Single Point Mutations Result in the Miss-Sorting of Glut4 to a Novel Membrane Compartment Associated with Stress Granule Proteins

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Song, XiaoMei ^a   Lichti, Cheryl F ^b   Townsend, R Reid ^a   Mueckler, Mike ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE TRANSPORTER 4; INSULIN;

ADIPOCYTE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL FRACTIONATION; CELL SELECTION; CELL SURFACE; CONTROLLED STUDY; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOADSORPTION; IMMUNOGOLD ELECTRON MICROSCOPY; MICROSCOPY; MUSCLE CELL; NONHUMAN; POINT MUTATION; POSTPRANDIAL STATE; PROTEIN MOTIF; STRESS; WILD TYPE;

3T3-L1 CELLS; ANIMALS; CHROMATOGRAPHY, LIQUID; CYTOPLASMIC GRANULES; CYTOPLASMIC VESICLES; GLUCOSE TRANSPORTER TYPE 4; MASS SPECTROMETRY; MICE; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; POINT MUTATION; PROTEIN FOLDING;

EID: 84880457866     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068516     Document Type: Article

References (59)

1. Bryant NJ, Govers R, James DE, (2002) Regulated transport of the glucose transporter GLUT4. Nature Reviews Molecular Cell Biology 3: 267-277.
2. James DE, Strube M, Mueckler M, (1989) Molecular cloning and characterization of an insulin regulatable glucose transporter. Nature 338: 83-87.
3. Calderhead DM, Kitagawa K, Tanner LI, Holman GD, Lienhard GE, (1990) Insulin regulation of the two glucose transporters in 3T3-L1 adipocytes. J Biol Chem 265: 13801-13808.
4. Cushman SW, Wardzala LJ, (1980) 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 255: 4758-4762.
5. Suzuki I, Kono T, (1980) Evidence that insulin causes translocation of glucose transport activity to the plasma membrane from an intracellular storage site. Proc Natl Acad Sci USA 77: 2542-2545.
6. Zierath JR, Krook A, Wallberg-Henriksson H, (1998) Insulin action in skeletal muscle from patients with NIDDM. [Review] [65 refs]. Mol Cell Biochem 182: 153-160.
7. Cline GW, Petersen KF, Krssak M, Shen J, Hundal RS, et al. (1999) Impaired glucose transport as a cause of decreased insulin-stimulated muscle glycogen synthesis in type 2 diabetes [see comments]. N Eng J Med 341: 240-246.
8. Kahn SE, Hull RL, Utzschneider KM, (2006) Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 444: 840-846.
9. Martinez L, Berenguer M, Bruce MC, Le Marchand-Brustel Y, Govers R, (2010) Rosiglitazone increases cell surface GLUT4 levels in 3T3-L1 adipocytes through an enhancement of endosomal recycling. Biochem Pharmacol 79: 1300-1309.
10. Doehner W, Gathercole D, Cicoira M, Krack A, Coats AJ, et al. (2010) Reduced glucose transporter GLUT4 in skeletal muscle predicts insulin resistance in non-diabetic chronic heart failure patients independently of body composition. Int J Cardiol 138: 19-24.
11. Waller AP, Burns TA, Mudge MC, Belknap JK, Lacombe VA, (2011) Insulin resistance selectively alters cell-surface glucose transporters but not their total protein expression in equine skeletal muscle. J Vet Intern Med 25: 315-321.
12. Ramm G, Slot JW, James DE, Stoorvogel W, (2000) Insulin recruits GLUT4 from specialized VAMP2-carrying vesicles as well as from the dynamic endosomal/trans-Golgi network in rat adipocytes. Mol Biol Cell 11: 4079-4091.
13. 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.
14. Govers R, Coster AC, James DE, (2004) Insulin increases cell surface GLUT4 levels by dose dependently discharging GLUT4 into a cell surface recycling pathway. Mol Cell Biol 24: 6456-6466.
15. Yeh TY, Sbodio JI, Tsun ZY, Luo B, Chi NW, (2007) Insulin-stimulated exocytosis of GLUT4 is enhanced by IRAP and its partner tankyrase. Biochem J 402: 279-290.
16. Slot JW, Geuze HJ, Gigengack S, Lienhard GE, James DE, (1991) Immuno-localization of the insulin regulatable glucose transporter in brown adipose tissue of the rat. J Cell Biol 113: 123-135.
17. Fujita H, Hatakeyama H, Watanabe TM, Sato M, Higuchi H, et al. (2010) Identification of three distinct functional sites of insulin-mediated GLUT4 trafficking in adipocytes using quantitative single molecule imaging. Mol Biol Cell 21: 2721-2731.
18. Blot V, McGraw TE, (2008) Molecular Mechanisms Controlling GLUT4 Intracellular Retention. Mol Biol Cell 19: 3477-3487.
19. Karylowski O, Zeigerer A, Cohen A, McGraw TE, (2004) GLUT4 is retained by an intracellular cycle of vesicle formation and fusion with endosomes. Mol Biol Cell 15: 870-882.
20. Jordens I, Molle D, Xiong W, Keller SR, McGraw TE, (2010) Insulin-regulated aminopeptidase is a key regulator of GLUT4 trafficking by controlling the sorting of GLUT4 from endosomes to specialized insulin-regulated vesicles. Mol Biol Cell 21: 2034-2044.
21. Coster AC, Govers R, James DE, (2004) Insulin stimulates the entry of GLUT4 into the endosomal recycling pathway by a quantal mechanism. Traffic 5: 763-771.
22. Yeh JI, Verhey KJ, Birnbaum MJ, (1995) Kinetic analysis of glucose transporter trafficking in fibroblasts and adipocytes. Biochemistry 34: 15523-15531.
23. Larance M, Ramm G, Stockli J, van Dam EM, Winata S, et al. (2005) Characterization of the role of the Rab GTPase-activating protein AS160 in insulin-regulated GLUT4 trafficking. J Biol Chem 280: 37803-37813.
24. Sheena A, Mohan SS, Haridas NP, Anilkumar G, (2011) Elucidation of the glucose transport pathway in glucose transporter 4 via steered molecular dynamics simulations. PLoS One 6: e25747.
25. El-Jack AK, Kandror KV, Pilch PF, (1999) The formation of an insulin-responsive vesicular cargo compartment is an early event in 3T3-L1 adipocyte differentiation. Mol Biol Cell 10: 1581-1594.
26. Gross DN, Farmer SR, Pilch PF, (2004) Glut4 storage vesicles without Glut4: transcriptional regulation of insulin-dependent vesicular traffic. Mol Cell Biol 24: 7151-7162.
27. Shi J, Huang G, Kandror KV, (2008) Self-assembly of Glut4 Storage Vesicles during Differentiation of 3T3-L1 Adipocytes. J Biol Chem 283: 30311-30321.
28. Melvin DR, Marsh BJ, Walmsley AR, James DE, Gould GW, (1999) Analysis of amino and carboxy terminal GLUT-4 targeting motifs in 3T3-L1 adipocytes using an endosomal ablation technique. Biochemistry 38: 1456-1462.
29. Marsh BJ, Martin S, Melvin DR, Martin LB, Alm RA, et al. (1998) Mutational analysis of the carboxy-terminal phosphorylation site of GLUT-4 in 3T3-L1 adipocytes. A J Physiol 275: E412-422.
30. Garippa RJ, Johnson A, Park J, Petrush RL, McGraw TE, (1996) The carboxyl terminus of GLUT4 contains a serine-leucine-leucine sequence that functions as a potent internalization motif in Chinese hamster ovary cells. J Biol Chem 271: 20660-20668.
31. Haney PM, Levy MA, Strube MS, Mueckler M, (1995) Insulin-sensitive targeting of the GLUT4 glucose transporter in L6 myoblasts is conferred by its COOH-terminal cytoplasmic tail. J Cell Biol 129: 641-658.
32. Shewan AM, Marsh BJ, Melvin DR, Martin S, Gould GW, et al. (2000) The cytosolic C-terminus of the glucose transporter GLUT4 contains an acidic cluster endosomal targeting motif distal to the dileucine signal. Biochem J 350: 99-107.
33. Shewan AM, Van Dam EM, Martin S, Luen TB, Hong W, et al. (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. 14: 973-986.
34. Song XM, Hresko RC, Mueckler M, (2008) 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 283: 12571-12585.
35. Corvera S, Chawla A, Chakrabarti R, Joly M, Buxton J, et al. (1994) A double leucine within the GLUT4 glucose transporter COOH-terminal domain functions as an endocytosis signal [published erratum appears in J Cell Biol 1994 Sep;126(6):1625]. J Cell Biol 126: 979-989.
36. Marsh BJ, Alm RA, McIntosh SR, James DE, (1995) Molecular regulation of GLUT-4 targeting in 3T3-L1 adipocytes. J Cell Biol 130: 1081-1091.
37. Al-Hasani H, Kunamneni RK, Dawson K, Hinck CS, Muller-Wieland D, et al. (2002) Roles of the N- and C-termini of GLUT4 in endocytosis. J Cell Sci 115: 131-140.
38. Khan AH, Capilla E, Hou JC, Watson RT, Smith JR, et al. (2004) Entry of newly synthesized GLUT4 into the insulin-responsive storage compartment is dependent upon both the amino terminus and the large cytoplasmic loop. J Biol Chem 279: 37505-37511.
39. Jordens I, Molle D, Xiong W, Keller SR, McGraw TE, (2010) Insulin-regulated aminopeptidase is a key regulator of GLUT4 trafficking by controlling the sorting of GLUT4 from endosomes to specialized insulin-regulated vesicles. Mol Biol Cell 21: 2034-2044.
40. Keller A, Nesvizhskii AI, Kolker E, Aebersold R, (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74: 5383-5392.
41. Perkins DN, Pappin DJ, Creasy DM, Cottrell JS, (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20: 3551-3567.
42. Polpitiya AD, Qian WJ, Jaitly N, Petyuk VA, Adkins JN, et al. (2008) DAnTE: a statistical tool for quantitative analysis of-omics data. Bioinformatics 24: 1556-1558.
43. Karpievitch Y, Stanley J, Taverner T, Huang J, Adkins JN, et al. (2009) A statistical framework for protein quantitation in bottom-up MS-based proteomics. Bioinformatics 25: 2028-2034.
44. Jedrychowski MP, Gartner CA, Gygi SP, Zhou L, Herz J, et al. (2010) Proteomic analysis of GLUT4 storage vesicles reveals LRP1 to be an important vesicle component and target of insulin signaling. J Biol Chem 285: 104-114.
45. Hashiramoto M, James DE, (2000) Characterization of insulin-responsive GLUT4 storage vesicles isolated from 3T3-L1 adipocytes. MolCell Biol 20: 416-427.
46. Augustin R, (2010) The protein family of glucose transport facilitators: It's not only about glucose after all. IUBMB Life 62: 315-333.
47. Kobayashi T, Winslow S, Sunesson L, Hellman U, Larsson C, (2012) PKCalpha binds G3BP2 and regulates stress granule formation following cellular stress. PloS one 7: e35820.
48. Vanderweyde T, Yu H, Varnum M, Liu-Yesucevitz L, Citro A, et al. (2012) Contrasting pathology of the stress granule proteins TIA-1 and G3BP in tauopathies. The Journal of neuroscience: the official journal of the Society for Neuroscience 32: 8270-8283.
49. Uldry M, Steiner P, Zurich MG, Beguin P, Hirling H, et al. (2004) Regulated exocytosis of an H+/myo-inositol symporter at synapses and growth cones. EMBO J 23: 531-540.
50. Tanner LI, Lienhard GE, (1987) Insulin elicits a redistribution of transferrin receptors in 3T3-L1 adipocytes through an increase in the rate constant for receptor externalization. J Biol Chem 262: 8975-8980.
51. Thong FS, Bilan PJ, Klip A, (2007) The Rab GTPase-activating protein AS160 integrates Akt, protein kinase C, and AMP-activated protein kinase signals regulating GLUT4 traffic. Diabetes 56: 414-423.
52. Shigematsu S, Watson RT, Khan AH, Pessin JE, (2003) The adipocyte plasma membrane caveolin functional/structural organization is necessary for the efficient endocytosis of GLUT4. J Biol Chem 278: 10683-10690.
53. Esk C, Chen CY, Johannes L, Brodsky FM, (2010) The clathrin heavy chain isoform CHC22 functions in a novel endosomal sorting step. J Cell Biol 188: 131-144.
54. Hajri T, Hall AM, Jensen DR, Pietka TA, Drover VA, et al. (2007) CD36-facilitated fatty acid uptake inhibits leptin production and signaling in adipose tissue. Diabetes 56: 1872-1880.
55. Coort SL, Hasselbaink DM, Koonen DP, Willems J, Coumans WA, et al. (2004) Enhanced sarcolemmal FAT/CD36 content and triacylglycerol storage in cardiac myocytes from obese zucker rats. Diabetes 53: 1655-1663.
56. Kolobova E, Efimov A, Kaverina I, Rishi AK, Schrader JW, et al. (2009) Microtubule-dependent association of AKAP350A and CCAR1 with RNA stress granules. Exp Cell Res 315: 542-555.
57. Solomon S, Xu Y, Wang B, David MD, Schubert P, et al. (2007) Distinct structural features of caprin-1 mediate its interaction with G3BP-1 and its induction of phosphorylation of eukaryotic translation initiation factor 2alpha, entry to cytoplasmic stress granules, and selective interaction with a subset of mRNAs. Mol Cell Biol 27: 2324-2342.
58. Irvine K, Stirling R, Hume D, Kennedy D, (2004) Rasputin, more promiscuous than ever: a review of G3BP. Int J Dev Biol 48: 1065-1077.
59. Roche SL, O'Sullivan JJ, Kantor PF, (2010) Hypertension after pediatric cardiac transplantation: detection, etiology, implications and management. Pediatr Transplant 14: 159-168.