• This record comes from PubMed

Electro-opening of a microtubule lattice in silico

. 2021 ; 19 () : 1488-1496. [epub] 20210304

Status PubMed-not-MEDLINE Language English Country Netherlands Media electronic-ecollection

Document type Journal Article

Links

PubMed 33815687
PubMed Central PMC7985272
DOI 10.1016/j.csbj.2021.02.007
PII: S2001-0370(21)00058-1
Knihovny.cz E-resources

Modulation of the structure and function of biomaterials is essential for advancing bio-nanotechnology and biomedicine. Microtubules (MTs) are self-assembled protein polymers that are essential for fundamental cellular processes and key model compounds for the design of active bio-nanomaterials. In this in silico study, a 0.5 μs-long all-atom molecular dynamics simulation of a complete MT with approximately 1.2 million atoms in the system indicated that a nanosecond-scale intense electric field can induce the longitudinal opening of the cylindrical shell of the MT lattice, modifying the structure of the MT. This effect is field-strength- and temperature-dependent and occurs on the cathode side. A model was formulated to explain the opening on the cathode side, which resulted from an electric-field-induced imbalance between electric torque on tubulin dipoles and cohesive forces between tubulin heterodimers. Our results open new avenues for electromagnetic modulation of biological and artificial materials through action on noncovalent molecular interactions.

See more in PubMed

Ross T.D., Lee H.J., Qu Z., Banks R.A., Phillips R., Thomson M. Controlling organization and forces in active matter through optically defined boundaries. Nature. 2019;572:224–229. doi: 10.1038/s41586-019-1447-1. URL:http://www.nature.com/articles/s41586-019-1447-1. PubMed DOI PMC

Duclos G., Adkins R., Banerjee D., Peterson M.S.E., Varghese M., Kolvin I., Baskaran A., Pelcovits R.A., Powers T.R., Baskaran A., Toschi F., Hagan M.F., Streichan S.J., Vitelli V., Beller D.A., Dogic Z. Topological structure and dynamics of three-dimensional active nematics. Science. 2020;367:1120–1124. doi: 10.1126/science.aaz4547. URL:https://www.sciencemag.org/lookup/doi/10.1126/science.aaz4547. PubMed DOI PMC

Chafai D.E., Sulimenko V., Havelka D., Kubínová L., Dráber P., Cifra M. Reversible and irreversible modulation of tubulin self-assembly by intense nanosecond pulsed electric fields. Adv. Mater. 2019;31 doi: 10.1002/adma.201903636. PubMed DOI

Kellogg E.H., Hejab N.M.A., Poepsel S., Downing K.H., DiMaio F., Nogales E. Near-atomic model of microtubule-tau interactions. Science. 2018;360:1242–1246. doi: 10.1126/science.aat1780. URL:http://www.sciencemag.org/lookup/doi/10.1126/science.aat1780. PubMed DOI PMC

Shaik S., Danovich D., Joy J., Wang Z., Stuyver T. Electric-field mediated chemistry: uncovering and exploiting the potential of (oriented) electric fields to exert chemical catalysis and reaction control. J. Am. Chem. Soc. 2020 doi: 10.1021/jacs.0c05128. jacs.0c05128. PubMed DOI

Aumeier C., Schaedel L., Gaillard J., John K., Blanchoin L., Théry M. Self-repair promotes microtubule rescue. Nat. Cell Biol. 2016;18:1054–1064. doi: 10.1038/ncb3406. URL:http://www.nature.com/doifinder/10.1038/ncb3406. PubMed DOI PMC

Schaedel L., Triclin S., Chrétien D., Abrieu A., Aumeier C., Gaillard J., Blanchoin L., Théry M., John K. Lattice defects induce microtubule self-renewal. Nat. Phys. 2019;15:830–838. doi: 10.1038/s41567-019-0542-4. URL:https://www.nature.com/articles/s41567-019-0542-4. PubMed DOI PMC

Janke C., Magiera M.M. The tubulin code and its role in controlling microtubule properties and functions. Nat. Rev. Mol. Cell Biol. 2020 doi: 10.1038/s41580-020-0214-3. URL:http://www.nature.com/articles/s41580-020-0214-3. PubMed DOI

Manka S.W., Moores C.A. The role of tubulin–tubulin lattice contacts in the mechanism of microtubule dynamic instability. Nature Struct. Mol. Biol. 2018;25:607–615. doi: 10.1038/s41594-018-0087-8. URL:http://www.nature.com/articles/s41594-018-0087-8. PubMed DOI PMC

Hoffmann C., Mazari E., Gosse C., Bonnemay L., Hostachy S., Gautier J., Gueroui Z. Magnetic control of protein spatial patterning to direct microtubule self-assembly. ACS Nano. 2013;7:9647–9654. doi: 10.1021/nn4022873. URL:http://pubs.acs.org/doi/abs/10.1021/nn4022873. PubMed DOI

Schaedel L., John K., Gaillard J., Nachury M.V., Blanchoin L., Théry M. Microtubules self-repair in response to mechanical stress. Nat. Mater. 2015;14:1156–1163. doi: 10.1038/nmat4396. URL:http://www.nature.com/doifinder/10.1038/nmat4396. PubMed DOI PMC

Yang G., Zhang X., Kochovski Z., Zhang Y., Dai B., Sakai F., Jiang L., Lu Y., Ballauff M., Li X., Liu C., Chen G., Jiang M. Precise and reversible protein-microtubule-like structure with helicity driven by dual supramolecular interactions. J. Am. Chem. Soc. 2016;138:1932–1937. doi: 10.1021/jacs.5b11733. URL:https://pubs.acs.org/doi/10.1021/jacs.5b11733. PubMed DOI

Hashemi Shabestari M., Meijering A., Roos W., Wuite G., Peterman E. vol. 582. Elsevier; 2017. Recent advances in biological single-molecule applications of optical tweezers and fluorescence microscopy; pp. 85–119. (Methods Enzymol.). URL:https://linkinghub.elsevier.com/retrieve/pii/S0076687916303202. PubMed

Lansky Z., Braun M., Lüdecke A., Schlierf M., ten Wolde P.R., Janson M.E., Diez S. Diffusible crosslinkers generate directed forces in microtubule networks. Cell. 2015;160:1159–1168. doi: 10.1016/j.cell.2015.01.051. URL:http://linkinghub.elsevier.com/retrieve/pii/S0092867415001294. PubMed DOI

Isozaki N., Shintaku H., Kotera H., Hawkins T.L., Ross J.L., Yokokawa R. Control of molecular shuttles by designing electrical and mechanical properties of microtubules. Sci. Robot. 2017;2:eaan4882. doi: 10.1126/scirobotics.aan4882. URL:http://robotics.sciencemag.org/lookup/doi/10.1126/scirobotics.aan4882. PubMed DOI

Carr L., Bardet S.M., Burke R.C., Arnaud-Cormos D., Leveque P., O’Connor R.P. Calcium-independent disruption of microtubule dynamics by nanosecond pulsed electric fields in U87 human glioblastoma cells. Sci. Rep. 2017;7 doi: 10.1038/srep41267. URL:http://www.nature.com/articles/srep41267. PubMed DOI PMC

Havelka D., Chafai D.E., Krivosudský O., Klebanovych A., Vostárek F., Kubínová L., Dráber P., Cifra M. Nanosecond pulsed electric field lab-on-chip integrated in super-resolution microscope for cytoskeleton imaging. Adv. Mater. Technol. 2020;5:1900669. doi: 10.1002/admt.201900669. URL:https://onlinelibrary.wiley.com/doi/abs/10.1002/admt.201900669 eprint. DOI

Chafai D.E., Vostárek F., Dráberová E., Havelka D., Arnaud-Cormos D., Leveque P., Janáček J., Kubínová L., Cifra M., Dráber P. Microtubule cytoskeleton remodeling by nanosecond pulsed electric fields. Adv. Biosyst. 2020;4:2000070. doi: 10.1002/adbi.202000070. URL:https://onlinelibrary.wiley.com/doi/abs/10.1002/adbi.202000070. PubMed DOI

Thompson G., Beier H., Ibey B. Tracking lysosome migration within chinese hamster ovary (cho) cells following exposure to nanosecond pulsed electric fields. Bioengineering. 2018;5:103. doi: 10.3390/bioengineering5040103. URL:http://www.mdpi.com/2306-5354/5/4/103. PubMed DOI 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. Biochimica et Biophysica Acta (BBA) – Biomembranes. 2018;1860:2175–2183. doi: 10.1016/j.bbamem.2018.08.017. URL:https://linkinghub.elsevier.com/retrieve/pii/S000527361830261X. PubMed DOI

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. 2014;19 055005 URL:http://biomedicaloptics.spiedigitallibrary.org/article.aspx?articleid=1873019. PubMed

English N.J., Waldron C.J. Perspectives on external electric fields in molecular simulation: progress, prospects and challenges. Phys. Chem. Chem. Phys. 2015;17:12407–12440. doi: 10.1039/C5CP00629E. URL:http://xlink.rsc.org/?DOI=C5CP00629E. PubMed DOI

Casciola M., Bonhenry D., Liberti M., Apollonio F., Tarek M. A molecular dynamic study of cholesterol rich lipid membranes: comparison of electroporation protocols. Bioelectrochemistry. 2014;100:11–17. doi: 10.1016/j.bioelechem.2014.03.009. URL:http://www.sciencedirect.com/science/article/pii/S1567539414000619. PubMed DOI

Xu D., Phillips J.C., Schulten K. Protein response to external electric fields: relaxation, hysteresis, and echo. J. Phys. Chem. 1996;100:12108–12121. URL:http://pubs.acs.org/doi/abs/10.1021/jp960076a.

Budi A., Legge F.S., Treutlein H., Yarovsky I. Electric field effects on insulin chain-b conformation. J. Phys. Chem. B. 2005;109:22641–22648. doi: 10.1021/jp052742q. URL:http://pubs.acs.org/doi/abs/10.1021/jp052742q. PubMed DOI

Apollonio F., D’Abramo M., Liberti M., Amadei A., Nola A.D., D’Inzeo G. 2006 IEEE MTT-S International Microwave Symposium Digest. 2006. Myoglobin as a case study for molecular simulations in the presence of a microwave electromagnetic field; pp. 1746–1749. iSSN: 0149-645X. DOI

Budi A., Legge F.S., Treutlein H., Yarovsky I. Effect of frequency on insulin response to electric field stress. J. Phys. Chem. B. 2007;111:5748–5756. doi: 10.1021/jp067248g. URL:http://pubs.acs.org/doi/abs/10.1021/jp067248g. PubMed DOI

Wang X., Li Y., He X., Chen S., Zhang J.Z.H. Effect of strong electric field on the conformational integrity of insulin. J. Phys. Chem. A. 2014;118:8942–8952. doi: 10.1021/jp501051r. URL:http://pubs.acs.org/doi/abs/10.1021/jp501051r. PubMed DOI

English N.J., Solomentsev G.Y., O’Brien P. Nonequilibrium molecular dynamics study of electric and low-frequency microwave fields on hen egg white lysozyme. J. Chem. Phys. 2009;131 doi: 10.1063/1.3184794. URL:http://scitation.aip.org/content/aip/journal/jcp/131/3/10.1063/1.3184794. PubMed DOI

Solomentsev G.Y., English N.J., Mooney D.A. Hydrogen bond perturbation in hen egg white lysozyme by external electromagnetic fields: A nonequilibrium molecular dynamics study. J. Chem. Phys. 2010;133 doi: 10.1063/1.3518975. URL:http://scitation.aip.org/content/aip/journal/jcp/133/23/10.1063/1.3518975. PubMed DOI

Todorova N., Bentvelzen A., English N.J., Yarovsky I. Electromagnetic-field effects on structure and dynamics of amyloidogenic peptides. J. Chem. Phys. 2016;144 doi: 10.1063/1.4941108. URL:http://scitation.aip.org/content/aip/journal/jcp/144/8/10.1063/1.4941108. PubMed DOI

Toschi F., Lugli F., Biscarini F., Zerbetto F. Effects of electric field stress on a PubMed DOI

Lugli F., Toschi F., Biscarini F., Zerbetto F. Electric field effects on short fibrils of a PubMed DOI

Singh A., Orsat V., Raghavan V. Soybean hydrophobic protein response to external electric field: a molecular modeling approach. Biomolecules. 2013;3:168–179. doi: 10.3390/biom3010168. URL:http://www.mdpi.com/2218-273X/3/1/168/ PubMed DOI PMC

Ojeda-May P., Garcia M.E. Electric field-driven disruption of a native PubMed DOI PMC

Astrakas L., Gousias C., Tzaphlidou M. Electric field effects on chignolin conformation. J. Appl. Phys. 2011;109 doi: 10.1063/1.3585867. URL:http://aip.scitation.org/doi/10.1063/1.3585867. DOI

Astrakas L.G., Gousias C., Tzaphlidou M. Structural destabilization of chignolin under the influence of oscillating electric fields. J. Appl. Phys. 2012;111 doi: 10.1063/1.3699389. URL:http://aip.scitation.org/doi/10.1063/1.3699389. DOI

Reale R., English N.J., Garate J.-A., Marracino P., Liberti M., Apollonio F. Human aquaporin 4 gating dynamics under and after nanosecond-scale static and alternating electric-field impulses: A molecular dynamics study of field effects and relaxation. J. Chem. Phys. 2013;139 doi: 10.1063/1.4832383. URL:http://aip.scitation.org/doi/10.1063/1.4832383. PubMed DOI

Marracino P., Bernardi M., Liberti M., Del Signore F., Trapani E., Gárate J.-A., Burnham C.J., Apollonio F., English N.J. Transprotein-electropore characterization: a molecular dynamics investigation on human AQP4. ACS Omega. 2018;3:15361–15369. doi: 10.1021/acsomega.8b02230. URL:http://pubs.acs.org/doi/10.1021/acsomega.8b02230. PubMed DOI PMC

E. della Valle, P. Marracino, O. Pakhomova, M. Liberti, F. Apollonio, Nanosecond pulsed electric signals can affect electrostatic environment of proteins below the threshold of conformational effects: The case study of SOD1 with a molecular simulation study, PLOS ONE 14 (2019) e0221685. URL:https://plos.org/10.1371/journal.pone.0221685. doi: 10.1371/journal.pone.0221685. PubMed PMC

Marklund E.G., Ekeberg T., Moog M., Benesch J.L.P., Caleman C. Controlling protein orientation in vacuum using electric fields. J. Phys. Chem. Lett. 2017;8:4540–4544. doi: 10.1021/acs.jpclett.7b02005. URL:https://pubs.acs.org/doi/10.1021/acs.jpclett.7b02005. PubMed DOI

Muscat S., Stojceski F., Danani A. Elucidating the effect of static electric field on Amyloid Beta 1–42 supramolecular assembly. J. Mol. Graph. Model. 2020;107535 doi: 10.1016/j.jmgm.2020.107535. URL:http://www.sciencedirect.com/science/article/pii/S1093326319306357. PubMed DOI

Saeidi H.R., Lohrasebi A., Mahnam K. External electric field effects on the mechanical properties of the PubMed DOI

Setayandeh S.S., Lohrasebi A. Influence of GHz electric fields on the mechanical properties of a microtubule. J. Mol. Model. 2015;21 doi: 10.1007/s00894-015-2637-x. URL:http://link.springer.com/10.1007/s00894-015-2637-x. PubMed DOI

Setayandeh S.S., Lohrasebi A. The effects of external electric fields of 900 MHz and 2450 MHz frequencies on DOI

Marracino P., Havelka D., Pruša J., Liberti M., Tuszynski J., Ayoub A.T., Apollonio F., Cifra M. Tubulin response to intense nanosecond-scale electric field in molecular dynamics simulation. Sci. Rep. 2019;9:10477. doi: 10.1038/s41598-019-46636-4. URL:https://doi.org/10.1038/s41598-019-46636-4. PubMed DOI PMC

Timmons J.J., Preto J., Tuszynski J.A., Wong E.T. Tubulin’s response to external electric fields by molecular dynamics simulations. PLOS ONE. 2018;13 doi: 10.1371/journal.pone.0202141. URL:https://plos.org/10.1371/journal.pone.0202141. PubMed DOI PMC

Pruša J., Cifra M. Molecular dynamics simulation of the nanosecond pulsed electric field effect on kinesin nanomotor. Sci. Rep. 2019;9 doi: 10.1038/s41598-019-56052-3. URL:http://www.nature.com/articles/s41598-019-56052-3. PubMed DOI PMC

English N.J., Mooney D.A. Denaturation of hen egg white lysozyme in electromagnetic fields: A molecular dynamics study. J. Chem. Phys. 2007;126 doi: 10.1063/1.2515315. URL:http://scitation.aip.org/content/aip/journal/jcp/126/9/10.1063/1.2515315. PubMed DOI

Marracino P., Apollonio F., Liberti M., d’Inzeo G., Amadei A. Effect of high exogenous electric pulses on protein conformation: myoglobin as a case study. J. Phys. Chem. 2013;B117:2273–2279. doi: 10.1021/jp309857b. URL:http://pubs.acs.org/doi/abs/10.1021/jp309857b. PubMed DOI

P. Marracino, Technology of High-Intensity Electric-Field Pulses: A Way to Control Protein Unfolding, Journal of Physical Chemistry & Biophysics 03 (2013). URL:http://www.omicsonline.org/technology-of-high-intensity-electric-field-pulses-a-way-to-control-protein-unfolding-2161-0398.1000117.php?aid=15472. doi: 10.4172/2161-0398.1000117.

Wu L., Zhao W., Yang R., Yan W. Pulsed electric field (PEF)-induced aggregation between lysozyme, ovalbumin and ovotransferrin in multi-protein system. Food Chem. 2015;175:115–120. doi: 10.1016/j.foodchem.2014.11.136. URL:http://linkinghub.elsevier.com/retrieve/pii/S0308814614018743. PubMed DOI

Tian M.-L., Fang T., Du M.-Y., Zhang F.-S. Effects of Pulsed Electric Field (PEF) Treatment on Enhancing Activity and Conformation of PubMed DOI

Hekstra D.R., White K.I., Socolich M.A., Henning R.W., Šrajer V., Ranganathan R. Electric-field-stimulated protein mechanics. Nature. 2016;540:400–405. doi: 10.1038/nature20571. URL:https://www.nature.com/articles/nature20571. PubMed DOI PMC

Urabe G., Katagiri T., Katsuki S. Intense pulsed electric fields denature urease protein. Bioelectricity. 2019 doi: 10.1089/bioe.2019.0021. bioe.2019.0021, URL:https://www.liebertpub.com/doi/10.1089/bioe.2019.0021. PubMed DOI PMC

G. Urabe, T. Sato, G. Nakamura, Y. Kobashigawa, H. Morioka, S. Katsuki, 1.2 MV/cm pulsed electric fields promote transthyretin aggregate degradation, Scientific Reports 10 (2020) 12003. URL:http://www.nature.com/articles/s41598-020-68681-0. doi: 10.1038/s41598-020-68681-0. PubMed PMC

Ayoub A.T., Klobukowski M., Tuszynski J.A. Detailed per-residue energetic analysis explains the driving force for microtubule disassembly. PLOS Comput. Biol. 2015;11 doi: 10.1371/journal.pcbi.1004313. URL:https://plos.org/10.1371/journal.pcbi.1004313. PubMed DOI PMC

Tuszynski J.A., Carpenter E.J., Huzil J.T., Malinski W., Luchko T., Luduena R.F. 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. 2006;50:341–358. doi: 10.1387/ijdb.052063jt. URL:http://www.intjdevbiol.com/paper.php?doi=052063jt. PubMed DOI

Salomon-Ferrer R., Götz A.W., Poole D., Le Grand S., Walker R.C. Routine microsecond molecular dynamics simulations with AMBER on GPUs. 2. Explicit solvent particle mesh Ewald. J. Chem. Theory Comput. 2013;9:3878–3888. doi: 10.1021/ct400314y. URL:https://pubs.acs.org/doi/10.1021/ct400314y. PubMed DOI

S. Le Grand, A.W. Götz, R.C. Walker, SPFP: Speed without compromise—A mixed precision model for GPU accelerated molecular dynamics simulations, Computer Physics Communications 184 (2013) 374–380. Publisher: Elsevier.

Jorgensen W.L., Chandrasekhar J., Madura J.D., Impey R.W., Klein M.L. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 1983;79:926–935. doi: 10.1063/1.445869. URL:http://aip.scitation.org/doi/10.1063/1.445869. DOI

Joung I.S., Cheatham T.E. Determination of alkali and halide monovalent ion parameters for use in explicitly solvated biomolecular simulations. J. Phys. Chem. 2008;B112:9020–9041. doi: 10.1021/jp8001614. URL:https://pubs.acs.org/doi/10.1021/jp8001614. PubMed DOI PMC

Meagher K.L., Redman L.T., Carlson H.A. Development of polyphosphate parameters for use with the AMBER force field. J. Comput. Chem. 2003;24:1016–1025. doi: 10.1002/jcc.10262. URL:http://doi.wiley.com/10.1002/jcc.10262. PubMed DOI

Miller B.R., McGee T.D., Swails J.M., Homeyer N., Gohlke H., Roitberg A.E. MMPBSA.py: An efficient program for end-state free energy calculations. J. Chem. Theory Comput. 2012;8:3314–3321. doi: 10.1021/ct300418h. URL:https://pubs.acs.org/doi/10.1021/ct300418h. PubMed DOI

Ayoub A., Staelens M., Prunotto A., Deriu M., Danani A., Klobukowski M., Tuszynski J. Explaining the microtubule energy balance: contributions due to dipole moments, charges, van der Waals and solvation energy. Int. J. Mol. Sci. 2017;18 doi: 10.3390/ijms18102042. 2042, URL:http://www.mdpi.com/1422-0067/18/10/2042. PubMed DOI PMC

T. Hou, J. Wang, Y. Li, W. Wang, Assessing the performance of the MM/PBSA and MM/GBSA methods. 1. The accuracy of binding free energy calculations based on molecular dynamics simulations, Journal of Chemical Information and Modeling 51 (2011) 69–82. URL:https://doi.org/10.1021/ci100275a. doi: 10.1021/ci100275a, publisher: American Chemical Society. PubMed PMC

Ayoub A.T., Craddock T.J., Klobukowski M., Tuszynski J. Analysis of the strength of interfacial hydrogen bonds between tubulin dimers using quantum theory of atoms in molecules. Biophys. J. 2014;107:740–750. doi: 10.1016/j.bpj.2014.05.047. URL:http://linkinghub.elsevier.com/retrieve/pii/S0006349514006766. PubMed DOI PMC

Díaz J.F., Valpuesta J.M., Chacón P., Diakun G., Andreu J.M. Changes in microtubule protofilament number induced by taxol binding to an easily accessible site: internal microtubule dynamics. J. Biol. Chem. 1998;273:33803–33810. doi: 10.1074/jbc.273.50.33803. URL:http://www.jbc.org/lookup/doi/10.1074/jbc.273.50.33803. PubMed DOI

C. Coombes, A. Yamamoto, M. McClellan, T.A. Reid, M. Plooster, G.W.G. Luxton, J. Alper, J. Howard, M.K. Gardner, Mechanism of microtubule lumen entry for the PubMed PMC

Mitchison T., Kirschner M. Dynamic instability of microtubule growth. Nature. 1984;312:237–242. URL:https://doi.org/10.1038/312237a0. PubMed

Seetapun D., Castle B.T., McIntyre A.J., Tran P.T., Odde D.J. Estimating the microtubule GTP cap size in vivo. Curr. Biol. 2012;22:1681–1687. doi: 10.1016/j.cub.2012.06.068. URL:http://www.sciencedirect.com/science/article/pii/S0960982212007440. PubMed DOI PMC

A.A. Hyman, S. Salser, D.N. Drechsel, N. Unwin, T.J. Mitchison, Role of gtp hydrolysis in microtubule dynamics: information from a slowly hydrolyzable analogue, gmpcpp., Molecular Biology of the Cell 3 (1992) 1155–1167. URL:https://doi.org/10.1091/mbc.3.10.1155. doi: 10.1091/mbc.3.10.1155. arXiv:https://doi.org/10.1091/mbc.3.10.1155, pMID: 1421572. PubMed PMC

Alushin G.M., Lander G.C., Kellogg E.H., Zhang R., Baker D., Nogales E. High-resolution microtubule structures reveal the structural transitions in PubMed DOI PMC

Kotnik T., Rems L., Tarek M., Miklavčič D. Membrane electroporation and electropermeabilization: mechanisms and models. Ann. Rev. Biophys. 2019;48:63–91. doi: 10.1146/annurev-biophys-052118-115451. PubMed DOI

Yarmush M.L., Golberg A., Serša G., Kotnik T., Miklavčič D. Electroporation-based technologies for medicine: principles, applications, and challenges. Annu. Rev. Biomed. Eng. 2014;16:295–320. doi: 10.1146/annurev-bioeng-071813-104622. URL:http://www.annualreviews.org/doi/10.1146/annurev-bioeng-071813-104622. PubMed DOI

Rols M.-P., Teissie J. Electropermeabilization of mammalian cells. Quantitative analysis of the phenomenon. Biophys. J. 1990;58:1089–1098. PubMed PMC

Joshi R.P., Schoenbach K.H. Bioelectric effects of intense ultrashort pulses. Crit. Rev. PubMed

Aragonès A.C., Haworth N.L., Darwish N., Ciampi S., Bloomfield N.J., Wallace G.G., Diez-Perez I., Coote M.L. Electrostatic catalysis of a Diels-Alder reaction. Nature. 2016;531:88–91. doi: 10.1038/nature16989. URL:http://www.nature.com/doifinder/10.1038/nature16989. PubMed DOI

Welborn V.V., Head-Gordon T. Fluctuations of electric fields in the active site of the enzyme ketosteroid isomerase. J. Am. Chem. Soc. 2019;141:12487–12492. doi: 10.1021/jacs.9b05323. URL:https://pubs.acs.org/doi/10.1021/jacs.9b05323. PubMed DOI

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...