Natriuretic peptides in cardiometabolic regulation and disease

Nature Reviews Cardiology

Volumn 11, Issue 7, 2014, Pages 403-412

  Zois, Nora E ^a   Bartels, Emil D ^a   Hunter, Ingrid ^a   Kousholt, Birgitte S ^b   Olsen, Lisbeth H ^c   Goetze, Jens P ^a  

^a Rigshospitalet   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ATRIAL NATRIURETIC FACTOR; BRAIN NATRIURETIC PEPTIDE; GLUCOSE; INSULIN; NATRIURETIC FACTOR; NATRIURETIC PEPTIDE TYPE C;

ATHEROSCLEROSIS; CARDIOMETABOLIC REGULATION; CARDIOMETABOLIC RISK; CARDIOVASCULAR DISEASE; CARDIOVASCULAR FUNCTION; DISEASE CONTROL; GLUCOSE BLOOD LEVEL; HEART INFARCTION; HEART PERFORMANCE; HUMAN; HYPERTENSION; INSULIN BLOOD LEVEL; LIFESTYLE; LIPOLYSIS; METABOLIC DISORDER; METABOLIC REGULATION; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN SECRETION; REGULATORY MECHANISM; REVIEW; RISK REDUCTION; THROMBOSIS;

BIOLOGICAL MARKERS; CARDIOVASCULAR DISEASES; DIABETES MELLITUS, TYPE 2; GLUCOSE INTOLERANCE; HUMANS; NATRIURETIC PEPTIDES; OBESITY;

EID: 84903277903     PISSN: 17595002     EISSN: 17595010     Source Type: Journal    
DOI: 10.1038/nrcardio.2014.64     Document Type: Review

References (160)

1. de Bold, A. J., Borenstein, H. B., Veress, A. T. & Sonnenberg, H. A rapid and potent natriuretic response to intravenous injection of atrial myocardial extract in rats. Life Sci. 28, 89-94 (1981).
2. Sudoh, T. et al. Cloning and sequence analysis of cDNA encoding a precursor for human brain natriuretic peptide. Biochem. Biophys. Res. Commun. 159, 1427-1434 (1989).
3. Sudoh, T., Minamino, N., Kangawa, K. & Matsuo, H. C-type natriuretic peptide (CNP): a new member of natriuretic peptide family identified in porcine brain. Biochem. Biophys. Res. Commun. 168, 863-870 (1990).
4. Kita, T. et al. Natriuretic and hypotensive effects of brain natriuretic peptide (BNP) in spontaneously hypertensive rats. Life Sci. 44, 1541-1545 (1989).
5. Richards, A. M. et al. Atrial natriuretic hormone has biological effects in man at physiological plasma concentrations. J. Clin. Endocrinol. Metab. 67, 1134-1139 (1988).
6. Burnett, J. C. Jr, Granger, J. P. & Opgenorth, T. J. Effects of synthetic atrial natriuretic factor on renal function and renin release. Am. J. Physiol. 247, F863-F866 (1984).
7. Davidson, N. C., Barr, C. S. & Struthers, A. D. C-type natriuretic peptide. An endogenous inhibitor of vascular angiotensin-converting enzyme activity. Circulation 93, 1155-1159 (1996).
8. Hunt, P. J., Richards, A. M., Espiner, E. A., Nicholls, M. G. & Yandle, T. G. Bioactivity and metabolism of C-type natriuretic peptide in normal man. J. Clin. Endocrinol. Metab. 78, 1428-1435 (1994).
9. Wei, C. M., Aarhus, L. L., Miller, V. M. & Burnett, J. C. Action of C-type natriuretic peptide in isolated canine arteries and veins. Am. J. Physiol. 264 (1 Pt 2), H71-H73 (1993).
10. Mukoyama, M. et al. Brain natriuretic peptide as a novel cardiac hormone in humans. Evidence for an exquisite dual natriuretic peptide system, atrial natriuretic peptide and brain natriuretic peptide. J. Clin. Invest. 87, 1402-1412 (1991).
11. Hasegawa, K. et al. Light and electron microscopic localization of brain natriuretic peptide in relation to atrial natriuretic peptide in porcine atrium. Immunohistocytochemical study using specific monoclonal antibodies. Circulation 84, 1203-1209 (1991).
12. Goetze, J. P., Friis-Hansen, L., Rehfeld, J. F., Nilsson, B. & Svendsen, J. H. Atrial secretion of B-type natriuretic peptide. Eur. Heart J. 27, 1648-1650 (2006).
13. Dietz, J. R. Release of natriuretic factor from rat heart-lung preparation by atrial distension. Am. J. Physiol. 247, R1093-R1096 (1984).
14. Sawada, Y. et al. Stretch-induced hypertrophic growth of cardiocytes and processing of brain-type natriuretic peptide are controlled by proprotein-processing endoprotease furin. J. Biol. Chem. 272, 20545-20554 (1997).
15. Yan, W., Wu, F., Morser, J. & Wu, Q. Corin, a transmembrane cardiac serine protease, acts as a pro-atrial natriuretic peptide-converting enzyme. Proc. Natl Acad. Sci. USA 97, 8525-8529 (2000).
16. Ichiki, T. et al. Corin is present in the normal human heart, kidney, and blood, with pro-B-type natriuretic peptide processing in the circulation. Clin. Chem. 57, 40-47 (2011).
17. Takahashi, T., Allen, P. D. & Izumo, S. Expression of A-, B-, and C-type natriuretic peptide genes in failing and developing human ventricles: correlation with expression of the Ca2+-ATPase gene. Circ. Res. 71, 9-17 (1992).
18. Suga, S. et al. Endothelial production of C-type natriuretic peptide and its marked augmentation by transforming growth factor-beta: possible existence of "vascular natriuretic peptide system". J. Clin. Invest. 90, 1145-1149 (1992).
19. Herman, J. P., Langub, M. C. Jr & Watson, R. E. Jr. Localization of C-type natriuretic peptide mRNA in rat hypothalamus. Endocrinology 133, 1903-1906 (1993).
20. Middendorff, R., Müller, D., Paust, H. J., Davidoff, M. S. & Mukhopadhyay, A. K. Natriuretic peptides in the human testis: evidence for a potential role of C-type natriuretic peptide in Leydig cells. J. Clin. Endocrinol. Metab. 81, 4324-4328 (1996).
21. Wu, C., Wu, F., Pan, J., Morser, J. & Wu, Q. Furin-mediated processing of Pro-C-type natriuretic peptide. J. Biol. Chem. 278, 25847-25852 (2003).
22. Chauhan, S. D., Hobbs, A. J. & Ahluwalia, A. C-type natriuretic peptide: new candidate for endothelium-derived hyperpolarising factor. Int. J. Biochem. Cell Biol. 36, 1878-1881 (2004).
23. Okamura, H. et al. Atrial natriuretic peptide receptors are present in brown adipose tissue. Biochem. Biophys. Res. Commun. 156, 1000-1006 (1988).
24. Sarzani, R., Dessi-Fulgheri, P., Paci, V. M., Espinosa, E. & Rappelli, A. Expression of natriuretic peptide receptors in human adipose and other tissues. J. Endocrinol. Invest. 19, 581-585 (1996).
25. Ropero, A. B. et al. The atrial natriuretic paptide and guanylyl cyclase-A system modulates pancreatic β-cell function. Endocrinology 151, 3665-3674 (2010).
26. Herman, J. P., Dolgas, C. M., Rucker, D. & Langub, M. C. Jr. Localization of natriuretic peptide-activated guanylate cyclase mRNAs in the rat brain. J. Comp. Neurol. 369, 165-187 (1996).
27. Schulz, S., Chinkers, M. & Garbers, D. L. The guanylate cyclase/receptor family of proteins. FASEB J. 3, 2026-2035 (1989).
28. Chinkers, M., Singh, S. & Garbers, D. L. Adenine nucleotides are required for activation of rat atrial natriuretic peptide receptor/guanylyl cyclase expressed in a baculovirus system. J. Biol. Chem. 266, 4088-4093 (1991).
29. Koller, K. J. & Goeddel, D. V. Molecular biology of the natriuretic peptides and their receptors. Circulation 86, 1081-1088 (1992).
30. Anand-Srivastava, M. B. Natriuretic peptide receptor-C signaling and regulation. Peptides 26, 1044-1059 (2005).
31. Scotland, R. S. et al. C-type natriuretic peptide inhibits leukocyte recruitment and platelet-leukocyte interactions via suppression of P-selectin expression. Proc. Natl Acad. Sci. USA 102, 14452-14457 (2005).
32. Mouawad, R., Li, Y. & Anand-Srivastava, M. B. Atrial natriuretic peptide-C receptor-induced attenuation of adenylyl cyclase signaling activates phosphatidylinositol turnover in A10 vascular smooth muscle cells. Mol. Pharmacol. 65, 917-924 (2004).
33. Suga, S. et al. Receptor selectivity of natriuretic peptide family, atrial natriuretic peptide, brain natriuretic peptide, and C-type natriuretic peptide. Endocrinology 130, 229-239 (1992).
34. Lin, X., Hänze, J., Heese, F., Sodmann, R. & Lang, R. E. Gene expression of natriuretic peptide receptors in myocardial cells. Circ. Res. 77, 750-758 (1995).
35. Schiffrin, E. L., Poissant, L., Cantin, M. & Thibault, G. Receptors for atrial natriuretic factor in cultured vascular smooth muscle cells. Life Sci. 38, 817-826 (1986).
36. Burgess, M. D. et al. C-type natriuretic peptide receptor expression in pancreatic alpha cells. Histochem. Cell Biol. 132, 95-103 (2009).
37. Anand-Srivastava, M. B., Gutkowska, J. & Cantin, M. The presence of atrial-natriuretic-factor receptors of ANF-R2 subtype in rat platelets: coupling to adenylate cyclase/cyclic AMP signal-transduction system. Biochem. J. 278, 211-217 (1991).
38. Komatsu, Y. et al. C-type natriuretic peptide (CNP) in rats and humans. Endocrinology 129, 1104-1106 (1991).
39. Herman, J. P., Dolgas, C. M., Marcinek, R. & Langub, M. C. Jr. Expression and glucocorticoid regulation of natriuretic peptide clearance receptor (NPR-C) mRNA in rat brain and choroid plexus. J. Chem. Neuroanat. 11, 257-265 (1996).
40. Yamashita, Y. et al. Concentration of mRNA for the natriuretic peptide receptor-C in hypertrophic chondrocytes of the fetal mouse tibia. J. Biochem. 127, 177-179 (2000).
41. Costello-Boerrigter, L. C. & Burnett, J. C. Jr. The prognostic value of N-terminal proB-type natriuretic peptide. Nat. Clin. Pract. Cardiovasc. Med. 4, 194-201 (2005).
42. Chabot, J. G., Morel, G., Kopelman, H., Belles-Isles, M. & Heisler, S. Atrial natriuretic factor and exocrine pancreas: autoradiographic localization of binding sites and ultrastructural evidence for internalization of endogenous ANF. Pancreas 2, 404-413 (1987).
43. Lindop, G. B., Mallon, E. A. & MacIntyre, G. Atrial natriuretic peptide in the heart and pancreas. Histol. Histopathol. 1, 147-154 (1986).
44. Jeandel, L. et al. Immunocytochemical localization, binding, and effects of atrial natriuretic peptide in rat adipocytes. Mol. Cell. Endocrinol. 62, 69-78 (1989).
45. Sengenès, C., Berlan, M., De Glisezinski, I., Lafontan, M. & Galitzky, J. Natriuretic peptides: a new lipolytic pathway in human adipocytes. FASEB J. 14, 1345-1351 (2000).
46. Sengenès, C. et al. Involvement of a cGMP-dependent pathway in the natriuretic peptide-mediated hormone-sensitive lipase phosphorylation in human adipocytes. J. Biol. Chem. 278, 48617-48626 (2003).
47. Miyashita, K. et al. Natriuretic peptides/cGMP/cGMP-dependent protein kinase cascades promote muscle mitochondrial biogenesis and prevent obesity. Diabetes 58, 2880-2892 (2009).
48. Engeli, S. et al. Natriuretic peptides enhance the oxidative capacity of human skeletal muscle. J. Clin. Invest. 122, 4675-4679 (2012).
49. Birkenfeld, A. L. et al. Lipid mobilization with physiological atrial natriuretic peptide concentrations in humans. J. Clin. Endocrinol. Metab. 90, 3622-3628 (2005).
50. Bartels, E. D., Nielsen, J. M., Bisgaard, L. S., Goetze, J. P. & Nielsen, L. B. Decreased expression of natriuretic peptides associated with lipid accumulation in cardiac ventricle of obese mice. Endocrinology 151, 5218-5225 (2010).
51. Heinisch, B. B. et al. B-type natriuretic peptide (BNP) affects the initial response to intravenous glucose: a randomised placebo-controlled cross-over study in healthy men. Diabetologia 55, 1400-1405 (2012).
52. Moro, C. et al. Atrial natriuretic peptide contributes to physiological control of lipid mobilization in humans. FASEB J. 18, 908-910 (2004).
53. Moro, C. et al. Exercise-induced lipid mobilization in subcutaneous adipose tissue is mainly related to natriuretic peptides in overweight men. Am. J. Physiol. Endocrinol. Metab. 295, E505-E513 (2008).
54. Olsen, M. H. et al. N-terminal pro brain natriuretic peptide is inversely related to metabolic cardiovascular risk factors and the metabolic syndrome. Hypertension 46, 660-666 (2005).
55. Wang, T. J. et al. Association of plasma natriuretic peptide levels with metabolic risk factors in ambulatory individuals. Circulation 115, 1345-1353 (2007).
56. Meirhaeghe, A. et al. Association between the T-381C polymorphism of the brain natriuretic peptide gene and risk of type 2 diabetes in human populations. Hum. Mol. Genet. 16, 1343-1350 (2007).
57. Magnusson, M. et al. Low plasma level of atrial natriuretic peptide predicts development of diabetes: the prospective Malmo Diet and Cancer study. J. Clin. Endocrinol. Metab. 97, 638-645 (2012).
58. Goetze, J. P. Plasma proANP decreases after meal intake. Clin. Chem. 59, 1270-1271 (2013).
59. Swinburn, B., Sacks, G. & Ravussin, E. Increased food energy supply is more than sufficient to explain the US epidemic of obesity. Am. J. Clin. Nutr. 90, 1453-1456 (2009).
60. Addisu, A., Gower, W. R. Jr, Landon, C. S. & Dietz, J. R. B-type natriuretic peptide decreases gastric emptying and absorption. Exp. Biol. Med. 233, 475-482 (2008).
61. Vila, G. et al. B-type natriuretic peptide modulates ghrelin, hunger, and satiety in healthy men. Diabetes 61, 2592-2596 (2012).
62. Tsukamoto, O. et al. Natriuretic peptides enhance the production of adiponectin in human adipocytes and in patients with chronic heart failure. J. Am. Coll. Cardiol. 53, 2070-2077 (2009).
63. Birkenfeld, A. L. et al. Atrial natriuretic peptide and adiponectin interactions in man. PLoS ONE 7, e43238 (2012).
64. Bordicchia, M. et al. Cardiac natriuretic peptides act via p38 MAPK to induce the brown fat thermogenic program in mouse and human adipocytes. J. Clin. Invest. 122, 1022-1036 (2012).
65. Stanford, K. I. et al. Brown adipose tissue regulates glucose homeostasis and insulin sensitivity. J. Clin. Invest. 123, 215-223 (2013).
66. Virtanen, K. A. et al. Functional brown adipose tissue in healthy adults. N. Engl. J. Med. 360, 1518-1525 (2009).
67. Cypess, A. M. et al. Identification and importance of brown adipose tissue in adult humans. N. Engl. J. Med. 360, 1509-1517 (2009).
68. Orava, J. et al. Blunted metabolic responses to cold and insulin stimulation in brown adipose tissue of obese humans. Obesity 21, 2279-2287 (2013).
69. Lockie, S. H. et al. Direct control of brown adipose tissue thermogenesis by central nervous system glucagon-like peptide-1 receptor signaling. Diabetes 61, 2753-2762 (2012).
70. Kim, M. et al. GLP-1 receptor activation and Epac2 link atrial natriuretic peptide secretion to control of blood pressure. Nat. Med. 19, 567-575 (2013).
71. Steinhelper, M. E., Cochrane, K. L. & Field, L. J. Hypotension in transgenic mice expressing atrial natriuretic factor fusion genes. Hypertension 16, 301-307 (1990).
72. Ogawa, Y. et al. Molecular cloning of the complementary DNA and gene that encode mouse brain natriuretic peptide and generation of transgenic mice that overexpress the brain natriuretic peptide gene. J. Clin. Invest. 93, 1911-1921 (1994).
73. John, S. W. et al. Blood pressure and fluid-electrolyte balance in mice with reduced or absent ANP. Am. J Physiol. 271 (1 Pt 2), R109-R114 (1996).
74. 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).
75. Lopez, M. J. et al. Salt-resistant hypertension in mice lacking the guanylyl cyclase-A receptor for atrial natriuretic peptide. Nature 378, 65-68 (1995).
76. Oliver, P. M. et al. Natriuretic peptide receptor 1 expression influences blood pressures of mice in a dose-dependent manner. Proc. Natl Acad. Sci. USA 95, 2547-2551 (1998).
77. Cataliotti, A. et al. 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 (2011).
78. Cataliotti, A., Costello-Boerrigter, L. C., Chen, H. H., Textor, S. C. & Burnett, J. C. Jr. Sustained blood pressure-lowering actions of subcutaneous B-type natriuretic peptide (nesiritide) in a patient with uncontrolled hypertension. Mayo Clin. Proc. 87, 413-415 (2012).
79. Cannone, V. et al. Atrial natriuretic peptide genetic variant rs5065 and risk for cardiovascular disease in the general community: a 9-year follow-up study. Hypertension 62, 860-865 (2013).
80. Newton-Cheh, C. et al. Association of common variants in NPPA and NPPB with circulating natriuretic peptides and blood pressure. Nat. Genet. 41, 348-353 (2009).
81. Arora, P. et al. Atrial natriuretic peptide is negatively regulated by microRNA-425. J. Clin. Invest. 123, 3378-3382 (2013).
82. Belluardo, P. et al. Lack of activation of molecular forms of the BNP system in human grade 1 hypertension and relationship to cardiac hypertrophy. Am. J. Physiol. Heart Circ. Physiol. 291, H1529-H1535 (2006).
83. Macheret, F. et al. Human hypertension is characterized by a lack of activation of the antihypertensive cardiac hormones ANP and BNP. J. Am. Coll. Cardiol. 60, 1558-1565 (2012).
84. Dries, D. L. et al. Corin gene minor allele defined by 2 missense mutations is common in blacks and associated with high blood pressure and hypertension. Circulation 112, 2403-2410 (2005).
85. Wang, T. J. et al. Impact of obesity on plasma natriuretic peptide levels. Circulation 109, 594-600 (2004).
86. Asferg, C. L. et al. Relative atrial natriuretic peptide deficiency and inadequate renin and angiotensin II suppression in obese hypertensive men. Hypertension 62, 147-153 (2013).
87. Chan, J. C. et al. Hypertension in mice lacking the proatrial natriuretic peptide convertase corin. Proc. Natl Acad. Sci. USA 102, 785-790 (2005).
88. Matsukawa, N. et al. The natriuretic peptide clearance receptor locally modulates the physiological effects of the natriuretic peptide system. Proc. Natl Acad. Sci. USA 96, 7403-7408 (1999).
89. Ehret, G. B. et al. Genetic variants in novel pathways influence blood pressure and cardiovascular disease risk. Nature 478, 103-109 (2011).
90. Weber, N. C., Blumenthal, S. B., Hartung, T., Vollmar, A. M. & Kiemer, A. K. ANP inhibits TNF-alpha-induced endothelial MCP-1 expression-involvement of p38 MAPK and MKP-1. J. Leukoc. Biol. 4, 932-941 (2003).
91. Burger, P. C. & Wagner, D. D. Platelet P-selectin facilitates atherosclerotic lesion development. Blood 101, 2661-2666 (2003).
92. Hutchinson, H. G., Trindade, P. T., Cunanan, D. B., Wu, C. F. & Pratt, R. E. Mechanisms of natriuretic-peptide-induced growth inhibition of vascular smooth muscle cells. Cardiovasc. Res. 35, 158-167 (1997).
93. Ikeda, M. et al. Natriuretic peptide family as a novel antimigration factor of vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 17, 731-736 (1997).
94. Itoh, H., Pratt, R. E. & Dzau, V. J. Atrial natriuretic polypeptide inhibits hypertrophy of vascular smooth muscle cells. J. Clin. Invest. 86, 1690-1697 (1990).
95. Kohno, M. et al. Effect of natriuretic peptide family on the oxidized LDL-induced migration of human coronary artery smooth muscle cells. Circ. Res. 81, 585-590 (1997).
96. Shinomiya, M. et al. C-type natriuretic peptide inhibits intimal thickening of rabbit carotid artery after balloon catheter injury. Biochem. Biophys. Res. Commun. 205, 1051-1056 (1994).
97. Ueno, H. et al. Local expression of C-type natriuretic peptide markedly suppresses neointimal formation in rat injured arteries through an autocrine/paracrine loop. Circulation 96, 2272-2279 (1997).
98. Gaspari, T. A., Barber, M. N., Woods, R. L. & Dusting, G. J. Type-C natriuretic peptide prevents development of experimental atherosclerosis in rabbits. Clin. Exp. Pharmacol. Physiol. 27, 653-655 (2000).
99. Larifla, L. et al. Inhibition of vascular smooth muscle cell proliferation and migration in vitro and neointimal hyperplasia in vivo by adenoviral-mediated atrial natriuretic peptide delivery. J. Gene Med. 14, 459-467 (2012).
100. Bouchie, J. L., Hansen, H. & Feener, E. P. Natriuretic factors and nitric oxide suppress plasminogen activator inhibitor-1 expression in vascular smooth muscle cells: role of cGMP in the regulation of the plasminogen system. Arterioscler. Thromb. Vasc. Biol. 18, 1771-1779 (1998).
101. Yoshizumi, M. et al. Natriuretic peptides regulate the expression of tissue factor and PAI-1 in endothelial cells. Thromb. Haemost. 82, 1497-1503 (1999).
102. Kairuz, E. M. et al. C-type natriuretic peptide (CNP) suppresses plasminogen activator inhibitor-1 (PAI-1) in vivo. Cardiovasc. Res. 66, 574-582 (2005).
103. Qian, J. Y. et al. Local expression of C-type natriuretic peptide suppresses inflammation, eliminates shear stress-induced thrombosis, and prevents neointima formation through enhanced nitric oxide production in rabbit injured carotid arteries. Circ. Res. 91, 1063-1069 (2002).
104. Loeb, A. L. & Gear, A. R. Potentiation of platelet aggregation by atrial natriuretic peptide. Life Sci. 43, 731-738 (1988).
105. De Caterina, R., Volpe, M., Atlas, S. A. & Weksler, B. B. Effects of atrial natriuretic factor on human platelet function. Life Sci. 37, 1395-1402 (1985).
106. Borgognone, A., Lowe, K. L., Watson, S. P. & Madhani, M. Natriuretic peptides induce weak VASP phosphorylation at serine 239 in platelets. Platelets 25, 1-7 (2013).
107. Strom, T. M., Weil, J. & Bidlingmaier, F. Platelet receptors for atrial natriuretic peptide in man. Life Sci. 40, 769-773 (1987).
108. Aszódi, A. et al. The vasodilator-stimulated phosphoprotein (VASP) is involved in cGMP-and cAMP-mediated inhibition of agonist-induced platelet aggregation, but is dispensable for smooth muscle function. EMBO J. 18, 37-48 (1999).
109. Akbar, H., Navran, S. S., Chang, J., Miller, D. D. & Feller, D. R. Investigation of the effects of phospholipase C on human platelets: evidence that aggregation induced by phospholipase C is independent of prostaglandin generation, released ADP and is modulated by cyclic AMP. Thromb. Res. 27, 405-417 (1982).
110. Butt, E. et al. cAMP-and cGMP-dependent protein kinase phosphorylation sites of the focal adhesion vasodilator-stimulated phosphoprotein (VASP) in vitro and in intact human platelets. J. Biol. Chem. 269, 14509-14517 (1994).
111. Smolenski, A. et al. Analysis and regulation of vasodilator-stimulated phosphoprotein serine 239 phosphorylation in vitro and in intact cells using a phosphospecific monoclonal antibody. J. Biol. Chem. 273, 20029-20035 (1998).
112. Zeng, G. et al. Roles for insulin receptor, PI3-kinase, and Akt in insulin-signaling pathways related to production of nitric oxide in human vascular endothelial cells. Circulation 101, 1539-1545 (2000).
113. Hashim, S., Li, Y. & Anand-Srivastava, M. B. Small cytoplasmic domain peptides of natriuretic peptide receptor-C attenuate cell proliferation through Giα protein/MAP kinase/PI3-kinase/AKT pathways. Am. J. Physiol. Heart Circ. Physiol. 291, H3144-H3153 (2006).
114. Alexander, M. R., Knowles, J. W., Nishikimi, T. & Maeda, N. Increased atherosclerosis and smooth muscle cell hypertrophy in natriuretic peptide receptor A-/-apolipoprotein E-/-mice. Arterioscler. Thromb. Vasc. Biol. 23, 1077-1082 (2003).
115. Naruko, T. et al. C-type natriuretic peptide in human coronary atherosclerotic lesions. Circulation 94, 3103-3108 (1996).
116. Vlachopoulos, C. et al. Amino-terminal pro-C-type natriuretic peptide is associated with arterial stiffness, endothelial function and early atherosclerosis. Atherosclerosis 211, 649-655 (2010).
117. Igaki, T. et al. Insulin suppresses endothelial secretion of C-type natriuretic peptide, a novel endothelium-derived relaxing peptide. Diabetes 45 (Suppl. 3), S62-S64 (1996).
118. Toth, M. et al. Hypoxia stimulates release of ANP and BNP from perfused rat ventricular myocardium. Am. J. Physiol. 266 (4 Pt 2), H1572-H1580 (1994).
119. Tateishi, J., Masutani, M., Ohyanagi, M. & Iwasaki, T. Transient increase in plasma brain (B-type) natriuretic peptide after percutaneous transluminal coronary angioplasty. Clin. Cardiol. 23, 776-780 (2000).
120. Goetze, J. P. et al. Increased cardiac BNP expression associated with myocardial ischemia. FASEB J. 17, 1105-1107 (2003).
121. Tamura, N. et al. Cardiac fibrosis in mice lacking brain natriuretic peptide. Proc. Natl Acad. Sci. USA 97, 4239-4244 (2000).
122. Langenickel, T. H. et al. Cardiac hypertrophy in transgenic rats expressing a dominant-negative mutant of the natriuretic peptide receptor B. Proc. Natl Acad. Sci. USA 103, 4735-4740 (2006).
123. Wang, Y. et al. Cardiomyocyte-restricted over-expression of C-type natriuretic peptide prevents cardiac hypertrophy induced by myocardial infarction in mice. Eur. J. Heart Fail. 9, 548-557 (2007).
124. Soeki, T. et al. C-type natriuretic peptide, a novel antifibrotic and antihypertrophic agent, prevents cardiac remodeling after myocardial infarction. J. Am. Coll. Cardiol. 45, 608-616 (2005).
125. Horio, T. et al. Gene expression, secretion, and autocrine action of C-type natriuretic peptide in cultured adult rat cardiac fibroblasts. Endocrinology 144, 2279-2284 (2003).
126. McKie, P. M., Sangaralingham, S. J. & Burnett, J. C. Jr. CD-NP: an innovative designer natriuretic peptide activator of particulate guanylyl cyclase receptors for cardiorenal disease. Curr. Heart Fail. Rep. 7, 93-99 (2010).
127. D'Souza, S. P. et al. B-type natriuretic peptide limits infarct size in rat isolated hearts via KATP channel opening. Am. J. Physiol. Heart Circ. Physiol. 284, H1592-H1600 (2003).
128. Burley, D. S. & Baxter, G. F. B-type natriuretic peptide at early reperfusion limits infarct size in the rat isolated heart. Basic Res. Cardiol. 102, 529-541 (2007).
129. Kousholt, B. S. et al. Natriuretic peptide infusion reduces myocardial injury during acute ischemia/reperfusion. Cardiovasc. Endocrin. 1, 4-12 (2012).
130. Okawa, H. et al. Preischemic infusion of alpha-human atrial natriuretic peptide elicits myoprotective effects against ischemia reperfusion in isolated rat hearts. Mol. Cell. Biochem. 248, 171-177 (2003).
131. Yang, X. M., Philipp, S., Downey, J. M. & Cohen, M. V. Atrial natriuretic peptide administered just prior to reperfusion limits infarction in rabbit hearts. Basic Res. Cardiol. 101, 311-318 (2006).
132. Zhang, W. W., Hasaniya, N. W., Premaratne, S. & McNamara, J. J. Atrial natriuretic peptide protects against ischemia-reperfusion injury in rabbit hearts in vivo. Vasc. Endovasc. Surg. 42, 263-267 (2008).
133. Hobbs, A., Foster, P., Prescott, C., Scotland, R. & Ahluwalia, A. Natriuretic peptide receptor-C regulates coronary blood flow and prevents myocardial ischemia/reperfusion injury: novel cardioprotective role for endothelium-derived C-type natriuretic peptide. Circulation 110, 1231-1235 (2004).
134. Kitakaze, M. et al. Human atrial natriuretic peptide and nicorandil as adjuncts to reperfusion treatment for acute myocardial infarction (J-WIND): two randomised trials. Lancet 370, 1483-1493 (2007).
135. Chen, H. H. et al. Low-dose nesiritide in human anterior myocardial infarction suppresses aldosterone and preserves ventricular function and structure: a proof of concept study. Heart 95, 1315-1319 (2009).
136. US National Library of Medicine. ClinicalTrials.gov [online], http://www.clinicaltrials.gov/ct2/show/NCT00573144 (2012).
137. Sangaralingham, S. J., Burnett, J. C. Jr, Mckie, P. M., Schirger, J. A. & Chen, H. H. Rationale and design of a randomized, double-blind, placebo-controlled clinical trial to evaluate the efficacy of B-type natriuretic peptide for the preservation of left ventricular function after anterior myocardial infarction. J. Card. Fail. 19, 533-539 (2013).
138. Gorbe, A. et al. Role of cGMP-PKG signaling in the protection of neonatal rat cardiac myocytes subjected to simulated ischemia/reoxygenation. Basic Res. Cardiol. 105, 643-650 (2010).
139. Fiedler, B. et al. cGMP-dependent protein kinase type I inhibits TAB1-p38 mitogen-activated protein kinase apoptosis signaling in cardiac myocytes. J. Biol. Chem. 281, 32831-32840 (2006).
140. Ren, B. et al. Brain natriuretic peptide limits myocardial infarct size dependent of nitric oxide synthase in rats. Clin. Chim. Acta 377, 83-87 (2007).
141. Murthy, K. S., Teng, B., Jin, J. & Makhlouf, G. M. G protein-dependent activation of smooth muscle eNOS via natriuretic peptide clearance receptor. Am. J. Physiol. 275 (6 Pt 1), C1409-C1416 (1998).
142. Hobbs, A., Foster, P., Prescott, C., Scotland, R. & Ahluwalia, A. Natriuretic peptide receptor-C regulates coronary blood flow and prevents myocardial ischemia/reperfusion injury. Circulation 110, 1231-1235 (2004).
143. Mtairag, el M. et al. Pharmacological potentiation of natriuretic peptide limits polymorphonuclear neutrophil-vascular cell interactions. Arterioscler. Thromb. Vasc. Biol. 22, 1824-1831 (2002).
144. Yancy, C. W. et al. 2013 ACCF/AHA guideline for the management of heart failure: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. Circulation 128, e240-e327 (2013).
145. Hawkridge, A. M. et al. Quantitative mass spectral evidence for the absence of circulating brain natriuretic peptide (BNP-32) in severe human heart failure. Proc. Natl Acad. Sci. USA 102, 17442-17447 (2005).
146. Niederkofler, E. E. et al. Detection of endogenous B-type natriuretic peptide at very low concentrations in patients with heart failure. Circ. Heart Fail. 1, 258-264 (2008).
147. Miller, W. L. et al. Comparison of mass spectrometry and clinical assay measurements of circulating fragments of B-type natriuretic peptide in patients with chronic heart failure. Circ. Heart Fail. 4, 355-360 (2011).
148. Sodi, R., Dubuis, E., Shenkin, A. & Hart, G. B-type natriuretic peptide (BNP) attenuates the L-type calcium current and regulates ventricular myocyte function. Regul. Pept. 151, 95-105 (2008).
149. Murthy, K. S. & Makhlouf, G. M. Identification of the G protein-activating domain of the natriuretic peptide clearance receptor (NPR-C). J. Biol. Chem. 274, 17587-17592 (1999).
150. Cao, L. & Gardner, D. G. Natriuretic peptides inhibit DNA synthesis in cardiac fibroblasts. Hypertension 25, 227-234 (1995).
151. Tokudome, T. et al. 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 (2004).
152. Horio, T. et al. Inhibitory regulation of hypertrophy by endogenous atrial natriuretic peptide in cultured cardiac myocytes. Hypertension 35, 19-24 (2000).
153. Fujita, S. et al. Atrial natriuretic peptide exerts protective action against angiotensin II-induced cardiac remodeling by attenuating inflammation via endothelin-1/endothelin receptor A cascade. Heart Vessels 28, 646-657 (2013).
154. Yasoda, A. et al. Natriuretic peptide regulation of endochondral ossification. Evidence for possible roles of the C-type natriuretic peptide/guanylyl cyclase-B pathway. J. Biol. Chem. 273, 11695-11700 (1998).
155. Mericq, V., Uyeda, J. A., Barnes, K. M., De Luca, F. & Baron, J. Regulation of fetal rat bone growth by C-type natriuretic peptide and cGMP. Pediatr. Res. 47, 189-193 (2000).
156. Chusho, H. et al. Dwarfism and early death in mice lacking C-type natriuretic peptide. Proc. Natl Acad. Sci. USA 98, 4016-4021 (2001).
157. Bartels, C. F. et al. Mutations in the transmembrane natriuretic peptide receptor NPR-B impair skeletal growth and cause acromesomelic dysplasia, type Maroteaux. Am. J. Hum. Genet. 75, 27-34 (2004).
158. Middendorff, R., Müller, D., Paust, H. J., Holstein, A. F. & Davidoff, M. S. New aspects of Leydig cell function. Adv. Exp. Med. Biol. 424, 125-138 (1997).
159. Middendorff, R. et al. Multiple roles of the messenger molecule cGMP in testicular function. Andrologia 32, 55-59 (2000).
160. Carvajal, J. A., Aguan, K., Thompson, L. P., Buhimschi, I. A. & Weiner, C. P. Natriuretic peptide-induced relaxation of myometrium from the pregnant guinea pig is not mediated by guanylate cyclase activation. J. Pharmacol. Exp. Ther. 297, 181-188 (2001).