PSD-95 promotes the stabilization of young synaptic contacts

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1633, 2014, Pages

  Taft, Christine E ^a   Turrigiano, Gina G ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

CaMKII; GluA2; Live imaging; PSD 95; Synapse stabilization

Indexed keywords

ENZYME ACTIVITY; MEMORY; MOLECULAR ANALYSIS; NEUROLOGY; PROTEIN; TIMESCALE;

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; DLGH4 PROTEIN, RAT; GREEN FLUORESCENT PROTEIN; LIPID; LIPOFECTAMINE; MEMBRANE PROTEIN; SIGNAL PEPTIDE;

ANALYSIS OF VARIANCE; ANIMAL; ARTICLE; CAMKII; CELL CULTURE; GLUA2; LONG EVANS RAT; MEMORY; METABOLISM; MOLECULAR DYNAMICS; PHYSIOLOGY; PSD-95; RAT; SYNAPSE; SYNAPSE STABILIZATION, LIVE IMAGING; TIME; TIME LAPSE IMAGING;

CAMKII; GLUA2; PSD-95; SYNAPSE STABILIZATION, LIVE IMAGING;

ANALYSIS OF VARIANCE; ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELLS, CULTURED; GREEN FLUORESCENT PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPIDS; MEMBRANE PROTEINS; MEMORY; MOLECULAR DYNAMICS SIMULATION; RATS; RATS, LONG-EVANS; SYNAPSES; TIME FACTORS; TIME-LAPSE IMAGING;

EID: 84888789357     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2013.0134     Document Type: Article

References (46)

1. Yoshihara Y, De Roo M, Muller D. 2009 Dendritic spine formation and stabilization. Curr. Opin. Neurobiol. 19, 146-153. (doi:10.1016/j.conb.2009.05.013)
2. Krueger DD, Tuffy LP, Papadopoulos T, Brose N. 2012 The role of neurexins and neuroligins in the formation, maturation, and function of verterate synaspes. Curr. Opin. Neurobiol. 22, 412-422. (doi:10.1016/j.conb.2012.02.012)
3. Okabe S, Kim HD, Miwa A, Kuriu T, Okado H. 1999 Continual remodeling of postsynaptic density and its regulation by synaptic activity. Nat. Neurosci. 2, 804-811. (doi:10.1038/12175)
4. Marrs GS, Green SH, Dailey ME. 2001 Rapid formation and remodeling of postsynaptic densities in developing dendrites. Nat. Neurosci. 4, 1006-1013. (doi:10.1038/nn717)
5. Gray NW, Weimer RM, Bureau I, Svoboda K. 2006 Rapid redistribution of synaptic PSD-95 in the neocortex in vivo. PLoS Biol. 4, e370. (doi:10.1371/ journal.pbio.0040370)
6. Kuriu T, Inoue A, Bito H, Sobue K, Okabe S. 2006 Differential control of postsynaptic density scaffolds via actin-dependent and-independent mechanisms. J. Neurosci. 26, 7693-7706. (doi:10.1523/ JNEUROSCI.0522-06.2006)
7. Tsuriel S, Geva R, Zamorano P, Dresback T, Boeckers T, Gundelfinder ED, Garner CC, Ziv NE. 2006 Local sharing as a predominant determinant of synaptic matrix molecular dynamics. PLoS Biol. 4, e271. (doi:10.1371/journal.pbio.0040271)
8. Wu GY, Cline HT. 1998 Stabilization of dendritic arbor structure in vivo by CaMKII. Science 279, 222-226. (doi:10.1126/science.279.5348.222)
9. Zou DJ, Cline HT. 1999 Postsynaptic calcium/ calmodulin-dependent protein kinase II is required to limit elaboration of presynaptic and postsynaptic neuronal arbors. J. Neurosci. 19, 8909-8918.
10. Lisman J, Schulman H, Cline H. 2002 The molecular basis of CaMKII function in synaptic and behavioral memory. Nat. Rev. Neurosci. 3, 175-190. (doi:10.1038/nrn753)
11. Kazama H, Morimoto-Tanifuji T, Nose A. 2003 Postsynaptic activation of calcium/calmodulindependent protein kinase II promotes coordinated pre-and postsynaptic maturation of Drosophila neuromuscular junctions. Neuroscience 117, 615-625. (doi:10.1016/S0306-4522(02)00923-5)
12. 2+/calmodulin-dependent protein kinase IIa in dendritic spine enlargement, long-term potentiation, and learning. J. Neurosci. 29, 7607-7618. (doi:10.1523/JNEUROSCI.0707-09.2009)
13. Pratt KG, Watt AJ, Griffith LC, Nelson SB, Turrigiano GG. 2003 Activity-dependent remodeling of presynaptic inputs by postsynaptic expression of activated CaMKII. Neuron 39, 269-281. (doi:10. 1016/S0896-6273(03)00422-7)
14. Pratt KG, Taft CE, Burbea M, Turrigiano GG. 2008 Dynamics underlying synaptic gain between pairs of cortical pyramidal neurons. Dev. Neurobiol. 68, 143-151. (doi:10.1002/dneu.20577)
15. Sugiyama Y, Kawabata I, Sobue K, Okabe S. 2005 Determination of absolute protein numbers in single synapses by a GFP-based calibration technique. Nat. Methods 2, 677-684. (doi:10.1038/ nmeth783)
16. Rao A, Cha EM, Craig AM. 2000 Mismatched appositions of presynaptic and postsynaptic components in isolated hippocampal neurons. J. Neurosci. 20, 8344-8353.
17. Ahmed R, Zha XM, Green SH, Dailey ME. 2006 Synaptic activity and F-actin coordinately regulate CaMKIIalpha localization to dendritic postsynaptic sites in developing hippocampal slices. Mol. Cell. Neurosci. 31, 37-51. (doi:10.1016/j.mcn. 2005.08.020)
18. Gerrow K, Romorini S, Nabi SM, Colicos MA, Sala C, El-Husseini A. 2006 A preformed complex of postsynaptic proteins is involved in excitatory synapse development. Neuron 49, 547-562. (doi:10.1016/j.neuron.2006.01.015)
19. De Roo M, Klauser P, Mendez P, Poglia L, Muller D. 2008 Activity-dependent PSD formation and stabilization of newly formed spines in hippocampal slice cultures. Cereb. Cortex 18, 151-161. (doi:10. 1093/cercor/bhm041)
20. Garner CC, Nash J, Huganir RL. 2000 PDZ domains in synapse assembly and signaling. Trends Cell Biol. 10, 274-280. (doi:10.1016/S0962-8924 (00)01783-9)
21. Prange O, Murphy TH. 2001 Modular transport of postsynaptic density-95 clusters and association with stable spine precursors during early development of cortical neurons. J. Neurosci. 21, 9325-9333.
22. Matsuzaki M, Ellis-Davies GC, Nemoto T, Miyashita Y, Iino M, Kasai H. 2001 Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat. Neurosci. 4, 1086-1092. (doi:10.1038/nn736)
23. El-Husseini AE, Schnell E, Chetkovich DM, Nicoll RA, Bredt DS. 2000 PSD-95 involvement in maturation of excitatory synapses. Science 290, 1364-1368.
24. El-Husseini AE et al. 2002 Synaptic strength regulated by palmitate cycling on PSD-95. Cell 108, 849-863. (doi:10.1016/S0092-8674(02)00683-9)
25. Beïque JC, Lin DT, Kang MG, Aizawa H, Takamiya K, Huganir RL. 2006 Synapse-specific regulation of AMPA receptor function by PSD-95. Proc. Natl Acad. Sci. USA 103, 19 535-19 540. (doi:10.1073/pnas. 0608492103)
26. Irie M, Hata Y, Takeuchi M, Ichtchenko K, Toyoda A, Hirao K, Takai Y, Rosahl TW, Südhof TC. 1997 Binding of neuroligins to PSD-95. Science 277, 1511-1515. (doi:10.1126/science.277.5331.1511)
27. Scheiffele P, Fan J, Choih J, Fetter R, Serafini T. 2000 Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 101, 657-669. (doi:10.1016/S0092-8674(00) 80877-6)
28. Sans N, Petralia RS, Wang YX, Blahos 2nd J, Hell JW, Wenthold RJ. 2000 A developmental change in NMDA receptor-associated proteins at hippocampal synapses. J. Neurosci. 20, 1260-1271.
29. Sun Q, Turrigiano GG. 2011 PSD-95 and PSD-93 play distinct signaling/scaffolding roles in synaptic scaling up and down. J. Neurosci. 31, 6800-6808. (doi:10.1523/JNEUROSCI.5616-10.2011)
30. Trachtenberg JT, Chen BE, Knott GW, Feng G, Sanes JR, Welker E, Svoboda K. 2002 Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420, 88-94. (doi:10.1038/ nature01273)
31. Ehrlich I, Klein M, Rumpel S, Malinow R. 2007 PSD-95 is required for activity-driven synapse stabilization. Proc. Natl Acad. Sci. USA 104, 4176-4181. (doi:10.1073/pnas.0609307104)
32. Wierenga CJ, Ibata K, Turrigiano GG. 2005 Postsynaptic expression of homeostatic plasticity at neocortical synapses. J. Neurosci. 25, 2895-2905. (doi:10.1523/JNEUROSCI.5217-04.2005)
33. Ibata K, Sun Q, Turrigiano GG. 2008 Rapid synaptic scaling induced by changes in postsynaptic firing. Neuron 57, 819-826. (doi:10.1016/j.neuron.2008. 02.031)
34. Shen K, Meyer T. 1999 Dynamic control of CaMKII translocation and localization in hippocampal neurons by NMDA receptor stimulation. Science 284, 162-166. (doi:10.1126/science.284.5411.162)
35. Kim E, Sheng M. 2004 PDZ domain proteins of synapses. Nat. Rev. Neurosci. 5, 771-781. (doi:10.1038/nrn1517)
36. Schnell E, Sizemore M, Karimzadegan S, Chen L, Bredt DS, Nicoll RA. 2002 Direct interactions between PSD-95 and stargazin control synaptic AMPA receptor number. Proc. Natl Acad. Sci. USA 99, 13 902-13 907. (doi:10.1073/pnas.172511199)
37. Ehrlich I, Malinow R. 2004 Postsynaptic density 95 controls AMPA receptor incorporation during longterm potentiation and experience-driven synaptic plasticity. J. Neurosci. 24, 916-927. (doi:10.1523/ JNEUROSCI.4733-03.2004)
38. Elias GM, Nicoll RA. 2007 Synaptic trafficking of glutamate receptors by MAGUK scaffolding proteins. Trends Cell Biol. 17, 343-352. (doi:10.1016/j.tcb. 2007.07.005)
39. Keith D, El-Husseini A. 2008 Excitation control: balancing PSD-95 function at the synapse. Front. Mol. Neurosci. 1, 4. (doi:10.3389/neuro.02.004.2008)
40. Beïque JC, Andrade R. 2003 PSD-95 regulates synaptic transmission and plasticity in rat cerebral cortex. J. Physiol. 546, 859-867. (doi:10.1113/ jphysiol.2002.031369)
41. Stein V, House DR, Bredt DS, Nicoll RA. 2003 Postsynaptic density-95 mimics and occludes hippocampal long-term potentiation and enhances long-term depression. J. Neurosci. 23, 5503-5506.
42. Elias GM, Funke L, Stein V, Grant SG, Bredt DS, Nicoll RA. 2006 Synapse-specific and developmentally regulated targeting of AMPA receptors by a family of MAGUK scaffolding proteins. Neuron 52, 307-320. (doi:10.1016/j.neuron.2006.09.012)
43. Xu W, Schluter OM, Steiner P, Czervionke BL, Sabatini B, Malenka RC. 2008 Molecular dissociation of the role of PSD-95 in regulating synaptic strength and LTD. Neuron 57, 248-262. (doi:10.1016/j. neuron.2007.11.027)
44. Kelsch W, Lin CW, Lois C. 2008 Sequential development of synapses in dendritic domains during adult neurogenesis. Proc. Natl Acad. Sci. USA 105, 16 803-16 808. (doi:10.1073/pnas. 0807970105)
45. Yoshii A, Sheng MH, Constantine-Paton M. 2003 Eye opening induces a rapid dendritic localization of PSD-95 in central visual neurons. Proc. Natl Acad. Sci. USA 100, 1334-1339. (doi:10.1073/pnas. 0335785100)
46. Steiner P, Higley MJ, Xu W, Czervionke BL, Malenka RC, Sabatini BL. 2008 Destabilization of the postsynaptic density by PSD-95 serine 73 phosphorylation inhibits spine growth and synaptic plasticity. Neuron 60, 788-802. (doi:10.1016/j. neuron.2008.10.014)