Structure, regulation and functions of particulate guanylyl cyclase type A
Małgorzata Mitkiewicz 1Abstract
Guanylyl cyclase type A (GC-A) belongs to the particulate guanylyl cyclases (pGC), which, like the soluble guanylyl cyclases (sGC), catalyze the synthesis of a common secondary messenger, namely cyclic GMP (cGMP), involved in many cellular processes. Although both forms of guanylyl cyclases produce the same secondary messenger, activation of each of them triggers different signaling pathways leading to different cellular effects. This indicates that the final effect of cGMP depends on the site of its synthesis in the cell (cytosol or cell membrane). Particulate guanylyl cyclase type A is a homodimeric protein activated by natriuretic peptides (ANP – atrial natriuretic peptide and BNP – brain natriuretic peptide) binding in the extracellular domain of the enzyme. The widespread expression of GC-A in different cell types and tissues suggests that this protein may regulate many cellular processes. Besides the role of GC-A in the cardiovascular system, which is the most thoroughly documented in the literature, it was observed that this protein is also involved in carcinogenesis and regulation of inflammatory reactions. This review describes important information about the structure, functions and regulation of GC-A catalytic activity, and the regulation of GC-A gene expression.
References
- 1. Ashman D.F., Lipton R., Melicow M.M., Price T.D.: Isolation of adenosine3’,5’-monophosphate and guanosine 3’,5’-monophosphatefrom rat urine. Biochem. Biophys. Res. Commun., 1963; 11: 330-334
Google Scholar - 2. Bender A.T., Ostenson C.L., Giordano D., Beavo J.A.: Differentiationof human monocytes in vitro with granulocyte-macrophage colony-stimulatingfactor and macrophage colony-stimulating factor producesdistinct changes in cGMP phosphodiesterase expression. Cell. Signal.,2004; 16: 365-374
Google Scholar - 3. Borán M.S., Baltrons M.A., García A.: The ANP-cGMP-protein kinaseG pathway induces a phagocytic phenotype but decreases inflammatorygene expression in microglial cells. Glia, 2008; 56: 394-411
Google Scholar - 4. Cao L., Wu J., Gardner D.G.: Atrial natriuretic peptide suppressesthe transcription of its guanylyl cyclase-linked receptor. J. Biol.Chem., 1995; 270: 24891-24897
Google Scholar - 5. Chao Y.C., Cheng C.J., Hsieh H.T., Lin C.C., Chen C.C., Yang R.B.:Guanylate cyclase-G, expressed in the Grueneberg ganglion olfactorysubsystem, is activated by bicarbonate. Biochem. J., 2010;432: 267-273
Google Scholar - 6. Chinkers M., Garbers D.L., Chang M.S., Lowe D.G., Chin H.M.,Goeddel D.V., Schulz S.: A membrane form of guanylate cyclaseis an atrial natriuretic peptide receptor. Nature, 1989; 338: 78-83
Google Scholar - 7. Chrisman T.D., Garbers D.L., Parks M.A., Hardman J.G.: Characterization of particulate and soluble guanylate cyclases from rat lung.J. Biol. Chem., 1975; 250: 374-381
Google Scholar - 8. Ciuman M., Siednienko J., Czyżyk R., Witwicka H., Kołosionek E.,Kobiałka M., Gorczyca W.A.: Cyclic GMP-dependent protein kinaseand soluble guanylyl cyclase disappear in elicited rat neutrophils.Biochim. Biophys. Acta, 2006; 1760: 1618-1623
Google Scholar - 9. Connelly L., Jacobs A.T., Palacios-Callender M., Moncada S., HobbsA.J.: Macrophage endothelial nitric-oxide synthase autoregulatescellular activation and pro-inflammatory protein expression. J. Biol.Chem., 2003; 278: 26480-26487
Google Scholar - 10. Currie M.G., Geller D.M., Cole B.R., Siegel N.R., Fok K.F., AdamsS.P., Eubanks S.R., Galluppi G.R., Needleman P.: Purification and sequenceanalysis of bioactive atrial peptides (atriopeptins). Science,1984; 223: 67-69
Google Scholar - 11. de Bold A.J., Borenstein H.B., Veress A.T., Sonnenberg H.: A rapidand potent natriuretic response to intravenous injection of atrialmyocardial extract in rats. Life Sci., 1981; 28: 89-94
Google Scholar - 12. Dolfini D., Gatta R., Mantovani R.: NF-Y and the transcriptionalactivation of CCAAT promoters. Crit. Rev. Biochem. Mol. Biol.,2012; 47: 29-49
Google Scholar - 13. Flora D.R., Potter L.R.: Prolonged atrial natriuretic peptide exposurestimulates guanylyl cyclase-A degradation. Endocrinology, 2010;151: 2769-2776
Google Scholar - 14. Flynn T.G., de Bold M.L., de Bold A.J.: The amino acid sequenceof an atrial peptide with potent diuretic and natriuretic properties.Biochem. Biophys. Res. Commun., 1983; 117: 859-865
Google Scholar - 15. Friebe A., Koesling D.: Regulation of nitric oxide-sensitive guanylylcyclase. Circ. Res., 2003; 93: 96-105
Google Scholar - 16. Garbers D.L., Gray J.P.: Guanylate cyclase from sperm of thesea urchin, Strongylocentrotus purpuratus. Methods Enzymol., 1974;38:196-199
Google Scholar - 17. Garg R., Oliver P.M., Maeda N., Pandey K.N.: Genomic structure,organization, and promoter region analysis of murine guanylylcyclase/atrial natriuretic peptide receptor-A gene. Gene, 2002;297: 123-133
Google Scholar - 18. Garg R., Pandey K.N.: Regulation of guanylyl cyclase/natriureticpeptide receptor-A gene expression. Peptides, 2005; 26: 1009-1023
Google Scholar - 19. Gorczyca W.A.: Cyklazy guanylanowe i ich udział w wewnątrzkomórkowymprzekazywaniu sygnału. W: Receptory i mechanizmyprzekazywania sygnału, red.: Nowak J.Z., Zawilska J.B., WydawnictwoNaukowe PWN, Warszawa 2004, 64-89
Google Scholar - 20. Guo D., Zhang J.J., Huang X.Y.: Stimulation of guanylyl cyclase-Dby bicarbonate. Biochemistry, 2009; 48: 4417-4422
Google Scholar - 21. Hamet P., Tremblay J., Pang S.C., Garcia R., Thibault G., GutkowskaJ., Cantin M., Genest J.: Effect of native and synthetic atrialnatriuretic factor on cyclic GMP. Biochem. Biophys. Res. Commun.,1984; 123: 515-527
Google Scholar - 22. Hardman J.G., Sutherland E.W.: Guanyl cyclase, an enzyme catalyzingthe formation of guanosine 3’,5’-monophosphate from guanosinetriphosphate. J. Biol. Chem., 1969; 244: 6363-6370
Google Scholar - 23. Heim J.M., Singh S., Gerzer R.: Effect of glycosylation on clonedANF-sensitive guanylyl cyclase. Life Sci., 1996; 59: 61-68
Google Scholar - 24. Hum D., Besnard S., Sanchez R., Devost D., Gossard F., Hamet P.,Tremblay J.: Characterization of a cGMP-response element in theguanylyl cyclase/natriuretic peptide receptor A gene promoter.Hypertension, 2004; 43:1270-1278
Google Scholar - 25. Ichiki T., Huntley B.K., Burnett J.C.Jr.: BNP molecular forms andprocessing by the cardiac serine protease corin. Adv. Clin. Chem.,2013; 61: 1-31
Google Scholar - 26. Kalra D., Baumgarten G., Dibbs Z., Seta Y., Sivasubramanian N.,Mann D.L.: Nitric oxide provokes tumor necrosis factor-α expressionin adult feline myocardium through a cGMP-dependent pathway.Circulation, 2000; 102: 1302-1307
Google Scholar - 27. Kamisaki Y., Saheki S., Nakane M., Palmieri J.A., Kuno T. ChangB.Y., Waldman S.A., Murad F.: Soluble guanylate cyclase from ratlung exists as a heterodimer. J. Biol. Chem., 1986; 261: 7236-7241
Google Scholar - 28. Kangawa K., Tawaragi Y., Oikawa S., Mizuno A., Sakuragawa Y.,Nakazato H., Fukuda A., Minamino N., Matsuo H.: Identification ofrat g atrial natriuretic polypeptide and characterization of the cDNAencoding its precursor. Nature, 1984; 312: 152-155
Google Scholar - 29. Kiemer A.K., Hartung T. Vollmar A.M.: cGMP-mediated inhibitionof TNF-a production by the atrial natriuretic peptide in murinemacrophages. J. Immunol., 2000; 165: 175-181
Google Scholar - 30. Kimura H., Murad F.: Evidence for two different forms of guanylatecyclase in rat heart. J. Biol. Chem., 1974; 249: 6910-6916
Google Scholar - 31. Kishimoto I., Rossi K., Garbers D.L.: A genetic model providesevidence that the receptor for atrial natriuretic peptide (guanylylcyclase-A) inhibits cardiac ventricular myocyte hypertrophy. Proc.Natl. Acad. Sci. USA, 2001; 98: 2703-2706
Google Scholar - 32. Kobiałka M., Witwicka H., Siednienko J., Gorczyca W.A.: Metabolismof cyclic GMP in peritoneal macrophages of rat and guineapig, Acta Biochim. Pol., 2003; 50: 837-848
Google Scholar - 33. Koesling D.: Modulators of soluble guanylyl cyclase. NaunynSchmiedebergs Arch. Pharmacol., 1998; 358: 123-126
Google Scholar - 34. Koesling D.: Studying the structure and regulation of solubleguanylyl cyclase. Methods, 1999; 19: 485-493
Google Scholar - 35. Koh G.Y., Nussenzveig D.R., Okolicany J., Price D.A., Maack T.:Dynamics of atrial natriuretic factor-guanylate cyclase receptors andreceptor-ligand complexes in cultured glomerular mesangial and renomedullaryinterstitial cells. J. Biol. Chem., 1992; 267: 11987-11994
Google Scholar - 36. Koller K.J., Lipari M.T., Goeddel D.V.: Proper glycosylation andphosphorylation of the type A natriuretic peptide receptor are requiredfor hormone-stimulated guanylyl cyclase activity. J. Biol.Chem., 1993; 268: 5997-6003
Google Scholar - 37. Kone B.C.: Molecular biology of natriuretic peptides and nitricoxide synthases. Cardiovasc. Res., 2001; 51: 429-441
Google Scholar - 38. Kong X., Wang X., Xu W., Behera S., Hellermann G., Kumar A.,Lockey R.F., Mohapatra S., Mohapatra S.S.: Natriuretic peptide receptorA as a novel anticancer target. Cancer Res., 2008; 68: 249-256
Google Scholar - 39. Kuhn M., Holtwick R., Baba H.A., Perriard J.C., Schmitz W., EhlerE.: Progressive cardiac hypertrophy and dysfunction in atrial natriureticpeptide receptor (GC-A) deficient mice. Heart, 2002; 87: 368-374
Google Scholar - 40. Kumar P., Arise K.K., Pandey K.N.: Transcriptional regulationof guanylyl cyclase/natriuretic peptide receptor-A gene. Peptides,2006; 27: 1762-1769
Google Scholar - 41. Kumar P., Bolden G., Arise K.K., Krazit S.T., Pandey K.N.: Regulationof natriuretic peptide receptor-A gene expression and stimulationof its guanylyl cyclase activity by transcription factor Ets-1.Biosci. Rep., 2009; 29: 57-70
Google Scholar - 42. Kumar P., Garg R., Bolden G., Pandey K.N.: Interactive roles ofEts-1, Sp1, and acetylated histones in the retinoic acid-dependentactivation of guanylyl cyclase/atrial natriuretic peptide receptor–A gene transcription. J. Biol. Chem., 2010; 285: 37521-37530
Google Scholar - 43. Kumar P., Periyasamy R., Das S., Neerukonda S., Mani I., PandeyK.N.: All-trans retinoic acid and sodium butyrate enhance natriureticpeptide receptor A gene transcription: role of histone modification.Mol. Pharmacol., 2014; 85: 946-957
Google Scholar - 44. Kumar P., Tripathi S., Pandey K.N.: Histone deacetylase inhibitorsmodulate the transcriptional regulation of guanylyl cyclase/natriuretic peptide receptor-A gene: interactive roles of modifiedhistones, histone acetyltransferase, p300, and Sp1. J. Biol. Chem.2014; 289: 6991-7002
Google Scholar - 45. Kurihara M., Katamine S., Saavedra J.M.: Atrial natriuretic peptide,ANP(99-126), receptors in rat thymocytes and spleen cells. Biochem.Biophys. Res. Commun., 1987; 145: 789-796
Google Scholar - 46. Ladetzki-Baehs K., Keller M., Kiemer A.K., Koch E., Zahler S., WendelA., Vollmar A.M.: Atrial natriuretic peptide, a regulator of nuclearfactor-κB activation in vivo. Endocrinology, 2007; 148: 332-336
Google Scholar - 47. Liang F., Schaufele F., Gardner D.G.: Functional interaction ofNF-Y and Sp1 is required for type a natriuretic peptide receptorgene transcription. J. Biol. Chem., 2001; 276: 1516-1522
Google Scholar - 48. Liang F., Schaufele F., Gardner D.G.: Sp1 dependence of natriureticpeptide receptor A gene transcription in rat aortic smoothmuscle cells. Endocrinology, 1999; 140: 1695-1701
Google Scholar - 49. Lowe D.G., Chang M.S., Hellmiss R., Chen E., Singh S., GarbersD.L., Goeddel D.V.: Human atrial natriuretic peptide receptor definesa new paradigm for second messenger signal transduction. EMBOJ., 1989; 8: 1377-1384
Google Scholar - 50. Lowe D.G., Fendly B.M.: Human natriuretic peptide receptor–A guanylyl cyclase. Hormone cross-linking and antibody reactivitydistinguish receptor glycoforms. J. Biol. Chem., 1992; 267: 21691-21697
Google Scholar - 51. Lowe D.G., Klisak I., Sparkes R.S., Mohandas T., Goeddel D.V.:Chromosomal distribution of three members of the human natriureticpeptide receptor/guanylyl cyclase gene family. Genomics, 1990;8: 304-312
Google Scholar - 52. Lucas K.A., Pitargi G.M., Kazerounian S., Ruiz-Stewart I., Park J.,Schulz S., Chepenik K.P., Waldman S.A.: Guanylyl cyclases and signalingby cyclic GMP. Pharmacol. Rev., 2000; 52: 375-414
Google Scholar - 53. Martel G., Hamet P., Tremblay J.: GREBP, a cGMP-response element-bindingprotein repressing the transcription of natriureticpeptide receptor 1 (NPR1/GCA). J. Biol. Chem., 2010; 285: 20926-20939
Google Scholar - 54. Misono K.S., Grammer R.T., Fukumi H., Inagami T.: Rat atrial natriureticfactor: isolation, structure and biological activities of fourmajor peptides. Biochem. Biophys. Res. Commun., 1984; 123: 444-451
Google Scholar - 55. Misono K.S., Philo J.S., Arakawa T., Ogata C.M., Qiu Y., OgawaH., Young H.S.: Structure, signaling mechanism and regulation ofthe natriuretic peptide receptor-guanylate cyclase. FEBS J., 2011;278: 1818-1829
Google Scholar - 56. Mitkiewicz M., Kuropatwa M., Kurowska E., Gorczyca W.A.: Differenteffects of soluble and particulate guanylyl cyclases on expressionof inflammatory cytokines in rat peripheral blood mononuclearcells. Immunobiology, 2011; 216: 423-430
Google Scholar - 57. Miyagi M., Zhang X., Misono K.S.: Glycosylation sites in the atrialnatriuretic peptide receptor: oligosaccharide structures are not requiredfor hormone binding. Eur. J. Biochem., 2000; 267: 5758-5768
Google Scholar - 58. Morita R., Ukyo N., Furuya M., Uchiyama T., Hori T.: Atrial natriureticpeptide polarizes human dendritic cells toward a Th2-promotingphenotype through its receptor guanylyl cyclase-coupledreceptor A. J. Immunol., 2003; 170: 5869-5875
Google Scholar - 59. Moriyama N., Taniguchi M., Miyano K., Miyoshi M., WatanabeT.: ANP inhibits LPS-induced stimulation of rat microglial cellsby suppressing NF-κB and AP-1 activations. Biochem. Biophys. Res.Commun., 2006; 350: 322-328
Google Scholar - 60. Müller D., Middendorff R., Olcese J., Mukhopadhyay A.K.: Centralnervous system-specific glycosylation of the type A natriureticpeptide receptor. Endocrinology, 2002; 143: 23-29
Google Scholar - 61. Nakayama T., Soma M., Takahashi Y., Rehemudula D., SatoM., Uwabo J., Izumi Y., Kanmatsuse K.: Nucleotide seguence of the5’-flanking region of the type A human natriuretic peptide receptorgene and association analysis using a novel microsatellite in essentialhypertension. Am. J. Hypertens., 1999; 12: 1144-1148
Google Scholar - 62. Nojiri T., Hosoda H., Tokudome T., Miura K., Ishikane S., KimuraT., Shintani Y., Inoue M., Sawabata N., Miyazato M., Okumura M.,Kangawa K.: Atrial natriuretic peptide inhibits lipopolysaccharide–induced acute lung injury. Pulm. Pharmacol. Ther., 2014; 29: 24-30
Google Scholar - 63. O’Dorisio M.S., Fertel R., Finkler E., Brooks R., Vassalo L.: Characterizationof cyclic nucleotide metabolism during human monocytedifferentiation. J. Leukoc. Biol., 1984; 35: 617-630
Google Scholar - 64. Ogawa H., Qiu Y., Ogata C.M., Misono K.S.: Crystal structure ofhormone-bound atrial natriuretic peptide receptor extracellular domain:rotation mechanism for transmembrane signal transduction.J. Biol. Chem., 2004; 279: 28625-28631
Google Scholar - 65. Ogawa H., Qiu Y., Philo J.S., Arakawa T., Ogata C.M., Misono K.S.:Reversibly bound chloride in the atrial natriuretic peptide receptorhormone-binding domain: possible allosteric regulation and a conservedstructural motif for the chloride-binding site. Protein Sci.,2010; 19: 544-557
Google Scholar - 66. Pandey K.N.: Ligand-mediated endocytosis and intracellular sequestrationof guanylyl cyclase/natriuretic peptide receptors: roleof GDAY motif. Mol. Cell. Biochem., 2010; 334: 81-98
Google Scholar - 67. Pandey K.N.: The functional genomics of guanylyl cuclase/natriureticpeptide receptor-A: perspectives and paradigms. FEBS J.,2011; 278: 1792-1807
Google Scholar - 68. Pandey K.N., Nguyen H.T., Garg R., Khurana M..L, Fink J.: Internalizationand trafficking of guanylyl (guanylate) cyclase/natriureticpeptide receptor A is regulated by an acidic tyrosine-based cytoplasmicmotif GDAY. Biochem. J., 2005; 388: 103-113
Google Scholar - 69. Pilz R.B., Broderick K.E.: Role of cyclic GMP in gene regulation.Front. Biosci., 2005; 10: 1239-1268
Google Scholar - 70. Pilz R.B., Casteel D.E.: Regulation of gene expression by cyclicGMP. Circ. Res., 2003; 93: 1034-1046
Google Scholar - 71. Potter L.R.: Guanylyl cyclase structure, function and regulation.Cell. Signal., 2011; 23: 1921-1926
Google Scholar - 72. Potter L.R.: Natriuretic peptide metabolism, clearance and degradation.FEBS J., 2011; 278: 1808-1817
Google Scholar - 73. Potter L.R.: Regulation and therapeutic targeting of peptide-activatedreceptor guanylyl cyclases. Pharmacol. Ther., 2011; 130: 71-82
Google Scholar - 74. Potter L.R., Abbey-Hosch S., Dickey D.M.: Natriuretic peptides,their receptors, and cyclic guanosine monophosphate-dependentsignaling functions. Endocr. Rev., 2006; 27: 47-72
Google Scholar - 75. Russwurm M., Koesling D.: Isoforms of NO-sensitive guanylylcyclase. Mol. Cell. Biochem., 2002; 230: 159-164
Google Scholar - 76. Schröter J., Zahedi R.P., Hartmann M., Gassner B., Gazinski A.,Waschke J., Sickmann A., Kuhn M.: Homologous desensitization ofguanylyl cyclase A, the receptor for atrial natriuretic peptide, isassociated with a complex phosphorylation pattern. FEBS J., 2010;277: 2440-2453
Google Scholar - 77. Schultz G., Bohme E., Munske K.: Guanyl cyclase. Determinationof enzyme activity. Life Sci., 1969; 8:1323-1332
Google Scholar - 78. Semenov A.G., Tamm N.N., Seferian K.R., Postnikov A.B., KarpovaN.S., Serebryanaya D.V., Koshkina E.V., Krasnoselsky M.I., KatrukhaA.G.: Processing of pro-B-type natriuretic peptide: furin and corinas candidate convertases. Clin. Chem., 2010; 56: 1166-1176
Google Scholar - 79. Shi S.J., Nguyen H.T., Sharma G.D., Navar L.G., Pandey K.N.: Geneticdisruption of atrial natriuretic peptide receptor-A alters reninand angiotensin II levels. Am. J. Physiol. Renal Physiol., 2001;281: F665-F673
Google Scholar - 80. Siednienko J., Nowak J., Moynagh P.N., Gorczyca W.A.: Nitricoxide affects IL-6 expression in human peripheral blood mononuclearcells involving cGMP-dependent modulation of NF-κB activity.Cytokine, 2011; 54: 282-288
Google Scholar - 81. Stone J.R., Marletta M.A.: Spectral and kinetic studies on theactivation of soluble guanylate cyclase by nitric oxide. Biochemistry,1996; 35: 1093-1099
Google Scholar - 82. Su J., Scholz P.M., Weiss H.R.: Differential effects of cGMP producedby soluble and particulate guanylyl cyclase on mouse ventricularmyocytes. Exp. Biol. Med., 2005; 230: 242-250
Google Scholar - 83. Sudoh T., Kangawa K., Minamino N., Matsuo H.: A new natriureticpeptide in porcine brain. Nature, 1988; 332: 78-81
Google Scholar - 84. Sun L., Wang H., Hu J., Han J., Matsunami H., Luo M.: Guanylylcyclase-D in the olfactory CO2 neurons is activated by bicarbonate.Proc. Natl. Acad. Sci. USA, 2009; 106: 2041-2046
Google Scholar - 85. Takahashi Y., Nakayama T., Soma M., Izumi Y., Kanmatsuse K.:Organization of the human natriuretic peptide receptor A gene.Biochem. Biophys. Res. Commun., 1998; 246: 736-739
Google Scholar - 86. Tsuruda T., Boerrigter G., Huntley B.K., Noser J.A., Cataliotti A.,Costello-Boerrigter L.C., Chen H.H., Burnett J.C.Jr.: Brain natriureticpeptide is produced in cardiac fibroblasts and induces matrix metallproteinases.Circ. Res., 2002; 91: 1127-1134
Google Scholar - 87. Vellaichamy E., Das S., Subramanian U., Maeda N., Pandey K.N.:Genetically altered mutant mouse models of guanylyl cyclase/natriureticpeptide receptor-A exhibit the cardiac expression of proinflammatorymediators in a gene-dose-dependent manner. Endocrinology,2014; 155: 1045-1056
Google Scholar - 88. Vellaichamy E., Khurana M.L., Fink J., Pandey K.N.: Involvementof the NF-κB/matrix metalloproteinase pathway in cardiac fibrosisof mice lacking guanylyl cyclase/natriuretic peptide receptor A. J.Biol. Chem., 2005; 280: 19230-19242
Google Scholar - 89. Vesely D.L., Clark L.C., Garces A.H., McAfee Q.W., Soto J., GowerW.R.Jr: Novel therapeutic approach for cancer using four cardiovascularhormones. Eur. J. Clin. Invest., 2004; 34: 674-682
Google Scholar - 90. Vodovar N., Séronde M.F., Laribi S., Gayat E., Lassus J., Boukef R.,Nouira S., Manivet P., Samuel J.L., Logeart D., Ishihara S., Cohen SolalA., Januzzi J.L.Jr, Richards A.M., Launay J.M., Mebazaa A.: Post-translationalmodifications enhance NT-proBNP and BNP production inacute decompensated heart failure. Eur. Heart J., 2014; 35: 3434-3441
Google Scholar - 91. Vollmar A.M.: The role of atrial natriuretic peptide in the immunesystem. Peptides, 2005; 26: 1086-1094
Google Scholar - 92. Waldman S.A., Rapoport R.M., Murad F.: Atrial natriuretic factorselectively activates particulate guanylate cyclase and elevates cyclicGMP in rat tissues. J. Biol. Chem., 1984; 259: 14332-14334
Google Scholar - 93. Wang D., Oparil S., Feng J.A., Li P., Perry G., Chen L.B., Dai M.,John S.W., Chen Y.F.: Effects of pressure overload on extracellularmatrix expression in the heart of the atrial natriuretic peptide-nullmouse. Hypertension, 2003; 42: 88-95
Google Scholar - 94. Wang W., Liao X., Fukuda K., Knappe S., Wu F., Dries D.L., QinJ., Wu Q.: Corin variant associated with hypertension and cardiachypertrophy exhibits impaired zymogen activation and natriureticpeptide processing activity. Circ. Res., 2008; 103: 502-508
Google Scholar - 95. Wang X., Raulji P., Mohapatra S.S., Patel R., Hellermann G., KongX., Vera P.L., Meyer-Siegler K.L., Coppola D., Mohapatra S.: Natriureticpeptide receptor as a novel target for prostate cancer. Mol.Cancer, 2011; 10: 56
Google Scholar - 96. White A.A., Aurbach G.D.: Detection of guanyl cyclase in mammaliantissues. Biochim. Biophys. Acta, 1969; 191: 686-697
Google Scholar - 97. Winquist R.J., Faison E.P., Waldman S.A., Schwartz K., Murad F.,Rapoport R.M.: Atrial natriuretic factor elicits an endothelium-independentrelaxation and activates particulate guanylate cyclase in vascularsmooth muscle. Proc. Natl. Acad. Sci. USA, 1984; 81: 7661-7664
Google Scholar - 98. Yamaguchi M., Rutledge L.J., Garbers D.L.: The primary structureof the rat guanylyl cyclase A/atrial natriuretic peptide receptorgene. J. Biol. Chem., 1990; 265: 20414-20420
Google Scholar - 99. Yan W., Wu F., Morser J., Wu Q.: Corin, a transmembrane cardiacserine protease, acts as a pro-atrial natriuretic peptide-convertingenzyme. Proc. Natl. Acad. Sci. USA, 2000; 97: 8525-8529
Google Scholar - 100. Yoder A.R., Stone M.D., Griffin T.J., Potter L.R.: Mass spectrometricidentification of phosphorylation sites in guanylyl cyclaseA and B. Biochemistry, 2010; 49: 10137-10145
Google Scholar - 101. Zabel U., Häusler C., Weeger M., Schmidt H.H.: Homodimerizationof soluble guanylyl cyclase subunits. Dimerization analysisusing a glutathione s-transferase affinity tag. J. Biol. Chem., 1999;274: 18149-18152
Google Scholar - 102. Zhao D., Vellaichamy E., Somanna N.K., Pandey K.N.: Guanylylcyclase/natriuretic peptide receptor-A gene disruption causes increasedadrenal angiotensin II and aldosterone levels. Am. J. Physiol.Renal Physiol., 2007; 293: F121-F127
Google Scholar