Analysis of muscle fibre input dynamics using a<i>myog</i>: GFP transgenic trout model

Rescan, Pierre‐Yves; Rallière, Cécile; Lebret, Véronique; Frétaud, Maxence

doi:10.1242/jeb.113704

Cited by 12 publications

(15 citation statements)

References 43 publications

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“…The persistence of myomaker expression in trout white muscle is associated with the persistence of new fiber formation from mosaic hyperplasia. Accordingly, the lowest expression of myomaker was observed in mature fish, when hyperplasia is reduced (20,28).…”

Section: Insertion Of Minisatellites In Trout Myomaker Proteinmentioning

confidence: 94%

Trout myomaker contains 14 minisatellites and two sequence extensions but retains fusogenic function

Landemaine

Ramirez-Martinez

Monestier

et al. 2019

Journal of Biological Chemistry

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The formation of new myofibers in vertebrates occurs by myoblast fusion and requires fusogenic activity of the musclespecific membrane protein myomaker. Here, using in silico (BLAST) genome analyses, we show that the myomaker gene from trout includes 14 minisatellites, indicating that it has an unusual structure compared with those of other animal species. We found that the trout myomaker gene encodes a 434 -amino acid (aa) protein, in accordance with its apparent molecular mass (ϳ40 kDa) observed by immunoblotting. The first half of the trout myomaker protein (1-220 aa) is similar to the 221-aa mouse myomaker protein, whereas the second half (222-234 aa) does not correspond to any known motifs and arises from two protein extensions. The first extension (ϳ70 aa) apparently appeared with the radiation of the bony fish clade Euteleostei, whereas the second extension (up to 236 aa) is restricted to the superorder Protacanthopterygii (containing salmonids and pike) and corresponds to the insertion of minisatellites having a length of 30 nucleotides. According to gene expression analyses, trout myomaker expression is consistently associated with the formation of new myofibers during embryonic development, postlarval growth, and muscle regeneration. Using cell-mixing experiments, we observed that trout myomaker has retained the ability to drive the fusion of mouse fibroblasts with C2C12 myoblasts. Our work reveals that trout myomaker has fusogenic function despite containing two protein extensions.

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Section: Insertion Of Minisatellites In Trout Myomaker Proteinmentioning

confidence: 94%

Trout myomaker contains 14 minisatellites and two sequence extensions but retains fusogenic function

Landemaine

Ramirez-Martinez

Monestier

et al. 2019

Journal of Biological Chemistry

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“…At post-larval stages, new myofibres are formed between existing muscle fibres throughout the myotome, thus producing a typical mosaic appearance in muscle cross sections [2]. A Myog:GFP transgenic trout model has revealed that mosaic hyperplasia is prevalent in the juvenile stage, but progressively decreases as trout age, and eventually ceases at approximately 18 months post-fertilization [7]. Nevertheless, potentially recruitable muscle stem cells are present in muscles of aged trout, as shown by their ability to form myofibres de novo after muscle injury [7, 8].…”

Section: Introductionmentioning

confidence: 99%

Global gene expression in muscle from fasted/refed trout reveals up-regulation of genes promoting myofibre hypertrophy but not myofibre production

et al. 2017

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BackgroundCompensatory growth is a phase of rapid growth, greater than the growth rate of control animals, that occurs after a period of growth-stunting conditions. Fish show a capacity for compensatory growth after alleviation of dietary restriction, but the underlying cellular mechanisms are unknown. To learn more about the contribution of genes regulating hypertrophy (an increase in muscle fibre size) and hyperplasia (the generation of new muscle fibres) in the compensatory muscle growth response in fish, we used high-density microarray analysis to investigate the global gene expression in muscle of trout during a fasting-refeeding schedule and in muscle of control-fed trout displaying normal growth.ResultsThe compensatory muscle growth signature, as defined by genes up-regulated in muscles of refed trout compared with control-fed trout, showed enrichment in functional categories related to protein biosynthesis and maturation, such as RNA processing, ribonucleoprotein complex biogenesis, ribosome biogenesis, translation and protein folding. This signature was also enriched in chromatin-remodelling factors of the protein arginine N-methyl transferase family. Unexpectedly, functional categories related to cell division and DNA replication were not inferred from the molecular signature of compensatory muscle growth, and this signature contained virtually none of the genes previously reported to be up-regulated in hyperplastic growth zones of the late trout embryo myotome and to potentially be involved in production of new myofibres, notably genes encoding myogenic regulatory factors, transmembrane receptors essential for myoblast fusion or myofibrillar proteins predominant in nascent myofibres.ConclusionGenes promoting myofibre growth, but not myofibre formation, were up-regulated in muscles of refed trout compared with continually fed trout. This suggests that a compensatory muscle growth response, resulting from the stimulation of hypertrophy but not the stimulation of hyperplasia, occurs in trout after refeeding. The generation of a large set of genes up-regulated in muscle of refed trout may yield insights into the molecular and cellular mechanisms controlling skeletal muscle mass in teleost and serve as a useful list of potential molecular markers of muscle growth in fish.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-017-3837-9) contains supplementary material, which is available to authorized users.

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“…Genes belonging to this functional category included genes encoding cell division cycle (cdc) 84 proteins (8), cyclin dependent kinases (6), cyclins (6), genes involved in chromosomes segregation 85 (20) as shown in figure 3. Enrichment in gene involved in DNA metabolic process and replication 86 such as minichromosome maintenance complex components, non-homologous end-joining factor1, 87 DNA polymerases, DNA primases, DNA topoisomerases, replication proteins were also found.…”

Section: Myogenic Precursors Extracted From Hyperplasic and Non-hypermentioning

confidence: 99%

“…The second process 31 refers to the formation of new muscle fibers throughout the entire myotome and is termed 32 hyperplasia [1][2][3]. A persistence of hyperplasic growth after juvenile stage was reported in large 33 final size fish as gilthead bream [4], carp [5], european sea bass [6] and rainbow trout [7,8]. 34 Nevertheless, this production of new muscle fibers decreases with age [7], and hyperplasia was no 35 longer observed in 18-months old trout [8].…”

mentioning

confidence: 99%

“…A persistence of hyperplasic growth after juvenile stage was reported in large 33 final size fish as gilthead bream [4], carp [5], european sea bass [6] and rainbow trout [7,8]. 34 Nevertheless, this production of new muscle fibers decreases with age [7], and hyperplasia was no 35 longer observed in 18-months old trout [8]. Furthermore, it is well known that fasting stops growth 36 [9] and an inhibition of in vitro proliferation of myogenic precursors in fasted rainbow trout has 37 been observed [10].…”

mentioning

confidence: 99%

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Histological, transcriptomic andin vitroanalysis reveal an intrinsic activated state of myogenic precursors in hyperplasic muscle of trout

Jagot

Sabin

Cam

et al. 2018

Preprint

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1Background 2The dramatic increase in myotomal muscle mass in post-hatching fish is related to their ability to 3 lastingly produce new muscle fibres, a process termed hyperplasia. The molecular and cellular 4 mechanisms underlying fish muscle hyperplasia largely remain unknown. In this study, we aimed to 5 characterize intrinsic properties of myogenic cells originating from fish hyperplasic muscle. For this 6 purpose, we compared in situ proliferation, in vitro cell behavior and transcriptomic profile of 7 myogenic precursors originating from hyperplasic muscle of juvenile trout (JT) and from non-8 hyperplasic muscle of fasted juvenile trout (FJT) and adult trout (AT). 9 Results 10For the first time, we showed that myogenic precursors proliferate in hyperplasic muscle from JT as 11 shown by in vivo BrdU labeling. This proliferative rate was very low in AT and FJT muscle. 12 Transcriptiomic analysis revealed that myogenic cells from FJT and AT displayed close expression 13 profiles with only 64 differentially expressed genes (BH corrected p-val < 0.001). In contrast, 2623 14 differentially expressed genes were found between myogenic cells from JT and from both FJT and 15 AT. Functional categories related to translation, mitochondrial activity, cell cycle, and myogenic 16 differentiation were inferred from genes up regulated in JT compared to AT and FJT myogenic cells. 17 Conversely, Notch signaling pathway, that signs cell quiescence, was inferred from genes down 18 regulated in JT compared to FJT and AT. In line with our transcriptomic data, in vitro JT myogenic 19 precursors displayed higher proliferation and differentiation capacities than FJT and AT myogenic 20 precursors. 21 Conclusions 22The transcriptomic analysis and examination of cell behavior converge to support the view that 23 myogenic cells extracted from hyperplastic muscle of juvenile trout are intrinsically more potent to 24

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Analysis of muscle fibre input dynamics using amyog: GFP transgenic trout model

Cited by 12 publications

References 43 publications

Trout myomaker contains 14 minisatellites and two sequence extensions but retains fusogenic function

Trout myomaker contains 14 minisatellites and two sequence extensions but retains fusogenic function

Global gene expression in muscle from fasted/refed trout reveals up-regulation of genes promoting myofibre hypertrophy but not myofibre production

Histological, transcriptomic andin vitroanalysis reveal an intrinsic activated state of myogenic precursors in hyperplasic muscle of trout

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