The DOI matches its Crossref record; 38 of the 38 references it cites were found in a registry or an index.
Tug-of-war between dissimilar teams of microtubule motors regulates transport and fission of endosomes
Open accessAbstract
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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“Support for this model includes studies of neuronal vesicles (Hendricks et al., 2010) and endosomes (Soppina et al., 2009).”
From Microtubule motors transport phagosomes in the RPE, and lack of KLC1 leads to AMD-like pathogenesis (2015) · cites this paper as Soppina et al., 2009
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Cites
The Molecular Motor Toolbox for Intracellular Transport
Vale, R. D. (2003) · Cell · doi:10.1016/s0092-8674(03)00111-9 · Cited by 1,982
Dynactin increases the processivity of the cytoplasmic dynein motor
King, S. J., & Schroer, T. A. (1999) · Nature Cell Biology · doi:10.1038/71338 · Cited by 661
Bidirectional transport along microtubules
Welte, M. A. (2004) · Current Biology · doi:10.1016/j.cub.2004.06.045 · Cited by 577
Tug-of-war as a cooperative mechanism for bidirectional cargo transport by molecular motors
Müller, M. J. I., Klumpp, S., & Lipowsky, R. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0706825105 · Cited by 521
Cytoplasmic dynein functions as a gear in response to load
Mallik, R., Carter, B. C., Lex, S. A., King, S. J., & Gross, S. P. (2004) · Nature · doi:10.1038/nature02293 · Cited by 494
Self-citationPowering membrane traffic in endocytosis and recycling
Soldati, T., & Schliwa, M. (2006) · Nature reviews. Molecular cell biology · doi:10.1038/nrm2060 · Cited by 378
Force-Induced Bidirectional Stepping of Cytoplasmic Dynein
Gennerich, A., Carter, A. P., Reck‐Peterson, S. L., & Vale, R. D. (2007) · Cell · doi:10.1016/j.cell.2007.10.016 · Cited by 376
Molecular motors: strategies to get along.
Mallik, R., & Gross, S. (2004) · Current Biology · doi:10.1016/j.cub.2004.10.046 · Cited by 344
Self-citationKlopfenstein, D. R., Tomishige, M., Stuurman, N., & Vale, R. D. (2002) · Cell · doi:10.1016/s0092-8674(02)00708-0 · Cited by 327
Conversion of Unc104/KIF1A Kinesin into a Processive Motor After Dimerization
Tomishige, M., Klopfenstein, D. R., & Vale, R. D. (2002) · Science · doi:10.1126/science.1073386 · Cited by 296
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Huotari, J., & Helenius, A. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.286 · Cited by 2,448
Axonal transport: cargo-specific mechanisms of motility and regulation
Maday, S., Twelvetrees, A. E., Moughamian, A. J., & Holzbaur, E. L. F. (2014) · Neuron · doi:10.1016/j.neuron.2014.10.019 · Cited by 683
Stochastic models of intracellular transport
Bressloff, P. C., & Newby, J. (2013) · Reviews of Modern Physics · doi:10.1103/revmodphys.85.135 · Cited by 637
Tug-of-War in Motor Protein Ensembles Revealed with a Programmable DNA Origami Scaffold
Derr, N. D., Goodman, B. S., Jungmann, R., Leschziner, A. E., Shih, W. M., & Reck‐Peterson, S. L. (2012) · Science · doi:10.1126/science.1226734 · Cited by 434
Bidirectional cargo transport: moving beyond tug of war
Hancock, W. O. (2014) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3853 · Cited by 447
Metadata
- Authors
- Soppina, V., Rai, A. K., Ramaiya, A. J., Barak, P., & Mallik, R.
- Affiliations
- Tata Institute of Fundamental Research (IN)
- 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
- 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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