Measuring expression heterogeneity of single-cell cytoskeletal protein complexes
Open accessPreprint — published as 10.1038/s41467-021-25212-3 · Paper page
Abstract
Multimeric cytoskeletal protein complexes orchestrate normal cellular function. However, protein-complex distributions in stressed, heterogeneous cell populations remain unknown. Cell staining and proximity-based methods have limited selectivity and/or sensitivity for endogenous multimeric protein-complex quantification from single cells. We introduce micro-arrayed, differential detergent fractionation to simultaneously detect protein complexes in 100s of individual cells. Fractionation occurs by 60 s size-exclusion electrophoresis with protein complex-stabilizing buffer that minimizes depolymerization. Co-detection of cytoskeletal protein complexes in U2OS cells treated with filamentous actin (F-actin) destabilizing LatA detects a subpopulation (~11%) exhibiting downregulated F-actin, but upregulated microtubule and intermediate filament protein complexes. Thus, some cells upregulate other cytoskeletal complexes to counteract the stress of LatA treatment. We also sought to understand the effect of non-chemical stress on cellular heterogeneity of F-actin. We find heat shock dysregulates F- and G-actin correlation. The assay overcomes selectivity limitations to biochemically quantify single-cell protein complexes perturbed with diverse stimuli.
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Cites
Santos, A. G., da Rocha, G. O., & de Andrade, J. B. (2019) · Scientific Reports · doi:10.1038/s41598-018-37186-2 · Cited by 8,495 · see citing works
In situ click chemistry generation of cyclooxygenase-2 inhibitors
Bhardwaj, A., Kaur, J., Wuest, M., & Wuest, F. (2017) · Nature Communications · doi:10.1038/s41467-016-0009-6 · Cited by 7,448 · see citing works
mclust 5: Clustering, Classification and Density Estimation Using Gaussian Finite Mixture Models
Scrucca, L., Fop, M., Murphy, T. B., & Adrian, E. R. (2016) · The R Journal · doi:10.32614/rj-2016-021 · Cited by 2,914 · see citing works
Direct observation of individual endogenous protein complexes in situ by proximity ligation
Söderberg, O., Gullberg, M., Jarvius, M., Ridderstråle, K., Leuchowius, K.-J., Jarvius, J., Wester, K., Hydbring, P., Bahram, F., Larsson, L.-G., et al. (2006) · Nature Methods · doi:10.1038/nmeth947 · Cited by 2,419 · see citing works
Lifeact: a versatile marker to visualize F-actin
Riedl, J., Crevenna, A. H., Kessenbrock, K., Yu, J. H., Neukirchen, D., Bista, M., Bradke, F., Jenne, D., Holak, T. A., Werb, Z., et al. (2008) · Nature Methods · doi:10.1038/nmeth.1220 · Cited by 2,189 · see citing works
A practical guide to single-molecule FRET
Roy, R., Hohng, S., & Ha, T. (2008) · Nature Methods · doi:10.1038/nmeth.1208 · Cited by 2,157 · see citing works
Actin, a Central Player in Cell Shape and Movement
Pollard, T. D., & Cooper, J. A. (2009) · Science · doi:10.1126/science.1175862 · Cited by 2,094 · see citing works
Effects of cytochalasin and phalloidin on actin.
Cooper, J. A. (1987) · The Journal of cell biology · doi:10.1083/jcb.105.4.1473 · Cited by 2,009 · see citing works
Feiner, N., Motone, F., Meyer, A., & Kuraku, S. (2019) · Scientific Reports · doi:10.1038/s41598-019-40055-1 · Cited by 1,988 · see citing works
Taniguchi, Y., Choi, P. J., Li, G.-W., Chen, H., Babu, M., Hearn, J., Emili, A., & Xie, X. S. (2010) · Science · doi:10.1126/science.1188308 · Cited by 1,982 · see citing works
RNA virus interference via CRISPR/Cas13a system in plants
Aman, R., Ali, Z., Butt, H., Mahas, A., Aljedaani, F., Khan, M. Z., Ding, S., & Mahfouz, M. (2018) · Genome Biology · doi:10.1186/s13059-017-1381-1 · Cited by 1,497 · see citing works
Stochastic protein expression in individual cells at the single molecule level
Cai, L., Friedman, N., & Xie, X. S. (2006) · Nature · doi:10.1038/nature04599 · Cited by 1,145 · see citing works
Martinón‐Torres, M., Li, X. J., Xia, Y., Benzonelli, A., Bevan, A., Ma, S., Huang, J., Wang, L., Lan, D., Liu, J., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-40613-7 · Cited by 1,090 · see citing works
Actin Binding Proteins: Regulation of Cytoskeletal Microfilaments
dos Remedios, C. G., Chhabra, D., Kekic, M., Dedova, I. V., Tsubakihara, M., Berry, D. A., & Nosworthy, N. J. (2003) · Physiological Reviews · doi:10.1152/physrev.00026.2002 · Cited by 1,058 · see citing works
Budnik, B., Levy, E., Harmange, G., & Slavov, N. (2018) · Genome Biology · doi:10.1186/s13059-018-1547-5 · Cited by 832 · see citing works
Inhibition of actin polymerization by latrunculin A
Coué, M., Brenner, S. L., Spector, I., & Korn, E. D. (1987) · FEBS Letters · doi:10.1016/0014-5793(87)81513-2 · Cited by 824 · see citing works
Bubb, M. R., Senderowicz, A. M., Sausville, E. A., Duncan, K. L., & Korn, E. D. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)36545-6 · Cited by 811 · see citing works
Cofilin Changes the Twist of F-Actin: Implications for Actin Filament Dynamics and Cellular Function
McGough, A. M., Pope, B. J., Chiu, W., & Weeds, A. G. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.138.4.771 · Cited by 762 · see citing works
Signaling Receptors for TGF-β Family Members
Heldin, C.-H., & Moustakas, A. (2016) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a022053 · Cited by 711 · see citing works
Protein–Protein Interactions Essentials: Key Concepts to Building and Analyzing Interactome Networks
Rivas, J. D. L., & Fontanillo, C. (2010) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000807 · Cited by 650 · see citing works
DeepCRISPR: Optimized CRISPR guide RNA design by deep learning
Chuai, G., Ma, H., Yan, J., Chen, M., Hong, N., Xue, D., Zhou, C., Zhu, C., Chen, K., Duan, B., et al. (2018) · Genome biology · doi:10.1186/s13059-018-1459-4 · Cited by 641 · see citing works
A proposal for validation of antibodies
Uhlen, M., Bandrowski, A., Carr, S., Edwards, A., Ellenberg, J., Lundberg, E., Rimm, D. L., Rodriguez, H., Hiltke, T., Snyder, M., et al. (2016) · Nature Methods · doi:10.1038/nmeth.3995 · Cited by 626 · see citing works
Integrin-mediated Signals Regulated by Members of the Rho Family of GTPases
Clark, E. A., King, W. G., Brugge, J. S., Symons, M. H., & Hynes, R. O. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.142.2.573 · Cited by 603 · see citing works
Zhu, Y., Piehowski, P. D., Zhao, R., Chen, J., Shen, Y., Moore, R. J., Shukla, A. K., Petyuk, V. A., Campbell-Thompson, M., Mathews, C. E., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-03367-w · Cited by 587 · see citing works
Movers and shakers: cell cytoskeleton in cancer metastasis
Fife, C. M., McCarroll, J. A., & Kavallaris, M. (2014) · British Journal of Pharmacology · doi:10.1111/bph.12704 · Cited by 550 · see citing works
Effects of Jasplakinolide on the Kinetics of Actin Polymerization
Bubb, M., Spector, I., Beyer, B. B., & Fosen, K. M. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.7.5163 · Cited by 528 · see citing works
Versatile protein tagging in cells with split fluorescent protein
Kamiyama, D., Sekine, S., Barsi‐Rhyne, B., Hu, J., Chen, B., Gilbert, L. A., Ishikawa, H., Leonetti, M. D., Marshall, W. F., Weissman, J. S., et al. (2016) · Nature Communications · doi:10.1038/ncomms11046 · Cited by 450 · see citing works
Hughes, A. J., Spelke, D. P., Xu, Z., Kang, C., Schaffer, D. V., & Herr, A. E. (2014) · Nature Methods · doi:10.1038/nmeth.2992 · Cited by 415 · see citing works
Self-citationIntermediate Filaments: Structure and AssemblyPreprint
Herrmann, H. O., & Aebi, U. (2016) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a018242 · Cited by 414 · see citing works
Protein length in eukaryotic and prokaryotic proteomes
Brocchieri, L. (2005) · Nucleic Acids Research · doi:10.1093/nar/gki615 · Cited by 414 · see citing works
Best practices and benchmarks for intact protein analysis for top-down mass spectrometry
Donnelly, D. P., Rawlins, C. M., DeHart, C. J., Fornelli, L., Schachner, L. F., Lin, Z., Lippens, J. L., Aluri, K. C., Sarin, R., Chen, B., et al. (2019) · Nature Methods · doi:10.1038/s41592-019-0457-0 · Cited by 377 · see citing works
Epigenetics and Human DiseasePreprint
Zoghbi, H. Y., & Beaudet, A. L. (2016) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a019497 · Cited by 361 · see citing works
Bray, D. (2000) · Garland Science eBooks · doi:10.1201/9780203833582 · Cited by 356 · see citing works
Li, J. J., Bickel, P. J., & Biggin, M. D. (2014) · PeerJ · doi:10.7717/peerj.270 · Cited by 279 · see citing works
Cytoskeletal crosstalk: when three different personalities team up
Huber, F., Boire, A., López, M. P., & Koenderink, G. H. (2014) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2014.10.005 · Cited by 277 · see citing works
Automated analysis of high‐content microscopy data with deep learning
Kraus, O. Z., Grys, B. T., Ba, J. L., Chong, Y. T., Frey, B. J., Boone, C. M., & Andrews, B. (2017) · Molecular Systems Biology · doi:10.15252/msb.20177551 · Cited by 274 · see citing works
How is actin polymerization nucleated in vivo?
Condeelis, J. (2001) · Trends in Cell Biology · doi:10.1016/s0962-8924(01)02008-6 · Cited by 258 · see citing works
Profiling protein expression in circulating tumour cells using microfluidic western blotting
Sinkala, E., Sollier‐Christen, E., Renier, C. M., Rosàs, E., Che, J., Heirich, K., Duncombe, T. A., Vlassakis, J., Yamauchi, K. A., Huang, H., et al. (2017) · Nature Communications · doi:10.1038/ncomms14622 · Cited by 246 · see citing works
Self-citationActin visualization at a glance
Melak, M., Plessner, M., & Grosse, R. (2017) · Journal of Cell Science · doi:10.1242/jcs.189068 · Cited by 239 · see citing works
Ultrasensitive single-cell proteomics workflow identifies >1000 protein groups per mammalian cell
Cong, Y., Motamedchaboki, K., Misal, S. A., Liang, Y., Guise, A. J., Truong, T., Huguet, R., Plowey, E. D., Zhu, Y., López‐Ferrer, D., et al. (2020) · Chemical Science · doi:10.1039/d0sc03636f · Cited by 229 · see citing works
Confidence interval for a coefficient of quartile variation
Bonett, D. G. (2005) · Computational Statistics & Data Analysis · doi:10.1016/j.csda.2005.05.007 · Cited by 221 · see citing works
Shelden, E. A., & Wadsworth, P. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.120.4.935 · Cited by 195 · see citing works
Drew, K., Lee, C., Huizar, R. L., Tu, F., Borgeson, B., McWhite, C. D., Ma, Y., Wallingford, J. B., & Marcotte, E. M. (2017) · Molecular Systems Biology · doi:10.15252/msb.20167490 · Cited by 191 · see citing works
Unpolymerized actin in fibroblasts and brain
Bray, D., & Thomas, C. (1976) · Journal of Molecular Biology · doi:10.1016/0022-2836(76)90233-3 · Cited by 183 · see citing works
HSF-1–mediated cytoskeletal integrity determines thermotolerance and life span
Baird, N. A., Douglas, P. M., Simic, M., Grant, A. R., Moresco, J. J., Wolff, S., Yates, J. R., Manning, G., & Dillin, A. G. (2014) · Science · doi:10.1126/science.1253168 · Cited by 181 · see citing works
Self-citationSingle cell–resolution western blotting
Kang, C., Yamauchi, K. A., Vlassakis, J., Sinkala, E., Duncombe, T. A., & Herr, A. E. (2016) · Nature Protocols · doi:10.1038/nprot.2016.089 · Cited by 178 · see citing works
Self-citation3D microniches reveal the importance of cell size and shape
Bao, M., Xie, J., Piruska, A., & Huck, W. T. S. (2017) · Nature Communications · doi:10.1038/s41467-017-02163-2 · Cited by 177 · see citing works
Senderowicz, A. M., Kaur, G., Sainz, E., Laing, C., Inman, W. D., Rodrı́guez, J., Crews, P., Malspeis, L., Grever, M. R., Sausville, E. A., et al. (1995) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/87.1.46 · Cited by 150 · see citing works
Characterization of the activities of actin-affecting drugs on tumor cell migration
Hayot, C., Debeir, O., Ham, P. V., Damme, M. V., Robert Kiss, A., & Decaestecker, C. (2005) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2005.06.006 · Cited by 145 · see citing works
Author Correction: The energy cost of polypeptide knot formation and its folding consequences
Bustamante, A., Sotelo-Campos, J., Guerra, D. G., Floor, M., Wilson, C. A. M., Bustamante, C., & Báez, M. (2017) · Nature Communications · doi:10.1038/s41467-017-02384-5 · Cited by 145 · see citing works
Cytoskeletal Proteins in Cancer and Intracellular Stress: A Therapeutic Perspective
Ong, M. S., Deng, S., Halim, C. E., Cai, W., Tan, T. Z., Huang, R. Y., Sethi, G., Hooi, S. C., Kumar, A. P., & Yap, C. T. (2020) · Cancers · doi:10.3390/cancers12010238 · Cited by 139 · see citing works
Spreading of trypsinized cells: Cytoskeletal dynamics and energy requirements
Bereiter‐Hahn, J., Luck, M. R., Miebach, T., Stelzer, E. H. K., & Vöth, M. (1990) · Journal of Cell Science · doi:10.1242/jcs.96.1.171 · Cited by 137 · see citing works
Cano, M. L., Lauffenburger, D. A., & Zigmond, S. H. (1991) · The Journal of Cell Biology · doi:10.1083/jcb.115.3.677 · Cited by 130 · see citing works
Rodbard, D., Kapadia, G. G., & Chrambach, A. (1971) · Analytical Biochemistry · doi:10.1016/0003-2697(71)90087-x · Cited by 129 · see citing works
Dynamic Reorganization of the Cytoskeleton during Apoptosis: The Two Coffins Hypothesis
Povea-Cabello, S., Oropesa-Ávila, M., de la Cruz‐Ojeda, P., Paz, M. V., de la Mata, M., Suarez-Rivero, J. M., Álvarez-Córdoba, M., Villalón-García, I., Cotán, D., Ybot‐González, P., et al. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18112393 · Cited by 123 · see citing works
Actin visualization at a glance
Melak, M., Plessner, M., & Grosse, R. (2017) · Development · doi:10.1242/dev.150052 · Cited by 120 · see citing works
Spracklen, A. J., Fagan, T. N., Lovander, K. E., & Tootle, T. L. (2014) · Developmental Biology · doi:10.1016/j.ydbio.2014.06.022 · Cited by 119 · see citing works
Mass Estimation of Native Proteins by Blue Native Electrophoresis
Wittig, I., Beckhaus, T., Wumaier, Z., Karas, M., & Schägger, H. (2010) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m900526-mcp200 · Cited by 117 · see citing works
Nieuwenhuizen, S., Puijk, R. S., van den Bemd, B. A. T., Aldrighetti, L. A., Arntz, M. J., van den Boezem, P. B., Bruynzeel, A. M. E., Burgmans, M. C., COBELLI, F. D., Coolsen, M. M. E., et al. (2020) · Cancers · doi:10.3390/cancers12071779 · Cited by 117 · see citing works
Cramer, L. P., Briggs, L. J., & Dawe, H. R. (2002) · Cell Motility and the Cytoskeleton · doi:10.1002/cm.10013 · Cited by 101 · see citing works
Structural insights into actin filament recognition by commonly used cellular actin markers
Kumari, A., Kesarwani, S., Javoor, M. G., Vinothkumar, K. R., & Sirajuddin, M. (2020) · The EMBO Journal · doi:10.15252/embj.2019104006 · Cited by 97 · see citing works
Kiuchi, T., Nagai, T., Ohashi, K., & Mizuno, K. (2011) · The Journal of Cell Biology · doi:10.1083/jcb.201101035 · Cited by 95 · see citing works
Actin cytoskeletal network in aging and cancer
Rao, K. M. K., & Cohen, H. J. (1991) · Mutation Research/DNAging · doi:10.1016/0921-8734(91)90007-x · Cited by 94 · see citing works
Microtubule-dependent transport and dynamics of vimentin intermediate filaments
Hookway, C., Ding, L., Davidson, M. W., Rappoport, J. Z., Danuser, G. M., & Gelfand, V. I. (2015) · Molecular Biology of the Cell · doi:10.1091/mbc.e14-09-1398 · Cited by 94 · see citing works
Roles of the actin cytoskeleton in aging and age-associated diseases
Lai, W., & Wong, W. (2020) · Ageing Research Reviews · doi:10.1016/j.arr.2020.101021 · Cited by 90 · see citing works
Knowles, G. C., & McCulloch, C. A. (1992) · Journal of Histochemistry & Cytochemistry · doi:10.1177/40.10.1527379 · Cited by 87 · see citing works
The effects of hyperthermia on the cytoskeleton: a review
Coss, R. A., & Linnemans, W. A. M. (1996) · International Journal of Hyperthermia · doi:10.3109/02656739609022507 · Cited by 85 · see citing works
Treadmilling of actin at physiological salt concentrations
Wegner, A. (1982) · Journal of Molecular Biology · doi:10.1016/0022-2836(82)90411-9 · Cited by 83 · see citing works
Correction: Actin visualization at a glance
Melak, M., Plessner, M., & Grosse, R. (2017) · Journal of Cell Science · doi:10.1242/jcs.204487 · Cited by 81 · see citing works
Leuchowius, K., Weibrecht, I., Landegren, U. D., Gedda, L., & Söderberg, O. (2009) · Cytometry Part A · doi:10.1002/cyto.a.20771 · Cited by 71 · see citing works
Actin-capping protein promotes microtubule stability by antagonizing the actin activity of mDia1
Bartolini, F., Ramalingam, N., & Gundersen, G. G. (2012) · Molecular Biology of the Cell · doi:10.1091/mbc.e12-05-0338 · Cited by 70 · see citing works
In Situ Proximity Ligation Assay for Microscopy and Flow Cytometry
Leuchowius, K., Weibrecht, I., & Söderberg, O. (2011) · Current Protocols in Cytometry · doi:10.1002/0471142956.cy0936s56 · Cited by 69 · see citing works
Hydrogel Pore‐Size Modulation for Enhanced Single‐Cell Western Blotting
Duncombe, T. A., Kang, C., Maity, S., Ward, T. M., Pegram, M. D., Murthy, N., & Herr, A. E. (2015) · Advanced Materials · doi:10.1002/adma.201503939 · Cited by 66 · see citing works
Self-citationAutomated Capillary Electrophoresis System for Fast Single-Cell Analysis
Dickinson, A. J., Armistead, P. M., & Allbritton, N. L. (2013) · Analytical Chemistry · doi:10.1021/ac4005887 · Cited by 64 · see citing works
Zhou, M., Uwugiaren, N., Williams, S. M., Moore, R. J., Zhao, R., Goodlett, D., Dapic, I., Paša-Tolić, L., & Zhu, Y. (2020) · Analytical Chemistry · doi:10.1021/acs.analchem.0c00467 · Cited by 62 · see citing works
The quantitation of G- and F-actin in cultured cells
Heacock, C. S., & Bamburg, J. R. (1983) · Analytical Biochemistry · doi:10.1016/0003-2697(83)90725-x · Cited by 60 · see citing works
Mechanisms responsible for F-actin stabilization after lysis of polymorphonuclear leukocytes.
Cano, M. L., Cassimeris, L., Fechheimer, M., & Zigmond, S. H. (1992) · The Journal of Cell Biology · doi:10.1083/jcb.116.5.1123 · Cited by 59 · see citing works
Spatial regulation of the actin cytoskeleton by HSF-1 during aging
Higuchi‐Sanabria, R., Paul, J. W., Durieux, J., Benitez, C., Frankino, P. A., Tronnes, S. U., Garcia, G., Daniele, J. R., Monshietehadi, S., & Dillin, A. G. (2018) · Molecular Biology of the Cell · doi:10.1091/mbc.e18-06-0362 · Cited by 58 · see citing works
Self-citationSubcellular western blotting of single cells
Yamauchi, K. A., & Herr, A. E. (2017) · Microsystems & Nanoengineering · doi:10.1038/micronano.2016.79 · Cited by 54 · see citing works
Self-citationLee, J. P., Kassianidou, E., MacDonald, J. I., Francis, M. B., & Kumar, S. (2016) · Biomaterials · doi:10.1016/j.biomaterials.2016.06.022 · Cited by 53 · see citing works
FOXM1 contributes to taxane resistance by regulating UHRF1-controlled cancer cell stemness
Yuan, B., Liu, Y., Yu, X., Yin, L., Peng, Y., Gao, Y., Zhu, Q., Cao, T., Yang, Y., Fan, X., et al. (2018) · Cell Death and Disease · doi:10.1038/s41419-018-0631-9 · Cited by 50 · see citing works
Microfluidic approaches for the analysis of protein–protein interactions in solution
Arter, W. E., Levin, A., Krainer, G., & Knowles, T. P. J. (2020) · Biophysical Reviews · doi:10.1007/s12551-020-00679-4 · Cited by 49 · see citing works
Actin stabilizing compounds show specific biological effects due to their binding mode
Wang, S., Crevenna, Á. H., Uǧur, İ., Marion, A., Antes, I., Kazmaier, U., Hoyer, M., Lamb, D. C., Gegenfurtner, F. A., Kliesmete, Z., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-46282-w · Cited by 48 · see citing works
Rectangular capillary electrophoresis: Some theoretical considerations
Cifuentes, A., & Poppe, H. (1994) · Chromatographia · doi:10.1007/bf02278753 · Cited by 47 · see citing works
A quantitative method to analyse F-actin distribution in cells
Zonderland, J., Wieringa, P. A., & Moroni, L. (2019) · MethodsX · doi:10.1016/j.mex.2019.10.018 · Cited by 44 · see citing works
Xiao, X., Geyer, V. F., Bowne‐Anderson, H., Howard, J., & Sbalzarini, I. F. (2016) · Medical Image Analysis · doi:10.1016/j.media.2016.03.007 · Cited by 43 · see citing works
In Situ Single‐Cell Western Blot on Adherent Cell Culture
Zhang, Y., Naguro, I., & Herr, A. E. (2019) · Angewandte Chemie International Edition · doi:10.1002/anie.201906920 · Cited by 41 · see citing works
Self-citationLyubchenko, T. A., Wurth, G. A., & Zweifach, A. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2002.033522 · Cited by 39 · see citing works
Zhang, X., Cui, X., Cheng, L., Guan, X., Li, H., Li, X., & Cheng, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0050899 · Cited by 32 · see citing works
Heidecker, M., Yan-Marriott, Y., & Marriott, G. (1995) · Biochemistry · doi:10.1021/bi00035a007 · Cited by 32 · see citing works
Chang, T., Huang, H., Ong, W.-K., Fu, Y.-J., Lee, O. K., Chien, S., & Ho, J. H. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2014.01.028 · Cited by 28 · see citing works
Self-citationDiamond, M. I., Cai, S., Boudreau, A., Carey, C. J., Lyle, N. J., Pappu, R. V., Swamidass, S. J., Bissell, M. J., Piwnica-Worms, H. M., & Shao, J. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.619874 · Cited by 28 · see citing works
Strong fascin expression promotes metastasis independent of its F-actin bundling activity
Heinz, L. S., Muhs, S., Schiewek, J., Grüb, S., Nalaskowski, M. M., Lin, Y., Wikman, H., Oliveira‐Ferrer, L., Lange, T., Wellbrock, J., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.22249 · Cited by 28 · see citing works
Wendel, H., & Dancker, P. (1986) · Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology · doi:10.1016/0167-4838(86)90088-9 · Cited by 28 · see citing works
A moving-boundary technique for the measurement of diffusion in liquids. triton X-100 in water
Leaist, D. G. (1991) · Journal of Solution Chemistry · doi:10.1007/bf00649527 · Cited by 25 · see citing works
Validation of an Algorithm to Quantify Changes in Actin Cytoskeletal Organization
Vindin, H., Bischof, L., Gunning, P. W., & Stehn, J. R. (2013) · SLAS DISCOVERY · doi:10.1177/1087057113503494 · Cited by 24 · see citing works
Bryce, N. S., Failes, T. W., Stehn, J. R., Baker, K., Stefan Zahler, A., Arzhaeva, Y., Bischof, L., Lyons, C., Dedova, I. V., Arndt, G. M., et al. (2019) · Cell Systems · doi:10.1016/j.cels.2019.09.002 · Cited by 22 · see citing works
Sum, C. S., Nickischer, D. R., Lei, M., Weston, A. D., Zhang, L., & Schweizer, L. (2014) · Current Chemical Genomics · doi:10.2174/2213988501408010016 · Cited by 21 · see citing works
Effect of heat on the microtubule disassembly and its relationship to body temperatures
Turi, Á., Lu, R. C., & Lin, P. (1981) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(81)80216-1 · Cited by 20 · see citing works
Ouimet, C. M., Dawod, M., Grinias, J. P., Assimon, V. A., Lodge, J. M., Mapp, A. K., Gestwicki, J. E., & Kennedy, R. T. (2018) · The Analyst · doi:10.1039/c7an02098h · Cited by 20 · see citing works
Immunoisolation of Protein Complexes from Xenopus
Conlon, F. L., Miteva, Y., Kaltenbrun, E., Wasson, L. K., Greco, T. M., & Cristea, I. M. (2012) · Methods in molecular biology · doi:10.1007/978-1-61779-992-1_21 · Cited by 19 · see citing works
Measuring expression heterogeneity of single-cell cytoskeletal protein complexes
Vlassakis, J., Hansen, L. L., Higuchi-Sanabria, R., Zhou, Y., Tsui, C. K., Dillin, A., Huang, H., & Herr, A. E. (2021) · Nature Communications · doi:10.1038/s41467-021-25212-3 · Cited by 16 · see citing works
Self-citationDynamic light-scattering study on polymerization process of muscle actin
Masai, J., Ishiwata, S., & Fujime, S. (1986) · Biophysical Chemistry · doi:10.1016/0301-4622(86)80017-5 · Cited by 15 · see citing works
Chapman, A. R., Lee, D. F., Cai, W., Ma, W., Li, X., Sun, W., & Xie, X. S. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2019.12.31.892190 · Cited by 12 · see citing works
Gavrilova, L. P., Korpacheva, I. I., Геннадиевна, С. С., & Yashin, V. A. (2013) · Cell and Tissue Biology · doi:10.1134/s1990519x13010045 · Cited by 12 · see citing works
Ali, R., Mir, H. A., Hamid, R., Shah, R. A., Khanday, F. A., & Saleem, S. (2021) · The Protein Journal · doi:10.1007/s10930-021-09963-y · Cited by 12 · see citing works
Borejdo, J., & Burlacu, S. (1991) · Journal of Muscle Research and Cell Motility · doi:10.1007/bf01738594 · Cited by 10 · see citing works
The effects of detergents on the polymerization properties of actin
Pozsonyi, K., Hild, G., Gróf, P., Gutay‐Tóth, Z., Bacsó, Z., & Nyitrai, M. (2010) · Cytometry Part A · doi:10.1002/cyto.a.20855 · Cited by 9 · see citing works
GeneFishing to reconstruct context specific portraits of biological processes
Liu, K., Theusch, E., Zhou, Y. F., Ashuach, T., Dosé, A. C., Bickel, P. J., Medina, M. W., & Huang, H. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1820340116 · Cited by 8 · see citing works
Self-citationIn Situ Single‐Cell Western Blot on Adherent Cell Culture
Zhang, Y., Naguro, I., & Herr, A. E. (2019) · Angewandte Chemie · doi:10.1002/ange.201906920 · Cited by 8 · see citing works
Self-citationSIFTER: Electrophoretic complex fractionation protocolPreprint
Vlassakis, J., Hansen, L. L., & Herr, A. E. (2021) · Research Square · doi:10.21203/rs.3.pex-1582/v1 · Cited by 1 · see citing works
Self-citationherrlabucb/SIFTER: First release of SIFTER
Vlassakis, J., Hansen, L. L., Higuchi‐Sanabria, R., Zhou, Y., Tsui, C. K., Dillin, A. G., Huang, H., & Herr, A. E. (2021) · Zenodo (CERN European Organization for Nuclear Research) · doi:10.5281/zenodo.5091208 · Cited by 1 · see citing works
Self-citation
Flagged first, then by citations
1 of the 113 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Gene function and cell surface protein association analysis based on single-cell multiomics data
Hu, H., Feng, Z., Lin, H., Cheng, J., Lyu, J., Zhang, Y., Zhao, J., Xu, F., Lin, T., Zhao, Q., et al. (2023) · Computers in Biology and Medicine · doi:10.1016/j.compbiomed.2023.106733 · Cited by 127 · see citing works
Analytical device miniaturization for the detection of circulating biomarkers
Natalia, A., Zhang, L., Sundah, N. R., Zhang, Y., & Shao, H. (2023) · Nature Reviews Bioengineering · doi:10.1038/s44222-023-00050-8 · Cited by 77 · see citing works
Microfluidic Impedance‐Deformability Cytometry for Label‐Free Single Neutrophil Mechanophenotyping
Petchakup, C., Yang, H., Gong, L., He, L., Tay, H. M., Dalan, R., Chung, A. J., Li, K. H. H., & Hou, H. W. (2022) · Small · doi:10.1002/smll.202104822 · Cited by 70 · see citing works
Recent advances in microfluidics for single-cell functional proteomics
Gebreyesus, S. T., Muneer, G., Huang, C., Siyal, A. A., Anand, M., Chen, Y., & Tu, H. (2023) · Lab on a Chip · doi:10.1039/d2lc01096h · Cited by 35 · see citing works
Xu, L., Xie, H., Wang, B., Zhu, Z., Jiang, H., Duan, X., Deng, S., Xu, J., Jiang, L., & Ding, X. (2023) · Analytical Chemistry · doi:10.1021/acs.analchem.3c01577 · Cited by 8 · see citing works
Gouthami, K., Nagajyothi, P. C., Shekhawat, D., Santra, A., Maity, S., Surtineni, V. P., Arjunan, S., Reddy, V. D., & Shim, J. (2025) · Molecular Biology Reports · doi:10.1007/s11033-025-10985-3 · Cited by 5 · see citing works
Muhammed, Y., Sabatino, M. D., & Lazenby, R. A. (2025) · The Journal of Physical Chemistry B · doi:10.1021/acs.jpcb.4c08793 · Cited by 5 · see citing works
Wang, N., Hou, Y., Lin, L., Xu, S., Lee, K., Yang, Y., Chen, Y., Li, Y., Wang, X., Wang, Y.-T., et al. (2025) · Advanced Science · doi:10.1002/advs.202416482 · Cited by 4 · see citing works
Recent Advances in Top‐Down Proteomics for Single‐Cell Research
Melby, J. A., Su, P., & Gomes, F. P. (2026) · Mass Spectrometry Reviews · doi:10.1002/mas.70031 · Cited by 3 · see citing works
Identification of Biomarkers and Mechanisms Associated with Apoptosis in Recurrent Pregnancy Loss
Zhao, X., Yang, Y., Xie, Q. M., Qiu, J., & Sun, X. (2024) · Biochemical Genetics · doi:10.1007/s10528-024-10932-0 · Cited by 3 · see citing works
A simple joint detection platform for high-throughput single-cell heterogeneity screening
Qiao, Y., Zhang, Q., He, Y., Cheng, T., & Tu, J. (2023) · Talanta · doi:10.1016/j.talanta.2023.125460 · Cited by 2 · see citing works
Single-Cell Protein Assays in Context: From 2D to 3D and In Situ Analysis
Baker, J. S., Joseph, N. I., Lao, A., & Vlassakis, J. (2025) · Annual Review of Analytical Chemistry · doi:10.1146/annurev-anchem-101724-105925 · Cited by 1 · see citing works
Self-citationMicroscale measurements of protein complexes from single cells
Dutta, T., & Vlassakis, J. (2024) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2024.102860 · Cited by 1 · see citing works
Self-citationNanotechnology for in vitro diagnostics of cancer
Liu, Y., Zhang, L., Sundah, N. R., Natalia, A., Chen, X., Tan, H. M., & Shao, H. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-22253-5.00016-9
Liu, J., Li, X., He, H., & Peng, M. (2026) · Sensors and Actuators B Chemical · doi:10.1016/j.snb.2026.140217
- Authors
- Vlassakis, J., Hansen, L. L., Higuchi-Sanabria, R., Zhou, Y., Tsui, C. K., Dillin, A., Huang, H., & Herr, A. E.
- Affiliations
- University of California, Berkeley (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Herr, Amy E.
- ORCID
- Venue
- Nature Communications
- Publisher
- openRxiv
- Published
- 2020-09-13
- Volume
- 12
- Issue
- 1
- Pages
- 4969-4969
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC8371148
- OpenAlex
- W3194320991
- Cited by
- 16
- References
- 113
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 2 · 2023: 5 · 2022: 1 · 2021: 1
- FWCI
- 1.17
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Nature Communications (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- eScholarship (California Digital Library) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- Funders
- National Science Foundation (1056035, 1106400, CAREER)
- U.S. Department of Defense (W81XWH-16, W81XWH, W81XWH1610002)
- Howard Hughes Medical Institute
- U.S. Department of Health and Human Services (1K99AG065200-01A1, R01CA203018, R01AG055891-01)
- National Institutes of Health (MDA-MB-231, W81XWH, NIH K99)
- National Institute on Aging (K99AG065200, R01AG055891)
- National Cancer Institute (R01CA203018)
- Division of Graduate Education (DGE‐1106400)
- Division of Chemical, Bioengineering, Environmental, and Transport Systems (CBET-1056035)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Physical Sciences › Chemistry › Spectroscopy › Advanced Proteomics Techniques and Applications
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
- Keywords
- single-cell heterogeneity, F-actin, microtubules, latrunculin A, heat shock, U2OS cells
- MeSH terms
- Actins, Animals, Cell Differentiation, Cell Line, Cytoskeletal Proteins, Cytoskeleton, Humans, Microtubules, Models, Biological, Genetic Heterogeneity, Heat-Shock Response, Bridged Bicyclo Compounds, Heterocyclic, Thiazolidines, Single-Cell Analysis
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