Reduction in soluble guanylyl cyclase-specific activity following prolonged treatment of porcine pulmonary artery with nitric oxide

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 293, Issue 1, 2007, Pages

  Perkins, William J ^a   Taniguchi, Miwa ^b   Warner, David O ^a   Chini, Eduardo N ^a   Jones, Keith A ^a  

^a MAYO CLINIC   (United States)

^b NAGASAKI UNIVERSITY   (Japan)

Author keywords

Guanosine 3 ,5 cyclic monophosphate; Nitric oxide; Pulmonary artery

Indexed keywords

3,3 BIS(2 AMINOETHYL) 1 HYDROXY 2 OXOTRIAZENE; CYCLIC AMP; CYCLIC GMP; DIAZONIUM COMPOUND; GUANYLATE CYCLASE; MANGANESE; MESSENGER RNA; NITRIC OXIDE; SUPEROXIDE DISMUTASE;

ANIMAL TISSUE; ARTICLE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY ARTERY; TISSUE CULTURE;

ANIMALS; CYCLIC AMP; CYCLIC GMP; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GUANYLATE CYCLASE; ISOMETRIC CONTRACTION; METALLOPORPHYRINS; NITRIC OXIDE; PHENYLEPHRINE; PHOSPHORIC DIESTER HYDROLASES; PULMONARY ARTERY; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RNA, MESSENGER; SOLUBILITY; SWINE; TIME FACTORS; TRIAZENES;

EID: 34447504986     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00368.2006     Document Type: Article

References (62)

1. Artz JD, Schmidt B, McCracken JL, Marletta MA. Effects of nitroglycerin on soluble guanylate cyclase: implications for nitrate tolerance. J Biol Chem 277: 18253-18256, 2002.
2. Balashova N, Chang FJ, Lamothe M, Sun Q, Beuve A. Characterization of a novel type of endogenous activator of soluble guanylyl cyclase. J Biol Chem 280: 2186-2196, 2005.
3. Becker-Andre M, Hahlbrock K. Absolute mRNA quantification using the polymerase chain reaction (PCR). A novel approach by a PCR aided transcript titration assay (PATTY). Nucleic Acids Res 17: 9437-9446, 1989.
4. Bellamy TC, Garthwaite J. Sub-second kinetics of the nitric oxide receptor, soluble guanylyl cyclase, in intact cerebellar cells. J Biol Chem 276: 4287-4292, 2001.
5. Bellamy TC, Wood J, Goodwin DA, Garthwaite J. Rapid desensitization of the nitric oxide receptor, soluble guanylyl cyclase, underlies diversity of cellular cGMP responses. Proc Natl Acad Sci USA 97: 2928-2933, 2000.
6. Brandes RP, Kim D, Schmitz-Winnenthal FH, Amidi M, Godecke A, Mulsch A, Busse R. Increased nitrovasodilator sensitivity in endothelial nitric oxide synthase knockout mice: role of soluble guanylyl cyclase. Hypertension 35: 231-236, 2000.
7. Busch CJ, Liu H, Graveline AR, Bloch KD. Nitric oxide induces phosphodiesterase 4B expression in rat pulmonary artery smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 290: L747-L753, 2006.
8. Chen AFY, Jiang SW, Crotty TB, Tsutsui M, Smith LA, O'Brien T, Katusic ZS. Effects of in vivo adventitial expression of recombinant endothelial nitric oxide synthase gene in cerebral arteries. Proc Natl Acad Sci USA 94: 12568-12573, 1997.
9. Chen L, Xin X, Eckhart AD, Yang N, Faber JE. Regulation of vascular smooth muscle growth by alpha 1-adrenoreceptor subtypes in vitro and in situ. J Biol Chem 270: 30980-30988, 1995.
10. Chen Z, Zhang J, Stamler JS. Identification of the enzymatic mechanism of nitroglycerin bioactivation. Proc Natl Acad Sci USA 99: 8306-8311, 2002.
11. Chini CC, Grande JP, Chini EN, Dousa TP. Compartmentalization of cAMP signaling in mesangial cells by phosphodiesterase isozymes PDE3 and PDE4. Regulation of superoxidation and mitogenesis. J Biol Chem 272: 9854-9859, 1997.
12. Chirgwin JM, Przybyla AE, MacDonald RJ, Rutter WJ. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18: 5294-5299, 1979.
13. Clementi E, Brown GC, Feelisch M, Moncada S. Persistent inhibition of cell respiration by nitric oxide: crucial role of S-nitrosylation of mitochondrial complex I and protective action of glutathione. Proc Natl Acad Sci USA 95: 7631-7636, 1998.
14. Filippov G, Bloch DB, Bloch KD. Nitric oxide decreases stability of mRNAs encoding soluble guanylate cyclase subunits in rat pulmonary artery smooth muscle cells. J Clin Invest 100: 942-948, 1997.
15. Geiselhoringer A, Werner M, Sigl K, Smital P, Worner R, Acheo L, Stieber J, Weinmeister P, Feil R, Feil S, Wegener J, Hofmann F, Schlossmann J. IRAG is essential for relaxation of receptor-triggered smooth muscle contraction by cGMP kinase. EMBO J 23: 4222-4231, 2004.
16. Gilliland G, Perrin S, Blanchard K, Bunn HF. Analysis of cytokine mRNA and DNA: detection and quantitation by competitive polymerase chain reaction. Proc Natl Acad Sci USA 87: 2725-2729, 1990.
17. 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.
18. Gupte SA, Rupawalla T, Phillibert D Jr, Wolin MS. NADPH and heme redox modulate pulmonary artery relaxation and guanylate cyclase activation by NO. Am J Physiol Lung Cell Mol Physiol 277: L1124-L1132, 1999.
19. Hanafy KA, Martin E, Murad F. CCTeta, a novel soluble guanylyl cyclase-interacting protein. J Biol Chem 279: 46946-46953, 2004.
20. 2+ in airway smooth muscle independently of cyclic nucleotides. Am J Physiol Lung Cell Mol Physiol 268: L166-L172, 1995.
21. Kanagy NL, Charpie JR, Dananberg J, Webb RC. Decreased sensitivity to vasoconstrictors in aortic rings after acute exposure to nitric oxide. Am J Physiol Heart Circ Physiol 271: H253-H260, 1996.
22. Keefer LK, Nims RW, Davies KM, Wink DA. "NONOates" (1-substituted diazen-1-ium-1,2-diolates) as nitric oxide donors: convenient nitric oxide dosage forms. Methods Enzymol 268: 281-293, 1996.
23. Kim D, Rybalkin SD, Pi X, Wang Y, Zhang C, Munzel T, Beavo JA, Berk BC, Yan C. Upregulation of phosphodiesterase 1A1 expression is associated with the development of nitrate tolerance. Circulation 104: 2338-2343, 2001.
24. Kim TD, Burstyn JN. Identification and partial purification of an endogenous inhibitor of soluble guanylyl cyclase from bovine lung. J Biol Chem 269: 15540-15545, 1994.
25. Kloss S, Furneaux H, Mulsch A. Post-transcriptional regulation of soluble guanylyl cyclase expression in rat aorta. J Biol Chem 278: 2377-2383, 2003.
26. Kullo IJ, Mozes G, Schwartz RS, Gloviczki P, Crotty TB, Barber DA, Katusic ZS, O'Brien T. Adventitial gene transfer of recombinant endothelial nitric oxide synthase to rabbit carotid arteries alters vascular reactivity. Circulation 96: 2254-2261, 1997.
27. Kullo IJ, Mozes G, Schwartz RS, Gloviczki P, Tsutsui M, Katusic ZS, O'Brien T. Enhanced endothelium-dependent relaxations after gene transfer of recombinant endothelial nitric oxide synthase to rabbit carotid arteries. Hypertension 30: 314-320, 1997.
28. Kwak YL, Jones KA, Warner DO, Perkins WJ. NO responsiveness in pulmonary artery and airway smooth muscle: the role of cGMP regulation. Am J Physiol Lung Cell Mol Physiol 290: L200-L208, 2006.
29. Kwak YL, Jones KA, Warner DO, Perkins WJ. Prolonged relaxation consistent with persisten soluble guanylyl cyclase activation in canine pulmonary artery following brief treatment with nitric oxide donors. Life Sci 79: 2001-2009, 2006.
30. Lowry AH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin reagent. J Biol Chem 193: 265-275, 1951.
31. Manktelow C, Bigatello LM, Hess D, Hurford WE. Physiologic determinants of the response to inhaled nitric oxide in patients with acute respiratory distress syndrome. Anesthesiology 87: 297-307, 1997.
32. Maragos CM, Morley D, Wink DA, Dunams TM, Saavedra JE, Hoffman A, Bove AA, Isaac L, Hrabie JA, Keefer LK. Complexes of NO with nucleophiles as agents for the controlled biological release of nitric oxide. Vasorelaxant effects. J Med Chem 34: 3242-3247, 1991.
33. Maurice DH, Palmer D, Tilley DG, Dunkerley HA, Netherton SJ, Raymond DR, Elbatarny HS, Jimmo SL. Cyclic nucleotide phosphodiesterase activity, expression, and targeting in cells of the cardiovascular system. Mol Pharmacol 64: 533-546, 2003.
34. Meddings JB, Scott RB, Fick GH. Analysis and comparison of sigmoidal curves: application to dose-response data. Am J Physiol Gastrointest Liver Physiol 257: G982-G989, 1989.
35. Mergia E, Friebe A, Dangel O, Russwurm M, Koesling D. Spare guanylyl cyclase NO receptors ensure high NO sensitivity in the vascular system. J Clin Invest 116: 1731-1737, 2006.
36. Mingone CJ, Gupte SA, Ali N, Oeckler RA, Wolin MS. Thiol oxidation inhibits nitric oxide-mediated pulmonary artery relaxation and guanylate cyclase stimulation. Am J Physiol Lung Cell Mol Physiol 290: L549-L557, 2006.
37. Moncada S, Rees DD, Schulz R, Palmer RM. Development and mechanism of a specific supersensitivity to nitrovasodilators after inhibition of vascular nitric oxide synthesis in vivo. Proc Natl Acad Sci USA 88: 2166-2170, 1991.
38. Moro MA, Russell RJ, Cellek S, Lizasoain I, Su YC, Darleyusmar VM, Radomski MW, Moncada S. cGMP mediates the vascular and platelet actions of nitric oxide-confirmation using an inhibitor of the soluble guanylyl cyclase. Proc Natl Acad Sci USA 93: 1480-1485, 1996.
39. Mullershausen F, Lange A, Mergia E, Friebe A, Koesling D. Desensitization of NO/cGMP signaling in smooth muscle: blood vessels versus airways. Mol Pharmacol 69: 1969-1974, 2006.
40. Mullershausen F, Russwurm M, Koesling D, Friebe A. The enhanced NO-induced cGMP response induced by long-term L-NAME treatment is not due to enhanced expression of NO-sensitive guanylyl cyclase. Vascul Pharmacol 40: 161-165, 2003.
41. Mullershausen F, Russwurm M, Thompson WJ, Liu L, Koesling D, Friebe A. Rapid nitric oxide-induced desensitization of the cGMP response is caused by increased activity of phosphodiesterase type 5 paralleled by phosphorylation of the enzyme. J Cell Biol 155: 271-278, 2001.
42. Mulsch A, Oelze M, Kloss S, Mollnau H, Topfer A, Smolenski A, Walter U, Stasch JP, Warnholtz A, Hink U, Meinertz T, Munzel T. Effects of in vivo nitroglycerin treatment on activity and expression of the guanylyl cyclase and cGMP-dependent protein kinase and their downstream target vasodilator-stimulated phosphoprotein in aorta. Circulation 103: 2188-2194, 2001.
43. Munzel T, Daiber A, Mulsch A. Explaining the phenomenon of nitrate tolerance. Circ Res 97: 618-628, 2005.
44. Munzel T, Li H, Mollnau H, Hink U, Matheis E, Hartmann M, Oelze M, Skatchkov M, Warnholtz A, Duncker L, Meinertz T, Forstermann U. Effects of long-term nitroglycerin treatment on endothelial nitric oxide synthase (NOS III) gene expression, NOS III-mediated superoxide production, and vascular NO bioavailability. Circ Res 86: E7-E12, 2000.
45. Munzel T, Sayegh H, Freeman BA, Tarpey MM, Harrison DG. Evidence for enhanced vascular superoxide anion production in nitrate tolerance. A novel mechanism underlying tolerance and cross-tolerance. J Clin Invest 95: 187-194, 1995.
46. 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 265: 16841-16845, 1990.
47. Nozik-Grayck E, Whalen EJ, Stamler JS, McMahon TJ, Chitano P, Piantadosi CA. S-nitrosoglutathione inhibits a1-adrenergic receptor-mediated vasoconstriction and ligand binding in pulmonary artery. Am J Physiol Lung Cell Mol Physiol 290: L136-L143, 2006.
48. Pauvert O, Salvail D, Rousseau E, Lugnier C, Marthan R, Savineau JP. Characterisation of cyclic nucleotide phosphodiesterase isoforms in the media layer of the main pulmonary artery. Biochem Pharmacol 63: 1763-1772, 2002.
49. Perkins WJ, Pabelick C, Warner DO, Jones KA. cGMP-independent mechanism of airway smooth muscle relaxation induced by S-nitrosoglutathione. Am J Physiol Cell Physiol 275: C468-C474, 1998.
50. Rabe KF, Tenor H, Dent G, Schudt C, Nakashima M, Magnussen H. Identification of PDE isozymes in human pulmonary artery and effect of selective PDE inhibitors. Am J Physiol Lung Cell Mol Physiol 266: L536-L543, 1994.
51. Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463-5467, 1977.
52. Shirasaki Y, Su C. Endothelium removal augments vasodilation by sodium nitroprusside and sodium nitrite. Eur J Pharmacol 114: 93-96, 1985.
53. Skatchkov MP, Sperling D, Hink U, Mulsch A, Harrison DG, Sindermann I, Meinertz T, Munzel T. Validation of lucigenin as a chemiluminescent probe to monitor vascular superoxide as well as basal vascular nitric oxide production. Biochem Biophys Res Commun 254: 319-324, 1999.
54. Soff GA, Cornwell TL, Cundiff DL, Gately S, Lincoln TM. Smooth muscle cell expression of type I cyclic GMP-dependent protein kinase is suppressed by continuous exposure to nitrovasodilators, theophylline, cyclic GMP, and cyclic AMP. J Clin Invest 100: 2580-2587, 1997.
55. Stasch JP, Schmidt PM, Nedvetsky PI, Nedvetskaya TY, HSA, Meurer S, Deile M, Taye A, Knorr A, Lapp H, Muller H, Turgay Y, Rothkegel C, Tersteegen A, Kemp-Harper B, Muller-Esterl W, Schmidt HH. Targeting the heme-oxidized nitric oxide receptor for selective vasodilatation of diseased blood vessels. J Clin Invest 116: 2552-2561, 2006.
56. Surks HK, Mochizuki N, Kasai Y, Georgescu SP, Tang KM, Ito M, Lincoln TM, Mendelsohn ME. Regulation of myosin phosphatase by a specific interaction with cGMP- dependent protein kinase Ialpha. Science 286: 1583-1587, 1999.
57. Sydow K, Daiber A, Oelze M, Chen Z, August M, Wendt M, Ullrich V, Mulsch A, Schulz E, Keaney JF Jr, Stamler JS, Munzel T. Central role of mitochondrial aldehyde dehydrogenase and reactive oxygen species in nitroglycerin tolerance and cross-tolerance. J Clin Invest 113: 482-489, 2004.
58. Ujiie K, Drewett JG, Yuen PS, Star RA. Differential expression of mRNA for guanylyl cyclase-linked endothelium-derived relaxing factor receptor subunits in rat kidney. J Clin Invest 91: 730-734, 1993.
59. Weber M, Lauer N, Mulsch A, Kojda G. The effect of peroxynitrite on the catalytic activity of soluble guanylyl cyclase. Free Radic Biol Med 31: 1360-1367, 2001.
60. Wu XB, Brune B, von Appen F, Ullrich V. Reversible activation of soluble guanylate cyclase by oxidizing agents. Arch Biochem Biophys 294: 75-82, 1992.
61. Yamashita T, Kawashima S, Ohashi Y, Ozaki M, Rikitake Y, Inoue N, Hirata K, Akita H, Yokoyama M. Mechanisms of reduced nitric oxide/cGMP-mediated vasorelaxation in transgenic mice overexpressing endothelial nitric oxide synthase. Hypertension 36: 97-102, 2000.
62. Yamashita T, Kawashima S, Ohashi Y, Ozaki M, Ueyama T, Ishida T, Inoue N, Hirata K, Akita H, Yokoyama M. Resistance to endotoxin shock in transgenic mice overexpressing endothelial nitric oxide synthase. Circulation 101: 931-937, 2000.