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A Revised Perspective on the Evolution of Troponin I and Troponin T Gene Families in Vertebrates

The troponin (Tn) complex, responsible for the Ca(2+) activation of striated muscle, is composed of three interacting protein subunits: TnC, TnI, and TnT, encoded by TNNC, TNNI, and TNNT genes. TNNI and TNNT are sister gene families, and in mammals the three TNNI paralogs (TNNI1, TNNI2, TNNI3), whic...

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Autores principales: Joyce, William, Ripley, Daniel M, Gillis, Todd, Black, Amanda Coward, Shiels, Holly A, Hoffmann, Federico G
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9825255/
https://www.ncbi.nlm.nih.gov/pubmed/36518048
http://dx.doi.org/10.1093/gbe/evac173
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author Joyce, William
Ripley, Daniel M
Gillis, Todd
Black, Amanda Coward
Shiels, Holly A
Hoffmann, Federico G
author_facet Joyce, William
Ripley, Daniel M
Gillis, Todd
Black, Amanda Coward
Shiels, Holly A
Hoffmann, Federico G
author_sort Joyce, William
collection PubMed
description The troponin (Tn) complex, responsible for the Ca(2+) activation of striated muscle, is composed of three interacting protein subunits: TnC, TnI, and TnT, encoded by TNNC, TNNI, and TNNT genes. TNNI and TNNT are sister gene families, and in mammals the three TNNI paralogs (TNNI1, TNNI2, TNNI3), which encode proteins with tissue-specific expression, are each in close genomic proximity with one of the three TNNT paralogs (TNNT2, TNNT3, TNNT1, respectively). It has been widely presumed that all vertebrates broadly possess genes of these same three classes, although earlier work has overlooked jawless fishes (cyclostomes) and cartilaginous fishes (chimeras, rays, and sharks), which are distantly related to other jawed vertebrates. With a new phylogenetic and synteny analysis of a diverse array of vertebrates including these taxonomic groups, we define five distinct TNNI classes (TNNI1-5), with TNNI4 and TNNI5 being only present in non-amniote vertebrates and typically found in tandem, and four classes of TNNT (TNNT1-4). These genes are located in four genomic loci that were generated by the 2R whole-genome duplications. TNNI3, encoding “cardiac TnI” in tetrapods, was independently lost in cartilaginous and ray-finned fishes. Instead, ray-finned fishes predominantly express TNNI1 in the heart. TNNI5 is highly expressed in shark hearts and contains a N-terminal extension similar to that of TNNI3 found in tetrapod hearts. Given that TNNI3 and TNNI5 are distantly related, this supports the hypothesis that the N-terminal extension may be an ancestral feature of vertebrate TNNI and not an innovation unique to TNNI3, as has been commonly believed.
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spelling pubmed-98252552023-01-09 A Revised Perspective on the Evolution of Troponin I and Troponin T Gene Families in Vertebrates Joyce, William Ripley, Daniel M Gillis, Todd Black, Amanda Coward Shiels, Holly A Hoffmann, Federico G Genome Biol Evol Research Article The troponin (Tn) complex, responsible for the Ca(2+) activation of striated muscle, is composed of three interacting protein subunits: TnC, TnI, and TnT, encoded by TNNC, TNNI, and TNNT genes. TNNI and TNNT are sister gene families, and in mammals the three TNNI paralogs (TNNI1, TNNI2, TNNI3), which encode proteins with tissue-specific expression, are each in close genomic proximity with one of the three TNNT paralogs (TNNT2, TNNT3, TNNT1, respectively). It has been widely presumed that all vertebrates broadly possess genes of these same three classes, although earlier work has overlooked jawless fishes (cyclostomes) and cartilaginous fishes (chimeras, rays, and sharks), which are distantly related to other jawed vertebrates. With a new phylogenetic and synteny analysis of a diverse array of vertebrates including these taxonomic groups, we define five distinct TNNI classes (TNNI1-5), with TNNI4 and TNNI5 being only present in non-amniote vertebrates and typically found in tandem, and four classes of TNNT (TNNT1-4). These genes are located in four genomic loci that were generated by the 2R whole-genome duplications. TNNI3, encoding “cardiac TnI” in tetrapods, was independently lost in cartilaginous and ray-finned fishes. Instead, ray-finned fishes predominantly express TNNI1 in the heart. TNNI5 is highly expressed in shark hearts and contains a N-terminal extension similar to that of TNNI3 found in tetrapod hearts. Given that TNNI3 and TNNI5 are distantly related, this supports the hypothesis that the N-terminal extension may be an ancestral feature of vertebrate TNNI and not an innovation unique to TNNI3, as has been commonly believed. Oxford University Press 2022-12-15 /pmc/articles/PMC9825255/ /pubmed/36518048 http://dx.doi.org/10.1093/gbe/evac173 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://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
Joyce, William
Ripley, Daniel M
Gillis, Todd
Black, Amanda Coward
Shiels, Holly A
Hoffmann, Federico G
A Revised Perspective on the Evolution of Troponin I and Troponin T Gene Families in Vertebrates
title A Revised Perspective on the Evolution of Troponin I and Troponin T Gene Families in Vertebrates
title_full A Revised Perspective on the Evolution of Troponin I and Troponin T Gene Families in Vertebrates
title_fullStr A Revised Perspective on the Evolution of Troponin I and Troponin T Gene Families in Vertebrates
title_full_unstemmed A Revised Perspective on the Evolution of Troponin I and Troponin T Gene Families in Vertebrates
title_short A Revised Perspective on the Evolution of Troponin I and Troponin T Gene Families in Vertebrates
title_sort revised perspective on the evolution of troponin i and troponin t gene families in vertebrates
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9825255/
https://www.ncbi.nlm.nih.gov/pubmed/36518048
http://dx.doi.org/10.1093/gbe/evac173
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