In vivo depletion of free thiols does not account for nitroglycerin-induced tolerance: A thiol-nitrate interaction hypothesis as an alternative explanation for nitroglycerin activity and tolerance

Journal of Pharmacology and Experimental Therapeutics

Volumn 278, Issue 3, 1996, Pages 1296-1305

  Haj Yehia, Abdullah I ^a   Benet, Leslie Z ^b  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCERYL TRINITRATE; NITROPRUSSIDE SODIUM; THIOL DERIVATIVE;

ALKYLATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CATECHOLAMINE DEPLETION; CONTROLLED STUDY; DISSOCIATION; DRUG EFFECT; DRUG TOLERANCE; HYPOTHESIS; INFERIOR CAVA VEIN; NITROSATION; NONHUMAN; PRIORITY JOURNAL; RAT; VASODILATATION;

ANIMALS; AORTA; CYCLIC GMP; DRUG TOLERANCE; ETHYLMALEIMIDE; GLUTATHIONE TRANSFERASE; MALE; NITRIC OXIDE; NITROGLYCERIN; NITROPRUSSIDE; PENICILLAMINE; RATS; RATS, SPRAGUE-DAWLEY; S-NITROSO-N-ACETYLPENICILLAMINE; SULFHYDRYL COMPOUNDS; SULFHYDRYL REAGENTS; VASODILATOR AGENTS;

EID: 0030433664     PISSN: 00223565     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (57)

1. - donation by S-nitrosothiols: Implication for regulation of physiological functions by S-nitrosylation and acceleration of disulfide formation. Arch. Biochem. Biophys. 318: 279-285, 1995.
2. BAUER, J. AND FUNG, H.-L.: Differential hemodynamic effect and tolerance properties of nitroglycerin and an S-nitrosothiol in experimental heart failure. J. Pharmacol. Exp. Ther. 256: 249-254, 1991.
3. BOESGAARD, S., ALDERSHVILLE, J., POULSEN, H. E., LOFT, S., ANDERSON, M. A. AND MEISTER, A.: Nitrate tolerance in vivo is not associated with depletion of arterial or venous thiol levels. Circ. Res. 74: 115-120, 1994.
4. DE GARAVILLA, L., VOLBERG, M. L., PRATT, P. F., SILVER, P. J. AND BUCHHOLZ, R. A.: Lack of cross-tolerance between nitroglycerin and endothelium-derived relaxing factor-mediated vasoactive agents in spontaneously hypertensive rate. Eur. J. Pharmacol. 234: 77-82, 1993.
5. DERUBERTIS, F. R. AND CRAVEN, P. A.: Activation of hepatic guanylate cyclase by N-methyl-N′-nitro-N-nitrosoguanidine: Effects of thiols, N-ethylmaleimide and divalent cations. J. Biol. Chem. 252: 5804-5814, 1977a.
6. DERUBERTIS, F. R. AND CRAVEN, P. A.: Activation of the renal cortical and hepatic guanylate cyclase-guanosine 3′,5′-monophosphate system by nitrosothiols: Divalent cation requirement and relationship to thiol reactivity. Biochim. Biophys. Acta 499: 337-351, 1977b.
7. DERUBERTIS, F. R. AND CRAVEN, P. A.: Effects of thiol inhibitors on hepatic guanylate cyclase: Evidence for the involvement of vicinal dithiols in the expression of basal and agonist-stimulated activity. Biochim. Biophys. Acta 524: 231-244, 1978.
8. Du, Z. Y., BUXTON, B. F. AND WOODMAN, O. L.: Tolerance to glyceryl trinitrate in isolated human internal mammary arteries. Thorac. Cardiovasc. Surg. 104: 1280-1284, 1992.
9. DUDA, T., GORACZNIAK, R. AND SHARMA, R.: The glycine residue of ATP regulatory module in receptor guanylate cyclase that is essential in natriuretic factor signaling. FEBS Lett. 335: 309-314, 1993.
10. DUPUIS, J., LALONDE, G., LEMIEUX, R. AND ROULEAU, J. L.: Tolerance to intravenous nitroglycerin in patients with congestive heart failure: Role of increased intravascular volume, neurohormonal activation and lack of prevention with N-acetylcysteine. J. Am. Coll. Cardiol. 16: 923-931, 1990.
11. FEELISCH, M. AND NOACK, E.: Correlation between nitric oxide formation during degradation of organic nitrates and activation of guanylate cyclase. Eur. J. Pharmacol. 139: 19-30, 1987.
12. FEELISCH, M., NOACK, E. AND SCHRÖDER, H.: Explanation of the discrepancy between the degree of organic nitrate decomposition, nitrite formation and guanylate cyclase stimulation. Eur. Heart J. 9: suppl. A, 57-62, 1988.
13. FEELISCH, M., TE POEL, M., ZAMORA, R., DEUSSEN, A. AND MONCADA, S.: Understanding the controversy over the identity of EDRF. Nature (Lond.) 368: 62-65, 1994.
14. FIELD, L., DILTS, R. V., RAVICHANDRAN, R., LENHERT, P. G. AND CARNAHAN, G. E.: An unusually stable thionitrite from N-acetyl-D,L-peniculamine: X-ray crystal and molecular structure of 2-(acetylamino)-2-carboxyl-1,1-dimethylethyl thionitrite. J. Chem. Soc. Chem. Commun. 1978: 249-250, 1978.
15. FUNG, H.-L., CHONG, S., KOWALUK, E. A., HOUGH, K. AND KAKEMI, M.: Mechanism for the pharmacologic interaction of organic nitrates with thiols: Existence of an extracellular pathway for the reversal of nitrate vascular tolerance by N-acetylcysteine. J. Pharmacol. Exp. Ther. 245: 524-530, 1988.
16. GOLDBERG, N. AND HADDOX, M.: Cyclic GMP metabolism and involvement in biological regulation. Annu. Rev. Biochem. 46: 823-896, 1977.
17. GRIENDLING, K. K., MINIERI, C. A., OLLERENSHAW, J. D. AND ALEXANDER, R. W.: Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ. Res. 74: 1141-1148, 1994.
18. GRUETTER, C. A. AND LEMKE, S. M.: Dissociation of cysteine and glutathione levels from nitroglycerin induced relaxation. Eur. J. Pharmacol. 111: 85-95, 1985.
19. GRUETTER, C. A. AND LEMKE, S. M.: Effects of sulfhydryl reagents on nitroglycerin-induced relaxation of bovine coronary artery. Can. J. Physiol. Pharmacol. 64: 1395-1401, 1986.
20. HAJ-YEHIA, A. I. AND BENET, L. Z.: Dissociation of tissue thiol content from nitroglycerin-induced cyclic-3′,5′-guanosine monophosphate and the state of tolerance: In vivo experiments in rats. J. Pharmacol. Exp. Ther. 278: 94-100, 1995a.
21. HAJ-YEHIA, A. I. AND BENET, L. Z.: Determination of aliphatic thiols by fluorometric high-performance liquid chromatography after pre-column derivatization with 2-(4-N-maleimidophenyl)-6-methyl-benzothiazole. Pharm. Res. 12: 155-160, 1995b.
22. HENRY, P. J., DRUMMER, O. H. AND HOROWITZ, J. D.: S-Nitrosothiols as vasodilators: Implications regarding tolerance to nitric oxide-containing vasodilators. Br. J. Pharmacol. 98: 757-766, 1989.
23. IGNARRO, L. J.: Endothelium-derived nitric oxide: Pharmacology and relationship to the action of organic nitrate esters. Pharm. Res. 6: 651-659, 1989.
24. IGNABBO, L. J. AND GRUETTER, C. A.: Requirements of thiols for activation of coronary arterial guanylate cyclase by glyceryl trinitrate and sodium nitrite: Possible involvement of S-nitrosothiol. Biochim. Biophys. Acta 631: 221-225, 1980.
25. IGNARRO, L. J., LIPPTON, H., EDWARDS, J. C., BARICOS, W. H., HYMAN, A. L., KADOWITZ, P. J. AND GRUETTER, C. A.: Mechanism of vascular smooth muscle relaxation by organic nitrates, nitrites, nitroprusside and nitric oxide: Evidence for the involvement of S-nitrosothiols as active intermediates. J. Pharmacol. Exp. Ther. 218: 739-749, 1981a.
26. IGNARRO, L. J., KADOWITZ, P. J. AND BARICOS, W. H.: Evidence that regulation of hepatic guanylate cyclase activity involves interaction between catalytic site - SH groups and both substrate and activator. Arch. Biochem. Biophys. 208: 75-86, 1981b.
27. ISONO, T., SATO, N., YAMAMOTO, T., SAWADA, T., YAMAZAKI, S., MIURA, S., FURUICHI, A., OZAKI, R., KOIBUCHI, Y. AND OHTSUKA, M.: Tolerance to vascular effect of a novel nitric oxide-donating vasodilator, FK409. Eur. J. Pharmacol. 260: 163-168, 1994.
28. ITAKURA, M., IWASHINA, M., MIZUNO, T., ITO, T., HAGIWARA, H. AND HIROSE, S.: Mutational analysis of disulfide bridges in the type C atrial natriuretic peptide receptor. J. Biol. Chem. 296: 8314-8318, 1994.
29. JIA, L. AND FURCHGOTT, R. F.: Inhibition by sulfhydryl compounds of vascular relaxation induced by nitric oxide and endothelium-derived relaxing factor. J. Pharmacol. Exp. Ther. 267: 371-378, 1993.
30. KEITH, R. A. AND BURKMAN, A. M.: In vitro induction of nitroglycerin (NTG) tolerance in vascular tissue at pH 7.4 and 9 occurs prior to the decrease in sulfhydryl (SH) content. Fed. Proc. 40: 729, 1981.
31. KOJDA, G., WILFRIED, M. AND NOACK, E.: Influence of endothelium and nitrovasodilators on free thiols and disulfides in porcine coronary smooth muscle. Eur. J. Pharmacol. 250: 385-394, 1993.
32. KOWALUK, E. A. AND FUNG, H.-L.: Spontaneous liberation of nitric oxide cannot account for in vitro vascular relaxation by S-nitrosothiols. J. Pharmacol. Exp. Ther. 255: 1256-1264, 1990.
33. KOWALUK, E. A. AND FUNG, H.-L.: Vascular nitric oxide-generating activities for organic nitrites and organic nitrates are distinct. J. Pharmacol. Exp. Ther. 259: 519-525, 1991.
34. KOWALUK, E. A., POLISZCZUK, S. AND FUNG, H.-L.: Tolerance to relaxation in rat aorta: Comparison of an S-nitrosothiol with nitroglycerin. Eur. J. Pharmacol. 144: 379-383, 1987.
35. KOWALUK, E. A., SETH, P. AND FUNG, H.-L.: Metabolic activation of sodium nitroprusside to nitric oxide in vascular smooth muscle. J. Pharmacol. Exp. Ther. 262: 916-922, 1992.
36. KUKOVETZ, W. R. AND HOLZMANN, S.: Tolerance and cross tolerance between SIN-1 and nitric oxide in bovine coronary arteries. J. Cardiovasc. Pharmacol. 14: suppl. 11, S40-S46, 1989.
37. KUKOVETZ, W. R., HOLZMANN, S. AND SCHMIDT, K: Cellular mechanisms of action of therapeutic nitric oxide donors. Eur. Heart J. 12: suppl. E, 16-24, 1991.
38. - formation. Biochem. J. 292: 545-550, 1993.
39. LEI, S., PAN, Z.-H., AGGARWAL, S., CHEN, H.-S., HARTMAN, J., SUCHER, N. AND LIPTON, S.: Effect of nitric oxide production on the redox modulatory site of the NMDA-receptor-channel complex. Neuron 8: 1087-1099, 1992.
40. LIPTON, S., CHOI, Y.-B., PAN, Z.-H., LEI, S., CHEN, H.-S., SUCHER, N., LOSCALZO, J., SINGEL, D. AND STAMLER, J.: A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature (Lond.) 864: 626-632, 1993.
41. LIU, Z., BRIEN, J. F., MARKS, G. S., MCLAUGHLIN, B. E. AND NAKATSU, K.: Lack of evidence for the involvement of cytochrome P-450 or other hemoproteins in metabolic activation of glyceryl trinitrate in rabbit aorta. J. Pharmacol. Exp. Ther. 264: 1432-1439, 1993.
42. MÜNZEL, T., HOLTZ, J., MÜLSCH, A., STEWART, D. J. AND BASSENGE, E.: Nitrate tolerance in epicardial arteries or in the venous system is not reversed by N-acetylcysteine in vivo, but tolerance-independent interactions exist. Circulation 79: 188-197, 1989.
43. MÜNZEL, T., SAYEGH, H., FREEMAN, B., TARPEY, M. AND HARRISON, D. G.: Evidence for enhanced vascular superoxide anion production in nitrate tolerance: A novel mechanism underlying tolerance and cross-tolerance. J. Clin. Invest. 95: 187-194, 1995a.
44. MÜNZEL, T., GIAID, A., KURZ, S., STEWART, D. J. AND HABRISON, D. G.: Evidence for a role of endothelin 1 and protein kinase C in nitroglycerin tolerance. Proc. Natl. Acad. Sci. U.S.A. 92: 5244-5248, 1995b.
45. NEEDLEMAN, P., JAKSCHIK, E. AND JOHNSON, E. M.: Sulfhydryl requirement for relaxation of vascular smooth muscle. J. Pharmacol. Exp. Ther. 187: 324-331, 1973.
46. NEEDLEMAN, P. AND JOHNSON, E. M., JR.: Mechanism of tolerance development to organic nitrates. J. Pharmacol. Exp. Ther. 184: 709-715, 1973.
47. PARKER, J. O., FARRELL, B., LAHEY, K. E. AND ROSE, B. F.: Nitrate tolerance: The lack of effect of N-acetylcysteine. Circulation 76: 572-576, 1987.
48. RAPAPORT, M. R., WALDMAN, S. A., GINSBURG, R., MOLINA, C. R. AND MURAD, F.: Effects of glyceryl trinitrate on endothelium-dependent and independent relaxation and cyclic GMP levels in rat aorta and human coronary artery. J. Cardiovasc. Pharmacol. 10: 82-89, 1987.
49. ROMANIN, C. H. R. AND KUKOVETZ, W. R.: Tolerance to nitroglycerin is caused by reduced guanylate cyclase activation. J. Mol. Cardiol. 21: 41-48, 1989.
50. SAKANASHI, M., MATSUZAKI, T. AND ANIYA, Y.: Nitroglycerin relaxes coronary artery of pig with no change in glutathione content or glutathione S-transferase activity. Br. J. Pharmacol. 103: 1905-1908, 1991.
51. SALVEMINI, D., PISTELLI, A. AND VANE, J.: Conversion of glyceryl trinitrate to nitric oxide in tolerant and non-tolerant smooth muscle and endothelial cells. Br. J. Pharmacol. 108: 162-169, 1993.
52. SCHARFSTEIN, J. S., KEANEY, J. F., SLIVKA, A., WELCH, G. N., VITA, J. A., STAMLER, J. S. AND LOSCALZO, J.: In vivo transfer of nitric oxide between a plasma protein-bound reservoir and low molecular weight thiols. J. Clin. Invest. 94: 1432-1439, 1994.
53. SCHRÖDER, H., LEITMAN, D., BENNETT, B., WALDMAN, S. AND MURAD, F.: Glyceryl trinitrate-induced desensitization of guanylate cyclase in cultured rat fibroblasts. J. Pharmacol. Exp. Ther. 246: 413-418, 1988.
54. SHAFFER, J., HAN, B.-J., CHERN, W. AND LEE, F.: Lack of tolerance to a 24-hour infusion of S-nitroso-N-acetylpenicillamine (SNAP) in conscious rabbits. J. Pharmacol. Exp. Ther. 260: 286-293, 1992.
55. STAMLER, J., SINGEL, D. AND LOSCALZO, J.: Biochemistry of nitric oxide and its redox-activated forms. Science (Wash. DC) 258: 1898-1905, 1993.
56. VINA, J., ESTELA, J. M., GUERRI, C. AND ROMERO, F. J.: Effect of ethanol on glutathione concentration in isolated hepatocytes. Biochem. J. 188: 549-553, 1980.
57. WALDMAN, S. A., RAPAPORT, R. M., GINSBURG, R. AND MURAD, F.: Desensitization to nitroglycerin in vascular smooth muscle from rat and human. Biochem. Pharmacol. 35: 3525-3531, 1986.