Cyclin-Dependent Kinase 5 in Axon Growth and Regeneration

International Review of Neurobiology

Volumn 105, Issue , 2012, Pages 91-115

  Ye, Tao ^a   Fu, Amy K Y ^a   Ip, Nancy Y ^a  

^a HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

Author keywords

Axon damage; Axon regeneration; Axonal transport; Cytoskeleton; Kinase; Neurotrophin; Protein degradation; Protein translation

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CYCLIN DEPENDENT KINASE 5; GUANOSINE TRIPHOSPHATASE; JANUS KINASE 2; MESSENGER RNA; NERVE GROWTH FACTOR; NEUROMODULIN; NEUROTROPHIN; NEUROTROPHIN 3; NEUROTROPHIN 4; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN CDC42; PROTEIN TYROSINE KINASE A; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; STAT3 PROTEIN; UVOMORULIN;

ARTICLE; BRAIN DEVELOPMENT; BRAIN FUNCTION; CELL CYCLE PROGRESSION; CENTRAL NERVOUS SYSTEM; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NERVE FIBER TRANSPORT; NERVOUS SYSTEM INJURY; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SPINAL GANGLION; TRANSCRIPTION ELONGATION;

EID: 84872418394     PISSN: 00747742     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-398309-1.00006-8     Document Type: Chapter

References (95)

1. Alilain W.J., Horn K.P., Hu H., Dick T.E., Silver J. Functional regeneration of respiratory pathways after spinal cord injury. Nature 2011, 475:196-200.
2. Atwal J.K., Pinkston-Gosse J., Syken J., Stawicki S., Wu Y., Shatz C., et al. PirB is a functional receptor for myelin inhibitors of axonal regeneration. Science 2008, 322:967-970.
3. Beaudette K.N., Lew J., Wang J.H. Substrate specificity characterization of a cdc2-like protein kinase purified from bovine brain. The Journal of Biological Chemistry 1993, 268:20825-20830.
4. Bloom O.E., Morgan J.R. Membrane trafficking events underlying axon repair, growth, and regeneration. Molecular and Cellular Neurosciences 2011, 48:339-348.
5. Boyd J.G., Gordon T. The neurotrophin receptors, trkB and p75, differentially regulate motor axonal regeneration. Journal of Neurobiology 2001, 49:314-325.
6. Bradke F., Dotti C.G. The role of local actin instability in axon formation. Science 1999, 283:1931-1934.
7. Bradke F., Fawcett J.W., Spira M.E. Assembly of a new growth cone after axotomy: The precursor to axon regeneration. Nature Reviews. Neuroscience 2012, 13:183-193.
8. Campbell D.S., Holt C.E. Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 2001, 32:1013-1026.
9. Cheng Q., Sasaki Y., Shoji M., Sugiyama Y., Tanaka H., Nakayama T., et al. Cdk5/p35 and Rho-kinase mediate ephrin-A5-induced signaling in retinal ganglion cells. Molecular and Cellular Neurosciences 2003, 24:632-645.
10. Cheung Z.H., Chin W.H., Chen Y., Ng Y.P., Ip N.Y. Cdk5 is involved in BDNF-stimulated dendritic growth in hippocampal neurons. PLoS Biology 2007, 5:e63.
11. Cheung Z.H., Fu A.K., Ip N.Y. Synaptic roles of Cdk5: Implications in higher cognitive functions and neurodegenerative diseases. Neuron 2006, 50:13-18.
12. Cheung Z.H., Gong K., Ip N.Y. Cyclin-dependent kinase 5 supports neuronal survival through phosphorylation of Bcl-2. The Journal of Neuroscience 2008, 28:4872-4877.
13. Cheung Z.H., Ip N.Y. Cdk5: A multifaceted kinase in neurodegenerative diseases. Trends in Cell Biology 2012, 22:169-175.
14. Chierzi S., Ratto G.M., Verma P., Fawcett J.W. The ability of axons to regenerate their growth cones depends on axonal type and age, and is regulated by calcium, cAMP and ERK. The European Journal of Neuroscience 2005, 21:2051-2062.
15. Conde C., Caceres A. Microtubule assembly, organization and dynamics in axons and dendrites. Nature Reviews. Neuroscience 2009, 10:319-332.
16. Del Rio J.A., Gonzalez-Billault C., Urena J.M., Jimenez E.M., Barallobre M.J., Pascual M., et al. MAP1B is required for Netrin 1 signaling in neuronal migration and axonal guidance. Current Biology 2004, 14:840-850.
17. Dhavan R., Tsai L.H. A decade of CDK5. Nature Reviews. Molecular Cell Biology 2001, 2:749-759.
18. Di Giovanni S., Knights C.D., Rao M., Yakovlev A., Beers J., Catania J., et al. The tumor suppressor protein p53 is required for neurite outgrowth and axon regeneration. The EMBO Journal 2006, 25:4084-4096.
19. Dill J., Wang H., Zhou F., Li S. Inactivation of glycogen synthase kinase 3 promotes axonal growth and recovery in the CNS. The Journal of Neuroscience 2008, 28:8914-8928.
20. Dillon C., Goda Y. The actin cytoskeleton: Integrating form and function at the synapse. Annual Review of Neuroscience 2005, 28:25-55.
21. El-Kadi A.M., Soura V., Hafezparast M. Defective axonal transport in motor neuron disease. Journal of Neuroscience Research 2007, 85:2557-2566.
22. Fang W.Q., Ip J.P., Li R., Ng Y.P., Lin S.C., Chen Y., et al. Cdk5-mediated phosphorylation of Axin directs axon formation during cerebral cortex development. The Journal of Neuroscience 2011, 31:13613-13624.
23. Fu W.Y., Chen Y., Sahin M., Zhao X.S., Shi L., Bikoff J.B., et al. Cdk5 regulates EphA4-mediated dendritic spine retraction through an ephexin1-dependent mechanism. Nature Neuroscience 2007, 10:67-76.
24. Fu A.K., Fu W.Y., Ng A.K., Chien W.W., Ng Y.P., Wang J.H., et al. Cyclin-dependent kinase 5 phosphorylates signal transducer and activator of transcription 3 and regulates its transcriptional activity. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:6728-6733.
25. Fu A.K., Ip F.C., Fu W.Y., Cheung J., Wang J.H., Yung W.H., et al. Aberrant motor axon projection, acetylcholine receptor clustering, and neurotransmission in cyclin-dependent kinase 5 null mice. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:15224-15229.
26. Giger R.J., Hollis E.R., Tuszynski M.H. Guidance molecules in axon regeneration. Cold Spring Harbor Perspectives in Biology 2010, 2:a001867.
27. Goldstein L.S., Yang Z. Microtubule-based transport systems in neurons: The roles of kinesins and dyneins. Annual Review of Neuroscience 2000, 23:39-71.
28. Harada T., Morooka T., Ogawa S., Nishida E. ERK induces p35, a neuron-specific activator of Cdk5, through induction of Egr1. Nature Cell Biology 2001, 3:453-459.
29. Hardy J. A hundred years of Alzheimer's disease research. Neuron 2006, 52:3-13.
30. Hay N., Sonenberg N. Upstream and downstream of mTOR. Genes & Development 2004, 18:1926-1945.
31. Hellal F., Hurtado A., Ruschel J., Flynn K.C., Laskowski C.J., Umlauf M., et al. Microtubule stabilization reduces scarring and causes axon regeneration after spinal cord injury. Science 2011, 331:928-931.
32. Hollis E.R., Jamshidi P., Low K., Blesch A., Tuszynski M.H. Induction of corticospinal regeneration by lentiviral trkB-induced Erk activation. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:7215-7220.
33. Hou Z., He L., Qi R.Z. Regulation of s6 kinase 1 activation by phosphorylation at ser-411. The Journal of Biological Chemistry 2007, 282:6922-6928.
34. Huynh M.A., Stegmuller J., Litterman N., Bonni A. Regulation of Cdh1-APC function in axon growth by Cdh1 phosphorylation. The Journal of Neuroscience 2009, 29:4322-4327.
35. Janke C., Kneussel M. Tubulin post-translational modifications: Encoding functions on the neuronal microtubule cytoskeleton. Trends in Neurosciences 2010, 33:362-372.
36. Jiang H., Guo W., Liang X., Rao Y. Both the establishment and the maintenance of neuronal polarity require active mechanisms: Critical roles of GSK-3beta and its upstream regulators. Cell 2005, 120:123-135.
37. Jovanovic J.N., Sihra T.S., Nairn A.C., Hemmings H.C., Greengard P., Czernik A.J. Opposing changes in phosphorylation of specific sites in synapsin I during Ca2+-dependent glutamate release in isolated nerve terminals. The Journal of Neuroscience 2001, 21:7944-7953.
38. Kadoya K., Tsukada S., Lu P., Coppola G., Geschwind D., Filbin M.T., et al. Combined intrinsic and extrinsic neuronal mechanisms facilitate bridging axonal regeneration one year after spinal cord injury. Neuron 2009, 64:165-172.
39. Kawauchi T., Chihama K., Nabeshima Y., Hoshino M. Cdk5 phosphorylates and stabilizes p27kip1 contributing to actin organization and cortical neuronal migration. Nature Cell Biology 2006, 8:17-26.
40. Kesavapany S., Amin N., Zheng Y.L., Nijhara R., Jaffe H., Sihag R., et al. p35/cyclin-dependent kinase 5 phosphorylation of ras guanine nucleotide releasing factor 2 (RasGRF2) mediates Rac-dependent Extracellular Signal-regulated kinase 1/2 activity, altering RasGRF2 and microtubule-associated protein 1b distribution in neurons. The Journal of Neuroscience 2004, 24:4421-4431.
41. Kesavapany S., Pareek T.K., Zheng Y.L., Amin N., Gutkind J.S., Ma W., et al. Neuronal nuclear organization is controlled by cyclin-dependent kinase 5 phosphorylation of Ras Guanine nucleotide releasing factor-1. Neuro-Signals 2006, 15:157-173.
42. Kim Y., Sung J.Y., Ceglia I., Lee K.W., Ahn J.H., Halford J.M., et al. Phosphorylation of WAVE1 regulates actin polymerization and dendritic spine morphology. Nature 2006, 442:814-817.
43. Ko J., Humbert S., Bronson R.T., Takahashi S., Kulkarni A.B., Li E., et al. p35 and p39 are essential for cyclin-dependent kinase 5 function during neurodevelopment. The Journal of Neuroscience 2001, 21:6758-6771.
44. Konishi Y., Stegmuller J., Matsuda T., Bonni S., Bonni A. Cdh1-APC controls axonal growth and patterning in the mammalian brain. Science 2004, 303:1026-1030.
45. Koprivica V., Cho K.S., Park J.B., Yiu G., Atwal J., Gore B., et al. EGFR activation mediates inhibition of axon regeneration by myelin and chondroitin sulfate proteoglycans. Science 2005, 310:106-110.
46. Lalioti V., Pulido D., Sandoval I.V. Cdk5, the multifunctional surveyor. Cell Cycle 2010, 9:284-311.
47. Lasorella A., Stegmuller J., Guardavaccaro D., Liu G., Carro M.S., Rothschild G., et al. Degradation of Id2 by the anaphase-promoting complex couples cell cycle exit and axonal growth. Nature 2006, 442:471-474.
48. Lee J.H., Kim H.S., Lee S.J., Kim K.T. Stabilization and activation of p53 induced by Cdk5 contributes to neuronal cell death. Journal of Cell Science 2007, 120:2259-2271.
49. Levy D.E., Darnell J.E. Stats: Transcriptional control and biological impact. Nature Reviews. Molecular Cell Biology 2002, 3:651-662.
50. Lew J., Winkfein R.J., Paudel H.K., Wang J.H. Brain proline-directed protein kinase is a neurofilament kinase which displays high sequence homology to p34cdc2. The Journal of Biological Chemistry 1992, 267:25922-25926.
51. Li C., Sasaki Y., Takei K., Yamamoto H., Shouji M., Sugiyama Y., et al. Correlation between semaphorin3A-induced facilitation of axonal transport and local activation of a translation initiation factor eukaryotic translation initiation factor 4E. The Journal of Neuroscience 2004, 24:6161-6170.
52. Liu Y., Cheng K., Gong K., Fu A.K., Ip N.Y. Pctaire1 phosphorylates N-ethylmaleimide-sensitive fusion protein: Implications in the regulation of its hexamerization and exocytosis. The Journal of Biological Chemistry 2006, 281:9852-9858.
53. Liu K., Lu Y., Lee J.K., Samara R., Willenberg R., Sears-Kraxberger I., et al. PTEN deletion enhances the regenerative ability of adult corticospinal neurons. Nature Neuroscience 2010, 13:1075-1081.
54. Liu K., Tedeschi A., Park K.K., He Z. Neuronal intrinsic mechanisms of axon regeneration. Annual Review of Neuroscience 2011, 34:131-152.
55. Maestre C., Delgado-Esteban M., Gomez-Sanchez J.C., Bolanos J.P., Almeida A. Cdk5 phosphorylates Cdh1 and modulates cyclin B1 stability in excitotoxicity. The EMBO Journal 2008, 27:2736-2745.
56. Meyerson M., Enders G.H., Wu C.L., Su L.K., Gorka C., Nelson C., et al. A family of human cdc2-related protein kinases. The EMBO Journal 1992, 11:2909-2917.
57. Moore D.L., Blackmore M.G., Hu Y., Kaestner K.H., Bixby J.L., Lemmon V.P., et al. KLF family members regulate intrinsic axon regeneration ability. Science 2009, 326:298-301.
58. Morfini G., Szebenyi G., Brown H., Pant H.C., Pigino G., DeBoer S., et al. A novel CDK5-dependent pathway for regulating GSK3 activity and kinesin-driven motility in neurons. The EMBO Journal 2004, 23:2235-2245.
59. Namgung U., Choi B.H., Park S., Lee J.U., Seo H.S., Suh B.C., et al. Activation of cyclin-dependent kinase 5 is involved in axonal regeneration. Molecular and Cellular Neurosciences 2004, 25:422-432.
60. Ng Y.P., Cheung Z.H., Ip N.Y. STAT3 as a downstream mediator of Trk signaling and functions. The Journal of Biological Chemistry 2006, 281:15636-15644.
61. Niethammer M., Smith D.S., Ayala R., Peng J., Ko J., Lee M.S., et al. NUDEL is a novel Cdk5 substrate that associates with LIS1 and cytoplasmic dynein. Neuron 2000, 28:697-711.
62. Nikolic M., Chou M.M., Lu W., Mayer B.J., Tsai L.H. The p35/Cdk5 kinase is a neuron-specific Rac effector that inhibits Pak1 activity. Nature 1998, 395:194-198.
63. North B.J., Marshall B.L., Borra M.T., Denu J.M., Verdin E. The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase. Molecular Cell 2003, 11:437-444.
64. O'Donnell M., Chance R.K., Bashaw G.J. Axon growth and guidance: Receptor regulation and signal transduction. Annual Review of Neuroscience 2009, 32:383-412.
65. Ohshima T., Ward J.M., Huh C.G., Longenecker G., Veeranna, Pant H.C., et al. Targeted disruption of the cyclin-dependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death. Proceedings of the National Academy of Sciences of the United States of America 1996, 93:11173-11178.
66. Paglini G., Pigino G., Kunda P., Morfini G., Maccioni R., Quiroga S., et al. Evidence for the participation of the neuron-specific CDK5 activator P35 during laminin-enhanced axonal growth. The Journal of Neuroscience 1998, 18:9858-9869.
67. Pandithage R., Lilischkis R., Harting K., Wolf A., Jedamzik B., Luscher-Firzlaff J., et al. The regulation of SIRT2 function by cyclin-dependent kinases affects cell motility. The Journal of Cell Biology 2008, 180:915-929.
68. Park K.K., Liu K., Hu Y., Smith P.D., Wang C., Cai B., et al. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 2008, 322:963-966.
69. Patrick G.N., Zukerberg L., Nikolic M., de la Monte S., Dikkes P., Tsai L.H. Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 1999, 402:615-622.
70. Polleux F., Snider W. Initiating and growing an axon. Cold Spring Harbor Perspectives in Biology 2010, 2:a001925.
71. Qi R.Z., Ching Y.P., Kung H.F., Wang J.H. Alpha-chimaerin exists in a functional complex with the Cdk5 kinase in brain. FEBS Letters 2004, 561:177-180.
72. Qiu J., Cafferty W.B., McMahon S.B., Thompson S.W. Conditioning injury-induced spinal axon regeneration requires signal transducer and activator of transcription 3 activation. The Journal of Neuroscience 2005, 25:1645-1653.
73. Rashid T., Banerjee M., Nikolic M. Phosphorylation of Pak1 by the p35/Cdk5 kinase affects neuronal morphology. The Journal of Biological Chemistry 2001, 276:49043-49052.
74. Sasaki Y., Cheng C., Uchida Y., Nakajima O., Ohshima T., Yagi T., et al. Fyn and Cdk5 mediate semaphorin-3A signaling, which is involved in regulation of dendrite orientation in cerebral cortex. Neuron 2002, 35:907-920.
75. Sasaki S., Shionoya A., Ishida M., Gambello M.J., Yingling J., Wynshaw-Boris A., et al. A LIS1/NUDEL/cytoplasmic dynein heavy chain complex in the developing and adult nervous system. Neuron 2000, 28:681-696.
76. Schalm S.S., Tee A.R., Blenis J. Characterization of a conserved C-terminal motif (RSPRR) in ribosomal protein S6 kinase 1 required for its mammalian target of rapamycin-dependent regulation. The Journal of Biological Chemistry 2005, 280:11101-11106.
77. Sengottuvel V., Leibinger M., Pfreimer M., Andreadaki A., Fischer D. Taxol facilitates axon regeneration in the mature CNS. The Journal of Neuroscience 2011, 31:2688-2699.
78. Shen Y., Tenney A.P., Busch S.A., Horn K.P., Cuascut F.X., Liu K., et al. PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 2009, 326:592-596.
79. Smith P.D., Sun F., Park K.K., Cai B., Wang C., Kuwako K., et al. SOCS3 deletion promotes optic nerve regeneration in vivo. Neuron 2009, 64:617-623.
80. Stegmuller J., Konishi Y., Huynh M.A., Yuan Z., Dibacco S., Bonni A. Cell-intrinsic regulation of axonal morphogenesis by the Cdh1-APC target SnoN. Neuron 2006, 50:389-400.
81. Su S.C., Tsai L.H. Cyclin-dependent kinases in brain development and disease. Annual Review of Cell and Developmental Biology 2011, 27:465-491.
82. Sun F., He Z. Neuronal intrinsic barriers for axon regeneration in the adult CNS. Current Opinion in Neurobiology 2010, 20:510-518.
83. Sun F., Park K.K., Belin S., Wang D., Lu T., Chen G., et al. Sustained axon regeneration induced by co-deletion of PTEN and SOCS3. Nature 2011, 480:372-375.
84. Suzuki K., Koike T. Mammalian Sir2-related protein (SIRT) 2-mediated modulation of resistance to axonal degeneration in slow Wallerian degeneration mice: A crucial role of tubulin deacetylation. Neuroscience 2007, 147:599-612.
85. Tanaka T., Serneo F.F., Tseng H.C., Kulkarni A.B., Tsai L.H., Gleeson J.G. Cdk5 phosphorylation of doublecortin ser297 regulates its effect on neuronal migration. Neuron 2004, 41:215-227.
86. Tsai S.Y., Yang L.Y., Wu C.H., Chang S.F., Hsu C.Y., Wei C.P., et al. Injury-induced Janus kinase/protein kinase C-dependent phosphorylation of growth-associated protein 43 and signal transducer and activator of transcription 3 for neurite growth in dorsal root ganglion. Journal of Neuroscience Research 2007, 85:321-331.
87. Verma P., Chierzi S., Codd A.M., Campbell D.S., Meyer R.L., Holt C.E., et al. Axonal protein synthesis and degradation are necessary for efficient growth cone regeneration. The Journal of Neuroscience 2005, 25:331-342.
88. Wada Y., Ishiguro K., Itoh T.J., Uchida T., Hotani H., Saito T., et al. Microtubule-stimulated phosphorylation of tau at Ser202 and Thr205 by cdk5 decreases its microtubule nucleation activity. Journal of Biochemistry 1998, 124:738-746.
89. Xin X., Wang Y., Ma X.M., Rompolas P., Keutmann H.T., Mains R.E., et al. Regulation of Kalirin by Cdk5. Journal of Cell Science 2008, 121:2601-2611.
90. Yan Z., Chi P., Bibb J.A., Ryan T.A., Greengard P. Roscovitine: A novel regulator of P/Q-type calcium channels and transmitter release in central neurons. The Journal of Physiology 2002, 540:761-770.
91. Yan D., Guo L., Wang Y. Requirement of dendritic Akt degradation by the ubiquitin-proteasome system for neuronal polarity. The Journal of Cell Biology 2006, 174:415-424.
92. Yin Y., Henzl M.T., Lorber B., Nakazawa T., Thomas T.T., Jiang F., et al. Oncomodulin is a macrophage-derived signal for axon regeneration in retinal ganglion cells. Nature Neuroscience 2006, 9:843-852.
93. Yoon B.C., Jung H., Dwivedy A., O'Hare C.M., Zivraj K.H., Holt C.E. Local translation of extranuclear lamin B promotes axon maintenance. Cell 2012, 148:752-764.
94. Yoshimura T., Kawano Y., Arimura N., Kawabata S., Kikuchi A., Kaibuchi K. GSK-3beta regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 2005, 120:137-149.
95. Zhang P., Yu P.C., Tsang A.H., Chen Y., Fu A.K., Fu W.Y., et al. S-nitrosylation of cyclin-dependent kinase 5 (cdk5) regulates its kinase activity and dendrite growth during neuronal development. The Journal of Neuroscience 2010, 30:14366-14370.