Skip to main content
Log in

Three dimensional atomic model and experimental validation for the ATP-regulated module (ARM) of the atrial natriuretic factor receptor guanylate cyclase

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

Atrial natriuretic factor (ANF) receptor guanylate cyclase (ANF-RGC) is a single chain transmembrane-spanning protein, containing both ANF binding and catalytic activities. ANF binding to the extracellular receptor domain activates the cytosolic catalytic domain, generating the second messenger cyclic GMP. Obligatory in this activation process is an intervening transduction step, which is regulated by the binding of ATP to the cyclase. The partial structural motif of the ATP binding domain of the cyclase has been elucidated and has been termed ATP Regulatory Module (ARM). The crystal structures of the tyrosine kinase domains of the human insulin receptor and haematopoietic cell kinase were used to derive a homology-based model of the ARM domain of ANF-RGC. The model identifies the precise configuration of the ATP-binding pocket in the ARM domain, accurately represents its ATP-dependent features, and shows that the ATP-dependent transduction phenomenon is a two-step mechanism. In the first step, ATP binds to its pocket and changes its configuration; in the second step, via an unknown protein kinase, it phosphorylates the cyclase for its full activation.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

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

    Google Scholar 

  2. Ignarro LJ, Cirino G, Casini A, Napoli C: Nitric oxide as a signaling molecule in the vascular system: An overview. J Cardiovasc Pharmacol 34: 879–886, 1999

    Google Scholar 

  3. Paul AK, Marala RB, Jaiswal RK, Sharma RK: Coexistence of atrial natriuretic factor receptor and guanylate cyclase in a Mr 180,000 protein of rat adrenocortical carcinoma membranes. Science 235: 1224–1226, 1987

    Google Scholar 

  4. Chinkers M, Garbers DL, Chang MS, Lowe DG, Chin H, Goeddel DV, Schultz S: Molecular cloning of a new type of cell surface receptor: A membrane form of guanylate cyclase is an atrial natriuretic peptide receptor. Nature 338: 78–83, 1989

    Google Scholar 

  5. 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 

  6. Chinkers M, Wilson EM: Ligand independent oligomerization of natriuretic peptide receptors. J Biol Chem 267: 18589–18597, 1992

    Google Scholar 

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

    Google Scholar 

  8. 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 

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

    Google Scholar 

  10. 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 

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

    Google Scholar 

  12. Koch KW: Purification and identification of photoreceptor guanylate cyclase. J Biol Chem 266: 86334–8637, 1991

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  15. Kuno T, Andersson W, 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 

  16. 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 

  17. Chang M-S, 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 

  18. 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, 1995

    Google Scholar 

  19. Koller KJ, Lowe DG, Bennett GL, Minamino N, Kangawa K, Matsuo H, Goeddel DV: Selective activation of the B natriuretic peptide receptor by C-type natriuretic peptide. Science 252: 121–123, 1991

    Google Scholar 

  20. Schulz S, Green CK, Yuen PST, Garbers DL: Guanylyl cyclase is a heat-stable enterotoxin receptor. Cell 179: 941–948, 1990

    Google Scholar 

  21. 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 

  22. de Bold AJ: Atrial natriuretic factor; a hormone produced by the heart. Science 230: 767–770, 1985

    Google Scholar 

  23. Sudoh T, Kangawa K, Minamino N, Matsuo H: A new natriuretic peptide in porcine brain. Nature (Lond) 332: 78–81, 1988

    Google Scholar 

  24. Ogawa Y, Itoh H, Nakao K: Molecular biology and biochemistry of natriuretic peptide family. Clin Exp Pharmacol Physiol. 22: 49–53, 1995

    Google Scholar 

  25. John SW, Krege JH, Oliver PM, Hagaman JR, Hodgin JB, Pang SC, Flynn TG, Smithies O: Genetic decreases in atrial natriuretic peptide and salt-sensitive hypertension. Science 267: 679–681, 1995

    Google Scholar 

  26. Lopez MJ, Wong SK, Kishimoto I, Dubois S, Mach V, Friesen J, Garbers DL, Beuve A: Salt-resistant hypertension in mice lacking the guanylyl cyclase-A receptor for atrial natriuretic peptide. Nature 378: 65–68, 1995

    Google Scholar 

  27. Kojima M, Minamino N, Kangawa K, Matsuo H: Cloning and sequence analysis of a cDNA encoding a precursor for rat C-type natriuretic peptide (CNP). FEBS Lett 76: 209–213, 1990

    Google Scholar 

  28. Sorci G, Spreca A, Donato R, Rambotti MG: Detection of membranebound guanylate cyclase activity in rat C6 glioma cells at different growth states following activation by natriuretic peptides. Brain Res 683: 51–58, 1995

    Google Scholar 

  29. Duda T, Goraczniak RM, Sharma RK: 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: 286–292, 1995

    Google Scholar 

  30. Sharma RK, Duda T: Plasma membrane guanylate cyclase. A multimodule transduction system. In: Honn (ed). Eicosanoids and Other Bioactive Lipids in Cancer Inflammation and Radiation Injury. Plenum Press, NY 1997, pp 271–279

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  35. 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 

  36. 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 

  37. 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 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  41. Hubbard SR, Wei L, Ellis L, Hendrickson WA: Crystal structure of the tyrosine kinase domain of the human insulin receptor. Nature 372: 746–753, 1994

    Google Scholar 

  42. Sicheri F, Moarefi I, Kuriyan J: Crystal structure of the Src family tyrosine kinase Hck. Nature 385: 602–609, 1997

    Google Scholar 

  43. Sambrook J, Fritsch EF, Maniatis T: In: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, 1989

    Google Scholar 

  44. Nambi P, Aiyar N, Sharma RK: Relationship of calcium and membrane guanylate cyclase in adrenocorticotropin-induced steroidogenesis. Endocrinology 111: 196–200, 1981

    Google Scholar 

  45. Knighton DR, Zheng JH, Ten Eyck LF, Ashford VA, Xuong NH, Taylor SS, Sowadski JM: Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science 253: 407–414, 1991

    Google Scholar 

  46. 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 

  47. 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 

  48. Marala RB, 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 

  49. Potter LR, Hunter T: Phosphorylation of the kinase homology domain is essential for activation of the A-type natriuretic peptide receptor. Mol Cell Biol 18: 2164–2172, 1998

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Duda, T., Yadav, P., Jankowska, A. et al. 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, 7–14 (2000). https://doi.org/10.1023/A:1007144328682

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1007144328682

Navigation