Atrial natriuretic peptide promotes cardiomyocyte survival by cGMP-dependent nuclear accumulation of zyxin and Akt

Journal of Clinical Investigation

Volumn 115, Issue 10, 2005, Pages 2716-2730

  Kato, Takahiro ^a   Muraski, John ^a   Chen, Yan ^a   Tsujita, Yasuyuki ^a   Wall, Jason ^a   Glembotski, Christopher C ^a   Schaefer, Erik ^b   Beckerle, Mary ^c   Sussman, Mark A ^a,d  

^a SAN DIEGO STATE UNIVERSITY   (United States)

^b Biosource International   (United States)

^c UNIVERSITY OF UTAH   (United States)

^d SAN DIEGO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ATRIAL NATRIURETIC FACTOR; CYCLIC GMP; DNA; FOCAL ADHESION KINASE 2; GREEN FLUORESCENT PROTEIN; LIM PROTEIN; PHALLOIDIN; PROTEIN KINASE B; ZYXIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOACCUMULATION; CELL NUCLEUS; CELL SURVIVAL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DNA CLEAVAGE; ENZYME ACTIVATION; HEART FAILURE; HEART MUSCLE CELL; HEART PROTECTION; IMMUNOBLOTTING; IN VIVO STUDY; MOUSE; NEWBORN; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; ATRIAL NATRIURETIC FACTOR; CELL NUCLEUS; CELL SURVIVAL; CELLS, CULTURED; CYCLIC GMP; CYTOSKELETAL PROTEINS; HUMANS; MICE; MICE, KNOCKOUT; MYOCYTES, CARDIAC; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

EID: 26444507242     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI24280     Document Type: Article

References (67)

1. Pidgeon, G.B., et al. 1996. Differing metabolism and bioactivity of atrial and brain natriuretic peptides in essential hypertension. Hypertension. 27:906-913.
2. Tonolo, G., et al. 1989. Low-dose infusion of atrial natriuretic factor in mild essential hypertension. Circulation. 80:893-902.
3. Hayashi, M., et al. 2001. Intravenous atrial natriuretic peptide prevents left ventricular remodeling in patients with first anterior acute myocardial infarction. J. Am. Coll. Cardiol. 37:1820-1826.
4. Lai, C.P., et al. 1993. Beneficial effects of atrial natriuretic peptide on exercise-induced myocardial ischemia in patients with stable effort angina pectoris. Circulation. 87:144-151.
5. Rosenthal, A.D., Moran, M., and Herrmann, H.C. 1990. Coronary hemodynamic effects of atrial natriuretic peptide in humans. J. Am. Coll. Cardiol. 16:1107-1113.
6. Herrmann, H.C., Rosenthal, A.D., and Davis, C.A. 1990. Cardiovascular effects of intracoronary atrial natriuretic peptide administration in man. Am. Heart J. 120:308-315.
7. Kato, H., et al. 1994. Suppression of hyperventilation-induced attacks with infusion of B-type (brain) natriuretic peptide in patients with variant angina. Am. Heart J. 128:1098-1104.
8. Clarkson, P.B., et al. 1996. Effects of brain natriuretic peptide on exercise hemodynamics and neurohormones in isolated diastolic heart failure. Circulation. 93:2037-2042.
9. Molina, C.R., et al. 1988. Hemodynamic, renal and endocrine effects of atrial natriuretic peptide infusion in severe heart failure. J. Am. Coll. Cardiol. 12:175-186.
10. Fifer, M.A., et al. 1990. Hemodynamic and renal effects of atrial natriuretic peptide in congestive heart failure. Am. J. Cardiol. 65:211-216.
11. Nakamura, M., et al. 1998. Vasodilatory effects of B-type natriuretic peptide are impaired in patients with chronic heart failure. Am. Heart J. 135:414-420.
12. Mizuno, O., Onishi, K., Dohi, K., and Nakano, T. 2001. Effects of therapeutic doses of human atrial natriuretic peptide on load and myocardial performance in patients with congestive heart failure. Am. J. Cardiol. 88:863-866.
13. Colucci, W.S., et al. 2000. Intravenous nesiritide, a natriuretic peptide, in the treatment of decompensated congestive heart failure. Nesiritide Study Group. N. Eng. J. Med. 343:246-253.
14. Fiscus, R.R., Tu, A.W., and Chew, S.B. 2001. Natriuretic peptides inhibit apoptosis and prolong the survival of serum-deprived PC12 cells. Neuroreport. 12:185-189.
15. Matsumura, T., et al. 1996. Neutral endopeptidase 24.11 in neutrophils modulates protective effects of natriuretic peptides against neutrophils-induced endothelial cytotoxity. J. Clin. Invest. 97:2192-2203.
16. Cottart, C.H., et al. 2003. Hepatic cytoprotection by nitric oxide and the cGMP pathway after ischemia-reperfusion in the rat. Nitric Oxide. 9:57-63.
17. Suenobu, N., Shichiri, M., Iwashina, M., Marumo, F., and Hirata, Y. 1999. Natriuretic peptides and nitric oxide induce endothelial apoptosis via a cGMP-dependent mechanism. Arterioscler. Thromb. Vasc. Biol. 19:140-146.
18. Han, B., et al. 2003. The opposing effects of endothelin-1 and C-type natriuretic peptide on apoptosis of neonatal rat cardiac myocytes. Eur. J. Pharmacol. 474:15-20.
19. Kato, K., et al. 2003. Adrenomedullin gene delivery attenuates myocardial infarction and apoptosis after ischemia and reperfusion. Am. J. Physiol. Heart Circ. Physiol. 285:H1506-H1514.
20. Wollert, K.C., et al. 2002. Gene transfer of cGMP-dependent protein kinase I enhances the antihypertrophic effects of nitric oxide in cardiomyocytes. Hypertension. 39:87-92.
21. Begum, N., Sandu, O.A., Ito, M., Lohmann, S.M., and Smolenski, A. 2002. Active Rho kinase (ROK-alpha) associates with insulin receptor substrate-1 and inhibits insulin signaling in vascular smooth muscle cells. J. Biol. Chem. 277:6214-6222.
22. Hood, J., and Granger, H.J. 1998. Protein kinase G mediates vascular endothelial growth factor-induced Raf-1 activation and proliferation in human endothelial cells. J. Biol. Chem. 273:23504-23508.
23. Kawasaki, K., et al. 2003. Activation of the phosphatidylinositol 3-kinase/protein kinase Akt pathway mediates nitric oxide-induced endothelial cell migration and angiogenesis. Mol. Cell. Biol. 23:5726-5737.
24. Chang, M.S., Lee, W.S., Chen, B.C., Sheu, J.R., and Lin, C.H. 2004. YC-1-induced cyclooxygenase-2 expression is mediated by cGMP-dependent activations of Ras, phosphoinositide-3-OH-kinase, Akt, and nuclear factor-kappaB in human pulmonary epithelial cells. Mol. Pharmacol. 66:561-571.
25. Pollman, M.J., Yamada, T., Horiuchi, M., and Gibbons, G.H. 1996. Vasoactive substances regulate vascular smooth muscle cell apoptosis: countervailing influences of nitric oxide and angiotensin II. Circ. Res. 79:748-756.
26. Fiscus, R.R. 2002. Involvement of cyclic GMP and protein kinase G in the regulation of apoptosis and survival in neural cells. Neurosignals. 11:175-190.
27. Fujio, Y., Nguyen, T., Wencker, D., Kitsis, R.N., and Walsh, K. 2000. Akt promotes survival of cardiomyocytes in vitro and protects against ischemia-reperfusion injury in mouse heart. Circulation. 101:660-667.
28. Matsui, T., Li, L., and Rosenzweig, A. 1999. Adenoviral gene transfer of activated phosphatidylinositol 3′-kinase and Akt inhibits apoptosis of hypoxic cardiomyocytes in vitro. Circulation. 100:2373-2379.
29. Negoro, S., et al. 2001. Glycoprotein 130 regulates cardiac myocyte survival in doxorubicin-induced apoptosis through phosphatidylinositol 3-kinase/Akt phosphorylation and Bcl-xL/caspase-3 interaction. Circulation. 103:555-561.
30. Torella, D., et al. 2004. Cardiac stem cell and myocyte aging, heart failure, and insulin-like growth factor-1 overexpression. Circ. Res. 94:514-524.
31. Camper-Kirby, D., et al. 2001. Myocardial Akt activation and gender: increased nuclear activity in females versus males. Circ. Res. 88:1020-1027.
32. Shiraishi, I., et al. 2004. Nuclear targeting of Akt enhances kinase activity and survival of cardiomyocytes. Circ. Res. 94:884-891.
33. Cattaruzza, M., Lattrich, C., and Hecker, M. 2004. Focal adhesion protein zyxin is a mechanosensitive modulator of gene expression in vascular smooth muscle cells. Hypertension. 43:726-730.
34. Smolenski, A., Poller, W., Walter, U., and Lohmann, S.M. 2000. Regulation of human endothelial cell focal adhesion sites and migration by cGMP-dependent protein kinase I. J. Biol. Chem. 275:25723-25732.
35. Nix, D.A., and Beckerle, M.C. 1997. Nuclear-cytoplasmic shuttling of the focal contact protein, zyxin: a potential mechanism for communication between sites of cell adhesion and the nucleus. J. Cell Biol. 138:1139-1147.
36. Nix, D.A., et al. 2001, Targeting of zyxin to sites of actin membrane interaction and to the nucleus. J. Biol. Chem. 276:34759-34767.
37. Melendez, J., et al. 2004. Cardiomyocyte apoptosis triggered by RAFTK/pyk2 via src kinase is antagonized by paxillin. J. Biol. Chem. 279:53516-53523.
38. Yin, H., Chao, L., and Chao, J. 2004. Adrenomedullin protects against myocardial apoptosis after ischemia/reperfusion through activation of Akt-GSK signaling. Hypertension. 43:109-116.
39. Babiker, FA., et al. 2004. 17beta-estradiol antagonizes cardiomyocyte hypertrophy by autocrine/paracrine stimulation of aguanylyl cyclase A receptor-cyclic guanosine monophosphate-dependent protein kinase pathway. Circulation. 109:269-276.
40. Bonthius, D.J., Karacay, B., and Pantazis, N.J. 2003. FGF-2, NGF and IGF-1, but not BDNF, utilize a nitric oxide pathway to signal neurotrophic and neuroprotective effects against alcohol toxicity in cerebellar granule cell cultures. Brain Res. Dev. Brain Res. 140:15-28.
41. Zahabi, A., Picard, S., Fortin, N., Reudelhuber, T.L., and Deschepper, C.F. 2003. 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.
42. Publication Committee for the VMAC Investigators (Vasodilatation in the Management of Acute CHF). 2002. Intravenous nesiritide vs nitroglycerin for treatment of decompensated congestive heart failure: a randomized controlled trial. JAMA. 287:1531-1540.
43. D'Souza, S.P., et al. 2003. B-type natriuretic peptide limits infarct size in rat isolated hearts via KATP channel opening. Am. J. Physiol. Heart Circ. Physiol. 284:H1592-H1600.
44. Kamijo, T., et al. 1999. Hemodynamic and hormonal responses to nicorandil in a canine model of acute ischemic heart failure: a comparison with cromakalim and nitroglycerin. J. Cardiovasc. Pharmacol. 33:93-101.
45. Padilla, F., Garcia-Dorado, D., Agullo, L., Pina, P., and Soler-Soler, J. 2001. Intravenous administration of the natriuretic peptide urodilatin at low doses during coronary reperfusion limits infarct size in anesthetized pigs. Cardiovasc. Res. 51:592-600.
46. Kook, H., Itoh, H., and Nakao, K. 2003. Physiological concentration of atrial natriuretic peptide induces endothelial regeneration in vitro. Am. J. Physiol. Heart Circ. Physiol. 284:H1388-H1397.
47. Lelievre, V., Pineau, N., Hu, Z., and Waschek, J.A. 2001. Proliferative actions of natriuretic peptides on neuroblastoma cells. Involvement of guanylyl cyclase and non-guanylyl cyclase pathways. J. Biol. Chem. 276:43668-43676.
48. Wu, C., Bishopric, N.H., and Pratt, R.E. 1997. Atrial natriuretic peptide induces apoptosis in neonatal rat cardiac myocytes. J. Biol. Chem. 272:14860-14866.
49. Kadrmas, J.L., and Beckerle, M.C. 2004. The LIM domain: from the cytoskeleton to the nucleus. Nat. Rev. Mol. Cell Biol. 5:920-931.
50. Hoffman, L.M., et al. 2003. Targeted disruption of the murine zyxin gene. Mol. Cell. Biol. 23:70-79.
51. Cho, H., Thorvaldsen, J.L., Chu, Q., Feng, F., and Birnbaum, M.J. 2001. Akt1/PKBalpha is required for normal growth but dispensable for maintenance of glucose homeostasis in mice. J. Biol. Chem. 276:38349-38352.
52. Brown, M.C., and Turner, C.E. 2004. Paxillin: adapting to change. Physiol. Rev. 84:1315-1339.
53. Calderone, A., Thaik, C., Takahashi, N., Chang, D.L.F., and Colucci, W.S. 1998. Nitric oxide, atrial natriuretic peptide and cyclic GMP inhibit the growth-promoting effects of norepinephrine in cardiac myocytes and fibroblasts. J. Clin. Invest. 101:812-818.
54. Rosenkranz, A.C., Woods, R.L., Dusting, G.J., and Ritchie, R.H. 2003. Antihypertrophic actions of the natriuretic peptides in adult rat cardiomyocytes: importance of cyclic GMP. Cardiovasc. Res. 57:515-522.
55. Shimojo, T., et al. 1999. Nitric oxide induces apoptotic death of cardiomyocytes via a cyclic-GMP-dependent pathway. Exp. Cell Res. 247:38-47.
56. Arstall, M.A., Sawyer, D.B., Fukazawa, R., and Kelly, R.A. 1999. Cytokine-mediated apoptosis in cardiac myocytes: the role of inducible nitric oxide synthase induction and peroxynitrite generation. Circ. Res. 85:829-840.
57. Takuma, K., et al. 2001. Anti-apoptotic effect of cGMP in cultured astrocytes: inhibition by cGMP-dependent protein kinase of mitochondrial permeable transition pore. J. Biol. Chem. 276:48093-48099.
58. Miyata, A., Kangawa, K., and Matsuo, H. 1986. Molecular forms of atrial natriuretic peptides in rat tissues and plasma. J. Hypertens. 4:S9-S11.
59. Murthy, K.K., Thibault, G., and Cantin, M. 1988. Contribution of blood and systemic circulation to the processing of pro-(atrial natriuretic factor). Biochem. J. 250:665-670.
60. Kuhn, M., et al. 2004. Left ventricular assist device support reverses altered cardiac expression and function of natriuretic peptides and receptors in end-stage heart failure. Cardiovasc. Res. 64:308-314.
61. Feil, R., Lohmann, S.M., de Jonge, H., Walter, U., and Hofmann, F. 2003. Cyclic GMP-dependent protein kinases and the cardiovascular system: insights from genetically modified mice [review]. Circ. Res. 93:907-916.
62. Tsutamoto, T., et al. 1993. Possibility of downregulation of atrial natriuretic peptide receptor coupled to guanylate cyclase in peripheral vascular beds of patients with chronic severe heart failure. Circulation. 87:70-75.
63. Shevchuk, N.A., et al. 2004. Construction of long DNA molecules using long PCR-based fusion of several fragments simultaneously. Nucleic Acids Res. 32:e19.
64. Melendez, J., et al. 2002. Activation of pyk2/related focal adhesion tyrosine kinase and focal adhesion kinase in cardiac remodeling. J. Biol. Chem. 277:45203-45210.
65. Sussman, M.A., et al. 1999. Pathogenesis of dilated cardiomyopathy: molecular, structural, and population analyses in tropomodulin-overexpressing transgenic mice. Am. J. Pathol. 155:2101-2113.
66. Melendez, J., et al. 2004. Cardiomyocyte apoptosis triggered by RAFTK/pyk2 via Src kinase is antagonized by paxillin. J. Biol. Chem. 279:53516-53523.
67. Morrison, L.E., Whittaker, R.J., Klepper, R.E., Wawrousek, E.F., and Glembotski, C.C. 2004. Roles for alphaB-crystallin and HSBP2 in protecting the myocardium from ischemia-reperfusion-induced damage in a KO mouse model. Am. J. Physiol. Heart Circ. Physiol. 286:H847-H855.