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Distribution of serotonergic and dopaminergic nerve fibers in the salivary gland complex of the cockroach Periplaneta americana.

Baumann O, Dames P, Kühnel D, Walz B - BMC Physiol. (2002)

Bottom Line: Salivary duct segments close to the acini are locally associated with dopaminergic and serotonergic fibers, whereas duct segments further downstream have only dopaminergic fibers on their surface and within the epithelium.Our results suggest that dopamine is released on the acinar surface, close to peripheral cells, and along the entire duct system.Moreover, the presence of serotonergic and dopaminergic fiber terminals on the reservoir indicates that the functions of this structure are also regulated by dopamine and serotonin.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institut für Biochemie und Biologie, Zoophysiologie, Universität Potsdam, Lennéstr, 7a, 14471 Potsdam, Germany. obaumann@rz.uni-potsdam.de

ABSTRACT

Background: The cockroach salivary gland consists of secretory acini with peripheral ion-transporting cells and central protein-producing cells, an extensive duct system, and a pair of reservoirs. Salivation is controlled by serotonergic and dopaminergic innervation. Serotonin stimulates the secretion of a protein-rich saliva, dopamine causes the production of a saliva without proteins. These findings suggest a model in which serotonin acts on the central cells and possibly other cell types, and dopamine acts selectively on the ion-transporting cells. To examine this model, we have analyzed the spatial relationship of dopaminergic and serotonergic nerve fibers to the various cell types.

Results: The acinar tissue is entangled in a meshwork of serotonergic and dopaminergic varicose fibers. Dopaminergic fibers reside only at the surface of the acini next to the peripheral cells. Serotonergic fibers invade the acini and form a dense network between central cells. Salivary duct segments close to the acini are locally associated with dopaminergic and serotonergic fibers, whereas duct segments further downstream have only dopaminergic fibers on their surface and within the epithelium. In addition, the reservoirs have both a dopaminergic and a serotonergic innervation.

Conclusion: Our results suggest that dopamine is released on the acinar surface, close to peripheral cells, and along the entire duct system. Serotonin is probably released close to peripheral and central cells, and at initial segments of the duct system. Moreover, the presence of serotonergic and dopaminergic fiber terminals on the reservoir indicates that the functions of this structure are also regulated by dopamine and serotonin.

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Dopaminergic nerve fibers within nerves that extend between acini Whole mounts of salivary glands were double-labeled with anti-dopamine (red) and BODIPY FL phallacidin (blue), and imaged by confocal microscopy. Acinar lobules (asterisks) are connected by nerves of large (broad arrows) and small (long arrows) diameter, containing dopaminergic fibers. In some of theses nerves, the dopaminergic fibers branch extensively and have numerous varicosities (b), suggesting that these sites represent neurohemal organs. Scale bar = 50 μm
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Figure 6: Dopaminergic nerve fibers within nerves that extend between acini Whole mounts of salivary glands were double-labeled with anti-dopamine (red) and BODIPY FL phallacidin (blue), and imaged by confocal microscopy. Acinar lobules (asterisks) are connected by nerves of large (broad arrows) and small (long arrows) diameter, containing dopaminergic fibers. In some of theses nerves, the dopaminergic fibers branch extensively and have numerous varicosities (b), suggesting that these sites represent neurohemal organs. Scale bar = 50 μm

Mentions: In addition to serotonergic fibers, the nerves interlinking the acinar lobules contained dopaminergic fibers with varicosities and fiber terminals (Fig. 6). In some regions of these nerves, the dopaminergic fibers ramified extensively and had numerous varicosities (Fig. 6b), suggesting that these structures represent neurohemal organs. Individual dopaminergic fibers of these nerves approached acinar lobules and formed a widely spaced network on the lobule surface (Fig. 7). These acinar-tissue-associated dopaminergic fibers had few varicosities irregularly distributed over their length and sidebranches with terminals on the tissue surface (Fig. 7a). Serial confocal sections through acinar lobules demonstrated that, in contrast to serotonergic fibers, dopaminergic fibers did not invade the acinar tissue but were confined to the surface (Fig. 7a,7b,7c,7d,7e,7f). However, extensive cross-linking by the use of glutaraldehyde as a fixative may have prevented penetration of the antibodies into the tissue, and thus the lack of anti-dopamine-immunoreactive structures within the acinar lobules might have been an artefact. Several lines of evidence indicated that this was not the case. First, immunoreactivity was also confined to the surface of the acinar lobules when anti-dopamine was applied to cryostat sections (Fig. 2c). Second, an identical staining pattern was obtained with anti-dopamine on whole-mounts fixed with a low concentration of glutaraldehyde (0.5%; data not shown), and with anti-TH on whole-mounts prepared by the same glutaraldehyde-free fixation protocol as that used for labeling with anti-serotonin (data not shown). Finally, anti-dopamine-positive fibers could be detected not only on the surface, but also within the tissue of other structures of the salivary gland complex (see below).


Distribution of serotonergic and dopaminergic nerve fibers in the salivary gland complex of the cockroach Periplaneta americana.

Baumann O, Dames P, Kühnel D, Walz B - BMC Physiol. (2002)

Dopaminergic nerve fibers within nerves that extend between acini Whole mounts of salivary glands were double-labeled with anti-dopamine (red) and BODIPY FL phallacidin (blue), and imaged by confocal microscopy. Acinar lobules (asterisks) are connected by nerves of large (broad arrows) and small (long arrows) diameter, containing dopaminergic fibers. In some of theses nerves, the dopaminergic fibers branch extensively and have numerous varicosities (b), suggesting that these sites represent neurohemal organs. Scale bar = 50 μm
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC117224&req=5

Figure 6: Dopaminergic nerve fibers within nerves that extend between acini Whole mounts of salivary glands were double-labeled with anti-dopamine (red) and BODIPY FL phallacidin (blue), and imaged by confocal microscopy. Acinar lobules (asterisks) are connected by nerves of large (broad arrows) and small (long arrows) diameter, containing dopaminergic fibers. In some of theses nerves, the dopaminergic fibers branch extensively and have numerous varicosities (b), suggesting that these sites represent neurohemal organs. Scale bar = 50 μm
Mentions: In addition to serotonergic fibers, the nerves interlinking the acinar lobules contained dopaminergic fibers with varicosities and fiber terminals (Fig. 6). In some regions of these nerves, the dopaminergic fibers ramified extensively and had numerous varicosities (Fig. 6b), suggesting that these structures represent neurohemal organs. Individual dopaminergic fibers of these nerves approached acinar lobules and formed a widely spaced network on the lobule surface (Fig. 7). These acinar-tissue-associated dopaminergic fibers had few varicosities irregularly distributed over their length and sidebranches with terminals on the tissue surface (Fig. 7a). Serial confocal sections through acinar lobules demonstrated that, in contrast to serotonergic fibers, dopaminergic fibers did not invade the acinar tissue but were confined to the surface (Fig. 7a,7b,7c,7d,7e,7f). However, extensive cross-linking by the use of glutaraldehyde as a fixative may have prevented penetration of the antibodies into the tissue, and thus the lack of anti-dopamine-immunoreactive structures within the acinar lobules might have been an artefact. Several lines of evidence indicated that this was not the case. First, immunoreactivity was also confined to the surface of the acinar lobules when anti-dopamine was applied to cryostat sections (Fig. 2c). Second, an identical staining pattern was obtained with anti-dopamine on whole-mounts fixed with a low concentration of glutaraldehyde (0.5%; data not shown), and with anti-TH on whole-mounts prepared by the same glutaraldehyde-free fixation protocol as that used for labeling with anti-serotonin (data not shown). Finally, anti-dopamine-positive fibers could be detected not only on the surface, but also within the tissue of other structures of the salivary gland complex (see below).

Bottom Line: Salivary duct segments close to the acini are locally associated with dopaminergic and serotonergic fibers, whereas duct segments further downstream have only dopaminergic fibers on their surface and within the epithelium.Our results suggest that dopamine is released on the acinar surface, close to peripheral cells, and along the entire duct system.Moreover, the presence of serotonergic and dopaminergic fiber terminals on the reservoir indicates that the functions of this structure are also regulated by dopamine and serotonin.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institut für Biochemie und Biologie, Zoophysiologie, Universität Potsdam, Lennéstr, 7a, 14471 Potsdam, Germany. obaumann@rz.uni-potsdam.de

ABSTRACT

Background: The cockroach salivary gland consists of secretory acini with peripheral ion-transporting cells and central protein-producing cells, an extensive duct system, and a pair of reservoirs. Salivation is controlled by serotonergic and dopaminergic innervation. Serotonin stimulates the secretion of a protein-rich saliva, dopamine causes the production of a saliva without proteins. These findings suggest a model in which serotonin acts on the central cells and possibly other cell types, and dopamine acts selectively on the ion-transporting cells. To examine this model, we have analyzed the spatial relationship of dopaminergic and serotonergic nerve fibers to the various cell types.

Results: The acinar tissue is entangled in a meshwork of serotonergic and dopaminergic varicose fibers. Dopaminergic fibers reside only at the surface of the acini next to the peripheral cells. Serotonergic fibers invade the acini and form a dense network between central cells. Salivary duct segments close to the acini are locally associated with dopaminergic and serotonergic fibers, whereas duct segments further downstream have only dopaminergic fibers on their surface and within the epithelium. In addition, the reservoirs have both a dopaminergic and a serotonergic innervation.

Conclusion: Our results suggest that dopamine is released on the acinar surface, close to peripheral cells, and along the entire duct system. Serotonin is probably released close to peripheral and central cells, and at initial segments of the duct system. Moreover, the presence of serotonergic and dopaminergic fiber terminals on the reservoir indicates that the functions of this structure are also regulated by dopamine and serotonin.

Show MeSH
Related in: MedlinePlus