Journal of Neuroscience, Vol 13, 4254-4271, Copyright © 1993 by Society for Neuroscience
Axonal guidance defects in a Caenorhabditis elegans mutant reveal cell- extrinsic determinants of neuronal morphology
S Hekimi and D Kershaw
Department of Biology, McGill University, Montreal, Quebec, Canada.
Mutations in the gene unc-53 of Caenorhabditis elegans result in behavioral
and anatomical abnormalities. Immunocytochemistry and electron microscopy
revealed neuroanatomical defects in all main longitudinal nervous tracts.
Whole tracts were found to be misguided in specific ways suggesting that
unc-53 affects pioneering axons. The four lateral microtubule cells (LMs),
which are probably pioneering neurons, were examined in greatest detail. In
the mutants, the processes of the LMs leave their normal position on the
body wall and terminate prematurely. Examination of five unc-53 alleles for
penetrance and expressivity of these defects revealed a spatial restriction
in the requirement for unc-53. The morphology and positioning of the branch
of the posterior lateral microtubule cells (PLMs) were also examined. In
wild-type animals, the PLM branches lack the ultrastructural
specializations of the main process, which include large microtubules,
apposition to the cuticle, and a polarized extracellular matrix (the
mantle). Two differences were noted in unc-53 mutants. First, a majority of
PLMs branch at random and display an abnormally enlarged branching point
and branch cross section. The unusual branch morphologies correlate with
branch position, rather than PLM length. Second, the ectopic branches
display the specific ultrastructural features characteristic of the main
process. Furthermore, after entering the ventral nerve cord, the abnormal
branches constantly change position relative to the other processes and the
hypodermis, retaining their specialized microtubules throughout, but
displaying a mantle only when in direct contact with hypodermis. Taken
together, these observations suggest that the differentiated features of
the PLMs, including process length, branch position, intracellular branch
morphology, and surrounding extracellular matrix, are locally specified by
cell-extrinsic cues, some of which require unc-53.
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