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Evolution of the membrane guanylate cyclase transduction system

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Abstract

Almost four decades of research in the field of membrane guanylate cyclases is discussed in this review. Primarily, it focuses on the chronological development of the field, recognizes major contributions of the original investigators, corrects certain misplaced facts, and projects its future trend.

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References

  1. Sutherland EW, Rall TW: Fractionation and characterization of a cyclic adenine ribonucleotide formed by tissue particles. J Biol Chem 232: 1077–1091, 1958

    Google Scholar 

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

    Google Scholar 

  3. Robison GA, Butcher RW, Sutherland EW: Adenyl cyclase as an adrenergic receptor. Ann NY Acad Sci 139: 703–723, 1967

    Google Scholar 

  4. Ariens EJ, Simonis AM: Aspects of molecular pharmacology. II. Theories of receptors and structure-action relationships. Farmaco Sci 21: 581–608, 1966

    Google Scholar 

  5. Ariens EJ: The structure-activity relationships of beta adrenergic drugs and beta adrenergic blocking drugs. Ann NY Acad Sci 139: 606–631, 1967

    Google Scholar 

  6. Birnbaumer L, Pohl SL, Michiel H, Krans MJ, Rodbell M: The actions of hormones on the adenyl cyclase system. Adv Biochem Psychopharmacol: 185–208, 1970

  7. Rodbell M, Birnbaumer L, Pohl SL, Krans HM: Properties of the adenyl cyclase systems in liver and adipose cells: The mode of action of hormones. Acta Diabetol Lat 7(suppl 1): 9–63, 1970

    Google Scholar 

  8. Rodbell M, Lin MC, Salomon Y, Londos C, Harwood JP, Martin BR, Rendell M, Berman M: The role of adenine and guanine nucleotides in the activity and response of adenylate cyclase systems to hormones: Evidence for multi-site transition states. Acta Endocrinol (Copenhagen) 191(suppl): 11–37, 1974

    Google Scholar 

  9. Rodbell M, Lin MC, Salomon Y, Londos C, Harwood JP, Martin BR, Rendell M, Berman M: Role of adenine and guanine nucleotides in the activity and response of adenylate cyclase systems to hormones: Eevidence for multisite transition states. Adv Cyclic Nucleotide Res 5: 3–29, 1975

    Google Scholar 

  10. Hepler JR, Gilman AG: G proteins. Trends Biochem Sci 17: 383–387, 1992

    Google Scholar 

  11. Birnbaumer L, Birnbaumer M: Signal transduction by G proteins: 1994 edition. J Recept Signal Transduct Res 15: 213–252, 1995

    Google Scholar 

  12. Feder D, Im MJ, Klein HW, Hekman M, Holzhofer A, Dees C, Levitzki A, Helmreich EJ, Pfeuffer T: Reconstitution of beta 1-adrenoceptor-dependent adenylate cyclase from purified components. EMBO J 5: 1509–1514, 1986. Erratum in: EMBO J 5: 3408, 1986

    Google Scholar 

  13. Negishi M, Ito S, Yokohama H, Hayashi H, Katada T, Ui M, Hayaishi O: Functional reconstitution of prostaglandin E receptor from bovine adrenal medulla with guanine nucleotide binding proteins. J Biol Chem 263: 6893–6900, 1988

    Google Scholar 

  14. Bansal VS, Majerus PW: Phosphatidylinositol-derived precursors and signals. Annu Rev Cell Biol 6: 41–67, 1990

    Google Scholar 

  15. Harden TK: G-protein-regulated phospholipase C. Identification of component proteins. Adv Sec Mess Phosphoprot Res 26: 11–34, 1992

    Google Scholar 

  16. Berridge MJ, Irvine RF: Inositol phosphates and cell signalling. Nature 341: 197–205, 1989

    Google Scholar 

  17. Nishizuka Y: The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature 334: 661–665, 1988

    Google Scholar 

  18. Strader CD, Fong TM, Tota MR, Underwood D, Dixon RA: Structure and function of G-protein-coupled receptors. Annu Rev Biochem 63: 101–132, 1994

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  22. Goldberg ND, O'Dea RF, Haddox MK: Cyclic GMP. Adv Cyclic Nucleotide Res 3: 155–223, 1973

    Google Scholar 

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

    Google Scholar 

  24. Schultz G, Bohme E, Munske K: Guanyl cyclase. Determination of enzyme activity. Life Sci 8: 1323–3213, 1969

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  32. Goldberg ND, Haddox MK, Hartle DK, Hadden JW: The biological role of cyclic 3′,5′-guanosine monophosphate. In: Krager and Basel (eds). Pharmacology and the Future of Man. Fifth International Congress on Pharmacology, San Francisco. Vol. 5, 1972, pp 146–169

  33. Goldberg ND, Haddox MK, Dunham E, Lopez C, Hadden JW: 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: B. Clarkson and R. Baserga (eds). The Cold Spring Harbor Symposium on the Regulation of Proliferation in Animal Cells. Cold Spring Harbor Laboratory, New York, 1974, pp 609–625

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  41. Somlyo AP, Somlyo AV, Friedmann N: Cyclic adenosine monophosphate, cyclic guanosine monophosphate, and glucagon: Effects on membrane potential and ion fluxes in the liver. Ann NY Acad Sci 185: 108–114, 1971

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  47. Murad F, Mittal C, Arnold WP, Ichikara K, Braughler M, El-Zayat M: Properties and regulation of guanylate cyclase: Activation by azide, nitro compounds, and hydroxyl radical and effects of heme containing proteins. In: G. Folco, R. Paolottie (eds). Molecular Biology and Pharmacology of Cyclic Nucleotides. Elsevier, Amsterdam, Netherlands, 1978, pp 33–42

    Google Scholar 

  48. Murad F, Mittal CK, Arnold WP, Katsuki S, Kimura H: 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, 1978

    Google Scholar 

  49. Mittal CK, Murad F: Properties and oxidative regulation of guanylate cyclase. J Cyclic Nucleotide Res 3: 381–391, 1977

    Google Scholar 

  50. Arnold WP, Mittal CK, Katsuki S, Murad F: 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, 1977

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  54. Mittal CK, Murad F: 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, 1977

    Google Scholar 

  55. Katsuki S, Arnold W, Mittal C, Murad F: 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, 1977

    Google Scholar 

  56. Katsuki S, Arnold WP, Murad F: 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, 1977

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  59. Bohme E, Grossmann G, Herz J, Mulsch A, Spies C, Schultz G: Regulation of cyclic GMP formation by soluble guanylate cyclase: Stimulation by NO-containing compounds. Adv Cyclic Nucleotide Prot Phosphoryl Res 17: 259–266, 1984

    Google Scholar 

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

    Google Scholar 

  61. Waldman SA, Sinacore MS, Lewicki JA, Chang LY, Murad F: Selective activation of particulate guanylate cyclase by a specific class of porphyrins. J Biol Chem 259: 4038–4042, 1984

    Google Scholar 

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

    Google Scholar 

  63. Sharma RK, Jaiswal RK, Duda T: Second messenger role of cyclic GMP in atrial natriuretic factor receptor mediated signal transduction: 180-kD 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., 1988, pp 77–96

  64. Sharma RK, Marala RB, Paul AK: Mediatory role of cyclic GMP in receptor-mediated signal transduction: Membrane guanylate cyclase and its coupling with atrial natriuretic factor receptor. In: B.M. Brenner, J.H. Laragh (eds). Advances in Peptide research, vol. II: American Society of Hypertension Symposium Series. Raven Press, New York, 1988, pp 61–77

    Google Scholar 

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

    Google Scholar 

  66. Pugh EN Jr, Duda T, Sitaramayya A, Sharma RK: Photoreceptor guanylate cyclases: A review. Biosci Rep 17: 29–73, 1997

    Google Scholar 

  67. Rall TW, Sutherland EW: The regulatory role of adenosine-3′,5′-phosphate. Cold Spring Harbor Symposia on Quantitative Biology 26: 347–354, 1961

    Google Scholar 

  68. Haynes RC Jr, Berthet L: Studies on the mechanism of action of the adrenocortictropic hormone. J Biol Chem 225: 115–124, 1957

    Google Scholar 

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

    Google Scholar 

  70. Sayers G: In: C.H. Gray (ed). Hormones in Blood. Academic Press, New York and London, 1967, pp 169–194

    Google Scholar 

  71. Garren LD: The mechanism of action of adrenocorticotropic hormone. Vitam Horm 26: 119–145, 1968

    Google Scholar 

  72. Bronsome ED Jr: Adrenal cortex. Annu Rev Physiol 30: 171–212,1968

    Google Scholar 

  73. Halkerston IDK: Cyclic AMP and adrenocortical function. Adv Cyclic Nucleotide Res 6: 99–136, 1975

    Google Scholar 

  74. Sharma RK, Sawhney RS: 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, 1978

    Google Scholar 

  75. Robinson GA, Butcher RW, Sutherland EW: In: Cyclic AMP. Academic Press, New York, 1971

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  82. Sharma RK: Abnormal Adrenocorticotropic hormone control in adrenocortical carcinoma. In: Sharma and Criss (eds). Endocrine Control of Neoplasia. Raven Press, New York, 1978, pp 13–52

    Google Scholar 

  83. Sharma RK, Ahmed NK, Sutliff L, 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, 1974

    Google Scholar 

  84. Sharma RK, Ahmed NK, Shanker G: 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, 1976

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  88. Neri G, Gambino AM, Mazzocchi G, Nussdorfer GG: 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, 1978

    Google Scholar 

  89. Sharma RK: 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, 1973

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  93. Rasmussen H: In: Calcium and Cyclic AMP as Synarchic Messengers. John Wiley & Sons Inc., New York, 1981

    Google Scholar 

  94. Kitabchi AE, Wilson DB, Sharma RK: 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, 1971

    Google Scholar 

  95. Hayashi K, Sala G, Catt K, Dufau ML: Regulation of steroidogenesis by adrenocorticotropic hormone in isolated adrenal cells. J Biol Chem 254: 6678–6683, 1979

    Google Scholar 

  96. Sayers G, Ma RM, Giordano ND: Isolated adrenal cells: corticosterone production in response to cyclic AMP (adenosine-3′,5′-monophosphate). Proc Soc Exp Biol Med 136: 619–622, 1971

    Google Scholar 

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

    Google Scholar 

  98. Ahrens H, Paul AK, Kuroda Y, Sharma RK: 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, 1982

    Google Scholar 

  99. Nambi P, Aiyar NV, Sharma RK: Adrenocorticotropin-dependent particulate guanylate cyclase in rat adrenal and adrenocortical carcinoma: Comparison of its properties with soluble guanylate cyclase and its relationship with AC TH-induced steroidogenesis. Arch Biochem Biophys 217: 638–646, 1982

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  102. Sharma RK, Marala RB, Duda T: 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, 1989

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  105. Paul AK: Particulate guanylate cyclase from adrenocortical carcinoma Purification, biochemical and immunological characterization. Doctoral thesis, University of Tennessee, 1986

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

    Google Scholar 

  107. Sharma RK: Guanylate cyclase and the adrenal natriuretic factor receptor. Response to S.A. Waldman, D.C. Leitman, J. Andresen, F. Murad. Science 240: 805–806, 1988

    Google Scholar 

  108. Kuno T, Andresen JW, Kamisaki Y, Waldman SA, Chang LY, Saheki S, Leitman DC, Nakane M, Murad F: Co-purification of an atrial natriuretic factor receptor and particulate guanylate cyclase from rat lung. J Biol Chem 261: 5817–5823, 1986

    Google Scholar 

  109. Takayanagi R, Inagami T, Snajdar RM, Imada T, Tamura M, Misono KS: 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, 1987

    Google Scholar 

  110. Meloche S, McNicoll N, Liu B, Ong H, De Lean A: Atrial natriuretic factor R1 receptor from bovine adrenal zona glomerulosa: Purification, characterization, and modulation by amiloride. Biochemistry 27: 8151–8158, 1988

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  116. de Bold AJ: Atrial natriuretic factor: An overview. Fed Proc 45: 2081–2085, 1986

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  119. Chartier L, Schiffrin E, Thibault G, Garcia R: 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: 2026–2028, 1984

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

    Google Scholar 

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

    Google Scholar 

  122. Pandey KN, Kovacs WJ, Inagami T: The inhibition of progesterone secretion and the regulation of cyclic nucleotides by atrial natriuretic factor in gonadotropin responsive murine Leydig tumor cells. Biochem Biophys Res Commun 133: 800–806, 1985

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  128. Chinkers M, Garbers DL, Chang MS, Lowe DG, Chin HM, Goeddel DV, Schulz S: A membrane form of guanylate cyclase is an atrial natriuretic peptide receptor. Nature 338: 78–83, 1989

    Google Scholar 

  129. Lowe DG, Chang MS, Hellmiss R, Chen E, Singh S, Garbers DL, Goeddel DV: Human atrial natriuretic peptide receptor defines a new paradigm for second messenger signal transduction. EMBO J: 1377–13784, 1989

  130. Schulz S, Singh S, Bellet RA, Singh G, Tubb DJ, Chin H, Garbers DL: The primary structure of a plasma membrane guanylate cyclase demonstrates diversity within this new receptor family. Cell: 1155–1162, 1989

  131. Chang MS, Lowe DG, Lewis M, Hellmiss R, Chen E, Goeddel DV: Differential activation by atrial and brain natriuretic peptides of two different receptor guanylate cyclases. Nature 341: 68–72, 1989

    Google Scholar 

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

    Google Scholar 

  133. Marala R, Duda T, Goraczniak RM, Sharma RK: 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, 1992

    Google Scholar 

  134. Schulz S, Green CK, Yuen PS, Garbers DL: Guanylyl cyclase is a heatstable enterotoxin receptor. Cell 63: 941–948, 1990

    Google Scholar 

  135. Singh S, Singh G, Heim JM, Gerzer R: 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, 1991

    Google Scholar 

  136. de Sauvage FJ, Camerato TR, Goeddel DV: Primary structure and functional expression of the human receptor for Escherichia coli heatstable enterotoxin. J Biol Chem 266: 17912–17918, 1991

    Google Scholar 

  137. Wada A, Hirayama T, Kitao S, Fujisawa J, Hidaka Y, Shimonishi Y: Pig intestinal membrane-bound receptor (guanylyl cyclase) for heatstable enterotoxin: cDNA cloning, functional expression, and characterization. Microbiol Immunol 38: 535–541, 1994

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  140. 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: Uroguanylin: Structure and activity of a second endogenous peptide that stimulates intestinal guanylate cyclase. Proc Natl Acad Sci USA: 10464–10468, 1993

  141. Khare S, Wilson D, Wali RK, Tien XY, Bissonnette M, Niedziela SM, Bolt MJ, Sitrin MD, Brasitus TA: Guanylin activates rat colonic particulate guanylate cyclase. Biochem Biophys Res Commun 203: 1432–1437, 1994

    Google Scholar 

  142. Koch KW: Purification and identification of photoreceptor guanylate cyclase. J Biol Chem 266: 8634–8637, 1991

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  148. Lowe DG, Dizhoor AM, Liu K, Gu Q, Spencer M, Laura R, Lu L, Hurley JB: Cloning and expression of a second photoreceptor-specific membrane retina guanylyl cyclase (RetGC), RetGC-2. Proc Natl Acad Sci USA 92: 5535–5539, 1995

    Google Scholar 

  149. Goraczniak RM, Duda T, Sharma RK: Calcium modulated signaling site in type 2 rod outer segment membrane guanylate cyclase (ROSGC2). Biochem Biophys Res Commun 245: 447–453, 1998

    Google Scholar 

  150. Duda T, Venkataraman V, Krishnan A, Sharma RK: 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, 1998

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  157. Wilkie SE, Newbold RJ, Deery E, Walker CE, Stinton I, Ramamurthy V, Hurley JB, Bhattacharya SS, Warren MJ, Hunt DM: Functional characterization of missense mutations at codon 838 in retinal guanylate cyclase correlates with disease severity in patients with autosomal dominant cone-rod dystrophy. Hum Mol Genet 9: 3065–3073, 2000

    Google Scholar 

  158. Ramamurthy V, Tucker C, Wilkie SE, Daggett V, Hunt DM, Hurley JB: 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, 2001

    Google Scholar 

  159. Fulle HJ, Vassar R, Foster DC, Yang RB, Axel R, Garbers DL: A receptor guanylyl cyclase expressed specifically in olfactory sensory neurons. Proc Natl Acad Sci USA 92: 3571–3575, 1995

    Google Scholar 

  160. Koch KW, Stryer L: Highly cooperative feedback control of retinal rod guanylate cyclase by calcium ions. Nature 334: 64–66, 1988

    Google Scholar 

  161. 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 PB, Baehr W: Molecular cloning and characterization of retinal photoreceptor guanylyl cyclase-activating protein. Neuron 13: 395–404, 1994

    Google Scholar 

  162. Dizhoor AM, Olshevskaya EV, Henzel WJ, Wong SC, Stults JT, Ankoudinova I, Hurley JB: Cloning, sequencing, and expression of a 24-kDa Ca(2+)-binding protein activating photoreceptor guanylyl cyclase. J Biol Chem 270: 25200–25206, 1995

    Google Scholar 

  163. Frins S, Bonigk W, Muller F, Kellner R, Koch KW: Functional characterization of a guanylyl cyclase-activating protein from vertebrate rods. Cloning, heterologous expression, and localization. J Biol Chem 271: 8022–8027, 1996

    Google Scholar 

  164. Pozdnyakov N, Yoshida A, Cooper NG, Margulis A, Duda T, Sharma RK, Sitaramayya A: A novel calcium-dependent activator of retinal rod outer segment membrane guanylate cyclase. Biochemistry 34: 14279–14283, 1995

    Google Scholar 

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

    Google Scholar 

  166. Haeseleer F, Sokal I, Li N, Pettenati M, Rao N, Bronson D, Wechter R, Baehr W, Palczewski K: Molecular characterization of a third member of the guanylyl cyclase-activating protein subfamily. J Biol Chem 274: 6526–6535, 1999

    Google Scholar 

  167. Kumar VD, Vijay-Kumar S, Krishnan A, Duda T, Sharma RK: A second calcium regulator of rod outer segment membrane guanylate cyclase, ROS-GC1: Neurocalcin. Biochemistry 38: 12614–12620, 1999

    Google Scholar 

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

    Google Scholar 

  169. Cooper N, Liu L, Yoshida A, Pozdnyakov N, Margulis A, Sitaramayya A: 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, 1995

    Google Scholar 

  170. Venkataraman V, Nagele R, Duda T, Sharma RK: 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, 2000

    Google Scholar 

  171. Duda T, Venkataraman V, Krishnan A, Nagele RG, Sharma RK: Negatively calcium-modulated membrane guanylate cyclase signaling system in the rat olfactory bulb. Biochemistry 40: 465446-465462, 2001

    Google Scholar 

  172. Venkataraman V, Duda T, Sharma RK: The alpha2D/A-adrenergic receptor-linked membrane guanylate cyclase: A new signal transduction system in the pineal gland. FEBS Lett 427: 69–73, 1998

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  175. Sharma RK: Two operational modes of transmembrane migration of cyclic GMP signaling pathway. In: K.N. Prasad, F.L. Meyskens Jr (eds). Nutrients and Cancer Prevention. The Humana Press, 1990, pp 3–18

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

    Google Scholar 

  177. Nambi P, Aiyar NV, Sharma RK: Solubilization of epinephrine-specific alpha-adrenergic receptors from adrenocortical carcinoma. FEBS Lett 140: 98–102, 1982

    Google Scholar 

  178. Nambi P, Aiyar NV, Sharma RK: Identification and characterization of ectopic alpha2-adrenergic receptors in adrenocortical carcinoma membranes. J Nutr Growth Cancer 1: 77–84, 1983

    Google Scholar 

  179. Chalberg SC, Duda T, Rhine JA, Sharma RK: Molecular cloning, sequencing and expression of an alpha2-adrenergic receptor complementary DNA from rat brain. Mol Cell Biochem 97: 161–172, 1990

    Google Scholar 

  180. Lanier SM, Downing S, Duzic E, Homcy CJ: Isolation of rat genomic clones encoding subtypes of the alpha2-adrenergic receptor. Identification of a unique receptor subtype. J Biol Chem 266: 10470–10478, 1991

    Google Scholar 

  181. O'Rourke MF, Iversen LJ, Lomasney JW, Bylund DB: 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, 1994

    Google Scholar 

  182. Wypijewski K, Duda T, Sharma RK: Structural, genetic and pharmacological identity of the rat alpha2-adrenergic receptor subtype cA2-47 and its molecular characterization in rat adrenal, adrenocortical carcinoma and bovine retina. Mol Cell Biochem 144: 181–190, 1995

    Google Scholar 

  183. Kobilka BK, Matsui H, Kobilka TS, Yang-Feng TL, Francke U, Caron MG, Lefkowitz RJ, Regan JW: Cloning, sequencing, and expression of the gene coding for the human platelet alpha2-adrenergic receptor. Science 238: 650–656, 1987

    Google Scholar 

  184. Regan JW, Nakata H, DeMarinis RM, Caron MG, Lefkowitz RJ: Purification and characterization of the human platelet alpha2-adrenergic receptor. J Biol Chem 261: 3894–3900, 1986

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  187. Duda T, Goraczniak RM, Sharma RK: Site-directed mutational analysis of a membrane guanylate cyclase cDNA reveals the atrial natriuretic factor signaling site. Proc Natl Acad Sci USA 88: 7882–7886, 1991

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  190. van den Akker F, Zhang X, Miyagi M, Huo X, Misono KS, Yee VC: Structure of the dimerized hormone-binding domain of a guanylylcyclase-coupled receptor. Nature 406: 101–104, 2000

    Google Scholar 

  191. Kurose H, Inagami T, Ui M: Participation of adenosine 5′-triphosphate in the activation of membrane-bound guanylate cyclase by the atrial natriuretic factor. FEBS Lett 219: 375–379, 1987

    Google Scholar 

  192. Chang CH, Kohse KP, Chang B, Hirata M, Jiang B, Douglas JE, Murad F: Characterization of ATP-stimulated guanylate cyclase activation in rat lung membranes. Biochim Biophys Acta 1052: 159–165, 1990

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  195. Chinkers M, Singh S, Garbers DL: Adenine nucleotides are required for activation of rat atrial natriuretic peptide receptor/guanylyl cyclase expressed in a baculovirus system. J Biol Chem 266: 4088–4093, 1991

    Google Scholar 

  196. Duda T, Goraczniak RM, Sitaramayya A, Sharma RK: Cloning and expression of an ATP-regulated human retina C-type natriuretic factor receptor guanylate cyclase. Biochemistry 32: 1391–1395, 1993

    Google Scholar 

  197. Lowe DG: The guanylate cylase-B receptor. Natriuretic peptides in health and disease. Series: Contemp Endocrinol 5: 35–50, 1997

    Google Scholar 

  198. Foster DC, Garbers DL: Dual role for adenine nucleotides in the regulation of the atrial natriuretic peptide receptor, guanylyl cyclase-A. Biol Chem 273: 16311–16318, 1998

    Google Scholar 

  199. Duda T, Yadav P, Jankowska A, Venkataraman V, Sharma RK: Three dimensional atomic model and experimental validation for the ATPRegulated Module (ARM) of the atrial natriuretic factor receptor guanylate cyclase. Mol Cell Biochem. 214: 7–14, 2000. Reprinted in: ibid 217: 165-172, 2001

    Google Scholar 

  200. Goraczniak RM, Duda T, Sharma RK: A structural motif that defines the ATP-regulatory module of guanylate cyclase in atrial natriuretic factor signalling. Biochem J 282: 533–537, 1992

    Google Scholar 

  201. Sharma RK, Yadav P, Duda T: Allosteric regulatory step and configuration of the ATP-binding pocket in atrial natriuretic factor receptor guanylate cyclase transduction mechanism. Can J Physiol Pramacol 79: 682–691, 2001

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  205. Koller KJ, de Sauvage FJ, Lowe DG, Goeddel DV: Conservation of the kinase-like regulatory domain is essential for activation of the natriuretic peptide receptor guanylyl cyclases. Mol Cell Biol 12: 2581–2590, 1992

    Google Scholar 

  206. Duda T, Goraczniak RM, Sharma RK: The glycine residue of ATP regulatory module in receptor guanylate cyclases that is essential in natriuretic factor signaling. FEBS Lett 335: 309–314, 1993

    Google Scholar 

  207. Larose L, McNicoll N, Ong H, De Lean A: Allosteric modulation by ATP of the bovine adrenal natriuretic factor R1 receptor functions. Biochemistry 30: 8990–8995, 1991

    Google Scholar 

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

    Google Scholar 

  209. Duda T, Sharma RK: 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, 1995

    Google Scholar 

  210. Duda T, Sharma RK: 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, 1995

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  213. Potter LR, Hunter T: A constitutively ‘phosphorylated’ guanylyl cyclase-linked atrial natriuretic peptide receptor mutant is resistant to desensitization. Mol Biol Cell 10: 1811–1820, 1999

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  216. Larose L, Rondeau JJ, Ong H, De Lean A: Phosphorylation of atrial natriuretic factor R1 receptor by serine/threonine protein kinases: Evidences for receptor regulation. Mol Cell Biochem 115: 203–211, 1992

    Google Scholar 

  217. Krishnan A, Goraczniak RM, Duda T, Sharma RK: Third calciummodulated rod outer segment membrane guanylate cyclase transduction mechanism. Mol Cell Biochem 178: 251–259, 1998

    Google Scholar 

  218. Duda T, Goraczniak R, Surgucheva I, Rudnicka-Nawrot M, Gorczyca WA, Palczewski K, Sitaramayya A, Baehr W, Sharma RK: Calcium modulation of bovine photoreceptor guanylate cyclase. Biochemistry 35: 8478–8482, 1996

    Google Scholar 

  219. Laura RP, Dizhoor AM, Hurley JB: The membrane guanylyl cyclase, retinal guanylyl cyclase-1, is activated through its intracellular domain. J Biol Chem 271: 11646–11651, 1996

    Google Scholar 

  220. Sokal I, Li N, Verlinde CL, Haeseleer F, Baehr W, Palczewski K: Ca(2+)-binding proteins in the retina: From discovery to etiology of human disease. Biochim Biophys Acta 1498: 233–251, 2000

    Google Scholar 

  221. Downes SM, Holder GE, Fitzke FW, Payne AM, Warren MJ, Bhattacharya SS, Bird AC: Autosomal dominant cone and cone-rod dystrophy with mutations in the guanylate cyclase activator 1A gene-encoding guanylate cyclase activating protein-1. Arch Ophthalmol 119: 96–105, 2001

    Google Scholar 

  222. Dizhoor AM: Regulation of cGMP synthesis in photoreceptors: Role in signal transduction and congenital diseases of the retina. Cell Signal 12: 711–719, 2000

    Google Scholar 

  223. Lange C, Duda T, Beyermann M, Sharma RK, Koch KW: 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, 1999

    Google Scholar 

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

    Google Scholar 

  225. Sokal I, Haeseleer F, Arendt A, Adman ET, Hargrave PA, Palczewski K: Identification of a guanylyl cyclase-activating protein-binding site within the catalytic domain of retinal guanylyl cyclase 1. Biochemistry 38: 1387–1393, 1999

    Google Scholar 

  226. Krylov DM, Hurley JB: Identification of proximate regions in a complex of retinal guanylyl cyclase 1 and guanylyl cyclase activating protein-1 by a novel mass spectrometry based method. J Biol Chem 2001

  227. Tucker CL, Laura RP, Hurley JB: Domain-specific stabilization of photoreceptor membrane guanylyl cyclase by adenine nucleotides and guanylyl cyclase activating proteins (GCAPs) Biochemistry 36: 11995–12000, 1997

    Google Scholar 

  228. Laura RP, Hurley JB: The kinase homology domain of retinal guanylyl cyclases 1 and 2 specifies the affinity and cooperativity of interaction with guanylyl cyclase activating protein-2. Biochemistry 37: 11264–11271, 1998

    Google Scholar 

  229. McInnes C, Sykes BD: Growth factor receptors: structure, mechanism, and drug discovery. Biopolymers 43: 339–366, 1997

    Google Scholar 

  230. Heldin CH: Dimerization of cell surface receptors in signal transduction. Cell 80: 213–223, 1995

    Google Scholar 

  231. Tesmer JJ, Sunahara RK, Gilman AG, Sprang SR: Crystal structure of the catalytic domains of adenylyl cyclase in a complex with Gsalpha. GTPgammaS. Science 278: 1907–1916, 1997

    Google Scholar 

  232. Giuili G, Scholl U, Bulle F, Guellaen G: Molecular cloning of the cDNAs coding for the two subunits of soluble guanylyl cyclase from human brain. FEBS Lett 304: 83–88, 1992

    Google Scholar 

  233. Harteneck C, Koesling D, Soling A, Schlutz G, Bohme F: Expression of soluble guanylyl cyclase. Catalytic activity requires two enzyme subunits. FEBS Lett 272: 221–223, 1990

    Google Scholar 

  234. Chinkers M, Wilson E: Ligand-independent oligomerization of natriuretic peptide receptors. Identification of heteromeric receptors and a dominant negative mutant. J Biol Chem 267: 18589–18597, 1992

    Google Scholar 

  235. Thorpe DS, Niu S, Morkin E: Overexprression of dimeric guanylyl cyclase cores of an atrial natriuretic peptide receptor. Biochem Biophys Res Commun 180: 538–544, 1991

    Google Scholar 

  236. Wilson E, Chinkers M: Identification of sequences mediating guanylyl cyclase dimerization. Biochemistry 34: 4696–4701, 1995

    Google Scholar 

  237. Lowe DG: Human natriuretic peptide receptor-A guanylyl cyclase is self-associated prior to hormone binding. Biochemistry 31: 10421–10425, 1992

    Google Scholar 

  238. Labrecque J, McNicoll N, Marquis M, DeLean A: A disulfide-bridged mutant of natriuretic peptide receptor-A displays constitutive activity. J Biol Chem 274: 9752–9759, 1999

    Google Scholar 

  239. Labrecque J, Deschenes J, McNicoll N, DeLean A: 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: 8064–8072, 2001

    Google Scholar 

  240. Yu H, Olshevskaya E, Duda T, Seno K, Hayashi F, Sharma RK, Dizhoor AM, Yamazaki A: Activation of retinal guanylyl cyclase-1 by Ca2+-binding proteins involves its dimerization. J Biol Chem 274: 15547–15555, 1999

    Google Scholar 

  241. Olshevskaya E, Ermilow AE, Dizhoor AM: Dimerization of guanylyl cyclase-activating protein and a mechanism of photoreceptor guanylyl cyclase activation. J Biol Chem 274: 25583–25587, 1999

    Google Scholar 

  242. Donato R: S100: A multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int J Biochem Cell Biol 33: 637–668, 2001

    Google Scholar 

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

    Google Scholar 

  244. Perrault I, Rozet JM, Gerber S, Kelsell RE, Souied E, Cabout A, Hunt H, Munnich A, Kaplan J: A ret-GC1 mutation in autosomal dominant cone-rod dystrophy. Am J Hum Genet 63: 651–654, 1998

    Google Scholar 

  245. van Ghelue M, Eriksen HL, Ponjavic V, Fagerheim T, Andreasson S, Forsman-Semb K, Sandgren O, Holmgren G, Tranebjaerg L. Autosomal dominant cone-rod dystrophy due to a missense mutation (R838C) in the guanylate cyclase 2D gene (GUCY2D) with preserved rod function in one branch of the family. Ophthalmic Genet 21: 197–209, 2000

    Google Scholar 

  246. Gregory-Evans K, Kelsell RE, Gregory-Evans CY, Downes SM, Fitzke FW, Holder GE, Simunovic M, Mollon JD, Taylor R, Hunt DM, Bird AC, Moore AT: Autosomal dominant cone-rod retinal dystrophy (CORD6) from heterozygous mutation of GUCY2D, which encodes retinal guanylate cyclase. Ophthalmology 107: 55–61, 2000

    Google Scholar 

  247. Weigell-Weber M, Fokstuen S, Torok B, Niemeyer G, Schinzel A, Hergersberg M: Codons 837 and 838 in the retinal guanylate cyclase gene on chromosome 17p: Hot spots for mutations in autosomal dominant cone-rod dystrophy? Arch Ophthalmol 118: 300, 2000

    Google Scholar 

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Sharma, R.K. Evolution of the membrane guanylate cyclase transduction system. Mol Cell Biochem 230, 3–30 (2002). https://doi.org/10.1023/A:1014280410459

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