Zum Hauptinhalt springen
Artikel
Lizenziert
Nicht lizenziert Erfordert eine Authentifizierung

Soluble guanylate cyclase in NO signaling transduction

  • Xiangshi Tan is a Professor of Chemistry and Biomedical Science of Fudan University, Shanghai, China. He received his PhD degree from Nanjing University in 1996, and after that he did postdoctoral research in CEA/Grenoble, France; Edinburgh University, UK; Ibaraki University, Japan. In 2000, Dr. Tan moved to Texas A & M University, USA and worked there for almost 8 years as a research scientist of Bioinorganic Chemistry. In 2007, he took the full Professor position of Fudan University, and he is also a visiting Professor of Texas A & M University. Dr. Tan’s research activities focus on Bioinorganic Chemistry & Chemical Biology of metalloenzymes and metalloproteins in physiology and pathology.

    ,

    Jie Pan is a PhD student in the Department of Chemistry of Fudan University, China. Her research is focused on structure, functions and mechanism of soluble guanylate cyclase (sGC). She has been working with Prof. Tan for more than 3 years on the project of sGC.

    und

    Fangfang Zhong received her PhD degree in Bioinorganic Chemistry from Fudan University in 2012 under the supervision of Prof. Tan, where her research activity was mainly focused on the expression, characterization and molecular mechanism of NO-signaling mediated by human soluble guanylate cyclase. She is currently a postdoctoral research associate at Dartmouth College, USA.

    EMAIL logo
Veröffentlicht/Copyright: 17. September 2013

Abstract

Nitric oxide (NO), a signaling molecule in the cardiovascular system, has been receiving increasing attention since Furchgott, Ignarro, and Murad were awarded the Nobel Prize in Physiology and Medicine for the discovery in 1998. Soluble guanylate cyclase (sGC), as an NO receptor, is a key metalloprotein in mediating NO signaling transduction. sGC is activated by NO to catalyze the conversion of guanosine 5′-triphosphate (GTP) to cyclic guanylate monophosphate (cGMP). The dysfunction of NO signaling results in many pathological disorders, including several cardiovascular diseases, such as arterial hypertension, pulmonary hypertension, heart failure and so on. Significant advances in its structure, function, mechanism, and physiological and pathological roles have been made throughout the past 15 years. We herein review the progress of sGC on structural, functional investigations, as well as the proposed activation/deactivation mechanism. The heme-dependent sGC stimulators and heme-independent sGC activators have also been summarized briefly.


Corresponding author: Xiangshi Tan, Department of Chemistry and Institutes of Biomedical Sciences, Fudan University, Shanghai 200433, China, e-mail:

About the authors

Jie Pan

Xiangshi Tan is a Professor of Chemistry and Biomedical Science of Fudan University, Shanghai, China. He received his PhD degree from Nanjing University in 1996, and after that he did postdoctoral research in CEA/Grenoble, France; Edinburgh University, UK; Ibaraki University, Japan. In 2000, Dr. Tan moved to Texas A & M University, USA and worked there for almost 8 years as a research scientist of Bioinorganic Chemistry. In 2007, he took the full Professor position of Fudan University, and he is also a visiting Professor of Texas A & M University. Dr. Tan’s research activities focus on Bioinorganic Chemistry & Chemical Biology of metalloenzymes and metalloproteins in physiology and pathology.

Fangfang Zhong

Jie Pan is a PhD student in the Department of Chemistry of Fudan University, China. Her research is focused on structure, functions and mechanism of soluble guanylate cyclase (sGC). She has been working with Prof. Tan for more than 3 years on the project of sGC.

Xiangshi Tan

Fangfang Zhong received her PhD degree in Bioinorganic Chemistry from Fudan University in 2012 under the supervision of Prof. Tan, where her research activity was mainly focused on the expression, characterization and molecular mechanism of NO-signaling mediated by human soluble guanylate cyclase. She is currently a postdoctoral research associate at Dartmouth College, USA.

This work was supported partly by the National Natural Science Foundation of China (No. 91013001, No. 20771029, No. 31270869), the Ph.D. Program of the Education Ministry of China (20100071110011), the high magnetic field laboratory of Chinese Academy of Science, and the Shanghai Synchrotron Radiation Facility (SSRF).

References

Aono, S. Metal-containing sensor proteins sensing diatomic gas molecules. Dalton Trans.2008, 24, 3137–3146.Suche in Google Scholar

Artz, J.D.; Schmidt, B.; McCracken, J.L.; Marletta, M.A. Effects of nitroglycerin on soluble guanylate cyclase: implications for nitrate tolerance. J. Biol. Chem.2002, 277, 18253–18256.Suche in Google Scholar

Ballou, D.P.; Zhao, Y.; Brandish, P.E.; Marletta, M.A. Revisiting the kinetics of nitric oxide (NO) binding to soluble guanylate cyclase: the simple NO-binding model is incorrect. Proc. Natl. Acad. Sci. USA2002, 99, 12097–12101.Suche in Google Scholar

Bellamy, T.C.; Garthwaite, J. Sub-second kinetics of the nitric oxide receptor, soluble guanylyl cyclase, in intact cerebellar cells. J. Biol. Chem.2001, 276, 4287–4292.Suche in Google Scholar

Bellamy, T.C.; Wood, J.; Goodwin, D.A.; Garthwaite, J. Rapid desensitization of the nitric oxide receptor, soluble guanylyl cyclase, underlies diversity of cellular cGMP responses. Proc. Natl. Acad. Sci. USA2000, 97, 2928–2933.Suche in Google Scholar

Bellamy, T.C.; Wood, J.; Garthwaite, J. On the activation of soluble guanylyl cyclase by nitric oxide. Proc. Natl. Acad. Sci. USA2002, 99, 507–510.Suche in Google Scholar

Bischoff, E.; Stasch, J.P. Effects of the sGC stimulator BAY 41-2272 are not mediated by phosphodiesterase 5 inhibition. Circulation2004, 110, e320–321; author reply e320–321.10.1161/01.CIR.0000142209.28862.12Suche in Google Scholar

Brandish, P.E.; Buechler, W.; Marletta, M.A. Regeneration of the ferrous heme of soluble guanylate cyclase from the nitric oxide complex: acceleration by thiols and oxyhemoglobin. Biochemistry1998, 37, 16898–16907.Suche in Google Scholar

Brandwein, H.J.; Lewicki, J.A.; Murad, F. Reversible inactivation of guanylate cyclase by mixed disulfide formation. J. Biol. Chem.1981, 256, 2958–2962.Suche in Google Scholar

Cai, C.; Chen, S.Y.; Zheng, Z.; Omwancha, J.; Lin, M.F.; Balk, S.P.; Shemshedini, L. Androgen regulation of soluble guanylyl cyclasealpha1 mediates prostate cancer cell proliferation. Oncogene2007, 26, 1606–1615.Suche in Google Scholar

Cary, S.P.; Winger, J.A.; Marletta, M.A. Tonic and acute nitric oxide signaling through soluble guanylate cyclase is mediated by nonheme nitric oxide, ATP, and GTP. Proc. Natl. Acad. Sci. USA2005, 102, 13064–13069.Suche in Google Scholar

Chen, K.; Pittman, R.N.; Popel, A.S. Nitric oxide in the vasculature: where does it come from and where does it go? A quantitative perspective. Antioxid. Redox Signal2008a, 10, 1185–1198.10.1089/ars.2007.1959Suche in Google Scholar

Chen, L.; Lyubimov, A.Y.; Brammer, L.; Vrielink, A.; Sampson, N.S. The binding and release of oxygen and hydrogen peroxide are directed by a hydrophobic tunnel in cholesterol oxidase. Biochemistry2008b, 47, 5368–5377.10.1021/bi800228wSuche in Google Scholar

Chirkov, Y.Y.; Horowitz, J.D. Impaired tissue responsiveness to organic nitrates and nitric oxide: a new therapeutic frontier? Pharmacol. Ther.2007, 116, 287–305.Suche in Google Scholar

Coulter, J.A.; McCarthy, H.O.; Xiang, J.; Roedl, W.; Wagner, E.; Robson, T.; Hirst, D.G. Nitric oxide–a novel therapeutic for cancer. Nitric Oxide2008, 19, 192–198.10.1016/j.niox.2008.04.023Suche in Google Scholar

de Mel, A.; Murad, F.; Seifalian, A.M. Nitric oxide: a guardian for vascular grafts? Chem. Rev.2011, 111, 5742–5767.Suche in Google Scholar

DeMaster, E.G.; Quast, B.J.; Redfern, B.; Nagasawa, H.T. Reaction of nitric oxide with the free sulfhydryl group of human serum albumin yields a sulfenic acid and nitrous oxide. Biochemistry1995, 34, 11494–11499.Suche in Google Scholar

Denninger, J.W.; Marletta, M.A. Guanylate cyclase and the NO/cGMP signaling pathway. Biochim. Biophys. Acta1999, 1411, 334–350.Suche in Google Scholar

Derbyshire, E.R.; Marletta, M.A. Butyl isocyanide as a probe of the activation mechanism of soluble guanylate cyclase. Investigating the role of non-heme nitric oxide. J. Biol. Chem.2007, 282, 35741–35748.Suche in Google Scholar

Evgenov, O.V.; Pacher, P.; Schmidt, P.M.; Hasko, G.; Schmidt, H.H.; Stasch, J.P. NO-independent stimulators and activators of soluble guanylate cyclase: discovery and therapeutic potential. Nat.Rev. Drug Discov.2006, 5, 755–768.Suche in Google Scholar

Fernhoff, N.B.; Derbyshire, E.R.; Marletta, M.A. A nitric oxide/cysteine interaction mediates the activation of soluble guanylate cyclase. Proc. Natl. Acad. Sci. USA2009, 106, 21602–21607.Suche in Google Scholar

Fernhoff, N.B.; Derbyshire, E.R.; Underbakke, E.S.; Marletta, M.A. Heme-assisted S-nitrosation desensitizes ferric soluble guanylate cyclase to nitric oxide. J. Biol. Chem.2012, 287, 43053–43062.Suche in Google Scholar

Fritz, B.G.; Hu, X.; Brailey, J.L.; Berry, R.E.; Walker, F.A.; Montfort, W.R. Oxidation and loss of heme in soluble guanylyl cyclase from Manduca sexta. Biochemistry2011, 50, 5813–5815.Suche in Google Scholar

Fritz, B.G.; Roberts, S.A.; Ahmed, A.; Breci, L.; Li, W.; Weichsel, A.; Brailey, J.L.; Wysocki, V.H.; Tama, F.; Montfort, W.R. Molecular model of a soluble guanylyl cyclase fragment determined by small-angle X-ray scattering and chemical cross-linking. Biochemistry2013, 52, 1568–1582.Suche in Google Scholar

Furchgott, R.F.; Zawadzki, J.V. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature1980, 288, 373–376.Suche in Google Scholar

Ghofrani, H.A.; Hoeper, M.M.; Halank, M.; Meyer, F.J.; Staehler, G.; Behr, J.; Ewert, R.; Weimann, G.; Grimminger, F. Riociguat for chronic thromboembolic pulmonary hypertension and pulmonary arterial hypertension: a phase II study. Eur. Respir. J.2010, 36, 792–799.Suche in Google Scholar

Gladwin, M.T. Deconstructing endothelial dysfunction: soluble guanylyl cyclase oxidation and the NO resistance syndrome. J. Clin. Invest.2006, 116, 2330–2332.Suche in Google Scholar

Gorren, A.C.; Russwurm, M.; Kollau, A.; Koesling, D.; Schmidt, K.; Mayer, B. Effects of nitroglycerin/L-cysteine on soluble guanylate cyclase: evidence for an activation/inactivation equilibrium controlled by nitric oxide binding and haem oxidation. Biochem. J.2005, 390(Pt. 2), 625–631.Suche in Google Scholar

Haase, N.; Haase, T.; Kraehling, J.R.; Behrends, S. Direct fusion of subunits of heterodimeric nitric oxide sensitive guanylyl cyclase leads to functional enzymes with preserved biochemical properties: evidence for isoform specific activation by ciguates. Biochem. Pharmacol.2010, 80, 1676–1683.Suche in Google Scholar

Hall, C.N.; Garthwaite, J. What is the real physiological NO concentration in vivo? Nitric Oxide2009, 21, 92–103.Suche in Google Scholar

Harteneck, C.; Koesling, D.; Soling, A.; Schultz, G.; Bohme, E. Expression of soluble guanylyl cyclase. Catalytic activity requires two enzyme subunits. FEBS Lett.1990, 272, 221–223.Suche in Google Scholar

Harteneck, C.; Wedel, B.; Koesling, D.; Malkewitz, J.; Bohme, E.; Schultz, G. Molecular cloning and expression of a new alpha-subunit of soluble guanylyl cyclase. Interchangeability of the alpha-subunits of the enzyme. FEBS Lett.1991, 292, 217–222.Suche in Google Scholar

Hess, D.T.; Matsumoto, A.; Kim, S.O.; Marshall, H.E.; Stamler, J.S. Protein S-nitrosylation: purview and parameters. Nat. Rev. Mol. Cell Biol.2005, 6, 150–166.Suche in Google Scholar

Hill, B.G.; Dranka, B.P.; Bailey, S.M.; Lancaster, J.R. Jr.; Darley-Usmar, V.M. What part of NO don’t you understand? Some answers to the cardinal questions in nitric oxide biology. J. Biol. Chem.2010, 285, 19699–19704.Suche in Google Scholar

Hoffmann, L.S.; Schmidt, P.M.; Keim, Y.; Hoffmann, C.; Schmidt, H.H.; Stasch, J.P. Fluorescence dequenching makes haem-free soluble guanylate cyclase detectable in living cells. PLoS One2011, 6, e23596.10.1371/journal.pone.0023596Suche in Google Scholar

Hsieh, C.L.; Cai, C.; Giwa, A.; Bivins, A.; Chen, S.Y.; Sabry, D.; Govardhan, K.; Shemshedini, L. Expression of a hyperactive androgen receptor leads to androgen-independent growth of prostate cancer cells. J. Mol. Endocrinol.2008, 41, 13–23.Suche in Google Scholar

Ignarro, L.J.; Wood, K.S.; Wolin, M.S. Activation of purified soluble guanylate cyclase by protoporphyrin IX. Proc. Natl. Acad. Sci. USA1982a, 79, 2870–2873.10.1073/pnas.79.9.2870Suche in Google Scholar

Ignarro, L.J.; Degnan, J.N.; Baricos, W.H.; Kadowitz, P.J.; Wolin, M.S. Activation of purified guanylate cyclase by nitric oxide requires heme. Comparison of heme-deficient, heme-reconstituted and heme-containing forms of soluble enzyme from bovine lung. Biochim. Biophys. Acta1982b, 718, 49–59.10.1016/0304-4165(82)90008-3Suche in Google Scholar

Ignarro, L.J.; Byrns, R.E.; Buga, G.M.; Wood, K.S. Endothelium-derived relaxing factor from pulmonary artery and vein possesses pharmacologic and chemical properties identical to those of nitric oxide radical. Circ. Res.1987, 61, 866–879.Suche in Google Scholar

Iyer, L.M.; Anantharaman, V.; Aravind, L. Ancient conserved domains shared by animal soluble guanylyl cyclases and bacterial signaling proteins. BMC Genomics2003, 4, 5.10.1186/1471-2164-4-5Suche in Google Scholar PubMed PubMed Central

Iyer, A.K.; Azad, N.; Wang, L.; Rojanasakul, Y. Role of S-nitrosylation in apoptosis resistance and carcinogenesis. Nitric Oxide2008, 19, 146–151.Suche in Google Scholar

Karow, D.S.; Pan, D.; Davis, J.H.; Behrends, S.; Mathies, R.A.; Marletta, M.A. Characterization of functional heme domains from soluble guanylate cyclase. Biochemistry2005, 44, 16266–16274.Suche in Google Scholar

Kharitonov, V.G.; Russwurm, M.; Magde, D.; Sharma, V.S.; Koesling, D. Dissociation of nitric oxide from soluble guanylate cyclase. Biochem. Biophys. Res. Commun.1997, 239, 284–286.Suche in Google Scholar

Ko, F.N.; Wu, C.C.; Kuo, S.C.; Lee, F.Y.; Teng, C.M. YC-1, a novel activator of platelet guanylate cyclase. Blood1994, 84, 4226–4233.Suche in Google Scholar

Kosowicz, J.G.; Boon, E.M. Insights into the distal heme pocket of H-NOX using fluoride as a probe for H-bonding interactions. J. Inorg. Biochem.2013, 126C, 91–95.Suche in Google Scholar

Kumar, V.; Martin, F.E.; Hahn, M.G.; Schaefer, M.; Stamler, J.S.; Stasch, J.P.; van den Akker, F. Insights into BAY 60-2770 activation and S-nitrosylation-dependent desensitization of soluble guanylyl cyclase via crystal structures of homologous Nostoc H-NOX domain complexes. Biochemistry2013, 52, 3601–3608.Suche in Google Scholar

Lawson, D.M.; Stevenson, C.E.; Andrew, C.R.; Eady, R.R. Unprecedented proximal binding of nitric oxide to heme: implications for guanylate cyclase. EMBO J.2000, 19, 5661–5671.Suche in Google Scholar

Lewicki, J.A.; Brandwein, H.J.; Waldman, S.A.; Murad, F. Purified guanylate cyclase: characterization, iodination and preparation of monoclonal antibodies. J. Cyclic Nucleotide Res.1980, 6, 283–296.Suche in Google Scholar

Lima, B.; Forrester, M.T.; Hess, D.T.; Stamler, J.S. S-nitrosylation in cardiovascular signaling. Circ. Res.2010, 106, 633–646.Suche in Google Scholar

Lubos, E.; Handy, D.E.; Loscalzo, J. Role of oxidative stress and nitric oxide in atherothrombosis. Front. Biosci.2008, 13, 5323–5344.Suche in Google Scholar

Ma, X.; Sayed, N.; Beuve, A.; van den Akker, F. NO and CO differentially activate soluble guanylyl cyclase via a heme pivot-bend mechanism. EMBO J.2007, 26, 578–588.Suche in Google Scholar

Ma, X.; Sayed, N.; Baskaran, P.; Beuve, A.; van den Akker, F. PAS-mediated dimerization of soluble guanylyl cyclase revealed by signal transduction histidine kinase domain crystal structure. J. Biol. Chem.2008, 283, 1167–1178.Suche in Google Scholar

Ma, X.; Beuve, A.; van den Akker, F. Crystal structure of the signaling helix coiled-coil domain of the beta1 subunit of the soluble guanylyl cyclase. BMC Struct. Biol.2010, 10, 2.Suche in Google Scholar

Makino, R.; Matsuda, H.; Obayashi, E.; Shiro, Y.; Iizuka, T.; Hori, H. EPR characterization of axial bond in metal center of native and cobalt-substituted guanylate cyclase. J. Biol. Chem.1999, 274, 7714–7723.Suche in Google Scholar

Margulis, A.; Sitaramayya, A. Rate of deactivation of nitric oxide-stimulated soluble guanylate cyclase: influence of nitric oxide scavengers and calcium. Biochemistry2000, 39, 1034–1039.10.1021/bi992040pSuche in Google Scholar PubMed

Martinez-Ruiz, A.; Cadenas, S.; Lamas, S. Nitric oxide signaling: classical, less classical, and nonclassical mechanisms. Free Radic. Biol. Med.2011, 51, 17–29.Suche in Google Scholar

Mayer, B.; Kleschyov, A.L.; Stessel, H.; Russwurm, M.; Munzel, T.; Koesling, D.; Schmidt, K. Inactivation of soluble guanylate cyclase by stoichiometric S-nitrosation. Mol. Pharmacol.2009, 75, 886–891.Suche in Google Scholar

McLaughlin, V.V.; Archer, S.L.; Badesch, D.B.; Barst, R.J.; Farber, H.W.; Lindner, J.R.; Mathier, M.A.; McGoon, M.D.; Park, M.H.; Rosenson, R.S.; Rubin, L.J.; Tapson, V.F.; Varga, J.; Harrington, RA.; Anderson, JL.; Bates, E.R.; Bridges, C.R.; Eisenberg, M.J.; Ferrari, V.A.; Grines, C.L.; Hlatky, M.A.; Jacobs, A.K.; Kaul, S.; Lichtenberg, R.C.; Lindner, J.R.; Moliterno, D.J.; Mukherjee, D.; Pohost, G.M.; Rosenson, R.S.; Schofield, R.S.; Shubrooks. S.J.; Stein, J.H.; Tracy, C.M.; Weitz, H.H.; Wesley, D.J.; ACCF/AHA. ACCF/AHA 2009 expert consensus document on pulmonary hypertension: a report of the American College of Cardiology Foundation Task Force on Expert Consensus Documents and the American Heart Association: developed in collaboration with the American College of Chest Physicians, American Thoracic Society, Inc., and the Pulmonary Hypertension Association. Circulation2009, 119, 2250–2294.Suche in Google Scholar

Mergia, E.; Russwurm, M.; Zoidl, G.; Koesling, D. Major occurrence of the new alpha2beta1 isoform of NO-sensitive guanylyl cyclase in brain. Cell. Signal.2003, 15, 189–195.Suche in Google Scholar

Meurer, S.; Pioch, S.; Gross, S.; Muller-Esterl, W. Reactive oxygen species induce tyrosine phosphorylation of and Src kinase recruitment to NO-sensitive guanylyl cyclase. J. Biol. Chem.2005, 280, 33149–33156.Suche in Google Scholar

Miller, T.W.; Cherney, M.M.; Lee, A.J.; Francoleon, N.E.; Farmer, P.J.; King, S.B.; Hobbs, A.J.; Miranda, K.M.; Burstyn, J.N.; Fukuto, J.M. The effects of nitroxyl (HNO) on soluble guanylate cyclase activity: interactions at ferrous heme and cysteine thiols. J. Biol. Chem.2009, 284, 21788–21796.Suche in Google Scholar

Mittendorf, J.; Weigand, S.; Alonso-Alija, C.; Bischoff, E.; Feurer, A.; Gerisch, M.; Kern, A.; Knorr, A.; Lang, D.; Muenter, K.; Radtke, M.; Schirok, H.; Schlemmer, K.H.; Stahl, E.; Straub, A.; Wunder, F.; Stasch, J.P. Discovery of riociguat (BAY 63-2521): a potent, oral stimulator of soluble guanylate cyclase for the treatment of pulmonary hypertension. ChemMedChem2009, 4, 853–865.Suche in Google Scholar

Moglich, A.; Ayers, R.A.; Moffat, K. Structure and signaling mechanism of Per-ARNT-Sim domains. Structure2009, 17, 1282–1294.Suche in Google Scholar

Murad, F. Shattuck Lecture. Nitric oxide and cyclic GMP in cell signaling and drug development. N. Engl. J. Med.2006, 355, 2003–2011.Suche in Google Scholar

Murthy, K.S. Modulation of soluble guanylate cyclase activity by phosphorylation. Neurochem. Int.2004, 45, 845–851.Suche in Google Scholar

Nakane, M.; Arai, K.; Saheki, S.; Kuno, T.; Buechler, W.; Murad, F. Molecular cloning and expression of cDNAs coding for soluble guanylate cyclase from rat lung. J. Biol. Chem.1990, 265, 16841–16845.Suche in Google Scholar

Nioche, P.; Berka, V.; Vipond, J.; Minton, N.; Tsai, A.L.; Raman, C.S. Femtomolar sensitivity of a NO sensor from Clostridium botulinum. Science2004, 306, 1550–1553.Suche in Google Scholar

Pacher, P.; Beckman, J.S.; Liaudet, L. Nitric oxide and peroxynitrite in health and disease. Physiol. Rev.2007, 87, 315–424.Suche in Google Scholar

Pan, J.; Xu, Q.; Lin, Y.; Zhong, F.; Tan, X. Human soluble guanylate cyclase as a nitric oxide sensor for no-signalling reveals a novel function of nitrite reductase. ChemComm.2013, 49, 7454–7456.Suche in Google Scholar

Pankey, E.A.; Bhartiya, M.; Badejo, A.M. Jr.; Haider, U.; Stasch, J.P.; Murthy, S.N.; Nossaman, B.D.; Kadowitz, P.J. Pulmonary and systemic vasodilator responses to the soluble guanylyl cyclase activator, BAY 60-2770, are not dependent on endogenous nitric oxide or reduced heme. Am. J. Physiol. Heart Circ. Physiol.2011, 300, H792–802.Suche in Google Scholar

Pellicena, P.; Karow, D.S.; Boon, E.M.; Marletta, M.A.; Kuriyan, J. Crystal structure of an oxygen-binding heme domain related to soluble guanylate cyclases. Proc. Natl. Acad. Sci. USA2004, 101, 12854–12859.Suche in Google Scholar

Pifarre, P.; Baltrons, M.A.; Foldi, I.; Garcia, A. NO-sensitive guanylyl cyclase beta1 subunit is peripherally associated to chromosomes during mitosis. Novel role in chromatin condensation and cell cycle progression. Int. J. Biochem. Cell Biol.2009, 41, 1719–1730.Suche in Google Scholar

Potter, L.R. Guanylyl cyclase structure, function and regulation. Cell. Signal.2011, 23, 1921–1926.Suche in Google Scholar

Rauch, A.; Leipelt, M.; Russwurm, M.; Steegborn, C. Crystal structure of the guanylyl cyclase Cya2. Proc. Natl. Acad. Sci. USA2008, 105, 15720–15725.Suche in Google Scholar

Riego, J.A.; Broniowska, K.A.; Kettenhofen, N.J.; Hogg, N. Activation and inhibition of soluble guanylyl cyclase by S-nitrosocysteine: involvement of amino acid transport system L. Free Radic. Biol. Med.2009, 47, 269–274.Suche in Google Scholar

Rothkegel, C.; Schmidt, P.M.; Atkins, D.J.; Hoffmann, L.S.; Schmidt, H.H.; Schroder, H.; Stasch, J.P. Dimerization region of soluble guanylate cyclase characterized by bimolecular fluorescence complementation in vivo. Mol. Pharmacol.2007, 72, 1181–1190.Suche in Google Scholar

Russwurm, M.; Behrends, S.; Harteneck, C.; Koesling, D. Functional properties of a naturally occurring isoform of soluble guanylyl cyclase. Biochem. J.1998, 335 (Pt. 1), 125–130.Suche in Google Scholar

Russwurm, M.; Koesling, D. NO activation of guanylyl cyclase. EMBO J.2004, 23, 4443–4450.Suche in Google Scholar

Sayed, N.; Baskaran, P.; Ma, X.; van den Akker, F.; Beuve, A. Desensitization of soluble guanylyl cyclase, the NO receptor, by S-nitrosylation. Proc. Natl. Acad. Sci. USA2007, 104, 12312–12317.Suche in Google Scholar

Sayed, N.; Kim, D.D.; Fioramonti, X.; Iwahashi, T.; Duran, W.N.; Beuve, A. Nitroglycerin-induced S-nitrosylation and desensitization of soluble guanylyl cyclase contribute to nitrate tolerance. Circ. Res.2008, 103, 606–614.Suche in Google Scholar

Schindler, U.; Strobel, H.; Schönafinger, K.; Linz, W.; Löhn, M.; Martorana, P.A.; Rütten, H.; Schindler, P.W.; Busch, A.E.; Sohn, M; Töpfer, A; Pistorius, A; Jannek, C; Mülsch, A. Biochemistry and pharmacology of novel anthranilic acid derivatives activating heme-oxidized soluble guanylyl cyclase. Mol. Pharmacol.2006, 69, 1260–1268.Suche in Google Scholar

Schmidt, P.; Schramm, M.; Schroder, H.; Stasch, J.P. Mechanisms of nitric oxide independent activation of soluble guanylyl cyclase. Eur. J. Pharmacol.2003, 468, 167–174.Suche in Google Scholar

Schmidt, P.M.; Schramm, M.; Schroder, H.; Wunder, F.; Stasch, J.P. Identification of residues crucially involved in the binding of the heme moiety of soluble guanylate cyclase. J. Biol. Chem.2004, 279, 3025–3032.Suche in Google Scholar

Stasch, J.P.; Becker, E.M.; Alonso-Alija, C.; Apeler, H.; Dembowsky, K.; Feurer, A.; Gerzer, R.; Minuth, T.; Perzborn, E.; Pleiss, U.; Schröder, H.; Schroeder, W.; Stahl, E.; Steinke, W.; Straub, A.; Schramm, M. NO-independent regulatory site on soluble guanylate cyclase. Nature2001, 410, 212–215.Suche in Google Scholar

Stasch, J.P.; Alonso-Alija, C.; Apeler, H.; Dembowsky, K.; Feurer, A.; Minuth, T.; Perzborn, E.; Schramm, M.; Straub, A. Pharmacological actions of a novel NO-independent guanylyl cyclase stimulator, BAY 41-8543: in vitro studies. Br. J. Pharmacol.2002, 135, 333–343.Suche in Google Scholar

Stasch, J.P.; Schmidt, P.M.; Nedvetsky, P.I.; Nedvetskaya, T.Y.; H S AK; Meurer, S.; Deile, M.; Taye, A.; Knorr, A.; Lapp, H.; Müller, H.; Turgay, Y.; Rothkegel, C.; Tersteegen, A.; Kemp-Harper, B.; Müller-Esterl, W.; Schmidt, H.H. Targeting the heme-oxidized nitric oxide receptor for selective vasodilatation of diseased blood vessels. J. Clin. Invest.2006, 116, 2552–2561.Suche in Google Scholar

Stasch, J.P.; Pacher, P.; Evgenov, O.V. Soluble guanylate cyclase as an emerging therapeutic target in cardiopulmonary disease. Circulation2011, 123, 2263–2273.Suche in Google Scholar

Stone, J.R.; Marletta, M.A. Soluble guanylate cyclase from bovine lung: activation with nitric oxide and carbon monoxide and spectral characterization of the ferrous and ferric states. Biochemistry1994, 33, 5636–5640.Suche in Google Scholar

Stone, J.R.; Marletta, M.A. Spectral and kinetic studies on the activation of soluble guanylate cyclase by nitric oxide. Biochemistry1996, 35, 1093–1099.Suche in Google Scholar

Surmeli, N.B.; Marletta, M.A. Insight into the rescue of oxidized soluble guanylate cyclase by the activator cinaciguat. Chembiochem2012, 13, 977–981.Suche in Google Scholar

Szabo, C.; Ischiropoulos, H.; Radi, R. Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat. Rev. Drug Discov.2007, 6, 662–680.Suche in Google Scholar

Thippeswamy, T.; McKay, J.S.; Quinn, J.P.; Morris, R. Nitric oxide, a biological double-faced janus–is this good or bad? Histol. Histopathol.2006, 21, 445–458.Suche in Google Scholar

Tsai, E.J.; Kass, D.A. Cyclic GMP signaling in cardiovascular pathophysiology and therapeutics. Pharmacol. Ther.2009, 122, 216–238.Suche in Google Scholar

Wang, H.; Zhong, F.; Pan, J., Li, W.; Su, J.; Huang, Z.X.; Tan, X. Structural and functional insights into the heme-binding domain of the human soluble guanylate cyclase alpha2 subunit and heterodimeric alpha2beta1. J. Biol. Inorg. Chem.2012, 17, 719–730.Suche in Google Scholar

Wang-Rosenke, Y.; Neumayer, H.H.; Peters, H. NO signaling through cGMP in renal tissue fibrosis and beyond: key pathway and novel therapeutic target. Curr. Med. Chem.2008, 15, 1396–1406.Suche in Google Scholar

Wedel, B.; Humbert, P.; Harteneck, C.; Foerster, J.; Malkewitz, J.; Bohme, E.; Schultz, G.; Koesling, D. Mutation of His-105 in the beta 1 subunit yields a nitric oxide-insensitive form of soluble guanylyl cyclase. Proc. Natl. Acad. Sci. USA1994, 91, 2592–2596.Suche in Google Scholar

Winger, J.A.; Derbyshire, E.R.; Marletta, M.A. Dissociation of nitric oxide from soluble guanylate cyclase and heme-nitric oxide/oxygen binding domain constructs. J. Biol. Chem.2007, 282, 897–907.Suche in Google Scholar

Winger, J.A.; Derbyshire, E.R.; Lamers, M.H.; Marletta, M.A.; Kuriyan, J. The crystal structure of the catalytic domain of a eukaryotic guanylate cyclase. BMC Struct. Biol.2008, 8, 42.Suche in Google Scholar

Yuen, P.S.; Potter, L.R.; Garbers, D.L. A new form of guanylyl cyclase is preferentially expressed in rat kidney. Biochemistry1990, 29, 10872–10878.Suche in Google Scholar

Zabel, U.; Hausler, C.; Weeger, M.; Schmidt, H.H. Homodimerization of soluble guanylyl cyclase subunits. Dimerization analysis using a glutathione s-transferase affinity tag. J. Biol. Chem.1999, 274, 18149–18152.Suche in Google Scholar

Zhao, Y.; Brandish, P.E.; Ballou, D.P.; Marletta, M.A. A molecular basis for nitric oxide sensing by soluble guanylate cyclase. Proc. Natl. Acad. Sci. USA1999, 96, 14753–14758.Suche in Google Scholar

Zhong, F.; Wang, H.; Ying, T.; Huang, Z.X.; Tan, X. Efficient expression of human soluble guanylate cyclase in Escherichia coli and its signaling-related interaction with nitric oxide. Amino Acids2010, 39, 399–408.Suche in Google Scholar

Zhong, F.; Pan, J.; Liu, X.; Wang, H.; Ying, T.; Su, J.; Huang, Z.X.; Tan, X. A novel insight into the heme and NO/CO binding mechanism of the alpha subunit of human soluble guanylate cyclase. J. Biol. Inorg. Chem.2011, 16, 1227–1239.Suche in Google Scholar

Received: 2013-7-17
Accepted: 2013-8-12
Published Online: 2013-09-17
Published in Print: 2013-12-01

©2013 by Walter de Gruyter Berlin Boston

Heruntergeladen am 22.4.2026 von https://www.degruyterbrill.com/document/doi/10.1515/revic-2013-0011/html
Button zum nach oben scrollen