Presynaptic and postsynaptic scaffolds: Dynamics fast and slow

Neuroscientist

Volumn 20, Issue 5, 2014, Pages 439-452

  Ziv, Noam E ^a   Fisher Lavie, Arava ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

FRAP; photoactivation; synaptic dynamics; synaptic scaffolds; synaptic tenacity

Indexed keywords

NEUROTRANSMITTER RECEPTOR;

DYNAMICS; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; NONHUMAN; PHOTOACTIVATION; POSTSYNAPTIC DENSITY; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC POTENTIAL; REVIEW; SYNAPSE; SYNAPSE VESICLE; ANIMAL; PHYSIOLOGY;

ANIMALS; SYNAPSES;

EID: 84907194005     PISSN: 10738584     EISSN: 10894098     Source Type: Journal    
DOI: 10.1177/1073858414523321     Document Type: Review

References (90)

1. Ashby MC, Maier SR, Nishimune A, Henley JM. Lateral diffusion drives constitutive exchange of AMPA receptors at dendritic spines and is regulated by spine morphology. J Neurosci. 2006 ; 26: 7046-55
2. Baitinger C, Willard M. Axonal transport of synapsin I-like proteins in rabbit retinal ganglion cells. J Neurosci. 1987 ; 7: 3723-35
3. Bats C, Groc L, Choquet D. The interaction between Stargazin and PSD-95 regulates AMPA receptor surface trafficking. Neuron. 2007 ; 53: 719-34
4. Calamai M, Specht CG, Heller J, Alcor D, Machado P, Vannier C, Triller A. Gephyrin oligomerization controls GlyR mobility and synaptic clustering. J Neurosci. 2009 ; 29: 7639-48
5. Cane M, Maco B, Knott G, Holtmaat A. The Relationship between PSD-95 Clustering and Spine Stability In Vivo. J Neurosci. 2014 ; 34: 2075-86
6. Charrier C, Machado P, Tweedie-Cullen RY, Rutishauser D, Mansuy IM, Triller A. A crosstalk between β1 and β3 integrins controls glycine receptor and gephyrin trafficking at synapses. Nat Neurosci. 2010 ; 13: 1388-95
7. Chi P, Greengard P, Ryan TA. Synapsin dispersion and reclustering during synaptic activity. Nat Neurosci. 2001 ; 4: 1187-93
8. Choquet D, Triller A. The dynamic synapse. Neuron. 2013 ; 80: 691-703
9. Cohen L, Koffman N, Meiri H, Yarom Y, Lampl I, Mizrahi A. Time-lapse electrical recordings of single neurons from the mouse neocortex. Proc Natl Acad Sci U S A. 2013a ; 110: 5665-70
10. Cohen LD, Zuchman R, Sorokina O, Müller A, Dieterich DC, Armstrong JD. Metabolic turnover of synaptic proteins: kinetics, interdependencies and implications for synaptic maintenance. PLoS One.. 2013b ; 8: e63191
11. Darcy KJ, Staras K, Collinson LM, Goda Y. Constitutive sharing of recycling synaptic vesicles between presynaptic boutons. Nat Neurosci. 2006 ; 9: 315-21
12. Dobie FA, Craig AM. Inhibitory synapse dynamics: coordinated presynaptic and postsynaptic mobility and the major contribution of recycled vesicles to new synapse formation. J Neurosci.. 2011 ; 31: 10481-93
13. Ehlers MD. Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat Neurosci. 2003 ; 6: 231-42
14. Feng W, Zhang M. Organization and dynamics of PDZ-domain-related supramodules in the postsynaptic density. Nat Rev Neurosci. 2009 ; 10: 87-99
15. Fernandez-Alfonso T, Kwan R, Ryan TA. Synaptic vesicles interchange their membrane proteins with a large surface reservoir during recycling. Neuron. 2006 ; 51: 179-86
16. Fernandez-Alfonso T, Ryan TA. A heterogeneous "resting" pool of synaptic vesicles that is dynamically interchanged across boutons in mammalian CNS synapses. Brain Cell Biol. 2008 ; 36: 87-100
17. Fischer M, Kaech S, Knutti D, Matus A. Rapid actin-based plasticity in dendritic spines. Neuron. 1998 ; 20: 847-54
18. Fisher-Lavie A, Zeidan A, Stern M, Garner CC, Ziv NE. Use dependence of presynaptic tenacity. J Neurosci. 2011 ; 31: 16770-80
19. Fisher-Lavie A, Ziv NE. Matching dynamics of presynaptic and postsynaptic scaffolds. J Neurosci. 2013 ; 33: 13094-100
20. Fu Y, Huang ZJ. Differential dynamics and activity-dependent regulation of alpha- and beta-neurexins at developing GABAergic synapses. Proc Natl Acad Sci U S A. 2010 ; 107: 22699-704
21. Fukata Y, Dimitrov A, Boncompain G, Vielemeyer O, Perez F, Fukata M. Local palmitoylation cycles define activity-regulated postsynaptic subdomains. J Cell Biol. 2013 ; 202: 145-61
22. Gray NW, Weimer RM, Bureau I, Svoboda K. Rapid redistribution of synaptic PSD-95 in the neocortex in vivo. PLoS Biol. 2006 ; 4: 2065-75
23. Grillo FW, Song S, Teles-Grilo Ruivo LM, Huang L, Gao G, Knott GW. Increased axonal bouton dynamics in the aging mouse cortex. Proc Natl Acad Sci U S A. 2013 ; 110: E1514-23
24. Gundelfinger ED, Fejtova A. Molecular organization and plasticity of the cytomatrix at the active zone. Curr Opin Neurobiol. 2012 ; 22: 423-30
25. Hellwig B, Schüz A, Aertsen A. Synapses on axon collaterals of pyramidal cells are spaced at random intervals: a Golgi study in the mouse cerebral cortex. Biol Cybern. 1994 ; 71: 1-12
26. Herzog E, Nadrigny F, Silm K, Biesemann C, Helling I, Bersot T. In vivo imaging of intersynaptic vesicle exchange using VGLUT1 Venus knock-in mice. J Neurosci. 2011 ; 31: 15544-59
27. Holtmaat A, Svoboda K. Experience-dependent structural synaptic plasticity in the mammalian brain. Nat Rev Neurosci. 2009 ; 10: 647-58
28. Holtmaat A, Wilbrecht L, Knott GW, Welker E, Svoboda K. Experience dependent and cell-type-specific spine growth in the neocortex. Nature. 2006 ; 441: 979-83
29. Jacob TC, Bogdanov YD, Magnus C, Saliba RS, Kittler JT, Haydon PG. Gephyrin regulates the cell surface dynamics of synaptic GABAA receptors. J Neurosci. 2005 ; 25: 10469-78
30. Kalla S, Stern M, Basu J, Varoqueaux F, Reim K, Rosenmund C. Molecular dynamics of a presynaptic active zone protein studied in Munc13-1-enhanced yellow fluorescent protein knock-in mutant mice. J Neurosci. 2006 ; 26: 13054-66
31. Kaufman M, Corner MA, Ziv NE. Long-term relationships between cholinergic tone, synchronous bursting and synaptic remodeling. PLoS One. 2012 ; 7: e40980
32. Kerr JM, Blanpied TA. Subsynaptic AMPA receptor distribution is acutely regulated by actin-driven reorganization of the postsynaptic density. J Neurosci. 2012 ; 32: 658-73
33. Kim SA, Sanabria H, Digman MA, Gratton E, Schwille P, Zipfel WR. Quantifying translational mobility in neurons: comparison between current optical techniques. J Neurosci. 2010 ; 30: 16409-16
34. Kneussel M, Loebrich S. Trafficking and synaptic anchoring of ionotropic inhibitory neurotransmitter receptors. Biol Cell. 2007 ; 99: 297-309
35. Krueger SR, Kolar A, Fitzsimonds RM. The presynaptic release apparatus is functional in the absence of dendritic contact and highly mobile within isolated axons. Neuron. 2003 ; 40: 945-57
36. Kuriu T, Inoue A, Bito H, Sobue K, Okabe S. Differential control of postsynaptic density scaffolds via actin-dependent and -independent mechanisms. J Neurosci. 2006 ; 26: 7693-706
37. Lee SJ, Escobedo-Lozoya Y, Szatmari EM, Yasuda R. Activation of CaMKII in single dendritic spines during long-term potentiation. Nature. 2009 ; 458: 299-304
38. Li Z, Murthy VN. Visualizing postendocytic traffic of synaptic vesicles at hippocampal synapses. Neuron. 2001 ; 31: 593-605
39. Lisman J, Raghavachari S. A unified model of the presynaptic and postsynaptic changes during LTP at CA1 synapses. Sci STKE. 2006 2006 ; re11:
40. Loebel A, Le Bé JV, Richardson MJ, Markram H, Herz AV. Matched pre- and post-synaptic changes underlie synaptic plasticity over long time scales. J Neurosci. 2013 ; 33: 6257-66
41. Loewenstein Y, Kuras A, Rumpel S. Multiplicative dynamics underlie the emergence of the log-normal distribution of spine sizes in the neocortex in vivo. J Neurosci. 2011 ; 31: 9481-8
42. MacGillavry HD, Song Y, Raghavachari S, Blanpied TA. Nanoscale scaffolding domains within the postsynaptic density concentrate synaptic AMPA receptors. Neuron. 2013 ; 78: 615-22
43. Matz J, Gilyan A, Kolar A, McCarvill T, Krueger SR. Rapid structural alterations of the active zone lead to sustained changes in neurotransmitter release. Proc Natl Acad Sci U S A. 2010 ; 107: 8836-41
44. Minerbi A, Kahana R, Goldfeld L, Kaufman M, Marom S, Ziv NE. Long-term relationships between synaptic tenacity, synaptic remodeling, and network activity. PLoS Biol. 2009 ; 7: e1000136
45. Mondin M, Labrousse V, Hosy E, Heine M, Tessier B, Levet F. Neurexin-neuroligin adhesions capture surface-diffusing AMPA receptors through PSD-95 scaffolds. J Neurosci. 2011 ; 31: 13500-15
46. Mostany R, Anstey JE, Crump KL, Maco B, Knott G, Portera-Cailliau C. Altered synaptic dynamics during normal brain aging. J Neurosci. 2013 ; 33: 4094-104
47. Nair D, Hosy E, Petersen JD, Constals A, Giannone G, Choquet D. Super-resolution imaging reveals that AMPA receptors inside synapses are dynamically organized in nanodomains regulated by PSD95. J Neurosci. 2013 ; 33: 13204-24
48. Nakagawa T, Futai K, Lashuel HA, Lo I, Okamoto K, Walz T. Quaternary structure, protein dynamics, and synaptic function of SAP97 controlled by L27 domain interactions. Neuron. 2004a ; 44: 453-67
49. Nakagawa T, Engler JA, Sheng M. The dynamic turnover and functional roles of alpha-actinin in dendritic spines. Neuropharmacology. 2004b ; 47: 734-45
50. Nelson CD, Kim MJ, Hsin H, Chen Y, Sheng M. Phosphorylation of threonine-19 of PSD-95 by GSK-3β is required for PSD-95 mobilization and long-term depression. J Neurosci. 2013 ; 33: 12122-35
51. Okabe S. Molecular dynamics of the excitatory synapse. Adv Exp Med Biol. 2012 ; 970: 131-52
52. Okabe S, Urushido T, Konno D, Okado H, Sobue K. Rapid redistribution of the postsynaptic density protein PSD-Zip45 (Homer 1c) and its differential regulation by NMDA receptors and calcium channels. J Neurosci. 2001 ; 21: 9561-71
53. Opazo P, Sainlos M, Choquet D. Regulation of AMPA receptor surface diffusion by PSD-95 slots. Curr Opin Neurobiol. 2012 ; 22: 453-60
54. Petrucci TC, Macioce P, Paggi P. Axonal transport kinetics and posttranslational modification of synapsin I in mouse retinal ganglion cells. J Neurosci. 1991 ; 11: 2938-46
55. Price JC, Guan S, Burlingame A, Prusiner SB, Ghaemmaghami S. Analysis of proteome dynamics in the mouse brain. Proc Natl Acad Sci U S A. 2010 ; 107: 14508-13
56. Ribrault C, Reingruber J, Petkovi M, Galli T, Ziv NE, Holcman D. Syntaxin1A lateral diffusion reveals transient and local SNARE interactions. J Neurosci. 2011 ; 31: 17590-602
57. Sharma K, Fong DK, Craig AM. Postsynaptic protein mobility in dendritic spines: long-term regulation by synaptic NMDA receptor activation. Mol Cell Neurosci. 2006 ; 31: 702-12
58. Scott DA, Das U, Tang Y, Roy S. Mechanistic logic underlying the axonal transport of cytosolic proteins. Neuron. 2011 ; 70: 441-54
59. Shen K, Meyer T. Dynamic control of CaMKII translocation and localization in hippocampal neurons by NMDA receptor stimulation. Science. 1999 ; 284: 162-6
60. Sheng M, Hoogenraad CC. The postsynaptic architecture of excitatory synapses: a more quantitative view. Annu Rev Biochem.. 2007 ; 76: 823-47
61. Shepherd GM, Harris KM. Three-dimensional structure and composition of CA3 ->CA1 axons in rat hippocampal slices: implications for presynaptic connectivity and compartmentalization. J Neurosci. 1998 ; 18: 8300-10
62. Shepherd GM, Raastad M, Andersen P. General and variable features of varicosity spacing along unmyelinated axons in the hippocampus and cerebellum. Proc Natl Acad Sci U S A. 2002 ; 99: 6340-5
63. Siksou L, Triller A, Marty S. Ultrastructural organization of presynaptic terminals. Curr Opin Neurobiol. 2011 ; 21: 261-8
64. Spangler SA, Schmitz SK, Kevenaar JT, de Graaff E, de Wit H, Demmers J. Liprin-α2 promotes the presynaptic recruitment and turnover of RIM1/CASK to facilitate synaptic transmission. J Cell Biol. 2013 ; 201: 915-28
65. Specht CG, Izeddin I, Rodriguez PC, El Beheiry M, Rostaing P, Darzacq X. Quantitative nanoscopy of inhibitory synapses: counting gephyrin molecules and receptor binding sites. Neuron.. 2013 ; 79: 308-21
66. Specht CG, Triller A. The dynamics of synaptic scaffolds. Bioessays. 2008 ; 30: 1062-74
67. Star EN, Newton AJ, Murthy VN. Real-time imaging of Rab3a and Rab5a reveals differential roles in presynaptic function. J Physiol. 2005 ; 569 (Pt 1). 103-17
68. Staras K, Branco T. Sharing vesicles between central presynaptic terminals: implications for synaptic function. Front Synaptic Neurosci.. 2010 ; 2: 20
69. Staras K, Branco T, Burden JJ, Pozo K, Darcy K, Marra V. A vesicle superpool spans multiple presynaptic terminals in hippocampal neurons. Neuron. 2010 ; 66: 37-44
70. Staras K, Mikulincer D, Gitler D. Monitoring and quantifying dynamic physiological processes in live neurons using fluorescence recovery after photobleaching. J Neurochem. 2013 ; 126: 213-22
71. Südhof TC. The presynaptic active zone. Neuron. 2012 ; 75: 11-25
72. Takahashi H, Yamazaki H, Hanamura K, Sekino Y, Shirao T. Activity of the AMPA receptor regulates drebrin stabilization in dendritic spine morphogenesis. J Cell Sci. 2009 ; 122 (Pt 8). 1211-9
73. Tang Y, Scott D, Das U, Gitler D, Ganguly A, Roy S. Fast vesicle transport is required for the slow axonal transport of synapsin. J Neurosci. 2013 ; 33: 15362-75
74. Thoumine O, Lambert M, Mège RM, Choquet D. Regulation of N-cadherin dynamics at neuronal contacts by ligand binding and cytoskeletal coupling. Mol Biol Cell. 2005 ; 17: 862-75
75. Tsukamoto-Yasui M, Sasaki T, Matsumoto W, Hasegawa A, Toyoda T, Usami A. Active hippocampal networks undergo spontaneous synaptic modification. PLoS One. 2007 ; 2: e1250
76. Tsuriel S, Fisher A, Wittenmayer N, Dresbach T, Garner CC, Ziv NE. Exchange and redistribution dynamics of the cytoskeleton of the active zone molecule bassoon. J Neurosci. 2009 ; 29: 351-8
77. Tsuriel S, Geva R, Zamorano P, Dresbach T, Boeckers T, Gundelfinger ED. Local sharing as a predominant determinant of synaptic matrix molecular dynamics. PLoS Biol. 2006 ; 4: e271
78. Usami A, Matsuki N, Ikegaya Y. Spontaneous plasticity of multineuronal activity patterns in activated hippocampal networks. Neural Plast. 2008 ; 2008: 108969
79. Verpelli C, Schmeisser MJ, Sala C, Boeckers TM. Scaffold proteins at the postsynaptic density. Adv Exp Med Biol. 2012 ; 970: 29-61
80. Vlachos A, Reddy-Alla S, Papadopoulos T, Deller T, Betz H. Homeostatic regulation of gephyrin scaffolds and synaptic strength at mature hippocampal GABAergic postsynapses. Cereb Cortex. 2013 ; 23: 2700-11
81. Waites CL, Leal-Ortiz SA, Okerlund N, Dalke H, Fejtova A, Altrock WD. Bassoon and Piccolo maintain synapse integrity by regulating protein ubiquitination and degradation. EMBO J. 2013 ; 32: 954-69
82. Waites CL, Specht CG, Härtel K, Leal-Ortiz S, Genoux D, Li D, Drisdel RC. Synaptic SAP97 isoforms regulate AMPA receptor dynamics and access to presynaptic glutamate. J Neurosci. 2009 ; 29: 4332-45
83. Westphal V, Rizzoli SO, Lauterbach MA, Kamin D, Jahn R, Hell SW. Video-rate far-field optical nanoscopy dissects synaptic vesicle movement. Science. 2008 ; 320: 246-9
84. Wienisch M, Klingauf J. Vesicular proteins exocytosed and subsequently retrieved by compensatory endocytosis are nonidentical. Nat Neurosci. 2006 ; 9: 1019-27
85. Yao I, Iida J, Nishimura W, Hata Y. Synaptic localization of SAPAP1, a synaptic membrane-associated protein. Genes Cells. 2003 ; 8: 121-9
86. Yao I, Takagi H, Ageta H, Kahyo T, Sato S, Hatanaka K. SCRAPPER-dependent ubiquitination of active zone protein RIM1 regulates synaptic vesicle release. Cell. 2007 ; 130: 943-57
87. Yasumatsu N, Matsuzaki M, Miyazaki T, Noguchi J, Kasai H. Principles of long-term dynamics of dendritic spines. J Neurosci. 2008 ; 28: 13592-608
88. Yudowski GA, Olsen O, Adesnik H, Marek KW, Bredt DS. Acute inactivation of PSD-95 destabilizes AMPA receptors at hippocampal synapses. PLoS One. 2013 ; 8: e53965
89. Zeidan A, Ziv NE. Neuroligin-1 loss is associated with reduced tenacity of excitatory synapses. PLoS One. 2012 ; 7: e42314
90. Zheng CY, Petralia RS, Wang YX, Kachar B, Wenthold RJ. SAP102 is a highly mobile MAGUK in spines. J Neurosci. 2010 ; 30: 4757-66