Beneficial effect of the soluble guanylyl cyclase stimulator bay 41-2272 on impaired penile erection in db/db-/- type II diabetic and obese mice

Journal of Pharmacology and Experimental Therapeutics

Volumn 353, Issue 2, 2015, Pages 330-339

  Nunes, Kenia Pedrosa ^a   Teixeira, Cleber E ^c   Priviero, Fernanda B M ^b   Toque, Haroldo A ^c   Webb, R Clinton ^c  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSIDADE SÃO FRANCISCO   (Brazil)

^c MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINO 5 CYCLOPROPYL 2 [1 (2 FLUOROBENZYL) 1H PYRAZOLO[3,4 B]PYRIDIN 3 YL]PYRIMIDINE; CYCLIC GMP; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; 3-(4-AMINO-5-CYCLOPROPYLPYRIMIDINE-2-YL)-1-(2-FLUOROBENZYL)-1H-PYRAZOLO(3,4-B)PYRIDINE; CELL RECEPTOR; GLUCOSE BLOOD LEVEL; GUANYLATE CYCLASE; LIPID; NITROPRUSSIDE SODIUM; PYRAZOLE DERIVATIVE; PYRIDINE DERIVATIVE; SOLUBLE GUANYLYL CYCLASE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL FUNCTION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CORPUS CAVERNOSUM MUSCLE; DRUG EFFICACY; DRUG POTENCY; ERECTILE DYSFUNCTION; MALE; MOUSE; MUSCLE RELAXATION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; ANIMAL; BLOOD; DRUG EFFECTS; DRUG INTERACTION; EPITHELIUM; GENE EXPRESSION REGULATION; GENETICS; GLUCOSE BLOOD LEVEL; METABOLISM; MOUSE MUTANT; PATHOLOGY; PATHOPHYSIOLOGY; PENIS; PENIS ERECTION; VASODILATATION;

ANIMALS; BLOOD GLUCOSE; CYCLIC GMP; DIABETES MELLITUS, TYPE 2; DRUG INTERACTIONS; EPITHELIUM; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GUANYLATE CYCLASE; LIPIDS; MALE; MICE; MICE, OBESE; MUSCLE RELAXATION; NADPH OXIDASE; NITROPRUSSIDE; OBESITY; OXIDATIVE STRESS; PENILE ERECTION; PENIS; PYRAZOLES; PYRIDINES; RECEPTORS, CYTOPLASMIC AND NUCLEAR; VASODILATION;

EID: 84929942431     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.114.220970     Document Type: Article

References (52)

1. Anderson EA, Hoffman RP, Balon TW, Sinkey CA, and Mark AL (1991) Hyperinsulinemia produces both sympathetic neural activation and vasodilation in normal humans. J Clin Invest 87:2246-2252.
2. Andersson KE (2011) Mechanisms of penile erection and basis for pharmacological treatment of erectile dysfunction. Pharmacol Rev 63:811-859.
3. Angulo J, González-Corrochano R, Cuevas P, Fernández A, La Fuente JM, Rolo F, Allona A, and Sáenz de Tejada I (2010) Diabetes exacerbates the functional deficiency of NO/cGMP pathway associated with erectile dysfunction in human corpus cavernosum and penile arteries. J Sex Med 7:758-768.
4. Angulo J, Peiró C, Cuevas P, Gabancho S, Fernández A, González-Corrochano R, La Fuente JM, Baron AD, Chen KS, and de Tejada IS (2009) The novel antioxidant, AC3056 (2,6-di-t-butyl-4-((dimethyl-4-methoxyphenylsilyl)methyloxy)phenol), reverses erectile dysfunction in diabetic rats and improves NO-mediated responses in penile tissue from diabetic men. J Sex Med 6:373-387.
5. Bacon CG, Mittleman MA, Kawachi I, Giovannucci E, Glasser DB, and Rimm EB (2006) A prospective study of risk factors for erectile dysfunction. J Urol 176: 217-221.
6. Baracat JS, Teixeira CE, Okuyama CE, Priviero FB, Faro R, Antunes E, and De Nucci G (2003) Relaxing effects induced by the soluble guanylyl cyclase stimulator BAY 41-2272 in human and rabbit corpus cavernosum. Eur J Pharmacol 477: 163-169.
7. Becker EM, Alonso-Alija C, Apeler H, Gerzer R, Minuth T, Pleiss U, Schmidt P, Schramm M, Schröder H, Schroeder W, et al. (2001) NO-independent regulatory site of direct sGC stimulators like YC-1 and BAY 41-2272. BMC Pharmacol 1:13.
8. Bischoff E, Schramm M, Straub A, Feurer A, and Stasch JP (2003) BAY 41-2272: a stimulator of soluble guanylyl cyclase induces nitric oxide-dependent penile erection in vivo. Urology 61:464-467.
9. Burnett AL, Musicki B, Jin L, and Bivalacqua TJ (2006) Nitric oxide/redox-based signalling as a therapeutic target for penile disorders. Expert Opin Ther Targets 10:445-457.
10. Carneiro FS, Giachini FR, Lima VV, Carneiro ZN, Leite R, Inscho EW, Tostes RC, and Webb RC (2008) Adenosine actions are preserved in corpus cavernosum from obese and type II diabetic db/db mouse. J Sex Med 5:1156-1166.
11. Cheah LS, Gwee MC, and Nirthanan S (2002) Characterization of the rat isolated retractor penis muscle as a model for the study of nitrergic transmission. J Pharmacol Toxicol Methods 47:79-85.
12. Chitaley K (2009) Type 1 and Type 2 diabetic-erectile dysfunction: same diagnosis (ICD-9), different disease? J Sex Med 6 (Suppl 3):262-268.
13. Chu NV and Edelman SV (2002) Erectile dysfunction and diabetes. Curr Diab Rep 2: 60-66.
14. Claudino MA, da Silva FH, Mónica FZ, Rojas-Moscoso JA, De Nucci G, and Antunes E (2011) Long-term oral treatment with BAY 41-2272 ameliorates impaired corpus cavernosum relaxations in a nitric oxide-deficient rat model. BJU Int 108:116-122.
15. Claudino MA, Franco-Penteado CF, Priviero FB, Camargo EA, Teixeira SA, Muscará MN, De Nucci G, Zanesco A, and Antunes E (2010) Upregulation of gp91phox subunit of NAD(P)H oxidase contributes to erectile dysfunction caused by longterm nitric oxide inhibition in rats: reversion by regular physical training. Urology 75:961-967.
16. Evgenov OV, Pacher P, Schmidt PM, Haskó G, Schmidt HH, and Stasch JP (2006) NO-independent stimulators and activators of soluble guanylate cyclase: discovery and therapeutic potential. Nat Rev Drug Discov 5:755-768.
17. Feeley RJ and Traish AM (2009) Obesity and erectile dysfunction: is androgen deficiency the common link? Scientific World Journal 9:676-684.
18. Giugliano F, Maiorino M, Bellastella G, Gicchino M, Giugliano D, and Esposito K (2010) Determinants of erectile dysfunction in type 2 diabetes. Int J Impot Res 22: 204-209.
19. Gratzke C, Angulo J, Chitaley K, Dai YT, Kim NN, Paick JS, Simonsen U, Uckert S, Wespes E, Andersson KE, et al. (2010) Anatomy, physiology, and pathophysiology of erectile dysfunction. J Sex Med 7:445-475.
20. Griendling KK, Sorescu D, and Ushio-Fukai M (2000) NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res 86:494-501.
21. Guzik TJ, Mussa S, Gastaldi D, Sadowski J, Ratnatunga C, Pillai R, and Channon KM (2002) Mechanisms of increased vascular superoxide production in human diabetes mellitus: role of NAD(P)H oxidase and endothelial nitric oxide synthase. Circulation 105:1656-1662.
22. Hidalgo-Tamola J and Chitaley K (2009) Review type 2 diabetes mellitus and erectile dysfunction. J Sex Med 6:916-926.
23. Isidro ML (2012) Sexual dysfunction in men with type 2 diabetes. Postgrad Med J 88: 152-159.
24. Jin L and Burnett AL (2008) NADPH oxidase: recent evidence for its role in erectile dysfunction. Asian J Androl 10:6-13.
25. Jin L, Lagoda G, Leite R, Webb RC, and Burnett AL (2008) NADPH oxidase activation: a mechanism of hypertension-associated erectile dysfunction. J Sex Med 5: 544-551.
26. Kalsi JS, Ralph DJ, Madge DJ, Kell PD, and Cellek S (2004) A comparative study of sildenafil, NCX-911 and BAY41-2272 on the anococcygeus muscle of diabetic rats. Int J Impot Res 16:479-485.
27. Kalsi JS, Rees RW, Hobbs AJ, Royle M, Kell PD, Ralph DJ, Moncada S, and Cellek S (2003) BAY41-2272, a novel nitric oxide independent soluble guanylate cyclase activator, relaxes human and rabbit corpus cavernosum in vitro. J Urol 169: 761-766.
28. Koupparis AJ, Jeremy JY, Muzaffar S, Persad R, and Shukla N (2005) Sildenafil inhibits the formation of superoxide and the expression of gp47 NAD[P]H oxidase induced by the thromboxane A2 mimetic, U46619, in corpus cavernosal smooth muscle cells. BJU Int 96:423-427.
29. Lasker GF, Maley JH, and Kadowitz PJ (2010) A review of the pathophysiology and novel treatments for erectile dysfunction. Adv Pharmacol Sci 2010:2010.
30. Lasker GF, Pankey EA, and Kadowitz PJ (2013) Modulation of soluble guanylate cyclase for the treatment of erectile dysfunction. Physiology (Bethesda) 28:262-269.
31. Lassègue B and Clempus RE (2003) Vascular NAD(P)H oxidases: specific features, expression, and regulation. Am J Physiol Regul Integr Comp Physiol 285: R277-R297.
32. Liu K, Liu XS, Xiao L, Shang J, Li MC, Xu YJ, and Liu HG (2012) NADPH oxidase activation: a mechanism of erectile dysfunction in a rat model of sleep apnea. J Androl 33:1186-1198.
33. Luttrell IP, Swee M, Starcher B, Parks WC, and Chitaley K (2008) Erectile dysfunction in the type II diabetic db/db mouse: impaired venoocclusion with altered cavernosal vasoreactivity and matrix. Am J Physiol Heart Circ Physiol 294: H2204-H2211.
34. McMahon CN, Smith CJ, and Shabsigh R (2006) Treating erectile dysfunction when PDE5 inhibitors fail. BMJ 332:589-592.
35. Moore CR and Wang R (2006) Pathophysiology and treatment of diabetic erectile dysfunction. Asian J Androl 8:675-684.
36. Nunes KP, Toque HA, Caldwell RB, Caldwell RW, and Webb RC (2011) Extracellular signal-regulated kinase (ERK) inhibition decreases arginase activity and improves corpora cavernosal relaxation in streptozotocin (STZ)-induced diabetic mice. J Sex Med 8:3335-3344.
37. Nunes KP and Webb RC. (2012) Mechanisms in erectile function and dysfunction: an overview, in Erectile Dysfunction: Disease-Associated Mechanisms and Novel Insights into Therapy (Nunes KP ed) pp 3-22, InTech, Rijeka, Croatia.
38. Priviero FB, Baracat JS, Teixeira CE, Claudino MA, De Nucci G, and Antunes E (2005) Mechanisms underlying relaxation of rabbit aorta by BAY 41-2272, a nitric oxide-independent soluble guanylate cyclase activator. Clin Exp Pharmacol Physiol 32:728-734.
39. Shukla N, Hotston M, Persad R, Angelini GD, and Jeremy JY (2009) The administration of folic acid improves erectile function and reduces intracavernosal oxidative stress in the diabetic rabbit. BJU Int 103:98-103.
40. Shukla N, Jones R, Persad R, Angelini GD, and Jeremy JY (2005) Effect of sildenafil citrate and a nitric oxide donating sildenafil derivative, NCX 911, on cavernosal relaxation and superoxide formation in hypercholesterolaemic rabbits. Eur J Pharmacol 517:224-231.
41. Silva FH, Lanaro C, Leiria LO, Rodrigues RL, Davel AP, Claudino MA, Toque HA, and Antunes E (2014) Oxidative stress associated with middle aging leads to sympathetic hyperactivity and downregulation of soluble guanylyl cyclase in corpus cavernosum. Am J Physiol Heart Circ Physiol 307:H1393-H1400.
42. Stasch JP, Becker EM, Alonso-Alija C, Apeler H, Dembowsky K, Feurer A, Gerzer R, Minuth T, Perzborn E, Pleiss U, et al. (2001) NO-independent regulatory site on soluble guanylate cyclase. Nature 410:212-215.
43. Tamler R (2009) Diabetes, obesity, and erectile dysfunction. Gend Med 6 (Suppl 1): 4-16.
44. Teixeira CE, Priviero FB, Claudino MA, Baracat JS, De Nucci G, Webb RC, and Antunes E (2006a) Stimulation of soluble guanylyl cyclase by BAY 41-2272 relaxes anococcygeus muscle: interaction with nitric oxide. Eur J Pharmacol 530: 157-165.
45. Teixeira CE, Priviero FB, Todd J, Jr, and Webb RC (2006b) Vasorelaxing effect of BAY 41-2272 in rat basilar artery: involvement of cGMP-dependent and independent mechanisms. Hypertension 47:596-602.
46. Teixeira CE, Priviero FB, and Webb RC (2006c) Molecular mechanisms underlying rat mesenteric artery vasorelaxation induced by the nitric oxide-independent soluble guanylyl cyclase stimulators BAY 41-2272 [5-cyclopropyl-2-[1-(2-fluorobenzyl)-1H-pyrazolo[3,4-b]pyridin-3-yl]pyrimidin-4-ylamine] and YC-1 [3-(5'-hydroxymethyl-2'-furyl)-1-benzyl Indazole]. J Pharmacol Exp Ther 317:258-266.
47. Teixeira CE, Priviero FB, and Webb RC (2007) Effects of 5-cyclopropyl-2-[1-(2-fluorobenzyl)-1H-pyrazolo[3,4-b]pyridine-3-yl]pyrimidin-4-ylamine (BAY 41-2272) on smooth muscle tone, soluble guanylyl cyclase activity, and NADPH oxidase activity/expression in corpus cavernosum from wild-type, neuronal, and endothelial nitric-oxide synthase null mice. J Pharmacol Exp Ther 322:1093-1102.
48. Toda N, Ayajiki K, and Okamura T (2005) Nitric oxide and penile erectile function. Pharmacol Ther 106:233-266.
49. Toque HA, Antunes E, Teixeira CE, and De Nucci G (2008) Increased cyclic guanosine monophosphate synthesis and calcium entry blockade account for the relaxant activity of the nitric oxide-independent soluble guanylyl cyclase stimulator BAY 41-2272 in the rabbit penile urethra. Urology 72:711-715.
50. Toque HA, Nunes KP, Yao L, Liao JK, Webb RC, Caldwell RB, and Caldwell RW (2013a) Activated Rho kinase mediates diabetes-induced elevation of vascular arginase activation and contributes to impaired corpora cavernosa relaxation: possible involvement of p38 MAPK activation. J Sex Med 10:1502-1515.
51. Toque HA, Nunes KP, Yao L, Xu Z, Kondrikov D, Su Y, Webb RC, Caldwell RB, and Caldwell RW (2013b) Akita spontaneously type 1 diabetic mice exhibit elevated vascular arginase and impaired vascular endothelial and nitrergic function. PLoS ONE 8:e72277.
52. Toque HA, Tostes RC, Yao L, Xu Z, Webb RC, Caldwell RB, and Caldwell RW (2011) Arginase II deletion increases corpora cavernosa relaxation in diabetic mice. J Sex Med 8:722-733.