Journal of the American Society of Hypertension
Volume 2, Issue 4 , Pages 210-226 , July 2008

Emerging roles of natriuretic peptides and their receptors in pathophysiology of hypertension and cardiovascular regulation

  • Kailash N. Pandey, PhD

      Affiliations

    • Corresponding Author InformationCorresponding author: Kailash N. Pandey, PhD, Department of Physiology SL39, Tulane University School of Medicine, 1430 Tulane Avenue, New Orleans, Louisiana 70112. Tel: 504-988-1628; fax: 504-988-2675.

Received 29 December 2007 ,Accepted 6 February 2008.

References 

  1. De Bold AJ, Borenstein HB, Veress AT, Sonnenberg H. A rapid and potent natriuretic response to intravenous injection of atrial myocardial extract in rats. Life Sci. 1981;28:89–94
  2. Drewett JG, Garbers DL. The family of guanylyl cyclase receptors and their ligands. Endocr Rev. 1994;15:135–162
  3. Brenner BM, Ballermann BJ, Gunning ME, Zeidel ML. Diverse biological actions of atrial natriuretic peptide. Physiol Rev. 1990;70:665–699
  4. McGrath MF, de Bold ML, de Bold AJ. The endocrine function of the heart. Trends Endocrinol Metab. 2005;16:469–477
  5. Pandey KN. Biology of natriuretic peptides and their receptors. Peptides. 2005;26:901–932
  6. LaPointe MC. Molecular regulation of the brain natriuretic peptide gene. Peptides. 2005;26:944–956
  7. Schulz S. C-type natriuretic peptide and guanylyl cyclase B-receptor. Peptides. 2005;26:1024–1034
  8. Schulz S, Singh S, Bellet RA, Singh G, Tubb DJ, Chin H, et al. The primary structure of a plasma membrane guanylate cyclase demonstrates diversity within this new receptor family. Cell. 1989;58:1155–1162
  9. Pandey KN, Singh S. Molecular cloning and expression of murine guanylate cyclase/atrial natriuretic factor receptor cDNA. J Biol Chem. 1990;265:12342–12348
  10. Koller KJ, Goddel DV. Molecular biology of the natriuretic peptides and their receptors. Circulation. 1992;86:1081–1088
  11. Kuhn M. Cardiac and intestinal natriuretic peptides: insights from genetically modified mice. Peptides. 2005;26:1078–1085
  12. Vollmer AM. The role of atrial natriuretic peptide in the immune system. Peptides. 2005;26:1087–1094
  13. De Bold AJ. Atrial natriuretic factor a hormone produced by the heart. Science. 1985;230:767–770
  14. Rosenzweig A, Seidman CE. Atrial natriuretic factor and related peptide hormones. Annu Rev Biochem. 1991;60:229–255
  15. Koller KJ, de Sauvage FJ, Lowe DG, Goeddel DV. Conservation of the kinase-like regulatory domain is essential for activation of the natriuretic peptide receptor guanylyl cyclases. Mol Cell Biol. 1992;12:2581–2590
  16. Maki M, Takayanagi R, Misono K, Pandey KN, Tibbetts C, Inagami T. Structure of rat atrial natriuretic factor precursor deduced from cDNA sequence. Nature. 1984;309:722–724
  17. Sudoh T, Minamino N, Kangawa K, Matsuo H. Brain natriuretic peptide-32: N-terminal six amino acid extended form of brain natriuretic peptide identified in porcine brain. Biochem Biophys Res Commun. 1988;155:726–732
  18. 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. 1990;168:863–870
  19. Phillips RA, Ardeljan M, Shimabukuro S, Goldman ME, Garbowit DL, Eison HB, et al. Normalization of left ventricular mass and associated changes in neurohormones and atrial natriuretic peptide after 1 year of sustained nifedipine therapy for severe hypertension. J Am Coll Cardiol. 1991;17:1595–1602
  20. Suga S, Nakao K, Hosoda K, Mukoyama M, Ogawa Y, Shirakami G, et al. Phenotype-related alteration in expression of natriuretic peptide receptors in aortic smooth muscle cells. Circ Res. 1992;71:34–39
  21. Stasch JP, Kazda S. Endothelin-1-induced vascular contractions: interactions with drugs affecting the calcium channel. J Cardiovasc Pharmacol. 1989;5:S63–S66discussion S74
  22. Soualmia H, Barthelemy C, Masson F, Maistre G, Eurin J, Carayon A. Angiotensin II-induced phosphoinositide production and atrial natriuretic peptide release in rat atrial tissue. J Cardiovasc Pharmacol. 1997;29:605–611
  23. Lachance D, Garcia R, Gutkowska J, Cantin M, Thibault G. Mechanisms of release of atrial natriuretic factor (I. Effect of several agonists and steroids on its release by atrial minces). Biochem Biophys Res Commun. 1986;135:1090–1098
  24. Thibault G, Amiri F, Garcia R. Regulation of natriuretic peptide secretion by the heart. Annu Rev Physiol. 1999;61:193–217
  25. McGrath MF, de Bold AJ. Determinants of natriuretic peptide gene expression. Peptides. 2005;26:933–943
  26. Seilhamer JJ, Arfsten A, Miller JA, Lundquist P, Scarborough RM, Lewicki JA, et al. Human and canine gene homologs of porcine brain natriuretic peptide. Biochem Biophys Res Commun. 1989;165:650–658
  27. Chan JC, Knudson O, Wu F, Morser J, Dole WP, Wu Q. Hypertension in mice lacking the proatrial natriuretic peptide convertase corin. Proc Natl Acad Sci U S A. 2005;102:785–790
  28. 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 U S A. 2000;97:8525–8529
  29. Kojima M, Minamino N, Kangawa K, Matsuo H. Cloning and sequence analysis of cDNA encoding a precursor for rat brain natriuretic peptide. Biochem Biophys Res Commun. 1989;159:1420–1426
  30. Mukoyama M, Nakao K, Hosoda K, Suga S, Saito Y, Ogawa Y, et al. Brain natriuretic peptide as a novel cardiac hormone in humans: evidence for an exquisite dual natriuretic peptide system, ANP and BNP. J Clin Invest. 1991;87:1402–1412
  31. Grepin C, Dagnino L, Robitaille L, Haberstroh L, Antakly T, Nemer M. A hormone-encoding gene identifies a pathway for cardiac but not skeletal muscle gene transcription. Mol Cell Biol. 1994;14:3115–3129
  32. Thuerauf DJ, Hanford DS, Glembotski CC. Regulation of rat brain natriuretic peptide transcription (A potential role for GATA-related transcription factors in myocardial cell gene expression). J Biol Chem. 1994;269:17772–17775
  33. Yoshimura M, Yasue H, Morita E, Sakaino N, Jougasaki M, Kurose M, et al. Hemodynamic renal and hormonal responses to brain natriuretic peptide infusion in patients with congestive heart failure. Circulation. 1991;84:1581–1588
  34. Omland T, Aakvaag A, Banarjee V, Caidahl K, Lie R, Nilsen D, et al. Plasma brain natriuretic peptide as an indicator of left ventricular systolic function and long-term survival after acute myocardial infarction: comparison with plasma atrial natriuretic peptide and N-terminal proatrial natriuretic peptide. Circulation. 1996;93:1963–1969
  35. Gardner D, Deschepper C, Ganong W, Hane S, Fiddes J, Baxter J, et al. Extra atrial expression of the gene for atrial natriuretic factor. Proc Natl Acad Sci U S A. 1986;83:6697–6701
  36. Cameron V, Aitken G, Ellmers L, Kennedy M, Espiner E. The sites of gene expression of atrial, brain, and C-type natriuretic peptides in mouse fetal development: temporal changes in embryos and placenta. Endocrinology. 1996;137:817–824
  37. Larsen TH, Saetersdal T. Regional appearance of atrial natriuretic peptide in the ventricles of infarcted rat hearts. Virchows Arch B Cell Pathol Incl Mol Pathol. 1993;64:309–314
  38. Glembotski CC. Cellular and molecular biology of B-type natriuretic peptide. In:  Samson WK,  Levin ER editor. Contemporary endocrinology: natriuretic peptides in health and disease. Totowa, New Jersey: Humana Press; 1997;p. 95–106
  39. Igaki T, Itoh H, Suga S, Hama N, Ogawa Y, Komatsu Y, et al. C-type natriuretic peptide in chronic renal failure and its action in humans. Kidney Int. 1996;49:S144–S147
  40. Ogawa Y, Nakao K, Nakagawa O, Komatsu Y, Hosoda K, Suga S, et al. Human C-type natriuretic peptide characterization of the gene and peptide. Hypertension. 1992;19:809–813
  41. Suga S, Itoh H, Komatsu Y, Ogawa Y, Hama N, Yoshimasa T, et al. Cytokine-induced C-type natriuretic peptide (CNP) secretion from vascular endothelial cells -evidence for CNP as a novel autocrine/paracrine regulator from endothelial cells. Endocrinology. 1993;133:3038–3041
  42. Suga S, Nakao K, Itoh H, Komatsu Y, Ogawa Y, Hama N, 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. 1992;90:1145–1149
  43. Tamura N, Ogawa Y, Yasoda A, Itoh H, Saito Y, Nakao K. Two cardiac natriuretic peptide genes (atrial natriuretic peptide and brain natriuretic peptide) are organized in tandem in the mouse and human genomes. J Mol Cell Cardiol. 1996;28:1811–1815
  44. Chen HH, Burnett JC. C-type natriuretic peptide, the endothelial component of the natriuretic peptide system. J Cardiovasc Pharmacol. 1998;32:S22–S28
  45. Hagiwara H, Sakaguchi H, Itakura M, Yoshimoto T, Furuya M, Tanaka S, et al. Autocrine regulation of rat chondrocyte proliferation by natriuretic peptide C and its receptor, natriuretic peptide receptor-B. J Biol Chem. 1994;269:10729–10733
  46. Wu C, Wu F, Pan J, Morser J, Wu Q. Furin-mediated processing of Pro-C-type natriuretic peptide. J Biol Chem. 2003;278:25847–25852
  47. Chun TH, Itoh H, Ogawa Y, Tamura N, Takaya K, Igaki T, et al. Shear stress augments expression of C-type natriuretic peptide and adrenomedullin. Hypertension. 1997;29:1296–1302
  48. Schweitz H, Vigne P, Moinier D, Frelin CH, Lazdunski M. A new member of the natriuretic peptide family is present in the venom of the green mamba (Dendroaspis angusticeps). J Biol Chem. 1992;267:13928–13932
  49. Lisy O, Jougasaki M, Heublein DM, Schirger JA, Chen HH, Wennberg PW, et al. Renal actions of synthetic Dendrocespis natriuretic pepide. Kidney Int. 1999;56:502–508
  50. Schulz-Knappe P, Forssmann K, Herbst F, Hock D, Pipkorn R, Forssmann WD. Isolation and structural analysis of urodilatin, a new peptide of the cardiodilatin (ANP)-family extracted from human urine. Klin Wochenschr. 1988;66:752–759
  51. Feller SM, Mägert HJ, Schulz-Knappe P, Forssmann WG. Urodilatin (hANF 95-126)-characteristics of a new atrial natriuretic factor peptide. In:  Struthers AD editors. Atrial natriuretic factor. Oxford: United Kingdom Blackwell; 1990;p. 209–226
  52. Goetz KL. Renal natriuretic peptide (urodilatin?) and atriopeptin: evolving concepts. Am J Physiol. 1991;261:F921–F932
  53. Saxenhofer H, Roselli A, Weidmann P, Forssmann WG, Bub A, Ferrari P, et al. Urodilatin, a natriuretic factor from kidneys can modify renal and cardiovascular function in men. Am J Physiol. 1990;259:F832–F838
  54. Emmeluth C, Drummer C, Gerzer R, Bie P. Roles of cephalic Na+ concentration and urodilatin in control of renal Na+ excretion. Am J Physiol. 1992;262:F513–F516
  55. Forssmann WG, Meyer M, Schulz-Knappe P. Urodilatin from cardiac hormones to clinical trials. Exp Nephrol. 1994;2:318–323
  56. Meyer M, Richter R, Brunkhorst R, Wrenger E, Schulz-Knappe P, Kist A, et al. Urodilatin is involved in sodium homeostasis and exerts sodium-state dependent natriuretic and diuretic effects. Am J Physiol. 1996;271:489–497
  57. Lowe DG, Chang M-S, Hellmiss R, Chen E, Singh S, Garbers DL, et al. Human atrial natriuretic peptide receptor defines a new paradigm for second messenger signal transduction. EMBO J. 1989;8:1377–1384
  58. Fuller F, Porter JG, Arfsten AE, Miller J, Schilling JW, Scarborough RM, et al. Atrial natriuretic peptide clearance receptor (Complete sequence and functional expression of cDNA clones). J Biol Chem. 1988;263:9395–9401
  59. Garbers DL. Guanylyl cyclase receptors and their endocrine, paracrine, and autocrine ligands. Cell. 1992;71:1–4
  60. Van den Akker F, Zhang X, Miyagi M, Huo X, Misono KS, Yee VC. Structure of the dimerized hormone-binding domain of a guanylyl-cyclase-coupled receptor. Nature. 2000;406:101–104
  61. Wilson EM, Chinkers M. Identification of sequences mediating guanylyl cyclase dimerization. Biochemistry. 1995;34:4696–4701
  62. Labrecque J, McNicoll N, Marquis M, De Lean A. A disulfide-bridged mutant of natriuretic peptide receptor-A displays constitutive activity (Role of receptor dimerization in signal transduction). J Biol Chem. 1999;274:9752–9759
  63. Garbers DL, Lowe DG. Guanylyl cyclase receptors. J Biol Chem. 1994;269:30741–30744
  64. Misono KS, Ogawa H, Qiu Y, Ogata CM. Structural studies of the natriuretic peptide receptor: a novel hormone-induced rotation mechanism for transmembrane signal transduction. Peptides. 2005;26:957–968
  65. Lucas KA, Pitari GM, Kazerounian S, Ruiz-Stewart I, Park J, Schulz S, et al. Guanylyl cyclases and signaling by cyclic GMP. Pharmacol Rev. 2000;52:375–414
  66. Koller KJ, Lowe DG, Bennett GL, Minamino N, Kangawa K, Matsuo H, et al. Selective activation of the B natriuretic peptide receptor by C-type natriuretic peptide (CNP). Science. 1991;252:120–123
  67. Bovy PR. Structure activity in the atrial natriuretic peptide (ANP) family. Med Res Rev. 1990;10:115–142
  68. Maack T, Suzuki M, Almeida FA, Nussenzveig D, Scarborough RM, McEnroe GA, et al. Physiological role of silent receptors of atrial natriuretic factor. Science. 1987;238:675–678
  69. Anand-Srivastava MB, Trachte GJ. Atrial natriuretic factor receptors and signal transduction mechanisms. Pharmacol Rev. 1993;45:455–497
  70. Zhou H, Murthy KS. Identification of the G-protein activation sequence of the single-transmembrane natriuretic peptide receptor C (NPR-C). Am J Physiol Cell Physiol. 2003;284:C1255–C1261
  71. Hamet P, Tremblay J, Pang SC, Garcia R, Thibault G, Gutkowska J, et al. Effect of native and synthetic atrial natriuretic factor on cyclic GMP. Biochem Biophys Res Commun. 1984;123:515–527
  72. Waldman SA, Rapoport RM, Murad F. Atrial natriuretic factor selectively activates particulate guanylate cyclase and elevates cyclic GMP in rat tissues. J Biol Chem. 1984;259:14332–14334
  73. Pandey KN, Kovacs WJ, Inagami T. The inhibition of progesterone secretion and the regulation of cyclic nucleotides by atrial natriuretic factor in gonadotropin responsive murine Leydig tumor cells. Biochem Biophys Res Commun. 1985;133:800–806
  74. Tremblay J, Gerzer R, Vinay P, Pang SC, Beliveau R, Hamet P. The increase of cGMP by atrial natriuretic factor correlates with the distribution of particulate guanylate cyclase. FEBS Lett. 1985;181:17–22
  75. Pandey KN. Stoichiometric analysis of internalization, recycling, and redistribution of photoaffinity-labeled guanylate cyclase/atrial natriuretic factor receptors in cultured murine Leydig tumor cells. J Biol Chem. 1993;268:4382–4390
  76. Potter LR, Garbers DL. Protein kinase C-dependent desensitization of the atrial natriuretic peptide receptor is mediated by dephosphorylation. J Biol Chem. 1994;269:14636–14642
  77. Pandey KN. Intracellular trafficking and metabolic turnover of ligand-bound guanylyl cyclase/atrial natriuretic peptide receptor-A into subcellular compartments. Mol Cell Biochem. 2002;230:61–72
  78. Sharma RK. Evolution of the membrane guanylate cyclase transduction system. Mol Cell Biochem. 2002;230:3–30
  79. Huo X, Abe T, Misono KS. Ligand binding-dependent limited proteolysis of the atrial natriuretic peptide receptor: juxtamembrane hinge structure essential for transmembrane signal transduction. Biochemistry. 1999;38:16941–16951
  80. Chinkers M, Singh S, Garbers DL. Adenine nucleotides are required for activation of rat atrial natriuretic peptide receptor/guanylyl cyclase expressed in a baculovirus system. J Biol Chem. 1991;266:4088–4093
  81. Goraczniak RM, Duda T, Sharma RK. A structural motif that defines the ATP-regulatory module of guanylate cyclase in atrial natriuretic factor signalling. Biochem J. 1992;282:533–537
  82. Kurose H, Inagami T, Ui M. Participation of adenosine 5'-triphosphate in the activation of membrane-bound guanylate cyclase by the atrial natriuretic factor. FEBS Lett. 1987;219:375–379
  83. Chang CH, Kohse KP, Chang B, Hirata M, Jiang B, Douglas JE, et al. Characterization of ATP-stimulated guanylate cyclase activation in rat lung membranes. Biochim Biophys Acta. 1990;1052:159–165
  84. Duda T, Goraczniak RM, Sharma RK. Site-directed mutational analysis of a membrane guanylate cyclase cDNA reveals the atrial natriuretic factor signaling site. Proc Natl Acad Sci U S A. 1991;88:7882–7886
  85. Gazzano H, Wu HI, Waldman SA. Adenine nucleotide regulation of particulate guanylate cyclase from rat lung. Biochim Biophys Acta. 1991;1077:99–106
  86. Larose L, McNicoll N, Ong H, De Lean A. Allosteric modulation by ATP of the bovine adrenal natriuretic factor R1 receptor functions. Biochemistry. 1991;30:8990–8995
  87. Wong SK, Ma CP, Foster DC, Chen AY, Garbers DL. The guanylyl cyclase-A receptor transduces an atrial natriuretic peptide/ATP activation signal in the absence of other proteins. J Biol Chem. 1995;270:30818–30822
  88. Duda T, Goraczniak RM, Sharma RK. The glycine residue of ATP regulatory module in receptor guanylate cyclases that is essential in natriuretic factor signaling. FEBS Lett. 1993;335:309–314
  89. Duda T, Venkataraman V, Ravichandran S, Sharma RK. ATP-regulated module (ARM) of the atrial natriuretic factor receptor guanylate cyclase. Peptides. 2005;26:969–984
  90. Chinkers M, Garbers DL, Chang MS, Lowe DG, Chin HM, Goeddel DV, et al. A membrane form of guanylate cyclase is an atrial natriuretic peptide receptor. Nature. 1989;338:78–83
  91. Van den Akker F. Structural insights into the ligand binding domains of membrane bound guanylyl cyclases and natriuretic peptide receptors. J Mol Biol. 2001;311:923–937
  92. Fenrick R, Bouchard N, McNicoll N, De Lean A. Glycosylation of asparagine 24 of the natriuretic peptide receptor-B is crucial for the formation of a competent ligand binding domain. Mol Cell Biochem. 1997;173:25–32
  93. Fenrick R, McNicoll N, De Lean A. Glycosylation is critical for natriuretic peptide receptor-B function. Mol Cell Biochem. 1996;165:103–109
  94. Lowe DG, Fendly BM. Human natriuretic peptide receptor-A guanylyl cyclase (Hormone cross-linking and antibody reactivity distinguish receptor glycoforms). J Biol Chem. 1992;267:21691–21697
  95. Heim JM, Singh S, Gerzer R. Effect of glycosylation on cloned ANF-sensitive guanylyl cyclase. Life Sci. 1996;59:PL61–PL68
  96. Koller KJ, Lipari MT, Goeddel DV. Proper glycosylation and phosphorylation of the type A natriuretic peptide receptor are required for hormone-stimulated guanylyl cyclase activity. J Biol Chem. 1993;268:5997–6003
  97. Pfeifer A, Klatt P, Massberg S, Ny L, Sausbier M, Hirneiss C, et al. Defective smooth muscle regulation in cGMP kinase I-deficient mice. EMBO J. 1998;17:3045–3051
  98. Kaupp UB, Seifert R. Cyclic nucleotide-gated ion channels. Physiol Rev. 2002;82:769–824
  99. Maurice DH, Palmer D, Tilley DG, Dunkerley HA, Netherton SJ, Raymond DR, et al. Cyclic nucleotide phosphodiesterase activity, expression, and targeting in cells of the cardiovascular system. Mol Pharmacol. 2003;64:533–546
  100. Rybalkin SD, Yan C, Bornfeldt KE, Beavo JA. Cyclic GMP phosphodiesterases and regulation of smooth muscle function. Circ Res. 2003;93:280–291
  101. Schlossmann J, Feil R, Hofmann F. Insights into cGMP signaling derived from cGMP kinase knockout mice. Front Biosci. 2005;10:1279–1289
  102. Shi SJ, Vellaichamy E, Chin SY, Smithies O, Navar LG, Pandey KN. Natriuretic peptide receptor A mediates renal sodium excretory responses to blood volume expansion. Am J Physiol Renal Physiol. 2003;285:F694–F702
  103. Levin ER, Gardner DG, Samson WK. Natriuretic peptides. N Engl J Med. 1998;339:321–328
  104. Cermak R, Kleta R, Forssmann WG, Schlatter E. Natriuretic peptides increase a K+ conductance in rat mesangial cells. Pflugers Arch. 1996;431:571–577
  105. Kremer S, Troyer D, Kreisberg J, Skorecki K. Interaction of atrial natriuretic peptide-stimulated guanylate cyclase and vasopressin-stimulated calcium signaling pathways in the glomerular mesangial cell. Arch Biochem Biophys. 1988;260:763–770
  106. Light DB, Schwiebert EM, Karlson KH, Stanton BA. Atrial natriuretic peptide inhibits a cation channel in renal inner medullary collecting duct cells. Science. 1989;243:383–385
  107. Nonoguchi H, Knepper MA, Manganiello VC. Effects of atrial natriuretic factor on cyclic guanosine monophosphate and cyclic adenosine monophosphate accumulation in microdissected nephron segments from rats. J Clin Invest. 1987;79:500–507
  108. Pandey KN, Kumar R, Li M, Nguyen H. Functional domains and expression of truncated atrial natriuretic peptide receptor-A: the carboxyl-terminal regions direct the receptor internalization and sequestration in COS-7 cells. Mol Pharmacol. 2000;57:259–267
  109. Appel RG. Mechanism of atrial natriuretic factor-induced inhibition of rat mesangial cell mitogenesis. Am J Physiol. 1990;259:E312–E318
  110. Appel RG. Growth-regulatory properties of atrial natriuretic factor. Am J Physiol. 1992;262:F911–F918
  111. Von Geldern TW, Budzik GP, Dillon TP, Holleman WH, Holst MA, Ksio Y, et al. Atrial natriuretic peptide antagonists (Biological evaluation and structural correlations). Mol Pharmacol. 1990;38:771–778
  112. Sano T, Morishita Y, Matsuda Y, Yamada K. Pharmacological profile of HS-142-1, a novel nonpeptide atrial natriuretic peptide antagonist of microbial origin I (Selective inhibition of the actions of natriuretic peptides in anesthetized rats). J Pharmacol Exp Ther. 1992;260:825–831
  113. Burnett JC, Granger JP, Opgenorth TJ. Effects of synthetic atrial natriuretic factor on renal function and renin release. Am J Physiol. 1984;247:F863–F866
  114. Kurtz A, Della Bruna R, Pfeilschifter J, Taugner R, Bauer C. Atrial natriuretic peptide inhibits renin release from juxtaglomerular cells by a cGMP-mediated process. Proc Natl Acad Sci U S A. 1986;83:4769–4773
  115. Melo LG, Veress AT, Chong CK, Pang SC, Flynn TG, Sonnenberg H. Salt-sensitive hypertension in ANP knockout mice: potential role of abnormal plasma renin activity. Am J Physiol. 1998;274:R255–R261
  116. Olson LJ, Lowe DG, Drewett JG. Novel natriuretic peptide receptor/guanylyl cyclase A-selective agonist inhibits angiotensin II- and forskolin-evoked aldosterone synthesis in a human zona glomerulosa cell line. Mol Pharmacol. 1996;50:430–435
  117. Shi SJ, Nguyen HT, Sharma GD, Navar LG, Pandey KN. Genetic disruption of atrial natriuretic peptide receptor-A alters renin and angiotensin II levels. Am J Physiol. 2001;281:F665–F673
  118. Meyer M, Forsmann WG. Renal actions of atrial natriuretic peptide. In:  Samson WK,  Levin ER editor. Contemporary endocrinology: natriuretic peptides in health and disease. Totawa, New Jersey: Humana Press; 1997;p. 147–170
  119. Paul RV, Ferguson T, Navar LG. ANF secretion and renal responses to volume expansion with equilibrated blood. Am J Physiol. 1988;255:F936–F943
  120. Ohyama Y, Miyamoto R, Morishita Y, Matsuda Y, Saito Y, Minamino N, et al. Stable expression of natriuretic peptide receptors effects of HS-142-1, a non-peptide ANP antagonist. Biochem Biophys Res Commun. 1992;189:336–342
  121. Delporte C, Poloczek P, Tastenoy M, Winard J, Christopher J. Atrial natriuretic peptide binds to ANP-R 1 receptors in neuroblastoma cells or is degraded extracellularly at the Ser-Phe bond. Eur J Pharmacol. 1992;227:247–256
  122. Kumar R, von Geldern TW, Calle RA, Pandey KN. Stimulation of atrial natriuretic peptide receptor/guanylyl cyclase-A signaling pathway antagonizes the activation of protein kinase C-alpha in murine Leydig cells. Biochim Biophys Acta. 1997;1356:221–228
  123. Khurana ML, Pandey KN. Receptor-mediated stimulatory effect of atrial natriuretic factor, brain natriuretic peptide, and C-type natriuretic peptide on testosterone production in purified mouse Leydig cells: activation of cholesterol side-chain cleavage enzyme. Endocrinology. 1993;133:2141–2149
  124. Misono KS. Atrial natriuretic factor binding to its receptor is dependent on chloride concentration: a possible feedback control mechanism in renal salt regulation. Circ Res. 2000;86:1135–1139
  125. Melo LG, Veress AT, Ackermann U, Steinhelper ME, Pang SC, Tse Y, et al. Chronic regulation of arterial blood pressure in ANP transgenic and knockout mice: role of cardiovascular sympathetic tone. Cardiovasc Res. 1999;43:437–444
  126. Zhao D, Vellaichamy E, Somanna NK, Pandey KN. Guanylyl cyclase/natriuretic peptide receptor-A gene disruption causes increased adrenal angiotensin II and aldosterone levels. Am J Physiol Renal Physiol. 2007;293:F121–F127
  127. Pandey KN. Vascular action natriuretic peptide receptor. In:  Sowers JR editors. Contemporary endocrinology: endocrinology of the vasculature. Totawa, New Jersey: Humana Press; 1996;p. 255–267
  128. Cao L, Wu J, Gardner DG. Atrial natriuretic peptide suppresses the transcription of its guanylyl cyclase-linked receptor. J Biol Chem. 1995;270:24891–24897
  129. Dey NB, Boerth NJ, Murphy-Ullrich JE, Chang PL, Prince CW, Lincoln TM. Cyclic GMP-dependent protein kinase inhibits osteopontin and thrombospondin production in rat aortic smooth muscle cells. Circ Res. 1998;82:139–146
  130. Kumar R, Cartledge WA, Lincoln TM, Pandey KN. Expression of guanylyl cyclase-A/atrial natriuretic peptide receptor blocks the activation of protein kinase C in vascular smooth muscle cells (Role of cGMP and cGMP-dependent protein kinase). Hypertension. 1997;29:414–421
  131. Hassid A. Atriopeptin II decreases cytosolic free Ca in cultured vascular smooth muscle cells. Am J Physiol. 1986;251:C681–C686
  132. Lincoln TM, Dey N, Sellak H. Invited review: cGMP-dependent protein kinase signaling mechanisms in smooth muscle: from the regulation of tone to gene expression. J Appl Physiol. 2001;91:1421–1430
  133. Lincoln TM, Komalavilas P, Cornwell TL. Pleiotropic regulation of vascular smooth muscle tone by cyclic GMP-dependent protein kinase. Hypertension. 1994;23:1141–1147
  134. Rashatwar SS, Cornwell TL, Lincoln TM. Effect of 8-bromo cGMP on Ca2+-ATPase by cGMP dependent protein kinase. Proc Natl Acad Sci U S A. 1987;84:5685–5689
  135. Cornwell TL, Lincoln TM. Regulation of intracellular Ca2+ levels in cultured vascular smooth muscle cells (Reduction of Ca2+ by atriopeptin and 8-bromo-cyclic GMP is mediated by cyclic GMP-dependent protein kinase). J Biol Chem. 1989;264:1146–1155
  136. Rho EH, Perkins WJ, Lorenz RR, Warner DO, Jones KA. Differential effects of soluble and particulate guanylyl cyclase on Ca(2+) sensitivity in airway smooth muscle. J Appl Physiol. 2002;92:257–263
  137. Sharma GD, Nguyen HT, Antonov AS, Gerrity RG, von Geldern T, Pandey KN. Expression of atrial natriuretic peptide receptor-A antagonizes the mitogen-activated protein kinases (Erk2 and P38MAPK) in cultured human vascular smooth muscle cells. Mol Cell Biochem. 2002;233:165–173
  138. Melo LG, Veress AT, Chong CK, Pang SC, Flynn TG, Sonnenberg H. Salt-sensitive hypertension in ANP knockout mice: potential role of abnormal plasma renin activity. Am J Physiol. 1998;274:R255–R261
  139. John SW, Krege JH, Oliver PM, Hagaman JR, Hodgin JB, Pang SC, et al. Genetic decreases in atrial natriuretic peptide and salt-sensitive hypertension. Science. 1995;267:679–681
  140. Melo LG, Steinhelper ME, Pang SC, Tse Y, Ackermann U. ANP in regulation of arterial pressure and fluid-electrolyte balance: lessons from genetic mouse models. Physiol Genomics. 2000;3:45–58
  141. Steinhelper ME, Cochran KL, Field LJ. Hypotension in transgenic mice expressing atrial natriuretic factor fusion genes. Hypertension. 1990;16:301–307
  142. Lin X, Hanze J, Heese F, Sodmann R, Lang RE. Gene expression of natriuretic peptide receptors in myocardial cells. Circ Res. 1995;77:750–758
  143. Franco V, Chen YF, Oparil S, Feng JA, Wang D, Hage F, et al. Atrial natriuretic peptide dose-dependently inhibits pressure overload-induced cardiac remodeling. Hypertension. 2004;44:746–750
  144. Richards AM. Natriuretic peptides: update on peptide release, bioactivity, and clinical use. Hypertension. 2007;50:25–30
  145. Wang D, Oparil S, Feng JA, Li P, Perry G, Chen LB, et al. Effects of pressure overload on extracellular matrix expression in the heart of the atrial natriuretic peptide-null mouse. Hypertension. 2003;42:88–95
  146. Pandey KN, Oliver PM, Maeda N, Smithies O. Hypertension associated with decreased testosterone levels in natriuretic peptide receptor-A gene-knockout and gene-duplicated mutant mouse models. Endocrinology. 1999;140:5112–5119
  147. Holtwick R, Baba HA, Ehler E, Risse D, Vobeta M, Gehrmann J, et al. Left but not right cardiac hypertrophy in atrial natriuretic peptide receptor-deficient mice is prevented by angiotensin type 1 receptor antagonist losartan. J Cardiovasc Pharmacol. 2002;40:725–734
  148. Holtwick R, Gotthardt M, Skryabin B, Steinmetz M, Potthast R, Zetsche B, et al. Smooth muscle-selective deletion of guanylyl cyclase-A prevents the acute but not chronic effects of ANP on blood pressure. Proc Natl Acad Sci U S A. 2002;99:7142–7147
  149. Kishimoto I, Dubois SK, Garbers DL. The heart communicates with the kidney exclusively through the guanylyl cyclase-A receptor: acute handling of sodium and water in response to volume expansion. Proc Natl Acad Sci U S A. 1996;93:6215–6219
  150. Lopez MJ, Wong SK, Kishimoto I, Dubois S, Mach V, Friesen J, et al. Salt-resistant hypertension in mice lacking the guanylyl cyclase-A receptor for atrial natriuretic peptide. Nature. 1995;378:65–68
  151. Oliver PM, Fox JE, Kim R, Rockman HA, Kim HS, Reddick RL, et al. Hypertension, cardiac hypertrophy, and sudden death in mice lacking natriuretic peptide receptor A. Proc Natl Acad Sci U S A. 1997;94:14730–14735
  152. Oliver PM, John SW, Purdy KE, Kim R, Maeda N, Goy MF, et al. Natriuretic peptide receptor 1 expression influences blood pressures of mice in a dose-dependent manner. Proc Natl Acad Sci U S A. 1998;95:2547–2551
  153. Knowles JW, Esposito G, Mao L, Hagaman JR, Fox JE, Smithies O, et al. Pressure-independent enhancement of cardiac hypertrophy in natriuretic peptide receptor A-deficient mice. J Clin Invest. 2001;107:975–984
  154. Vellaichamy E, Zhao D, Somanna N, Pandey KN. Genetic disruption of guanylyl cyclase/natriuretic peptide receptor-A upregulates ACE and AT1 receptor gene expression and signaling: role in cardiac hypertrophy. Physiol Genomics. 2007;31:193–202
  155. Zhao L, Long L, Morrell NW. NPRA-deficient mice show increased susceptibility to hypoxia-induced pulmonary hypertension. Circulation. 1999;99:605–607
  156. Vellaichamy E, Khurana ML, Fink J, Pandey KN. Involvement of the NF-kappa B/matrix metalloproteinase pathway in cardiac fibrosis of mice lacking guanylyl cyclase/natriuretic peptide receptor A. J Biol Chem. 2005;280:19230–19242
  157. Atarashi K, Mulrow PJ, Franco-Saenz R, Snajdar R, Rapp J. Inhibition of aldosterone production by an atrial extract. Science. 1984;224:992–994
  158. Antunes-Rodrigues J, Machado BH, Andrade HA, Mauad H, Ramalho MJ, Reis LC, et al. Carotid aortic and renal baroreceptors mediate the atrial natriuretic peptide release induced by blood volume expansion. Proc Natl Acad Sci U S A. 1992;89:6829–6831
  159. Klinger JR, Warburton RR, Pietras L, Oliver P, Fox J, Smithies O, et al. Targeted disruption of the gene for natriuretic peptide receptor-A worsens hypoxia-induced cardiac hypertrophy. Am J Physiol Heart Circ Physiol. 2002;282:H58–H65
  160. Tamura N, Ogawa Y, Chusho H, Nakamura K, Nakao K, Suda M, et al. Cardiac fibrosis in mice lacking brain natriuretic peptide. Proc Natl Acad Sci U S A. 2000;97:4239–4244
  161. Chusho H, Tamura N, Ogawa Y, Yasoda A, Suda M, Miyazawa T, et al. Dwarfism and early death in mice lacking C-type natriuretic peptide. Proc Natl Acad Sci U S A. 2001;98:4016–4021
  162. Wang Y, de Waard MC, Sterner-Kock A, Stepan H, Schultheiss HP, Duncker DJ, et al. Cardiomyocyte-restricted over-expression of C-type natriuretic peptide prevents cardiac hypertrophy induced by myocardial infarction in mice. Eur J Heart Fail. 2007;9:548–557
  163. Tamura N, Doolittle LK, Hammer RE, Shelton JM, Richardson JA, Garbers DL. Critical roles of the guanylyl cyclase B receptor in endochondral ossification and development of female reproductive organs. Proc Natl Acad Sci U S A. 2004;101:17300–17305
  164. Tsuji T, Kunieda T. A loss-of-function mutation in natriuretic peptide receptor 2 (Npr2) gene is responsible for disproportionate dwarfism in cn/cn mouse. J Biol Chem. 2005;280:14288–14292
  165. Bartels CF, Bukulmez H, Padayatti P, Rhee DK, van Ravenswaaij-Arts C, Pauli RM, et al. Mutations in the transmembrane natriuretic peptide receptor NPR-B impair skeletal growth and cause acromesomelic dysplasia, type Maroteaux. Am J Hum Genet. 2004;75:27–34
  166. Matsukawa N, Grzesik WJ, Takahashi N, Pandey KN, Pang S, Yamauchi M, et al. The natriuretic peptide clearance receptor locally modulates the physiological effects of the natriuretic peptide system. Proc Natl Acad Sci U S A. 1999;96:7403–7408
  167. Jaubert J, Jaubert F, Martin N, Washburn LL, Lee BK, Eicher EM, et al. Three new allelic mouse mutations that cause skeletal overgrowth involve the natriuretic peptide receptor C gene (Npr3). Proc Natl Acad Sci U S A. 1999;96:10278–10283
  168. Tsutamoto T, Kanamori T, Morigami N, Sugimoto Y, Yamaoka O, Kinoshita M. Possibility of downregulation of atrial natriuretic peptide receptor coupled to guanylate cyclase in peripheral vascular beds of patients with chronic severe heart failure. Circulation. 1993;87:70–75
  169. Wei C-M, Heublein DM, Perrella MA, Lerman A, Rodeheffer RJ, McGregor CGA, et al. Natriuretic peptide system in human heart failure. Circulation. 1993;88:1004–1009
  170. Chen HH, Burnett JC. The natriuretic peptides in heart failure. Proc Assoc Am Physicians. 1999;111:406–416
  171. Reinhart K, Meisner M, Brunkhorst FM. Markers for sepsis diagnosis: what is useful?. Crit Care Clin. 2006;22:503–519ix–x
  172. Felker GM, Petersen JW, Mark DB. Natriuretic peptides in the diagnosis and management of heart failure. CMAJ. 2006;175:611–617
  173. See R, de Lemos JA. Current status of risk stratification methods in acute coronary syndromes. Curr Cardiol Rep. 2006;8:282–288
  174. Jaffe AS, Babuin L, Apple FS. Biomarkers in acute cardiac disease: the present and the future. J Am Coll Cardiol. 2006;48:1–11
  175. Yoshimura M, Yasue H, Okumura K, Ogawa H, Jougasaki M, Mukoyama M, et al. Different secretion patterns of atrial natriuretic peptide and brain natriuretic peptide in patients with congestive heart failure. Circulation. 1993;87:464–469
  176. Ellmers LJ, Knowles JW, Kim HS, Smithies O, Maeda N, Cameron VA. Ventricular expression of natriuretic peptides in Npr1(-/-) mice with cardiac hypertrophy and fibrosis. Am J Physiol Heart Circ Physiol. 2002;283:H707–H714
  177. Doust JA, Pietrzak E, Dobson A, Glasziou P. How well does B-type natriuretic peptide predict death and cardiac events in patients with heart failure: systematic review. BMJ. 2005;330–625
  178. Khan IA, Fink J, Nass C, Chen H, Christenson R, de Filippi CR. N-terminal pro-B-type natriuretic peptide and B-type natriuretic peptide for identifying coronary artery disease and left ventricular hypertrophy in ambulatory chronic kidney disease patients. Am J Cardiol. 2006;97:1530–1534
  179. Anwaruddin S, Lloyd-Jones DM, Baggish A, Chen A, Krauser D, Tung R, et al. Renal function, congestive heart failure, and amino-terminal pro-brain natriuretic peptide measurement: results from the proBNP investigation of dyspnea in the emergency Department (PRIDE) study. J Am Coll Cardiol. 2006;47:91–97
  180. McCullough PA, Duc P, Omland T, McCord J, Nowak RM, Hollander JE, et al. B-type natriuretic peptide and renal function in the diagnosis of heart failure: an analysis from the breathing not properly multinational study. Am J Kidney Dis. 2003;41:571–579
  181. Hanford DS, Glembotski CC. Stabilization of the B-type natriuretic peptide mRNA in cardiac myocytes by alpha-adrenergic receptor activation potential roles for protein kinase C and mitogen-activated protein kinase. Mol Endocrinol. 1996;10:1719–1727
  182. Hanford DS, Thuerauf DJ, Murray SF, Glembotski CC. Brain natriuretic peptide is induced by α1-adrenergic agonists as a primary response gene in cultured rat cardiac myocytes. J Biol Chem. 1994;269:26227–26233
  183. Horio T, Nishikimi T, Yoshihara F, Matsuo H, Takishita S, Kangawa K. Inhibitory regulation of hypertrophy by endogenous atrial natriuretic peptide in cultured cardiac myocytes. Hypertension. 2000;35:19–24
  184. Silberbach M, Gorenc T, Hershberger RE, Stork PJS, Steyger PS, Roberts CTJ. Extracellular signal-regulated protein kinase activation is required for the anti-hypertrophic effect of atrial natriuretic factor in neonatal rat ventricular myocytes. J Biol Chem. 1999;274:24858–24864
  185. Vellaichamy E, Sommana NK, Pandey KN. Reduced cGMP signaling activates NF-kappaB in hypertrophied hearts of mice lacking natriuretic peptide receptor-A. Biochem Biophys Res Commun. 2005;327:106–111
  186. 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
  187. Nakanishi M, Saito Y, Kishimoto I, Harada M, Kuwahara K, Takahashi N, et al. Role of natriuretic peptide receptor guanylyl cyclase-A in myocardial infarction evaluated using genetically engineered mice. Hypertension. 2005;46:441–447
  188. Angelis E, Tse MY, Adams MA, Pang SC. Effect of AT2 blockade on cardiac hypertrophy as induced by high dietary salt in the proatrial natriuretic peptide (ANP) gene-disrupted mouse. Can J Physiol Pharmacol. 2006;84:625–634
  189. Sangaralingham SJ, Tse MY, Pang SC. Estrogen protects against the development of salt-induced cardiac hypertrophy in heterozygous proANP gene-disrupted mice. J Endocrinol. 2007;194:143–152
  190. Ellmers LJ, Scott NJ, Piuhola J, Maeda N, Smithies O, Frampton CM, et al. Npr1-regulated gene pathways contributing to cardiac hypertrophy and fibrosis. J Mol Endocrinol. 2007;38:245–257
  191. Tokudome T, Horio T, Kishimoto I, Soeki T, Mori K, Kawano Y, et al. Calcineurin-nuclear factor of activated T cells pathway-dependent cardiac remodeling in mice deficient in guanylyl cyclase A, a receptor for atrial and brain natriuretic peptides. Circulation. 2005;111:3095–3104
  192. Li Y, Kishimoto I, Saito Y, Harada M, Kuwahara K, Izumi T, et al. Androgen contributes to gender-related cardiac hypertrophy and fibrosis in mice lacking the gene encoding guanylyl cyclase-A. Endocrinology. 2004;145:951–958
  193. Li Y, Kishimoto I, Saito Y, Harada M, Kuwahara K, Izumi T, et al. Guanylyl cyclase-A inhibits angiotensin II type 1A receptor-mediated cardiac remodeling, an endogenous protective mechanism in the heart. Circulation. 2002;106:1722–1728
  194. Holtwick R, van Eickels M, Skryabin BV, Baba HA, Bubikat A, Begrow F, et al. Pressure-independent cardiac hypertrophy in mice with cardiomyocyte-restricted inactivation of the atrial natriuretic peptide receptor guanylyl cyclase-A. J Clin Invest. 2003;111:1399–1407
  195. Kilic A, Bubikat A, Gassner B, Baba HA, Kuhn M. Local actions of atrial natriuretic peptide counteract angiotensin II stimulated cardiac remodeling. Endocrinology. 2007;148:4162–4169
  196. Kilic A, Velic A, De Windt LJ, Fabritz L, Voss M, Mitko D, et al. Enhanced activity of the myocardial Na+/H+ exchanger NHE-1 contributes to cardiac remodeling in atrial natriuretic peptide receptor-deficient mice. Circulation. 2005;112:2307–2317
  197. Sabrane K, Gambaryan S, Brandes RP, Holtwick R, Voss M, Kuhn M. Increased sensitivity to endothelial nitric oxide (NO) contributes to arterial normotension in mice with vascular smooth muscle-selective deletion of the atrial natriuretic peptide (ANP) receptor. J Biol Chem. 2003;278:17963–17968
  198. Sabrane K, Kruse MN, Fabritz L, Zetsche B, Mitko D, Skryabin BV, et al. Vascular endothelium is critically involved in the hypotensive and hypovolemic actions of atrial natriuretic peptide. J Clin Invest. 2005;115:1666–1674
  199. Alexander MR, Knowles JW, Nishikimi T, Maeda N. Increased atherosclerosis and smooth muscle cell hypertrophy in natriuretic peptide receptor A-/-apolipoprotein E-/- mice. Arterioscler Thromb Vasc Biol. 2003;23:1077–1082
  200. Langenickel TH, Buttgereit J, Pagel-Langenickel I, Lindner M, Monti J, Beuerlein K, et al. Cardiac hypertrophy in transgenic rats expressing a dominant-negative mutant of the natriuretic peptide receptor B. Proc Natl Acad Sci U S A. 2006;103:4735–4740
  201. Masciotra S, Picard S, Deschepper CF. Cosegregation analysis in genetic crosses suggests a protective role for atrial natriuretic factor against ventricular hypertrophy. Circ Res. 1999;84:1453–1458
  202. Deschepper CF, Masciotra S, Zahabi A, Boutin-Ganache I, Picard S, Reudelhuber TL. Function alterations of the Nppa promoter are linked to cardiac ventricular hypertrophy in WKY/WKHA rat crosses. Circ Res. 2001;88:223–228
  203. Deschepper CF. The many possible benefits of natriuretic peptides after myocardial infarction. Hypertension. 2005;46:271–272

 This study was supported by Grants from the National Institutes of Health (HL57531 and HL62147).

 Conflict of interest: none.

PII: S1933-1711(08)00013-2

doi: 10.1016/j.jash.2008.02.001

Journal of the American Society of Hypertension
Volume 2, Issue 4 , Pages 210-226 , July 2008