Identification, presence, and possible multifunctional regulatory role of invertebrate gonadotropin-releasing hormone/corazonin molecule in the great pond snail (Lymnaea stagnalis)

Fodor, I; Zrínyi, Zita; Horváth, Réka; Herczeg, Róbert; Büki, Gergely; Koene, Joris M.; Tsai, Pei‐San; Pirger, Zsolt

doi:10.1016/j.ygcen.2020.113621

Cited by 11 publications

(24 citation statements)

References 39 publications

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“…(b) Members of the GnRH superfamily cited in this article partition into two groups. Peptides from Octopus , Aplysia , and Lymnaea that were originally identified as GnRH are classified as Lophotrochozoa corazonins according to the nomenclature of Zandawala et al (2018) (see also Plachetzki et al, 2016; Tsai, 2018; Fodor, Urbán, et al, 2020; Fodor, Zrinyi, et al, 2020). Peptides from Aplysia californica and Biomphalaria glabrata that were designated molluscan adipokinetic hormones (AKH) are classified Lophotrochozoa GnRH.…”

Section: Resultsmentioning

confidence: 99%

“…In panpulmonates, precursors encoding the peptide pQNYHFSNGWYA‐NH 2 were mined from the genome of B . glabrata and from a Lymnaea stagnalis neural transcriptome (Adema et al, 2017; Fodor, Zrinyi, et al, 2020; Figure 1(b)). As more was learned about the GnRH superfamily and their receptors, it was determined that these peptides should more accurately be reclassified as corazonin‐related peptides (Figure 1(b); see Plachetzki et al, 2016; Zandawala et al, 2018; Tsai, 2018; Fodor, Urbán, et al, 2020; Fodor, Zrinyi, et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

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Identification and localization of a gonadotropin‐releasing hormone‐related neuropeptide in Biomphalaria, an intermediate host for schistosomiasis

Rosa-Casillas

Jesús

Rodríguez³

et al. 2021

J of Comparative Neurology

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Freshwater snails of the genus Biomphalaria serve as obligatory hosts for the digenetic trematode Schistosoma mansoni, the causative agent for the most widespread form of intestinal schistosomiasis. Within Biomphalaria, S. mansoni larvae multiply and transform into the cercariae form that can infect humans. Trematode development and proliferation is thought to be facilitated by modifications of host behavior and physiological processes, including a reduction of reproduction known as “parasitic castration.” As neuropeptides participate in the control of reproduction across phylogeny, a neural transcriptomics approach was undertaken to identify peptides that could regulate Biomphalaria reproductive physiology. The present study identified a transcript in Biomphalaria alexandrina that encodes a peptide belonging to the gonadotropin‐releasing hormone (GnRH) superfamily. The precursor and the predicted mature peptide, pQIHFTPDWGNN‐NH2 (designated Biom‐GnRH), share features with peptides identified in other molluscan species, including panpulmonates, opisthobranchs, and cephalopods. An antibody generated against Biom‐GnRH labeled neurons in the cerebral, pedal, and visceral ganglia of Biomphalaria glabrata. GnRH‐like immunoreactive fiber systems projected to all central ganglia. In the periphery, immunoreactive material was detected in the ovotestis, oviduct, albumen gland, and nidamental gland. As these structures serve crucial roles in the production, transport, nourishment, and encapsulation of eggs, disruption of the GnRH system of Biomphalaria could contribute to reduced reproductive activity in infected snails.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Identification and localization of a gonadotropin‐releasing hormone‐related neuropeptide in Biomphalaria, an intermediate host for schistosomiasis

Rosa-Casillas

Jesús

Rodríguez³

et al. 2021

J of Comparative Neurology

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“…Oct-GnRH, like echinoderm GnRHs, is composed of 12 amino acids and conserves amino acids corresponding to pyro-Glu, His 2 , Ser 4 , Gly 6 , Pro 9 , and C-terminally amidated Gly 10 in typical vertebrate GnRHs and tunicate t-GnRH6, -10, and -11 (Table 1) This amino acid sequence identity demonstrates that oct-GnRH shares more common amino acids with vertebrate and tunicate GnRHs compared with the echinoderm GnRHs SpGnRHP and ArGnRH. Oct-GnRH-like peptides [9,[40][41][42][43][44] have also been identified in other protostomes, including bivalves, gastropods, annelids, and crustaceans (Table 1). In contrast, GnRH-like peptides have not been identified in insects or nematodes, although CRZs and AKHs, which are believed to have originated from common ancestors of GnRHs, are found in these organisms [7,9,11].…”

Section: Protostome Gnrhsmentioning

confidence: 99%

Invertebrate Gonadotropin-Releasing Hormone Receptor Signaling and Its Relevant Biological Actions

Sakai

Yamamoto

Matsubara

et al. 2020

IJMS

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Gonadotropin-releasing hormones (GnRHs) play pivotal roles in reproduction via the hypothalamus-pituitary-gonad axis (HPG axis) in vertebrates. GnRHs and their receptors (GnRHRs) are also conserved in invertebrates lacking the HPG axis, indicating that invertebrate GnRHs do not serve as “gonadotropin-releasing factors” but, rather, function as neuropeptides that directly regulate target tissues. All vertebrate and urochordate GnRHs comprise 10 amino acids, whereas amphioxus, echinoderm, and protostome GnRH-like peptides are 11- or 12-residue peptides. Intracellular calcium mobilization is the major second messenger for GnRH signaling in cephalochordates, echinoderms, and protostomes, while urochordate GnRHRs also stimulate cAMP production pathways. Moreover, the ligand-specific modulation of signal transduction via heterodimerization between GnRHR paralogs indicates species-specific evolution in Ciona intestinalis. The characterization of authentic or putative invertebrate GnRHRs in various tissues and their in vitro and in vivo activities indicate that invertebrate GnRHs are responsible for the regulation of both reproductive and nonreproductive functions. In this review, we examine our current understanding of and perspectives on the primary sequences, tissue distribution of mRNA expression, signal transduction, and biological functions of invertebrate GnRHs and their receptors.

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“…CRZs, first discovered in the American cockroach ( Periplaneta americana ) 8 , are multifunctional peptides and part of the GnRH superfamily 1 . The misinterpretation of sequence and function of the first discovered invGnRH/CRZ (in the common octopus, Octopus vulgaris ) has led to the its name oct-GnRH 2 , 9 ; however, recent structural, phylogenetic, and phylogenomic analyzes suggest that molluscan GnRHs are more related to CRZs and a nomenclature change should be considered 1 , 5 , 10 – 13 . A more global understanding of invGnRH/CRZ evolution requires further exploration of species-specific functions and structure of invGnRH/CRZ molecules.…”

Section: Introductionmentioning

confidence: 99%

“…We have recently determined the cDNA sequence of invGnRH/CRZ (termed ly-GnRH/CRZ) in L. stagnalis and characterized the transcript and peptide distribution in the CNS and some peripheral organs 5 . The functional/active peptide was deduced to be an undecapeptide with an N-terminal pyroglutamate and a C-terminal alanine amide (pQNYHFSNGWYA-NH 2 ).…”

Section: Introductionmentioning

confidence: 99%

Functional characterization and related evolutionary implications of invertebrate gonadotropin-releasing hormone/corazonin in a well-established model species

Fodor

Svigruha

Bozsó

et al. 2021

Sci Rep

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In vertebrates, gonadotropin-releasing hormone (GnRH) peptide is the central mediator of reproduction. Homologous peptides have previously also been identified in molluscan species. However, emerging evidence suggests that these molecules might serve diverse regulatory functions and proposes to consider them as corazonin (CRZ). We previously isolated the full-length cDNA of the invGnRH/CRZ peptide (termed ly-GnRH/CRZ) in the well-established invertebrate model species, the great pond snail Lymnaea stagnalis; however, its predicted functions remain to be verified. In this study, we first confirmed the presence of the deduced active peptide from the central nervous system of L. stagnalis. Further, we performed in vivo and in vitro studies to explore the functions of ly-GnRH/CRZ. Injection of sexually mature specimens with synthetic active peptide had an inhibitory effect on locomotion and an acceleratory effect on egg-laying, but had no effect on feeding. The previously predicted modulatory effect of ly-GnRH/CRZ was supported by its identified co-localization with serotonin on the surface of the heart atria. Lastly, we demonstrated not only the presence of ly-GnRH/CRZ in the penial complex but also that ly-GnRH/CRZ-containing neurons project to the efferent penis nerve, suggesting ly-GnRH/CRZ may directly modulate the motor output of this peripheral tissue. Overall, our findings strongly support that ly-GnRH/CRZ is a multifunctional neuropeptide. These results contribute to the understanding of the GnRH superfamily and, more broadly, disciplines such as comparative endocrinology and neurobiology.

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Identification, presence, and possible multifunctional regulatory role of invertebrate gonadotropin-releasing hormone/corazonin molecule in the great pond snail (Lymnaea stagnalis)

Cited by 11 publications

References 39 publications

Identification and localization of a gonadotropin‐releasing hormone‐related neuropeptide in Biomphalaria, an intermediate host for schistosomiasis

Identification and localization of a gonadotropin‐releasing hormone‐related neuropeptide in Biomphalaria, an intermediate host for schistosomiasis

Invertebrate Gonadotropin-Releasing Hormone Receptor Signaling and Its Relevant Biological Actions

Functional characterization and related evolutionary implications of invertebrate gonadotropin-releasing hormone/corazonin in a well-established model species

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