Uptake of osteoblast-derived extracellular vesicles promotes the differentiation of osteoclasts in the zebrafish scale

Kobayashi-Sun, Jingjing; Yamamori, Shiori; Kondo, Mao; Kuroda, Junpei; Ikegame, Mika; Suzuki, Nobuo; Kitamura, Kei; Hattori, Atsuhiko; Yamaguchi, Masatoshi; Kobayashi, Isao

doi:10.1038/s42003-020-0925-1

Cited by 52 publications

(36 citation statements)

References 54 publications

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“…In an alternative scenario, our observation of upregulated osteogenic transcripts in osteoclasts could reflect the uptake of osteoblast-released exosomes, a process that was recently shown to occur in regenerating zebrafish scales. (64) These osteoblast-derived exosomes could not only contain factors driving osteoclast differentiation, as reported by Kobayashi-Sun and colleagues, (64) but also osteogenic mRNAs. However, we observed that the majority of upregulated osteogenic genes (i) is already expressed at basal levels in noninduced macrophages, and (ii) encode secreted or transmembrane proteins.…”

Section: Dynamic Transcriptome Changes In Activated Macrophages Suggementioning

confidence: 63%

Macrophages Switch to an Osteo‐Modulatory Profile Upon RANKL Induction in a Medaka (Oryzias latipes) Osteoporosis Model

et al. 2020

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In mammals, osteoclasts differentiate from macrophages in the monocyte lineage. Although many factors driving osteoclast formation are known, the detailed processes underlying precursor recruitment, differentiation, and interaction of macrophages with other cell types involved in bone remodeling are poorly understood. Using live imaging in a transgenic medaka osteoporosis model, where ectopic osteoclasts are induced by RANKL expression, we show that a subset of macrophages is recruited to bone matrix to physically interact with bone-forming osteoblast progenitors. These macrophages subsequently differentiate into cathepsin K-(ctsk-) positive osteoclasts. One day later, other macrophages are recruited to clear dying osteoclasts from resorbed bone by phagocytosis. To better understand the molecular changes underlying these dynamic processes, we performed transcriptome profiling of activated macrophages upon RANKL induction. This revealed an upregulation of several bone-related transcripts. Besides osteoclast markers, we unexpectedly also found expression of osteoblast-promoting signals in activated macrophages, suggesting a possible non-cell autonomous role in osteogenesis. Finally, we show that macrophage differentiation into osteoclasts is dependent on inflammatory signals. Medaka deficient for TNFα or treated with the TNFα-inhibitor pentoxifylline exhibited impaired macrophage recruitment and osteoclast differentiation. These results show the involvement of inflammatory signals and the dynamics of a distinct subset of macrophages during osteoclast formation.

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Section: Dynamic Transcriptome Changes In Activated Macrophages Suggementioning

confidence: 63%

Macrophages Switch to an Osteo‐Modulatory Profile Upon RANKL Induction in a Medaka (Oryzias latipes) Osteoporosis Model

et al. 2020

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“…Fractured zebrafish scales revealed a previously unrecognized cellular mechanism of osteoblast–osteoclast communication via osteoblast‐derived extracellular vesicles promoting osteoclast differentiation. ( 255 )…”

Section: Modeling Hormonal Bone Disorders In Zebrafish Fins and Scalesmentioning

confidence: 99%

Skeletal Biology and Disease Modeling in Zebrafish

Dietrich

Fiedler

Kurzyukova

et al. 2020

Journal of Bone and Mineral Research

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Zebrafish are teleosts (bony fish) that share with mammals a common ancestor belonging to the phylum Osteichthyes, from which their endoskeletal systems have been inherited. Indeed, teleosts and mammals have numerous genetically conserved features in terms of skeletal elements, ossification mechanisms, and bone matrix components in common. Yet differences related to bone morphology and function need to be considered when investigating zebrafish in skeletal research. In this review, we focus on zebrafish skeletal architecture with emphasis on the morphology of the vertebral column and associated anatomical structures. We provide an overview of the different ossification types and osseous cells in zebrafish and describe bone matrix composition at the microscopic tissue level with a focus on assessing mineralization. Processes of bone formation also strongly depend on loading in zebrafish, as we elaborate here. Furthermore, we illustrate the high regenerative capacity of zebrafish bones and present some of the technological advantages of using zebrafish as a model. We highlight zebrafish axial and fin skeleton patterning mechanisms, metabolic bone disease such as after immunosuppressive glucocorticoid treatment, as well as osteogenesis imperfecta (OI) and osteopetrosis research in zebrafish. We conclude with a view of why larval zebrafish xenografts are a powerful tool to study bone metastasis. © 2021 American Society for Bone and Mineral Research (ASBMR).

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“…This indicates that the autophagy activity may be upregulated during the repair response and suggests a role for autophagy in bone repair. Similarly, these tools could also be utilised within the zebrafish scale system which was recently used to model the fracture repair response (Kobayashi-Sun et al 2020 ). Using both of these models, the impact of autophagy modulating drugs, such as rapamycin, on the rate of fracture repair could be explored.…”

Section: Current Tools Available To Study Autophagy In Zebrafishmentioning

confidence: 99%

Zebrafish as a model to study autophagy and its role in skeletal development and disease

Hammond

Lane

2020

Histochem Cell Biol

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In the last twenty years, research using zebrafish as a model organism has increased immensely. With the many advantages that zebrafish offer such as high fecundity, optical transparency, ex vivo development, and genetic tractability, they are well suited to studying developmental processes and the effect of genetic mutations. More recently, zebrafish models have been used to study autophagy. This important protein degradation pathway is needed for cell and tissue homeostasis in a variety of contexts. Correspondingly, its dysregulation has been implicated in multiple diseases including skeletal disorders. In this review, we explore how zebrafish are being used to study autophagy in the context of skeletal development and disease, and the ways these areas are intersecting to help identify potential therapeutic targets for skeletal disorders.

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Uptake of osteoblast-derived extracellular vesicles promotes the differentiation of osteoclasts in the zebrafish scale

Cited by 52 publications

References 54 publications

Macrophages Switch to an Osteo‐Modulatory Profile Upon RANKL Induction in a Medaka (Oryzias latipes) Osteoporosis Model

Macrophages Switch to an Osteo‐Modulatory Profile Upon RANKL Induction in a Medaka (Oryzias latipes) Osteoporosis Model

Skeletal Biology and Disease Modeling in Zebrafish

Zebrafish as a model to study autophagy and its role in skeletal development and disease

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