Fol. Biol. 2018, 64, 35-40

https://doi.org/10.14712/fb2018064020035

Notch and Cdk5 in Zebrafish mindbomb Mutant: Co-regulation or Coincidence?

Jyotshna Kanungo1,2, M. T. Goswami3, H. C. Pant2

1Division of Neurotoxicology, National Center for Toxicological Research, US Food and Drug Administration, Jefferson, AR, USA
2National Institute of Neuronal Disorders and Stroke, National Institute of Health, Bethesda, MD, USA
3National Institute of Children’s Health and Development, National Institute of Health, Bethesda, MD, USA

Received May 2018
Accepted May 2018

References

1. Ables, J. L., Breunig, J. J., Eisch, A. J., Rakic, P. (2011) Not(ch) just development: Notch signalling in the adult brain. Nat. Rev. Neurosci. 12, 269-283.
2. Acconcia, F., Sigismund, S., Polo, S. (2009) Ubiquitin in trafficking: the network at work. Exp. Cell Res. 315, 1610-1618.
3. Berezovska, O., McLean, P., Knowles, R., Frosh, M., Lu, F. M., Lux, S. E., Hyman, B. T. (1999) Notch1 inhibits neurite outgrowth in postmitotic primary neurons. Neuroscience 93, 433-439.
4. Cheung, Z. H., Fu, A. K., Ip, N. Y. (2006) Synaptic roles of Cdk5: implications in higher cognitive functions and neurodegenerative diseases. Neuron 50, 13-18.
5. Cheung, Z. H., Gong, K, Ip, N. Y. (2008) Cyclin-dependent kinase 5 supports neuronal survival through phosphorylation of Bcl-2. J. Neurosci. 28, 4872-4877.
6. Cheung, Z. H., Ip, N. Y. (2012) Cdk5: a multifaceted kinase in neurodegenerative diseases. Trends Cell. Biol. 22, 169-175.
7. Cho, B., Cho, H. M., Kim, H. J., Jeong, J., Park, S. K., Hwang, E. M., Park, J. Y., Kim, W. R., Kim, H., Sun, W. (2014) CDK5-dependent inhibitory phosphorylation of Drp1 during neuronal maturation. Exp. Mol. Med. 46, e105.
8. Choe, E. A., Liao, L., Zhou, J. Y., Cheng, D., Duong, D. M., Jin, P., Tsai, L. H., Peng, J. (2007) Neuronal morphogenesis is regulated by the interplay between cyclin-dependent kinase 5 and the ubiquitin ligase mind bomb 1. J. Neurosci. 27, 9503-9512.
9. Cicero, S., Herrup, K. (2005) Cyclin-dependent kinase 5 is essential for neuronal cell cycle arrest and differentiation. J. Neurosci. 25, 9658-9668.
10. Clague, M. J., Urbe, S. (2010) Ubiquitin: same molecule, different degradation pathways. Cell 143, 682-685.
11. Connell-Crowley, L., Le Gall, M., Vo, D. J., Giniger, E. (2000) The cyclin-dependent kinase Cdk5 controls multiple aspects of axon patterning in vivo. Curr. Biol. 10, 599-602.
12. Cruz, J. C., Tsai, L. H. (2004) A Jekyll and Hyde kinase: roles for Cdk5 in brain development and disease. Curr. Opin. Neurobiol. 14, 390-394.
13. Deblandre, G. A., Lai, E. C., Kintner, C. (2001) Xenopus neuralized is a ubiquitin ligase that interacts with XDelta1 and regulates Notch signaling. Dev. Cell 1, 795-806.
14. Dhavan, R., Tsai, L. H. (2001) A decade of CDK5. Nat. Rev. Mol. Cell. Biol. 2, 749-759.
15. Franklin, J. L., Berechid, B. E., Cutting, F. B., Presente, A., Chambers, C. B., Foltz, D. R., Ferreira, A., Nye, J. S. (1999) Autonomous and non-autonomous regulation of mammalian neurite development by Notch1 and Delta1. Curr. Biol. 9, 1448-1457.
16. Gao, M., Labuda, T., Xia, Y., Gallagher, E., Fang, D., Liu, Y. C., Karin, M. (2004) Jun turnover is controlled through JNK-dependent phosphorylation of the E3 ligase Itch. Science 306, 271-275.
17. Hellstrom, M., Phng, L. K., Hofmann, J. J., Wallgard, E., Coultas, L., Lindblom, P., Alva, J., Nilsson, A. K., Karlsson, L., Gaiano, N., Yoon, K., Rossant, J., Iruela-Arispe, M. L., Kalen, M., Gerhardt, H., Betsholtz, C. (2007) Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 445, 776-780.
18. Hwang, J., Kim, H. S., Seok, J. W., Kim, J. D., Koun, S., Park, S. Y., Lee, J., Kim, H. S., Kim, H. S., Kim, K. S., Chang, K. T., Ryoo, Z. Y., Wang, S. M., Huh, T. L., Lee, S. (2009) Transcriptome analysis of the zebrafish mind bomb mutant. Mol. Genet. Genomics 281, 77-85.
19. Itoh, M., Kim, C. H., Palardy, G., Oda, T., Jiang, Y. J., Maust, D., Yeo, S. Y., Lorick, K., Wright, G. J., Ariza-McNaughton, L., Weissman, A. M., Lewis, J., Chandrasekharappa, S. C., Chitnis, A. B. (2003) Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta. Dev. Cell 4, 67-82.
20. Kanungo, J., Li, B. S., Goswami, M., Zheng, Y. L., Ramchandran, R., Pant, H. C. (2007) Cloning and characterization of zebrafish (Danio rerio) cyclin-dependent kinase 5. Neurosci. Lett. 412, 233-238.
21. Kanungo, J., Zheng, Y. L., Amin, N. D., Pant, H. C. (2008) The Notch signaling inhibitor DAPT down-regulates cdk5 activity and modulates the distribution of neuronal cytoskeletal proteins. J. Neurochem. 106, 2236-2248.
22. Kanungo, J., Zheng, Y. L., Amin, N. D., Kaur, S., Ramchandran, R., Pant, H. C. (2009) Specific inhibition of cyclindependent kinase 5 activity induces motor neuron development in vivo. Biochem. Biophys. Res. Commun. 386, 263-267.
23. Kim, C., Yun, N., Lee, J., Youdim, M., Ju, C., Kim, W. K., Han., P. L., Oh, Y. J. (2016) Phosphorylation of Chip at Ser20 by Cdk5 promotes tAIF-mediated neuronal death. Cell Death Differ. 23, 333-346.
24. 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.
25. Koo, B. K., Lim, H. S., Song, R., Yoon, M. J., Yoon, K. J., Moon, J. S., Kim, Y. W., Kwon, M. C., Yoo, K. W., Kong, M. P., Lee, J., Chitnis, A. B., Kim, C. H., Kong, Y. Y. (2005) Mind bomb 1 is essential for generating functional Notch ligands to activate Notch. Development 132, 3459-3470.
26. Kopan, R., Ilagan, M. X. (2009) The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137, 216-233.
27. Kwon, Y. T., Tsai, L. H., Crandall, J. E. (1999) Callosal axon guidance defects in p35(-/-) mice. J. Comp. Neurol. 415, 218-229.
28. Lai, E. C., Roegiers, F., Qin, X., Jan Y.N., Rubin, G. M. (2005) The ubiquitin ligase Drosophila Mind bomb promotes Notch signaling by regulating the localization and activity of Serrate and Delta. Development 132, 2319-2332.
29. Le Borgne, R., Bardin, A., Schweisguth, F. (2005) The roles of receptor and ligand endocytosis in regulating Notch signaling. Development 132, 1751-1762.
30. Liu, K. C., Leuckx, G., Sakano, D., Seymour, P. A., Mattsson, C. L., Rautio, L., Staels, W., Verdonck, Y., Serup, P., Kume, S., Heimberg, H., Andersson, O. (2018) Inhibition of Cdk5 promotes β-cell differentiation from ductal progenitors. Diabetes 67, 58-70.
31. Meloty-Kapella, L., Shergill, B., Kuon, J., Botvinick, E., Weinmaster, G. (2012) Notch ligand endocytosis generates mechanical pulling force dependent on dynamin, epsins, and actin. Dev. Cell 22, 1299-1312.
32. Merk, H., Zhang, S., Lehr, T., Muller, C., Ulrich, M., Bibb, J. A., Adams, R. H., Bracher, F., Zahler, S., Vollmar, A. M., Liebl, J. (2016) Inhibition of endothelial Cdk5 reduces tumor growth by promoting non-productive angiogenesis. Oncotarget 7, 6088-6104.
33. Meyerson, M., Enders, G. H., Wu, C. L., Su, L. K., Gorka, C., Nelson, C., Harlow, E., Tsai, L. H. (1992) A family of human cdc2-related protein kinases. EMBO J. 11, 2909-2917.
34. Miller, A. C., Lyons, E. L., Herman, T. G. (2009) cis-Inhibition of Notch by endogenous Delta biases the outcome of lateral inhibition. Curr. Biol. 19, 1378-1383.
35. 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 Dev. 10, 816-825.
36. Ohshima, T., Ward, J. M., Huh, C. G., Longenecker, G., Veeranna, Pant, H. C., Brady, R. O., Martin, L. J., 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. USA 93, 11173-11178.
37. 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, 615-622.
38. Pavlopoulos, E., Pitsouli, C., Klueg, K. M., Muskavitch, M. A., Moschonas, N. K., Delidakis, C. (2001) Neuralized encodes a peripheral membrane protein involved in delta signaling and endocytosis. Dev. Cell 1, 807-816.
39. Pitsouli, C., Delidakis, C. (2005) The interplay between DSL proteins and ubiquitin ligases in Notch signaling. Development 132, 4041-4050.
40. Redmond, L., Oh, S. R., Hicks, C., Weinmaster, G., Ghosh, A. (2000) Nuclear Notch1 signaling and the regulation of dendritic development. Nat. Neurosci. 3, 30-40.
41. Sestan, N., Artavanis-Tsakonas, S., Rakic, P. (1999) Contactdependent inhibition of cortical neurite growth mediated by notch signaling. Science 286, 741-746.
42. Shelton, S. B., Johnson, G. V. (2004) Cyclin-dependent kinase- 5 in neurodegeneration. J. Neurochem. 88, 1313-1326.
43. Sprinzak, D., Lakhanpal, A., Lebon, L., Santat, L. A., Fontes, M. E., Anderson, G. A., Garcia-Ojalvo, J., Elowitz, M. B. (2010) Cis-interactions between Notch and Delta generate mutually exclusive signalling states. Nature 465, 86-90.
44. Tanaka, T., Veeranna, Ohshima, T., Rajan, P., Amin, N. D., Cho, A., Sreenath, T., Pant, H. C., Brady, R. O., Kulkarni, A. B. (2001) Neuronal cyclin-dependent kinase 5 activity is critical for survival. J. Neurosci. 21, 550-558.
45. Tang, Z., Shu, H., Oncel, D., Chen, S., Yu, H. (2004) Phosphorylation of Cdc20 by Bub1 provides a catalytic mechanism for APC/C inhibition by the spindle checkpoint. Mol. Cell 16, 387-397.
46. Veeranna, Amin, N. D., Ahn, N.G, Jaffe H, Winters, C. A., Grant, P., Pant, H. C. (1998) Mitogen-activated protein kinases (Erk1,2) phosphorylate Lys-Ser-Pro (KSP) repeats in neurofilament proteins NF-H and NF-M. J. Neurosci. 18, 4008-4021.
47. Wang, W., Struhl, G. (2005) Distinct roles for Mind bomb, neuralized and epsin in mediating DSL endocytosis and signaling in Drosophila. Development 132, 2883-2894.
48. Wang, Y., Xie, W. Y., He, Y., Wang, M., Yang, Y. R., Zhang, Y., Yin, D. M., Jordan-Sciutto, K. L., Han, J. S., Wang, Y. (2006) Role of CDK5 in neuroprotection from serum deprivation by μ-opioid receptor agonist. Exp. Neurol. 202, 313-323.
49. Weinmaster, G., Kintner, C. (2003) Modulation of notch signaling during somitogenesis. Annu. Rev. Cell. Dev. Biol. 19, 367-395.
50. Weinmaster, G., Fischer, J. A. (2011) Notch ligand ubiquitylation: what is it good for? Dev. Cell 21, 134-144.
51. Yeh, E., Dermer, M., Commisso, C., Zhou, L., McGlade, C. J., Boulianne, GL. (2001) Neuralized functions as an E3 ubiquitin ligase during Drosophila development. Curr. Biol. 11, 1675-1679.
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