Role of a class DHC1b dynein in retrograde transport of IFT motors and IFT raft particles along cilia, but not dendrites, in chemosensory neurons of living Caenorhabditis elegans

Dawn Signor, Karen P. Wedatman, Jose T. Orozco, Noelle D. Dwyer, Cornelia I. Bargmann, Lesilee S. Rose, Jonathan M. Scholey

Research output: Contribution to journalArticle

209 Citations (Scopus)

Abstract

The heterotrimeric motor protein, kinesin-II, and its presumptive cargo, can be observed moving anterogradely at 0.7 μm/s by intraflagellar transport (IFT) within sensory cilia of chemosensory neurons of living Caenorhabditis elegans, using a fluorescence microscope-based transport assay (Orozco, J.T, K.P. Wedaman, D. Signor, H. Brown, L. Rose, and J.M. Scholey. 1999. Nature. 398:674). Here, we report that kinesin-II, and two of its presumptive cargo molecules, OSM-1 and OSM-6, all move at ~1.1 μm/s in the retrograde direction along cilia and dendrites, which is consistent with the hypothesis that these proteins are retrieved from the distal endings of the cilia by a retrograde transport pathway that moves them along cilia and then dendrites, back to the neuronal cell body. To test the hypothesis that the minus end- directed microtubule motor protein, cytoplasmic dynein, drives this retrograde transport pathway, we visualized movement of kinesin-II and its cargo along dendrites and cilia in a che-3 cytoplasmic dynein mutant background, and observed an inhibition of retrograde transport in cilia but not in dendrites. In contrast, anterograde IFT proceeds normally in che-3 mutants. Thus, we propose that the class DHC1b cytoplasmic dynein, CHE-3, is specifically responsible for the retrograde transport of the anterograde motor, kinesin-II, and its cargo within sensory cilia, but not within dendrites.

Original languageEnglish (US)
Pages (from-to)519-530
Number of pages12
JournalJournal of Cell Biology
Volume147
Issue number3
DOIs
StatePublished - Nov 1 1999

Fingerprint

Dyneins
Cilia
Caenorhabditis elegans
Dendrites
Neurons
Cytoplasmic Dyneins
Microtubule Proteins
Proteins
Fluorescence
kinesin-II

Keywords

  • Caenorhabditis elegans
  • Dynein
  • Intraflagellar transport
  • Kinesin
  • Neuron transport

ASJC Scopus subject areas

  • Cell Biology

Cite this

Role of a class DHC1b dynein in retrograde transport of IFT motors and IFT raft particles along cilia, but not dendrites, in chemosensory neurons of living Caenorhabditis elegans. / Signor, Dawn; Wedatman, Karen P.; Orozco, Jose T.; Dwyer, Noelle D.; Bargmann, Cornelia I.; Rose, Lesilee S.; Scholey, Jonathan M.

In: Journal of Cell Biology, Vol. 147, No. 3, 01.11.1999, p. 519-530.

Research output: Contribution to journalArticle

Signor, Dawn ; Wedatman, Karen P. ; Orozco, Jose T. ; Dwyer, Noelle D. ; Bargmann, Cornelia I. ; Rose, Lesilee S. ; Scholey, Jonathan M. / Role of a class DHC1b dynein in retrograde transport of IFT motors and IFT raft particles along cilia, but not dendrites, in chemosensory neurons of living Caenorhabditis elegans. In: Journal of Cell Biology. 1999 ; Vol. 147, No. 3. pp. 519-530.
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AU - Signor, Dawn

AU - Wedatman, Karen P.

AU - Orozco, Jose T.

AU - Dwyer, Noelle D.

AU - Bargmann, Cornelia I.

AU - Rose, Lesilee S.

AU - Scholey, Jonathan M.

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AB - The heterotrimeric motor protein, kinesin-II, and its presumptive cargo, can be observed moving anterogradely at 0.7 μm/s by intraflagellar transport (IFT) within sensory cilia of chemosensory neurons of living Caenorhabditis elegans, using a fluorescence microscope-based transport assay (Orozco, J.T, K.P. Wedaman, D. Signor, H. Brown, L. Rose, and J.M. Scholey. 1999. Nature. 398:674). Here, we report that kinesin-II, and two of its presumptive cargo molecules, OSM-1 and OSM-6, all move at ~1.1 μm/s in the retrograde direction along cilia and dendrites, which is consistent with the hypothesis that these proteins are retrieved from the distal endings of the cilia by a retrograde transport pathway that moves them along cilia and then dendrites, back to the neuronal cell body. To test the hypothesis that the minus end- directed microtubule motor protein, cytoplasmic dynein, drives this retrograde transport pathway, we visualized movement of kinesin-II and its cargo along dendrites and cilia in a che-3 cytoplasmic dynein mutant background, and observed an inhibition of retrograde transport in cilia but not in dendrites. In contrast, anterograde IFT proceeds normally in che-3 mutants. Thus, we propose that the class DHC1b cytoplasmic dynein, CHE-3, is specifically responsible for the retrograde transport of the anterograde motor, kinesin-II, and its cargo within sensory cilia, but not within dendrites.

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