α-Lipoic acid decreases thiol reactivity of the insulin receptor and protein tyrosine phosphatase 1B in 3T3-L1 adipocytes

Biochemical Pharmacology

Volumn 66, Issue 5, 2003, Pages 849-858

  Cho, Kyung Joo ^a   Moini, Hadi ^b   Shon, Hee Kyung ^a   Chung, An Sik ^a   Packer, Lester ^b  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

3T3 L1 adipocytes; Glucose uptake; Insulin; Insulin receptor; Protein tyrosine phosphatase; Thiols; Lipoic acid

Indexed keywords

DIPHENYLIODONIUM SALT; GLUCOSE; HYDROGEN PEROXIDE; INSULIN; INSULIN RECEPTOR; LINOLEIC ACID; OXIDIZING AGENT; PROTEIN TYROSINE PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE 1B; THIOL GROUP; UNCLASSIFIED DRUG;

ADIPOCYTE; ALKYLATION; ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; CELL STIMULATION; CONTROLLED STUDY; ENZYME ACTIVITY; GLUCOSE TRANSPORT; INSULIN SENSITIVITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION;

EID: 0041976916     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-2952(03)00395-2     Document Type: Article

References (48)

1. Berg A., de Kok A. 2-Oxo acid dehydrogenase multienzyme complexes. The central role of the lipoyl domain. Biol. Chem. 378(7):1997;617-634.
2. Packer L., Witt E.H., Tritschler H.J. Alpha-lipoic acid as a biological antioxidant. Free Radic. Biol. Med. 19(2):1995;227-250.
3. Jacob S., Henriksen E.J., Schiemann A.L., Simon I., Clancy D.E., Tritschler H.J., Jung W.I., Augustin H.J., Dietze G.J. Enhancement of glucose disposal in patients with type 2 diabetes by alpha-lipoic acid. Arzneimittelforschung. 45(8):1995;872-874.
4. Ziegler D., Hanefeld M., Ruhnau K.J., Hasche H., Lobisch M., Schutte K., Kerum G., Malessa R. Treatment of symptomatic diabetic polyneuropathy with the antioxidant alpha-lipoic acid: a 7-month multicenter randomized controlled trial (ALADIN III Study). ALADIN III Study Group. Alpha-Lipoic Acid in Diabetic Neuropathy. Diabetes Care. 22(8):1999;1296-1301.
5. Jacob S., Henriksen E.J., Tritschler H.J., Augustin H.J., Dietze G.J. Improvement of insulin-stimulated glucose-disposal in type 2 diabetes after repeated parenteral administration of thioctic acid. Exp. Clin. Endocrinol. Diabetes. 104(3):1996;284-288.
6. Jacob S., Ruus P., Hermann R., Tritschler H.J., Maerker E., Renn W., Augustin H.J., Dietze G.J., Rett K. Oral administration of RAC-alpha-lipoic acid modulates insulin sensitivity in patients with type-2 diabetes mellitus: a placebo-controlled pilot trial. Free Radic. Biol. Med. 27(3/4):1999;309-314.
7. Henriksen E.J., Jacob S., Streeper R.S., Fogt D.L., Hokama J.Y., Tritschler H.J. Stimulation by alpha-lipoic acid of glucose transport activity in skeletal muscle of lean and obese Zucker rats. Life Sci. 61(8):1997;805-812.
8. Yaworsky K., Somwar R., Ramlal T., Tritschler H.J., Klip A., Yaworsky K. Engagement of the insulin-sensitive pathway in the stimulation of glucose transport by alpha-lipoic acid in 3T3-L1 adipocytes. Diabetologia. 43(3):2000;294-303.
9. Konrad D., Somwar R., Sweeney G., Yaworsky K., Hayashi M., Ramlal T., Klip A. The antihyperglycemic drug alpha-lipoic acid stimulates glucose uptake via both GLUT4 translocation and GLUT4 activation: potential role of p38 mitogen-activated protein kinase in GLUT4 activation. Diabetes. 50(6):2001;1464-1471.
10. Schmid E., El Benna J., Galter D., Klein G., Droge W. Redox priming of the insulin receptor beta-chain associated with altered tyrosine kinase activity and insulin responsiveness in the absence of tyrosine autophosphorylation. FASEB J. 12(10):1998;863-870.
11. Hayes G.R., Lockwood D.H. Role of insulin receptor phosphorylation in the insulinomimetic effects of hydrogen peroxide. Proc. Natl. Acad. Sci. U.S.A. 84(22):1987;8115-8119.
12. Koshio O., Akanuma Y., Kasuga M. Hydrogen peroxide stimulates tyrosine phosphorylation of the insulin receptor and its tyrosine kinase activity in intact cells. Biochem. J. 250(1):1988;95-101.
13. Schmid E., Hotz-Wagenblatt A., Hacj V., Droge W. Phosphorylation of the insulin receptor kinase by phosphocreatine in combination with hydrogen peroxide: the structural basis of redox priming. FASEB J. 13(12):1999;1491-1500.
14. ++-dependent thiol stimulation of glucose metabolism in white fat cells. J. Biol. Chem. 247(19):1972;6218-6223.
15. alphai2. J. Biol. Chem. 272(15):1997;10135-10143.
16. Mahadev K., Zilbering A., Zhu L., Goldstein B.J. Insulin-stimulated hydrogen peroxide reversibly inhibits protein-tyrosine phosphatase 1b in vivo and enhances the early insulin action cascade. J. Biol. Chem. 276(24):2001;21938-21942.
17. Mahadev K., Wu X., Zilbering A., Zhu L., Lawrence J.T., Goldstein B.J. Hydrogen peroxide generated during cellular insulin stimulation is integral to activation of the distal insulin signaling cascade in 3T3-L1 adipocytes. J. Biol. Chem. 276(52):2001;48662-48669.
18. Moini H., Tirosh O., Park Y.C., Cho K.-J., Packer L. R-α-Lipoic acid action on cell redox status, the insulin receptor, and glucose uptake in 3T3-L1 adipocytes. Arch. Biochem. Biophys. 397(2):2002;384-391.
19. Tirosh O., Sen C.K., Roy S., Packer L. Cellular and mitochondrial changes in glutamate-induced HT4 neuronal cell death. Neuroscience. 97(3):2000;531-541.
20. Garant M.J., Kole S., Maksimova E.M., Bernier M. Reversible change in thiol redox status of the insulin receptor alpha-subunit in intact cells. Biochemistry. 38(18):1999;5896-5904.
21. Chen H., Wertheimer S.J., Lin C.H., Katz S.L., Amrein K.E., Burn P., Quon M.J. Protein-tyrosine phosphatases PTP1B and syp are modulators of insulin-stimulated translocation of GLUT4 in transfected rat adipose cells. J. Biol. Chem. 272(12):1997;8026-8031.
22. Packer L. Biothiols: monothiols and dithiols, protein thiols, and thiyl radicals. In: Methods in Enzymology, vol. 251. New York: Academic Press; 1995.
23. Doussiere J., Gaillard J., Vignais P.V. The heme component of the neutrophil NADPH oxidase complex is a target for aryliodonium compounds. Biochemistry. 38(14):1999;3694-3703.
24. Stolk J., Hiltermann T.J., Dijkman J.H., Verhoeven A.J. Characteristics of the inhibition of NADPH oxidase activation in neutrophils by apocynin, a methoxy-substituted catechol. Am. J. Respir. Cell. Mol. Biol. 11(1):1994;95-102.
25. O'Donnell B.V., Tew D.G., Jones O.T., England P.J. Studies on the inhibitory mechanism of iodonium compounds with special reference to neutrophil NADPH oxidase. Biochem. J. 290(Pt 1):1993;41-49.
26. Estrada D.E., Ewart H.S., Tsakiridis T., Volchuk A., Ramlal T., Tritschler H., Klip A. Stimulation of glucose uptake by the natural coenzyme alpha-lipoic acid/thioctic acid: participation of elements of the insulin signaling pathway. Diabetes. 45(12):1996;1798-1804.
27. Karlsson F.A., Grunfeld C., Kahn C.R., Roth J. Regulation of insulin receptors and insulin responsiveness in 3T3-L1 fatty fibroblasts. Endocrinology. 104(5):1979;1383-1392.
28. Rubin C.S., Rubin C.S., Hirsch A., Fung C., Rosen O.M. Development of hormone receptors and hormonal responsiveness in vitro. Insulin receptors and insulin sensitivity in the preadipocyte and adipocyte forms of 3T3-L1 cells. J. Biol. Chem. 253(20):1978;7570-7578.
29. Shimizu M., Torti F., Roth R.A. Characterization of the insulin and insulin-like growth factor receptors and responsitivity of a fibroblast/adipocyte cell line before and after differentiation. Biochem. Biophys. Res. Commun. 137(1):1986;552-558.
30. Marin-Hincapie M., Garofalo R.S. Drosophila insulin receptor: lectin-binding properties and a role for oxidation-reduction of receptor thiols in activation. Endocrinology. 136(6):1995;2357-2366.
31. Dicter N., Madar Z., Tirosh O. Alpha-lipoic acid inhibits glycogen synthesis in rat soleus muscle via its oxidative activity and the uncoupling of mitochondria. J. Nutr. 132(10):2002;3001-3006.
32. Sen C.K., Roy S., Han D., Packer L. Regulation of cellular thiols in human lymphocytes by alpha-lipoic acid: a flow cytometric analysis. Free Radic. Biol. Med. 22(7):1997;1241-1257.
33. Czech M.P., Lawrence J.C. Jr., Lynn W.S. Evidence for the involvement of sulfhydryl oxidation in the regulation of fat cell hexose transport by insulin. Proc. Natl. Acad. Sci. U.S.A. 71(10):1974;4173-4177.
34. Wilden P.A., Pessin J.E. Differential sensitivity of the insulin-receptor kinase to thiol and oxidizing agents in the absence and presence of insulin. Biochem. J. 245(2):1987;325-331.
35. Clark S., Konstantopoulos N. Sulphydryl agents modulate insulin- and epidermal growth factor (EGF)-receptor kinase via reaction with intracellular receptor domains: differential effects on basal vs. activated receptors. Biochem. J. 292(Pt 1):1993;217-223.
36. Chen J.J., Kosower N.S., Petryshyn R., London I.M. The effects of N-ethylmaleimide on the phosphorylation and aggregation of insulin receptors in the isolated plasma membranes of 3T3-F442A adipocytes. J. Biol. Chem. 261(2):1986;902-908.
37. Jhun B.H., Hah J.S., Jung C.Y. Phenylarsine oxide causes an insulin-dependent, GLUT4-specific degradation in rat adipocytes. J. Biol. Chem. 266(33):1991;22260-22265.
38. Yang J., Clark A.E., Harrison R., Kozka I.J., Holman G.D. Trafficking of glucose transporters in 3T3-L1 cells. Inhibition of trafficking by phenylarsine oxide implicates a slow dissociation of transporters from trafficking proteins. Biochem. J. 281(Pt 3):1992;809-817.
39. Han Y.P., Kohanski R.A. Phenylarsine oxide inhibits insulin activation of phosphatidylinositol 3′-kinase. Biochem. Biophys. Res. Commun. 239(1):1997;316-321.
40. Levenson R.M., Blackshear P.J. Insulin-stimulated protein tyrosine phosphorylation in intact cells evaluated by giant two-dimensional gel electrophoresis. J. Biol. Chem. 264(33):1989;19984-19993.
41. Garcia-Morales P., Minami Y., Luong E., Klausner R.D., Samelson L.E. Tyrosine phosphorylation in T cells is regulated by phosphatase activity: studies with phenylarsine oxide. Proc. Natl. Acad. Sci. U.S.A. 87(23):1990;9255-9259.
42. 2-generating system that is activated by insulin via a mechanism bypassing the receptor kinase. J. Clin. Invest. 89(3):1992;1006-1013.
43. Kirsch M., De Groot H. NAD(P)H, a directly operating antioxidant? FASEB. J. 15(9):2001;1569-1574.
44. Doussiere J., Poinas A., Blais C., Vignais P.V. Phenylarsine oxide as an inhibitor of the activation of the neutrophil NADPH oxidase - identification of the beta subunit of the flavocytochrome b component of the NADPH oxidase as a target site for phenylarsine oxide by photoaffinity labeling and photoinactivation. Eur. J. Biochem. 251(3):1998;649-658.
45. Clark R.A., Volpp B.D., Leidal K.G., Nauseef W.M. Two cytosolic components of the human neutrophil respiratory burst oxidase translocate to the plasma membrane during cell activation. J. Clin. Invest. 85(3):1990;714-721.
46. Denu J.M., Dixon J.E. Protein tyrosine phosphatases: mechanisms of catalysis and regulation. Curr. Opin. Chem. Biol. 2(5):1998;633-641.
47. Herrlich P., Bohmer F.D. Redox regulation of signal transduction in mammalian cells. Biochem. Pharmacol. 59(1):2000;35-41.
48. Elchebly M., Payette P., Michaliszyn E. Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B gene. Science. 283:1999;1544-1548.