Cdk5 activation induces hippocampal CA1 cell death by directly phosphorylating NMDA receptors

Nature Neuroscience

Volumn 6, Issue 10, 2003, Pages 1039-1047

  Wang, Jian ^a   Liu, ShuHong ^a   Fu, YangPing ^a   Wang, Jerry H ^a   Lu, YouMing ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 5; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; RECEPTOR SUBUNIT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; CATALYSIS; CELL DAMAGE; CELL PROTECTION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME MECHANISM; FOREBRAIN; HIPPOCAMPUS; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PYRAMIDAL NERVE CELL; RAT;

AMINO ACID SEQUENCE; ANIMALS; BRAIN ISCHEMIA; CELL DEATH; CYCLIN-DEPENDENT KINASE 5; CYCLIN-DEPENDENT KINASES; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GENETIC VECTORS; HIPPOCAMPUS; MUTATION; NERVE DEGENERATION; ORGAN CULTURE TECHNIQUES; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; RECOMBINANT FUSION PROTEINS; REPERFUSION INJURY; SERINE;

EID: 0141542665     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1119     Document Type: Article

References (50)

1. Nakatomi, H. et al. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110, 429-441 (2002).
2. Jover, T. et al. Estrogen protects against global ischemia-induced neuronal death and prevents activation of apoptotic signaling cascades in the hippocampal CA1. J. Neurosci. 22, 2115-2124 (2002).
3. Choi, D. W. Calcium-mediated neurotoxicity: relationship to specific channel types and role in ischemic damage. Trends Neurosci. 11, 465-469 (1988).
4. Choi, D.W. Calcium: still center-stage in hypoxic-ischemic neuronal death. Trends Neurosci. 18, 58-60 (1995).
5. Simon, R.P., Swan, J.H., Griffiths, T. & Meldrum, B.S. Blockade of N-methyl-D-aspartate receptors may protect against ischemic damage in the brain. Science 226, 850-852 (1984).
6. Faden, A.I., Demediuk, P., Panter, S.S. & Vink, R. The role of excitatory amino acids and NMDA receptors in traumatic brain injury. Science 244, 798-800 (1989).
7. Sattler, R. & Tymianski, M. Molecular mechanisms of glutamate receptor-mediated excitotoxic neuronal cell death. Mol. Neurobiol. 24, 107-129 (2001).
8. Hollmann, M. & Heinemann, S. Cloned glutamate receptors. Annu. Rev. Neurosci. 17, 31-108 (1994).
9. Kutsuwada, T. et al. Molecular diversity of the NMDA receptor channel. Nature 358, 36-41 (1992).
10. Meguro, H. et al. Functional characterization of a heteromeric NMDA receptor channel expressed from cloned cDNAs. Nature 357, 70-704 (1992).
11. Monyer, H. et al. Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256, 1217-1221 (1992).
12. Cull-Candy, S., Brickley, S. & Farrant, M. NMDA receptor subunits: diversity, development and disease. Curr. Opin. Neurobiol. 11, 327-335 (2001).
13. Abel, T. & Lattal, K.M. Molecular mechanisms of memory acquisition, consolidation and retrieval. Curr. Opin. Neurobiol. 11, 180-187 (2001).
14. Lee, J.M., Zipfel, G.J. & Choi, D.W. The changing landscape of ischaemic brain injury mechanisms. Nature 399 (Suppl.), A7-14 (1999).
15. Meldrum, B. & Garthwaite, J. Excitatory amino acid neurotoxicity and neurodegenerative diseases. Trends Pharmacol. Sci. 11, 379-387 (1990).
16. Scannevin, R.H. & Huganir, R.L. Postsynaptic organization and regulation of excitatory synapses. Nat. Rev. Neurosci. 1,133-141 (2000).
17. Ali, D.W & Salter, M.W. NMDA receptor regulation by Src kinase signalling in excitatory synaptic transmission and plasticity. Curr. Opin. Neurobiol. 11, 336-342 (2001).
18. Li, B. S. et al. Regulation of NMDA receptors by cyclin-dependent kinase-5. Proc. Natl. Acad. Sci. USA 98, 12742-12747 (2001).
19. Lew, J., Beaudette, K., Litwin, C.M. & Wang, J. H. Purification and characterization of a novel proline-directed protein kinase from bovine brain. J. Biol. Chem. 267, 13383-13390 (1992).
20. Tsai, L.H., Delalle, I., Caviness, V.S., Chae, T. & Harlow, E. p35 is a neural-specific regulatory subunit of cyclin-dependent kinase 5. Nature 371, 419-423 (1994).
21. Greengard, P., Allen, P.B. & Nairn, A. C. Beyond the dopamine receptor: the DARPP-32/protein phosphatase-1 cascade. Neuron 23, 435-447 (1999).
22. Chae, T. et al. Mice lacking p35, a neuronal specific activator of Cdk5, display cortical lamination defects, seizures, and adult lethality. Neuron 18, 29-42 (1997).
23. Patrick, G. et al. Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 402, 615-622 (1999).
24. Nguyen, M.D., Larivirre, R.C. & Julien, J.P. Deregulation of Cdk5 in a mouse model of ALS: toxicity alleviated by perikaryal neurofilament inclusions. Neuron 30, 135-147 (2001).
25. Lee, M.S., Kwon, Y.T., Li, M., Peng, J., Friedlander, R.M. & Tsai, L.H. Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature 405, 360-364 (2000).
26. Ohshima, T. et al. 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 (1996).
27. Nikolic, M., Dudek, H., Kwon, Y.T., Ramos, Y.F. & Tsai, L. H. The Cdk5/p35 kinase is essential for neurite outgrowth during neuronal differentiation. Genes Dev. 10, 816-825 (1996).
28. Barria, A. & Malinow, R. Subunit-specific NMDA receptor trafficking to synapses. Neuron 35, 345-353 (2002).
29. Carroll, R.C. & Zukin, R.S. NMDA-receptor trafficking and targeting: implications for synaptic transmission and plasticity. Trends Neurosci. 25, 571-577 (2002).
30. Gong, X. et al. Cdk5-mediated inhibition of the protective effects of transcription factor MEF2 in neurotoxicity-induced apoptosis. Neuron 38, 33-46 (2003).
31. Mitani, A. et al. Postischemic enhancements of N-methyl-D-aspartic acid (NMDA) and non-NMDA receptor-mediated responses in hippocampal CA1 pyramidal neurons. J. Cereb. Blood Flow Metab. 18, 1088-1098 (1998).
32. Andine, P., Jacobson, I. & Hagberg, H. Calcium uptake evoked by electrical stimulation is enhanced postischemically and precedes delayed neuronal death in CA1 of rat hippocampus: involvement of N-methyl-D-aspartate receptors. J. Cereb. Blood Flow. Metab. 8, 799-807 (1988).
33. Kirino, T. Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res. 239, 57-69 (1982).
34. Benveniste, H., Drejer, J., Schousboe, A. & Diemer, N.H. Elevation of the extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis. J. Neurochem. 43, 1369-1374 (1984).
35. Hagberg, H. et al. Ischemia-induced shift of inhibitory and excitatory amino acids from intra- to extracellular compartments. J. Cereb. Blood Flow Metab. 5, 413-419 (1985).
36. Migaud, M. et al. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature 396, 433-439 (1998).
37. Brenman, J.E. et al. Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and alpha1-syntrophin mediated by PDZ domains. Cell 84, 757-767 (1996).
38. Dawson, V.L., Dawson, T.M., London, E.D., Bredt, D.S. & Snyder, S.H. Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc. Natl. Acad. Sci. USA 88, 6368-6371 (1991).
39. Wang, F., O'Hare, M.J. & Park, D,S. Cyclin-dependent kinases and stroke. Expert. Opin. Ther. Targets 5, 557-567 (2001).
40. Neumar, R.W. et al. Calpain activity in the rat brain after transient forebrain ischemia. Exp. Neurol. 170, 27-35 (2001).
41. Liu, H.N., Giasson, B.I., Mushynski, W.E. & Almazan, G. AMPA receptor-mediated toxicity in oligodendrocyte progenitors involves for radical generation and activation of JNK, calpain and caspase 3. J. Neurochem. 82, 398-409 (2002).
42. Minger, S.L. et al. Glutamate receptor antagonists inhibit calpain-mediated cytoskeletal proteolysis in focal cerebral ischemia. Brain Res. 810, 181-199 (1998).
43. Jonas, P., & Burnashev, N. Molecular mechanisms controlling calcium entry through AMPA-type glutamate receptor channels, Neuron 15, 987-990 (1995).
44. 2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15, 193-204 (1995).
45. 2+ influx in hippocampal CA1 neurons of gerbil. J. Neurosci. 17, 6179-6188 (1997).
46. 2+-permeable AMPA receptors in neurological disorders. Trends Neurosci. 20, 464-470 (1997).
47. Zhu, D.Y., Liu, S.H., Sun, S. & Lu, Y.M. Expression of inducible nitric oxide synthase after focal cerebral ischemia stimulates neurogenesis in the adult rodent dentate gyrus. J. Neurosci. 23, 223-239 (2003).
48. Liu, S.H., Wang, J., Zhu, D.Y., Fu, Y.P. & Lu, Y.M. Generation of functional inhibitory neurons in the adult rat hippocampus. J. Neurosci. 23, 732-736 (2003).
49. 2 subunits produces long-term depression at CA1 inhibitory synapses. J. Neurosci. 23, 826-836 (2003).
50. Carlin, R. K., Grab, D. J., Cohen, R. S. & Siekevitz, P. Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities. J. Cell Biol. 86, 831-845 (1980).