Genome-wide analysis of intermuscular bone development reveals changes of key genes expression and signaling pathways in blunt snout bream (Megalobrama amblycephala)

Chen, Jing; Chen, Xiuli; Huang, Xin; Huang, Guanghua; Gao, Zexia; Wang, Weimin; Liu, Han

doi:10.1016/j.ygeno.2020.09.062

Cited by 12 publications

(4 citation statements)

References 51 publications

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“…For a controlled breeding of cyprinid fish species without IBs, significant progress could be made by understanding the mechanism of IB formation [ 8 , 13 , 26 ] and by identifying the key genes that regulate the process. Recent studies have demonstrated the involvement of tendons and osteoblasts in IB formation [ 8 , 27 ]. Here, we specifically identified four cell clusters related to tendons and IBs (tendon progenitor cells, mature tenocytes, differentiating tenocytes and osteoblasts).…”

Section: Discussionmentioning

confidence: 99%

Single-cell transcriptomes and runx2b−/− mutants reveal the genetic signatures of intermuscular bone formation in zebrafish

Nie

Wan

Chen

et al. 2022

National Science Review

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Intermuscular bones (IBs) are mineralized spicules, present in the myosepta of many, but not all teleost species. IBs are often small and sharp, and they consequently limit how the fish can be processed, cause injury or trauma if lodged in consumers' throat or mouth and therefore affect the appeal of the fish to many consumers. The development of IBs in teleosts is still not fully understood and the molecular basis of IB development remains to be established. Here, the characteristics of IB tissue is evaluated based on single-cell transcriptomic in wild-type zebrafish. The analysis defined 18 distinct cell types. Differentiation trajectories showed that IBs are derived from tendons and that a core tendon-osteoblast cell lineage is related to IB formation. In particular, the functions of 10 candidate genes were evaluated via CRISPR-Cas9 mutants. Among those, runx2b−/− mutants completely lost IBs, while swimming performance, growth, and bone mineral density were not significantly different form runx2b+/+zebrafish. Comparative scRNA-seq analysis in runx2b−/−and runx2b+/+zebrafish revealed the role of osteoblasts in IB formation. In addition, differentially expressed genes were enriched in TGF-β/BMP pathway after runx2b deletion. This study provide evidence for a crucial role of runx2b regulation in IB formation. Genetic breeding can target runx2b regulation and generate strains of commercial fish species without IBs, which can improve the safe consumption and economic value of many farmed fish species.

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Section: Discussionmentioning

confidence: 99%

Single-cell transcriptomes and runx2b−/− mutants reveal the genetic signatures of intermuscular bone formation in zebrafish

Nie

Wan

Chen

et al. 2022

National Science Review

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“…Three pathways, respectively, for cardiac muscle contraction, regulation of actin cytoskeleton, and vascular smooth muscle contraction have certain correlations with muscle contraction. Previous research has demonstrated that IBs may be associated with the regulation of muscle contraction [ 12 , 31 , 32 ]. Bone is isolated by a layer of osteoblasts connected by tight and gap junctions with unique cellular functions and complex molecular composition [ 33 ].…”

Section: Discussionmentioning

confidence: 99%

“…Additionally, a previous study with histological–transcriptomic–proteomic data suggested that IBs are gradually formed through intramembranous ossification without a cartilaginous phase [ 11 ]. Another study compared the orthologous gene families of fish with and without IBs and demonstrated the functional importance of key signaling pathways associated with IB formation [ 12 ]. Some studies have characterized the expression of some genes related to IB development, such as sclerostin ( sost ) in Carassius auratus [ 13 ], tenomodulin ( tnmd ) and bone morphogenetic protein s ( bmps ) in M. amblycephala [ 14 ], and muscle segment homeobox 3 ( msx 3 ) in Hemibarbus labeo [ 15 ], and the influence of some genes on IB formation has also been verified.…”

Section: Introductionmentioning

confidence: 99%

Comparison of Myosepta Development and Transcriptome Profiling between Blunt Snout Bream with and Tilapia without Intermuscular Bones

Zhou

Chang

Chen

et al. 2021

Biology

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Intermuscular bones (IBs) are small spicule-like bones located in the myosepta of basal teleosts, which negatively affect the edibleness and economic value of fish. Blunt snout bream (Megalobrama amblycephala, with epineural and epipleural IBs) and tilapia (Oreochromis niloticus, without epineural and epipleural IBs) are two major aquaculture species and ideal models for studying the formation mechanisms of fish IBs. Here, we compared myosepta development between M. amblycephala and O. niloticus, based on histological analysis, transcriptome profiling, and expression analysis of bone-related genes. The histological results showed that dye condensation began to appear in the myosepta 20 days post hatching (dph) in M. amblycephala, and IBs could be clearly observed 50 dph in the myosepta, based on different staining methods. However, in O. niloticus, dye condensation was not observed in the myosepta from 10 to 60 dph. Differentially expressed genes (DEGs) at different developmental stages were screened by comparing the transcriptomes of M. amblycephala and O. niloticus, and KEGG analysis demonstrated that these DEGs were enriched in many bone-related pathways, such as focal adhesion, calcium, and Wnt signaling pathways. Quantitative PCR was performed to further compare the expression levels of some bone-related genes (scxa, scxb, runx2a, runx2b, bgp, sp7, col1a2, entpd5a, entpd5b, phex, alpl, and fgf23). All the tested genes (except for alpl) exhibited higher expression levels in M. amblycephala than in O. niloticus. A comparison of the dorsal and abdominal muscle tissues between the two species also revealed significant expression differences for most of the tested genes. The results suggest that scxa, scxb, runx2a, runx2b, entpd5a, col1a2, and bgp may play important roles in IB development. Our findings provide some insights into the molecular mechanisms of IB formation, as well as clues for further functional analysis of the identified genes to better understand the development of IBs.

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“…Intramembranous ossification is the direct differentiation of mesenchymal cells into osteoblasts without forming cartilage ( Gilbert & Barresi, 2016 ). Transcriptome data from the blunt snout bream show that chondrocyte-related genes, including col2a1 , ihha , mmp13 , sox9 , timp2a , fgfr3 , and ctgfa , are expressed at higher levels in stage 1 (S1), but at lower levels in stages 2 (S2) and 3 (S3) during IB development ( Chen et al, 2021a ).…”

Section: Origins Of Ibsmentioning

confidence: 99%

Molecular mechanisms of intermuscular bone development in fish: a review

Li¹,

Zhang²,

Liu³

et al. 2021

Zoological Research

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Intermuscular bones (IBs) are slender linear bones embedded in muscle, which ossify from tendons through a process of intramembranous ossification, and only exist in basal teleosts. IBs are essential for fish swimming, but they present a choking risk during human consumption, especially in children, which can lead to commercial risks that have a negative impact on the aquaculture of these fish. In this review, we discuss the morphogenesis and functions of IBs, including their underlying molecular mechanisms, as well as the advantages and disadvantages of different methods for IB studies and techniques for breeding and generating IB-free fish lines. This review reveals that the many key genes involved in tendon development, osteoblast differentiation, and bone formation, e.g., scxa , msxC , sost , twist , bmps , and osterix , also play roles in IB development. Thus, this paper provides useful information for the breeding of new fish strains without IBs via genome editing and artificial selection.

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Genome-wide analysis of intermuscular bone development reveals changes of key genes expression and signaling pathways in blunt snout bream (Megalobrama amblycephala)

Cited by 12 publications

References 51 publications

Single-cell transcriptomes and runx2b−/− mutants reveal the genetic signatures of intermuscular bone formation in zebrafish

Single-cell transcriptomes and runx2b−/− mutants reveal the genetic signatures of intermuscular bone formation in zebrafish

Comparison of Myosepta Development and Transcriptome Profiling between Blunt Snout Bream with and Tilapia without Intermuscular Bones

Molecular mechanisms of intermuscular bone development in fish: a review

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