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The types and numbers of kinesins and dyneins transporting endocytic cargoes modulate their motility and response to tau

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Beaudet, Daniel, Berger, Christopher L., Hendricks, Adam G.·2024·Journal of Biological Chemistry
DOI 10.1016/j.jbc.2024.107323PMC PMC11130734
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Abstract

Organelles and vesicular cargoes are transported by teams of kinesin and dynein motors along microtubules. We isolated endocytic organelles from cells at different stages of maturation and reconstituted their motility along microtubules in vitro. We asked how the sets of motors transporting a cargo determine its motility and response to the microtubule-associated protein tau. Here, we find that phagosomes move in both directions along microtubules, but the directional bias changes during maturation. Early phagosomes exhibit retrograde-biased transport while late phagosomes are directionally unbiased. Correspondingly, early and late phagosomes are bound by different numbers and combinations of kinesins-1, -2, -3, and dynein. Tau stabilizes microtubules and directs transport within neurons. While single-molecule studies show that tau differentially regulates the motility of kinesins and dynein in vitro, less is known about its role in modulating the trafficking of endogenous cargoes transported by their native teams of motors. Previous studies showed that tau preferentially inhibits kinesin motors, which biases late phagosome transport towards the microtubule minus-end. Here, we show that tau strongly inhibits long-range, dynein-mediated motility of early phagosomes. Tau reduces forces generated by teams of dynein motors on early phagosomes and accelerates dynein unbinding under load. Thus, cargoes differentially respond to tau, where dynein complexes on early phagosomes are more sensitive to tau inhibition than those on late phagosomes. Mathematical modeling further explains how small changes in the number of kinesins and dynein on cargoes impact the net directionality but also that cargoes with different sets of motors respond differently to tau.

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  • Kinesin-1 and kinesin-3 are major drivers of anterograde transport in axons, trafficking endosomes, lysosomes, mRNA, and other cargoes.

    “Kinesin-1 and kinesin-3 are major drivers of anterograde transport in axons, trafficking endosomes, lysosomes, mRNA, and other cargoes (Jenkins et al., 2012; Beaudet et al., 2024; Nagpal et al., 2024).”

    From Tau hyperphosphorylation impairs cooperative binding to microtubules and perturbs organelle trafficking in neurons (2026) · cites this paper as Beaudet et al., 2024

    The paper’s introductory passage (indexed under Abstract; page unavailable) identifies kinesin-1 and kinesin-3 among the principal motors driving anterograde transport and associates them with endosomes and lysosomes. It does not establish the full claim about transport of those cargoes specifically in axons or mention mRNA as a cargo in that passage. (LLM, conf=0.87)

    Experimental — accuracy not yet measured

  • Our results are consistent with a tug-of-war mechanism, in which tau acts as a selective barrier that preferentially inhibits kinesins-1 and -3, thereby shifting the balance toward dynein-driven transport.

    “Our results are consistent with a tug-of-war mechanism, in which tau acts as a selective barrier that preferentially inhibits kinesins-1 and -3, thereby shifting the balance toward dynein-driven transport”

    From Tau hyperphosphorylation impairs cooperative binding to microtubules and perturbs organelle trafficking in neurons (2026) · cites this paper as Beaudet et al., 2024

    The paper describes tau as a selective barrier and says kinesins-1 and -3 are more sensitive to it than dynein (background passage; page unavailable). The Results report minus-end–biased transport for bidirectional cargoes, consistent with a shift toward dynein, but also strong inhibition of retrograde cargoes. The claim omits this cargo-dependent qualification and implies a general shift toward dynein-driven transport. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • Endogenous cargo transport involves organelle-specific motor-adaptor complexes containing multiple redundant motor types and variable copy numbers.

    “endogenous cargo transport involves organelle-specific motor-adaptor complexes containing multiple redundant motor types and variable copy numbers”

    From Tau hyperphosphorylation impairs cooperative binding to microtubules and perturbs organelle trafficking in neurons (2026) · cites this paper as Beaudet et al., 2024

    The Results section (‘EPs and LPs move differently and are transported by different sets of motors’; page unavailable) documents multiple motor types and varying numbers of motors on phagosomes. The Discussion section (‘What determines if a cargo moves unidirectionally or bidirectionally?’; page unavailable) describes cargo-specific adaptor–motor complexes. The paper does not establish that the motor types are functionally redundant; it describes differences in their roles and effects on transport. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • The transport effects of tau hyperphosphorylation are determined not only by changes in tau-motor interactions but also by cargo-specific motor compositions and their differential sensitivities to tau.

    “the transport effects of tau hyperphosphorylation are determined not only by changes in tau-motor interactions but also by cargo-specific motor compositions and their differential sensitivities to tau”

    From Tau hyperphosphorylation impairs cooperative binding to microtubules and perturbs organelle trafficking in neurons (2026) · cites this paper as Beaudet et al., 2024

    The Results and Discussion (page unavailable) show that cargoes carry different sets of motors and respond differently to tau. The Discussion predicts that posttranslational changes to tau could have cargo-specific transport effects, but the paper does not establish effects of tau hyperphosphorylation specifically or attribute them to changed tau–motor interactions. (LLM, conf=0.87)

    Experimental — accuracy not yet measured

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Authors
Beaudet, D., Berger, C. L., & Hendricks, A. G.
Affiliations
  • McGill University (CA)
  • University of Vermont (US)
Corresponding author
Hendricks, Adam G.
ORCID
Venue
Journal of Biological Chemistry
Publisher
Elsevier BV
Published
2024-06
Volume
300
Issue
6
Pages
107323
ISSN
0021-9258 (ISSN-L)
DOI
10.1016/j.jbc.2024.107323
PMC
PMC11130734
OpenAlex
W4395449360
Cited by
15
References
5
Citations by year
2026: 9 · 2025: 5 · 2024: 1
FWCI
3.18
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Biological Chemistry (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • National Institutes of Health
  • National Institute of General Medical Sciences (R01GM132646)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
  • Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
Keywords
tau protein, kinesin, dynein, microtubule motility, retrograde transport, phagosome maturation, microtubule stabilization, mathematical modeling of transport
MeSH terms
Animals, Biological Transport, Dyneins, Endocytosis, Humans, Microtubules, Phagosomes, Kinesins, tau Proteins, Mice

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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

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