A nanoscale resolution view on synaptic vesicle dynamics

Synapse

Volumn 69, Issue 5, 2015, Pages 256-267

  Maschi, Dario ^a,b   Klyachko, Vitaly A ^a,b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

Author keywords

Single particle tracking; Vesicle recycling

Indexed keywords

MOLECULAR MOTOR;

ARTICLE; CELLULAR DISTRIBUTION; CYTOSKELETON; DIFFRACTION; IMAGING; MEMBRANE VESICLE; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; SYNAPSE VESICLE; ANIMAL; EXOCYTOSIS; HUMAN; LIMIT OF DETECTION; MICROSCOPY; PHYSIOLOGY; PROCEDURES; ULTRASTRUCTURE;

ANIMALS; EXOCYTOSIS; HUMANS; LIMIT OF DETECTION; MICROSCOPY; SYNAPTIC VESICLES;

EID: 84925351605     PISSN: 08874476     EISSN: 10982396     Source Type: Journal    
DOI: 10.1002/syn.21795     Document Type: Article

References (98)

1. Alcor D, Gouzer G, Triller A. 2009. Single-particle tracking methods for the study of membrane receptors dynamics. Eur J Neurosci 30:987-997.
2. Allingham JS, Smith R, Rayment I. 2005. The structural basis of blebbistatin inhibition and specificity for myosin II. Nat Struct Mol Biol 12:378-379.
3. Aravanis AM, Pyle JL, Tsien RW. 2003. Single synaptic vesicles fusing transiently and successively without loss of identity Nature 423:643-647.
4. Bal M, Leitz J, Reese AL, Ramirez DM, Durakoglugil M, Herz J, Monteggia LM, Kavalali ET. 2013 Reelin mobilizes a VAMP7-dependent synaptic vesicle pool and selectively augments spontaneous neurotransmission. Neuron 80:934-946.
5. Bates M, Huang B, Zhuang X. 2008. Super-resolution microscopy by nanoscale localization of photo-switchable fluorescent probes. Curr Opin Chem Biol 12:505-514.
6. Benfenati F. 2011. Synapsins-molecular function, development and disease. Semin Cell Dev Biol 22:377.
7. Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S, Bonifacino JS, Davidson MW, Lippincott-Schwartz J, Hess HF. 2006. Imaging intracellular fluorescent proteins at nanometer resolution. Science 313:1642-1645.
8. Bridgman PC. 1999. Myosin Va movements in normal and dilute-lethal axons provide support for a dual filament motor complex. J Cell Biol 146:1045-1060.
9. Bykhovskaia M. 2011. Synapsin regulation of vesicle organization and functional pools. Semin Cell Dev Biol 22:387-392.
10. Chung C, Barylko B, Leitz J, Liu X, Kavalali ET. 2010. Acute dynamin inhibition dissects synaptic vesicle recycling pathways that drive spontaneous and evoked neurotransmission. J. Neurosci 30:1363-1376.
11. Cingolani LA, Goda Y. 2008. Actin in action: The interplay between the actin cytoskeleton and synaptic efficacy. Nat Rev Neurosci 9:344-356.
12. Darcy KJ, Staras K, Collinson LM, Goda Y. 2006. Constitutive sharing of recycling synaptic vesicles between presynaptic boutons. Nat Neurosci 9:315-321.
13. Denker A, Rizzoli SO. 2010. Synaptic vesicle pools: An update. Front Synaptic Neurosci 2:135.
14. Doussau F, Augustine GJ. 2000. The actin cytoskeleton and neurotransmitter release: An overview. Biochimie 82:353-363.
15. Dumoulin A, Triller A, Kneussel M. 2009. Cellular transport and membrane dynamics of the glycine receptor. Front Mol Neurosci 2:28.
16. Fernandez-Alfonso T, Ryan TA. 2006. The efficiency of the synaptic vesicle cycle at central nervous system synapses. Trends Cell Biol 16:413-420.
17. Frank T, Rutherford MA, Strenzke N, Neef A, Pangrsic T, Khimich D, Fejtova A, Gundelfinger ED, Liberman MC, Harke B, Bryan KE, Lee A, Egner A, Riedel D, Moser T. 2010. Bassoon and the synaptic ribbon organize Ca(2)+ channels and vesicles to add release sites and promote refilling. Neuron 68:724-738.
18. Fredj NB, Burrone J. 2009. A resting pool of vesicles is responsible for spontaneous vesicle fusion at the synapse. Nat Neurosci 12:751-759.
19. Gaffield M, Rizzoli SO, Betz WJ. 2006. Mobility of synaptic vesicles in different pools in resting and stimulated frog motor nerve terminals. Neuron 51:317-325.
20. Gaffield MA, Betz WJ. 2007. Synaptic vesicle mobility in mouse motor nerve terminals with and without synapsin. J Neurosci 27:13691-13700.
21. Granseth B, Odermatt B, Royle SJ, Lagnado L. 2006. Clathrin-mediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses. Neuron 51:773-786.
22. Harata N, Pyle JL, Aravanis AM, Mozhayeva M, Kavalali ET, Tsien RW. 2001. Limited numbers of recycling vesicles in small CNS nerve terminals: Implications for neural signaling and vesicular cycling. Trends Neurosci 24:637-643.
23. Hell SW. 2003. Toward fluorescence nanoscopy. Nat Biotechnol 21:1347-1355.
24. Hell SW. 2007. Far-field optical nanoscopy. Science 316:1153-1158.
25. Hell SW, Dyba M, Jakobs S. 2004. Concepts for nanoscale resolution in fluorescence microscopy. Curr Opin Neurobiol 14:599-609.
26. Henkel AW, Simpson LL, Ridge RM, Betz WJ. 1996. Synaptic vesicle movements monitored by fluorescence recovery after photobleaching in nerve terminals stained with FM1-43. J Neurosci 16:3960-3967.
27. Holt M, Cooke A, Neef A, Lagnado L. 2004. High mobility of vesicles supports continuous exocytosis at a ribbon synapse. Curr Biol 14:173-183.
28. Hoopmann P, Rizzoli SO, Betz WJ. 2012. Imaging synaptic vesicle recycling by staining and destaining vesicles with FM dyes. Cold Spring Harb Protoc 2012:77-83.
29. Hua Y, Sinha R, Thiel CS, Schmidt R, Huve J, Martens H, Hell SW, Egner A, Klingauf J. 2011a. A readily retrievable pool of synaptic vesicles. Nat Neurosci 14:833-839.
30. Hua Z, Leal-Ortiz S, Foss SM, Waites CL, Garner CC, Voglmaier SM, Edwards RH. 2011b. v-SNARE composition distinguishes synaptic vesicle pools. Neuron 71:474-487.
31. Huang B, Bates M, Zhuang X. 2009. Super-resolution fluorescence microscopy. Annu Rev Biochem 78:993-1016.
32. Jaqaman K, Loerke D, Mettlen M, Kuwata H, Grinstein S, Schmid SL, Danuser G. 2008. Robust single-particle tracking in live-cell time-lapse sequences. Nat Methods 5:695-702.
33. Kamin D, Lauterbach MA, Westphal V, Keller J, Schonle A, Hell SW, Rizzoli SO. 2010. High- and low-mobility stages in the synaptic vesicle cycle. Biophys J 99:675-684.
34. Kavalali ET, Jorgensen EM. 2013. Visualizing presynaptic function. Nat Neurosci 17:10-16.
35. Kim JH, von Gersdorff H. 2012. Suppression of spikes during posttetanic hyperpolarization in auditory neurons: The role of temperature, I(h) currents, and the Na(+)-K(+)-ATPase pump. J Neurophysiol 108:1924-1932.
36. Kisiel M, McKenzie K, Stewart B. 2014. Localization and mobility of synaptic vesicles in Myosin VI mutants of Drosophila. PLoS One 9:e102988.
37. Klyachko VA, Stevens CF. 2006. Temperature-dependent shift of balance among the components of short-term plasticity in hippocampal synapses. J Neurosci 26:6945-6957.
38. Kneussel M, Triller A, Choquet D. 2014. SnapShot: Receptor dynamics at plastic synapses. Cell 157:1738-1738, e1731.
39. Kononenko NL, Puchkov D, Classen GA, Walter AM, Pechstein A, Sawade L, Kaempf N, Trimbuch T, Lorenz D, Rosenmund C, Maritzen T, Haucke V. 2014. Clathrin/AP-2 mediate synaptic vesicle reformation from endosome-like vacuoles but are not essential for membrane retrieval at central synapses. Neuron 82:981-988.
40. Kovacs M, Toth J, Hetenyi C, Malnasi-Csizmadia A, Sellers JR. 2004. Mechanism of blebbistatin inhibition of myosin II. J Biol Chem 279:35557-35563.
41. Kraszewski K, Daniell L, Mundigl O, de Camilli P. 1996. Mobility of synaptic vesicles in nerve endings monitored by recovery from photobleaching of synaptic vesicle-associated fluorescence. J Neurosci 16:5905-5913.
42. Kushmerick C, Renden R, von Gersdorff H. 2006. Physiological temperatures reduce the rate of vesicle pool depletion and short-term depression via an acceleration of vesicle recruitment. J Neurosci 26:1366-1377.
43. Lauterbach MA, Keller J, Schonle A, Kamin D, Westphal V, Rizzoli SO, Hell SW. 2010. Comparing video-rate STED nanoscopy and confocal microscopy of living neurons. J Biophotonics 3:417-424.
44. Lee S, Jung KJ, Jung HS, Chang S. 2012. Dynamics of multiple trafficking behaviors of individual synaptic vesicles revealed by quantum-dot based presynaptic probe. PLoS One 7:e38045.
45. Lemke EA, Klingauf J. 2005. Single synaptic vesicle tracking in individual hippocampal boutons at rest and during synaptic activity. J Neurosci 25:11034-11044.
46. Levitan ES. 2008. Signaling for vesicle mobilization and synaptic plasticity. Mol Neurobiol 37:39-43.
47. Li Z, Burrone J, Tyler WJ, Hartman KN, Albeanu DF, Murthy VN. 2005. Synaptic vesicle recycling studied in transgenic mice expressing synaptopHluorin. Proc Natl Acad Sci USA 102:6131-6136.
48. Liu TT, Kishimoto T, Hatakeyama H, Nemoto T, Takahashi N, Kasai H. 2005. Exocytosis and endocytosis of small vesicles in PC12 cells studied with TEPIQ (two-photon extracellular polar-tracer imaging-based quantification) analysis. J Physiol 568:917-929.
49. Maglione M, Sigrist SJ. 2013. Seeing the forest tree by tree: Super-resolution light microscopy meets the neurosciences. Nat Neurosci 16:790-797.
50. Mercer AJ, Chen M, Thoreson WB. 2011. Lateral mobility of presynaptic L-type calcium channels at photoreceptor ribbon synapses. J Neurosci 31:4397-4406.
51. Mercer AJ, Szalewski RJ, Jackman SL, Van Hook MJ, Thoreson WB. 2012. Regulation of presynaptic strength by controlling Ca2+ channel mobility: Effects of cholesterol depletion on release at the cone ribbon synapse. J Neurophysiol 107:3468-3478.
52. Micheva KD, Smith SJ. 2005. Strong effects of subphysiological temperature on the function and plasticity of mammalian presynaptic terminals. J Neurosci 25:7481-7488.
53. Murthy VN, Stevens CF. 1998. Synaptic vesicles retain their identity through the endocytic cycle. Nature 392:497-501.
54. Nelson AJ, Hess ST. 2014. Localization microscopy: Mapping cellular dynamics with single molecules. J Microsc 254:1-8.
55. Opazo F, Punge A, Buckers J, Hoopmann P, Kastrup L, Hell SW, Rizzoli SO. 2010. Limited intermixing of synaptic vesicle components upon vesicle recycling. Traffic 11:800-812.
56. Osseforth C, Moffitt JR, Schermelleh L, Michaelis J. 2014. Simultaneous dual-color 3D STED microscopy. Opt Express 22:7028-7039.
57. Park H, Li Y, Tsien RW. 2012. Influence of synaptic vesicle position on release probability and exocytotic fusion mode. Science 335:1362-1366.
58. Park H, Toprak E, Selvin PR. 2007. Single-molecule fluorescence to study molecular motors. Q Rev Biophys 40:87-111.
59. Peng A, Rotman Z, Deng PY, Klyachko VA. 2012. Differential motion dynamics of synaptic vesicles undergoing spontaneous and activity-evoked endocytosis. Neuron 73:1108-1115.
60. Prekeris R, Terrian DM. 1997. Brain myosin V is a synaptic vesicle-associated motor protein: evidence for a Ca2+-dependent interaction with the synaptobrevin-synaptophysin complex. J Cell Biol 137:1589-1601.
61. Pyott SJ, Rosenmund C. 2002. The effects of temperature on vesicular supply and release in autaptic cultures of rat and mouse hippocampal neurons. J Physiol 539:523-535.
62. Raingo J, Khvotchev M, Liu P, Darios F, Li YC, Ramirez DM, Adachi M, Lemieux P, Toth K, Davletov B, Kavalali ET. 2012. VAMP4 directs synaptic vesicles to a pool that selectively maintains asynchronous neurotransmission. Nat Neurosci 15:738-745.
63. Roelandse M, Matus A. 2004. Hypothermia-associated loss of dendritic spines. J Neurosci 24:7843-7847.
64. Rose SD, Lejen T, Casaletti L, Larson RE, Pene TD, Trifaro JM. 2003. Myosins II and V in chromaffin cells: myosin V is a chromaffin vesicle molecular motor involved in secretion. J Neurochem 85:287-298.
65. Rust MJ, Bates M, Zhuang X. 2006. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 3:793-795.
66. Ryan TA, Reuter H, Smith SJ. 1997. Optical detection of a quantal presynaptic membrane turnover. Nature 388:478-482.
67. Samson F, Donoso JA, Heller-Bettinger I, Watson D, Himes RH. 1979. Nocodazole action on tubulin assembly, axonal ultrastructure and fast axoplasmic transport. J Pharmacol Exp Ther 208:411-417.
68. Sankaranarayanan S, Atluri PP, Ryan TA. 2003. Actin has a molecular scaffolding, not propulsive, role in presynaptic function. Nat Neurosci 6:127-135.
69. Sankaranarayanan S, Ryan TA. 2000. Real-time measurements of vesicle-SNARE recycling in synapses of the central nervous system. Nat Cell Biol 2:197-204.
70. Sara Y, Virmani T, Deák F, Liu X, Kavalali ET. 2005. An isolated pool of vesicles recycles at rest and drives spontaneous neurotransmission. Neuron 45:563-573.
71. Schikorski T, Stevens CF. 2001. Morphological correlates of functionally defined synaptic vesicle populations. Nat Neurosci 4:391-395.
72. Schikorski T. 2014 Readily releasable vesicles recycle at the active zone of hippocampal synapses. Proc Natl Acad Sci USA 111:5415-5420.
73. Schnell E, Nicoll RA. 2001. Hippocampal synaptic transmission and plasticity are preserved in myosin Va mutant mice. J Neurophysiol 85:1498-1501.
74. Seabrooke S, Qiu X, Stewart BA. 2010. Nonmuscle Myosin II helps regulate synaptic vesicle mobility at the Drosophila neuromuscular junction. BMC Neurosci 11:37.
75. Shtrahman M, Yeung C, Nauen DW, Bi GQ, Wu XL. 2005. Probing vesicle dynamics in single hippocampal synapses. Biophys J 89:3615-3627.
76. Shupliakov O, Bloom O, Gustafsson JS, Kjaerulff O, Low P, Tomilin N, Pieribone VA, Greengard P, Brodin L. 2002. Impaired recycling of synaptic vesicles after acute perturbation of the presynaptic actin cytoskeleton. Proc Natl Acad Sci USA 99:14476-14481.
77. Sigrist SJ, Sabatini BL. 2011. Optical super-resolution microscopy in neurobiology. Curr Opin Neurobiol 22:86-93.
78. Small A, Stahlheber S. 2014. Fluorophore localization algorithms for super-resolution microscopy. Nat Methods 11:267-279.
79. Smith CS, Joseph N, Rieger B, Lidke KA. 2010. Fast, single-molecule localization that achieves theoretically minimum uncertainty. Nat Methods 7:373-375.
80. Sochacki KA, Larson BT, Sengupta DC, Daniels MP, Shtengel G, Hess HF, Taraska JW. 2012. Imaging the post-fusion release and capture of a vesicle membrane protein. Nat Commun 3:1154.
81. Takagishi Y, Futaki S, Itoh K, Espreafico EM, Murakami N, Murata Y, Mochida S. 2005. Localization of myosin II and V isoforms in cultured rat sympathetic neurones and their potential involvement in presynaptic function. J Physiol 569:195-208.
82. Thompson RE, Larson DR, Webb WW. 2002. Precise naneter localization analysis for individual fluorescent probes. Biophys J 82:2775-2783.
83. Thoreson WB, Mercer AJ, Cork KM, Szalewski RJ. 2013. Lateral mobility of L-type calcium channels in synaptic terminals of retinal bipolar cells. Mol Vis 19:16-24.
84. tom Dieck S, Altrock WD, Kessels MM, Qualmann B, Regus H, Brauner D, Fejtova A, Bracko O, Gundelfinger ED, Brandstatter JH. 2005. Molecular dissection of the photoreceptor ribbon synapse: Physical interaction of Bassoon and RIBEYE is essential for the assembly of the ribbon complex. J Cell Biol 168:825-836.
85. Volgushev M, Kudryashov I, Chistiakova M, Mukovski M, Niesmann J, Eysel UT. 2004. Probability of transmitter release at neocortical synapses at different temperatures. J Neurophysiol 92:212-220.
86. Watanabe S, Rost BR, Camacho-Pérez M, Davis MW, Söhl-Kielczynski B, Rosenmund C, Jorgensen EM. 2013a. Ultrafast endocytosis at mouse hippocampal synapses. Nature. 504:242-247.
87. Watanabe S, Liu Q, Davis MW, Hollopeter G, Thomas N, Jorgensen NB, Jorgensen EM. 2013b. Ultrafast endocytosis at Caenorhabditis elegans neuromuscular junctions. Elife 2:e00723.
88. Watanabe S, Trimbuch T, Camacho-Pérez M, Rost BR, Brokowski B, Söhl-Kielczynski B, Felies A, Davis MW, Rosenmund C, Jorgensen EM. 2014. Clathrin regenerates synaptic vesicles from endosomes. Nature 2014 515:228-33.
89. Westphal V, Rizzoli SO, Lauterbach MA, Kamin D, Jahn R, Hell SW. 2008. Video-rate far-field optical nanoscopy dissects synaptic vesicle movement. Science 320:246-249.
90. Wienisch M, Klingauf J. 2006. Vesicular proteins exocytosed and subsequently retrieved by compensatory endocytosis are nonidentical. Nat Neurosci 9:1019-1027.
91. Wildanger D, Medda R, Kastrup L, Hell SW. 2009. A compact STED microscope providing 3D nanoscale resolution. J Microsc 236:35-43.
92. Willig KI, Harke B, Medda R, Hell SW. 2007. STED microscopy with continuous wave beams. Nat Methods 4:915-918.
93. Willig KI, Rizzoli SO, Westphal V, Jahn R, Hell SW. 2006. STED microscopy reveals that synaptotagmin remains clustered after synaptic vesicle exocytosis. Nature 440:935-939.
94. Wolter S, Schuttpelz M, Tscherepanow M, S VDL, Heilemann M, Sauer M. 2010. Real-time computation of subdiffraction-resolution fluorescence images. J Microsc 237:12-22.
95. Wu Y, Yeh FL, Mao F, Chapman ER. 2009. Biophysical characterization of styryl dye-membrane interactions. Biophys J 97:101-109.
96. Yeung C, Shtrahman M, Wu XL. 2007. Stick-and-diffuse and caged diffusion: A comparison of two models of synaptic vesicle dynamics. Biophys J 92:2271-2280.
97. Zenisek D, Steyer JA, Almers W. 2000. Transport, capture and exocytosis of single synaptic vesicles at active zones. Nature 406:849-854.
98. Zhang Q, Li Y, Tsien RW. 2009. The dynamic control of kiss-and-run and vesicular reuse probed with single nanoparticles. Science 323:1448-1453.