Membrane association facilitates degradation and cleavage of the cyclin-dependent kinase 5 activators p35 and p39

Biochemistry

Volumn 49, Issue 26, 2010, Pages 5482-5493

  Minegishi, Seiji ^a   Asada, Akiko ^a   Miyauchi, Shinya ^a   Fuchigami, Takahiro ^a   Saito, Taro ^a   Hisanaga, Shin Ichi ^a  

^a TOKYO METROPOLITAN UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALPAINS; CLEAVAGE RATES; CYCLIN-DEPENDENT KINASE; DEGRADATION RATE; MEMBRANE ASSOCIATION; MEMBRANE BINDING; MYRISTOYLATION; N-TERMINALS; PATHOLOGICAL FUNCTIONS; PROTEASOMAL DEGRADATION;

BINDING ENERGY;

DEGRADATION;

CALPAIN; CYCLIN DEPENDENT KINASE 5; PROTEASOME; PROTEIN P10; PROTEIN P35; PROTEIN P39;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; MEMBRANE; MEMBRANE BINDING; MYRISTYLATION; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN FUNCTION; RAT; REGULATORY MECHANISM;

CALPAIN; CELL LINE; CELL MEMBRANE; CYCLIN-DEPENDENT KINASE 5; ENZYME ACTIVATION; HUMANS; KINETICS; MYRISTIC ACID; NERVE TISSUE PROTEINS; NEURONS; PROTEASOME ENDOPEPTIDASE COMPLEX;

EID: 77954187920     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100631f     Document Type: Article

References (51)

1. Dhavan, R. and Tsai, L. H. (2001) A decade of CDK5 Nat. Rev. Mol. Cell Biol. 2, 749-759
2. Shelton, S. B. and Johnson, G. V. W. (2004) Cyclin-dependent kinase-5 in neurodegeneration J. Neurochem. 88, 1313-1326
3. Cheung, Z. H., Fu, A. K., and Ip, N. Y. (2006) Synaptic roles of Cdk5: Implications in higher cognitive functions and neurodegenerative diseases Neuron 50, 13-18
4. Angelo, M., Plattner, F., and Giese, K. P. (2006) Cyclin-dependent kinase 5 in synaptic plasticity, learning and memory J. Neurochem. 99, 353-370
5. Tang, D. and Wang, J. H. (1996) Cyclin-dependent kinase 5 (Cdk5) and neuron-specific Cdk5 activators Prog. Cell Cycle Res. 2, 205-216
6. Hisanaga, S. and Saito, T. (2003) The regulation of cyclin-dependent kinase 5 activity through the metabolism of p35 or p39 Cdk5 activator Neurosignals 12, 221-229
7. Qi, Z., Huang, Q. Q., Lee, K. Y., Lew, J., and Wang, J. H. (1995) Reconstitution of neuronal Cdc2-like kinase from bacteria-expressed Cdk5 and an active fragment of the brain-specific activator. Kinase activation in the absence of Cdk5 phosphorylation J. Biol. Chem. 270, 10847-10854
8. Patrick, G. N., Zhou, P., Kwon, Y. T., Howley, P. M., and Tsai, L. H. (1998) p35, the neuronal-specific activator of cyclin-dependent kinase 5 (Cdk5) is degraded by the ubiquitin-proteasome pathway J. Biol. Chem. 273, 24057-24064
9. Saito, T., Ishiguro, K., Onuki, R., Nagai, Y., Kishimoto, T., and Hisanaga, S. (1998) Okadaic acid-stimulated degradation of p35, an activator of CDK5, by proteasome in cultured neurons Biochem. Biophys. Res. Commun. 252, 775-778
10. Patzke, H. and Tsai, L. H. (2002) Calpain-mediated cleavage of the cyclin-dependent kinase-5 activator p39 to p29 J. Biol. Chem. 277, 8054-8060
11. Morgan, D. O. (1997) Cyclin-dependent kinases: Engines, clocks, and microprocessors Annu. Rev. Cell Dev. Biol. 13, 261-291
12. Wei, F. Y., Tomizawa, K., Ohshima, T., Asada, A., Saito, T., Nguyen, C., Bibb, J. A., Ishiguro, K., Kulkarni, A. B., Pant, H. C., Mikoshiba, K., Matsui, H., and Hisanaga, S. (2005) Control of cyclin-dependent kinase 5 (Cdk5) activity by glutamatergic regulation of p35 stability J. Neurochem. 93, 502-512
13. 2+/calmodulin-dependent protein kinase II upon downregulation of cyclin-dependent kinase 5-p35 J. Neurosci. Res. 84, 747-754
14. Boutin, J. A. (1997) Myristoylation Cell. Signalling 9, 15-35
15. 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
16. 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 cyclin-dependent kinase 5 complexes J. Neurochem. 106, 1325-1336
17. 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
18. 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
19. Kusakawa, G., Saito, T., Onuki, R., Ishiguro, K., Kishimoto, T., and Hisanaga, S. (2000) Calpain-dependent proteolytic cleavage of the p35 cyclin-dependent kinase 5 activator to p25 J. Biol. Chem. 275, 17166-17172
20. 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
21. Patzke, H., Maddineni, U., Ayala, R., Morabito, M., Volker, J., Dikkes, P., Ahlijanian, M. K., and Tsai, L. H. (2003) Partial rescue of the p35-/- brain phenotype by low expression of a neuronal-specific enolase p25 transgene J. Neurosci. 23, 2769-2778
22. 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
23. Chae, T., Kwon, Y. T., Bronson, R., Dikkes, P., Li, E., and 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
24. Ko, J., Humbert, S., Bronson, R. T., Takahashi, S., Kulkarni, A. B., Li, E., and Tsai, L. H. (2001) p35 and p39 are essential for cyclin-dependent kinase 5 function during neurodevelopment J. Neurosci. 21, 6758-6771
25. 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
26. Tabuchi, A., Oh, E., Taoka, A., Sakurai, H., Tsuchiya, T., and Tsuda, M. (1996) Rapid attenuation of AP-1 transcriptional factors associated with nitric oxide (NO)-mediated neuronal cell death J. Biol. Chem. 271, 31061-31067
27. Endo, R., Saito, T., Asada, A., Kawahara, H., Ohshima, T., and Hisanaga, S. (2009) Commitment of 1-methyl-4-phenylpyrinidinium ion-induced neuronal cell death by proteasome-mediated degradation of p35 cyclin-dependent kinase 5 activator J. Biol. Chem. 284, 26029-26039
28. Saito, T., Onuki, R., Fujita, Y., Kusakawa, G., Ishiguro, K., Bibb, J. A., Kishimoto, T., and Hisanaga, S. (2003) Developmental regulation of the proteolysis of the p35 cyclin-dependent kinase 5 activator by phosphorylation J. Neurosci. 23, 1189-1197 (Pubitemid 36258898)
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. Kamei, H., Saito, T., Ozawa, M., Fujita, Y., Asada, A., Bibb, J. A., Saido, T. C., Sorimachi, H., and Hisanaga, S. (2007) Suppression of calpain-dependent cleavage of the CDK5 activator p35 to p25 by site-specific phosphorylation J. Biol. Chem. 282, 1687-1694
31. Obaya, A. J. and Sedivy, J. M. (2002) Regulation of cyclin-Cdk activity in mammalian cells Cell. Mol. Life Sci. 59, 126-142
32. Moroy, T. and Geisen, C. (2004) Cyclin E Int. J. Biochem. Cell Biol. 36, 1424-1439
33. Lin, D. I., Barbash, O., Kumar, K. G., Weber, J. D., Harper, J. W., Klein-Szanto, A. J., Rustgi, A., Fuchs, S. Y., and Diehl, J. A. (2006) Phosphorylation-dependent ubiquitination of cyclin D1 by the SCF (FBX4-αB Crystallin) complex Mol. Cell 24, 355-366
34. Sakaue-Sawano, A., Ohtawa, K., Hama, H., Kawano, M., Ogawa, M., and Miyawaki, A. (2008) Tracing the silhouette of individual cells in S/G2/M phases with fluorescence Chem. Biol. 15, 1243-1248
35. Lin, H. K., Wang, G., Chen, Z., Teruya-Feldstein, J., Liu, Y., Chan, C. H., Yang, W. L., Erdjument-Bromage, H., Nakayama, K. I., Nimer, S., Tempst, P., and Pandolfi, P. P. (2009) Phosphorylation-dependent regulation of cytosolic localization and oncogenic function of Skp2 by Akt/PKB Nat. Cell Biol. 11, 420-432
36. Gong, X., Tang, X., Wiedmann, M., Wang, X., Peng, J., Zheng, D., Blair, L. A., Marshall, J., and Mao, Z. (2003) Cdk5-mediated inhibition of the protective effects of transcription factor MEF2 in neurotoxicity-induced apoptosis Neuron 38, 33-46
37. Saito, T., Konno, T., Hosokawa, T., Asada, A., Ishiguro, K., and Hisanaga, S. (2007) p25/cyclin-dependent kinase 5 promotes the progression of cell death in nucleus of endoplasmic reticulum-stressed neurons J. Neurochem. 102, 133-140
38. Suzuki, K., Hata, S., Kawabata, Y., and Sorimachi, H. (2004) Structure, activation, and biology of calpain Diabetes 53, S12-S18
39. Tomimatsu, Y., Idemoto, S., Moriguchi, S., Watanabe, S., and Nakanishi, H. (2002) Proteases involved in long-term potentiation Life Sci. 72, 355-361
40. 2+-binding proteins Biochim. Biophys. Acta 1600, 51-60
41. Selkoe, D. J. (2001) Alzheimers disease: Genes, proteins, and therapy Physiol. Rev. 81, 741-766
42. Wu, X., Jiang, X., Marini, A. M., and Lipsky, R. H. (2005) Delineating and understanding cerebellar neuroprotective pathways: Potential implication for protecting the cortex Ann. N.Y. Acad. Sci. 1053, 39-47
43. Kepe, V., Huang, S. C., Small, G. W., and Barrio, J. R. (2006) Visualizing pathology deposits in the living brain of patients with Alzheimers disease Methods Enzymol. 412, 144-160 (Pubitemid 44548579)
44. Vaisid, T., Kosower, N. S., Katzav, A., Chapman, J., and Barnoy, S. (2007) Calpastatin levels affect calpain activation and calpain proteolytic activity in APP transgenic mouse model of Alzheimers disease Neurochem. Int. 51, 391-397
45. Nakayama, J., Yoshizawa, T., Yamamoto, N., and Arinami, T. (2002) Mutation analysis of the calpastatin gene (CAST) in patients with Alzheimers disease Neurosci. Lett. 320, 77-80
46. Higuchi, M., Tomioka, M., Takano, J., Shirotani, K., Iwata, N., Masumoto, H., Maki, M., Itohara, S., and Saido, T. C. (2005) Distinct mechanistic roles of calpain and caspase activation in neurodegeneration as revealed in mice overexpressing their specific inhibitors J. Biol. Chem. 280, 15229-15237
47. Ho, M. A., Ou, C., Chan, Y. R., Chein, C. T., and Pi, H. (2008) The utility F-box for protein destruction Cell. Mol. Life Sci. 65, 1977-2000
48. Hunter, T. (2007) The Age of Crosstalk: Phosphorylation, Ubiquitination, and Beyond Mol. Cell 28, 730-738
49. dAzzo, A., Bongiovanni, A., and Nastasi, T. (2005) E3 ubiqutin ligases as regulators of membrane protein trafficking and degrdation Traffic 6, 429-441
50. Ohshima, T., Ogura, H., Tomizawa, K., Hayashi, K., Suzuki, H., Saito, T., Kamei, H., Nishi, A., Bibb, J. A., Hisanaga, S., Matsui, H., and Mikoshiba, K. (2005) Impairment of hippocampal long-term depression and defective spatial learning and memory in p35 mice J. Neurochem. 94, 917-925
51. Fu, A. K., Fu, W. Y., Ng, A. K., Chien, W. W., Ng, Y. P., Wang, J. H., and Ip, N. Y. (2004) Cyclin-dependent kinase 5 phosphorylates signal transducer and activator of transcription 3 and regulates its transcriptional activity Proc. Natl. Acad. Sci. U.S.A. 101, 6728-6733