Control of AMPK-related kinases by USP9X and atypical Lys 29/Lys33-linked polyubiquitin chains

Biochemical Journal

Volumn 411, Issue 2, 2008, Pages 249-260

  Al Hakim, Abdallah K ^a   Zagorska, Anna ^a   Chapman, Louise ^a   Deak, Maria ^a   Peggie, Mark ^a   Alessi, Dario R ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Deubiquitination; LKB1; Protein kinase; Ubiquitin specific protease; Ubiquitination

Indexed keywords

DEUBIQUITINATION; PROTEIN KINASE; UBIQUITIN-SPECIFIC PROTEASE; UBIQUITINATION;

BINDING ENERGY; CELLS; GENE EXPRESSION; MONOMERS; MUTAGENESIS;

ENZYME ACTIVITY;

AMP ACTIVATED PROTEIN KINASE RELATED KINASE 5; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LYSINE; MICROTUBULE AFFINITY REGULATING KINASE 4; POLYUBIQUITIN; PROTEINASE; UBIQUITIN SPECIFIC PROTEASE 9; UNCLASSIFIED DRUG; MARK4 PROTEIN, HUMAN; NUAK1 PROTEIN, HUMAN; PROTEIN KINASE; PROTEIN SERINE THREONINE KINASE; REPRESSOR PROTEIN; UBIQUITIN THIOLESTERASE; USP9X PROTEIN, HUMAN;

ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; UBIQUITINATION; AMINO ACID SEQUENCE; CELL LINE; CHEMISTRY; ENZYME ACTIVATION; ENZYME SPECIFICITY; GENETICS; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION; PROTEIN BINDING; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; CELL LINE; ENZYME ACTIVATION; HUMANS; LYSINE; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; POLYUBIQUITIN; PROTEIN BINDING; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; REPRESSOR PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY; UBIQUITIN THIOLESTERASE;

EID: 42449090346     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20080067     Document Type: Article

References (42)

1. Hemminki, A., Markie, D., Tomlinson, I., Avizienyte, E., Roth, S., Loukola, A., Bignell, G., Warren, W., Aminoff, M., Hoglund, P. et al. (1998) A serine/threonine kinase gene defective in Peutz-Jeghers syndrome. Nature 391, 184-187
2. Alessi, D. R., Sakamoto, K. and Bayascas, J. R. (2006) LKB1-dependent signaling pathways. Annu. Rev. Biochem. 75, 137-163
3. Kahn, B. B., Alguier, T., Carting, D. and Hardie, D. G. (2005) AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab. 1, 15-25
4. Lizcano, J. M., Goransson, O., Toth, R., Deak, M., Morrice, N. A., Boudeau, J., Hawley, S. A., Udd, L., Makela, T. P., Hardie, D. G. and Alessi, D. R. (2004) LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. EMBO J. 23, 833-843
5. Guo, S. and Kemphues, K. J. (1995) Par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed. Cell 81, 611-620
6. Shulman, J. M., Benton, R. and St Johnston, D. (2000) The Drosophila homolog of C. elegans PAR-1 organizes the oocyte cytoskeleton and directs oskar mRNA localization to the posterior pole. Cell 101, 377-388
7. Kusakabe, M. and Nishida, E. (2004) The polarity-inducing kinase Par-1 controls Xenopus gastrulation in cooperation with 14-3-3 and aPKC. EMBO J. 23, 4190-4201
8. Kishi, M., Pan, Y. A., Crump, J. G. and Sanes, J. R. (2005) Mammalian SAD kinases are required for neuronal polarization. Science 307, 929-932
9. Barnes, A. P., Lilley, B. N., Pan, Y. A., Plummer, L. J., Powell, A. W., Raines, A. N., Sanes, J. R. and Polleux, F. (2007) LKB1 and SAD kinases define a pathway required for the polarization of cortical neurons. Cell 129, 549-563
10. Shelly, M., Cancedda, L., Heilshorn, S., Sumbre, G. and Poo, M. M. (2007) LKB1/STRAD promotes axon initiation during neuronal polarization. Cell 129, 565-577
11. Brajenovic, M., Joberty, G., Kuster, B., Bouwmeester, T. and Drewes, G. (2003) Comprehensive proteomic analysis of human Par protein complexes reveals an interconnected protein network. J. Biol. Chem. 279, 12804-12811
12. Suzuki, A., Hirata, M., Kamimura, K., Maniwa, R., Yamanaka, T., Mizuno, K., Kishikawa, M., Hirose, H., Amano, Y., Izumi, N. et al. (2004) aPKC acts upstream of PAR-1b in both the establishment and maintenance of mammalian epithelial polarity. Curr. Biol. 14, 1425-1435
13. Al-Hakim, A. K., Goransson, O., Deak, M., Toth, R., Campbell, D. G., Morrice, N. A., Prescott, A. R. and Alessi, D. R. (2005) 14-3-3 cooperates with LKB1 to regulate the activity and localization of QSK and SIK. J. Cell Sci. 118, 5661-5673
14. Goransson, O., Deak, M., Wullschleger, S., Morrice, N. A., Prescott, A. R. and Alessi, D. R. (2006) Regulation of the polarity kinases PAR-1/MARK by 14-3-3 interaction and phosphorylation. J. Cell Sci. 119, 4059-4070
15. Jones, M. H., Furlong, R. A., Burkin, H., Chalmers, I. J., Brown, G. M., Khwaja, O. and Affara, N. A. (1996) The Drosophila developmental gene fat facets has a human homologue in Xp11.4 which escapes X-inactivation and has related sequences on Yq11.2. Hum. Mol. Genet. 5, 1695-1701
16. 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
17. Zhu, X., Menard, R. and Sulea, T. (2007) High incidence of ubiquitin-like domains in human ubiquitin-specific proteases. Proteins 69, 1-7
18. Fischer-Vize, J. A., Rubin, G. M. and Lehmann, R. (1992) The fat facets gene is required for Drosophila eye and embryo development. Development 116, 985-1000
19. Huang, Y., Baker, R. T. and Fischer-Vize, J. A. (1995) Control of cell fate by a deubiquitinating enzyme encoded by the fat facets gene. Science 270, 1828-1831
20. DiAntonio, A., Haghighi, A. P., Portman, S. L., Lee, J. D., Amaranto, A. M. and Goodman, C. S. (2001) Ubiquitination-dependent mechanisms regulate synaptic growth and function. Nature 412, 449-452
21. Cadavid, A. L., Ginzel, A. and Fischer, J. A. (2000) The function of the Drosophila fat facets deubiquitinating enzyme in limiting photoreceptor cell number is intimately associated with endocytosis. Development 127, 1727-1736
22. Chen, X., Zhang, B. and Fischer, J. A. (2002) A specific protein substrate for a deubiquitinating enzyme: liquid facets is the substrate of Fat facets. Genes Dev. 16, 289-294
23. 2+-dependent decrease of protein ubiquitination at synapses. Proc. Natl. Acad. Sci. U.S.A. 100, 14908-14913
24. Eun, S. H., Lea, K., Overstreet, E., Stevens, S., Lee, J. H. and Fischer, J. A. (2007) Identification of genes that interact with Drosophila liquid facets. Genetics 175, 1163-1174
25. Taya, S., Yamamoto, T., Kanai-Azuma, M., Wood, S. A. and Kaibuchi, K. (1999) The deubiquitinating enzyme Fam interacts with and stabilizes β-catenin. Genes Cells 4, 757-767
26. Taya, S., Yamamoto, T., Kano, K., Kawano, Y., Iwamatsu, A., Tsuchiya, T., Tanaka, K., Kanai-Azuma, M., Wood, S. A., Mattick, J. S. and Kaibuchi, K. (1998) The Ras target AF-6 is a substrate of the fam deubiquitinating enzyme. J. Cell Biol. 142, 1053-1062
27. Vong, Q. P., Cao, K., Li, H. Y., Iglesias, P. A. and Zheng, Y. (2005) Chromosome alignment and segregation regulated by ubiquitination of survivin. Science 310, 1499-1504
28. Mouchantaf, R., Azakir, B. A., McPherson, P. S., Millard, S. M., Wood, S. A. and Angers, A. (2006) The ubiquitin ligase itch is auto-ubiquitylated in vivo and in vitro but is protected from degradation by interacting with the deubiquitylating enzyme FAM/USP9X. J. Biol. Chem. 281, 38738-38747
29. Kerscher, O., Felberbaum, R. and Hochstrasser, M. (2006) Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu. Rev. Cell Dev. Biol. 22, 159-180
30. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M., Mann, M. and Seraphin, B. (1999) A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 17, 1030-1032
31. Swerdlow, P. S., Finley, D. and Varshavsky, A. (1986) Enhancement of immunoblot sensitivity by heating of hydrated filters. Anal. Biochem. 156, 147-153
32. Biondi, R. M., Komander, D., Thomas, C. C., Lizcano, J. M., Deak, M., Alessi, D. R. and Van Aalten, D. M. (2002) High resolution crystal structure of the human PDK1 catalytic domain defines the regulatory phosphopeptide docking site. EMBO J. 21, 4219-4228
33. Durocher, Y., Perret, S. and Kamen, A. (2002) High-level and high-throughput recombinant protein production by transient transfection of suspension-growing human 293-EBNA1 cells. Nucleic Acids Res. 30, E9
34. Amerik, A. Y. and Hochstrasser, M. (2004) Mechanism and function of deubiquitinating enzymes. Biochim. Biophys. Acta 1695, 189-207
35. Chen, Z. J. (2005) Ubiquitin signalling in the HF-κB pathway. Nat. Cell Biol. 7, 758-765
36. Peng, J., Schwartz, D., Elias, J. E., Thoreen, C. C., Cheng, D., Marsischky, G., Roelofs, J., Finley, D. and Gygi, S. P. (2003) A proteomics approach to understanding protein ubiquitination. Nat. Biotechnol. 21, 921-926
37. Kirkpatrick, D. S., Denison, C. and Gygi, S. P. (2005) Weighing in on ubiquitin: the expanding role of mass-spectrometry-based proteomics. Nat. Cell Biol. 7, 750-757
38. Chastagner, P., Israel, A. and Brou, C. (2006) Itch/AIP4 mediates Deltex degradation through the formation of K29-linked polyubiquitin chains. EMBO Rep. 7, 1147-1153
39. Murray, R. Z., Jolly, L. A. and Wood, S. A. (2004) The FAM deubiquitylating enzyme localizes to multiple points of protein trafficking in epithelia, where it associates with E-cadherin and β-catenin. Mol. Biol. Cell 15, 1591-1599
40. Pantaleon, M., Kanai-Azuma, M., Mattick, J. S., Kaibuchi, K., Kaye, P. L. and Wood, S. A. (2001) FAM deubiquitylating enzyme is essential for preimplantation mouse embryo development. Mech. Dev. 109, 151-160
41. Jaleel, M., Villa, F., Deak, M., Toth, R., Prescott, A. R., Van Aalten, D. M. and Alessi, D. R. (2006) The ubiquitin-associated domain of AMPK-related kinases regulates conformation and LKB1-mediated phosphorylation and activation. Biochem. J. 394, 545-555
42. Murphy, J. M., Korzhnev, D. M., Ceccarelli, D. F., Briant, D. J., Zarrine-Afsar, A., Sicheri, F., Kay, L. E. and Pawson, T. (2007) Conformational instability of the MARK3 UBA domain compromises ubiquitin recognition and promotes interaction with the adjacent kinase domain. Proc. Natl. Acad. Sci. U.S.A. 104, 14336-14341