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

doi:10.1083/jcb.147.3.519

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© The Rockefeller University Press, 0021-9525/1999//519 $5.00
The Journal of Cell Biology, Volume 147, Number 3, , 1999 519-530

Original Article

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^a, Karen P. Wedaman^a, Jose T. Orozco^a, Noelle D. Dwyer^b, Cornelia I. Bargmann^b, Lesilee S. Rose^a, and Jonathan M. Scholey^a

^a Section of Molecular and Cellular Biology, University of California Davis, Davis, California 95616
^b Department of Anatomy, Howard Hughes Medical Institute, University of California, San Francisco, San Francisco, California 94143
Section of Molecular and Cellular Biology, 1 Shields Avenue, University of California, Davis, Davis, CA 95616.(530) 752-7522(530) 752-2271

jmscholey{at}ucdavis.edu

The heterotrimeric motor protein, kinesin-II, and its presumptivecargo, can be observed moving anterogradely at 0.7 µm/sby intraflagellar transport (IFT) within sensory cilia of chemosensoryneurons of living Caenorhabditis elegans, using a fluorescencemicroscope–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 presumptivecargo molecules, OSM-1 and OSM-6, all move at $~$ 1.1 µm/sin the retrograde direction along cilia and dendrites, whichis consistent with the hypothesis that these proteins are retrievedfrom the distal endings of the cilia by a retrograde transportpathway that moves them along cilia and then dendrites, backto the neuronal cell body. To test the hypothesis that the minusend–directed microtubule motor protein, cytoplasmic dynein,drives this retrograde transport pathway, we visualized movementof kinesin-II and its cargo along dendrites and cilia in a che-3cytoplasmic dynein mutant background, and observed an inhibitionof retrograde transport in cilia but not in dendrites. In contrast,anterograde IFT proceeds normally in che-3 mutants. Thus, wepropose that the class DHC1b cytoplasmic dynein, CHE-3, is specificallyresponsible for the retrograde transport of the anterogrademotor, kinesin-II, and its cargo within sensory cilia, but notwithin dendrites.

Key Words: dynein • kinesin • intraflagellar transport • Caenorhabditis elegans • neuron transport

1.used in this paper: DHC, dynein heavy chain; IFT, intraflagellartransport; KAP, kinesin-II accessory polypeptide; ORF, openreading frame

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