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.
The heterotrimeric motor protein, kinesin-II, and its presumptive cargo, can be observed moving anterogradely at 0.7 microm/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 approximately 1.1 microm/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.
Signor
D
D
Section of Molecular and Cellular Biology, University of California Davis, Davis, California 95616, USA.
Wedaman
K P
KP
Orozco
J T
JT
Dwyer
N D
ND
Bargmann
C I
CI
Rose
L S
LS
Scholey
J M
JM
D000818:Animals; D030801:Animals, Genetically Modified; D001370:Axonal Transport; D017173:Caenorhabditis elegans / Q000235:genetics / Q000378:metabolism*; D029742:Caenorhabditis elegans Proteins; D002135:Calcium-Binding Proteins / Q000378:metabolism*; D002923:Cilia / Q000378:metabolism*; D003712:Dendrites / Q000378:metabolism*; D004398:Dyneins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D005407:Flagella / Q000378:metabolism; D017238:Genes, Helminth / Q000235:genetics / Q000502:physiology; D015801:Helminth Proteins / Q000235:genetics / Q000378:metabolism; D016547:Kinesins; D007700:Kinetics; D008856:Microscopy, Fluorescence; D020409:Molecular Motor Proteins / Q000378:metabolism; D008969:Molecular Sequence Data; D009124:Muscle Proteins / Q000378:metabolism*; D009154:Mutation / Q000235:genetics; D009475:Neurons, Afferent / Q000166:cytology / Q000378:metabolism*; D009479:Neuropeptides / Q000235:genetics / Q000378:metabolism; D010641:Phenotype; D011993:Recombinant Fusion Proteins / Q000235:genetics / Q000378:metabolism
D029742:Caenorhabditis elegans Proteins; D002135:Calcium-Binding Proteins; D015801:Helminth Proteins; D020409:Molecular Motor Proteins; D009124:Muscle Proteins; D009479:Neuropeptides; C400274:OSM-1 protein, C elegans; C111073:Osm-6 protein, C elegans; D011993:Recombinant Fusion Proteins; C074152:kinesin-II; D004398:Dyneins; D016547:Kinesins