Increased mechanical loading through controlled swimming exercise induces bone formation and mineralization in adult zebrafish

Suniaga, Santiago; Rolvien, Tim; Scheidt, Annika vom; Fiedler, Imke A.K.; Bale, Hrishikesh; Huysseune, Ann; Witten, P. Eckhard; Amling, Michael; Busse, Björn

doi:10.1038/s41598-018-21776-1

Cited by 91 publications

(133 citation statements)

References 67 publications

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“…The Chihuahua zebrafish can be considered as a suitable animal model reflecting osseous changes occurring in human patients suffering from classical dominant OI. Further investigations of this model will be of great value for improving current treatment strategies of OI, particularly in the form of novel drug‐screening tests and drug administration, as well as in the form of conventional therapies including musculoskeletal exercise …”

Section: Discussionmentioning

confidence: 99%

Severely Impaired Bone Material Quality in Chihuahua Zebrafish Resembles Classical Dominant Human Osteogenesis Imperfecta

Fiedler

Schmidt

Wölfel

et al. 2018

Journal of Bone and Mineral Research

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Excessive skeletal deformations and brittle fractures in the vast majority of patients suffering from osteogenesis imperfecta (OI) are a result of substantially reduced bone quality. Because the mechanical competence of bone is dependent on the tissue characteristics at small length scales, it is of crucial importance to assess how OI manifests at the micro- and nanoscale of bone. In this context, the Chihuahua (Chi/+) zebrafish, carrying a heterozygous glycine substitution in the α1 chain of collagen type I, has recently been proposed as a suitable animal model of classical dominant OI, showing skeletal deformities, altered mineralization patterns, and a smaller body size. This study assessed the bone quality properties of Chi/+ at multiple length scales using micro-computed tomography (micro-CT), histomorphometry, quantitative back-scattered electron imaging, Fourier-transform infrared spectroscopy, nanoindentation, and X-ray microscopy. At the skeletal level, the Chi/+ displays smaller body size, deformities, and fracture calli in the ribs. Morphological changes at the whole bone level showed that the vertebrae in Chi/+ had a smaller size, smaller thickness, and distorted shape. At the tissue level, Chi/+ displayed a higher degree of mineralization, lower collagen maturity, lower mineral maturity, altered osteoblast morphology, and lower osteocyte lacunar density compared to wild-type zebrafish. The alterations in the cellular, compositional, and structural properties of Chi/+ bones bear an explanation for the impaired local mechanical properties, which promote an increase in overall bone fragility in Chi/+. The quantitative assessment of bone quality in Chi/+ thus further validates this mutant as an important model reflecting osseous characteristics associated with human classical dominant OI. © 2018 American Society for Bone and Mineral Research.

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Section: Discussionmentioning

confidence: 99%

Severely Impaired Bone Material Quality in Chihuahua Zebrafish Resembles Classical Dominant Human Osteogenesis Imperfecta

Fiedler

Schmidt

Wölfel

et al. 2018

Journal of Bone and Mineral Research

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“…Scans were acquired at 40 kV and 240 μA with a 0.25 mm aluminum filter. Ring artifacts and beam hardening corrections were the same for all scans, during reconstruction with NRecon software (Bruker) according to previously established protocols (Busse et al, 2019;Fiedler et al, 2018;Suniaga et al, 2018).…”

Section: X-ray and µCt Analysesmentioning

confidence: 99%

FGFR3 is a positive regulator of osteoblast expansion and differentiation during zebrafish skull vault development

Dambroise

Ktorza

Brombin

et al. 2020

Preprint

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AbstractGain- or loss-of-function mutations in fibroblast growth factor receptor 3 (FGFR3) result in cranial vault defects - highlighting the protein’s role in membranous ossification. Zebrafish express high levels of fgfr3 during skull development; in order to study FGFR3’s role in cranial vault development, we generated the first fgfr3 loss-of-function zebrafish (fgfr3lof/lof). The mutant fish exhibited major changes in the craniofacial skeleton, with a lack of sutures, abnormal frontal and parietal bones, and the presence of ectopic bones. Integrated analyses (in vivo imaging, and single-cell RNA sequencing of the osteoblast lineage) of zebrafish fgfr3lof/lof revealed a delay in osteoblast expansion and differentiation, together with changes in the extracellular matrix. These findings demonstrate that fgfr3 is a positive regulator of osteogenesis. We hypothesize that changes in the extracellular matrix within growing bone impair cell-cell communication, mineralization, and new osteoblast recruitment.

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“…Different letters indicate significant differences between gill arches, and asterisks denote significant differences between control and treatment groups (p < .05) [Color figure can be viewed at wileyonlinelibrary.com] Bone growth is thought to require dynamic cycles of mechanical loading to stimulate collagen production and mineralization by osteoblasts (DiGirolamo, Kiel, & Esser, 2013;Fiaz, Van Leeuwen, & Kranenbarg, 2010). Mechanical forces during feeding trigger bone growth in cichlid jaws (Witten & Hall, 2015), and swim training similarly increases bone formation and mineralization of Atlantic salmon Salmo salar (Totland et al, 2011) and zebrafish Danio rerio (Fiaz et al, 2012;Suniaga et al, 2018). In water-breathing fishes, the gill arches and filaments would be subject to forces from flowing water, muscular contractions, and distortion caused by movement of the mouth and opercula during the ventilatory cycle.…”

Section: Plasticity Of Gill Filaments and Archesmentioning

confidence: 99%

Gill remodelling during terrestrial acclimation in the amphibious fish Polypterus senegalus

Turko

Maini

Wright

et al. 2019

Journal of Morphology

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Fishes are effectively weightless in water due to the buoyant support of the environment, but amphibious fishes must cope with increased effective weight when on land. Delicate structures such as gills are especially vulnerable to collapse and loss of surface area out of water. We tested the ‘structural support’ hypothesis that amphibious Polypterus senegalus solve this problem using phenotypically plastic changes that provide mechanical support and increase stiffness at the level of the gill lamellae, the filaments, and the whole arches. After 7 d in terrestrial conditions, enlargement of an inter‐lamellar cell mass filled the water channels between gill lamellae, possibly to provide structural support and/or reduce evaporative water loss. Similar gill remodelling has been described in several other actinopterygian fishes, suggesting this may be an ancestral trait. There was no change in the mechanical properties or collagen composition of filaments or arches after 7 days out of water, but 8 months of terrestrial acclimation caused a reduction in gill arch length and mineralized bone volume. Thus, rather than increasing the size and stiffness of the gill skeleton, P. senegalus may instead reduce investment in supportive gill tissue while on land. These results are strikingly similar to the evolutionary trend of gill loss that occurred during the tetrapod invasion of land, raising the possibility that genetic assimilation of gill plasticity was an underlying mechanism.

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Increased mechanical loading through controlled swimming exercise induces bone formation and mineralization in adult zebrafish

Cited by 91 publications

References 67 publications

Severely Impaired Bone Material Quality in Chihuahua Zebrafish Resembles Classical Dominant Human Osteogenesis Imperfecta

Severely Impaired Bone Material Quality in Chihuahua Zebrafish Resembles Classical Dominant Human Osteogenesis Imperfecta

FGFR3 is a positive regulator of osteoblast expansion and differentiation during zebrafish skull vault development

Gill remodelling during terrestrial acclimation in the amphibious fish Polypterus senegalus

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