Sumoylation of p35 Modulates p35/Cyclin-Dependent Kinase (Cdk) 5 Complex Activity

NeuroMolecular Medicine

Volumn 17, Issue 1, 2015, Pages 12-23

  Büchner, Anja ^a,e   Krumova, Petranka ^a,b   Ganesan, Sundar ^c   Bähr, Mathias ^a   Eckermann, Katrin ^a,e   Weishaupt, Jochen H ^a,d  

^a UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^b NOVARTIS PHARMA AG   (Switzerland)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d UNIVERSITY OF ULM   (Germany)

^e Center for Nanoscale Microscopy and Molecular Physiology of the Brain (CNMPB)   (Germany)

Author keywords

FRET FLIM; Oxidative stress; p35 Cdk5 activity; Sumoylation

Indexed keywords

CYCLIN DEPENDENT KINASE 5; LYSINE; PROTEIN P35; SUMO 1 PROTEIN; SUMO 2 PROTEIN; HYBRID PROTEIN; NERVE PROTEIN; NEURONAL CDK5 ACTIVATOR (P25-P35); PROTEIN BINDING; SUMO PROTEIN; SUMO1 PROTEIN, HUMAN; SUMO2 PROTEIN, HUMAN;

ARTICLE; BIOCHEMISTRY; CELL FREE SYSTEM; CONJUGATION; CONTROLLED STUDY; DEGENERATIVE DISEASE; DISEASE ASSOCIATION; ENZYME ACTIVITY; ENZYME REGULATION; FLUORESCENCE LIFETIME IMAGING MICROSCOPY; FLUORESCENCE MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; IN VITRO STUDY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SUMOYLATION; ANIMAL; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN ANALYSIS; RAT; TRANSFORMED CELL LINE;

ANIMALS; CELL LINE, TRANSFORMED; CELL-FREE SYSTEM; CONSERVED SEQUENCE; CYCLIN-DEPENDENT KINASE 5; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEK293 CELLS; HELA CELLS; HUMANS; LYSINE; NERVE TISSUE PROTEINS; OXIDATIVE STRESS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; RATS; RECOMBINANT FUSION PROTEINS; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; SUMO-1 PROTEIN; SUMOYLATION;

EID: 84925484643     PISSN: 15351084     EISSN: 15591174     Source Type: Journal    
DOI: 10.1007/s12017-014-8336-4     Document Type: Article

References (56)

1. Amor, S., Peferoen, L. A., Vogel, D. Y., Breur, M., van der Valk, P., Baker, D., et al. (2014). Inflammation in neurodegenerative diseases–an update. Immunology,142(2), 151–166.
2. Asada, A., Yamamoto, N., Gohda, M., Saito, T., Hayashi, N., & Hisanaga, S. (2008). Myristoylation of p39 and p35 is a determinant of cytoplasmic or nuclear localization of active cyclin-dependent kinase 5 complexes. Journal of Neurochemistry,106(3), 1325–1336.
3. Bernier-Villamor, V., Sampson, D. A., Matunis, M. J., & Lima, C. D. (2002). Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1. Cell,108(3), 345–356.
4. Bossis, G., & Melchior, F. (2006). Regulation of SUMOylation by reversible oxidation of SUMO conjugating enzymes. Molecular Cell,21(3), 349–357.
5. 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(1), 29–42.
6. Choe, E. A., Liao, L., Zhou, J. Y., Cheng, D., Duong, D. M., Jin, P., et al. (2007). Neuronal morphogenesis is regulated by the interplay between cyclin-dependent kinase 5 and the ubiquitin ligase mind bomb 1. Journal of Neuroscience,27(35), 9503–9512.
7. Day, R. N., Booker, C. F., & Periasamy, A. (2008). Characterization of an improved donor fluorescent protein for Forster resonance energy transfer microscopy. Journal of Biomedial Optics,13(3), 031203.
8. Desterro, J. M., Rodriguez, M. S., Kemp, G. D., & Hay, R. T. (1999). Identification of the enzyme required for activation of the small ubiquitin-like protein SUMO-1. Journal of Biological Chemistry,274(15), 10618–10624.
9. Dhavan, R., & Tsai, L. H. (2001). A decade of CDK5. Nature Reviews Molecular Cell Biology,2(10), 749–759.
10. Eckermann, K. (2013). SUMO and parkinson’s disease. Neuromolecular Med,15(4), 737–759.
11. Feligioni, M., & Nistico, R. (2013). SUMO: a (oxidative) stressed protein. Neuromolecular Medicine,15(4), 707–719.
12. Fu, X., Choi, Y. K., Qu, D., Yu, Y., Cheung, N. S., & Qi, R. Z. (2006). Identification of nuclear import mechanisms for the neuronal Cdk5 activator. Journal of Biological Chemistry,281(51), 39014–39021.
13. Gill, G. (2004). SUMO and ubiquitin in the nucleus: different functions, similar mechanisms? Genes & Development,18(17), 2046–2059.
14. Golebiowski, F., Matic, I., Tatham, M. H., Cole, C., Yin, Y., Nakamura, A., et al. (2009). System-wide changes to SUMO modifications in response to heat shock. Science Signaling, 2(72), ra24.
15. Gong, L., Millas, S., Maul, G. G., & Yeh, E. T. (2000). Differential regulation of sentrinized proteins by a novel sentrin-specific protease. Journal of Biological Chemistry,275(5), 3355–3359.
16. Halliwell, B., Clement, M. V., & Long, L. H. (2000). Hydrogen peroxide in the human body. FEBS Letters,486(1), 10–13.
17. Hecker, C. M., Rabiller, M., Haglund, K., Bayer, P., & Dikic, I. (2006). Specification of SUMO1- and SUMO2-interacting motifs. Journal of Biological Chemistry,281(23), 16117–16127.
18. Hsiao, K., Bozdagi, O., & Benson, D. L. (2014). Axonal cap-dependent translation regulates presynaptic p35. Developmental Neurobiology,74(3), 351–364.
19. Jaffray, E. G., & Hay, R. T. (2006). Detection of modification by ubiquitin-like proteins. Methods,38(1), 35–38.
20. Kim, E. T., Kim, K. K., Matunis, M. J., & Ahn, J. H. (2009). Enhanced SUMOylation of proteins containing a SUMO-interacting motif by SUMO-Ubc9 fusion. Biochemical and Biophysical Research Communications,388(1), 41–45.
21. Krumova, P., Meulmeester, E., Garrido, M., Tirard, M., Hsiao, H. H., Bossis, G., et al. (2011). Sumoylation inhibits alpha-synuclein aggregation and toxicity. Journal of Cell Biology,194(1), 49–60.
22. Krumova, P., & Weishaupt, J. H. (2013). Sumoylation in neurodegenerative diseases. Cellular and Molecular Life Sciences,70(12), 2123–2138.
23. Li, Z., David, G., Hung, K. W., DePinho, R. A., Fu, A. K., & Ip, N. Y. (2004). Cdk5/p35 phosphorylates mSds3 and regulates mSds3-mediated repression of transcription. Journal of Biological Chemistry,279(52), 54438–54444.
24. Macauley, M. S., Errington, W. J., Scharpf, M., Mackereth, C. D., Blaszczak, A. G., Graves, B. J., et al. (2006). Beads-on-a-string, characterization of ETS-1 sumoylated within its flexible N-terminal sequence. Journal of Biological Chemistry,281(7), 4164–4172.
25. Mahajan, R., Delphin, C., Guan, T., Gerace, L., & Melchior, F. (1997). A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell,88(1), 97–107.
26. Matunis, M. J., Coutavas, E., & Blobel, G. (1996). A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex. Journal of Cell Biology,135(6 Pt 1), 1457–1470.
27. Mukhopadhyay, D., & Dasso, M. (2007). Modification in reverse: the SUMO proteases. Trends in Biochemical Sciences,32(6), 286–295.
28. Nagai, T., Ibata, K., Park, E. S., Kubota, M., Mikoshiba, K., & Miyawaki, A. (2002). A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nature Biotechnology,20(1), 87–90.
29. Nguyen, M. D., Lariviere, R. C., & Julien, J. P. (2001). Deregulation of Cdk5 in a mouse model of ALS: toxicity alleviated by perikaryal neurofilament inclusions. Neuron,30(1), 135–147.
30. Nikolic, M., Dudek, H., Kwon, Y. T., Ramos, Y. F., & Tsai, L. H. (1996). The cdk5/p35 kinase is essential for neurite outgrowth during neuronal differentiation. Genes & Development,10(7), 816–825.
31. O’Hare, M. J., Kushwaha, N., Zhang, Y., Aleyasin, H., Callaghan, S. M., Slack, R. S., et al. (2005). Differential roles of nuclear and cytoplasmic cyclin-dependent kinase 5 in apoptotic and excitotoxic neuronal death. Journal of Neuroscience,25(39), 8954–8966.
32. Osuga, H., Osuga, S., Wang, F., Fetni, R., Hogan, M. J., Slack, R. S., et al. (2000). Cyclin-dependent kinases as a therapeutic target for stroke. Proceedings of the National Academy of Sciences USA,97(18), 10254–10259.
33. Patrick, G. N., Zhou, P., Kwon, Y. T., Howley, P. M., & Tsai, L. H. (1998). p35, the neuronal-specific activator of cyclin-dependent kinase 5 (Cdk5) is degraded by the ubiquitin-proteasome pathway. Journal of Biological Chemistry,273(37), 24057–24064.
34. Patrick, G. N., Zukerberg, L., Nikolic, M., de la Monte, S., Dikkes, P., & Tsai, L. H. (1999). Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature,402(6762), 615–622.
35. Patzke, H., & Tsai, L. H. (2002). Calpain-mediated cleavage of the cyclin-dependent kinase-5 activator p39 to p29. Journal of Biological Chemistry,277(10), 8054–8060.
36. Poon, R. Y., Lew, J., & Hunter, T. (1997). Identification of functional domains in the neuronal Cdk5 activator protein. Journal of Biological Chemistry,272(9), 5703–5708.
37. Sahlgren, C. M., Pallari, H. M., He, T., Chou, Y. H., Goldman, R. D., & Eriksson, J. E. (2006). A nestin scaffold links Cdk5/p35 signaling to oxidant-induced cell death. EMBO Journal,25(20), 4808–4819.
38. Saitoh, H., & Hinchey, J. (2000). Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. Journal of Biological Chemistry,275(9), 6252–6258.
39. Sapetschnig, A., Rischitor, G., Braun, H., Doll, A., Schergaut, M., Melchior, F., et al. (2002). Transcription factor Sp3 is silenced through SUMO modification by PIAS1. EMBO Journal,21(19), 5206–5215.
40. Shea, T. B., Zheng, Y. L., Ortiz, D., & Pant, H. C. (2004). Cyclin-dependent kinase 5 increases perikaryal neurofilament phosphorylation and inhibits neurofilament axonal transport in response to oxidative stress. Journal of Neuroscience Research,76(6), 795–800.
41. Shin, E. J., Shin, H. M., Nam, E., Kim, W. S., Kim, J. H., Oh, B. H., et al. (2012). DeSUMOylating isopeptidase: a second class of SUMO protease. EMBO Reports,13(4), 339–346.
42. Shukla, V., Mishra, S. K., & Pant, H. C. (2011). Oxidative stress in neurodegeneration. Advance Pharmacology Science,2011, 572634.
43. Smith, P. D., Crocker, S. J., Jackson-Lewis, V., Jordan-Sciutto, K. L., Hayley, S., Mount, M. P., et al. (2003). Cyclin-dependent kinase 5 is a mediator of dopaminergic neuron loss in a mouse model of Parkinson’s disease. Proceedings of the National Academy of Sciences USA,100(23), 13650–13655.
44. Su, S. C., & Tsai, L. H. (2011). Cyclin-dependent kinases in brain development and disease. Annual Review of Cell and Developmental Biology,27, 465–491.
45. Sun, K. H., Chang, K. H., Clawson, S., Ghosh, S., Mirzaei, H., Regnier, F., et al. (2011). Glutathione-S-transferase P1 is a critical regulator of Cdk5 kinase activity. Journal of Neurochemistry,118(5), 902–914.
46. Tan, T. C., Valova, V. A., Malladi, C. S., Graham, M. E., Berven, L. A., Jupp, O. J., et al. (2003). Cdk5 is essential for synaptic vesicle endocytosis. Nature Cell Biology,5(8), 701–710.
47. Tang, D., Chun, A. C., Zhang, M., & Wang, J. H. (1997). Cyclin-dependent kinase 5 (Cdk5) activation domain of neuronal Cdk5 activator. Evidence of the existence of cyclin fold in neuronal Cdk5a activator. Journal of Biological Chemistry,272(19), 12318–12327.
48. Tang, D., Yeung, J., Lee, K. Y., Matsushita, M., Matsui, H., Tomizawa, K., et al. (1995). An isoform of the neuronal cyclin-dependent kinase 5 (Cdk5) activator. Journal of Biological Chemistry,270(45), 26897–26903.
49. Tarricone, C., Dhavan, R., Peng, J., Areces, L. B., Tsai, L. H., & Musacchio, A. (2001). Structure and regulation of the CDK5-p25(nck5a) complex. Molecular Cell,8(3), 657–669.
50. Tatham, M. H., Jaffray, E., Vaughan, O. A., Desterro, J. M., Botting, C. H., Naismith, J. H., et al. (2001). Polymeric chains of SUMO-2 and SUMO-3 are conjugated to protein substrates by SAE1/SAE2 and Ubc9. Journal of Biological Chemistry,276(38), 35368–35374.
51. Tsai, L. H., Delalle, I., Caviness, V. S, Jr, Chae, T., & Harlow, E. (1994). p35 is a neural-specific regulatory subunit of cyclin-dependent kinase 5. Nature,371(6496), 419–423.
52. van den Heuvel, S., & Harlow, E. (1993). Distinct roles for cyclin-dependent kinases in cell cycle control. Science,262(5142), 2050–2054.
53. Verstegen, A. M., Tagliatti, E., Lignani, G., Marte, A., Stolero, T., Atias, M., et al. (2014). Phosphorylation of synapsin I by cyclin-dependent kinase-5 sets the ratio between the resting and recycling pools of synaptic vesicles at hippocampal synapses. Journal of Neuroscience,34(21), 7266–7280.
54. Weishaupt, J. H., Kussmaul, L., Grotsch, P., Heckel, A., Rohde, G., Romig, H., et al. (2003). Inhibition of CDK5 is protective in necrotic and apoptotic paradigms of neuronal cell death and prevents mitochondrial dysfunction. Molecular and Cellular Neuroscience,24(2), 489–502.
55. Wittmann, C., Chockley, P., Singh, S. K., Pase, L., Lieschke, G. J., & Grabher, C. (2012). Hydrogen peroxide in inflammation: messenger, guide, and assassin. Advances in Hematology,2012, 541471.
56. Zukerberg, L. R., Patrick, G. N., Nikolic, M., Humbert, S., Wu, C. L., Lanier, L. M., et al. (2000). Cables links Cdk5 and c-Abl and facilitates Cdk5 tyrosine phosphorylation, kinase upregulation, and neurite outgrowth. Neuron,26(3), 633–646.