FMRF-NH2-related neuropeptides in Biomphalaria spp., intermediate hosts for schistosomiasis: Precursor organization and immunohistochemical localization

Theodor Bilharz Research Institute

Bibliographic Information

Authors: Rolón-Martínez S.; Habib M.R.; Mansour T.A.; Díaz-Ríos M.; Rosenthal J.J.C.; Zhou X.-N.; Croll R.P.; Miller M.W.

Journal: Journal of Comparative Neurology

Publisher: John Wiley and Sons Inc

Publication Date: 11 June 2021

Volume / Issue: Volume 529 / Issue 13

Pages: 3336–3358

ISSN: 219967

DOI: 10.1002/cne.25195

Scopus: View on Scopus

PubMed: 34041754

Document Type: Article

Access: All Open Access; Green Open Access

Authors and Affiliations

Rolón-Martínez S., Institute of Neurobiology and Department of Anatomy and Neurobiology, University of Puerto Rico, Medical Sciences Campus, San Juan, Puerto Rico; Habib M.R., Medical Malacology Laboratory, Theodor Bilharz Research Institute, Giza, Egypt; Mansour T.A., Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, CA, United States, Department of Clinical Pathology, School of Medicine, University of Mansoura, Mansoura, Egypt; Díaz-Ríos M., Department of Biology, Bowdoin College, Brunswick, ME, United States; Rosenthal J.J.C., Marine Biological Laboratory, Woods Hole, MA, United States; Zhou X.-N., National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai, China; Croll R.P., Department of Physiology and Biophysics, Dalhousie University, Halifax, NS, Canada; Miller M.W., Institute of Neurobiology and Department of Anatomy and Neurobiology, University of Puerto Rico, Medical Sciences Campus, San Juan, Puerto Rico

Abstract

Freshwater snails of the genus Biomphalaria serve as intermediate hosts for the digenetic trematode Schistosoma 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 in Biomphalaria glabrata, the major intermediate host for S. mansoni in the Western Hemisphere. Three transcripts that encode peptides belonging to the FMRF-NH2-related peptide (FaRP) family were identified in B. glabrata. One transcript encoded a precursor polypeptide (Bgl-FaRP1; 292 amino acids) that included eight copies of the tetrapeptide FMRF-NH2 and single copies of FIRF-NH2, FLRF-NH2, and pQFYRI-NH2. The second transcript encoded a precursor (Bgl-FaRP2; 347 amino acids) that comprised 14 copies of the heptapeptide GDPFLRF-NH2 and 1 copy of SKPYMRF-NH2. The precursor encoded by the third transcript (Bgl-FaRP3; 287 amino acids) recapitulated Bgl-FaRP2 but lacked the full SKPYMRF-NH2 peptide. The three precursors shared a common signal peptide, suggesting a genomic organization described previously in gastropods. Immunohistochemical studies were performed on the nervous systems of B. glabrata and B. alexandrina, a major intermediate host for S. mansoni in 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-NH2 peptides 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 in Biomphalaria. © 2021 Wiley Periodicals LLC.

Keywords

Biomphalaria alexandrina; Biomphalaria glabrata; neuropeptides; pond snail; pulmonate mollusk; Schistosoma mansoni; Amino Acid Sequence; Animals; Biomphalaria; FMRFamide; Optical Imaging; Schistosomiasis mansoni; Transcriptome; amino acid; oligonucleotide; phenylalanylmethionylarginylphenylalaninamide like peptide; streptavidin; thyroglobulin; neuropeptide; phenylalanylmethionylarginylphenylalaninamide; Article; bioinformatics; central nervous system; controlled study; feeding; fluorescence in situ hybridization; ganglion; gene sequence; human; human tissue; immunohistochemistry; intermediate host; nerve cell; nonhuman; reproduction; RNA extraction; schistosomiasis; sequence alignment; animal; fluorescence imaging; genetics; isolation and purification; metabolism; procedures

Citation Information

Scopus Citations: 5

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