Molecular and Cellular Biochemistry

, Volume 334, Issue 1–2, pp 37–51 | Cite as

Atrial natriuretic factor-receptor guanylate cyclase signal transduction mechanism

  • Teresa Duda


Atrial natriuretic factor (ANF) receptor guanylate cyclase (ANF-RGC), like the other members of the membrane guanylate cyclase family, is a single transmembrane-spanning protein. The transmembrane domain separates the protein into two regions, extracellular and intracellular. The extracellular region contains the ANF-binding domain and the intracellular region the catalytic domain located at the C-terminus of the protein. Preceding the catalytic domain, the intracellular region is comprised of the following functional domains: juxtaposed 40 amino acids to the transmembrane domain is the ATP-regulated module (ARM) domain [also termed the kinase homology domain (KHD)], and the putative dimerization domain. The ANF-RGC signaling is initiated by hormone, ANF, binding to its extracellular binding site. The binding signal is transduced through the transmembrane domain to the intracellular portion where ATP binding to the ARM domain partially activates the cyclase and prepares it for subsequent steps involving phosphorylation and attaining the fully activated state. This chapter reviews the signaling modules of ANF-RGC.


ANF ANF receptor Membrane guanylate cyclase Cyclic GMP Signal transduction 



This research was supported by NIH award LH 084584. I wish to express my sincere gratefulness to Dr. Rameshwar K. Sharma, Distinguished Professor, Salus University, for introducing me to the membrane guanylate cyclase transduction research, for years of guidance, support, and collaboration.


  1. 1.
    Paul AK, Marala RB, Jaiswal RK, Sharma RK (1987) Coexistence of guanylate cyclase and atrial natriuretic factor receptor in a 180-kD protein. Science 235:1224–1226PubMedGoogle Scholar
  2. 2.
    Paul AK (1986) Particulate guanylate cyclase from adrenocortical carcinoma 494. Purification, biochemical and immunological characterization. Doctoral thesis, University of TennesseeGoogle Scholar
  3. 3.
    Kuno T, Andresen JW, Kamisaki Y, Waldman SA, Chang LY, Saheki S, Leitman DC, Nakane M, Murad F (1986) Co-purification of an atrial natriuretic factor receptor and particulate guanylate cyclase from rat lung. J Biol Chem 261:5817–5823PubMedGoogle Scholar
  4. 4.
    Meloche S, McNicoll N, Liu B, Ong H, De Lean A (1988) Atrial natriuretic factor R1 receptor from bovine adrenal zona glomerulosa: purification, characterization, and modulation by amiloride. Biochemistry 27:8151–8158PubMedGoogle Scholar
  5. 5.
    Takayanagi R, Inagami T, Snajdar RM, Imada T, Tamura M, Misono KS (1987) Two distinct forms of receptors for atrial natriuretic factor in bovine adrenocortical cells. Purification, ligand binding, and peptide mapping. J Biol Chem 262:12104–12113PubMedGoogle Scholar
  6. 6.
    Chinkers M, Garbers DL, Chang MS, Lowe DG, Chin HM, Goeddel DV, Schulz S (1989) A membrane form of guanylate cyclase is an atrial natriuretic peptide receptor. Nature 338:78–83PubMedGoogle Scholar
  7. 7.
    Duda T, Goraczniak RM, Sharma RK (1991) Site-directed mutational analysis of a membrane guanylate cyclase cDNA reveals the atrial natriuretic factor signaling site. Proc Natl Acad Sci USA 88:7882–7886PubMedGoogle Scholar
  8. 8.
    Lowe DG, Chang MS, Hellmiss R, Chen E, Singh S, Garbers DL, Goeddel DV (1989) Human atrial natriuretic peptide receptor defines a new paradigm for second messenger signal transduction. EMBO J 8:1377–13784PubMedGoogle Scholar
  9. 9.
    Marala R, Duda T, Goraczniak RM, Sharma RK (1992) Genetically tailored atrial natriuretic factor-dependent guanylate cyclase: immunological and functional identity with 180 kDa membrane guanylate cyclase and ATP signaling site. FEBS Lett 296:254–258PubMedGoogle Scholar
  10. 10.
    Pandey KN, Singh S (1990) Molecular cloning and expression of murine guanylate cyclase/atrial natriuretic factor receptor cDNA. J Biol Chem 265:12342–12348PubMedGoogle Scholar
  11. 11.
    Chang MS, Lowe DG, Lewis M, Hellmiss R, Chen E, Goeddel DV (1989) Differential activation by atrial and brain natriuretic peptides of two different receptor guanylate cyclases. Nature 341:68–72PubMedGoogle Scholar
  12. 12.
    Schulz S, Singh S, Bellet RA, Singh G, Tubb DJ, Chin H, Garbers DL (1989) The primary structure of a plasma membrane guanylate cyclase demonstrates diversity within this new receptor family. Cell 58:1155–1162PubMedGoogle Scholar
  13. 13.
    Duda T, Goraczniak RM, Sitaramayya A, Sharma RK (1993) Cloning and expression of an ATP-regulated human retina C-type natriuretic factor receptor guanylate cyclase. Biochemistry 32:1391–1395PubMedGoogle Scholar
  14. 14.
    de Sauvage FJ, Camerato TR, Goeddel DV (1991) Primary structure and functional expression of the human receptor for Escherichia coli heat-stable enterotoxin. J Biol Chem 266:17912–17918PubMedGoogle Scholar
  15. 15.
    Hamra FK, Forte LR, Eber SL, Pidhorodeckyj NV, Krause WJ, Freeman RH, Chin DT, Tompkins JA, Fok KF, Smith CE, Duffin KL, Siegel NR, Currie MG (1993) Uroguanylin: structure and activity of a second endogenous peptide that stimulates intestinal guanylate cyclase. Proc Natl Acad Sci USA 90:10464–10468PubMedGoogle Scholar
  16. 16.
    Khare S, Wilson D, Wali RK, Tien XY, Bissonnette M, Niedziela SM, Bolt MJ, Sitrin MD, Brasitus TA (1994) Guanylin activates rat colonic particulate guanylate cyclase. Biochem Biophys Res Commun 203:1432–1437PubMedGoogle Scholar
  17. 17.
    Schulz S, Green CK, Yuen PS, Garbers DL (1990) Guanylyl cyclase is a heat-stable enterotoxin receptor. Cell 63:941–948PubMedGoogle Scholar
  18. 18.
    Singh S, Singh G, Heim JM, Gerzer R (1991) Isolation and expression of a guanylate cyclase-coupled heat stable enterotoxin receptor cDNA from a human colonic cell line. Biochem Biophys Res Commun 179:1455–1463PubMedGoogle Scholar
  19. 19.
    Goraczniak RM, Duda T, Sitaramayya A, Sharma RK (1994) Structural and functional characterization of the rod outer segment membrane guanylate cyclase. Biochem J 302:455–461PubMedGoogle Scholar
  20. 20.
    Shyjan AW, de Sauvage FJ, Gillett NA, Goeddel DV, Lowe DG (1992) Molecular cloning of a retina-specific membrane guanylyl cyclase. Neuron 9:727–737PubMedGoogle Scholar
  21. 21.
    Lowe DG (1995) Gene Bank accession number M92432Google Scholar
  22. 22.
    Koch KW (1991) Purification and identification of photoreceptor guanylate cyclase. J Biol Chem 266:8634–8637PubMedGoogle Scholar
  23. 23.
    Lowe DG, Dizhoor AM, Liu K, Gu Q, Spencer M, Laura R, Lu L, Hurley JB (1995) Cloning and expression of a second photoreceptor-specific membrane retina guanylyl cyclase (RetGC), RetGC-2. Proc Natl Acad Sci USA 92:5535–5539PubMedGoogle Scholar
  24. 24.
    Goraczniak RM, Duda T, Sharma RK (1998) Calcium modulated signaling site in type 2 rod outer segment membrane guanylate cyclase (ROS-GC2). Biochem Biophys Res Commun 245:447–453PubMedGoogle Scholar
  25. 25.
    Yang RB, Foster DC, Garbers DL, Fulle HJ (1995) Two membrane forms of guanylyl cyclase found in the eye. Proc Natl Acad Sci USA 92:602–606PubMedGoogle Scholar
  26. 26.
    Duda T, Jankowska A, Venkataraman V, Nagele RG, Sharma RK (2001) A novel calcium-regulated membrane guanylate cyclase transduction system in the olfactory neuroepithelium. Biochemistry 40:12067–12077PubMedGoogle Scholar
  27. 27.
    Fulle HJ, Vassar R, Foster DC, Yang RB, Axel R, Garbers DL (1995) A receptor guanylyl cyclase expressed specifically in olfactory sensory neurons. Proc Natl Acad Sci USA 92:3571–3575PubMedGoogle Scholar
  28. 28.
    Schulz S, Wedel BJ, Matthews A, Garbers DL (1998) The cloning and expression of a new guanylyl cyclase orphan receptor. J Biol Chem 273:1032–1037PubMedGoogle Scholar
  29. 29.
    Wedel BJ, Garbers DL (1997) New insights on the functions of the guanylyl cyclase receptors. FEBS Lett 410:29–33PubMedGoogle Scholar
  30. 30.
    Dizhoor AM, Olshevskaya EV, Henzel WJ, Wong SC, Stults JT, Ankoudinova I, Hurley JB (1995) Cloning, sequencing, and expression of a 24-kDa Ca(2 +)-binding protein activating photoreceptor guanylyl cyclase. J Biol Chem 270:25200–25206PubMedGoogle Scholar
  31. 31.
    Pozdnyakov N, Yoshida A, Cooper NG, Margulis A, Duda T, Sharma RK, Sitaramayya A (1995) A novel calcium-dependent activator of retinal rod outer segment membrane guanylate cyclase. Biochemistry 34:14279–14283PubMedGoogle Scholar
  32. 32.
    Margulis A, Pozdnyakov N, Sitaramayya A (1996) Activation of bovine photoreceptor guanylate cyclase by S100 proteins. Biochem Biophys Res Commun 218:243–247PubMedGoogle Scholar
  33. 33.
    Palczewski K, Subbaraya I, Gorczyca WA, Helekar BS, Ruiz CC, Ohguro H, Huang J, Zhao X, Crabb JW, Johnson RS, Walsh KA, Gray-Keller MP, Detwiler P, Baehr W (1994) Molecular cloning and characterization of retinal photoreceptor guanylyl cyclase-activating protein. Neuron 13:395–404PubMedGoogle Scholar
  34. 34.
    Frins S, Bönigk W, Müller F, Kellner R, Koch KW (1996) Functional characterization of a guanylyl cyclase-activating protein from vertebrate rods: cloning, heterologous expression, and localization. J Biol Chem 271:8022–8027PubMedGoogle Scholar
  35. 35.
    Duda T, Goraczniak RM, Sharma RK (1996) Molecular characterization of S100A1-S100B protein in retina and its activation mechanism of bovine photoreceptor guanylate cyclase. Biochemistry 35:6263–6266PubMedGoogle Scholar
  36. 36.
    Duda T, Goraczniak R, Surgucheva I, Rudnicka-Nawrot M, Gorczyca WA, Palczewski K, Sitaramayya A, Baehr W, Sharma RK (1996) Calcium modulation of bovine photoreceptor guanylate cyclase. Biochemistry 35:8478–8482PubMedGoogle Scholar
  37. 37.
    Kumar VD, Vijay-Kumar S, Krishnan A, Duda T, Sharma RK (1999) A second calcium regulator of rod outer segment membrane guanylate cyclase, ROS-GC1: neurocalcin. Biochemistry 38:12614–12620PubMedGoogle Scholar
  38. 38.
    Duda T, Krishnan R, Sharma RK (2006) GCAP1: antithetical calcium sensor of ROS-GC transduction machinery. Calcium Binding Proteins 1:102–107Google Scholar
  39. 39.
    Sharma RK (2002) Evolution of the membrane guanylate cyclase transduction system. Mol Cell Biochem 230:3–30PubMedGoogle Scholar
  40. 40.
    Leinders-Zufall T, Cockerham RE, Michalakis S, Biel M, Garbers DL, Reed RR, Zufall F, Munger SD (2007) Contribution of the receptor guanylyl cyclase GC-D to chemosensory function in the olfactory epithelium. Proc Natl Acad Sci USA 104:14507–14512PubMedGoogle Scholar
  41. 41.
    Duda T, Sharma RK (2008) ONE-GC membrane guanylate cyclase, a trimodal odorant signal transducer. Biochem Biophys Res Commun 367:440–445PubMedGoogle Scholar
  42. 42.
    Duda T, Sharma RK (2009) Ca2+-modulated ONE-GC odorant signal transduction. FEBS Lett 583:1327–1330PubMedGoogle Scholar
  43. 43.
    Sun L, Wang H, Hu J, Han J, Matsunami H, Luo M (2009) Guanylyl cyclase-D in the olfactory CO2 neurons is activated by bicarbonate. Proc Natl Acad Sci USA 106:2041–2046PubMedGoogle Scholar
  44. 44.
    Guo D, Zhang JJ, Huang XY (2009) Stimulation of guanylyl cyclase-D by bicarbonate. Biochemistry 48:4417–4422PubMedGoogle Scholar
  45. 45.
    Labrecque J, Mc Nicoll N, Marquis M, De Lean A (1999) A disulfide-bridged mutant of natriuretic peptide receptor-A displays constitutive activity. Role of receptor dimerization in signal transduction. J Biol Chem 274:9752–9759PubMedGoogle Scholar
  46. 46.
    Yu H, Olshevskaya E, Duda T, Seno K, Hayashi F, Sharma RK, Dizhoor AM, Yamazaki A (1999) Activation of retinal guanylyl cyclase-1 by Ca2+-binding proteins involves its dimerization. J Biol Chem 274:15547–15555PubMedGoogle Scholar
  47. 47.
    Wilson EM, Chinkers M (1995) Identification of sequences mediating guanylyl cyclase dimerization. Biochemistry 3:4696–4701Google Scholar
  48. 48.
    Thorpe DS, Niu S, Morkin E (1991) Overexpression of dimeric guanylyl cyclase cores of an atrial natriuretic peptide receptor. Biochem Biophys Res Commun 180:538–544PubMedGoogle Scholar
  49. 49.
    Liu Y, Ruoho AE, Rao VD, Hurley JH (1997) Catalytic mechanism of the adenylyl and guanylyl cyclases: modeling and mutational analysis. Proc Natl Acad Sci USA 9:13414–13419Google Scholar
  50. 50.
    Yang RB, Garbers DL (1997) Two eye guanylyl cyclases are expressed in the same photoreceptor cells and form homomers in preference to heteromers. J Biol Chem 272:13738–13742PubMedGoogle Scholar
  51. 51.
    Qiu Y, Ogawa H, Miyagi M, Misono KS (2004) Constitutive activation and uncoupling of the atrial natriuretic peptide receptor by mutations at the dimer interface. Role of the dimer structure in signalling. J Biol Chem 279:6115–6123PubMedGoogle Scholar
  52. 52.
    Sharma RK, Duda T, Venkataraman V, Koch K-W (2004) Calcium-modulated mammalian membrane guanylate cyclase ROS-GC transduction machinery in sensory neurons: a universal concept. Curr Topics Biochem Res 6:111–144Google Scholar
  53. 53.
    Hartmann M, Skryabin BV, Müller T, Gazinski A, Schröter J, Gassner B, Nikolaev VO, Bünemann M, Kuhn M (2008) Alternative splicing of the guanylyl cyclase-A receptor modulates atrial natriuretic peptide signaling. J Biol Chem 283:22313–28320Google Scholar
  54. 54.
    McNicoll N, Gagnon J, Rondeau JJ, Ong H, De Léan A (1996) Localization by photoaffinity labeling of natriuretic peptide receptor-A binding domain. Biochemistry 35:12950–12956PubMedGoogle Scholar
  55. 55.
    McNicoll N, Escher E, Wilkes BC, Schiller PW, Ong H, De Léan A (1992) Highly efficient photoaffinity labeling of the hormone binding domain of atrial natriuretic factor receptor. Biochemistry 31:4487–4493PubMedGoogle Scholar
  56. 56.
    Misono KS (2002) Natriuretic peptide receptor: structure and signaling. Mol Cell Biochem 230:49–60PubMedGoogle Scholar
  57. 57.
    He X, Nishio K, Misono KS (1995) High-yield affinity alkylation of the atrial natriuretic factor receptor binding site. Bioconjug Chem 6:541–548PubMedGoogle Scholar
  58. 58.
    Misono KS, Ogawa H, Qiu Y, Ogata CM (2005) Structural studies of the natriuretic peptide receptor: a novel hormone-induced rotation mechanism for transmembrane signal transduction. Peptides 26:957–968PubMedGoogle Scholar
  59. 59.
    Ogawa H, Zhang X, Qiu Y, Ogata CM, Misono KS (2003) Crystallization and preliminary X-ray analysis of the atrial natriuretic peptide (ANP) receptor extracellular domain complex with ANP: use of ammonium sulfate as the cryosalt. Acta Crystallogr D 59:1831–1833PubMedGoogle Scholar
  60. 60.
    Ogawa H, Qiu Y, Ogata CM, Misono KS (2004) Crystal structure of hormone-bound atrial natriuretic peptide receptor extracellular domain: rotation mechanism for transmembrane signal transduction. J Biol Chem 279:28625–28631PubMedGoogle Scholar
  61. 61.
    Heim JM, Singh S, Gerzer R (1996) Effect of glycosylation on cloned ANF-sensitive guanylyl cyclase. Life Sci 59:PL61–PL68PubMedGoogle Scholar
  62. 62.
    Koller KJ, Lipari MT, Goeddel DV (1993) Proper glycosylation and phosphorylation of the type A natriuretic peptide receptor are required for hormone-stimulated guanylyl cyclase activity. J Biol Chem 268:5997–6003PubMedGoogle Scholar
  63. 63.
    Lowe DG, Fendly BM (1992) Human natriuretic peptide receptor-A guanylyl cyclase. Hormone cross-linking and antibody reactivity distinguish receptor glycoforms. J Biol Chem 267:21691–21697PubMedGoogle Scholar
  64. 64.
    Miyagi M, Zhang X, Misono KS (2000) Glycosylation sites in the atrial natriuretic peptide receptor: oligosaccharide structures are not required for hormone binding. Eur J Biochem 267:5758–5768PubMedGoogle Scholar
  65. 65.
    Miyagi M, Misono KS (2000) Disulfide bond structure of the atrial natriuretic peptide receptor extracellular domain: conserved disulfide bonds among guanylate cyclase-coupled receptors. Biochim Biophys Acta 1478:30–38PubMedGoogle Scholar
  66. 66.
    Huo X, Abe T, Misono KS (1999) Ligand binding-dependent limited proteolysis of the atrial natriuretic peptide receptor: juxtamembrane hinge structure essential for transmembrane signal transduction. Biochemistry 38:16941–16951PubMedGoogle Scholar
  67. 67.
    Labrecque J, Deschênes J, McNicoll N, De Léan A (2001) Agonistic induction of a covalent dimer in a mutant of natriuretic peptide receptor-A documents a juxtamembrane interaction that accompanies receptor activation. J Biol Chem 276:8064–8072PubMedGoogle Scholar
  68. 68.
    Duda T, Sharma RK (2005) Two membrane juxtaposed signaling modules in ANF-RGC are interlocked. Biochem Biophys Res Commun 332:149–156PubMedGoogle Scholar
  69. 69.
    Ogawa H, Qiu Y, Huang L, Tam-Chang SW, Young HS, Misono KS (2009) Structure of the atrial natriuretic peptide receptor extracellular domain in the unbound and hormone-bound states by single-particle electron microscopy. FEBS J 276:1347–1355PubMedGoogle Scholar
  70. 70.
    Chang CH, Kohse KP, Chang B, Hirata M, Jiang B, Douglas JE, Murad F (1990) Characterization of ATP-stimulated guanylate cyclase activation in rat lung membranes. Biochim Biophys Acta 1052:159–165PubMedGoogle Scholar
  71. 71.
    Kurose H, Inagami T, Ui M (1987) Participation of adenosine 5′-triphosphate in the activation of membrane-bound guanylate cyclase by the atrial natriuretic factor. FEBS Lett 219:375–379PubMedGoogle Scholar
  72. 72.
    Duda T, Venkataraman V, Ravichandran S, Sharma RK (2005) ATP-regulated module (ARM) of the atrial natriuretic factor receptor guanylate cyclase. Peptides 26:969–984PubMedGoogle Scholar
  73. 73.
    Chinkers M, Singh S, Garbers DL (1991) Adenine nucleotides are required for activation of rat atrial natriuretic peptide receptor/guanylyl cyclase expressed in a baculovirus system. J Biol Chem 266:4088–4093PubMedGoogle Scholar
  74. 74.
    Marala RB, Sitaramayya A, Sharma RK (1991) Dual regulation of atrial natriuretic factor-dependent guanylate cyclase activity by ATP. FEBS Lett 281:73–76PubMedGoogle Scholar
  75. 75.
    Wong SK, Ma CP, Foster DC, Chen AY, Garbers DL (1995) The guanylyl cyclase-A receptor transduces an atrial natriuretic peptide/ATP activation signal in the absence of other proteins. J Biol Chem 270:30818–30822PubMedGoogle Scholar
  76. 76.
    Goraczniak RM, Duda T, Sharma RK (1992) A structural motif that defines the ATP-regulatory module of guanylate cyclase in atrial natriuretic factor signalling. Biochem J 282:533–537PubMedGoogle Scholar
  77. 77.
    Duda T, Goraczniak RM, Sharma RK (1993) The glycine residue of ATP regulatory module in receptor guanylate cyclases that is essential in natriuretic factor signaling. FEBS Lett 335:309–314PubMedGoogle Scholar
  78. 78.
    Larose L, McNicoll N, Ong H, De Léan A (1991) Allosteric modulation by ATP of the bovine adrenal natriuretic factor R1 receptor functions. Biochemistry 30:8990–8995PubMedGoogle Scholar
  79. 79.
    Cole FE, Rondon I, Iwata T, Hardee E, Frohlich ED (1989) Effect of ATP and amiloride on ANF binding and stimulation of cyclic GMP accumulation in rat glomerular membranes. Life Sci 45:477–484PubMedGoogle Scholar
  80. 80.
    Foster DC, Garbers DL (1998) Dual role for adenine nucleotides in the regulation of the atrial natriuretic peptide receptor, guanylyl cyclase-A. J Biol Chem 273:16311–16318PubMedGoogle Scholar
  81. 81.
    Joubert S, Jossart C, McNicoll N, De Léan A (2005) Atrial natriuretic peptide-dependent photolabeling of a regulatory ATP-binding site on the natriuretic peptide receptor-A. FEBS J 272:5572–5583PubMedGoogle Scholar
  82. 82.
    Burczynska B, Duda T, Sharma RK (2007) ATP signaling site in the ARM domain of atrial natriuretic factor receptor guanylate cyclase. Mol Cell Biochem 301:193–207Google Scholar
  83. 83.
    Chinkers M, Garbers DL (1989) The protein kinase domain of the ANP receptor is required for signaling. Science 245:1392–1394PubMedGoogle Scholar
  84. 84.
    Wierenga RK, Hol WG (1983) Predicted nucleotide-binding properties of p21 protein and its cancer-associated variant. Nature 302:842–844PubMedGoogle Scholar
  85. 85.
    Hanks SK, Quinn AM, Hunter T (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241:42–52PubMedGoogle Scholar
  86. 86.
    Duda T, Sharma RK (1995) ATP bimodal switch that regulates the ligand binding and signal transduction activities of the atrial natriuretic factor receptor guanylate cyclase. Biochem Biophys Res Commun 209:286–292PubMedGoogle Scholar
  87. 87.
    Duda T, Yadav P, Jankowska A, Venkataraman V, Sharma RK (2001) Three dimensional atomic model and experimental validation for the ATP-regulated module (ARM) of the atrial natriuretic factor receptor guanylate cyclase. Mol Cell Biochem 217:165–172PubMedGoogle Scholar
  88. 88.
    Sharma RK, Yadav P, Duda T (2001) Allosteric regulatory step and configuration of the ATP-binding pocket in atrial natriuretic factor receptor guanylate cyclase transduction mechanism. Can J Physiol Pharmacol 79:682–691PubMedGoogle Scholar
  89. 89.
    Duda T, Bharill S, Wojtas I, Yadav P, Gryczynski I, Gryczynski Z, Sharma RK (2009) Atrial natriuretic factor receptor guanylate cyclase signaling: new ATP-regulated transduction motif. Mol Cell Biochem 324:39–53PubMedGoogle Scholar
  90. 90.
    Jewett JR, Koller KJ, Goeddel DV, Lowe DG (1993) Hormonal induction of low affinity receptor guanylyl cyclase. EMBO J 12:769–777PubMedGoogle Scholar
  91. 91.
    Duda T, Sharma RK (1990) Regulation of guanylate cyclase activity by atrial natriuretic factor and protein kinase C. Mol Cell Biochem 93:179–184PubMedGoogle Scholar
  92. 92.
    Larose L, Rondeau JJ, Ong H, De Lean A (1992) Phosphorylation of atrial natriuretic factor R1 receptor by serine/threonine protein kinases: evidences for receptor regulation. Mol Cell Biochem 115:203–211PubMedGoogle Scholar
  93. 93.
    Sharma RK, Marala RB, Duda T (1989) Purification and characterization of the 180-kDa membrane guanylate cyclase containing atrial natriuretic factor receptor from rat adrenal gland and its regulation by protein kinase C. Steroids 53:437–460PubMedGoogle Scholar
  94. 94.
    Potter LR, Hunter T (1999) A constitutively “phosphorylated” guanylyl cyclase-linked atrial natriuretic peptide receptor mutant is resistant to desensitization. Mol Biol Cell 10:1811–1820PubMedGoogle Scholar
  95. 95.
    Potter LR, Hunter T (1998) Identification and characterization of the major phosphorylation sites of the B-type natriuretic peptide receptor. J Biol Chem 273:15533–15539PubMedGoogle Scholar
  96. 96.
    Potter LR, Hunter T (1999) Identification and characterization of the phosphorylation sites of the guanylyl cyclase-linked natriuretic peptide receptors A and B. Methods 19:506–520PubMedGoogle Scholar
  97. 97.
    Antos LK, Abbey-Hosch SE, Flora DR, Potter LR (2005) ATP-independent activation of natriuretic peptide receptors. J Biol Chem 280:26928–26932PubMedGoogle Scholar
  98. 98.
    Antos LK, Potter LR (2007) Adenine nucleotides decrease the apparent Km of endogenous natriuretic peptide receptors for GTP. Am J Physiol Endocrinol Metab 293:E1756–E1763PubMedGoogle Scholar
  99. 99.
    Sharma RK, Jaiswal RK, Duda T (1988) Second messenger role of cyclic GMP in atrial natriuretic factor receptor mediated signal transduction: 180 kDa membrane guanylate cyclase, its coupling with atrial natriuretic factor receptor and its regulation by protein kinase C. In: Needleman P (ed) Biological and molecular aspects of atrial factors. UCLA symposia on molecular and cellular biology, New series, vol 81. Alan R. Liss, Inc., pp 77–96Google Scholar
  100. 100.
    Sharma RK, Marala RB, Paul AK (1988) Mediatory role of cyclic GMP in receptor-mediated signal transduction: membrane guanylate cyclase and its coupling with atrial natriuretic factor receptor. In: Brenner BM, Laragh JH (eds) Advances in peptide research, vol II. American Society of Hypertension Symposium Series. Raven Press, New York, pp 61–77Google Scholar
  101. 101.
    Thorpe DS, Morkin E (1990) The carboxyl region contains the catalytic domain of the membrane form of guanylate cyclase. J Biol Chem 265:14717–14720PubMedGoogle Scholar
  102. 102.
    Thorpe DS, Niu S, Morkin E (1996) The guanylyl cyclase core of an atrial natriuretic peptide receptor: enzymatic properties and basis for cooperativity. Biochem Biophys Res Commun 218:670–673PubMedGoogle Scholar
  103. 103.
    Tremblay J, Huot C, Koch C, Potier M (1991) Characterization of the functional domains of the natriuretic peptide receptor/guanylate cyclase by radiation inactivation. Biol Chem 266:8171–8175Google Scholar
  104. 104.
    Miao ZH, Song DL, Douglas JG, Chang CH (1995) Mutational inactivation of the catalytic domain of guanylate cyclase-A receptor. Hypertension 25:694–698PubMedGoogle Scholar
  105. 105.
    Thompson DK, Garbers DL (1995) Dominant negative mutations of the guanylyl cyclase-A receptor. Extracellular domain deletion and catalytic domain point mutations. J Biol Chem 270:425–430PubMedGoogle Scholar
  106. 106.
    Wedel BJ, Foster DC, Miller DE, Garbers DL (1997) A mutation of the atrial natriuretic peptide (guanylyl cyclase-A) receptor results in a constitutively hyperactive enzyme. Proc Natl Acad Sci USA 94:459–462PubMedGoogle Scholar
  107. 107.
    Tucker CL, Hurley JH, Miller TR, Hurley JB (1998) Two amino acid substitutions convert a guanylyl cyclase, RetGC-1, into an adenylyl cyclase. Proc Natl Acad Sci USA 95:5993–5997PubMedGoogle Scholar
  108. 108.
    Venkataraman V, Duda T, Ravichandran S, Sharma RK (2008) Neurocalcin delta modulation of ROS-GC1, a new model of Ca(2+) signaling. Biochemistry 47:6590–6601Google Scholar
  109. 109.
    Garbers DL (1992) Guanylyl cyclase receptors and their endocrine, paracrine, and autocrine ligands. Cell 71:1–4PubMedGoogle Scholar
  110. 110.
    Juilfs DM, Fülle HJ, Zhao AZ, Houslay MD, Garbers DL, Beavo JA (1997) A subset of olfactory neurons that selectively express cGMP-stimulated phosphodiesterase (PDE2) and guanylyl cyclase-D define a unique olfactory signal transduction pathway. Proc Natl Acad Sci USA 94:3388–3395PubMedGoogle Scholar
  111. 111.
    Yamazaki A, Yu H, Yamazaki M, Honkawa H, Matsuura I, Usukura J, Yamazaki RK (2003) A critical role for ATP in the stimulation of retinal guanylyl cyclase by guanylyl cyclase-activating proteins. J Biol Chem 278:33150–33360PubMedGoogle Scholar
  112. 112.
    Yamazaki M, Usukura J, Yamazaki RK, Yamazaki A (2005) ATP binding is required for physiological activation of retinal guanylate cyclase. Biochem Biophys Res Commun 338:1291–1298PubMedGoogle Scholar
  113. 113.
    Yamazaki A, Yamazaki M, Yamazaki RK, Usukura J (2006) Illuminated rhodopsin is required for strong activation of retinal guanylate cyclase by guanylate cyclase-activating proteins. Biochemistry 45:1899–1909PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC. 2009

Authors and Affiliations

  1. 1.The Unit of Regulatory and Molecular Biology, Research Divisions of Biochemistry and Molecular BiologySalus UniversityElkins ParkUSA

Personalised recommendations