Structural basis for the different stability and activity between the Cdk5 complexes with p35 and p39 activators

Journal of Biological Chemistry

Volumn 288, Issue 45, 2013, Pages 32433-32439

  Saito, Taro ^a   Yano, Masashi ^a   Kawai, Yusei ^a   Asada, Akiko ^a   Wada, Mitsuhito ^b   Doi, Hirofumi ^b,c   Hisanaga, Shin Ichi ^a  

^a TOKYO METROPOLITAN UNIVERSITY   (Japan)

^b Celestar Lexico Sciences Inc   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION DOMAIN; C-TERMINAL REGIONS; CYCLIN-DEPENDENT KINASE; HYDROGEN BOND NETWORKS; HYDROGEN-BOND FORMATION; NONIONIC DETERGENTS; STRUCTURAL BASIS; THREE-DIMENSIONAL STRUCTURE;

AMINO ACIDS; CHEMICAL ACTIVATION; COMPLEX NETWORKS; COMPLEXATION; DETERGENTS; ENZYMES;

HYDROGEN BONDS;

CYCLIN DEPENDENT KINASE 5; PROTEIN P35; PROTEIN P39;

ALPHA HELIX; AMINO ACID SUBSTITUTION; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; HUMAN; HUMAN CELL; HYDROGEN BOND; HYDROPHOBICITY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY;

CDK (CYCLIN-DEPENDENT KINASE); CDK5; COMPUTER MODELING; CYCLINS; HYDROGEN BOND; NEURONS; P35; P39; SERINE-THREONINE PROTEIN KINASE; SUBUNIT INTERACTION;

AMINO ACID SUBSTITUTION; ANIMALS; CARRIER PROTEINS; CYCLIN-DEPENDENT KINASE 5; HEK293 CELLS; HUMANS; HYDROGEN BONDING; MICE; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; MUTATION, MISSENSE; NERVE TISSUE PROTEINS; PROTEIN STABILITY; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84887416906     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.512293     Document Type: Article

References (30)

1. Morgan, D. O. (1997) Cyclin-dependent kinases. Engines, clocks, and microprocessors. Annu. Rev. Cell Dev. Biol. 13, 261-291
2. Murray, A. W. (2004) Recycling the cell cycle. Cyclins revisited. Cell 116, 221-234
3. Hisanaga, S., and Endo, R. (2010) Regulation and role of cyclin-dependent kinase activity in neuronal survival and death. J. Neurochem. 115, 1309-1321
4. Su, S. C., and Tsai, L.-H. (2011) Cyclin-dependent kinases in brain development and disease. Annu. Rev. Cell Dev. Biol. 27, 465-491
5. Cheung, Z. H., and Ip, N. Y. (2012) Cdk5. A multifaceted kinase in neurodegenerative diseases. Trends Cell Biol. 22, 169-175
6. Ohshima, T., Ward, J. M., Huh, C. G., Longenecker, G., Veeranna, Pant, H. C., Brady, R. O., Martin, L. J., and Kulkarni, A. B. (1996) Targeted disruption of the cyclin-dependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death. Proc. Natl. Acad. Sci. U.S.A. 93, 11173-11178
7. Gilmore, E. C., Ohshima, T., Goffinet, A. M., Kulkarni, A. B., and Herrup, K. (1998) Cyclin-dependent kinase 5-deficient mice demonstrate novel developmental arrest in cerebral cortex. J. Neurosci. 18, 6370-6377
8. Ko, J., Humbert, S., Bronson, R. T., Takahashi, S., Kulkarni, A. B., Li, E., Tsai, L.-H. (2001) p35 and p39 are essential for cyclin-dependent kinase 5 function during neurodevelopment. J. Neurosci. 21, 6758-6771
9. Chae, T., Kwon, Y. T., Bronson, R., Dikkes, P., Li, E., Tsai, L.-H. (1997) Mice lacking p35, a neuronal specific activator of Cdk5, display cortical lamination defects, seizures, and adult lethality. Neuron 18, 29-42
10. Patrick, G. N., Zukerberg, L., Nikolic, M., de la Monte, S., Dikkes, P., and Tsai, L.-H. (1999) Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 402, 615-622
11. Kusakawa, G., Saito, T., Onuki, R., Ishiguro, K., Kishimoto, T., and Hisanaga, S. (2000) Calpain-dependent proteolytic cleavage of the p35 CDK5 activtor to p25. J. Biol. Chem. 275, 17166-17172
12. Lee, M. S., Kwon, Y. T., Li, M., Peng, J., Friedlander, R. M., and Tsai, L.-H. (2000) Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature 405, 360-364
13. Cruz, J. C., and Tsai, L. H. (2004) Cdk5 deregulation in the pathogenesis of Alzheimer's disease. Trends Mol. Med. 10, 452-458
14. Shukla, V., Skuntz, S., and Pant, H. C. (2012) Deregulated Cdk5 activity is involved in inducing Alzheimer's disease. Arch. Med. Res. 43, 655-662
15. Asada, A., Yamamoto, N., Gohda, M., Saito, T., Hayashi, N., and Hisanaga, S. (2008) Myristoylation of p39 and p35 is a determinant of cytoplasmic or nuclear localization of active cycline-dependent kinase 5 (Cdk5) complexes. J. Neurochem. 106, 1325-1336
16. Asada, A., Saito, T., and Hisanaga, S. (2012) Subcellular localization of active Cdk5 is determined by its own kinase activity. J. Cell Sci. 125, 3421-3429
17. Minegishi, S., Asada, A., Miyauchi, S., Fuchigami, T., Saito, T., and Hisanaga, S. (2010) Membrane association facilitates degradation and cleavage of the cyclin-dependent kinase 5 activators p35 and p39. Biochemistry 49, 5482-5493
18. Luo, S., Vacher, C., Davies, J. E., and Rubinsztein, D. C. (2005) Cdk5 phosphorylation of huntingtin reduces its cleavage by caspases. Implications for mutant huntingtin toxicity. J. Cell Biol. 169, 647-656
19. Schilling, B., Gafni, J., Torcassi, C., Cong, X., Row, R. H., LaFevre-Bernt, M. A., Cusack, M. P., Ratovitski, T., Hirschhorn, R., Ross, C. A., Gibson, B. W., and Ellerby, L. M. (2006) Huntingtin phosphorylation sites mapped by mass spectrometry. Modulation of cleavage and toxicity. J. Biol. Chem. 281, 23686-23697
20. Kaminosono, S., Saito, T., Oyama, F., Ohshima, T., Asada, A., Nagai, Y., Nukina, N., and Hisanaga, S. (2008) Suppression of mutant huntingtin aggregate formation by Cdk5/p35 through the effect on microtubule stability. J. Neurosci. 28, 8747-8755
21. Tang, D., Yeung, J., Lee, K. Y., Matsushita, M., Matsui, H., Tomizawa, K., Hatase, O., and Wang, J. H. (1995) An isoform of the neuronal cyclin-dependent kinase 5 (Cdk5) activator. J. Biol. Chem. 270, 26897-26903
22. Zheng, M., Leung, C. L., and Liem, R. K. (1998) Region-specific expression of cyclin-dependent kinase 5 (cdk5) and its activators, p35 and p39, in the developing and adult rat central nervous system. J. Neurobiol. 35, 141-159
23. Tarricone, C., Dhavan, R., Peng, J., Areces, L. B., Tsai, L. H., and Musacchio, A. (2001) Structure and regulation of the CDK5-p25(nck5a) complex. Mol. Cell 8, 657-669
24. Yamada, M., Saito, T., Sato, Y., Kawai, Y., Sekigawa, A., Hamazumi, Y., Asada, A., Wada, M., Doi, H., and Hisanaga, S. (2007) Cdk5-p39 is a labile complex with the similar substrate specificity to Cdk5-p35. J. Neurochem. 102, 1477-1487
25. Mapelli, M., Massimiliano, L., Crovace, C., Seeliger, M. A., Tsai, L. H., Meijer, L., and Musacchio, A. (2005) Mechanism of CDK5/p25 binding by CDK inhibitors. J. Med. Chem. 48, 671-679
26. Ahn, J. S., Radhakrishnan, M. L., Mapelli, M., Choi, S., Tidor, B., Cuny, G. D., Musacchio, A., Yeh, L. A., Kosik, K. S. (2005) Defining Cdk5 ligand chemical space with small molecule inhibitors of tau phosphorylation. Chem. Biol. 12, 811-823
27. Eisenberg, D., Weiss, R. M., and Terwilliger, T. C. (1982) The helical hydrophobic moment. A measure of the amphiphilicity of a helix. Nature 299, 371-374
28. Zhu, Y.-S., Saito, T., Asada, A., Maekawa, S., and Hisanaga, S. (2005) Activation of latent cyclin-dependent kinase 5 (Cdk5)-p35 complexes by membrane dissociation. J. Neurochem. 94, 1535-1545
29. Takahashi, S., Saito, T., Hisanaga, S., Pant, H. C., and Kulkarni, A. B. (2003) Tau phosphorylation by cyclin-dependent kinase 5/p39 during brain development reduces its affinity for microtubules. J. Biol. Chem. 278, 10506-10515
30. Ledee, D. R., Gao, C. Y., Seth, R., Fariss, R. N., Tripathi, B. K., and Zelenka, P. S. (2005)Aspecific interaction between muskelin and the cyclin-dependent kinase 5 activator p39 promotes peripheral localization of muskelin. J. Biol. Chem. 280, 21376-21383