R, Firth AL, Yuan JX, Hammond HK (2011) Beneficial effects of adenylyl cyclase type 6 (AC6) expression persist using a catalytically inactive AC6 mutant. Mol Pharmacol 79:381-388
41. Gao MH, Tang T, Miyanohara A, Feramisco JR, Hammond HK (2010) beta(1)-Adrenergic receptor vs adenylyl cyclase 6 expression in cardiac myocytes: differences in transgene localization and intracellular signaling. Cell Signal 22:584-589
42. Ghigo A, Perino A, Mehel H, Zahradnikova AJ, Morello F, Leroy J, Nikolaev VO, Damilano F, Cimino J, De Luca E, Richter W, Westenbroek R, Catterall WA, Zhang J, Yan C, Conti M, Gomez AM, Vandecasteele G, Hirsch E, Fischmeister R (2012) PI3KY Protects against catecholamine-induced ventricular arrhythmia through PKA-mediated regulation of distinct phosphodiesterases. Circulation 126:2073-2083
43. Gille A, Lushington GH, Mou TC, Doughty MB, Johnson RA, Seifert R (2004) Differential inhibition of adenylyl cyclase isoforms and soluble guanylyl cyclase by purine and pyrimidine nucleotides. J Biol Chem 279:19955-19969 (Pubitemid 38623438)
44. Grimm M, Brown JH (2010) β-Adrenergic receptor signaling in the heart: role of CaMKII. J Mol Cell Cardiol 48:322-330
45. Guellich A, Gao S, Hong C, Yan L, Wagner TE, Dhar SK, Ghaleh B, Hittinger L, Iwatsubo K, Ishikawa Y, Vatner SF, Vatner DE (2010) Effects of cardiac overexpression of type 6 adenylyl cyclase affects on the response to chronic pressure overload. Am J Physiol Heart Circ Physiol 299:H707-H712
46. Gwathmey JK, Yerevanian A, Hajjar RJ (2013) Targeting sarcoplasmic reticulum calcium ATPase by gene therapy. Hum Gene Ther 24:937-947
47. Hambleton R, Krall J, Tikishvili E, Honeggar M, Ahmad F, Manganiello VC, Movsesian MA (2005) Isoforms of cyclic nucleotide phosphodiesterase PDE3 and their contribution to cAMP-hydrolytic activity in subcellular fractions of human myocardium. J Biol Chem 280:39168-39174 (Pubitemid 41713868)
48. Hammond J, Balligand JL (2012) Nitric oxide synthase and cyclic GMP signaling in cardiac myocytes: from contractility to remodeling. J Mol Cell Cardiol 52:330-340
49. Hanoune J, Defer N (2001) Regulation and role of adenylyl cyclase isoforms. Annu Rev Pharmacol Toxicol 41:145-174 (Pubitemid 32385886)
50. Hartzell HC, Fischmeister R (1986) Opposite effects of cyclic GMP and cyclic AMP on Ca2+ current in single heart cells. Nature 323:273-275 (Pubitemid 16054316)
51. Houslay MD, Adams DR (2003) PDE4 cAMP phosphodiesterases: modular enzymes that orchestrate signalling cross-talk, desensitization and compartmentalization. Biochem J 370:1-18 (Pubitemid 36259414)
52. Houslay MD, Baillie GS, Maurice DH (2007) cAMP-Specific phosphodiesterase-4 enzymes in the cardiovascular system: a molecular toolbox for generating compartmentalized cAMP signaling. Circ Res 100:950-966 (Pubitemid 46598920)
53. Hu CL, Chandra R, Ge H, Pain J, Yan L, Babu G, Depre C, Iwatsubo K, Ishikawa Y, Sadoshima J, Vatner SF, Vatner DE (2009) Adenylyl cyclase type 5 protein expression during cardiac development and stress. Am J Physiol Heart Circ Physiol 297:H1776-H1782
54. Huston E, Beard M, McCallum F, Pyne NJ, Vandenabeele P, Scotland G, Houslay MD (2000) The cAMP-specific phosphodiesterase PDE4A5 is cleaved downstream of its SH3 interaction domain by caspase-3. Consequences for altered intracellular distribution. J Biol Chem 275:28063-28074
55. Iwamoto T, Okumura S, Iwatsubo K, Kawabe J, Ohtsu K, Sakai I, Hashimoto Y, Izumitani A, Sango K, Ajiki K, Toya Y, Umemura S, Goshima Y, Arai N, Vatner SF, Ishikawa Y (2003) Motor dysfunction in type 5 adenylyl cyclase-null mice. J Biol Chem 278:16936-16940 (Pubitemid 36799567)
56. Iwatsubo K, Bravo C, Uechi M, Baljinnyam E, Nakamura T, Umemura M, Lai L, Gao S, Yan L, Zhao X, Park M, Qiu H, Okumura S, Iwatsubo M, Vatner DE, Vatner SF, Ishikawa Y (2012) Prevention of heart failure in mice by an antiviral agent that inhibits type 5 cardiac adenylyl cyclase. Am J Physiol Heart Circ Physiol 302:H2622-H2628
57. Jurevicius J, Fischmeister R (1996) cAMP compartmentation is responsible for a local activation of cardiac Ca2+ channels by β-adrenergic agonists. Proc Natl Acad Sci U S A 93:295-299
58. Kapiloff MS, Piggott LA, Sadana R, Li J, Heredia LA, Henson E, Efendiev R, Dessauer CW (2009) An adenylyl cyclase-mAKAPbeta signaling complex regulates cAMP levels in cardiac myocytes. J Biol Chem 284:23540-23546
59. Kass DA (2012) Cardiac role of cyclic-GMP hydrolyzing phosphodiesterase type 5: from experimental models to clinical trials. Curr Heart Fail Rep 9:192-199
60. Kikura M, Morita K, Sato S (2004) Pharmacokinetics and a simulation model of colforsin daropate, new forskolin derivative inotropic vasodilator, in patients undergoing coronary artery bypass grafting. Pharmacol Res 49:275-281 (Pubitemid 38064339)
61. Krupinski J, Coussen F, Bakalyar HA, Tang WJ, Feinstein PG, Orth K, Slaughter C, Reed RR, Gilman AG (1989) Adenylyl cyclase amino acid sequence: possible channel- or transporter-like structure. Science 244:1558-1564 (Pubitemid 19189731)
62. Lai L, Yan L, Gao S, Hu CL, Ge H, Davidow A, Park M, Bravo C, Iwatsubo K, Ishikawa Y, Auwerx J, Sinclair DA, Vatner SF, Vatner DE (2013) Type 5 adenylyl cyclase increases oxidative stress by transcriptional regulation of manganese superoxide dismutase via the SIRT1/FoxO3a pathway. Circulation 127:1692-1701
63. Lai NC, Roth DM, Gao MH, Tang T, Dalton N, Lai YY, Spellman M, Clopton P, Hammond HK (2004) Intracoronary adenovirus encoding adenylyl cyclase VI increases left ventricular function in heart failure. Circulation 110:330-336 (Pubitemid 38955502)
64. Lai NC, Tang T, Gao MH, Saito M, Takahashi T, Roth DM, Hammond HK (2008) Activation of cardiac adenylyl cyclase expression increases function of the failing ischemic heart in mice. J Am Coll Cardiol 51:1490-1497 (Pubitemid 351470034)
65. Lee DI, Kass DA (2012) Phosphodiesterases and cyclic GMP regulation in heart muscle. Physiology (Bethesda) 27:248-258
66. Lehnart SE, Wehrens XH, Marks AR (2005) Defective ryanodine receptor interdomain interactions may contribute to intracellular Ca2+ leak: a novel therapeutic target in heart failure. Circulation 111:3342-3346
67. Lehnart SE, Wehrens XHT, Reiken S, Warrier S, Belevych AE, Harvey RD, Richter W, Jin SLC, Conti M, Marks A (2005) Phosphodiesterase 4D deficiency in the ryanodine receptor complex promotes heart failure and arrhythmias. Cell 123:23-35
68. Leroy J, Abi-Gerges A, Nikolaev VO, Richter W, Lechêne P, Mazet J-L, Conti M, Fischmeister R, Vandecasteele G (2008) Spatiotemporal dynamics of β-adrenergic cAMP signals and L-type Ca2+ channel regulation in adult rat ventricular myocytes: role of phosphodiesterases. Circ Res 102:1091-1100 (Pubitemid 351667863)
69. Leroy J, Richter W, Mika D, Castro LRV, Abi-Gerges A, Xie M, Scheitrum C, Lefebvre F, Schittl J, Westenbroek R, Catterall WA, Charpentier F, Conti M, Fischmeister R, Vandecasteele G (2011) Phosphodiesterase 4B in the cardiac L-type Ca2+ channel complex regulates Ca2+ current and protects against ventricular arrhythmias. J Clin Invest 121:2651-2561
70. Lohse MJ, Engelhardt S, Eschenhagen T (2003) What is the role of β-adrenergic signaling in heart failure? Circ Res 93:896-906 (Pubitemid 37433227)
71. Lugnier C (2006) Cyclic nucleotide phosphodiesterase (PDE) superfamily: a new target for the development of specific therapeutic agents. Pharmacol Ther 109:366-398
72. Lugnier C, Muller B, Lebec A, Beaudry C, Rousseau E (1993) Characterization of indolidan-sensitive and rolipram-sensitive cyclic nucleotide phosphodiesterases in canine and human cardiac microsomal fractions. J Pharmacol Exp Ther 265:1142-1151 (Pubitemid 23321013)
73. Martin TP, Currie S, Baillie GS (2014) The cardioprotective role of small heat-shock protein 20. Biochem Soc Trans 42:270-273
74. Martinez SE (2007) PDE2 structure and functions. In: Beavo JA, Francis S, Houslay M (eds) Cyclic nucleotide phosphodiesterases in health and disease. CRC Press, Taylor & Francis Group, Boca Raton, Florida, USA, pp 55-77
75. Marx SO, Reiken S, Hisamatsu Y, Jayaraman T, Burkhoff D, Rosemblit N, Marks AR (2000) PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (Ryanodine receptor): defective regulation in failing hearts. Cell 101:365-376
76. Masunaga R, Nagasaka A, Sawai Y, Hayakawa N, Nakai A, Hotta K, Kato Y, Hishida H, Takahashi H, Naka M, Shimada Y, Tanaka T, Hidaka H, Itoh M (2004) Changes in cyclic nucleotide phosphodiesterase activity and calmodulin concentration in heart muscle of cardiomyopathic hamsters. J Mol Cell Cardiol 37:767-774 (Pubitemid 39194568)
77. Mattick P, Parrington J, Odia E, Simpson A, Collins T, Terrar D (2007) Ca2+- stimulated adenylyl cyclase isoform AC1 is preferentially expressed in guinea-pig sino-atrial node cells and modulates the If pacemaker current. J Physiol 582:1195-1203 (Pubitemid 47104348)
78. McMurray JJ, Adamopoulos S, Anker SD, Auricchio A, Bohm M, Dickstein K, Falk V, Filippatos G, Fonseca C, Gomez-Sanchez MA, Jaarsma T, Kober L, Lip GY, Maggioni AP, Parkhomenko A, Pieske BM, Popescu BA, Ronnevik PK, Rutten FH, Schwitter J, Seferovic P, Stepinska J, Trindade PT, Voors AA, Zannad F, Zeiher A (2012) ESCGuidelines for the diagnosis and treatment of acute and chronic heart failure 2012: the Task Force for the Diagnosis and Treatment of Acute and Chronic Heart Failure 2012 of the European Society of Cardiology. Developed in collaboration with the Heart Failure Association (HFA) of the ESC. Eur Heart J 33:1787-1847
79. Mehel H, Emons J, Vettel C, Wittköpper K, Seppelt D, Dewenter M, Lutz S, Sossalla S, Maier LS, Lechêne P, Leroy J, Lefebvre F, Varin A, Eschenhagen T, Nattel S, Dobrev D, Zimmermann W-H, Nikolaev VO, Vandecasteele G, Fischmeister R, El-Armouche A (2013) Phoshodiesterase-2 is upregulated in human failing hearts and blunts β-adrenergic responses in cardiomyocytes. J Am Coll Cardiol 62:1596-1606
80. Mika D, Bobin P, Pomérance M, Lechêne P, Westenbroek R, Catterall WA, Vandecasteele G, Leroy J, Fischmeister R (2013) Differential regulation of cardiac excitation-contraction coupling by cAMP phosphodiesterase subtypes. Cardiovasc Res 100:336-346
81. Mika D, Leroy J, Vandecasteele G, Fischmeister R (2012) PDEs create local domains of cAMP signaling. J Mol Cell Cardiol 52:323-329
82. Mika D, Richter W, Westenbroek RE, Catterall WA, Conti M (2014) PDE4B mediates local feedback regulation of β1-adrenergic cAMP signaling in a sarcolemmal compartment of cardiacmyocytes. J Cell Sci 127:1033-1042
83. Miller CL, Oikawa M, Cai Y, Wojtovich AP, Nagel DJ, Xu X, Xu H, Florio V, Rybalkin SD, Beavo JA, Chen YF, Li JD, Blaxall BC, Abe J, Yan C (2009) Role of Ca2+/calmodulin-stimulated cyclic nucleotide phosphodiesterase 1 in mediating cardiomyocyte hypertrophy. Circ Res 105:956-964
84. Mokni W, Keravis T, Etienne-Selloum N, Walter A, Kane MO, Schini-Kerth VB, Lugnier C (2010) Concerted regulation of cGMP and cAMP phosphodiesterases in early cardiac hypertrophy induced by angiotensin II. PLoS One 5:e14227
85. Molina CE, Leroy J, Xie M, Richter W, Lee I-O, Maack C, Rucker-Martin C, Donzeau-Gouge P, Verde I, Hove-Madsen L, Barriga M, Conti M, Vandecasteele G, Fischmeister R (2012) Cyclic AMP phosphodiesterase type 4 protects against atrial arrhythmias. J Am Coll Cardiol 59:2182-2190
86. Mongillo M, McSorley T, Evellin S, Sood A, Lissandron V, Terrin A, Huston E, Hannawacker A, Lohse MJ, Pozzan T, Houslay MD, Zaccolo M (2004) Fluorescence resonance energy transfer-based analysis of cAMP dynamics in live neonatal rat cardiac myocytes reveals distinct functions of compartmentalized phosphodiesterases. Circ Res 95:65-75
87. Morel E, Marcantoni A, Gastineau M, Birkedal R, Rochais F, Garnier A, Lompré A-M, Vandecasteele G, Lezoualc'h F (2005) The cAMP-binding protein Epac induces cardiomyocyte hypertrophy. Circ Res 97:1296-1304
88. Morisco C, Zebrowski DC, Vatner DE, Vatner SF, Sadoshima J (2001) β-Adrenergic cardiac hypertrophy is mediated primarily by the β1-subtype in the rat heart. J Mol Cell Cardiol 33:561-573
89. Movsesian MA (2004) Altered cAMP-mediated signalling and its role in the pathogenesis of dilated cardiomyopathy. Cardiovasc Res 62:450-459 (Pubitemid 38648959)
90. Movsesian MA, Bristow MR (2005) Alterations in cAMP-mediated signaling and their role in the pathophysiology of dilated cardiomyopathy. Curr Top Dev Biol 68:25-48 (Pubitemid 43588862)
91. Nagendran J, Archer SL, Soliman D, Gurtu V, Moudgil R, Haromy A, St Aubin C, Webster L, Rebeyka IM, Ross DB, Light PE, Dyck JR, Michelakis ED (2007) Phosphodiesterase type 5 is highly expressed in the hypertrophied human right ventricle, and acute inhibition of phosphodiesterase type 5 improves contractility. Circulation 116:238-248 (Pubitemid 47196559)
92. Nikolaev VO, Bunemann M, Schmitteckert E, Lohse MJ, Engelhardt S (2006) Cyclic AMP imaging in adult cardiac myocytes reveals far-reaching β1-adrenergic but locally confined β2-adrenergic receptor-mediated signaling. Circ Res 99:1084-1091 (Pubitemid 44729932)
93. Nikolaev VO, Moshkov A, Lyon AR, Miragoli M, Novak P, Paur H, Lohse MJ, Korchev YE, Harding SE, Gorelik J (2010) Beta2-adrenergic receptor redistribution in heart failure changes cAMP compartmentation. Science 327:1653-1657
94. Oikawa M, Wu M, Lim S, Knight WE, Miller CL, Cai Y, Lu Y, Blaxall BC, Takeishi Y, Abe JI, Yan C (2013) Cyclic nucleotide phosphodiesterase 3A1 protects the heart against ischemia-reperfusion injury. J Mol Cell Cardiol 64:11-19
95. Okumura S, Kawabe J, Yatani A, Takagi G, Lee MC, Hong C, Liu J, Takagi I, Sadoshima J, Vatner DE, Vatner SF, Ishikawa Y (2003) Type 5 adenylyl cyclase disruption alters not only sympathetic but also parasympathetic and calcium-mediated cardiac regulation. Circ Res 93:364-371 (Pubitemid 37048249)
96. Okumura S, Takagi G, Kawabe J, Yang GP, Lee MC, Hong C, Liu J, Vatner DE, Sadoshima J, Vatner SF, Ishikawa Y (2003) Disruption of type 5 adenylyl cyclase gene preserves cardiac function against pressure overload. Proc Natl Acad Sci U S A 100:9986-9990 (Pubitemid 37087055)
97. Okumura S, Vatner DE, Kurotani R, Bai Y, Gao S, Yuan Z, Iwatsubo K, Ulucan C, Kawabe J, Ghosh K, Vatner SF, Ishikawa Y (2007) Disruption of type 5 adenylyl cyclase enhances desensitization of cyclic adenosine monophosphate signal and increases Akt signal with chronic catecholamine stress. Circulation 116:1776-1783 (Pubitemid 350287102)
98. Omori K, Kotera J (2007) Overview of PDEs and their regulation. Circ Res 100:309-327
99. Osadchii OE (2007) Cardiac hypertrophy induced by sustained β-adrenoreceptor activation: pathophysiological aspects. Heart Fail Rev 12:66-86
100. Osadchii OE (2007) Myocardial phosphodiesterases and regulation of cardiac contractility in health and cardiac disease. Cardiovasc Drugs Ther 21:171-194
101. Ostrom RS, Naugle JE, Hase M, Gregorian C, Swaney JS, Insel PA, Brunton LL, Meszaros JG (2003) Angiotensin II enhances adenylyl cyclase signaling via Ca2+/calmodulin. Gq-Gs cross-talk regulates collagen production in cardiac fibroblasts. J Biol Chem 278:24461-24468 (Pubitemid 37548597)
102. Packer M, Carver JR, Rodeheffer RJ, Ivanhoe RJ, DiBianco R, Zeldis SM, Hendrix GH, Bommer WJ, Elkayam U, Kukin ML et al (1991) Effect of oral milrinone on mortality in severe chronic heart failure. The PROMISE Study Research Group. N Engl J Med 325:1468-1475
103. Pandit J, Forman MD, Fennell KF, Dillman KS, Menniti FS (2009) Mechanism for the allosteric regulation of phosphodiesterase 2A deduced from the X-ray structure of a near full-length construct. Proc Natl Acad Sci U S A 106:18225-18230
104. Patrucco E, Albergine MS, Santana LF, Beavo JA (2010) Phosphodiesterase 8A (PDE8A) regulates excitation-contraction coupling in ventricular myocytes. J Mol Cell Cardiol 49:330-333
105. 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 (2004) PI3Kgamma modulates the cardiac response to chronic pressure overload by distinct kinase-dependent and -independent effects. Cell 118:375-387 (Pubitemid 39061117)
106. Pavan B, Biondi C, Dalpiaz A (2009) Adenylyl cyclases as innovative therapeutic goals. Drug Discov Today 14:982-991
107. Pereira L, Métrich M, Fernández-Velasco M, Lucas A, Leroy J, Perrier R, Morel E, Fischmeister R, Richard S, Bénitah J-P, Lezoualc'h F, Gómez AM (2007) The cAMP binding protein Epac modulates Ca2+ sparks by Ca2+/calmodulin kinase signalling pathway in rat cardiac myocytes. J Physiol 583:685-694
108. Perino A, Ghigo A, Ferrero E, Morello F, Santulli G, Baillie GS, Damilano F, Dunlop AJ, Pawson C, Walser R, Levi R, Altruda F, Silengo L, Langeberg LK, Neubauer G, Heymans S, Lembo G, Wymann MP, Wetzker R, Houslay MD, Iaccarino G, Scott JD, Hirsch E (2011) Integrating cardiac PIP3 and cAMP signaling through a PKA anchoring function of p110gamma. Mol Cell 42:84-95
109. Petrashevskaya N, Gaume BR, Mihlbachler KA, Dorn GW 2nd, Liggett SB (2008) Bitransgenesis with beta(2)-adrenergic receptors or adenylyl cyclase fails to improve beta(1)-adrenergic receptor cardiomyopathy. Clin Transl Sci 1:221-227
110. Phan HM, Gao MH, Lai NC, Tang T, Hammond HK (2007) New signaling pathways associated with increased cardiac adenylyl cyclase 6 expression: implications for possible congestive heart failure therapy. Trends Cardiovasc Med 17:215-221 (Pubitemid 47532726)
111. Piddo AM, Sanchez MI, Sapaghagar M, Corbalan R, Foncea R, Ebensperger R, Godoy I, Melendez J, Jalil JE, Lavandero S (1996) Cyclic AMP-dependent protein kinase and mechanical heart function in ventricular hypertrophy induced by pressure overload or secondary to myocardial infarction. J Mol Cell Cardiol 28:1073-1083
112. Pokreisz P, Vandenwijngaert S, Bito V, Van den Bergh A, Lenaerts I, Busch C, Marsboom G, Gheysens O, Vermeersch P, Biesmans L, Liu X, Gillijns H, Pellens M, Van Lommel A, Buys E, Schoonjans L, Vanhaecke J, Verbeken E, Sipido K, Herijgers P, Bloch KD, Janssens SP (2009) Ventricular phosphodiesterase-5 expression is increased in patients with advanced heart failure and contributes to adverse ventricular remodeling after myocardial infarction in mice. Circulation 119:408-416
113. Redfield MM, Chen HH, Borlaug BA, Semigran MJ, Lee KL, Lewis G, LeWinter MM, Rouleau JL, Bull DA, Mann DL, Deswal A, Stevenson LW, Givertz MM, Ofili EO, O'Connor CM, Felker GM, Goldsmith SR, Bart BA, McNulty SE, Ibarra JC, Lin G, Oh JK, Patel MR, Kim RJ, Tracy RP, Velazquez EJ, Anstrom KJ, Hernandez AF, Mascette AM, Braunwald E (2013) Effect of phosphodiesterase-5 inhibition on exercise capacity and clinical status in heart failure with preserved ejection fraction: a randomized clinical trial. JAMA 309:1268-1277
114. Richter W, Day P, Agraval R, Bruss MD, Granier S, Wang YL, Rasmussen SGF, Horner K, Wang P, Lei T, Patterson AJ, Kobilka BK, Conti M (2008) Signaling from β1-and β2-adrenergic receptors is defined by differential interactions with PDE4. EMBO J 27:384-393 (Pubitemid 351161657)
115. Richter W, Jin SL, Conti M (2005) Splice variants of the cyclic nucleotide phosphodiesterase PDE4D are differentially expressed and regulated in rat tissue. Biochem J 388:803-811 (Pubitemid 40941566)
116. Richter W, Mika D, Blanchard E, Day P, Conti M (2013) β1- adrenergic receptor antagonists signal via PDE4 translocation. EMBO Rep 14:276-283
117. Richter W, Xie M, Scheitrum C, Krall J, Movsesian MA, Conti M (2011) Conserved expression and functions of PDE4 in rodent and human heart. Basic Res Cardiol 106:249-262
118. Rochais F, Abi-Gerges A, Horner K, Lefebvre F, Cooper DMF, Conti M, Fischmeister R, Vandecasteele G (2006) A specific pattern of phosphodiesterases controls the cAMP signals generated by different Gs-coupled receptors in adult rat ventricular myocytes. Circ Res 98:1081-1088
119. Rochais F, Vandecasteele G, Lefebvre F, Lugnier C, Lum H, Mazet J-L, Cooper DMF, Fischmeister R (2004) 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 279:52095-52105 (Pubitemid 39656582)
120. Roth DM, Bayat H, Drumm JD, Gao MH, Swaney JS, Ander A, Hammond HK (2002) Adenylyl cyclase increases survival in cardiomyopathy. Circulation 105:1989-1994 (Pubitemid 34437629)
121. Sadana R, Dessauer CW (2009) Physiological roles for G protein-regulated adenylyl cyclase isoforms: insights from knockout and overexpression studies. Neurosignals 17:5-22
122. Sastry A, Arnold E, Gurji H, Iwasa A, Bui H, Hassankhani A, Patel HH, Feramisco JR, Roth DM, Lai NC, Hammond HK, Narayan SM (2006) Cardiac-directed expression of adenylyl cyclase VI facilitates atrioventricular nodal conduction. J Am Coll Cardiol 48:559-565 (Pubitemid 44093943)
123. Sato N, Asai K, Okumura S, Takagi G, Shannon RP, FujitaYamaguchi Y, Ishikawa Y, Vatner SF, Vatner DE (1999) Mechanisms of desensitization to a PDE inhibitor (Milrinone) in conscious dogs with heart failure. Am J Physiol Heart Circ Physiol 45:H1699-H1705 (Pubitemid 29246559)
124. Schillace RV, Scott JD (1999) Organization of kinases, phosphatases, and receptor signaling complexes. J Clin Invest 103:761-765 (Pubitemid 29152620)
125. Shahid M, Nicholson CD (1990) Comparison of cyclic nucleotide phosphodiesterase isoenzymes in rat and rabbit ventricular myocardium - positive inotropic and phosphodiesterase inhibitory effects of Org-30029, milrinone and rolipram. Naunyn-Schmiedebergs Arch Pharmacol 342:698-705
126. Sin YY, Edwards HV, Li X, Day JP, Christian F, Dunlop AJ, Adams DR, Zaccolo M, Houslay MD, Baillie GS (2011) Disruption of the cyclic AMP phosphodiesterase-4 (PDE4)-HSP20 complex attenuates the beta-agonist induced hypertrophic response in cardiac myocytes. J Mol Cell Cardiol 50:872-883
127. Smith CJ, Huang R, Sun D, Ricketts S, Hoegler C, Ding JZ, Moggio RA, Hintze TH (1997) Development of decompensated dilated cardiomyopathy is associated with decreased gene expression and activity of the milrinone-sensitive cAMP phosphodiesterase PDE3A. Circulation 96:3116-3123 (Pubitemid 27500116)
128. Stangherlin A, Gesellchen F, Zoccarato A, Terrin A, Fields LA, Berrera M, Surdo NC, Craig MA, Smith G, Hamilton G, Zaccolo M (2011) cGMP Signals modulate cAMP levels in a compartment-specific manner to regulate catecholamine- dependent signaling in cardiac myocytes. Circ Res 108:929-939
129. Sugano Y, Lai NC, Gao MH, Firth AL, Yuan JX, Lew WY, Hammond HK (2011) Activated expression of cardiac adenylyl cyclase 6 reduces dilation and dysfunction of the pressure-overloaded heart. Biochem Biophys Res Commun 405:349-355
130. Sun B, Li H, Shakur Y, Hensley J, Hockman S, Kambayashi J, Manganiello VC, Liu Y (2007) Role of phosphodiesterase type 3A and 3B in regulating platelet and cardiac function using subtype-selective knockout mice. Cell Signal 19:1765-1771 (Pubitemid 46935432)
131. Swaney JS, Roth DM, Olson ER, Naugle JE, Meszaros JG, Insel PA (2005) Inhibition of cardiac myofibroblast formation and collagen synthesis by activation and overexpression of adenylyl cyclase. Proc Natl Acad Sci U S A 102:437-442 (Pubitemid 40116785)
132. Takahashi T, Tang T, Lai NC, Roth DM, Rebolledo B, Saito M, Lew WY, Clopton P, Hammond HK (2006) Increased cardiac adenylyl cyclase expression is associated with increased survival after myocardial infarction. Circulation 114:388-396 (Pubitemid 44264820)
133. Tang T, Gao MH, Lai NC, Firth AL, Takahashi T, Guo T, Yuan JX, Roth DM, Hammond HK (2008) Adenylyl cyclase type 6 deletion decreases left ventricular function via impaired calcium handling. Circulation 117:61-69 (Pubitemid 350291182)
134. Tang T, Hammond HK (2013) Gene transfer for congestive heart failure: update 2013. Transl Res 161:313-320
135. Tang T, Hammond HK, Firth A, Yang Y, Gao MH, Yuan JX, Lai NC (2011) Adenylyl cyclase 6 improves calcium uptake and left ventricular function in aged hearts. J Am Coll Cardiol 57:1846-1855
136. Tang T, Lai NC, Hammond HK, Roth DM, Yang Y, Guo T, Gao MH (2010) Adenylyl cyclase 6 deletion reduces left ventricular hypertrophy, dilation, dysfunction, and fibrosis in pressure-overloaded female mice. J Am Coll Cardiol 55:1476-1486
137. Tang T, Lai NC, Roth DM, Drumm J, Guo T, Lee KW, Han PL, Dalton N, Gao MH (2006) Adenylyl cyclase type V deletion increases basal left ventricular function and reduces left ventricular contractile responsiveness to beta-adrenergic stimulation. Basic Res Cardiol 101:117-126 (Pubitemid 43250803)
138. Tasken K, Aandahl EM (2004) Localized effects of cAMP mediated by distinct routes of protein kinase A. Physiol Rev 84:137-167 (Pubitemid 38049878)
139. Tepe NM, Lorenz JN, Yatani A, Dash R, Kranias EG, Dorn GW 2nd, Liggett SB (1999) Altering the receptor-effector ratio by transgenic overexpression of type V adenylyl cyclase: enhanced basal catalytic activity and function without increased cardiomyocyte beta-adrenergic signalling. Biochemistry 38:16706-16713
140. Terrenoire C, HouslayMD, Baillie GS, Kass RS (2009) The cardiac IKs potassium channel macromolecular complex includes the phosphodiesterase PDE4D3. J Biol Chem 284:9140-9146
141. Tesmer JJ, Sunahara RK, Gilman AG, Sprang SR (1997) Crystal structure of the catalytic domains of adenylyl cyclase in a complex with Gsalpha.GTPgammaS. Science 278:1907-1916 (Pubitemid 28013225)
142. Timofeyev V, He Y, Tuteja D, Zhang Q, Roth DM, Hammond HK, Chiamvimonvat N (2006) Cardiac-directed expression of adenylyl cyclase reverses electrical remodeling in cardiomyopathy. J Mol Cell Cardiol 41:170-181 (Pubitemid 43946968)
143. Timofeyev V, Myers RE, Kim HJ, Woltz RL, Sirish P, Heiserman J, Li N, Singapuri A, Tang T, Yarov-Yarovoy V, Yamoah EN, Hammond HK, Chiamvimonvat N (2013) Adenylyl cyclase subtype-specific compartmentalization: differential regulation of L-type Ca2+ current in ventricular myocytes. Circ Res 112:1567-1576
144. Timofeyev V, Porter CA, Tuteja D, Qiu H, Li N, Tang T, Singapuri A, Han PL, Lopez JE, Hammond HK, Chiamvimonvat N (2010) Disruption of adenylyl cyclase type V does not rescue the phenotype of cardiac-specific overexpression of Galphaq protein-induced cardiomyopathy. Am J Physiol Heart Circ Physiol 299:H1459-H1467
145. Vandecasteele G, Verde I, Rucker-Martin C, Donzeau-Gouge P, Fischmeister R (2001) Cyclic GMP regulation of the L-type Ca2+ channel current in human atrial myocytes. J Physiol 533:329-340 (Pubitemid 32519991)
146. Vandeput F, Szabo-Fresnais N, Ahmad F, Kho C, Lee A, Krall J, Dunlop A, Hazel MW, Wohlschlegel JA, Hajjar RJ, Houslay MD, Manganiello VC, Movsesian MA (2013) Selective regulation of cyclic nucleotide phosphodiesterase PDE3A isoforms. Proc Natl Acad Sci U S A 110:19778-19783
147. Vandeput F, Wolda SL, Krall J, Hambleton R, Uher L, McCaw KN, Radwanski PB, Florio V, Movsesian MA (2007) Cyclic nucleotide phosphodiesterase PDE1C in human cardiac myocytes. J Biol Chem 282:32749-32757 (Pubitemid 350159317)
148. Vatner SF, Yan L, Ishikawa Y, Vatner DE, Sadoshima J (2009) Adenylyl cyclase type 5 disruption prolongs longevity and protects the heart against stress. Circ J 73:195-200
149. Verde I, Pahlke G, Salanova M, Zhang G, Wang S, Coletti D, Onuffer J, Jin SLC, Conti M (2001) Myomegalin is a novel protein of the Golgi/centrosome that interacts with a cyclic nucleotide phosphodiesterase. J Biol Chem 276:11189-11198 (Pubitemid 38089303)
150. Wechsler J, Choi YH, Krall J, Ahmad F, Manganiello VC, Movsesian MA (2002) Isoforms of cyclic nucleotide phosphodiesterase PDE3A in cardiac myocytes. J Biol Chem 277:38072-38078 (Pubitemid 35154659)
151. Wright PT, Nikolaev VO, O'Hara T, Diakonov I, Bhargava A, Tokar S, Schobesberger S, Shevchuk AI, Sikkel MB, Wilkinson R, Trayanova NA, Lyon AR, Harding SE, Gorelik J (2014) Caveolin-3 regulates compartmentation of cardiomyocyte beta2-adrenergic receptor-mediated cAMP signaling. J Mol Cell Cardiol 67:38-48
152. Yan L, Vatner DE, O'Connor JP, Ivessa A, Ge H, Chen W, Hirotani S, Ishikawa Y, Sadoshima J, Vatner SF (2007) Type 5 adenylyl cyclase disruption increases longevity and protects against stress. Cell 130:247-258 (Pubitemid 47081133)
153. Younes A, Lyashkov AE, Graham D, Sheydina A, Volkova MV, Mitsak M, Vinogradova TM, Lukyanenko YO, Li Y, Ruknudin AM, Boheler KR, van Eyk J, Lakatta EG (2008) Ca2+-stimulated basal adenylyl cyclase activity localization in membrane lipid microdomains of cardiac sinoatrial nodal pacemaker cells. J Biol Chem 283:14461-14468