Targeting NADPH Oxidase Decreases Oxidative Stress in the Transgenic Sickle Cell Mouse Penis

Journal of Sexual Medicine

Volumn 9, Issue 8, 2012, Pages 1980-1987

  Musicki, Biljana ^a   Liu, Tongyun ^a   Sezen, Sena F ^a   Burnett, Arthur L ^a  

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

Author keywords

Antioxidants; ENOS Uncoupling; Priapism

Indexed keywords

4 HYDROXYNONENAL; ANTIOXIDANT; APOCYNIN; CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUTATHIONE PEROXIDASE 1; GLYCOPROTEIN GP 91; MANGANESE SUPEROXIDE DISMUTASE; PROTEIN P47; PROTEIN P67; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG ACTIVITY; ENZYME ACTIVATION; FEMALE; HEMIZYGOSITY; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PENIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; SICKLE CELL ANEMIA; WESTERN BLOTTING;

EID: 84864504837     PISSN: 17436095     EISSN: 17436109     Source Type: Journal    
DOI: 10.1111/j.1743-6109.2012.02798.x     Document Type: Article

References (52)

1. Wood KC, Granger DN. Sickle cell disease: Role of reactive oxygen and nitrogen metabolites. Clin Exp Pharmacol Physiol 2007;34:926-32.
2. Wood KC, Hsu LL, Gladwin MT. Sickle cell disease vasculopathy: A state of nitric oxide resistance. Free Radic Biol Med 2008;44:1506-28.
3. Elahi MM, Kong YX, Matata BM. Oxidative stress as a mediator of cardiovascular disease. Oxid Med Cell Longev 2009;2:259-69.
4. Wood KC, Hebbel RP, Granger DN. Endothelial cell NADPH oxidase mediates the cerebral microvascular dysfunction in sickle cell transgenic mice. FASEB J 2005;19:989-91.
5. Pritchard KA Jr, Ou J, Ou Z, Shi Y, Franciosi JP, Signorino P, Kaul S, Ackland-Berglund C, Witte K, Holzhauer S, Mohandas N, Guice KS, Oldham KT, Hillery CA. Hypoxia-induced acute lung injury in murine models of sickle cell disease. Am J Physiol Lung Cell Mol Physiol 2004;286:L705-14.
6. Wood KC, Hebbel RP, Lefer DJ, Granger DN. Critical role of endothelial cell-derived nitric oxide synthase in sickle cell disease-induced microvascular dysfunction. Free Radic Biol Med 2006;40:1443-53.
7. Hsu LL, Champion HC, Campbell-Lee SA, Bivalacqua TJ, Manci EA, Diwan BA, Schimel DM, Cochard AE, Wang X, Schechter AN, Noguchi CT, Gladwin MT. Hemolysis in sickle cell mice causes pulmonary hypertension due to global impairment in nitric oxide bioavailability. Blood 2007;109:3088-98.
8. Hasanato RM. Zinc and antioxidant vitamin deficiency in patients with severe sickle cell anemia. Ann Saudi Med 2006;26:17-21.
9. Prasad AS. Zinc deficiency in patients with sickle cell disease. Am J Clin Nutr 2002;75:181-2.
10. Varma RN, Mankad VN, Phelps DD, Jenkins LD, Suskind RM. Depressed erythrocyte glutathione reductase activity in sickle cell disease. Am J Clin Nutr 1983;38:884-7.
11. Natta CL, Chen LC, Chow CK. Selenium and glutathione peroxidase levels in sickle cell anemia. Acta Haematol 1990;83:130-2.
12. Dasgupta T, Fabry ME, Kaul DK. Antisickling property of fetal hemoglobin enhances nitric oxide bioavailability and ameliorates organ oxidative stress in transgenic-knockout sickle mice. Am J Physiol Regul Integr Comp Physiol 2010;298:R394-402.
13. Schacter L, Warth JA, Gordon EM, Prasad A, Klein BL. Altered amount and activity of superoxide dismutase in sickle cell anemia. FASEB J 1988;2:237-43.
14. Das SK, Nair RC. Superoxide dismutase, glutathione peroxidase, catalase and lipid peroxidation of normal and sickled erythrocytes. Br J Haematol 1980;44:87-92.
15. Montague DK, Jarow J, Broderick GA, Dmochowski RR, Heaton JP, Lue TF, Nehra A, Sharlip ID; Members of the Erectile Dysfunction Guideline Update Panel; Americal Urological Association. Guideline on the management of priapism. J Urol 2003;170:1318-24.
16. Burnett AL, Bivalacqua TJ. Priapism: Current principles and practice. Urol Clin North Am 2007;34:631-42.
17. Burnett AL, Bivalacqua TJ. Priapism: New concepts in medical and surgical management. Urol Clin North Am 2011;38:185-94.
18. Wen J, Jiang X, Dai Y, Zhang Y, Tang Y, Sun H, Mi T, Phatarpekar PV, Kellems RE, Blackburn MR, Xia Y. Increased adenosine contributes to penile fibrosis, a dangerous feature of priapism, via A2B adenosine receptor signaling. FASEB J 2010;24:740-9.
19. Bivalacqua TJ, Musicki B, Hsu LL, Gladwin MT, Burnett AL, Champion HC. Establishment of a transgenic sickle-cell mouse model to study the pathophysiology of priapism. J Sex Med 2009;6:2494-504.
20. Broderick GA, Kadioglu A, Bivalacqua TJ, Ghanem H, Nehra A, Shamloul R. Priapism: Pathogenesis, epidemiology, and management. J Sex Med 2010;7:476-500.
21. Burnett AL, Bivalacqua TJ, Champion HC, Musicki B. Long-term oral phosphodiesterase 5 inhibitor therapy alleviates recurrent priapism. Urology 2006;67:1043-8.
22. Burnett AL, Bivalacqua TJ, Champion HC, Musicki B. Feasibility of the use of phosphodiesterase type 5 inhibitors in a pharmacologic prevention program for recurrent priapism. J Sex Med 2006;3:1077-84.
23. Champion HC, Bivalacqua TJ, Takimoto E, Kass DA, Burnett AL. Phosphodiesterase-5A dysregulation in penile erectile tissue is a mechanism of priapism. Proc Natl Acad Sci U S A 2005;102:1661-6.
24. Mi T, Abbasi S, Zhang H, Uray K, Chunn JL, Xia LW, Molina JG, Weisbrodt NW, Kellems RE, Blackburn MR, Xia Y. Excess adenosine in murine penile erectile tissues contributes to priapism via A2B adenosine receptor signaling. J Clin Invest 2008;118:1491-501.
25. Kanika ND, Tar M, Tong Y, Kuppam DS, Melman A, Davies KP. The mechanism of opiorphin-induced experimental priapism in rats involves activation of the polyamine synthetic pathway. Am J Physiol Cell Physiol 2009;297:C916-27.
26. Musicki B, Champion HC, Hsu LL, Bivalacqua TJ, Burnett AL. Post-translational inactivation of endothelial nitric oxide synthase in the transgenic sickle cell mouse penis. J Sex Med 2011;8:419-26.
27. Kanika ND, Melman A, Davies KP. Experimental priapism is associated with increased oxidative stress and activation of protein degradation pathways in corporal tissue. Int J Impot Res 2010;22:363-73.
28. Paszty C, Brion CM, Manci E, Witkowska HE, Stevens ME, Mohandas N, Rubin EM. Transgenic knockout mice with exclusively human sickle hemoglobin and sickle cell disease. Science 1997;278:876-8.
29. Musicki B, Liu T, Lagoda GA, Strong TD, Sezen SF, Johnson JM, Burnett AL. Hypercholesterolemia-induced erectile dysfunction: Endothelial nitric oxide synthase (eNOS) uncoupling in the mouse penis by NAD(P)H oxidase. J Sex Med 2010;7:3023-32.
30. Hurt KJ, Musicki B, Palese MA, Crone JC, Becker RE, Moriaruty JL, Snyder SH, Burnett AL. Akt-dependent phosphorylation of endothelial nitric oxide synthase mediated penile erection. Proc Natl Acad Sci U S A 2002;99:4061-6.
31. Musicki B, Liu T, Strong T, Jin L, Laughlin MH, Turk JR, Burnett AL. Low-fat diet and exercise preserve eNOS regulation and endothelial function in the penis of early atherosclerotic pigs: A molecular analysis. J Sex Med 2008;5:552-61.
32. Wedgwood S, Lakshminrusimha S, Farrow KN, Czech L, Gugino SF, Soares F, Russell JA, Steinhorn RH. Apocynin improves oxygenation and increases eNOS in persistent pulmonary hypertension of the newborn. Am J Physiol Lung Cell Mol Physiol 2012;302:L616-26.
33. Yang Y, Sharma R, Sharma A, Awasthi S, Awasthi YC. Lipid peroxidation and cell cycle signaling: 4-hydroxynonenal, a key molecule in stress mediated signaling. Acta Biochim Pol 2003;50:319-36.
34. Muneer A, Cellek S, Ralph DJ, Minhas S. The investigation of putative agents, using an in vitro model, to prevent cavernosal smooth muscle dysfunction during low-flow priapism. BJU Int 2008;102:988-92.
35. Montezano AC, Burger D, Ceravolo GS, Yusuf H, Montero M, Touyz RM. Novel Nox homologues in the vasculature: Focusing on Nox4 and Nox5. Clin Sci (Lond) 2011;120:131-41.
36. Shukla N, Hotston M, Persad R, Angelini GD, Jeremy JY. The administration of folic acid improves erectile function and reduces intracavernosal oxidative stress in the diabetic rabbit. BJU Int 2009;103:98-103.
37. Jin HR, Kim WJ, Song JS, Piao S, Choi MJ, Tumurbaatar M, Shin SH, Yin GN, Koh GY, Ryu JK, Suh JK. Intracavernous delivery of a designed angiopoietin-1 variant rescues erectile function by enhancing endothelial regeneration in the streptozotocin-induced diabetic mouse. Diabetes 2011;60:969-80.
38. Jin L, Lagoda G, Leite R, Webb RC, Burnett AL. NADPH oxidase activation: A mechanism of hypertension-associated erectile dysfunction. J Sex Med 2008;5:544-51.
39. Claudino MA, Franco-Penteado CF, Priviero FB, Camargo EA, Teixeira SA, Muscará MN, De Nucci G, Zanesco A, Antunes E. Upregulation of gp91phox subunit of NAD(P)H oxidase contributes to erectile dysfunction caused by long-term nitric oxide inhibition in rats: Reversion by regular physical training. Urology 2010;75:961-7.
40. Kietadisorn R, Juni RP, Moens AL. Tackling endothelial dysfunction by modulating NOS-uncoupling: New insights in pathogenesis and therapeutic possibilities. Am J Physiol Endocrinol Metab 2012;302:E481-95.
41. Chen W, Druhan LJ, Chen CA, Hemann C, Chen YR, Berka V, Tsai AL, Zweier JL. Peroxynitrite induces destruction of the tetrahydrobiopterin and heme in endothelial nitric oxide synthase: Transition from reversible to irreversible enzyme inhibition. Biochemistry 2010;49:3129-37.
42. Alp NJ, Channon KM. Regulation of endothelial nitric oxide synthase by tetrahydrobiopterin in vascular disease. Arterioscler Thromb Vasc Biol 2004;24:413-20.
43. Kaul DK, Liu XD, Chang HY, Nagel RL, Fabry ME. Effect of fetal hemoglobin on microvascular regulation in sickle transgenic-knockout mice. J Clin Invest 2004;114:1136-45.
44. Johnson JM, Bivalacqua TJ, Lagoda GA, Burnett AL, Musicki B. eNOS-uncoupling in age-related erectile dysfunction. Int J Impot Res 2011;23:43-8.
45. Zhang M, Song P, Xu J, Zou MH. Activation of NAD(P)H oxidases by thromboxane A2 receptor uncouples endothelial nitric oxide synthase. Arterioscler Thromb Vasc Biol 2011;31:125-32.
46. Landmesser U, Dikalov S, Price SR, McCann L, Fukai T, Holland SM, Mitch WE, Harrison DG. Oxidation of tetrahydrobiopterin leads to uncoupling of endothelial cell nitric oxide synthase in hypertension. J Clin Invest 2003;111:1201-9.
47. Dikalova AE, Gongora MC, Harrison DG, Lambeth JD, Dikalov S, Griendling KK. Upregulation of Nox1 in vascular smooth muscle leads to impaired endothelium-dependent relaxation via eNOS uncoupling. Am J Physiol Heart Circ Physiol 2010;299:H673-9.
48. Crabtree MJ, Channon KM. Synthesis and recycling of tetrahydrobiopterin in endothelial function and vascular disease. Nitric Oxide 2011;25:81-8.
49. Schnog JB, Teerlink T, van der Dijs FP, Duits AJ, Muskiet FA. Plasma levels of asymmetric dimethylarginine (ADMA), an endogenous nitric oxide synthase inhibitor, are elevated in sickle cell disease. Ann Hematol 2005;84:282-6.
50. Loscalzo J. Antioxidant enzyme deficiencies and vascular disease. Expert Rev Endocrinol Metab 2010;5:15-8.
51. Blankenberg S, Rupprecht HJ, Bickel C, Torzewski M, Hafner G, Tiret L, Smieja M, Cambien F, Meyer J, Lackner KJ; AtheroGene Investigators. Glutathione peroxidase 1 activity and cardiovascular events in patients with coronary artery disease. N Engl J Med 2003;349:1605-13.
52. Dayal S, Brown KL, Weydert CJ, Oberley LW, Arning E, Bottiglieri T, Faraci FM, Lentz SR. Deficiency of glutathione peroxidase-1 sensitizes hyperhomocysteinemic mice to endothelial dysfunction. Arterioscler Thromb Vasc Biol 2002;22:1996-2002.