Skip to main content
SpringerLink
Log in

Membrane guanylate cyclase is a beautiful signal transduction machine: overview

Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

This article is a sequel to the four earlier comprehensive reviews which covered the field of membrane guanylate cyclase from its origin to the year 2002 (Sharma in Mol Cell Biochem 230:3–30, 2002) and then to the year 2004 (Duda et al. in Peptides 26:969–984, 2005); and of the Ca2+-modulated membrane guanylate cyclase to the year 1997 (Pugh et al. in Biosci Rep 17:429–473, 1997) and then to 2004 (Sharma et al. in Curr Top Biochem Res 6:111–144, 2004). This article contains three parts. The first part is “Historical”; it is brief, general, and freely borrowed from the earlier reviews, covering the field from its origin to the year 2004 (Sharma in Mol Cell Biochem, 230:3–30, 2002; Duda et al. in Peptides 26:969–984, 2005). The second part focuses on the “Ca2+-modulated ROS-GC membrane guanylate cyclase subfamily”. It is divided into two sections. Section “Historical” and covers the area from its inception to the year 2004. It is also freely borrowed from an earlier review (Sharma et al. in Curr Top Biochem Res 6:111–144, 2004). Section “Ca2+-modulated ROS-GC membrane guanylate cyclase subfamily” covers the area from the year 2004 to May 2009. The objective is to focus on the chronological development, recognize major contributions of the original investigators, correct misplaced facts, and project on the future trend of the field of mammalian membrane guanylate cyclase. The third portion covers the present status and concludes with future directions in the field.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price includes VAT (France)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Ashman DF, Lipton R, Melicow MM, Price TD (1963) Isolation of adenosine 3′,5′-monophosphate and guanosine 3′,5′-monophosphate from rat urine. Biochem Biophys Res Commun 11:330–334

    CAS  PubMed  Google Scholar 

  2. Sutherland EW, Rall TW (1960) The relation of adenosine-3′,5′-triphosphate and phosphorylase to the actions of catecholamines and other hormones. Pharmacol Rev 12:265–299

    CAS  Google Scholar 

  3. Goldberg ND, Dietz SB, O’Toole AG (1969) Cyclic guanosine 3′,5′-monophosphate in mammalian tissues and urine. J Biol Chem 244:4458–4466

    CAS  PubMed  Google Scholar 

  4. Ishikawa E, Ishikawa S, Davis JW, Sutherland EW (1969) Determination of guanosine 3′,5′-monophosphate in tissues and of guanyl cyclase in rat intestine. J Biol Chem 244:6371–6376

    CAS  PubMed  Google Scholar 

  5. Goldberg ND, O’Dea RF, Haddox MK (1973) Cyclic GMP. Adv Cyclic Nucleotide Res 3:155–223

    CAS  PubMed  Google Scholar 

  6. White AA, Aurbach GD (1969) Detection of guanyl cyclase in mammalian tissues. Biochim Biophys Acta 191:686–697

    CAS  PubMed  Google Scholar 

  7. Schultz G, Böhme E, Munske K (1969) Guanyl cyclase. Determination of enzyme activity. Life Sci 8:1323–1332

    CAS  PubMed  Google Scholar 

  8. Hardman JG, Sutherland EW (1969) Guanyl cyclase, an enzyme catalyzing the formation of guanosine 3′,5′-monophosphate from guanosine triphosphate. J Biol Chem 244:6363–6370

    CAS  PubMed  Google Scholar 

  9. Kimura H, Murad F (1974) Evidence for two different forms of guanylate cyclase in rat heart. J Biol Chem 249:6910–6916

    CAS  PubMed  Google Scholar 

  10. Kimura H, Murad F (1975) Subcellular localization of guanylate cyclase. Life Sci 17:837–843

    CAS  PubMed  Google Scholar 

  11. Hardman JG, Sutherland EW (1965) A cyclic 3′,5′-nucleotide phosphodiesterase from heart with specificity for uridine 3′,5′-phosphate. J Biol Chem 240:3704–3705

    CAS  PubMed  Google Scholar 

  12. Goldberg ND, Haddox MK (1977) Cyclic GMP metabolism and involvement in biological regulation. Annu Rev Biochem 46:823–896

    CAS  PubMed  Google Scholar 

  13. 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: Biological and molecular aspects of atrial factors. Alan R. Liss Inc., pp 77–96

  14. 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. American Society of Hypertension Symposium Series, vol II. Raven Press, New York, 61–77

  15. Sharma RK, Duda T, Goraczniak R, Sitaramayya A (1997) Membrane guanylate cyclase signal transduction system. Indian J Biochem Biophys 34:40–49

    CAS  PubMed  Google Scholar 

  16. George WJ, Polson JB, O’Toole AG, Goldberg ND (1970) Elevation of guanosine 3′,5′-cyclic phosphate in rat heart after perfusion with acetylcholine. Proc Natl Acad Sci USA 66:398–403

    CAS  PubMed  Google Scholar 

  17. Goldberg ND, Haddox MK, Nicol SE, Glass DB, Sanford CH, Kuehl FA Jr, Estensen R (1975) Biologic regulation through opposing influences of cyclic GMP and cyclic AMP: the Yin Yang hypothesis. Adv Cyclic Nucleotide Res 5:307–330

    CAS  PubMed  Google Scholar 

  18. Goldberg ND, Haddox MK, Hartle DK, Hadden JW (1972) The biological role of cyclic 3′,5′-guanosine monophosphate. In: Krager S (ed) Pharmacology and the future of the man. Fifth international congress on pharmacology, vol 5, San Francisco, pp 146–169

  19. Goldberg ND, Haddox MK, Dunham E, Lopez C, Hadden JW (1974) The Yin Yang hypothesis of biological control: opposing influences of cyclic GMP and cyclic AMP in the regulation of cell proliferation and other biological processes. In: Clarkson B, Beserga R (eds) Cold Spring Harbor symposium of the regulation of proliferation in animal cells. Cold Spring Harbor Laboratory, New York, pp 609–625

    Google Scholar 

  20. Goldberg ND, Haddox MK, Estensen R, White JG, Lopez C, Hadden JW (1974) Evidence for a dualism between cyclic GMP and cyclic AMP in the regulation of cell proliferation and other cellular processes. In: Brown W, Lichenstein L, Parker C (eds) Cyclic AMP. Cell growth and the immune response. Springer, New York, pp 247–262

    Google Scholar 

  21. Glinsmann WH, Hern EP (1969) Inactivation of rat liver glycogen synthetase by 3′,5′-cyclic nucleotides. Biochem Biophys Res Commun 36:931–936

    CAS  PubMed  Google Scholar 

  22. Glinsmann WH, Hern EP, Linarelli LG, Farese RV (1969) Similarities between effects of adenosine 3′,5′-monophosphate and guanosine 3′,5′-monophosphate on liver and adrenal metabolism. Endocrinology 85:711–719

    CAS  PubMed  Google Scholar 

  23. Conn HO, Karl IS, Steiner A, Kipnis DM (1971) Studies of the mechanism of action of 3′,5′-cyclic nucleotides on hepatic glucose production. Biochem Biophys Res Commun 45:436–443

    CAS  PubMed  Google Scholar 

  24. Exton JH, Hardman JG, Williams TF, Sutherland EW, Park CR (1971) Effects of guanosine 3′,5′-monophosphate on the perfused rat liver. J Biol Chem 246:2658–2664

    CAS  PubMed  Google Scholar 

  25. Guder W, Wieland O (1970) The effect of cyclic nucleotides on glucose synthesis in isolated rat kidney tubules. Hoppe Seylers Z Physiol Chem 351:291–292

    CAS  PubMed  Google Scholar 

  26. Friedmann N, Somlyo AV, Somlyo AP (1971) Cyclic adenosine and guanosine monophosphates and glucagon: effect on liver membrane potentials. Science 171:400–402

    CAS  PubMed  Google Scholar 

  27. Somlyo AP, Somlyo AV, Friedmann N (1971) Cyclic adenosine monophosphate, cyclic guanosine monophosphate, and glucagon: effects on membrane potential and ion fluxes in the liver. Ann N Y Acad Sci 185:108–114

    Article  CAS  PubMed  Google Scholar 

  28. Sayers G, Beall RJ, Seelig S (1972) Isolated adrenal cells: adrenocorticotropic hormone, calcium, steroidogenesis, and cyclic adenosine monophosphate. Science 175:1131–1133

    CAS  PubMed  Google Scholar 

  29. Kitabchi AE, Sharma RK (1971) Corticosteroidogenesis in isolated adrenal cells of rats. I. Effect of corticotropins and 3′,5′-cyclic nucleotides on corticosterone production. Endocrinology 88:1109–1116

    CAS  PubMed  Google Scholar 

  30. Mahaffee D, Ney RL (1970) Effects of nucleotides possessing a 3′,5′-cyclic monophosphate on adrenal steroidogenesis. Metabolism 19:1104–1108

    CAS  PubMed  Google Scholar 

  31. Brandwein H, Lewicki J, Murad F (1981) Production and characterization of monoclonal antibodies to soluble rat lung guanylate cyclase. Proc Natl Acad Sci USA 78:4241–4245

    CAS  PubMed  Google Scholar 

  32. Wallach D, Pastan I (1976) Stimulation of membranous guanylate cyclase by concentrations of calcium that are in the physiological range. Biochem Biophys Res Commun 72:859–865

    CAS  PubMed  Google Scholar 

  33. Murad F, Mittal CK, Arnold WP, Ichikara K, Braughlet M, El-Zayat M (1978) Properties and regulation of guanylate cyclase: activation by azide, nitro compounds, and hydroxyl radical and effects of heme containing proteins. In: Folco G, Paolotiie R (eds) Molecular biology and pharmacology of cyclic nucleotides. Elsevier, Amsterdam, pp 33–42

    Google Scholar 

  34. Murad F, Mittal CK, Arnold WP, Katsuki S, Kimura H (1978) Guanylate cyclase: activation by azide, nitro compounds, nitric oxide, and hydroxyl radical and inhibition by hemoglobin and myoglobin. Adv Cyclic Nucleotide Res 9:145–158

    CAS  PubMed  Google Scholar 

  35. Mittal CK, Murad F (1977) Activation of guanylate cyclase by superoxide dismutase and hydroxyl radical: a physiological regulator of guanosine 3′,5′-monophosphate formation. Proc Natl Acad Sci USA 74:4360–4364

    CAS  PubMed  Google Scholar 

  36. Arnold WP, Mittal CK, Katsuki S, Murad F (1977) Nitric oxide activates guanylate cyclase and increases guanosine 3′,5′-cyclic monophosphate levels in various tissue preparations. Proc Natl Acad Sci USA 74:3203–3207

    CAS  PubMed  Google Scholar 

  37. Mittal CK, Kimura H, Murad F (1977) Purification and properties of a protein required for sodium azide activation of guanylate cyclase. J Biol Chem 252:4384–4390

    CAS  PubMed  Google Scholar 

  38. Waldman SA, Lewicki JA, Brandwein HJ, Murad F (1982) Partial purification and characterization of particulate guanylate cyclase from rat liver after solubilization with trypsin. J Cyclic Nucleotide Res 8:359–370

    CAS  PubMed  Google Scholar 

  39. Arnold WP, Aldred R, Murad F (1977) Cigarette smoke activates guanylate cyclase and increases guanosine 3′,5′-monophosphate in tissues. Science 198:934–936

    CAS  PubMed  Google Scholar 

  40. Katsuki S, Arnold W, Mittal C, Murad F (1977) Stimulation of guanylate cyclase by sodium nitroprusside, nitroglycerin and nitric oxide in various tissue preparations and comparison to the effects of sodium azide and hydroxylamine. J Cyclic Nucleotide Res 3:23–35

    CAS  PubMed  Google Scholar 

  41. Katsuki S, Arnold WP, Murad F (1977) Effects of sodium nitroprusside, nitroglycerin, and sodium azide on levels of cyclic nucleotides and mechanical activity of various tissues. J Cyclic Nucleotide Res 3:239–247

    CAS  PubMed  Google Scholar 

  42. Gill GN, McCune RW (1979) Guanosine 3′,5′-monophosphate-dependent protein kinase. Curr Top Cell Regul 15:1–45

    CAS  PubMed  Google Scholar 

  43. Murad F, Arnold WP, Mittal CK, Braughler JM (1979) Properties and regulation of guanylate cyclase and some proposed functions for cyclic GMP. Adv Cyclic Nucleotide Res 11:175–204

    CAS  PubMed  Google Scholar 

  44. Pugh EN Jr, Duda T, Sitaramayya A, Sharma RK (1997) Photoreceptor guanylate cyclases: a review. Biosci Rep 17:429–473

    CAS  PubMed  Google Scholar 

  45. Rall TW, Sutherland EW (1961) The regulatory role of adenosine-3′,5′-phosphate. Cold Spring Harb Symp Quant Biol 26:347–354

    CAS  PubMed  Google Scholar 

  46. Haynes RC Jr, Berthet L (1957) Studies on the mechanism of action of the adrenocorticotropic hormone. J Biol Chem 225:115–124

    CAS  PubMed  Google Scholar 

  47. Haynes RC Jr (1958) The activation of adrenal phosphorylase by the adrenocorticotropic hormone. J Biol Chem 233:1220–1222

    CAS  PubMed  Google Scholar 

  48. Sayers G (1967) In: Gray CH (ed) Hormones in blood. Academic Press, New York and London, 169–194

  49. Garren LD (1968) The mechanism of action of adrenocorticotropic hormone. Vitam Horm 26:119–145

    CAS  PubMed  Google Scholar 

  50. Bronsome ED Jr (1968) Adrenal cortex. Annu Rev Physiol 30:171–212

    Google Scholar 

  51. Halkerston ID (1975) Cyclic AMP and adrenocortical function. Adv Cyclic Nucleotide Res 6:99–136

    CAS  PubMed  Google Scholar 

  52. Sharma RK, Sawhney RS (1978) Metabolic regulation of steroidogenesis in isolated adrenal cell. Investigation of the adrenocorticotropic hormone, guanosine 3′,5′-monophosphate, and adenosine 3′,5′-monophosphate control step. Biochemistry 17:316–321

    CAS  PubMed  Google Scholar 

  53. Robinson GA, Butcher RW, Sutherland EW (1971) Cyclic AMP. Academic Press, New York

    Google Scholar 

  54. Haynes RC Jr, Koritz SB, Peron FG (1959) Influence of adenosine 3′,5′-monophosphate on corticoid production by rat adrenal glands. J Biol Chem 234:1421–1423

    CAS  PubMed  Google Scholar 

  55. Farese RV, Linarelli LG, Glinsmann WH, Ditzion BR, Paul MI, Pauk GA (1969) Persistence of the steroidogenic effect of adenosine-3′,5′-monophosphate in vitro: evidence for a third factor during the steroidogenic effect of ACTH. Endocrinology 85:867–874

    CAS  PubMed  Google Scholar 

  56. Tsang CP, Péron FG (1971) Effects of adenosine-3′,5′-monophosphate on steroidogenesis and glycolysis in the rat adrenal gland incubated in vitro. Steroids 17:453–469

    CAS  PubMed  Google Scholar 

  57. Rivkin I, Chasin M (1971) Nucleotide specificity of the steroidogenic response of rat adrenal cell suspensions prepared by collagenase digestion. Endocrinology 88:664–670

    CAS  PubMed  Google Scholar 

  58. Scarpa A, Baldassare J, Inesi G (1972) The effect of calcium ionophores on fragmented sarcoplasmic reticulum. J Gen Physiol 60:735–749

    CAS  PubMed  Google Scholar 

  59. Sharma RK, Hashimoto K, Kitabchi AE (1972) Steroidogenesis in isolated adrenal cells of rat. 3. Morphological and biochemical correlation of cholesterol and cholesterol ester content in ACTH and N6-2′-O-dibutyryl-adenosine-3′,5′-monophosphate activated adrenal cells. Endocrinology 91:994–1003

    CAS  PubMed  Google Scholar 

  60. Sharma RK, Ahmed NK, Sutliff LS (1974) Brush JS. Metabolic regulation of steroidogenesis in isolated adrenal cells of the rat. ACTH regulation of cGMP and cAMP levels and steroidogenesis. FEBS Lett 45:107–110

    CAS  PubMed  Google Scholar 

  61. Sharma RK, Ahmed NK, Shanker G (1976) Metabolic regulation of steroidogenesis in isolated adrenal cells of rat. Relationship of adrenocorticotropin-, adenosine 3′,5′-monophosphate-and guanosine 3′,5′-monophosphate-stimulated steroidogenesis with the activation of protein kinase. Eur J Biochem 70:427–433

    CAS  PubMed  Google Scholar 

  62. Perchellet JP, Shanker G, Sharma R (1978) Regulatory role of guanosine 3′,5′-monophosphate in adrenocorticotropin hormone-induced steroidogenesis. Science 199:311–312

    CAS  PubMed  Google Scholar 

  63. Sharma RK, Hashimoto K (1972) Ultrastructural studies and metabolic regulation of isolated adrenocortical carcinoma cells of rat. Cancer Res 32:666–674

    CAS  PubMed  Google Scholar 

  64. Harrington CA, Fenimore DC, Farmer RW (1978) Regulation of adrenocortical steroidogenesis by cyclic 3′,5′-guanosine monophosphate in isolated rat adrenal cells. Biochem Biophys Res Commun 85:55–61

    CAS  PubMed  Google Scholar 

  65. Neri G, Gambino AM, Mazzocchi G, Nussdorfer GG (1978) Effects of chronic treatment with ACTH on the intracellular levels of cyclic-AMP and cyclic-GMP in the rat adrenal cortex. Experientia 34:815–817

    CAS  PubMed  Google Scholar 

  66. Sharma RK (1973) Metabolic regulation of steroidogenesis in adrenocortical carcinoma cells of rat. Effect of adrenocorticotropin and adenosine cyclic 3′,5′-monophosphate on corticosteroidogenesis. Eur J Biochem 32:506–512

    CAS  PubMed  Google Scholar 

  67. Haksar A, Péron FG (1973) The role of calcium in the steroidogenic response of rat adrenal cells to adrenocorticotropic hormone. Biochim Biophys Acta 313:363–371

    CAS  PubMed  Google Scholar 

  68. Bowyer F, Kitabchi AE (1974) Dual role of calcium in steroidogenesis in the isolated adrenal cell of rat. Biochem Biophys Res Commun 57:100–105

    CAS  PubMed  Google Scholar 

  69. Perchellet JP, Sharma RK (1979) Mediatory role of calcium and guanosine 3′,5′-monophosphate in adrenocorticotropin-induced steroidogenesis by adrenal cells. Science 203:1259–1261

    CAS  PubMed  Google Scholar 

  70. Rasmussen H (1981) Calcium and cyclic AMP as synarchic messengers. Wiley, New York

    Google Scholar 

  71. Kitabchi AE, Wilson DB, Sharma RK (1971) Steroidogenesis in isolated adrenal cells of rat. II. Effect of caffeine on ACTH and cyclic nucleotide-induced steroidogenesis and its relation to cyclic nucleotide phosphodiesterase (PDE). Biochem Biophys Res Commun 44:898–904

    CAS  PubMed  Google Scholar 

  72. Hayashi K, Sala G, Catt K, Dufau ML (1979) Regulation of steroidogenesis by adrenocorticotropic hormone in isolated adrenal cells. The intermediate role of cyclic nucleotides. J Biol Chem 254:6678–6683

    CAS  PubMed  Google Scholar 

  73. Sayers G, Ma RM, Giordano ND (1978) Isolated adrenal cells: corticosterone production in response. Proc Soc Exp Biol Med 136:619–622

    Google Scholar 

  74. Laychock SG, Hardman JG (1978) Effects of sodium nitroprusside and ascorbic acid on rat adrenocortical cell cGMP levels and steroidogenesis. J Cyclic Nucleotide Res 4:335–344

    CAS  PubMed  Google Scholar 

  75. Ahrens H, Paul AK, Kuroda Y, Sharma RK (1982) Adrenocortical cyclic GMP-dependent protein kinase: purification, characterization, and modification of its activity by calmodulin, and its relationship with steroidogenesis. Arch Biochem Biophys 215:597–609

    CAS  PubMed  Google Scholar 

  76. Nambi P, Aiyar NV, Sharma RK (1982) Adrenocorticotropin-dependent particulate guanylate cyclase in rat adrenal and adrenocortical carcinoma: comparison of its properties with soluble guanylate cycles and its relationship with ACTH-induced steroidogenesis. Arch Biochem Biophys 217:638–646

    CAS  PubMed  Google Scholar 

  77. Nambi P, Sharma RK (1981) Adrenocorticotropic hormone-responsive guanylate cyclase in the particulate fraction of rat adrenal glands. Endocrinology 108:2025–2027

    CAS  PubMed  Google Scholar 

  78. Nambi P, Sharma RK (1981) Demonstration of ACTH-sensitive particulate guanylate cyclase in adrenocortical carcinoma. Biochem Biophys Res Commun 100:508–514

    CAS  PubMed  Google Scholar 

  79. 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 53:437–460

    CAS  PubMed  Google Scholar 

  80. Anglard P, Zwiller J, Vincendon G, Louis JC (1985) Regulation of cyclic AMP and cyclic GMP levels by adrenocorticotropic hormone in cultured neurons. Biochem Biophys Res Commun 133:286–292

    CAS  PubMed  Google Scholar 

  81. Waldman SA, Rapoport RM, Murad F (1984) Atrial natriuretic factor selectively activates particulate guanylate cyclase and elevates cyclic GMP in rat tissues. J Biol Chem 259:14332–14334

    CAS  PubMed  Google Scholar 

  82. Hamet P, Tremblay J, Pang SC, Garcia R, Thibault G, Gutkowska J, Cantin M, Genest J (1984) Effect of native and synthetic atrial natriuretic factor on cyclic GMP. Biochem Biophys Res Commun 123:515–527

    CAS  PubMed  Google Scholar 

  83. Paul AK (1986) Particulate guanylate cyclase from adrenocortical carcinoma 494. Purification, biochemical and immunological characterization. Doctoral Thesis, University of Tennessee

  84. Paul AK, Marala RB, Jaiswal RK, Sharma RK (1987) Coexistence of guanylate cyclase and atrial natriuretic factor receptor in a 180-kD protein. Science 235:1224–1226

    CAS  PubMed  Google Scholar 

  85. Sharma RK (1988) Guanylate cyclase and the atrial natriuretic factor receptor. Response to Waldman SA, Leitman DC, Anderson J, Murad F. Science 240:805–806

    CAS  Google Scholar 

  86. 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 261:5817–5823

    CAS  PubMed  Google Scholar 

  87. Sharma RK (2002) Evolution of membrane guanylate cyclase transduction system. Mol Cell Biochem 230:30–30

    Google Scholar 

  88. 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 262:12104–12113

    CAS  PubMed  Google Scholar 

  89. Meloche S, McNicoll N, Liu B, Ong H, De Léan A (1988) Atrial natriuretic factor R1 receptor from bovine adrenal zona glomerulosa: purification, characterization, and modulation by amyloidal. Biochemistry 27:8151–8158

    CAS  PubMed  Google Scholar 

  90. Marala RB, Sharma RK (1988) Characterization of atrial-natriuretic-factor-receptor-coupled membrane guanylate cyclase from rat and mouse testes. Biochem J 251:301–304

    CAS  PubMed  Google Scholar 

  91. Ballermann BJ, Marala RB, Sharma RK (1988) Characterization and regulation by protein kinase C of renal glomerular atrial natriuretic peptide receptor-coupled guanylate cyclase. Biochem Biophys Res Commun 157:755–761

    CAS  PubMed  Google Scholar 

  92. de Bold AJ (1982) Atrial natriuretic factor of the rat heart. Studies on isolation and properties. Proc Soc Exp Biol Med 170:133–138

    PubMed  Google Scholar 

  93. Cantin M, Genest J (1985) The heart, an endocrine gland. Ann Endocrinol (Paris) 46:219–228

    CAS  Google Scholar 

  94. Schwartz D, Geller DM, Manning PT, Siegel NR, Fok KF, Smith CE, Needleman P (1985) Ser-Leu-Arg-Arg-atriopeptin III: the major circulating form of atrial peptide. Science 229:397–400

    CAS  PubMed  Google Scholar 

  95. de Bold AJ (1986) Atrial natriuretic factor: an overview. Fed Proc 45:2081–2085

    PubMed  Google Scholar 

  96. Atlas SA, Laragh JH (1986) Atrial natriuretic peptide: a new factor in hormonal control of blood pressure and electrolyte homeostasis. Annu Rev Med 37:397–414

    CAS  PubMed  Google Scholar 

  97. Atarashi K, Mulrow PJ, Franco-Saenz R, Snajdar R, Rapp J (1984) Inhibition of aldosterone production by an atrial extract. Science 224:992–994

    CAS  PubMed  Google Scholar 

  98. Chartier L, Schiffrin E, Thibault G, Garcia R (1984) Atrial natriuretic factor inhibits the stimulation of aldosterone secretion by angiotensin II, ACTH and potassium in vitro and angiotensin II-induced steroidogenesis in vivo. Endocrinology 115:2026–2028

    CAS  PubMed  Google Scholar 

  99. De Léan A, Racz K, Gutkowska J, Nguyen TT, Cantin M, Genest J (1984) Specific receptor-mediated inhibition by synthetic atrial natriuretic factor of hormone-stimulated steroidogenesis in cultured bovine adrenal cells. Endocrinology 115:1636–1638

    PubMed  Google Scholar 

  100. Kudo T, Baird A (1984) Inhibition of aldosterone production in the adrenal glomerulosa by atrial natriuretic factor. Nature 312:756–757

    CAS  PubMed  Google Scholar 

  101. Pandey KN, Kovacs WJ, Inagami T (1985) 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 133:800–806

    CAS  PubMed  Google Scholar 

  102. Nakamura M, Odaguchi K, Shimizu T, Nakamura Y, Okamoto M (1985) Stimulation of corticosterone production by atrial natriuretic polypeptide in hypophysectomized rats. Eur J Pharmacol 117:285–286

    CAS  PubMed  Google Scholar 

  103. Jaiswal N, Paul AK, Jaiswal RK, Sharma RK (1986) Atrial natriuretic factor regulation of cyclic GMP levels and steroidogenesis in isolated fasciculata cells of rat adrenal cortex. FEBS Lett 199:121–124

    CAS  PubMed  Google Scholar 

  104. Bex F, Corbin A (1985) Atrial natriuretic factor stimulates testosterone production by mouse interstitial cells. Eur J Pharmacol 115:125–126

    CAS  PubMed  Google Scholar 

  105. Mukhopadhyay AK, Schumacher M, Leidenberger FA (1986) Steroidogenic effect of atrial natriuretic factor in isolated mouse Leydig cells is mediated by cyclic GMP. Biochem J 239:463–467

    CAS  PubMed  Google Scholar 

  106. Pandey KN, Inagami T, Misono KS (1986) Atrial natriuretic factor receptor on cultured Leydig tumor cells: ligand binding and photoaffinity labeling. Biochemistry 25:8467–8472

    CAS  PubMed  Google Scholar 

  107. 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 338:78–83

    CAS  PubMed  Google Scholar 

  108. 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 8:1377–1384

    CAS  PubMed  Google Scholar 

  109. Pandey KN, Singh S (1990) Molecular cloning and expression of murine guanylate cyclase/atrial natriuretic factor receptor cDNA. J Biol Chem 265:12342–12348

    CAS  PubMed  Google Scholar 

  110. 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 88:7882–7886

    CAS  PubMed  Google Scholar 

  111. 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 296:254–258

    CAS  PubMed  Google Scholar 

  112. 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 58:1155–1162

    CAS  PubMed  Google Scholar 

  113. 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 341:68–72

    CAS  PubMed  Google Scholar 

  114. Currie MG, Fok KF, Kato J, Moore RJ, Hamra FK, Duffin KL, Smith CE (1992) Guanylin: an endogenous activator of intestinal guanylate cyclase. Proc Natl Acad Sci USA 89:947–951

    CAS  PubMed  Google Scholar 

  115. Wiegand RC, Kato J, Currie MG (1992) Rat guanylin cDNA: characterization of the precursor of an endogenous activator of intestinal guanylate cyclase. Biochem Biophys Res Commun 185:812–817

    CAS  PubMed  Google Scholar 

  116. 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 266:17912–17918

    PubMed  Google Scholar 

  117. 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 179:1455–1463

    CAS  PubMed  Google Scholar 

  118. 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 90:10464–10468

    CAS  PubMed  Google Scholar 

  119. 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 203:1432–1437

    CAS  PubMed  Google Scholar 

  120. Sharma RK, Duda T, Sitaramayya A (1994) Plasma membrane guanylate cyclase is a multimodule transduction system: Minireview. Amino Acids 7:117–127

    CAS  Google Scholar 

  121. Sharma RK, Duda T (1997) Plasma membrane guanylate cyclase. A multimodule transduction system. Adv Exp Med Biol 407:271–279

    CAS  PubMed  Google Scholar 

  122. Drewett JG, Garbers DL (1994) The family of guanylyl cyclase receptors and their ligands. Endocr Rev 15:135–162

    CAS  PubMed  Google Scholar 

  123. Garbers DL, Koesling D, Schultz G (1994) Guanylyl cyclase receptors. Mol Biol Cell 5:1–5

    CAS  PubMed  Google Scholar 

  124. Duda T, Goraczniak RM, Sharma RK (1994) Glutamic acid-332 residue of the type C natriuretic peptide receptor guanylate cyclase is important for signaling. Biochemistry 33:7430–7433

    CAS  PubMed  Google Scholar 

  125. Duda T, Goraczniak RM, Sharma RK (1995) Single amino acid residue-linked signaling shifts in the transduction activities of atrial and type C natriuretic factor receptor guanylate cyclases. Biochem Biophys Res Commun 212:1046–1053

    CAS  PubMed  Google Scholar 

  126. 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 279:28625–28631

    CAS  PubMed  Google Scholar 

  127. 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 219:375–379

    CAS  PubMed  Google Scholar 

  128. 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 1052:159–165

    CAS  PubMed  Google Scholar 

  129. Chinkers M, Garbers DL (1989) The protein kinase domain of the ANP receptor is required for signaling. Science 245:1392–1394

    CAS  PubMed  Google Scholar 

  130. Marala RB, Sitaramayya A, Sharma RK (1991) Dual regulation of atrial natriuretic factor-dependent guanylate cyclase activity by ATP. FEBS Lett 281:73–76

    CAS  PubMed  Google Scholar 

  131. 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 266:4088–4093

    CAS  PubMed  Google Scholar 

  132. 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 32:1391–1395

    CAS  PubMed  Google Scholar 

  133. 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 282:533–537

    CAS  PubMed  Google Scholar 

  134. Duda T, Sharma RK (2005) Two membrane juxtaposed signaling modules in ANF-RGC are interlocked. Biochem Biophys Res Commun 332:149–156

    CAS  PubMed  Google Scholar 

  135. Duda T, Venkataraman V, Ravichandran S, Sharma RK (2005) ATP-regulated module (ARM) of the atrial natriuretic factor receptor guanylate cyclase. Peptides 26:969–984

    CAS  PubMed  Google Scholar 

  136. 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 79:682–691

    CAS  PubMed  Google Scholar 

  137. Wierenga RK, Hol WG (1983) Predicted nucleotide-binding properties of p21 protein and its cancer-associated variant. Nature 302:842–844

    CAS  PubMed  Google Scholar 

  138. Hanks SK, Quinn AM, Hunter T (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241:42–52

    CAS  PubMed  Google Scholar 

  139. Duda T, Goraczniak RM, Sharma RK (1993) Core sequence of ATP regulatory module in receptor guanylate cyclases. FEBS Lett 315:143–148

    CAS  PubMed  Google Scholar 

  140. 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 335:309–314

    CAS  PubMed  Google Scholar 

  141. Larose L, McNicoll N, Ong H, De Léan A (1991) Allosteric modulation by ATP of the bovine adrenal natriuretic factor R1 receptor functions. Biochemistry 30:990–995

    Google Scholar 

  142. Jewett JR, Koller KJ, Goeddel DV, Lowe DG (1993) Hormonal induction of low affinity receptor guanylyl cyclase. EMBO J 12:769–777

    CAS  PubMed  Google Scholar 

  143. 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 209:286–292

    CAS  PubMed  Google Scholar 

  144. Duda T, Sharma RK (1995) ATP modulation of the ligand binding and signal transduction activities of the type C natriuretic peptide receptor guanylate cyclase. Mol Cell Biochem 152:179–183

    CAS  PubMed  Google Scholar 

  145. Singh S, Lowe DG, Thorpe DS, Rodriguez H, Kuang WJ, Dangott LJ, Chinkers M, Goeddel DV, Garbers DL (1988) Membrane guanylate cyclase is a cell-surface receptor with homology to protein kinases. Nature 334:708–712

    CAS  PubMed  Google Scholar 

  146. Duda T, Yadav P, Jankowska A, Venkataraman V, Sharma RK (2000) Three dimensional atomic model and experimental validation for the ATP-regulated module (ARM) of the atrial natriuretic factor receptor guanylate cyclase. Mol Cell Biochem 214(1–2):7–14 (erratum in Mol Cell Biochem 217:165–172)

    CAS  PubMed  Google Scholar 

  147. Potter LR, Hunter T (1998) Identification and characterization of the major phosphorylation sites of the B-type natriuretic peptide receptor. J Biol Chem 273:15533–15539

    CAS  PubMed  Google Scholar 

  148. Potter LR, Hunter T (1999) A constitutively “phosphorylated” guanylyl cyclase-linked atrial natriuretic peptide receptor mutant is resistant to desensitization. Mol Biol Cell 10:1811–1820

    CAS  PubMed  Google Scholar 

  149. Potter LR, Hunter T (1999) Identification and characterization of the phosphorylation sites of the guanylyl cyclase-linked natriuretic peptide receptors A and B. Methods 19:506–520

    CAS  PubMed  Google Scholar 

  150. Duda T, Sharma RK (1990) Regulation of guanylate cyclase activity by atrial natriuretic factor and protein kinase C. Mol Cell Biochem 93:179–184

    CAS  PubMed  Google Scholar 

  151. 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 115:203–211

    CAS  PubMed  Google Scholar 

  152. 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 273:16311–16318

    CAS  PubMed  Google Scholar 

  153. Perchellet JP, Sharma RK (1980) Ectopic alpha-adrenergic mediated accumulation of guanosine 3′,5′-monophosphate in isolated adrenocortical carcinoma cells. Endocrinology 106:1589–1593

    CAS  PubMed  Google Scholar 

  154. Shanker G, Sharma RK (1980) Characterization of ectopic alpha-adrenergic binding receptors of adrenocortical carcinoma cells. Endocrinology 106:1594–1598

    CAS  PubMed  Google Scholar 

  155. Chalberg SC, Duda T, Rhine JA, Sharma RK (1990) Molecular cloning, sequencing and expression of an alpha 2-adrenergic receptor complementary DNA from rat brain. Mol Cell Biochem 97:161–172

    CAS  PubMed  Google Scholar 

  156. Wypijewski K, Duda T, Sharma RK (1995) Structural, genetic and pharmacological identity of the rat alpha 2-adrenergic receptor subtype cA2–47 and its molecular characterization in rat adrenal, adrenocortical carcinoma and bovine retina. Mol Cell Biochem 144:181–190

    CAS  PubMed  Google Scholar 

  157. Venkataraman V, Duda T, Galoian K, Sharma RK (1996) Molecular and pharmacological identity of the alpha 2D-adrenergic receptor subtype in bovine retina and its photoreceptors. Mol Cell Biochem 159:129–138

    CAS  PubMed  Google Scholar 

  158. Jaiswal N, Sharma RK (1986) Dual regulation of adenylate cyclase and guanylate cyclase: alpha 2-adrenergic signal transduction in adrenocortical carcinoma cells. Arch Biochem Biophys 249:616–619

    CAS  PubMed  Google Scholar 

  159. Sharma RK (1990) Two operational modes of transmembrane migration og cyclic GMP signal pathway. In: Prasad KN, Meyskens FL Jr (eds) Nutrients and cancer prevention. Humana Press, Englewood Clifts, pp 3–18

    Google Scholar 

  160. Cohen AI, Hall IA, Ferrendelli JA (1978) Calcium and cyclic nucleotide regulation in incubated mouse retinas. J Gen Physiol 71:595–612

    CAS  PubMed  Google Scholar 

  161. Cote RH, Biernbaum MS, Nicol GD, Bownds MD (1984) Light-induced decreases in cGMP concentration precede changes in membrane permeability in frog rod photoreceptors. J Biol Chem 259:9635–9641

    CAS  PubMed  Google Scholar 

  162. Lolley RN, Racz E (1982) Calcium modulation of cyclic GMP synthesis in rat visual cells. Vision Res 22(12):1481–1486

    CAS  PubMed  Google Scholar 

  163. Woodruff ML, Bownds MD (1979) Amplitude, kinetics, and reversibility of a light-induced decrease in guanosine 3′,5′-cyclic monophosphate in frog photoreceptor membranes. J Gen Physiol 73:629–653

    CAS  PubMed  Google Scholar 

  164. Pugh EN Jr, Cobbs WH (1986) Visual transduction in vertebrate rods and cones: a tale of two transmitters, calcium and cyclic GMP. Vision Res 26:1613–1643

    CAS  PubMed  Google Scholar 

  165. Stryer L (1986) Cyclic GMP cascade of vision. Annu Rev Neurosci 9:87–119

    CAS  PubMed  Google Scholar 

  166. Fesenko EE, Kolesnikov SS, Lyubarsky AL (1985) Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature 313:310–313

    CAS  PubMed  Google Scholar 

  167. Kaupp UB, Niidome T, Tanabe T, Terada S, Bönigk W, Stühmer W, Cook NJ, Kangawa K, Matsuo H, Hirose T, Miyata T, Numa S (1989) Primary structure and functional expression from complementary DNA of the rod photoreceptor cyclic GMP-gated channel. Nature 342:762–766

    CAS  PubMed  Google Scholar 

  168. Lamb TD, Matthews HR, Torre V (1986) Incorporation of calcium buffers into salamander retinal rods: a rejection of the calcium hypothesis of phototransduction. J Physiol 372:315–349

    CAS  PubMed  Google Scholar 

  169. Matthews HR, Torre V, Lamb TD (1985) Effects on the photoresponse of calcium buffers and cyclic GMP incorporated into the cytoplasm of retinal rods. Nature 313:582–585

    CAS  PubMed  Google Scholar 

  170. Shinozawa T, Sokabe M, Terada S, Matsusaka H, Yoshizawa T (1987) Detection of cyclic GMP binding protein and ion channel activity in frog rod outer segments. J Biochem 102:281–290

    CAS  PubMed  Google Scholar 

  171. Horio Y, Murad F (1991) Solubilization of guanylyl cyclase from bovine rod outer segments and effects of lowering Ca2 + and nitro compounds. J Biol Chem 266:3411–3415

    CAS  PubMed  Google Scholar 

  172. Horio Y, Murad F (1133) Purification of guanylyl cyclase from rod outer segments. Biochim Biophys Acta 81–88:1991

    Google Scholar 

  173. Stryer L (1991) Visual excitation and recovery. J Biol Chem 266:10711–10714

    CAS  PubMed  Google Scholar 

  174. Shyjan AW, de Sauvage FJ, Gillett NA, Goeddel DV, Lowe DG (1992) Molecular cloning of a retina-specific membrane guanylyl cyclase. Neuron 9:727–737

    CAS  PubMed  Google Scholar 

  175. Margulis A, Goraczniak RM, Duda T, Sharma RK, Sitaramayya A (1993) Structural and biochemical identity of retinal rod outer segment membrane guanylate cyclase. Biochem Biophys Res Commun 194:855–861

    CAS  PubMed  Google Scholar 

  176. Goraczniak RM, Duda T, Sitaramayya A, Sharma RK (1994) Structural and functional characterization of the rod outer segment membrane guanylate cyclase. Biochem J 302:455–461

    CAS  PubMed  Google Scholar 

  177. Koch KW (1991) Purification and identification of photoreceptor guanylate cyclase. J Biol Chem 266:8634–8637

    CAS  PubMed  Google Scholar 

  178. Hayashi F, Yamazaki A (1991) Polymorphism in purified guanylate cyclase from vertebrate rod photoreceptors. Proc Natl Acad Sci USA 88:4746–4750

    CAS  PubMed  Google Scholar 

  179. 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 92:5535–5539

    CAS  PubMed  Google Scholar 

  180. Goraczniak R, Duda T, Sharma RK (1997) Structural and functional characterization of a second subfamily member of the calcium-modulated bovine rod outer segment membrane guanylate cyclase, ROS-GC2. Biochem Biophys Res Commun 234:666–670

    CAS  PubMed  Google Scholar 

  181. Dizhoor AM, Lowe DG, Olshevskaya EV, Laura RP, Hurley JB (1994) The human photoreceptor membrane guanylyl cyclase, RetGC, is present in outer segments and is regulated by calcium and a soluble activator. Neuron 12:1345–1352

    CAS  PubMed  Google Scholar 

  182. 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 270:25200–25206

    CAS  PubMed  Google Scholar 

  183. 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 271:8022–8027

    CAS  PubMed  Google Scholar 

  184. Palczewski K, Subbaraya I, Gorczyca WA, Helekar BS, Ruiz CC, Ohguro H, Huang J, Zhao X, Crabb JW, Johnson RS, Baehr W (1994) Molecular cloning and characterization of retinal photoreceptor guanylyl cyclase-activating protein. Neuron 13:395–404

    CAS  PubMed  Google Scholar 

  185. 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 35:8478–8482

    CAS  PubMed  Google Scholar 

  186. 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. Res Trends, Curr Top Biochem Res 6:111–144

    CAS  Google Scholar 

  187. Koch KW, Duda T, Sharma RK (2002) Photoreceptor specific guanylate cyclases in vertebrate phototransduction. Mol Cell Biochem 230:97–106

    CAS  PubMed  Google Scholar 

  188. Burns ME, Baylor DA (2001) Activation, deactivation, and adaptation in vertebrate photoreceptor cells. Annu Rev Neurosci 24:779–805

    CAS  PubMed  Google Scholar 

  189. Kaupp UB, Seifert R (2002) Cyclic nucleotide-gated ion channels. Physiol Rev 82:769–824

    CAS  PubMed  Google Scholar 

  190. Pugh EN Jr, Lamb TD (2000) Phototransduction in vertebrate rods and cones: molecular mechanisms of amplification, recovery and light adaptation. In: Stavenga DG, DeGrip WJ, Pugh EN Jr (eds) Handbook of biological physics. Elsevier, North-Holland, pp 183–255

  191. Ridge KD, Abdulaev NG, Sousa M, Palczewski K (2003) Phototransduction: crystal clear. Trends Biochem Sci 28:479–487

    CAS  PubMed  Google Scholar 

  192. Pugh EN Jr, Nikonov S, Lamb TD (1999) Molecular mechanisms of vertebrate photoreceptor light adaptation. Curr Opin Neurobiol 9:410–418

    CAS  PubMed  Google Scholar 

  193. Hwang JY, Lange C, Helten A, Höppner-Heitmann D, Duda T, Sharma RK, Koch KW (2003) Regulatory modes of rod outer segment membrane guanylate cyclase differ in catalytic efficiency and Ca(2+)-sensitivity. Eur J Biochem 270:3814–3821

    CAS  PubMed  Google Scholar 

  194. Olshevskaya EV, Ermilov AN, Dizhoor AM (1999) Dimerization of guanylyl cyclase-activating protein and a mechanism of photoreceptor guanylyl cyclase activation. J Biol Chem 274:25583–25587

    CAS  PubMed  Google Scholar 

  195. Hwang JY, Schlesinger R, Koch KW (2004) Irregular dimerization of guanylate cyclase-activating protein 1 mutants causes loss of target activation. Eur J Biochem 271:3785–3793

    CAS  PubMed  Google Scholar 

  196. Hwang JY, Koch KW (2002) The myristoylation of the neuronal Ca2+-sensors guanylate cyclase-activating protein 1 and 2. Biochim Biophys Acta 1600:111–117

    CAS  PubMed  Google Scholar 

  197. Hwang JY, Koch KW (2002) Calcium- and myristoyl-dependent properties of guanylate cyclase-activating protein-1 and protein-2. Biochemistry 41:13021–13028

    CAS  PubMed  Google Scholar 

  198. Lange C, Duda T, Beyermann M, Sharma RK, Koch KW (1999) Regions in vertebrate photoreceptor guanylyl cyclase ROS-GC1 involved in Ca(2+)-dependent regulation by guanylyl cyclase-activating protein GCAP-1. FEBS Lett 460:27–31

    CAS  PubMed  Google Scholar 

  199. Krishnan A, Goraczniak RM, Duda T, Sharma RK (1998) Third calcium-modulated rod outer segment membrane guanylate cyclase transduction mechanism. Mol Cell Biochem 178:251–259

    CAS  PubMed  Google Scholar 

  200. Duda T, Fik-Rymarkiewicz E, Venkataraman V, Krishnan R, Koch KW, Sharma RK (2005) The calcium-sensor guanylate cyclase activating protein type 2 specific site in rod outer segment membrane guanylate cyclase type 1. Biochemistry 44:7336–7345

    CAS  PubMed  Google Scholar 

  201. Schrem A, Lange C, Beyermann M, Koch KW (1999) Identification of a domain in guanylyl cyclase-activating protein 1 that interacts with a complex of guanylyl cyclase and tubulin in photoreceptors. J Biol Chem 274:6244–6249

    CAS  PubMed  Google Scholar 

  202. 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 274:15547–15555

    CAS  PubMed  Google Scholar 

  203. Howes KA, Pennesi ME, Sokal I, Church-Kopish J, Schmidt B, Margolis D, Frederick JM, Rieke F, Palczewski K, Wu SM, Detwiler PB, Baehr W (2002) GCAP1 rescues rod photoreceptor response in GCAP1/GCAP2 knockout mice. EMBO J 21:1545–1554

    CAS  PubMed  Google Scholar 

  204. Pennesi ME, Howes KA, Baehr W, Wu SM (2003) Guanylate cyclase-activating protein (GCAP) 1 rescues cone recovery kinetics in GCAP1/GCAP2 knockout mice. Proc Natl Acad Sci USA 100:6783–6788

    CAS  PubMed  Google Scholar 

  205. Mendez A, Burns ME, Sokal I, Dizhoor AM, Baehr W, Palczewski K, Baylor DA, Chen J (2001) Role of guanylate cyclase-activating proteins (GCAPs) in setting the flash sensitivity of rod photoreceptors. Proc Natl Acad Ski USA 98:9948–9953

    CAS  Google Scholar 

  206. Duda T, Venkataraman V, Krishnan A, Sharma RK (1998) Rod outer segment membrane guanylate cyclase type 1 (ROS-GC1) gene: structure, organization and regulation by phorbol ester, a protein kinase C activator. Mol Cell Biochem 189:63–70

    CAS  PubMed  Google Scholar 

  207. Yang RB, Fülle HJ, Garbers DL (1996) Chromosomal localization and genomic organization of genes encoding guanylyl cyclase receptors expressed in olfactory sensory neurons and retina. Genomics 31:367–372

    CAS  PubMed  Google Scholar 

  208. Johnston JP, Farhangfar F, Aparicio JG, Nam SH, Applebury ML (1997) The bovine guanylate cyclase GC-E gene and 5′ flanking region. Gene 193:219–227

    CAS  PubMed  Google Scholar 

  209. Duda T, Koch KW (2002) Retinal diseases linked with photoreceptor guanylate cyclase. Mol Cell Biochem 230:129–138

    CAS  PubMed  Google Scholar 

  210. Perrault I, Rozet JM, Calvas P, Gerber S, Camuzat A, Dollfus H, Châtelin S, Souied E, Ghazi I, Leowski C, Bonnemaison M, Le Paslier D, Frézal J, Dufier JL, Pittler S, Munnich A, Kaplan J (1996) Retinal-specific guanylate cyclase gene mutations in Leber’s congenital amaurosis. Nat Genet 14:461–464

    CAS  PubMed  Google Scholar 

  211. Duda T, Venkataraman V, Goraczniak R, Lange C, Koch KW, Sharma RK (1999) Functional consequences of a rod outer segment membrane guanylate cyclase (ROS-GC1) gene mutation linked with Leber’s congenital amaurosis. Biochemistry 38:509–515

    CAS  PubMed  Google Scholar 

  212. Kelsell RE, Gregory-Evans K, Payne AM, Perrault I, Kaplan J, Yang RB, Garbers DL, Bird AC, Moore AT, Hunt DM (1998) Mutations in the retinal guanylate cyclase (RETGC-1) gene in dominant cone-rod dystrophy. Hum Mol Genet 7:1179–1184

    CAS  PubMed  Google Scholar 

  213. Duda T, Krishnan A, Venkataraman V, Lange C, Koch KW, Sharma RK (1999) Mutations in the rod outer segment membrane guanylate cyclase in a cone-rod dystrophy cause defects in calcium signaling. Biochemistry 38:13912–13919

    CAS  PubMed  Google Scholar 

  214. Duda T, Venkataraman V, Jankowska A, Lange C, Koch KW, Sharma RK (2000) Impairment of the rod outer segment membrane guanylate cyclase dimerization in a cone-rod dystrophy results in defective calcium signaling. Biochemistry 39:12522–12533

    CAS  PubMed  Google Scholar 

  215. Tucker CL, Woodcock SC, Kelsell RE, Ramamurthy V, Hunt DM, Hurley JB (1999) Biochemical analysis of a dimerization domain mutation in RetGC-1 associated with dominant cone-rod dystrophy. Proc Natl Acad Sci USA 96:9039–9044

    CAS  PubMed  Google Scholar 

  216. Newbold RJ, Deery EC, Walker CE, Wilkie SE, Srinivasan N, Hunt DM, Bhattacharya SS, Warren MJ (2001) The destabilization of human GCAP1 by a proline to leucine mutation might cause cone-rod dystrophy. Hum Mol Genet Jan 10:47–54

    CAS  Google Scholar 

  217. Dizhoor AM, Boikov SG, Olshevskaya EV (1998) Constitutive activation of photoreceptor guanylate cyclase by Y99C mutant of GCAP-1. Possible role in causing human autosomal dominant cone degeneration. J Biol Chem 273:17311–17314

    CAS  PubMed  Google Scholar 

  218. Sokal I, Li N, Surgucheva I, Warren MJ, Payne AM, Bhattacharya SS, Baehr W, Palczewski K (1998) GCAP1 (Y99C) mutant is constitutively active in autosomal dominant cone dystrophy. Mol Cell 2:129–133

    CAS  PubMed  Google Scholar 

  219. Wilkie SE, Li Y, Deery EC, Newbold RJ, Garibaldi D, Bateman JB, Zhang H, Lin W, Zack DJ, Bhattacharya SS, Warren MJ, Hunt DM, Zhang K (2001) Identification and functional consequences of a new mutation (E155G) in the gene for GCAP1 that causes autosomal dominant cone dystrophy. Am J Hum Genet 69:471–480

    CAS  PubMed  Google Scholar 

  220. Cooper N, Liu L, Yoshida A, Pozdnyakov N, Margulis A, Sitaramayya A (1995) The bovine rod outer segment guanylate cyclase, ROS-GC, is present in both outer segment and synaptic layers of the retina. J Mol Neurosci 6:211–222

    CAS  PubMed  Google Scholar 

  221. Liu X, Seno K, Nishizawa Y, Hayashi F, Yamazaki A, Matsumoto H, Wakabayashi T, Usukura J (1994) Ultrastructural localization of retinal guanylate cyclase in human and monkey retinas. Exp Eye Res 59(6):761–768

    CAS  PubMed  Google Scholar 

  222. Redburn DA, Thomas TN (1979) Isolation of synaptosomal fractions from rabbit retina. J Neurosci Methods 1:235–242

    CAS  PubMed  Google Scholar 

  223. Venkataraman V, Duda T, Vardi N, Koch K-W, Sharma RK (2003) Calcium-modulated guanylate cyclase transduction machinery in the photoreceptor–bipolar synaptic region. Biochemistry 42:5640–5648

    CAS  PubMed  Google Scholar 

  224. Krizaj D, Copenhagen DR (2002) Calcium regulation in photoreceptors. Front Biosci 7:d2023–d2044

    CAS  PubMed  Google Scholar 

  225. Pozdnyakov N, Goraczniak R, Margulis A, Duda T, Sharma RK, Yoshida A, Sitaramayya A (1997) Structural and functional characterization of retinal calcium-dependent guanylate cyclase activator protein (CD-GCAP): identity with S100beta protein. Biochemistry 36:14159–14166

    CAS  PubMed  Google Scholar 

  226. 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 34:14279–14283

    CAS  PubMed  Google Scholar 

  227. 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 35:6263–6266

    CAS  PubMed  Google Scholar 

  228. Duda T, Goraczniak RM, Pozdnyakov N, Sitaramayya A, Sharma RK (1998) Differential activation of rod outer segment membrane guanylate cyclases, ROS-GC1 and ROS-GC2, by CD-GCAP and identification of the signaling domain. Biochem Biophys Res Commun 242:118–122

    CAS  PubMed  Google Scholar 

  229. Margulis A, Pozdnyakov N, Sitaramayya A (1996) Activation of bovine photoreceptor guanylate cyclase by S100 proteins. Biochem Biophys Res Commun 218:243–247

    CAS  PubMed  Google Scholar 

  230. Duda T, Koch KW, Venkataraman V, Lange C, Beyermann M, Sharma RK (2002) Ca(2+) sensor S100beta-modulated sites of membrane guanylate cyclase in the photoreceptor-bipolar synapse. EMBO J 21:2547–2556

    CAS  PubMed  Google Scholar 

  231. Terasawa M, Nakano A, Kobayashi R, Hidaka H (1992) Neurocalcin: a novel calcium-binding protein from bovine brain. J Biol Chem 267:19596–19599

    CAS  PubMed  Google Scholar 

  232. Okazaki K, Watanabe M, Ando Y, Hagiwara M, Terasawa M, Hidaka H (1992) Full sequence of neurocalcin, a novel calcium-binding protein abundant in central nervous system. Biochem Biophys Res Commun 185:147–153

    CAS  PubMed  Google Scholar 

  233. 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 38:12614–12620

    CAS  PubMed  Google Scholar 

  234. Kumar VD, Hidaka H, Okazaki K, Vijay-Kumar S (1996) Crystallization and preliminary X-ray crystallographic studies of recombinant bovine neurocalcin delta. Proteins 25:261–264

    CAS  PubMed  Google Scholar 

  235. Vijay-Kumar S, Kumar VD (1999) Crystal structure of recombinant bovine neurocalcin. Nat Struct Biol 6:80–88

    CAS  PubMed  Google Scholar 

  236. Matsumura H, Shiba T, Inoue T, Harada S, Kai Y (1998) A novel mode of target recognition suggested by the 2.0 A structure of holo S100B from bovine brain. Structure 6:233–241

    CAS  PubMed  Google Scholar 

  237. Duda T, Venkataraman V, Sharma RK (2007) Constitution and operational principles of the retinal and odorant-linked neurocalcin δ-dependent Ca2+ modulated ROS-GC transduction machinery. In: Philipov P, Koch KW (eds) Neuronal calcium sensor proteins. Nova Science Publishers, Inc, New York

    Google Scholar 

  238. Krishnan A, Venkataraman V, Fik-Rymarkiewicz E, Duda T, Sharma RK (2004) Structural, biochemical, and functional characterization of the calcium sensor neurocalcin delta in the inner retinal neurons and its linkage with the rod outer segment membrane guanylate cyclase transduction system. Biochemistry 43:2708–2723

    CAS  PubMed  Google Scholar 

  239. Burgess WH, Jemiolo DK, Kretsinger RH (1980) Interaction of calcium and calmodulin in the presence of sodium dodecyl sulfate. Biochim Biophys Acta 623:257–270

    CAS  PubMed  Google Scholar 

  240. Ladant D (1995) Calcium and membrane binding properties of bovine neurocalcin delta expressed in Escherichia coli. J Biol Chem 270:3179–3185

    CAS  PubMed  Google Scholar 

  241. Duda T, Venkataraman V, Krishnan A, Nagele RG, Sharma RK (2001) Negatively calcium-modulated membrane guanylate cyclase signaling system in the rat olfactory bulb. Biochemistry 40:4654–4662

    CAS  PubMed  Google Scholar 

  242. Shepherd GM, Greer CA (1998) Olfactory bulb. In: Shepherd GM (ed) The synaptic organization of the brain. Oxford University Press, New York, pp 159–203

  243. Pinching AJ, Powell TP (1971) The neuron types of the glomerular layer of the olfactory bulb. J Cell Sci 9:305–345

    CAS  PubMed  Google Scholar 

  244. 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 40:12067–12077

    CAS  PubMed  Google Scholar 

  245. Duda T, Fik-Rymarkiewicz E, Venkataraman V, Krishnan A, Sharma RK (2004) Calcium-modulated ciliary membrane guanylate cyclase transduction machinery: constitution and operational principles. Mol Cell Biochem 267:107–122 (erratum in: Mol Cell Biochem 273:225–226, 2005)

    CAS  PubMed  Google Scholar 

  246. Fülle HJ, Vassar R, Foster DC, Yang RB, Axel R, Garbers DL (1999) A receptor guanylyl cyclase expressed specifically in olfactory sensory neurons. Proc Natl Acad Sci USA 92:3571–3575

    Google Scholar 

  247. 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 signa transduction pathway. Proc Natl Acad Sci USA 94:3388–3395

    CAS  PubMed  Google Scholar 

  248. Meyer MR, Angele A, Kremmer E, Kaupp UB, Muller F (2000) A cGMP-signaling pathway in a subset of olfactory sensory neurons. Proc Natl Acad Sci USA 97:10595–10600

    CAS  PubMed  Google Scholar 

  249. Moon C, Jaberi P, Otto-Bruc A, Baehr W, Palczewski K, Ronnett GV (1998) Calcium-sensitive particulate guanylyl cyclase as a modulator of cAMP in olfactory receptor neurons. J Neurosci 18:3195–3205

    CAS  PubMed  Google Scholar 

  250. Duda T, Sharma RK (2004) S100B-modulated Ca2+-dependent ROS-GC1 transduction machinery in the gustatory epithelium: a new mechanism in gustatory transduction. FEBS Lett 577:393–398

    CAS  PubMed  Google Scholar 

  251. Herness MS, Gilbertson TA (1999) Cellular mechanisms of taste transduction. Annu Rev Physiol 61:873–900

    CAS  PubMed  Google Scholar 

  252. Yamamoto T, Nagai T, Shimura T, Yasoshima Y (1998) Roles of chemical mediators in the taste system. Jpn J Pharmacol 76:325–348

    CAS  PubMed  Google Scholar 

  253. Misaka T, Kusakabe Y, Emori Y, Arai S, Abe K (1998) Molecular cloning and taste bud-specific expression of a novel cyclic nucleotide-gated channel. Ann N Y Acad Sci 855:150–159

    CAS  PubMed  Google Scholar 

  254. Asanuma N, Nomura H (1995) Cytochemical localization of guanylyl cyclase activity in rabbit taste bud cells. Chem Senses 20:231–237

    CAS  PubMed  Google Scholar 

  255. Doolin RE, Gilbertson TA (1996) Distribution and characterization of functional amiloride-sensitive sodium channels in rat tongue. J Gen Physiol 107:545–554

    CAS  PubMed  Google Scholar 

  256. Jaiswal RK, Sharma RK (1985) Purification and biochemical characterization of alpha 2-adrenergic receptor from the rat adrenocortical carcinoma. Biochem Biophys Res Commun 130:58–64

    CAS  PubMed  Google Scholar 

  257. Bylund DB, Eikenberg DC, Hieble JP, Langer SZ, Lefkowitz RJ, Minneman KP, Molinoff PB, Ruffolo RR Jr, Trendelenburg U (1994) International Union of Pharmacology nomenclature of adrenoreceptors. Pharmacol Rev 46:121–136

    CAS  PubMed  Google Scholar 

  258. Lanier SM, Downing S, Duzic E, Homcy CJ (1991) Isolation of rat genomic clones encoding subtypes of the alpha 2-adrenergic receptor. Identification of a unique receptor subtype. J Biol Chem 266:10470–10478

    CAS  PubMed  Google Scholar 

  259. O’Rourke MF, Iversen LJ, Lomasney JW, Bylund DB (1994) Species orthologs of the alpha-2A adrenergic receptor: the pharmacological properties of the bovine and rat receptors differ from the human and porcine receptors. J Pharmacol Exp Ther 271:735–740

    PubMed  Google Scholar 

  260. Venkataraman V, Duda T, Sharma RK (1999) Alpha2D/A-adrenergic receptor gene induction in the retina by phorbol ester: involvement of an AP-2 element. Genes Cells 4:161–173

    CAS  PubMed  Google Scholar 

  261. Venkataraman V, Duda T, Sharma RK (1998) The alpha(2D/A)-adrenergic receptor-linked membrane guanylate cyclase: a new signal transduction system in the pineal gland. FEBS Lett 427:69–73

    CAS  PubMed  Google Scholar 

  262. Venkataraman V, Nagele R, Duda T, Sharma RK (2000) Rod outer segment membrane guanylate cyclase type 1-linked stimulatory and inhibitory calcium signaling systems in the pineal gland: biochemical, molecular, and immunohistochemical evidence. Biochemistry 39:6042–6052

    CAS  PubMed  Google Scholar 

  263. Yang RB, Foster DC, Garbers DL, Fülle HJ (1995) Two membrane forms of guanylyl cyclase found in the eye. Proc Natl Acad Sci USA 92:602–606

    CAS  PubMed  Google Scholar 

  264. Takahashi JS, Recourse PJ, Bauman L, Menace M (1984) Spectral sensitivity of a novel photoreceptive system mediating entrainment of mammalian circadian rhythms. Nature 308:186–188

    CAS  PubMed  Google Scholar 

  265. Korf HW, Schomerus C, Stehle JH (1998) The pineal organ, its hormone melatonin, and the photoneuroendocrine system. Adv Anat Embryol Cell Biol 146:1–100

    CAS  PubMed  Google Scholar 

  266. Racké K, Krupa H, Schröder H, Vollrath L (1989) In vitro synthesis of dopamine and noradrenaline in the isolated rat pineal gland: day-night variations and effects of electrical stimulation. J Neurochem 53:354–361

    PubMed  Google Scholar 

  267. Duda T, Sharma RK (2008) ONE-GC membrane guanylate cyclase, a trimodal odorant signal transducer. Biochem Biophys Res Commun 367:440–445

    CAS  PubMed  Google Scholar 

  268. Garbers DL (1976) Sea urchin sperm guanylate cyclase. Purification and loss of cooperativity. J Biol Chem 251:4071–4077

    CAS  PubMed  Google Scholar 

  269. Garbers DL (1978) Sea urchin sperm guanylate cyclase antibody. Cross-reactivity various rat tissue guanylate cyclases. J Biol Chem 253:1898–1901

    CAS  PubMed  Google Scholar 

  270. Garbers DL, Murad F (1979) Guanylate cyclase assay methods. Adv Cyclic Nucleotide Res 10:57–67

    CAS  PubMed  Google Scholar 

  271. White AA, Zenser TV (1974) Preparation and characterization of guanylate cyclase from bovine lung. Methods Enzymol 38:192–195

    CAS  PubMed  Google Scholar 

  272. Keirns JJ, Miki N, Bitensky MW (1974) Preparation of vertebrate photoreceptor membranes for study of adenylate cyclase, guanylate cyclase, and cyclic nucleotide phosphodiesterase. Methods Enzymol 38:153–155

    CAS  PubMed  Google Scholar 

  273. Schultz G (1974) General principles of assays for adenylate cyclase and guanylate cyclase activity. Methods Enzymol 38:115–125

    CAS  PubMed  Google Scholar 

  274. Seifert W, Rudland PS (1974) Proceedings: cyclic GMP, guanylate cyclase and growth control. Hoppe Seylers Z Physiol Chem 355:1255

    CAS  PubMed  Google Scholar 

  275. Garbers DL, Suddath JL, Hardman JG (1975) Enzymatic formation of inosine 3′,5′-monophosphate and of 2′-deoxyguanosine 3′,5′-monophosphate. Inosinate and deoxyguanylate cyclase activity. Biochim Biophys Acta 377:174–185

    CAS  PubMed  Google Scholar 

  276. Chrisman TD, Garbers DL, Parks MA, Hardman JG (1975) Characterization of particulate and soluble guanylate cyclases from rat lung. J Biol Chem 250:374–381

    CAS  PubMed  Google Scholar 

  277. Virmaux N, Nullans G, Goridis C (1976) Guanylate cyclase in vertebrate retina: evidence for specific association with rod outer segments. J Neurochem 26:233–235

    CAS  PubMed  Google Scholar 

  278. 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 278:33150–33160

    CAS  PubMed  Google Scholar 

  279. Yamazaki M, Usukura J, Yamazaki RK, Yamazaki A (2005) ATP binding is required for physiological activation of retinal guanylate cyclase. Biochem Biophys Res Commun 338:1291–1298

    CAS  PubMed  Google Scholar 

  280. Antos LK, Abbey-Hosch SE, Flora DR, Potter LR (2005) ATP-independent activation of natriuretic peptide receptors. J Biol Chem 280:26928–26932

    CAS  PubMed  Google Scholar 

  281. Burczynska B, Duda T, Sharma RK (2007) ATP signaling site in the ARM domain of atrial natriuretic factor receptor guanylate cyclase. Mol Cell Biochem 301:93–107

    CAS  PubMed  Google Scholar 

  282. 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 272:5572–5583

    CAS  PubMed  Google Scholar 

  283. 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 1478:30–38

    CAS  PubMed  Google Scholar 

  284. Labrecque J, Mc Nicoll N, Marquis M, De Léan A (1999) A disulfide-bridged mutant of natriuretic peptide receptor-A displays constitutive activity. Role of receptor dimerization in signal transduction. J Biol Chem 274:9752–9759

    CAS  PubMed  Google Scholar 

  285. 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 324:39–53

    CAS  PubMed  Google Scholar 

  286. Potter LR, Hunter T (2001) Guanylyl cyclase-linked natriuretic peptide receptors: structure and regulation. J Biol Chem 276:6057–6060

    CAS  PubMed  Google Scholar 

  287. 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 268:5997–6003

    CAS  PubMed  Google Scholar 

  288. Burgoyne RD (2007) Neuronal calcium sensor proteins: generating diversity in neuronal Ca2+ signalling. Nat Rev Neurosci 8:182–193

    CAS  PubMed  Google Scholar 

  289. Koch KW (2006) GCAPs, the classical neuronal calcium sensors in the retina—a Ca2+-relay model of guanylate cyclase activation. Calcium Binding Proteins 1:3–6

    Google Scholar 

  290. Ramamurthy V, Tucker C, Wilkie SE, Daggett V, Hunt DM, Hurley JB (2001) Interactions within the coiled-coil domain of RetGC-1 guanylyl cyclase are optimized for regulation rather than for high affinity. J Biol Chem 276:26218–26229

    CAS  PubMed  Google Scholar 

  291. 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 272:13738–13742

    CAS  PubMed  Google Scholar 

  292. Venkataraman V, Duda T, Ravichandran S, Sharma RK (2008) Neurocalcin delta Modulation of ROS-GC1, a new model of Ca(2+) signaling. Biochemistry 47:6590–6601

    CAS  PubMed  Google Scholar 

  293. Sharma RK, Duda T (2006) Calcium sensor neurocalcin δ-modulated ROS-GC transduction machinery in the retinal and olfactory neurons. Calcium Binding Proteins 1:7–11

    CAS  Google Scholar 

  294. 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 104:14507–14512

    CAS  PubMed  Google Scholar 

  295. Duda T, Sharma RK (2009) Ca2+-modulated ONE-GC odorant signal transduction. FEBS Lett 583:1327–1330

    CAS  PubMed  Google Scholar 

  296. Krishnan A, Duda T, Pertzev A, Kobayashi M, Takamatsu K, Sharma RK (2009) Hippocalcin, new Ca(2+) sensor of a ROS-GC subfamily member, ONE-GC, membrane guanylate cyclase transduction system. Mol Cell Biochem 325:1–14

    CAS  PubMed  Google Scholar 

  297. Fik-Rymarkiewicz E, Duda T, Sharma RK (2006) Novel frequenin-modulated Ca2+-signaling membrane guanylate cyclase (ROS-GC) transduction pathway in bovine hippocampus. Mol Cell Biochem 291:187–204

    CAS  PubMed  Google Scholar 

  298. Duda T, Krishnan R, Sharma RK (2006) GCAP1, antithetical calcium sensor of ROS-GC transduction machinery. Calcium Binding Proteins 1:102–107

    Google Scholar 

  299. 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 106:2041–2046

    CAS  PubMed  Google Scholar 

  300. Guo D, Zhang JJ, Huang XY (2009) Stimulation of guanylyl cyclase-D by bicarbonate. Biochemistry 48:4417–4422

    CAS  PubMed  Google Scholar 

  301. Hu J, Zhong C, Ding C, Chi Q, Walz A, Mombaerts P, Matsunami H, Luo M (2007) Detection of near-atmospheric concentrations of CO2 by an olfactory subsystem in the mouse. Science 317:953–957

    CAS  PubMed  Google Scholar 

  302. Fleischer J, Mamasuew K, Breer H (2009) Expression of cGMP signaling elements in the Grueneberg ganglion. Histochem Cell Biol 131:75–88

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This investigator expresses his gratitude to all the fellows for their contributions in his laboratory; to Dr. Teresa Duda for her dedication, collegiality and contributions in these studies; to Drs. Ari Sitaramayya and Karl-Wilhelm Koch for fruitful collaborations. He is indebted to his wife Joan Sharma for her patience and continuous moral support; to his daughter Sanya S. Khajuria for spending painful hours in editing this manuscript. He feels fortunate to have the friendship and support of Dr. Naranjan S. Dhalla, Distinguished Professor, University of Manitoba, Winnipeg, Canada. He gratefully acknowledges the continuous support for the last 35 years by the numerous USPHS awards from the National Institutes of Health, the beginning awards from the National Science Foundation and the Damon Runyon Walter Winchell Cancer Fund. At present, this investigator is the Distinguished Professor of Biochemistry and Molecular Biology in the Salus University; he is thankful to Dr. Anthony Di Stefano, Academic Vice President, for awarding him this honor.

Author information

Authors and Affiliations

  1. Research Divisions of Biochemistry and Molecular Biology, The Unit of Regulatory and Molecular Biology, Salus University, Elkins Park, PA, 19027, USA

    Rameshwar K. Sharma

Authors
  1. Rameshwar K. Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rameshwar K. Sharma.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sharma, R.K. Membrane guanylate cyclase is a beautiful signal transduction machine: overview. Mol Cell Biochem 334, 3–36 (2010). https://doi.org/10.1007/s11010-009-0336-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11010-009-0336-6

Keywords

Search

Navigation