Direct and indirect control of mitogen-activated protein kinase pathway-associated components, BRAP/IMP E3 ubiquitin ligase and CRAF/RAF1 kinase, by the deubiquitylating enzyme USP15

Journal of Biological Chemistry

Volumn 287, Issue 51, 2012, Pages 43007-43018

  Hayes, Sebastian D ^a,b   Liu, Han ^a   MacDonald, Ewan ^a,c   Sanderson, Christopher M ^a   Coulson, Judy M ^a   Clague, Michael J ^a   Urbé, Sylvie ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b HARVARD MEDICAL SCHOOL   (United States)

^c INSTITUTE OF FOOD RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COILED COIL REGIONS; E3 LIGASE; INACTIVE MUTANTS; INDIRECT CONTROL; LIGASES; MAPK SIGNALING; MITOGEN ACTIVATED PROTEIN KINASE; N-TERMINALS; NEGATIVE REGULATORS; PROTEASOMAL DEGRADATION; SCAFFOLD PROTEIN; SIGNAL AMPLITUDE; UBIQUITIN LIGASES; UBIQUITYLATION;

PROTEINS;

ENZYME ACTIVITY;

BRCA1 ASSOCIATED PROTEIN; ENZYME; EPIDERMAL GROWTH FACTOR; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PLATELET DERIVED GROWTH FACTOR; RAF PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN SPECIFIC PROTEIN 11; UBIQUITIN SPECIFIC PROTEIN 15; UBIQUITIN SPECIFIC PROTEIN 4; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; HELA CELL; MOLECULAR WEIGHT; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; TWO HYBRID SYSTEM; UBIQUITINATION;

BIOCATALYSIS; CELL LINE; ENDOPEPTIDASES; ENZYME ACTIVATION; ENZYME STABILITY; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; PLATELET-DERIVED GROWTH FACTOR; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS C-RAF; RNA, SMALL INTERFERING; TRANSCRIPTION, GENETIC; TWO-HYBRID SYSTEM TECHNIQUES; UBIQUITIN THIOLESTERASE; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84871111938     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.386938     Document Type: Article

References (42)

1. Chiu, Y. H., Zhao, M., and Chen, Z. J. (2009) Ubiquitin in NF-κB signaling. Chem. Rev. 109, 1549-1560
2. Kolch, W. (2005) Coordinating ERK/MAPK signalling through scaffolds and inhibitors. Nat. Rev. Mol. Cell Biol. 6, 827-837
3. Jura, N., Scotto-Lavino, E., Sobczyk, A., and Bar-Sagi, D. (2006) Differential modification of Ras proteins by ubiquitination. Mol. Cell 21, 679-687
4. Xu, L., Lubkov, V., Taylor, L. J., and Bar-Sagi, D. (2010) Feedback regulation of Ras signaling by Rabex-5-mediated ubiquitination. Curr. Biol. 20, 1372-1377
5. Lu, Z., Xu, S., Joazeiro, C., Cobb, M. H., and Hunter, T. (2002) The PHD domain of MEKK1 acts as an E3 ubiquitin ligase and mediates ubiquitination and degradation of ERK1/2. Mol. Cell 9, 945-956
6. Matheny, S. A., Chen, C., Kortum, R. L., Razidlo, G. L., Lewis, R. E., and White, M. A. (2004) Ras regulates assembly of mitogenic signalling complexes through the effector protein IMP. Nature 427, 256-260
7. Chen, C., Lewis, R. E., and White, M. A. (2008) IMP modulates KSR1-dependent multivalent complex formation to specify ERK1/2 pathway activation and response thresholds. J. Biol. Chem. 283, 12789-12796
8. Matheny, S. A., and White, M. A. (2009) Signaling threshold regulation by the Ras effector IMP. J. Biol. Chem. 284, 11007-11011
9. Sowa, M. E., Bennett, E. J., Gygi, S. P., and Harper, J. W. (2009) Defining the human deubiquitinating enzyme interaction landscape. Cell 138, 389-403
10. Ventii, K. H., and Wilkinson, K. D. (2008) Protein partners of deubiquitinating enzymes. Biochem. J. 414, 161-175
11. Sacco, J. J., Coulson, J. M., Clague, M. J., and Urbé, S. (2010) Emerging roles of deubiquitinases in cancer-associated pathways. IUBMB Life 62, 140-157
12. Smith, F. D., and Scott, J. D. (2002) Signaling complexes. Junctions on the intracellular information super highway. Curr. Biol. 12, R32-R40
13. Brooks, C. L., Li, M., Hu, M., Shi, Y., and Gu, W. (2007) The p53-Mdm2-HAUSP complex is involved in p53 stabilization by HAUSP. Oncogene 26, 7262-7266
14. Wertz, I. E., O'Rourke, K. M., Zhou, H., Eby, M., Aravind, L., Seshagiri, S., Wu, P., Wiesmann, C., Baker, R., Boone, D. L., Ma, A., Koonin, E. V., and Dixit, V. M. (2004) De-ubiquitination and ubiquitin ligase domains of A20 down-regulate NF-κB signalling. Nature 430, 694-699
15. Heyninck, K., and Beyaert, R. (2005) A20 inhibits NF-κB activation by dual ubiquitin-editing functions. Trends Biochem. Sci. 30, 1-4
16. Komander, D., Clague, M. J., and Urbé, S. (2009) Breaking the chains. Structure and function of the deubiquitinases. Nat. Rev. Mol. Cell Biol. 10, 550-563
17. Nijman, S. M., Luna-Vargas, M. P., Velds, A., Brummelkamp, T. R., Dirac, A. M., Sixma, T. K., and Bernards, R. (2005) A genomic and functional inventory of deubiquitinating enzymes. Cell 123, 773-786
18. Deshaies, R. J., and Joazeiro, C. A. (2009) RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 78, 399-434
19. Markson, G., Kiel, C., Hyde, R., Brown, S., Charalabous, P., Bremm, A., Semple, J., Woodsmith, J., Duley, S., Salehi-Ashtiani, K., Vidal, M., Komander, D., Serrano, L., Lehner, P., and Sanderson, C. M. (2009) Analysis of the human E2 ubiquitin conjugating enzyme protein interaction network. Genome Res. 19, 1905-1911
20. Ye, Y., Scheel, H., Hofmann, K., and Komander, D. (2009) Dissection of USP catalytic domains reveals five common insertion points. Mol. Biosyst. 5, 1797-1808
21. Faronato, M., Urbé, S., and Coulson, J. C. (2010) USP15 (ubiquitin-specific peptidase 15). Atlas Genet. Cytogenet. Oncol. Hematol. url: http://atlasgeneticsoncology.org/Genes/USP15ID44585ch12q14.html
22. Lehner, B., and Sanderson, C. M. (2004) A protein interaction framework for human mRNA degradation. Genome Res. 14, 1315-1323
23. Asada, M., Ohmi, K., Delia, D., Enosawa, S., Suzuki, S., Yuo, A., Suzuki, H., and Mizutani, S. (2004) Brap2 functions as a cytoplasmic retention protein for p21 during monocyte differentiation. Mol. Cell. Biol. 24, 8236-8243
24. Abramoff, M. D., Magalhaes, P. J., and Ram, S. J. (2004) Image processing with ImageJ. Biophotonics Int. 11, 36-42
25. Winters, B. S., Raj, B. K., Robinson, E. E., Foty, R. A., and Corbett, S. A. (2006) Three-dimensional culture regulates Raf-1 expression to modulate fibronectin matrix assembly. Mol. Biol. Cell 17, 3386-3396
26. Joazeiro, C. A., Wing, S. S., Huang, H., Leverson, J. D., Hunter, T., and Liu, Y. C. (1999) The tyrosine kinase negative regulator c-Cbl as a RING-type, E2-dependent ubiquitin-protein ligase. Science 286, 309-312
27. Zheng, N., Wang, P., Jeffrey, P. D., and Pavletich, N. P. (2000) Structure of a c-Cbl-UbcH7 complex. RING domain function in ubiquitin-protein ligases. Cell 102, 533-539
28. Matheny, S. A., and White, M. A. (2006) Ras-sensitive IMP modulation of the Raf/MEK/ERK cascade through KSR1. Methods Enzymol. 407, 237-247
29. Song, E. J., Werner, S. L., Neubauer, J., Stegmeier, F., Aspden, J., Rio, D., Harper, J. W., Elledge, S. J., Kirschner, M. W., and Rape, M. (2010) The Prp19 complex and the Usp4Sart3 deubiquitinating enzyme control reversible ubiquitination at the spliceosome. Genes Dev. 24, 1434-1447
30. Karasarides, M., Chiloeches, A., Hayward, R., Niculescu-Duvaz, D., Scanlon, I., Friedlos, F., Ogilvie, L., Hedley, D., Martin, J., Marshall, C. J., Springer, C. J., and Marais, R. (2004) B-RAF is a therapeutic target in melanoma. Oncogene 23, 6292-6298
31. Hunter, T. (2007) The age of crosstalk. Phosphorylation, ubiquitination, and beyond. Mol. Cell 28, 730-738
32. Liu, H., Urbé, S., and Clague, M. J. (2012) Selective protein degradation in cell signalling. Semin. Cell Dev. Biol. 23, 509-514
33. de Jong, R. N., Ab, E., Diercks, T., Truffault, V., Daniëls, M., Kaptein, R., and Folkers, G. E. (2006) Solution structure of the human ubiquitin-specific protease 15 DUSP domain. J. Biol. Chem. 281, 5026-5031
34. Elliott, P. R., Liu, H., Pastok, M. W., Grossmann, G. J., Rigden, D. J., Clague, M. J., Urbé, S., and Barsukov, I. L. (2011) Structural variability of the ubiquitin specific protease DUSP-UBL double domains. FEBS Lett. 585, 3385-3390
35. Barretina, J., Caponigro, G., Stransky, N., Venkatesan, K., Margolin, A. A., Kim, S., Wilson, C. J., Lehár, J., Kryukov, G. V., Sonkin, D., Reddy, A., Liu, M., Murray, L., Berger, M. F., Monahan, J. E., Morais, P., Meltzer, J., Korejwa, A., Jané-Valbuena, J., Mapa, F. A., Thibault, J., Bric-Furlong, E., Raman, P., Shipway, A., Engels, I. H., Cheng, J., Yu, G. K., Yu, J., Aspesi, P., Jr., de Silva, M., Jagtap, K., Jones, M. D., Wang, L., Hatton, C., Palescandolo, E., Gupta, S., Mahan, S., Sougnez, C., Onofrio, R. C., Liefeld, T., MacConaill, L., Winckler, W., Reich, M., Li, N., Mesirov, J. P., Gabriel, S. B., Getz, G., Ardlie, K., Chan, V., Myer, V. E., Weber, B. L., Porter, J., Warmuth, M., Finan, P., Harris, J. L., Meyerson, M., Golub, T. R., Morrissey, M. P., Sellers, W. R., Schlegel, R., and Garraway, L. A. (2012) The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 483, 603-617
36. Czyzyk, J., Chen, H. C., Bottomly, K., and Flavell, R. A. (2008) p21 Ras/impedes mitogenic signal propagation regulates cytokine production and migration in CD4 T cells. J. Biol. Chem. 283, 23004-23015
37. Inui, M., Manfrin, A., Mamidi, A., Martello, G., Morsut, L., Soligo, S., Enzo, E., Moro, S., Polo, S., Dupont, S., Cordenonsi, M., and Piccolo, S. (2011) USP15 is a deubiquitylating enzyme for receptor-activated SMADs. Nat. Cell Biol. 13, 1368-1375
38. Beck, T. W., Brennscheidt, U., Sithanandam, G., Cleveland, J., and Rapp, U. R. (1990) Molecular organization of the human Raf-1 promoter region. Mol. Cell. Biol. 10, 3325-3333
39. Dhanasekaran, D. N., Kashef, K., Lee, C. M., Xu, H., and Reddy, E. P. (2007) Scaffold proteins of MAP-kinase modules. Oncogene 26, 3185-3202
40. Lin, J., Harding, A., Giurisato, E., and Shaw, A. S. (2009) KSR1 modulates the sensitivity of mitogen-activated protein kinase pathway activation in T cells without altering fundamental system outputs. Mol. Cell. Biol. 29, 2082-2091
41. Poulikakos, P. I., Zhang, C., Bollag, G., Shokat, K. M., and Rosen, N. (2010) RAF inhibitors transactivate RAF dimers and ERK signalling in cells with wild-type BRAF. Nature 464, 427-430
42. Heidorn, S. J., Milagre, C., Whittaker, S., Nourry, A., Niculescu-Duvas, I., Dhomen, N., Hussain, J., Reis-Filho, J. S., Springer, C. J., Pritchard, C., and Marais, R. (2010) Kinase-dead BRAF and oncogenic RAS cooperate to drive tumor progression through CRAF. Cell 140, 209-221