![[Feedback]](/icons/banner/feedbackACT.gif){kind=icon}
![[For Subscribers]](/icons/banner/subscriberACT.gif){kind=icon}
![[Archive]](/icons/banner/archiveACT.gif){kind=icon}
![[Search]](/icons/banner/searchACT.gif){kind=icon}
|
|
|
|
|
||
A more recent version of this article appeared on July 1, 2002
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Submitted on February 5, 2002
Revised on March 21, 2002
Accepted on April 12, 2002
1 Department of Biochemistry, Weill Medical College of Cornell University, New York, NY 10021
2 Department of Biochemistry and Program in Physiology, Biophysics and Molecular Medicine, Weill Medical College of Cornell University, New York, NY 10021
3 Department of Cell Biology, New York University School of Medicine, New York, NY 10016-6437
* Corresponding author. E-mail address: temcgraw{at}med.cornell.edu.
Insulin regulates glucose uptake into fat and muscle by modulating the distribution of the GLUT4 glucose transporter between the surface and interior of cells. The GLUT4 trafficking pathway overlaps with the general endocytic recycling pathway, but the degree and functional significance of the overlap are not known. In this study of intact adipocytes, we demonstrate, using a compartment specific fluorescence-quenching assay, that GLUT4 is equally distributed among two intracellular pools: the transferrin receptor (TR)-containing endosomes and a specialized compartment that excludes the TR. These pools of GLUT4 are in dynamic communication with one another and with the cell surface. Insulin-induced redistribution of GLUT4 to the surface requires mobilization of both pools. These data establish a role for the general endosomal system in the specialized, insulin-regulated trafficking of GLUT4. Trafficking through the general endosomal system is regulated by rab11. Here we show that rab11 is required for the transport of GLUT4 from endosomes to the specialized compartment and for the insulin-induced translocation to the cell surface, emphasizing the importance of the general endosomal pathway in the specialized trafficking of GLUT4. Based on these findings we propose a two-step model for GLUT4 trafficking in which the general endosomal recycling compartment plays a specialized role in the insulin-regulated traffic of GLUT4. This compartment-based model provides the framework for understanding insulin-regulated trafficking at a molecular level.
This article has been cited by other articles:
|
|
 |
|
  J. Shi, G. Huang, and K. V. Kandror Self-assembly of Glut4 Storage Vesicles during Differentiation of 3T3-L1 Adipocytes J. Biol. Chem., October 31, 2008; 283(44): 30311 - 30321. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
V. K. Randhawa, S. Ishikura, I. Talior-Volodarsky, A. W. P. Cheng, N. Patel, J. H. Hartwig, and A. Klip GLUT4 Vesicle Recruitment and Fusion Are Differentially Regulated by Rac, AS160, and Rab8A in Muscle Cells J. Biol. Chem., October 3, 2008; 283(40): 27208 - 27219. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Ishikura and A. Klip Muscle cells engage Rab8A and myosin Vb in insulin-dependent GLUT4 translocation Am J Physiol Cell Physiol, October 1, 2008; 295(4): C1016 - C1025. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 V. Blot and T. E. McGraw Molecular Mechanisms Controlling GLUT4 Intracellular Retention Mol. Biol. Cell, August 1, 2008; 19(8): 3477 - 3487. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
X. M. Song, R. C. Hresko, and M. Mueckler Identification of Amino Acid Residues within the C Terminus of the Glut4 Glucose Transporter That Are Essential for Insulin-stimulated Redistribution to the Plasma Membrane J. Biol. Chem., May 2, 2008; 283(18): 12571 - 12585. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. Williams and J. E. Pessin Mapping of R-SNARE function at distinct intracellular GLUT4 trafficking steps in adipocytes J. Cell Biol., January 28, 2008; 180(2): 375 - 387. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. M. Muretta, I. Romenskaia, and C. C. Mastick Insulin Releases Glut4 from Static Storage Compartments into Cycling Endosomes and Increases the Rate Constant for Glut4 Exocytosis J. Biol. Chem., January 4, 2008; 283(1): 311 - 323. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. I. Welsh, S. E. Leney, B. Lloyd-Lewis, M. Wherlock, A. J. Lindsay, M. W. McCaffrey, and J. M. Tavare Rip11 is a Rab11- and AS160-RabGAP-binding protein required for insulin-stimulated glucose uptake in adipocytes J. Cell Sci., December 1, 2007; 120(23): 4197 - 4208. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Li, P. J. Peters, M. Bai, J. Dai, E. Bos, T. Kirchhausen, K. V. Kandror, and V. W. Hsu An ACAP1-containing clathrin coat complex for endocytic recycling J. Cell Biol., July 24, 2007; 178(3): 453 - 464. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Huang, L. M. Lifshitz, C. Jones, K. D. Bellve, C. Standley, S. Fonseca, S. Corvera, K. E. Fogarty, and M. P. Czech Insulin Stimulates Membrane Fusion and GLUT4 Accumulation in Clathrin Coats on Adipocyte Plasma Membranes Mol. Cell. Biol., May 1, 2007; 27(9): 3456 - 3469. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. M. Muretta, I. Romenskaia, P. A. Cassiday, and C. C. Mastick Expression of a synapsin IIb site 1 phosphorylation mutant in 3T3-L1 adipocytes inhibits basal intracellular retention of Glut4 J. Cell Sci., April 1, 2007; 120(7): 1168 - 1177. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Saraste and B. Goud Functional Symmetry of Endomembranes Mol. Biol. Cell, April 1, 2007; 18(4): 1430 - 1436. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. B. Hurov, M. Huang, L. S. White, J. Lennerz, C. S. Choi, Y.-R. Cho, H.-J. Kim, J. L. Prior, D. Piwnica-Worms, L. C. Cantley, et al. Loss of the Par-1b/MARK2 polarity kinase leads to increased metabolic rate, decreased adiposity, and insulin hypersensitivity in vivo PNAS, March 27, 2007; 104(13): 5680 - 5685. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Shi and K. V. Kandror The Luminal Vps10p Domain of Sortilin Plays the Predominant Role in Targeting to Insulin-responsive Glut4-containing Vesicles J. Biol. Chem., March 23, 2007; 282(12): 9008 - 9016. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. Campanoni and M. R. Blatt Membrane trafficking and polar growth in root hairs and pollen tubes J. Exp. Bot., January 1, 2007; 58(1): 65 - 74. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. A. Eyster, Q. S. Duggins, G. J. Gorbsky, and A. L. Olson Microtubule Network Is Required for Insulin Signaling through Activation of Akt/Protein Kinase B: EVIDENCE THAT INSULIN STIMULATES VESICLE DOCKING/FUSION BUT NOT INTRACELLULAR MOBILITY J. Biol. Chem., December 22, 2006; 281(51): 39719 - 39727. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. Gonzalez and T. E. McGraw Insulin Signaling Diverges into Akt-dependent and -independent Signals to Regulate the Recruitment/Docking and the Fusion of GLUT4 Vesicles to the Plasma Membrane Mol. Biol. Cell, October 1, 2006; 17(10): 4484 - 4493. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. M. Kong, K. A. Horan, A. Sriratana, C. G. Bailey, L. J. Collyer, H. H. Nandurkar, A. Shisheva, M. J. Layton, J. E. J. Rasko, T. Rowe, et al. Phosphatidylinositol 3-Phosphate [PtdIns(3)P] Is Generated at the Plasma Membrane by an Inositol Polyphosphate 5-Phosphatase: Endogenous PtdIns(3)P Can Promote GLUT4 Translocation to the Plasma Membrane. Mol. Cell. Biol., August 1, 2006; 26(16): 6065 - 6081. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Mari, P. Monzo, V. Kaddai, F. Keslair, T. Gonzalez, Y. Le Marchand-Brustel, and M. Cormont The Rab4 effector Rabip4 plays a role in the endocytotic trafficking of Glut 4 in 3T3-L1 adipocytes J. Cell Sci., April 1, 2006; 119(7): 1297 - 1306. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
O. J. Martin, A. Lee, and T. E. McGraw GLUT4 Distribution between the Plasma Membrane and the Intracellular Compartments Is Maintained by an Insulin-modulated Bipartite Dynamic Mechanism J. Biol. Chem., January 6, 2006; 281(1): 484 - 490. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
O. A. Jovanovic, F. D. Brown, and J. G. Donaldson An Effector Domain Mutant of Arf6 Implicates Phospholipase D in Endosomal Membrane Recycling Mol. Biol. Cell, January 1, 2006; 17(1): 327 - 335. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Ishiki and A. Klip Minireview: Recent Developments in the Regulation of Glucose Transporter-4 Traffic: New Signals, Locations, and Partners Endocrinology, December 1, 2005; 146(12): 5071 - 5078. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Larance, G. Ramm, J. Stockli, E. M. van Dam, S. Winata, V. Wasinger, F. Simpson, M. Graham, J. R. Junutula, M. Guilhaus, et al. Characterization of the Role of the Rab GTPase-activating Protein AS160 in Insulin-regulated GLUT4 Trafficking J. Biol. Chem., November 11, 2005; 280(45): 37803 - 37813. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Bose, A. Guilherme, S. Huang, A. C. Hubbard, C. R. Lane, N. A. Soriano, and M. P. Czech The v-SNARE Vti1a Regulates Insulin-stimulated Glucose Transport and Acrp30 Secretion in 3T3-L1 Adipocytes J. Biol. Chem., November 4, 2005; 280(44): 36946 - 36951. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Ishiki, V. K. Randhawa, V. Poon, L. JeBailey, and A. Klip Insulin Regulates the Membrane Arrival, Fusion, and C-terminal Unmasking of Glucose Transporter-4 via Distinct Phosphoinositides J. Biol. Chem., August 5, 2005; 280(31): 28792 - 28802. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. S. L. Thong, C. B. Dugani, and A. Klip Turning Signals On and Off: GLUT4 Traffic in the Insulin-Signaling Highway Physiology, August 1, 2005; 20(4): 271 - 284. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G.-Y. Liu, V. Kulasingam, R. T. Alexander, N. Touret, A. M. Fong, D. D. Patel, and L. A. Robinson Recycling of the Membrane-anchored Chemokine, CX3CL1 J. Biol. Chem., May 20, 2005; 280(20): 19858 - 19866. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
V. A. Lizunov, H. Matsumoto, J. Zimmerberg, S. W. Cushman, and V. A. Frolov Insulin stimulates the halting, tethering, and fusion of mobile GLUT4 vesicles in rat adipose cells J. Cell Biol., May 9, 2005; 169(3): 481 - 489. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. A. Eyster, Q. S. Duggins, and A. L. Olson Expression of Constitutively Active Akt/Protein Kinase B Signals GLUT4 Translocation in the Absence of an Intact Actin Cytoskeleton J. Biol. Chem., May 6, 2005; 280(18): 17978 - 17985. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Yang and G. D. Holman Insulin and Contraction Stimulate Exocytosis, but Increased AMP-activated Protein Kinase Activity Resulting from Oxidative Metabolism Stress Slows Endocytosis of GLUT4 in Cardiomyocytes J. Biol. Chem., February 11, 2005; 280(6): 4070 - 4078. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. C. Berwick, G. C. Dell, G. I. Welsh, K. J. Heesom, I. Hers, L. M. Fletcher, F. T. Cooke, and J. M. Tavare Protein kinase B phosphorylation of PIKfyve regulates the trafficking of GLUT4 vesicles J. Cell Sci., December 1, 2004; 117(25): 5985 - 5993. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
V. K. Randhawa, F. S.L. Thong, D. Y. Lim, D. Li, R. R. Garg, R. Rudge, T. Galli, A. Rudich, and A. Klip Insulin and Hypertonicity Recruit GLUT4 to the Plasma Membrane of Muscle Cells by Using N-Ethylmaleimide-sensitive Factor-dependent SNARE Mechanisms but Different v-SNAREs: Role of TI-VAMP Mol. Biol. Cell, December 1, 2004; 15(12): 5565 - 5573. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. Wertheim, Z. Cai, and T. E. McGraw The Transcription Factor CCAAT/Enhancer-binding Protein {alpha} Is Required for the Intracellular Retention of GLUT4 J. Biol. Chem., October 1, 2004; 279(40): 41468 - 41476. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Zeigerer, M. K. McBrayer, and T. E. McGraw Insulin Stimulation of GLUT4 Exocytosis, but Not Its Inhibition of Endocytosis, Is Dependent on RabGAP AS160 Mol. Biol. Cell, October 1, 2004; 15(10): 4406 - 4415. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Guilherme, N. A. Soriano, P. S. Furcinitti, and M. P. Czech Role of EHD1 and EHBP1 in Perinuclear Sorting and Insulin-regulated GLUT4 Recycling in 3T3-L1 Adipocytes J. Biol. Chem., September 17, 2004; 279(38): 40062 - 40075. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Malikova, J. Shi, and K. V. Kandror V-type ATPase is involved in biogenesis of GLUT4 vesicles Am J Physiol Endocrinol Metab, September 1, 2004; 287(3): E547 - E552. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Govers, A. C. F. Coster, and D. E. James Insulin Increases Cell Surface GLUT4 Levels by Dose Dependently Discharging GLUT4 into a Cell Surface Recycling Pathway Mol. Cell. Biol., July 15, 2004; 24(14): 6456 - 6466. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. T. Watson, M. Kanzaki, and J. E. Pessin Regulated Membrane Trafficking of the Insulin-Responsive Glucose Transporter 4 in Adipocytes Endocr. Rev., April 1, 2004; 25(2): 177 - 204. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
O. Karylowski, A. Zeigerer, A. Cohen, and T. E. McGraw GLUT4 Is Retained by an Intracellular Cycle of Vesicle Formation and Fusion with Endosomes Mol. Biol. Cell, February 1, 2004; 15(2): 870 - 882. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. S. Bae, H. Cho, J. Mu, and M. J. Birnbaum Isoform-specific Regulation of Insulin-dependent Glucose Uptake by Akt/Protein Kinase B J. Biol. Chem., December 5, 2003; 278(49): 49530 - 49536. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. L. Olson, C. A. Eyster, Q. S. Duggins, and J. B. Knight Insulin Promotes Formation of Polymerized Microtubules by a Phosphatidylinositol 3-Kinase-Independent, Actin-Dependent Pathway in 3T3-L1 Adipocytes Endocrinology, November 1, 2003; 144(11): 5030 - 5039. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. K. I. Perera, M. Clarke, N. J. Morris, W. Hong, L. H. Chamberlain, and G. W. Gould Syntaxin 6 Regulates Glut4 Trafficking in 3T3-L1 Adipocytes Mol. Biol. Cell, July 1, 2003; 14(7): 2946 - 2958. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Roosterman, F. Schmidlin, and N. W. Bunnett Rab5a and rab11a mediate agonist-induced trafficking of protease-activated receptor 2 Am J Physiol Cell Physiol, May 1, 2003; 284(5): C1319 - C1329. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Sano, S. Kane, E. Sano, C. P. Miinea, J. M. Asara, W. S. Lane, C. W. Garner, and G. E. Lienhard Insulin-stimulated Phosphorylation of a Rab GTPase-activating Protein Regulates GLUT4 Translocation J. Biol. Chem., April 18, 2003; 278(17): 14599 - 14602. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. M. Shewan, E. M. van Dam, S. Martin, T. B. Luen, W. Hong, N. J. Bryant, and D. E. James GLUT4 Recycles via a trans-Golgi Network (TGN) Subdomain Enriched in Syntaxins 6 and 16 But Not TGN38: Involvement of an Acidic Targeting Motif Mol. Biol. Cell, March 1, 2003; 14(3): 973 - 986. [Abstract] [Full Text] [PDF]
|
|
