Hippocampal LTP triggers proteasome-mediated SPAR degradation in CA1 neurons

Synapse

Volumn 66, Issue 2, 2012, Pages 142-150

  Chen, Ying ^a   Yuanxiang, Pingan ^a   Knöpfel, Thomas ^b   Thomas, Ulrich ^c   Behnisch, Thomas ^a  

^a FUDAN UNIVERSITY   (China)

^b RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^c LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

Author keywords

CDK5; Hippocampus; LTP; Polo like kinase 2; Postsynaptic density; Semliki forest virus; SPAR; Ubiquitin proteasome pathway

Indexed keywords

CYCLIN DEPENDENT KINASE 5; NERVE PROTEIN; POSTSYNAPTIC DENSITY PROTEIN; PROTEASOME; SPINE ASSOCIATED RAP GTPASE ACTIVATING PROTEIN; UBIQUITIN PROTEASOME SYSTEM; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CONFOCAL MICROSCOPY; HIPPOCAMPAL CA1 REGION; LONG TERM POTENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RAT;

ANIMALS; CA1 REGION, HIPPOCAMPAL; CYCLIN-DEPENDENT KINASE 5; DOWN-REGULATION; GTPASE-ACTIVATING PROTEINS; LONG-TERM POTENTIATION; NEURONS; ORGAN CULTURE TECHNIQUES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN SYNTHESIS INHIBITORS; RATS; RATS, WISTAR;

EID: 83055184246     PISSN: 08874476     EISSN: 10982396     Source Type: Journal    
DOI: 10.1002/syn.20994     Document Type: Article

References (41)

1. Behnisch T, Matsushita S, Knopfel T. 2004. Imaging of gene expression during long-term potentiation. Neuroreport 15: 2039-2043.
2. Bliss TV, Collingridge GL. 1993. A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 361: 31-39.
3. Bramham CR, Wells DG. 2007. Dendritic mRNA: Transport, translation and function. Nat Rev Neurosci 8: 776-789.
4. Cai F, Frey JU, Sanna PP, Behnisch T. 2010. Protein degradation by the proteasome is required for synaptic tagging and the heterosynaptic stabilization of hippocampal late-phase long-term potentiation. Neuroscience 169: 1520-1526.
5. Craiu A, Gaczynska M, Akopian T, Gramm CF, Fenteany G, Goldberg AL, Rock KL. 1997. Lactacystin and clasto-lactacystin beta-lactone modify multiple proteasome beta-subunits and inhibit intracellular protein degradation and major histocompatibility complex class I antigen presentation. J Biol Chem 272: 13437-13445.
6. Deadwyler SA, Dunwiddie T, Lynch G. 1987. A critical level of protein synthesis is required for long-term potentiation. Synapse 1: 90-95.
7. Du JL, Wei HP, Wang ZR, Wong ST, Poo MM. 2009. Long-range retrograde spread of LTP and LTD from optic tectum to retina. Proc Natl Acad Sci USA 106: 18890-18896.
8. Ehlers MD. 2003. Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat Neurosci 6: 231-242.
9. Ehrengruber MU, Lundstrom K, Schweitzer C, Heuss C, Schlesinger S, Gahwiler BH. 1999. Recombinant Semliki Forest virus and Sindbis virus efficiently infect neurons in hippocampal slice cultures. Proc Natl Acad Sci USA 96: 7041-7046.
10. Foley AG, Hartz BP, Gallagher HC, Ronn LC, Berezin V, Bock E, Regan CM. 2000. A synthetic peptide ligand of neural cell adhesion molecule (NCAM) IgI domain prevents NCAM internalization and disrupts passive avoidance learning. J Neurochem 74: 2607-2613.
11. Fonseca R, Vabulas RM, Hartl FU, Bonhoeffer T, Nagerl UV. 2006. A balance of protein synthesis and proteasome-dependent degradation determines the maintenance of LTP. Neuron 52: 239-245.
12. Frey S, Frey JU. 2008. Synaptic tagging and cross-tagging and related associative reinforcement processes of functional plasticity as the cellular basis for memory formation. Prog Brain Res 169: 117-143.
13. Frey U, Frey S, Schollmeier F, Krug M. 1996. Influence of actinomycin D, a RNA synthesis inhibitor, on long-term potentiation in rat hippocampal neurons in vivo and in vitro. J Physiol 490(Part 3): 703-711.
14. Frey U, Krug M, Reymann KG, Matthies H. 1988. Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res 452: 57-65.
15. Hegde AN. 2004. Ubiquitin-proteasome-mediated local protein degradation and synaptic plasticity. Prog Neurobiol 73: 311-357.
16. Hernandez PJ, Abel T. 2008. The role of protein synthesis in memory consolidation: Progress amid decades of debate. Neurobiol Learn Mem 89: 293-311.
17. Jager T, Behnisch T, Reymann KG. 2002. High frequency stimulation-induced dendritic calcium waves in rat hippocampal neurons. Neurosci Lett 335: 103-106.
18. Jakawich SK, Neely RM, Djakovic SN, Patrick GN, Sutton MA. 2010. An essential postsynaptic role for the ubiquitin proteasome system in slow homeostatic synaptic plasticity in cultured hippocampal neurons. Neuroscience 171: 1016-1031.
19. Jiang YH, Armstrong D, Albrecht U, Atkins CM, Noebels JL, Eichele G, Sweatt JD, Beaudet AL. 1998. Mutation of the Angelman ubiquitin ligase in mice causes increased cytoplasmic p53 and deficits of contextual learning and long-term potentiation. Neuron 21: 799-811.
20. Karpova A, Mikhaylova M, Thomas U, Knopfel T, Behnisch T. 2006. Involvement of protein synthesis and degradation in long-term potentiation of schaffer collateral CA1 synapses. J Neurosci 26: 4949-4955.
21. Kauselmann G, Weiler M, Wulff P, Jessberger S, Konietzko U, Scafidi J, Staubli U, Bereiter-Hahn J, Strebhardt K, Kuhl D. 1999. The polo-like protein kinases Fnk and Snk associate with a Ca(2+)- and integrin-binding protein and are regulated dynamically with synaptic plasticity. EMBO J 18: 5528-5539.
22. Krucker T, Siggins GR, Halpain S. 2000. Dynamic actin filaments are required for stable long-term potentiation (LTP) in area CA1 of the hippocampus. Proc Natl Acad Sci USA 97: 6856-6861.
23. Leutgeb JK, Frey JU, Behnisch T. 2005. Single cell analysis of activity-dependent cyclic AMP-responsive element-binding protein phosphorylation during long-lasting long-term potentiation in area CA1 of mature rat hippocampal-organotypic cultures. Neuroscience 131: 601-610.
24. Leutgeb JK, Frey JU, Behnisch T. 2003. LTP in cultured hippocampal-entorhinal cortex slices from young adult (P25-30) rats. J Neurosci Methods 130: 19-32.
25. Lopez-Salon M, Alonso M, Vianna MR, Viola H, Mello e Souza, Izquierdo I, Pasquini JM, Medina JH. 2001. The ubiquitin-proteasome cascade is required for mammalian long-term memory formation. Eur J Neurosci 14: 1820-1826.
26. Lu XJ, Chen XQ, Weng J, Zhang HY, Pak DT, Luo JH, Du JZ. 2009. Hippocampal spine-associated Rap-specific GTPase-activating protein induces enhancement of learning and memory in postnatally hypoxia-exposed mice. Neuroscience 162: 404-414.
27. Malenka RC, Nicoll RA. 1999. Long-term potentiation-A decade of progress? Science 285: 1870-1874.
28. Malinow R, Schulman H, Tsien RW. 1989. Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP. Science 245: 862-866.
29. Matthies H, Frey U, Reymann K, Krug M, Jork R, Schroeder H. 1990. Different mechanisms and multiple stages of LTP. Adv Exp Med Biol 268: 359-368.
30. Mochida H, Sato K, Sasaki S, Yazawa I, Kamino K, Momose-Sato Y. 2001. Effects of anisomycin on LTP in the hippocampal CA1: Long-term analysis using optical recording. Neuroreport 12: 987-991.
31. Pak DT, Sheng M. 2003. Targeted protein degradation and synapse remodeling by an inducible protein kinase. Science 302: 1368-1373.
32. Pak DT, Yang S, Rudolph-Correia S, Kim E, Sheng M. 2001. Regulation of dendritic spine morphology by SPAR, a PSD-95-associated RapGAP. Neuron 31: 289-303.
33. Perez-Otano I, Ehlers MD. 2005. Homeostatic plasticity and NMDA receptor trafficking. Trends Neurosci 28: 229-238.
34. Richter M, Murai KK, Bourgin C, Pak DT, Pasquale EB. 2007. The EphA4 receptor regulates neuronal morphology through SPAR-mediated inactivation of Rap GTPases. J Neurosci 27: 14205-14215.
35. Roberson ED, English JD, Adams JP, Selcher JC, Kondratick C, Sweatt JD. 1999. The mitogen-activated protein kinase cascade couples PKA and PKC to cAMP response element binding protein phosphorylation in area CA1 of hippocampus. J Neurosci 19: 4337-4348.
36. Seeburg DP, Feliu-Mojer M, Gaiottino J, Pak DT, Sheng M. 2008. Critical role of CDK5 and Polo-like kinase 2 in homeostatic synaptic plasticity during elevated activity. Neuron 58: 571-583.
37. Seeburg DP, Pak D, Sheng M. 2005. Polo-like kinases in the nervous system. Oncogene 24: 292-298.
38. Seeburg DP, Sheng M. 2008. Activity-induced Polo-like kinase 2 is required for homeostatic plasticity of hippocampal neurons during epileptiform activity. J Neurosci 28: 6583-6591.
39. Spilker C, Kreutz MR. 2010. RapGAPs in brain: Multipurpose players in neuronal Rap signalling. Eur J Neurosci 32: 1-9.
40. Stanton PK, Sarvey JM. 1984. Blockade of long-term potentiation in rat hippocampal CA1 region by inhibitors of protein synthesis. J Neurosci 4: 3080-3088.
41. Yi JJ, Ehlers MD. 2007. Emerging roles for ubiquitin and protein degradation in neuronal function. Pharmacol Rev 59: 14-39.