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Electronic Energy Migration in Microtubules

[Image: see text] The repeating arrangement of tubulin dimers confers great mechanical strength to microtubules, which are used as scaffolds for intracellular macromolecular transport in cells and exploited in biohybrid devices. The crystalline order in a microtubule, with lattice constants short en...

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Autores principales: Kalra, Aarat P., Benny, Alfy, Travis, Sophie M., Zizzi, Eric A., Morales-Sanchez, Austin, Oblinsky, Daniel G., Craddock, Travis J. A., Hameroff, Stuart R., MacIver, M. Bruce, Tuszyński, Jack A., Petry, Sabine, Penrose, Roger, Scholes, Gregory D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Chemical Society 2023
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10037452/
https://www.ncbi.nlm.nih.gov/pubmed/36968538
http://dx.doi.org/10.1021/acscentsci.2c01114
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author Kalra, Aarat P.
Benny, Alfy
Travis, Sophie M.
Zizzi, Eric A.
Morales-Sanchez, Austin
Oblinsky, Daniel G.
Craddock, Travis J. A.
Hameroff, Stuart R.
MacIver, M. Bruce
Tuszyński, Jack A.
Petry, Sabine
Penrose, Roger
Scholes, Gregory D.
author_facet Kalra, Aarat P.
Benny, Alfy
Travis, Sophie M.
Zizzi, Eric A.
Morales-Sanchez, Austin
Oblinsky, Daniel G.
Craddock, Travis J. A.
Hameroff, Stuart R.
MacIver, M. Bruce
Tuszyński, Jack A.
Petry, Sabine
Penrose, Roger
Scholes, Gregory D.
author_sort Kalra, Aarat P.
collection PubMed
description [Image: see text] The repeating arrangement of tubulin dimers confers great mechanical strength to microtubules, which are used as scaffolds for intracellular macromolecular transport in cells and exploited in biohybrid devices. The crystalline order in a microtubule, with lattice constants short enough to allow energy transfer between amino acid chromophores, is similar to synthetic structures designed for light harvesting. After photoexcitation, can these amino acid chromophores transfer excitation energy along the microtubule like a natural or artificial light-harvesting system? Here, we use tryptophan autofluorescence lifetimes to probe energy hopping between aromatic residues in tubulin and microtubules. By studying how the quencher concentration alters tryptophan autofluorescence lifetimes, we demonstrate that electronic energy can diffuse over 6.6 nm in microtubules. We discover that while diffusion lengths are influenced by tubulin polymerization state (free tubulin versus tubulin in the microtubule lattice), they are not significantly altered by the average number of protofilaments (13 versus 14). We also demonstrate that the presence of the anesthetics etomidate and isoflurane reduce exciton diffusion. Energy transport as explained by conventional Förster theory (accommodating for interactions between tryptophan and tyrosine residues) does not sufficiently explain our observations. Our studies indicate that microtubules are, unexpectedly, effective light harvesters.
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spelling pubmed-100374522023-03-25 Electronic Energy Migration in Microtubules Kalra, Aarat P. Benny, Alfy Travis, Sophie M. Zizzi, Eric A. Morales-Sanchez, Austin Oblinsky, Daniel G. Craddock, Travis J. A. Hameroff, Stuart R. MacIver, M. Bruce Tuszyński, Jack A. Petry, Sabine Penrose, Roger Scholes, Gregory D. ACS Cent Sci [Image: see text] The repeating arrangement of tubulin dimers confers great mechanical strength to microtubules, which are used as scaffolds for intracellular macromolecular transport in cells and exploited in biohybrid devices. The crystalline order in a microtubule, with lattice constants short enough to allow energy transfer between amino acid chromophores, is similar to synthetic structures designed for light harvesting. After photoexcitation, can these amino acid chromophores transfer excitation energy along the microtubule like a natural or artificial light-harvesting system? Here, we use tryptophan autofluorescence lifetimes to probe energy hopping between aromatic residues in tubulin and microtubules. By studying how the quencher concentration alters tryptophan autofluorescence lifetimes, we demonstrate that electronic energy can diffuse over 6.6 nm in microtubules. We discover that while diffusion lengths are influenced by tubulin polymerization state (free tubulin versus tubulin in the microtubule lattice), they are not significantly altered by the average number of protofilaments (13 versus 14). We also demonstrate that the presence of the anesthetics etomidate and isoflurane reduce exciton diffusion. Energy transport as explained by conventional Förster theory (accommodating for interactions between tryptophan and tyrosine residues) does not sufficiently explain our observations. Our studies indicate that microtubules are, unexpectedly, effective light harvesters. American Chemical Society 2023-01-12 /pmc/articles/PMC10037452/ /pubmed/36968538 http://dx.doi.org/10.1021/acscentsci.2c01114 Text en © 2023 The Authors. Published by American Chemical Society https://creativecommons.org/licenses/by/4.0/Permits the broadest form of re-use including for commercial purposes, provided that author attribution and integrity are maintained (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Kalra, Aarat P.
Benny, Alfy
Travis, Sophie M.
Zizzi, Eric A.
Morales-Sanchez, Austin
Oblinsky, Daniel G.
Craddock, Travis J. A.
Hameroff, Stuart R.
MacIver, M. Bruce
Tuszyński, Jack A.
Petry, Sabine
Penrose, Roger
Scholes, Gregory D.
Electronic Energy Migration in Microtubules
title Electronic Energy Migration in Microtubules
title_full Electronic Energy Migration in Microtubules
title_fullStr Electronic Energy Migration in Microtubules
title_full_unstemmed Electronic Energy Migration in Microtubules
title_short Electronic Energy Migration in Microtubules
title_sort electronic energy migration in microtubules
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10037452/
https://www.ncbi.nlm.nih.gov/pubmed/36968538
http://dx.doi.org/10.1021/acscentsci.2c01114
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