Summary
The sense of touch is conferred by the conjoint function of somatosensory neurons and skin cells. These cells meet across a gap filled by a basal lamina, an ancient structure found in metazoans. Using Caenorhabditis elegans, we show that membrane-matrix complexes containing laminin, nidogen, and the MEC-4 mechano-electrical transduction channel reside at this interface and are instrumental for proper touch sensation. These complexes fail to coalesce in touch-insensitive extracellular matrix mutants and in dissociated neurons. MEC-4, but not laminin or nidogen, is destabilized by point mutations in the C-terminal Kunitz domain of the extracellular matrix component, MEC-1. Thus, neuron-epithelial cell interfaces are instrumental in mechanosensory complex assembly and function. Loss of nidogen reduces the density of mechanoreceptor complexes and the amplitude of the touch-evoked currents they carry. These findings imply that somatosensory neurons secrete proteins that actively repurpose the basal lamina to generate special-purpose mechanosensory complexes responsible for vibrotactile sensing.
Competing Interest Statement
The authors have declared no competing interest.
Footnotes
In addition to extensive edits to the text, this revision includes new data and new analyses. New data: TEM datastacks showing the ultrastructure of the TRN-associated ECM, LAM-1 distribution, effect of epi-1(gm57) and lam-3(ok2030) on MEC-4 puncta distribution. This revision omits an FEM model that was present in the initial version. The revision also includes rigorous statistical analysis of how mutation affects the distribution of MEC-4 channels, NID-1 nidogen, and LAM-2/3 laminins. It opens with a new diagram showing the position of TRNs in the nematode body and concludies with a new diagram summarizing a model synthesizing the experimental findings.