Abstract
GROWTH cones in developing nervous systems encounter a sequence of extracellular cues during migration1,2. In theory, a growth cone can navigate by selectively expressing or activating surface receptor(s) that recognize extracellular cues appropriate to each migratory phase. Using the simple Caenorhabditis elegans nervous system, we attempted to demonstrate that path selection by migrating growth cones can be predictably altered by ectopic expression of a single receptor. The unc-5 gene of C. elegans encodes a unique receptor of the immunoglobulin superfamily (UNC-5), required cell-autonomously to guide growth cone and mesodermal cell migrations in a dorsal direction on the epidermis3,4. We report here that the UNC-5 receptor induces dorsally oriented axon trajectories when ectopically expressed in the touch receptor neurons which normally extend pioneer axons longitudinally or ventrally on the epidermis5. These errant trajectories depend on unc-6, which encodes a putative epidermal path cue6, just as normal dorsally oriented axon trajectories do (such as those of certain motor neurons4), suggesting that UNC-5 acts to reorient the touch cell growth cones by using its normal guidance mechanisms. These results support previous evidence that UNC-5 and UNC-6 play instructive rules in guiding growth cone migrations on the epidermis in C. elegans 4) and indicate that pioneering growth cones, which normally migrate in different directions, may use equivalent intracellular signalling mechanisms for guidance.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Dodd, J. & Jessell, T. M. Science 242, 692–699 (1988).
Harrelson, A. L. & Goodman, C. S. Science 242, 700–707 (1988).
Leung-Hagesteijn, C. et al. Cell 71, 289–299 (1992).
Hedgecock, E. M., Culotti, J. G. & Hall, D. H. Neuron 2, 61–85 (1990).
Chalfie, M. & Sulston, J. Devl Biol. 82, 358–370 (1981)
Ishii, N., Wadsworth, W. G., Stern, B. D., Culotti, J. G. & Hedgecock, E. M. Neuron 9, 873–881 (1992).
Hamelin, M., Scott, I. M., Way, J. C. & Culotti, J. G. EMBO J. 11, 2885–2893 (1992).
Mello, C. C., Kramer, J. M., Stinchcomb, D. & Ambros, V. EMBO J. 10, 3959–3970 (1991).
Sulston, J. E. & Horvitz, H. R. Devl Biol. 56, 110–156 (1977).
Sulston, J. E., Schierenberg, E., White, J. G. & Thomson, J. N. Devl Biol. 100, 64–119 (1983).
Hedgecock, E. M., Culotti, J. G., Hall, D. H. & Stern, B. D. Development 100, 365–382 (1987).
Brenner, S. Brit. Med. Bull. 29, 269–271 (1973).
White, J. G., Southgate, E., Thomson, J. N. & Brenner, S. Phil. Trans. R. Soc. B275, 327–348 (1976).
Kimble, J. & Hirsh, D. Devl Biol. 70, 396–417 (1979).
Fire, A., Harrison, S. W. & Dixon, D. D. Gene 93, 189–196 (1990).
Brenner, S. Genetics 77, 71–94 (1974).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Hamelin, M., Zhou, Y., Su, MW. et al. Expression of the UNC-5 guidance receptor in the touch neurons of C. elegans steers their axons dorsally. Nature 364, 327–330 (1993). https://doi.org/10.1038/364327a0
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/364327a0
This article is cited by
-
Unc5C and DCC act downstream of Ctip2 and Satb2 and contribute to corpus callosum formation
Nature Communications (2014)
-
Less than 5 Netrin-1 molecules initiate attraction but 200 Sema3A molecules are necessary for repulsion
Scientific Reports (2012)
-
UNC-6 and UNC-40 promote dendritic growth through PAR-4 in Caenorhabditis elegans neurons
Nature Neuroscience (2011)
-
UNC-129 regulates the balance between UNC-40 dependent and independent UNC-5 signaling pathways
Nature Neuroscience (2009)
-
Netrin signal transduction and the guanine nucleotide exchange factor DOCK180 in attractive signaling
Nature Neuroscience (2008)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.