Two degradation pathways of the p35 Cdk5 (Cyclin-dependent Kinase) activation subunit, dependent and independent of ubiquitination

Journal of Biological Chemistry

Volumn 291, Issue 9, 2016, Pages 4649-4657

  Takasugi, Toshiyuki ^a   Minegishi, Seiji ^a   Asada, Akiko ^a   Saito, Taro ^a   Kawahara, Hiroyuki ^a   Hisanaga, Shin Ichi ^a  

^a TOKYO METROPOLITAN UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL DEATH; CHEMICAL ACTIVATION; DEGRADATION; ENZYMES; NEURODEGENERATIVE DISEASES; PROTEINS;

AMINO ACID SEQUENCE; CYCLIN-DEPENDENT KINASE; DEGRADATION MECHANISM; DEGRADATION PATHWAYS; HOMEODOMAIN TRANSCRIPTION FACTOR; NEURONAL ACTIVITIES; PHYSIOLOGICAL CONDITION; REGULATORY SUBUNITS;

NEURONS;

ARGININE; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CYCLIN DEPENDENT KINASE 5; CYCLOHEXIMIDE; EPOXOMICIN; HOMEODOMAIN PROTEIN; LYSINE; PROTEASOME; PROTEIN P35; TRANSCRIPTION FACTOR NKX3.1; UNCLASSIFIED DRUG; CDK5 PROTEIN, MOUSE; CDK5R1 PROTEIN, MOUSE; PHOSPHOTRANSFERASE; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME REGULATION; ENZYME REPRESSION; GENE MUTATION; HISTONE PHOSPHORYLATION; IMMUNOFLUORESCENCE; MOUSE; MYRISTYLATION; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN STABILITY; UBIQUITINATION; WILD TYPE; AMINO ACID SUBSTITUTION; ANIMAL; BRAIN CORTEX; CELL CULTURE; CHEMISTRY; COMPARATIVE STUDY; CYTOLOGY; ENZYMOLOGY; GENETICS; HALF LIFE TIME; HEK293 CELL LINE; HUMAN; INSTITUTE FOR CANCER RESEARCH MOUSE; LIPOYLATION; MAMMALIAN EMBRYO; METABOLISM; MUTATION; TUMOR CELL LINE;

AMINO ACID SUBSTITUTION; ANIMALS; CELL LINE, TUMOR; CELLS, CULTURED; CEREBRAL CORTEX; CYCLIN-DEPENDENT KINASE 5; EMBRYO, MAMMALIAN; ENZYME ACTIVATION; HALF-LIFE; HEK293 CELLS; HUMANS; LIPOYLATION; MICE, INBRED ICR; MUTATION; NEURONS; PHOSPHOTRANSFERASES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STABILITY; PROTEOLYSIS; RECOMBINANT PROTEINS; UBIQUITINATION;

EID: 84964613625     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.692871     Document Type: Article

References (57)

1. Malumbres, M. (2014) Cyclin-dependent kinases. Genome Biol. 15, 122
2. Hisanaga, S., and Endo, R. (2010) Regulation and role of cyclin-dependent kinase activity in neuronal survival and death. J. Neurochem. 115, 1309-1321
3. Shah, K., and Lahiri, D. K. (2014) Cdk5 activity in the brain: multiple paths of regulation. J. Cell Sci. 127, 2391-2400
4. Chae, T., and 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
5. Ohshima, T., and 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
6. Gilmore, E. C., Ohshima, T., Goffinet, A. M., and 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
7. 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
8. Lee, K. Y., and Rosales, J. L., Tang, D., and Wang, J. H. (1996) Interaction of cyclin-dependent kinase 5 (Cdk5) and neuronal Cdk5 activator in bovine brain. J. Biol. Chem. 271, 1538-1543
9. 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
10. Harada, T., Morooka, T., Ogawa, S., and Nishida, E. (2001) ERK induces p35, a neuron-specific activator of Cdk5, through induction of Egr1. Nat. Cell Biol. 3, 453-459
11. Bogush, A., Pedrini, S., Pelta-Heller, J., Chan, T., Yang, Q., Mao, Z., Sluzas, E., Gieringer, T., and Ehrlich, M. E. (2007) AKT and CDK5/p35 mediate brain derived neurotrophic factor induction of DRPP-32 in medium size spiny neuron in vitro. J. Biol. Chem. 282, 7352-7359
12. Patrick, G. N., Zhou, P., Kwon, Y. T., and 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
13. 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
14. Wei, F. Y., Tomizawa, K., Ohshima, T., Asada, A., Saito, T., Nguyen, C, and 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
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 p39andp35 is a determinant of cytoplasmic or nuclear localization of active cyclin-dependent kinase 5 complexes. J. Neurochem. 106, 1325-1336
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. 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
19. Lee, M. S., and 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
20. Engmann, O., Hortobágyi, T., Thompson, A. J., Guadagno, J., Troakes, C, Soriano, S., Al-Sarraj, S., Kim, Y., and Giese, K. P. (2011) Cyclin-dependent kinase 5 activator p25 is generated during memory formation and is reduced at an early stage in Altzheiner's disease. Biol. Psychiatry 70, 159-168
21. Rei, D., Mason, X., Seo, J., Gräff, J., Rudenko, A., Wang, J., Rueda, R., Siegert, S., Cho, S., Canter, R. G., and Mungenast, A. E., Deisseroth, K., and Tsai, L. H. (2015) Basolateral amygdala bidirectionally modulates stress-induced hippocampal learning and memory deficits through a p25/Cdk5-dependent pathway. Proc. Natl. Acad. Sci. U.S.A. 112, 7291-7296
22. Cruz, J. C, and Tsai, L. H. (2004) Cdk5 deregulation in pathogenesis of Alzheimer disease. TrendsMol. Med. 10, 452-458
23. Hershko, A., and Ciechanover, A. (1992) The ubiquitin system for protein degradation. Annu. Rev. Biochem. 61, 761-807
24. Ravid, T., and Hochstrasser, M. (2008) Diversity of degradation signals in the ubiquitin-proteasome system. Nat. Rev. Mol. Cell Biol. 9, 679-690
25. Tanaka, K., Suzuki, T., Hattori, N, and Mizuno, Y. (2004) Ubiquitin, proteasome and parkin. Biochim. Biophys. Acta 1695, 235-247
26. Sakamaki, J., Fu, A., Reeks, C, Baird, S., Depatie, C, Al Azzabi, M., Bardeesy, N, Gingras, A. C, Yee, S. P., and Screaton, R. A. (2014) Role of the SIK-p35 PJA2 complex in pancreatic β-cell functional compensation. Nat Cell Biol. 16, 234-244
27. Murakami, Y., Matsufuji, S., Hayashi, S., Tanahashi, N, and Tanaka, K. (2000) Degradation of ornithine decarboxylase by the 26S proteasome. Biochem. Biophys. Res. Commun. 267, 1-6
28. Hoyt, M. A., Zhang, M., and Coffino, P. (2003) Ubiquitin-independent mechanisms of mouse ornithine decarboxylase are conserved between mammalian and fugal cells. J. Biol. Chem. 278, 12135-12143
29. Peña, M. M., Xing, Y. Y., Koli, S., and Berger, F. G. (2006) Role of N-terminal residues in the ubiquitin-independent degradation of human thymidylate synthase. Biochem. J. 394, 355-363
30. Peña, M. M., Melo, S. P., and Xing, Y. Y., White, K., Barbour, K. W., and Berger, F. G. (2009) The intrinsically disordered N-terminal domain of thymidylate synthase targets the enzyme to the ubiquitin-independent proteasomal degradation pathway. J. Biol. Chem. 284, 31597-31607
31. Ha, S.W., Ju, D., and Xie, Y. (2012) The N-terminal domain of Rpn4 serves as a portable ubiquitin-independent degron and is recognized by specific 19S RP subunits. Biochem. Biophys. Res. Commun. 419, 226-231
32. Chen, X., Chi, Y., Bloecher, A., Aebersold, R., and Clurman, B. E., and Roberts, J. M. (2004) N-Acetylation and ubiquitin-independent proteasomal degradation of p21 (Cip 1). Mol. Cell 16, 839-847
33. Tsvetkov, P., Reuven, N., and Shaul, Y. (2010) Ubiquitin-independent p53 proteasomal degradation. Cell Death Differ. 17, 103-108
34. Basbous, J., Jariel-Encontre, I., Gomard, T., Bossis, G., and Piechaczyk, M. (2008) Ubiquitin-independent versus ubiquitin-dependent proteasomal degradation of the c-Fos and Fra-1 trunscription factors: is there a unique answer? Biochimie 90, 296-305
35. Rao, V., Guan, B., Mutton, L. N., and Bieberich, C. J. (2012) Proline-mediate proteasomal degradation of the prostate-specific tumor suppressor NKX3.1. J. Biol. Chem. 287, 36331-36340
36. Kawauchi, T., Chihama, K., Nishimura, Y. V., Nabeshima, Y., and Hoshino, M. (2005) MAP1B phosphorylation is differentially regulated by Cdk5/p35, Cdk5/p25, and JNK. Biochem. Biophys. Res. Commun. 331, 50-55
37. 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
38. Hosokawa, T., Saito, T., Asada, A., Fukunaga, K., and Hisanaga, S. (2010) Quantitative measurement of in vivo phosphorylation states of Cdk5 activator p35 by Phos-tag SDS-PAGE. Mol. Cell Proteomics 9, 1133-1143
39. Sato, K., Minegishi, S., Takano, J., Plattner, F., Saito, T., Asada, A., Kawahara, H., Iwata, N., Saido, T. C., and Hisanaga, S. (2011) Calpastatin, an endogenous calpain-inhibitor protein, regulates the cleavage of the Cdk5 activator p35 to p25. J. Neurochem. 117, 504-515
40. Kamei, H., Saito, T., Ozawa, M., Fujita, Y., Asada, A., Bibb, J. A., and 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
41. Rodriguez, M. S., and Desterro, J. M., Lain, S., Lane, D. P., and Hay, R. T. (2000) Multiple C-terminal lysine residues target p53 for ubiquitin-proteasome-mediated degradation. Mol. Cell. Biol. 20, 8458-8467
42. Guan, B., Pungaliya, P., Li, X., Uquillas, C., and Mutton, L. N., Rubin, E. H., and Bieberich, C. J. (2008) Ubiquitination by TOPORS regulate the prostate tumor suppressor NKX3.1. J. Biol. Chem. 283, 4834-4840
43. Morgan, D. O. (1997) Cyclin-dependent kinases: engines, clocks, and microprocessors. Annu. Rev. Cell Dev. Biol. 13, 261-291
44. Benanti, J. A. (2012) Codination of cell growth and divition by the ubiquitin-proteasome system. Semin. Cell Dev. Biol. 23, 492-498
45. 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
46. Kravtsova-Ivantsiv, Y., and Ciechanover, A. (2012) Non-canonical ubiquitin-based signals for proteasomal degradation. J. Cell Sci. 125, 539-548
47. Erales, J., and Coffino, P. (2014) Ubiquitin-independent proteasomal degradation. Biochim. Biophys. Acta 1843, 216-221
48. Coffino, P. (2001) Antizyme, a mediator of ubiquitin-independent proteasomal degradation. Biochimie 83, 319-323
49. Takeuchi, J., Chen, H., Hoyt, M. A., and Coffino, P. (2008) Structural element of the ubiquitin-independent proteasomal degron of ornithine decarboxylase. Biochem. J. 410, 401-407
50. Chen, X., and Barton, L. F., Chi, Y., Clurman, B. E., and Roberts, J. M. (2007) Ubiquitin-independent degradation of cell-cycle inhibitor by the REGgammma proteasome. Mol. Cell 26, 843-852
51. Yuksek, K., and Chen, W. L., Chien, D., and Ou, J. H. (2009) Ubiquitin-independent degradation of hepatitis C virus F protein. J. Virol. 83, 612-621
52. Melo, S.P., Barbour, K. W., and Berger, F. G. (2011) Cooperation between an intrinsically disordered region and a helical segment is required for ubiuquitin-independent degradation by the proteasome. J. Biol. Chem. 286, 36559-36567
53. Tarricone, C, Dhavan, R., Peng, J., Areces, L. B., and Tsai, L. H., and Musacchio, A. (2001) Structure and regulation of the CDK5-p25(nck5a) complex. Mol. Cell 8, 657-669
54. Abbas, T., Sivaprasad, U., Terai, K., Amador, V., Pagano, M., and Dutta, A. (2008) PCNA-dependent regulation of p21 ubiquitylation and degradation via the CRL4Cdt2 ubiquitin ligase complex. Gene Dev. 22, 2496-2506
55. Bornstein, G., Bloom, J., Sitry-Shevah, D., Nakayama, K., Pagano, M., and Hershko, A. (2003) Role of the SCFSkp2 ubiquitin ligase in the degradation of p21Cip1 in S phase. J. Biol. Chem. 278, 25752-25757
56. Zhang, H., and Cohen, S. N. (2004) Smurf 2 up-regulation activates telomere-dependent senescence. Genes Dev. 18, 3028-3040
57. 2+/calmodulin-dependent protein kinase II upon down-regulation of cyclin-dependent kinase 5-p35. J. Neurosci. Res. 84, 747-754