AMPK-Dependent Degradation of TXNIP upon Energy Stress Leads to Enhanced Glucose Uptake via GLUT1

Molecular Cell

Volumn 49, Issue 6, 2013, Pages 1167-1175

  Wu, Ning ^a,b   Zheng, Bin ^c   Shaywitz, Adam ^b,e   Dagon, Yossi ^b   Tower, Christine ^b   Bellinger, Gary ^b   Shen, Che Hung ^c   Wen, Jennifer ^d   Asara, John ^b   McGraw, Timothy E ^d   Kahn, Barbara B ^b   Cantley, Lewis C ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^c NewYork Presbyterian Hospital   (United States)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

^e AMGEN INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; ADENOSINE TRIPHOSPHATE; GLUCOSE TRANSPORTER 1; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; THIOREDOXIN INTERACTING PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DEGRADATION; GENE CONTROL; GLUCOSE TRANSPORT; INTERNALIZATION; MIGRATION INHIBITION; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; PHOSPHORYLATION;

ADENYLATE KINASE; AMINO ACID SEQUENCE; ANIMALS; CARRIER PROTEINS; CLATHRIN-COATED VESICLES; CONSERVED SEQUENCE; ENDOCYTOSIS; GLUCOSE; GLUCOSE TRANSPORTER TYPE 1; HEP G2 CELLS; HUMANS; MICE; MOLECULAR SEQUENCE DATA; PROTEIN TRANSPORT; PROTEOLYSIS; TIME-LAPSE IMAGING;

EID: 84875813063     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.01.035     Document Type: Article

References (51)

1. Abbud W., Habinowski S., Zhang J.Z., Kendrew J., Elkairi F.S., Kemp B.E., Witters L.A., Ismail-Beigi F. Stimulation of AMP-activated protein kinase (AMPK) is associated with enhancement of Glut1-mediated glucose transport. Arch. Biochem. Biophys. 2000, 380:347-352.
2. Alvarez C.E. On the origins of arrestin and rhodopsin. BMC Evol. Biol. 2008, 8:222.
3. Augustin R. The protein family of glucose transport facilitators: It's not only about glucose after all. IUBMB Life 2010, 62:315-333.
4. Baker A.F., Koh M.Y., Williams R.R., James B., Wang H., Tate W.R., Gallegos A., Von Hoff D.D., Han H., Powis G. Identification of thioredoxin-interacting protein 1 as a hypoxia-inducible factor 1alpha-induced gene in pancreatic cancer. Pancreas 2008, 36:178-186.
5. Barnes K., Ingram J.C., Porras O.H., Barros L.F., Hudson E.R., Fryer L.G., Foufelle F., Carling D., Hardie D.G., Baldwin S.A. Activation of GLUT1 by metabolic and osmotic stress: potential involvement of AMP-activated protein kinase (AMPK). J. Cell Sci. 2002, 115:2433-2442.
6. Becuwe M., Vieira N., Lara D., Gomes-Rezende J., Soares-Cunha C., Casal M., Haguenauer-Tsapis R., Vincent O., Paiva S., Léon S. A molecular switch on an arrestin-like protein relays glucose signaling to transporter endocytosis. J. Cell Biol. 2012, 196:247-259.
7. Billiet L., Furman C., Cuaz-Pérolin C., Paumelle R., Raymondjean M., Simmet T., Rouis M. Thioredoxin-1 and its natural inhibitor, vitamin D3 up-regulated protein 1, are differentially regulated by PPARalpha in human macrophages. J. Mol. Biol. 2008, 384:564-576.
8. Blot V., McGraw T.E. Use of quantitative immunofluorescence microscopy to study intracellular trafficking: studies of the GLUT4 glucose transporter. Methods Mol. Biol. 2008, 457:347-366.
9. Bodnar J.S., Chatterjee A., Castellani L.W., Ross D.A., Ohmen J., Cavalcoli J., Wu C., Dains K.M., Catanese J., Chu M., et al. Positional cloning of the combined hyperlipidemia gene Hyplip1. Nat. Genet. 2002, 30:110-116.
10. Cha-Molstad H., Saxena G., Chen J., Shalev A. Glucose-stimulated expression of Txnip is mediated by carbohydrate response element-binding protein, p300, and histone H4 acetylation in pancreatic beta cells. J. Biol. Chem. 2009, 284:16898-16905.
11. Chen K.S., DeLuca H.F. Isolation and characterization of a novel cDNA from HL-60 cells treated with 1,25-dihydroxyvitamin D-3. Biochim. Biophys. Acta 1994, 1219:26-32.
12. Chutkow W.A., Patwari P., Yoshioka J., Lee R.T. Thioredoxin-interacting protein (Txnip) is a critical regulator of hepatic glucose production. J. Biol. Chem. 2008, 283:2397-2406.
13. Draheim K.M., Chen H.B., Tao Q., Moore N., Roche M., Lyle S. ARRDC3 suppresses breast cancer progression by negatively regulating integrin beta4. Oncogene 2010, 29:5032-5047.
14. Eyster C.A., Higginson J.D., Huebner R., Porat-Shliom N., Weigert R., Wu W.W., Shen R.F., Donaldson J.G. Discovery of new cargo proteins that enter cells through clathrin-independent endocytosis. Traffic 2009, 10:590-599.
15. Fryer L.G., Foufelle F., Barnes K., Baldwin S.A., Woods A., Carling D. Characterization of the role of the AMP-activated protein kinase in the stimulation of glucose transport in skeletal muscle cells. Biochem. J. 2002, 363:167-174.
16. Gwinn D.M., Shackelford D.B., Egan D.F., Mihaylova M.M., Mery A., Vasquez D.S., Turk B.E., Shaw R.J. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol. Cell 2008, 30:214-226.
17. Han S.H., Jeon J.H., Ju H.R., Jung U., Kim K.Y., Yoo H.S., Lee Y.H., Song K.S., Hwang H.M., Na Y.S., et al. VDUP1 upregulated by TGF-beta1 and 1,25-dihydorxyvitamin D3 inhibits tumor cell growth by blocking cell-cycle progression. Oncogene 2003, 22:4035-4046.
18. Hardie D.G., Ross F.A., Hawley S.A. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat. Rev. Mol. Cell Biol. 2012, 13:251-262.
19. Hui T.Y., Sheth S.S., Diffley J.M., Potter D.W., Lusis A.J., Attie A.D., Davis R.A. Mice lacking thioredoxin-interacting protein provide evidence linking cellular redox state to appropriate response to nutritional signals. J. Biol. Chem. 2004, 279:24387-24393.
20. Hui S.T., Andres A.M., Miller A.K., Spann N.J., Potter D.W., Post N.M., Chen A.Z., Sachithanantham S., Jung D.Y., Kim J.K., Davis R.A. Txnip balances metabolic and growth signaling via PTEN disulfide reduction. Proc. Natl. Acad. Sci. USA 2008, 105:3921-3926.
21. Ikarashi M., Takahashi Y., Ishii Y., Nagata T., Asai S., Ishikawa K. Vitamin D3 up-regulated protein 1 (VDUP1) expression in gastrointestinal cancer and its relation to stage of disease. Anticancer Res. 2002, 22(6C):4045-4048.
22. Jeon J.H., Lee K.N., Hwang C.Y., Kwon K.S., You K.H., Choi I. Tumor suppressor VDUP1 increases p27(kip1) stability by inhibiting JAB1. Cancer Res. 2005, 65:4485-4489.
23. Junn E., Han S.H., Im J.Y., Yang Y., Cho E.W., Um H.D., Kim D.K., Lee K.W., Han P.L., Rhee S.G., Choi I. Vitamin D3 up-regulated protein 1 mediates oxidative stress via suppressing the thioredoxin function. J. Immunol. 2000, 164:6287-6295.
24. Kawaguchi T., Osatomi K., Yamashita H., Kabashima T., Uyeda K. Mechanism for fatty acid " sparing" effect on glucose-induced transcription: regulation of carbohydrate-responsive element-binding protein by AMP-activated protein kinase. J. Biol. Chem. 2002, 277:3829-3835.
25. Kim K.Y., Shin S.M., Kim J.K., Paik S.G., Yang Y., Choi I. Heat shock factor regulates VDUP1 gene expression. Biochem. Biophys. Res. Commun. 2004, 315:369-375.
26. Lerner A.G., Upton J.P., Praveen P.V., Ghosh R., Nakagawa Y., Igbaria A., Shen S., Nguyen V., Backes B.J., Heiman M., et al. IRE1α induces thioredoxin-interacting protein to activate the NLRP3 inflammasome and promote programmed cell death under irremediable ER stress. Cell Metab. 2012, 16:250-264.
27. MacGurn J.A., Hsu P.C., Smolka M.B., Emr S.D. TORC1 regulates endocytosis via Npr1-mediated phosphoinhibition of a ubiquitin ligase adaptor. Cell 2011, 147:1104-1117.
28. MacGurn J.A., Hsu P.C., Emr S.D. Ubiquitin and membrane protein turnover: from cradle to grave. Annu. Rev. Biochem. 2012, 81:231-259.
29. McGraw T.E., Greenfield L., Maxfield F.R. Functional expression of the human transferrin receptor cDNA in Chinese hamster ovary cells deficient in endogenous transferrin receptor. J. Cell Biol. 1987, 105:207-214.
30. Mihaylova M.M., Shaw R.J. The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat. Cell Biol. 2011, 13:1016-1023.
31. Nabhan J.F., Pan H., Lu Q. Arrestin domain-containing protein 3 recruits the NEDD4 E3 ligase to mediate ubiquitination of the beta2-adrenergic receptor. EMBO Rep. 2010, 11:605-611.
32. Nishinaka Y., Masutani H., Oka S., Matsuo Y., Yamaguchi Y., Nishio K., Ishii Y., Yodoi J. Importin alpha1 (Rch1) mediates nuclear translocation of thioredoxin-binding protein-2/vitamin D(3)-up-regulated protein 1. J. Biol. Chem. 2004, 279:37559-37565.
33. Nishiyama A., Matsui M., Iwata S., Hirota K., Masutani H., Nakamura H., Takagi Y., Sono H., Gon Y., Yodoi J. Identification of thioredoxin-binding protein-2/vitamin D(3) up-regulated protein 1 as a negative regulator of thioredoxin function and expression. J. Biol. Chem. 1999, 274:21645-21650.
34. Oslowski C.M., Hara T., O'Sullivan-Murphy B., Kanekura K., Lu S., Hara M., Ishigaki S., Zhu L.J., Hayashi E., Hui S.T., et al. Thioredoxin-interacting protein mediates ER stress-induced β cell death through initiation of the inflammasome. Cell Metab. 2012, 16:265-273.
35. Parikh H., Carlsson E., Chutkow W.A., Johansson L.E., Storgaard H., Poulsen P., Saxena R., Ladd C., Schulze P.C., Mazzini M.J., et al. TXNIP regulates peripheral glucose metabolism in humans. PLoS Med. 2007, 4:e158.
36. Patwari P., Higgins L.J., Chutkow W.A., Yoshioka J., Lee R.T. The interaction of thioredoxin with Txnip. Evidence for formation of a mixed disulfide by disulfide exchange. J. Biol. Chem. 2006, 281:21884-21891.
37. Reed B.C., Cefalu C., Bellaire B.H., Cardelli J.A., Louis T., Salamon J., Bloecher M.A., Bunn R.C. GLUT1CBP(TIP2/GIPC1) interactions with GLUT1 and myosin VI: evidence supporting an adapter function for GLUT1CBP. Mol. Biol. Cell 2005, 16:4183-4201.
38. Schulze P.C., Yoshioka J., Takahashi T., He Z., King G.L., Lee R.T. Hyperglycemia promotes oxidative stress through inhibition of thioredoxin function by thioredoxin-interacting protein. J. Biol. Chem. 2004, 279:30369-30374.
39. Scott J.W., Norman D.G., Hawley S.A., Kontogiannis L., Hardie D.G. Protein kinase substrate recognition studied using the recombinant catalytic domain of AMP-activated protein kinase and a model substrate. J. Mol. Biol. 2002, 317:309-323.
40. Sheth S.S., Castellani L.W., Chari S., Wagg C., Thipphavong C.K., Bodnar J.S., Tontonoz P., Attie A.D., Lopaschuk G.D., Lusis A.J. Thioredoxin-interacting protein deficiency disrupts the fasting-feeding metabolic transition. J. Lipid Res. 2005, 46:123-134.
41. Sheth S.S., Bodnar J.S., Ghazalpour A., Thipphavong C.K., Tsutsumi S., Tward A.D., Demant P., Kodama T., Aburatani H., Lusis A.J. Hepatocellular carcinoma in Txnip-deficient mice. Oncogene 2006, 25:3528-3536.
42. Stoltzman C.A., Peterson C.W., Breen K.T., Muoio D.M., Billin A.N., Ayer D.E. Glucose sensing by MondoA:Mlx complexes: a role for hexokinases and direct regulation of thioredoxin-interacting protein expression. Proc. Natl. Acad. Sci. USA 2008, 105:6912-6917.
43. Vander Heiden M.G., Cantley L.C., Thompson C.B. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009, 324:1029-1033.
44. Viollet B., Athea Y., Mounier R., Guigas B., Zarrinpashneh E., Horman S., Lantier L., Hebrard S., Devin-Leclerc J., Beauloye C., et al. AMPK: Lessons from transgenic and knockout animals. Front. Biosci. 2009, 14:19-44.
45. Wang Z., Rong Y.P., Malone M.H., Davis M.C., Zhong F., Distelhorst C.W. Thioredoxin-interacting protein (txnip) is a glucocorticoid-regulated primary response gene involved in mediating glucocorticoid-induced apoptosis. Oncogene 2006, 25:1903-1913.
46. Yan G.R., Xu S.H., Tan Z.L., Liu L., He Q.Y. Global identification of miR-373-regulated genes in breast cancer by quantitative proteomics. Proteomics 2011, 11:912-920.
47. Yu F.X., Goh S.R., Dai R.P., Luo Y. Adenosine-containing molecules amplify glucose signaling and enhance txnip expression. Mol. Endocrinol. 2009, 23:932-942.
48. Zeigerer A., McBrayer M.K., McGraw T.E. Insulin stimulation of GLUT4 exocytosis, but not its inhibition of endocytosis, is dependent on RabGAP AS160. Mol. Biol. Cell 2004, 15:4406-4415.
49. Zhang P., Wang C., Gao K., Wang D., Mao J., An J., Xu C., Wu D., Yu H., Liu J.O., Yu L. The ubiquitin ligase itch regulates apoptosis by targeting thioredoxin-interacting protein for ubiquitin-dependent degradation. J. Biol. Chem. 2010, 285:8869-8879.
50. Zhou R., Tardivel A., Thorens B., Choi I., Tschopp J. Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat. Immunol. 2010, 11:136-140.
51. Zhou J., Yu Q., Chng W.J. TXNIP (VDUP-1, TBP-2): a major redox regulator commonly suppressed in cancer by epigenetic mechanisms. Int. J. Biochem. Cell Biol. 2011, 43:1668-1673.