Cdk5 regulates EphA4-mediated dendritic spine retraction through an ephexin1-dependent mechanism

Nature Neuroscience

Volumn 10, Issue 1, 2007, Pages 67-76

  Fu, Wing Yu ^a   Chen, Yu ^a   Sahin, Mustafa ^b,c   Zhao, Xiao Su ^a   Shi, Lei ^a   Bikoff, Jay B ^b,c   Lai, Kwok On ^a   Yung, Wing Ho ^d   Fu, Amy K Y ^a   Greenberg, Michael E ^b,c   Ip, Nancy Y ^a  

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

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 5; EPHEXIN1 PROTEIN; EPHRIN RECEPTOR A4; GUANINE NUCLEOTIDE EXCHANGE FACTOR; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BRAIN; CONTROLLED STUDY; CYTOSKELETON; DENDRITIC SPINE; ENZYME ACTIVATION; ENZYME ACTIVITY; HIPPOCAMPUS; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; SYNAPSE;

ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE 5; DENDRITIC SPINES; EMBRYO; ENZYME ACTIVATION; EXCITATORY POSTSYNAPTIC POTENTIALS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; LUMINESCENT PROTEINS; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEURONS; PATCH-CLAMP TECHNIQUES; PHOSPHORYLATION; RECEPTOR, EPHA1; RECEPTOR, EPHA4; RHOA GTP-BINDING PROTEIN; TRANSFECTION; TYROSINE;

EID: 33845899093     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1811     Document Type: Article

References (50)

1. Ethell, I.M. & Pasquale, E.B.Molecular mechanisms of dendritic spine development and remodeling. Prog. Neurobiol. 75, 161-205 (2005).
2. Henkemeyer, M., Itkis, O.S., Ngo, M., Hickmott, P.W. & Ethell, I.M. Multiple EphB receptor tyrosine kinases shape dendritic spines in the hippocampus. J. Cell Biol. 163, 1313-1326 (2003).
3. Contractor, A. et al. Trans-synaptic Eph receptor-ephrin signaling in hippocampal mossy fiber LTP. Science 296, 1864-1869 (2002).
4. Grunwald, I.C. et al. Hippocampal plasticity requires postsynaptic ephrinBs. Nat. Neurosci. 7, 33-40 (2004).
5. O'Leary, D.D. & Wilkinson, D.G. Eph receptors and ephrins in neural development. Curr. Opin. Neurobiol. 9, 65-73 (1999).
6. Wilkinson, D.G. Multiple roles of EPH receptors and ephrins in neural development. Nat. Rev. Neurosci. 2, 155-164 (2001).
7. Gerlai, R. Eph receptors and neural plasticity. Nat. Rev. Neurosci. 2, 205-209 (2001).
8. Henderson, J.T. et al. The receptor tyrosine kinase EphB2 regulates NMDA-dependent synaptic function. Neuron 32, 1041-1056 (2001).
9. Murai, K.K., Nguyen, L.N., Irie, F., Yamaguchi, Y. & Pasquale, E.B. Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling. Nat. Neurosci. 6, 153-160 (2003).
10. Dalva, M.B. et al. EphB receptors interact with NMDA receptors and regulate excitatory synapse formation. Cell 103, 945-956 (2000).
11. Penzes, P. et al. Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin. Neuron 37, 263-274 (2003).
12. Murai, K.K. & Pasquale, E.B. New exchanges in eph-dependent growth cone dynamics. Neuron 46, 161-163 (2005).
13. Nakayama, A.Y., Harms, M.B. & Luo, L. Small GTPases Rac and Rho in the maintenance of dendritic spines and branches in hippocampal pyramidal neurons. J. Neurosci. 20, 5329-5338 (2000).
14. Irie, F. & Yamaguchi, Y. EphB receptors regulate dendritic spine development via intersectin, Cdc42 and N-WASP. Nat. Neurosci. 5, 1117-1118 (2002).
15. Morabito, M.A., Sheng, M. & Tsai, L.H. Cyclin-dependent kinase 5 phosphorylates the N-terminal domain of the postsynaptic density protein PSD-95 in neurons. J.Neurosci. 24, 865-876 (2004).
16. Zukerberg, L.R. et al. Cables links Cdk5 and c-Abl and facilitates Cdk5 tyrosine phosphorylation, kinase upregulation, and neurite outgrowth. Neuron 26, 633-646 (2000).
17. Sasaki, Y. et al. Fyn and Cdk5 mediate semaphorin-3A signaling, which is involved in regulation of dendrite orientation in cerebral cortex. Neuron 35, 907-920 (2002).
18. Fu, A.K. et al. Cdk5 is involved in neuregulin-induced AChR expression at the neuromuscular junction. Nat. Neurosci. 4, 374-381 (2001).
19. Yamaguchi, Y. & Pasquale, E.B. Eph receptors in the adult brain. Curr. Opin. Neurobiol. 14, 288-296 (2004).
20. Flanagan, J.G. & Vanderhaeghen, P. The ephrins and Eph receptors in neural development. Annu. Rev. Neurosci. 21, 309-345 (1998).
21. Ching, Y.P., Qi, Z. & Wang, J.H. Cloning of three novel neuronal Cdk5 activator binding proteins. Gene 242, 285-294 (2000).
22. Cheng, K. & Ip, N.Y. Cdk5: a new player at synapses. Neurosignals 12, 180-190 (2003).
23. Knoll, B. & Drescher, U. Src family kinases are involved in EphA receptor-mediated retinal axon guidance. J. Neurosci. 24, 6248-6257 (2004).
24. Sahin, M. et al. Eph-dependent tyrosine phosphorylation of ephexin1 modulates growth cone collapse. Neuron 46, 191-204 (2005).
25. Cowan, C.W. et al. Vav family GEFs link activated Ephs to endocytosis and axon guidance. Neuron 46, 205-217 (2005).
26. Tolias, K.F. et al. The Rac1-GEF Tiam1 couples the NMDA receptor to the activity-dependent development of dendritic arbors and spines. Neuron 45, 525-538 (2005).
27. Cheng, Q. et al. Cdk5/p35 and Rho-kinase mediate ephrin-A5-induced signaling in retinal ganglion cells. Mol. Cell. Neurosci. 24, 632-645 (2003).
28. Egea, J. et al. Regulation of EphA 4 kinase activity is required for a subset of axon guidance decisions suggesting a key role for receptor clustering in Eph function. Neuron 47, 515-528 (2005).
29. Ehlers, M.D. Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat. Neurosci. 6, 231-242 (2003).
30. Lai, K.O., Ip, F.C., Cheung, J., Fu, A.K. & Ip, N.Y. Expression of Eph receptors in skeletal muscle and their localization at the neuromuscular junction. Mol. Cell. Neurosci. 17, 1034-1047 (2001).
31. Hall, A. Rho GTPases and the actin cytoskeleton. Science 279, 509-514 (1998).
32. Shamah, S.M. et al. EphA receptors regulate growth cone dynamics through the novel guanine nucleotide exchange factor ephexin. Cell 105, 233-244 (2001).
33. Dhavan, R. & Tsai, L.H. A decade of CDK5. Nat. Rev.Mol. Cell Biol. 2, 749-759 (2001).
34. Cheung, Z.H., Fu, A.K.Y. & Ip, N.Y. Synaptic roles of Cdk5: implications in higher cognitive functions and neurodegenerative diseases. Neuron 50, 13-18 (2006).
35. Fu, W.Y., Fu, A.K., Lok, K.C., Ip, F.C. & Ip, N.Y. Induction of Cdk5 activity in rat skeletal muscle after nerve injury. Neuroreport 13, 243-247 (2002).
36. Fu, A.K. et al. Aberrant motor axon projection, acetylcholine receptor clustering, and neurotransmission in cyclin-dependent kinase 5 null mice. Proc. Natl. Acad. Sci. USA 102, 15224-15229 (2005).
37. Yuste, R. & Bonhoeffer, T. Genesis of dendritic spines: insights from ultrastructural and imaging studies. Nat. Rev. Neurosci. 5, 24-34 (2004).
38. Bryan, B. et al. GEFT, a Rho family guanine nucleotide exchange factor, regulates neurite outgrowth and dendritic spine formation. J. Biol. Chem. 279, 45824-45832 (2004).
39. Ryan, X.P. et al. The Rho-specific GEF Lfc interacts with neurabin and spinophilin to regulate dendritic spine morphology. Neuron 47, 85-100 (2005).
40. Zhang, H., Webb, D.J., Asmussen, H., Niu, S. & Horwitz, A.F.A. GIT1/PIX/Rac/PAK signaling module regulates spine morphogenesis and synapse formation through MLC. J. Neurosci. 25, 3379-3388 (2005).
41. Ohshima, T. et al. Impairment of hippocampal long-term depression and defective spatial learning and memory in p35 mice. J. Neurochem. 94, 917-925 (2005).
42. Kennedy, M.B., Beale, H.C., Carlisle, H.J. & Washburn, L.R. Integration of biochemical signalling in spines. Nat. Rev. Neurosci. 6, 423-434 (2005).
43. Muller, D., Toni, N. & Buchs, P.A. Spine changes associated with long-term potentiation. Hippocampus 10, 596-604 (2000).
44. Toni, N., Buchs, P.A., Nikonenko, I., Bron, C.R. & Muller, D. LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 402, 421-425 (1999).
45. Engert, F. & Bonhoeffer, T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66-70 (1999).
46. Zhou, Q., Homma, K.J. & Poo, M.M. Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44, 749-757 (2004).
47. Nagerl, U.V., Eberhorn, N., Cambridge, S.B. & Bonhoeffer, T. Bidirectional activity-dependent morphological plasticity in hippocampal neurons. Neuron 44, 759-767 (2004).
48. Gerlai, R. et al. Regulation of learning by EphA receptors: a protein targeting study. J. Neurosci. 19, 9538-9549 (1999).
49. Ip, N.Y., Li, Y., Yancopoulos, G.D. & Lindsay, R.M. Cultured hippocampal neurons show responses to BDNF, NT-3, and NT-4, but not NGF. J. Neurosci. 13, 3394-3405 (1993).
50. Sala, C. et al. Regulation of dendritic spine morphology and synaptic function by Shank and Homer. Neuron 31, 115-130 (2001).