Home LiteratureArticle Details
PMID: 8645171 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Roles of insulin, guanosine 5'-[gamma-thio]triphosphate and phorbol 12-myristate 13-acetate in signalling pathways of GLUT4 translocation.

The Biochemical journal ·Vol. 315 ( Pt 3) ·1996-05-01 ·Pages 875-82

Todaka M, Hayashi H, Imanaka T, Mitani Y, Kamohara S, Kishi K, Tamaoka K, Kanai F, Shichiri M, Morii N, Narumiya S, Ebina Y

Abstract

Insulin, guanosine 5'-[gamma-thio]triphosphate (GTP[S] and phorbol 12-myristate 13-acetate (PMA) trigger the translocation of Gl UT4 (type 4 glucose transporter; insulin-sensitive glucose transporter) from an intracellular pool to the cell surface. We have developed a highly sensitive and quantitative method to detect GLUT4 immunologically on the surface of intact 3T3-L1 adipocytes and Chinese hamster ovary (CHO) cells, using c-myc epitope-tagged GLUT4 (GLUT4myc). We examined the roles of insulin, GTP[S] and PMA in the signalling pathways of GLUT4 translocation in the CHO cell system. Among small molecular GTP-binding proteins, ras, rab3D, rad and rho seem to be candidates as signal transmitters of insulin-stimulated GLUT4 translocation. Overexpression of wild-type H-ras and the dominant negative mutant H-rass17N in our cell system respectively enhanced and blocked insulin-stimulated activation of mitogen-activated protein kinase, but did not affect insulin-stimulated GLUT4 translocation. Overexpression of rab3D or rad in the cells did not affect GLUT4 translocation triggered by insulin, GTP[S] or PMA. Treatment with Botulinum C3 exoenzyme, a specific inhibitor of rho, had no effect on GLUT4 translocation induced by insulin, GTP[S] or PMA. Therefore these small molecular GTP-binding proteins are not likely to be involved in GLUT4 translocation. In addition, insulin, GTP[S] and PMA apparently stimulate GLUT4 translocation through independent pathways.

MeSH Terms
3T3 Cells Animals Biological Transport, Active/drug effects CHO Cells Cricetinae GTP-Binding Proteins/genetics,metabolism Glucose Transporter Type 4 Guanosine 5'-O-(3-Thiotriphosphate)/pharmacology Insulin/pharmacology Mice Models, Biological Monosaccharide Transport Proteins/metabolism Muscle Proteins Phosphatidylinositol 3-Kinases Phosphotransferases (Alcohol Group Acceptor)/metabolism Protein Kinase C/metabolism Signal Transduction/drug effects Tetradecanoylphorbol Acetate/pharmacology
Chemicals
Glucose Transporter Type 4 Insulin Monosaccharide Transport Proteins Muscle Proteins Slc2a4 protein, mouse Guanosine 5'-O-(3-Thiotriphosphate) Phosphatidylinositol 3-Kinases Phosphotransferases (Alcohol Group Acceptor) Protein Kinase C GTP-Binding Proteins Tetradecanoylphorbol Acetate
Authors & Affiliations
12 authors, click to expand affiliations / ORCID
Todaka M
Department of Enzyme Genetics, University of Tokushima, Kuramoto-cho, Japan.
Hayashi H
Imanaka T
Mitani Y
Kamohara S
Kishi K
Tamaoka K
Kanai F
Shichiri M
Morii N
Narumiya S
Ebina Y
References (60)
60 references, click to expand
  1. Platelet-derived growth factor triggers translocation of the insulin-regulatable glucose transporter (type 4) predominantly through phosphatidylinositol 3-kinase binding sites on the receptor.
    Proc Natl Acad Sci U S A. 1995 Feb 14;92(4):1077-81 PMID: 7862637
  2. Activation of mitogen-activated protein kinase and phosphatidylinositol 3'-kinase is not sufficient for the hormonal stimulation of glucose uptake, lipogenesis, or glycogen synthesis in 3T3-L1 adipocytes.
    J Biol Chem. 1995 Feb 17;270(7):3442-6 PMID: 7852430
  3. A human phosphatidylinositol 3-kinase complex related to the yeast Vps34p-Vps15p protein sorting system.
    EMBO J. 1995 Jul 17;14(14):3339-48 PMID: 7628435
  4. Possible domains responsible for intracellular targeting and insulin-dependent translocation of glucose transporter type 4.
    Biochem J. 1995 Aug 1;309 ( Pt 3):813-23 PMID: 7543750
  5. Roles of 1-phosphatidylinositol 3-kinase and ras in regulating translocation of GLUT4 in transfected rat adipose cells.
    Mol Cell Biol. 1995 Oct;15(10):5403-11 PMID: 7565691
  6. Potential mechanism of insulin action on glucose transport in the isolated rat adipose cell. Apparent translocation of intracellular transport systems to the plasma membrane.
    J Biol Chem. 1980 May 25;255(10):4758-62 PMID: 6989818
  7. Evidence that insulin causes translocation of glucose transport activity to the plasma membrane from an intracellular storage site.
    Proc Natl Acad Sci U S A. 1980 May;77(5):2542-5 PMID: 6771756
  8. Role of a guanine nucleotide-binding regulatory protein in the hydrolysis of hepatocyte phosphatidylinositol 4,5-bisphosphate by calcium-mobilizing hormones and the control of cell calcium. Studies utilizing aluminum fluoride.
    J Biol Chem. 1985 Nov 25;260(27):14477-83 PMID: 2997209
  9. Hormonal regulation of mammalian glucose transport.
    Annu Rev Biochem. 1986;55:1059-89 PMID: 3527041
  10. Phorbol esters imitate in rat fat-cells the full effect of insulin on glucose-carrier translocation, but not on 3-O-methylglucose-transport activity.
    Biochem J. 1988 Feb 1;249(3):865-70 PMID: 3281656
  11. The molecular heterogeneity of protein kinase C and its implications for cellular regulation.
    Nature. 1988 Aug 25;334(6184):661-5 PMID: 3045562
  12. Regulation of glucose carrier activity by AlCl3 and phospholipase C in fat-cells.
    Biochem J. 1988 Dec 1;256(2):515-20 PMID: 3066348
  13. Characterizations of two distinct Ca2+-dependent phospholipid-binding proteins of 68-kDa isolated from human placenta.
    J Biol Chem. 1989 Oct 15;264(29):17222-30 PMID: 2529258
  14. Molecular cloning and characterization of a novel type of regulatory protein (GDI) for smg p25A, a ras p21-like GTP-binding protein.
    Mol Cell Biol. 1990 Aug;10(8):4116-22 PMID: 2115118
  15. Insulin regulation of the two glucose transporters in 3T3-L1 adipocytes.
    J Biol Chem. 1990 Aug 15;265(23):13801-8 PMID: 2199443
  16. Exofacial photolabelling of the human erythrocyte glucose transporter with an azitrifluoroethylbenzoyl-substituted bismannose.
    Biochem J. 1990 Aug 1;269(3):615-22 PMID: 2390055
  17. Microinjection of recombinant p21rho induces rapid changes in cell morphology.
    J Cell Biol. 1990 Sep;111(3):1001-7 PMID: 2118140
  18. Effect of a dominant inhibitory Ha-ras mutation on neuronal differentiation of PC12 cells.
    Mol Cell Biol. 1990 Oct;10(10):5324-32 PMID: 2118994
  19. Insulin and nonhydrolyzable GTP analogs induce translocation of GLUT 4 to the plasma membrane in alpha-toxin-permeabilized rat adipose cells.
    J Biol Chem. 1991 Mar 5;266(7):4037-40 PMID: 1999400
  20. Differential sorting of two glucose transporters expressed in insulin-sensitive cells.
    Am J Physiol. 1991 Mar;260(3 Pt 1):C570-80 PMID: 2003579
  21. The translocation of the glucose transporter sub-types GLUT1 and GLUT4 in isolated fat cells is differently regulated by phorbol esters.
    Biochem J. 1991 May 1;275 ( Pt 3):597-600 PMID: 2039438
  22. Immunoelectron microscopic demonstration of insulin-stimulated translocation of glucose transporters to the plasma membrane of isolated rat adipocytes and masking of the carboxyl-terminal epitope of intracellular GLUT4.
    Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6893-7 PMID: 1713695
  23. Clostridium botulinum C3 ADP-ribosyltransferase gene. Cloning, sequencing, and expression of a functional protein in Escherichia coli.
    J Biol Chem. 1991 Oct 15;266(29):19312-9 PMID: 1918048
  24. Cloning of a Rab3 isotype predominantly expressed in adipocytes.
    Proc Natl Acad Sci U S A. 1992 Jun 1;89(11):5049-52 PMID: 1594612
  25. Insulin treatment stimulates the tyrosine phosphorylation of the alpha-type 85-kDa subunit of phosphatidylinositol 3-kinase in vivo.
    J Biol Chem. 1992 Nov 5;267(31):22575-80 PMID: 1385401
  26. IRS-1 activates phosphatidylinositol 3'-kinase by associating with src homology 2 domains of p85.
    Proc Natl Acad Sci U S A. 1992 Nov 1;89(21):10350-4 PMID: 1332046
  27. Activation of the zeta isozyme of protein kinase C by phosphatidylinositol 3,4,5-trisphosphate.
    J Biol Chem. 1993 Jan 5;268(1):13-6 PMID: 8380153
  28. The alpha-type 85-kDa subunit of phosphatidylinositol 3-kinase is phosphorylated at tyrosines 368, 580, and 607 by the insulin receptor.
    J Biol Chem. 1993 Apr 5;268(10):7107-17 PMID: 8385099
  29. Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting.
    Science. 1993 Apr 2;260(5104):88-91 PMID: 8385367
  30. The SH2/SH3 domain-containing protein GRB2 interacts with tyrosine-phosphorylated IRS1 and Shc: implications for insulin control of ras signalling.
    EMBO J. 1993 May;12(5):1929-36 PMID: 8491186
  31. ADP-ribosylation of the rhoA gene product by botulinum C3 exoenzyme causes Swiss 3T3 cells to accumulate in the G1 phase of the cell cycle.
    Oncogene. 1993 Jun;8(6):1449-55 PMID: 8502473
  32. The insulin receptor substrate 1 associates with the SH2-containing phosphotyrosine phosphatase Syp.
    J Biol Chem. 1993 Jun 5;268(16):11479-81 PMID: 8505282
  33. The ras signaling pathway mimics insulin action on glucose transporter translocation.
    Proc Natl Acad Sci U S A. 1993 May 15;90(10):4460-4 PMID: 8389451
  34. Direct demonstration of insulin-induced GLUT4 translocation to the surface of intact cells by insertion of a c-myc epitope into an exofacial GLUT4 domain.
    J Biol Chem. 1993 Jul 5;268(19):14523-6 PMID: 7686158
  35. The function of GRB2 in linking the insulin receptor to Ras signaling pathways.
    Science. 1993 Jun 25;260(5116):1953-5 PMID: 8316835
  36. Rab GDP dissociation inhibitor as a general regulator for the membrane association of rab proteins.
    J Biol Chem. 1993 Aug 25;268(24):18143-50 PMID: 8349690
  37. 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
  38. cAMP antagonizes p21ras-directed activation of extracellular signal-regulated kinase 2 and phosphorylation of mSos nucleotide exchange factor.
    EMBO J. 1993 Nov;12(11):4211-20 PMID: 8223435
  39. Mitogen-activated protein kinase (MAP kinase), MAP kinase kinase and c-Mos stimulate glucose transport in Xenopus oocytes.
    Biochem J. 1993 Oct 15;295 ( Pt 2):351-5 PMID: 8240233
  40. Rad: a member of the Ras family overexpressed in muscle of type II diabetic humans.
    Science. 1993 Nov 26;262(5138):1441-4 PMID: 8248782
  41. Mitogen-activated protein kinase activation is not sufficient for stimulation of glucose transport or glycogen synthase in 3T3-L1 adipocytes.
    J Biol Chem. 1993 Dec 15;268(35):26422-7 PMID: 8253768
  42. Nck associates with the SH2 domain-docking protein IRS-1 in insulin-stimulated cells.
    Proc Natl Acad Sci U S A. 1993 Dec 15;90(24):11713-7 PMID: 8265614
  43. Essential role of phosphatidylinositol 3-kinase in insulin-induced glucose transport and antilipolysis in rat adipocytes. Studies with a selective inhibitor wortmannin.
    J Biol Chem. 1994 Feb 4;269(5):3568-73 PMID: 8106400
  44. Activation of the Ras/mitogen-activated protein kinase signaling pathway alone is not sufficient to induce glucose uptake in 3T3-L1 adipocytes.
    Mol Cell Biol. 1994 Apr;14(4):2372-7 PMID: 7511205
  45. Ras signaling in the activation of glucose transport by insulin.
    Proc Natl Acad Sci U S A. 1994 May 24;91(11):4644-8 PMID: 8197113
  46. Tyrosine kinase-deficient mutant human insulin receptors (Met1153-->Ile) overexpressed in transfected rat adipose cells fail to mediate translocation of epitope-tagged GLUT4.
    Proc Natl Acad Sci U S A. 1994 Jun 7;91(12):5587-91 PMID: 8202531
  47. 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
  48. 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
  49. Rab proteins in regulated exocytosis.
    Trends Biochem Sci. 1994 Apr;19(4):164-8 PMID: 8016866
  50. A complex of GRB2-dynamin binds to tyrosine-phosphorylated insulin receptor substrate-1 after insulin treatment.
    EMBO J. 1994 Jul 1;13(13):3033-8 PMID: 8039498
  51. Banting Lecture. Insulin action, diabetogenes, and the cause of type II diabetes.
    Diabetes. 1994 Aug;43(8):1066-84 PMID: 8039601
  52. The IRS-1 signaling system.
    Trends Biochem Sci. 1994 Jul;19(7):289-93 PMID: 8048169
  53. Phosphatidylinositol-3-OH kinase as a direct target of Ras.
    Nature. 1994 Aug 18;370(6490):527-32 PMID: 8052307
  54. 1-Phosphatidylinositol 3-kinase activity is required for insulin-stimulated glucose transport but not for RAS activation in CHO cells.
    Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7415-9 PMID: 8052599
  55. Syp (SH-PTP2) is a positive mediator of growth factor-stimulated mitogenic signal transduction.
    J Biol Chem. 1994 Aug 19;269(33):21244-8 PMID: 8063747
  56. Role of p21ras in insulin-stimulated glucose transport in 3T3-L1 adipocytes.
    J Biol Chem. 1994 Aug 26;269(34):21391-4 PMID: 8063767
  57. Growth factor-induced stimulation of hexose transport in 3T3-L1 adipocytes: evidence that insulin-induced translocation of GLUT4 is independent of activation of MAP kinase.
    Cell Signal. 1994 Mar;6(3):313-20 PMID: 7917789
  58. Evidence for a role of phosphatidylinositol 3-kinase in the regulation of glucose transport in Xenopus oocytes.
    J Biol Chem. 1994 Oct 28;269(43):26622-5 PMID: 7929393
  59. Epidermal growth factor triggers the translocation of insulin-responsive glucose transporter (GLUT4).
    Biochem Biophys Res Commun. 1994 Nov 30;205(1):857-63 PMID: 7999123
  60. Cloning and characterization of a G protein-activated human phosphoinositide-3 kinase.
    Science. 1995 Aug 4;269(5224):690-3 PMID: 7624799
Article Info
Journal
The Biochemical journal
Abbr.
Biochem J
ISSN
0264-6021
Published
1996-05-01
Pages
875-82
Language
English
Region
England
NLM ID
2984726R
PMCID
PMC1217288
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: [email protected]