The myogenic electric organ of Sternopygus macrurus: a non-contractile tissue with a skeletal muscle transcriptome
In most electric fish species, the electric organ (EO) derives from striated muscle cells that suppress many muscle properties. In the gymnotiform Sternopygus macrurus, mature electrocytes, the current-producing cells of the EO, do not contain sarcomeres, yet they continue to make some cytoskeletal...
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PeerJ Inc.
2016-04-01
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author | Matthew Pinch Robert Güth Manoj P. Samanta Alexander Chaidez Graciela A. Unguez |
author_facet | Matthew Pinch Robert Güth Manoj P. Samanta Alexander Chaidez Graciela A. Unguez |
author_sort | Matthew Pinch |
collection | DOAJ |
description | In most electric fish species, the electric organ (EO) derives from striated muscle cells that suppress many muscle properties. In the gymnotiform Sternopygus macrurus, mature electrocytes, the current-producing cells of the EO, do not contain sarcomeres, yet they continue to make some cytoskeletal and sarcomeric proteins and the muscle transcription factors (MTFs) that induce their expression. In order to more comprehensively examine the transcriptional regulation of genes associated with the formation and maintenance of the contractile sarcomere complex, results from expression analysis using qRT-PCR were informed by deep RNA sequencing of transcriptomes and miRNA compositions of muscle and EO tissues from adult S. macrurus. Our data show that: (1) components associated with the homeostasis of the sarcomere and sarcomere-sarcolemma linkage were transcribed in EO at levels similar to those in muscle; (2) MTF families associated with activation of the skeletal muscle program were not differentially expressed between these tissues; and (3) a set of microRNAs that are implicated in regulation of the muscle phenotype are enriched in EO. These data support the development of a unique and highly specialized non-contractile electrogenic cell that emerges from a striated phenotype and further differentiates with little modification in its transcript composition. This comprehensive analysis of parallel mRNA and miRNA profiles is not only a foundation for functional studies aimed at identifying mechanisms underlying the transcription-independent myogenic program in S. macrurus EO, but also has important implications to many vertebrate cell types that independently activate or suppress specific features of the skeletal muscle program. |
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spelling | doaj.art-eca2631cae7843cb9bc52c6b409734fc2023-12-03T10:52:41ZengPeerJ Inc.PeerJ2167-83592016-04-014e182810.7717/peerj.1828The myogenic electric organ of Sternopygus macrurus: a non-contractile tissue with a skeletal muscle transcriptomeMatthew Pinch0Robert Güth1Manoj P. Samanta2Alexander Chaidez3Graciela A. Unguez4Department of Biology, New Mexico State University, Las Cruces, NM, United StatesDepartment of Biology, New Mexico State University, Las Cruces, NM, United StatesSystemix Institute, Redmond, WA, United StatesDepartment of Biology, New Mexico State University, Las Cruces, NM, United StatesDepartment of Biology, New Mexico State University, Las Cruces, NM, United StatesIn most electric fish species, the electric organ (EO) derives from striated muscle cells that suppress many muscle properties. In the gymnotiform Sternopygus macrurus, mature electrocytes, the current-producing cells of the EO, do not contain sarcomeres, yet they continue to make some cytoskeletal and sarcomeric proteins and the muscle transcription factors (MTFs) that induce their expression. In order to more comprehensively examine the transcriptional regulation of genes associated with the formation and maintenance of the contractile sarcomere complex, results from expression analysis using qRT-PCR were informed by deep RNA sequencing of transcriptomes and miRNA compositions of muscle and EO tissues from adult S. macrurus. Our data show that: (1) components associated with the homeostasis of the sarcomere and sarcomere-sarcolemma linkage were transcribed in EO at levels similar to those in muscle; (2) MTF families associated with activation of the skeletal muscle program were not differentially expressed between these tissues; and (3) a set of microRNAs that are implicated in regulation of the muscle phenotype are enriched in EO. These data support the development of a unique and highly specialized non-contractile electrogenic cell that emerges from a striated phenotype and further differentiates with little modification in its transcript composition. This comprehensive analysis of parallel mRNA and miRNA profiles is not only a foundation for functional studies aimed at identifying mechanisms underlying the transcription-independent myogenic program in S. macrurus EO, but also has important implications to many vertebrate cell types that independently activate or suppress specific features of the skeletal muscle program.https://peerj.com/articles/1828.pdfTranscriptomeSkeletal muscleElectric organElectric fishMyogenic regulatory factorsMyogenic transcriptome |
spellingShingle | Matthew Pinch Robert Güth Manoj P. Samanta Alexander Chaidez Graciela A. Unguez The myogenic electric organ of Sternopygus macrurus: a non-contractile tissue with a skeletal muscle transcriptome PeerJ Transcriptome Skeletal muscle Electric organ Electric fish Myogenic regulatory factors Myogenic transcriptome |
title | The myogenic electric organ of Sternopygus macrurus: a non-contractile tissue with a skeletal muscle transcriptome |
title_full | The myogenic electric organ of Sternopygus macrurus: a non-contractile tissue with a skeletal muscle transcriptome |
title_fullStr | The myogenic electric organ of Sternopygus macrurus: a non-contractile tissue with a skeletal muscle transcriptome |
title_full_unstemmed | The myogenic electric organ of Sternopygus macrurus: a non-contractile tissue with a skeletal muscle transcriptome |
title_short | The myogenic electric organ of Sternopygus macrurus: a non-contractile tissue with a skeletal muscle transcriptome |
title_sort | myogenic electric organ of sternopygus macrurus a non contractile tissue with a skeletal muscle transcriptome |
topic | Transcriptome Skeletal muscle Electric organ Electric fish Myogenic regulatory factors Myogenic transcriptome |
url | https://peerj.com/articles/1828.pdf |
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