Insulin/insulin-like growth factor (IGF) stimulation abrogates an association between a deubiquitinating enzyme USP7 and insulin receptor substrates (IRSs) followed by proteasomal degradation of IRSs

Biochemical and Biophysical Research Communications

Volumn 423, Issue 1, 2012, Pages 122-127

  Yoshihara, Hidehito ^a   Fukushima, Toshiaki ^a,b   Hakuno, Fumihiko ^a   Saeki, Yasushi ^c   Tanaka, Keiji ^c   Ito, Akihiro ^d   Yoshida, Minoru ^d   Iemura, Shun ichiro ^e   Natsume, Tohru ^e   Asano, Tomoichiro ^b   Chida, Kazuhiro ^a   Girnita, Leonard ^f   Takahashi, Shin Ichiro ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b HIROSHIMA UNIVERSITY   (Japan)

^c TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^d RIKEN   (Japan)

^e NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^f KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

CIAP; Degradation; Deubiquitinating enzyme; DUB; Erk; Grb2; GST; IGF; Insulin; Insulin receptor substrate (IRS); Insulin like growth factor (IGF); IRS; IRSAP; KI; LC MS MS; MATH; MEK; Phosphatidylinositol 3 kinase; PI3K; PMSF; Proteasome; PVDF; SH2; Ubiquitin specific protease 7 (USP7); USP7

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; INSULIN RECEPTOR SUBSTRATE 2; PHOSPHATIDYLINOSITOL 3 KINASE; SOMATOMEDIN C; UBIQUITIN; UBIQUITIN SPECIFIC PROTEASE 7; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CELL FRACTIONATION; CELL NUCLEUS; CELLULAR DISTRIBUTION; CYTOPLASM; ENZYME ACTIVATION; NEGATIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UBIQUITINATION;

HEK293 CELLS; HUMANS; INSULIN; INSULIN RECEPTOR SUBSTRATE PROTEINS; INSULIN-LIKE GROWTH FACTOR I; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STABILITY; PROTEOLYSIS; RNA, SMALL INTERFERING; UBIQUITIN THIOLESTERASE;

EID: 84862696018     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2012.05.093     Document Type: Article

References (31)

1. Taniguchi C.M., Emanuelli B., Kahn C.R. Critical nodes in signalling pathways: insights into insulin action. Nat. Rev. Mol. Cell Biol. 2006, 7:85-96.
2. Jones J.I., Clemmons D.R. Insulin-like growth factors and their binding proteins: biological actions. Endocr. Rev. 1995, 16:3-34.
3. Kido Y., Burks D.J., Withers D., Bruning J.C., Kahn C.R., White M.F., Accili D. Tissue-specific insulin resistance in mice with mutations in the insulin receptor, IRS-1, and IRS-2. J. Clin. Invest. 2000, 105:199-205.
4. Shimomura I., Matsuda M., Hammer R.E., Bashmakov Y., Brown M.S., Goldstein J.L. Decreased IRS-2 and increased SREBP-1c lead to mixed insulin resistance and sensitivity in livers of lipodystrophic and ob/ob mice. Mol. Cell 2000, 6:77-86.
5. Kerouz N.J., Horsch D., Pons S., Kahn C.R. Differential regulation of insulin receptor substrates-1 and -2 (IRS-1 and IRS-2) and phosphatidylinositol 3-kinase isoforms in liver and muscle of the obese diabetic (ob/ob) mouse. J. Clin. Invest. 1997, 100:3164-3172.
6. Rondinone C.M., Wang L.M., Lonnroth P., Wesslau C., Pierce J.H., Smith U. Insulin receptor substrate (IRS) 1 is reduced and IRS-2 is the main docking protein for phosphatidylinositol 3-kinase in adipocytes from subjects with non-insulin-dependent diabetes mellitus. Proc. Natl. Acad. Sci. U S A 1997, 94:4171-4175.
7. Rui L., Yuan M., Frantz D., Shoelson S., White M.F. SOCS-1 and SOCS-3 block insulin signaling by ubiquitin-mediated degradation of IRS1 and IRS2. J. Biol. Chem. 2002, 277:42394-42398.
8. Xu X., Sarikas A., Dias-Santagata D.C., Dolios G., Lafontant P.J., Tsai S.C., Zhu W., Nakajima H., Nakajima H.O., Field L.J., Wang R., Pan Z.Q. The CUL7 E3 ubiquitin ligase targets insulin receptor substrate 1 for ubiquitin-dependent degradation. Mol. Cell 2008, 30:403-414.
9. Nakao R., Hirasaka K., Goto J., Ishidoh K., Yamada C., Ohno A., Okumura Y., Nonaka I., Yasutomo K., Baldwin K.M., Kominami E., Higashibata A., Nagano K., Tanaka K., Yasui N., Mills E.M., Takeda S., Nikawa T. Ubiquitin ligase Cbl-b is a negative regulator for insulin-like growth factor 1 signaling during muscle atrophy caused by unloading. Mol. Cell. Biol. 2009, 29:4798-4811.
10. Shi J., Luo L., Eash J., Ibebunjo C., Glass D.J. The SCF-Fbxo40 complex induces IRS1 ubiquitination in skeletal muscle, limiting IGF1 signaling. Dev. Cell 2011, 21:835-847.
11. Rui L., Fisher T.L., Thomas J., White M.F. Regulation of insulin/insulin-like growth factor-1 signaling by proteasome-mediated degradation of insulin receptor substrate-2. J. Biol. Chem. 2001, 276:40362-40367.
12. Haruta T., Uno T., Kawahara J., Takano A., Egawa K., Sharma P.M., Olefsky J.M., Kobayashi M. A rapamycin-sensitive pathway down-regulates insulin signaling via phosphorylation and proteasomal degradation of insulin receptor substrate-1. Mol. Endocrinol. 2000, 14:783-794.
13. Fukushima T., Arai T., Ariga-Nedachi M., Okajima H., Ooi Y., Iijima Y., Sone M., Cho Y., Ando Y., Kasahara K., Ozoe A., Yoshihara H., Chida K., Okada S., Kopchick J.J., Asano T., Hakuno F., Takahashi S. Insulin receptor substrates form high-molecular-mass complexes that modulate their availability to insulin/insulin-like growth factor-I receptor tyrosine kinases. Biochem. Biophys. Res. Commun. 2011, 404:767-773.
14. Kabuta T., Hakuno F., Asano T., Takahashi S. Insulin receptor substrate-3 functions as transcriptional activator in the nucleus. J. Biol. Chem. 2002, 277:6846-6851.
15. Fukushima T., Nedachi T., Akizawa H., Akahori M., Hakuno F., Takahashi S. Distinct modes of activation of phosphatidylinositol 3-kinase in response to cyclic adenosine 3',5'-monophosphate or insulin-like growth factor I play different roles in regulation of cyclin D1 and p27Kip1 in FRTL-5 cells. Endocrinology 2008, 149:3729-3742.
16. Natsume T., Yamauchi Y., Nakayama H., Shinkawa T., Yanagida M., Takahashi N., Isobe T. A direct nanoflow liquid chromatography-tandem mass spectrometry system for interaction proteomics. Anal. Chem. 2002, 74:4725-4733.
17. Hakuno F., Kurihara S., Watson R.T., Pessin J.E., Takahashi S. 53BP2S, interacting with insulin receptor substrates, modulates insulin signaling. J. Biol. Chem. 2007, 282:37747-37758.
18. Fukushima T., Okajima H., Yamanaka D., Ariga M., Nagata S., Ito A., Yoshida M., Asano T., Chida K., Hakuno F., Takahashi S. HSP90 interacting with IRS-2 is involved in cAMP-dependent potentiation of IGF-I signals in FRTL-5 cells. Mol. Cell. Endocrinol. 2011, 344:81-89.
19. Li M., Chen D., Shiloh A., Luo J., Nikolaev A.Y., Qin J., Gu W. Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilization. Nature 2002, 416:648-653.
20. Briaud I., Dickson L.M., Lingohr M.K., McCuaig J.F., Lawrence J.C., Rhodes C.J. Insulin receptor substrate-2 proteasomal degradation mediated by a mammalian target of rapamycin (mTOR)-induced negative feedback down-regulates protein kinase B-mediated signaling pathway in beta-cells. J. Biol. Chem. 2005, 280:2282-2293.
21. Harrington L.S., Findlay G.M., Lamb R.F. Restraining PI3K: mTOR signalling goes back to the membrane. Trends Biochem. Sci. 2005, 30:35-42.
22. Sowa M.E., Bennett E.J., Gygi S.P., Harper J.W. Defining the human deubiquitinating enzyme interaction landscape. Cell 2009, 138:389-403.
23. Li W., Bengtson M.H., Ulbrich A., Matsuda A., Reddy V.A., Orth A., Chanda S.K., Batalov S., Joazeiro C.A. Genome-wide and functional annotation of human E3 ubiquitin ligases identifies MULAN, a mitochondrial E3 that regulates the organelle's dynamics and signaling. PLoS ONE 2008, 3:e1487.
24. Nicholson B., Suresh Kumar K.G. The multifaceted roles of USP7: new therapeutic opportunities. Cell Biochem. Biophys. 2011, 60:61-68.
25. Li M., Brooks C.L., Kon N., Gu W. A dynamic role of HAUSP in the p53-Mdm2 pathway. Mol. Cell 2004, 13:879-886.
26. Hu M., Gu L., Li M., Jeffrey P.D., Gu W., Shi Y. Structural basis of competitive recognition of p53 and MDM2 by HAUSP/USP7: implications for the regulation of the p53-MDM2 pathway. PLoS Biol. 2006, 4:e27.
27. Hu M., Li P., Li M., Li W., Yao T., Wu J.W., Gu W., Cohen R.E., Shi Y. Crystal structure of a UBP-family deubiquitinating enzyme in isolation and in complex with ubiquitin aldehyde. Cell 2002, 111:1041-1054.
28. Meulmeester E., Pereg Y., Shiloh Y., Jochemsen A.G. ATM-mediated phosphorylations inhibit Mdmx/Mdm2 stabilization by HAUSP in favor of p53 activation. Cell Cycle 2005, 4:1166-1170.
29. Sarkari F., La Delfa A., Arrowsmith C.H., Frappier L., Sheng Y., Saridakis V. Further insight into substrate recognition by USP7: structural and biochemical analysis of the HdmX and Hdm2 interactions with USP7. J. Mol. Biol. 2010, 402:825-837.
30. Takano A., Usui I., Haruta T., Kawahara J., Uno T., Iwata M., Kobayashi M. Mammalian target of rapamycin pathway regulates insulin signaling via subcellular redistribution of insulin receptor substrate 1 and integrates nutritional signals and metabolic signals of insulin. Mol. Cell. Biol. 2001, 21:5050-5062.
31. Toyoshima Y., Tokita R., Ohne Y., Hakuno F., Noguchi T., Minami S., Kato H., Takahashi S.-I. Dietary protein deprivation upregulates insulin signaling and inhibits gluconeogenesis in rat liver. J. Mol. Endocrinol. 2010, 45:329-340.