Excitotoxic loss of post-synaptic sites is distinct temporally and mechanistically from neuronal death

Journal of Neurochemistry

Volumn 104, Issue 2, 2008, Pages 364-375

  Waataja, Jonathan J ^a   Kim, Hee Jung ^a   Roloff, Alan M ^a   Thayer, Stanley A ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

Excitotoxicity; N methyl D aspartate; Neurodegeneration; Post synaptic density protein 95; Proteasome; Synapse

Indexed keywords

CALCIUM ION; CYCLIN DEPENDENT KINASE INHIBITOR 2A; GREEN FLUORESCENT PROTEIN; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROPROTECTIVE AGENT; NEUROTRANSMITTER; NEUROTRANSMITTER RECEPTOR; POSTSYNAPTIC DENSITY PROTEIN 95; TOXIN;

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CELL SURVIVAL; CONCENTRATION (PARAMETERS); CONFOCAL MICROSCOPY; CONTROLLED STUDY; DRUG SCREENING; EXCITOTOXICITY; HIPPOCAMPUS; IMMUNOREACTIVITY; MOLECULAR IMAGING; NERVE CELL NECROSIS; NERVE DEGENERATION; NEUROPROTECTION; NEUROTRANSMISSION; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SENSITIVITY ANALYSIS; SYNAPSE; SYNAPTIC TRANSMISSION; UBIQUITINATION;

ANIMALS; CALCIUM; CELL DEATH; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, MAMMALIAN; ENZYME INHIBITORS; EXCITATORY POSTSYNAPTIC POTENTIALS; GENE EXPRESSION REGULATION; GLUTAMIC ACID; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; HYPOGLYCEMIC AGENTS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; NEURONS; NEUROTOXINS; PALMITATES; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; TIME FACTORS; TRANSFECTION;

RATTUS;

EID: 37349113057     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2007.04973.x     Document Type: Article

References (46)

1. Arnold D. B. Clapham D. E. (1999) Molecular determinants for subcellular localization of PSD-95 with an interacting K+ channel. Neuron 23, 149 157.
2. Bingol B. Schuman E. M. (2005) Synaptic protein degradation by the ubiquitin proteasome system. Curr. Opin. Neurobiol. 15, 536 541.
3. Blackstone C. Sheng M. (2002) Postsynaptic calcium signaling microdomains in neurons. Front. Biosci. 7, D872 D885.
4. Blitzer R. D., Iyengar R. Landau E. M. (2005) Postsynaptic signaling networks: cellular cogwheels underlying long-term plasticity. Biol. Psychiatry 57, 113 119.
5. Bolshakov V. Y., Golan H., Kandel E. R. Siegelbaum S. A. (1997) Recruitment of new sites of synaptic transmission during the cAMP-dependent late phase of LTP at CA3-CA1 synapses in the hippocampus. Neuron 19, 635 651.
6. Buttini M., Masliah E., Barbour R. et al. (2005) Beta-amyloid immunotherapy prevents synaptic degeneration in a mouse model of Alzheimer's disease. J. Neurosci. 25, 9096 9101.
7. Choi D. W., Maulucci-Gedde M. Kriegstein A. R. (1987) Glutamate neurotoxicity in cortical cell culture. J. Neurosci. 7, 357 368.
8. Colledge M., Snyder E. M., Crozier R. A., Soderling J. A., Jin Y., Langeberg L. K., Lu H., Bear M. F. Scott J. D. (2003) Ubiquitination regulates PSD-95 degradation and AMPA receptor surface expression. Neuron 40, 595 607.
9. Dawson V. L., Dawson T. M., Bartley D. A., Uhl G. R. Snyder S. H. (1993) Mechanisms of nitric oxide-mediated neurotoxicity in primary brain cultures. J. Neurosci. 13, 2651 2661.
10. Desai N. S. (2003) Homeostatic plasticity in the CNS: synaptic and intrinsic forms. J. Physiol. Paris 97, 391 402.
11. Ebihara T., Kawabata I., Usui S., Sobue K. Okabe S. (2003) Synchronized formation and remodeling of postsynaptic densities: long-term visualization of hippocampal neurons expressing postsynaptic density proteins tagged with green fluorescent protein. J. Neurosci. 23, 2170 2181.
12. El-Husseini A. E., Craven S. E., Chetkovich D. M., Firestein B. L., Schnell E., Aoki C. Bredt D. S. (2000a) Dual palmitoylation of PSD-95 mediates its vesiculotubular sorting, postsynaptic targeting, and ion channel clustering. J. Cell Biol. 148, 159 172.
13. El-Husseini A. E., Schnell E., Chetkovich D. M., Nicoll R. A. Bredt D. S. (2000b) PSD-95 involvement in maturation of excitatory synapses. Science 290, 1364 1368.
14. Emery D. L., Royo N. C., Fischer I., Saatman K. E. McIntosh T. K. (2003) Plasticity following injury to the adult central nervous system: is recapitulation of a developmental state worth promoting? J. Neurotrauma 20, 1271 1292.
15. Fiala J. C., Spacek J. Harris K. M. (2002) Dendritic spine pathology: cause or consequence of neurological disorders? Brain Res. Rev. 39, 29 54.
16. Finkbeiner S., Cuervo A. M., Morimoto R. I. Muchowski P. J. (2006) Disease-modifying pathways in neurodegeneration. J. Neurosci. 26, 10349 10357.
17. Glazner G. W., Chan S. L., Lu C. Mattson M. P. (2000) Caspase-mediated degradation of AMPA receptor subunits: a mechanism for preventing excitotoxic necrosis and ensuring apoptosis. J. Neurosci. 20, 3641 3649.
18. Ikegaya Y., Kim J. A., Baba M., Iwatsubo T., Nishiyama N. Matsuki N. (2001) Rapid and reversible changes in dendrite morphology and synaptic efficacy following NMDA receptor activation: implication for a cellular defense against excitotoxicity. J. Cell Sci. 114, 4083 4093.
19. Kim D. Thayer S. A. (2001) Cannabinoids inhibit the formation of new synapses between hippocampal neurons in culture. J. Neurosci. 21, RC146.
20. Kouznetsova M., Kelley B., Shen M. Thayer S. A. (2002) Desensitization of cannabinoid-mediated presynaptic inhibition of neurotransmission between rat hippocampal neurons in culture. Mol. Pharmacol. 61, 477 485.
21. Lang S. B., Stein V., Bonhoeffer T. Lohmann C. (2007) Endogenous brain-derived neurotrophic factor triggers fast calcium transients at synapses in developing dendrites. J. Neurosci. 27, 1097 1105.
22. Lardi-Studler B. Fritschy J.-M. (2007) Matching of pre- and postsynaptic specializations during synaptogenesis. Neuroscientist 13, 115 126.
23. Lin Y., Skeberdis V. A., Francesconi A., Bennett M. V. L. Zukin R. S. (2004) Postsynaptic density protein-95 regulates NMDA channel gating and surface expression. J. Neurosci. 24, 10138 10148.
24. Ma L., Zablow L., Kandel E. R. Siegelbaum S. A. (1999) Cyclic AMP induces functional presynaptic boutons in hippocampal CA3- CA1 neuronal cultures. Nat. Neurosci. 2, 24 30.
25. Malenka R. C. (2003) Synaptic plasticity and AMPA receptor trafficking. Ann. N Y Acad. Sci. 1003, 1 11.
26. Marrs G. S., Green S. H. Dailey M. E. (2001) Rapid formation and remodeling of postsynaptic densities in developing dendrites. Nat. Neurosci. 4, 1006 1013.
27. Masliah E. Terry R. (1993) The role of synaptic proteins in the pathogenesis of disorders of the central nervous system. Brain Pathol. 3, 77 85.
28. Naraghi M. Neher E. (1997) Linearized buffered Ca2+ diffusion in microdomains and its implications for calculation of [Ca2+] at the mouth of a calcium channel. J. Neurosci. 17, 6961 6973.
29. Nitsch R. Frotscher M. (1992) Reduction of posttraumatic transneuronal "early gene" activation and dendritic atrophy by the N-methyl-D-aspartate receptor antagonist MK-801. Proc. Natl Acad. Sci. USA 89, 5197 5200.
30. Okabe S., Kim H. D., Miwa A., Kuriu T. Okado H. (1999) Continual remodeling of postsynaptic density and its regulation by synaptic activity. Nature Neurosci. 2, 804 811.
31. Okabe S., Miwa A. Okado H. (2001) Spine formation and correlated assembly of presynaptic and postsynaptic molecules. J. Neurosci. 21, 6105 6114.
32. Olney J. W., Fuller T. de Gubareff T. (1979) Acute dendrotoxic changes in the hippocampus of kainate treated rats. Brain Res. 176, 91 100.
33. Palop J. J., Chin J. Mucke L. (2006) A network dysfunction perspective on neurodegenerative diseases. Nature 443, 768 773.
34. Pottorf W. J., Johanns T. M., Derrington S. M., Strehler E. E., Enyedi A. Thayer S. A. (2006) Glutamate-induced protease-mediated loss of plasma membrane Ca pump activity in rat hippocampal neurons. J. Neurochem. 98, 1646 1656.
35. Rubinsztein D. C. (2006) The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 443, 780 786.
36. Sa M. J., Madeira M. D., Ruela C., Volk B., Mota-Miranda A. Paula-Barbosa M. M. (2004) Dendritic changes in the hippocampal formation of AIDS patients: a quantitative Golgi study. Acta Neuropathol. (Berl) 107, 97 110.
37. Sanchez A. L., Matthews B. J., Meynard M. M., Hu B., Javed S. Cohen Cory S. (2006) BDNF increases synapse density in dendrites of developing tectal neurons in vivo. Development 133, 2477 2486.
38. Sattler R., Xiong Z., Lu W. Y., Hafner M., MacDonald J. F. Tymianski M. (1999) Specific coupling of NMDA receptor activation to nitric oxide neurotoxicity by PSD-95 protein. Science 284, 1845 1848.
39. Shi S., Hayashi Y., Esteban J. A. Malinow R. (2001) Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105, 331 343.
40. Sunico C. R., Portillo F., Gonzalez-Forero D. Moreno-Lopez B. (2005) Nitric-oxide-directed synaptic remodeling in the adult mammal CNS. J. Neurosci. 25, 1448 1458.
41. Swann J. W., Al-Noori S., Jiang M. Lee C. L. (2000) Spine loss and other dendritic abnormalities in epilepsy. Hippocampus 10, 617 625.
42. Tymianski M., Charlton M. P., Carlen P. L. Tator C. H. (1994) Properties of neuroprotective cell-permeant Ca2+ chelators: effects on [Ca2+](i) and glutamate neurotoxicity in vitro. J. Neurophysiol. 72, 1973 1992.
43. Xia Z. G., Dudek H., Miranti C. K. Greenberg M. E. (1996) Calcium influx via the nmda receptor induces immediate early gene transcription by a map kinase/erk-dependent mechanism. J. Neurosci. 16, 5425 5436.
44. Yakura T., Fukuda Y. Sawai H. (2002) Effect of Bcl-2 overexpression on establishment of ipsilateral retinocollicular projection in mice. Neurosci. 110, 667 673.
45. Zhang Y., Xiong Y. Yarbrough W. G. (1998) ARF promotes MDM2 degradation and stabilizes p53: ARF-INK4a locus deletion impairs both the Rb and p53 tumor suppression pathways. Cell 92, 725 734.
46. Ziff E. B. (1997) Enlightening the postsynaptic density. Neuron 19, 1163 1174.