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Cited by 106Microtubule and mitosis dynamicsCellular Mechanics and InteractionsCancer Treatment and Pharmacology

Kinesin expands and stabilizes the GDP-microtubule lattice

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Peet, Daniel R., Burroughs, Nigel J., Cross, Robert A.·2018·Nature Nanotechnology
DOI 10.1038/s41565-018-0084-4PMC PMC5937683

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Abstract

Kinesin-1 is a nanoscale molecular motor that walks towards the fast-growing (plus) ends of microtubules, hauling molecular cargo to specific reaction sites in cells. Kinesin-driven transport is central to the self-organization of eukaryotic cells and shows great promise as a tool for nano-engineering 1 . Recent work hints that kinesin may also play a role in modulating the stability of its microtubule track, both in vitro 2,3 and in vivo 4 , but the results are conflicting 5-7 and the mechanisms are unclear. Here, we report a new dimension to the kinesin-microtubule interaction, whereby strong-binding state (adenosine triphosphate (ATP)-bound and apo) kinesin-1 motor domains inhibit the shrinkage of guanosine diphosphate (GDP) microtubules by up to two orders of magnitude and expand their lattice spacing by ~1.6%. Our data reveal an unexpected mechanism by which the mechanochemical cycles of kinesin and tubulin interlock, and so allow motile kinesins to influence the structure, stability and mechanics of their microtubule track.

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  • Various microtubule-binding proteins have higher affinities for expanded or compacted lattices in vitro and can induce lattice expansion or compaction, respectively.

    “various microtubule-binding proteins have higher affinities for expanded or compacted lattices in vitro and can also induce lattice expansion or compaction, respectively (Ferro et al., 2022; Guedes-Dias et al., 2019; Peet et al., 2018; Shima et al., 2018; Watanabe et al., 2020; Zhang et al., 2017)”

    From StableMARK-decorated microtubules in cells have expanded lattices (2025) · cites this paper as Peet et al., 2018

  • In vitro, at high concentrations in the no-nucleotide state, the kinesin-1 motor domain can extend microtubule lattice spacing, suggesting it prefers to bind to the expanded lattice conformation at lower concentrations.

    “Third, in vitro experiments have revealed that at high concentrations in the no-nucleotide state, the kinesin-1 motor domain can extend MT lattice spacing, suggesting that it prefers to bind to this expanded MT lattice conformation at lower concentrations (Peet et al., 2018; Shima et al., 2018).”

    From A live-cell marker to visualize the dynamics of stable microtubules throughout the cell cycle (2023) · cites this paper as Peet et al., 2018

  • Kinesin binding expands the microtubule lattice, suggesting that exclusive binding may arise from competition for an expanded versus compacted lattice.

    “Apart from steric clashes between tau and kinesin9,41, kinesin binding expands the microtubule lattice4,6 suggesting that exclusive binding may arise from competition for an expanded versus compacted lattice.”

    From Microtubule lattice spacing governs cohesive envelope formation of tau family proteins (2022) · cites this paper as [4]

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Research works printed but not linked: 26

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  18. [18]Arora K KIF14 binds tightly to microtubules and adopts a rigor-like conformation J Mol Biol 2014 426 2997 3015 24949858
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Authors
Peet, D. R., Burroughs, N. J., & Cross, R. A.
Affiliations
University of Warwick (GB)
Corresponding author
Cross, Robert A.
ORCID
Venue
Nature Nanotechnology
Publisher
Springer Science and Business Media LLC
Published
2018-03-12
Volume
13
Issue
5
Pages
386-391
ISSN
  • 1748-3387 (ISSN-L)
  • 1748-3395
DOI
10.1038/s41565-018-0084-4
PMC
PMC5937683
OpenAlex
W2791508075
Cited by
106
References
3
Citations by year
2026: 17 · 2025: 10 · 2024: 15 · 2023: 16 · 2022: 13 · 2021: 12 · 2020: 10 · 2019: 10 · 2018: 3
FWCI
4.79
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Nanotechnology (publishedVersion)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • Warwick Research Archive Portal (University of Warwick) (acceptedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • Wellcome Trust (103895/Z/14/Z)
  • University of Warwick
  • Directorate for Biological Sciences
  • Biotechnology and Biological Sciences Research Council (BB/G530233/1)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
  • Health Sciences › Medicine › Oncology › Cancer Treatment and Pharmacology
Keywords
kinesin-1, microtubule lattice, microtubule stability, lattice spacing, mechanochemical cycle, tubulin, molecular motors, freight transport
MeSH terms
Adenylyl Imidodiphosphate, Animals, Guanosine Diphosphate, Microtubules, Swine, Kinesins, Amino Acid Substitution, Mutation, Missense

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