Beneficial effect of the nitric oxide donor compound 3-(1,3-Dioxoisoindolin-2-yl) benzyl nitrate on dysregulated phosphodiesterase 5, NADPH Oxidase, and Nitrosative Stress in the Sickle Cell Mouse Penis: Implication for Priapism Treatment

Journal of Pharmacology and Experimental Therapeutics

Volumn 359, Issue 2, 2016, Pages 230-237

  Silva, Fábio H ^a,b   Karakus, Serkan ^a   Musicki, Biljana ^a   Matsui, Hotaka ^a   Bivalacqua, Trinity J ^a   Dos Santos, Jean L ^c   Costa, Fernando F ^b   Burnett, Arthur L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CAMPINAS   (Brazil)

^c SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

3 (1,3 DIOXOISOINDOLIN 2 YL)BENZYL NITRATE; 3 NITROTYROSINE; ACETYLCHOLINE; CYCLIC GMP; ENDOTHELIAL NITRIC OXIDE SYNTHASE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE DONOR; NITROPRUSSIDE SODIUM; PHOSPHODIESTERASE V; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; UNCLASSIFIED DRUG; 3-(1,3-DIOXOISOINDOLIN-2-YL)BENZYL NITRATE; 3-NITROTYROSINE; ACTIN BINDING PROTEIN; CELL ADHESION MOLECULE; CYBB PROTEIN, MOUSE; ISOINDOLE DERIVATIVE; MEMBRANE PROTEIN; NITRIC ACID DERIVATIVE; PHOSPHOPROTEIN; PHTHALIMIDE DERIVATIVE; REACTIVE NITROGEN SPECIES; TYROSINE; VASODILATOR-STIMULATED PHOSPHOPROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROSTIMULATION; ENZYME INHIBITION; IN VITRO STUDY; IN VIVO STUDY; LIMIT OF QUANTITATION; MALE; MOUSE; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PHENOTYPE; PRIAPISM; PRIORITY JOURNAL; PROTEIN EXPRESSION; SICKLE CELL ANEMIA; ANALOGS AND DERIVATIVES; ANIMAL; COMPLICATION; DOSE RESPONSE; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; HUMAN; METABOLISM; PENIS; PHOSPHORYLATION; TIME FACTOR;

ACETYLCHOLINE; ANEMIA, SICKLE CELL; ANIMALS; CELL ADHESION MOLECULES; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 5; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRIC STIMULATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; ISOINDOLES; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICROFILAMENT PROTEINS; NADPH OXIDASE; NITRATES; NITRIC OXIDE DONORS; NITROPRUSSIDE; OXIDATIVE STRESS; PENIS; PHOSPHOPROTEINS; PHOSPHORYLATION; PHTHALIMIDES; PRIAPISM; REACTIVE NITROGEN SPECIES; TIME FACTORS; TYROSINE;

EID: 84990963166     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.116.235473     Document Type: Article

References (39)

1. Adeyoju AB, Olujohungbe ABK, Morris J, Yardumian A, Bareford D, Akenova A, Akinyanju O, Cinkotai K, and O'Reilly PH (2002) Priapism in sickle-cell disease; incidence, risk factors and complications: an international multicentre study. BJU Int 90:898-902.
2. Anele UA, Le BV, Resar LMS, and Burnett AL (2015) How I treat priapism. Blood 125:3551-3558.
3. Bivalacqua TJ, Musicki B, Hsu LL, Berkowitz DE, Champion HC, and Burnett AL (2013) Sildenafil citrate-restored eNOS and PDE5 regulation in sickle cell mouse penis prevents priapism via control of oxidative/nitrosative stress. PLoS One 8: e68028.
4. Bonaventura D, Lunardi CN, Rodrigues GJ, Neto MA, and Bendhack LM (2008) A novel mechanism of vascular relaxation induced by sodium nitroprusside in the isolated rat aorta. Nitric Oxide 18:287-295.
5. Burnett AL (2006) The role of nitric oxide in erectile dysfunction: implications for medical therapy. J Clin Hypertens 8(SUPPL. 4):53-62.
6. Burnett AL (2008) Molecular pharmacotherapeutic targeting of PDE5 for preservation of penile health. J Androl 29:3-14.
7. Carson CC and Lue TF (2005) Phosphodiesterase type 5 inhibitors for erectile dysfunction. BJU Int 96:257-280.
8. Champion HC, Bivalacqua TJ, Takimoto E, Kass DA, and Burnett AL (2005) Phosphodiesterase-5A dysregulation in penile erectile tissue is a mechanism of priapism. Proc Natl Acad Sci USA 102:1661-1666.
9. Claudino MA, Franco-Penteado CF, Corat MAF, Gimenes AP, Passos LAC, Antunes E, and Costa FF (2009) Increased cavernosal relaxations in sickle cell mice priapism are associated with alterations in the NO-cGMP signaling pathway. J Sex Med 6:2187-2196.
10. dos Santos JL, Lanaro C, Lima LM, Gambero S, Franco-Penteado CF, Alexandre-Moreira MS, Wade M, Yerigenahally S, Kutlar A, Meiler SE, et al. (2011) Design, synthesis, and pharmacological evaluation of novel hybrid compounds to treat sickle cell disease symptoms. J Med Chem 54:5811-5819.
11. Francis SH, Busch JL, Corbin JD, and Sibley D (2010) cGMP-dependent protein kinases and cGMP phosphodiesterases in nitric oxide and cGMP action. Pharmacol Rev 62:525-563.
12. Frey RS, Ushio-Fukai M, and Malik AB (2009) NADPH oxidase-dependent signaling in endothelial cells: role in physiology and pathophysiology. Antioxid Redox Signal 11:791-810.
13. Hurt KJ, Musicki B, Palese MA, Crone JK, Becker RE, Moriarity JL, Snyder SH, and Burnett AL (2002) Akt-dependent phosphorylation of endothelial nitric-oxide synthase mediates penile erection. Proc Natl Acad Sci USA 99:4061-4066.
14. Hurt KJ, Sezen SF, Lagoda GF, Musicki B, Rameau GA, Snyder SH, and Burnett AL (2012) Cyclic AMP-dependent phosphorylation of neuronal nitric oxide synthase mediates penile erection. Proc Natl Acad Sci USA 109:16624-16629.
15. Kanika ND, Tar M, Tong Y, Kuppam DSR, Melman A, and Davies KP (2009) The mechanism of opiorphin-induced experimental priapism in rats involves activation of the polyamine synthetic pathway. Am J Physiol Cell Physiol 297: C916-C927.
16. Kato GJ (2012) Priapism in sickle-cell disease: a hematologist's perspective. J Sex Med 9:70-78.
17. 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.
18. Kowaluk EA, Seth P, and Fung HL (1992) Metabolic activation of sodium nitro-prusside to nitric oxide in vascular smooth muscle. J Pharmacol Exp Ther 262: 916-922.
19. Lagoda G, Sezen SF, Cabrini MR, Musicki B, and Burnett AL (2013) Molecular analysis of erection regulatory factors in sickle cell disease associated priapism in the human penis. J Urol 189:762-768.
20. Lagoda G, Sezen SF, Hurt KJ, Cabrini MR, Mohanty DK, and Burnett AL (2014) Sustained nitric oxide (NO)-releasing compound reverses dysregulated NO signal transduction in priapism. FASEB J 28:76-84.
21. Lin C-S, Chow S, Lau A, Tu R, and Lue TF (2002) Human PDE5A gene encodes three PDE5 isoforms from two alternate promoters. Int J Impot Res 14:15-24.
22. Lionnet F, Hammoudi N, Stojanovic KS, Avellino V, Grateau G, Girot R, and Haymann J-P (2012) Hemoglobin sickle cell disease complications: a clinical study of 179 cases. Haematologica 97:1136-1141.
23. Mi T, Abbasi S, Zhang H, Uray K, Chunn JL, Xia LW, Molina JG, Weisbrodt NW, Kellems RE, Blackburn MR, et al. (2008) Excess adenosine in murine penile erectile tissues contributes to priapism via A2B adenosine receptor signaling. J Clin Invest 118:1491-1501.
24. Musicki B, Liu T, Sezen SF, and Burnett AL (2012) Targeting NADPH oxidase decreases oxidative stress in the transgenic sickle cell mouse penis. J Sex Med 9:1980-1987.
25. Nangle MR, Cotter MA, and Cameron NE (2004) An in vitro investigation of aorta and corpus cavernosum from eNOS and nNOS gene-deficient mice. Pflugers Arch 448:139-145.
26. Ning C, Wen J, Zhang Y, Dai Y, Wang W, Zhang W, Qi L, Grenz A, Eltzschig HK, Blackburn MR, et al. (2014) Excess adenosine A2B receptor signaling contributes to priapism through HIF-1a mediated reduction of PDE5 gene expression. FASEB J 28:2725-2735.
27. Nunes KP, Teixeira CE, Priviero FBM, Toque HA, and Webb RC (2015) Beneficial effect of the soluble guanylyl cyclase stimulator BAY 41-2272 on impaired penile erection in db/db-/- type II diabetic and obese mice. J Pharmacol Exp Ther 353:330-339.
28. Nur E, Biemond BJ, Otten H-M, Brandjes DP, and Schnog J-JB; CURAMA Study Group (2011) Oxidative stress in sickle cell disease; pathophysiology and potential implications for disease management. Am J Hematol 86:484-489.
29. Oelze M, Mollnau H, Hoffmann N, Warnholtz A, Bodenschatz M, Smolenski A, Walter U, Skatchkov M, Meinertz T, and Münzel T (2000) Vasodilator-stimulated phosphoprotein serine 239 phosphorylation as a sensitive monitor of defective nitric oxide/cGMP signaling and endothelial dysfunction. Circ Res 87:999-1005.
30. Olujohungbe AB, Adeyoju A, Yardumian A, Akinyanju O, Morris J, Westerdale N, Akenova Y, Kehinde MO, Anie K, Howard J, et al. (2011) A prospective diary study of stuttering priapism in adolescents and young men with sickle cell anemia: report of an international randomized control trial-the priapism in sickle cell study. J Androl 32:375-382.
31. Pacher P, Beckman JS, and Liaudet L (2007) Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87:315-424.
32. Pászty C, Brion CM, Manci E, Witkowska HE, Stevens ME, Mohandas N, and Rubin EM (1997) Transgenic knockout mice with exclusively human sickle hemoglobin and sickle cell disease. Science 278:876-878.
33. Piel FB, Patil AP, Howes RE, Nyangiri OA, Gething PW, Dewi M, Temperley WH, Williams TN, Weatherall DJ, and Hay SI (2013) Global epidemiology of sickle haemoglobin in neonates: a contemporary geostatistical model-based map and population estimates. Lancet 381:142-151.
34. Rees DC, Williams TN, and Gladwin MT (2010) Sickle-cell disease. Lancet 376: 2018-2031.
35. Salonia A, Eardley I, Giuliano F, Hatzichristou D, Moncada I, Vardi Y, Wespes E, and Hatzimouratidis K; European Association of Urology (2014) European Association of Urology guidelines on priapism. Eur Urol 65:480-489.
36. Selemidis S, Dusting GJ, Peshavariya H, Kemp-Harper BK, and Drummond GR (2007) Nitric oxide suppresses NADPH oxidase-dependent superoxide production by S-nitrosylation in human endothelial cells. Cardiovasc Res 75:349-358.
37. Silva FH, Leiria LO, Alexandre EC, Davel APC, Mónica FZ, De Nucci G, and Antunes E (2014) Prolonged therapy with the soluble guanylyl cyclase activator BAY 60-2770 restores the erectile function in obese mice. J Sex Med 11:2661-2670.
38. Teixeira CE, Priviero FBM, and Webb RC (2007) Effects of 5-cyclopropyl-2-[1-(2-fluoro-benzyl)-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.
39. Wood KC, Hebbel RP, and Granger DN (2005) Endothelial cell NADPH oxidase mediates the cerebral microvascular dysfunction in sickle cell transgenic mice. FASEB J 19:989-991.