Home LiteratureArticle Details
PMID: 12134073 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Small GTP-binding protein TC10 differentially regulates two distinct populations of filamentous actin in 3T3L1 adipocytes.

Molecular biology of the cell ·Vol. 13 ·No. 7 ·2002-07-00 ·Pages 2334-46

Kanzaki M, Watson RT, Hou JC, Stamnes M, Saltiel AR, Pessin JE

Abstract

TC10 is a member of the Rho family of small GTP-binding proteins that has previously been implicated in the regulation of insulin-stimulated GLUT4 translocation in adipocytes. In a manner similar to Cdc42-stimulated actin-based motility, we have observed that constitutively active TC10 (TC10/Q75L) can induce actin comet tails in Xenopus oocyte extracts in vitro and extensive actin polymerization in the perinuclear region when expressed in 3T3L1 adipocytes. In contrast, expression of TC10/Q75L completely disrupted adipocyte cortical actin, which was specific for TC10, because expression of constitutively active Cdc42 was without effect. The effect of TC10/Q75L to disrupt cortical actin was abrogated after deletion of the amino terminal extension (DeltaN-TC10/Q75L), whereas this deletion retained the ability to induce perinuclear actin polymerization. In addition, alteration of perinuclear actin by expression of TC10/Q75L, a dominant-interfering TC10/T31N mutant or a mutant N-WASP protein (N-WASP/DeltaVCA) reduced the rate of VSV G protein trafficking to the plasma membrane. Furthermore, TC10 directly bound to Golgi COPI coat proteins through a dilysine motif in the carboxyl terminal domain consistent with a role for TC10 regulating actin polymerization on membrane transport vesicles. Together, these data demonstrate that TC10 can differentially regulate two types of filamentous actin in adipocytes dependent on distinct functional domains and its subcellular compartmentalization.

MeSH Terms
3T3 Cells Actins/metabolism Adipocytes/drug effects,metabolism Amino Acid Motifs Animals Bacterial Proteins Bacterial Toxins/pharmacology Biological Transport/physiology Bridged Bicyclo Compounds, Heterocyclic/pharmacology CHO Cells Cell Nucleus/metabolism Coatomer Protein/metabolism Cricetinae Cytoplasmic Vesicles/metabolism Enzyme Activation Golgi Apparatus/metabolism Mice Microinjections Microscopy, Confocal Mutagenesis, Site-Directed Nerve Tissue Proteins/genetics,metabolism Oocytes/physiology Thiazoles/pharmacology Thiazolidines Time Factors Wiskott-Aldrich Syndrome Protein, Neuronal Xenopus laevis cdc42 GTP-Binding Protein/genetics,metabolism rho GTP-Binding Proteins/genetics,metabolism
Chemicals
Actins Bacterial Proteins Bacterial Toxins Bridged Bicyclo Compounds, Heterocyclic Coatomer Protein Nerve Tissue Proteins Thiazoles Thiazolidines Wasl protein, mouse Wiskott-Aldrich Syndrome Protein, Neuronal toxB protein, Clostridium difficile Rhoq protein, mouse cdc42 GTP-Binding Protein rho GTP-Binding Proteins latrunculin B
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Kanzaki Makoto
Department of Physiology and Biophysics, The University of Iowa, Iowa City, Iowa 52242, USA.
Watson Robert T
Hou June Chunqiu
Stamnes Mark
Saltiel Alan R
Pessin Jeffrey E
References (66)
66 references, click to expand
  1. Signaling to actin dynamics.
    J Cell Biol. 1999 Jul 26;146(2):267-72 PMID: 10427083
  2. Cellular functions of TC10, a Rho family GTPase: regulation of morphology, signal transduction and cell growth.
    Oncogene. 1999 Jul 1;18(26):3831-45 PMID: 10445846
  3. The Borgs, a new family of Cdc42 and TC10 GTPase-interacting proteins.
    Mol Cell Biol. 1999 Oct;19(10):6585-97 PMID: 10490598
  4. Activation of the CDC42 effector N-WASP by the Shigella flexneri IcsA protein promotes actin nucleation by Arp2/3 complex and bacterial actin-based motility.
    J Cell Biol. 1999 Sep 20;146(6):1319-32 PMID: 10491394
  5. Reconstitution of actin-based motility of Listeria and Shigella using pure proteins.
    Nature. 1999 Oct 7;401(6753):613-6 PMID: 10524632
  6. Effects of cytoskeleton-disrupting drugs on ouabain-stimulated catecholamine secretion from cultured adrenal chromaffin cells.
    Biochem Pharmacol. 1988 Sep 1;37(17):3357-9 PMID: 3401261
  7. Peripheral actin filaments control calcium-mediated catecholamine release from streptolysin-O-permeabilized chromaffin cells.
    Eur J Cell Biol. 1988 Jun;46(2):316-26 PMID: 2844537
  8. Actin involvement in exocytosis from PC12 cells: studies on the influence of botulinum C2 toxin on stimulated noradrenaline release.
    J Neurochem. 1989 Feb;52(2):370-6 PMID: 2492057
  9. Cyclin synthesis drives the early embryonic cell cycle.
    Nature. 1989 May 25;339(6222):275-80 PMID: 2566917
  10. Cycling of actin assembly in synaptosomes and neurotransmitter release.
    Neuron. 1989 Aug;3(2):257-65 PMID: 2576215
  11. Effects of caerulein on the apical cytoskeleton of the pancreatic acinar cell.
    J Clin Invest. 1990 Nov;86(5):1649-57 PMID: 1700797
  12. Cortical filamentous actin disassembly and scinderin redistribution during chromaffin cell stimulation precede exocytosis, a phenomenon not exhibited by gelsolin.
    J Cell Biol. 1991 Jun;113(5):1057-67 PMID: 1645735
  13. A comparative study of the actin-based motilities of the pathogenic bacteria Listeria monocytogenes, Shigella flexneri and Rickettsia conorii.
    J Cell Sci. 1999 Jun;112 ( Pt 11):1697-708 PMID: 10318762
  14. Synip: a novel insulin-regulated syntaxin 4-binding protein mediating GLUT4 translocation in adipocytes.
    Mol Cell. 1999 Jun;3(6):751-60 PMID: 10394363
  15. Actin-dependent propulsion of endosomes and lysosomes by recruitment of N-WASP.
    J Cell Biol. 2000 Feb 7;148(3):519-30 PMID: 10662777
  16. Actin filaments play a critical role in insulin-induced exocytotic recruitment but not in endocytosis of GLUT4 in isolated rat adipocytes.
    Biochem J. 2000 Mar 1;346 Pt 2:321-8 PMID: 10677349
  17. The golgi-associated COPI-coated buds and vesicles contain beta/gamma -actin.
    Proc Natl Acad Sci U S A. 2000 Feb 15;97(4):1560-5 PMID: 10677499
  18. Atypical protein kinases Clambda and -zeta associate with the GTP-binding protein Cdc42 and mediate stress fiber loss.
    Mol Cell Biol. 2000 Apr;20(8):2880-9 PMID: 10733591
  19. Dynamics and retention of misfolded proteins in native ER membranes.
    Nat Cell Biol. 2000 May;2(5):288-95 PMID: 10806480
  20. Rho family GTPase Cdc42 is essential for the actin-based motility of Shigella in mammalian cells.
    J Exp Med. 2000 Jun 5;191(11):1905-20 PMID: 10839806
  21. Spectrin tethers and mesh in the biosynthetic pathway.
    J Cell Sci. 2000 Jul;113 ( Pt 13):2331-43 PMID: 10852813
  22. Latrunculin alters the actin-monomer subunit interface to prevent polymerization.
    Nat Cell Biol. 2000 Jun;2(6):376-8 PMID: 10854330
  23. Activated ADP-ribosylation factor assembles distinct pools of actin on golgi membranes.
    J Biol Chem. 2000 Jun 23;275(25):18824-9 PMID: 10777475
  24. The gamma-subunit of the coatomer complex binds Cdc42 to mediate transformation.
    Nature. 2000 Jun 15;405(6788):800-4 PMID: 10866202
  25. A complex of N-WASP and WIP integrates signalling cascades that lead to actin polymerization.
    Nat Cell Biol. 2000 Jul;2(7):441-8 PMID: 10878810
  26. The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42.
    Nat Cell Biol. 2000 Aug;2(8):531-9 PMID: 10934474
  27. CAP defines a second signalling pathway required for insulin-stimulated glucose transport.
    Nature. 2000 Sep 14;407(6801):202-7 PMID: 11001060
  28. Insulin-stimulated GLUT4 translocation requires the CAP-dependent activation of TC10.
    Nature. 2001 Apr 19;410(6831):944-8 PMID: 11309621
  29. cdc42 regulates the exit of apical and basolateral proteins from the trans-Golgi network.
    EMBO J. 2001 May 1;20(9):2171-9 PMID: 11331583
  30. Insulin-induced cortical actin remodeling promotes GLUT4 insertion at muscle cell membrane ruffles.
    J Clin Invest. 2001 Aug;108(3):371-81 PMID: 11489930
  31. Lipid raft microdomain compartmentalization of TC10 is required for insulin signaling and GLUT4 translocation.
    J Cell Biol. 2001 Aug 20;154(4):829-40 PMID: 11502760
  32. Actin microfilaments facilitate the retrograde transport from the Golgi complex to the endoplasmic reticulum in mammalian cells.
    Traffic. 2001 Oct;2(10):717-26 PMID: 11576448
  33. Insulin-stimulated GLUT4 translocation in adipocytes is dependent upon cortical actin remodeling.
    J Biol Chem. 2001 Nov 9;276(45):42436-44 PMID: 11546823
  34. Insulin stimulates actin comet tails on intracellular GLUT4-containing compartments in differentiated 3T3L1 adipocytes.
    J Biol Chem. 2001 Dec 28;276(52):49331-6 PMID: 11606595
  35. Golgi vesicle proteins are linked to the assembly of an actin complex defined by mAbp1.
    Mol Biol Cell. 2002 Feb;13(2):621-31 PMID: 11854417
  36. Destabilization of actin filaments as a requirement for the secretion of catecholamines from permeabilized chromaffin cells.
    FEBS Lett. 1986 Nov 24;208(2):357-63 PMID: 3536577
  37. Inhibition of actin polymerization by latrunculin A.
    FEBS Lett. 1987 Mar 23;213(2):316-8 PMID: 3556584
  38. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors.
    Cell. 1992 Aug 7;70(3):389-99 PMID: 1643657
  39. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling.
    Cell. 1992 Aug 7;70(3):401-10 PMID: 1643658
  40. Cholecystokinin JMV-180 and caerulein effects on the pancreatic acinar cell cytoskeleton.
    Pancreas. 1993 Sep;8(5):638-46 PMID: 7508112
  41. Disassembly of the actin network inhibits insulin-dependent stimulation of glucose transport and prevents recruitment of glucose transporters to the plasma membrane.
    J Biol Chem. 1994 Nov 25;269(47):29934-42 PMID: 7961991
  42. Insulin receptor substrate-1 (IRS1) and Shc compete for a limited pool of Grb2 in mediating insulin downstream signaling.
    J Biol Chem. 1994 Dec 9;269(49):31107-14 PMID: 7983051
  43. Chromaffin cell cortical actin network dynamics control the size of the release-ready vesicle pool and the initial rate of exocytosis.
    Neuron. 1995 Feb;14(2):353-63 PMID: 7857644
  44. Actin filament disassembly is a sufficient final trigger for exocytosis in nonexcitable cells.
    J Cell Biol. 1995 Feb;128(4):589-98 PMID: 7860632
  45. Effect of disruption of actin filaments by Clostridium botulinum C2 toxin on insulin secretion in HIT-T15 cells and pancreatic islets.
    Mol Biol Cell. 1994 Nov;5(11):1199-213 PMID: 7865885
  46. The Ras-related protein Cdc42Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts.
    Mol Cell Biol. 1995 Apr;15(4):1942-52 PMID: 7891688
  47. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia.
    Cell. 1995 Apr 7;81(1):53-62 PMID: 7536630
  48. The GTPase-activating protein n-chimaerin cooperates with Rac1 and Cdc42Hs to induce the formation of lamellipodia and filopodia.
    Mol Cell Biol. 1996 Sep;16(9):5069-80 PMID: 8756665
  49. The small GTP-binding proteins, Rac and Rho, regulate cytoskeletal organization and exocytosis in mast cells by parallel pathways.
    Mol Biol Cell. 1996 Sep;7(9):1429-42 PMID: 8885237
  50. Microfilament dynamics during cell movement and chemotaxis monitored using a GFP-actin fusion protein.
    Curr Biol. 1997 Mar 1;7(3):176-83 PMID: 9276758
  51. Myosin II is involved in the production of constitutive transport vesicles from the TGN.
    J Cell Biol. 1997 Jul 28;138(2):291-306 PMID: 9230072
  52. ER-to-Golgi transport visualized in living cells.
    Nature. 1997 Sep 4;389(6646):81-5 PMID: 9288971
  53. The cortical actin cytoskeleton of lactotropes as an intracellular target for the control of prolactin secretion.
    Endocrinology. 1997 Dec;138(12):5374-84 PMID: 9389523
  54. Rho GTPases and the actin cytoskeleton.
    Science. 1998 Jan 23;279(5350):509-14 PMID: 9438836
  55. Actin filaments participate in the relocalization of phosphatidylinositol3-kinase to glucose transporter-containing compartments and in the stimulation of glucose uptake in 3T3-L1 adipocytes.
    Biochem J. 1998 May 1;331 ( Pt 3):917-28 PMID: 9560323
  56. Neural Wiskott-Aldrich syndrome protein is implicated in the actin-based motility of Shigella flexneri.
    EMBO J. 1998 May 15;17(10):2767-76 PMID: 9582270
  57. Actin dynamics in living mammalian cells.
    J Cell Sci. 1998 Jun;111 ( Pt 12):1649-58 PMID: 9601095
  58. Cdc42 is required for membrane dependent actin polymerization in vitro.
    FEBS Lett. 1998 May 15;427(3):353-6 PMID: 9637256
  59. ADP ribosylation factor regulates spectrin binding to the Golgi complex.
    Proc Natl Acad Sci U S A. 1998 Jul 21;95(15):8607-12 PMID: 9671725
  60. Characterization of the association of the actin-binding protein, IQGAP, and activated Cdc42 with Golgi membranes.
    J Biol Chem. 1998 Aug 28;273(35):22537-44 PMID: 9712880
  61. Actin filaments facilitate insulin activation of the src and collagen homologous/mitogen-activated protein kinase pathway leading to DNA synthesis and c-fos expression.
    J Biol Chem. 1998 Oct 23;273(43):28322-31 PMID: 9774456
  62. Distinct cellular effects and interactions of the Rho-family GTPase TC10.
    Curr Biol. 1998 Oct 22;8(21):1151-60 PMID: 9799731
  63. Kinetic analysis of secretory protein traffic and characterization of golgi to plasma membrane transport intermediates in living cells.
    J Cell Biol. 1998 Dec 14;143(6):1485-503 PMID: 9852146
  64. The Arp2/3 complex mediates actin polymerization induced by the small GTP-binding protein Cdc42.
    Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15362-7 PMID: 9860974
  65. Identification of inducible genes at the early stage of adipocyte differentiation of 3T3-L1 cells.
    Biochem Biophys Res Commun. 1999 Jan 19;254(2):299-305 PMID: 9918832
  66. Specific isoforms of actin-binding proteins on distinct populations of Golgi-derived vesicles.
    J Biol Chem. 1999 Apr 16;274(16):10743-50 PMID: 10196146
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
2002-07-00
Pages
2334-46
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC117317
Subset
IM
Grants
NIDDK NIH HHS · R01 DK059291 · United States
NIDDK NIH HHS · DK-25295 · United States
NIDDK NIH HHS · DK-59291 · United States
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]