Comparative transcriptome analysis of fast twitch muscle and slow twitch muscle in Takifugu rubripes

Gao, Kailun; Wang, Zhicheng; Zhou, Xiaoxu; Wang, Haoze; Kong, Dewen; Jiang, Chen; Wang, Xiuli; Jiang, Zhiqiang; Qiu, Xuemei

doi:10.1016/j.cbd.2017.08.002

Cited by 9 publications

(9 citation statements)

References 53 publications

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“…Gene expression in metabolic pathways differed greatly between the two main muscle fibre types: red and white muscle. The pathways enriched for upregulation in either tissue matched physiological expectations based on measurement of enzyme concentrations [39,47,69], alongside previous studies both in bluefin tuna [49] and other fish [70,71], with upregulation of aerobic metabolism genes in red muscle and anaerobic metabolism genes in white muscle.…”

Section: Metabolic Gene Expression Does Not Differ Between Warm and Csupporting

confidence: 80%

Skeletal muscle and cardiac transcriptomics of a regionally endothermic fish, the Pacific bluefin tuna, Thunnus orientalis

et al. 2020

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Background The Pacific bluefin tuna (Thunnus orientalis) is a regionally endothermic fish that maintains temperatures in their swimming musculature, eyes, brain and viscera above that of the ambient water. Within their skeletal muscle, a thermal gradient exists, with deep muscles, close to the backbone, operating at elevated temperatures compared to superficial muscles near the skin. Their heart, by contrast, operates at ambient temperature, which in bluefin tunas can range widely. Cardiac function in tunas reduces in cold waters, yet the heart must continue to supply blood for metabolically demanding endothermic tissues. Physiological studies indicate Pacific bluefin tuna have an elevated cardiac capacity and increased cold-tolerance compared to warm-water tuna species, primarily enabled by increased capacity for sarcoplasmic reticulum calcium cycling within the cardiac muscles. Results Here, we compare tissue-specific gene-expression profiles of different cardiac and skeletal muscle tissues in Pacific bluefin tuna. There was little difference in the overall expression of calcium-cycling and cardiac contraction pathways between atrium and ventricle. However, expression of a key sarcoplasmic reticulum calcium-cycling gene, SERCA2b, which plays a key role maintaining intracellular calcium stores, was higher in atrium than ventricle. Expression of genes involved in aerobic metabolism and cardiac contraction were higher in the ventricle than atrium. The two morphologically distinct tissues that derive the ventricle, spongy and compact myocardium, had near-identical levels of gene expression. More genes had higher expression in the cool, superficial muscle than in the warm, deep muscle in both the aerobic red muscle (slow-twitch) and anaerobic white muscle (fast-twitch), suggesting thermal compensation. Conclusions We find evidence of widespread transcriptomic differences between the Pacific tuna ventricle and atrium, with potentially higher rates of calcium cycling in the atrium associated with the higher expression of SERCA2b compared to the ventricle. We find no evidence that genes associated with thermogenesis are upregulated in the deep, warm muscle compared to superficial, cool muscle. Heat generation may be enabled by by the high aerobic capacity of bluefin tuna red muscle.

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Section: Metabolic Gene Expression Does Not Differ Between Warm and Csupporting

confidence: 80%

Skeletal muscle and cardiac transcriptomics of a regionally endothermic fish, the Pacific bluefin tuna, Thunnus orientalis

et al. 2020

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“…At the same time, more ATP are synthesized by upregulated ATP synthase using the proton gradients across the inner mitochondrial membrane generated by electron transport ( Chaban, Boekema & Dudkina, 2014 ). Therefore, it was inferred that the higher oxidative phosphorylation to ensure more energy supply for slow-twitch muscle to maintain normal function and development compared to fast-twitch muscle in P. dentex , which was supported by previous studies in other fishes such as T. rubripes , P. mesopotamicus , and Thunnus orientalis ( Mareco et al, 2015 ; Gao et al, 2017 ; Ciezarek et al, 2020 ).…”

Section: Discussionsupporting

confidence: 58%

“…Over the past decades, extensive researches have been conducted on teleost skeletal muscle, the classification of muscle fiber types ( Kronnie et al, 1983 ; Silva et al, 2008 ), the biochemical component distinctions between different muscle types ( Gibb & Dickson, 2002 ), the impact of stress and nutrition on the growth of fast-twitch muscle ( Aedo et al, 2015 ; Magnoni et al, 2015 ), and the function of single gene in muscle differentiation and development ( Chauvigne et al, 2005 ; Macqueen & Johnston, 2006 ) were formulated clearly. Recently, limited studies on comparing the gene expression patterns between fast-twitch and slow-twitch muscles of Takifugu rubripes ( Gao et al, 2017 ), Piaractus mesopotamicus ( Mareco et al, 2015 ), and Schizothorax prenanti ( Li et al, 2019 ), have revealed that the complex transcriptional regulatory mechanisms in both metabolic pathways and structural components. However, given the significant correlation between swimming performance, muscle proportion, and energy metabolism ( Gibb & Dickson, 2002 ; Drazen, Dugan & Friedman, 2013 ; Teulier et al, 2019 ), studies on these species with relatively weak swimming ability were not enough to characterize the molecular components and regulatory mechanisms that control the muscle types of all teleost, especially for highly athletic species.…”

Section: Introductionmentioning

confidence: 99%

Expression profiles and transcript properties of fast-twitch and slow-twitch muscles in a deep-sea highly migratory fish, Pseudocaranx dentex

Wang

Yang

et al. 2022

PeerJ

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Fast-twitch and slow-twitch muscles are the two principal skeletal muscle types in teleost with obvious differences in metabolic and contractile phenotypes. The molecular mechanisms that control and maintain the different muscle types remain unclear yet. Pseudocaranx dentex is a highly mobile active pelagic fish with distinctly differentiated fast-twitch and slow-twitch muscles. Meanwhile, P. dentex has become a potential target species for deep-sea aquaculture because of its considerable economic value. To elucidate the molecular characteristics in the two muscle types of P. dentex, we generated 122 million and 130 million clean reads from fast-twitch and slow-witch muscles using RNA-Seq, respectively. Comparative transcriptome analysis revealed that 2,862 genes were differentially expressed. According to GO and KEGG analysis, the differentially expressed genes (DEGs) were mainly enriched in energy metabolism and skeletal muscle structure related pathways. Difference in the expression levels of specific genes for glycolytic and lipolysis provided molecular evidence for the differences in energy metabolic pathway between fast-twitch and slow-twitch muscles of P. dentex. Numerous genes encoding key enzymes of mitochondrial oxidative phosphorylation pathway were significantly upregulated at the mRNA expression level suggested slow-twitch muscle had a higher oxidative phosphorylation to ensure more energy supply. Meanwhile, expression patterns of the main skeletal muscle developmental genes were characterized, and the expression signatures of Sox8, Myod1, Calpain-3, Myogenin, and five insulin-like growth factors indicated that more myogenic cells of fast-twitch muscle in the differentiating state. The analysis of important skeletal muscle structural genes showed that muscle type-specific expression of myosin, troponin and tropomyosin may lead to the phenotypic structure differentiation. RT-qPCR analysis of twelve DEGs showed a good correlation with the transcriptome data and confirmed the reliability of the results presented in the study. The large-scale transcriptomic data generated in this study provided an overall insight into the thorough gene expression profiles of skeletal muscle in a highly mobile active pelagic fish, which could be valuable for further studies on molecular mechanisms responsible for the diversity and function of skeletal muscle.

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“…The expression levels of genes related to energy metabolism can provide insight into differences in mitochondrial numbers between SM and FM. Here, we compared the expression levels of genes involved in aerobic and anaerobic metabolism in SM and FM using transcriptome data of T. rubripes [19].…”

Section: Gene Signatures Of Energy Metabolism Are Different Between S...mentioning

confidence: 99%

“…This investigation aims to provide insights into how these adaptations effectively meet the cellular bioenergetic requirements of both slow-and fast-twitch muscles. T. rubripes is a commonly found fish in the Yellow Sea, with a fully sequenced genome [16] and extensive research-including transcriptome analysis-on its SM and FM [17][18][19][20]. In addition, its anatomically distinct distribution of different types of skeletal muscles makes T. rubripes an exceptional model for investigating mitochondrial networks in different skeletal muscle types.…”

Section: Introductionmentioning

confidence: 99%

Mitochondrial Homeostasis Regulating Mitochondrial Number and Morphology Is a Distinguishing Feature of Skeletal Muscle Fiber Types in Marine Teleosts

Li,

Wang,

Zeng

et al. 2024

IJMS

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Fishes’ skeletal muscles are crucial for swimming and are differentiated into slow-twitch muscles (SM) and fast-twitch muscles (FM) based on physiological and metabolic properties. Consequently, mitochondrial characteristics (number and morphology) adapt to each fiber type’s specific functional needs. However, the mechanisms governing mitochondrial adaptation to the specific bioenergetic requirements of each fiber type in teleosts remain unclear. To address this knowledge gap, we investigated the mitochondrial differences and mitochondrial homeostasis status (including biogenesis, autophagy, fission, and fusion) between SM and FM in teleosts using Takifugu rubripes as a representative model. Our findings reveal that SM mitochondria are more numerous and larger compared to FM. To adapt to the increased mitochondrial number and size, SM exhibit elevated mitochondrial biogenesis and dynamics (fission/fusion), yet show no differences in mitochondrial autophagy. Our study provides insights into the adaptive mechanisms shaping mitochondrial characteristics in teleost muscles. The abundance and elongation of mitochondria in SM are maintained through elevated mitochondrial biogenesis, fusion, and fission, suggesting an adaptive response to fulfill the bioenergetic demands of SM that rely extensively on OXPHOS in teleosts. Our findings enhance our understanding of mitochondrial adaptations in diverse muscle types among teleosts and shed light on the evolutionary strategies of bioenergetics in fishes.

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Comparative transcriptome analysis of fast twitch muscle and slow twitch muscle in Takifugu rubripes

Cited by 9 publications

References 53 publications

Skeletal muscle and cardiac transcriptomics of a regionally endothermic fish, the Pacific bluefin tuna, Thunnus orientalis

Skeletal muscle and cardiac transcriptomics of a regionally endothermic fish, the Pacific bluefin tuna, Thunnus orientalis

Expression profiles and transcript properties of fast-twitch and slow-twitch muscles in a deep-sea highly migratory fish, Pseudocaranx dentex

Mitochondrial Homeostasis Regulating Mitochondrial Number and Morphology Is a Distinguishing Feature of Skeletal Muscle Fiber Types in Marine Teleosts

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