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Retinoids regulate a developmental checkpoint for tissue regeneration in Drosophila.

ABSTRACT: Damage to Drosophila imaginal discs elicits a robust regenerative response from the surviving tissue [1-4]. However, as in other organisms, developmental progression and differentiation can restrict the regenerative capacity of Drosophila tissues. Experiments in Drosophila and other holometabolous insects have demonstrated that either damage to imaginal tissues [5, 6] or transplantation of a damaged imaginal disc [7, 8] delays the onset of metamorphosis. Therefore, in Drosophila there appears to be a mechanism that senses tissue damage and extends the larval phase to coordinate tissue regeneration with the overall developmental program of the organism. However, how such a pathway functions remains unknown. Here we demonstrate that a developmental checkpoint extends larval growth after imaginal disc damage by inhibiting the transcription of the gene encoding PTTH, a neuropeptide that promotes the release of the steroid hormone ecdysone. Using a genetic screen, we identify a previously unsuspected role for retinoid biosynthesis in regulating PTTH expression and delaying development in response to tissue damage. Retinoid signaling plays an important but poorly defined role in several vertebrate regeneration models [9-11]. Our findings demonstrate that retinoid biosynthesis in Drosophila is important for the maintenance of a condition that is permissive for regenerative growth.

SUBMITTER: Halme A

PROVIDER: S-EPMC2847081 | biostudies-literature | 2010 Mar

REPOSITORIES: biostudies-literature

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Retinoids regulate a developmental checkpoint for tissue regeneration in Drosophila.

Halme Adrian A Cheng Michelle M Hariharan Iswar K IK

Current biology : CB 20100301 5

Damage to Drosophila imaginal discs elicits a robust regenerative response from the surviving tissue [1-4]. However, as in other organisms, developmental progression and differentiation can restrict the regenerative capacity of Drosophila tissues. Experiments in Drosophila and other holometabolous insects have demonstrated that either damage to imaginal tissues [5, 6] or transplantation of a damaged imaginal disc [7, 8] delays the onset of metamorphosis. Therefore, in Drosophila there appears to ...[more]

PMID: 20189388

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Project description:Cells with in vitro properties similar to those of bone marrow stromal stem cells are present in tooth pulp as quiescent cells that are mobilized by damage. These dental pulp stem cells (DPSCs) respond to damage by stimulating proliferation and differentiation into odontoblast-like cells that form dentine to repair the damage. In continuously growing mouse incisors, tissue at the incisor tips is continuously being damaged by the shearing action between the upper and lower teeth acting to self-sharpen the tips. We investigated mouse incisor tips as a model for the role of DPSCs in a continuous natural repair/regeneration process. We show that the pulp at the incisor tip is composed of a disorganized mass of mineralized tissue produced by odontoblast-like cells. These cells become embedded into the mineralized tissue that is rapidly formed and then lost during feeding. Tetracycline labeling not only revealed the expected incorporation into newly synthesized dentine formation of the incisor but also a zone covering the pulp cavity at the tips of the incisors that is mineralized very rapidly. This tissue was dentine-like but had a significantly lower mineral content than dentine as determined by Raman spectroscopy. The mineral was more crystalline than dentine, indicative of small, defect-free mineral particles. To identify the origin of cells responsible for deposition of this mineralized tissue, we genetically labeled perivascular cells by crossing NG2(ERT2) Cre and Nestin Cre mice with reporter mice. A large number of pericyte-derived cells were visible in the pulp of incisor tips with some having elongated, odontoblast-like shapes. These results show that in mouse incisors, rapid, continuous mineralization occurs at the tip to seal off the pulp tissue from the external environment. The mineral is formed by perivascular-derived cells that differentiate into cells expressing dentin sialo-phosphoprotein (DSPP) and produce a dentine-like material in a process that functions as continuous natural tissue regeneration.

Dataset Information

Retinoids regulate a developmental checkpoint for tissue regeneration in Drosophila.

Publications

Retinoids regulate a developmental checkpoint for tissue regeneration in Drosophila.

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