Reptiles are the only amniotes that maintain the capacity to regenerate appendages. This study presents the first anatomical and histological evidence of tail repair with regrowth in an archosaur, the American alligator. The regrown alligator tails constituted approximately 6–18% of the total body length and were morphologically distinct from original tail segments. Gross dissection, radiographs, and magnetic resonance imaging revealed that caudal vertebrae were replaced by a ventrally-positioned, unsegmented endoskeleton. This contrasts with lepidosaurs, where the regenerated tail is radially organized around a central endoskeleton. Furthermore, the regrown alligator tail lacked skeletal muscle and instead consisted of fibrous connective tissue composed of type I and type III collagen fibers. The overproduction of connective tissue shares features with mammalian wound healing or fibrosis. The lack of skeletal muscle contrasts with lizards, but shares similarities with regenerated tails in the tuatara and regenerated limbs in Xenopus adult frogs, which have a cartilaginous endoskeleton surrounded by connective tissue, but lack skeletal muscle. Overall, this study of wild-caught, juvenile American alligator tails identifies a distinct pattern of wound repair in mammals while exhibiting features in common with regeneration in lepidosaurs and amphibia.
The lizards are evolutionarily the closest vertebrates to humans that demonstrate the ability to regenerate entire appendages containing cartilage, muscle, skin, and nervous tissue. We previously isolated PAX7-positive cells from muscle of the green anole lizard, Anolis carolinensis, that can differentiate into multinucleated myotubes and express the muscle structural protein, myosin heavy chain. Studying gene expression in these satellite/progenitor cell populations from A. carolinensis can provide insight into the mechanisms regulating tissue regeneration. We generated a transcriptome from proliferating lizard myoprogenitor cells and compared them to transcriptomes from the mouse and human tissues from the ENCODE project using XGSA, a statistical method for cross-species gene set analysis. These analyses determined that the lizard progenitor cell transcriptome was most similar to mammalian satellite cells. Further examination of specific GO categories of genes demonstrated that among genes with the highest level of expression in lizard satellite cells were an increased number of genetic regulators of chondrogenesis, as compared to mouse satellite cells. In micromass culture, lizard PAX7-positive cells formed Alcian blue and collagen 2a1 positive nodules, without the addition of exogenous morphogens, unlike their mouse counterparts. Subsequent quantitative RT-PCR confirmed up-regulation of expression of chondrogenic regulatory genes in lizard cells, including bmp2, sox9, runx2, and cartilage specific structural genes, aggrecan and collagen 2a1. Taken together, these data suggest that tail regeneration in lizards involves significant alterations in gene regulation with expanded musculoskeletal potency.
Reptiles are the only amniotes that maintain the capacity to lose and regrow entire appendages. Among reptiles, tail regeneration has been extensively studied in Lepidosauria, the subclass that includes lizards, but this study presents the first anatomical and histological evidence of tail regeneration in an archosaur, the American alligator (Alligator mississippiensis). All animals were wild caught juveniles or sub‐adults with an average total body length of 133.4±29.2cm (n=3). Although the duration of tail regrowth is unknown, the average length of the regenerated tail was 15.7±7.3cm. The regenerated tail was externally distinct from the original tail. The scales were compacted and lacked organization as well as dorsal scutes. Gross dissection, radiographs, and magnetic resonance imaging revealed that the caudal vertebrae were replaced by a ventrally‐positioned, unsegmented endoskeleton. This contrasts with lepidosaurs, where the regenerated tail is radially organized around a central endoskeleton, but shares commonality with urodele amphibians that regrow a tail with a clear dorsal‐ventral axis. Immunohistochemistry confirmed that this alligator structure was composed of cartilage, which formed a hollow rod with foramina distributed along the proximal‐distal axis. Furthermore, in contrast to the original tail, the regenerated tail lacked skeletal muscle and instead featured adipose and fibrous connective tissue supplied by a dense network of newly established axons and blood vessels. Despite substantial regrowth of the tail, the deposition of extensive connective tissue is reminiscent of mammalian wound healing or fibrosis. Using Herovici’s stain, it was shown that the regenerated tail is composed of both type I and type III collagen fibers. The lack of muscle contrasts with the lepidosaurs, which regrow functional skeletal muscle groups, but shares similarities with regenerated limbs in Xenopus adult frogs, which have a cartilaginous endoskeleton surrounded by connective tissue, but lacking skeletal muscle. Overall, this study of regeneration in the alligator identifies a distinct pattern of regrowth with features in common with lepidosaurs, amphibia, and wound repair in mammals. Further analysis will help to shed light on the conservation of regeneration in amniote vertebrates. Support or Funding Information This work was funded by the College of Liberal Arts and Sciences at Arizona State University to KK.
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