4D Single-particle tracking with asynchronous read-out single-photon avalanche diode array detector.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
23 Jul 2024
23 Jul 2024
Historique:
received:
13
09
2023
accepted:
14
07
2024
medline:
24
7
2024
pubmed:
24
7
2024
entrez:
23
7
2024
Statut:
epublish
Résumé
Single-particle tracking techniques enable investigation of the complex functions and interactions of individual particles in biological environments. Many such techniques exist, each demonstrating trade-offs between spatiotemporal resolution, spatial and temporal range, technical complexity, and information content. To mitigate these trade-offs, we enhanced a confocal laser scanning microscope with an asynchronous read-out single-photon avalanche diode array detector. This detector provides an image of the particle's emission, precisely reflecting its position within the excitation volume. This localization is utilized in a real-time feedback system to drive the microscope scanning mechanism and ensure the particle remains centered inside the excitation volume. As each pixel is an independent single-photon detector, single-particle tracking is combined with fluorescence lifetime measurement. Our system achieves 40 nm lateral and 60 nm axial localization precision with 100 photons and sub-millisecond temporal sampling for real-time tracking. Offline tracking can refine this precision to the microsecond scale. We validated the system's spatiotemporal resolution by tracking fluorescent beads with diffusion coefficients up to 10 μm
Identifiants
pubmed: 39043637
doi: 10.1038/s41467-024-50512-9
pii: 10.1038/s41467-024-50512-9
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
6188Subventions
Organisme : EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council)
ID : 818699
Organisme : EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council)
ID : 818699
Organisme : EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council)
ID : 818699
Organisme : EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council)
ID : 818699
Organisme : EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council)
ID : 818699
Organisme : EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council)
ID : 855923
Organisme : Associazione Italiana per la Ricerca sul Cancro (Italian Association for Cancer Research)
ID : 23053
Organisme : Ministero dell'Istruzione, dell'Università e della Ricerca (Ministry of Education, University and Research)
ID : 2017P352Z4
Organisme : EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council)
ID : 818699
Informations de copyright
© 2024. The Author(s).
Références
Shen, H. et al. Single particle tracking: from theory to biophysical applications. Chem. Rev. 117, 7331–7376 (2017).
pubmed: 28520419
doi: 10.1021/acs.chemrev.6b00815
Schaar, H. M. Vd et al. Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells. PLOS Pathog. 4, e1000244 (2008).
pubmed: 19096510
pmcid: 2592694
doi: 10.1371/journal.ppat.1000244
Ruthardt, N., Lamb, D. C. & Bräuchle, C. Single-particle tracking as a quantitative microscopy-based approach to unravel cell entry mechanisms of viruses and pharmaceutical nanoparticles. Mol. Ther. 19, 1199–1211 (2011).
pubmed: 21654634
pmcid: 3129551
doi: 10.1038/mt.2011.102
Johnson, C., Exell, J., Lin, Y., Aguilar, J. & Welsher, K. D. Capturing the start point of the virus-cell interaction with high-speed 3D single-virus tracking. Nat. Methods 19, 1642–1652 (2022).
pubmed: 36357694
pmcid: 10154077
doi: 10.1038/s41592-022-01672-3
Saxton, M. J. & Jacobson, K. SINGLE-PARTICLE TRACKING:Applications to membrane dynamics. Annu. Rev. Biophys. Biomol. Struct. 26, 373–399 (1997).
pubmed: 9241424
doi: 10.1146/annurev.biophys.26.1.373
Triller, A. & Choquet, D. New concepts in synaptic biology derived from single-molecule imaging. Neuron 59, 359–374 (2008).
pubmed: 18701063
doi: 10.1016/j.neuron.2008.06.022
Biermann, B. et al. Imaging of molecular surface dynamics in brain slices using single-particle tracking. Nat. Commun. 5, 3024 (2014).
pubmed: 24429796
doi: 10.1038/ncomms4024
Bayle, V. et al. Single-particle tracking photoactivated localization microscopy of membrane proteins in living plant tissues. Nat. Protoc. 16, 1600–1628 (2021).
pubmed: 33627844
doi: 10.1038/s41596-020-00471-4
Kural, C. et al. Kinesin and dynein move a peroxisome in vivo: A tug-of-war or coordinated movement? Science 308, 1469–1472 (2005).
pubmed: 15817813
doi: 10.1126/science.1108408
Deguchi, T. et al. Direct observation of motor protein stepping in living cells using MINFLUX. Science 379, 1010–1015 (2023).
pubmed: 36893247
pmcid: 7614483
doi: 10.1126/science.ade2676
Burov, S., Jeon, J.-H., Metzler, R. & Barkai, E. Single particle tracking in systems showing anomalous diffusion: the role of weak ergodicity breaking. Phys. Chem. Chem. Phys. 13, 1800–1812 (2011).
pubmed: 21203639
doi: 10.1039/c0cp01879a
Höfling, F. & Franosch, T. Anomalous transport in the crowded world of biological cells. Rep. Prog. Phys. 76, 046602 (2013).
pubmed: 23481518
doi: 10.1088/0034-4885/76/4/046602
Toprak, E., Balci, H., Blehm, B. H. & Selvin, P. R. Three-Dimensional Particle Tracking via Bifocal Imaging. Nano Lett. 7, 2043–2045 (2007).
pubmed: 17583964
doi: 10.1021/nl0709120
Manley, S. et al. High-density mapping of single-molecule trajectories with photoactivated localization microscopy. Nat. Methods 5, 155–157 (2008).
pubmed: 18193054
doi: 10.1038/nmeth.1176
Appelhans, T. et al. Nanoscale organization of mitochondrial microcompartments revealed by combining tracking and localization microscopy. Nano Lett. 12, 610–616 (2012).
pubmed: 22201267
doi: 10.1021/nl203343a
Sauer, M. & Heilemann, M. Single-molecule localization microscopy in eukaryotes. Chem. Rev. 117, 7478–7509 (2017).
pubmed: 28287710
doi: 10.1021/acs.chemrev.6b00667
Lelek, M. et al. Single-molecule localization microscopy. Nat. Rev. Methods Primers 1, 1–27 (2021).
doi: 10.1038/s43586-021-00038-x
Cang, H., Xu, C. S., Montiel, D. & Yang, H. Guiding a confocal microscope by single fluorescent nanoparticles. Opt. Lett. 32, 2729–2731 (2007).
pubmed: 17873950
doi: 10.1364/OL.32.002729
Lessard, G. A., Goodwin, P. M. & Werner, J. H. Three-dimensional tracking of individual quantum dots. Appl. Phys. Lett. 91, 224106 (2007).
doi: 10.1063/1.2819074
Dunlap, M. K. et al. Super-resolution photoluminescence lifetime and intensity mapping of interacting CdSe/CdS quantum dots. Appl. Phys. Lett. 116, 021103 (2020).
doi: 10.1063/1.5132563
Enderlein, J. Tracking of fluorescent molecules diffusing within membranes. Appl. Phys. B 71, 773–777 (2000).
doi: 10.1007/s003400000409
Kis-Petikova, K. & Gratton, E. Distance measurement by circular scanning of the excitation beam in the two-photon microscope. Microsc. Res. Tech. 63, 34–49 (2004).
pubmed: 14677132
doi: 10.1002/jemt.10417
Annibale, P., Dvornikov, A. & Gratton, E. Electrically tunable lens speeds up 3D orbital tracking. Biomed. Opt. Express 6, 2181–2190 (2015).
pubmed: 26114037
pmcid: 4473752
doi: 10.1364/BOE.6.002181
Perillo, E. P. et al. Deep and high-resolution three-dimensional tracking of single particles using nonlinear and multiplexed illumination. Nat. Commun. 6, 7874 (2015).
pubmed: 26219252
doi: 10.1038/ncomms8874
Hou, S., Lang, X. & Welsher, K. Robust real-time 3D single-particle tracking using a dynamically moving laser spot. Opt. Lett. 42, 2390–2393 (2017).
pubmed: 28614318
doi: 10.1364/OL.42.002390
Hou, S., Exell, J. & Welsher, K. Real-time 3D single molecule tracking. Nat. Commun. 11, 3607 (2020).
pubmed: 32680983
pmcid: 7368020
doi: 10.1038/s41467-020-17444-6
McHale, K., Berglund, A. J. & Mabuchi, H. Quantum dot photon statistics measured by three-dimensional particle tracking. Nano Lett. 7, 3535–3539 (2007).
pubmed: 17949048
doi: 10.1021/nl0723376
Balzarotti, F. et al. Nanometer resolution imaging and tracking of fluorescent molecules with minimal photon fluxes. Science 355, 606–612 (2017).
pubmed: 28008086
doi: 10.1126/science.aak9913
Eilers, Y., Ta, H., Gwosch, K. C., Balzarotti, F. & Hell, S. W. MINFLUX monitors rapid molecular jumps with superior spatiotemporal resolution. Proc. Natl. Acad. Sci. USA 115, 6117–6122 (2018).
pubmed: 29844182
pmcid: 6004438
doi: 10.1073/pnas.1801672115
Masullo, L. A. et al. Pulsed interleaved MINFLUX. Nano Lett. 21, 840–846 (2021).
pubmed: 33336573
doi: 10.1021/acs.nanolett.0c04600
Schmidt, R. et al. MINFLUX nanometer-scale 3D imaging and microsecond-range tracking on a common fluorescence microscope. Nat. Commun. 12, 1478 (2021).
pubmed: 33674570
pmcid: 7935904
doi: 10.1038/s41467-021-21652-z
Masullo, L. A., Lopez, L. F. & Stefani, F. D. A common framework for single-molecule localization using sequential structured illumination. Biophys. Rep. 2, 100036 (2022).
Berezin, M. Y. & Achilefu, S. Fluorescence lifetime measurements and biological imaging. Chem. Rev. 110, 2641–2684 (2010).
pubmed: 20356094
pmcid: 2924670
doi: 10.1021/cr900343z
Datta, R., Heaster, T. M., Sharick, J. T., Gillette, A. A. & Skala, M. C. Fluorescence lifetime imaging microscopy: fundamentals and advances in instrumentation, analysis, and applications. J. Biomed. Opt. 25, 071203 (2020).
pubmed: 32406215
pmcid: 7219965
doi: 10.1117/1.JBO.25.7.071203
van Heerden, B., Vickers, N. A., Krüger, T. P. J. & Andersson, S. B. Real-time feedback-driven single-particle tracking: A aurvey and perspective. Small 18, 2107024 (2022).
doi: 10.1002/smll.202107024
Liao, F., Zhou, F. & Chai, Y. Neuromorphic vision sensors: Principle, progress and perspectives. J. Semicond. 42, 013105 (2021).
doi: 10.1088/1674-4926/42/1/013105
Cabriel, C., Monfort, T., Specht, C. G. & Izeddin, I. Event-based vision sensor enables fast and dense single-molecule localization microscopy. Nat. Photon. 17, 1105–1113 (2023).
Buttafava, M. et al. SPAD-based asynchronous-readout array detectors for image-scanning microscopy. Optica 7, 755–765 (2020).
doi: 10.1364/OPTICA.391726
Slenders, E. et al. Cooled SPAD array detector for low light-dose fluorescence laser scanning microscopy. Biophys. Rep. 1, 100025 (2021).
Castello, M. et al. A robust and versatile platform for image scanning microscopy enabling super-resolution FLIM. Nat. Methods 16, 175–178 (2019).
pubmed: 30643212
doi: 10.1038/s41592-018-0291-9
Tenne, R. et al. Super-resolution enhancement by quantum image scanning microscopy. Nat. Photon. 13, 116–122 (2019).
doi: 10.1038/s41566-018-0324-z
Koho, S. V. et al. Two-photon image-scanning microscopy with SPAD array and blind image reconstruction. Biomed. Opt. Express 11, 2905–2924 (2020).
pubmed: 32637232
pmcid: 7316014
doi: 10.1364/BOE.374398
Sroda, A. et al. SOFISM: Super-resolution optical fluctuation image scanning microscopy. Optica 7, 1308–1316 (2020).
doi: 10.1364/OPTICA.399600
Tortarolo, G. et al. Focus image scanning microscopy for sharp and gentle super-resolved microscopy. Nat. Commun. 13, 7723 (2022).
pubmed: 36513680
pmcid: 9747786
doi: 10.1038/s41467-022-35333-y
Zunino, A., Castello, M. & Vicidomini, G. Reconstructing the image scanning microscopy dataset: an inverse problem. Inverse Probl. 39, 064004 (2023).
Slenders, E. et al. Confocal-based fluorescence fluctuation spectroscopy with a SPAD array detector. Light Sci. Appl. 10, 31 (2021).
pubmed: 33542179
pmcid: 7862647
doi: 10.1038/s41377-021-00475-z
Perego, E. et al. Single-photon microscopy to study biomolecular condensates. Nat. Commun. 14, 8224 (2023).
pubmed: 38086853
pmcid: 10716487
doi: 10.1038/s41467-023-43969-7
Rossetta, A. et al. The BrightEyes-TTM as an open-source time-tagging module for democratising single-photon microscopy. Nat. Commun. 13, 7406 (2022).
pubmed: 36456575
pmcid: 9715684
doi: 10.1038/s41467-022-35064-0
Kao, H. P. & Verkman, A. S. Tracking of single fluorescent particles in three dimensions: use of cylindrical optics to encode particle position. Biophys. J. 67, 1291–1300 (1994).
pubmed: 7811944
pmcid: 1225486
doi: 10.1016/S0006-3495(94)80601-0
Ragan, T., Huang, H., So, P. & Gratton, E. 3D Particle tracking on a two-photon microscope. J. Fluoresc. 16, 325–336 (2006).
pubmed: 16544202
doi: 10.1007/s10895-005-0040-1
Huang, B., Wang, W., Bates, M. & Zhuang, X. Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science 319, 810–813 (2008).
pubmed: 18174397
pmcid: 2633023
doi: 10.1126/science.1153529
Di Rienzo, C., Gratton, E., Beltram, F. & Cardarelli, F. Spatiotemporal fluctuation analysis: A powerful tool for the future nanoscopy of molecular processes. Biophys.J.111, 679–685 (2016).
pubmed: 27558712
pmcid: 5002078
doi: 10.1016/j.bpj.2016.07.015
Tortarolo, G. et al. Compact and effective photon-resolved image scanning microscope. Adv. Photon. 6, 016003 (2024).
doi: 10.1117/1.AP.6.1.016003
Kay, S. M. Fundamentals of Statistical Signal Processing: Estimation theory (Prentice-Hall PTR, 2013).
Abraham, A. V., Ram, S., Chao, J., Ward, E. S. & Ober, R. J. Quantitative study of single molecule location estimation techniques. Opt. Express 17, 23352–23373 (2009).
pubmed: 20052043
doi: 10.1364/OE.17.023352
Chao, J., Ward, E. S. & Ober, R. J. Fisher information theory for parameter estimation in single molecule microscopy: tutorial. JOSA A 33, B36–B57 (2016).
pubmed: 27409706
doi: 10.1364/JOSAA.33.000B36
Verkman, A. S. Solute and macromolecule diffusion in cellular aqueous compartments. Trends Biochem. Sci. 27, 27–33 (2002).
pubmed: 11796221
doi: 10.1016/S0968-0004(01)02003-5
Kumar, M., Mommer, M. S. & Sourjik, V. Mobility of cytoplasmic, membrane, and DNA-binding proteins in escherichia coli. Biophys. J. 98, 552–559 (2010).
pubmed: 20159151
pmcid: 2820653
doi: 10.1016/j.bpj.2009.11.002
Abu-Arish, A., Porcher, A., Czerwonka, A., Dostatni, N. & Fradin, C. High mobility of bicoid captured by fluorescence correlation spectroscopy: implication for the rapid establishment of its gradient. Biophys. J. 99, L33–L35 (2010).
pubmed: 20712981
pmcid: 2920644
doi: 10.1016/j.bpj.2010.05.031
Swaminathan, R., Hoang, C. P. & Verkman, A. S. Photobleaching recovery and anisotropy decay of green fluorescent protein GFP-S65T in solution and cells: cytoplasmic viscosity probed by green fluorescent protein translational and rotational diffusion. Biophys. J. 72, 1900–1907 (1997).
pubmed: 9083693
pmcid: 1184383
doi: 10.1016/S0006-3495(97)78835-0
Colyer, R. A., Lee, C. & Gratton, E. A novel fluorescence lifetime imaging system that optimizes photon efficiency. Microsc. Res. Tech. 71, 201–213 (2008).
pubmed: 18008362
doi: 10.1002/jemt.20540
Lagarto, J., Hares, J. D., Dunsby, C. & French, P. M. W. Development of Low-Cost Instrumentation for Single Point Autofluorescence Lifetime Measurements. J. Fluoresc. 27, 1643–1654 (2017).
pubmed: 28540652
pmcid: 5583312
doi: 10.1007/s10895-017-2101-7
Cooper, G. M.The Cell 2nd edn (Sinauer Associates, 2000).
Platt, F. M., d’Azzo, A., Davidson, B. L., Neufeld, E. F. & Tifft, C. J. Lysosomal storage diseases. Nat. Rev. Dis. Primers 4, 1–25 (2018).
Sun, A. Lysosomal storage disease overview. J. Transl. Med. 6, 476–476 (2018).
Root, J., Merino, P., Nuckols, A., Johnson, M. & Kukar, T. Lysosome dysfunction as a cause of neurodegenerative diseases: Lessons from frontotemporal dementia and amyotrophic lateral sclerosis. Neurobiol. Dis. 154, 105360 (2021).
pubmed: 33812000
pmcid: 8113138
doi: 10.1016/j.nbd.2021.105360
Udayar, V., Chen, Y., Sidransky, E. & Jagasia, R. Lysosomal dysfunction in neurodegeneration: emerging concepts and methods. Trends Neurosci. 45, 184–199 (2022).
pubmed: 35034773
pmcid: 8854344
doi: 10.1016/j.tins.2021.12.004
Fennelly, C. & Amaravadi, R. K. in Lysosomal Biology in Cancer (eds Öllinger, K. & Appelqvist, H.) Lysosomes: Methods and Protocols Methods in Molecular Biology, 293–308 (Springer, New York, NY, 2017). https://doi.org/10.1007/978-1-4939-6934-0_19 .
Tang, T. et al. The role of lysosomes in cancer development and progression. Cell Biosci. 10, 131 (2020).
pubmed: 33292489
pmcid: 7677787
doi: 10.1186/s13578-020-00489-x
Machado, E. R., Annunziata, I., van de Vlekkert, D., Grosveld, G. C. & d’Azzo, A. Lysosomes and Cancer Progression: A Malignant Liaison. Front. cell Dev. Biol. 9, https://doi.org/10.3389/fcell.2021.642494 (2021).
Bonam, S. R., Wang, F. & Muller, S. Lysosomes as a therapeutic target. Nat. Rev. Drug Discov. 18, 923–948 (2019).
pubmed: 31477883
pmcid: 7097195
doi: 10.1038/s41573-019-0036-1
Geisslinger, F., Müller, M., Vollmar, A. M. & Bartel, K. Targeting Lysosomes in Cancer as Promising Strategy to Overcome Chemoresistance—A Mini Review. Front. oncol.10, https://www.frontiersin.org/articles/10.3389/fonc.2020.01156 (2020).
Iulianna, T., Kuldeep, N. & Eric, F. The Achilles’ heel of cancer: targeting tumors via lysosome-induced immunogenic cell death. Cell Death Dis. 13, 1–10 (2022).
doi: 10.1038/s41419-022-04912-8
Jongsma, M. L. M. et al. An ER-associated pathway defines endosomal architecture for controlled cargo transport. Cell 166, 152–166 (2016).
pubmed: 27368102
pmcid: 4930482
doi: 10.1016/j.cell.2016.05.078
Cabukusta, B. & Neefjes, J. Mechanisms of lysosomal positioning and movement. Traffic 19, 761–769 (2018).
pubmed: 29900632
pmcid: 6175085
doi: 10.1111/tra.12587
Wubbolts, R. et al. Opposing motor activities of dynein and kinesin determine retention and transport of MHC class II-containing compartments. J. Cell Sci. 112, 785–795 (1999).
pubmed: 10036229
doi: 10.1242/jcs.112.6.785
Jordens, I. et al. The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors. Curr. Biol. 11, 1680–1685 (2001).
pubmed: 11696325
doi: 10.1016/S0960-9822(01)00531-0
Matteoni, R. & Kreis, T. E. Translocation and clustering of endosomes and lysosomes depends on microtubules. J. Cell Biol. 105, 1253–1265 (1987).
pubmed: 3308906
doi: 10.1083/jcb.105.3.1253
Goo, M. S. et al. Activity-dependent trafficking of lysosomes in dendrites and dendritic spines. J. Cell Biol.216, 2499–2513 (2017).
pubmed: 28630145
pmcid: 5551717
doi: 10.1083/jcb.201704068
Hess, S. T., Sheets, E. D., Wagenknecht-Wiesner, A. & Heikal, A. A. Quantitative analysis of the fluorescence properties of intrinsically fluorescent proteins in living cells. Biophys. J. 85, 2566–2580 (2003).
pubmed: 14507719
pmcid: 1303480
doi: 10.1016/S0006-3495(03)74679-7
Lee, S. & Higuchi, H. 3D rotational motion of an endocytic vesicle on a complex microtubule network in a living cell. Biomed. Opt. Express 10, 6611–6624 (2019).
pubmed: 31853420
pmcid: 6913383
doi: 10.1364/BOE.10.006611
Tregidgo, C. L., Levitt, J. A. & Suhling, K. Effect of refractive index on the fluorescence lifetime of green fluorescent protein. J. Biomed. Opt. 13, 031218 (2008).
pubmed: 18601542
doi: 10.1117/1.2937212
Nakabayashi, T., Wang, H.-P., Kinjo, M. & Ohta, N. Application of fluorescence lifetime imaging of enhanced green fluorescent protein to intracellular pH measurements. Photochem. Photobiol. Sci. 7, 668–670 (2008).
pubmed: 18528549
doi: 10.1039/b800391b
Kepten, E., Weron, A., Sikora, G., Burnecki, K. & Garini, Y. Guidelines for the fitting of anomalous diffusion mean square displacement graphs from single particle tracking experiments. PLOS ONE 10, e0117722 (2015).
pubmed: 25680069
pmcid: 4334513
doi: 10.1371/journal.pone.0117722