Global phosphoproteomics identifies a major role for AKT and 14-3-3 in regulating EDC3

Molecular and Cellular Proteomics

Volumn 9, Issue 4, 2010, Pages 682-694

  Larance, Mark ^a,b   Rowland, Alexander F ^a   Hoehn, Kyle L ^a   Humphreys, David T ^c   Preiss, Thomas ^b,c   Guilhaus, Michael ^b   James, David E ^a  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c VICTOR CHANG CARDIAC RESEARCH INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; INSULIN; MESSENGER RNA; PROTEIN KINASE B; SERINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; DOWNSTREAM PROCESSING; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEOMICS; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION;

14-3-3 PROTEINS; ANIMALS; BINDING SITES; CELLS, CULTURED; CHO CELLS; CRICETINAE; CRICETULUS; GENE EXPRESSION REGULATION; HUMANS; MICE; MICRORNAS; NIH 3T3 CELLS; ONCOGENE PROTEIN V-AKT; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN INTERACTION MAPPING; PROTEOMICS; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RNA INTERFERENCE; RNA STABILITY;

MAMMALIA;

EID: 77950664407     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M900435-MCP200     Document Type: Article

References (70)

1. Cohen, P. (2006) Timeline-the twentieth century struggle to decipher insulin signalling. Nat. Rev. Mol. Cell Biol. 7, 867-873
2. Cross, D. A., Alessi, D. R., Cohen, P., Andjelkovich, M., and Hemmings, B. A. (1995) Inhibition of glycogen synthase kinase-3 by insulin-mediated by protein kinase B. Nature 378, 785-789 (Pubitemid 26004411)
3. Rena, G., Guo, S., Cichy, S. C., Unterman, T. G., and Cohen, P. (1999) Phosphorylation of the transcription factor forkhead family member FKHR by protein kinase B. J. Biol. Chem. 274, 17179-17183 (Pubitemid 129519052)
4. Manning, B. D., Tee, A. R., Logsdon, M. N., Blenis, J., and Cantley, L. C. (2002) Identification of the tuberous sclerosis complex-2 tumor suppres- sor gene product tuberin as a target of the phosphoinositide 3-kinase/ Akt pathway. Mol. Cell 10, 151-162 (Pubitemid 34876569)
5. Christ, B., and Nath, A. (1993) The glucagon-insulin antagonism in the regulation of cytosolic protein binding to the 3′ end of phosphoenolpyruvate carboxykinase mRNA in cultured rat hepatocytes-possible involvement in the stabilization of the mRNA. Eur. J. Biochem. 215, 541-547 (Pubitemid 23246822)
6. Flores-Riveros, J. R., McLenithan, J. C., Ezaki, O., and Lane, M. D. (1993) Insulin down-regulates expression of the insulin-responsive glucose transporter (Glut4) gene-effects on transcription and mRNA turnover. Proc. Natl. Acad. Sci. U.S.A. 90, 512-516 (Pubitemid 23028893)
7. O'Brien, R. M., and Granner, D. K. (1996) Regulation of gene expression by insulin. Physiol. Rev. 76, 1109-1161
8. Okubo, M., Villar-Palasi, C., Nagasaka, Y., Larner, J., Larner, A. C., Bai, G., and Lee, E. Y. C. (1991) Long-term effects of insulin on the enzyme activity and messenger RNA of glycogen synthase in rat hepatoma H4 cells-an effect of insulin on glycogen synthase mRNA stability. Arch. Biochem. Biophys. 288, 126-130
9. Woodcroft, K. J., Hafner, M. S., and Novak, R. F. (2002) Insulin signaling in the transcriptional and posttranscriptional regulation of CYP2E1 expression. Hepatology 35, 263-273
10. Lagos-Quintana, M., Rauhut, R., Lendeckel, W., and Tuschl, T. (2001) Identification of novel genes coding for small expressed RNAs. Science 294, 853-858 (Pubitemid 33032103)
11. Lau, N. C., Lim, L. P., Weinstein, E. G., and Bartel, D. P. (2001) An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294, 858-862
12. Lee, R. C., and Ambros, V. (2001) An extensive class of small RNAs in Caenorhabditis elegans. Science 294, 862-864
13. Franks, T. M., and Lykke-Andersen, J. (2008) The control of mRNA decapping and P-body formation. Mol. Cell 32, 605-615
14. Parker, R., and Sheth, U. (2007) P bodies and the control of mRNA translation and degradation. Mol. Cell 25, 635-646 (Pubitemid 46341926)
15. Eulalio, A., Rehwinkel, J., Stricker, M., Huntzinger, E., Yang, S. F., Doerks, T., Dorner, S., Bork, P., Boutros, M., and Izaurralde, E. (2007) Targetspecific requirements for enhancers of decapping in miRNA-mediated gene silencing. Genes Dev. 21, 2558-2570 (Pubitemid 47607667)
16. Fenger-Grøn, M., Fillman, C., Norrild, B., and Lykke-Andersen, J. (2005) Multiple processing body factors and the ARE binding protein TTP activate mRNA decapping. Mol. Cell 20, 905-915 (Pubitemid 41814879)
17. Tritschler, F., Braun, J. E., Eulalio, A., Truffault, V., Izaurralde, E., and Weichenrieder, O. (2009) Structural basis for the mutually exclusive anchoring of P body components EDC3 and Tral to the DEAD box protein DDX6/Me31B. Mol. Cell 33, 661-668
18. Ling, S. H., Decker, C. J., Walsh, M. A., She, M., Parker, R., and Song, H. (2008) Crystal structure of human Edc3 and its functional implications. Mol. Cell. Biol. 28, 5965-5976
19. Rehwinkel, J., Behm-Ansmant, I., Gatfield, D., and Izaurralde, E. (2005) A crucial role for GW182 and the DCP1:DCP2 decapping complex in miRNA-mediated gene silencing. RNA 11, 1640-1647 (Pubitemid 41505538)
20. Manning, B. D., and Cantley, L. C. (2007) AKT/PKB signaling: navigating downstream. Cell 129, 1261-1274
21. Obata, T., Yaffe, M. B., Leparc, G. G., Piro, E. T., Maegawa, H., Kashiwagi, A., Kikkawa, R., and Cantley, L. C. (2000) Peptide and protein library screening defines optimal substrate motifs for AKT/PKB. J. Biol. Chem. 275, 36108-36115
22. Olsen, J. V., Blagoev, B., Gnad, F., Macek, B., Kumar, C., Mortensen, P., and Mann, M. (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648 (Pubitemid 44647421)
23. Ong, S. E., Blagoev, B., Kratchmarova, I., Kristensen, D. B., Steen, H., Pandey, A., and Mann, M. (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 1, 376-386
24. Larance, M., Ramm, G., Stöckli, J., van Dam, E. M., Winata, S., Wasinger, V., Simpson, F., Graham, M., Junutula, J. R., Guilhaus, M., and James, D. E. (2005) Characterization of the role of the Rab GTPase-activating protein AS160 in insulin-regulated GLUT4 trafficking. J. Biol. Chem. 280, 37803-37813 (Pubitemid 41642391)
25. Ridley, A. J., Paterson, H. F., Johnston, C. L., Diekmann, D., and Hall, A. (1992) The small GTP-binding protein Rac regulates growth factor-induced membrane ruffling. Cell 70, 401-410
26. Hoehn, K. L., Hohnen-Behrens, C., Cederberg, A., Wu, L. E., Turner, N., Yuasa, T., Ebina, Y., and James, D. E. (2008) IRS1-independent defects define major nodes of insulin resistance. Cell Metab. 7, 421-433 (Pubitemid 351598028)
27. Ramm, G., Larance, M., Guilhaus, M., and James, D. E. (2006) A role for 14-3-3 in insulin-stimulated GLUT4 translocation through its interaction with the RabGAP AS160. J. Biol. Chem. 281, 29174-29180 (Pubitemid 44507061)
28. Brummer, T., Martin, P., Herzog, S., Misawa, Y., Daly, R. J., and Reth, M. (2006) Functional analysis of the regulatory requirements of B-Raf and the B-Raf(V600E) oncoprotein. Oncogene 25, 6262-6276 (Pubitemid 44564743)
29. Laemmli, U. K. (1970) Cleavage of structural proteins during assembly of head of bacteriophage-T4. Nature 227, 680-685
30. Clancy, J. L., Nousch, M., Humphreys, D. T., Westman, B. J., Beilharz, T. H., and Preiss, T. (2007) Methods to analyze microRNA-mediated control of mRNA translation. Methods Enzymol. 431, 83-111
31. Brummer, T., Larance, M., Herrera Abreu, M. T., Lyons, R. J., Timpson, P., Emmerich, C. H., Fleuren, E. D., Lehrbach, G. M., Schramek, D., Guilhaus, M., James, D. E., and Daly, R. J. (2008) Phosphorylation-dependent binding of 14-3-3 terminates signalling by the Gab2 docking protein. EMBO J. 27, 2305-2316
32. Haas, W., Faherty, B. K., Gerber, S. A., Elias, J. E., Beausoleil, S. A., Bakalarski, C. E., Li, X., Villé n, J., and Gygi, S. P. (2006) Optimization and use of peptide mass measurement accuracy in shotgun proteomics. Mol. Cell. Proteomics 5, 1326-1337
33. Cox, J., and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372
34. 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. (1999) Akt promotes cell survival by phosphorylating and inhibiting a forkhead transcription factor. Cell 96, 857-868 (Pubitemid 29165088)
35. Kovacina, K. S., Park, G. Y., Bae, S. S., Guzzetta, A. W., Schaefer, E., Birnbaum, M. J., and Roth, R. A. (2003) Identification of a proline-rich Akt substrate as a 14-3-3 binding partner. J. Biol. Chem. 278, 10189-10194 (Pubitemid 36800278)
36. Lynch, D. K., and Daly, R. J. (2002) PKB-mediated negative feedback tightly regulates mitogenic signalling via Gab2. EMBO J. 21, 72-82
37. Schmidlin, M., Lu, M., Leuenberger, S. A., Stoecklin, G., Mallaun, M., Gross, B., Gherzi, R., Hess, D., Hemmings, B. A., and Moroni, C. (2004) The ARE-dependent mRNA-destabilizing activity of BRF1 is regulated by protein kinase B. EMBO J. 23, 4760-4769 (Pubitemid 40069706)
38. Obenauer, J. C., Cantley, L. C., and Yaffe, M. B. (2003) Scansite 2.0: Proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res. 31, 3635-3641
39. Puntervoll, P., Linding, R., Gemünd, C., Chabanis-Davidson, S., Mattingsdal, M., Cameron, S., Martin, D. M., Ausiello, G., Brannetti, B., Costantini, A., Ferrè , F., Maselli, V., Via, A., Cesareni, G., Diella, F., Superti-Furga, G., Wyrwicz, L., Ramu, C., McGuigan, C., Gudavalli, R., Letunic, I., Bork, P., Rychlewski, L., Küster, B., Helmer-Citterich, M., Hunter, W. N., Aasland, R., and Gibson, T. J. (2003) ELM server: a new resource for investigating short functional sites in modular eukaryotic proteins. Nucleic Acids Res. 31, 3625-3630
40. Bustos, D. M., and Iglesias, A. A. (2006) Intrinsic disorder is a key characteristic in partners that bind 14-3-3 proteins. Proteins 63, 35-42
41. Linding, R., Russell, R. B., Neduva, V., and Gibson, T. J. (2003) GlobPlot: exploring protein sequences for globularity and disorder. Nucleic Acids Res. 31, 3701-3708 (Pubitemid 37442227)
42. Wang, B., Yang, H., Liu, Y. C., Jelinek, T., Zhang, L., Ruoslahti, E., and Fu, H. (1999) Isolation of high-affinity peptide antagonists of 14-3-3 proteins by phage display. Biochemistry 38, 12499-12504 (Pubitemid 129516221)
43. Mackintosh, C. (2004) Dynamic interactions between 14-3-3 proteins and phosphoproteins regulate diverse cellular processes. Biochem. J. 381, 329-342
44. Yaffe, M. B. (2002) How do 14-3-3 proteins work?-gatekeeper phosphorylation and the molecular anvil hypothesis. FEBS Lett. 513, 53-57
45. Pillai, R. S., Bhattacharyya, S. N., Artus, C. G., Zoller, T., Cougot, N., Basyuk, E., Bertrand, E., and Filipowicz, W. (2005) Inhibition of translational initiation by Let-7 microRNA in human cells. Science 309, 1573-1576 (Pubitemid 41266485)
46. Betel, D., Wilson, M., Gabow, A., Marks, D. S., and Sander, C. (2008) The microRNA.org resource: targets and expression. Nucleic Acids Res. 36, D149-D153
47. Trinkle-Mulcahy, L., Andersen, J., Lam, Y. W., Moorhead, G., Mann, M., and Lamond, A. I. (2006) Repo-Man recruits PP1 gamma to chromatin and is essential for cell viability. J. Cell Biol. 172, 679-692 (Pubitemid 43306225)
48. Brengues, M., and Parker, R. (2007) Accumulation of polyadenylated mRNA, Pab1, eIF4E, and eIF4G with P-bodies in Saccharomyces cerevisiae. Mol. Biol. Cell 18, 2592-2602 (Pubitemid 47025724)
49. Hoyle, N. P., Castelli, L. M., Campbell, S. G., Holmes, L. E., and Ashe, M. P. (2007) Stress-dependent relocalization of translationally primed mRNPs to cytoplasmic granules that are kinetically and spatially distinct from P-bodies. J. Cell Biol. 179, 65-74
50. Liang, X. H., Jackson, S., Seaman, M., Brown, K., Kempkes, B., Hibshoosh, H., and Levine, B. (1999) Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402, 672-676 (Pubitemid 129516338)
51. Bestor, T., Laudano, A., Mattaliano, R., and Ingram, V. (1988) Cloning and sequencing of a cDNA-encoding DNA methyltransferase of mouse cells- the carboxyl-terminal domain of the mammalian enzymes is related to bacterial restriction methyltransferases. J. Mol. Biol. 203, 971-983
52. Park, Y., Yoon, S. K., and Yoon, J. B. (2008) TRIP12 functions as an E3 ubiquitin ligase of APP-BP1. Biochem. Biophys. Res. Commun. 374, 294-298
53. Bartel, D. P. (2009) MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233
54. Filipowicz, W., Bhattacharyya, S. N., and Sonenberg, N. (2008) Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat. Rev. Genet. 9, 102-114
55. Flynt, A. S., and Lai, E. C. (2008) Biological principles of microRNA-mediated regulation: shared themes amid diversity. Nat. Rev. Genet. 9, 831-842
56. Meister, G. (2007) miRNAs get an early start on translational silencing. Cell 131, 25-28
57. Pillai, R. S., Bhattacharyya, S. N., and Filipowicz, W. (2007) Repression of protein synthesis by miRNAs: how many mechanisms? Trends. Cell Biol. 17, 118-126
58. Aebersold, R., and Goodlett, D. R. (2001) Mass spectrometry in proteomics. Chem. Rev. 101, 269-295
59. Mann, M., Ong, S. E., Grønborg, M., Steen, H., Jensen, O. N., and Pandey, A. (2002) Analysis of protein phosphorylation using mass spectrometry: deciphering the phosphoproteome. Trends Biotechnol. 20, 261-268 (Pubitemid 34451062)
60. Eulalio, A., Behm-Ansmant, I., and Izaurralde, E. (2007) P bodies: at the crossroads of post-transcriptional pathways. Nat. Rev. Mol. Cell Biol. 8, 9-22
61. Aizer, A., Brody, Y., Ler, L. W., Sonenberg, N., Singer, R. H., and Shav-Tal, Y. (2008) The dynamics of mammalian P body transport, assembly, and disassembly in vivo. Mol. Biol. Cell 19, 4154-4166
62. Tritschler, F., Eulalio, A., Helms, S., Schmidt, S., Coles, M., Weichenrieder, O., Izaurralde, E., and Truffault, V. (2008) Similar modes of interaction enable trailer hitch and EDC3 to associate with DCP1 and Me31B in distinct protein complexes. Mol. Cell. Biol. 28, 6695-6708
63. Tritschler, F., Eulalio, A., Truffault, V., Hartmann, M. D., Helms, S., Schmidt, S., Coles, M., Izaurralde, E., and Weichenrieder, O. (2007) A divergent Sm fold in EDC3 proteins mediates DCPI binding and P-body targeting. Mol. Cell. Biol. 27, 8600-8611
64. Benjamin, D., Schmidlin, M., Min, L., Gross, B., and Moroni, C. (2006) BRF1 protein turnover and mRNA decay activity are regulated by protein kinase B at the same phosphorylation sites. Mol. Cell. Biol. 26, 9497-9507 (Pubitemid 44904441)
65. Marderosian, M., Sharma, A., Funk, A. P., Vartanian, R., Masri, J., Jo, O. D., and Gera, J. F. (2006) Tristetraprolin regulates Cyclin D1 and c-myc mRNA stability in response to rapamycin in an Akt-dependent manner via p38 MAPK signaling. Oncogene 25, 6277-6290 (Pubitemid 44564744)
66. Chu, C. Y., and Rana, T. M. (2006) Translation repression in human cells by microRNA-induced gene silencing requires RCK/p54. PLoS Biol. 4, e210
67. Stalder, L., and Mühlemann, O. (2009) Processing bodies are not required for mammalian nonsense-mediated mRNA decay. RNA 15, 1265-1273
68. Decker, C. J., Teixeira, D., and Parker, R. (2007) Edc3p and a glutamine/asparagine-rich domain of Lsm4p function in processing body assembly in Saccharomyces cerevisiae. J. Cell Biol. 179, 437-449 (Pubitemid 350074789)
69. Eulalio, A., Behm-Ansmant, I., Schweizer, D., and Izaurralde, E. (2007) P-body formation is a consequence, not the cause, of RNA-mediated gene silencing. Mol. Cell. Biol. 27, 3970-3981 (Pubitemid 47010995)
70. Stoecklin, G., Mayo, T., and Anderson, P. (2006) ARE-mRNA degradation requires the 5′-3′ decay pathway. EMBO Rep. 7, 72-77