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Non-specific cargo–filament interactions slow down motor-driven transport

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Abstract

Active, motor-based cargo transport is important for many cellular functions and cellular development. However, the cell interior is complex and crowded and could have many weak, non-specific interactions with the cargo being transported. To understand how cargo-environment interactions will affect single motor cargo transport and multi-motor cargo transport, we use an artificial quantum dot cargo bound with few (~ 1) to many (~ 5–10) motors allowed to move in a dense microtubule network. We find that kinesin-driven quantum dot cargo is slower than single kinesin-1 motors. Excitingly, there is some recovery of the speed when multiple motors are attached to the cargo. To determine the possible mechanisms of both the slow down and recovery of speed, we have developed a computational model that explicitly incorporates multi-motor cargos interacting non-specifically with nearby microtubules, including, and predominantly with the microtubule on which the cargo is being transported. Our model has recovered the experimentally measured average cargo speed distribution for cargo-motor configurations with few and many motors, implying that numerous, weak, non-specific interactions can slow down cargo transport and multiple motors can reduce these interactions thereby increasing velocity.

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Data availability

Data sets generated during the current study are available from the corresponding authors on reasonable request.

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Acknowledgements

The work presented here was partially supported by National Science Foundation grant PRFB# 1611801 to JAL and NSF INSPIRE Award #1344203 to JLR. JLR was also partially supported by a grant from the Mathers Foundation. RKC was supported by a grant from the Mathers Foundation and Moore Foundation grant # 4308.1.AG and DQ acknowledge support from the National Science Foundation (NSF-DMS-1616926 to AG) and NSF-CREST: Center for Cellular and Biomolecular Machines at UC Merced (NSF-HRD-1547848 and NSF-HRD-2112675 to AG). AG also acknowledges support from the NSF Center for Engineering Mechanobiology grant CMMI-1548571. AG would also like to acknowledge the hospitality of the Aspen Center for Physics, which is supported by National Science Foundation grant PHY-1607611, where some of this work was done.

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Author notes

  1. Joelle A. Labastide and David A. Quint have contributed equally to this work.

Authors and Affiliations

  1. Department of Physics, University of Massachusetts, 710 North Pleasant Street, Amherst, MA, 01003-9337, USA

    Joelle A. Labastide, Reilly K. Cullen & Jennifer L. Ross

  2. Department of Physics, University of California, Merced, 5200 North Lake Rd, Merced, CA, 95343, USA

    David A. Quint, Bryan Maelfeyt & Ajay Gopinathan

  3. NSF-CREST: Center for Cellular and Biomolecular Machines (CCBM), University of California Merced, Merced, USA

    David A. Quint, Bryan Maelfeyt & Ajay Gopinathan

  4. Division of Basic and Translational Biophysics, Eunice Kennedy Shriver National Institute of Child Health and Human Development, NIH, Bethesda, MD, USA

    Reilly K. Cullen

  5. Department of Physics, Syracuse University, Crouse Drive, Syracuse, NY 13104, USA

    Jennifer L. Ross

  6. Lawrence Livermore National Laboratory, Livermore, CA, 94550, USA

    David A. Quint

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Contributions

JAL conceived and designed the work, performed data acquisition, analysis, and interpretation of data, drafted and edited the manuscript, and is accountable for the work. DAQ conceived and designed the work, performed simulations and theoretical calculations, analyzed and interpreted data, drafted and edited the manuscript, and is accountable for the work. JAL and DAQ contributed equally to the work. RKC helped with data acquisition, analysis, and interpretation of data. BM helped with data analysis and interpretation of data. AG conceived and designed the simulation work, analyzed and interpreted data, drafted and edited the manuscript, and is accountable for the work. JLR conceived and designed the experimental work, analyzed and interpreted data, drafted and edited the manuscript, and is accountable for the work.

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Correspondence to Jennifer L. Ross or Ajay Gopinathan.

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Labastide, J.A., Quint, D.A., Cullen, R.K. et al. Non-specific cargo–filament interactions slow down motor-driven transport. Eur. Phys. J. E 46, 134 (2023). https://doi.org/10.1140/epje/s10189-023-00394-4

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