STED Nanoscopy Reveals the Ubiquity of Subcortical Cytoskeleton Periodicity in Living Neurons

Cell Reports

Volumn 10, Issue 8, 2015, Pages 1246-1251

  D'Este, Elisa ^a   Kamin, Dirk ^a   Göttfert, Fabian ^a   El Hady, Ahmed ^a,b   Hell, StefanW ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; RHODAMINE; SILICON RHODAMINE; UNCLASSIFIED DRUG; FLUORESCENT DYE;

ACTIN FILAMENT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL LABELING; CELLULAR DISTRIBUTION; DENDRITE; DIAGNOSTIC PROCEDURE; MOLECULAR IMAGING; MOUSE; NANOANALYSIS; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REGULATORY MECHANISM; STIMULATED EMISSION DEPLETION NANOSCOPY; SUBCORTEX; ANIMAL; C57BL MOUSE; CELL CULTURE; CHEMISTRY; CYTOLOGY; CYTOSKELETON; FEMALE; FLUORESCENCE MICROSCOPY; MALE; METABOLISM; NANOTECHNOLOGY; PHYSIOLOGY; RANVIER NODE; RAT; WISTAR RAT;

ACTINS; ANIMALS; CELLS, CULTURED; CYTOSKELETON; DENDRITES; FEMALE; FLUORESCENT DYES; MALE; MICE; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE; NANOTECHNOLOGY; NERVE NET; NEURONS; RANVIER'S NODES; RATS; RATS, WISTAR;

EID: 84924619572     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.02.007     Document Type: Article

References (32)

1. Al-Bassam S., Xu M., Wandless T.J., Arnold D.B. Differential trafficking of transport vesicles contributes to the localization of dendritic proteins. Cell Rep. 2012, 2:89-100.
2. Arnold D.B., Gallo G. Structure meets function: actin filaments and myosin motors in the axon. J.Neurochem. 2014, 129:213-220.
3. Boiko T., Vakulenko M., Ewers H., Yap C.C., Norden C., Winckler B. Ankyrin-dependent and -independent mechanisms orchestrate axonal compartmentalization of L1 family members neurofascin and L1/neuron-glia cell adhesion molecule. J.Neurosci. 2007, 27:590-603.
4. Davis J.Q., Lambert S., Bennett V. Molecular composition of the node of Ranvier: identification of ankyrin-binding cell adhesion molecules neurofascin (mucin+/third FNIII domain-) and NrCAM at nodal axon segments. J.Cell Biol. 1996, 135:1355-1367.
5. Dotti C.G., Sullivan C.A., Banker G.A. The establishment of polarity by hippocampal neurons in culture. J.Neurosci. 1988, 8:1454-1468.
6. Einheber S., Zanazzi G., Ching W., Scherer S., Milner T.A., Peles E., Salzer J.L. The axonal membrane protein Caspr, a homologue of neurexin IV, is a component of the septate-like paranodal junctions that assemble during myelination. J.Cell Biol. 1997, 139:1495-1506.
7. Fifková E. Actin in the nervous system. Brain Res. 1985, 356:187-215.
8. Fifková E., Delay R.J. Cytoplasmic actin in neuronal processes as a possible mediator of synaptic plasticity. J.Cell Biol. 1982, 95:345-350.
9. Fonseca R. Activity-dependent actin dynamics are required for the maintenance of long-term plasticity and for synaptic capture. Eur. J. Neurosci. 2012, 35:195-206.
10. Göttfert F., Wurm C.A., Mueller V., Berning S., Cordes V.C., Honigmann A., Hell S.W. Coaligned dual-channel STED nanoscopy and molecular diffusion analysis at 20nm resolution. Biophys. J. 2013, 105:L01-L03.
11. 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.
12. Jones S.L., Korobova F., Svitkina T. Axon initial segment cytoskeleton comprises a multiprotein submembranous coat containing sparse actin filaments. J.Cell Biol. 2014, 205:67-81.
13. Korobova F., Svitkina T. Molecular architecture of synaptic actin cytoskeleton in hippocampal neurons reveals a mechanism of dendritic spine morphogenesis. Mol. Biol. Cell 2010, 21:165-176.
14. Lukinavičius G., Reymond L., D'Este E., Masharina A., Göttfert F., Ta H., Güther A., Fournier M., Rizzo S., Waldmann H., et al. Fluorogenic probes for live-cell imaging of the cytoskeleton. Nat. Methods 2014, 11:731-733.
15. Peles E., Salzer J.L. Molecular domains of myelinated axons. Curr. Opin. Neurobiol. 2000, 10:558-565.
16. Petersen J.D., Kaech S., Banker G. Selective microtubule-based transport of dendritic membrane proteins arises in concert with axon specification. J.Neurosci. 2014, 34:4135-4147.
17. Punge A., Rizzoli S.O., Jahn R., Wildanger J.D., Meyer L., Schönle A., Kastrup L., Hell S.W. 3D reconstruction of high-resolution STED microscope images. Microsc. Res. Tech. 2008, 71:644-650.
18. Ramachandran B., Frey J.U. Interfering with the actin network and its effect on long-term potentiation and synaptic tagging in hippocampal CA1 neurons in slices invitro. J.Neurosci. 2009, 29:12167-12173.
19. Rasband M.N. The axon initial segment and the maintenance of neuronal polarity. Nat. Rev. Neurosci. 2010, 11:552-562.
20. Sankaranarayanan S., Atluri P.P., Ryan T.A. Actin has a molecular scaffolding, not propulsive, role in presynaptic function. Nat. Neurosci. 2003, 6:127-135.
21. Schnell U., Dijk F., Sjollema K.A., Giepmans B.N. Immunolabeling artifacts and the need for live-cell imaging. Nat. Methods 2012, 9:152-158.
22. Song A.H., Wang D., Chen G., Li Y., Luo J., Duan S., Poo M.M. A selective filter for cytoplasmic transport at the axon initial segment. Cell 2009, 136:1148-1160.
23. Spillane M., Ketschek A., Jones S.L., Korobova F., Marsick B., Lanier L., Svitkina T., Gallo G. The actin nucleating Arp2/3 complex contributes to the formation of axonal filopodia and branches through the regulation of actin patch precursors to filopodia. Dev. Neurobiol. 2011, 71:747-758.
24. Susuki K., Rasband M.N. Spectrin and ankyrin-based cytoskeletons at polarized domains in myelinated axons. Exp. Biol. Med. (Maywood) 2008, 233:394-400.
25. 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.
26. Testa I., Urban N.T., Jakobs S., Eggeling C., Willig K.I., Hell S.W. Nanoscopy of living brain slices with low light levels. Neuron 2012, 75:992-1000.
27. Urban N.T., Willig K.I., Hell S.W., Nägerl U.V. STED nanoscopy of actin dynamics in synapses deep inside living brain slices. Biophys. J. 2011, 101:1277-1284.
28. Waites C.L., Leal-Ortiz S.A., Andlauer T.F., Sigrist S.J., Garner C.C. Piccolo regulates the dynamic assembly of presynaptic F-actin. J.Neurosci. 2011, 31:14250-14263.
29. Watanabe K., Al-Bassam S., Miyazaki Y., Wandless T.J., Webster P., Arnold D.B. Networks of polarized actin filaments in the axon initial segment provide a mechanism for sorting axonal and dendritic proteins. Cell Rep. 2012, 2:1546-1553.
30. Willig K.I., Steffens H., Gregor C., Herholt A., Rossner M.J., Hell S.W. Nanoscopy of filamentous actin in cortical dendrites of a living mouse. Biophys. J. 2014, 106:L01-L03.
31. Xu K., Babcock H.P., Zhuang X. Dual-objective STORM reveals three-dimensional filament organization in the actin cytoskeleton. Nat. Methods 2012, 9:185-188.
32. Xu K., Zhong G., Zhuang X. Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons. Science 2013, 339:452-456.