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PMID: 7537758 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Insulin receptor phosphorylation, insulin receptor substrate-1 phosphorylation, and phosphatidylinositol 3-kinase activity are decreased in intact skeletal muscle strips from obese subjects.

The Journal of clinical investigation ·Vol. 95 ·No. 5 ·1995-05-00 ·Pages 2195-204

Goodyear LJ, Giorgino F, Sherman LA, Carey J, Smith RJ, Dohm GL

Abstract

To determine whether the impaired insulin-stimulated glucose uptake in obese individuals is associated with altered insulin receptor signaling, we measured both glucose uptake and early steps in the insulin action pathway in intact strips of human skeletal muscle. Biopsies of rectus abdominus muscle were taken from eight obese and eight control subjects undergoing elective surgery (body mass index 52.9 +/- 3.6 vs 25.7 +/- 0.9). Insulin-stimulated 2-deoxyglucose uptake was 53% lower in muscle strips from obese subjects. Additional muscle strips were incubated in the basal state or with 10(-7) M insulin for 2, 15, or 30 min. In the lean subjects, tyrosine phosphorylation of the insulin receptor and insulin receptor substrate-1 (IRS-1), measured by immunoblotting with anti-phosphotyrosine antibodies, was significantly increased by insulin at all time points. In the skeletal muscle from the obese subjects, insulin was less effective in stimulating tyrosine phosphorylation (maximum receptor and IRS-1 phosphorylation decreased by 35 and 38%, respectively). Insulin stimulation of IRS-1 immunoprecipitable phosphatidylinositol 3-kinase (PI 3-kinase) activity also was markedly lower in obese subjects compared with controls (10- vs 35-fold above basal, respectively). In addition, the obese subjects had a lower abundance of the insulin receptor, IRS-1, and the p85 subunit of PI 3-kinase (55, 54, and 64% of nonobese, respectively). We conclude that impaired insulin-stimulated glucose uptake in skeletal muscle from severely obese subjects is accompanied by a deficiency in insulin receptor signaling, which may contribute to decreased insulin action.

MeSH Terms
Adult Biological Transport/drug effects Biopsy Glucose/metabolism Humans In Vitro Techniques Insulin/pharmacology Insulin Receptor Substrate Proteins Muscle, Skeletal/drug effects,metabolism,pathology Obesity/metabolism,pathology Phosphatidylinositol 3-Kinases Phosphoproteins/metabolism Phosphorylation Phosphotransferases (Alcohol Group Acceptor)/metabolism Phosphotyrosine Receptor, Insulin/metabolism Reference Values Tyrosine/analogs & derivatives
Chemicals
IRS1 protein, human Insulin Insulin Receptor Substrate Proteins Phosphoproteins Phosphotyrosine Tyrosine Phosphatidylinositol 3-Kinases Phosphotransferases (Alcohol Group Acceptor) Receptor, Insulin Glucose
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Goodyear L J
Research Division, Joslin Diabetes Center, Boston, MA 02215, USA.
Giorgino F
Sherman L A
Carey J
Smith R J
Dohm G L
References (56)
56 references, click to expand
  1. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  2. Skeletal muscle protein tyrosine phosphatase activity and tyrosine phosphatase 1B protein content are associated with insulin action and resistance.
    J Clin Invest. 1994 Mar;93(3):1156-62 PMID: 8132755
  3. Insulin stimulates the phosphorylation of the 95,000-dalton subunit of its own receptor.
    Science. 1982 Jan 8;215(4529):185-7 PMID: 7031900
  4. Insulin secretion, insulin resistance, and obesity.
    Int J Obes. 1982;6 Suppl 1:73-82 PMID: 6749725
  5. Insulin activates a tyrosine-specific protein kinase in extracts of 3T3-L1 adipocytes and human placenta.
    Proc Natl Acad Sci U S A. 1982 Nov;79(22):6792-6 PMID: 6294652
  6. Tyrosine phosphorylation of the insulin receptor beta subunit activates the receptor-associated tyrosine kinase activity.
    J Biol Chem. 1984 Apr 25;259(8):5277-86 PMID: 6538876
  7. The disposal of an oral glucose load in healthy subjects. A quantitative study.
    Diabetes. 1985 Jun;34(6):580-8 PMID: 3891471
  8. Diabetes-induced functional and structural changes in insulin receptors from rat skeletal muscle.
    J Clin Invest. 1986 Jan;77(1):260-70 PMID: 3003151
  9. Replacement of insulin receptor tyrosine residues 1162 and 1163 compromises insulin-stimulated kinase activity and uptake of 2-deoxyglucose.
    Cell. 1986 Jun 6;45(5):721-32 PMID: 3518947
  10. Studies on the mechanism of insulin resistance in the liver from humans with noninsulin-dependent diabetes. Insulin action and binding in isolated hepatocytes, insulin receptor structure, and kinase activity.
    J Clin Invest. 1986 Jul;78(1):249-58 PMID: 3522628
  11. Intrinsic differences of insulin receptor kinase activity in red and white muscle.
    J Biol Chem. 1986 Nov 15;261(32):14939-44 PMID: 3021758
  12. Decreased kinase activity of insulin receptors from adipocytes of non-insulin-dependent diabetic subjects.
    J Clin Invest. 1987 Jan;79(1):240-50 PMID: 3540010
  13. Human insulin receptors mutated at the ATP-binding site lack protein tyrosine kinase activity and fail to mediate postreceptor effects of insulin.
    J Biol Chem. 1987 Feb 5;262(4):1842-7 PMID: 3100537
  14. Replacement of lysine residue 1030 in the putative ATP-binding region of the insulin receptor abolishes insulin- and antibody-stimulated glucose uptake and receptor kinase activity.
    Proc Natl Acad Sci U S A. 1987 Feb;84(3):704-8 PMID: 3101064
  15. Insulin-receptor kinase activity of adipose tissue from morbidly obese humans with and without NIDDM.
    Diabetes. 1987 May;36(5):620-5 PMID: 3032715
  16. Insulin receptor kinase in human skeletal muscle from obese subjects with and without noninsulin dependent diabetes.
    J Clin Invest. 1987 May;79(5):1330-7 PMID: 3033021
  17. Phosphatidylinositol 3-kinase activation is required for insulin stimulation of pp70 S6 kinase, DNA synthesis, and glucose transporter translocation.
    Mol Cell Biol. 1994 Jul;14(7):4902-11 PMID: 8007986
  18. Inhibition of the translocation of GLUT1 and GLUT4 in 3T3-L1 cells by the phosphatidylinositol 3-kinase inhibitor, wortmannin.
    Biochem J. 1994 Jun 15;300 ( Pt 3):631-5 PMID: 8010944
  19. Alternative pathway of insulin signalling in mice with targeted disruption of the IRS-1 gene.
    Nature. 1994 Nov 10;372(6502):186-90 PMID: 7526222
  20. Phorbol ester-induced serine phosphorylation of the insulin receptor decreases its tyrosine kinase activity.
    J Biol Chem. 1988 Mar 5;263(7):3440-7 PMID: 3125181
  21. Type I phosphatidylinositol kinase makes a novel inositol phospholipid, phosphatidylinositol-3-phosphate.
    Nature. 1988 Apr 14;332(6165):644-6 PMID: 2833705
  22. Lilly lecture 1987. The triumvirate: beta-cell, muscle, liver. A collusion responsible for NIDDM.
    Diabetes. 1988 Jun;37(6):667-87 PMID: 3289989
  23. An in vitro human muscle preparation suitable for metabolic studies. Decreased insulin stimulation of glucose transport in muscle from morbidly obese and diabetic subjects.
    J Clin Invest. 1988 Aug;82(2):486-94 PMID: 3403714
  24. Effects of hypercortisolemia and diabetes on skeletal muscle insulin receptor function in vitro and in vivo.
    Am J Physiol. 1989 Jan;256(1 Pt 1):E39-48 PMID: 2643342
  25. PDGF-dependent tyrosine phosphorylation stimulates production of novel polyphosphoinositides in intact cells.
    Cell. 1989 Apr 7;57(1):167-75 PMID: 2467744
  26. A defective intramolecular autoactivation cascade may cause the reduced kinase activity of the skeletal muscle insulin receptor from patients with non-insulin-dependent diabetes mellitus.
    J Biol Chem. 1989 Jun 5;264(16):9497-504 PMID: 2722845
  27. The dynamics of the glucose transporter.
    Trends Biochem Sci. 1988 Jun;13(6):226-31 PMID: 3076284
  28. Phosphatidylinositol kinase or an associated protein is a substrate for the insulin receptor tyrosine kinase.
    J Biol Chem. 1990 Jan 5;265(1):396-400 PMID: 1688432
  29. Activation of phosphatidylinositol 3-kinase by insulin.
    Proc Natl Acad Sci U S A. 1990 Feb;87(4):1411-5 PMID: 2154747
  30. Evidence against altered expression of GLUT1 or GLUT4 in skeletal muscle of patients with obesity or NIDDM.
    Diabetes. 1990 Jul;39(7):865-70 PMID: 2354749
  31. Exercise training increases glucose transporter protein GLUT-4 in skeletal muscle of obese Zucker (fa/fa) rats.
    FEBS Lett. 1990 Jul 30;268(1):13-6 PMID: 2200706
  32. Expression of insulin regulatable glucose transporters in skeletal muscle from type 2 (non-insulin-dependent) diabetic patients.
    Diabetologia. 1990 Oct;33(10):625-7 PMID: 2258000
  33. Decreased expression of glucose transporter in muscle from insulin-resistant patients.
    Am J Physiol. 1991 Mar;260(3 Pt 1):E459-63 PMID: 2003599
  34. Abnormal regulation of protein tyrosine phosphatase activities in skeletal muscle of insulin-resistant humans.
    Diabetes. 1991 Jul;40(7):939-42 PMID: 1647997
  35. Structure of the insulin receptor substrate IRS-1 defines a unique signal transduction protein.
    Nature. 1991 Jul 4;352(6330):73-7 PMID: 1648180
  36. Insulin stimulation of phosphatidylinositol 3-kinase activity maps to insulin receptor regions required for endogenous substrate phosphorylation.
    J Biol Chem. 1992 Jan 15;267(2):1367-74 PMID: 1309768
  37. Surgical treatment of obesity and its effect on diabetes: 10-y follow-up.
    Am J Clin Nutr. 1992 Feb;55(2 Suppl):582S-585S PMID: 1733132
  38. Phosphatidylinositol-3-kinase in isolated rat adipocytes. Activation by insulin and subcellular distribution.
    J Biol Chem. 1992 Feb 15;267(5):3423-8 PMID: 1310686
  39. Changes in tyrosine phosphorylation of insulin receptors and a 170,000 molecular weight nonreceptor protein in vivo in skeletal muscle of streptozotocin-induced diabetic rats: effects of insulin and glucose.
    Endocrinology. 1992 Mar;130(3):1433-44 PMID: 1531627
  40. YMXM motifs of IRS-1 define substrate specificity of the insulin receptor kinase.
    Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2027-31 PMID: 1312712
  41. Gene expression of GLUT4 in skeletal muscle from insulin-resistant patients with obesity, IGT, GDM, and NIDDM.
    Diabetes. 1992 Apr;41(4):465-75 PMID: 1535055
  42. Insulin resistance in obese Zucker rat (fa/fa) skeletal muscle is associated with a failure of glucose transporter translocation.
    J Clin Invest. 1992 Oct;90(4):1568-75 PMID: 1401086
  43. Components of signaling pathways for insulin and insulin-like growth factor-I in muscle myoblasts and myotubes.
    Endocrinology. 1992 Nov;131(5):2196-202 PMID: 1385098
  44. Insulin stimulation of phosphatidylinositol 3-kinase activity and association with insulin receptor substrate 1 in liver and muscle of the intact rat.
    J Biol Chem. 1992 Nov 5;267(31):22171-7 PMID: 1385396
  45. Regulation of insulin receptor substrate-1 in liver and muscle of animal models of insulin resistance.
    J Clin Invest. 1992 Nov;90(5):1839-49 PMID: 1331176
  46. Phosphatidylinositol 3-kinase: a novel effector.
    Cell Growth Differ. 1992 Oct;3(10):747-52 PMID: 1332743
  47. A tightly associated serine/threonine protein kinase regulates phosphoinositide 3-kinase activity.
    Mol Cell Biol. 1993 Mar;13(3):1657-65 PMID: 8382773
  48. The insulin and insulin-like growth factor-I receptor substrate IRS-1 associates with and activates phosphatidylinositol 3-kinase in vitro.
    J Biol Chem. 1993 Apr 5;268(10):7358-64 PMID: 8385105
  49. Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting.
    Science. 1993 Apr 2;260(5104):88-91 PMID: 8385367
  50. Defect in skeletal muscle phosphatidylinositol-3-kinase in obese insulin-resistant mice.
    J Clin Invest. 1993 Apr;91(4):1358-66 PMID: 8386184
  51. Glucocorticoid regulation of insulin receptor and substrate IRS-1 tyrosine phosphorylation in rat skeletal muscle in vivo.
    J Clin Invest. 1993 May;91(5):2020-30 PMID: 7683695
  52. Insulin-stimulated GLUT4 translocation is relevant to the phosphorylation of IRS-1 and the activity of PI3-kinase.
    Biochem Biophys Res Commun. 1993 Sep 15;195(2):762-8 PMID: 8396927
  53. Regulation of phosphatidylinositol 3-kinase by insulin in rat skeletal muscle.
    Am J Physiol. 1993 Nov;265(5 Pt 1):E736-42 PMID: 8238500
  54. The insulin signaling system.
    J Biol Chem. 1994 Jan 7;269(1):1-4 PMID: 8276779
  55. PI 3-kinase is a dual specificity enzyme: autoregulation by an intrinsic protein-serine kinase activity.
    EMBO J. 1994 Feb 1;13(3):522-33 PMID: 8313897
  56. Insulin binding and glucose uptake differences in rodent skeletal muscles.
    Diabetes. 1981 Aug;30(8):702-4 PMID: 7018974
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
1995-05-00
Pages
2195-204
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC295829
Subset
IM
Grants
NIDDK NIH HHS · DK36836 · United States
NIDDK NIH HHS · DK46121 · United States
NIGMS NIH HHS · GM36428 · United States
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