Abstract
Background: Corticotropin-releasing hormone (CRH) mediates physiological responses to stressors in mammals by triggering pituitary secretion of adrenocorticotropic hormone, which stimulates adrenal release of cortisol. CRH belongs to a family of related neuropeptides that include sauvagine, urotensin-I, and urocortins in vertebrates and the diuretic hormone DH44 in insects, indicating that the evolutionary origin of this neuropeptide family can be traced to the common ancestor of the Bilateria. However, little is known about CRH-type neuropeptides in deuterostome invertebrates. Methods: Here, we used mass spectrometry, mRNA in situ hybridization, and immunohistochemistry to investigate the structure and expression of a CRH-type neuropeptide (ArCRH) in the starfish Asterias rubens (phylum Echinodermata). Results: ArCRH is a 40-residue peptide with N-terminal pyroglutamylation and C-terminal amidation, and it has a widespread pattern of expression in A. rubens. In the central nervous system comprising the circumoral nerve ring and 5 radial nerve cords, ArCRH-expressing cells and fibres were revealed in both the ectoneural region and the hyponeural region, which contains the cell bodies of motoneurons. Accordingly, ArCRH immunoreactivity was detected in innervation of the ampulla and podium of locomotory organs (tube feet), and ArCRH is the first neuropeptide to be identified as a marker for nerve fibres located in the muscle layer of these organs. ArCRH immunoreactivity was also revealed in protractile organs that mediate gas exchange (papulae), the apical muscle, and the digestive system. Conclusions: Our findings provide the first insights into CRH-type neuropeptide expression and function in the unique context of the pentaradially symmetrical body plan of an echinoderm.
Highlights
Investigation of the phylogenetic distribution of Corticotropin-releasing hormone (CRH)/UCN-type neuropeptide signalling in vertebrates by comparative analysis of genome sequence data indicates that a common ancestor of vertebrates would have had 1 gene encoding a CRH/urocortin 1 (UCN1)-type neuropeptide, 1 gene encoding a urocortin 2 (UCN2)/urocortin 3 (UCN3)-type neuropeptide, and 1 gene encoding a receptor for these 2 neuropeptides
Determination of the Structure of the A. rubens CRHType Neuropeptide A. rubens CRH-type neuropeptide (ArCRH) and Comparison with the Sequences of CRH and CRH-Related Peptides in Other Taxa A cDNA encoding the ArCRH precursor (ArCRHP) has been cloned and sequenced [36], confirming a previously reported transcript sequence obtained from analysis of A. rubens neural transcriptome sequence data [35] (GenBank accession number KT601710.1)
We report the first analysis of the molecular structure and expression of a CRH-type neuropeptide in an echinoderm – the starfish A. rubens
Summary
A family of related bioactive peptides was discovered in vertebrates, and more recently genes encoding CRH/sauvagine/urotensin-1-like peptides named urocortin 1 (UCN1), urocortin 2 (UCN2), and urocortin 3 (UCN3) were identified in humans and other mammals [10,11,12]. Investigation of the phylogenetic distribution of CRH/UCN-type neuropeptide signalling in vertebrates by comparative analysis of genome sequence data indicates that a common ancestor of vertebrates would have had 1 gene encoding a CRH/UCN1-type neuropeptide, 1 gene encoding a UCN2/UCN3-type neuropeptide, and 1 gene encoding a receptor for these 2 neuropeptides. Genes encoding CRH-type precursors and CRH-type receptors have been identified in the invertebrate chordates Ciona intestinalis (sub-phylum Urochordata) and Branchiostoma floridae (sub-phylum Cephalochordata), providing insights into the pre-vertebrate origins of CRH-type neuropeptide signalling in the phylum Chordata [17, 18].
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