Insulin stimulation of glucose uptake in skeletal muscles and adipose tissues in vivo is NO dependent

American Journal of Physiology - Endocrinology and Metabolism

Volumn 274, Issue 4 37-4, 1998, Pages

  Roy, Denis ^a   Perreault, Mylène ^a   Marette, André ^a,b  

^a UNIVERSITÉ LAVAL   (Canada)

^b LAVAL UNIVERSITY   (Canada)

Author keywords

Endothelial type nitric oxide synthase; Endothelium; Extensor digitorum longus; Neuronal type nitric oxide synthase; Nitric oxide; Soleus; Vascular beds

Indexed keywords

DEOXYGLUCOSE; GLUCOSE; HUMAN INSULIN; LACTIC ACID; N(G) METHYLARGININE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; SODIUM CHLORIDE; TRITIUM;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXTENSOR DIGITORUM LONGUS MUSCLE; FAST MUSCLE; GASTROCNEMIUS MUSCLE; GLUCOSE TRANSPORT; GLUCOSE UTILIZATION; HEART MUSCLE; HYPERINSULINEMIA; IN VIVO STUDY; MALE; NONHUMAN; PRIORITY JOURNAL; QUADRICEPS FEMORIS MUSCLE; RAT; SKELETAL MUSCLE; SLOW MUSCLE; SOLEUS MUSCLE; TIBIALIS ANTERIOR MUSCLE;

EID: 0031958254     PISSN: 01931849     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpendo.1998.274.4.e692     Document Type: Article

References (36)

1. Balon, T. W., and J. L. Nadler. Nitric oxide release is present from incubated skeletal muscle preparations. J. Appl. Physiol. 77: 2519-2521, 1994.
2. Balon, T. W., and J. L. Nadler. Evidence that nitric oxide increases glucose transport in skeletal muscle. J. Appl. Physiol. 82: 359-363, 1997.
3. Baron, A. D. Hemodynamic actions of insulin. Am. J. Physiol. 267 (Endocrinol. Metab. 30): E187-E202, 1994.
4. Baron, A. D. The coupling of glucose metabolism and perfusion in human skeletal muscle. The potential role of endothelium-derived nitric oxide. Diabetes 45, Suppl. 1: S105-S109, 1996.
5. Baron, A. D., G. Brechtel-Hook, A. Johnson, J. Cronin, R. Learning, and H. O. Steinberg. Effect of perfusion rate on the time course of insulin-mediated skeletal muscle glucose uptake. Am. J. Physiol. 271 (Endocrinol. Metab. 34): E1067-E1072, 1996.
6. Baron, A. D., H. O. Steinberg, H. Chaker, R. Learning, A. Johnson, and G. Brechtel. Insulin-mediated skeletal muscle vasodilation contributes to both insulin sensitivity and responsiveness in lean humans. J. Clin. Invest. 96: 786-792, 1995.
7. Baron, A. D., J. S. Zhu, S. Marshall, O. Irsula, G. Brechtel, and C. Keech. Insulin resistance after hypertension induced by the nitric oxide synthesis inhibitor L-NMMA in rats. Am. J. Physiol. 269 (Endocrinol. Metab. 32): E709-E715, 1995.
8. Bédard, S., B. Marcotte, and A. Marette. Cytokines modulate glucose transport in skeletal muscle by inducing the expression of inducible nitric oxide synthase. Biochem. J. 325: 487-493, 1997.
9. Chen, Y. L., and E. J. Messina. Dilation of isolated skeletal muscle arterioles by insulin is endothelium dependent and nitric oxide mediated. Am. J. Physiol. 270 (Heart Circ. Physiol. 39): H2120-H2124, 1996.
10. G-monomethyl-L-arginine inhibits the blood flow but not the insulin-like response of forearm muscle to IGF-I: possible role of nitric oxide in muscle protein synthesis. J. Clin. Invest. 97: 1319-1328, 1996.
11. Hansen, P. A., E. A. Gulve, and J. O. Holloszy. Suitability of 2-deoxyglucose for in vitro measurement of glucose transport activity in skeletal muscle. J. Appl. Physiol. 76: 979-985, 1994.
12. Henriksen, E. J., R. E. Bourey, K. J. Rodnick, L. Koranyi, A. Permutt, and J. O. Holloszy. Glucose transporter protein content and glucose transport capacity in rat skeletal muscles. Am. J. Physiol. 259 (Endocrinol. Metab. 22): E593-E598, 1990.
13. James, D. E., K. M. Burleigh, and E. W. Kraegen. In vivo glucose metabolism in individual tissues of the rat. J. Biol. Chem. 261: 6366-6374, 1986.
14. James, D. E., A. B. Jenkins, and E. W. Kraegen. Heterogeneity of insulin action in individual muscles in vivo: euglycemic clamp studies in rats. Am. J. Physiol. 248 (Endocrinol. Metab. 11): E567-E574, 1985.
15. Kahn, B. B. Facilitative glucose transporters: regulatory mechanisms and dysregulation in diabetes. J. Clin. Invest. 89: 1367-74, 1992.
16. Kapur, S., S. Bédard, B. Marcotte, C. H. Côté, and A. Marette. Expression of nitric oxide synthase in skeletal muscle: a novel role for nitric oxide as a modulator of insulin action. Diabetes 46: 1691-1700, 1997.
17. Kern, M., J. A. Wells, J. M. Stephens, C. W. Elton, J. E. Friedman, E. B. Tapscott, P. H. Pekala, and L. Dohm. Insulin responsiveness in skeletal muscle is determined by glucose transporter (GLUT4) protein level. Biochem. J. 270: 397-400, 1990.
18. Klip, A., and A. Marette. Acute and chronic signals controlling glucose transport in-skeletal muscle. J. Cell. Biochem. 48: 51-60, 1992.
19. Kobzik, L., M. B. Reid, D. S. Bredt, and J. S. Stamler. Nitric oxide in skeletal muscle. Nature 372: 546-548, 1994.
20. Kobzik, L., B. Stringer, J. L. Balligand, M. B. Reid, and J. S. Stamler. Endothelial type nitric oxide synthase in skeletal muscle fibers - mitochondrial relationships. Biochem. Biophys. Res. Commun. 211: 375-381, 1995.
21. Kraegen, E. W., D. E. James, A. B. Jenkins, and D. J. Chisholm. Dose-response curves for in vivo insulin sensitivity in individual tissues in rats. Am. J. Physiol. 248 (Endocrinol. Metab. 11): E353-E362, 1985.
22. Marette, A., J. M. Richardson, T. Ramlal, T. W. Balon, M. Vranic, J. E. Pessin, and A. Klip. Abundance, localization, and insulin-induced translocation of glucose transporters in red and white muscle. Am. J. Physiol. 263 (Cell Physiol. 32): C443-C452, 1992.
23. Mitchell, D., and K. Tyml. Nitric oxide release in rat skeletal muscle capillary. Am. J. Physiol. 270 (Heart Circ. Physiol. 39): H1696-H1703, 1996.
24. Nakane, M., H. H. H. W. Schmidt, J. S. Pollock, F. U., and F. Murad. Cloned human brain nitric oxide synthase is highly expressed in skeletal muscle. FEBS Lett. 316: 175-180, 1993.
25. Pette, D., and R. S. Staron. Cellular and molecular diversities of mammalian skeletal muscle fibers. Rev. Physiol. Biochem. Pharmacol. 116: 1-76, 1990.
26. Pître, M., A. Nadeau, and H. Bachelard. Insulin sensitivity and hemodynamic responses to insulin in Wistar-Kyoto and spontaneously hypertensive rats. Am. J. Physiol. 271 (Endocrinol. Metab. 34): E658-E668, 1996.
27. Rees, D. D., R. M. J. Palmer, R. Schulz, H. F. Hodson, and S. Moncada. Characterization of three inhibitors of endothelial nitric oxide synthase in vitro and in vivo. Br. J. Pharmacol. 101: 746-752, 1990.
28. Ribière, C., A. M. Jaubert, N. Gaudiot, D. Sabourault, M. L. Marcus, J. L. Boucher, D. Denishenriot, and Y. Giudicelli. White adipose tissue nitric oxide synthase - a potential source for NO production. Biochem. Biophys. Res. Commun. 222: 706-712, 1996.
29. G-nitro-L-arginine methyl ester causes glomerular nitrite production in long-term incubations. Nephron 73: 97-98, 1996.
30. Scherrer, U., D. Randin, P. Vollenweider, L. Vollenweider, and P. Nicod. Nitric oxide release accounts for insulin's vascular effects in humans. J. Clin. Invest. 94: 2511-2515, 1994.
31. Shibata, H., F. Pérusse, A. Vallerand, and L. J. Bukowiecki. Cold exposure reverses inhibitory effects of fasting on peripheral glucose uptake in rats. Am. J. Physiol. 257 (Regulatory Integrative Comp. Physiol. 26): R96-R101, 1989.
32. Steinberg, H. O., G. Brechtel, A. Johnson, N. Fineberg, and A. D. Baron. Insulin-mediated skeletal muscle vasodilation is nitric oxide dependent. A novel action of insulin to increase nitric oxide release. J. Clin. Invest. 94: 1172-1179, 1994.
33. Swislocki, A., T. Eason, and G. A. Kaysen. Oral administration of the nitric oxide biosynthesis inhibitor, N-nitro-L-arginine methyl ester (L-NAME), causes hypertension, but not glucose intolerance or insulin resistance, in rats. Am. J. Hypertens. 8: 1009-1014, 1995.
34. Vallerand, A. L., F. Pérusse, and L. J. Bukowiecki. Cold exposure potentiates the effect of insulin on in vivo glucose uptake. Am. J. Physiol. 253 (Endocrinol. Metab. 16): E179-E186, 1987.
35. G-nitro-L-arginine methyl ester in plasma by high-performance liquid chromatography. J. Chromatogr. B Biomed. Appl. 660: 170-175, 1994.
36. Young, M. E., G. K. Radda, and B. Leighton. Nitric oxide stimulates glucose transport and metabolism in rat skeletal muscle in vitro. Biochem. J. 322: 223-228, 1997.