An immunohistochemical analysis of peptidergic neurons apparently associated with reproduction and growth in Biomphalaria alexandrina

Acker, Madison; Habib, Mohamed R.; Beach, Griffin A.; Doyle, Jillian M.; Croll, Roger P.

doi:10.1016/j.ygcen.2019.03.017

Cited by 5 publications

(7 citation statements)

References 74 publications

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“…The pattern of staining produced by the commercial FMRF‐NH 2 antibody was in general agreement with previous observations in numerous gastropods (e.g., Acker et al, 2019; Boer et al, 1980; Cardot & Fellman, 1983; Cooke & Gelperin, 1988; Elekes & Ude, 1994; Lehman & Price, 1987; Lloyd et al, 1987; Schot & Boer, 1982). The FMRF‐NH 2 antibody reacts with both tetrapeptide and extended FaRPs, requiring only a C ‐terminal aromatic amino acid, a penultimate arginine residue, and a total length of at least four residues (Greenberg et al, 1988).…”

Section: Methodssupporting

confidence: 89%

“…As reported previously by Acker et al (2019), FMRF‐NH 2 ‐li cells were located in the ventral lobe of the left cerebral hemiganglion, a lateralized cluster of neurons associated with innervation of male reproductive structures (Li & Chase, 1995; van Golen et al, 1995; Koene et al, 2000). FMRF‐NH 2 ‐li cells (90.6 ± 22.4, n = 3) in the ventral lobe of B .…”

Section: Resultssupporting

confidence: 61%

“…In gastropods, male mating behavior is controlled by a distributed central network located ipsilateral to the reproductive organs (de Boer et al, 1996; Li & Chase, 1995; Van Duivenboden & Ter Maat, 1988). Numerous neuropeptides, including the FaRPs, have been localized to neurons that project to the male reproductive complex (de Lange, de Boer, et al, 1998; de Lange, Joosse, & van Minnen, 1998; Croll & Van Minnen, 1992; Smit et al, 2003; Acker et al, 2019; reviewed by Koene, 2010). The FMRF‐NH 2 tetrapeptides and heptapeptides modulate contraction of the penis retractor muscle of L .…”

Section: Discussionmentioning

confidence: 99%

“…Peripheral functions include regulation of muscle contraction (Austin et al, 1983; Cottrell et al, 1983; Lehman & Greenberg, 1987) and cardioregulation (Alevizos et al, 1989; Buckett, Peters, & Benjamin, 1990; Buckett, Peters, Dockray, et al, 1990; Brezden et al, 1991). Central neurons that express FaRPs participate in the control of reproductive behaviors (Acker et al, 2019; Brussaard et al, 1988; van Golen et al, 1995) and feeding (Alania et al, 2004; Lloyd et al, 1987; Murphy, 1990; Vilim et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

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

Rolón‐Martínez

Habib

Mansour

et al. 2021

J of Comparative Neurology

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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.

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Section: Methodssupporting

confidence: 89%

Section: Resultssupporting

confidence: 61%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Rolón‐Martínez

Habib

Mansour

et al. 2021

J of Comparative Neurology

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“…Therefore, we propose that this difference may reflect the complexity of neuromuscular circuits. Such grouping of neurons is well-known in gastropods (Vallejo et al, 2014;Acker et al, 2019) and cephalopods (Wollesen et al, 2010;Webber et al, 2017;Shigeno et al, 2018) on land or in water, animals that have developed appropriate sensory-motor neuronal machinery.…”

Section: Discussionmentioning

confidence: 99%

Distribution of Molecules Related to Neurotransmission in the Nervous System of the Mussel Crenomytilus grayanus

et al. 2020

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In bivalves neurotransmitters are involved in a variety of behaviors, but their diversity and distribution in the nervous system of these organisms remains somewhat unclear. Here, we first examined immunohistochemically the distributions of neurons containing different neurotransmitters, neuropeptides, and related enzymes, as well as the proliferative status of neurons in the ganglia of the mussel Crenomytilus grayanus. H-Phe-Met-Arg-Phe-NH2 (FMRFamide), choline acetyltransferase (ChAT), γaminobutyric acid (GABA) and tyrosine hydroxylase (TH) were found to be expressed by neurons in all the ganglia, whereas serotonin (5-HT) neurons were found only in the cerebropleural and pedal, but not visceral ganglia. Moreover, incubation of living mussels in the presence of a 5-HT precursor (5-HTP) confirmed the absence of 5-HT-containing neurons from the visceral ganglia, indicating that the "serotonin center" of the visceral nervous system is located in the cerebral ganglia. Furthermore, immunostaining of molecules related to neurotransmission together with α-acetylated tubulin demonstrated that this cytoskeletal protein may be a potential pan-neuronal marker in bivalves. Adult mussel neurons do not proliferate, but a population of proliferating PCNA-LIP cells which do not express any of the neurotransmitters examined, perhaps glia cells, was detected in the ganglia. These novel findings suggest that the nervous system of bivalves contains a broad variety of signal molecules most likely involved in the regulation of different physiological and behavioral processes. In addition, proliferating cells may maintain and renew glial cells and neurons throughout the lives of bivalves.

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Biochemical and apoptotic changes in the nervous and ovotestis tissues of Biomphalaria alexandrina following infection with Schistosoma mansoni

Habib

Ghoname

Ali

et al. 2020

Experimental Parasitology

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An immunohistochemical analysis of peptidergic neurons apparently associated with reproduction and growth in Biomphalaria alexandrina

Cited by 5 publications

References 74 publications

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

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

Distribution of Molecules Related to Neurotransmission in the Nervous System of the Mussel Crenomytilus grayanus

Biochemical and apoptotic changes in the nervous and ovotestis tissues of Biomphalaria alexandrina following infection with Schistosoma mansoni

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An immunohistochemical analysis of peptidergic neurons apparently associated with reproduction and growth in Biomphalaria alexandrina

Cited by 5 publications

References 74 publications

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

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

Distribution of Molecules Related to Neurotransmission in the Nervous System of the Mussel Crenomytilus grayanus

Biochemical and apoptotic changes in the nervous and ovotestis tissues of Biomphalaria alexandrina following infection with Schistosoma mansoni

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Product

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

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