Abstract Freshwater snails of the genusBiomphalariaserve as intermediate hosts for the digenetic trematodeSchistosoma mansoni, the etiological agent for the most widespread form of intestinal schistosomiasis. As neuropeptide signaling in host snails can be altered by trematode infection, a neural transcriptomics approach was undertaken to identify peptide precursors inBiomphalaria glabrata, the major intermediate host forS.mansoniin the Western Hemisphere. Three transcripts that encode peptides belonging to the FMRF‐NH2‐related peptide (FaRP) family were identified inB.glabrata. One transcript encoded a precursor polypeptide (Bgl‐FaRP1; 292 amino acids) that included eight copies of the tetrapeptide FMRF‐NH2and single copies of FIRF‐NH2, FLRF‐NH2, and pQFYRI‐NH2. The second transcript encoded a precursor (Bgl‐FaRP2;347amino acids) that comprised 14 copies of the heptapeptide GDPFLRF‐NH2and 1 copy of SKPYMRF‐NH2. The precursor encoded by the third transcript (Bgl‐FaRP3; 287 amino acids) recapitulatedBgl‐FaRP2but lacked the full SKPYMRF‐NH2peptide. The three precursors shared a common signal peptide, suggesting a genomic organization described previously in gastropods. Immunohistochemical studies were performed on the nervous systems ofB.glabrataandB.alexandrina, a major intermediate host forS.mansoniin Egypt. FMRF‐NH2‐like immunoreactive (FMRF‐NH2‐li) neurons were located in regions of the central nervous system associated with reproduction, feeding, and cardiorespiration. Antisera raised against non‐FMRF‐NH2peptides present in the tetrapeptide and heptapeptide precursors labeled independent subsets of the FMRF‐NH2‐li neurons. This study supports the participation of FMRF‐NH2‐related neuropeptides in the regulation of vital physiological and behavioral systems that are altered by parasitism inBiomphalaria.
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The FMRF-NH2 gated sodium channel of Biomphalaria glabrata: Localization and expression following infection by Schistosoma mansoni
The neglected tropical disease schistosomiasis impacts over 700 million people globally. Schistosoma mansoni , the trematode parasite that causes the most common type of schistosomiasis, requires planorbid pond snails of the genus Biomphalaria to support its larval development and transformation to the cercarial form that can infect humans. A greater understanding of neural signaling systems that are specific to the Biomphalaria intermediate host could lead to novel strategies for parasite or snail control. This study examined a Biomphalaria glabrata neural channel that is gated by the neuropeptide FMRF-NH 2 . The Biomphalaria glabrata FMRF-NH 2 gated sodium channel ( Bgl- FaNaC) amino acid sequence was highly conserved with FaNaCs found in related gastropods, especially the planorbid Planorbella trivolvis (91% sequence identity). In common with the P . trivolvis FaNaC, the B . glabrata channel exhibited a low affinity (EC 50 : 3 x 10 −4 M) and high specificity for the FMRF-NH 2 agonist. Its expression in the central nervous system, detected with immunohistochemistry and in situ hybridization, was widespread, with the protein localized mainly to neuronal fibers and the mRNA confined to cell bodies. Colocalization of the Bgl- FaNaC message with its FMRF-NH 2 agonist precursor occurred in some neurons associated with male mating behavior. At the mRNA level, Bgl- FaNaC expression was decreased at 20 and 35 days post infection (dpi) by S . mansoni . Increased expression of the transcript encoding the FMRF-NH 2 agonist at 35 dpi was proposed to reflect a compensatory response to decreased receptor levels. Altered FMRF-NH 2 signaling could be vital for parasite proliferation in its intermediate host and may therefore present innovative opportunities for snail control.
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- Award ID(s):
- 1736019
- PAR ID:
- 10427968
- Editor(s):
- Cwiklinski, Krystyna
- Date Published:
- Journal Name:
- PLOS Neglected Tropical Diseases
- Volume:
- 17
- Issue:
- 6
- ISSN:
- 1935-2735
- Page Range / eLocation ID:
- e0011249
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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