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Serotonin increases cilia-driven particle transport via an acetylcholine-independent pathway in the mouse trachea.

König P, Krain B, Krasteva G, Kummer W - PLoS ONE (2009)

Bottom Line: Classical neuromediators such as noradrenalin and acetylcholine increase ciliary beat frequency and thus cilia-driven transport.The increase in particle transport speed was totally prevented by methysergide (100 microM).Blockade of muscarinic receptors by atropine (1 microM) did not reduce the effect of serotonin, although it was effective in preventing the increase in particle transport speed mediated by muscarine (100 microM).

View Article: PubMed Central - PubMed

Affiliation: Institut für Anatomie, Zentrum für medizinische Struktur- und Zellbiologie, Universität zu Lübeck, Lübeck, Germany. koenig@anat.uni-luebeck.de

ABSTRACT

Background: Mucociliary clearance in the airways is driven by the coordinated beating of ciliated cells. Classical neuromediators such as noradrenalin and acetylcholine increase ciliary beat frequency and thus cilia-driven transport. Despite the fact that the neuromediator serotonin is ciliostimulatory in invertebrates and has been implied in releasing acetylcholine from the airway epithelium, its role in regulating cilia function in vertebrate airways is not established.

Methodology/principal findings: We examined the effects of serotonin on ciliary beat frequency and cilia-driven particle transport in the acutely excised submerged mouse trachea and determined the sources of serotonin in this tissue by immunohistochemistry. Serotonin (100 microM) increased cilary beat frequency (8.9+/-1.2 Hz to 17.0+/-2.7 Hz) and particle transport speed (38.9+/-4.6 microm/s to 83.4+/-8.3 microm/s) to an extent that was comparable to a supramaximal dose of ATP. The increase in particle transport speed was totally prevented by methysergide (100 microM). Blockade of muscarinic receptors by atropine (1 microM) did not reduce the effect of serotonin, although it was effective in preventing the increase in particle transport speed mediated by muscarine (100 microM). Immunohistochemistry demonstrated serotonin in mast cells pointing towards mast cells and platelets as possible endogenous sources of serotonin.

Conclusions/significance: These results indicate that serotonin is a likely endogenous mediator that can increase cilia-driven transport independent from acetylcholine during activation of mast cells and platelets.

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Mast cells contain serotonin in the mouse trachea.A, B. Fluorescence microscopy. Serotonin-immunolabeling is located in mast cells (A and B; arrow) Epithelium = e; cartilage = *. C, D. The presence of mast cells in the epithelium and in the lamina propria is shown in semithin sections. Arrows = mast cells, Arrowheads = capillaries. E, F. Toluidine blue staining of subepithelial mast cells in a trachea whole-mount. E. View from the lumen onto the epithelium. F. Same area as in E but with the focal plane below the epithelium. Arrows = toluidine blue-stained mast cells. Bars in A, B = 50 µm, in C, D = 10 µm, in E, F = 20 µm.
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pone-0004938-g007: Mast cells contain serotonin in the mouse trachea.A, B. Fluorescence microscopy. Serotonin-immunolabeling is located in mast cells (A and B; arrow) Epithelium = e; cartilage = *. C, D. The presence of mast cells in the epithelium and in the lamina propria is shown in semithin sections. Arrows = mast cells, Arrowheads = capillaries. E, F. Toluidine blue staining of subepithelial mast cells in a trachea whole-mount. E. View from the lumen onto the epithelium. F. Same area as in E but with the focal plane below the epithelium. Arrows = toluidine blue-stained mast cells. Bars in A, B = 50 µm, in C, D = 10 µm, in E, F = 20 µm.

Mentions: Serotonin-immunoreactivity was observed in mast cells in the lamina propria of the mouse trachea (Figure 7A, B), identified by numerous granula (Figure 7A inset). The labelling intensity was higher in mast cells found in the epithelial layer than in mast cells that were located under the basal membrane in the connective tissue in close proximity to blood vessels. In vessels that still contained blood, serotonin-immunoreactivity was found in platelets (not shown).The presence of mast cells in the subepithelial layer and in the epithelium was validated in conventional semithin sections (Figure 7C, D) and in whole mount preparations of tracheae using toluidine blue (Figure 7E, F).


Serotonin increases cilia-driven particle transport via an acetylcholine-independent pathway in the mouse trachea.

König P, Krain B, Krasteva G, Kummer W - PLoS ONE (2009)

Mast cells contain serotonin in the mouse trachea.A, B. Fluorescence microscopy. Serotonin-immunolabeling is located in mast cells (A and B; arrow) Epithelium = e; cartilage = *. C, D. The presence of mast cells in the epithelium and in the lamina propria is shown in semithin sections. Arrows = mast cells, Arrowheads = capillaries. E, F. Toluidine blue staining of subepithelial mast cells in a trachea whole-mount. E. View from the lumen onto the epithelium. F. Same area as in E but with the focal plane below the epithelium. Arrows = toluidine blue-stained mast cells. Bars in A, B = 50 µm, in C, D = 10 µm, in E, F = 20 µm.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2654158&req=5

pone-0004938-g007: Mast cells contain serotonin in the mouse trachea.A, B. Fluorescence microscopy. Serotonin-immunolabeling is located in mast cells (A and B; arrow) Epithelium = e; cartilage = *. C, D. The presence of mast cells in the epithelium and in the lamina propria is shown in semithin sections. Arrows = mast cells, Arrowheads = capillaries. E, F. Toluidine blue staining of subepithelial mast cells in a trachea whole-mount. E. View from the lumen onto the epithelium. F. Same area as in E but with the focal plane below the epithelium. Arrows = toluidine blue-stained mast cells. Bars in A, B = 50 µm, in C, D = 10 µm, in E, F = 20 µm.
Mentions: Serotonin-immunoreactivity was observed in mast cells in the lamina propria of the mouse trachea (Figure 7A, B), identified by numerous granula (Figure 7A inset). The labelling intensity was higher in mast cells found in the epithelial layer than in mast cells that were located under the basal membrane in the connective tissue in close proximity to blood vessels. In vessels that still contained blood, serotonin-immunoreactivity was found in platelets (not shown).The presence of mast cells in the subepithelial layer and in the epithelium was validated in conventional semithin sections (Figure 7C, D) and in whole mount preparations of tracheae using toluidine blue (Figure 7E, F).

Bottom Line: Classical neuromediators such as noradrenalin and acetylcholine increase ciliary beat frequency and thus cilia-driven transport.The increase in particle transport speed was totally prevented by methysergide (100 microM).Blockade of muscarinic receptors by atropine (1 microM) did not reduce the effect of serotonin, although it was effective in preventing the increase in particle transport speed mediated by muscarine (100 microM).

View Article: PubMed Central - PubMed

Affiliation: Institut für Anatomie, Zentrum für medizinische Struktur- und Zellbiologie, Universität zu Lübeck, Lübeck, Germany. koenig@anat.uni-luebeck.de

ABSTRACT

Background: Mucociliary clearance in the airways is driven by the coordinated beating of ciliated cells. Classical neuromediators such as noradrenalin and acetylcholine increase ciliary beat frequency and thus cilia-driven transport. Despite the fact that the neuromediator serotonin is ciliostimulatory in invertebrates and has been implied in releasing acetylcholine from the airway epithelium, its role in regulating cilia function in vertebrate airways is not established.

Methodology/principal findings: We examined the effects of serotonin on ciliary beat frequency and cilia-driven particle transport in the acutely excised submerged mouse trachea and determined the sources of serotonin in this tissue by immunohistochemistry. Serotonin (100 microM) increased cilary beat frequency (8.9+/-1.2 Hz to 17.0+/-2.7 Hz) and particle transport speed (38.9+/-4.6 microm/s to 83.4+/-8.3 microm/s) to an extent that was comparable to a supramaximal dose of ATP. The increase in particle transport speed was totally prevented by methysergide (100 microM). Blockade of muscarinic receptors by atropine (1 microM) did not reduce the effect of serotonin, although it was effective in preventing the increase in particle transport speed mediated by muscarine (100 microM). Immunohistochemistry demonstrated serotonin in mast cells pointing towards mast cells and platelets as possible endogenous sources of serotonin.

Conclusions/significance: These results indicate that serotonin is a likely endogenous mediator that can increase cilia-driven transport independent from acetylcholine during activation of mast cells and platelets.

Show MeSH
Related in: MedlinePlus