Mechanical splitting of microtubules into protofilament bundles by surface-bound kinesin-1

VanDelinder, Virginia; Adams, Peter G.; Bachand, George D.

doi:10.1038/srep39408

Mechanical splitting of microtubules into protofilament bundles by surface-bound kinesin-1

Journal Article · Wed Dec 21 00:00:00 EST 2016 · Scientific Reports

DOI:https://doi.org/10.1038/srep39408· OSTI ID:1339254

VanDelinder, Virginia ^[1]; Adams, Peter G. ^[2]; Bachand, George D. ^[1]

Sandia National Lab. (SNL-NM), Albuquerque, NM (United States). Center for Integrated Nanotechnologies
Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Center for Integrated Nanotechnologies

The fundamental biophysics of gliding microtubule (MT) motility by surface-tethered kinesin-1 motor proteins has been widely studied, as well as applied to capture and transport analytes in bioanalytical microdevices. In these systems, phenomena such as molecular wear and fracture into shorter MTs have been reported due the mechanical forces applied on the MT during transport. In the present work, we show that MTs can be split longitudinally into protofilament bundles (PFBs) by the work performed by surface-bound kinesin motors. We examine the properties of these PFBs using several techniques (e.g., fluorescence microscopy, SEM, AFM), and show that the PFBs continue to be mobile on the surface and display very high curvature compared to MT. Further, higher surface density of kinesin motors and shorter kinesin-surface tethers promote PFB formation, whereas modifying MT with GMPCPP or higher paclitaxel concentrations did not affect PFB formation.

View Accepted Manuscript (DOE)

Research Organization:: Los Alamos National Lab. (LANL), Los Alamos, NM (United States); Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: AC04-94AL85000; AC52-06NA25396; SC0001035

OSTI ID:: 1339254

Report Number(s):: SAND2017--0052J; srep39408

Journal Information:: Scientific Reports, Journal Name: Scientific Reports Vol. 6; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (39)

End-stabilized microtubules observed in vitro: Stability, subunit interchange, and breakage Dye, Rick B.; Flicker, Paula F.; Lien, David Y. Cell Motility and the Cytoskeleton, Vol. 21, Issue 3 https://doi.org/10.1002/cm.970210302	journal	January 1992
Kinesin does not support the motility of zinc-macrotubes Ray, Sanghamitra; Wolf, Sharon G.; Howard, Jonathon Cell Motility and the Cytoskeleton, Vol. 30, Issue 2 https://doi.org/10.1002/cm.970300206	journal	January 1995
Modeling elastic properties of microtubule tips and walls Jánosi, Imre M.; Chrétien, Denis; Flyvbjerg, Henrik European Biophysics Journal, Vol. 27, Issue 5 https://doi.org/10.1007/s002490050160	journal	August 1998
Force and velocity measured for single kinesin molecules Svoboda, Karel; Block, Steven M. Cell, Vol. 77, Issue 5 https://doi.org/10.1016/0092-8674(94)90060-4	journal	June 1994
High-Resolution Microtubule Structures Reveal the Structural Transitions in αβ-Tubulin upon GTP Hydrolysis Alushin, Gregory M.; Lander, Gabriel C.; Kellogg, Elizabeth H. Cell, Vol. 157, Issue 5 https://doi.org/10.1016/j.cell.2014.03.053	journal	May 2014
Towards the application of cytoskeletal motor proteins in molecular detection and diagnostic devices Korten, Till; Månsson, Alf; Diez, Stefan Current Opinion in Biotechnology, Vol. 21, Issue 4 https://doi.org/10.1016/j.copbio.2010.05.001	journal	August 2010
Straight GDP-Tubulin Protofilaments Form in the Presence of Taxol Elie-Caille, Céline; Severin, Fedor; Helenius, Jonne Current Biology, Vol. 17, Issue 20 https://doi.org/10.1016/j.cub.2007.08.063	journal	October 2007
How does taxol stabilize microtubules? Arnal, Isabelle; Wade, Richard H. Current Biology, Vol. 5, Issue 8 https://doi.org/10.1016/s0960-9822(95)00180-1	journal	August 1995
Photodamage and the Importance of Photoprotection in Biomolecular-Powered Device Applications VanDelinder, Virginia; Bachand, George D. Analytical Chemistry, Vol. 86, Issue 1 https://doi.org/10.1021/ac403187g	journal	December 2013
Tubulin Bond Energies and Microtubule Biomechanics Determined from Nanoindentation in Silico Kononova, Olga; Kholodov, Yaroslav; Theisen, Kelly E. Journal of the American Chemical Society, Vol. 136, Issue 49 https://doi.org/10.1021/ja506385p	journal	November 2014
On the Mechanism of Trolox as Antiblinking and Antibleaching Reagent Cordes, Thorben; Vogelsang, Jan; Tinnefeld, Philip Journal of the American Chemical Society, Vol. 131, Issue 14 https://doi.org/10.1021/ja809117z	journal	April 2009
Molecular biomimetics: nanotechnology through biology Sarikaya, Mehmet; Tamerler, Candan; Jen, Alex K. -Y. Nature Materials, Vol. 2, Issue 9 https://doi.org/10.1038/nmat964	journal	September 2003
Molecular wear of microtubules propelled by surface-adhered kinesins Dumont, Emmanuel L. P.; Do, Catherine; Hess, Henry Nature Nanotechnology, Vol. 10, Issue 2 https://doi.org/10.1038/nnano.2014.334	journal	January 2015
Structural rearrangements in tubulin following microtubule formation Krebs, Angelika; Goldie, Kenneth N.; Hoenger, Andreas EMBO reports, Vol. 6, Issue 3 https://doi.org/10.1038/sj.embor.7400360	journal	March 2005
Applications of peptide and protein-based materials in bionanotechnology de la Rica, Roberto; Matsui, Hiroshi Chemical Society Reviews, Vol. 39, Issue 9 https://doi.org/10.1039/b917574c	journal	January 2010
Controlling self-assembly of microtubule spools via kinesin motor density Lam, A. T.; Curschellas, C.; Krovvidi, D. Soft Matter, Vol. 10, Issue 43 https://doi.org/10.1039/c4sm01518e	journal	January 2014
Parallel computation with molecular-motor-propelled agents in nanofabricated networks Nicolau, Dan V.; Lard, Mercy; Korten, Till Proceedings of the National Academy of Sciences, Vol. 113, Issue 10 https://doi.org/10.1073/pnas.1510825113	journal	February 2016
Kinesin Takes One 8-nm Step for Each ATP That It Hydrolyzes Coy, David L.; Wagenbach, Michael; Howard, Jonathon Journal of Biological Chemistry, Vol. 274, Issue 6 https://doi.org/10.1074/jbc.274.6.3667	journal	February 1999
Microtubule dynamics and microtubule caps: a time-resolved cryo- electron microscopy study Mandelkow, E. M. The Journal of Cell Biology, Vol. 114, Issue 5 https://doi.org/10.1083/jcb.114.5.977	journal	September 1991
Tubulin protofilaments and kinesin-dependent motility. Kamimura, S.; Mandelkow, E. The Journal of Cell Biology, Vol. 118, Issue 4 https://doi.org/10.1083/jcb.118.4.865	journal	August 1992
Kinesin follows the microtubule's protofilament axis Ray, S. The Journal of Cell Biology, Vol. 121, Issue 5 https://doi.org/10.1083/jcb.121.5.1083	journal	June 1993
Structural changes accompanying GTP hydrolysis in microtubules: information from a slowly hydrolyzable analogue guanylyl-(alpha,beta)- methylene-diphosphonate Hyman, A. A. The Journal of Cell Biology, Vol. 128, Issue 1 https://doi.org/10.1083/jcb.128.1.117	journal	January 1995
Structure of growing microtubule ends: two-dimensional sheets close into tubes at variable rates Chretien, D. The Journal of Cell Biology, Vol. 129, Issue 5 https://doi.org/10.1083/jcb.129.5.1311	journal	June 1995
Processivity of the Motor Protein Kinesin Requires Two Heads Hancock, William O.; Howard, Jonathon The Journal of Cell Biology, Vol. 140, Issue 6 https://doi.org/10.1083/jcb.140.6.1395	journal	March 1998
Loop formation of microtubules during gliding at high density Liu, Lynn; Tüzel, Erkan; Ross, Jennifer L. Journal of Physics: Condensed Matter, Vol. 23, Issue 37 https://doi.org/10.1088/0953-8984/23/37/374104	journal	August 2011
The role of casein in supporting the operation of surface bound kinesin Verma, Vivek; Hancock, William O.; Catchmark, Jeffrey M. Journal of Biological Engineering, Vol. 2, Issue 1 https://doi.org/10.1186/1754-1611-2-14	journal	January 2008
A Single Protofilament Is Sufficient to Support Unidirectional Walking of Dynein and Kinesin Shibata, Keitaro; Miura, Michi; Watanabe, Yuta PLoS ONE, Vol. 7, Issue 8 https://doi.org/10.1371/journal.pone.0042990	journal	August 2012
Taxol Allosterically Alters the Dynamics of the Tubulin Dimer and Increases the Flexibility of Microtubules Mitra, Arpita; Sept, David Biophysical Journal, Vol. 95, Issue 7 https://doi.org/10.1529/biophysj.108.133884	journal	October 2008
Why Microtubules run in Circles - Mechanical Hysteresis of the Tubulin Lattice Ziebert, Falko; Mohrbach, Hervé; Kulić, Igor M. arXiv https://doi.org/10.48550/arxiv.1405.4469	text	January 2014
Protein-based Nanotechnology: Kinesin–Microtubule-driven Systems for Bioanalytical Applications Hancock, William O. Nanotechnologies for the Life Sciences https://doi.org/10.1002/9783527610419.ntls0042	book	August 2007
Integration of Photoswitchable Proteins, Photosynthetic Reaction Centers and Semiconductor/Biomolecule Hybrids with Electrode Supports for Optobioelectronic Applications Wang, Fuan; Liu, Xiaoqing; Willner, Itamar Advanced Materials, Vol. 25, Issue 3 https://doi.org/10.1002/adma.201201772	journal	August 2012
Analysis of Microtubule Curvature Bicek, Andrew D.; Tüzel, Erkan; Kroll, Daniel M. Methods in Cell Biology https://doi.org/10.1016/S0091-679X(07)83010-X	book	January 2007
Nanotechnology: convergence with modern biology and medicine Roco, Mihail C. Current Opinion in Biotechnology, Vol. 14, Issue 3 https://doi.org/10.1016/S0958-1669(03)00068-5	journal	June 2003
How does taxol stabilize microtubules? Arnal, Isabelle; Wade, Richard H. Current Biology, Vol. 5, Issue 8 https://doi.org/10.1016/S0960-9822(95)00180-1	journal	August 1995
Protein damage, repair and proteolysis Chondrogianni, Niki; Petropoulos, Isabelle; Grimm, Stefanie Molecular Aspects of Medicine, Vol. 35 https://doi.org/10.1016/j.mam.2012.09.001	journal	February 2014
Observing the Mushroom-to-Brush Transition for Kinesin Proteins Dumont, Emmanuel L. P.; Belmas, Herve; Hess, Henry Langmuir, Vol. 29, Issue 49 https://doi.org/10.1021/la4030712	journal	November 2013
Controlling self-assembly of microtubule spools via kinesin motor density Lam, A. T.; Curschellas, C.; Krovvidi, D. Soft Matter, Vol. 10, Issue 43 https://doi.org/10.1039/C4SM01518E	journal	January 2014
Why Microtubules Run in Circles: Mechanical Hysteresis of the Tubulin Lattice Ziebert, Falko; Mohrbach, Hervé; Kulić, Igor M. Physical Review Letters, Vol. 114, Issue 14 https://doi.org/10.1103/PhysRevLett.114.148101	journal	April 2015
The bending of sliding microtubules imaged by confocal light microscopy and negative stain electron microscopy Amos, L. A.; Amos, W. B. Journal of Cell Science, Vol. 1991, Issue Supplement 14 https://doi.org/10.1242/jcs.1991.Supplement_14.20	journal	January 1991

Cited By (8)

High-Resolution Imaging of a Single Gliding Protofilament of Tubulins by HS-AFM Keya, Jakia Jannat; Inoue, Daisuke; Suzuki, Yuki Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-06249-1	journal	July 2017
USP21 modulates Goosecoid function through deubiquitination Liu, Fuwei; Fu, Qian; Li, Yunpeng Bioscience Reports, Vol. 39, Issue 7 https://doi.org/10.1042/bsr20182148	journal	July 2019
Microtubules: From understanding their dynamics to using them as potential therapeutic targets Ilan, Yaron Journal of Cellular Physiology, Vol. 234, Issue 6 https://doi.org/10.1002/jcp.27978	journal	November 2018
Curvature-Sensitive Kinesin Binding Can Explain Microtubule Ring Formation and Reveals Chaotic Dynamics in a Mathematical Model Pearce, Simon P.; Heil, Matthias; Jensen, Oliver E. Bulletin of Mathematical Biology, Vol. 80, Issue 11 https://doi.org/10.1007/s11538-018-0505-4	journal	September 2018
Kinesin expands and stabilizes the GDP-microtubule lattice Peet, Daniel R.; Burroughs, Nigel J.; Cross, Robert A. Nature Nanotechnology, Vol. 13, Issue 5 https://doi.org/10.1038/s41565-018-0084-4	journal	March 2018
Non-equilibrium assembly of microtubules: from molecules to autonomous chemical robots Hess, H.; Ross, Jennifer L. Chemical Society Reviews, Vol. 46, Issue 18 https://doi.org/10.1039/c7cs00030h	journal	January 2017
The model of local axon homeostasis - explaining the role and regulation of microtubule bundles in axon maintenance and pathology Hahn, Ines; Voelzmann, André; Liew, Yu-Ting Neural Development, Vol. 14, Issue 1 https://doi.org/10.1186/s13064-019-0134-0	journal	November 2019
Curvature-sensitive kinesin binding can explain microtubule ring formation and reveals chaotic dynamics in a mathematical model Pearce, Simon P.; Heil, Matthias; Jensen, Oliver E. arXiv https://doi.org/10.48550/arxiv.1803.07312	preprint	January 2018

Similar Records

Characterizing the Number of Kinesin Motors Bound to Microtubules in the Gliding Motility Assay Using FLIC Microscopy [Book Chapter]

Journal Article · Wed Apr 27 20:00:00 EDT 2022 · Methods in Molecular Biology · OSTI ID:1883173

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Mechanical splitting of microtubules into protofilament bundles by surface-bound kinesin-1

Citation Formats

References (39)

Cited By (8)

Similar Records

Related Subjects