Dataset Information

Genetic Reprogramming of Positional Memory in a Regenerating Appendage.

ABSTRACT: Certain vertebrates such as salamanders and zebrafish are able to regenerate complex tissues (e.g., limbs and fins) with remarkable fidelity. However, how positional information of the missing structure is recalled by appendage stump cells has puzzled researchers for centuries. Here, we report that sizing information for adult zebrafish tailfins is encoded within proliferating blastema cells during a critical period of regeneration. Using a chemical mutagenesis screen, we identified a temperature-sensitive allele of the gene encoding DNA polymerase alpha subunit 2 (pola2) that disrupts fin regeneration in zebrafish. Temperature shift assays revealed a 48-h window of regeneration, during which positional identities could be disrupted in pola2 mutants, leading to regeneration of miniaturized appendages. These fins retained memory of the new size in subsequent rounds of amputation and regeneration. Similar effects were observed upon transient genetic or pharmacological disruption of progenitor cell proliferation after plucking of zebrafish scales or head or tail amputation in amphioxus and annelids. Our results provide evidence that positional information in regenerating tissues is not hardwired but malleable, based on regulatory mechanisms that appear to be evolutionarily conserved across distantly related phyla.

SUBMITTER: Wang YT

PROVIDER: S-EPMC6917923 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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Genetic Reprogramming of Positional Memory in a Regenerating Appendage.

Wang Ying-Ting YT Tseng Tzu-Lun TL Kuo Yu-Chia YC Yu Jr-Kai JK Su Yi-Hsien YH Poss Kenneth D KD Chen Chen-Hui CH

Current biology : CB 20191127 24

Certain vertebrates such as salamanders and zebrafish are able to regenerate complex tissues (e.g., limbs and fins) with remarkable fidelity. However, how positional information of the missing structure is recalled by appendage stump cells has puzzled researchers for centuries. Here, we report that sizing information for adult zebrafish tailfins is encoded within proliferating blastema cells during a critical period of regeneration. Using a chemical mutagenesis screen, we identified a temperatur ...[more]

PMID: 31786062

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Project description:BACKGROUND:The endogenous ability to dedifferentiate, re-pattern, and re-differentiate adult cells to repair or replace damaged or missing structures is exclusive to only a few tetrapod species. The Mexican axolotl is one example of these species, having the capacity to regenerate multiple adult structures including their limbs by generating a group of progenitor cells, known as the blastema, which acquire pattern and differentiate into the missing tissues. The formation of a limb regenerate is dependent on cells in the connective tissues that retain memory of their original position in the limb, and use this information to generate the pattern of the missing structure. Observations from recent and historic studies suggest that blastema cells vary in their potential to pattern distal structures during the regeneration process; some cells are plastic and can be reprogrammed to obtain new positional information while others are stable. Our previous studies showed that positional information has temporal and spatial components of variation; early bud (EB) and apical late bud (LB) blastema cells are plastic while basal-LB cells are stable. To identify the potential cellular and molecular basis of this variation, we compared these three cell populations using histological and transcriptional approaches. RESULTS:Histologically, the basal-LB sample showed greater tissue organization than the EB and apical-LB samples. We also observed that cell proliferation was more abundant in EB and apical-LB tissue when compared to basal-LB and mature stump tissue. Lastly, we found that genes associated with cellular differentiation were expressed more highly in the basal-LB samples. CONCLUSIONS:Our results characterize histological and transcriptional differences between EB and apical-LB tissue compared to basal-LB tissue. Combined with our results from a previous study, we hypothesize that the stability of positional information is associated with tissue organization, cell proliferation, and pathways of cellular differentiation.

Dataset Information

Genetic Reprogramming of Positional Memory in a Regenerating Appendage.

Publications

Genetic Reprogramming of Positional Memory in a Regenerating Appendage.

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