Identification of the tyrosine phosphatase PTP-MEG2 as an antagonist of hepatic insulin signaling

Cell Metabolism

Volumn 3, Issue 5, 2006, Pages 367-378

  Cho, Charles Y ^a,b   Koo, Seung Hoi ^c,d   Wang, Yan ^a   Callaway, Scott ^e   Hedrick, Susan ^c   Mak, Puiying A ^a   Orth, Anthony P ^a   Peters, Eric C ^a   Saez, Enrique ^a   Montminy, Marc ^c   Schultz, Peter G ^a,b   Chanda, Sumit K ^a  

^a GENOMICS INSTITUTE OF THE NOVARTIS RESEARCH FOUNDATION   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^d Sungkyunkwan University School of Medicine   (South Korea)

^e VALA SCIENCES INC   (United States)

Author keywords

SIGNALING

Indexed keywords

GLUCOSE; INSULIN; INSULIN RECEPTOR; PROTEIN TYROSINE PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE MEG2; RNA; TRANSCRIPTION FACTOR FKHR; UNCLASSIFIED DRUG;

ADENOVIRUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DIABETES MELLITUS; ENZYME ACTIVITY; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; HUMAN; HUMAN CELL; HYPERGLYCEMIA; INSULIN SENSITIVITY; LIVER CELL; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ANIMALS; BLOOD GLUCOSE; CELL LINE, TUMOR; DIABETES MELLITUS, TYPE 2; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; GLUCOSE-6-PHOSPHATASE; GREEN FLUORESCENT PROTEINS; HEPATOCYTES; HUMANS; INSULIN; INSULIN RESISTANCE; LIVER; MALE; MICE; PROMOTER REGIONS (GENETICS); PROMOTER REGIONS, GENETIC; PROTEIN TYROSINE PHOSPHATASES; PROTEIN TYROSINE PHOSPHATASES, NON-RECEPTOR; PROTEIN-TYROSINE-PHOSPHATASE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, INSULIN; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 33748331432     PISSN: 15504131     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cmet.2006.03.006     Document Type: Article

References (40)

1. Accili D., and Arden K. FoxOs at the crossroads of cellular metabolism, differentiation, and transformation. Cell 117 (2004) 421-426
2. Alonso A., Sasin J., Bottini N., Friedberg I., Friedberg I., Osterman A., Godzik A., Hunter T., Dixon J., and Mustelin T. Protein tyrosine phosphatases in the human genome. Cell 117 (2004) 699-711
3. Altomonte J., Richter A., Harbaran S., Suriawinata J., Nakae J., Thung S.N., Meseck M., Accili D., and Dong H. Inhibition of Foxo1 function is associated with improved fasting glycemia in diabetic mice. Am. J. Physiol. Endocrinol. Metab. 285 (2003) E718-E728
4. Altomonte J., Cong L., Harbaran S., Richter A., Xu J., Meseck M., and Dong H.H. Foxo1 mediates insulin action on apoC-III and triglyceride metabolism. J. Clin. Invest. 114 (2004) 1493-1503
5. Asante-Appiah E., and Kennedy B.P. Protein tyrosine phosphatases: the quest for negative regulators of insulin action. Am. J. Physiol. Endocrinol. Metab. 284 (2003) E663-E670
6. Ayala J.E., Streeper R.S., Desgrosellier J.S., Durham S.K., Suwanichkul A., Svitek C.A., Goldman J.K., Barr F.G., Powell D.R., and O'Brien R.M. Conservation of an insulin response unit between mouse and human glucose-6-phosphatase catalytic subunit gene promoters: transcription factor FKHR binds the insulin response sequence. Diabetes 48 (1999) 1885-1889
7. Barthel A., and Schmoll D. Novel concepts in insulin regulation of hepatic gluconeogenesis. Am. J. Physiol. Endocrinol. Metab. 285 (2003) E685-E692
8. Barthel A., Schmoll D., and Unterman T.G. FoxO proteins in insulin action and metabolism. Trends Endocrinol. Metab. 16 (2005) 183-189
9. Brown R.A., Domin J., Arcaro A., Waterfield M.D., and Shepherd P.R. Insulin activates the alpha isoform of class II phosphoinositide 3 kinase. J. Biol. Chem. 274 (1999) 14529-14532
10. Brunet A., Bonni A., Zigmond M.J., Lin M.Z., Juo P., Hu L.S., Anderson M.J., Arden K.C., Blenis J., and Greenberg M.E. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96 (1999) 857-868
11. Brunet A., Park J., Tran H., Hu L.S., Hemmings B.A., and Greenberg M.E. Protein kinase SGK mediates survival signals by phosphorylating the forkhead transcription factor FKHRL1 (FOXO3a). Mol. Cell. Biol. 21 (2001) 952-965
12. Brunet A., Sweeney L.B., Sturgill J.F., Chua K.F., Greer P.L., Lin Y., Tran H., Ross S.E., Mostoslavsky R., Cohen H.Y., et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303 (2004) 2011-2015
13. Chanda S.K., White S., Orth A.P., Reisdorph R., Miraglia L., Thomas R.S., DeJesus P., Mason D.E., Huang Q., Vega R., et al. Genome-scale functional profiling of the mammalian AP-1 signaling pathway. Proc. Natl. Acad. Sci. USA 100 (2003) 12153-12158
14. Cho H., Mu J., Kim J.K., Thorvaldsen J.L., Chu Q., Crenshaw III E.B., Kaestner K.H., Bartolomei M.S., Shulman G.I., and Birnbaum M.J. Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB beta). Science 292 (2001) 1728-1731
15. Du K., Herzig S., Kulkarni R.N., and Montminy M. TRB3: a tribbles homolog that inhibits Akt/PKB activation by insulin in liver. Science 300 (2003) 1574-1577
16. Elchebly M., Payette P., Michaliszyn E., Cromlish W., Collins S., Loy A.L., Normandin D., Cheng A., Himms-Hagen J., Chan C.C., et al. Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B gene. Science 283 (1999) 1544-1548
17. Ellis L., Clauser E., Morgan D.O., Edery M., Roth R.A., and Rutter W.J. Replacement of insulin receptor tyrosine residues 1162 and 1163 compromises insulin-stimulated kinase activity and uptake of 2-deoxyglucose. Cell 45 (1986) 721-732
18. Galic S., Klingler-Hoffmann M., Fodero-Tavoletti M.T., Puryer M.A., Meng T.C., Tonks N.K., and Tiganis T. Regulation of insulin receptor signaling by the protein tyrosine phosphatase TCPTP. Mol. Cell. Biol. 23 (2003) 2096-2108
19. Galic S., Hauser C., Kahn B.B., Haj F.G., Neel B.G., Tonks N.K., and Tiganis T. Coordinated regulation of insulin signaling by the protein tyrosine phosphatases PTP1B and TCPTP. Mol. Cell. Biol. 25 (2005) 819-829
20. Haj F.G., Verveer P.J., Squire A., Neel B.G., and Bastiaens P.I. Imaging sites of receptor dephosphorylation by PTP1B on the surface of the endoplasmic reticulum. Science 295 (2002) 1708-1711
21. Harada J.N., Bower K.E., Orth A.P., Callaway S., Nelson C.G., Laris C., Hogenesch J.B., Vogt P.K., and Chanda S.K. Identification of novel mammalian growth regulatory factors by genome scale quantitative image analysis. Genome Res. 15 (2005) 1136-1144
22. Huynh H., Wang X., Li W., Bottini N., Williams S., Nika K., Ishihara H., Godzik A., and Mustelin T. Homotypic secretory vesicle fusion induced by the protein tyrosine phosphatase MEG2 depends on polyphosphoinositides in T cells. J. Immunol. 171 (2003) 6661-6671
23. Huynh H., Bottini N., Williams S., Cherepanov V., Musumeci L., Saito K., Bruckner S., Vachon E., Wang X., Kruger J., et al. Control of vesicle fusion by a tyrosine phosphatase. Nat. Cell Biol. 6 (2004) 831-839
24. Klaman L.D., Boss O., Peroni O.D., Kim J.K., Martino J.L., Zabolotny J.M., Moghal N., Lubkin M., Kim Y.B., Sharpe A.H., et al. Increased energy expenditure, decreased adiposity, and tissue-specific insulin sensitivity in protein-tyrosine phosphatase 1B-deficient mice. Mol. Cell. Biol. 20 (2000) 5479-5489
25. Koo S.H., Satoh H., Herzig S., Lee C.H., Hedrick S., Kulkarni R., Evans R.M., Olefsky J., and Montminy M. PGC-1 promotes insulin resistance in liver through PPAR-alpha-dependent induction of TRB-3. Nat. Med. 10 (2004) 530-534
26. Kruger J.M., Fukushima T., Cherepanov V., Borregaard N., Loeve C., Shek C., Sharma K., Tanswell A.K., Chow C.W., and Downey G.P. Protein-tyrosine phosphatase MEG2 is expressed by human neutrophils. Localization to the phagosome and activation by polyphosphoinositides. J. Biol. Chem. 277 (2002) 2620-2628
27. Motta M.C., Divecha N., Lemieux M., Kamel C., Chen D., Gu W., Bultsma Y., McBurney M., and Guarente L. Mammalian SIRT1 represses forkhead transcription factors. Cell 116 (2004) 551-563
28. Nakae J., Biggs III W.H., Kitamura T., Cavenee W.K., Wright C.V., Arden K.C., and Accili D. Regulation of insulin action and pancreatic beta-cell function by mutated alleles of the gene encoding forkhead transcription factor Foxo1. Nat. Genet. 32 (2002) 245-253
29. Nakamura N., Ramaswamy S., Vazquez F., Signoretti S., Loda M., and Sellers W.R. Forkhead transcription factors are critical effectors of cell death and cell cycle arrest downstream of PTEN. Mol. Cell. Biol. 20 (2000) 8969-8982
30. Puigserver P., Rhee J., Donovan J., Walkey C.J., Yoon J.C., Oriente F., Kitamura Y., Altomonte J., Dong H., Accili D., and Spiegelman B.M. Insulin-regulated hepatic gluconeogenesis through FOXO1-PGC-1alpha interaction. Nature 423 (2003) 550-555
31. Ren J.M., Li P.M., Zhang W.R., Sweet L.J., Cline G., Shulman G.I., Livingston J.N., and Goldstein B.J. Transgenic mice deficient in the LAR protein-tyrosine phosphatase exhibit profound defects in glucose homeostasis. Diabetes 47 (1998) 493-497
32. Salomon A.R., Ficarro S.B., Brill L.M., Brinker A., Phung Q.T., Ericson C., Sauer K., Brock A., Horn D.M., Schultz P.G., and Peters E.C. Profiling of tyrosine phosphorylation pathways in human cells using mass spectrometry. Proc. Natl. Acad. Sci. USA 100 (2003) 443-448
33. Strausberg R.L., Feingold E.A., Klausner R.D., and Collins F.S. The mammalian gene collection. Science 286 (1999) 455-457
34. Su A.I., Wiltshire T., Batalov S., Lapp H., Ching K.A., Block D., Zhang J., Soden R., Hayakawa M., Kreiman G., Cooke M.P., Walker J.R., and Hogenesch J.B. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc. Natl. Acad. Sci. USA 101 (2004) 6062-6067
35. Ueki K., Yballe C.M., Brachmann S.M., Vicent D., Watt J.M., Kahn C.R., and Cantley L.C. Increased insulin sensitivity in mice lacking p85beta subunit of phosphoinositide 3-kinase. Proc. Natl. Acad. Sci. USA 99 (2002) 419-424
36. Wang X., Huynh H., Gjorloff-Wingren A., Monosov E., Stridsberg M., Fukuda M., and Mustelin T. Enlargement of secretory vesicles by protein tyrosine phosphatase PTP-MEG2 in rat basophilic leukemia mast cells and Jurkat T cells. J. Immunol. 168 (2002) 4612-4619
37. Wang Y., Vachon E., Zhang J., Cherepanov V., Kruger J., Li J., Saito K., Shannon P., Bottini N., Huynh H., et al. Tyrosine phosphatase MEG2 modulates murine development and platelet and lymphocyte activation through secretory vesicle function. J. Exp. Med. 202 (2005) 1587-1597
38. White M.F. Insulin signaling in health and disease. Science 302 (2003) 1710-1711
39. Zabolotny J.M., Kim Y.B., Peroni O.D., Kim J.K., Pani M.A., Boss O., Klaman L.D., Kamatkar S., Shulman G.I., Kahn B.B., and Neel B.G. Overexpression of the LAR (leukocyte antigen-related) protein-tyrosine phosphatase in muscle causes insulin resistance. Proc. Natl. Acad. Sci. USA 98 (2001) 5187-5192
40. Zhao R., Fu X., Li Q., Krantz S.B., and Zhao Z.J. Specific interaction of protein tyrosine phosphatase-MEG2 with phosphatidylserine. J. Biol. Chem. 278 (2003) 22609-22614