Cited by 349Microtubule and mitosis dynamicsCellular transport and secretionCellular Mechanics and Interactions

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Tug-of-war between dissimilar teams of microtubule motors regulates transport and fission of endosomes

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Soppina, Virupakshi, Rai, Arpan Kumar, Ramaiya, Avin Jayesh, Barak, Pradeep, Mallik, Roop·2009·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.0906524106PMC PMC2770008

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Abstract

Intracellular transport is interspersed with frequent reversals in direction due to the presence of opposing kinesin and dynein motors on organelles that are carried as cargo. The cause and the mechanism of reversals are unknown, but are a key to understanding how cargos are delivered in a regulated manner to specific cellular locations. Unlike established single-motor biophysical assays, this problem requires understanding of the cooperative behavior of multiple interacting motors. Here we present measurements inside live Dictyostelium cells, in a cell extract and with purified motors to quantify such an ensemble function of motors. We show through precise motion analysis that reversals during endosome motion are caused by a tug-of-war between kinesin and dynein. Further, we use a combination of optical trap-based force measurements and Monte Carlo simulations to make the surprising discovery that endosome transport uses many (approximately four to eight) weak and detachment-prone dyneins in a tug-of-war against a single strong and tenacious kinesin. We elucidate how this clever choice of dissimilar motors and motor teams achieves net transport together with endosome fission, both of which are important in controlling the balance of endocytic sorting. To the best of our knowledge, this is a unique demonstration that dynein and kinesin function differently at the molecular level inside cells and of how this difference is used in a specific cellular process, namely endosome biogenesis. Our work may provide a platform to understand intracellular transport of a variety of organelles in terms of measurable quantities.

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Authors: Soppina, V., Rai, A. K., Ramaiya, A. J., Barak, P., & Mallik, R.
Affiliations: Tata Institute of Fundamental Research (IN)
ORCID: Soppina, Virupakshi
Rai, Arpan Kumar
Mallik, Roop
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2009-11-17
Volume: 106
Issue: 46
Pages: 19381-19386
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.0906524106
PMC: PMC2770008
OpenAlex: W2033859483
Cited by: 349
References: 38
Citations by year: 2026: 4 · 2025: 9 · 2024: 7 · 2023: 21 · 2022: 14 · 2021: 18 · 2020: 23 · 2019: 19 · 2018: 17 · 2017: 26 · 2016: 27 · 2015: 18 · 2014: 30 · 2013: 29 · 2012: 33
FWCI: 12.90
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Wellcome Trust (WT079214MA)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
Keywords: microtubule motor proteins, kinesin, dynein, intracellular transport, tug-of-war, Dictyostelium, optical trapping, Monte Carlo simulation, endocytic sorting
MeSH terms: Dictyostelium, Dyneins, Microspheres, Microtubules, Monte Carlo Method, Endosomes, Kinesins

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Tug-of-war between dissimilar teams of microtubule motors regulates transport and fission of endosomes

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