Cyclic GMP-dependent signaling in cardiac myocytes

Circulation Journal

Volumn 76, Issue 8, 2012, Pages 1819-1825

  Takimoto, Eiki ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

cGMP dependent protein kinase; Cyclic GMP (cGMP); Myocytes; Phosphodiesterases

Indexed keywords

8 BROMO CYCLIC GMP; ANGIOTENSIN II; BETA 3 ADRENERGIC RECEPTOR; BRAIN NATRIURETIC PEPTIDE; CALCIUM CHANNEL L TYPE; CONNECTIN; CYCLIC AMP; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENDOTHELIN 1; GLYCOGEN SYNTHASE KINASE 3BETA; INDUCIBLE NITRIC OXIDE SYNTHASE; NESIRITIDE; NEURONAL NITRIC OXIDE SYNTHASE; PHENYLEPHRINE; PHOSPHODIESTERASE I; PHOSPHODIESTERASE III; PHOSPHODIESTERASE V; PHOSPHOLAMBAN; SILDENAFIL; TADALAFIL; TRANSIENT RECEPTOR POTENTIAL CHANNEL C; TROPONIN I; VARDENAFIL;

CARDIOMYOPATHY; HEART FAILURE; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HEART PROTECTION; HEART VENTRICLE HYPERTROPHY; HUMAN; ISCHEMIA; MITOCHONDRIAL PERMEABILITY; REVIEW; SIGNAL TRANSDUCTION;

3',5'-CYCLIC-GMP PHOSPHODIESTERASES; ANIMALS; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 5; HEART DISEASES; HUMANS; MULTICENTER STUDIES AS TOPIC; MUSCLE PROTEINS; MYOCYTES, CARDIAC; PHOSPHODIESTERASE 5 INHIBITORS; SECOND MESSENGER SYSTEMS;

EID: 84864386275     PISSN: 13469843     EISSN: 13474820     Source Type: Journal    
DOI: 10.1253/circj.CJ-12-0664     Document Type: Review

References (78)

1. Tsai EJ, Kass DA. Cyclic GMP signaling in cardiovascular pathophysiology and therapeutics. Pharmacol Ther 2009; 122: 216-238.
2. Francis SH, Busch JL, Corbin JD, Sibley D. cGMP-dependent protein kinases and cGMP phosphodiesterases in nitric oxide and cGMP action. Pharmacol Rev 2010; 62: 525-563.
3. Fischmeister R, Castro LR, bi-Gerges A, Rochais F, Jurevicius J, Leroy J, et al. Compartmentation of cyclic nucleotide signaling in the heart: The role of cyclic nucleotide phosphodiesterases. Circ Res 2006; 99: 816-828.
4. Lima B, Forrester MT, Hess DT, Stamler JS. S-nitrosylation in cardiovascular signaling. Circ Res 2010; 106: 633-646.
5. Nakahira A, Minamiyama Y, Takemura S, Hirai H, Sasaki Y, Okada S, et al. Coadministration of carvedilol attenuates nitrate tolerance by preventing cytochrome p450 depletion. Circ J 2010; 74: 1711-1717.
6. Ziolo MT, Kohr MJ, Wang H. Nitric oxide signaling and the regulation of myocardial function. J Mol Cell Cardiol 2008; 45: 625-632.
7. Friebe A, Koesling D. The function of NO-sensitive guanylyl cyclase: What we can learn from genetic mouse models. Nitric Oxide 2009; 21: 149-156.
8. Heo KS, Fujiwara K, Abe J. Disturbed-flow-mediated vascular reactive oxygen species induce endothelial dysfunction. Circ J 2011; 75: 2722-2730.
9. Takimoto E, Kass DA. Role of oxidative stress in cardiac hypertrophy and remodeling. Hypertension 2007; 49: 241-248.
10. Kishimoto I, Tokudome T, Nakao K, Kangawa K. Natriuretic peptide system: An overview of studies using genetically engineered animal models. FEBS J 2011; 278: 1830-1841.
11. Kuhn M. Structure, regulation, and function of mammalian membrane guanylyl cyclase receptors, with a focus on guanylyl cyclase-A. Circ Res 2003; 93: 700-709.
12. Kalra PR, Clague JR, Bolger AP, Anker SD, Poole-Wilson PA, Struthers AD, et al. Myocardial production of C-type natriuretic peptide in chronic heart failure. Circulation 2003; 107: 571-573.
13. Wollert KC, Yurukova S, Kilic A, Begrow F, Fiedler B, Gambaryan S, et al. Increased effects of C-type natriuretic peptide on contractility and calcium regulation in murine hearts overexpressing cyclic GMP-dependent protein kinase I. Br J Pharmacol 2003; 140: 1227-1236.
14. Schlossmann J, Ammendola A, Ashman K, Zong X, Huber A, Neubauer G, et al. Regulation of intracellular calcium by a signalling complex of IRAG, IP3 receptor and cGMP kinase Ibeta. Nature 2000; 404: 197-201.
15. Francis SH, Blount MA, Corbin JD. Mammalian cyclic nucleotide phosphodiesterases: Molecular mechanisms and physiological functions. Physiol Rev 2011; 91: 651-690.
16. 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 2012; 90: 328-336.
17. Vandeput F, Wolda SL, Krall J, Hambleton R, Uher L, McCaw KN, et al. Cyclic nucleotide phosphodiesterase PDE1C1 in human cardiac myocytes. J Biol Chem 2007; 282: 32749-32757.
18. Vandeput F, Krall J, Ockaili R, Salloum FN, Florio V, Corbin JD, et al. CGMP-hydrolytic activity and its inhibition by sildenafil in normal and failing human and mouse myocardium. J Pharmacol Exp Ther 2009; 330: 884-891.
19. Mongillo M, Tocchetti CG, Terrin A, Lissandron V, Cheung YF, Dostmann WR, et al. Compartmentalized phosphodiesterase-2 activity blunts beta-adrenergic cardiac inotropy via an NO/cGMP-dependent pathway. Circ Res 2006; 98: 226-234.
20. Zaccolo M, Movsesian MA. cAMP and cGMP signaling cross-talk: Role of phosphodiesterases and implications for cardiac pathophysiology. Circ Res 2007; 100: 1569-1578.
21. Sun B, Li H, Shakur Y, Hensley J, Hockman S, Kambayashi J, et al. Role of phosphodiesterase type 3A and 3B in regulating platelet and cardiac function using subtype-selective knockout mice. Cell Signal 2007; 19: 1765-1771.
22. Nagendran J, Archer SL, Soliman D, Gurtu V, Moudgil R, Haromy A, et al. Phosphodiesterase type 5 is highly expressed in the hypertrophied human right ventricle, and acute inhibition of phosphodiesterase type 5 improves contractility. Circulation 2007; 116: 238-248.
23. Pokreisz P, Vandenwijngaert S, Bito V, Van den BA, Lenaerts I, Busch C, et al. Ventricular phosphodiesterase-5 expression is increased in patients with advanced heart failure and contributes to adverse ventricular remodeling after myocardial infarction in mice. Circulation 2009; 119: 408-416.
24. 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 2012; 5: 79-86.
25. Takimoto E, Champion HC, Li M, Belardi D, Ren S, Rodriguez ER, et al. Chronic inhibition of cyclic GMP phosphodiesterase 5A prevents and reverses cardiac hypertrophy. Nat Med 2005; 11: 214-222.
26. Lu Z, Xu X, Hu X, Lee S, Traverse JH, Zhu G, et al. Oxidative stress regulates left ventricular PDE5 expression in the failing heart. Circulation 2010; 121: 1474-1483.
27. Senzaki H, Smith CJ, Juang GJ, Isoda T, Mayer SP, Ohler A, et al. Cardiac phosphodiesterase 5 (cGMP-specific) modulates beta-adrenergic signaling in vivo and is down-regulated in heart failure. FASEB J 2001; 15: 1718-1726.
28. Takimoto E, Champion HC, Belardi D, Moslehi J, Mongillo M, Mergia E, et al. cGMP catabolism by phosphodiesterase 5A regulates cardiac adrenergic stimulation by NOS3-dependent mechanism. Circ Res 2005; 96: 100-109.
29. Burgoyne JR, Madhani M, Cuello F, Charles RL, Brennan JP, Schroder E, et al. Cysteine redox sensor in PKGIa enables oxidant-induced activation. Science 2007; 317: 1393-1397.
30. Prysyazhna O, Rudyk O, Eaton P. Single atom substitution in mouse protein kinase G eliminates oxidant sensing to cause hypertension. Nat Med 2012; 18: 286-290.
31. Wegener JW, Nawrath H, Wolfsgruber W, Kuhbandner S, Werner C, Hofmann F, et al. cGMP-dependent protein kinase I mediates the negative inotropic effect of cGMP in the murine myocardium. Circ Res 2002; 90: 18-20.
32. Layland J, Li JM, Shah AM. Role of cyclic GMP-dependent protein kinase in the contractile response to exogenous nitric oxide in rat cardiac myocytes. J Physiol 2002; 540: 457-467.
33. 2+ current in cardiac myocytes. J MolCell Cardiol 2009; 47: 304-314.
34. Wang H, Viatchenko-Karpinski S, Sun J, Gyorke I, Benkusky NA, Kohr MJ, et al. Regulation of myocyte contraction via neuronal nitric oxide synthase: Role of ryanodine receptor S-nitrosylation. J Physiol 2010; 588: 2905-2917.
35. Lee DI, Vahebi S, Tocchetti CG, Barouch LA, Solaro RJ, Takimoto E, et al. PDE5A suppression of acute beta-adrenergic activation requires modulation of myocyte beta-3 signaling coupled to PKG-mediated troponin I phosphorylation. Basic Res Cardiol 2010; 105: 337-347.
36. Yang L, Liu G, Zakharov SI, Bellinger AM, Mongillo M, Marx SO. Protein kinase G phosphorylates Cav1.2 alpha1c and beta2 subunits. Circ Res 2007; 101: 465-474.
37. Borlaug BA, Melenovsky V, Marhin T, Fitzgerald P, Kass DA. Sildenafil inhibits beta-adrenergic-stimulated cardiac contractility in humans. Circulation 2005; 112: 2642-2649.
38. Takimoto E, Belardi D, Tocchetti CG, Vahebi S, Cormaci G, Ketner EA, et al. Compartmentalization of cardiac beta-adrenergic inotropy modulation by phosphodiesterase type 5. Circulation 2007; 115: 2159-2167.
39. Lainchbury JG, Burnett JC Jr, Meyer D, Redfield MM. Effects of natriuretic peptides on load and myocardial function in normal and heart failure dogs. Am J Physiol Heart Circ Physiol 2000; 278: 33-40.
40. Bishu K, Hamdani N, Mohammed SF, Kruger M, Ohtani T, Ogut O, et al. Sildenafil and B-type natriuretic peptide acutely phosphorylate titin and improve diastolic distensibility in vivo. Circulation 2011; 124: 2882-2891.
41. Kruger M, Kotter S, Grutzner A, Lang P, Andresen C, Redfield MM, et al. Protein kinase G modulates human myocardial passive stiffness by phosphorylation of the titin springs. Circ Res 2009; 104: 87-94.
42. Stangherlin A, Gesellchen F, Zoccarato A, Terrin A, Fields LA, Berrera M, et al. cGMP signals modulate cAMP levels in a compartment-specific manner to regulate catecholamine-dependent signaling in cardiac myocytes. Circ Res 2011; 108: 929-939.
43. Frey N, Olson EN. Cardiac hypertrophy: The good, the bad, and the ugly. Annu Rev Physiol 2003; 65: 45-79.
44. Kass DA, Takimoto E. Regulation and role of myocyte cyclic GMP- dependent protein kinase-1. Proc Natl Acad Sci USA 2010; 107: E98-99; author reply.
45. Zhang M, Takimoto E, Hsu S, Lee DI, Nagayama T, Danner T, et al. Myocardial remodeling is controlled by myocyte-targeted gene regulation of phosphodiesterase type 5. J Am Coll Cardiol 2010; 56: 2021-2030.
46. Frantz S, Klaiber M, Baba HA, Oberwinkler H, Volker K, Gabetaner B, et al. Stress-dependent dilated cardiomyopathy in mice with cardiomyocyte-restricted inactivation of cyclic GMP-dependent protein kinase I. Eur Heart J 2011 December 23 [Epub ahead of print].
47. Zahabi A, Picard S, Fortin N, Reudelhuber TL, Deschepper CF. Expression of constitutively active guanylate cyclase in cardiomyocytes inhibits the hypertrophic effects of isoproterenol and aortic constriction on mouse hearts. J Biol Chem 2003; 278: 47694-47699.
48. Kim KH, Kim YJ, Ohn JH, Yang J, Lee SE, Lee SW, et al. Longterm effects of sildenafil in a rat model of chronic mitral regurgitation: Benefits of ventricular remodeling and exercise capacity. Circulation 2012; 125: 1390-1401.
49. 2+/calmodulin-stimulated cyclic nucleotide phosphodiesterase 1 in mediating cardiomyocyte hypertrophy. Circ Res 2009; 105: 956-964.
50. Dorn GW 2nd, Force T. Protein kinase cascades in the regulation of cardiac hypertrophy. J Clin Invest 2005; 115: 527-537.
51. 2+-calcineurin-NFAT cascade in cardiac myocytes. Cardiovasc Res 2004; 63: 450-457.
52. Fiedler B, Lohmann SM, Smolenski A, Linnemuller S, Pieske B, Schroder F, et al. Inhibition of calcineurin-NFAT hypertrophy signaling by cGMP-dependent protein kinase type I in cardiac myocytes. Proc Natl Acad Sci USA 2002; 99: 11363-11368.
53. Koitabashi N, Aiba T, Hesketh GG, Rowell J, Zhang M, Takimoto E, et al. 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 2010; 48: 713-724.
54. Hsu S, Nagayama T, Koitabashi N, Zhang M, Zhou L, Bedja D, et al. Phosphodiesterase 5 inhibition blocks pressure overload-induced cardiac hypertrophy independent of the calcineurin pathway. Cardiovasc Res 2009; 81: 301-309.
55. Takimoto E, Koitabashi N, Hsu S, Ketner EA, Zhang M, Nagayama T, et al. Regulator of G protein signaling 2 mediates cardiac compensation to pressure overload and antihypertrophic effects of PDE5 inhibition in mice. J Clin Invest 2009; 119: 408-420.
56. Tokudome T, Kishimoto I, Horio T, Arai Y, Schwenke DO, Hino J, et al. Regulator of G-protein signaling subtype 4 mediates antihypertrophic effect of locally secreted natriuretic peptides in the heart. Circulation 2008; 117: 2329-2339.
57. Klaiber M, Kruse M, Volker K, Schroter J, Feil R, Freichel M, et al. Novel insights into the mechanisms mediating the local antihypertrophic effects of cardiac atrial natriuretic peptide: Role of cGMP- dependent protein kinase and RGS2. Basic Res Cardiol 2010; 105: 583-595.
58. Schafer S, Ellinghaus P, Janssen W, Kramer F, Lustig K, Milting H, et al. Chronic inhibition of phosphodiesterase 5 does not prevent pressure-overload-induced right-ventricular remodelling. Cardiovasc Res 2009; 82: 30-39.
59. Burley DS, Ferdinandy P, Baxter GF. Cyclic GMP and protein kinase-G in myocardial ischaemia-reperfusion: Opportunities and obstacles for survival signaling. Br J Pharmacol 2007; 152: 855-869.
60. Kukreja RC, Salloum FN, Das A, Koka S, Ockaili RA, Xi L. Emerging new uses of phosphodiesterase-5 inhibitors in cardiovascular diseases. Exp Clin Cardiol 2011; 16: e30-e35.
61. Gorbe A, Giricz Z, Szunyog A, Csont T, Burley DS, Baxter GF, et al. Role of cGMP-PKG signaling in the protection of neonatal rat cardiac myocytes subjected to simulated ischemia/reoxygenation. Basic Res Cardiol 2010; 105: 643-650.
62. Fiedler B, Feil R, Hofmann F, Willenbockel C, Drexler H, Smolenski A, et al. cGMP-dependent protein kinase type I inhibits TAB1-p38 mitogen-activated protein kinase apoptosis signaling in cardiac myocytes. J Biol Chem 2006; 281: 32831-32840.
63. Takahashi R, Uchiyama A, Iguchi N, Mashimo T, Fujino Y. Effects of continuous venovenous hemofiltration on the pharmacology of carperitide, a recombinant human atrial natriuretic peptide. Circ J 2010; 74: 1888-1894.
64. Kitakaze M, Asakura M, Kim J, Shintani Y, Asanuma H, Hamasaki T, et al. Human atrial natriuretic peptide and nicorandil as adjuncts to reperfusion treatment for acute myocardial infarction (J-WIND): Two randomised trials. Lancet 2007; 370: 1483-1493.
65. Ardehali H, O'Rourke B. Mitochondrial K(ATP) channels in cell survival and death. J Mol Cell Cardiol 2005; 39: 7-16.
66. Costa AD, Garlid KD, West IC, Lincoln TM, Downey JM, Cohen MV, et al. Protein kinase G transmits the cardioprotective signal from cytosol to mitochondria. Circ Res 2005; 97: 329-336.
67. Das A, Xi L, Kukreja RC. Protein kinase G-dependent cardioprotective mechanism of phosphodiesterase-5 inhibition involves phosphorylation of ERK and GSK3beta. J Biol Chem 2008; 283: 29572-29585.
68. 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 2009; 296: H1236-H1243.
69. Sanada S, Komuro I, Kitakaze M. Pathophysiology of myocardial reperfusion injury: Preconditioning, postconditioning, and translational aspects of protective measures. Am J Physiol Heart Circ Physiol 2011; 301: H1723-H1741.
70. Madhani M, Hall AR, Cuello F, Charles RL, Burgoyne JR, Fuller W, et al. Phospholemman Ser69 phosphorylation contributes to sildenafil-induced cardioprotection against reperfusion injury. Am J Physiol Heart Circ Physiol 2010; 299: H827-H836.
71. Khairallah M, Khairallah RJ, Young ME, Allen BG, Gillis MA, Danialou G, et al. Sildenafil and cardiomyocyte-specific cGMP signaling prevent cardiomyopathic changes associated with dystrophin deficiency. Proc Natl Acad Sci USA 2008; 105: 7028-7033.
72. Ascah A, Khairallah M, Daussin F, Bourcier-Lucas C, Godin R, Allen BG, et al. Stress-induced opening of the permeability transition pore in the dystrophin-deficient heart is attenuated by acute treatment with sildenafil. Am J Physiol Heart Circ Physiol 2011; 300: H144-H153.
73. Lewis GD, Lachmann J, Camuso J, Lepore JJ, Shin J, Martinovic ME, et al. Sildenafil improves exercise hemodynamics and oxygen uptake in patients with systolic heart failure. Circulation 2007; 115: 59-66.
74. Lindman BR, Zajarias A, Madrazo JA, Shah J, Gage BF, Novak E, et al. Effects of phosphodiesterase type 5 inhibition on systemic and pulmonary hemodynamics and ventricular function in patients with severe symptomatic aortic stenosis. Circulation 2012; 125: 2353-2362.
75. Guazzi M, Vicenzi M, Arena R, Guazzi MD. PDE5 inhibition with sildenafil improves left ventricular diastolic function, cardiac geom- etry, and clinical status in patients with stable systolic heart failure: Results of a 1-year, prospective, randomized, placebo-controlled study. Circ Heart Fail 2011; 4: 8-17.
76. Giannetta E, Isidori AM, Galea N, Carbone I, Mandosi E, Vizza CD, et al. Chronic inhibition of cyclic GMP phosphodiesterase 5a im- proves diabetic cardiomyopathy: A randomized, controlled clinical trial using magnetic resonance imaging with myocardial tagging. Circulation 2012; 125: 2323-2333.
77. O'Connor CM, Starling RC, Hernandez AF, Armstrong PW, Dickstein K, Hasselblad V, et al. Effect of nesiritide in patients with acute de- compensated heart failure. N Engl J Med 2011; 365: 32-43.
78. Sezai A, Wakui S, Akiyama K, Hata M, Yoshitake I, Unosawa S, et al. Myocardial protective effect of human atrial natriuretic peptide in cardiac surgery: "hANP shot" in clinical safety trial. Circ J 2011; 75: 2144-2150.