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Global analysis of gene expression in Xenopus hindlimbs during stage-dependent complete and incomplete regeneration

ABSTRACT: Xenopus laevis tadpoles are capable of limb regeneration following amputation, in a process which initially involves the formation of a blastema. However, Xenopus has full regenerative capacity only through premetamorphic stages. We have used the Affymetrix Xenopus laevis Genome Genechip® microarray to perform a large-scale screen of gene expression in the regeneration-complete, stage 53 (st53), and regeneration-incomplete, stage 57 (st57), hindlimbs at 1 and 5 days post-amputation. Through an exhaustive reannotation of the Genechip® and a variety of comparative bioinformatic analyses, we have identified genes that are differentially expressed between the regeneration-complete and –incomplete stages, detected the transcriptional changes associated with the regenerating blastema, and compared these results with those of other regeneration researchers. We focus particular attention on striking transcriptional activity observed in genes associated with patterning, stress response, and inflammation. Overall, this work provides the most comprehensive views yet of a regenerating limb and different transcriptional compositions of regeneration-competent and deficient tissues. Keywords: Expression profiling

ORGANISM(S): Xenopus laevis

PROVIDER: GSE4738 | GEO | 2006/08/11

SECONDARY ACCESSION(S): PRJNA95677

REPOSITORIES: GEO

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Transcription profiling of Xenopus hindlimbs during stage-dependent complete and incomplete regeneration

Project description:Xenopus laevis tadpoles are capable of limb regeneration following amputation, in a process which initially involves the formation of a blastema. However, Xenopus has full regenerative capacity only through premetamorphic stages. We have used the Affymetrix Xenopus laevis Genome GenechipÂ® microarray to perform a large-scale screen of gene expression in the regeneration-complete, stage 53 (st53), and regeneration-incomplete, stage 57 (st57), hindlimbs at 1 and 5 days post-amputation. Through an exhaustive reannotation of the GenechipÂ® and a variety of comparative bioinformatic analyses, we have identified genes that are differentially expressed between the regeneration-complete and âincomplete stages, detected the transcriptional changes associated with the regenerating blastema, and compared these results with those of other regeneration researchers. We focus particular attention on striking transcriptional activity observed in genes associated with patterning, stress response, and inflammation. Overall, this work provides the most comprehensive views yet of a regenerating limb and different transcriptional compositions of regeneration-competent and deficient tissues. Experiment Overall Design: This experiment measures gene expression in regeneration competent stage 53 and regeneration non-competent stage 57 Xenopus laevis hindlimbs, at 1 and 5 days post-amputation. Four replicates for each condition were used. Hindlimbs at either st53 or st57 were amputated unilaterally or bilaterally at the mid-zeugopodia level. One (1dPA) and 5 days (5dPA) after amputation tissues were collected 1mm proximal to the original level of amputation. Total RNA was isolated using RNaqueous micro kit (Ambion, inc.). One microgram of total RNA was amplified with the the Affymetrix 2 cycle kit and assayed per Genechip using standard Affymetrix protocols.

2008-06-13 | E-GEOD-4738 | biostudies-arrayexpress

Comparison of regenerating and non regenerating transgenic stage 52 Xenopus hind limbs

Project description:Epimorphic regeneration is the process by which complete regeneration of a complex structure such as a limb occurs through production of a proliferating blastema. This type of regeneration is rare among vertebrates but does occur in the African clawed frog Xenopus laevis, traditionally a model organism for the study of early development. Xenopus tadpoles can regenerate tails, limb buds and the lens of the eye, although the ability of the latter two organs to regenerate diminishes with advancing developmental stage. Using a heat shock inducible transgene that remains silent unless activated, we have established a stable line of transgenic Xenopus in which the BMP inhibitor Noggin can be over-expressed at any time during development. We have previously shown that activation of this transgene blocks regeneration of the tail and limb of Xenopus tadpoles. In the current study, we have taken advantage of this transgenic line to directly compare gene expression in same stage regenerating vs. non-regenerating hind limb buds. Using Affymetrix gene chip analysis, we have identified genes whose expression levels are linked to regenerative success. These include the BMP inhibitor Gremlin and the stress protein Hsp60 (no blastema in zebrafish). Analysis of overrepresented Gene Ontology functional groupings suggests that successful regeneration in the Xenopus hind limb depends on induction of stress response pathways. Furthermore, as expected, genes involved in embryonic development and growth are also significantly over-represented in regenerating early hind limb buds. Keywords: Differential expression, regeneration

2008-06-30 | GSE9813 | GEO

Blastemal progenitors modulate immune signaling during early limb regeneration.

Project description:Blastema formation is a hallmark of limb regeneration that requires proliferation and migration of progenitors derived from many tissues to the amputation plane. To better understand the genetic programs that initiate limb regeneration, we reasoned that blastemal progenitors would be among early proliferating cells in the stump following amputation. Here we separately profiled dividing and non-dividing stump tissues, as well as the wound epidermis, during early axolotl limb regeneration to examine transcriptional programs of blastemal progenitors. We provide a description of the changes in gene expression specific to early dividing cells at the site of amputation, inclusive of progenitors for the regenerating limb. This work collectively demonstrates differential suppression/activation of core developmental signaling pathways in subsets of the early regenerating limb and further suggests that interleukin-8 (il-8) signaling is important for regeneration.

2019-01-01 | GSE111213 | GEO

Fibroblast Dedifferentiation as a Determinant of Successful Regeneration

Project description:Limb regeneration, while observed lifelong in salamanders, is restricted to pre-metamorphic stages in Xenopus laevis frogs. After amputation, post-metamorphic frogs form a blastema that grows only an unsegmented cartilage rod. Whether this loss is due to systemic factors such as the immune system or due to an intrinsic incapability of cells to form competent stem cells has been unclear. Here, we use genetic fate mapping to establish that, as in axolotl, connective tissue (CT) cells form the post-metamorphic frog blastema. Using heterochronic transplantation into the limb bud and single-cell transcriptomic profiling, we show that axolotl CT cells fully dedifferentiate and integrate to form lineages including cartilage in the developing limb. In contrast, frog blastema CT cells do not fully re-express the limb bud progenitor program, even when transplanted into the limb bud. Correspondingly, transplanted cells contribute to extraskeletal CT but not to developing cartilage. Further, using single-cell RNA-seq analysis we find that the embryonic and the adult frog cartilage differentiation programs are molecularly distinct. This work defines intrinsic restrictions in CT dedifferentiation as a limitation in adult regeneration.

2021-05-24 | GSE165901 | GEO

Evi5 is required for Xenopus limb and tail regeneration

Project description:Amphibians such as the salamanders and the African clawed frog Xenopus are great models for regeneration studies because they can fully regenerate their lost organs. While axolotl can regenerate damaged organs throughout its lifetime, Xenopus has a limited regeneration capacity after metamorphosis. The ecotropic viral integrative factor 5 (Evi5), a cell-cycle-regulated protein that prevents cells from entering mitosis prematurely, is of great interest for it is highly upregulated in the limb blastema of axolotls, but its expression level remains unchanged in the fibroblastema of postmetamorphic frogs. Yet, its role in regeneration competent context in Xenopus has not been fully analyzed. Here we show that Evi5 is also upregulated in Xenopus tadpoles after limb and tail amputation, as it is in axolotls. Down-regulation of Evi5 with morpholino antisense oligos (Mo) impairs wound healing and blastema formation in limbs and tails in both axolotls and Xenopus tadpoles, suggesting a conserved function for Evi5 in regeneration. Using skin punch as a healing model we show that Evi5 is also involved in cell migration during wound healing. RNA-sequencing analysis shows that in addition to reduced signaling of Lepr, Pdgfa, Gdf5, evi5 Mo also downregulate lysine demethylases kdm6b and kdm7a, which are also required for limb regeneration. Thus, our results demonstrate that Evi5 plays a critical role in the regeneration of multiple systems in amphibians.

2022-11-24 | GSE218034 | GEO

Three Distinct Phases of Regeneration-Specific Gene Expression in the Axolotl Blastema

Project description:The salamander has the remarkable ability to regenerate its limb after amputation. Cells at the site of amputation form a blastema and then proliferate and differentiate to regrow the limb. To better understand this process, we have performed deep RNA sequencing of the blastema over a time course. We find genes expressed in three phases with a prominent burst in oncogene expression during the first day, blastemal/limb bud genes peaking at 7 to 14 days, and markers for terminal differentiation upregulated later. We compare these expression patterns to those in a mouse digit amputation model to identify genes specific to the regenerative response. We find that limb patterning genes, SALL genes, and genes involved in the proteasome, adult stem cell, embryonic stem cell, retinoid metabolism, and WNT and NOTCH signaling are regeneration-specific. We establish the “Axolomics” Database, which provides a tool for depositing, retrieving, and searching axolotl-related “omic” information. The experiment includes two time course data sets. One is from mouse digit amputation, another is from Axolotl digit amputation

2013-09-01 | E-GEOD-34394 | biostudies-arrayexpress

Identification of genes differentially expressed during half-head regeneration in Schmidtea mediterranea

Project description:We used Nimblegen arrays with design 2007-11-06_Smed_ESTs_4_exp to measure changes in gene expression during a timecourse of regeneration of one side of the head in Schmidtea mediterranea flatworms. Following amputation of one side of the head, samples were collected from both the regeneration blastema and non-regenerating side of the head on days 2, 3, and 4 post-amputation. Gene expression in these samples was compared to that in non-regenerating control samples collected at the time of amputation.

2014-12-01 | GSE62551 | GEO

Single cell RNA-seq of tail tissue from regeneration-competent and -incompetent Xenopus laevis tadpoles

Project description:Xenopus laevis tadpoles differ in their regenerative potential according to their developmental stage. Here, we focus on tail regeneration following amputation. By comparing the regenerative response during the naturally occurring regeneration-competent and -incompetent stages, scRNAseq can reveal cell type changes that are required for successful regeneration.

2019-04-23 | E-MTAB-7716 | biostudies-arrayexpress

Single-cell level transcriptomic anaylsis of the homeostatic and regenerating axolotl limb

Project description:Regeneration of complex multi-tissue structures, such as limbs, requires the coordinated effort of multiple cell types. In axolotl limb regeneration, the wound epidermis and blastema have been extensively studied via histology, grafting, and bulk-tissue RNA-sequencing. However, studying the contributions of these tissues is hindered due to limited information regarding the molecular identity of the cell types in regenerating limbs. By performing unbiased single-cell RNA-sequencing on over 25,000 cells from axolotl limbs, we identify a plethora of cellular diversity within epidermal, mesenchymal, and hematopoietic lineages in homeostatic and regenerating limbs. We identify regeneration-induced genes, develop putative trajectories for blastema cell differentiation, and propose the molecular identity and origin of fibroblast-derived blastema progenitor cells residing in homeostatic limbs. This work will enable application of molecular techniques to assess the contribution of these populations to limb regeneration. It will also facilitate work aimed at identifying transcripts and cells critical for limb regeneration.

2018-10-25 | GSE121737 | GEO

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Project description:Injury is a common occurrence in the life of most if not all organisms. Because injury and the extent of damage inflicted are not predictable events, pre-existing tissues must somehow determine how much tissue needs to be restored. It has been known for over a century that amputation position along a proximal-distal (P/D) axis determines the regeneration speed of amputated limbs in regeneration-competent animals1. Yet, it is not clear how an injured limb conveys positional information during regeneration to faithfully restore pre-existing morphologies and functions. Here, we profiled millimetric caudal fins regenerating proximal and distal amputations in the African killifish (Nothobranchius furzeri). We report position-specific, differential modulation of the spatial distribution, duration, and magnitude of proliferation, and the possibility to predict blastema sizes. Regenerating fins profiled by single cell RNA sequencing identified a Transient Regeneration-Activated Cell State (TRACS) enriched in extracellular matrix (ECM) components and modifiers that is proportionally amplified to match a given amputation position. We located this transient cell state to the basal epidermis by gene expression and confocal microscopy, and propose a role for these cells in transducing positional information to the regeneration blastema. Understanding the temporal deployment of regenerative cell states may hold the key to set up a successful regeneration event in organisms with limited regenerative abilities such as humans.

2024-04-01 | GSE260629 | GEO

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