Transcriptomic identification of starfish neuropeptide precursors yields new insights into neuropeptide evolution

doi:10.1098/rsob.150224

. 2016 Feb;6(2):150224.

doi: 10.1098/rsob.150224.

Transcriptomic identification of starfish neuropeptide precursors yields new insights into neuropeptide evolution

Dean C Semmens¹, Olivier Mirabeau², Ismail Moghul¹, Mahesh R Pancholi¹, Yannick Wurm¹, Maurice R Elphick³

Affiliations

¹ School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, UK.
² Institut Curie, Genetics and Biology of Cancers Unit, INSERM U830, PSL Research University, Paris 75005, France.
³ School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, UK m.r.elphick@qmul.ac.uk.

PMID: 26865025
PMCID: PMC4772807
DOI: 10.1098/rsob.150224

Transcriptomic identification of starfish neuropeptide precursors yields new insights into neuropeptide evolution

Dean C Semmens et al. Open Biol. 2016 Feb.

. 2016 Feb;6(2):150224.

doi: 10.1098/rsob.150224.

Authors

Dean C Semmens¹, Olivier Mirabeau², Ismail Moghul¹, Mahesh R Pancholi¹, Yannick Wurm¹, Maurice R Elphick³

Affiliations

¹ School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, UK.
² Institut Curie, Genetics and Biology of Cancers Unit, INSERM U830, PSL Research University, Paris 75005, France.
³ School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, UK m.r.elphick@qmul.ac.uk.

PMID: 26865025
PMCID: PMC4772807
DOI: 10.1098/rsob.150224

Abstract

Neuropeptides are evolutionarily ancient mediators of neuronal signalling in nervous systems. With recent advances in genomics/transcriptomics, an increasingly wide range of species has become accessible for molecular analysis. The deuterostomian invertebrates are of particular interest in this regard because they occupy an 'intermediate' position in animal phylogeny, bridging the gap between the well-studied model protostomian invertebrates (e.g. Drosophila melanogaster, Caenorhabditis elegans) and the vertebrates. Here we have identified 40 neuropeptide precursors in the starfish Asterias rubens, a deuterostomian invertebrate from the phylum Echinodermata. Importantly, these include kisspeptin-type and melanin-concentrating hormone-type precursors, which are the first to be discovered in a non-chordate species. Starfish tachykinin-type, somatostatin-type, pigment-dispersing factor-type and corticotropin-releasing hormone-type precursors are the first to be discovered in the echinoderm/ambulacrarian clade of the animal kingdom. Other precursors identified include vasopressin/oxytocin-type, gonadotropin-releasing hormone-type, thyrotropin-releasing hormone-type, calcitonin-type, cholecystokinin/gastrin-type, orexin-type, luqin-type, pedal peptide/orcokinin-type, glycoprotein hormone-type, bursicon-type, relaxin-type and insulin-like growth factor-type precursors. This is the most comprehensive identification of neuropeptide precursor proteins in an echinoderm to date, yielding new insights into the evolution of neuropeptide signalling systems. Furthermore, these data provide a basis for experimental analysis of neuropeptide function in the unique context of the decentralized, pentaradial echinoderm bauplan.

Keywords: deuterostome; echinoderm; evolution; neuropeptide; starfish.

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Figures

**Figure 1.**
Animal phylogeny. Phylogenetic diagram showing the position of the phylum Echinodermata (shown in red; e.g. starfish) in the deuterostomian branch of the animal kingdom. The Bilateria comprise two super-phyla—the deuterostomes and the protostomes. The deuterostomes comprise the chordates (vertebrates, urochordates and cephalochordates) and the ambulacrarians (hemichordates and echinoderms). The protostomes comprise the lophotrochozoans (e.g. molluscs and annelids) and the ecdysozoans (e.g. arthropods and nematodes). The Cnidaria (e.g. sea anemones) are basal to the Bilateria. Images of representative animals from each phylum were obtained from http://phylopic.org or were created by the authors or by M. Zandawala (Stockholm University).

**Figure 2.**
Precursors of neuropeptides in *A. rubens* that provide novel insights into neuropeptide evolution at the superphylum/phylum level. Predicted signal peptides are shown in blue, putative neuropeptides are shown in red (with cysteine (C) residues underlined), C-terminal glycine (G) residues that are putative substrates for amidation are shown in orange and putative dibasic/tribasic cleavage sites are shown in green.

**Figure 3.**
Alignment of ArKP1 and ArKP2 with other kisspeptin (KP)-type peptides. Accession numbers for the corresponding precursor proteins are: Arub, *A. rubens* KP-type precursor [GenBank: KT601705]; Spur, *S. purpuratus* KP-type precursor [GI:374768013]; Skow, *S. kowalevskii* KP-type precursor [GI:187123982]; Bflo1, *B. floridae* KP-type precursor 1 [GI:260826607]; Bflo2, *B. floridae* KP-type precursor 2 [GI:260827077]; Bflo3, *B. floridae* KP-type precursor 3 [GI:260826605]; Bflo4, *B. floridae* KP-type precursor 4 [GI:260793233]; Hsap, *Homo sapiens* KiSS-1 metastasis-suppressor precursor [GI:21950713].

**Figure 4.**
Alignment of ArMCH with other melanin-concentration hormone (MCH)-type peptides. Accession numbers for the corresponding precursor proteins are: Arub, *A. rubens* MCH-type precursor [GenBank: KT601706]; Spur, *S. purpuratus* MCH-type precursor [GI:109402760]; Skow, *S. kowalevskii* MCH-type precursor [GI:187231810]; Trub, *Takifugu rubripes* MCH precursor [GI:410918650]; Hsap, *H. sapiens* MCH precursor [GI:187445].

**Figure 5.**
Alignment of ArTK1 and ArTK2 with other tachykinin (TK)-type peptides. Accession numbers for the corresponding precursor proteins are: Arub, *A. rubens* TK-type precursor [GenBank: KT601707]; Spur, *S. purpuratus* TK-type precursor [GI:109402899]; Cint, *C. intestinalis* TK-type precursor [GI:74136064]; Hsap_SubP, *H. sapiens* β-prepro TK precursor [GI:29482]; Hsap_NKB, *H. sapiens* neurokinin-β precursor [GI:48146502]; Hsap_NKA, *H. sapiens* TK4 precursor [GI:117938255]; Ctel, *Capitella teleta* [GI:161289578]; Lgig1, *Lottia gigantea* TK-type precursor 1 [GI:676441944]; Lgig2, *L. gigantea* TK-type precursor 2 [GI:163525452]; Dmel, *D. melanogaster* TK precursor [GI:442618676].

**Figure 6.**
Alignment of ArSS with other somatostatin (SS)-type peptides and AST-C-type peptides. Accession numbers for the corresponding precursor proteins are: Arub, *A. rubens* SS-type precursor [GenBank: KT601708]; Spur, *S. purpuratus* SS-type precursor [GI:390344260]; Bflo, *B. floridae* SS-type precursor [JGI:72051]; Hsap_SS, *H. sapiens* SS precursor [GI:21619155]; Hsap_CORT, *H. sapiens* cortistatin (CORT) precursor [GI:110645815]; Ctel, *C. teleta* AST-C-type precursor [GI:161295377]; Lgig, *L. gigantea* AST-C-type precursor [GI:163505903]; Dmel_AstC, *D. melanogaster* AST-C-type precursor [GI:665407583]; Dmel_AstCC, *D. melanogaster* AST-CC-type precursor [GI:665407585].

**Figure 7.**
Alignment of ArPDF1 and ArPDF2 with other pigment-dispersing factor (PDF)-type peptides. Accession numbers for the corresponding precursor proteins are: Arub, *A. rubens* PDF-type precursor [GenBank: KT601709]; Spur, *S. purpuratus* PDF-type precursor [GI:115899431]; Skow, *S. kowalevskii* PDF-type precursor [GI:187067819]; Ctel, *C. teleta* PDF-type precursor [JGI:204689]; Lgig, *L. gigantea* cerebrin precursor [GI:676458325]; Dmel, *D. melanogaster* PDF precursor [GI:281362639]; Cele, *C. elegans* PDF precursor [GI:25149644].

**Figure 8.**
Alignment of ArCRH with other corticotropin-releasing hormone (CRH)-type peptides. Accession numbers for the corresponding precursor proteins are: Arub, *A. rubens* CRH-type precursor [GenBank: KT601710]; Skow1, *S. kowalevskii* CRH-type precursor 1 [GI:281433636]; Skow2, *S. kowalevskii* CRH-type precursor 2 [GI:281433636]; Bflo, *B. floridae* CRH-type precursor [GI:260786674]; Hsap_CRH, *H. sapiens* CRH precursor [GI:30583744]; Hsap_UCN, *H. sapiens* urocortin (UCN) precursor [GI:49457481]; Hsap_UCN2, *H. sapiens* stresscopin-related protein precursor [GI:14029393]; Hsap_UCN3, *H. sapiens* stresscopin precursor [GI:15026913]; Ctel1, *C. teleta* CRH-type precursor 1 [GI:161303031]; Ctel2, *C. teleta* CRH-type precursor 2 [JGI:190906]; Ctel3, *C. teleta* CRH-type precursor 3 [JGI:190906]; Ctel4, *C. teleta* CRH-type precursor 4 [JGI:194553]; Lgig1, *L. gigantea* CRH-type precursor 1 [GI:676493124]; Lgig2, *L. gigantea* CRH-type precursor 2 [GI:163524672].

**Figure 9.**
Precursors of neuropeptides in *A. rubens* that are novel echinoderm representatives of bilaterian neuropeptide families. Predicted signal peptides are shown in blue, putative neuropeptides are shown in red (with cysteine (C) residues underlined), C-terminal glycine (G) residues that are putative substrates for amidation are shown in orange and putative dibasic cleavage sites are shown in green. For the (a) asterotocin and (b) NGFFYamide precursors, the C-terminal neurophysin domain (with the characteristic 14 cysteine (c) residues underlined) is shown in purple.

**Figure 10.**
Alignment of asterotocin with other vasopressin/oxytocin (VP/OT)-type peptides. Accession numbers for the corresponding precursor proteins are: Arub, *A. rubens* asterotocin precursor [GenBank: KT601711], Spur, *S. purpuratus* echinotocin precursor [GI:390337108]; Skow, *S. kowalevskii* VP/OT-type precursor [GI:187155721]; Bflo, *B. floridae* VP/OT-type precursor [GI:260828088]; Hsap_VP, *H. sapiens* VP precursor [GI:340298]; Hsap_OT, *H. sapiens* OT precursor [GI:189410]; Ctel, *C. teleta* VP/OT-type precursor [JGI:173251]; Lgig, *L. gigantea* VP/OT-type precursor [JGI:53893]; Dpul, *Daphnia pulex* VP/OT-type precursor [JGI:59567].

**Figure 11.**
Alignment of *A. rubens* GnRH-type peptides/precursors with other gonadotropin-releasing hormone (GnRH)-type peptides/precursors. (a) Alignment of GnRH-type peptides. Accession numbers for the corresponding precursor proteins are: Arub, *A. rubens* GnRH-type precursor 1 [GenBank: KT601712]; Spur, *S. purpuratus* GnRH-type precursor 1 [GI:390361802]; Skow, *S. kowalevskii* GnRH-type precursor [GI:585702722]; Bflo, *B. floridae* GnRH-type precursor [GI:568818760]; Hsap1, *H. sapiens* GnRH precursor 1 [GI:133908609]; Hsap2, *H. sapiens* GnRH precursor 2 [GI:109731929]; Ctel, *C. teleta* GnRH-type precursor [GI:161294493]; Acal, *A. californica* GnRH-type precursor [GI:325296898]; Dmel_CORZ, *D. melanogaster* corazonin (CORZ) precursor [GI:386765761]; Dmel_AKH, *D. melanogaster* adipokinetic hormone (AKH) precursor [GI:281365621]. (b) Alignment of GnRH-type precursors. Accession numbers for the corresponding precursor proteins are: Arub_GnRH1P, *A. rubens* GnRH-type precursor 1 [GenBank: KT601712]; Spur_GnRH1P, *S. purpuratus* GnRH-type precursor 1 [GI:390361802]; Arub_GnRH2P, *A. rubens* GnRH-type precursor 2 [GenBank: KT601713]; Spur_GnRH2P, *S. purpuratus* GnRH-type precursor 2 [GI:109403263].

**Figure 12.**
Alignment of ArTRH with other thyrotropin-releasing hormone (TRH)-type peptides. Accession numbers for the corresponding precursor proteins are: Arub, *A. rubens* TRH-type precursor [GenBank: KT601714]; Spur, *S. purpuratus* TRH-type precursor [GI:109402869]; Skow, *S. kowalevskii* TRH-type precursor [GI:187216047]; Bflo, *B. floridae* TRH-type precursor [GI:260784028]; Hsap, *H. sapiens* TRH precursor [GI:485464565]; Pdum, *P. dumerilii* EFLGamide precursor [GI:332167915].

**Figure 13.**
Alignment of ArCT with other calcitonin (CT)-type peptides. Accession numbers for the corresponding precursor proteins are: Arub, *A. rubens* CT-type precursor [GenBank: KT601715]; Spur, *S. purpuratus* CT-type precursor [GI:115767208]; Skow, *S. kowalevskii* CT-type precursor [GI:187217193]; Bflo1, *B. floridae* CT-type precursor 1 [GI:260826569]; Bflo2, *B. floridae* CT-type precursor 2 [GI:260826567]; Bflo3, *B. floridae* CT-type precursor 3 [GI:260826573]; Bflo4, *B. floridae* CT-type precursor 4 [GI:260812099]; Hsap_Calc, *H. sapiens* CT precursor [GI:179819]; Hsap_CGRP1, *H. sapiens* CT gene-related peptide (CGRP) 1 precursor [GI:269784661]; Hsap_IAPP, *H. sapiens* islet amyloid polypeptide (IAPP) precursor [GI:109255169]; Hsap_ADML, *H. sapiens* adrenomedullin precursor [GI:675022745]; Hsap_ADM2, *H. sapiens* adrenomedullin 2 precursor [GI:41016725]; Ctel, *C. teleta* CT-type precursor [GI: 161220966]; Lgig1, *L. gigantea* CT-type precursor 1 [GI:163526287]; Lgig2, *L. gigantea* CT-type precursor 2 [GI:676481265].

**Figure 14.**
Alignment of ArCCK1 and ArCCK2 with other cholecystokinin (CCK)-type peptides. Accession numbers for the corresponding precursor proteins are: Arub, *A. rubens* CCK-type precursor [GenBank: KT601716]; Spur, *S. purpuratus* CCK-type precursor [GI:390355380]; Skow1, *S. kowalevskii* CCK-type precursor 1 [GI:585688033]; Skow2, *S. kowalevskii* CCK-type precursor 2 [GI:187061456]; Cint, *C. intestinalis* cionin precursor [GI:10799472]; Hsap_CCK-8, *H. sapiens* CCK precursor [GI:30582820]; Hsap_Gast-6, *H. sapiens* gastrin precursor [GI:47481291]; Ctel, *C. teleta* CCK-type precursor [GI:161296032]; Lgig1, *L. gigantea* CCK-type precursor 1 [GI:161296032]; Lgig2, *L. gigantea* CCK-type precursor 2 [GI:52414496]; Dmel_SK, *D. melanogaster* sulfakinin (SK) precursor [GI:386765036].

**Figure 15.**
Alignment of ArOX1 and ArOX2 with other orexin (OX)-type peptides. Accession numbers for the corresponding precursor proteins are: Arub1, *A. rubens* OX-type precursor 1 [GenBank: KT601717]; Arub2, *A. rubens* OX-type precursor 2 [GenBank: KT601718]; Spur1, *S. purpuratus* OX-type precursor 1 [GI:346420309]; Spur2, *S. purpuratus* OX-type precursor 2 [GI:346419879]; Skow, *S. kowalevskii* OX-type precursor [GI:585662697]; Bflo1, *B. floridae* OX-type precursor 1 [GI:260807454]; Bflo2, *B. floridae* OX-type precursor 2 [GI:260780718]; Hsap_OX, *H. sapiens* OX precursor [GI:4557634].

**Figure 16.**
Alignment of ArLQ with other luqin (LQ)-type peptides and alignment of a conserved C-terminal domain of LQ-type precursor proteins. Accession numbers for the corresponding precursor proteins are: Arub, *A. rubens* LQ-type precursor [GenBank: KT601719]; Spur, *S. purpuratus* LQ-type precursor [GI:390331828]; Skow, *S. kowalevskii* LQ-type precursor [GI:585716464]; Ctel, *C. teleta* LQ-type precursor [GI:161280144]; Lgig, *L. gigantea* LQ-type precursor [GI:163510328]; Dpul, *D. pulex* LQ-type precursor [JGI:251691]; Dvir, *Drosophila virilis* LQ-type precursor [GI: 968114152].

**Figure 17.**
Alignment of representative *A. rubens* PP/orcokinin-type peptide with other PP/orcokinin-type peptides. Accession numbers for the corresponding precursor proteins are: Arub, *A. rubens* PP/orcokinin-type precursor [GenBank: KT601720]; Spur1, *S. purpuratus* PP/orcokinin-type precursor 1 [GI:390335272]; Spur2, *S. purpuratus* PP/orcokinin-type precursor 2 [GI:390352581]; Ctel, *C. teleta* PP-type precursor [GI:161190484]; Lgig, *L. gigantea* PP-type precursor [GI:163513756]; Dmel, *D. melanogaster* orcokinin precursor [GI:442624594].

**Figure 18.**
Precursors of cysteine-rich peptide hormones and growth factors in *A. rubens*. Predicted signal peptides are shown in blue, putative peptide hormones/growth-factors are shown in red (with cysteine (C) residues underlined), C-terminal glycine (G) residues that are putative substrates for amidation are shown in orange and putative dibasic cleavage sites are shown in green. For ArIGFP1 and ArIGFP2, the C-peptide is shown in black, the D-domain (for ArIGFP1) is shown in olive and the E-domain is shown in maroon.

**Figure 19.**
Alignment of glycoprotein/bursicon hormone-type precursors. Accession numbers for the corresponding precursor proteins are: Arub_GPA2_1, *A. rubens* glycoprotein hormone α-2 (GPA2)-type precursor 1 [GenBank: KT601721]; Arub_GPA2_2, *A. rubens* GPA2-type precursor 2 [GenBank: KT601722]; Arub_GPB5_1, *A. rubens* glycoprotein hormone β-5 (GPB5)-type precursor 1 [GenBank: KT601723], Arub_GPB5_2, *A. rubens* GPB5-type precursor 2 [GenBank: KT601724]; Arub_GPB5_3, *A. rubens* GPB5-type precursor 3 [GenBank: KT601725]; Arub_BursA, *A. rubens* bursicon-α-type precursor [GenBank: KT601726]; Arub_BursB, *A. rubens* bursicon-β-type precursor [GenBank: KT601727]; Hsap_GPA2, *H. sapiens* GPA2 precursor [GI:189491650]; Hsap_GPB5, *H. sapiens* GPB5 precursor [GI:21427593]; Hsap_FSHB, *H. sapiens* follicle-stimulating hormone (FSH) β-precursor [GI:124014246]; Hsap_CGB7, *H. sapiens* chorionic gonadotropin (CG) β-polypeptide 7 precursor [GI:15451749]; Hsap_LSHB, *H. sapiens* luteinizing hormone (LH) β-polypeptide precursor [GI:15431286]; Hsap_TSHB, *H. sapiens* the putative IGF-type receptor (TSH) β-precursor [GI:47479817]; Dmel_GPA2, *D. melanogaster* GPA2 precursor [GI:320546230]; Dmel_TSHB, *D. melanogaster* glycoprotein hormone β-subunit-related protein precursor [GI:21427595]; Dmel_BursA, *D. melanogaster* bursicon-α precursor [GI:665394724]; Dmel_BursB, *D. melanogaster* bursicon-β precursor [GI:62392020].

**Figure 20.**
Alignment of insulin/relaxin/insulin-like growth factor (IGF)-type precursors. Accession numbers for the corresponding precursor proteins are: Arub_Rel1, *A. rubens* relaxin-like gonad-stimulating peptide precursor [GenBank: KT601728]; Arub_Rel2, *A. rubens* relaxin-like peptide precursor 2 [GenBank: KT601729]; Arub_IGF1, *A. rubens* IGF-type precursor 1 [GenBank: KT601730]; Arub_IGF2, *A. rubens* IGF-type precursor 2 [GenBank: KT601731]; Spur_IGF1, *S. purpuratus* IGF-type precursor 1 [GI:390333650]; Spur_IGF2, *S. purpuratus* IGF-type precursor 2 [GI:390333648]; Skow, *S. kowalevskii* IGF-type precursor [GI:187064073]; Bflo1, *B. floridae* IGF-type precursor 1 [JGI:72897]; Bflo2, *B. floridae* IGF-type precursor 2 [JGI:74371]; Bflo3, *B. floridae* IGF-type precursor 3 [JGI:77763]; Bflo4, *B. floridae* IGF-type precursor 4 [JGI:100967]; Hsap_INS, *H. sapiens* insulin (INS) precursor [GI:186429]; Hsap_IGF1, *H. sapiens* IGF precursor [GI:49456676]; Hsap_REL1, *H. sapiens* relaxin-1 precursor [GI:35932]; Hsap_REL2, *H. sapiens* relaxin-2 precursor [GI:35926]; Hsap_REL3, *H. sapiens* relaxin-3 precursor [GI:17484095]; Dmel_INSL1, *D. melanogaster* insulin-like (INSL) peptide 1 precursor [GI:317423340]; Dmel_INSL2, *D. melanogaster* INSL peptide 2 precursor [GI:442631434]; Dmel_INSL3, *D. melanogaster* INSL peptide 3 precursor [GI:221331056]; Dmel_INSL4, *D. melanogaster* INSL peptide 4 precursor [GI:442631435]; Dmel_INSL5, *D. melanogaster* INSL peptide 5 precursor [GI:320545737]; Dmel_INSL6, *D. melanogaster* INSL peptide 6 precursor [GI:442614930]; Dmel_INSL7, *D. melanogaster* INSL peptide 7 precursor [GI:386763756]; Dmel_INSL8, *D. melanogaster* INSL peptide 8 precursor [GI:386771312].

**Figure 21.**
Precursors of putative neuropeptides in *A. rubens* that do not share apparent sequence similarity with known neuropeptide families. Predicted signal peptides are shown in blue, putative peptides are shown in red (with cysteine (C) residues underlined), C-terminal glycine (G) residues that are putative substrates for amidation are shown in orange and putative dibasic cleavage sites are shown in green.

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[1] Beets I, Temmerman L, Janssen T, Schoofs L. 2013. Ancient neuromodulation by vasopressin/oxytocin-related peptides. Worm 2, e24246 (doi:10.4161/worm.24246) - DOI - PMC - PubMed

[2] Beets I, Temmerman L, Janssen T, Schoofs L. 2013. Ancient neuromodulation by vasopressin/oxytocin-related peptides. Worm 2, e24246 (doi:10.4161/worm.24246) - DOI - PMC - PubMed

[3] Taghert PH, Nitabach MN. 2012. Peptide neuromodulation in invertebrate model systems. Neuron 76, 82–97. (doi:10.1016/j.neuron.2012.08.035) - DOI - PMC - PubMed

[4] Taghert PH, Nitabach MN. 2012. Peptide neuromodulation in invertebrate model systems. Neuron 76, 82–97. (doi:10.1016/j.neuron.2012.08.035) - DOI - PMC - PubMed

[5] Grimmelikhuijzen CJP, Williamson M, Hansen GN. 2004. Neuropeptides in cnidarians. In Cell signalling in prokaryotes and lower Metazoa (ed. Fairweather I.), pp. 115–139. Dordrecht, The Netherlands: Springer.

[6] Grimmelikhuijzen CJP, Williamson M, Hansen GN. 2004. Neuropeptides in cnidarians. In Cell signalling in prokaryotes and lower Metazoa (ed. Fairweather I.), pp. 115–139. Dordrecht, The Netherlands: Springer.

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Transcriptomic identification of starfish neuropeptide precursors yields new insights into neuropeptide evolution

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