Fast Leaps between Millisecond Confinements Govern Ase1 Diffusion along Microtubules
Language English Country Germany Media print-electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
Grant support
LL1602
Ministry of Education, Youth and Sports of the Czech Republic
- Keywords
- Ase1, coarse-grain model, energy landscape, interferometric scattering microscopy, scattering labels,
- MeSH
- Cell Division MeSH
- Spatio-Temporal Analysis MeSH
- Microtubules metabolism MeSH
- Swine MeSH
- Protein Domains MeSH
- Microtubule-Associated Proteins chemistry metabolism MeSH
- Molecular Dynamics Simulation MeSH
- Protein Transport MeSH
- Single Molecule Imaging MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Microtubule-Associated Proteins MeSH
Diffusion is the most fundamental mode of protein translocation within cells. Confined diffusion of proteins along the electrostatic potential constituted by the surface of microtubules, although modeled meticulously in molecular dynamics simulations, has not been experimentally observed in real-time. Here, interferometric scattering microscopy is used to directly visualize the movement of the microtubule-associated protein Ase1 along the microtubule surface at nanometer and microsecond resolution. Millisecond confinements of Ase1 and fast leaps between these positions of dwelling preferentially occurring along the microtubule protofilaments are resolved, revealing Ase1's mode of diffusive translocation along the microtubule's periodic surface. The derived interaction potential closely matches the tubulin-dimer periodicity and the distribution of the electrostatic potential on the microtubule lattice. It is anticipated that mapping the interaction landscapes for different proteins on microtubules, finding plausible energetic barriers of different positioning and heights, can provide valuable insights into regulating the dynamics of essential cytoskeletal processes, such as intracellular cargo trafficking, cell division, and morphogenesis, all of which rely on diffusive translocation of proteins along microtubules.
See more in PubMed
J. Helenius, G. Brouhard, Y. Kalaidzidis, S. Diez, J. Howard, Nature 2006, 441, 115.
M. Braun, Z. Lansky, G. Fink, F. Ruhnow, S. Diez, M. E. Janson, Nat. Cell Biol. 2011, 13, 1259.
V. Henrichs, L. Grycova, C. Barinka, Z. Nahacka, J. Neuzil, S. Diez, J. Rohlena, M. Braun, Z. Lansky, Nat. Commun. 2020, 11, 3123.
S. Forth, K.-C. Hsia, Y. Shimamoto, T. M. Kapoor, Cell 2014, 157, 420.
Z. Lansky, M. Braun, A. Lüdecke, M. Schlierf, P. R. ten Wolde, M. E. Janson, S. Diez, Cell 2015, 160, 1159.
E. H. Kellogg, S. Howes, S.-C. Ti, E. Ramírez-Aportela, T. M. Kapoor, P. Chacón, E. Nogales, Proc. Natl. Acad. Sci. USA 2016, 113, 9430.
R. Subramanian, E. M. Wilson-Kubalek, C. P. Arthur, M. J. Bick, E. A. Campbell, S. A. Darst, R. A. Milligan, T. M. Kapoor, Cell 2010, 142, 433.
H. Wierenga, P. R. ten Wolde, Phys. Rev. Lett. 2020, 125, 078101.
L. S. Bigman, Y. Levy, Proc. Natl. Acad. Sci. USA 2020, 117, 8876.
C. Mollinari, J.-P. Kleman, W. Jiang, G. Schoehn, T. Hunter, R. L. Margolis, J. Cell Biol. 2002, 157, 1175.
I. Loïodice, J. Staub, T. G. Setty, N.-P. T. Nguyen, A. Paoletti, P. T. Tran, Mol. Biol. Cell 2005, 16, 1756.
A. Yamashita, M. Sato, A. Fujita, M. Yamamoto, T. Toda, Mol. Biol. Cell 2005, 16, 1378.
M. E. Janson, R. Loughlin, I. Loïodice, C. Fu, D. Brunner, F. J. Nédélec, P. T. Tran, Cell 2007, 128, 357.
S. Wijeratne, R. Subramanian, eLife 2018, 7, e32595.
L. C. Kapitein, M. E. Janson, S. M. J. L. van den Wildenberg, C. C. Hoogenraad, C. F. Schmidt, E. J. G. Peterman, Curr. Biol. 2008, 18, 1713.
L. S. Bigman, Y. Levy, Biophys. J. 2020, 118, 3008.
C. Eggeling, J. Widengren, R. Rigler, C. A. M. Seidel, Anal. Chem. 1998, 70, 2651.
J. Vogelsang, R. Kasper, C. Steinhauer, B. Person, M. Heilemann, M. Sauer, P. Tinnefeld, Angew. Chem., Int. Ed. 2008, 47, 5465.
R. W. Taylor, V. Sandoghdar, Nano Lett. 2019, 19, 4827.
H. Ueno, S. Nishikawa, R. Iino, K. V. Tabata, S. Sakakihara, T. Yanagida, H. Noji, Biophys. J. 2010, 98, 2014.
H. Isojima, R. Iino, Y. Niitani, H. Noji, M. Tomishige, Nat. Chem. Biol. 2016, 12, 290.
K. Lindfors, T. Kalkbrenner, P. Stoller, V. Sandoghdar, Phys. Rev. Lett. 2004, 93, 037401.
K. Holanová, M. Vala, M. Piliarik, Opt. Laser Technol. 2019, 109, 323.
J. Andrecka, J. O. Arroyo, Y. Takagi, G. de Wit, A. Fineberg, L. MacKinnon, G. Young, J. R. Sellers, P. Kukura, eLife 2015, 4, e05413.
K. J. Mickolajczyk, N. C. Deffenbaugh, J. O. Arroyo, J. Andrecka, P. Kukura, W. O. Hancock, Proc. Natl. Acad. Sci. USA 2015, 112, E7186.
G. de Wit, D. Albrecht, H. Ewers, P. Kukura, Biophys. J. 2018, 114, 2945.
F. Reina, S. Galiani, D. Shrestha, E. Sezgin, G. de Wit, D. Cole, B. C. Lagerholm, P. Kukura, C. Eggeling, J. Phys. D: Appl. Phys. 2018, 51, 235401.
C.-Y. Cheng, Y.-H. Liao, C.-L. Hsieh, Nanoscale 2019, 11, 568.
M. Piliarik, V. Sandoghdar, Nat. Commun. 2014, 5, 4495.
C.-L. Hsieh, Opt. Commun. 2018, 422, 69.
M. Vala, Ł. Bujak, A. G. Marín, K. Holanová, V. Henrichs, M. Braun, Z. Lánský, M. Piliarik, Small Methods 2021, 5, 2000985.
S. Spindler, J. Ehrig, K. König, T. Nowak, M. Piliarik, H. E. Stein, R. W. Taylor, E. Garanger, S. Lecommandoux, I. D. Alves, V. Sandoghdar, J. Phys. D: Appl. Phys. 2016, 49, 274002.
M. Krishnan, N. Mojarad, P. Kukura, V. Sandoghdar, Nature 2010, 467, 692.
R. W. Taylor, R. G. Mahmoodabadi, V. Rauschenberger, A. Giessl, A. Schambony, V. Sandoghdar, Nat. Photonics 2019, 13, 480.
H. M. L. Robert, K. Holanová, Ł. Bujak, M. Vala, V. Henrichs, Z. Lánský, M. Piliarik, Nat. Commun. 2021, 12, 2921.
M. Ernst, T. John, M. Guenther, C. Wagner, U. F. Schaefer, C.-M. Lehr, Biophys. J. 2017, 112, 172.
J. Atherton, M. Stouffer, F. Francis, C. A. Moores, Acta Crystallogr., Sect. D: Struct. Biol. 2018, 74, 572.
C. Janke, M. M. Magiera, Nat. Rev. Mol. Cell Biol. 2020, 21, 307.
A. A. Hyman, D. Chrétien, I. Arnal, R. H. Wade, J. Cell Biol. 1995, 128, 117.
M. S. Woody, J. H. Lewis, M. J. Greenberg, Y. E. Goldman, E. M. Ostap, Biophys. J. 2016, 111, 273.
A. Vemu, J. Atherton, J. O. Spector, A. Szyk, C. A. Moores, A. Roll-Mecak, J. Biol. Chem. 2016, 291, 12907.
M. Kikkawa, T. Ishikawa, T. Nakata, T. Wakabayashi, N. Hirokawa, J. Cell Biol. 1994, 127, 1965.
I. Zhernov, S. Diez, M. Braun, Z. Lansky, Curr. Biol. 2020, 30, 3342.
Y. Okada, H. Higuchi, N. Hirokawa, Nature 2003, 424, 574.
G. Fink, L. Hajdo, K. J. Skowronek, C. Reuther, A. A. Kasprzak, S. Diez, Nat. Cell Biol. 2009, 11, 717.
M. H. Hinrichs, A. Jalal, B. Brenner, E. Mandelkow, S. Kumar, T. Scholz, J. Biol. Chem. 2012, 287, 38559.
B. Y. Monroy, D. L. Sawyer, B. E. Ackermann, M. M. Borden, T. C. Tan, K. M. Ori-McKenney, Nat. Commun. 2018, 9, 1487.
P. J. Hooikaas, M. Martin, T. Mühlethaler, G.-J. Kuijntjes, C. A. E. Peeters, E. A. Katrukha, L. Ferrari, R. Stucchi, D. G. F. Verhagen, W. E. van Riel, I. Grigoriev, A. F. M. Altelaar, C. C. Hoogenraad, S. G. D. Rüdiger, M. O. Steinmetz, L. C. Kapitein, A. Akhmanova, J. Cell Biol. 2019, 218, 1298.
S. Westermann, H.-W. Wang, A. Avila-Sakar, D. G. Drubin, E. Nogales, G. Barnes, Nature 2006, 440, 565.
G. J. Brouhard, J. H. Stear, T. L. Noetzel, J. Al-Bassam, K. Kinoshita, S. C. Harrison, J. Howard, A. A. Hyman, Cell 2008, 132, 79.
P. Bieling, I. A. Telley, T. Surrey, Cell 2010, 142, 420.
G. J. Hoeprich, A. R. Thompson, D. P. McVicker, W. O. Hancock, C. L. Berger, Biophys. J. 2014, 106, 1691.
A. Mitra, F. Ruhnow, S. Girardo, S. Diez, Proc. Natl. Acad. Sci. USA 2018, 115, E7950.
M. Castoldi, A. V. Popov, Protein Expression Purif. 2003, 32, 83.
J.-Y. Tinevez, N. Perry, J. Schindelin, G. M. Hoopes, G. D. Reynolds, E. Laplantine, S. Y. Bednarek, S. L. Shorte, K. W. Eliceiri, Methods 2017, 115, 80.
J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, A. Cardona, Nat. Methods 2012, 9, 676.
C. T. Rueden, J. Schindelin, M. C. Hiner, B. E. DeZonia, A. E. Walter, E. T. Arena, K. W. Eliceiri, BMC Bioinformatics 2017, 18, 529.
X. Michalet, Phys. Rev. E 2010, 82, 041914.
H. Qian, M. P. Sheetz, E. L. Elson, Biophys. J. 1991, 60, 910.
https://Github.Com/Bujakl/Ase1_step, 2021.
J. K. Noel, P. C. Whitford, K. Y. Sanbonmatsu, J. N. Onuchic, Nucleic Acids Res. 2010, 38, W657.
J. K. Noel, M. Levi, M. Raghunathan, H. Lammert, R. L. Hayes, J. N. Onuchic, P. C. Whitford, PLoS Comput. Biol. 2016, 12, e1004794.
A. Azia, Y. Levy, J. Mol. Biol. 2009, 393, 527.
M. J. Abraham, T. Murtola, R. Schulz, S. Páll, J. C. Smith, B. Hess, E. Lindahl, SoftwareX 2015, 1-2, 19.
W. Humphrey, A. Dalke, K. Schulten, J. Mol. Graphics 1996, 14, 33.
Surpassing the Diffraction Limit in Label-Free Optical Microscopy
Electro-detachment of kinesin motor domain from microtubule in silico
Lab-on-chip microscope platform for electro-manipulation of a dense microtubules network
