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3D genome organization in tissue regeneration: functional requirement of long-range chromatin loops [Hi-C]

ABSTRACT: The three-dimensional (3D) organization of the genome plays a fundamental role in gene expression regulation. However, little is known about how transcriptional responses are influenced by changes in genome architecture during tissue regeneration. Here, we used Hi-C to profile 3D chromatin conformation during Drosophila wing imaginal disc regeneration. We found that, although compartments and topologically associating domains (TADs) are largely maintained, regeneration is accompanied by reduced compartmentalization and increased boundary insulation. Notably, we identified three long-range chromatin loops with increased contact frequency during regeneration. Precise deletion of their anchors demonstrated that these loops are essential for proper disc regeneration but dispensable for normal wing development. Furthermore, disruption of any of these loops resulted in convergent changes in both gene expression and H3K4me1 3D environment, suggesting their coordinated activity during regeneration. These findings provide functional evidence that 3D genome architecture actively contributes to the regenerative process.

ORGANISM(S): Drosophila melanogaster

PROVIDER: GSE304452 | GEO | 2025/12/28

REPOSITORIES: GEO

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Project description:Research on the ability of certain organisms to reconstruct missing structures of their bodies is still in its infancy, despite numerous efforts performed in multiple species. Using expression profile analyses on different timepoints that cover wound healing and regeneration processes (0, 24 and 72 hours post injury), we studied the regenerative behaviour of fragmented wing imaginal discs of D. melanogaster implanted into adult flies. First, through the comparison between cut and intact discs, we identified the effect of implantation on the regeneration process. Filtering this information, we then constructed the specific early regeneration gene signature of wing discs in which multiple transcription factors, immune response genes and members of the JNK, Notch and WNT signaling pathways seem to play an important role. We next compared the transcriptomes of discs 24 and 72 hours after fragmentation to characterize the regenerative machinery and observed a temporal decrease in the cellular metabolic processes, RNA processing and gene expression machinery, suggesting the discs normal activity was stopped on this first interval of time in response to injury and implantation offences. Based on the expression patterns, we elaborated a catalogue of genes involved in wing disc regeneration divided into four classes (wound healing, regeneration, quick response, constant response). Imaginal discs from third instar larvae were 3/4 fragmented, implanted into the abdomen of adult flies and cultured. In order to subtract the noise due to implantation, we repeated the same protocol using intact discs that were cultivated for 24h. Therefore, a total of 12 microarrays were hybridized: four microarrays (with total RNA from non cut wing discs at 0 and 24 hours) were used to assess the effect of the implantation procedure in intact wing discs and the rest (8) were used to measure changes in gene expression in the first 24 hours after disc dissection and implantation (total RNA from wing discs at 0 and 24 hours was hybridized) and during the period between 24 and 72 hours after the cut (total RNA from wing discs at 24 and 72 hours was hybridized). At least two independent total RNA extractions were carried out (using the RNeasy Protect Mini Kit from Qiagen Inc.) for each condition. The four microarrays hybridized for each pair of conditions were done in biological replicate pairs with dyes swapped to take dye bias into account. The whole set of microarrays was normalized following the same protocol, extracting in each case the list of significant genes (at least 1.5-fold change, FDR adjusted pvalue < 0.05).

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3D genome organization in tissue regeneration: functional requirement of long-range chromatin loops [Hi-C]

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