Genomic organization of the FMRFamide gene in Lymnaea: multiple exons encoding novel neuropeptides

Kellett, Elaine; Saunders, S. J.; Li, Ka Wan; Staddon, Julian W.; Benjamin, Paul R.; Burke, Julian F.

doi:10.1523/jneurosci.14-11-06564.1994

Cited by 47 publications

(58 citation statements)

References 25 publications

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“…These observations suggest that HasPC2 has a general role in processing neuropeptides such as FMRFamide and related peptides throughout the life cycle of haliotids and possibly other gastropods. In all other animals studied, FMRFamide and related peptides are produced by proteolytic cleavage from a precursor protein with subsequent amidation of the individual peptides (Kellett et al, 1994;Favrel et al, 1998). This is the first study to show a convertase is expressed early in molluscan development.…”

Section: B Amentioning

confidence: 88%

“…The control, in which no cDNA template was used (blank), was negative. (A) Alignment of predicted amino acid sequence of PC2 catalytic regions from H. asinina (this study), H. rubra (this study), Aplysia (Nagle et al, 1995), and Lymnaea (Kellett et al, 1994). Black shading represents identical residues in all the sequences and grey shading indicates similar residues.…”

Section: Larval Expression Of H Asinina Pc2 By Rt-pcrmentioning

confidence: 99%

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Expression of prohormone convertase 2 and the generation of neuropeptides in the developing nervous system of the gastropod Haliotis

Cummins¹,

York²,

Hanna³

et al. 2009

Int. J. Dev. Biol.

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Prohormone convertase 2 (PC2) belongs to a family of enzymes involved in the proteolytic maturation of neuropeptide precursors into mature peptides that act as neurotransmitters, neuromodulators or neurohormones. Here we show that a gene encoding a PC2-like enzyme (HasPC2) is expressed during larval development and in the adult ganglia of the vetigastropod Haliotis asinina. HasPC2 exhibits high sequence identity to other gastropod PC2s and thus is likely to function in peptide processing. Analysis of HasPC2 expression indicates that it is activated early in nervous system development. During trochophore and early veliger larval stages, HasPC2 is expressed in the vicinity of the forming ganglia of the central nervous system and parts of the putative peripheral nervous system. Later in larval development, at the time the veliger becomes competent to interact with the external environment and initiate metamorphosis, HasPC2 expression largely restricts to cells of the major ganglia and their commissures. Profiling of veliger larvae by bioinformatic approaches suggests the expression of a variety of peptides. Direct MALDI-MS-based peptide profiling of juvenile Haliotis cerebral ganglia (brain) reveals an abundance of neuropeptides, including FMRFamide-related peptides and APGWamide, compatible with PC2 functioning in neuropeptide processing in these regions. These results are consistent with PC2 regulating neuropeptide generation in the earliest functioning of the gastropod nervous system. KEY WORDS: prohormone convertase, abalone, neuropeptide, developmentNeuropeptides are widespread in the animal kingdom and are often involved in the control of critical functions throughout the life cycle. The regulation of development by peptidergic hormones is a common feature of multicellular animals and has been studied in great detail in arthropods and vertebrates. Strikingly, investigations reveal that insects are as well or even better supplied with neuropeptides than mammals. In insects, neuropeptides regulate not only the functioning of endocrine glands, but also a wide range of physiological and developmental processes (Reumer et al., 2008). Although a complete developmental peptidome analysis has not been established for other major invertebrate groups, such as the molluscs, numerous immunolocalization studies suggest that neuropeptides are equally important for their development. For instance, in gastropods FMRFamide and related peptides are amongst the earliest neurotransmitters expressed Int. J. Dev. Biol. 53: 1081-1088 (2009) Abbreviations used in this paper: DIG, digoxigenin; MALDI-MS, matrix-assisted laser desorption/ionization MS; PBS, phosphate-buffered solution; PC, prohormone convertase; RACE, rapid amplification of cDNA ends; WMISH, whole-mount in situ hybridization.within the larval nervous system (Croll and Voronezhskaya, 1996;Dickinson et al., 1999; Dickinson et al., 2000;Haszprunar et al., 2002;Dickinson and Croll, 2003; Croll, 2006). In the adult stages of these same animals, neuropeptides pl...

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Section: B Amentioning

confidence: 88%

Section: Larval Expression Of H Asinina Pc2 By Rt-pcrmentioning

confidence: 99%

Expression of prohormone convertase 2 and the generation of neuropeptides in the developing nervous system of the gastropod Haliotis

Cummins¹,

York²,

Hanna³

et al. 2009

Int. J. Dev. Biol.

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“…The occurrence of a signal peptide sequence that is encoded by a different exon to the exon encoding putative neuropeptides is of particular interest because this is a feature that has been reported before in some, but not all, neuropeptide precursor genes. For example, in the mollusc Lymnaea stagnalis the precursor for the neuropeptide FMRFamide is encoded by an mRNA derived from two exons, with exon 1 encoding the signal peptide and exon 2 encoding multiple copies of FMRFamide (Kellett et al, 1994). In contrast, in Drosophila melanogaster the precursor for FMRFamide-like peptides is encoded by a single exon (Schneider and Taghert, 1990).…”

Section: Discussionmentioning

confidence: 99%

“…In the case of the Lymnaea FMRFamide gene, an explanation for the presence of a separate exon that encodes the signal peptide is provided by the occurrence of additional neuropeptideencoding exons (3,4,5) located downstream from the FMRFamide-encoding exon (2). Consequently, transcripts of this gene can be alternatively spliced to give rise to two different mRNAs: one encoding the signal peptide (exon 1) and the FMRFamide products of exon 2 and the other encoding the signal peptide (exon 1) and the alternative neuropeptides encoded by exons 3, 4 and 5 (Kellett et al, 1994). Although the occurrence of a separate signal peptide-encoding exon does not in itself necessarily imply the existence of multiple neuropeptide-encoding exons that are alternatively spliced, it is possible that in Strongylocentrotus purpuratus there are additional neuropeptide-encoding exon(s) located downstream of the exon encoding SpurS1-SpurS7.…”

Section: Discussionmentioning

confidence: 99%

Molecular characterisation of SALMFamide neuropeptides in sea urchins

Elphick

Thorndyke²

2005

Journal of Experimental Biology

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SUMMARY The SALMFamides are a family of neuropeptides found in species belonging to the phylum Echinodermata. Members of this family have been identified in starfish (class Asteroidea) and in sea cucumbers (class Holothuroidea) but not in other echinoderms. Our aim here was to characterise SALMFamide neuropeptides in sea urchins (class Echinoidea). Radioimmunoassays for the starfish SALMFamides S1 and S2 were used to test for related peptides in whole-body acetone extracts of the sea urchin Echinus esculentus. Fractionation of extracts using high performance liquid chromatography (HPLC)revealed several peaks of SALMFamide-like immunoreactivity, with two S2-like immunoreactive peaks (3 and 4) being the most prominent. However, peak 4 could not be purified to homogeneity and although peak 3 was purified, only a partial sequence (MRYH) could be obtained. An alternative strategy for identification of echinoid SALMFamides was provided by sequencing the genome of the sea urchin Strongylocentrotus purpuratus. Analysis of whole-genome shotgun sequence data using the Basic Local Alignment Search Tool (BLAST) identified a contig (347664) that contains a coding region for seven putative SALMFamide neuropeptides(PPVTTRSKFTFamide, DAYSAFSFamide, GMSAFSFamide, AQPSFAFamide, GLMPSFAFamide,PHGGSAFVFamide and GDLAFAFamide), which we have named SpurS1-SpurS7,respectively. Three of these peptides (SpurS1-3) have the C-terminal sequences TFamide or SFamide, which are identical or similar to the C-terminal region of the starfish SALMFamide S2. This may explain the occurrence of several S2-like immunoreactive peptides in extracts of Echinus esculentus. Detailed analysis of the sequence of contig 347664 indicated that the SALMFamide gene in Strongylocentrotus purpuratus comprises two exons,with the first exon encoding a signal peptide sequence and the second exon encoding SpurS1-SpurS7. Characterisation of this gene is important because it is the first echinoderm neuropeptide precursor sequence to be identified and,more specifically, it provides our first insight into the structure and organisation of a SALMFamide gene in an echinoderm. In particular, it has revealed a hitherto unknown complexity in the diversity of SALMFamide neuropeptides that may occur in an echinoderm species because all previous studies, which relied on peptide purification and sequencing, revealed only two SALMFamide neuropeptides in each species examined. It now remains to be established whether or not the occurrence of more than two SALMFamides in Strongylocentrotus purpuratus is a feature that is peculiar to this species and to echinoids in general or is more widespread across the phylum Echinodermata. Identification of SpurS1-SpurS7 provides the basis for comparative analysis of the physiological actions of these peptides in sea urchins and for exploitation of the sea urchin genome sequence to identify the receptor(s) that mediate effects of SALMFamides in echinoderms.

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“…Smit et al 1992Smit et al , 1993Smit et al , 2001Kellett et al 1994 ; Table 1). Only a small proportion of the ESTs (y9 %) were derived from previously isolated L. stagnalis sequences, but 12 of the most abundant ESTs that we isolated have been isolated previously as cDNAs (Table 1).…”

Section: R E S U L T Smentioning

confidence: 99%

An expressed sequence tag survey of gene expression in the pond snail Lymnaea stagnalis, an intermediate vector of Fasciola hepatica

Davison

Blaxter

2005

Parasitology

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The pond snail Lymnaea stagnalis is an intermediate vector for the liver fluke Fasciola hepatica, a common parasite of ruminants and humans. Yet, despite being a disease of medical and economic importance, as well as a potentially useful comparative tool, the genetics of the relationship between Lymnaea and Fasciola has barely been investigated. As a complement to forthcoming F. hepatica expressed sequence tags (ESTs), we generated 1320 ESTs from L. stagnalis central nervous system (CNS) libraries. We estimate that these sequences derive from 771 different genes, of which 374 showed significant similarity to proteins in public databases, and 169 were similar to ESTs from the snail vector Biomphalaria glabrata. These L. stagnalis ESTs will provide insight into the function of the snail CNS, as well as the molecular components of behaviour and response to parasitism. In the future, the comparative analysis of Lymnaea/Fasciola with Biomphalaria/Schistosoma will help to understand both conserved and divergent aspects of the host-parasite relationship. The L. stagnalis ESTs will also assist gene prediction in the forthcoming B. glabrata genome sequence. The dataset is available for searching on the worldwide web at http://zeldia.cap.ed.ac.uk/mollusca.html.

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Genomic organization of the FMRFamide gene in Lymnaea: multiple exons encoding novel neuropeptides

Cited by 47 publications

References 25 publications

Expression of prohormone convertase 2 and the generation of neuropeptides in the developing nervous system of the gastropod Haliotis

Expression of prohormone convertase 2 and the generation of neuropeptides in the developing nervous system of the gastropod Haliotis

Molecular characterisation of SALMFamide neuropeptides in sea urchins

An expressed sequence tag survey of gene expression in the pond snail Lymnaea stagnalis, an intermediate vector of Fasciola hepatica

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