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Somatostatin-type and allatostatin-C–type neuropeptides are paralogous and have opposing myoregulatory roles in an echinoderm

Somatostatin (SS) and allatostatin-C (ASTC) are inhibitory neuropeptides in chordates and protostomes, respectively, which hitherto were identified as orthologs. However, echinoderms have two SS/ASTC-type neuropeptides (SS1 and SS2), and here, our analysis of sequence data indicates that SS1 is an o...

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Autores principales: Zhang, Ya, Yañez-Guerra, Luis Alfonso, Tinoco, Ana B., Escudero Castelán, Nayeli, Egertová, Michaela, Elphick, Maurice R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8851493/
https://www.ncbi.nlm.nih.gov/pubmed/35145030
http://dx.doi.org/10.1073/pnas.2113589119
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author Zhang, Ya
Yañez-Guerra, Luis Alfonso
Tinoco, Ana B.
Escudero Castelán, Nayeli
Egertová, Michaela
Elphick, Maurice R.
author_facet Zhang, Ya
Yañez-Guerra, Luis Alfonso
Tinoco, Ana B.
Escudero Castelán, Nayeli
Egertová, Michaela
Elphick, Maurice R.
author_sort Zhang, Ya
collection PubMed
description Somatostatin (SS) and allatostatin-C (ASTC) are inhibitory neuropeptides in chordates and protostomes, respectively, which hitherto were identified as orthologs. However, echinoderms have two SS/ASTC-type neuropeptides (SS1 and SS2), and here, our analysis of sequence data indicates that SS1 is an ortholog of ASTC and SS2 is an ortholog of SS. The occurrence of both SS-type and ASTC-type neuropeptides in echinoderms provides a unique context to compare their physiological roles. Investigation of the expression and actions of the ASTC-type neuropeptide ArSS1 in the starfish Asterias rubens revealed that it causes muscle contraction (myoexcitation), contrasting with myoinhibitory effects of the SS-type neuropeptide ArSS2. Our findings suggest that SS-type and ASTC-type neuropeptides are paralogous and originated by gene duplication in a common ancestor of the Bilateria, with only one type being retained in chordates (SS) and protostomes (ASTC) but with both types being retained in echinoderms. Loss of ASTC-type and SS-type neuropeptides in chordates and protostomes, respectively, may have been due to their functional redundancy as inhibitory regulators of physiological processes. Conversely, the retention of both neuropeptide types in echinoderms may be a consequence of the evolution of a myoexcitatory role for ASTC-type neuropeptides mediated by as yet unknown signaling mechanisms.
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spelling pubmed-88514932022-02-18 Somatostatin-type and allatostatin-C–type neuropeptides are paralogous and have opposing myoregulatory roles in an echinoderm Zhang, Ya Yañez-Guerra, Luis Alfonso Tinoco, Ana B. Escudero Castelán, Nayeli Egertová, Michaela Elphick, Maurice R. Proc Natl Acad Sci U S A Biological Sciences Somatostatin (SS) and allatostatin-C (ASTC) are inhibitory neuropeptides in chordates and protostomes, respectively, which hitherto were identified as orthologs. However, echinoderms have two SS/ASTC-type neuropeptides (SS1 and SS2), and here, our analysis of sequence data indicates that SS1 is an ortholog of ASTC and SS2 is an ortholog of SS. The occurrence of both SS-type and ASTC-type neuropeptides in echinoderms provides a unique context to compare their physiological roles. Investigation of the expression and actions of the ASTC-type neuropeptide ArSS1 in the starfish Asterias rubens revealed that it causes muscle contraction (myoexcitation), contrasting with myoinhibitory effects of the SS-type neuropeptide ArSS2. Our findings suggest that SS-type and ASTC-type neuropeptides are paralogous and originated by gene duplication in a common ancestor of the Bilateria, with only one type being retained in chordates (SS) and protostomes (ASTC) but with both types being retained in echinoderms. Loss of ASTC-type and SS-type neuropeptides in chordates and protostomes, respectively, may have been due to their functional redundancy as inhibitory regulators of physiological processes. Conversely, the retention of both neuropeptide types in echinoderms may be a consequence of the evolution of a myoexcitatory role for ASTC-type neuropeptides mediated by as yet unknown signaling mechanisms. National Academy of Sciences 2022-02-10 2022-02-15 /pmc/articles/PMC8851493/ /pubmed/35145030 http://dx.doi.org/10.1073/pnas.2113589119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Biological Sciences
Zhang, Ya
Yañez-Guerra, Luis Alfonso
Tinoco, Ana B.
Escudero Castelán, Nayeli
Egertová, Michaela
Elphick, Maurice R.
Somatostatin-type and allatostatin-C–type neuropeptides are paralogous and have opposing myoregulatory roles in an echinoderm
title Somatostatin-type and allatostatin-C–type neuropeptides are paralogous and have opposing myoregulatory roles in an echinoderm
title_full Somatostatin-type and allatostatin-C–type neuropeptides are paralogous and have opposing myoregulatory roles in an echinoderm
title_fullStr Somatostatin-type and allatostatin-C–type neuropeptides are paralogous and have opposing myoregulatory roles in an echinoderm
title_full_unstemmed Somatostatin-type and allatostatin-C–type neuropeptides are paralogous and have opposing myoregulatory roles in an echinoderm
title_short Somatostatin-type and allatostatin-C–type neuropeptides are paralogous and have opposing myoregulatory roles in an echinoderm
title_sort somatostatin-type and allatostatin-c–type neuropeptides are paralogous and have opposing myoregulatory roles in an echinoderm
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8851493/
https://www.ncbi.nlm.nih.gov/pubmed/35145030
http://dx.doi.org/10.1073/pnas.2113589119
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