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Recent advancements in understanding fin regeneration in zebrafish

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Abstract Zebrafish have the remarkable ability to fully regenerate a lost appendage, faithfully restoring its size, shape and tissue patterning. Studies over the past decades have identified mechanisms underlying the formation, spatial organization, and regenerative growth of the blastema, a pool of proliferative progenitor cells. The patterning of newly forming tissue is tightly regulated to ensure proper rebuilding of anatomy. Precise niche regulation of retinoic acid and sonic hedgehog signaling ensures adherence to ray—interray boundaries. The molecular underpinnings of systems underlying re‐establishment of pre‐amputation size and shape (positional information) are also slowly starting to emerge. Osteoblasts play an important role as a cellular source of regenerating skeletal elements, and in zebrafish both osteoblast dedifferentiation as well as de novo osteoblast formation occurs. Both dedifferentiation and proliferation are tightly controlled, which makes it interesting to compare it to tumorigenesis, and to identify potential players involved in these processes. This article is categorized under: Adult Stem Cells, Tissue Renewal, and Regeneration > Regeneration
The zebrafish caudal fin. (a) Brightfield image (left) and scheme (right) of an adult caudal fin. Shown is only the exoskeletal part of the fin that extends from the body, which is formed by fin rays. The dashed lines represent the segmented bifurcating fin rays running from proximal to distal. Medial rays are shorter than lateral rays, resulting in a shape with two lobes. Note that for the caudal fin the proximodistal axis is the same as the rostral‐caudal axis. (b) A single layer of osteoblasts is located on the inner and outer surface of the segmented hemiray bone, as revealed by immunofluorescence using the Zn5 antigen, that labels osteoblasts of all differentiation stages, and also cells located at the joints (yellow arrows) between segments. Scale bar = 10 μm. (c) Whole mount view of a single bifurcated ray with segments and actinotrichia. (d) Cross section of the caudal fin
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Model for concurrent regulations during regeneration and tumorigenesis. The FK506‐binding protein FKBP is upregulated both in the regeneration blastema as well as in cancer cells. FKBPs inhibit calcineurin which itself inhibits regeneration, thus promoting outgrowth during regeneration. Similarly, potential tumor suppressors might act adversely on both tumor growth and regenerative growth. Red dashed line, amputation site; orange cones, blastemas; brown area, interray tissue; magenta line, wound epidermis
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Sources for osteoblasts during regeneration. Schematic longitudinal view of a single ray. (a) Mature osteoblasts in the stump dedifferentiate, migrate into the blastema and re‐differentiate. (b) After osteoblast ablation, osteoblasts form de novo in the regenerate. (c) Osteoblast progenitor cells (OPC) in the joints migrate into the blastema and differentiate to osteoblasts
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Establishment of ray—interray organization. (a) Whole mount view of the expression domains of cyp26a and shh during regeneration. (b) Inhibition of RA degradation results in loss of shh expression and ectopic bone formation
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Models for positional information and growth rate regulation. (a) A putative proximodistal molecular gradient in the fin results in different concentrations of unknown molecules at proximal and distal amputation sites, which effect growth rates. Growth rates of proximal amputation sites are higher. (b) Elevated growth at proximal amputation sites might be regulated by differential characteristics of the blastema. For v‐ATPase activity, aldh1a2 expression and Fgf signaling, increased levels in proximal compared to distal blastemas have been demonstrated. Schematic longitudinal view of a single ray; gray lines, bone; red dashed lines, amputation sites; green area; field of v‐ATPase activity, aldh1a2 expression and Fgf‐signaling
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Early steps of fin regeneration. (a) After amputation, the wound is closed within 12 hours postamputation (hpa) by migrating epithelial cells which form a multilayered epithelium, the wound epidermis. Next, a blastema (orange), an accumulation of proliferative, undifferentiated cells, is formed atop of each ray by distally migrating cells. During regenerative outgrowth, blastema cells proliferate and differentiate to replace missing tissue. (b) Accumulation of a population of small mesenchymal cells, which constitute the blastema, is primarily seen distally to rays in differential interference contrast (DIC) images, and highlighted with DAPI and phalloidin staining. Expression of genes like msxb, that are considered blastema markers, is strongest in the mesenchyme distal to the bony fin rays. Thus, blastemas are largely confined to the regenerate distal to rays, and blastemas sensu stricto do not form in the interrays. Scale bars, 100 μm (left), 10 μm (right)
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