Chronic inhibition of cyclic GMP phosphodiesterase 5A prevents and reverses cardiac hypertrophy

Nature Medicine

Volumn 11, Issue 2, 2005, Pages 214-222

  Takimoto, Eiki ^a   Champion, Hunter C ^a   Li, Manxiang ^a   Belardi, Diego ^a   Ren, Shuxun ^b   Rodriguez, E Rene ^a   Bedja, Djahida ^a   Gabrielson, Kathleen L ^a   Wang, Yibin ^b   Kass, David A ^a  

^a DEPARTMENT OF PATHOLOGY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; CYCLIC GMP DEPENDENT PROTEIN KINASE; CYCLIC GMP PHOSPHODIESTERASE; CYCLIC GMP PHOSPHODIESTERASE 5A; EMD 360527; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHODIESTERASE V INHIBITOR; PROTEIN KINASE B; SILDENAFIL; TADALAFIL; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA CONSTRICTION; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME DEGRADATION; ENZYME INHIBITION; GENETIC ENGINEERING; HEART FAILURE; HEART FUNCTION; HEART HYPERTROPHY; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE OVERLOAD; HEART VENTRICLE PRESSURE; HEART VENTRICLE REMODELING; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; TREATMENT OUTCOME;

1-PHOSPHATIDYLINOSITOL 3-KINASE; 3',5'-CYCLIC-GMP PHOSPHODIESTERASE; ANIMALS; ANIMALS, NEWBORN; BLOOD PRESSURE; CALCINEURIN; CARDIOMEGALY; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; DNA-BINDING PROTEINS; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HEART; HEMODYNAMIC PROCESSES; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYOCARDIUM; NFATC TRANSCRIPTION FACTORS; NUCLEAR PROTEINS; PHOSPHODIESTERASE INHIBITORS; PIPERAZINES; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; TRANSCRIPTION FACTORS;

EID: 20044363270     PISSN: 10788956     EISSN: None     Source Type: Journal    
DOI: 10.1038/nm1175     Document Type: Article

References (50)

1. Frey, N. & Olson, E.N. Cardiac hypertrophy: the good, the bad, and the ugly. Annu. Rev. Physiol. 65, 45-79 (2003).
2. Frey, N., Katus, H.A., Olson, E.N. & Hill, J.A. Hypertrophy of the heart: a new therapeutic target? Circulation 109, 1580-1589 (2004).
3. Bueno, O.F. et al. Impaired cardiac hypertrophic response in calcineurin A β-deficient mice. Proc. Natl. Acad. Sci. USA 99, 4586-4591 (2002).
4. Matsui, T., Nagoshi, T. & Rosenzweig, A. Akt and PI 3-kinase signaling in cardiomyocyte hypertrophy and survival. Cell Cycle 2, 220-223 (2003).
5. Antos, C.L. et al. Activated glycogen synthase-3 β suppresses cardiac hypertrophy in vivo. Proc. Natl. Acad. Sci. USA 99, 907-912 (2002).
6. , Kishimoto, I., Rossi, K. & Garbers, D.L. A genetic model provides evidence that the receptor for atrial natriuretic peptide (guanylyl cyclase-A) inhibits cardiac ventricular myocyte hypertrophy. Proc. Natl. Acad. Sci. USA 98, 2703-2706 (2001).
7. Zahabi, A., Picard, S., Fortin, N., Reudelhuber, T.L. & Deschepper, C.F. Expression of constitutively active guanylate cyclase in cardiomyocytes inhibits the hypertrophic effects of isoproterenol and aortic constriction on mouse hearts. J. Biol. Chem. 278, 47694-47699 (2003).
8. Fiedler, B. et al. Inhibition of calcineurin-NFAT hypertrophy signaling by cGMP-dependent protein kinase type I in cardiac myocytes. Proc. Natl. Acad. Sci. USA 99, 11363-11368 (2002).
9. Wollert, K.C. et al. Gene transfer of cGMP-dependent protein kinase I enhances the antihypertrophic effects of nitric oxide in cardiomyocytes. Hypertension 39, 87-92 (2002).
10. Knowles, J.W. et al. Pressure-independent enhancement of cardiac hypertrophy in natriuretic peptide receptor A-deficient mice. J. Clin. Invest. 107, 975-984 (2001).
11. Rybalkin, S.D., Yan, C., Bornfeldt, K.E. & Beavo, J.A. Cyclic GMP phosphodiesterases and regulation of smooth muscle function. Circ. Res. 93, 280-291 (2003).
12. Francis, S.H., Turko, I.V. & Corbin, J.D. Cyclic nucleotide phosphodiesterases: relating structure and function. Prog. Nucleic Acid Res. Mol. Biol. 65, 1-52 (2001).
13. Reffelmann, T. & Kloner, R.A. Therapeutic potential of phosphodiesterase 5 inhibition for cardiovascular disease. Circulation 108, 239-244 (2003).
14. Goldstein, I. et al. Oral sildenafil in the treatment of erectile dysfunction. Sildenafil Study Group. N. Engl. J. Med. 338, 1397-1404 (1998).
15. Sastry, B.K., Narasimhan, C., Reddy, N.K. & Raju, B.S. Clinical efficacy of sildenafil in primary pulmonary hypertension: a randomized, placebo-controlled, double-blind, crossover study. J. Am. Coll. Cardiol. 43, 1149-1153 (2004).
16. Senzaki, H. et al. Cardiac phosphodiesterase 5 (cGMP-specific) modulates β-adrenergic signaling in vivo and is down-regulated in heart failure. FASEB J. 15, 1718-1726 (2001).
17. Takimoto, E. et al. Cyclic GMP catabolism by PDE5A regulates cardiac adrenergic stimulation by NOS3-dependent mechanism. Circ. Res. 96, 100-109 (2005).
18. Corbin, J. et al. Sildenafil citrate does not affect cardiac contractility in human or dog heart. Curr. Med. Res. Opin. 19, 747-752 (2003).
19. Molkentin, J.D. et al. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93, 215-228 (1998).
20. Semeniuk, L.M. et al. Time-dependent systolic and diastolic function in mice overexpressing calcineurin. Am. J. Physiol. Heart Circ. Physiol. 284, H425-H430 (2003).
21. Bueno, O.F. & Molkentin, J.D. Involvement of extracellular signal-regulated kinases 1/2 in cardiac hypertrophy and cell death. Circ. Res. 91, 776-781 (2002).
22. Minamino, T. et al. MEKK1 is essential for cardiac hypertrophy and dysfunction induced by Gq. Proc. Natl. Acad. Sci. USA 99, 3866-3871 (2002).
23. Zou, Y. et al. Isoproterenol activates extracellular signal-regulated protein kinases in cardiomyocytes through calcineurin. Circulation 104, 102-108 (2001).
24. Bueno, O.F. et al. The MEK1-ERK1/2 signaling pathway promotes compensated cardiac hypertrophy in transgenic mice. EMBO J. 19, 6341-6350 (2000).
25. Condorelli, G. et al. Akt induces enhanced myocardial contractility and cell size in vivo in transgenic mice. Proc. Natl. Acad. Sci. USA 99, 12333-12338 (2002).
26. Matsui, T. et al. Phenotypic spectrum caused by transgenic overexpression of activated Akt in the heart. J. Biol. Chem. 277, 22896-22901 (2002).
27. Oudit, G.Y. et al. The role of phosphoinositide-3 kinase and PTEN in cardiovascular physiology and disease. J. Mol. Cell Cardiol. 37, 449-471 (2004).
28. Crackower, M.A. et al. Regulation of myocardial contractility and cell size by distinct PI3K-PTEN signaling pathways. Cell 110, 737-749 (2002).
29. Patrucco, E. et al. PI3Kγ modulates the cardiac response to chronic pressure overload by distinct kinase-dependent and -independent effects. Cell 118, 375-387 (2004).
30. Hardt, S.E. & Sadoshima, J. Glycogen synthase kinase-3β: a novel regulator of cardiac hypertrophy and development. Circ. Res. 90, 1055-1063 (2002).
31. Juhaszova, M. et al. Glycogen synthase kinase-3β mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore. J. Clin. Invest. 113, 1535-1549 (2004).
32. Tanji, C. et al. A-kinase anchoring protein AKAP220 binds to glycogen synthase kinase-3β (GSK-3β) and mediates protein kinase A-dependent inhibition of GSK-3β. J. Biol. Chem. 277, 36955-36961 (2002).
33. Shin, S.Y., Yoon, S.C., Kim, Y.H., Kim, Y.S. & Lee, Y.H. Phosphorylation of glycogen synthase kinase-3β at serine-9 by phospholipase Cγ1 through protein kinase C in rat 3Y1 fibroblasts. Exp. Mol. Med. 34, 444-450 (2002).
34. Kim, D. et al. Upregulation of phosphodiesterase 1A1 expression is associated with the development of nitrate tolerance. Circulation 104, 2338-2343 (2001).
35. Ni, X.P., Safai, M., Rishi, R., Baylis, C. & Humphreys, M.H. Increased activity of cGMP-specific phosphodiesterase (PDE5) contributes to resistance to atrial natriuretic peptide natriuresis in the pregnant rat. J. Am. Soc. Nephrol. 15, 1254-1260 (2004).
36. Rybalkin, S.D., Rybalkina, I.G., Shimizu-Alpergine, M., Tang, X.B. & Beavo, J.A. PDE5 is converted to an activated state upon cGMP binding to the GAF A domain. EMBO J. 22, 469-478 (2003).
37. Francis, S.H. et al. Phosphorylation of isolated human phosphodiesterase-5 regulatory domain induces an apparent conformational change and increases cGMP binding affinity. J. Biol. Chem. 277, 47581-47587 (2002).
38. Massion, P.B., Feron, O., Dessy, C. & Balligand, J.L. Nitric oxide and cardiac function: ten years after, and continuing. Circ. Res. 93, 388-398 (2003).
39. Champion, H.C. et al. Modulation of in vivo cardiac function by myocyte-specific nitric oxide synthase-3. Circ. Res. 94, 657-663 (2004).
40. Holtwick, R. et al. Pressure-independent cardiac hypertrophy in mice with cardiomyocyte-restricted inactivation of the atrial natriuretic peptide receptor guanylyl cyclase-A. J. Clin. Invest. 111, 1399-1407 (2003).
41. Oliver, P.M. et al. Hypertension, cardiac hypertrophy, and sudden death in mice lacking natriuretic peptide receptor A. Proc. Natl. Acad. Sci. USA 94, 14730-14735 (1997).
42. Kotera, J., Grimes, K.A., Corbin, J.D. & Francis, S.H. cGMP-dependent protein kinase protects cGMP from hydrolysis by phosphodiesterase-5. Biochem. J. 372, 419-426 (2003).
43. Pilz, R.B. & Casteel, D.E. Regulation of gene expression by cyclic GMP. Circ. Res. 93, 1034-1046 (2003).
44. 2-terminal kinase activation in the heart. Cross-talk between cardiac hypertrophic signaling pathways. J. Biol. Chem. 275, 13571-13579 (2000).
45. De Windt, L.J. et al. Calcineurin-mediated hypertrophy protects cardiomyocytes from apoptosis in vitro and in vivo: an apoptosis-independent model of dilated heart failure. Circ. Res. 86, 255-263 (2000).
46. Esposito, G. et al. Genetic alterations that inhibit in vivo pressure-overload hypertrophy prevent cardiac dysfunction despite increased wall stress. Circulation 105, 85-92 (2002).
47. Wilkins, B.J. et al. Calcineurin/N FAT coupling participates in pathological, but not physiological, cardiac hypertrophy. Circ. Res. 94, 110-118 (2004).
48. Michael, A. et al. Glycogen synthase kinase-3β regulates growth, calcium homeostasis, and diastolic function in the heart. J. Biol. Chem. 279, 21383-21393 (2004).
49. Walker, D.K. et al. Pharmacokinetics and metabolism of sildenafil in mouse, rat, rabbit, dog and man. Xenobiotica 29, 297-310 (1999).
50. Akao, M., Ohler, A., O'Rourke, B. & Marban, E. Mitochondrial ATP-sensitive potassium channels inhibit apoptosis induced by oxidative stress in cardiac cells. Circ. Res. 88, 1267-1275 (2001).