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The Rise and Fall of TRP-N, an Ancient Family of Mechanogated Ion Channels, in Metazoa
Mechanoreception, the sensing of mechanical forces, is an ancient means of orientation and communication and tightly linked to the evolution of motile animals. In flies, the transient-receptor-potential N protein (TRP-N) was found to be a cilia-associated mechanoreceptor. TRP-N belongs to a large an...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2015
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4494053/ https://www.ncbi.nlm.nih.gov/pubmed/26100409 http://dx.doi.org/10.1093/gbe/evv091 |
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author | Schüler, Andreas Schmitz, Gregor Reft, Abigail Özbek, Suat Thurm, Ulrich Bornberg-Bauer, Erich |
author_facet | Schüler, Andreas Schmitz, Gregor Reft, Abigail Özbek, Suat Thurm, Ulrich Bornberg-Bauer, Erich |
author_sort | Schüler, Andreas |
collection | PubMed |
description | Mechanoreception, the sensing of mechanical forces, is an ancient means of orientation and communication and tightly linked to the evolution of motile animals. In flies, the transient-receptor-potential N protein (TRP-N) was found to be a cilia-associated mechanoreceptor. TRP-N belongs to a large and diverse family of ion channels. Its unusually long N-terminal repeat of 28 ankyrin domains presumably acts as the gating spring by which mechanical energy induces channel gating. We analyzed the evolutionary origins and possible diversification of TRP-N. Using a custom-made set of highly discriminative sequence profiles we scanned a representative set of metazoan genomes and subsequently corrected several gene models. We find that, contrary to other ion channel families, TRP-N is remarkably conserved in its domain arrangements and copy number (1) in all Bilateria except for amniotes, even in the wake of several whole-genome duplications. TRP-N is absent in Porifera but present in Ctenophora and Placozoa. Exceptional multiplications of TRP-N occurred in Cnidaria, independently along the Hydra and the Nematostella lineage. Molecular signals of subfunctionalization can be attributed to different mechanisms of activation of the gating spring. In Hydra this is further supported by in situ hybridization and immune staining, suggesting that at least three paralogs adapted to nematocyte discharge, which is key for predation and defense. We propose that these new candidate proteins help explain the sensory complexity of Cnidaria which has been previously observed but so far has lacked a molecular underpinning. Also, the ancient appearance of TRP-N supports a common origin of important components of the nervous systems in Ctenophores, Cnidaria, and Bilateria. |
format | Online Article Text |
id | pubmed-4494053 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2015 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-44940532015-07-09 The Rise and Fall of TRP-N, an Ancient Family of Mechanogated Ion Channels, in Metazoa Schüler, Andreas Schmitz, Gregor Reft, Abigail Özbek, Suat Thurm, Ulrich Bornberg-Bauer, Erich Genome Biol Evol Research Article Mechanoreception, the sensing of mechanical forces, is an ancient means of orientation and communication and tightly linked to the evolution of motile animals. In flies, the transient-receptor-potential N protein (TRP-N) was found to be a cilia-associated mechanoreceptor. TRP-N belongs to a large and diverse family of ion channels. Its unusually long N-terminal repeat of 28 ankyrin domains presumably acts as the gating spring by which mechanical energy induces channel gating. We analyzed the evolutionary origins and possible diversification of TRP-N. Using a custom-made set of highly discriminative sequence profiles we scanned a representative set of metazoan genomes and subsequently corrected several gene models. We find that, contrary to other ion channel families, TRP-N is remarkably conserved in its domain arrangements and copy number (1) in all Bilateria except for amniotes, even in the wake of several whole-genome duplications. TRP-N is absent in Porifera but present in Ctenophora and Placozoa. Exceptional multiplications of TRP-N occurred in Cnidaria, independently along the Hydra and the Nematostella lineage. Molecular signals of subfunctionalization can be attributed to different mechanisms of activation of the gating spring. In Hydra this is further supported by in situ hybridization and immune staining, suggesting that at least three paralogs adapted to nematocyte discharge, which is key for predation and defense. We propose that these new candidate proteins help explain the sensory complexity of Cnidaria which has been previously observed but so far has lacked a molecular underpinning. Also, the ancient appearance of TRP-N supports a common origin of important components of the nervous systems in Ctenophores, Cnidaria, and Bilateria. Oxford University Press 2015-06-22 /pmc/articles/PMC4494053/ /pubmed/26100409 http://dx.doi.org/10.1093/gbe/evv091 Text en © The Author(s) 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Research Article Schüler, Andreas Schmitz, Gregor Reft, Abigail Özbek, Suat Thurm, Ulrich Bornberg-Bauer, Erich The Rise and Fall of TRP-N, an Ancient Family of Mechanogated Ion Channels, in Metazoa |
title | The Rise and Fall of TRP-N, an Ancient Family of Mechanogated Ion Channels, in Metazoa |
title_full | The Rise and Fall of TRP-N, an Ancient Family of Mechanogated Ion Channels, in Metazoa |
title_fullStr | The Rise and Fall of TRP-N, an Ancient Family of Mechanogated Ion Channels, in Metazoa |
title_full_unstemmed | The Rise and Fall of TRP-N, an Ancient Family of Mechanogated Ion Channels, in Metazoa |
title_short | The Rise and Fall of TRP-N, an Ancient Family of Mechanogated Ion Channels, in Metazoa |
title_sort | rise and fall of trp-n, an ancient family of mechanogated ion channels, in metazoa |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4494053/ https://www.ncbi.nlm.nih.gov/pubmed/26100409 http://dx.doi.org/10.1093/gbe/evv091 |
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