Selective nitrergic neurodegeneration in diabetes mellitus - A nitric oxide-dependent phenomenon

British Journal of Pharmacology

Volumn 128, Issue 8, 1999, Pages 1804-1812

  Cellek, Selim ^a   Rodrigo, José ^b   Lobos, Edgar ^a   Fernández, Patricia ^b   Serrano, Julia ^b   Moncada, Salvador ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b INSTITUTO CAJAL   (Spain)

Author keywords

Diabetes mellitus; Erectile dysfunction; Impotence; Neurodegeneration; Nitrergic; Nitric oxide; Penile erection; Streptozotocin

Indexed keywords

N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; STREPTOZOCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETES MELLITUS; ENZYME ACTIVITY; IMMUNOHISTOCHEMISTRY; IMPOTENCE; MALE; NERVE DEGENERATION; NERVE STIMULATION; NEUROPROTECTION; NONHUMAN; NORADRENERGIC NERVE; PENIS ERECTION; PRIORITY JOURNAL; RAT;

EID: 0033429245     PISSN: 00071188     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.bjp.0702981     Document Type: Article

References (52)

1. ANDERSSON, K.E. (1993). The pharmacology of lower urinary tract smooth muscles and penile erectile tissues. Pharmacol. Rev., 45, 253-308.
2. ANDERSSON, K.E. & WAGNER, G. (1995). Physiology of penile erection. Physiol. Rev., 75, 191-235.
3. AZADZOI, K.M. & SAEZ DE TEJADA, I. (1992). Diabetes mellitus impairs neurogenic and endothelium-dependent relaxation of rabbit corpus cavernosum smooth muscle. J. Urol., 148, 1587-1591.
4. BAYNES, J.W. (1991). Role of oxidative stress in development of complications in diabetes. Diabetes, 40, 405-412.
5. BIAN, K., DAVIS, K., KURET, J., BINDER, L. & MURAD, F. (1999). Nitrotyrosine formation with endotoxin-induced kidney injury detected by immunohistochemistry. Am. J. Physiol., 277, F33-F40.
6. BRINDLEY, G.S. (1986). Pilot experiments on the action of drugs injected into the human corpus cavernosum penis. Br. J. Pharmacol., 87, 495-500.
7. BURNETT, A.L, LOWENSTEIN, C.J., BREDT, D.S., CHANG, T.S.K. & SNYDER, S.H. (1992). Nitric oxide: a physiological mediator of penile erection. Science, 257, 401-403.
8. BUSH, P.A., ARONSON. W.J., BUGA, G.M., RAJFER, J. & IGNARRO, L.J. (1992). Nitric oxide is a potent relaxant of human and rabbit corpus cavernosum. J. Urol., 147, 1650-1655.
9. 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. U.S.A., 94, 8226-8231.
10. CHRIST, G.J., KIM, D.C., TAUB, H.C., GONDRE, C.M. & MELMAN, A. (1995). Characterization of nitroglycerine-induced relaxation in human corpus cavernosum smooth muscle: implications to erectile physiology and dysfunction. Can. J. Physiol. Pharmacol., 73, 1714-1726.
11. CLARKE, B.F., EWING, D.J. & CAMPBELL, I.W. (1979). Diabetic autonomic neuropathy. Diabetologia, 17, 195-212.
12. DAVIES, R.E., BASHFORT, P.M. & DOCHERTY, R.J. (1998). A comparison of the effects of capsaicin with inhibitory nerve stimulation in the rat anococcygeus muscle in vitro. Eur. J. Pharmacol., 355, 195-202.
13. DAWSON, V.L., DAWSON, T.M., LONDON, E.D., BREDT, D.S. & SNYDER, S.H. (1991). Nitric oxide mediates glutamate neurotoxicity in primary cortical culture. Proc. Nat. Acad. Sci. U.S.A., 88, 6368-6371.
14. ELABBADY, A.A., GAGNON, C., HASSOUNA, M.M., BEGIN, L.R. & ELHILALI, M.M. (1995). Diabetes mellitus increases nitric oxide synthase in penises but not in major pelvic ganglia of rats. Br. J. Urol., 76, 196-202.
15. El-SAKKA, A.I., LIN, C.S., CHUI, RM., DAHIYA, R. & LUE, T.F. (1999). Effects of diabetes on nitric oxide synthase and growth factor genes and protein expression in an animal model. Int. J. Impot. Res., 11, 123-132.
16. FAERMN, I., GLOCER, L., FOX, D., JADZINSKY, M.N. & RAPAPORT, M. (1974). Impotence and diabetes: Histological studies of the autonomic nervous fibers of the corpora cavernosa in important diabetic males. Diabetes, 23, 971-976.
17. FINBERG, J.P.M., LEVY, S. & VARDI, Y. (1993). Inhibition of nerve stimulation-induced vasodilatation incorpora cavernosa of the pithed rat by blockade of nitric oxide synthase. Br. J. Pharmacol., 108, 1038-1042.
18. HOLMQUIST, F., HEDLUND, H. & ANDERSSON, K.E. (1992). Characterization of inhibitory neurotransmission in the isolated corpus cavernosum from rabbit and man. J. Physiol., 449, 295-311.
19. G-nitro-L-arginine on the erectile response to cavernous nerve stimulation in the rabbit. Acta Physiol. Scand., 143, 299-304.
20. HONING, M.L., MORRISON, P.J., BANGA, J.D., STROES, E.S. & RABELINK, T.J. (1998). Nitric oxide availability in diabetes mellitus. Diabetes. Metab. Rev., 14, 241-249.
21. KASAKOV, L., CELLEK, S. & MONCADA, S. (1995). Characterization of nitrergic neurotransmission during short- and long-term electrical stimulation of the rabbit anococcygeus muscle. Br. J. Pharmacol., 115, 149-1154.
22. KIM, N., AZADOZOI, K.M., GOLDSTEIN, I. & SAENZ DE TEJADA, I. (1991). A nitric oxide-like factor mediates non-adrenergic non-cholinergic neurogenic relaxation of penile corpus cavenosum smooth muscle. J. Clin. Invest., 88, 112-118.
23. KNOWLES, R.G. & SALTER, M. (1997). Measurement of NOS activity by conversion of radiolabeled arginine to citrulline using ion-exchange separation. In: Titheradge, M.A. (ed.). Methods in Molecular Biology. Humana Press: Totowa, pp. 67-73.
24. KOLB, K., KIESEL, U., KRONCKE, K.D. & KOLB-BACHOFE, V. (1991). Suppression of low dose streptozotocin-induced diabetes in mice by administration of a nitric oxide synthase inhibitor. Life Sci., 49, PL213-PL217.
25. LI, C.G. & RAND, M.J. (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.
26. LINCOLN, J., CROWE, R., BLACKLAY, P.F., PRYOR, J.P., LUMLEY, J.S. & BURNSTOCK, G. (1987). Changes in the vipergic, cholinergic and adrenergic innervation of human penile tissue in diabetic and non-diabetic impotent males. J. Urol., 137, 1053-1059.
27. LUE, T. & TANAGHO, E. (1987). Physiology of erection and pharmacological management of impotence. J. Urol., 137, 829-836.
28. LYALL, F., GIBSON, J.L., GREER, I.A., BROCKMAN, D.E., EIS, A.L. & MYATT, L. (1998). Increased nitrotyrosine in the diabetic placenta: evidence for oxidative stress. Diabetes Care, 21, 1753-1758.
29. MELMAN, A. & HENRY, D.P. (1979). The possible role of catecholamines of the corporal bodies in the penile erection. J. Urol., 121, 419-421.
30. MONCADA, S., HIGGS, E.A. & FURCHGOTT, R.F. (1997). International Union of Pharmacology Nomenclature in Nitric Oxide Research. Pharmacol. Rev., 49, 137-142.
31. MONCADA, S., PALMER, R.M. & HIGGS, E.A. (1991). Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev., 43, 109-142.
32. NAVA, E., SALAZAR, F.J., BENTURA, M.L., MURILLO, R.M., FERNANDEZ, A.P., SERRANO, J & RODRIGO, J. (1999). Intrarenal distribution of constitutive nitric oxide synthases and nitrotyrosine in spontaneous hypertension. Acta Physiol. Scand., 167 (Suppl): 34.
33. NAVARRO, J., SANCHEZ, A., SAIZ, J., RUILOPE, L.M., GARCIA-ESTAN, J., ROMERO, J.C., MONCADA, S. & LAHERA, V. (1994). Hormonal, renal and metabolic alterations during hypertension induced by chronic inhibition of NO in rats. Am. J. Physiol., 267, R1516-R1521.
34. OKAMURA, T., AYAJIKI, K., FUJIOKA, H., TODA, M., FUJIMIYA, M. & TODA, N. (1999). Effects of endothelial impairment by saponin on the responses to vasodilators and nitrergic nerve stimulation in isolated canine corpus cavernosum. Br. J. Pharmacol., 127, 802-808.
35. PALMER, R.M.J., ASHTON, D.S. & MONCADA, S. (1988). Vascular endothelial cells synthesize nitric oxide from L-arginine. Nature, 333, 664-666.
36. G-nitro-L-arginine pharmacokinetics in rats after a single intravascular or oral dose: an appearance of secondary concentration time peaks. Drug. Metab. Dispos., 21, 962-964.
37. RAKIETEN, N., RAKIETEN, M.L. & NADKARNI, M.V. (1963). Studies on the diabetogenic action of streptozotocin (NSC-37917). Cancer Chemother. Rep., 29, 91-98.
38. REHMAN, J., CHENVEN, E., BRINK, P., PETERSON, B., WALCOTT, W., WEN, Y.P., MELMAN, A. & CHRIST, G. (1997). Diminished neurogenic but not pharmacological erections in the 2- to 3-month experimentally diabetic F-344 rat. Am. J. Physiol., 272, H1960-H1971.
39. RODRIGO, J., RIVEROS-MORENO, V., BENTURA, M.L., UTTENTHAL, L.O., HIGGS, E.A., FERNANDEZ, A.P., POLAK, J.M., MONCADA, S., MARTINEZ-MURILLO, R. (1997). Subcellular localization of nitric oxide synthase in the cerebral ventricular system, subfornical organ, area postrema, and blood vessels of the rat brain. J. Comp. Neurol., 378, 522-534.
40. RODRIGO, J., SPRINGALL, D.R., UTTENTHAL, O., BENTURA, M.L., ABADIA-MOLINA, F., RIVEROS-MORENO, V., MARTINEZ-MURILLO, R., POLAK, J.M. & MONCADA, S. (1994). Localization of nitric oxide synthase in adult rat brain. Phil. Trans. R. Soc. Lond. B., 345, 175-221.
41. RODRIGO, J., UTTENTHAL, L.O., PEINADO, M.A., ESTEBAN, F.J., FERNANDEZ, A.P., SERRANO, J., MARTINEZ DE VELASCO, J., SANTACANA, M., BENTURA, M.L., MARTINEZ-MURILLO, R., PEDROSA, J.A. (1998). Distribution of nitric oxide synthase in the esophagus of the cat and monkey. J. Auton, Nerv. Syst., 70, 164-179.
42. RUBIN, A. & BABBOTT, D. (1958). Impotence and diabetes mellitus. J.A.M.A., 168, 498-500.
43. SAENZ DE TAJADA, I., BLANCO, R., GOLDSTEIN, I., AZADZOI, K., DE LAS KRANE, R.J. & COHEN, R.A. (1988). Cholinergic neurotransmission in human corpus cavernosum. I. Responses of the isolated tissue. Am. J. Physiol., 254, H468-H472.
44. SAENZ DE TEJADA, I., GOLDSTEIN, I., AZADZOI, K.M., KRANE, R.J. & COHEN, R.A. (1989). Impaired neurogenic and endothelium-mediated relaxation of penile smooth muscle from diabetic men with impotence. New Engl. J. Med., 320, 1025.
45. SCHIRAR, A., GIULIANO, F., RAMPI, O. & ROUSSEAU, J.P. (1994). A large proportion of pelvic neurons innervating the corpora cavernosa of the rat penis exhibit NADPH-diaphorase activity. Cell Tissue Res., 278, 517-525.
46. G-nitro-L-arginine in rats. Br. J. Pharmacol., 111, 394-396.
47. TAUB, H.C., LERNER, S.E., MELMAN, A. & CHRIST, G.J. (1993). Relationship between contraction and relaxation in human and rabbit corpus cavernosum. Urology, 42, 698-704.
48. TEIXEIRA, C.E., BENTO, A.C., LOPES-MARTINS, R.A., TEIXEIRA, S.A., VON EICKESTEDT, V., MUSCARA, M.N., ARANTES, E.C., GIGLIO, J.R., ANTUNES, E. & DE NUCCI, G. (1998). Effect of Tityus serrulatus scorpion venom on the rabbit isolated corpus cavernosum and the involvement of NANC nitrergic nerve fibres. Br. J. Pharmacol., 123, 435-442.
49. TRIGO-ROCHA, F., ARONSON, W.J., HOHENFELLNER, L.J., IGNARRO, L.J., RAJEER, L.J., RAJEER, J. & LUE, T.F. (1993). Nitric oxide and cGMP: mediators of pelvic nerve-stimulated erection in dogs. Am. J. Physiol., 264, H419-H422.
50. UTTENTHAL, L.O., ALONSO, D., FERNANDEZ, A.P., CAMPBELL, R.D., MORO, M.A., LEZA, J.C., LISAZOAIN, I., ESTEBAN, F.J., BARROSO, J.B., VALDERRAMA, R., PEDROSA, J.A, PEINADO, M.A., SERRANO, J., RICHARD, A., BENTURA, M.L., SANTACANA, M., MARTINEZ-MURILLO, R. & RODRIGO, J. (1998). Neuronal and inducible nitric oxide synthase and nitrotyrosine immunoreactivities in the cerebral cortex of the aging rat. Microsc. Res. Tech., 43, 75-88.
51. dp (Type II) rats with erectile dysfunction. Endocrinology, 136, 5709-5717.
52. WAGNER, G. & BRINDLEY, G.S. (1980). The effect of atropin and α- and β-blockers on human penile erection: a controlled pilot study. In: Zorgiotti, A.W. & Rossi, G. (eds.). Vasculogenic Impotence. Thomas: Springfield, IL. pp. 77-81.