Retrograde modulation of presynaptic release probability through signaling mediated by PSD-95-neuroligin

Nature Neuroscience

Volumn 10, Issue 2, 2007, Pages 186-195

  Futai, Kensuke ^a,b   Kim, Myung Jong ^a   Hashikawa, Tsutomu ^b   Scheiffele, Peter ^c   Sheng, Morgan ^a   Hayashi, Yasunori ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^c College of Physicians and Surgeons ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUREXIN; NEUROLIGIN; POSTSYNAPTIC DENSITY PROTEIN 95;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HIPPOCAMPUS; NONHUMAN; PLASTICITY; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PYRAMIDAL NERVE CELL; RAT; RAT STRAIN;

ANIMALS; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; NEUROTRANSMITTER AGENTS; ORGAN CULTURE TECHNIQUES; PRESYNAPTIC TERMINALS; PROBABILITY; PROTEIN TRANSPORT; PYRAMIDAL CELLS; RATS; SIGNAL TRANSDUCTION; SYNAPTIC MEMBRANES; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES;

EID: 33846564563     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1837     Document Type: Article

References (50)

1. Liu, G., Choi, S. & Tsien, R.W. Variability of neurotransmitter concentration and nonsaturation of postsynaptic AMPA receptors at synapses in hippocampal cultures and slices. Neuron 22, 395-409 (1999).
2. Dobrunz, L.E. & Stevens, C.F. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18, 995-1008 (1997).
3. Rosenmund, C., Clements, J.D. & Westbrook, G.L. Nonuniform probability of glutamate release at a hippocampal synapse. Science 262, 754-757 (1993).
4. Conti, R. & Lisman, J. The high variance of AMPA receptor- and NMDA receptor-mediated responses at single hippocampal synapses: evidence for multiquantal release. Proc. Natl. Acad. Sci. USA 100, 4885-4890 (2003).
5. Matsuzaki, M. et al. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat. Neurosci. 4, 1086-1092 (2001).
6. Shepherd, G.M. & Harris, K.M. Three-dimensional structure and composition of CA3-4CA1 axons in rat hippocampal slices: implications for presynaptic connectivity and compartmentalization. J. Neurosci. 18, 8300-8310 (1998).
7. Schikorski, T. & Stevens, C.F. Quantitative ultrastructural analysis of hippocampal excitatory synapses. J. Neurosci. 17, 5858-5867 (1997).
8. Sun, H.Y., Lyons, S.A. & Dobrunz, L.E. Mechanisms of target-cell specific short-term plasticity at Schaffer collateral synapses onto interneurones versus pyramidal cells in juvenile rats. J. Physiol. (Lond.) 568, 815-840 (2005).
9. Pratt, K.G., Watt, A.J., Griffith, L.C., Nelson, S.B. & Turrigiano, G.G. Activity-dependent remodeling of presynaptic inputs by postsynaptic expression of activated CaMKII. Neuron 39, 269-281 (2003).
10. Kazama, H., Morimoto-Tanifuji, T. & Nose, A. Postsynaptic activation of calcium/calmodulin-dependent protein kinase II promotes coordinated pre- and postsynaptic maturation of Drosophila neuromuscular junctions. Neuroscience 117, 615-625 (2003).
11. Haghighi, A.P. et al. Retrograde control of synaptic transmission by postsynaptic CaMKII at the Drosophila neuromuscular junction. Neuron 39, 255-267 (2003).
12. Zucker, R.S. & Regehr, W.G. Short-term synaptic plasticity. Annu. Rev. Physiol. 64, 355-405 (2002).
13. Irie, M. et al. Binding of neuroligins to PSD-95. Science 277, 1511-1515 (1997).
14. Chih, B., Engelman, H. & Scheiffele, P. Control of excitatory and inhibitory synapse formation by neuroligins. Science 307, 1324-1328 (2005).
15. Ichtchenko, K. et al. Neuroligin 1: a splice site-specific ligand for b-neurexins. Cell 81, 435-443 (1995).
16. El-Husseini, A.E., Schnell, E., Chetkovich, D.M., Nicoll, R.A. & Bredt, D.S. PSD-95 involvement in maturation of excitatory synapses. Science 290, 1364-1368 (2000).
17. Scheiffele, P., Fan, J., Choih, J., Fetter, R. & Serafini, T. Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 101, 657-669 (2000).
18. Dean, C. et al. Neurexin mediates the assembly of presynaptic terminals. Nat. Neurosci. 6, 708-716 (2003).
19. Graf, E.R., Zhang, X., Jin, S.X., Linhoff, M.W. & Craig, A.M. Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 119, 1013-1026 (2004).
20. Dean, C. & Dresbach, T. Neuroligins and neurexins: linking cell adhesion, synapse formation and cognitive function. Trends Neurosci. 29, 21-29 (2006).
21. Ehrlich, I. & Malinow, R. Postsynaptic density 95 controls AMPA receptor incorporation during long-term potentiation and experience-driven synaptic plasticity. J. Neurosci. 24, 916-927 (2004).
22. Nakagawa, T. et al. Quaternary structure, protein dynamics, and synaptic function of SAP97 controlled by L27 domain interactions. Neuron 44, 453-467 (2004).
23. Schnell, E. et al. Direct interactions between PSD-95 and stargazin control synaptic AMPA receptor number. Proc. Natl. Acad. Sci. USA 99, 13902-13907 (2002).
24. Noguchi, J., Matsuzaki, M., Ellis-Davies, G.C. & Kasai, H. Spine-neck geometry determines NMDA receptor-dependent Ca2+ signaling in dendrites. Neuron 46, 609-622 (2005).
25. Monyer, H. et al. Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256, 1217-1221 (1992).
26. Scheuber, A., Miles, R. & Poncer, J.C. Presynaptic Cav2.1 and Cav2.2 differentially influence release dynamics at hippocampal excitatory synapses. J. Neurosci. 24, 10402-10409 (2004).
27. Oertner, T.G., Sabatini, B.L., Nimchinsky, E.A. & Svoboda, K. Facilitation at single synapses probed with optical quantal analysis. Nat. Neurosci. 5, 657-664 (2002).
28. Christie, J.M. & Jahr, C.E. Multivesicular release at Schaffer collateral-CA1 hippocampal synapses. J. Neurosci. 26, 210-216 (2006).
29. Songyang, Z. et al. Recognition of unique carboxyl-terminal motifs by distinct PDZ domains. Science 275, 73-77 (1997).
30. Debanne, D., Gähwiler, B.H. & Thompson, S.M. Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures. J. Physiol. (Lond.) 507, 237-247 (1998).
31. Pavlidis, P. & Madison, D.V. Synaptic transmission in pair recordings from CA3 pyramidal cells in organotypic culture. J. Neurophysiol. 81, 2787-2797 (1999).
32. Piomelli, D. The molecular logic of endocannabinoid signalling. Nat. Rev. Neurosci. 4, 873-884 (2003).
33. Chavis, P. & Westbrook, G. Integrins mediate functional pre- and postsynaptic maturation at a hippocampal synapse. Nature 411, 317-321 (2001).
34. Contractor, A. et al. Trans-synaptic Eph receptor-ephrin signaling in hippocampal mossy fiber LTP. Science 296, 1864-1869 (2002).
35. Jungling, K. et al. N-cadherin transsynaptically regulates short-term plasticity at glutamatergic synapses in embryonic stem cell-derived neurons. J. Neurosci. 26, 6968-6978 (2006).
36. Regalado, M.P., Terry-Lorenzo, R.T., Waites, C.L., Garner, C.C. & Malenka, R.C. Transsynaptic signaling by postsynaptic synapse-associated protein 97. J. Neurosci. 26, 2343-2357 (2006).
37. Varoqueaux, F. et al. Neuroligins determine synapse maturation and function. Neuron 51, 741-754 (2006).
38. Migaud, M. et al. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature 396, 433-439 (1998).
39. Missler, M. et al. a-Neurexins couple Ca2+ channels to synaptic vesicle exocytosis. Nature 423, 939-948 (2003).
40. 2+ channels. J. Neurosci. 25, 4330-4342 (2005).
41. Boucard, A.A., Chubykin, A.A., Comoletti, D., Taylor, P. & Südhof, T.C. A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to α- and β-neurexins. Neuron 48, 229-236 (2005).
42. Dekay, J.G., Chang, T.C., Mills, N., Speed, H.E. & Dobrunz, L.E. Responses of excitatory hippocampal synapses to natural stimulus patterns reveal a decrease in short-term facilitation and increase in short-term depression during postnatal development. Hippocampus 16, 66-79 (2006).
43. Petralia, R.S., Sans, N., Wang, Y.X. & Wenthold, R.J. Ontogeny of postsynaptic density proteins at glutamatergic synapses. Mol. Cell. Neurosci. 29, 436-452 (2005).
44. Song, J.Y., Ichtchenko, K., Südhof, T.C. & Brose, N. Neuroligin 1 is a postsynaptic celladhesion molecule of excitatory synapses. Proc. Natl. Acad. Sci. USA 96, 1100-1105 (1999).
45. Yoshii, A., Sheng, M.H. & Constantine-Paton, M. Eye opening induces a rapid dendritic localization of PSD-95 in central visual neurons. Proc. Natl. Acad. Sci. USA 100, 1334-1339 (2003).
46. Reyes, A. et al. Target-cell-specific facilitation and depression in neocortical circuits. Nat. Neurosci. 1, 279-285 (1998).
47. Koester, H.J. & Johnston, D. Target cell-dependent normalization of transmitter release at neocortical synapses. Science 308, 863-866 (2005).
48. Okamoto, K., Nagai, T., Miyawaki, A. & Hayashi, Y. Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat. Neurosci. 7, 1104-1112 (2004).
49. Matsuzaki, M., Honkura, N., Ellis-Davies, G.C. & Kasai, H. Structural basis of long-term potentiation in single dendritic spines. Nature 429, 761-766 (2004).
50. Fifková , E. & Van Harreveld, A. Long-lasting morphological changes in dendritic spines of dentate granular cells following stimulation of the entorhinal area. J. Neurocytol. 6, 211-230 (1977).