Understanding the in-vivo relevance of S-nitrosothiols in insulin action

Canadian Journal of Physiology and Pharmacology

Volumn 90, Issue 7, 2012, Pages 887-894

  Fernandes, Ana B ^a   Guarino, Maria P ^b   Macedo, M Paula ^a  

^a UNIVERSIDADE NOVA DE LISBOA   (Portugal)

^b Portuguese Diabetes Association Education and Research Center (APDP ERC)   (Portugal)

Author keywords

Glutathione; Hepatic parasympathetic nerves; Insulin sensitivity; Nitric oxide; Nitrosothiols; Nitrosylation

Indexed keywords

GLUCOSE; HUMAN INSULIN; INSULIN; LINSIDOMINE; N ACETYL S NITROSOPENICILLAMINE; S NITROSOGLUTATHIONE;

ANALYTIC METHOD; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DENERVATION; DRUG MECHANISM; FEEDING; HYPOTHESIS; IN VIVO STUDY; INSULIN SENSITIVITY; MALE; NONHUMAN; PRIORITY JOURNAL; RAPID INSULIN SENSITIVITY TEST; RAT;

ANIMALS; BLOOD GLUCOSE; FASTING; INSULIN; INSULIN RESISTANCE; MALE; MOLSIDOMINE; NITRIC OXIDE; POSTPRANDIAL PERIOD; RATS; RATS, WISTAR; S-NITROSO-N-ACETYLPENICILLAMINE; S-NITROSOGLUTATHIONE; S-NITROSOTHIOLS;

EID: 84863707319     PISSN: 00084212     EISSN: 12057541     Source Type: Journal    
DOI: 10.1139/Y2012-090     Document Type: Article

References (42)

1. Badal, S., Brown, P.D., and Ragoobirsingh, D. 2006. Nitric oxide agents impair insulin-mediated signal transduction in rat skeletal muscle. BMC Biochem. 7(1): 17. doi:10.1186/1471-2091-7-17. PMID:16729893.
2. Baron, A.D., Steinberg, H.O., Chaker, H., Leaming, R., Johnson, A., and Brechtel, G. 1995. Insulin-mediated skeletal muscle vasodilation contributes to both insulin sensitivity and responsiveness in lean humans. J. Clin. Invest. 96(2): 786-792. doi:10.1172/ JCI118124. PMID:7635973.
3. Carvalho-Filho, M.A., Ueno, M., Hirabara, S.M., Seabra, A.B., Carvalheira, J.B., de Oliveira, M.G., et al. 2005. S-nitrosation of the insulin receptor, insulin receptor substrate 1, and protein kinase B/Akt: a novel mechanism of insulin resistance. Diabetes, 54(4): 959-967. doi:10.2337/diabetes.54.4.959. PMID:15793233.
4. Carvalho-Filho, M.A., Ueno, M., Carvalheira, J.B., Velloso, L.A., and Saad, M.J. 2006. Targeted disruption of iNOS prevents LPS-induced S-nitrosation of IRbeta/IRS-1 and Akt and insulin resistance in muscle of mice. Am. J. Physiol. Endocrinol. Metab. 291(3): E476-E482. doi:10.1152/ajpendo.00422.2005. PMID: 16638822.
5. Clark, M.G., Wallis, M.G., Barrett, E.J., Vincent, M.A., Richards, S.M., Clerk, L.H., and Rattigan, S. 2003. Blood flow and muscle metabolism: a focus on insulin action. Am. J. Physiol. Endocrinol. Metab. 284(2): E241-E258. PMID:12531739.
6. Elrod, J.W., Calvert, J.W., Gundewar, S., Bryan, N.S., and Lefer, D.J. 2008. Nitric oxide promotes distant organ protection: evidence for an endocrine role of nitric oxide. Proc. Natl. Acad. Sci. U.S.A. 105 (32): 11430-11435. doi:10.1073/pnas.0800700105. PMID: 18685092.
7. Fernandes, A.B., Patarrao, R.S., Videira, P.A., and Macedo, M.P. 2011. Understanding postprandial glucose clearance by peripheral organs: the role of the hepatic parasympathetic system. J. Neuroendocrinol. 23(12): 1288-1295. doi:10.1111/j.1365-2826. 2011.02226.x. PMID:21933289.
8. Foster, M.W., McMahon, T.J., and Stamler, J.S. 2003. S-nitrosylation in health and disease. Trends Mol. Med. 9(4): 160-168. doi:10. 1016/S1471-4914(03)00028-5. PMID:12727142.
9. Foster, M.W., Hess, D.T., and Stamler, J.S. 2009. Protein S-nitrosylation in health and disease: a current perspective. Trends Mol. Med. 15(9): 391-404. doi:10.1016/j.molmed.2009.06.007. PMID:19726230.
10. Guarino, M.P., and Macedo, M.P. 2006. Co-administration of glutathione and nitric oxide enhances insulin sensitivity in Wistar rats. Br. J. Pharmacol. 147(8): 959-965. doi:10.1038/sj.bjp. 0706691. PMID:16491098.
11. Guarino, M.P., Correia, N.C., Lautt, W.W., and Macedo, M.P. 2004. Insulin sensitivity is mediated by the activation of the ACh/NO/ cGMP pathway in rat liver. Am. J. Physiol. Gastrointest. Liver Physiol. 287(3): G527-G532. doi:10.1152/ajpgi.00085.2004. PMID:15331351.
12. Hogg, N. 2002. The biochemistry and physiology of S-nitrosothiols. Annu. Rev. Pharmacol. Toxicol. 42(1): 585-600. doi:10.1146/ annurev.pharmtox.42.092501.104328. PMID:11807184.
13. Jia, L., Bonaventura, C., Bonaventura, J., and Stamler, J.S. 1996. S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control. Nature, 380(6571): 221-226. doi:10.1038/ 380221a0. PMID:8637569.
14. Kashiba, M., Kasahara, E., Chien, K.C., and Inoue, M. 1999. Fates and vascular action of S-nitrosoglutathione and related compounds in the circulation. Arch. Biochem. Biophys. 363(2): 213-218. doi:10.1006/abbi.1998.1055. PMID:10068442.
15. Kashiba-Iwatsuki, M., Kitoh, K., Kasahara, E., Yu, H., Nisikawa, M., Matsuo, M., and Inoue, M. 1997. Ascorbic acid and reducing agents regulate the fates and functions of S-nitrosothiols. J. Biochem. 122(6): 1208-1214. doi:10.1093/oxfordjournals.jbchem. a021883. PMID:9498567.
16. Latour, M.G., and Lautt, W.W. 2002a. The hepatic vagus nerve in the control of insulin sensitivity in the rat. Auton. Neurosci. 95(1-2): 125-130. doi:10.1016/S1566-0702(01)00390-3. PMID:11871777.
17. Latour, M.G., and Lautt, W.W. 2002b. Insulin sensitivity regulated by feeding in the conscious unrestrained rat. Can. J. Physiol. Pharmacol. 80(1): 8-12. doi:10.1139/y01-094. PMID:11911229.
18. Lautt, W.W., Wang, X., Sadri, P., Legare, D.J., and Macedo, M.P. 1998. Rapid insulin sensitivity test (RIST). Can. J. Physiol. Pharmacol. 76(12): 1080-1086. doi:10.1139/y98-127. PMID: 10326829.
19. Lautt, W.W., Macedo, M.P., Sadri, P., Takayama, S., Duarte Ramos, F., and Legare, D.J. 2001. Hepatic parasympathetic (HISS) control of insulin sensitivity determined by feeding and fasting. Am. J. Physiol. Gastrointest. Liver Physiol. 281(1): G29-G36. PMID: 11408252.
20. Lira, V.A., Soltow, Q.A., Long, J.H., Betters, J.L., Sellman, J.E., and Criswell, D.S. 2007. Nitric oxide increases GLUT4 expression and regulates AMPK signaling in skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 293(4): E1062-E1068. doi:10.1152/ajpendo. 00045.2007. PMID:17666490.
21. Mayer, B., Pfeiffer, S., Schrammel, A., Koesling, D., Schmidt, K., and Brunner, F. 1998. A new pathway of nitric oxide/cyclic GMP signaling involving S-nitrosoglutathione. J. Biol. Chem. 273(6): 3264-3270. doi:10.1074/jbc.273.6.3264. PMID:9452441.
22. McGrowder, D., Ragoobirsingh, D., and Dasgupta, T. 2002a. Decreased insulin binding to mononuclear leucocytes and erythrocytes from dogs after S-nitroso-N-acetypenicillamine administration. BMC Biochem. 3(1): 1. doi:10.1186/1471-2091-3-1. PMID:11825341.
23. McGrowder, D., Ragoobirsingh, D., and Dasgupta, T. 2002b. The enhancement of the hyperglycemic effect of S-nitrosoglutathione and S-nitroso-N-acetylpenicillamine by vitamin C in an animal model. BMC Pharmacol. 2(1): 18. doi:10.1186/1471-2210-2-18. PMID:12230634.
24. McGrowder, D., Ragoobirsingh, D., and Brown, P. 2006. Acute effects of exogenous nitric oxide on glucose uptake in skeletal muscle of normoglycaemic and diabetic rats. Med. Sci. Monit. 12 (1): BR28-BR35. PMID:16369460.
25. Miersch, S., and Mutus, B. 2005. Protein S-nitrosation: biochemistry and characterization of protein thiol-NO interactions as cellular signals. Clin. Biochem. 38(9): 777-791. doi:10.1016/j. clinbiochem.2005.05.014. PMID:16005861.
26. Ming, Z., and Lautt, W.W. 2011. HISS, not insulin, causes vasodilation in response to administered insulin. J. Appl. Physiol. 110(1): 60-68. doi:10.1152/japplphysiol.00714.2010. PMID: 20829499.
27. Moore, M.C., Satake, S., Baranowski, B., Hsieh, P.S., Neal, D.W., and Cherrington, A.D. 2002. Effect of hepatic denervation on peripheral insulin sensitivity in conscious dogs. Am. J. Physiol. Endocrinol. Metab. 282(2): E286-E296. PMID:11788359.
28. Patarrão, R.S., Lautt, W.W., Afonso, R.A., Ribeiro, R.T., Guarino, M.P., Fernandes, A.B., et al. 2008. Meal-induced insulin sensitization and its parasympathetic regulation in humans. Can. J. Physiol. Pharmacol. 86(12): 880-888. doi:10.1139/Y08-080. PMID: 19088809.
29. Radomski, M.W., Palmer, R.M., and Moncada, S. 1987. Endogenous nitric oxide inhibits human platelet adhesion to vascular endothelium. Lancet, 330(8567): 1057-1058. doi:10.1016/ S0140-6736(87)91481-4. PMID:2889967.
30. Rassaf, T., Feelisch, M., and Kelm, M. 2004. Circulating NO pool: assessment of nitrite and nitroso species in blood and tissues. Free Radic. Biol. Med. 36(4): 413-422. doi:10.1016/j.freeradbiomed. 2003.11.011. PMID:14975444.
31. Reid, M.A., Latour, M.G., Legare, D.J., Rong, N., and Lautt, W.W.2002. Comparison of the rapid insulin sensitivity test (RIST), the insulin tolerance test (ITT), and the hyperinsulinemic euglycemic clamp (HIEC) to measure insulin action in rats. Can. J. Physiol. Pharmacol. 80(8): 811-818. doi:10.1139/y02-102. PMID: 12269792.
32. Schafer, J., Legare, D.J., and Lautt, W.W. 2010. Acetylcholinesterase antagonist potentiated insulin action in fed but not fasted state. J. Pharmacol. Exp. Ther. 333(2): 621-628. doi:10.1124/jpet.109. 164509. PMID:20133391.
33. Scherrer, U., Randin, D., Vollenweider, P., Vollenweider, L., and Nicod, P. 1994. Nitric oxide release accounts for insulin's vascular effects in humans. J. Clin. Invest. 94(6): 2511-2515. doi:10.1172/ JCI117621. PMID:7989610
34. Schrammel, A., Gorren, A.C., Schmidt, K., Pfeiffer, S., and Mayer, B.2003. S-nitrosation of glutathione by nitric oxide, peroxynitrite, and (*)NO/O(2)(*-). Free Radic. Biol. Med. 34(8): 1078-1088. doi:10.1016/S0891-5849(03)00038-8. PMID:12684093.
35. Stamler, J.S. 2003. Hemoglobin and nitric oxide. N. Engl. J. Med. 349(4): 402-405. doi:10.1056/NEJM200307243490419. PMID:12878751.
36. Stamler, J.S., Singel, D.J., and Loscalzo, J. 1992. Biochemistry of nitric oxide and its redox-activated forms. Science, 258(5090):1898-1902. doi:10.1126/science.1281928. PMID:1281928.
37. Stamler, J.S., Lamas, S., and Fang, F.C. 2001. Nitrosylation. The prototypic redox-based signaling mechanism. Cell, 106(6): 675-683. doi:10.1016/S0092-8674(01)00495-0. PMID:11572774.
38. Terrettaz, J., Assimacopoulos-Jeannet, F., and Jeanrenaud, B. 1986.Inhibition of hepatic glucose production by insulin in vivo in rats:contribution of glycolysis. Am. J. Physiol. 250(4): E346-E351.PMID:3008568.
39. Xie, H., and Lautt, W.W. 1996. Insulin resistance of skeletal muscle produced by hepatic parasympathetic interruption. Am. J. Physiol.270(5): E858-E863. PMID:8967475.
40. Xie, H., Tsybenko, V.A., Johnson, M.V., and Lautt, W.W. 1993.Insulin resistance of glucose response produced by hepatic denervations. Can. J. Physiol. Pharmacol. 71(2): 175-178.doi:10.1139/y93-024. PMID:8319140.
41. Yasukawa, T., Tokunaga, E., Ota, H., Sugita, H., Martyn, J.A., and Kaneki, M. 2005. S-nitrosylation-dependent inactivation of Akt/protein kinase B in insulin resistance. J. Biol. Chem. 280(9):7511-7518. doi:10.1074/jbc.M411871200. PMID:15632167.
42. Zhang, Y., and Hogg, N. 2005. S-nitrosothiols: cellular formation and transport. Free Radic. Biol. Med. 38(7): 831-838. doi:10.1016/j.freeradbiomed.2004.12.016. PMID:15749378.