Lab-on-chip microscope platform for electro-manipulation of a dense microtubules network
Status PubMed-not-MEDLINE Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
35165315
PubMed Central
PMC8844285
DOI
10.1038/s41598-022-06255-y
PII: 10.1038/s41598-022-06255-y
Knihovny.cz E-zdroje
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Pulsed electric field (PEF) technology is promising for the manipulation of biomolecular components and has potential applications in biomedicine and bionanotechnology. Microtubules, nanoscopic tubular structures self-assembled from protein tubulin, serve as important components in basic cellular processes as well as in engineered biomolecular nanosystems. Recent studies in cell-based models have demonstrated that PEF affects the cytoskeleton, including microtubules. However, the direct effects of PEF on microtubules are not clear. In this work, we developed a lab-on-a-chip platform integrated with a total internal reflection fluorescence microscope system to elucidate the PEF effects on a microtubules network mimicking the cell-like density of microtubules. The designed platform enables the delivery of short (microsecond-scale), high-field-strength ([Formula: see text] 25 kV/cm) electric pulses far from the electrode/electrolyte interface. We showed that microsecond PEF is capable of overcoming the non-covalent microtubule bonding force to the substrate and translocating the microtubules. This microsecond PEF effect combined with macromolecular crowding led to aggregation of microtubules. Our results expand the toolbox of bioelectronics technologies and electromagnetic tools for the manipulation of biomolecular nanoscopic systems and contribute to the understanding of microsecond PEF effects on a microtubule cytoskeleton.
BIOCEV Institute of Biotechnology of the Czech Academy of Sciences Prague Czechia
Institute of Measurement Science of the Slovak Academy of Sciences Bratislava Slovakia
Institute of Photonics and Electronics of the Czech Academy of Sciences Prague Czechia
Institute of Physiology of the Czech Academy of Sciences Prague Czechia
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Nogales, E. & Alushin, G. 4.6 Tubulin and microtubule structure: Mechanistic insights into dynamic instability and its biological relevance. in Comprehensive Biophysics. 72–92. http://linkinghub.elsevier.com/retrieve/pii/B9780123749208004070 (Elsevier, 2012).
Coedert M, Spillantini MC, Rutherford D, Crowther RA. Multiple isoforms of human microtubule-associated protein tau: Sequences and localization in neurofibrillah tangles of Alzheimer’s disease. Neuron. 1989;3:519–26. doi: 10.1016/0896-6273(89)90210-9. PubMed DOI
Matamoros, A. J. & Baas, P. W. Microtubules in health and degenerative disease of the nervous system. Brain Res. Bull.126, 217–225. https://linkinghub.elsevier.com/retrieve/pii/S036192301630140X (2016). PubMed PMC
Marchisella, F., Coffey, E. T. & Hollos, P. Microtubule and microtubule associated protein anomalies in psychiatric disease: MAP anomalies in psychiatric disease. Cytoskeleton73, 596–611. http://doi.wiley.com/10.1002/cm.21300 (2016). PubMed DOI
Churchill, C. D. M., Klobukowski, M. & Tuszynski, J. A. Elucidating the mechanism of action of the clinically approved taxanes: A comprehensive comparison of local and allosteric effects. Chem. Biol. Drug Des.86, 1253–1266. http://doi.wiley.com/10.1111/cbdd.12595 (2015). PubMed DOI
Schaedel, L. et al. Lattice defects induce microtubule self-renewal. Nat. Phys.15, 830–838. https://www.nature.com/articles/s41567-019-0542-4 (2019). PubMed PMC
Gudimchuk, N. B. et al. Mechanisms of microtubule dynamics and force generation examined with computational modeling and electron cryotomography. Nat. Commun.11, 3765. https://www.nature.com/articles/s41467-020-17553-2 (2020). PubMed PMC
Kent, I. A. & Lele, T. P. Microtubule-based force generation. Wiley Interdiscip.Rev. Nanomed. Nanobiotechnol.9, e1428. http://doi.wiley.com/10.1002/wnan.1428 (2017). PubMed DOI PMC
Hirokawa, N., Noda, Y., Tanaka, Y. & Niwa, S. Kinesin superfamily motor proteins and intracellular transport. Nat. Rev. Mol. Cell Biol.10, 682–696. http://www.nature.com/articles/nrm2774 (2009). PubMed
Kalra, A. P. et al. All wired up: An exploration of the electrical properties of microtubules and tubulin. ACS Nano. https://pubs.acs.org/doi/10.1021/acsnano.0c06945 (2020). PubMed DOI
Marracino, P. et al. Tubulin response to intense nanosecond-scale electric field in molecular dynamics simulation. Sci. Rep.9, 10477 (2019). 10.1038/s41598-019-46636-4. PubMed DOI PMC
Serša, G., Bosnjak, M., Čemažar, M. & Heller, R. Preclinical studies on electrochemotherapy. in Handbook of Electroporation (Miklavčič, D. ed.). 1511–1525. http://link.springer.com/10.1007/978-3-319-32886-7_45 (Springer, 2017). DOI
Todorovic, V. & Cemazar, M. Combined treatment of electrochemotherapy with immunomodulators. in Handbook of Electroporation. 1717–1731. (2016).
Kotnik, T. et al. Electroporation-based applications in biotechnology. Trends Biotechnol.33, 480–488. http://linkinghub.elsevier.com/retrieve/pii/S0167779915001249 (2015). PubMed
Vorobiev, E. & Lebovka, N. Application of pulsed electric fields for root and tuber crops biorefinery. in Handbook of Electroporation. 2899–2922. (2017).
Graybill, P. M. & Davalos, R. V. Cytoskeletal disruption after electroporation and its significance to pulsed electric field therapies. Cancers34 (2020). PubMed PMC
Kanthou, C. et al. The endothelial cytoskeleton as a target of electroporation-based therapies. Mol. Cancer Ther.5, 3145–3152. https://mct.aacrjournals.org/content/5/12/3145 (2006). (Publisher: American Association for Cancer Research Section: Research Articles: Therapeutics, Targets, and Development). PubMed
Meulenberg, C. J. W., Todorovic, V. & Cemazar, M. Differential cellular ffects of electroporation and electrochemotherapy in monolayers of human microvascular endothelial cells. PLOS ONE7, e52713. https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0052713 (2012). (Publisher: Public Library of Science). PubMed PMC
Carr, L. et al. Calcium-independent disruption of microtubule dynamics by nanosecond pulsed electric fields in U87 human glioblastoma cells. Sci. Rep.7, 41267. http://www.nature.com/articles/srep41267 (2017). PubMed PMC
Havelka, D. et al. Nanosecond pulsed electric field lab-on-chip integrated in super-resolution microscope for cytoskeleton imaging. Adv. Mater. Technol.5, 1900669. 10.1002/admt.201900669. _eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1002/admt.201900669 (2020). DOI
Chafai, D. E. et al. Microtubule cytoskeleton remodeling by nanosecond pulsed electric fields. Adv. Biosyst.4, 2000070. https://onlinelibrary.wiley.com/doi/abs/10.1002/adbi.202000070 (2020). PubMed DOI
Thompson, G., Beier, H. & Ibey, B. Tracking lysosome migration within Chinese hamster ovary (CHO) cells following exposure to nanosecond pulsed electric fields. Bioengineering5, 103. http://www.mdpi.com/2306-5354/5/4/103 (2018). PubMed PMC
Hristov, K., Mangalanathan, U., Casciola, M., Pakhomova, O. N. & Pakhomov, A. G. Expression of voltage-gated calcium channels augments cell susceptibility to membrane disruption by nanosecond pulsed electric field. Biochim. Biophys. Acta (BBA) Biomembr.1860, 2175–2183. https://linkinghub.elsevier.com/retrieve/pii/S000527361830261X (2018). PubMed
Thompson, G. L., Roth, C. C., Dalzell, D. R., Kuipers, M. & Ibey, B. L. Calcium influx affects intracellular transport and membrane repair following nanosecond pulsed electric field exposure. J. Biomed. Opt.19, 055005–055005. http://biomedicaloptics.spiedigitallibrary.org/article.aspx?articleid=1873019 (2014). PubMed
Dalmay, C. et al. A microfluidic biochip for the nanoporation of living cells. Biosensors Bioelectron.26, 4649–4655. http://linkinghub.elsevier.com/retrieve/pii/S095656631100176X (2011). PubMed
Merla, C. et al. A wide-band bio-chip for real-time optical detection of bioelectromagnetic interactions with cells. Sci. Rep.8, 5044. http://www.nature.com/articles/s41598-018-23301-w (2018). PubMed PMC
Sweeney, D. C., Weaver, J. C. & Davalos, R. V. Characterization of cell membrane permeability in vitro Part I: Transport behavior induced by single-pulse electric fields*. Technol. Cancer Res. Treat.17, 1533033818792491. 10.1177/1533033818792491 (2018). (Publisher: SAGE Publications Inc). PubMed DOI PMC
Yu, C.-H. et al. Measuring microtubule polarity in spindles with second-harmonic generation. Biophys. J.106, 1578–1587. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4008835/ (2014). PubMed PMC
Katrukha, E. A., Jurriens, D., Salas Pastene, D. M. & Kapitein, L. C. Quantitative mapping of dense microtubule arrays in mammalian neurons. eLife10, e67925. 10.7554/eLife.67925 (2021). (Publisher: eLife Sciences Publications, Ltd). PubMed DOI PMC
Sano, M. B. et al. Bursts of bipolar microsecond pulses inhibit tumor growth. Sci. Rep.5, 14999. https://www.nature.com/articles/srep14999 (2015). (Publisher: Nature Publishing Group). PubMed PMC
Ringel-Scaia, V. M. et al. High-frequency irreversible electroporation is an effective tumor ablation strategy that induces immunologic cell death and promotes systemic anti-tumor immunity. EBioMedicine44, 112–125. https://www.sciencedirect.com/science/article/pii/S2352396419303445 (2019). PubMed PMC
Van den Heuvel, M. G. L., De Graaff, M. P., Lemay, S. G. & Dekker, C. Electrophoresis of individual microtubules in microchannels. Proc. Natl. Acad. Sci.104, 7770–7775. http://www.pnas.org/content/104/19/7770.short (2007). PubMed PMC
Kim, K. et al. Electric field-induced reversible trapping of microtubules along metallic glass microwire electrodes. J. Appl. Phys.117, 144701. http://aip.scitation.org/doi/10.1063/1.4917203 (2015). DOI
Allen, S. et al. Detection of antigen-antibody binding events with the atomic force microscope PubMed DOI
Sanchez, T., Welch, D., Nicastro, D. & Dogic, Z. Cilia-like beating of active microtubule bundles. Science333, 456–459. https://science.sciencemag.org/content/333/6041/456 (2011). (Publisher: American Association for the Advancement of Science Section: Report). PubMed PMC
Sanchez, T. & Dogic, Z. Engineering oscillating microtubule bundles. in Methods in Enzymology. Vol. 524. 205–224. https://linkinghub.elsevier.com/retrieve/pii/B9780123979452000123 (Elsevier, 2013). PubMed
Kosaka, P. M. et al. Tackling reproducibility in microcantilever biosensors: A statistical approach for sensitive and specific end-point detection of immunoreactions. Analyst138, 863–872. http://xlink.rsc.org/?DOI=C2AN36192B (2013). PubMed
Siahaan, V. et al. Kinetically distinct phases of tau on microtubules regulate kinesin motors and severing enzymes. Nat. Cell Biol.21, 1086–1092. http://www.nature.com/articles/s41556-019-0374-6 (2019). PubMed
Muscat, S., Stojceski, F. & Danani, A. Elucidating the effect of static electric field on amyloid beta 1–42 supramolecular assembly. J. Mol. Graph. Model.96, 107535. https://linkinghub.elsevier.com/retrieve/pii/S1093326319306357 (2020). PubMed
Průša, J. & Cifra, M. Molecular dynamics simulation of the nanosecond pulsed electric field effect on kinesin nanomotor. Sci. Rep.9, 19721. http://www.nature.com/articles/s41598-019-56052-3 (2019). PubMed PMC
Hekstra, D. R. et al. Electric-field-stimulated protein mechanics. Nature540, 400–405. https://www.nature.com/articles/nature20571 (2016). PubMed PMC
Urabe, G. et al. 1.2 MV/cm pulsed electric fields promote transthyretin aggregate degradation. Sci. Rep.10, 12003. http://www.nature.com/articles/s41598-020-68681-0 (2020). PubMed PMC
Chafai, D. E. et al. Reversible and irreversible modulation of tubulin self-assembly by intense nanosecond pulsed electric fields. Adv. Mater.31, 1903636. 10.1002/adma.201903636 (2019). PubMed
Uppalapati, M., Huang, Y.-M., Aravamuthan, V., Jackson, T. N. & Hancock, W. O. “Artificial mitotic spindle” generated by dielectrophoresis and protein micropatterning supports bidirectional transport of kinesin-coated beads. Integr. Biol.3, 57–64. http://xlink.rsc.org/?DOI=C0IB00065E (2011). PubMed PMC
Uppalapati, M., Huang, Y.-M., Jackson, T. N. & Hancock, W. O. Microtubule alignment and manipulation using AC electrokinetics. Small4, 1371–1381. http://doi.wiley.com/10.1002/smll.200701088 (2008). PubMed DOI
Böhm, K. J., Mavromatos, N. E., Michette, A., Stracke, R. & Unger, E. Movement and alignment of microtubules in electric fields and electric-dipole-moment estimates. Electromagnet. Biol. Med.24, 319–330. http://www.tandfonline.com/doi/full/10.1080/15368370500380010 (2005). DOI
van den Heuvel, M. G. L., Butcher, C. T., Lemay, S. G., Diez, S. & Dekker, C. Electrical docking of microtubules for kinesin-driven motility in nanostructures. Nano Lett.5, 235–241. http://pubs.acs.org/doi/abs/10.1021/nl048291n (2005). PubMed DOI
Isozaki, N. et al. Control of molecular shuttles by designing electrical and mechanical properties of microtubules. Sci. Robot.2, eaan4882. http://robotics.sciencemag.org/lookup/doi/10.1126/scirobotics.aan4882 (2017). PubMed DOI
Stracke R, Böhm K, Wollweber L, Tuszynski J, Unger E. Analysis of the migration behaviour of single microtubules in electric fields. Biochem. Biophys. Res. Commun. 2002;293:602–609. doi: 10.1016/S0006-291X(02)00251-6. PubMed DOI
Kalra, A. P. et al. Revealing and attenuating the electrostatic properties of tubulin and its polymers. Small 2003560. https://onlinelibrary.wiley.com/doi/abs/10.1002/smll.202003560. _eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1002/smll.202003560 (2020). PubMed DOI
Tuszynski, J. A. et al. The evolution of the structure of tubulin and its potential consequences for the role and function of microtubules in cells and embryos. Int. J. Develop. Biol.50, 341–358. http://www.intjdevbiol.com/paper.php?doi=052063jt (2006). PubMed
Janke, C. & Magiera, M. M. The tubulin code and its role in controlling microtubule properties and functions. Nat. Rev. Mol. Cell Biol.21, 307–326. https://www.nature.com/articles/s41580-020-0214-3 (2020). (Publisher: Nature Publishing Group). PubMed
Roll-Mecak, A. Intrinsically disordered tubulin tails: complex tuners of microtubule functions? Semin. Cell Dev. Biol.37, 11–19 . http://linkinghub.elsevier.com/retrieve/pii/S1084952114002936 (2015). PubMed PMC
Ayoub, A. et al. Explaining the microtubule energy balance: Contributions due to dipole moments, charges, van der Waals and solvation energy. Int. J. Mol. Sci.18, 2042. http://www.mdpi.com/1422-0067/18/10/2042 (2017). PubMed PMC
Bujak, Ł. et al. Fast leaps between millisecond confinements govern Ase1 diffusion along microtubules. Small Methods5, 2100370. https://onlinelibrary.wiley.com/doi/abs/10.1002/smtd.202100370. _eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1002/smtd.202100370 (2021). PubMed DOI
Domenge, C. et al. Antitumor electrochemotherapy: New advances in the clinical protocol. Cancer77, 956–963. https://onlinelibrary.wiley.com/doi/pdf/10.1002/%28SICI%291097-0142%2819960301%2977%3A5%3C956%3A%3AAID-CNCR23%3E3.0.CO%3B2-1 (1996). PubMed DOI
Gehl, J. & Serša, G. Electrochemotherapy and its clinical applications. in Handbook of Electroporation (Miklavčič, D. ed.). 1771–1786. http://link.springer.com/10.1007/978-3-319-32886-7_91. (Springer International Publishing, 2017). DOI
Kotnik, T., Bobanović, F. & Miklavcic, D. Sensitivity of transmembrane voltage induced by applied electric fields—A theoretical analysis. Bioelectrochem. Bioenerg.43, 285–291. https://www.sciencedirect.com/science/article/pii/S0302459897000238 (1997).
Gell, C. et al. Purification of tubulin from porcine brain. in Microtubule Dynamics (Straube, A. ed.). Vol. 777. 15–28. http://link.springer.com/10.1007/978-1-61779-252-6_2 (Humana Press, 2011). PubMed DOI
Nitzsche, B. et al. Studying kinesin motors by optical 3D-nanometry in gliding motility assays. in Methods in Cell Biology. Vol. 95. 247–271. http://linkinghub.elsevier.com/retrieve/pii/S0091679X10950140 (Elsevier, 2010). PubMed
Molecular dynamics simulation dataset of a kinesin on tubulin heterodimers in electric field
Electro-detachment of kinesin motor domain from microtubule in silico