Home LiteratureArticle Details
PMID: 7000825 Published · ppublish English Journal Article

Antibody-induced desensitization of the insulin receptor. Studies of the mechanism of desensitization in 3T3-L1 fatty fibroblasts.

The Journal of clinical investigation ·Vol. 66 ·No. 5 ·1980-11-00 ·Pages 1124-34

Grunfeld C, Van Obberghen E, Karlsson FA, Kahn CR

Abstract

Antibodies against the insulin receptor (Anti-R), which are found in the serum of type B patients with the syndrome of insulin resistance and acanthosis nigricans, inhibit the binding of insulin to its receptor and mimic the actions of insulin when studied acutely in vitro. After prolonged exposure of 3T3-L1 cells to Anti-R, the insulinomimetic activity is lost, and the cells show a marked decrease in their maximal response to insulin (antibody-induced desensitization), thus providing a model for the insulin resistance seen in vivo. This study explores in detail the mechanism and specificity of desensitization in 3T3-L1 cells.Desensitization, like the insulinomimetic activity of Anti-R, requires bivalence. Monovalent preparations of Anti-R inhibit insulin binding and shift the insulin biological dose-response curve to the right, but do not decrease the maximal insulin response. The affinity of monovalent Anti-R is less than that of the native antibody. Cross-linking of monovalent Anti-R reconstitutes its insulinomimetic activity and partially reconstitutes desensitization. Desensitized cells are resistant to the insulinomimetic actions of concanavalin A, which interacts with the insulin receptor, but are not desensitized to spermine and vitamin K(5), insulinomimetic agents that are thought to act independently of the insulin receptor. Glucose, pyruvate, or certain hexoses are required in the incubation media for desensitization to occur. Although Anti-R is taken up into cells and degraded by lysosomes, chloroquine, cycloheximide, colchicine, and cytochalasin E have little influence on the induction of or recovery from antibody-induced desensitization. These data suggest that desensitization is not merely due to the inhibition of insulin binding, but is a complex process involving a decreased ability of the receptor to generate a biological response.

MeSH Terms
Animals Antibodies Cell Line Fibroblasts/immunology Glucose/metabolism Immunoglobulin Fab Fragments Insulin/metabolism Insulin Antagonists Insulin Resistance Receptor, Insulin/immunology Substrate Specificity
Chemicals
Antibodies Immunoglobulin Fab Fragments Insulin Insulin Antagonists Receptor, Insulin Glucose
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Grunfeld C
Van Obberghen E
Karlsson F A
Kahn C R
References (38)
38 references, click to expand
  1. An improved fluorometric assay for DNA.
    Anal Biochem. 1971 Jan;39(1):197-201 PMID: 5544593
  2. Inhibitors of ribosome functions.
    Annu Rev Microbiol. 1971;25:487-562 PMID: 4949424
  3. Insulin-like activity of concanavalin A and wheat germ agglutinin--direct interactions with insulin receptors.
    Proc Natl Acad Sci U S A. 1973 Feb;70(2):485-9 PMID: 4510292
  4. Microtubules.
    Annu Rev Biochem. 1973;42:507-40 PMID: 4581232
  5. Insulin-dependent regulation of insulin receptor concentrations: a direct demonstration in cell culture.
    Proc Natl Acad Sci U S A. 1974 Jan;71(1):84-8 PMID: 4359334
  6. Commentary. Lysosomotropic agents.
    Biochem Pharmacol. 1974 Sep 15;23(18):2495-531 PMID: 4606365
  7. Hexose transport in isolated brown fat cells. A model system for investigating insulin action on membrane transport.
    J Biol Chem. 1974 Sep 10;249(17):5421-7 PMID: 4413673
  8. An established pre-adipose cell line and its differentiation in culture.
    Cell. 1974 Oct;3(2):127-33 PMID: 4426090
  9. Induction of sugar transport in chick embryo fibroblasts by hexose starvation. Evidence for transcriptional regulation of transport.
    J Biol Chem. 1975 Jan 25;250(2):593-600 PMID: 1167542
  10. Antibodies that impair insulin receptor binding in an unusual diabetic syndrome with severe insulin resistance.
    Science. 1975 Oct 3;190(4209):63-5 PMID: 170678
  11. The syndromes of insulin resistance and acanthosis nigricans. Insulin-receptor disorders in man.
    N Engl J Med. 1976 Apr 1;294(14):739-45 PMID: 176581
  12. Induction of lipogenesis during differentiation in a "preadipocyte" cell line.
    J Biol Chem. 1976 Oct 25;251(20):6462-4 PMID: 10298
  13. Characterization of antibodies to the insulin receptor: a cause of insulin-resistant diabetes in man.
    J Clin Invest. 1976 Dec;58(6):1442-9 PMID: 993353
  14. Direct method for detection and characterization of cell surface receptors for insulin by means of 125I-labeled autoantibodies against the insulin receptor.
    Proc Natl Acad Sci U S A. 1976 Nov;73(11):4115-9 PMID: 1069300
  15. Insulin-like effects of polyamines in fat cells. Mediation by H2O2 formation.
    J Biol Chem. 1977 Jan 25;252(2):560-2 PMID: 833144
  16. Insulin stimulation of glucose transport in adipose cells. An energy-dependent process.
    Biochemistry. 1977 Mar 22;16(6):1151-8 PMID: 849412
  17. Effects of autoantibodies to the insulin receptor on isolated adipocytes. Studies of insulin binding and insulin action.
    J Clin Invest. 1977 Nov;60(5):1094-106 PMID: 908753
  18. Alterations in insulin binding accompanying differentiation of 3T3-L1 preadipocytes.
    Proc Natl Acad Sci U S A. 1977 Nov;74(11):4876-80 PMID: 303773
  19. Myasthenia gravis (first of two parts).
    N Engl J Med. 1978 Jan 19;298(3):136-42 PMID: 201840
  20. Activation of glycogen synthase in rat adipocytes by insulin and glucose involves increased glucose transport and phosphorylation.
    J Biol Chem. 1978 Apr 10;253(7):2104-13 PMID: 204641
  21. Anti-insulin receptor antibodies inhibit insulin binding and stimulate glucose metabolism in skeletal muscle.
    Diabetologia. 1978 May;14(5):311-7 PMID: 648762
  22. Differentiation of 3T3-L1 fibroblasts to adipocytes. Effect of insulin and indomethacin on the levels of insulin receptors.
    J Biol Chem. 1978 Jul 10;253(13):4693-6 PMID: 659443
  23. Direct visualization of binding, aggregation, and internalization of insulin and epidermal growth factor on living fibroblastic cells.
    Proc Natl Acad Sci U S A. 1978 Jun;75(6):2659-63 PMID: 307249
  24. Effects of anti-insulin receptor autoantibodies on the metabolism of human adipocytes.
    Diabetes. 1978 Sep;27(9):938-45 PMID: 689305
  25. Evidence that glucose 6-phosphate regulates protein synthesis initiation in reticulocyte lysates.
    J Biol Chem. 1978 Oct 25;253(20):7163-72 PMID: 701241
  26. 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. 1978 Oct 25;253(20):7570-8 PMID: 81205
  27. Development of hormone receptors and hormone responsiveness in vitro. Effect of prolonged insulin treatment on hexose uptake in 3T3-L1 adipocytes.
    J Biol Chem. 1978 Oct 25;253(20):7579-83 PMID: 701271
  28. Direct demonstration that receptor crosslinking or aggregation is important in insulin action.
    Proc Natl Acad Sci U S A. 1978 Sep;75(9):4209-13 PMID: 279910
  29. Immunoprecipitation of the insulin receptor: a sensitive assay for receptor antibodies and a specific technique for receptor purification.
    J Clin Endocrinol Metab. 1979 Jan;48(1):59-65 PMID: 422707
  30. Autoantibodies to the insulin receptor activate glycogen synthase in rat adipocytes.
    Mol Cell Biochem. 1978 Dec 22;22(2-3):153-7 PMID: 106236
  31. Desensitization of the insulin receptor at an early postreceptor step by prolonged exposure to antireceptor antibody.
    Proc Natl Acad Sci U S A. 1979 Feb;76(2):809-13 PMID: 284401
  32. Regulation of insulin receptors and insulin responsiveness in 3T3-L1 fatty fibroblasts.
    Endocrinology. 1979 May;104(5):1383-92 PMID: 436783
  33. The underlying insulin receptor in patients with antireceptor autoantibodies: demonstration of normal binding and immunological properties.
    J Clin Endocrinol Metab. 1979 Jul;49(1):110-9 PMID: 447809
  34. Insulin-receptor antibodies mimic a late insulin effect.
    Nature. 1979 Aug 9;280(5722):500-2 PMID: 460430
  35. Insulin regulation of lipoprotein lipase activity and release in 3T3-L1 adipocytes. Separation and dependence of hormonal effects on hexose metabolism and synthesis of RNA and protein.
    J Biol Chem. 1979 Oct 25;254(20):10021-9 PMID: 489580
  36. Direct demonstration of separate receptors for growth and metabolic activities of insulin and multiplication-stimulating activity (an insulinlike growth factor) using antibodies to the insulin receptor.
    J Clin Invest. 1980 Jul;66(1):130-40 PMID: 6995478
  37. Effects of antiinsulin receptor autoantibody on the metabolism of rat adipocytes.
    J Clin Endocrinol Metab. 1978 Jul;47(1):66-77 PMID: 400715
  38. Structural units of human 7S gamma globulin.
    J Clin Invest. 1960 Dec;39:1933-41 PMID: 13701434
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
1980-11-00
Pages
1124-34
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC371551
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com