Keeping at Arm’s Length during Regeneration

Tornini, Valerie A.; Poss, Kenneth D.

doi:10.1016/j.devcel.2014.04.007

Cited by 51 publications

(46 citation statements)

References 70 publications

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“…We and others (15,17,18) hypothesized that molecular effectors of positional memory are expressed in gradients along the proximodistal axis of uninjured appendages. To identify candidate molecules that might be involved in this process, we performed RNA sequencing (RNA-seq) and label-free quantification (LFQ) proteomics on proximal, middle, and distal regions of uninjured zebrafish caudal fins (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Cell-cell communication is controlled through signal transduction pathways. Several of these pathways, such as RA, WNT, and FGF signaling, have known roles in growth control and patterning during appendage development and regeneration (10,18,53). Therefore, we manually curated lists of genes with known roles in RA, WNT, and FGF signaling (Datasets S10, S11, and S12, respectively).…”

Section: Resultsmentioning

confidence: 99%

“…Positional memory is proposed to be established by molecules that exist in a gradient in uninjured appendages (15)(16)(17)(18). These gradients are interpreted by the masses of mesenchymal stem cells (blastemas) that form at the distal tip of amputated appendages.…”

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confidence: 99%

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

Rabinowitz

Robitaille

Wang

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Regeneration requires cells to regulate proliferation and patterning according to their spatial position. Positional memory is a property that enables regenerating cells to recall spatial information from the uninjured tissue. Positional memory is hypothesized to rely on gradients of molecules, few of which have been identified. Here, we quantified the global abundance of transcripts, proteins, and metabolites along the proximodistal axis of caudal fins of uninjured and regenerating adult zebrafish. Using this approach, we uncovered complex overlapping expression patterns for hundreds of molecules involved in diverse cellular functions, including development, bioelectric signaling, and amino acid and lipid metabolism. Moreover, 32 genes differentially expressed at the RNA level had concomitant differential expression of the encoded proteins. Thus, the identification of proximodistal differences in levels of RNAs, proteins, and metabolites will facilitate future functional studies of positional memory during appendage regeneration.regeneration | positional memory | growth control | zebrafish | caudal fin

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

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

Rabinowitz

Robitaille

Wang

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…Unlike mammalian appendages, the adult zebrafish caudal fin perfectly restores tissue organization, size and shape in response to injury or resection (Tornini and Poss, 2014). Regeneration of the fin skeleton, which comprises bony rays (lepidotrichia) that extend along the proximal-distal axis, depends on the coordinated growth, differentiation and positioning of osteoblasts (Obs).…”

Section: Introductionmentioning

confidence: 99%

Shh promotes direct interactions between epidermal cells and osteoblast progenitors to shape regenerated zebrafish bone

et al. 2017

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Zebrafish innately regenerate amputated fins by mechanisms that expand and precisely position injury-induced progenitor cells to re-form tissue of the original size and pattern. For example, cell signaling networks direct osteoblast progenitors (pObs) to rebuild thin cylindrical bony rays with a stereotypical branched morphology. Hedgehog/ Smoothened (Hh/Smo) signaling has been variably proposed to stimulate overall fin regenerative outgrowth or promote ray branching. Using a photoconvertible patched2 reporter, we resolve active Hh/Smo output to a narrow distal regenerate zone comprising pObs and adjacent motile basal epidermal cells. This Hh/Smo activity is driven by epidermal Sonic hedgehog a (Shha) rather than Ob-derived Indian hedgehog a (Ihha), which nevertheless functions atypically to support bone maturation. Using BMS-833923, a uniquely effective Smo inhibitor, and high-resolution imaging, we show that Shha/Smo is functionally dedicated to ray branching during fin regeneration. Hh/ Smo activation enables transiently divided clusters of Shha-expressing epidermis to escort pObs into similarly split groups. This co-movement likely depends on epidermal cellular protrusions that directly contact pObs only where an otherwise occluding basement membrane remains incompletely assembled. Progressively separated pObs pools then continue regenerating independently to collectively reform a now branched skeletal structure.

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“…The permanent cell cycle exit provides a powerful tumor suppressor mechanism, but the downside is a limited ability to repair tissue damage. Some animals, such as urodele amphibians and teleost fish, are famous for their regenerative ability; they can-for instance-regrow a severed limb or tail [reviewed in (2)]. As mammals, we are unfortunately not capable of regenerating body parts; in fact, we are not even that good at repairing organ damage.…”

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confidence: 99%