Phosphodiesterases and cyclic GMP regulation in heart muscle

Physiology

Volumn 27, Issue 4, 2012, Pages 248-258

  Lee, Dong I ^a   Kass, David A ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE 1; PHOSPHODIESTERASE;

ANIMAL; ENZYMOLOGY; HEART; HEART MUSCLE; HUMAN; METABOLISM; PHYSIOLOGY; REVIEW;

ANIMALS; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASE TYPE I; HEART; HUMANS; MYOCARDIUM; PHOSPHORIC DIESTER HYDROLASES;

EID: 84864927698     PISSN: 15489213     EISSN: 15489221     Source Type: Journal    
DOI: 10.1152/physiol.00011.2012     Document Type: Review

References (99)

1. Adamo CM, Dai DF, Percival JM, Minami E, Willis MS, Patrucco E, Froehner SC, Beavo JA. Sildenafil reverses cardiac dysfunction in the mdx mouse model of Duchenne muscular dystrophy. Proc Natl Acad Sci USA 107: 19079-19083, 2010.
2. Andersen A, Nielsen JM, Peters CD, Schou UK, Sloth E, Nielsen-Kudsk JE. Effects of phosphodiesterase-5 inhibition by sildenafil in the pressure overloaded right heart. Eur J Heart Failure 10: 1158-1165, 2008.
3. Beavo JA, Hardman JG, Sutherland EW. Stimulation of adenosine 3',5'-monophosphate hydrolysis by guanosine 3',5'-monophosphate. J Biol Chem 246: 3841-3846, 1971.
4. Bender AT, Beavo JA. Cyclic nucleotide phosphodiesterases: molecular regulation to clinical use. Pharmacol Rev 58: 488-520, 2006.
5. Bishu K, Hamdani N, Mohammed SF, Kruger M, Ohtani T, Ogut O, Brozovich FV, Burnett JC Jr, Linke WA, Redfield MM. Sildenafil and B-type natriuretic peptide acutely phosphorylate titin and improve diastolic distensibility in vivo. Circulation 124: 2882-2891, 2011.
6. Borlaug BA, Melenovsky V, Marhin T, Fitzgerald P, Kass DA. Sildenafil inhibits beta-adrenergic-stimulated cardiac contractility in humans. Circulation 112: 2642-2649, 2005.
7. Castro LR, Schittl J, Fischmeister R. Feedback control through cGMP-dependent protein kinase contributes to differential regulation and compartmentation of cGMP in rat cardiac myocytes. Circ Res 107: 1232-1240, 2010.
8. Castro LR, Verde I, Cooper DM, Fischmeister R. Cyclic guanosine monophosphate compartmentation in rat cardiac myocytes. Circulation 113: 2221-2228, 2006.
9. Chau VQ, Salloum FN, Hoke NN, Abbate A, Kukreja RC. Mitigation of the progression of heart failure with sildenafil involves inhibition of RhoA/Rho-kinase pathway. Am J Physiol Heart Circ Physiol 300: H2272-H2279, 2011.
10. Clapham JC, Wilderspin AF. Cloning of dog heart PDE1A-A first detailed characterization at the molecular level in this species. Gene 268: 165-171, 2001.
11. Coquil JF, Franks DJ, Wells JN, Dupuis M, Hamet P. Characteristics of a new binding protein distinct from the kinase for guanosine 3=: 5=-monophosphate in rat platelets. Biochim Biophys Acta 631: 148-165, 1980.
12. Corbin J, Rannels S, Neal D, Chang P, Grimes K, Beasley A, Francis S. Sildenafil citrate does not affect cardiac contractility in human or dog heart. Curr Med Res Opin 19: 747-752, 2003.
13. Corbin JD, Turko IV, Beasley A, Francis SH. Phosphorylation of phosphodiesterase-5 by cyclic nucleotide-dependent protein kinase alters its catalytic and allosteric cGMP-binding activities. Eur J Biochem 267: 2760-2767, 2000.
14. Das A, Salloum FN, Xi L, Rao YJ, Kukreja RC. ERK phosphorylation mediates sildenafil-induced myocardial protection against ischemia-reperfusion injury in mice. Am J Physiol Heart Circ Physiol 296: H1236-H1243, 2009.
15. Das A, Xi L, Kukreja RC. Phosphodiesterase-5 inhibitor sildenafil preconditions adult cardiac myocytes against necrosis and apoptosis. Essential role of nitric oxide signaling. J Biol Chem 280: 12944-12955, 2005.
16. Das A, Xi L, Kukreja RC. Protein kinase Gdependent cardioprotective mechanism of phosphodiesterase-5 inhibition involves phosphorylation of ERK and GSK3beta. J Biol Chem 283: 29572-29585, 2008.
17. Dunkern TR, Hatzelmann A. Characterization of inhibitors of phosphodiesterase 1C on a human cellular system. FEBS J 274: 4812-4824, 2007.
18. Fischmeister R, Castro L, bi-Gerges A, Rochais F, Vandecasteele G. Species-and tissue-dependent effects of NO and cyclic GMP on cardiac ion channels. Comp Biochem Physiol A Mol Integr Physiol 142: 136-143, 2005.
19. Fisher PW, Salloum F, Das A, Hyder H, Kukreja RC. Phosphodiesterase-5 inhibition with sildenafil attenuates cardiomyocyte apoptosis and left ventricular dysfunction in a chronic model of doxorubicin cardiotoxicity. Circulation 111: 1601-1610, 2005.
20. Francis SH. The role of cGMP-dependent protein kinase in controlling cardiomyocyte cGMP. Circ Res 107: 1164-1166, 2010.
21. Francis SH, Blount MA, Corbin JD. Mammalian cyclic nucleotide phosphodiesterases: molecular mechanisms and physiological functions. Physiol Rev 91: 651-690, 2011.
22. Francis SH, Lincoln TM, Corbin JD. Characterization of a novel cGMP binding protein from rat lung. J Biol Chem 255: 620-626, 1980.
23. Giannetta E, Isidori AM, Galea N, Carbone I, Mandosi E, Vizza CD, Naro F, Morano S, Fedele F, Lenzi A. Chronic inhibition of cyclic GMP phosphodiesterase 5A improves diabetic cardiomyopathy: a randomized, controlled clinical trial using magnetic resonance imaging with myocardial tagging. Circulation 125: 2323-2333, 2012.
24. Guazzi M, Arena R. The impact of pharmacotherapy on the cardiopulmonary exercise test response in patients with heart failure: a mini review. Curr Vasc Pharmacol 7: 557-569, 2009.
25. Guazzi M, Vicenzi M, Arena R, Guazzi MD. PDE5 inhibition with sildenafil improves left ventricular diastolic function, cardiac geometry, and clinical status in patients with stable systolic heart failure: results of a 1-year, prospective, randomized, placebo-controlled study. Circ Heart Fail 4: 8-17, 2011.
26. Heikaus CC, Pandit J, Klevit RE. Cyclic nucleotide binding GAF domains from phosphodiesterases: structural and mechanistic insights. Structure 17: 1551-1557, 2009.
27. Hoke NN, Salloum FN, Kass DA, Das A, Kukreja RC. Preconditioning by phosphodiesterase-5 inhibition improves therapeutic efficacy of adiposederived stem cells following myocardial infarction in mice. Stem Cells 30: 326-335, 2012.
28. Hsu S, Nagayama T, Koitabashi N, Zhang M, Zhou L, Bedja D, Gabrielson KL, Molkentin JD, Kass DA, Takimoto E. Phosphodiesterase 5 inhibition blocks pressure overload-induced cardiac hypertrophy independent of the calcineurin pathway. Cardiovasc Res 81: 301-309, 2009.
29. Johnson WB, Katugampola S, Able S, Napier C, Harding SE. Profiling of cAMP and cGMP phosphodiesterases in isolated ventricular cardiomyocytes from human hearts: comparison with rat and guinea pig. Life Sci 90: 328-336, 2012.
30. Kim D, Rybalkin SD, Pi X, Wang Y, Zhang C, Munzel T, Beavo JA, Berk BC, Yan C. Upregulation of phosphodiesterase 1A1 expression is associated with the development of nitrate tolerance. Circulation 104: 2338-2343, 2001.
31. Kim KH, Kim YJ, Ohn JH, Yang J, Lee SE, Lee SW, Kim HK, Seo JW, Sohn DW. Long-term effects of sildenafil in a rat model of chronic mitral regurgitation: benefits of ventricular remodeling and exercise capacity. Circulation 125: 1390-1401, 2012.
32. Kobayashi YM, Rader EP, Crawford RW, Iyengar NK, Thedens DR, Faulkner JA, Parikh SV, Weiss RM, Chamberlain JS, Moore SA, Campbell KP. Sarcolemma-localized nNOS is required to maintain activity after mild exercise. Nature 456: 511-515, 2008.
33. Koitabashi N, Aiba T, Hesketh GG, Rowell J, Zhang M, Takimoto E, Tomaselli GF, Kass DA. Cyclic GMP/PKG-dependent inhibition of TRPC6 channel activity and expression negatively regulates cardiomyocyte NFAT activation. Novel mechanism of cardiac stress modulation by PDE5 inhibition. J Mol Cell Cardiol 48: 713-724, 2010.
34. Koka S, Das A, Zhu SG, Durrant D, Xi L, Kukreja RC. Long-acting phosphodiesterase-5 inhibitor tadalafil attenuates doxorubicin-induced cardiomyopathy without interfering with chemotherapeutic effect. J Pharmacol Exp Ther 334: 1023-1030, 2010.
35. Koka S, Kukreja RC. Attenuation of doxorubicininduced cardiotoxicity by tadalafil: a long acting phosphodiesterase-5 inhibitor. Mol Cell Pharmacol 2: 173-178, 2010.
36. Kruger M, Kotter S, Grutzner A, Lang P, Andresen C, Redfield MM, Butt E, dos Remedios CG, Linke WA. Protein kinase G modulates human myocardial passive stiffness by phosphorylation of the titin springs. Circ Res 104: 87-94, 2009.
37. Kruger M, Linke WA. Titin-based mechanical signalling in normal and failing myocardium. J Mol Cell Cardiol 46: 490-498, 2009.
38. Kukreja RC, Salloum F, Das A, Ockaili R, Yin C, Bremer YA, Fisher PW, Wittkamp M, Hawkins J, Chou E, Kukreja AK, Wang X, Marwaha VR, Xi L. Pharmacological preconditioning with sildenafil: basic mechanisms and clinical implications. Vascul Pharmacol 42: 219-232, 2005.
39. Kuwahara K, Wang Y, McAnally J, Richardson JA, Bassel-Duby R, Hill JA, Olson EN. TRPC6 fulfills a calcineurin signaling circuit during pathologic cardiac remodeling. J Clin Invest 116: 3114-3126, 2006.
40. Lee DI, Vahebi S, Tocchetti CG, Barouch LA, Solaro RJ, Takimoto E, Kass DA. PDE5A suppression of acute beta-adrenergic activation requires modulation of myocyte beta-3 signaling coupled to PKG-mediated troponin I phosphorylation. Basic Res Cardiol 105: 337-347, 2010.
41. Lewis GD, Shah R, Shahzad K, Camuso JM, Pappagianopoulos PP, Hung J, Tawakol A, Gerszten RE, Systrom DM, Bloch KD, Semigran MJ. Sildenafil improves exercise capacity and quality of life in patients with systolic heart failure and secondary pulmonary hypertension. Circulation 116: 1555-1562, 2007.
42. Loughney K, Martins TJ, Harris EA, Sadhu K, Hicks JB, Sonnenburg WK, Beavo JA, Ferguson K. Isolation and characterization of cDNAs corresponding to two human calcium, calmodulin-regulated, 3',5'-cyclic nucleotide phosphodiesterases. J Biol Chem 271: 796-806, 1996.
43. Lu Z, Xu X, Hu X, Lee S, Traverse JH, Zhu G, Fassett J, Tao Y, Zhang P, dos RC, Pritzker M, Hall JL, Garry DJ, Chen Y. Oxidative stress regulates left ventricular PDE5 expression in the failing heart. Circulation 121: 1474-1483, 2010.
44. Lugnier C. Cyclic nucleotide phosphodiesterase (PDE) superfamily: a new target for the development of specific therapeutic agents. Pharmacol Ther 109: 366-398, 2006.
45. Lugnier C, Schoeffter P, Le BA, Strouthou E, Stoclet JC. Selective inhibition of cyclic nucleotide phosphodiesterases of human, bovine and rat aorta. Biochem Pharmacol 35: 1743-1751, 1986.
46. Madhani M, Hall AR, Cuello F, Charles RL, Burgoyne JR, Fuller W, Hobbs AJ, Shattock MJ, Eaton P. Phospholemman Ser69 phosphorylation contributes to sildenafil-induced cardioprotection against reperfusion injury. Am J Physiol Heart Circ Physiol 299: H827-H836, 2010.
47. Martinez SE, Bruder S, Schultz A, Zheng N, Schultz JE, Beavo JA, Linder JU. Crystal structure of the tandem GAF domains from a cyanobacterial adenylyl cyclase: modes of ligand binding and dimerization. Proc Natl Acad Sci USA 102: 3082-3087, 2005.
48. Martinez SE, Wu AY, Glavas NA, Tang XB, Turley S, Hol WG, Beavo JA. The two GAF domains in phosphodiesterase 2A have distinct roles in dimerization and in cGMP binding. Proc Natl Acad Sci USA 99: 13260-13265, 2002.
49. Miller CL, Cai Y, Oikawa M, Thomas T, Dostmann WR, Zaccolo M, Fujiwara K, Yan C. Cyclic nucleotide phosphodiesterase 1A: a key regulator of cardiac fibroblast activation and extracellular matrix remodeling in the heart. Basic Res Cardiol 106: 1023-1039, 2011.
50. 2+/calmodulin-stimulated cyclic nucleotide phosphodiesterase 1 in mediating cardiomyocyte hypertrophy. Circ Res 105: 956-964, 2009.
51. Miller CL, Yan C. Targeting cyclic nucleotide phosphodiesterase in the heart: therapeutic implications. J Cardiovasc Transl Res 3: 507-515, 2010.
52. Mokni W, Keravis T, Etienne-Selloum N, Walter A, Kane MO, Schini-Kerth VB, Lugnier C. Concerted regulation of cGMP and cAMP phosphodiesterases in early cardiac hypertrophy induced by angiotensin II. PLos One 5: e14227, 2010.
53. Mongillo M, Tocchetti CG, Terrin A, Lissandron V, Cheung YF, Dostmann WR, Pozzan T, Kass DA, Paolocci N, Houslay MD, Zaccolo M. Compartmentalized phosphodiesterase-2 activity blunts beta-adrenergic cardiac inotropy via an NO/ cGMP-dependent pathway. Circ Res 98: 226-234, 2006.
54. Movsesian MA, Kukreja RC. Phosphodiesterase inhibition in heart failure. Handb Exp Pharmacol: 237-249, 2011.
55. Nagayama T, Hsu S, Zhang M, Koitabashi N, Bedja D, Gabrielson KL, Takimoto E, Kass DA. Pressure-overload magnitude-dependence of the anti-hypertrophic efficacy of PDE5A inhibition. J Mol Cell Cardiol 46: 560-567, 2009.
56. Nagayama T, Hsu S, Zhang M, Koitabashi N, Bedja D, Gabrielson KL, Takimoto E, Kass DA. Sildenafil stops progressive chamber, cellular, and molecular remodeling and improves calcium handling and function in hearts with pre-existing advanced hypertrophy caused by pressure overload. J Am Coll Cardiol 53: 207-215, 2009.
57. Nagayama T, Zhang M, Hsu S, Takimoto E, Kass DA. Sustained soluble guanylate cyclase stimulation offsets nitric-oxide synthase inhibition to restore acute cardiac modulation by sildenafil. J Pharmacol Exp Ther 326: 380-387, 2008.
58. 2+/ calmodulin-stimulated phosphodiesterase 1A in vascular smooth muscle cell growth and survival. Circ Res 98: 777-784, 2006.
59. Nagendran J, Archer SL, Soliman D, Gurtu V, Moudgil R, Haromy A, St AC, Webster L, Rebeyka IM, Ross DB, Light PE, Dyck JR, Michelakis ED. 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, 2007.
60. Nishida M, Watanabe K, Sato Y, Nakaya M, Kitajima N, Ide T, Inoue R, Kurose H. Phosphorylation of TRPC6 channels at Thr69 is required for antihypertrophic effects of phosphodiesterase 5 inhibition. J Biol Chem 285: 13244-13253, 2010.
61. Onody A, Zvara A, Hackler L Jr, Vigh L, Ferdinandy P, Puskas LG. Effect of classic preconditioning on the gene expression pattern of rat hearts: a DNA microarray study. FEBS Lett 536: 35-40, 2003.
62. Pandit J, Forman MD, Fennell KF, Dillman KS, Menniti FS. Mechanism for the allosteric regulation of phosphodiesterase 2A deduced from the X-ray structure of a near full-length construct. Proc Natl Acad Sci USA 106: 18225-18230, 2009.
63. Pokreisz P, Vandenwijngaert S, Bito V, Van den BA, Lenaerts I, Busch C, Marsboom G, Gheysens O, Vermeersch P, Biesmans L, Liu X, Gillijns H, Pellens M, Van LA, Buys E, Schoonjans L, Vanhaecke J, Verbeken E, Sipido K, Herijgers P, Bloch KD, Janssens SP. 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, 2009.
64. Reed TM, Repaske DR, Snyder GL, Greengard P, Vorhees CV. Phosphodiesterase 1B knock-out mice exhibit exaggerated locomotor hyperactivity and DARPP-32 phosphorylation in response to dopamine agonists and display impaired spatial learning. J Neurosci 22: 5188-5197, 2002.
65. Rentero C, Monfort A, Puigdomenech P. Identification and distribution of different mRNA variants produced by differential splicing in the human phosphodiesterase 9A gene. Biochem Biophys Res Commun 301: 686-692, 2003.
66. Rosman GJ, Martins TJ, Sonnenburg WK, Beavo JA, Ferguson K, Loughney K. Isolation and characterization of human cDNAs encoding a cGMP-stimulated 3=,5=-cyclic nucleotide phosphodiesterase. Gene 191: 89-95, 1997.
67. Rowell J, Koitabashi N, Kass DA. TRP-ing up heart and vessels: canonical transient receptor potential channels and cardiovascular disease. J Cardiovasc Trans Res 3: 516-524, 2010.
68. Rybalkin SD, Rybalkina I, Beavo JA, Bornfeldt KE. Cyclic nucleotide phosphodiesterase 1C promotes human arterial smooth muscle cell proliferation. Circ Res 90: 151-157, 2002.
69. Rybalkin SD, Rybalkina IG, Shimizu-Albergine M, Tang XB, Beavo JA. PDE5 is converted to an activated state upon cGMP binding to the GAF A domain. EMBO J 22: 469-478, 2003.
70. Rybalkin SD, Yan C, Bornfeldt KE, Beavo JA. Cyclic GMP phosphodiesterases and regulation of smooth muscle function. Circ Res 93: 280-291, 2003.
71. Sander M, Chavoshan B, Harris SA, Iannaccone ST, Stull JT, Thomas GD, Victor RG. Functional muscle ischemia in neuronal nitric oxide synthase-deficient skeletal muscle of children with Duchenne muscular dystrophy. Proc Natl Acad Sci USA 97: 13818-13823, 2000.
72. Schafer S, Ellinghaus P, Janssen W, Kramer F, Lustig K, Milting H, Kast R, Klein M. Chronic inhibition of phosphodiesterase 5 does not prevent pressure-overload-induced right-ventricular remodelling. Cardiovasc Res 82: 30-39, 2009.
73. Senzaki H, Smith CJ, Juang GJ, Isoda T, Mayer SP, Ohler A, Paolocci N, Tomaselli GF, Hare JM, Kass DA. Cardiac phosphodiesterase 5 (cGMPspecific) modulates beta-adrenergic signaling in vivo and is down-regulated in heart failure. FASEB J 15: 1718-1726, 2001.
74. Shan X, Quaile MP, Monk JK, French B, Cappola TP, Margulies KB. Differential expression of PDE5 in failing and nonfailing human myocardium. Circ Heart Fail 5: 79-86, 2012.
75. Sharma RK, Wang JH. Differential regulation of bovine brain calmodulin-dependent cyclic nucleotide phosphodiesterase isoenzymes by cyclic AMP-dependent protein kinase and calmodulindependent phosphatase. Proc Natl Acad Sci USA 82: 2603-2607, 1985.
76. Sonnenburg WK, Seger D, Beavo JA. Molecular cloning of a cDNA encoding the "61-kDa" calmodulin-stimulated cyclic nucleotide phosphodiesterase. Tissue-specific expression of structurally related isoforms. J Biol Chem 268: 645-652, 1993.
77. Sonnenburg WK, Seger D, Kwak KS, Huang J, Charbonneau H, Beavo JA. Identification of inhibitory and calmodulin-binding domains of the PDE1A1 and PDE1A2 calmodulin-stimulated cyclic nucleotide phosphodiesterases. J Biol Chem 270: 30989-31000, 1995.
78. Sopory S, Balaji S, Srinivasan N, Visweswariah SS. Modeling and mutational analysis of the GAF domain of the cGMP-binding, cGMP-specific phosphodiesterase, PDE5. FEBS Lett 539: 161-166, 2003.
79. Stangherlin A, Gesellchen F, Zoccarato A, Terrin A, Fields LA, Berrera M, Surdo NC, Craig MA, Smith G, Hamilton G, Zaccolo M. cGMP signals modulate cAMP levels in a compartment-specific manner to regulate catecholamine-dependent signaling in cardiac myocytes. Circ Res 108: 929-939, 2011.
80. Stephenson DT, Coskran TM, Wilhelms MB, Adamowicz WO, O'Donnell MM, Muravnick KB, Menniti FS, Kleiman RJ, Morton D. Immunohistochemical localization of phosphodiesterase 2A in multiple mammalian species. J Histochem Cytochem 57: 933-949, 2009.
81. Takimoto E, Belardi D, Tocchetti CG, Vahebi S, Cormaci G, Ketner EA, Moens AL, Champion HC, Kass DA. Compartmentalization of cardiac betaadrenergic inotropy modulation by phosphodiesterase type 5. Circulation 115: 2159-2167, 2007.
82. 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 96: 100-109, 2005.
83. Takimoto E, Champion HC, Li M, Belardi D, Ren S, Rodriguez ER, Bedja D, Gabrielson KL, Wang Y, Kass DA. Chronic inhibition of cyclic GMP phosphodiesterase 5A prevents and reverses cardiac hypertrophy. Nat Med 11: 214-222, 2005.
84. Takimoto E, Koitabashi N, Hsu S, Ketner EA, Zhang M, Nagayama T, Bedja D, Gabrielson KL, Blanton R, Siderovski DP, Mendelsohn ME, Kass DA. Regulator of G protein signaling 2 mediates cardiac compensation to pressure overload and antihypertrophic effects of PDE5 inhibition in mice. J Clin Invest 119: 408-420, 2009.
85. Tokudome T, Kishimoto I, Horio T, Arai Y, Schwenke DO, Hino J, Okano I, Kawano Y, Kohno M, Miyazato M, Nakao K, Kangawa K. Regulator of G-protein signaling subtype 4 mediates antihypertrophic effect of locally secreted natriuretic peptides in the heart. Circulation 117: 2329-2339, 2008.
86. Tsai EJ, Kass DA. Cyclic GMP signaling in cardiovascular pathophysiology and therapeutics. Pharmacol Ther 122: 216-238, 2009.
87. 2+ channel current in human atrial myocytes. J Physiol 533: 329-340, 2001.
88. Vandeput F, Krall J, Ockaili R, Salloum FN, Florio V, Corbin JD, Francis SH, Kukreja RC, Movsesian MA. cGMP-hydrolytic activity and its inhibition by sildenafil in normal and failing human and mouse myocardium. J Pharmacol Exp Ther 330: 884-891, 2009.
89. Vandeput F, Wolda SL, Krall J, Hambleton R, Uher L, McCaw KN, Radwanski PB, Florio V, Movsesian MA. Cyclic nucleotide phosphodiesterase PDE1C1 in human cardiac myocytes. J Biol Chem 282: 32749-32757, 2007.
90. Wallis RM, Corbin JD, Francis SH, Ellis P. Tissue distribution of phosphodiesterase families and the effects of sildenafil on tissue cyclic nucleotides, platelet function, and the contractile responses of trabeculae carneae and aortic rings in vitro. Am J Cardiol 83: 3C-12C, 1999.
91. 2+ current in cardiac myocytes. J Mol Cell Cardiol 47: 304-314, 2009.
92. Wang H, Robinson H, Ke H. Conformation changes, N-terminal involvement, and cGMP signal relay in the phosphodiesterase-5 GAF domain. J Biol Chem 285: 38149-38156, 2010.
93. Wu AY, Tang XB, Martinez SE, Ikeda K, Beavo JA. Molecular determinants for cyclic nucleotide binding to the regulatory domains of phosphodiesterase 2A. J Biol Chem 279: 37928-37938, 2004.
94. 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 67: 973-979, 2003.
95. Zaccolo M, Movsesian MA. cAMP and cGMP signaling cross-talk: role of phosphodiesterases and implications for cardiac pathophysiology. Circ Res 100: 1569-1578, 2007.
96. Zhang M, Kass DA. Phosphodiesterases and cardiac cGMP: evolving roles and controversies. Trends Pharmacol Sci 32: 360-365, 2011.
97. Zhang M, Koitabashi N, Nagayama T, Rambaran R, Feng N, Takimoto E, Koenke T, O'Rourke B, Champion HC, Crow MT, Kass DA. Expression, activity, and pro-hypertrophic effects of PDE5A in cardiac myocytes. Cell Signal 20: 2231-2236, 2008.
98. Zhang M, Takimoto E, Hsu S, Lee DI, Nagayama T, Danner T, Koitabashi N, Barth AS, Bedja D, Gabrielson KL, Wang Y, Kass DA. Myocardial remodeling is controlled by myocyte-targeted gene regulation of phosphodiesterase type 5. J Am Coll Cardiol 56: 2021-2030, 2010.
99. Zoraghi R, Bessay EP, Corbin JD, Francis SH. Structural and functional features in human PDE5A1 regulatory domain that provide for allosteric cGMP binding, dimerization, and regulation. J Biol Chem 280: 12051-12063, 2005.