Phosphorylation and degradation of S6K1 (p70S6K1) in response to persistent JNK1 Activation

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1832, Issue 12, 2013, Pages 1980-1988

  Zhang, Jin ^a   Gao, Zhanguo ^a   Ye, Jianping ^a  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

Author keywords

Inflammation; Insulin resistance; Liver; Obesity; TNF

Indexed keywords

I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 1; PROTEASOME; S6 KINASE; STRESS ACTIVATED PROTEIN KINASE 1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; IMMUNOPRECIPITATION; MALE; MOUSE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN STABILITY; UBIQUITINATION; WESTERN BLOTTING;

EID: 84882790100     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2013.06.013     Document Type: Article

References (31)

1. Um S.H., D'Alessio D., Thomas G. Nutrient overload, insulin resistance, and ribosomal protein S6 kinase 1, S6K1. Cell Metab. 2006, 3:393-402.
2. Magnuson B., Ekim B., Fingar D.C. Regulation and function of ribosomal protein S6 kinase (S6K) within mTOR signalling networks. Biochem. J. 2012, 441:1-21.
3. Carlson C.J., White M.F., Rondinone C.M. Mammalian target of rapamycin regulates IRS-1 serine 307 phosphorylation. Biochem. Biophys. Res. Commun. 2004, 316:533-539.
4. Harrington L.S., Findlay G.M., Gray A., Tolkacheva T., Wigfield S., Rebholz H., Barnett J., Leslie N.R., Cheng S., Shepherd P.R., Gout I., Downes C.P., Lamb R.F. The TSC1-2 tumor suppressor controls insulin-PI3K signaling via regulation of IRS proteins. J. Cell Biol. 2004, 166:213-223.
5. Ozes O.N., Akca H., Mayo L.D., Gustin J.A., Maehama T., Dixon J.E., Donner D.B. A phosphatidylinositol 3-kinase/Akt/mTOR pathway mediates and PTEN antagonizes tumor necrosis factor inhibition of insulin signaling through insulin receptor substrate-1. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:4640-4645.
6. Tremblay F., Brule S., Hee Um S., Li Y., Masuda K., Roden M., Sun X.J., Krebs M., Polakiewicz R.D., Thomas G., Marette A. Identification of IRS-1 Ser-1101 as a target of S6K1 in nutrient- and obesity-induced insulin resistance. PNAS 2007, 104:14056-14061.
7. Zhang J., Gao Z., Yin J., Quon M.J., Ye J. S6K directly phosphorylates IRS-1 on Ser-270 to promote insulin resistance in response to TNF-α signaling through IKK2. J. Biol. Chem. 2008, 283:35375-35382.
8. Um S.H., Frigerio F., Watanabe M., Picard F., Joaquin M., Sticker M., Fumagalli S., Allegrini P.R., Kozma S.C., Auwerx J., Thomas G. Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity. Nature 2004, 431:200-205.
9. Lee D.-F., Kuo H.-P., Chen C.-T., Hsu J.-M., Chou C.-K., Wei Y., Sun H.-L., Li L.-Y., Ping B., Huang W.-C., He X., Hung J.-Y., Lai C.-C., Ding Q., Su J.-L., Yang J.-Y., Sahin A.A., Hortobagyi G.N., Tsai F.-J., Tsai C.-H., Hung M.-C. IKK[beta] suppression of TSC1 links inflammation and tumor angiogenesis via the mTOR pathway. Cell 2007, 130:440-455.
10. Gao Z., Yin J., Zhang J., He Q., McGuinness O.P., Ye J. Inactivation of NF-kappaB p50 leads to insulin sensitization in liver through post-translational inhibition of p70S6K. J. Biol. Chem. 2009, 284:18368-18376.
11. Dennis P.B., Pullen N., Pearson R.B., Kozma S.C., Thomas G. Phosphorylation sites in the autoinhibitory domain participate in p70(s6k) activation loop phosphorylation. J. Biol. Chem. 1998, 273:14845-14852.
12. Frodin M., Antal T.L., Dummler B.A., Jensen C.J., Deak M., Gammeltoft S., Biondi R.M. A phosphoserine/threonine-binding pocket in AGC kinases and PDK1 mediates activation by hydrophobic motif phosphorylation. EMBO J. 2002, 21:5396-5407.
13. Pullen N., Dennis P.B., Andjelkovic M., Dufner A., Kozma S.C., Hemmings B.A., Thomas G. Phosphorylation and activation of p70s6k by PDK1. Science 1998, 279:707-710.
14. Price D.J., Mukhopadhyay N.K., Avruch J. Insulin-activated protein kinases phosphorylate a pseudosubstrate synthetic peptide inhibitor of the p70 S6 kinase. J. Biol. Chem. 1991, 266:16281-16284.
15. Lehman J.A., Calvo V., Gomez-Cambronero J. Mechanism of ribosomal p70S6 kinase activation by granulocyte macrophage colony-stimulating factor in neutrophils: cooperation of a MEK-related, THR421/SER424 kinase and a rapamycin-sensitive, m-TOR-related THR389 kinase. J. Biol. Chem. 2003, 278:28130-28138.
16. Papst P.J., Sugiyama H., Nagasawa M., Lucas J.J., Maller J.L., Terada N. Cdc2-cyclin B phosphorylates p70 S6 kinase on Ser411 at mitosis. J. Biol. Chem. 1998, 273:15077-15084.
17. Isotani S., Hara K., Tokunaga C., Inoue H., Avruch J., Yonezawa K. Immunopurified mammalian target of rapamycin phosphorylates and activates p70 S6 kinase alpha in vitro. J. Biol. Chem. 1999, 274:34493-34498.
18. Alessi D.R., Kozlowski M.T., Weng Q.P., Morrice N., Avruch J. 3-Phosphoinositide-dependent protein kinase 1 (PDK1) phosphorylates and activates the p70 S6 kinase in vivo and in vitro. Curr. Biol. 1998, 8:69-81.
19. Thomas G. The S6 kinase signaling pathway in the control of development and growth. Biol. Res. 2002, 35:305-313.
20. Gwalter J., Wang M.L., Gout I. The ubiquitination of ribosomal S6 kinases is independent from the mitogen-induced phosphorylation/activation of the kinase. Int. J. Biochem. Cell Biol. 2009, 41:828-833.
21. Wang M.L., Panasyuk G., Gwalter J., Nemazanyy I., Fenton T., Filonenko V., Gout I. Regulation of ribosomal protein S6 kinases by ubiquitination. Biochem. Biophys. Res. Commun. 2008, 369:382-387.
22. Gao Z., Hwang D., Bataille F., Lefevre M., York D., Quon M.J., Ye J. Serine phosphorylation of insulin receptor substrate 1 by inhibitor KappaB kinase complex. J. Biol. Chem. 2002, 277:48115-48121.
23. Schalm S.S., Blenis J. Identification of a conserved motif required for mTOR signaling. Curr. Biol. 2002, 12:632-639.
24. Xu G., Marshall C.A., Lin T.A., Kwon G., Munivenkatappa R.B., Hill J.R., Lawrence J.C., McDaniel M.L. Insulin mediates glucose-stimulated phosphorylation of PHAS-I by pancreatic beta cells. An insulin-receptor mechanism for autoregulation of protein synthesis by translation. J. Biol. Chem. 1998, 273:4485-4491.
25. Iiboshi Y., Papst P.J., Kawasome H., Hosoi H., Abraham R.T., Houghton P.J., Terada N. Amino acid-dependent control of p70(s6k). Involvement of tRNA aminoacylation in the regulation. J. Biol. Chem. 1999, 274:1092-1099.
26. Gao Z., Yin J., Z.J., He Q., McGuinness O.P., Ye J. Inactivation of NF-κB p50 leads to insulin sensitization in liver through post-translational inhibition of p70S6K. J. Biol. Chem. 2009, 284:18368-18376.
27. Mukhopadhyay N.K., Price D.J., Kyriakis J.M., Pelech S., Sanghera J., Avruch J. An array of insulin-activated, proline-directed serine/threonine protein kinases phosphorylate the p70 S6 kinase. J. Biol. Chem. 1992, 267:3325-3335.
28. Ferrari S., Bannwarth W., Morley S.J., Totty N.F., Thomas G. Activation of p70s6k is associated with phosphorylation of four clustered sites displaying Ser/Thr-Pro motifs. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:7282-7286.
29. Banerjee P., Ahmad M.F., Grove J.R., Kozlosky C., Price D.J., Avruch J. Molecular structure of a major insulin/mitogen-activated 70-kDaS6 protein kinase. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:8550-8554.
30. Han J.W., Pearson R.B., Dennis P.B., Thomas G. Rapamycin, wortmannin, and the methylxanthine SQ20006 inactivate p70s6k by inducing dephosphorylation of the same subset of sites. J. Biol. Chem. 1995, 270:21396-21403.
31. Ferrari S., Pearson R.B., Siegmann M., Kozma S.C., Thomas G. The immunosuppressant rapamycin induces inactivation of p70s6k through dephosphorylation of a novel set of sites. J. Biol. Chem. 1993, 268:16091-16094.