Extracellular signal-regulated kinases phosphorylate mitogen-activated protein kinase phosphatase 3/DUSP6 at serines 159 and 197, two sites critical for its proteasomal degradation

Molecular and Cellular Biology

Volumn 25, Issue 2, 2005, Pages 854-864

  Marchetti, Sandrine ^a,b   Gimond, Clotilde ^a   Chambard, Jean Claude ^a   Touboul, Thomas ^a   Roux, Danièle ^a   Pouysségur, Jacques ^a   Pagès, Gilles ^a  

^a CENTRE ANTOINE LACASSAGNE   (France)

^b INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE TRANSFERASE; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 3; PROTEASOME; PROTEIN TYROSINE PHOSPHATASE; SERINE; TETRACYCLINE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL CLONE; CHIMERA; CONTROLLED STUDY; ENZYME DEGRADATION; ENZYME INACTIVATION; ENZYME STABILITY; FIBROBLAST; HALF LIFE TIME; HAMSTER; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION;

ANIMALS; CELL LINE; ENZYME STABILITY; MAP KINASE KINASE 1; MAP KINASE KINASE 2; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN-TYROSINE-PHOSPHATASE; RECOMBINANT FUSION PROTEINS; SERINE; SIGNAL TRANSDUCTION;

ANIMALIA; CRICETINAE; TRIXIS;

EID: 11844294679     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.2.854-864.2005     Document Type: Article

References (42)

1. Alessi, D. R., N. Gomez, G. Moorhead, T. Lewis, S. M. Keyse, and P. Cohen. 1995. Inactivation of p42 MAP kinase by protein phosphatase 2A and a protein tyrosine phosphatase, but not CL100, in various cell lines. Curr. Biol. 5:283-295.
2. Breitschopf, K., J. Haendeler, P. Malchow, A. M. Zeiher, and S. Dimmeler. 2000. Posttranslational modification of Bcl-2 facilitates its proteasome-dependent degradation: molecular characterization of the involved signaling pathway. Mol. Cell. Biol. 20:1886-1896.
3. Brondello, J. M., J. Pouyssegur, and F. R. McKenzie. 1999. Reduced MAP kinase phosphatase-1 degradation after p42/p44MAPK-dependent phosphorylation. Science 286:2514-2517.
4. Brunet, A., D. Roux, P. Lenormand, S. Dowd, S. Keyse, and J. Pouyssegur. 1999. Nuclear translocation of p42/p44 mitogen-activated protein kinase is required for growth factor-induced gene expression and cell cycle entry. EMBO J. 18:664-674.
5. Camps, M., C. Chabert, M. Muda, U. Beschert, C. Gillieron, and S. Arkinstall. 1998. Induction of the mitogen-activated protein kinase phosphatase MKP3 by nerve growth factor in differentiating PC12. FEES Lett. 425:271-276.
6. Camps, M., A. Nichols, and S. Arkinstall. 2000. Dual specificity phosphatases: a gene family for control of MAP kinase function. FASEB J. 14:6-16.
7. Camps, M., A. Nichols, C. Gillieron, B. Antonsson, M. Muda, C. Chabert, U. Beschert, and S. Arkinstall. 1998. Catalytic activation of the phosphatase MKP-3 by ERK2 mitogen-activated protein kinase. Science 280:1262-1265.
8. Dorfman, K., D. Carrasco, M. Gruda, C. Ryan, S. A. Lira, and R. Bravo. 1996. Disruption of the erp/mkp-1 gene does not affect mouse development: normal MAP kinase activity in ERP/MKP-1-deficient fibroblasts. Oncogene 13:925-931.
9. Doye, A., A. Mettouchi, G. Bossis, R. Clement, C. Buisson-Touati, G. Flatau, L. Gagnoux, M. Piechaczyk, P. Boquet, and E. Lemichez. 2002. CNF1 exploits the ubiquitin-proteasome machinery to restrict Rho GTPase activation for bacterial host cell invasion. Cell 111:553-564.
10. Eblaghie, M. C., J. S. Lunn, R. J. Dickinson, A. E. Munsterberg, J. J. Sanz-Ezquerro, E. R. Farrell, J. Mathers, S. M. Keyse, K. Storey, and C. Tickle. 2003. Negative feedback regulation of FGF signaling levels by Pyst1/ MKP3 in chick embryos. Curr. Biol. 13:1009-1018.
11. Farooq, A., G. Chaturvedi, S. Mujtaba, O. Plotnikova, L. Zeng, C. Dhalluin, R. Ashton, and M. M. Zhou. 2001. Solution structure of ERK2 binding domain of MAPK phosphatase MKP-3: structural insights into MKP-3 activation by ERK2. Mol. Cell 7:387-399.
12. Fjeld, C. C., A. E. Rice, Y. Kim, K. R. Gee, and J. M. Denu. 2000. Mechanistic basis for catalytic activation of mitogen-activated protein kinase phosphatase 3 by extracellular signal-regulated kinase. J. Biol. Chem. 275:6749-6757.
13. Groom, L. A., A. A. Sneddon, D. R. Alessi, S. Dowd, and S. M. Keyse. 1996. Differential regulation of the MAP, SAP and RK/p38 kinases by Pyst1, a novel cytosolic dual-specificity phosphatase. EMBO J. 15:3621-3632.
14. Kamakura, S., T. Moriguchi, and E. Nishida. 1999. Activation of the protein kinase ERK5/BMK1 by receptor tyrosine kinases. Identification and characterization of a signaling pathway to the nucleus. J. Biol. Chem. 274:26563-26571.
15. Karihaloo, A., D. A. O'Rourke, C. Nickel, K. Spokes, and L. G. Cantley, 2001. Differential MAPK pathways utilized for HGF- and EGF-dependent renal epithelial morphogenesis. J. Biol. Chem. 276:9166-9173.
16. Kato, Y., V. V. Kravchenko, R. I. Tapping, J. Han, R. J. Ulevitch, and J. D. Lee. 1997. BMK1/ERK5 regulates serum-induced early gene expression through transcription factor MEF2C. EMBO J. 16:7054-7066.
17. Kawakami, Y., J. Rodriguez-Leon, C. M. Koth, D. Buscher, T. Itoh, A. Raya, J. K. Ng, C. R. Esteban, S. Takahashi, D. Henrique, M. F. Schwarz, H. Asahara, and J. C. Izpisua Belmonte. 2003. MKP3 mediates the cellular response to FGF8 signalling in the vertebrate limb. Nat. Cell Biol. 5:513-519.
18. Keyse, S. M. 2000. Protein phosphatases and the regulation of mitogen-activated protein kinase signalling. Curr. Opin. Cell Biol. 12:186-192.
19. Kim, M., G.-H. Cha, S. Kim, J. H. Lee, J. Park, H. Koh, K.-Y. Choi, and J. Chung. 2004. MKP-3 has essential roles as a negative regulator of the Ras/mitogen-activated protein kinase pathway during Drosophila development. Mol. Cell. Biol. 24:573-583.
20. Le Gall, M., J. C. Chambard, J. P. Breittmayer, D. Grall, J. Pouyssegur, and E. Van Obberghen-Schilling. 2000. The p42/p44 MAP kinase pathway prevents apoptosis induced by anchorage and serum removal. Mol. Biol. Cell 11:1103-1112.
21. Lenormand, P., M. McMahon, and J. Pouyssegur. 1996. Oncogenic Raf-1 activates p70 S6 kinase via a mitogen-activated protein kinase-independent pathway. J. Biol. Chem. 271:15762-15768.
22. Ley, R., K. Balmanno, K. Hadfield, C. Weston, and S. J. Cook. 2003. Activation of the ERK1/2 signaling pathway promotes phosphorylation and proteasome-dependent degradation of the BH3-only protein, Bim. J. Biol. Chem. 278:18811-18816.
23. Luciano, F., A. Jacquel, P. Colosetti, M. Herrant, S. Cagnol, G. Pages, and P. Auberger. 2003. Phosphorylation of Bim-EL by Erk1/2 on serine 69 promotes its degradation via the proteasome pathway and regulates its proapoptotic function. Oncogene 22:6785-6793.
24. Marchetti, S., C. Gimond, D. Roux, E. Gothic, J. Pouyssegur, and G. Pages. 2004. Inducible expression of a MAP kinase phosphatase-3-GFP chimera specifically blunts fibroblast growth and ras-dependent tumor formation in nude mice. J. Cell. Physiol. 199:441-450.
25. Milanini-Mongiat, J., J. Pouyssegur, and G. Pages. 2002. Identification of two Sp1 phosphorylation sites for p42/p44 mitogen-activated protein kinases: their implication in vascular endothelial growth factor gene transcription. J. Biol. Chem. 277:20631-20639.
26. Mody, N., J. Leitch, C. Armstrong, J. Dixon, and P. Cohen. 2001. Effects of MAP kinase cascade inhibitors on the MKK5/ERK5 pathway. FEBS Lett. 502:21-24.
27. Muda, M., A. Theodosiou, C. Gillieron, A. Smith, C. Chabert, M. Camps, U. Boschert, N. Rodrigues, K. Davies, A. Ashworth, and S. Arkinstall. 1998. The mitogen-activated protein kinase phosphatase-3 N-terminal noncatalytic region is responsible for tight substrate binding and enzymatic specificity. J. Biol. Chem. 273:9323-9329.
28. Muda, M., A. Theodosiou, N. Rodrigues, U. Boschert, M. Camps, C. Gillieron, K. Davies, A. Ashworth, and S. Arkinstall. 1996. The dual specificity phosphatases M3/6 and MKP-3 are highly selective for inactivation of distinct mitogen-activated protein kinases. J. Biol. Chem. 271:27205-27208.
29. Nichols, A., M. Camps, C. Gillieron, C. Chabert, A. Brunet, J. Wilsbacher, M. Cobb, J. Pouyssegur, J. P. Shaw, and S. Arkinstall. 2000. Substrate recognition domains within extracellular signal-regulated kinase mediate binding and catalytic activation of mitogen-activated protein kinase phosphatase-3. J. Biol. Chem. 275:24613-24621.
30. Pearson, G., F. Robinson, T. Beers Gibson, B. E. Xu, M. Karandikar, K. Berman, and M. H. Cobb. 2001. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev. 22:153-183.
31. Pouyssegur, J., V. Volmat, and P. Lenormand. 2002. Fidelity and spatiotemporal control in MAP kinase (ERKs) signalling. Biochem. Pharmacol. 64:755-763.
32. Reffas, S., and W. Schlegel. 2000. Compartment-specific regulation of extracellular signal-regulated kinase (ERK) and c-Jun N-terminal kinase (JNK) mitogen-activated protein kinases (MAPKs) by ERK-dependent and non-ERK-dependent inductions of MAPK phosphatase (MKP)-3 and MKP-1 in differentiating P19 cells. Biochem. J. 352:701-708.
33. Rigas, J. D., R. H. Hoff, A. E. Rice, A. C. Hengge, and J. M. Denu. 2001. Transition state analysis and requirement of Asp-262 general acid/base catalyst for full activation of dual-specificity phosphatase MKP3 by extracellular regulated kinase. Biochemistry 40:4398-4406.
34. Smith, D. B., and K. S. Johnson. 1988. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 67:31-40.
35. Sohaskey, M. L., and J. E. Ferrell, Jr. 2002. Activation of p42 mitogen-activated protein kinase (MAPK), but not c-Jun NH(2)-terminal kinase, induces phosphorylation and stabilization of MAPK phosphatase XCL100 in Xenopus oocytes. Mol. Biol. Cell 13:454-468.
36. Squires, M. S., P. M. Nixon, and S. J. Cook. 2002. Cell-cycle arrest by PD184352 requires inhibition of extracellular signal-regulated kinases (ERK) 1/2 but not ERK5/BMK1. Biochem. J. 366:673-680.
37. Stewart, A. E., S. Dowd, S. M. Keyse, and N. Q. McDonald. 1999. Crystal structure of the MAPK phosphatase Pyst1 catalytic domain and implications for regulated activation. Nat. Struct. Biol. 6:174-181.
38. Theodosiou, A., and A. Ashworth. 2002. MAP kinase phosphatases. Genome Biol. 3:reviews3009.1-3009.10. [Online.]
39. Volmat, V., M. Camps, S. Arkinstall, J. Pouyssegur, and P. Lenormand. 2001. The nucleus, a site for signal termination by sequestration and inactivation of p42/p44 MAP kinases. J. Cell Sci. 114:3433-3443.
40. Yehia, G., F. Schlotter, R. Razavi, A. Alessandrini, and C. A. Molina. 2001. Mitogen-activated protein kinase phosphorylates and targets inducible cAMP early repressor to ubiquitin-mediated destruction. J. Biol. Chem. 276:35272-35279.
41. Zhao, Y., and Z. Y. Zhang. 2001. The mechanism of dephosphorylation of extracellular signal-regulated kinase 2 by mitogen-activated protein kinase phosphatase 3. J. Biol. Chem. 276:32382-32391.
42. Zhou, B., L. Wu, K. Shen, J. Zhang, D. S. Lawrence, and Z. Y. Zhang. 2001. Multiple regions of MAP kinase phosphatase 3 are involved in its recognition and activation by ERK2. J. Biol. Chem. 276:6506-6515.