Real-time imaging of single synaptic vesicles in live neurons
Received date: 03 Feb 2016
Accepted date: 13 Apr 2016
Published date: 17 May 2016
Copyright
Recent advances in fluorescence microscopy have provided researchers with powerful new tools to visualize cellular processes occurring in real time, giving researchers an unprecedented opportunity to address many biological questions that were previously inaccessible. With respect to neurobiology, these real-time imaging techniques have deepened our understanding of molecular and cellular processes, including the movement and dynamics of single proteins and organelles in living cells. In this review, we summarize recent advances in the field of real-time imaging of single synaptic vesicles in live neurons.
Key words: single synaptic vesicle; real-time imaging; exocytosis; tracking
Chenglong Yu , Min Zhang , Xianan Qin , Xiaofeng Yang , Hyokeun Park . Real-time imaging of single synaptic vesicles in live neurons[J]. Frontiers in Biology, 2016 , 11(2) : 109 -118 . DOI: 10.1007/s11515-016-1397-z
1 |
Alabi A A, Tsien R W (2012). Synaptic vesicle pools and dynamics. Cold Spring HarbPerspectBiol, 4(8): a013680
|
2 |
Alabi A A, Tsien R W (2013). Perspectives on kiss-and-run: role in exocytosis, endocytosis, and neurotransmission. Annu Rev Physiol, 75: 393–422
|
3 |
Andreae L C, Fredj N B, Burrone J (2012). Independent vesicle pools underlie different modes of release during neuronal development. J Neurosci, 32(5): 1867–1874
|
4 |
Aravanis A M, Pyle J L, Tsien R W (2003). Single synaptic vesicles fusing transiently and successively without loss of identity. Nature, 423(6940): 643–647
|
5 |
Atasoy D, Ertunc M, Moulder K L, Blackwell J, Chung C, Su J, Kavalali E T (2008). Spontaneous and evoked glutamate release activates two populations of NMDA receptors with limited overlap. J Neurosci, 28(40): 10151–10166
|
6 |
Axelrod D, Thompson N L, Burghardt T P (1983). Total internal inflection fluorescent microscopy. J Microsc, 129(Pt 1): 19–28
|
7 |
Baba K, Nishida K (2012).Single-molecule tracking in living cells using single quantum dot applications. Theranostics, 2(7): 655–667
|
8 |
Balaji J, Ryan T A (2007). Single-vesicle imaging reveals that synaptic vesicle exocytosis and endocytosis are coupled by a single stochastic mode. Proc Natl Acad Sci U S A, 104(51): 20576–20581
|
9 |
Barroso M M(2011). Quantum Dots in Cell Biology. J Histochem Cytochem, 59: 237–251
|
10 |
Betzig E, Patterson G H, Sougrat R, Lindwasser O W, Olenych S, Bonifacino J S, Davidson M W, Lippincott-Schwartz J, Hess H F (2006). Imaging intracellular fluorescent proteins at nanometer resolution. Science, 313(5793): 1642–1645
|
11 |
Bianchini P, Peres C, Oneto M, Galiani S, Vicidomini G, Diaspro A (2015). STED nanoscopy: a glimpse into the future. Cell Tissue Res, 360(1): 143–150
|
12 |
Blum C, Meixner A J, Subramaniam V (2004). Room temperature spectrally resolved single-molecule spectroscopy reveals new spectral forms and photophysical versatility of aequorea green fluorescent protein variants. Biophys J, 87(6): 4172–4179
|
13 |
Bottrill M, Green M (2011). Some aspects of quantum dot toxicity. Chem Commun (Camb), 47(25): 7039–7050
|
14 |
Buxbaum A R, Yoon Y J, Singer R H, Park H Y (2015). Single-molecule insights into mRNA dynamics in neurons. Trends Cell Biol, 25(8): 468–475
|
15 |
Chang Y P, Pinaud F, Antelman J, Weiss S (2008). Tracking bio-molecules in live cells using quantum dots. J Biophotonics, 1(4): 287–298
|
16 |
Chater T E, Goda Y (2014). The role of AMPA receptors in postsynaptic mechanisms of synaptic plasticity. Front Cell Neurosci, 8: 401
|
17 |
Chéreau R, Tønnesen J, Nägerl U V (2015). STED microscopy for nanoscale imaging in living brain slices. Methods, 88: 57–66
|
18 |
Choquet D, Triller A (2013).The dynamic synapse. Neuron, 80(3): 691–703
|
19 |
Chung C, Barylko B, Leitz J, Liu X, Kavalali E T (2010). Acute dynamin inhibition dissects synaptic vesicle recycling pathways that drive spontaneous and evoked neurotransmission. J Neurosci, 30(4): 1363–1376
|
20 |
Coelho M, Maghelli N, Tolić-Nørrelykke I M (2013). Single-molecule imaging in vivo: the dancing building blocks of the cell. Integr Biol (Camb), 5(5): 748–758
|
21 |
Dahan M, Lévi S, Luccardini C, Rostaing P, Riveau B, Triller A (2003). Diffusion dynamics of glycine receptors revealed by single-quantum dot tracking. Science, 302(5644): 442–445
|
22 |
Darcy K J, Staras K, Collinson L M, Goda Y (2006). Constitutive sharing of recycling synaptic vesicles between presynaptic boutons. Nat Neurosci, 9(3): 315–321
|
23 |
Deniz A A, Mukhopadhyay S, Lemke E A (2008). Single-molecule biophysics: at the interface of biology, physics and chemistry. J R Soc Interface, 5(18): 15–45
|
24 |
DePina A S, Wöllert T, Langford G M (2007). Membrane associated nonmuscle myosin II functions as a motor for actin-based vesicle transport in clam oocyte extracts. Cell Motil Cytoskeleton, 64(10): 739–755
|
25 |
Dreosti E, Lagnado L (2011). Optical reporters of synaptic activity in neural circuits. Exp Physiol, 96(1): 4–12
|
26 |
Duzdevich D, Greene E C (2013). Towards physiological complexity with in vitro single-molecule biophysics. Philos Trans R SocLond B BiolSci, 368(1611): 20120271
|
27 |
Fernandez-Alfonso T, Ryan T A (2008). A heterogeneous “resting” pool of synaptic vesicles that is dynamically interchanged across boutons in mammalian CNS synapses. Brain Cell Biol, 36(1-4): 87–100
|
28 |
Fernández-Suárez M, Ting A Y (2008). Fluorescent probes for super-resolution imaging in living cells. Nat Rev Mol Cell Biol, 9(12): 929–943
|
29 |
Fioravante D, Regehr W G (2011). Short-term forms of presynaptic plasticity. Curr Opin Neurobiol, 21(2): 269–274
|
30 |
Gandhi S P, Stevens C F (2003). Three modes of synaptic vesicular recycling revealed by single-vesicle imaging. Nature, 423(6940): 607–613
|
31 |
Giepmans B N, Adams S R, Ellisman M H, Tsien R Y (2006). The fluorescent toolbox for assessing protein location and function. Science, 312(5771): 217–224
|
32 |
Groc L, Choquet D (2006). AMPA and NMDA glutamate receptor trafficking: multiple roads for reaching and leaving the synapse. Cell Tissue Res, 326(2): 423–438
|
33 |
Gu H, Lazarenko R M, Koktysh D, Iacovitti L, Zhang Q (2015). A Stem Cell-Derived Platform for Studying Single Synaptic Vesicles in Dopaminergic Synapses. Stem Cells Transl Med, 4(8): 887–893
|
34 |
Gust A, Zander A, Gietl A, Holzmeister P, Schulz S, Lalkens B, Tinnefeld P, Grohmann D (2014). A starting point for fluorescence-based single-molecule measurements in biomolecular research. Molecules, 19(10): 15824–15865
|
35 |
Haas B L, Matson J S, DiRita V J, Biteen J S (2014). Imaging live cells at the nanometer-scale with single-molecule microscopy: obstacles and achievements in experiment optimization for microbiology. Molecules, 19(8): 12116–12149
|
36 |
Harke B, Keller J, Ullal C K, Westphal V, Schönle A, Hell S W (2008). Resolution scaling in STED microscopy. Opt Express, 16(6): 4154–4162
|
37 |
Hell S W, Wichmann J (1994). Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Opt Lett, 19(11): 780–782
|
38 |
Herzog E, Nadrigny F, Silm K, Biesemann C, Helling I, Bersot T, Steffens H, Schwartzmann R, Nägerl U V, El Mestikawy S, Rhee J, Kirchhoff F, Brose N (2011). In vivo imaging of intersynaptic vesicle exchange using VGLUT1 Venus knock-in mice. J Neurosci, 31(43): 15544–15559
|
39 |
Howarth M, Liu W, Puthenveetil S, Zheng Y, Marshall L F, Schmidt M M, Wittrup K D, Bawendi M G, Ting A Y (2008). Monovalent, reduced-size quantum dots for imaging receptors on living cells. Nat Methods, 5(5): 397–399
|
40 |
Hua Y, Sinha R, Martineau M, Kahms M, Klingauf J (2010). A common origin of synaptic vesicles undergoing evoked and spontaneous fusion. Nat Neurosci, 13(12): 1451–1453
|
41 |
Ifrim M F, Williams K R, Bassell G J (2015). Single-molecule imaging of PSD-95 mRNA translation in dendrites and its dysregulation in a mouse model of fragile X syndrome. J Neurosci, 35(18): 7116–7130
|
42 |
Jahn R, Fasshauer D (2012). Molecular machines governing exocytosis of synaptic vesicles. Nature, 490(7419): 201–207
|
43 |
Joo C, Balci H, Ishitsuka Y, Buranachai C, Ha T (2008).Advances in single-molecule fluorescence methods for molecular biology. Annu Rev Biochem, 77: 51–76
|
44 |
Kamin D, Lauterbach M A, Westphal V, Keller J, Schönle A, Hell S W, Rizzoli S O (2010). High- and low-mobility stages in the synaptic vesicle cycle. Biophys J, 99(2): 675–684
|
45 |
Kavalali E T (2015). The mechanisms and functions of spontaneous neurotransmitter release. Nat Rev Neurosci, 16(1): 5–16
|
46 |
Kavalali E T, Jorgensen E M (2014). Visualizing presynaptic function. Nat Neurosci, 17(1): 10–16
|
47 |
Kharazia V N, Weinberg R J (1997). Tangential synaptic distribution of NMDA and AMPA receptors in rat neocortex. NeurosciLett, 238(1-2): 41–44
|
48 |
Kural C, Kim H, Syed S, Goshima G, Gelfand V I, Selvin P R (2005). Kinesin and dynein move a peroxisome in vivo: a tug-of-war or coordinated movement? Science, 308(5727): 1469–1472
|
49 |
Kusumi A, Tsunoyama T A, Hirosawa K M, Kasai R S, Fujiwara T K (2014).Tracking single molecules at work in living cells. Nat ChemBiol, 10(7): 524–532
|
50 |
Kwakowsky A, Potapov D, Abrahám I M (2013).Tracking of single receptor molecule mobility in neuronal membranes: a quick theoretical and practical guide. J Neuroendocrinol, 25(11): 1231–1237
|
51 |
Lavis L D, Raines R T (2014). Bright building blocks for chemical biology. ACS ChemBiol, 9(4): 855–866
|
52 |
Lee S, Jung K J, Jung H S, Chang S (2012). Dynamics of multiple trafficking behaviors of individual synaptic vesicles revealed by quantum-dot based presynaptic probe. PLoS One, 7(5): e38045
|
53 |
Leitz J, Kavalali E T (2011). Ca²⁺ influx slows single synaptic vesicle endocytosis. J Neurosci, 31(45): 16318–16326
|
54 |
Leitz J, Kavalali E T (2014). Fast retrieval and autonomous regulation of single spontaneously recycling synaptic vesicles. Elife, 3: e03658
|
55 |
Levi V, Gratton E (2007). Exploring dynamics in living cells by tracking single particles. Cell Biochem Biophys, 48(1): 1–15
|
56 |
Liu G (2003). Presynaptic control of quantal size: kinetic mechanisms and implications for synaptic transmission and plasticity. Curr Opin Neurobiol, 13(3): 324–331
|
57 |
Liu Z, Lavis L D, Betzig E (2015). Imaging live-cell dynamics and structure at the single-molecule level. Mol Cell, 58(4): 644–659
|
58 |
Loy K, Welzel O, Kornhuber J, Groemer T W (2014). Common strength and localization of spontaneous and evoked synaptic vesicle release sites. Mol Brain, 7: 23
|
59 |
Mahler B, Spinicelli P, Buil S, Quelin X, Hermier J P, Dubertret B (2008). Towards non-blinking colloidal quantum dots. Nat Mater, 7(8): 659–664
|
60 |
Makino H, Malinow R (2009). AMPA receptor incorporation into synapses during LTP: the role of lateral movement and exocytosis. Neuron, 64(3): 381–390
|
61 |
Manzo C, Garcia-Parajo M F (2015). A review of progress in single particle tracking: from methods to biophysical insights. Rep Prog Phys, 78(12): 124601
|
62 |
Maschi D, Klyachko V A (2015).A nanoscale resolution view on synaptic vesicle dynamics. Synapse, 69(5): 256–267
|
63 |
Mattoussi H, Palui G, Na H B (2012). Luminescent quantum dots as platforms for probing in vitro and in vivo biological processes. Adv Drug Deliv Rev, 64(2): 138–166
|
64 |
Maysinger D, Ji J, Hutter E, Cooper E (2015). Nanoparticle-based and bioengineered probes and sensors to detect physiological and pathological biomarkers in neural cells. Front Neurosci, 9: 480
|
65 |
Medintz I L, Uyeda H T, Goldman E R, Mattoussi H (2005). Quantum dot bioconjugates for imaging, labelling and sensing. Nat Mater, 4(6): 435–446
|
66 |
Michalet X, Colyer R A, Scalia G, Ingargiola A, Lin R, Millaud J E, Weiss S, Siegmund O H, Tremsin A S, Vallerga J V, Cheng A, Levi M, Aharoni D, Arisaka K, Villa F, Guerrieri F, Panzeri F, Rech I, Gulinatti A, Zappa F, Ghioni M, Cova S (2013). Development of new photon-counting detectors for single-molecule fluorescence microscopy. Philos Trans R SocLond B Biol Sci, 368(1611): 20120035
|
67 |
Michalet X, Pinaud F F, Bentolila L A, Tsay J M, Doose S, Li J J, Sundaresan G, Wu A M, Gambhir S S, Weiss S (2005). Quantum dots for live cells, in vivo imaging, and diagnostics. Science, 307(5709): 538–544
|
68 |
Midorikawa M, Sakaba T (2015). Imaging exocytosis of single synaptic vesicles at a fast CNS presynaptic terminal. Neuron, 88(3): 492–498
|
69 |
Miesenböck G, De Angelis D A, Rothman J E (1998). Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature, 394(6689): 192–195
|
70 |
Mochida S (2011). Activity-dependent regulation of synaptic vesicle exocytosis and presynaptic short-term plasticity. Neurosci Res, 70(1): 16–23
|
71 |
Monico C, Capitanio M, Belcastro G, Vanzi F, Pavone F S (2013). Optical methods to study protein-DNA interactions in vitro and in living cells at the single-molecule level. Int J Mol Sci, 14(2): 3961–3992
|
73 |
Müller T, Schumann C, Kraegeloh A (2012). STED microscopy and its applications: new insights into cellular processes on the nanoscale. Chemphyschem, 13(8): 1986–2000
|
74 |
Murthy V N, De Camilli P (2003). Cell biology of the presynaptic terminal. Annu Rev Neurosci, 26: 701–728
|
75 |
Nan X, Sims P A, Chen P, Xie X S (2005). Observation of individual microtubule motor steps in living cells with endocytosed quantum dots. J Phys Chem B, 109(51): 24220–24224
|
76 |
Neupane B, Ligler F S, Wang G (2014). Review of recent developments in stimulated emission depletion microscopy: applications on cell imaging. J Biomed Opt, 19(8): 080901
|
77 |
Opazo P, Sainlos M, Choquet D (2012). Regulation of AMPA receptor surface diffusion by PSD-95 slots. Curr Opin Neurobiol, 22(3): 453–460
|
78 |
Park H, Hanson G T, Duff S R, Selvin P R (2004). Nanometre localization of single ReAsH molecules. J Microsc, 216(Pt 3): 199–205
|
79 |
Park H, Li Y, Tsien R W (2012). Influence of synaptic vesicle position on release probability and exocytotic fusion mode. Science, 335(6074): 1362–1366
|
82 |
Park H, Toprak E, Selvin P R (2007). Single-molecule fluorescence to study molecular motors. Q Rev Biophys, 40(1): 87–111
|
83 |
Pechstein A, Shupliakov O (2010). Taking a back seat: synaptic vesicle clustering in presynaptic terminals. Front Synaptic Neurosci, 2: 143
|
84 |
Peng A, Rotman Z, Deng P Y, Klyachko V A (2012).Differential motion dynamics of synaptic vesicles undergoing spontaneous and activity-evoked endocytosis. Neuron, 73(6): 1108–1115
|
85 |
Ramirez D M, Kavalali E T (2011).Differential regulation of spontaneous and evoked neurotransmitter release at central synapses. Curr Opin Neurobiol, 21(2): 275–282
|
86 |
Ratnayaka A, Marra V, Branco T, Staras K (2011). Extrasynaptic vesicle recycling in mature hippocampal neurons. Nat Commun, 2: 531
|
87 |
Regehr W G (2012). Short-term presynaptic plasticity . Cold Spring Harb Perspect Biol, 4(7): a005702
|
88 |
Rust M J, Bates M, Zhuang X (2006). Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods, 3(10): 793–795
|
89 |
Sakaba T (2006). Roles of the fast-releasing and the slowly releasing vesicles in synaptic transmission at the calyx of Held. J Neurosci, 26(22): 5863–5871
|
90 |
Sara Y, Bal M, Adachi M, Monteggia L M, Kavalali E T (2011). Use-dependent AMPA receptor block reveals segregation of spontaneous and evoked glutamatergic neurotransmission. J Neurosci, 31(14): 5378–5382
|
91 |
Smith A M, Nie S (2010). Semiconductor nanocrystals: structure, properties, and band gap engineering. Acc Chem Res, 43(2): 190–200
|
92 |
Staras K, Branco T, Burden J J, Pozo K, Darcy K, Marra V, Ratnayaka A, Goda Y (2010). A vesicle superpool spans multiple presynaptic terminals in hippocampal neurons. Neuron, 66(1): 37–44
|
93 |
Steyer J A, Almers W (2001). A real-time view of life within 100 nm of the plasma membrane. Nat Rev Mol Cell Biol, 2(4): 268–275
|
94 |
Südhof T C (2004). The synaptic vesicle cycle. Annu Rev Neurosci, 27: 509–547
|
95 |
Südhof T C(2008). Neurotransmitter release. Handb Exp Pharmacol, (184): 1–21
|
96 |
Takamori S, Holt M, Stenius K, Lemke E A, Grønborg M, Riedel D, Urlaub H, Schenck S, Brügger B, Ringler P, Møller S A, Rammner B, Gräter F, Hub J S, De Groot B L, Mieskes G, Moriyama Y, Klingauf J, Grubmüller H, Heuser J, Wieland F, Jahn R (2006). Molecular anatomy of a trafficking organelle. Cell, 127(4): 831–846
|
97 |
Tardin C, Cognet L, Bats C, Lounis B, Choquet D (2003). Direct imaging of lateral movements of AMPA receptors inside synapses. EMBO J, 22(18): 4656–4665
|
98 |
Tatavarty V, Ifrim M F, Levin M, Korza G, Barbarese E, Yu J, Carson J H (2012). Single-molecule imaging of translational output from individual RNA granules in neurons. MolBiol Cell, 23(5): 918–929
|
99 |
Thompson R E, Larson D R, Webb W W (2002). Precise nanometer localization analysis for individual fluorescent probes. Biophys J, 82(5): 2775–2783
|
100 |
Triller A, Choquet D (2008).New concepts in synaptic biology derived from single-molecule imaging. Neuron, 59(3): 359–374
|
101 |
Warshaw D M, Kennedy G G, Work S S, Krementsova E B, Beck S, Trybus K M (2005). Differential labeling of myosin V heads with quantum dots allows direct visualization of hand-over-hand processivity. Biophys J, 88(5): L30–L32
|
102 |
Westphal V, Rizzoli S O, Lauterbach M A, Kamin D, Jahn R, Hell S W (2008). Video-rate far-field optical nanoscopy dissects synaptic vesicle movement. Science, 320(5873): 246–249
|
103 |
Wilhelm B G, Groemer T W, Rizzoli S O (2010). The same synaptic vesicles drive active and spontaneous release. Nat Neurosci, 13(12): 1454–1456
|
104 |
Willig K I, Rizzoli S O, Westphal V, Jahn R, Hell S W (2006). STED microscopy reveals that synaptotagmin remains clustered after synaptic vesicle exocytosis. Nature, 440(7086): 935–939
|
105 |
Wu Y, Yeh F L, Mao F, Chapman E R (2009). Biophysical characterization of styryl dye-membrane interactions. Biophys J, 97(1): 101–109
|
106 |
Xia T, Li N, Fang X (2013). Single-molecule fluorescence imaging in living cells. Annu Rev PhysChem, 64: 459–480
|
107 |
Xie X S, Trautman J K (1998). Optical studies of single molecules at room temperature. Annu Rev PhysChem, 49: 441–480
|
108 |
Yang Y, Calakos N (2013). Presynaptic long-term plasticity. Front Synaptic Neurosci, 5: 8
|
109 |
Yildiz A, Forkey J N, McKinney S A, Ha T, Goldman Y E, Selvin P R (2003).Myosin V walks hand-over-hand: single fluorophore imaging with 1.5-nm localization. Science, 300(5628): 2061–2065
|
110 |
Yildiz A, Selvin P R (2005). Fluorescence imaging with one nanometer accuracy: application to molecular motors. Acc Chem Res, 38(7): 574–582
|
111 |
Zenisek D, Steyer J A, Almers W (2000). Transport, capture and exocytosis of single synaptic vesicles at active zones. Nature, 406(6798): 849–854
|
112 |
Zhang Q, Cao Y Q, Tsien R W (2007). Quantum dots provide an optical signal specific to full collapse fusion of synaptic vesicles. Proc Natl Acad Sci U S A, 104(45): 17843–17848
|
113 |
Zhang Q, Li Y, Tsien R W (2009). The dynamic control of kiss-and-run and vesicular reuse probed with single nanoparticles. Science, 323(5920): 1448–1453
|
114 |
Zhang R, Rothenberg E, Fruhwirth G, Simonson P D, Ye F, Golding I, Ng T, Lopes W, Selvin P R (2011). Two-photon 3D FIONA of individual quantum dots in an aqueous environment. Nano Lett, 11(10):4074–4078
|
115 |
Zhou X, Wang L (2010). Uses of single-particle tracking in living cells. Drug Discov Ther, 4(2): 62–69
|
116 |
Zhu Y, Xu J, Heinemann S F (2009). Two pathways of synaptic vesicle retrieval revealed by single-vesicle imaging. Neuron, 61(3): 397–411
|
/
〈 | 〉 |