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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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Related in: MedlinePlus

Serotonin increases particle transport speed and ciliary beat frequency.A. Cumulative increase of serotonin concentration increases cilia-driven particle transport speed. Statistical analysis: global Friedman test followed by a Wilcoxon test to compare selected time points. Mean±S.E.M. is shown. N = 6 tracheae from 6 animals. P values below 0.05 are set in bold type. B. The increase in cilia-driven particle transport speed is paralleled by an increase in ciliary beat frequency. Mean±S.E.M. is shown. Statistical analysis: Global Friedman test followed by a Wilcoxon test to compare selected time points. N = 6 tracheae from 6 animals for the measurement for particle transport speed, and n = 40 cells from 4 tracheae from 4 animals. S.E.M. was calculated using the number of animals. P values below 0.05 are set in bold type.
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pone-0004938-g004: Serotonin increases particle transport speed and ciliary beat frequency.A. Cumulative increase of serotonin concentration increases cilia-driven particle transport speed. Statistical analysis: global Friedman test followed by a Wilcoxon test to compare selected time points. Mean±S.E.M. is shown. N = 6 tracheae from 6 animals. P values below 0.05 are set in bold type. B. The increase in cilia-driven particle transport speed is paralleled by an increase in ciliary beat frequency. Mean±S.E.M. is shown. Statistical analysis: Global Friedman test followed by a Wilcoxon test to compare selected time points. N = 6 tracheae from 6 animals for the measurement for particle transport speed, and n = 40 cells from 4 tracheae from 4 animals. S.E.M. was calculated using the number of animals. P values below 0.05 are set in bold type.

Mentions: Cumulative application of 10 nM and 1 µM serotonin did not increase the particle transport speed significantly over the initial speed prior to stimulation. Stimulation with 100 µM serotonin increased the particle transport speed from 47.9±10.4 µm/s (33 min) to 87.5±7.0 µm/s (45 min; p = 0.028; Figure 4A). The concentration of 100 µM serotonin was used in further experiments.


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)

Serotonin increases particle transport speed and ciliary beat frequency.A. Cumulative increase of serotonin concentration increases cilia-driven particle transport speed. Statistical analysis: global Friedman test followed by a Wilcoxon test to compare selected time points. Mean±S.E.M. is shown. N = 6 tracheae from 6 animals. P values below 0.05 are set in bold type. B. The increase in cilia-driven particle transport speed is paralleled by an increase in ciliary beat frequency. Mean±S.E.M. is shown. Statistical analysis: Global Friedman test followed by a Wilcoxon test to compare selected time points. N = 6 tracheae from 6 animals for the measurement for particle transport speed, and n = 40 cells from 4 tracheae from 4 animals. S.E.M. was calculated using the number of animals. P values below 0.05 are set in bold type.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0004938-g004: Serotonin increases particle transport speed and ciliary beat frequency.A. Cumulative increase of serotonin concentration increases cilia-driven particle transport speed. Statistical analysis: global Friedman test followed by a Wilcoxon test to compare selected time points. Mean±S.E.M. is shown. N = 6 tracheae from 6 animals. P values below 0.05 are set in bold type. B. The increase in cilia-driven particle transport speed is paralleled by an increase in ciliary beat frequency. Mean±S.E.M. is shown. Statistical analysis: Global Friedman test followed by a Wilcoxon test to compare selected time points. N = 6 tracheae from 6 animals for the measurement for particle transport speed, and n = 40 cells from 4 tracheae from 4 animals. S.E.M. was calculated using the number of animals. P values below 0.05 are set in bold type.
Mentions: Cumulative application of 10 nM and 1 µM serotonin did not increase the particle transport speed significantly over the initial speed prior to stimulation. Stimulation with 100 µM serotonin increased the particle transport speed from 47.9±10.4 µm/s (33 min) to 87.5±7.0 µm/s (45 min; p = 0.028; Figure 4A). The concentration of 100 µM serotonin was used in further experiments.

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