Entry of newly synthesized GLUT4 into the insulin-responsive storage compartment is GGA dependent

EMBO Journal

Volumn 23, Issue 10, 2004, Pages 2059-2070

  Watson, Robert T ^a   Khan, Ahmir H ^b   Furukawa, Megumi ^a   Hou, June Chunqiu ^a   Li, Lin ^c   Kanzaki, Makoto ^a   Okada, Shuichi ^d   Kandror, Konstantin V ^c   Pessin, Jeffrey E ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d GUNMA UNIVERSITY   (Japan)

Author keywords

Biosynthesis; GGA; GLUT4; Insulin; Trafficking

Indexed keywords

GLUCOSE TRANSPORTER 4;

ANIMAL CELL; ARTICLE; CELL STRAIN 3T3; CELL VACUOLE; CELLULAR DISTRIBUTION; ELECTROPORATION; INTRACELLULAR TRANSPORT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; PROTEIN TARGETING; SIGNAL TRANSDUCTION;

3T3-L1 CELLS; ADAPTOR PROTEINS, VESICULAR TRANSPORT; ADP-RIBOSYLATION FACTORS; ANIMALS; BIOLOGICAL TRANSPORT; CELL MEMBRANE; DYNAMINS; ELECTROPORATION; ENDOCYTOSIS; GLUCOSE TRANSPORTER TYPE 1; GLUCOSE TRANSPORTER TYPE 4; INSULIN; INTRACELLULAR MEMBRANES; MEMBRANE GLYCOPROTEINS; MICE; MONOSACCHARIDE TRANSPORT PROTEINS; MUSCLE PROTEINS; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; TRANSPORT VESICLES; VIRAL ENVELOPE PROTEINS;

ANIMALIA;

EID: 2942616407     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600159     Document Type: Article

References (40)

1. Al-Hasani H, Hinck CS, Cushman SW (1998) Endocytosis of the glucose transporter GLUT4 is mediated by the GTPase dynamin. J Biol Chem 273: 17504-17510
2. Baumann CA, Ribon V, Kanzaki K, Thurmond DC, Mora S, Shigematsu S, Bickel PE, Pessin JE, Saltiel AR (2000) CAP defines a second signaling pathway required for insulin-stimulated glucose transport. Nature 407: 202-207
3. Bergmann JE (1989) Using temperature-sensitive mutants of VSV to study membrane protein biogenesis. Methods Cell Biol 32: 85-110
4. Bogan JS, Lodish HF (1999) Two compartments for insulin-stimulated exocytosis in 3T3-L1 adipocytes defined by endogenous ACRP30 and GLUT4. J Cell Biol 146: 609-620
5. Bryant NJ, Govers R, James DE (2002) Regulated transport of the glucose transporter GLUT4. Nat Rev Mol Cell Biol 3: 267-277
6. Chiang SH, Baumann CA, Kanzaki M, Thurmond DC, Watson RT, Neudauer CL, Macara IG, Pessin JE, Salteil AR (2001) Insulin-stimulated GLUT4 translocation requires the CAP-dependent activation of TC10. Nature 410: 944-948
7. Czech MP, Corvera S (1999) Signaling mechanisms that regulate glucose transport. J Biol Chem 274: 1865-1868
8. de Wit H, Lichtenstein Y, Geuze HJ, Kelly RB, van der Sluijs P, Klumperman J (1999) Synaptic vesicles form by budding from tubular extensions of sorting endosomes in PC12 cells. Mol Biol Cell 10: 4163-4176
9. Dobson SP, Livingstone C, Gould GW, Tavare JM (1996) Dynamics of insulin-stimulated translocation of GLUT4 in single living cells visualised using green fluorescent protein. FEBS Lett 393: 179-184
10. Elmendorf JS, Boeglin DJ, Pessin JE (1999) Temporal separation of insulin-stimulated GLUT4/IRAP vesicle plasma membrane docking and fusion in 3T3L1 adipocytes. J Biol Chem 274: 37357-37361
11. Elmendorf JS, Chen D, Pessin JE (1998) Guanosine 5′ -O-(3-thiotriphosphate) (GTPgammaS) stimulation of GLUT4 translocation is tyrosine kinase-dependent. J Biol Chem 273: 13289-13296
12. Foster LJ, Li D, Randhawa VK, Klip A (2001) Insulin accelerates inter-endosomal GLUT4 traffic via phosphatidylinositol 3-kinase and protein kinase B. J Biol Chem 276: 44212-44221
13. Garza LA, Birnbaum MJ (2000) Insulin-responsive aminopeptidase trafficking in 3T3-L1 adipocytes. J Biol Chem 275: 2560-2567
14. Helliwell SB, Losko S, Kaiser CA (2001) Components of a ubiquitin ligase complex specify polyubiquitination and intracellular trafficking of the general amino acid permease. J Cell Biol 153: 649-662
15. Holman GD, Sandoval IV (2001) Moving the insulin-regulated glucose transporter GLUT4 into and out of storage. Trends Cell Biol 11: 173-179
16. Kandror KV, Pilch PF (1994) gp160, a tissue-specific marker for insulin-activated glucose transport. Proc Natl Acad Sci USA 91: 8017-8021
17. Kandror KV, Pilch PF (1996) Compartmentalization of protein traffic in insulin-sensitive cells. Am J Physiol 271: E1-E14
18. Kanzaki M, Watson RT, Khan AH, Pessin JE (2001) Insulin stimulates actin comet tails on intracellular GLUT4 containing compartments in differentiated 3T3L1 adipocytes. J Biol Chem 276: 49331-49336
19. Kao AW, Ceresa BP, Santeler SR, Pessin JE (1998) Expression of a dominant interfering dynamin mutant in 3T3L1 adipocytes inhibits GLUT4 endocytosis without affecting insulin signaling. J Biol Chem 273: 25450-25457
20. Klausner RD, Donaldson JG, Lippincott-Schwartz J (1992) Brefeldin A: insights into the control of membrane traffic and organelle structure. J Cell Biol 116: 1071-1080
21. Lampson MA, Schmoranzer J, Zeigerer A, Simon SM, McGraw TE (2001) Insulin-regulated release from the endosomal recycling compartment is regulated by budding of specialized vesicles. Mol Biol Cell 12: 3489-3501
22. Lemmon SK, Traub LM (2000) Sorting in the endosomal system in yeast and animal cells. Curr Opin Cell Biol 12: 457-466
23. Malide D, St-Denis JF, Keller SR, Cushman SW (1997) Vp165 and GLUT4 share similar vesicle pools along their trafficking pathways in rat adipose cells. FEBS Lett 409: 461-468
24. Martin S, Rice JE, Gould GW, Keller SR, Slot JW, James DE (1997) The glucose transporter GLUT4 and the aminopeptidase vp165 colocalise in tubulo-vesicular elements in adipocytes and cardiomyocytes. J Cell Sci 110: 2281-2291
25. Orci L, Glick BS, Rothman JE (1986) A new type of coated vesicular carrier that appears not to contain clathrin: its possible role in protein transport within the Golgi stack. Cell 46: 171-184
26. Palacios S, Lalioti V, Martinez-Arca S, Chattopadhyay S, Sandoval IV (2001) Recycling of the insulin-sensitive glucose transporter GLUT4. Access of surface internalized GLUT4 molecules to the perinuclear storage compartment is mediated by the Phe5-Gln6-Gln7-Ile8 motif. J Biol Chem 276: 3371-3383
27. Pelham HR (1991) Recycling of proteins between the endoplasmic reticulum and Golgi complex. Curr Opin Cell Biol 3: 585-591
28. Pessin J, Thurmond D, Elmendorf J, Coker K, Okada S (1999) Molecular basis of insulin-stimulated GLUT4 vesicle trafficking: location! location!. location!. J Biol Chem 274: 2593-2596
29. Puertollano R, Aguilar RC, Gorshkova I, Crouch RJ, Bonifacino JS (2001) Sorting of mannose 6-phosphate receptors mediated by the GGAs. Science 292: 1712-1716
30. Rea S, James D (1997) Moving GLUT4: the biogenesis and trafficking of GLUT4 storage vesicles. Diabetes 46: 1667-1677
31. Régnier-Vigouroux A, Tooze SA, Huttner WB (1991) Newly synthesized synaptophysin is transported to synaptic-like microvesicles via constitutive secretory vesicles and the plasma membrane. EMBO J 10: 3589-3601
32. Roberg KJ, Rowley N, Kaiser CA (1997) Physiological regulation of membrane protein sorting late in the secretory pathway of Saccharomyces cerevisiae. J Cell Biol 137: 1469-1482
33. Satoh S, Nishimura H, Clark AE, Kozka IJ, Vannucci SJ, Simpson IA, Quon MJ, Cushman SW, Holman GD (1993) Use of bismannose photolabel to elucidate insulin-regulated GLUT4 subcellular trafficking kinetics in rat adipose cells. Evidence that exocytosis is a critical site of hormone action. J Biol Chem 268: 17820-17829
34. Shewan AM, Van Dam EM, Martin S, Luen TB, Hong W, Bryant NJ, James DE (2003) 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 14: 973-986
35. Shigematsu S, Khan AH, Kanzaki M, Pessin JE (2002) Intracellular insulin-responsive glucose transporter (GLUT4) distribution but not insulin-stimulated GLUT4 exocytosis and recycling are microtubule dependent. Mol Endocrinol 16: 1060-1068
36. Subtil A, Lampson MA, Keller SR, McGraw TE (2000) Characterization of the insulin-regulated endocytic recycling mechanism in 3T3-L1 adipocytes using a novel reporter molecule. J Biol Chem 275: 4787-4795
37. Volchuk A, Narine S, Foster LJ, Grabs D, De Camilli P, Klip A (1998) Perturbation of dynamin II with an amphiphysin SH3 domain increases GLUT4 glucose transporters at the plasma membrane in 3T3-L1 adipocytes. Dynamin II participates in GLUT4 endocytosis. J Biol Chem 273: 8169-8176
38. Watson RT, Pessin JE (2001) Intracellular organization of insulin signaling and GLUT4 translocation. Recent Prog Horm Res 56: 175-193
39. Watson RT, Shigematsu S, Chiang SH, Mora S, Kanzaki M, Macara IG, Saltiel AR, Pessin JE (2001) Lipid raft microdomain compartmentalization of TC10 is required for insulin signaling and GLUT4 translocation. J Cell Biol 154: 829-840
40. Xu Z, Kandror KV (2002) Translocation of small preformed vesicles is responsible for the insulin activation of glucose transport in adipose cells. Evidence from the in vitro reconstitution assay. J Biol Chem 277: 47972-47975