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Glutamatergic modulation of synaptic-like vesicle recycling in mechanosensory lanceolate nerve terminals of mammalian hair follicles

Banks, Robert W.; Cahusac, Peter M.B.; Graca, Anna; Kain, Nakul; Shenton, Fiona; Singh, Paramjeet; Nj°a, Arild; Simon, Anna; Watson, Sonia; Slater, Clarke R.; Bewick, Guy S.

Glutamatergic modulation of synaptic-like vesicle recycling in mechanosensory lanceolate nerve terminals of mammalian hair follicles Thumbnail


Authors

Peter M.B. Cahusac

Anna Graca

Nakul Kain

Fiona Shenton

Paramjeet Singh

Arild Nj°a

Anna Simon

Sonia Watson

Clarke R. Slater

Guy S. Bewick



Abstract

Our aim in the present study was to determine whether a glutamatergic modulatory system involving synaptic-like vesicles (SLVs) is present in the lanceolate ending of the mouse and rat hair follicle and, if so, to assess its similarity to that of the rat muscle spindle annulospiral ending we have described previously. Both types of endings are formed by the peripheral sensory terminals of primary mechanosensory dorsal root ganglion cells, so the presence of such a system in the lanceolate ending would provide support for our hypothesis that it is a general property of fundamental importance to the regulation of the responsiveness of the broad class of primary mechanosensory endings. We show not only that an SLV-based system is present in lanceolate endings, but also that there are clear parallels between its operation in the two types of mechanosensory endings. In particular, we demonstrate that, as in the muscle spindle: (i) FM1-43 labels the sensory terminals of the lanceolate ending, rather than the closely associated accessory (glial) cells; (ii) the dye enters and leaves the terminals primarily by SLV recycling; (iii) the dye does not block the electrical response to mechanical stimulation, in contrast to its effect on the hair cell and dorsal root ganglion cells in culture; (iv) SLV recycling is Ca2+ sensitive; and (v) the sensory terminals are enriched in glutamate. Thus, in the lanceolate sensory ending SLV recycling is itself regulated, at least in part, by glutamate acting through a phospholipase D-coupled metabotropic glutamate receptor.

Citation

Banks, R. W., Cahusac, P. M., Graca, A., Kain, N., Shenton, F., Singh, P., …Bewick, G. S. (2013). Glutamatergic modulation of synaptic-like vesicle recycling in mechanosensory lanceolate nerve terminals of mammalian hair follicles. The Journal of Physiology, 591(10), 2523-2540. https://doi.org/10.1113/jphysiol.2012.243659

Journal Article Type Article
Publication Date May 1, 2013
Deposit Date May 20, 2013
Publicly Available Date Mar 29, 2024
Journal Journal of Physiology
Print ISSN 0022-3751
Electronic ISSN 1469-7793
Publisher Wiley
Peer Reviewed Peer Reviewed
Volume 591
Issue 10
Pages 2523-2540
DOI https://doi.org/10.1113/jphysiol.2012.243659

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