Melatonin inhibits nitric oxide signaling by increasing PDE5 phosphorylation in coronary arteries

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 303, Issue 12, 2012, Pages

  Shukla, Praveen ^a   Sun, Chengwen ^a   O'Rourke, Stephen T ^a  

^a NORTH DAKOTA STATE UNIVERSITY   (United States)

Author keywords

cGMP; Melatonin MT2 receptors; Phosphodiesterase 5; Protein kinase G; Smooth muscle relaxation

Indexed keywords

4 PHENYL 2 PROPIONAMIDOTETRALIN; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; CYCLIC GMP DEPENDENT PROTEIN KINASE INHIBITOR; GUANOSINE PHOSPHATE; HORMONE RECEPTOR BLOCKING AGENT; MELATONIN; MELATONIN 2 RECEPTOR; NITRIC OXIDE; NITROPRUSSIDE SODIUM; PHOSPHODIESTERASE V; SILDENAFIL; UNCLASSIFIED DRUG; ZAPRINAST;

ANIMAL TISSUE; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CORONARY ARTERY; CORONARY ARTERY DILATATION; DEGRADATION; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME PHOSPHORYLATION; INTRACELLULAR SIGNALING; ISOLATED ARTERY; MUSCLE ISOMETRIC CONTRACTION; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CORONARY VESSELS; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 5; MELATONIN; MODELS, ANIMAL; NITRIC OXIDE; NITROPRUSSIDE; PHOSPHORYLATION; RECEPTOR, MELATONIN, MT2; SIGNAL TRANSDUCTION; SWINE; VASODILATION;

EID: 84871336395     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00211.2012     Document Type: Article

References (60)

1. Artemyev NO. Binding of transducin to light-activated rhodopsin prevents transducin interaction with the rod cGMP phosphodiesterase gamma-subunit. Biochemistry 36: 4188-4193, 1997.
2. Ballard SA, Gingell CJ, Tang K, Turner LA, Price ME, Naylor AM. Effects of sildenafil on the relaxation of human corpus cavernosum tissue in vitro and on the activities of cyclic nucleotide phosphodiesterase isozymes. J Urol 159: 2164-2171, 1998.
3. Bender AT, Beavo JA. Cyclic nucleotide phosphodiesterases: molecular regulation to clinical use. Pharmacol Rev 58: 488-520, 2006.
4. Boolell M, Allen MJ, Ballard SA, Gepi-Attee S, Muirhead GJ, Naylor AM, Osterloh IH, Gingell C. Sildenafil: an orally active type 5 cyclic GMP-specific phosphodiesterase inhibitor for the treatment of penile erectile dysfunction. Int J Impot Res 8: 47-52, 1996.
5. Browning C, Beresford I, Fraser N, Giles H. Pharmacological characterization of human recombinant melatonin mt(1) and MT(2) receptors. Br J Pharmacol 129: 877-886, 2000.
6. Brunner H, Cockcroft JR, Deanfield J, Donald A, Ferrannini E, Halcox J, Kiowski W, Luscher TF, Mancia G, Natali A, Oliver JJ, Pessina AC, Rizzoni D, Rossi GP, Salvetti A, Spieker LE, Taddei S, Webb DJ. Endothelial function and dysfunction. Part II: association with cardiovascular risk factors and diseases. A statement by the Working Group on Endothelins and Endothelial Factors of the European Society of Hypertension. J Hypertens 23: 233-246, 2005.
7. Burns F, Rodger IW, Pyne NJ. The catalytic subunit of protein kinase A triggers activation of the type V cyclic GMP-specific phosphodiesterase from guinea-pig lung. Biochem J 283: 487-491, 1992.
8. Butt E, Geiger J, Jarchau T, Lohmann SM, Walter U. The cGMPdependent protein kinase-gene, protein, and function. Neurochem Res 18: 27-42, 1993.
9. Capsoni S, Stankov BM, Fraschini F. Reduction of regional cerebral blood flow by melatonin in young rats. Neuroreport 6: 1346-1348, 1995.
10. Cook JS, Sauder CL, Ray CA. Melatonin differentially affects vascular blood flow in humans. Am J Physiol Heart Circ Physiol 300: H670-H674, 2011.
11. Corbin JD, Ogreid D, Miller JP, Suva RH, Jastorff B, Doskeland SO. Studies of cGMP analog specificity and function of the two intrasubunit binding sites of cGMP-dependent protein kinase. J Biol Chem 261: 1208-1214, 1986.
12. Corbin JD, Turko IV, Beasley A, Francis SH. Phosphorylation of phosphodiesterase-5 by cyclic nucleotide-dependent protein kinase alters its catalytic and allosteric cGMP-binding activities. Eur J Biochem 267: 2760-2767, 2000.
13. Dostmann WR, Taylor MS, Nickl CK, Brayden JE, Frank R, Tegge WJ. Highly specific, membrane-permeant peptide blockers of cGMPdependent protein kinase Iα inhibit NO-induced cerebral dilation. Proc Natl Acad Sci USA 97: 14772-14777, 2000.
14. Dou D, Zheng X, Qin X, Qi H, Liu L, Raj JU, Gao Y. Role of cGMP-dependent protein kinase in development of tolerance to nitroglycerine in porcine coronary arteries. Br J Pharmacol 153: 497-507, 2008.
15. Dubocovich ML, Masana MI, Iacob S, Sauri DM. Melatonin receptor antagonists that differentiate between the human Mel1a and Mel1b recombinant subtypes are used to assess the pharmacological profile of the rabbit retina ML1 presynaptic heteroreceptor. Naunyn Schmiedebergs Arch Pharmacol 355: 365-375, 1997.
16. Dubocovich ML, Rivera-Bermudez MA, Gerdin MJ, Masana MI. Molecular pharmacology, regulation and function of mammalian melatonin receptors. Front Biosci 8: 1093-1108, 2003.
17. 2 is present in the human cardiovascular system. J Pineal Res 35: 40-44, 2003.
18. Evans BK, Mason R, Wilson VG. Evidence for direct vasoconstrictor activity of melatonin in "pressurized" segments of isolated caudal artery from juvenile rats. Naunyn Schmiedebergs Arch Pharmacol 346: 362-365, 1992.
19. Francis SH, Busch JL, Corbin JD, Sibley D. cGMP-dependent protein kinases and cGMP phosphodiesterases in nitric oxide and cGMP action. Pharmacol Rev 62: 525-563, 2010.
20. Francis SH, Corbin JD. Structure and function of cyclic nucleotidedependent protein kinases. Annu Rev Physiol 56: 237-272, 1994.
21. Francis SH, Noblett BD, Todd BW, Wells JN, Corbin JD. Relaxation of vascular and tracheal smooth muscle by cyclic nucleotide analogs that preferentially activate purified cGMP-dependent protein kinase. Mol Pharmacol 34: 506-517, 1988.
22. Francis SH, Thomas MK, Corbin JD. Cyclic GMP-binding cyclic GMP-specific phosphodiesterase from lung. In: Structure, Regulation and Drug Action, edited by Beavo J, Houslay M. Chichester, UK: Wiley, 1990, p. 117-135.
23. Garthwaite J, Southam E, Boulton CL, Nielsen EB, Schmidt K, Mayer B. Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one. Mol Pharmacol 48: 184-188, 1995.
24. +channels and endothelial factors. Br J Pharmacol 123: 1533-1540, 1998.
25. Geary GG, Krause DN, Duckles SP. Melatonin directly constricts rat cerebral arteries through modulation of potassium channels. Am J Physiol Heart Circ Physiol 273: H1530-H1536, 1997.
26. Gopal VK, Francis SH, Corbin JD. Allosteric sites of phosphodiesterase-5 (PDE5). A potential role in negative feedback regulation of cGMP signaling in corpus cavernosum. Eur J Biochem 268: 3304-3312, 2001.
27. Hofmann F, Ammendola A, Schlossmann J. Rising behind NO: cGMPdependent protein kinases. J Cell Sci 113: 1671-1676, 2000.
28. Ignarro LJ. Endothelium-derived nitric oxide: actions and properties. FASEB J 3: 31-36, 1989.
29. Ignarro LJ, Kadowitz PJ. The pharmacological and physiological role of cyclic GMP in vascular smooth muscle relaxation. Annu Rev Pharmacol Toxicol 25: 171-191, 1985.
30. Kannan MS, Johnson DE. Modulation of nitric oxide-dependent relaxation of pig tracheal smooth muscle by inhibitors of guanylyl cyclase and calcium activated potassium channels. Life Sci 56: 2229-2238, 1995.
31. Kowaluk EA, Seth P, Fung HL. Metabolic activation of sodium nitroprusside to nitric oxide in vascular smooth muscle. J Pharmacol Exp Ther 262: 916-922, 1992.
32. Krause DN, Barrios VE, Duckles SP. Melatonin receptors mediate potentiation of contractile responses to adrenergic nerve stimulation in rat caudal artery. Eur J Pharmacol 276: 207-213, 1995.
33. Krause ND, Geary GG, Doolen S, Duckles PS. Melatonin and cardiovascular function. In: Melatonin after Four Decades, edited by Olcese J. New York: Kluwer Academic/Plenum, 2000, p. 184-188.
34. Lincoln TM, Cornwell TL. Towards an understanding of the mechanism of action of cyclic AMP and cyclic GMP in smooth muscle relaxation. Blood Vessels 28: 129-137, 1991.
35. Mahle CD, Goggins GD, Agarwal P, Ryan E, Watson AJ. Melatonin modulates vascular smooth muscle tone. J Biol Rhythms 12: 690-696, 1997.
36. Moreno L, Losada B, Cogolludo A, Lodi F, Lugnier C, Villamor E, Moro M, Tamargo J, Perez-Vizcaino F. Postnatal maturation of phosphodiesterase 5 (PDE5) in piglet pulmonary arteries: activity, expression, effects of PDE5 inhibitors, and role of the nitric oxide/cyclic GMP pathway. Pediatr Res 56: 563-570, 2004.
37. 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.
38. Murthy KS. Activation of phosphodiesterase 5 and inhibition of guanylate cyclase by cGMP-dependent protein kinase in smooth muscle. Biochem J 360: 199-208, 2001.
39. Murthy KS. Contractile agonists attenuate cGMP levels by stimulating phosphorylation of cGMP-specific PDE5; an effect mediated by RhoA/ PKC-dependent inhibition of protein phosphatase 1. Br J Pharmacol 153: 1214-1224, 2008.
40. Natochin M, Granovsky AE, Artemyev NO. Regulation of transducin GTPase activity by human retinal RGS. J Biol Chem 272: 17444-17449, 1997.
41. Nelson MT, Quayle JM. Physiological roles and properties of potassium channels in arterial smooth muscle. Am J Physiol Cell Physiol 268: C799-C822, 1995.
42. Ni XP, Safai M, Rishi R, Baylis C, Humphreys MH. Increased activity of cGMP-specific phosphodiesterase (PDE5) contributes to resistance to atrial natriuretic peptide natriuresis in the pregnant rat. J Am Soc Nephrol 15: 1254-1260, 2004.
43. Pandi-Perumal SR, Trakht I, Srinivasan V, Spence DW, Maestroni GJ, Zisapel N, Cardinali DP. Physiological effects of melatonin: role of melatonin receptors and signal transduction pathways. Prog Neurobiol 85: 335-353, 2008.
44. Pfeifer A, Klatt P, Massberg S, Ny L, Sausbier M, Hirneiss C, Wang GX, Korth M, Aszodi A, Andersson KE, Krombach F, Mayerhofer A, Ruth P, Fassler R, Hofmann F. Defective smooth muscle regulation in cGMP kinase I-deficient mice. EMBO J 17: 3045-3051, 1998.
45. Poppe H, Rybalkin SD, Rehmann H, Hinds TR, Tang XB, Christensen AE, Schwede F, Genieser HG, Bos JL, Doskeland SO, Beavo JA, Butt E. Cyclic nucleotide analogs as probes of signaling pathways. Nat Methods 5: 277-278, 2008.
46. Rybalkin SD, Rybalkina IG, Feil R, Hofmann F, Beavo JA. Regulation of cGMP-specific phosphodiesterase (PDE5) phosphorylation in smooth muscle cells. J Biol Chem 277: 3310-3317, 2002.
47. Rybalkin SD, Rybalkina IG, Shimizu-Albergine M, Tang XB, Beavo JA. PDE5 is converted to an activated state upon cGMP binding to the GAF A domain. EMBO J 22: 469-478, 2003.
48. 2+ sensitization of contraction in vascular smooth muscle. J Biol Chem 275: 21722-21729, 2000.
49. Shibata S, Satake N, Takagi T, Usui H. Vasorelaxing action of melatonin in rabbit basilar artery. Gen Pharmacol 20: 677-680, 1989.
50. 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 Iα. Science 286: 1583-1587, 1999.
51. Taylor MS, Okwuchukwuasanya C, Nickl CK, Tegge W, Brayden JE, Dostmann WR. Inhibition of cGMP-dependent protein kinase by the cell-permeable peptide DT-2 reveals a novel mechanism of vasoregulation. Mol Pharmacol 65: 1111-1119, 2004.
52. Ting KN, Dunn WR, Davies DJ, Sugden D, Delagrange P, Guardiola-Lemaitre B, Scalbert E, Wilson VG. Studies on the vasoconstrictor action of melatonin and putative melatonin receptor ligands in the tail artery of juvenile Wistar rats. Br J Pharmacol 122: 1299-1306, 1997.
53. Tunstall RR, Shukla P, Grazul-Bilska A, Sun C, O'Rourke ST. MT2 receptors mediate the inhibitory effects of melatonin on nitric oxideinduced relaxation of porcine isolated coronary arteries. J Pharmacol Exp Ther 336: 127-133, 2011.
54. Vanhoutte PM. Endothelial dysfunction: the first step toward coronary arteriosclerosis. Circ J 73: 595-601, 2009.
55. Viswanathan M, Laitinen JT, Saavedra JM. Expression of melatonin receptors in arteries involved in thermoregulation. Proc Natl Acad Sci USA 87: 6200-6203, 1990.
56. Viswanathan M, Scalbert E, Delagrange P, Guardiola-Lemaitre B, Saavedra JM. Melatonin receptors mediate contraction of a rat cerebral artery. Neuroreport 8: 3847-3849, 1997.
57. Weekley LB. Melatonin-induced relaxation of rat aorta: interaction with adrenergic agonists. J Pineal Res 11: 28-34, 1991.
58. +channels in porcine tracheal smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 270: L338-L345, 1996.
59. Yang Q, Scalbert E, Delagrange P, Vanhoutte PM, O'Rourke ST. Melatonin potentiates contractile responses to serotonin in isolated porcine coronary arteries. Am J Physiol Heart Circ Physiol 280: H76-H82, 2001.
60. + currents by cGMP-dependent protein kinase in tracheal smooth muscle and Chinese hamster ovary cells. J Biol Chem 271: 19760-19767, 1996.