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Histamine Immunoreactive Elements in the Central and Peripheral Nervous Systems of the Snail, Biomphalaria spp., Intermediate Host for Schistosoma mansoni.

Habib MR, Mohamed AH, Osman GY, Sharaf El-Din AT, Mossalem HS, Delgado N, Torres G, Rolón-Martínez S, Miller MW, Croll RP - PLoS ONE (2015)

Bottom Line: This study thus shows that histamine is an abundant transmitter in these snails and its distribution suggest involvement in numerous neural circuits.In addition to providing novel subjects for comparative studies of histaminegic neurons in gastropods, Biomphalaria is also the major intermediate host for the digenetic trematode parasite, which causes human schistosomiasis.The study therefore provides a foundation for understanding potential roles for histamine in interactions between the snail hosts and their trematode parasites.

View Article: PubMed Central - PubMed

Affiliation: Medical Malacology Laboratory, Theodor Bilharz Research Institute, Giza, Egypt; Department of Physiology and Biophysics, Dalhousie University, Halifax, Nova Scotia, Canada.

ABSTRACT
Histamine appears to be an important transmitter throughout the Animal Kingdom. Gastropods, in particular, have been used in numerous studies establishing potential roles for this biogenic amine in the nervous system and showing its involvement in the generation of diverse behaviours. And yet, the distribution of histamine has only previously been described in a small number of molluscan species. The present study examined the localization of histamine-like immunoreactivity in the central and peripheral nervous systems of pulmonate snails of the genus Biomphalaria. This investigation demonstrates immunoreactive cells throughout the buccal, cerebral, pedal, left parietal and visceral ganglia, indicative of diverse regulatory functions in Biomphalaria. Immunoreactivity was also present in statocyst hair cells, supporting a role for histamine in graviception. In the periphery, dense innervation by immunoreactive fibers was observed in the anterior foot, perioral zone, and other regions of the body wall. This study thus shows that histamine is an abundant transmitter in these snails and its distribution suggest involvement in numerous neural circuits. In addition to providing novel subjects for comparative studies of histaminegic neurons in gastropods, Biomphalaria is also the major intermediate host for the digenetic trematode parasite, which causes human schistosomiasis. The study therefore provides a foundation for understanding potential roles for histamine in interactions between the snail hosts and their trematode parasites.

No MeSH data available.


Related in: MedlinePlus

HA-like immunoreactivity in the cerebral ganglia.A: Dorsal view of the left cerebral ganglion of B. glabrata. The white arrow and double asterisks denote clusters along the lateral margin of the dorsal surface while the white arrowhead indicates an identified individual neuron at the base of the tentacular nerve (Tn). The star, single asterisk and bracket indicate ventral clusters that are not clearly in focus. B: Higher magnification view of area in part A indicated by the rectangle with the arrow showing an axon projecting from a cell in the lateral cluster. C: A deeper focus showing additional cells along the ventral surface in a similar region of another specimen of B. glabrata. D: Medial and, E: lateral regions of the right cerebral ganglia of B. alexandrina, as seen from a ventral vantage. The confocal z-stack spanned the thickness of the ganglion so that both dorsal and ventral cells are shown in the projection and many of the same cells and cell clusters indicated by stars, asterisks and double asterisks can be recognized here as described above for B. glabrata. One cluster of neurons (D, asterisk) is situated near the origin of the cerebral commissure (Cc) and another (E, star) near the cerebral-pleural connective (CPlc). The anterolateral cluster of neurons observed on the dorsal surface (A, double asterisk) continues to the anterior ventral surface (E, double asterisk) near the origin of the cerebral-buccal connective and lip nerves (out of view). Additional individual cells are located anterolaterally on the dorsal surface (E, large solid white arrows), and near the center of the ganglion on the ventral surface (D, large solid white arrows), and one solitary cell (E, small solid white arrow) at the base of the cerebral-buccal connective (diagonally above and out of view of this image). Numerous immunoreactive fibers can be observed in the cerebral commissures and connectives (large, solid white arrowheads). F: Ventral view of the left cerebral ganglia of B. alexandrina. Two clusters of neurons are observed, one (star) located at the origin of cerebral pleural connective (CPlc) and the other (asterisk) near the cerebral commissure (out of view to the left of this image). The subesophageal cerebral commissure contains a pair of fine immunoreactive filaments exiting the anterior ventral surface of the cerebral ganglia (contrasted black arrow). Scale bars = 50 μm, all panels.
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pone.0129800.g004: HA-like immunoreactivity in the cerebral ganglia.A: Dorsal view of the left cerebral ganglion of B. glabrata. The white arrow and double asterisks denote clusters along the lateral margin of the dorsal surface while the white arrowhead indicates an identified individual neuron at the base of the tentacular nerve (Tn). The star, single asterisk and bracket indicate ventral clusters that are not clearly in focus. B: Higher magnification view of area in part A indicated by the rectangle with the arrow showing an axon projecting from a cell in the lateral cluster. C: A deeper focus showing additional cells along the ventral surface in a similar region of another specimen of B. glabrata. D: Medial and, E: lateral regions of the right cerebral ganglia of B. alexandrina, as seen from a ventral vantage. The confocal z-stack spanned the thickness of the ganglion so that both dorsal and ventral cells are shown in the projection and many of the same cells and cell clusters indicated by stars, asterisks and double asterisks can be recognized here as described above for B. glabrata. One cluster of neurons (D, asterisk) is situated near the origin of the cerebral commissure (Cc) and another (E, star) near the cerebral-pleural connective (CPlc). The anterolateral cluster of neurons observed on the dorsal surface (A, double asterisk) continues to the anterior ventral surface (E, double asterisk) near the origin of the cerebral-buccal connective and lip nerves (out of view). Additional individual cells are located anterolaterally on the dorsal surface (E, large solid white arrows), and near the center of the ganglion on the ventral surface (D, large solid white arrows), and one solitary cell (E, small solid white arrow) at the base of the cerebral-buccal connective (diagonally above and out of view of this image). Numerous immunoreactive fibers can be observed in the cerebral commissures and connectives (large, solid white arrowheads). F: Ventral view of the left cerebral ganglia of B. alexandrina. Two clusters of neurons are observed, one (star) located at the origin of cerebral pleural connective (CPlc) and the other (asterisk) near the cerebral commissure (out of view to the left of this image). The subesophageal cerebral commissure contains a pair of fine immunoreactive filaments exiting the anterior ventral surface of the cerebral ganglia (contrasted black arrow). Scale bars = 50 μm, all panels.

Mentions: The cerebral ganglia of B. glabrata and B. alexandrina contained numerous HA-Lir neurons in a range of sizes (Fig 4) and again homologous individual cells and clusters of cells could be recognized in the two species. Two prominent clusters of cells were located on the lateral margins of the dorsal surface of the each cerebral ganglion. The first cluster of small (10–15μm diameter) cells was located anterior to the origin of the tentacular nerve (Fig 4A, white double asterisks) while the second group of larger (15–20 μm) cells was located posterior to the nerve origin (Fig 4A and 4B, white arrows). A single intensely labeled neuron (15–20 μm) was observed overlying the base of the tentacular nerve located between these two clusters (Fig 4A and 4B, white arrowheads). Two additional dorsal neurons were reliably located as a separated pair of cells on the anterior dorsal margin of each cerebral ganglion (Fig 4D, large, solid white arrows).


Histamine Immunoreactive Elements in the Central and Peripheral Nervous Systems of the Snail, Biomphalaria spp., Intermediate Host for Schistosoma mansoni.

Habib MR, Mohamed AH, Osman GY, Sharaf El-Din AT, Mossalem HS, Delgado N, Torres G, Rolón-Martínez S, Miller MW, Croll RP - PLoS ONE (2015)

HA-like immunoreactivity in the cerebral ganglia.A: Dorsal view of the left cerebral ganglion of B. glabrata. The white arrow and double asterisks denote clusters along the lateral margin of the dorsal surface while the white arrowhead indicates an identified individual neuron at the base of the tentacular nerve (Tn). The star, single asterisk and bracket indicate ventral clusters that are not clearly in focus. B: Higher magnification view of area in part A indicated by the rectangle with the arrow showing an axon projecting from a cell in the lateral cluster. C: A deeper focus showing additional cells along the ventral surface in a similar region of another specimen of B. glabrata. D: Medial and, E: lateral regions of the right cerebral ganglia of B. alexandrina, as seen from a ventral vantage. The confocal z-stack spanned the thickness of the ganglion so that both dorsal and ventral cells are shown in the projection and many of the same cells and cell clusters indicated by stars, asterisks and double asterisks can be recognized here as described above for B. glabrata. One cluster of neurons (D, asterisk) is situated near the origin of the cerebral commissure (Cc) and another (E, star) near the cerebral-pleural connective (CPlc). The anterolateral cluster of neurons observed on the dorsal surface (A, double asterisk) continues to the anterior ventral surface (E, double asterisk) near the origin of the cerebral-buccal connective and lip nerves (out of view). Additional individual cells are located anterolaterally on the dorsal surface (E, large solid white arrows), and near the center of the ganglion on the ventral surface (D, large solid white arrows), and one solitary cell (E, small solid white arrow) at the base of the cerebral-buccal connective (diagonally above and out of view of this image). Numerous immunoreactive fibers can be observed in the cerebral commissures and connectives (large, solid white arrowheads). F: Ventral view of the left cerebral ganglia of B. alexandrina. Two clusters of neurons are observed, one (star) located at the origin of cerebral pleural connective (CPlc) and the other (asterisk) near the cerebral commissure (out of view to the left of this image). The subesophageal cerebral commissure contains a pair of fine immunoreactive filaments exiting the anterior ventral surface of the cerebral ganglia (contrasted black arrow). Scale bars = 50 μm, all panels.
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Related In: Results  -  Collection

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Show All Figures
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pone.0129800.g004: HA-like immunoreactivity in the cerebral ganglia.A: Dorsal view of the left cerebral ganglion of B. glabrata. The white arrow and double asterisks denote clusters along the lateral margin of the dorsal surface while the white arrowhead indicates an identified individual neuron at the base of the tentacular nerve (Tn). The star, single asterisk and bracket indicate ventral clusters that are not clearly in focus. B: Higher magnification view of area in part A indicated by the rectangle with the arrow showing an axon projecting from a cell in the lateral cluster. C: A deeper focus showing additional cells along the ventral surface in a similar region of another specimen of B. glabrata. D: Medial and, E: lateral regions of the right cerebral ganglia of B. alexandrina, as seen from a ventral vantage. The confocal z-stack spanned the thickness of the ganglion so that both dorsal and ventral cells are shown in the projection and many of the same cells and cell clusters indicated by stars, asterisks and double asterisks can be recognized here as described above for B. glabrata. One cluster of neurons (D, asterisk) is situated near the origin of the cerebral commissure (Cc) and another (E, star) near the cerebral-pleural connective (CPlc). The anterolateral cluster of neurons observed on the dorsal surface (A, double asterisk) continues to the anterior ventral surface (E, double asterisk) near the origin of the cerebral-buccal connective and lip nerves (out of view). Additional individual cells are located anterolaterally on the dorsal surface (E, large solid white arrows), and near the center of the ganglion on the ventral surface (D, large solid white arrows), and one solitary cell (E, small solid white arrow) at the base of the cerebral-buccal connective (diagonally above and out of view of this image). Numerous immunoreactive fibers can be observed in the cerebral commissures and connectives (large, solid white arrowheads). F: Ventral view of the left cerebral ganglia of B. alexandrina. Two clusters of neurons are observed, one (star) located at the origin of cerebral pleural connective (CPlc) and the other (asterisk) near the cerebral commissure (out of view to the left of this image). The subesophageal cerebral commissure contains a pair of fine immunoreactive filaments exiting the anterior ventral surface of the cerebral ganglia (contrasted black arrow). Scale bars = 50 μm, all panels.
Mentions: The cerebral ganglia of B. glabrata and B. alexandrina contained numerous HA-Lir neurons in a range of sizes (Fig 4) and again homologous individual cells and clusters of cells could be recognized in the two species. Two prominent clusters of cells were located on the lateral margins of the dorsal surface of the each cerebral ganglion. The first cluster of small (10–15μm diameter) cells was located anterior to the origin of the tentacular nerve (Fig 4A, white double asterisks) while the second group of larger (15–20 μm) cells was located posterior to the nerve origin (Fig 4A and 4B, white arrows). A single intensely labeled neuron (15–20 μm) was observed overlying the base of the tentacular nerve located between these two clusters (Fig 4A and 4B, white arrowheads). Two additional dorsal neurons were reliably located as a separated pair of cells on the anterior dorsal margin of each cerebral ganglion (Fig 4D, large, solid white arrows).

Bottom Line: This study thus shows that histamine is an abundant transmitter in these snails and its distribution suggest involvement in numerous neural circuits.In addition to providing novel subjects for comparative studies of histaminegic neurons in gastropods, Biomphalaria is also the major intermediate host for the digenetic trematode parasite, which causes human schistosomiasis.The study therefore provides a foundation for understanding potential roles for histamine in interactions between the snail hosts and their trematode parasites.

View Article: PubMed Central - PubMed

Affiliation: Medical Malacology Laboratory, Theodor Bilharz Research Institute, Giza, Egypt; Department of Physiology and Biophysics, Dalhousie University, Halifax, Nova Scotia, Canada.

ABSTRACT
Histamine appears to be an important transmitter throughout the Animal Kingdom. Gastropods, in particular, have been used in numerous studies establishing potential roles for this biogenic amine in the nervous system and showing its involvement in the generation of diverse behaviours. And yet, the distribution of histamine has only previously been described in a small number of molluscan species. The present study examined the localization of histamine-like immunoreactivity in the central and peripheral nervous systems of pulmonate snails of the genus Biomphalaria. This investigation demonstrates immunoreactive cells throughout the buccal, cerebral, pedal, left parietal and visceral ganglia, indicative of diverse regulatory functions in Biomphalaria. Immunoreactivity was also present in statocyst hair cells, supporting a role for histamine in graviception. In the periphery, dense innervation by immunoreactive fibers was observed in the anterior foot, perioral zone, and other regions of the body wall. This study thus shows that histamine is an abundant transmitter in these snails and its distribution suggest involvement in numerous neural circuits. In addition to providing novel subjects for comparative studies of histaminegic neurons in gastropods, Biomphalaria is also the major intermediate host for the digenetic trematode parasite, which causes human schistosomiasis. The study therefore provides a foundation for understanding potential roles for histamine in interactions between the snail hosts and their trematode parasites.

No MeSH data available.


Related in: MedlinePlus