ENOS-uncoupling in age-related erectile dysfunction

International Journal of Impotence Research

Volumn 23, Issue 2, 2011, Pages 43-48

  Johnson, J M ^a   Bivalacqua, T J ^a   Lagoda, G A ^a   Burnett, A L ^a   Musicki, B ^a  

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

Author keywords

erection; oxidative stress; penis; tetrahydrobiopterin

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; SEPIAPTERIN; TETRAHYDROBIOPTERIN; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

AGE DISTRIBUTION; AGED; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ELECTROSTIMULATION; ENDOTHELIAL DYSFUNCTION; ERECTILE DYSFUNCTION; MALE; NONHUMAN; OXIDATIVE STRESS; PENIS ERECTION; PRIORITY JOURNAL; RAT; WESTERN BLOTTING;

AGING; ANIMALS; ERECTILE DYSFUNCTION; MALE; NITRIC OXIDE SYNTHASE TYPE III; OXIDATIVE STRESS; PENILE ERECTION; PENIS; PTERINS; RATS; RATS, INBRED F344; THIOBARBITURIC ACID REACTIVE SUBSTANCES;

EID: 79955844140     PISSN: 09559930     EISSN: 14765489     Source Type: Journal    
DOI: 10.1038/ijir.2011.2     Document Type: Article

References (39)

1. Garban H, Vernet D, Freedman A, Rajfer J, Gonzalez-Cadavid N. Effect of aging on nitric oxide-mediated penile erection in rats. Am J Physiol 1995; 268: H467-H475.
2. Haas C, Seftel AD, Razmjouei K, Ganz MB, Hampel N, Ferguson K. Erectile dysfunction in aging: upregulation of endothelial nitric oxide synthase. Urology 1998; 51: 516-522. (Pubitemid 28136700)
3. Melman A, Biggs G, Davies K, Zhao W, Tar MT, Christ GJ. Gene transfer with a vector expressing Maxi-K from a smooth muscle-specific promoter restores erectile function in the aging rat. Gene Ther 2008; 15: 364-370. (Pubitemid 351267378)
4. Feldman HA, Goldstein I, Hatzichristou DG, Krane RJ, McKinlay JB. Impotence and its medical and psychosocial correlates: results of the Massachusetts male aging study. J Urol 1994; 151: 54-61. (Pubitemid 24046934)
5. Carrier S, Nagaraju P, Morgan DM, Baba K, Nunes L, Lue TF. Age decreases nitric oxide synthase-containing nerve fibers in the rat penis. J Urol 1997; 157: 1088-1092. (Pubitemid 27066323)
6. Aversa A, Bruzziches R, Francomano D, Natali M, Gareri P, Spera G. Endothelial dysfunction and erectile dysfunction in the aging man. Int J Urol 2010; 17: 38-47.
7. Hannan JL, Blaser MC, Oldfield L, Pang JJ, Adams SM, Pang SC et al. Morphological and functional evidence for the contribution of the pudendal artery in aging-induced erectile dysfunction. J Sex Med 2010; 7: 3373-3384.
8. Bakircioglu ME, Sievert KD, Nunes L, Lau A, Lin CS, Lue TF. Decreased trabecular smooth muscle and caveolin-1 expression in the penile tissue of aged rats. J Urol 2001; 166: 734-738. (Pubitemid 32652309)
9. Davila HH, Rajfer J, Gonzalez-Cadavid NF. Corporal veno-occlusive dysfunction in the aging rat: evaluation by caverno-sometry and cavernosography. Urology 2004; 64: 1261-1266. (Pubitemid 39647086)
10. Ferrini MG, Magee TR, Vernet D, Rajfer J, Gonzalez-Cadavid NF. Aging-related expression of inducible nitric oxide synthase and markers of tissue damage in the rat penis. Biol Reprod 2001; 64: 974-982. (Pubitemid 32174071)
11. Ferrini MG, Davila H, Valente EG, Gonzalez-Cadavid NF, Rajfer J. Aging-related induction of inducible nitric oxide synthase (NOS2A) is vasculo-protective in the arterial media. Cardiovasc Res 2004; 61: 796-805. (Pubitemid 38249479)
12. Pu XY, Wang XH, Gao WC, Yang ZH, Li SL, Wang HP et al. Insulin-like growth factor-1 restores erectile function in aged rats: modulation the integrity of smooth muscle and nitric oxide-cyclic guanosine monophosphate signaling activity. J Sex Med 2008; 5: 1345-1354.
13. Rajasekaran M, Kasyan A, Jain A, Kim SW, Monga M. Altered growth factor expression in the aging penis: the Brown-Norway rat model. J Androl 2002; 23: 393-399. (Pubitemid 34297328)
14. Jin L, Liu T, Lagoda GA, Champion HC, Bivalacqua TJ, Burnett AL. Elevated RhoA/Rho-kinase activity in the aged rat penis: mechanism for age-associated erectile dysfunction. FASEB J 2006; 20: 536-538. (Pubitemid 46671241)
15. Champion HC, Bivalacqua TJ, Hyman AL, Ignarro LJ, Hellstrom WJ, Kadowitz PJ. Gene transfer of endothelial nitric oxide synthase to the penis augments erectile responses in the aged rat. Proc Natl Acad Sci USA 1999; 96: 11648-11652. (Pubitemid 29487435)
16. Bivalacqua TJ, Champion HC, Mehta YS, Abdel-Mageed AB, Sikka SC, Ignarro LJ et al. Adenoviral gene transfer of endothelial nitric oxide synthase (eNOS) to the penis improves age-related erectile dysfunction in the rat. Int J Impot Res 2000; 12(3 suppl): S8-S17. (Pubitemid 32049653)
17. Musicki B, Kramer MF, Becker RE, Burnett AL. Age-related changes in phosphorylation of endothelial nitric oxide synthase in the rat penis. J Sex Med 2005; 2: 347-357. (Pubitemid 40744375)
18. Bivalacqua TJ, Burnett AL, Hellstrom WJ, Champion HC. Overexpression of arginase in the aged mouse penis impairs erectile function and decreases eNOS activity: influence of in vivo gene therapy of anti-arginase. Am J Physiol Heart Circ Physiol 2007; 292: H1340-H1351. (Pubitemid 46377122)
19. Musicki B, Champion HC, Becker RE, Liu T, Kramer MF, Burnett AL. Erection capability is potentiated by chronic sildenafil treatment: role of blood flow-induced endothelial nitric oxide synthase phosphorylation. Mol Pharmacol 2005; 8: 26-232.
20. Hedlund P, Aszodi A, Pfeifer A, Alm P, Hofmann F, Ahmad M et al. Erectile dysfunction in cylic GMP-dependent kinase I-deficient mice. Proc Natl Acad Sci USA 2000; 97: 2349-2354. (Pubitemid 30134072)
21. Bivalacqua TJ, Armstrong JS, Biggerstaff J, Abdel-Mageed AB, Kadowitz PJ, Hellstrom WJ et al. Gene transfer of extracellular SOD to the penis reduces O2-* and improves erectile function in aged rats. Am J Physiol Heart Circ Physiol 2003; 284: H1408-H1421. (Pubitemid 36348605)
22. Touyz RM, Schiffrin EL. Reactive oxygen species in vascular biology: implications in hypertension. Histochem Cell Biol 2004; 122: 339-352. (Pubitemid 39506592)
23. Channon KM. Tetrahydrobiopterin: regulator of endothelial nitric oxide synthase in vascular disease. Trends Cardiovasc Med 2004; 14: 323-327. (Pubitemid 41110612)
24. Katusic ZS, d'Uscio LV, Nath KA. Vascular protection by tetrahydrobiopterin: progress and therapeutic prospects. Trends Pharmacol Sci 2009; 30: 48-54.
25. Musicki B, Liu T, Strong T, Jin L, Laughlin MH, Turk JR et 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: 552-561. (Pubitemid 351337881)
26. Musicki B, Liu T, Lagoda GA, Strong TD, Sezen SF, Johnson JM et 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: 3023-3032.
27. Wang S, Xu J, Song P, Wu Y, Zhang J, Chul Choi H et al. Acute inhibition of guanosine triphosphate cyclohydrolase 1 un¬couples endothelial nitric oxide synthase and elevates blood pressure. Hypertension 2008; 52: 484-490.
28. 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: 1443-1453.
29. Hurt KJ, Musicki B, Palese MA, Crone JK, Becker RE, Moriarity JL et al. Akt-dependent phosphorylation of endothelial nitric-oxide synthase mediates penile erection. Proc Natl Acad Sci USA 2002; 99: 4061-4066. (Pubitemid 34252229)
30. Sindler AL, Delp MD, Reyes R, Wu G, Muller-Delp JM. Effects of aging and exercise training on eNOS uncoupling in skeletal muscle resistance arterioles. J Physiol 2009; 587: 3885-3897.
31. Yang YM, Huang A, Kaley G, Sun D. eNOS uncoupling and endothelial dysfunction in aged vessels. Am J Physiol Heart Circ Physiol 2009; 297: H1829-H1836.
32. Delp MD, Behnke BJ, Spier SA, Wu G, Muller-Delp JM. Ageing diminishes endothelium-dependent vasodilatation and tetra-hydrobiopterin content in rat skeletal muscle arterioles. J Physiol 2008; 586: 1161-1168. (Pubitemid 351267353)
33. Eskurza I, Myerburgh LA, Kahn ZD, Seals DR. Tetrahydro-biopterin augments endothelium-dependent dilatation in sedentary but not in habitually exercising older adults. J Physiol 2005; 568: 1057-1065. (Pubitemid 41646042)
34. Del Rio D, Stewart AJ, Pellegrini N. A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutr Metab Cardiovasc Dis 2005; 15: 316-328. (Pubitemid 41190990)
35. Drummen GP, van Liebergen LC, Op den Kamp JA, Post JA. C11-BODIPY(581/591), an oxidation-sensitive fluorescent li-pid peroxidation probe: (micro)spectroscopic characterization and validation of methodology. Free Radic Biol Med 2002; 33: 473-490. (Pubitemid 34874969)
36. Catala A. Lipid peroxidation of membrane phospholipids generates hydroxy-alkenals and oxidized phospholipids active in physiological and/or pathological conditions. Chem Phys Lipids 2009; 157: 1-11.
37. Peterson TE, d'Uscio LV, Cao S, Wang XL, Katusic ZS. Guanosine triphosphate cyclohydrolase I expression and enzymatic activity are present in caveolae of endothelial cells. Hypertension 2009; 53: 189-195.
38. Hyland K. Inherited disorders affecting dopamine and serotonin: critical neurotransmitters derived from aromatic amino acids. J Nutr 2007; 137(6 Suppl 1): 1568S-1572S. (Pubitemid 46855509)
39. Gangula PR, Mukhopadhyay S, Ravella K, Cai S, Channon KM, Garfield RE et al. Tetrahydrobiopterin (BH4), a cofactor for nNOS, restores gastric emptying and nNOS expression in female diabetic rats. Am J Physiol Gastrointest Liver Physiol 2010; 298: G692-G699.