The internal architecture of dendritic spines revealed by super-resolution imaging: What did we learn so far?

Experimental Cell Research

Volumn 335, Issue 2, 2015, Pages 180-186

  MacGillavry, Harold D ^a   Hoogenraad, Casper C ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Actin; Dendritic spine; Glutamate receptors; Postsynaptic density; Super resolution; Synapse

Indexed keywords

ACTIN; ACTIN BINDING PROTEIN; ACTIN RELATED PROTEIN 2-3 COMPLEX; AMPA RECEPTOR; ANKYRIN; DOPAMINE 1 RECEPTOR; GLUTAMATE RECEPTOR; METABOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; SPECTRIN;

ACTIN FILAMENT; BRAIN CELL; CYTOSKELETON; DENDRITIC SPINE; MOLECULAR IMAGING; NERVE CELL PLASTICITY; NONHUMAN; PALMITOYLATION; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVIEW; SPINE; SYNAPSE; SYNAPTIC TRANSMISSION; ANIMAL; HUMAN; METABOLISM; MICROSCOPY; PHYSIOLOGY; ULTRASTRUCTURE;

ACTIN CYTOSKELETON; ANIMALS; DENDRITIC SPINES; HUMANS; MICROSCOPY; RECEPTORS, GLUTAMATE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84937642570     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2015.02.024     Document Type: Review

References (65)

1. Matsuzaki M., Ellis-Davies G.C., Nemoto T., Miyashita Y., Iino M., Kasai H. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat. Neurosci. 2001, 4:1086-1092.
2. Harris K.M., Stevens J.K. Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J. Neurosci. 1989, 9:2982-2997.
3. Bosch M., Hayashi Y. Structural plasticity of dendritic spines. Curr. Opin. Neurobiol. 2012, 22:383-388.
4. Maglione M., Sigrist S.J. Seeing the forest tree by tree: super-resolution light microscopy meets the neurosciences. Nat. Neurosci. 2013, 16:790-797.
5. Triller A., Choquet D. New concepts in synaptic biology derived from single-molecule imaging. Neuron 2008, 59:359-374.
6. Huang B., Babcock H., Zhuang X. Breaking the diffraction barrier: super-resolution imaging of cells. Cell 2010, 143:1047-1058.
7. Sheng M., Hoogenraad C. The postsynaptic architecture of excitatory synapses: a more quantitative view. Annu. Rev. Biochem. 2007, 76:823-847.
8. Malenka R.C., Bear M.F. LTP and LTD: an embarrassment of riches. Neuron 2004, 44:5-21.
9. MacGillavry H.D., Kerr J.M., Blanpied T.A. Lateral organization of the postsynaptic density. Mol. Cell. Neurosci. 2011, 48:321-331.
10. Franks K.M., Stevens C.F., Sejnowski T.J. Independent sources of quantal variability at single glutamatergic synapses. J. Neurosci. 2003, 23:3186-3195.
11. Raghavachari S., Lisman J.E. Properties of quantal transmission at CA1 synapses. J. Neurophysiol. 2004, 92:2456-2467.
12. Lisman J.E., Raghavachari S., Tsien R.W. The sequence of events that underlie quantal transmission at central glutamatergic synapses. Nat. Rev. Neurosci. 2007, 8:597-609.
13. Freche D., Pannasch U., Rouach N., Holcman D. Synapse geometry and receptor dynamics modulate synaptic strength. PLoS One 2011, 6:e25122.
14. Ehlers M., Heine M., Groc L., Lee M., Choquet D. Diffusional trapping of GluR1 AMPA receptors by input-specific synaptic activity. Neuron 2007, 54:447-460.
15. Heine M., Groc L., Frischknecht R., Béïque J., Lounis B., Rumbaugh G., Huganir R., Cognet L., Choquet D. Surface mobility of postsynaptic AMPAwRs tunes synaptic transmission. Science 2008, 320:201-205.
16. Kerr J.M., Blanpied T.A. Subsynaptic AMPA receptor distribution is acutely regulated by actin-driven reorganization of the postsynaptic density. J. Neurosci. 2012, 32:658-673.
17. Masugi-Tokita M., Tarusawa E., Watanabe M., Molnar E., Fujimoto K., Shigemoto R. Number and density of AMPA receptors in individual synapses in the rat cerebellum as revealed by SDS-digested freeze-fracture replica labeling. J. Neurosci. 2007, 27:2135-2144.
18. Tarusawa E., Matsui K., Budisantoso T., Molnar E., Watanabe M., Matsui M., Fukazawa Y., Shigemoto R. Input-specific intrasynaptic arrangements of ionotropic glutamate receptors and their impact on postsynaptic responses. J. Neurosci. 2009, 29:12896-12908.
19. Dani A., Huang B., Bergan J., Dulac C., Zhuang X. Superresolution imaging of chemical synapses in the brain. Neuron 2010, 68:843-856.
20. Hoze N., Nair D., Hosy E., Sieben C., Manley S., Herrmann A., Sibarita J.B., Choquet D., Holcman D. Heterogeneity of AMPA receptor trafficking and molecular interactions revealed by superresolution analysis of live cell imaging. Proc. Natl. Acad. Sci. USA 2012, 109:17052-17057.
21. MacGillavry H.D., Song Y., Raghavachari S., Blanpied T.A. Nanoscale scaffolding domains within the postsynaptic density concentrate synaptic AMPA receptors. Neuron 2013, 78:615-622.
22. Nair D., Hosy E., Petersen J.D., Constals A., Giannone G., Choquet D., Sibarita J.B. Super-resolution imaging reveals that ampa receptors inside synapses are dynamically organized in nanodomains regulated by PSD95. J. Neurosci. 2013, 33:13204-13224.
23. Fukata Y., Dimitrov A., Boncompain G., Vielemeyer O., Perez F., Fukata M. Local palmitoylation cycles define activity-regulated postsynaptic subdomains. J. Cell Biol. 2013, 202:145-161.
24. Turrigiano G.G., Leslie K.R., Desai N.S., Rutherford L.C., Nelson S.B. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 1998, 391:892-896.
25. Granger A.J., Shi Y., Lu W., Cerpas M., Nicoll R.A. LTP requires a reserve pool of glutamate receptors independent of subunit type. Nature 2013, 493:495-500.
26. Hosokawa T., Mitsushima D., Kaneko R., Hayashi Y. Stoichiometry and Phosphoisotypes of Hippocampal AMPA-Type Glutamate Receptor Phosphorylation. Neuron 2015, 85:60-67.
27. Blanpied T.A., Scott D.B., Ehlers M.D. Dynamics and regulation of clathrin coats at specialized endocytic zones of dendrites and spines. Neuron 2002, 36:435-449.
28. Tardin C., Cognet L., Bats C., Lounis B., Choquet D. Direct imaging of lateral movements of AMPA receptors inside synapses. EMBO J. 2003, 22:4656-4665.
29. Lopez-Bendito G., Shigemoto R., Fairen A., Lujan R. Differential distribution of group I metabotropic glutamate receptors during rat cortical development. Cereb. Cortex 2002, 12:625-638.
30. Westin L., Reuss M., Lindskog M., Aperia A., Brismar H. Nanoscopic spine localization of Norbin, an mGluR5 accessory protein. BMC Neurosci. 2014, 15:45.
31. Ladepeche L., Dupuis J.P., Bouchet D., Doudnikoff E., Yang L., Campagne Y., Bezard E., Hosy E., Groc L. Single-molecule imaging of the functional crosstalk between surface NMDA and dopamine D1 receptors. Proc. Natl. Acad. Sci. USA 2013, 110:18005-18010.
32. Smith K.R., Kopeikina K.J., Fawcett-Patel J.M., Leaderbrand K., Gao R., Schurmann B., Myczek K., Radulovic J., Swanson G.T., Penzes P. Psychiatric risk factor ANK3/ankyrin-G nanodomains regulate the structure and function of glutamatergic synapses. Neuron 2014, 84:399-415.
33. Frost N.A., Kerr J.M., Lu H.E., Blanpied T.A. A network of networks: cytoskeletal control of compartmentalized function within dendritic spines. Curr. Opin. Neurobiol. 2010, 20:578-587.
34. Hotulainen P., Hoogenraad C.C. Actin in dendritic spines: connecting dynamics to function. J. Cell Biol. 2010, 189:619-629.
35. Urban N.T., Willig K.I., Hell S.W., Nagerl U.V. STED nanoscopy of actin dynamics in synapses deep inside living brain slices. Biophys. J. 2011, 101:1277-1284.
36. Izeddin I., Specht C.G., Lelek M., Darzacq X., Triller A., Zimmer C., Dahan M. Super-resolution dynamic imaging of dendritic spines using a low-affinity photoconvertible actin probe. PLoS One 2011, 6:e15611.
37. Honkura N., Matsuzaki M., Noguchi J., Ellis-Davies G.C., Kasai H. The subspine organization of actin fibers regulates the structure and plasticity of dendritic spines. Neuron 2008, 57:719-729.
38. Chazeau A., Mehidi A., Nair D., Gautier J.J., Leduc C., Chamma I., Kage F., Kechkar A., Thoumine O., Rottner K., Choquet D., Gautreau A., Sibarita J.B., Giannone G. Nanoscale segregation of actin nucleation and elongation factors determines dendritic spine protrusion. EMBO J. 2014, 33:2745-2764.
39. N.A. Frost, H.D. MacGillavry, H.E. Lu, T.A. Blanpied, 2013. Live-cell PALM of intracellular proteins in neurons, in: U. Valentin Nargerl, Antoine Triller (Eds.), Nanoscale Imaging of Synapses, vol. 84, pp. 93-123.
40. Tatavarty V., Das S., Yu J. Polarization of actin cytoskeleton is reduced in dendritic protrusions during early spine development in hippocampal neuron. Mol. Biol. Cell 2012, 23:3167-3177.
41. Tatavarty V., Kim E.J., Rodionov V., Yu J. Investigating sub-spine actin dynamics in rat hippocampal neurons with super-resolution optical imaging. PLoS One 2009, 4:e7724.
42. Frost N.A., Shroff H., Kong H., Betzig E., Blanpied T.A. Single-molecule discrimination of discrete perisynaptic and distributed sites of actin filament assembly within dendritic spines. Neuron 2010, 67:86-99.
43. Burette A.C., Lesperance T., Crum J., Martone M., Volkmann N., Ellisman M.H., Weinberg R.J. Electron tomographic analysis of synaptic ultrastructure. J. Comp. Neurol. 2012, 520:2697-2711.
44. Rotty J.D., Wu C., Bear J.E. New insights into the regulation and cellular functions of the ARP2/3 complex. Nat. Rev. Mol. Cell Biol. 2013, 14:7-12.
45. Racz B., Weinberg R.J. Organization of the Arp2/3 complex in hippocampal spines. J. Neurosci. 2008, 28:5654-5659.
46. Han K., Holder J.L., Schaaf C.P., Lu H., Chen H., Kang H., Tang J., Wu Z., Hao S., Cheung S.W., Yu P., Sun H., Breman A.M., Patel A., Lu H.C., Zoghbi H.Y. SHANK3 overexpression causes manic-like behaviour with unique pharmacogenetic properties. Nature 2013, 503:72-77.
47. Qualmann B., Boeckers T.M., Jeromin M., Gundelfinger E.D., Kessels M.M. Linkage of the actin cytoskeleton to the postsynaptic density via direct interactions of Abp1 with the ProSAP/Shank family. J. Neurosci. 2004, 24:2481-2495.
48. Du Y., Weed S.A., Xiong W.C., Marshall T.D., Parsons J.T. Identification of a novel cortactin SH3 domain-binding protein and its localization to growth cones of cultured neurons. Mol. Cell. Biol. 1998, 18:5838-5851.
49. Naisbitt S., Kim E., Tu J., Xiao B., Sala C., Valtschanoff J., Weinberg R., Worley P., Sheng M. Shank, a novel family of postsynaptic density proteins that binds to the NMDA receptor/PSD-95/GKAP complex and cortactin. Neuron 1999, 23:569-582.
50. Blanpied T.A., Kerr J.M., Ehlers M.D. Structural plasticity with preserved topology in the postsynaptic protein network. Proc. Natl. Acad. Sci. USA 2008, 105:12587-12592.
51. Lu H.E., MacGillavry H.D., Frost N.A., Blanpied T.A. Multiple spatial and kinetic subpopulations of CaMKII in spines and dendrites as resolved by single-molecule tracking PALM. J. Neurosci. 2014, 34:7600-7610.
52. Wagner W., Brenowitz S.D., Hammer J.A. Myosin-Va transports the endoplasmic reticulum into the dendritic spines of Purkinje neurons. Nat. Cell Biol. 2011, 13:40-48.
53. Wang Z., Edwards J.G., Riley N., Provance D.W., Karcher R., Li X.D., Davison I.G., Ikebe M., Mercer J.A., Kauer J.A., Ehlers M.D. Myosin Vb mobilizes recycling endosomes and AMPA receptors for postsynaptic plasticity. Cell 2008, 135:535-548.
54. Bourne J.N., Harris K.M. Balancing structure and function at hippocampal dendritic spines. Annu. Rev. Neurosci. 2008, 31:47-67.
55. Adrian M., Kusters R., Wierenga C.J., Storm C., Hoogenraad C.C., Kapitein L.C. Barriers in the brain: resolving dendritic spine morphology and compartmentalization. Front. Neuroanat. 2014, 8:142.
56. Nagerl U.V., Willig K.I., Hein B., Hell S.W., Bonhoeffer T. Live-cell imaging of dendritic spines by STED microscopy. Proc. Natl. Acad. Sci. USA 2008, 105:18982-18987.
57. Frost N.A., Lu H.E., Blanpied T.A. Optimization of cell morphology measurement via single-molecule tracking PALM. PLoS One 2012, 7:e36751.
58. Takasaki K., Sabatini B.L. Super-resolution 2-photon microscopy reveals that the morphology of each dendritic spine correlates with diffusive but not synaptic properties. Front. Neuroanat. 2014, 8:29.
59. Tonnesen J., Katona G., Rozsa B., Nagerl U.V. Spine neck plasticity regulates compartmentalization of synapses. Nat. Neurosci. 2014, 17:678-685.
60. Ewers H., Tada T., Petersen J.D., Racz B., Sheng M., Choquet D. A septin-dependent diffusion barrier at dendritic spine necks. PLoS One 2014, 9:e113916.
61. Ries J., Kaplan C., Platonova E., Eghlidi H., Ewers H. A simple, versatile method for GFP-based super-resolution microscopy via nanobodies. Nat. Methods 2012, 9:582-584.
62. Opazo F., Levy M., Byrom M., Schafer C., Geisler C., Groemer T.W., Ellington A.D., Rizzoli S.O. Aptamers as potential tools for super-resolution microscopy. Nat. Methods 2012, 9:938-939.
63. Jungmann R., Avendano M.S., Woehrstein J.B., Dai M., Shih W.M., Yin P. Multiplexed 3D cellular super-resolution imaging with DNA-PAINT and Exchange-PAINT. Nat. Methods 2014, 11:313-318.
64. Shim S.H., Xia C., Zhong G., Babcock H.P., Vaughan J.C., Huang B., Wang X., Xu C., Bi G.Q., Zhuang X. Super-resolution fluorescence imaging of organelles in live cells with photoswitchable membrane probes. Proc. Natl. Acad. Sci. USA 2012, 109:13978-13983.
65. Revelo N.H., Kamin D., Truckenbrodt S., Wong A.B., Reuter-Jessen K., Reisinger E., Moser T., Rizzoli S.O. A new probe for super-resolution imaging of membranes elucidates trafficking pathways. J. Cell Biol. 2014, 205:591-606.