دورية أكاديمية

Super-resolved trajectory-derived nanoclustering analysis using spatiotemporal indexing.

التفاصيل البيبلوغرافية
العنوان: Super-resolved trajectory-derived nanoclustering analysis using spatiotemporal indexing.
المؤلفون: Wallis TP; Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, The University of Queensland, Brisbane, QLD, 4072, Australia. t.wallis@uq.edu.au., Jiang A; Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, The University of Queensland, Brisbane, QLD, 4072, Australia., Young K; School of Mathematics and Physics, The University of Queensland, Brisbane, QLD, 4072, Australia., Hou H; Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, The University of Queensland, Brisbane, QLD, 4072, Australia., Kudo K; Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, The University of Queensland, Brisbane, QLD, 4072, Australia., McCann AJ; Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, The University of Queensland, Brisbane, QLD, 4072, Australia., Durisic N; Queensland Brain Institute, The University of Queensland, Brisbane, QLD, 4072, Australia., Joensuu M; Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, The University of Queensland, Brisbane, QLD, 4072, Australia.; Australian Institute for Bioengineering and Nanotechnology, The University of Queensland, Brisbane, QLD, 4072, Australia., Oelz D; School of Mathematics and Physics, The University of Queensland, Brisbane, QLD, 4072, Australia., Nguyen H; School of Mathematics and Physics, The University of Queensland, Brisbane, QLD, 4072, Australia., Gormal RS; Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, The University of Queensland, Brisbane, QLD, 4072, Australia. r.gormal@uq.edu.au., Meunier FA; Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, The University of Queensland, Brisbane, QLD, 4072, Australia. f.meunier@uq.edu.au.; School of Biomedical Sciences, The University of Queensland, Brisbane, QLD, 4072, Australia. f.meunier@uq.edu.au.
المصدر: Nature communications [Nat Commun] 2023 Jun 08; Vol. 14 (1), pp. 3353. Date of Electronic Publication: 2023 Jun 08.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Nature Pub. Group Country of Publication: England NLM ID: 101528555 Publication Model: Electronic Cited Medium: Internet ISSN: 2041-1723 (Electronic) Linking ISSN: 20411723 NLM ISO Abbreviation: Nat Commun Subsets: PubMed not MEDLINE; MEDLINE
أسماء مطبوعة: Original Publication: [London] : Nature Pub. Group
مواضيع طبية MeSH: Proteins*/metabolism , Algorithms*, Cell Membrane/metabolism ; Spatio-Temporal Analysis
مستخلص: Single-molecule localization microscopy techniques are emerging as vital tools to unravel the nanoscale world of living cells by understanding the spatiotemporal organization of protein clusters at the nanometer scale. Current analyses define spatial nanoclusters based on detections but neglect important temporal information such as cluster lifetime and recurrence in "hotspots" on the plasma membrane. Spatial indexing is widely used in video games to detect interactions between moving geometric objects. Here, we use the R-tree spatial indexing algorithm to determine the overlap of the bounding boxes of individual molecular trajectories to establish membership in nanoclusters. Extending the spatial indexing into the time dimension allows the resolution of spatial nanoclusters into multiple spatiotemporal clusters. Using spatiotemporal indexing, we found that syntaxin1a and Munc18-1 molecules transiently cluster in hotspots, offering insights into the dynamics of neuroexocytosis. Nanoscale spatiotemporal indexing clustering (NASTIC) has been implemented as a free and open-source Python graphic user interface.
(© 2023. The Author(s).)
التعليقات: Erratum in: Nat Commun. 2023 Jul 25;14(1):4468. (PMID: 37491417)
References: Choquet, D., Sainlos, M. & Sibarita, J. B. Advanced imaging and labelling methods to decipher brain cell organization and function. Nat. Rev. Neurosci. 22, 237–255 (2021).
Kusumi, A., Tsunoyama, T. A., Hirosawa, K. M., Kasai, R. S. & Fujiwara, T. K. Tracking single molecules at work in living cells. Nat. Chem. Biol. 10, 524–532 (2014). (PMID: 2493707010.1038/nchembio.1558)
Choquet, D. Linking nanoscale dynamics of AMPA receptor organization to plasticity of excitatory synapses and learning. J. Neurosci. 38, 9318–9329 (2018). (PMID: 30381423670599610.1523/JNEUROSCI.2119-18.2018)
Goncalves, J. et al. Nanoscale co-organization and coactivation of AMPAR, NMDAR, and mGluR at excitatory synapses. Proc. Natl Acad. Sci. USA 117, 14503–14511 (2020). (PMID: 32513712732197710.1073/pnas.1922563117)
Bademosi, A. T. et al. In vivo single-molecule tracking at the Drosophila presynaptic motor nerve terminal. J. Vis. Exp. 131, e56952 (2018).
Bademosi, A. T. et al. In vivo single-molecule imaging of syntaxin1A reveals polyphosphoinositide- and activity-dependent trapping in presynaptic nanoclusters. Nat. Commun. 8, 13660 (2017). (PMID: 2804504810.1038/ncomms14492)
Bademosi, A. T. et al. Trapping of syntaxin1a in presynaptic nanoclusters by a clinically relevant general anesthetic. Cell Rep. 22, 427–440 (2018). (PMID: 2932073810.1016/j.celrep.2017.12.054)
Chai, Y. J. et al. Munc18-1 is a molecular chaperone for alpha-synuclein, controlling its self-replicating aggregation. J. Cell Biol. 214, 705–718 (2016). (PMID: 27597756502109210.1083/jcb.201512016)
Gormal, R. S. et al. Modular transient nanoclustering of activated beta2-adrenergic receptors revealed by single-molecule tracking of conformation-specific nanobodies. Proc. Natl Acad. Sci. USA 117, 30476–30487 (2020). (PMID: 33214152772017310.1073/pnas.2007443117)
Harper, C. B. et al. An epilepsy-associated SV2A mutation disrupts synaptotagmin-1 expression and activity-dependent trafficking. J. Neurosci. 40, 4586–4595 (2020). (PMID: 32341095727585310.1523/JNEUROSCI.0210-20.2020)
Kasula, R. et al. The Munc18-1 domain 3a hinge-loop controls syntaxin-1A nanodomain assembly and engagement with the SNARE complex during secretory vesicle priming. J. Cell Biol. 214, 847–858 (2016). (PMID: 27646276503740610.1083/jcb.201508118)
Padmanabhan, P. et al. Need for speed: super-resolving the dynamic nanoclustering of syntaxin-1 at exocytic fusion sites. Neuropharmacology 169, 107554 (2020). (PMID: 3082634310.1016/j.neuropharm.2019.02.036)
Haas, K. T. et al. Pre-post synaptic alignment through neuroligin-1 tunes synaptic transmission efficiency. Elife 7, e31755 (2018).
Ester, M., Kriegel, H. P., Sander, J. & Xu, X. A density-based algorithm for discovering clusters in large spatial databases with noise. In Proc. 2nd International Conference on Knowledge Discovery and Data Mining (KDD’96), 226–231 (1996).
Levet, F. et al. SR-Tesseler: a method to segment and quantify localization-based super-resolution microscopy data. Nat. Methods 12, 1065–1071 (2015). (PMID: 2634404610.1038/nmeth.3579)
Andronov, L., Orlov, I., Lutz, Y., Vonesch, J. L. & Klaholz, B. P. ClusterViSu, a method for clustering of protein complexes by Voronoi tessellation in super-resolution microscopy. Sci. Rep. 6, 24084 (2016). (PMID: 27068792482863810.1038/srep24084)
Khater, I. M., Nabi, I. R. & Hamarneh, G. A review of super-resolution single-molecule localization microscopy cluster analysis and quantification methods. Patterns 1, 100038 (2020). (PMID: 33205106766039910.1016/j.patter.2020.100038)
Griffié, J. et al. Dynamic Bayesian cluster analysis of live-cell single molecule localization microscopy datasets. Small Methods 2, 1800008 (2018).
Finkel, A. Quad trees, a data structure for retrieval on composite keys. Acta Inform. 4, 1–9 (1974). (PMID: 10.1007/BF00288933)
Gutmann, A. R-trees: a dynamic index structure for spatial searching. In Proc. 1984 ACM SIGMOD International Conference on Management of Data (SIGMOD ‘84), 47–57 (1984).
Figueiredo, M. An R-tree collision detection algorithm for polygonal models. In Proc. IASTED International Conference (2009).
Zhai, R. G. & Bellen, H. J. The architecture of the active zone in the presynaptic nerve terminal. Physiology 19, 262–270 (2004). (PMID: 1538175410.1152/physiol.00014.2004)
Sudhof, T. C. The presynaptic active zone. Neuron 75, 11–25 (2012). (PMID: 22794257374308510.1016/j.neuron.2012.06.012)
Tang, A. H. et al. A trans-synaptic nanocolumn aligns neurotransmitter release to receptors. Nature 536, 210–214 (2016). (PMID: 27462810500239410.1038/nature19058)
Nieves, D. J. et al. A framework for evaluating the performance of SMLM cluster analysis algorithms. Nat. Methods 20, 259–267 (2021).
Betzig, E. et al. Imaging intracellular fluorescent proteins at nanometer resolution. Science 313, 1642–1645 (2006). (PMID: 1690209010.1126/science.1127344)
Hess, S. T., Girirajan, T. P. & Mason, M. D. Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys. J. 91, 4258–4272 (2006). (PMID: 16980368163568510.1529/biophysj.106.091116)
Manley, S. et al. High-density mapping of single-molecule trajectories with photoactivated localization microscopy. Nat. Methods 5, 155–157 (2008). (PMID: 1819305410.1038/nmeth.1176)
Sudhof, T. C. & Rothman, J. E. Membrane fusion: grappling with SNARE and SM proteins. Science 323, 474–477 (2009). (PMID: 19164740373682110.1126/science.1161748)
Han, L. et al. Rescue of Munc18-1 and -2 double knockdown reveals the essential functions of interaction between Munc18 and closed syntaxin in PC12 cells. Mol. Biol. Cell 20, 4962–4975 (2009). (PMID: 19812250278573910.1091/mbc.e09-08-0712)
Rickman, C., Meunier, F. A., Binz, T. & Davletov, B. High affinity interaction of syntaxin and SNAP-25 on the plasma membrane is abolished by botulinum toxin E. J. Biol. Chem. 279, 644–651 (2004). (PMID: 1455119910.1074/jbc.M310879200)
Meunier, F. A. & Gutierrez, L. M. Captivating new roles of F-actin cortex in exocytosis and bulk endocytosis in neurosecretory cells. Trends Neurosci. 39, 605–613 (2016). (PMID: 2747499310.1016/j.tins.2016.07.003)
Malintan, N. T. et al. Abrogating Munc18-1-SNARE complex interaction has limited impact on exocytosis in PC12 cells. J. Biol. Chem. 284, 21637–21646 (2009). (PMID: 19483085275588710.1074/jbc.M109.013508)
Martin, S. et al. The Munc18-1 domain 3a loop is essential for neuroexocytosis but not for syntaxin-1A transport to the plasma membrane. J. Cell Sci. 126, 2353–2360 (2013). (PMID: 2376192310.1242/jcs.126813)
Papadopulos, A. et al. Activity-driven relaxation of the cortical actomyosin II network synchronizes Munc18-1-dependent neurosecretory vesicle docking. Nat. Commun. 6, 6297 (2015). (PMID: 2570883110.1038/ncomms7297)
Wallis, T. P. et al. Saturated free fatty acids and association with memory formation. Nat. Commun. 12, 3443 (2021). (PMID: 34103527818764810.1038/s41467-021-23840-3)
Joensuu, M., Wallis, T. P., Saber, S. H. & Meunier, F. A. Phospholipases in neuronal function: a role in learning and memory? J. Neurochem. 153, 300–333 (2020). (PMID: 3174599610.1111/jnc.14918)
Hamilton, J. D. Time Series Analysis (Princeton University Press, 1994).
Lehmann, E. L. & Romano, J. P. Testing Statistical Hypotheses (Springer, 2005).
Ullrich, A. et al. Dynamical organization of syntaxin-1A at the presynaptic active zone. PLoS Comput. Biol. 11, e1004407 (2015). (PMID: 26367029456934210.1371/journal.pcbi.1004407)
Jahn, R. & Fasshauer, D. Molecular machines governing exocytosis of synaptic vesicles. Nature 490, 201–207 (2012). (PMID: 23060190446165710.1038/nature11320)
Angelov, B. & Angelova, A. Nanoscale clustering of the neurotrophin receptor TrkB revealed by super-resolution STED microscopy. Nanoscale 9, 9797–9804 (2017). (PMID: 2868239610.1039/C7NR03454G)
Monnier, N. et al. Inferring transient particle transport dynamics in live cells. Nat. Methods 12, 838–840 (2015). (PMID: 26192083473353310.1038/nmeth.3483)
Persson, F., Linden, M., Unoson, C. & Elf, J. Extracting intracellular diffusive states and transition rates from single-molecule tracking data. Nat. Methods 10, 265–269 (2013). (PMID: 2339628110.1038/nmeth.2367)
Padmanabhan, P., Martinez-Marmol, R., Xia, D., Gotz, J. & Meunier, F. A. Frontotemporal dementia mutant Tau promotes aberrant Fyn nanoclustering in hippocampal dendritic spines. Elife 8, e45040 (2019).
Joensuu, M. et al. Subdiffractional tracking of internalized molecules reveals heterogeneous motion states of synaptic vesicles. J. Cell Biol. 215, 277–292 (2016). (PMID: 27810917508068310.1083/jcb.201604001)
Ripley, B. D. Modeling spatial patterns. J. R. Stat. Soc. B Stat. Methodol. 39, 172–212 (1977).
Giannone, G., Hosy, E., Sibarita, J. B., Choquet, D. & Cognet, L. High-content super-resolution imaging of live cell by uPAINT. Methods Mol. Biol. 950, 95–110 (2013). (PMID: 2308687210.1007/978-1-62703-137-0_7)
Subach, F. V. et al. Photoactivatable mCherry for high-resolution two-color fluorescence microscopy. Nat. Methods 6, 153–159 (2009). (PMID: 19169259290123110.1038/nmeth.1298)
Rickman, C. & Duncan, R. R. Munc18/syntaxin interaction kinetics control secretory vesicle dynamics. J. Biol. Chem. 285, 3965–3972 (2010). (PMID: 1974889110.1074/jbc.M109.040402)
Lang, T. & Jahn, R. Core proteins of the secretory machinery. Handb. Exp. Pharmacol. 184, 107–127 (2008).
Cisse, I. I. et al. Real-time dynamics of RNA polymerase II clustering in live human cells. Science 341, 664–667 (2013). (PMID: 2382888910.1126/science.1239053)
Salavessa, L. et al. Cytokine receptor cluster size impacts its endocytosis and signaling. Proc. Natl Acad. Sci. USA 118, e2024893118 (2021).
Joensuu, M. L. et al. Synaptotagmin 1 mediates toxicity of botulinum neurotoxin type A. EMBOJ e112095 https://doi.org/10.15252/embj.2022112095 , (2022).
Martinez-Marmol, R. et al. Fyn nanoclustering requires switching to an open conformation and is enhanced by FTLD-Tau biomolecular condensates. Mol. Psychiatry 28, 946–962 (2023).
Small, C. H. et al. SV2A-Syt1 interaction controls surface nanoclustering and access to recycling synaptic vesicles. Prepint at bioRxiv https://doi.org/10.1101/2021.12.08.471864 (2022).
Kubala, M. H., Kovtun, O., Alexandrov, K. & Collins, B. M. Structural and thermodynamic analysis of the GFP:GFP-nanobody complex. Protein Sci. 19, 2389–2401 (2010). (PMID: 20945358300940610.1002/pro.519)
Joensuu, M. et al. Visualizing endocytic recycling and trafficking in live neurons by subdiffractional tracking of internalized molecules. Nat. Protoc. 12, 2590–2622 (2017). (PMID: 2918977510.1038/nprot.2017.116)
Kechkar, A., Nair, D., Heilemann, M., Choquet, D. & Sibarita, J. B. Real-time analysis and visualization for single-molecule based super-resolution microscopy. PLoS ONE 8, e62918 (2013). (PMID: 23646160363990110.1371/journal.pone.0062918)
معلومات مُعتمدة: R21 AG080435 United States AG NIA NIH HHS
المشرفين على المادة: 0 (Proteins)
تواريخ الأحداث: Date Created: 20230608 Date Completed: 20230612 Latest Revision: 20231213
رمز التحديث: 20231215
مُعرف محوري في PubMed: PMC10250379
DOI: 10.1038/s41467-023-38866-y
PMID: 37291117
قاعدة البيانات: MEDLINE
الوصف
تدمد:2041-1723
DOI:10.1038/s41467-023-38866-y