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Molecular Mechanisms of Intermuscular Bone Development in Fish: a Review

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Molecular Mechanisms of Intermuscular Bone Development in Fish: a Review Li et al. Zool. Res. 2021, 42(3): 362−376 https://doi.org/10.24272/j.issn.2095-8137.2021.044 Review Open Access Molecular mechanisms of intermuscular bone development in fish: a review Bo Li1,2, Yuan-Wei Zhang3,4, Xiao Liu2, Li Ma1,*, Jun-Xing Yang3,4,* 1 Cave Fish Development and Evolution Research Group, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan 650223, China 2 College of Life Sciences, Capital Normal University, Beijing 100048, China 3 State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Innovative Academy of Seed Design, Chinese Academy of Sciences, Kunming, Yunnan 650223, China 4 Yunnan Key Laboratory of Plateau Fish Breeding, Yunnan Engineering Research Center for Plateau-Lake Health and Restoration, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan 650223, China ABSTRACT Keywords: Intermuscular bones; Molecular Intermuscular bones (IBs) are slender linear bones mechanisms; Intramembranous ossification; Bone embedded in muscle, which ossify from tendons formation; Genome editing; Artificial selection through a process of intramembranous ossification, INTRODUCTION and only exist in basal teleosts. IBs are essential for fish swimming, but they present a choking risk during Vertebrate bones develop from the paraxial mesoderm, lateral human consumption, especially in children, which plate mesoderm, or cranial neural crest, and their can lead to commercial risks that have a negative endochondral ossification occurs in six stages: i.e., impact on the aquaculture of these fish. In this commitment, compaction, proliferation, growth, chondrocyte review, we discuss the morphogenesis and functions death, and bone cell generation (Gilbert & Barresi, 2016). In teleosts, ribs are formed by endochondral ossification. of IBs, including their underlying molecular However, intermuscular bones (IBs), also named mechanisms, as well as the advantages and intramyoseptal bones or myoseptal spines (Bing, 1962), are disadvantages of different methods for IB studies late developing bones that appear after axial skeleton and and techniques for breeding and generating IB-free limb bone formation (Bing, 1962) and form from tendons by fish lines. This review reveals that the many key intramembranous ossification without a cartilage phase. IBs genes involved in tendon development, osteoblast are slender linear structures about one-third to one-half of the differentiation, and bone formation, e.g., scxa, msxC, length of the ribs (Li et al., 2013) and are inserted into the sost, twist, bmps, and osterix, also play roles in IB myosepta between adjacent myomeres (Yang et al., 2019c) development. Thus, this paper provides useful from the head to tail in an orderly manner (Li et al., 2013). These bones only occur in teleosts (Patterson & Johnson, information for the breeding of new fish strains without IBs via genome editing and artificial Received: 07 February 2021; Accepted: 08 May 2021; Online: 17 May selection. 2021 This is an open-access article distributed under the terms of the Foundation items: This work was supported by the National Natural Creative Commons Attribution Non-Commercial License (http:// Science Foundation of China (U1702233 and U1902202), Program of creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted the Chinese Academy of Sciences (XDA24030505 and non-commercial use, distribution, and reproduction in any medium, XDA23080502), and Program of Yunnan Provincial Science and provided the original work is properly cited. Technology Department (202003AD150017 and 2018FY001-007) Copyright ©2021 Editorial Office of Zoological Research, Kunming *Corresponding authors, E-mail: [email protected]; yangjx@mail. Institute of Zoology, Chinese Academy of Sciences kiz.ac.cn 1995). In most basal teleosts, the few occurring IBs are myorhabdoi (Li et al., 2017; Nie et al., 2020). Epicentrals are relatively simple in morphology. In contrast, IBs have located in the central vertebrae of the horizontal septum, completely disappeared in certain teleost lineages, such as epineurals are located above the horizontal septum and the spiny finfish Perciformes (Li et al., 2013; Patterson & attached to the neural arches in the epaxial myoseptum, and Johnson, 1995), but are found in several ancient species, epipleurals are located under the horizontal spetum and such as Pholidophorus bechei Agassiz and Oligopleurus attached to the ribs or hemal arches in the hypaxial (Lund, 1966). In other teleost lineages, e.g., cyprinids, IBs are myoseptum (Gemballa & Britz, 1998; Li et al., 2017; Patterson extremely complex in morphology and range from 73 to 169 in & Johnson, 1995; Yang et al., 2019c). Furthermore, one or number (Yang et al., 2019c). two types of unattached IBs, called myorhabdoi, are also As early as the 1930s, scientists recognized the influence of present in a small number of teleost species (Nie et al., 2020). diet on IB development in carp species (Hirsch, 1938). These myorhabdoi are not attached to the axial skeleton but Although subsequent studies focused on IB number, genetic are located in the ventral and dorsal forward flexures of the variability, and breeding in carp (Bing, 1962; Kossmann, 1972; myoseptum (Patterson & Johnson, 1995). Current data Lieder, 1961; Moav et al., 1975; Sengbusch & Meske, 1967), indicate that basal teleosts (Osteoglossomorpha) only have reducing IBs in such species remains a challenging mission epineurals; Clupeomorpha and Elopomorpha have epineurals, for aquaculturists. In aquaculture, fish species and meat epicentrals, and epipleurals; and Ostariophysi, e.g., quality are of paramount importance in food production. In Cypriniformes and Characiformes, lack epicentrals, 2016, the Food and Agriculture Organization of the United suggesting that epicentrals appeared later and degenerated Nations (FAO) estimated that Cypriniformes species account earlier during evolution (Nie et al., 2020; Yang et al., 2019c). for ~70% of total fish farming production worldwide (Nie et al., In North Atlantic herring (Clupea harengus), IBs are 2020). There are four popular domestic species in China, cylindrical, thin, and fiber-like, and the mid-shaft region has a including black carp (Mylopharyngodon piceus), grass carp homogenous ellipsoidal cross-sectional area. Although tissue (Ctenopharyngodon idella), silver carp (Hypophthalmichthys mineral density (TMD) is not dependent on fish size, crystal molitrix), and bighead carp (Hypophthalmichthys nobilis). In length is larger and Young’s modulus is lower in the IBs of 2018, these species contributed to 26.4% of total finfish large fish compared to small fish (Fiedler et al., 2019). produced from aquaculture worldwide (FAO, 2020). In Relative to mammalian bones (i.e., mouse tibiae), IBs have addition, IB-containing Characiformes species, such as similar TMD, lower Young’s modulus, similar strength, and tambaqui (Colossoma macropomum), account for a higher ductility (Fiedler et al., 2019). In mature IBs of the blunt substantial proportion of consumed fish (142 000 tons in 2016) snout bream (Wuchang bream, Megalobrama amblycephala), and are important commercial species in areas such as the a great number of mature osteoblasts are distributed along the Amazon River basin (Woynárovich & Van Anrooy, 2019). edge of the bone matrix, and osteocytes are apparent in the Fish protein is an important part of a healthy human diet and center area of the bone matrix (Liu et al., 2017). critical for normal physical development in children. However, According to morphological classification, IBs can be IBs increase the risk for choking in adults and children and divided into seven categories: i.e., non-fork type (I-type), one- can cause serious and potentially lethal complications if end-unequal-bi-fork type (卜-type), one-end‐equal‐bi‐fork type ingested (Knight & Lesser, 1989), thus reducing their (Y-type), one‐end‐multi‐fork type, two‐end‐bi‐fork type, two‐ commercial value (Nie et al., 2020). Moreover, IBs increase end‐multi‐fork type, and tree‐branch type (Nie et al., 2020). difficulty in food processing, affect meat freshness, and reduce The IBs in cyprinids are more complex than in other species the commercial value of fish products (Li et al., 2013; Yang et and almost all seven different shaped epineural IBs are al., 2019c). To address these issues, new strains of IB-free represented. Epipleural IBs are simpler than epineurals and fish produced by genome editing and artificial selection would most are non-forked (Nie et al., 2020). be of enormous significance in both basic research and The shape of IBs exhibits a pattern from simple to complex aquaculture. To the best of our knowledge, however, most during evolution from Osteoglossomorpha to Ostariophysi (Lv current research has focused on the number and morphology et al., 2007), during which time IB number increased of IBs, while the molecular mechanisms underlying the gradually, then decreased gradually (Table1). The forked IBs development of IBs remain poorly understood. In this review, start from the non-forked I-type via two evolutionary paths: 1. we discuss current knowledge on the morphogenesis of IBs, I-type — 卜 -type — Y-type — one-end-multi-fork type; 2. I- including inducing factors and molecular mechanisms, as well type — 卜-type — Y-type — two-end-bi-fork type — two-end- as research methods and practical applications for studies on multi -fork type — tree-branch type (Lv et al., 2007). IBs. This paper should provide a theoretical basis
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