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Cited by 365Microtubule and mitosis dynamicsHereditary Neurological DisordersCellular transport and secretion

Cytoplasmic dynein, the dynactin complex, and kinesin are interdependent and essential for fast axonal transport

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Martin, MaryAnn, Iyadurai, Stanley J., Gassman, Andrew, Gindhart, Joseph G., Hays, Thomas S., Saxton, William M.·1999·Molecular Biology of the Cell
DOI 10.1091/mbc.10.11.3717PMC PMC25669
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Abstract

In axons, organelles move away from (anterograde) and toward (retrograde) the cell body along microtubules. Previous studies have provided compelling evidence that conventional kinesin is a major motor for anterograde fast axonal transport. It is reasonable to expect that cytoplasmic dynein is a fast retrograde motor, but relatively few tests of dynein function have been reported with neurons of intact organisms. In extruded axoplasm, antibody disruption of kinesin or the dynactin complex (a dynein activator) inhibits both retrograde and anterograde transport. We have tested the functions of the cytoplasmic dynein heavy chain (cDhc64C) and the p150(Glued) (Glued) component of the dynactin complex with the use of genetic techniques in Drosophila. cDhc64C and Glued mutations disrupt fast organelle transport in both directions. The mutant phenotypes, larval posterior paralysis and axonal swellings filled with retrograde and anterograde cargoes, were similar to those caused by kinesin mutations. Why do specific disruptions of unidirectional motor systems cause bidirectional defects? Direct protein interactions of kinesin with dynein heavy chain and p150(Glued) were not detected. However, strong dominant genetic interactions between kinesin, dynein, and dynactin complex mutations in axonal transport were observed. The genetic interactions between kinesin and either Glued or cDhc64C mutations were stronger than those between Glued and cDhc64C mutations themselves. The shared bidirectional disruption phenotypes and the dominant genetic interactions demonstrate that cytoplasmic dynein, the dynactin complex, and conventional kinesin are interdependent in fast axonal transport.

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  • The data are consistent with a model for bidirectional coordination in which activities of Kinesin-1 and dynein might be linked via physical contacts, and point to a role of KLCs in this linkage.

    “Thus, our data is consistent with a model for bidirectional coordination in which activities of Kinesin-1 and dynein might be linked via physical contacts (Martin et al., 1999), and points to a role of KLCs in this linkage.”

    From Stable kinesin and dynein assemblies drive the axonal transport of mammalian prion protein vesicles (2011) · cites this paper as Martin et al., 1999

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Research works printed but not linked: 3

  1. [10]10. Flybase. A genome database. 1999. <http://flybase.bio.indiana.edu/> <http://flybase.bio.indiana.edu/>. . [[Google Scholar](https://scholar.google.com/scholar_lookup?title=A%20genome%20database.&publication_year=1999&)]
  2. [13]13. Gallagher S, Smith J. Electrophoretic separation of proteins. In: Ausubel F, Brent R, Kingston R, Moore D, Seidman J, Smith J, Struhl K, editors. Current Protocols in Molecular Biology. Boston, MA: Current Protocols; 1991. pp. 10.2.1–10.2.18. [[Google Scholar](https://scholar.google.com/scholar_lookup?title=Current%20Protocols%20in%20Molecular%20Biology&author=S%20Gallagher&author=J%20Smith&publication_year=1991&)]
  3. [43]43. Roberts D. Basic Drosophila care and techniques. In: Roberts D, editor. Drosophila: A Practical Approach. Oxford, UK: IRL Press; 1986. pp. 1–38. [[Google Scholar](https://scholar.google.com/scholar_lookup?title=Drosophila:%20A%20Practical%20Approach&author=D%20Roberts&publication_year=1986&)]

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Authors
Martin, M., Iyadurai, S. J., Gassman, A., Gindhart, J. G., Hays, T. S., & Saxton, W. M.
Affiliations
  • Indiana University Bloomington (US)
  • University of Minnesota (US)
  • University of Massachusetts Boston (US)
ORCID
Venue
Molecular Biology of the Cell
Publisher
American Society for Cell Biology (ASCB)
Published
1999-11
Volume
10
Issue
11
Pages
3717-3728
ISSN
  • 1059-1524 (ISSN-L)
  • 1939-4586
DOI
10.1091/mbc.10.11.3717
PMC
PMC25669
OpenAlex
W2144151547
Cited by
365
References
58
Citations by year
2026: 3 · 2025: 7 · 2024: 7 · 2023: 8 · 2022: 13 · 2021: 5 · 2020: 11 · 2019: 8 · 2018: 9 · 2017: 21 · 2016: 9 · 2015: 11 · 2014: 14 · 2013: 14 · 2012: 26
FWCI
3.90
Type
journal article
Language
en
Open access
Locations
  • Molecular Biology of the Cell (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • Howard Hughes Medical Institute
  • American Heart Association
  • National Institutes of Health
  • National Institute of General Medical Sciences (GM-44757, R01GM044757, R56GM044757, R01GM046295, GM-46295)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Hereditary Neurological Disorders
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
Keywords
cytoplasmic dynein, dynactin, kinesin, fast axonal transport, anterograde transport, retrograde transport, microtubule motor proteins, dynein heavy chain, p150Glued, axonal swellings, Drosophila neurons
MeSH terms
Dynactin Complex, Animals, Axons, Cytoplasm, Drosophila, Dyneins, Microscopy, Electron, Microtubule-Associated Proteins, Mutation, Phenotype, Precipitin Tests, Kinesins, Microscopy, Confocal, Microscopy, Video

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