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How precise is limb regeneration in axolotls?

Ferchault de Réaumur, in 1712, said that during regeneration “Nature gives back to the animal precisely and only that which it has lost, and she gives back to it all that it has lost”. Since then, we are amazed of seeing that if we amputate, for example, the limb of an axolotl, it regrows up to the same size and shape as the original limb. Moreover, this regenerated limb is as functional as the original one. Similarly, if we cut a planarian in ten pieces, the new ten flatworms that are formed in few days look identical to the original planarian. So, it seems that what Réaumur said 300 years ago, mainly stands true. But, what happens if we analyze the regenerated structures in deep detail? Are they really identical to the original one? In other words, how perfect is regeneration?

Now, a recent paper from the laboratories of Rui Diogo and Elly Tanaka describes the exact pattern of regeneration of 35 muscles that form the arm, forearm and hand of the axolotl’s forelimb as well as a pectoral muscle, the coracoradialis (http://www.ncbi.nlm.nih.gov/pubmed/24692358). This study is part of a larger project to characterize the development, homologies and evolution of many body muscles of all major vertebrate clades. Here, they used transgenic axolotls that expressed GFP in all muscle fibers. They analyzed the pattern of regeneration of these muscles in forelimbs that were experimentally amputated at the level of the arm as well as forelimbs that were amputated “naturally” from bites by other axolotls. In total they analyzed 23 regenerated forelimbs and found out that there were muscle anomalies in 10 of them (43%). This is surprisingly high under the assumption of the precision of regeneration. However, the total number of anomalies in these 23 regenerated forelimbs was only 20, so in average each forelimb had anomalies in only 2,5% of the total number of muscles (n=36) examined. Moreover, the percentage of anomalous muscle was much higher in those regenerates after bite-induced “natural amputations” (3,9% of muscles affected) than in the experimentally amputated regenerates (1,5%). This could be explained by recurrent aggressions affecting different regions compared with the precise and unique experimental amputation.

Another interesting observation was that none of the muscle defects seen in these regenerates was seen in the original limbs analyzed. Remarkably, one of the most common anomalies seen in 35% of the regenerated forelimbs (8 of the 23 regenerated forelimbs analyzed) was the presence of a fleshy coracoradialis at the level of the arm. Usually, this muscle only has a thin tendon at the level of the arm. This anomaly does not necessarily change the main function of this muscle (to flex the forearm). From an evolutionary perspective this anomaly is really interesting because this fleshy configuration resembles very much the fleshy biceps brachii of amniotes, which suggests a parallel between a regeneration defect and a major phenotypic change that occurred during tetrapod limb evolution. In fact, it has been suggested that at least part of the biceps brachii corresponds to the amphibian coracoradialis and, therefore, it could mean that at some point in evolution the tendinous part of the coracoradialis of amphibians had to become associated with fleshy fibers. The authors discuss then that, as suggested by other authors, there is often a parallel between anomalies occurring because of natural or experimental reasons and the normal phenotype found in their closest relatives. This could be interpreted because evolution is highly constrained and, as a consequence, similar phenotypes are often created. In fact, some other of the anomalies in the pattern of the regenerated muscles found in this study are normally found in other non-urodele taxa.

Finally, the authors also investigated the similarities in muscle morphogenesis between regeneration and embryonic development. In both cases, muscles appear to differentiate following a proximodistal and a radioulnar gradient. However, they found here that there is also a ventro-dorsal gradient of differentiation at least for the forearm muscles, that has not been previously seen during embryogenesis, and that would be worthy to further characterize in the future.

In summary, this study addresses how precise is the regeneration of the axolotl limb. On one side they observed that a large percentage of the regenerated limbs showed anomalies in the muscle pattern. But, on the other side, the average number of muscles affected in each limb was really low. Remarkably, they found a common anomaly seen in most of the limbs, which could have further implications for the evolution of muscles in tetrapods.

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Francesc Cebrià

Francesc Cebrià

Francesc Cebrià

I am a Biologist and Professor at the University of Barcelona. I do my research on a fascinating animal: freshwater planarians. You can cut them in as many pieces as you want and each piece will regenerate a complete new flatworm in very few days. In this blog I will keep you updated on the latest news on the field of animal regeneration. You will be able to follow the latest research on how planarians, axolotls, newts, cnidarians and other animals are able to regenerate parts of their bodies

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