Localization of tyrosine hydroxylase‐like immunoreactivity in the nervous systems of Biomphalaria glabrata and Biomphalaria alexandrina, intermediate hosts for schistosomiasis

Abstract

Planorbid snails of the genus Biomphalaria are major intermediate hosts for the digenetic trematode parasite Schistosoma mansoni. Evidence suggests that levels of the neurotransmitter dopamine (DA) are reduced during the course of S. mansoni multiplication and transformation within the snail. This investigation used immunohistochemical methods to localize tyrosine hydroxylase (TH), the rate-limiting enzyme in the biosynthesis of catecholamines, in the nervous system of Biomphalaria. The two species examined, Biomphalaria glabrata and Biomphalaria alexandrina, are the major intermediate hosts for S. mansoni in sub-Saharan Africa, where more than 90% of global cases of human intestinal schistosomiasis occur. TH-like immunoreactive (THli) neurons were distributed throughout the central nervous system (CNS) and labeled fibers were present in all commissures, connectives, and nerves. Some asymmetries were observed, including a large distinctive neuron (LPeD1) in the pedal ganglion described previously in several pulmonates. The majority of TH-like immunoreactive neurons were detected in the peripheral nervous system (PNS), especially in lip and foot regions of the anterior integument. Independent observations supporting the dopaminergic phenotype of THli neurons included 1) block of LPeD1 synaptic signaling by the D2/3 antagonist sulpiride, and 2) the similar localization of aqueous aldehyde (FaGlu) induced fluorescence. The distribution of THli neurons indicates that, as in other gastropods, dopamine functions as a sensory neurotransmitter and in the regulation of feeding and reproductive behaviors in Biomphalaria. It is hypothesized that infection could stimulate transmitter release from dopaminergic sensory neurons and that dopaminergic signaling could contribute to modifications of both host and parasite behavior.

GABA‐like immunoreactivity in Biomphalaria: Colocalization with tyrosine hydroxylase‐like immunoreactivity in the feeding motor systems of panpulmonate snails

“…and in four to six small neurons near the origin of the T n. (Figure a,d, arrows ). As reported by Vallejo et al (), the T n. also contained a bundle of THli fibers that originated from small peripheral cells in the tentacle epithelium. The THli fiber bundle was more compact than the GABAli axons and occupied a distinct portion of the nerve (Figure b,e).…”

“…A previous study showed that prominent THli fiber systems in the lip nerves originate predominantly from peripheral neurons (Vallejo et al, ). A group of THli central neurons was observed in the anterolateral region the cerebral ganglion, however (Figure e,h, arrowheads) , prompting double‐labeling experiments to test for the presence of GABA‐TH colocalization.…”

“…It specifically labels neurons that are stained with several independent catecholaminergic markers, including the glyoxylic acid (Kabotyanski, Baxter, & Byrne, ; Rathouz & Kirk, ) and the formaldehyde (Fa)‐glutaraldehyde (Glu) histofluorescent techniques (Croll, ; Díaz‐Ríos et al, ; Goldstein & Schwartz, ). We previously reported that synaptic signals produced by neurons labeled with this antibody in B. glabrata were blocked by the dopamine antagonist sulpiride (Vallejo et al, ).…”

“…The present study was designed with three objectives: (a) We first mapped the distribution of GABA‐like immunoreactivity (li) in the nervous systems of two species of panpulmonate snails, Biomphalaria glabrata and Biomphalaria alexandrina . In previous studies, we fully mapped the localization of catecholamines in the nervous systems of these species (Vallejo et al, ) and showed that TH provided a reliable means of labeling neurons that utilize DA as a neurotransmitter (Vallejo et al, ). This work is part of our investigation of neurotransmitters in intermediate snail hosts for larval trematodes that cause the tropical disease schistosomiasis (see also Delgado, Vallejo, & Miller, ; Habib et al, ; Mansour et al, ).…”

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

“…mansoni larvae, the larvae could, in turn. also affect the snails through aminergic pathways as suggested by Delgado et al [34] and Vallejo et al [35]. For example, serotonin may be involved in parasitic castration [67], leading to a redirection of energy resources in infected snails [68][69][70][71][72].…”