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

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

Research output: Contribution to journalArticle

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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 Ca 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.
Original languageEnglish
Pages (from-to)2523-2540
Number of pages18
JournalThe Journal of Physiology
Volume591
Issue number10
Early online date25 Feb 2013
DOIs
Publication statusPublished - 15 May 2013

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Hair Follicle
Synaptic Vesicles
Muscle Spindles
Spinal Ganglia
Glutamic Acid
Coloring Agents
Phospholipase D
Metabotropic Glutamate Receptors
Neuroglia
Cell Culture Techniques

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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; Njå, Arild; Simon, Anna; Watson, Sonia; Slater, Clarke R.; Bewick, Guy S.

In: The Journal of Physiology, Vol. 591, No. 10, 15.05.2013, p. 2523-2540.

Research output: Contribution to journalArticle

Banks, RW, Cahusac, PMB, Graca, A, Kain, N, Shenton, F, Singh, P, Njå, A, Simon, A, Watson, S, Slater, CR & Bewick, GS 2013, 'Glutamatergic modulation of synaptic-like vesicle recycling in mechanosensory lanceolate nerve terminals of mammalian hair follicles', The Journal of Physiology, vol. 591, no. 10, pp. 2523-2540. https://doi.org/10.1113/jphysiol.2012.243659
Banks, Robert W. ; Cahusac, Peter M.B. ; Graca, Anna ; Kain, Nakul ; Shenton, Fiona ; Singh, Paramjeet ; Njå, 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. In: The Journal of Physiology. 2013 ; Vol. 591, No. 10. pp. 2523-2540.
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