Dataset Information

Mechanisms of muscle gene regulation in the electric organ of Sternopygus macrurus.

ABSTRACT: Animals perform a remarkable diversity of movements through the coordinated mechanical contraction of skeletal muscle. This capacity for a wide range of movements is due to the presence of muscle cells with a very plastic phenotype that display many different biochemical, physiological and morphological properties. What factors influence the maintenance and plasticity of differentiated muscle fibers is a fundamental question in muscle biology. We have exploited the remarkable potential of skeletal muscle cells of the gymnotiform electric fish Sternopygus macrurus to trans-differentiate into electrocytes, the non-contractile electrogenic cells of the electric organ (EO), to investigate the mechanisms that regulate the skeletal muscle phenotype. In S. macrurus, mature electrocytes possess a phenotype that is intermediate between muscle and non-muscle cells. How some genes coding for muscle-specific proteins are downregulated while others are maintained, and novel genes are upregulated, is an intriguing problem in the control of skeletal muscle and EO phenotype. To date, the intracellular and extracellular factors that generate and maintain distinct patterns of gene expression in muscle and EO have not been defined. Expression studies in S. macrurus have started to shed light on the role that transcriptional and post-transcriptional events play in regulating specific muscle protein systems and the muscle phenotype of the EO. In addition, these findings also represent an important step toward identifying mechanisms that affect the maintenance and plasticity of the muscle cell phenotype for the evolution of highly specialized non-contractile tissues.

SUBMITTER: Guth R

PROVIDER: S-EPMC3680507 | biostudies-other | 2013 Jul

REPOSITORIES: biostudies-other

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Mechanisms of muscle gene regulation in the electric organ of Sternopygus macrurus.

Güth Robert R Pinch Matthew M Unguez Graciela A GA

The Journal of experimental biology 20130701 Pt 13

Animals perform a remarkable diversity of movements through the coordinated mechanical contraction of skeletal muscle. This capacity for a wide range of movements is due to the presence of muscle cells with a very plastic phenotype that display many different biochemical, physiological and morphological properties. What factors influence the maintenance and plasticity of differentiated muscle fibers is a fundamental question in muscle biology. We have exploited the remarkable potential of skelet ...[more]

PMID: 23761472

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Project description:BackgroundAfrican weakly-electric fishes of the family Mormyridae are able to produce and perceive weak electric signals (typically less than one volt in amplitude) owing to the presence of a specialized, muscle-derived electric organ (EO) in their tail region. Such electric signals, also known as Electric Organ Discharges (EODs), are used for objects/prey localization, for the identification of conspecifics, and in social and reproductive behaviour. This feature might have promoted the adaptive radiation of this family by acting as an effective pre-zygotic isolation mechanism. Despite the physiological and evolutionary importance of this trait, the investigation of the genetic basis of its function and modification has so far remained limited. In this study, we aim at: i) identifying constitutive differences in terms of gene expression between electric organ and skeletal muscle (SM) in two mormyrid species of the genus Campylomormyrus: C. compressirostris and C. tshokwe, and ii) exploring cross-specific patterns of gene expression within the two tissues among C. compressirostris, C. tshokwe, and the outgroup species Gnathonemus petersii.ResultsTwelve paired-end (100 bp) strand-specific RNA-seq Illumina libraries were sequenced, producing circa 330 M quality-filtered short read pairs. The obtained reads were assembled de novo into four reference transcriptomes. In silico cross-tissue DE-analysis allowed us to identify 271 shared differentially expressed genes between EO and SM in C. compressirostris and C.tshokwe. Many of these genes correspond to myogenic factors, ion channels and pumps, and genes involved in several metabolic pathways. Cross-species analysis has revealed that the electric organ transcriptome is more variable in terms of gene expression levels across species than the skeletal muscle transcriptome.ConclusionsThe data obtained indicate that: i) the loss of contractile activity and the decoupling of the excitation-contraction processes are reflected by the down-regulation of the corresponding genes in the electric organ's transcriptome; ii) the metabolic activity of the EO might be specialized towards the production and turn-over of membrane structures; iii) several ion channels are highly expressed in the EO in order to increase excitability; iv) several myogenic factors might be down-regulated by transcription repressors in the EO.

Project description:Electric organs (EOs) have evolved independently in vertebrates six times from skeletal muscle (SM). The transcriptional changes accompanying this developmental transformation are not presently well understood. Mormyrids and gymnotiforms are two highly convergent groups of weakly electric fish that have independently evolved EOs: while much is known about development and gene expression in gymnotiforms, very little is known about development and gene expression in mormyrids. This lack of data limits prospects for comparative work. We report here on the characterization of 28 differentially expressed genes between SM and EO tissues in the mormyrid Brienomyrus brachyistius, which were identified using suppressive subtractive hybridization (SSH). Forward and reverse SSH was performed on tissue samples of EO and SM resulting in one cDNA library enriched with mRNAs expressed in EO, and a second library representing mRNAs unique to SM. Nineteen expressed sequence tags (ESTs) were identified in EO and nine were identified in SM using BLAST searching of Danio rerio sequences available in NCBI databases. We confirmed differential expression of all 28 ESTs using RT-PCR. In EO, these ESTs represent four classes of proteins: (1) ion pumps, including the ?- and ?-subunits of Na(+)/K(+)-ATPase, and a plasma membrane Ca(2+)-ATPase; (2) Ca(2+)-binding protein S100, several parvalbumin paralogs, calcyclin-binding protein and neurogranin; (3) sarcomeric proteins troponin I, myosin heavy chain and actin-related protein complex subunit 3 (Arcp3); and (4) the transcription factors enhancer of rudimentary homolog (ERH) and myocyte enhancer factor 2A (MEF2A). Immunohistochemistry and western blotting were used to demonstrate the translation of seven proteins (myosin heavy chain, Na(+)/K(+)-ATPase, plasma membrane Ca(2+)-ATPase, MEF2, troponin and parvalbumin) and their cellular localization in EO and SM. Our findings suggest that mormyrids express several paralogs of muscle-specific genes and the proteins they encode in EOs, unlike gymnotiforms, which may post-transcriptionally repress several sarcomeric proteins. In spite of the similarity in the physiology and function of EOs in mormyrids and gymnotiforms, this study indicates that the mechanisms of development in the two groups may be considerably different.

Dataset Information

Mechanisms of muscle gene regulation in the electric organ of Sternopygus macrurus.

Publications

Mechanisms of muscle gene regulation in the electric organ of Sternopygus macrurus.

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