ATM and GLUT1-S490 Phosphorylation Regulate GLUT1 Mediated Transport in Skeletal Muscle

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Andrisse, Stanley ^a   Patel, Gaytri D ^a   Chen, Joseph E ^a   Webber, Andrea M ^a   Spears, Larry D ^a,b   Koehler, Rikki M ^a   Robinson Hill, Rona M ^a   Ching, James K ^a,c   Jeong, Imju ^a,d   Fisher, Jonathan S ^a  

^a SAINT LOUIS UNIVERSITY   (United States)

^b WASHINGTON UNIVERSITY   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; DEHYDROASCORBIC ACID; DOXORUBICIN; GIPC1 PROTEIN; GLUCOSE; GLUCOSE TRANSPORTER 1; PDZ PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL SURFACE; CONTROLLED STUDY; EXTENSOR DIGITORUM LONGUS MUSCLE; GLUCOSE TRANSPORT; INHIBITION KINETICS; MOUSE; MUTATIONAL ANALYSIS; MYOBLAST; NONHUMAN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SKELETAL MUSCLE; SOLEUS MUSCLE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL LINE; GLUCOSE TRANSPORTER TYPE 1; IMMUNOPRECIPITATION; MICE; MUSCLE, SKELETAL; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN TRANSPORT; RATS;

ATAXIA TELANGIECTASIA;

EID: 84878916478     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066027     Document Type: Article

References (60)

1. Stumvoll M, Gerich J, (2001) Clinical features of insulin resistance and beta cell dysfunction and the relationship to type 2 diabetes. Clin Lab Med 21: 31-51.
2. Kahn SE, (2003) The relative contributions of insulin resistance and beta-cell dysfunction to the pathophysiology of Type 2 diabetes. Diabetologia 46: 3-19.
3. Im SS, Kwon SK, Kim TH, Kim HI, Ahn YH, (2007) Regulation of glucose transporter type 4 isoform gene expression in muscle and adipocytes. IUBMB Life 59: 134-145.
4. Cheatham B, (2000) GLUT4 and company: SNAREing roles in insulin-regulated glucose uptake. Trends Endocrinol Metab 11: 356-361.
5. Ciaraldi TP, Mudaliar S, Barzin A, Macievic JA, Edelman SV, et al. (2005) Skeletal muscle GLUT1 transporter protein expression and basal leg glucose uptake are reduced in type 2 diabetes. J Clin Endocrinol Metab 90: 352-358.
6. Krook A, Wallberg-Henriksson H, Zierath JR, (2004) Sending the signal: molecular mechanisms regulating glucose uptake. Med Sci Sports Exerc 36: 1212-1217.
7. Zisman A, Peroni OD, Abel ED, Michael MD, Mauvais-Jarvis F, et al. (2000) Targeted disruption of the glucose transporter 4 selectively in muscle causes insulin resistance and glucose intolerance. Nat Med 6: 924-928.
8. Rudich A, Konrad D, Torok D, Ben-Romano R, Huang C, et al. (2003) Indinavir uncovers different contributions of GLUT4 and GLUT1 towards glucose uptake in muscle and fat cells and tissues. Diabetologia 46: 649-658.
9. Korcok J, Dixon SJ, Lo TC, Wilson JX, (2003) Differential effects of glucose on dehydroascorbic acid transport and intracellular ascorbate accumulation in astrocytes and skeletal myocytes. Brain Res 993: 201-207.
10. Rumsey SC, Kwon O, Xu GW, Burant CF, Simpson I, et al. (1997) Glucose transporter isoforms GLUT1 and GLUT3 transport dehydroascorbic acid. J Biol Chem 272: 18982-18989.
11. Rumsey SC, Daruwala R, Al-Hasani H, Zarnowski MJ, Simpson IA, et al. (2000) Dehydroascorbic acid transport by GLUT4 in Xenopus oocytes and isolated rat adipocytes. J Biol Chem 275: 28246-28253.
12. Verhey KJ, Hausdorff SF, Birnbaum MJ, (1993) Identification of the carboxy terminus as important for the isoform-specific subcellular targeting of glucose transporter proteins. J Cell Biol 123: 137-147.
13. Dauterive R, Laroux S, Bunn RC, Chaisson A, Sanson T, et al. (1996) C-terminal mutations that alter the turnover number for 3-O-methylglucose transport by GLUT1 and GLUT4. J Biol Chem 271: 11414-11421.
14. Reed BC, Cefalu C, Bellaire BH, Cardelli JA, Louis T, et al. (2005) GLUT1CBP(TIP2/GIPC1) interactions with GLUT1 and myosin VI: evidence supporting an adapter function for GLUT1CBP. Mol Biol Cell 16: 4183-4201.
15. Wieman HL, Horn SR, Jacobs SR, Altman BJ, Kornbluth S, et al. (2009) An essential role for the Glut1 PDZ-binding motif in growth factor regulation of Glut1 degradation and trafficking. Biochem J 418: 345-367.
16. Kasahara T, Maeda M, Boles E, Kasahara M, (2009) Identification of a key residue determining substrate affinity in the human glucose transporter GLUT1. Biochim Biophys Acta 1788: 1051-1055.
17. Zhang JZ, Abbud W, Prohaska R, Ismail-Beigi F, (2001) Overexpression of stomatin depresses GLUT-1 glucose transporter activity. Am J Physiol Cell Physiol 280: C1277-1283.
18. Jeong I, Patel AY, Zhang Z, Patil PB, Nadella ST, et al. (2010) Role of ataxia telangiectasia mutated in insulin signalling of muscle-derived cell lines and mouse soleus. Acta Physiol (Oxf) 198: 465-475.
19. Halaby MJ, Hibma JC, He J, Yang DQ, (2008) ATM protein kinase mediates full activation of Akt and regulates glucose transporter 4 translocation by insulin in muscle cells. Cell Signal 20: 1555-1563.
20. Miles PD, Treuner K, Latronica M, Olefsky JM, Barlow C, (2007) Impaired insulin secretion in a mouse model of ataxia telangiectasia. Am J Physiol Endocrinol Metab 293: E70-74.
21. Schneider JG, Finck BN, Ren J, Standley KN, Takagi M, et al. (2006) ATM-dependent suppression of stress signaling reduces vascular disease in metabolic syndrome. Cell Metab 4: 377-389.
22. Matsuoka S, Ballif BA, Smogorzewska A, McDonald ER, 3rd, Hurov KE, et al (2007) ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316: 1160-1166.
23. Hickson I, Zhao Y, Richardson CJ, Green SJ, Martin NM, et al. (2004) Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res 64: 9152-9159.
24. Rainey MD, Charlton ME, Stanton RV, Kastan MB, (2008) Transient inhibition of ATM kinase is sufficient to enhance cellular sensitivity to ionizing radiation. Cancer Res 68: 7466-7474.
25. Barlow C, Hirotsune S, Paylor R, Liyanage M, Eckhaus M, et al. (1996) Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 86: 159-171.
26. Wieman HL, Wofford JA, Rathmell JC, (2007) Cytokine stimulation promotes glucose uptake via phosphatidylinositol-3 kinase/Akt regulation of Glut1 activity and trafficking. Mol Biol Cell 18: 1437-1446.
27. Bilan PJ, Mitsumoto Y, Maher F, Simpson IA, Klip A, (1992) Detection of the GLUT3 facilitative glucose transporter in rat L6 muscle cells: regulation by cellular differentiation, insulin and insulin-like growth factor-I. Biochem Biophys Res Commun 186: 1129-1137.
28. Wijesekara N, Tung A, Thong F, Klip A, (2006) Muscle cell depolarization induces a gain in surface GLUT4 via reduced endocytosis independently of AMPK. Am J Physiol Endocrinol Metab 290: E1276-1286.
29. Ishikura S, Antonescu CN, Klip A (2010) Documenting GLUT4 exocytosis and endocytosis in muscle cell monolayers. Curr Protoc Cell Biol Chapter 15: Unit 15 15.
30. Ju JS, Smith JL, Oppelt PJ, Fisher JS, (2005) Creatine feeding increases GLUT4 expression in rat skeletal muscle. Am J Physiol Endocrinol Metab 288: E347-352.
31. Smith JL, Ju JS, Saha BM, Racette BA, Fisher JS, (2004) Levodopa with carbidopa diminishes glycogen concentration, glycogen synthase activity, and insulin-stimulated glucose transport in rat skeletal muscle. J Appl Physiol 97: 2339-2346.
32. Murata H, Hruz PW, Mueckler M, (2000) The mechanism of insulin resistance caused by HIV protease inhibitor therapy. J Biol Chem 275: 20251-20254.
33. Kahn BB, Flier JS, (1990) Regulation of glucose-transporter gene expression in vitro and in vivo. Diabetes Care 13: 548-564.
34. Klip A, Marette A, (1992) Acute and chronic signals controlling glucose transport in skeletal muscle. J Cell Biochem 48: 51-60.
35. Kahn BB, (1994) Dietary regulation of glucose transporter gene expression: tissue specific effects in adipose cells and muscle. J Nutr 124: 1289S-1295S.
36. Guillet-Deniau I, Leturque A, Girard J, (1994) Expression and cellular localization of glucose transporters (GLUT1, GLUT3, GLUT4) during differentiation of myogenic cells isolated from rat foetuses. J Cell Sci 107 (Pt 3): 487-496.
37. Huang J, Yang J, Maity B, Mayuzumi D, Fisher RA, (2011) Regulator of G protein signaling 6 mediates doxorubicin-induced ATM and p53 activation by a reactive oxygen species-dependent mechanism. Cancer Res 71: 6310-6319.
38. Hornbeck PV, Kornhauser JM, Tkachev S, Zhang B, Skrzypek E, et al. (2012) PhosphoSitePlus: a comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res 40: D261-270.
39. Blom N, Sicheritz-Ponten T, Gupta R, Gammeltoft S, Brunak S, (2004) Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics 4: 1633-1649.
40. Carruthers A, DeZutter J, Ganguly A, Devaskar SU, (2009) Will the original glucose transporter isoform please stand up! Am J Physiol Endocrinol Metab. 297: E836-848.
41. Ching JK, Spears LD, Armon JL, Renth AL, Andrisse S, Collins IV RL, Fisher JS (2013) Impaired insulin-stimulated glucose transport in ATM-deficient mouse skeletal muscle. Applied Physiology, Nutrition, and Metabolism in press.
42. Hirakawa T, Galet C, Kishi M, Ascoli M, (2003) GIPC binds to the human lutropin receptor (hLHR) through an unusual PDZ domain binding motif, and it regulates the sorting of the internalized human choriogonadotropin and the density of cell surface hLHR. J Biol Chem 278: 49348-49357.
43. Bunn RC, Jensen MA, Reed BC, (1999) Protein interactions with the glucose transporter binding protein GLUT1CBP that provide a link between GLUT1 and the cytoskeleton. Mol Biol Cell 10: 819-832.
44. Stiffler MA, Grantcharova VP, Sevecka M, MacBeath G, (2006) Uncovering quantitative protein interaction networks for mouse PDZ domains using protein microarrays. J Am Chem Soc 128: 5913-5922.
45. Beuming T, Skrabanek L, Niv MY, Mukherjee P, Weinstein H, (2005) PDZBase: a protein-protein interaction database for PDZ-domains. Bioinformatics 21: 827-828.
46. Mueckler M, Makepeace C, (2009) Model of the exofacial substrate-binding site and helical folding of the human Glut1 glucose transporter based on scanning mutagenesis. Biochemistry 48: 5934-5942.
47. Sun L, Zeng X, Yan C, Sun X, Gong X, et al. (2012) Crystal structure of a bacterial homologue of glucose transporters GLUT1-4. Nature 490: 361-366.
48. Edinger AL, Cinalli RM, Thompson CB, (2003) Rab7 prevents growth factor-independent survival by inhibiting cell-autonomous nutrient transporter expression. Dev Cell 5: 571-582.
49. Lum JJ, Bauer DE, Kong M, Harris MH, Li C, et al. (2005) Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 120: 237-248.
50. Rathmell JC, Fox CJ, Plas DR, Hammerman PS, Cinalli RM, et al. (2003) Akt-directed glucose metabolism can prevent Bax conformation change and promote growth factor-independent survival. Mol Cell Biol 23: 7315-7328.
51. Viniegra JG, Martinez N, Modirassari P, Losa JH, Parada Cobo C, et al. (2005) Full activation of PKB/Akt in response to insulin or ionizing radiation is mediated through ATM. J Biol Chem 280: 4029-4036.
52. Katz EB, Stenbit AE, Hatton K, DePinho R, Charron MJ, (1995) Cardiac and adipose tissue abnormalities but not diabetes in mice deficient in GLUT4. Nature 377: 151-155.
53. De Rosa S, Cirillo P, Paglia A, Sasso L, Di Palma V, et al. (2010) Reactive oxygen species and antioxidants in the pathophysiology of cardiovascular disease: does the actual knowledge justify a clinical approach? Curr Vasc Pharmacol 8: 259-275.
54. Anderson EJ, Lustig ME, Boyle KE, Woodlief TL, Kane DA, et al. (2009) Mitochondrial H2O2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J Clin Invest 119: 573-581.
55. Henriksen EJ, Diamond-Stanic MK, Marchionne EM, (2011) Oxidative stress and the etiology of insulin resistance and type 2 diabetes. Free Radic Biol Med 51: 993-999.
56. Maddux BA, See W, Lawrence JC Jr, Goldfine AL, Goldfine ID, et al. (2001) Protection against oxidative stress-induced insulin resistance in rat L6 muscle cells by mircomolar concentrations of alpha-lipoic acid. Diabetes 50: 404-410.
57. Bonnard C, Durand A, Peyrol S, Chanseaume E, Chauvin MA, et al. (2008) Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J Clin Invest 118: 789-800.
58. Wilson CM, Mitsumoto Y, Maher F, Klip A, (1995) Regulation of cell surface GLUT1, GLUT3, and GLUT4 by insulin and IGF-I in L6 myotubes. FEBS Lett 368: 19-22.
59. Wood IS, Trayhurn P, (2003) Glucose transporters (GLUT and SGLT): expanded families of sugar transport proteins. Br J Nutr 89: 3-9.
60. Stuart CA, Howell ME, Zhang Y, Yin D, (2009) Insulin-stimulated translocation of glucose transporter (GLUT) 12 parallels that of GLUT4 in normal muscle. J Clin Endocrinol Metab 94: 3535-3542.