Inhibitors of phosphodiesterase 5 (PDE 5) inhibit the nerve-induced release of nitric oxide from the rabbit corpus cavernosum

British Journal of Pharmacology

Volumn 150, Issue 3, 2007, Pages 353-360

  Hallen K ^a,b   Wiklund, N P ^a,b   Gustafsson, L E ^b  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

cGMP; Corpus cavernosum; Neurotransmission; Nitric oxide; PDE; Rabbit; Sildenafil; Tadalafil; Vardenafil; Zaprinast

Indexed keywords

CYCLIC GMP; GUANETHIDINE; NITRIC OXIDE; PHENYLEPHRINE; PHOSPHODIESTERASE INHIBITOR; PHOSPHODIESTERASE V INHIBITOR; SCOPOLAMINE; SILDENAFIL; TADALAFIL; VARDENAFIL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHEMOLUMINESCENCE; CONTROLLED STUDY; CORPUS CAVERNOSUM; ELECTRIC FIELD; ELECTROSTIMULATION; MALE; MONOTHERAPY; MUSCLE RELAXATION; MUSCLE TONE; NEGATIVE FEEDBACK; NERVE STIMULATION; NONHUMAN; PRIAPISM; PRIORITY JOURNAL; RABBIT; REPRODUCIBILITY;

3',5'-CYCLIC-GMP PHOSPHODIESTERASE; ANIMALS; CARBOLINES; CYCLIC GMP; IMIDAZOLES; IMPOTENCE; MALE; MUSCLE, SMOOTH; NITRERGIC NEURONS; NITRIC OXIDE; PENIS; PHOSPHODIESTERASE INHIBITORS; PIPERAZINES; PRIAPISM; PURINES; RABBITS; SULFONES; TRIAZINES;

EID: 33846863130     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1038/sj.bjp.0706991     Document Type: Article

References (56)

1. Andersson KE, Wagner G (1995). Physiology of penile erection. Physiol Rev 75: 191-236.
2. Aoyagi T, Hayakawa K, Miyaji K, Ishikawa H, Hata M (1999). Sildenafil induced priapism. Bull Tokyo Dent Coll 40: 215-217.
3. Ballard SA, Gingell CJ, Tang K, Turner LA, Price ME, Naylor AM (1998). 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.
4. Blount MA, Beasley A, Zoraghi R, Sekhar KR, Bessay EP, Francis SH et al. (2004). Binding of tritiated sildenafil, tadalafil, or vardenafil to the phosphodiesterase-5 catalytic site displays potency, specificity, heterogeneity, and cGMP stimulation. Mol Pharmacol 66: 144-152.
5. Boolell M, Allen MJ, Ballard SA, Gepi-Attee S, Muirhead GJ, Naylor AM et al. (1996). 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.
6. Brindley GS (1986). Pilot experiments on the actions of drugs injected into the human corpus cavernosum penis. Br J Pharmacol 87: 495-500.
7. Burnett AL (2002). Nitric oxide regulation of penile erection: biology and therapeutic implications. J Androl 23: S20-S26.
8. Burnett AL, Lowenstein CJ, Bredt DS, Chang TS, Snyder SH (1992). Nitric oxide: a physiologic mediator of penile erection. Science 257: 401-403.
9. Bush PA, Aronson WJ, Buga GM, Rajfer J, Ignarro LJ (1992). Nitric oxide is a potent relaxant of human and rabbit corpus cavernosum. J Urol 147: 1650-1655.
10. Butt E, Bernhardt M, Smolenski A, Kotsonis P, Frohlich LG, Sickmann A et al. (2000). Endothelial nitric-oxide synthase (type III) is activated and becomes calcium independent upon phosphorylation by cyclic nucleotide-dependent protein kinases. J Biol Chem 275: 5179-5187.
11. Cellek S, Kasakov L, Moncada S (1996). Inhibition of nitrergic relaxations by a selective inhibitor of the soluble guanylate cyclase. Br J Pharmacol 118: 137-140.
12. Cellek S, Moncada S (1997). Nitrergic control of peripheral sympathetic responses in the human corpus cavernosum: a comparison with other species. Proc Natl Acad Sci USA 94: 8226-8231.
13. Cellek S, Rodrigo J, Lobos E, Fernandez P, Serrano J, Moncada S (1999). Selective nitrergic neurodegeneration in diabetes mellitus - a nitric oxide-dependent phenomenon. Br J Pharmacol 128: 1804-1812.
14. Colasanti M, Persichini T, Cavalieri E, Fabrizi C, Mariotto S, Menegazzi M et al. (1999). Rapid inactivation of NOS-I by lipopolysaccharide plus interferon-gamma-induced tyrosine phosphorylation. J Biol Chem 274: 9915-9917.
15. Corbin JD, Francis SH, Webb DJ (2002). Phosphodiesterase type 5 as a pharmacologic target in erectile dysfunction. Urology 60: 4-11.
16. Dail WG, Barba V, Leyba L, Galindo R (1995). Neural and endothelial nitric oxide synthase activity in rat penile erectile tissue. Cell Tissue Res 282: 109-116.
17. Dawson TM, Steiner JP, Dawson VL, Dinerman JL, Uhl GR, Snyder SH (1993). Immunosuppressant FK506 enhances phosphorylation of nitric oxide synthase and protects against glutamate neurotoxicity. Proc Natl Acad Sci USA 90: 9808-9812.
18. Dinerman JL, Steiner JP, Dawson TM, Dawson V, Snyder SH (1994). Cyclic nucleotide dependent phosphorylation of neuronal nitric oxide synthase inhibits catalytic activity. Neuropharmacology 33: 1245-1251.
19. Dorr LD, Brody MJ (1967). Hemodynamic mechanisms of erection in the canine penis. Am J Physiol 213: 1526-1531.
20. Eardley I, Cartledge J (2002). Tadalafil (Cialis) for men with erectile dysfunction. Int J Clin Pract 56: 300-304.
21. Francis SH, Corbin JD (2003). Molecular mechanisms and pharmacokinetics of phosphodiesterase-5 antagonists. Curr Urol Rep 4: 457-465.
22. Giuliano F, Bernabe J, Alexandre L, Niewoehner U, Haning H, Bischoff E (2003). Pro-erectile effect of vardenafil: in vitro experiments in rabbits and in vivo comparison with sildenafil in rats. Eur Urol 44: 731-736.
23. Hallén K, Gustafsson LE, Wiklund NP (2005). Nerve-induced release of nitric oxide from the rabbit corpus cavernosum is modulated by cyclic guanosine 3′,5′-monophosphate. Neuroscience 133: 169-174.
24. Hallén K, Olgart C, Gustafsson LE, Wiklund NP (2001). Modulation of neuronal nitric oxide release by soluble guanylyl cyclase in guinea pig colon. Biochem Biophys Res Commun 280: 1130-1134.
25. Holmquist F, Stief CG, Jonas U, Andersson KE (1991). Effects of the nitric oxide synthase inhibitor NG-nitro-L-arginine on the erectile response to cavernous nerve stimulation in the rabbit. Acta Physiol Scand 143: 299-304.
26. http://www.cbs.dtu.dk/services/NetPhos.
27. http://www.expasy.org/uniprot/P29476.
28. Ignarro LJ, Bush PA, Buga GM, Wood KS, Fukuto JM, Rajfer J (1990). Nitric oxide and cyclic GMP formation upon electrical field stimulation cause relaxation of corpus cavernosum smooth muscle. Biochem Biophys Res Commun 170: 843-850.
29. Iversen HH, Wiklund NP, Gustafsson LE (1994). Nitric oxide-like activity in guinea pig colon as determined by effector responses, bioassay and chemiluminescence analysis. Acta Physiol Scand 152: 315-322.
30. Jeremy JY, Ballard SA, Naylor AM, Miller MA, Angelini GD (1997). Effects of sildenafil, a type-5 cGMP phosphodiesterase inhibitor, and papaverine on cyclic GMP and cyclic AMP levels in the rabbit corpus cavernosum in vitro. Br J Urol 79: 958-963.
31. Keast JR (1992). A possible neural source of nitric oxide in the rat penis. Neurosci Lett 143: 69-73.
32. Kim NN (2003). Phosphodiesterase type 5 inhibitors: a biochemical and clinical correlation survey. Int J Impot Res 15 (Suppl 5): S13-S19.
33. Klotz T, Sachse R, Heidrich A, Jockenhovel F, Rohde G, Wensing G et al. (2001). Vardenafil increases penile rigidity and tumescence in erectile dysfunction patients: a RigiScan and pharmacokinetic study. World J Urol 19: 32-39.
34. Kuthe A, Wiedenroth A, Magert HJ, Uckert S, Forssmann WG, Stief CG et al. (2001). Expression of different phosphodiesterase genes in human cavernous smooth muscle. J Urol 165: 280-283.
35. Lefkowitz RJ (1996). G protein-coupled receptors and receptor kinases: from molecular biology to potential therapeutic applications. Nat Biotechnol 14: 283-286.
36. Leone AM, Wiklund NP, Hokfelt T, Brundin L, Moncada S (1994). Release of nitric oxide by nerve stimulation in the human urogenital tract. Neuroreport 5: 733-736.
37. Li CG, Rand MJ (1989). Evidence for a role of nitric oxide in the neurotransmitter system mediating relaxation of the rat anococcygeus muscle. Clin Exp Pharmacol Physiol 16: 933-938.
38. Liu XR, Gillespie JS, Gibson IF, Martin W (1991). Effects of NG-substituted analogues of L-arginine on NANC relaxation of the rat anococcygeus and bovine retractor penis muscles and the bovine penile artery. Br J Pharmacol 104: 53-58.
39. Magee T, Fuentes AM, Garban H, Rajavashisth T, Marquez D, Rodriguez JA et al. (1996). Cloning of a novel neuronal nitric oxide synthase expressed in penis and lower urinary tract. Biochem Biophys Res Commun 226: 145-151.
40. Makhlouf A, Kshirsagar A, Niederberger C (2006). Phosphodiesterase 11: a brief review of structure, expression and function. Int J Impot Res 18: 501-509.
41. McMahon CG (2003). Priapism associated with concurrent use of phosphodiesterase inhibitor drugs and intracavernous injection therapy. Int J Impot Res 15: 383-384.
42. Mount PF, Fraser SA, Watanabe Y, Lane N, Katsis F, Chen ZP et al. (2005). Phosphorylation of neuronal and endothelial nitric oxide synthase in the kidney with high and low salt diets. Nephron Physiol 102: p36-p50.
43. Olgart C, Hallén K, Wiklund NP, Iversen HH, Gustafsson LE (1998). Blockade of nitrergic neuroeffector transmission in guinea-pig colon by a selective inhibitor of soluble guanylyl cyclase. Acta Physiol Scand 162: 89-95.
44. Olgart C, Wiklund NP, Gustafsson LE (1997). Blockade of nitric oxide-evoked smooth muscle contractions by an inhibitor of guanylyl cyclase. Neuroreport 8: 3355-3358.
45. Qiu Y, Kraft P, Lombardi E, Clancy J (2000). Rabbit corpus cavernosum smooth muscle shows a different phosphodiesterase profile than human corpus cavernosum. J Urol 164: 882-886.
46. Rajfer J, Aronson WJ, Bush PA, Dorey FJ, Ignarro LJ (1992). Nitric oxide as a mediator of relaxation of the corpus cavernosum in response to nonadrenergic, noncholinergic neurotransmission. N Engl J Med 326: 90-94.
47. Saenz de Tejada I, Goldstein I, Azadzoi K, Krane RJ, Cohen RA (1989). Impaired neurogenic and endothelium-mediated relaxation of penile smooth muscle from diabetic men with impotence. N Engl J Med 320: 1025-1030.
48. (2+) neurotoxicity. Neuroscience 100: 651-661.
49. Song T, Hatano N, Kume K, Sugimoto K, Yamaguchi F, Tokuda M et al. (2005). Inhibition of neuronal nitric-oxide synthase by phosphorylation at Threonine1296 in NG108-15 neuronal cells. FEBS Lett 579: 5658-5662.
50. Stief CG, Uckert S, Becker AJ, Truss MC, Jonas U (1998). The effect of the specific phosphodiesterase (PDE) inhibitors on human and rabbit cavernous tissue in vitro and in vivo. J Urol 159: 1390-1393.
51. Waldkirch E, Uckert S, Yildirim H, Sohn M, Jonas U, Stief CG et al. (2005). Cyclic AMP-specific and cyclic GMP-specific phosphodiesterase isoenzymes in human cavernous arteries - immunohistochemical distribution and functional significance. World J Urol 23: 405-410.
52. Weeks JL, Zoraghi R, Beasley A, Sekhar KR, Francis SH, Corbin JD (2005). High biochemical selectivity of tadalafil, sildenafil and vardenafil for human phosphodiesterase 5A1 (PDE5) over PDE11A4 suggests the absence of PDE11A4 cross-reaction in patients. Int J Impot Res 17: 5-9.
53. Wiklund CU, Wiklund NP, Gustafsson LE (1993). Modulation of neuroeffector transmission by endogenous nitric oxide: a role for acetylcholine receptor-activated nitric oxide formation, as indicated by measurements of nitric oxide/nitrite release. Eur J Pharmacol 240: 235-242.
54. Wiklund NP, Cellek S, Leone AM, Iversen HH, Gustafsson LE, Brundin L et al. (1997). Visualisation of nitric oxide released by nerve stimulation. J Neurosci Res 47: 224-232.
55. Yonessi M, Saeedi M (2005). A double-blind placebo-controlled evaluation of the effect of topical sildenafil on erectile dysfunction. J Appl Res 5: 289-294.
56. Zoche M, Beyermann M, Koch KW (1997). Introduction of a phosphate at serine 741 of the calmodulin-binding domain of the neuronal nitric oxide synthase (NOS-1) prevents binding of calmodulin. Biol Chem 378: 851-857.