Transcriptomic, proteomic, and metabolomic landscape of positional memory in the caudal fin of zebrafish

Rabinowitz, Jeremy S.; Robitaille, Aaron M.; Wang, Yuliang; Ray, Catherine A.; Thummel, Ryan; Gu, Haiwei; Djukovic, Danijel; Raftery, Daniel; Berndt, Jason D.; Moon, Randall T.

doi:10.1073/pnas.1620755114

Cited by 88 publications

(90 citation statements)

References 92 publications

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“…Perathoner et al (2014) have shown that a gain-of-function mutation in the voltage-gated potassium channel displays a long fin phenotype in adult zebrafish. Consistent with these studies, the results of the transcriptome, proteome, and metabolome analyses in regenerating fins have suggested that there is a gradient of expression of ion channels within the zebrafish fin (Rabinowitz et al, 2017). Consistent with these studies, the results of the transcriptome, proteome, and metabolome analyses in regenerating fins have suggested that there is a gradient of expression of ion channels within the zebrafish fin (Rabinowitz et al, 2017).…”

Section: Entity Of Positional Informationsupporting

confidence: 57%

Robust and local positional information within a fin ray directs fin length during zebrafish regeneration

et al. 2018

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It has been proposed that cells are regulated to form specific morphologies and sizes according to positional information. However, the entity and nature of positional information have not been fully understood yet. The zebrafish caudal fin has a characteristic V-shape; dorsal and ventral fin rays are longer than the central ones. This fin shape regenerates irrespective of the sites or shape of fin amputation. It is thought that reformation of tissue occurs according to positional information. In this study, we developed a novel transplantation procedure for grafting a whole fin ray to an ectopic position and examined whether the information that specifies fin length exists within each fin ray. Intriguingly, when long and short fin rays were swapped, they regenerated to form longer or shorter fin rays than the adjacent host fin rays, respectively. Further, the abnormal fin ray lengths were maintained for a long time, more than 5 months, and after further re-amputation. In contrast to intra-fin grafting, when fin ray grafting was performed between fish, cells in the grafts disappeared due to immune rejection, and the grafted fin rays adapted to the host position to form a normal fin. Together, our data suggest that the information that directs fin length does exist in cells within a single fin ray and that it has a robust property-it is stable for a long time and is hard to rewrite. Our study highlighted a novel positional information mechanism for directing regenerating fin length.

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Section: Entity Of Positional Informationsupporting

confidence: 57%

Robust and local positional information within a fin ray directs fin length during zebrafish regeneration

et al. 2018

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“…For instance, new transgenic mice, axolotls, and zebrafish have been employed to determine the sources of new cells in regenerating tissues (122). In addition, genome-wide profiling, which can be combined with new genome-editing technologies, has uncovered novel factors and concepts during tissue regeneration (13; 29; 79; 94). In this review, we focus on some of the central questions in tissue regeneration research, what has been learned recently to address these questions, and how genetic strategies have enabled these studies.…”

Section: Introductionmentioning

confidence: 99%

Regeneration Genetics

Chen

Poss

2017

Annu. Rev. Genet.

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Understanding how and why animals regenerate complex tissues has potential to transform regenerative medicine. Here we present an overview of genetic approaches that have recently been applied to dissect mechanisms of regeneration. We describe new advances that relate to central objectives of regeneration biolsts researching different tissues and species. These objectives include defining the cellular sources and key cell behaviors in regenerating tissue; elucidating molecular triggers and brakes for regeneration; and defining the earliest events that control the presence of these molecular factors.

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“…In future studies, it should be interesting to examine whether the observed thermally induced plasticity of the caudal fin is mediated by alterations of the expression of genes like fgfs, shh, bmp2b , and cx43 , which are involved in the growth and differentiation of the caudal‐fin rays (Govindan & Iovine, ; Lee, Grill, Sanchez, Murphy‐Ryan, & Poss, ; Quint et al, ; Sims, Eble, & Iovine, ; Wills, Kidd, Lepilina, & Poss, ). Such alterations might occur at the level of individual genes, or be part of a thermally induced modification of the “positional identity” gradient, a prespecification gradient that controls the position‐dependent growth and differentiation of fin rays (Mari‐Beffa & Murciano, ; Rabinowitz et al, ).…”

Section: Discussionmentioning

confidence: 99%

“…This stability could be explained by a fusion of the adjacent to the bifurcation segments, which is happening in association with the fusion of the proximal segments (Figure ). The positioning of these two fusions might be determined by the “positional identity” gradient, a prespecification gradient that controls the position‐dependent growth and differentiation of fin rays (Mari‐Beffa & Murciano, ; Rabinowitz et al, ). Anatomically, the fusion of the proximal segments of caudal lepidotrichia with fish growth might serve the insertion of growing caudal‐fin musculature, and specifically of m. interradialis which controls the individual movement of each fin ray (Flammang, ; Lauder, ).…”

Section: Discussionmentioning

confidence: 99%

Segmentation pattern of zebrafish caudal fin is affected by developmental temperature and defined by multiple fusions between segments

et al. 2018

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Caudal-fin lepidotrichia is composed of numerous segments, which are linked to each other by intersegmental joints. During fish growth, lepidotrichia elongate by the addition of new segments at their distal margin, whereas the length of each segment remains constant after it is formed. In the present paper, we examined whether the water temperature affects the segmentation pattern of the juvenile and adult caudal fin. For this purpose, zebrafish (Danio rerio) embryos and larvae were exposed to three different temperature conditions (24°C, 28°C, and 32°C) from the pharyngula stage (1 day postfertilization [dpf]) to metamorphosis, whereas the control temperature (28°C) was applied to all the groups before and after this period. Results demonstrated that water temperature had a significant effect on the length of the segments of each lepidotrichium, at both the juvenile and adult stages. Moreover, at higher temperatures, there was a significant proximal shift of the position of the first bifurcation of the second lepidotrichium of the dorsal lobe. At all the experimental conditions, the length of proximal segment was not constant during fish growth, but it followed a discontinuous saltatory growth. Histological analysis of the proximal lepidotrichia segments revealed that the observed apparent growth of segments is the result of fusions between segments. Fusion occurs not by mineralization of the intersegmental joints, but by bone deposition around the joints.

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Transcriptomic, proteomic, and metabolomic landscape of positional memory in the caudal fin of zebrafish

Cited by 88 publications

References 92 publications

Robust and local positional information within a fin ray directs fin length during zebrafish regeneration

Robust and local positional information within a fin ray directs fin length during zebrafish regeneration

Regeneration Genetics

Segmentation pattern of zebrafish caudal fin is affected by developmental temperature and defined by multiple fusions between segments

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