Activity-dependent coordinated mobility of hippocampal inhibitory synapses visualized with presynaptic and postsynaptic tagged-molecular markers

Molecular and Cellular Neuroscience

Volumn 49, Issue 2, 2012, Pages 184-195

  Kuriu, Toshihiko ^a   Yanagawa, Yuchio ^b,c   Konishi, Shiro ^a  

^a TOKUSHIMA BUNRI UNIVERSITY   (Japan)

^b GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Inhibitory synapse; Structural plasticity; Synapse development; Synapse formation

Indexed keywords

FLUORESCENT DYE; GEPHYRIN; MOLECULAR MARKER; RED FLUORESCENT PROTEIN; TETRODOTOXIN; VESICULAR INHIBITORY AMINO ACID TRANSPORTER; YELLOW FLUORESCENT PROTEIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DENDRITE; DEVELOPMENTAL STAGE; DISSOCIATION; ELECTROPHYSIOLOGY; GABAERGIC SYSTEM; HIPPOCAMPUS; IMAGE ANALYSIS; IMMUNOCYTOCHEMISTRY; INHIBITION KINETICS; MORPHOLOGY; MOUSE; NERVE CELL; NONHUMAN; PHYSICAL MOBILITY; POSTSYNAPTIC INHIBITION; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; SYNAPTIC INHIBITION;

ANIMALS; AXONS; CARRIER PROTEINS; CELLS, CULTURED; DENDRITIC SPINES; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; NEURONS; PRESYNAPTIC TERMINALS; RATS; SYNAPSES; TIME-LAPSE IMAGING; VESICULAR INHIBITORY AMINO ACID TRANSPORT PROTEINS;

EID: 84856775533     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2011.11.002     Document Type: Article

References (43)

1. Bannai H., Levi S., Schweizer C., Inoue T., Launey T., Racine V., Sibarita J.B., Mikoshiba K., Triller A. Activity-dependent tuning of inhibitory neurotransmission based on GABAAR diffusion dynamics. Neuron 2009, 62:670-682.
2. Bonhoeffer T., Yuste R. Spine motility. Phenomenology, mechanisms, and function. Neuron 2002, 35:1019-1027.
3. Colicos M.A., Collins B.E., Sailor M.J., Goda Y. Remodeling of synaptic actin induced by photoconductive stimulation. Cell 2001, 107:605-616.
4. Csicsvari J., Hirase H., Czurko A., Buzsaki G. Reliability and state dependence of pyramidal cell-interneuron synapses in the hippocampus: an ensemble approach in the behaving rat. Neuron 1998, 21:179-189.
5. Dunaevsky A., Blazeski R., Yuste R., Mason C. Spine motility with synaptic contact. Nat. Neurosci. 2001, 4:685-686.
6. Ebihara T., Kawabata I., Usui S., Sobue K., Okabe S. Synchronized formation and remodeling of postsynaptic densities: long-term visualization of hippocampal neurons expressing postsynaptic density proteins tagged with green fluorescent protein. J. Neurosci. 2003, 23:2170-2181.
7. Ehrensperger M.V., Hanus C., Vannier C., Triller A., Dahan M. Multiple association states between glycine receptors and gephyrin identified by SPT analysis. Biophys. J. 2007, 92:3706-3718.
8. Engert F., Bonhoeffer T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 1999, 399:66-70.
9. Esclapez M., Tillakaratne N.J., Kaufman D.L., Tobin A.J., Houser C.R. Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J. Neurosci. 1994, 14:1834-1855.
10. Fischer M., Kaech S., Knutti D., Matus A. Rapid actin-based plasticity in dendritic spines. Neuron 1998, 20:847-854.
11. Fuhrmann J.C., Kins S., Rostaing P., El Far O., Kirsch J., Sheng M., Triller A., Betz H., Kneussel M. Gephyrin interacts with Dynein light chains 1 and 2, components of motor protein complexes. J. Neurosci. 2002, 22:5393-5402.
12. Hanus C., Ehrensperger M.V., Triller A. Activity-dependent movements of postsynaptic scaffolds at inhibitory synapses. J. Neurosci. 2006, 26:4586-4595.
13. Harris K.M., Kater S.B. Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function. Annu. Rev. Neurosci. 1994, 17:341-371.
14. Hartman K.N., Pal S.K., Burrone J., Murthy V.N. Activity-dependent regulation of inhibitory synaptic transmission in hippocampal neurons. Nat. Neurosci. 2006, 9:642-649.
15. Jacob T.C., Bogdanov Y.D., Magnus C., Saliba R.S., Kittler J.T., Haydon P.G., Moss S.J. Gephyrin regulates the cell surface dynamics of synaptic GABAA receptors. J. Neurosci. 2005, 25:10469-10478.
16. Kameyama K., Sohya K., Ebina T., Fukuda A., Yanagawa Y., Tsumoto T. Difference in binocularity and ocular dominance plasticity between GABAergic and excitatory cortical neurons. J. Neurosci. 2010, 30:1551-1559.
17. Kasai H., Fukuda M., Watanabe S., Hayashi-Takagi A., Noguchi J. Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci. 2010, 33:121-129.
18. Kneussel M. Dynamic stabilization: structural plasticity at inhibitory postsynaptic sites. Traffic 2006, 7:1604-1606.
19. Konur S., Yuste R. Developmental regulation of spine and filopodial motility in primary visual cortex: reduced effects of activity and sensory deprivation. J. Neurobiol. 2004, 59:236-246.
20. Konur S., Yuste R. Imaging the motility of dendritic protrusions and axon terminals: roles in axon sampling and synaptic competition. Mol. Cell. Neurosci. 2004, 27:427-440.
21. Korkotian E., Segal M. Regulation of dendritic spine motility in cultured hippocampal neurons. J. Neurosci. 2001, 21:6115-6124.
22. 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, 26:7693-7706.
23. Kuriu T., Yanagawa Y., Konishi S. Formation and dynamics of GABAergic inhibitory synaptic connections between hippocampal interneurons and pyramidal neurons. Program No. 551.20. Neuroscience Meeting Planner 2010, Society for Neuroscience, San Diego, CA, Online.
24. Legendre P. The glycinergic inhibitory synapse. Cell. Mol. Life Sci. 2001, 58:760-793.
25. Maas C., Tagnaouti N., Loebrich S., Behrend B., Lappe-Siefke C., Kneussel M. Neuronal cotransport of glycine receptor and the scaffold protein gephyrin. J. Cell Biol. 2006, 172:441-451.
26. Maletic-Savatic M., Malinow R., Svoboda K. Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 1999, 283:1923-1927.
27. Matsuzaki M., Honkura N., Ellis-Davies G.C., Kasai H. Structural basis of long-term potentiation in single dendritic spines. Nature 2004, 429:761-766.
28. McIntire S.L., Reimer R.J., Schuske K., Edwards R.H., Jorgensen E.M. Identification and characterization of the vesicular GABA transporter. Nature 1997, 389:870-876.
29. Megias M., Emri Z., Freund T.F., Gulyas A.I. Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 2001, 102:527-540.
30. Meier J., Vannier C., Serge A., Triller A., Choquet D. Fast and reversible trapping of surface glycine receptors by gephyrin. Nat. Neurosci. 2001, 4:253-260.
31. Mody I., De Koninck Y., Otis T.S., Soltesz I. Bridging the cleft at GABA synapses in the brain. Trends Neurosci. 1994, 17:517-525.
32. Moss S.J., Smart T.G. Constructing inhibitory synapses. Nat. Rev. Neurosci. 2001, 2:240-250.
33. Nagai T., Ibata K., Park E.S., Kubota M., Mikoshiba K., Miyawaki A. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 2002, 20:87-90.
34. Nikonenko I., Jourdain P., Muller D. Presynaptic remodeling contributes to activity-dependent synaptogenesis. J. Neurosci. 2003, 23:8498-8505.
35. Okabe S., Kim H.D., Miwa A., Kuriu T., Okado H. Continual remodeling of postsynaptic density and its regulation by synaptic activity. Nat. Neurosci. 1999, 2:804-811.
36. Prior P., Schmitt B., Grenningloh G., Pribilla I., Multhaup G., Beyreuther K., Maulet Y., Werner P., Langosch D., Kirsch J., et al. Primary structure and alternative splice variants of gephyrin, a putative glycine receptor-tubulin linker protein. Neuron 1992, 8:1161-1170.
37. Sagne C., El Mestikawy S., Isambert M.F., Hamon M., Henry J.P., Giros B., Gasnier B. Cloning of a functional vesicular GABA and glycine transporter by screening of genome databases. FEBS Lett. 1997, 417:177-183.
38. Shaner N.C., Campbell R.E., Steinbach P.A., Giepmans B.N., Palmer A.E., Tsien R.Y. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 2004, 22:1567-1572.
39. Studler B., Fritschy J.M., Brunig I. GABAergic and glutamatergic terminals differentially influence the organization of GABAergic synapses in rat cerebellar granule cells in vitro. Neuroscience 2002, 114:123-133.
40. Umeda T., Ebihara T., Okabe S. Simultaneous observation of stably associated presynaptic varicosities and postsynaptic spines: morphological alterations of CA3-CA1 synapses in hippocampal slice cultures. Mol. Cell. Neurosci. 2005, 28:264-274.
41. Wang Y., Kakizaki T., Sakagami H., Saito K., Ebihara S., Kato M., Hirabayashi M., Saito Y., Furuya N., Yanagawa Y. Fluorescent labeling of both GABAergic and glycinergic neurons in vesicular GABA transporter (VGAT)-venus transgenic mouse. Neuroscience 2009, 164:1031-1043.
42. Wierenga C.J., Becker N., Bonhoeffer T. GABAergic synapses are formed without the involvement of dendritic protrusions. Nat. Neurosci. 2008, 11:1044-1052.
43. Yu W., Jiang M., Miralles C.P., Li R.W., Chen G., de Blas A.L. Gephyrin clustering is required for the stability of GABAergic synapses. Mol. Cell. Neurosci. 2007, 36:484-500.