Molecular mechanisms underlying cardiac antihypertrophic and antifibrotic effects of natriuretic peptides

Journal of Molecular Medicine

Volumn 90, Issue 1, 2012, Pages 5-13

  Calvieri, Camilla ^a   Rubattu, Speranza ^a,b   Volpe, Massimo ^a,b,c  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b IRCCS NEUROMED   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Calcineurin NFAT; Cardiac hypertrophy and fibrosis; Natriuretic peptides; NHE 1; NPRC; TGF 1

Indexed keywords

BRAIN NATRIURETIC PEPTIDE; CALCINEURIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALMODULIN; CARIPORIDE; CYCLOSPORIN A; GLYCOGEN SYNTHASE KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; NATRIURETIC PEPTIDE RECEPTOR B; NATRIURETIC PEPTIDE TYPE C; PHENYLEPHRINE; RGS4 PROTEIN; SILDENAFIL; SMAD PROTEIN; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD6 PROTEIN; SMAD7 PROTEIN; SODIUM ION; SODIUM PROTON EXCHANGE PROTEIN 1; STRESS ACTIVATED PROTEIN KINASE; TACROLIMUS; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR NFAT3; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA3; TRANSIENT RECEPTOR POTENTIAL CHANNEL 3; TRANSIENT RECEPTOR POTENTIAL CHANNEL 6; UNINDEXED DRUG;

ALKALINITY; AMINO ACID SUBSTITUTION; CHRONOTROPISM; CONGESTIVE CARDIOMYOPATHY; GENE EXPRESSION; GENETIC TRANSCRIPTION; HEART FAILURE; HEART INFARCTION; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE REMODELING; HUMAN; HYPERTROPHIC CARDIOMYOPATHY; MYOFIBROBLAST; NONHUMAN; PROTEIN DEPHOSPHORYLATION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; REPERFUSION INJURY; REVIEW; SODIUM TRANSPORT; UPREGULATION; VASCULAR RESISTANCE;

ANIMALS; CALCINEURIN; CARDIOMEGALY; FIBROSIS; HUMANS; MYOCARDIUM; NATRIURETIC PEPTIDE, C-TYPE; NATRIURETIC PEPTIDES; NFATC TRANSCRIPTION FACTORS; SIGNAL TRANSDUCTION; SMAD PROTEINS; SODIUM-HYDROGEN ANTIPORTER; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84857367504     PISSN: 09462716     EISSN: 14321440     Source Type: Journal    
DOI: 10.1007/s00109-011-0801-z     Document Type: Review

References (100)

1. Piechota M, Banach M, Jacon A, Rysz J (2008) Natriuretic peptides in cardiovascular diseases. Cell Mol Biol Lett 13:155-181
2. Battistoni A, Rubattu S, Volpe M. (2011) Circulating biomarkers with preventive, diagnostic and prognostic implications in cardiovascular diseases. Int J Cardiol
3. Qi W, Mathisen P, Kjekshus J, Simonsen S, Bjornerheim R, Endresen K, Hall C (2001) Natriuretic peptides in patients with aortic stenosis. Am Heart J 142:725-732 (Pubitemid 32900502)
4. Nishikimi T, Yoshihara F, Morimoto A, Ishikawa K, Ishimitsu T, Saito Y, Kangawa K, Matsuo H, Omae T, Matsuoka H (1996) Relationship between left ventricular geometry and natriuretic peptide levels in essential hypertension. Hypertension 28:22-30 (Pubitemid 26231085)
5. Cavallero S, González GE, Puyó AM, Rosón MI, Pérez S, Morales C, Hertig CM, Gelpi RJ, Fernández BE (2007) Atrial natriuretic peptide behaviour and myocyte hypertrophic profile in combined pressure and volume-induced cardiac hypertrophy. J Hypertens 25:1940-1950 (Pubitemid 47356636)
6. Rubattu S, Sciarretta S, Valenti V, Stanzione R, Volpe M (2008) Natriuretic peptides: an update on bioactivity, potential therapeutic use and implication in cardiovascular diseases. Am J Hypertens 21:733-741 (Pubitemid 351913612)
7. Ellmers LJ, Scott NJ, Piuhola J, Maeda N, Smithies O, Frampton CM, Richards AM, Cameron VA (2007) Npr1-regulated gene pathways contributing to cardiac hypertrophy and fibrosis. J Mol Endocrinol 38:245-257 (Pubitemid 46351607)
8. Kishimoto I, Tokudome T, Horio T, Garbers DL, Nakao K, Kangawa K (2009) Natriuretic peptide signaling via guanylyl cyclase (GC)-A: an endogenous protective mechanism of the heart. Curr Cardiol Rev 5:45-51
9. Kishimoto I, Rossi K, Garbers DL (2001) A genetic model provides evidence that the receptor for atrial natriuretic peptide (guanylyl cyclase-A) inhibits cardiac ventricular myocyte hypertrophy. Proc Natl Acad Sci U S A 98:2703-2706 (Pubitemid 32209546)
10. Holtwick R, van Eickels M, Skryabin BV, Baba HA, Bubikat A, Begrow F, Schneider MD, Garbers DL, Kuhn M (2003) 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 (Pubitemid 36554711)
11. Knowles JW, Esposito G, Mao L, Hagaman JR, Fox JE, Smithies O, Rockman HA, Maeda N (2001) Pressure-independent enhancement of cardiac hypertrophy in natriuretic peptide receptor A-deficient mice. J Clin Invest 107:975-984 (Pubitemid 32328002)
12. Rosenkranz AC, Woods RL, Dusting GJ, Ritchie RH (2003) Antihypertrophic actions of the natriuretic peptides in adult rat cardiomyocytes: importance of cyclic GMP. Cardiovasc Res 57:515-522 (Pubitemid 36144228)
13. Rubattu S, Bigatti G, Evangelista A, Lanzani C, Stanzione R, Zagato L, Manunta P, Marchitti S, Venturelli V, Bianchi G et al (2006) Association of atrial natriuretic peptide and type a natriuretic peptide receptor gene polymorphisms with left ventricular mass in human essential hypertension. J Am Coll Cardiol 48:499-505 (Pubitemid 44093966)
14. Rubattu S, Sciarretta S, Ciavarella GM, Venturelli V, De Paolis P, Tocci G, De Biase L, Ferrucci A, Volpe M (2007) Reduced levels of pro-atrial natriuretic peptide in hypertensive patients with metabolic syndrome and their relationship with LVH. J Hypertens 25:833-839 (Pubitemid 46402866)
15. Kapoun AM, Liang F, O'Young G, Damm DL, Quon D, White RT, Munson K, Lam A, Schreiner GF, Protter AA (2004) B-type natriuretic peptide exerts broad functional opposition to transforming growth factor-beta in primary human cardiac fibroblasts: fibrosis, myofibroblast conversion, proliferation, and inflammation. Circ Res 94:453-461 (Pubitemid 38326280)
16. Tamura N, Ogawa Y, Chusho H, Nakamura K, Nakao K, Suda M, Kasahara M, Hashimoto R, Katsuura G, Mukoyama M et al (2000) Cardiac fibrosis in mice lacking brain natriuretic peptide. Proc Natl Acad Sci U S A 97:4239-4244 (Pubitemid 30226117)
17. Ogawa Y, Tamura N, Chusho H, Nakao K (2001) Brain natriuretic peptide appears to act locally as an antifibrotic factor in the heart. Can J Physiol Pharmacol 79:723-729 (Pubitemid 32745039)
18. Richards AM (2011) C-type natriuretic peptide and cardiac fibrosis. Hypertension 57:154-155
19. Bueno OF, van Rooij E, Molkentin JD, Doevendans PA, De Windt LJ (2002) Calcineurin and hypertrophic heart disease: novel insights and remaining questions. Cardiovasc Res 53:806-821 (Pubitemid 34261019)
20. Molkentin JD, Lu JR, Antos CL, Markham B, Richardson J, Robbins J, Grant SR, Olson EN (1998) A calcineurindependent transcriptional pathway for cardiac hypertrophy. Cell 93:215-228 (Pubitemid 28180855)
21. Molkentin JD (2004) Calcineurin-NFAT signaling regulates the cardiac hypertrophic response in coordination with the MAPKs. Cardiovasc Res 63:467-475 (Pubitemid 38970191)
22. Rothermel BA, McKinsey TA, Vega RB, Nicol RL, Mammen P, Yang J, Antos CL, Shelton JM, Bassel-Duby R, Olson EN et al (2001) Myocyte-enriched calcineurin-interacting protein, MCIP1, inhibits cardiac hypertrophy in vivo. Proc Natl Acad Sci U S A 98:3328-3333 (Pubitemid 32220845)
23. Rothermel BA, Vega RB, Williams RS (2003) The role of modulatory calcineurin-interacting proteins in calcineurin signaling. Trends Cardiovasc Med 13:15-21 (Pubitemid 36120545)
24. Tamirisa P, Blumer KJ, Muslin AJ (1999) RGS4 inhibits Gprotein signaling in cardiomyocytes. Circulation 99:441-447 (Pubitemid 29051272)
25. Wu X, Eder P, Chang B, Molkentin JD (2010) TRPC channels are necessary mediators of pathologic cardiac hypertrophy. Proc Natl Acad Sci U S A 107:7000-7005
26. Heineke J, Molkentin JD (2006) Regulation of cardiac hypertrophy by intracellular signaling pathways. Nat Rev Mol Cell Biol 7:589-600 (Pubitemid 44325350)
27. Lim HW, De Windt LJ, Steinberg L, Taigen T, Witt SA, Kimball TR, Molkentin JD (2000) Calcineurin expression, activation, and function in cardiac pressure-overload hypertrophy. Circulation 101:2431-2437 (Pubitemid 30329136)
28. Saito T, Fukuzawa J, Osaki J, Sakuragi H, Yao N, Haneda T, Fujino T, Wakamiya N, Kikuchi K, Hasebe N (2003) Roles of calcineurin and calcium/calmodulin-dependent protein kinase II in pressure overload-induced cardiac hypertrophy. J Mol Cell Cardiol 35:1153-1160 (Pubitemid 37083259)
29. Eto Y, Yonekura K, Sonoda M, Arai N, Sata M, Sugiura S, Takenaka K, Gualberto A, Hixon ML, Wagner MW et al (2000) Calcineurin is activated in rat hearts with physiological left ventricular hypertrophy induced by voluntary exercise training. Circulation 101:2134-2137 (Pubitemid 30253039)
30. Oliveira RS, Ferreira JC, Gomes ER, Paixão NA, Rolim NP, Medeiros A, Guatimosim S, Brum PC (2009) Cardiac antiremodelling effect of aerobic training is associated with a reduction in the calcineurin/NFAT signaling pathway in heart failure mice. J Physiol 587:3899-3910
31. Shimoyama M, Hayashi D, Zou Y, Takimoto E, Mizukami M, Monzen K, Kudoh S, Hiroi Y, Yazaki Y, Nagai R et al (2000) Calcineurin inhibitor attenuates the development and induces the regression of cardiac hypertrophy in rats with salt-sensitive hypertension. Circulation 102:1996-2004
32. Takeda Y, Yoneda T, Demura M, Usukura M, Mabuchi H (2002) Calcineurin inhibition attenuates mineralocorticoid-induced cardiac hypertrophy. Circulation 105:677-679 (Pubitemid 34157368)
33. Wilkins BJ, Dai YS, Bueno OF, Parsons SA, Xu J, Plank DM, Jones F, Kimball TR, Molkentin JD (2004) Calcineurin/NFAT coupling participates in pathological, but not physiological, cardiac hypertrophy. Circ Res 94:110-118 (Pubitemid 38064105)
34. Sussman MA, Lim HW, Gude N, Taigen T, Olson EN, Robbins J, Colbert MC, Gualberto A, Wieczorek DF, Molkentin JD (1998) Prevention of cardiac hypertrophy in mice by calcineurin inhibition. Science 281:1690-1693 (Pubitemid 28435588)
35. Lim HW, De Windt LJ, Mante J, Kimball TR, Witt SA, Sussman MA, Molkentin JD (2000) Reversal of cardiac hypertrophy in transgenic disease models by calcineurin inhibition. J Mol Cell Cardiol 32:697-709 (Pubitemid 30658937)
36. Tokudome T, Horio T, Kishimoto I, Soeki T, Mori K, Kawano Y, Kohno M, Garbers DL, Nakao K, Kangawa K (2005) Calcineurin-nuclear factor of activated T cells pathwaydependent cardiac remodeling in mice deficient in guanylyl cyclase A, a receptor for atrial and brain natriuretic peptides. Circulation 111:3095-3104 (Pubitemid 40847787)
37. Tokudome T, Kishimoto I, Horio T, Arai Y, Schwenke DO, Hino J, Okano I, Kawano Y, Kohno M, Miyazato M et al (2008) Regulator of G-protein signaling subtype 4 mediates antihypertrophic effect of locally secreted natriuretic peptides in the heart. Circulation 117:2329-2339 (Pubitemid 351653552)
38. Klaiber M, Kruse M, Völker K, Schröter J, Feil R, Freichel M, Gerling A, Feil S, Dietrich A, Londoño JE et al (2010) Novel insights into the mechanisms mediating the local antihypertrophic effects of cardiac atrial natriuretic peptide: role of cGMPdependent protein kinase and RGS2. Basic Res Cardiol 105:583-595
39. Kinoshita H, Kuwahara K, Nishida M, Jian Z, Rong X, Kiyonaka S, Kuwabara Y, Kurose H, Inoue R, Mori Y et al (2010) Inhibition of TRPC6 channel activity contributes to the antihypertrophic effects of natriuretic peptides-guanylyl cyclase-A signaling in the heart. Circ Res 106:1849-1860
40. Glenn DJ, Rahmutula D, Nishimoto M, Liang F, Gardner DG (2009) Atrial natriuretic peptide suppresses endothelin gene expression and proliferation in cardiac fibroblasts through a GATA4-dependent mechanism. Cardiovasc Res 84:209-217
41. Jankowski M (2009) GATA4, a new regulator of cardiac fibroblasts, is sensitive to natriuretic peptides. Cardiovasc Res 84:176-177
42. Karmazyn M, Kilić A, Javadov S (2008) The role of NHE-1 in myocardial hypertrophy and remodelling. J Mol Cell Cardiol 44:647-653
43. Cingolani HE, Ennis IL (2007) Sodium-hydrogen exchanger, cardiac overload, and myocardial hypertrophy. Circulation 115:1090-1100 (Pubitemid 46673171)
44. Khandoudi N, Ho J, Karmazyn M (1994) Role of Na(+)-H+ exchange in mediating effects of endothelin-1 on normal and ischemic/reperfused hearts. Circ Res 75:369-378 (Pubitemid 24228329)
45. Ito N, Kagaya Y, Weinberg EO, Barry WH, Lorell BH (1997) Endothelin and angiotensin II stimulation of Na+-H+exchange is impaired in cardiac hypertrophy. J Clin Invest 99:125-135 (Pubitemid 27058303)
46. Cingolani HE (1999) Na+/H+exchange hyperactivity and myocardial hypertrophy: are they linked phenomena? Cardiovasc Res 44:462-467 (Pubitemid 30012046)
47. Young MJ (2008) Mechanisms of mineralocorticoid receptormediated cardiac fibrosis and vascular inflammation. Curr Opin Nephrol Hypertens 17:174-180 (Pubitemid 351253043)
48. Baartscheer A, Schumacher CA, van Borren MM, Belterman CN, Coronel R, Fiolet JW (2003) Increased Na+/H+-exchange activity is the cause of increased [Na+]i and underlies disturbed calcium handling in the rabbit pressure and volume overload heart failure model. Cardiovasc Res 57:1015-1024 (Pubitemid 36324606)
49. Baartscheer A, Hardziyenka M, Schumacher CA, Belterman CN, van Borren MM, Verkerk AO, Coronel R, Fiolet JW (2008) Chronic inhibition of the Na+/H+-exchanger causes regression of hypertrophy, heart failure, and ionic and electrophysiological remodeling. Br J Pharmacol 154:1266-1275 (Pubitemid 351992061)
50. Baartscheer A, Schumacher CA, van Borren MM, Belterman CN, Coronel R, Opthof T, Fiolet JW (2005) Chronic inhibition of Na+/H+-exchanger attenuates cardiac hypertrophy and prevents cellular remodeling in heart failure. Cardiovasc Res 65:83-92 (Pubitemid 40038481)
51. Pérez NG, Piaggio MR, Ennis IL, Garciarena CD, Morales C, Escudero EM, Cingolani OH, Chiappe de Cingolani G, Yang XP, Cingolani HE (2007) Phosphodiesterase 5A inhibition induces Na+/H+exchanger blockade and protection against myocardial infarction. Hypertension 49:1095-1103 (Pubitemid 351664333)
52. Dostal DE, Baker KM (1998) Angiotensin and endothelin: messengers that couple ventricular stretch to the Na+/H+ exchanger and cardiac hypertrophy. Circ Res 83:870-873 (Pubitemid 28489084)
53. Kilic A, Velic A, De Windt LJ, Fabritz L, Voss M, Mitko D, Zwiener M, Baba HA, van Eickels M, Schlatter E et al (2005) Enhanced activity of the myocardial Na+/H+exchanger NHE-1 contributes to cardiac remodeling in atrial natriuretic peptide receptor-deficient mice. Circulation 112:2307-2317 (Pubitemid 41464574)
54. Kilic A, Rajapurohitam V, Sandberg SM, Zeidan A, Hunter JC, Said Faruq N, Lee CY, Burnett JC Jr, Karmazyn M (2010) A novel chimeric natriuretic peptide reduces cardiomyocyte hypertrophy through the NHE-1-calcineurin pathway. Cardiovasc Res 88:434-442
55. Dobaczewski M, Chen W, Frangogiannis NG (2011) Transforming growth factor (TGF)-β signaling in cardiac remodeling. J Mol Cell Cardiol
56. Rosenkranz S (2004) TGF-beta1 and angiotensin networking in cardiac remodeling. Cardiovasc Res 63:423-432 (Pubitemid 38970186)
57. Bujak M, Frangogiannis NG (2007) The role of TGF-beta signaling in myocardial infarction and cardiac remodeling. Cardiovasc Res 74:184-195 (Pubitemid 46517504)
58. Ramos-Mondragón R, Galindo CA, Avila G (2008) Role of TGF-beta on cardiac structural and electrical remodeling. Vasc Health Risk Manag 4:1289-1300
59. Leask A, Abraham DJ (2004) TGF-beta signaling and the fibrotic response. FASEB J 18:816-827
60. Wang B, Omar A, Angelovska T, Drobic V, Rattan SG, Jones SC, Dixon IM (2007) Regulation of collagen synthesis by inhibitory Smad7 in cardiac myofibroblasts. Am J Physiol Heart Circ Physiol 293:H1282-H1290 (Pubitemid 47254231)
61. Kuwahara F, Kai H, Tokuda K, Kai M, Takeshita A, Egashira K, Imaizumi T (2002) Transforming growth factor-beta function blocking prevents myocardial fibrosis and diastolic dysfunction in pressure-overloaded rats. Circulation 106:130-135 (Pubitemid 34747453)
62. Hein S, Arnon E, Kostin S, Schönburg M, Elsässer A, Polyakova V, Bauer EP, Klövekorn WP, Schaper J (2003) Progression from compensated hypertrophy to failure in the pressure-overloaded human heart: structural deterioration and compensatory mechanisms. Circulation 107:984-991 (Pubitemid 36258721)
63. Chen YF, Feng JA, Li P, Xing D, Ambalavanan N, Oparil S (2006) Atrial natriuretic peptide-dependent modulation of hypoxia-induced pulmonary vascular remodeling. Life Sci 79:1357-1365 (Pubitemid 44215927)
64. Rosenkranz S, Flesch M, Amann K, Haeuseler C, Kilter H, Seeland U, Schluter K-D, Bohm M (2002) Alterations of β-adrenergic signaling and cardiac hypertrophy in transgenic mice overexpressing TGF-β1. Am J Physiol Heart 283: H1253-H1262
65. Brooks WW, Conrad CH (2000) Myocardial fibrosis in transforming growth factor beta (1) heterozygous mice. J Mol Cell Cardiol 32:187-195 (Pubitemid 30670342)
66. Teekakirikul P, Eminaga S, Toka O, Alcalai R, Wang L, Wakimoto H, Nayor M, Konno T, Gorham JM, Wolf CM et al (2010) Cardiac fibrosis in mice with hypertrophic cardiomyopathy is mediated by non-myocyte proliferation and requires Tgf- β. J Clin Invest 120:3520-3529
67. Li RK, Li G, Mickle DA, Weisel RD, Merante F, Luss H, Rao V, Christakis GT, Williams WG (1997) Overexpression of transforming growth factor-beta1 and insulin-like growth factor-1 in patients with idiopathic hypertrophic cardiomyopathy. Circulation 96:874-881 (Pubitemid 27329622)
68. Sanderson JE, Lai KB, Shum IO, Wei S, Chow LT (2001) Transforming growth factor-beta(1) expression in dilated cardiomyopathy. Heart 86:701-708
69. Lim H, Zhu YZ (2006) Role of transforming growth factor-beta in the progression of heart failure. Cell Mol Life Sci 63:2584-2596 (Pubitemid 44800713)
70. Li P, Wang D, Lucas J, Oparil S, Xing D, Cao X, Novak L, Renfrow MB, Chen YF (2008) Atrial natriuretic peptide inhibits transforming growth factor beta-induced Smad signaling and myofibroblast transformation in mouse cardiac fibroblasts. Circ Res 102:185-192 (Pubitemid 351651122)
71. Buxton IL, Duan D (2008) Cyclic GMP/protein kinase G phosphorylation of Smad3 blocks transforming growth factor- beta-induced nuclear Smad translocation: a key antifibrogenic mechanism of atrial natriuretic peptide. Circ Res 102:151-153 (Pubitemid 351651117)
72. He JG, Chen YL, Chen BL, Huang YY, Yao FJ, Chen SL, Dong YG (2010) B-type natriuretic peptide attenuates cardiac hypertrophy via the transforming growth factor-ß1/smad7 pathway in vivo and in vitro. Clin Exp Pharmacol Physiol 37:283-289
73. Stingo AJ, Clavell AL, Heiblein DM, Wei CM, Pittelkow MR, Burnett JC Jr (1992) Presence of C-type natriuretic peptide in cultured human endothelial cells and plasma. Am J Physiol 263: H1318-H1321
74. Honing ML, Smits P, Morrison PJ, Burnett JC Jr, Rabelink TJ (2001) C-type natriuretic peptide-induced vasodilation is dependent on hyperpolarization in human forearm resistance vessels. Hypertension 37:1179-1183 (Pubitemid 32304022)
75. Hutchinson HG, Trindade PT, Cunanan DB, Wu CF, Pratt RE (1997) Mechanisms of natriuretic peptide-induced growth inhibition of vascular smooth muscle cells. Cardiovasc Res 35:158-167 (Pubitemid 27374753)
76. Furuya M, Miyazaki T, Honbou N, Kawashima K, Ohno T, Tanaka S, Kangawa K, Matsuo H (1995) C-type natriuretic peptide inhibits intimal thickening after vascular injury. Ann NY Acad Sci 748:517-523
77. Tokudome T, Horio T, Soeki T, Mori K, Kishimoto I, Suga S, Yoshihara F, Kawano Y, Kohno M, Kangawa K (2004) Inhibitory effect of C-type natriuretic peptide (CNP) on cultured cardiac myocyte hypertrophy: interference between CNP and endothelin-1 signaling pathways. Endocrinology 145:2131-2140 (Pubitemid 38535041)
78. Soeki T, Kishimoto I, Okumura H, Tokudome T, Horio T, Mori K, Kangawa K (2005) C-type natriuretic peptide, a novel antifibrotic and antihypertrophic agent, prevents cardiac remodeling after myocardial infarction. J Am Coll Cardiol 45:608-616 (Pubitemid 40222257)
79. Horio T, Tokudome T, Maki T, Yoshihara F, Suga S, Nishikimi T, Kojima M, Kawano Y, Kangawa K (2003) Gene expression, secretion, and autocrine action of C-type natriuretic peptide in cultured adult rat cardiac fibroblasts. Endocrinology 144:2279-2284 (Pubitemid 36629878)
80. Del Ry S, Cabiati M, Lionetti V, Emdin M, Recchia FA, Giannessi D (2008) Expression of C-type natriureitc peptide and of its receptor NPR-B in normal and failing heart. Peptides 29:2208-2215 (Pubitemid 50311068)
81. Kalra PR, Clague JR, Bolger AP, Anker SD, PooleWilson PA, Struthers AD, Coats AJ (2003) Myocardial production of C-type natriuretic peptide in chronic heart failure. Circulation 107:571-573 (Pubitemid 36176806)
82. Dickey DM, Flora DR, Bryan PM, Xu X, Chen Y, Potter LR (2007) Differential regulation of membrane guanylyl cyclases in congestive heart failure: natriuretic peptide receptor (NPR)-B, not NPR-A, is the predominant natriureitc peptide receptor in the failing heart. Endocrinology 148:3518-3522 (Pubitemid 46997008)
83. Pagel-Langenickel I, Buttgereit J, Bader M, Langenickel TH (2007) Natriuretic peptide receptor B signaling in the cardiovascular system: protection from cardiac hypertrophy. J Mol Med 85:797-810 (Pubitemid 47077112)
84. Langenickel TH, Buttgereit J, Pagel-Langenickel I, Lindner M, Monti J, Beuerlein K, Al-Saadi N, Plehm R, Popova E, Tank J et al (2006) Cardiac hypertrophy in transgenic rats expressing a dominant-negative mutant of the natriuretic peptide receptor B. Proc Natl Acad Sci U S A 103:4735-4740
85. Herring N, Zamman JA, Paterson DJ (2001) Natriuretic peptides like NO facilitate cardiac vagal neurotransmission and bradycardia via a cGMP pathway. Am J Physiol Heart Circ Physiol 281: H2318-H2327
86. Sangaralingham SJ, Huntley BK, Martin FL, McKie PM, Bellavia D, Ichiki T, Harders GE, Chen HH, Burnett JC Jr (2011) The aging heart, myocardial fibrosis, and its relationship to circulating C-type natriuretic peptide. Hypertension 57:201-207
87. Rubattu S, Sciarretta S, Morriello A, Calvieri C, Battistoni A, Volpe M (2010) NPR-C: a component of the natriuretic peptide family with implications in human diseases. J Mol Med 88:889-897
88. Matsukawa N, Grzesik WJ, Takahashi N, Pandey KN, Pang S, Yamauchi M, Smithies O (1999) The natriuretic peptide clearance receptor locally modulates the physiological effects of the natriuretic peptide system. Proc Natl Acad Sci U S A 96:7403-7408 (Pubitemid 29299674)
89. Chauhan SD, Nilsson H, Ahluwalia A, Hobbs AJ (2003) Release of C-type natriuretic peptide accounts for the biological activity of endothelium-derived hyperpolarizing factor. Proc Natl Aca Sci U S A 100:1426-1431 (Pubitemid 36184018)
90. Rose RA, Lomax AE, Giles WR (2003) Inhibition of L-type Ca2 + current by C-type natriuretic peptide in bullfrog atrial myocytes: an NPR-C-mediated effect. Am J Physiol Heart Circ Physiol 285:H2454-H2462 (Pubitemid 37443062)
91. Horikawa YT, Panneerselvam M, Kawaraguchi Y, Tsutsumi YM, Ali SS, Balijepalli RC, Murray F, Head BP, Niesman IR, Rieg T et al (2011) Cardiac-specific overexpression of caveolin-3 attenuates cardiac hypertrophy and increases natriuretic peptide expression and signaling. J Am Coll Cardiol 31(57):2273-2283
92. Cataliotti A, Tonne JM, Bellavia D, Martin FL, Oehler EA, Harders GE, Campbell JM, Peng KW, Russell SJ, Malatino LS et al (2011) Long-term cardiac pro-B-type natriuretic peptide gene delivery prevents the development of hypertensive heart disease in spontaneously hypertensive rats. Circulation 123:1297-1305
93. Hayashi M, Tsutamoto T, Wada A, Maeda K, Mabuchi N, Tsutsui T, Horie H, Ohnishi M, Kinoshita M (2001) Intravenous atrial natriuretic peptide prevents left ventricular remodeling in patients with first anterior acute myocardial infarction. J Am Coll Cardiol 37:1820-1826 (Pubitemid 32499965)
94. Sezai A, Hata M, Wakui S, Niino T, Takayama T, Hirayama A, Saito S, Minami K (2007) Efficacy of continuous low-dose hANP administration in patients undergoing emergent coronary artery bypass grafting for acute coronary syndrome. Circ J 71:1401-1407 (Pubitemid 47381271)
95. Hillock RJ, Frampton CM, Yandle TG, Troughton RW, Lainchbury JG, Richards AM (2008) B-type natriuretic peptide infusions in acute myocardial infarction. Heart 94:617-622 (Pubitemid 351580137)
96. Kitakaze M, Asakura M, Kim J, Shintani Y, Asanuma H, Hamasaki T, Seguchi O, Myoishi M, Minamino T, Ohara T et al (2007) Human atrial natriuretic peptide and nicorandil as adjuncts to reperfusion treatment for acute myocardial infarction (J-WIND): two randomized trials. Lancet 370:1483-1493 (Pubitemid 47625560)
97. Hata N, Seino Y, Tsutamoto T, Hiramitsu S, Kaneko N, Yoshikawa T, Yokoyama H, Tanaka K, Mizuno K, Nejima J et al (2008) Effects of carperitide on the long-term prognosis of patients with acute decompensated chronic heart failure-the PROTECT multicenter randomized controlled study. Circ J 72:1787-1793
98. Abraham WT, Adams KF, Fonarow GC, Costanzo MR, Berkowitz RL, LeJemtel TH, Cheng ML, Wynne J (2005) Inhospital mortality in patients with acute decompensated heart failure requiring intravenous vasoactive medications. An analysis from the Acute Decompensated Heart Failure National Registry (ADHERE). J Am Coll Cardiol 46:57-64 (Pubitemid 40905130)
99. Rouleau JL, Pfeffer MA, Stewart DJ, Isaac D, Sestier F, Kerut EK, Porter CB, Proulx G, Qian C, Block AJ (2000) Comparison of vasopeptidase inhibitor, omapatrilat, and lisinopril on exercise tolerance and morbidity in patients with heart failure: IMPRESS randomized trial. Lancet 356:615-620 (Pubitemid 30627587)
100. Cuculi F, Erne P (2011) Combined neutral endopeptidases inhibitors. Expert Opin Invest Drugs 20:457-463