The immune system and brain regeneration in earthworms

Among the few animals that can regenerate a whole brain, freshwater planarians and some annelids are well-studied models, although our knowledge on how this process is achieved at the molecular level is much more limited in annelids. Now, a recent paper from the laboratory of Barbara Plytycz reports on the role that the immune system may play in the regeneration of the brain in the earthworm Dendrobaena veneta (http://www.ncbi.nlm.nih.gov/pubmed/25863277). In this species, the brain is constituted by two hemiganglia, which are connected to the subpharyngeal ganglion and the ventral nerve cord.

In their experimental set up to remove the brain of the worms the authors used two different strategies. In one of them the worms were temporarily immobilized by an electric shock whereas others were anesthetized with Prilocaine. These two methods had different impacts on the immune system of the treated animals. In the case of the electroshock it induced the extrusion of the coleomic fluid within which free-floating coelomocytes and soluble factors involved in the immune response are present. However, Prilocaine resulted in a minimum loss of coelomic fluid, thus preserving the components of the immune system. The authors then compared brain regeneration in these two different scenarios. At the cellular and histological levels the D. veneta brain is characterized by: i) a cellular layer of neurons and glial cells of heterogeneous cell size and larger cells with eosinophilic, basophilic and polychromatophilic staining properties; ii) a well-structured neuropile; iii) very few diving cells in the neural tissues but some within the perineural sheet; and iv) a perineural sheet rich in capillaries.

When using these features to characterize the regenerated brains 4 weeks after surgery the authors found out that the worms that went through electric shock (coelomocyte-extruded worms) regenerated smaller and less organized brains compared to those that went through the Prilocaine treatment. Thus, these brains had a thinner cellular layer, a seemingly random organization of nerve fibers in the neuropile, few mitotic cells in the regenerating brain and its surroundings and very poor presence of capillaries. In contrast, the regenerated brains of the Prilocaine-treated animals displayed many histological features very similar to those from the controls. Moreover, a significant number of mitotic cells were found within the regenerated brain and its surroundings.

As brain function has been also linked to regulation of reproduction in these animals the authors next checked whether this faster and more successful brain regeneration in this last group of animals was also linked to a faster recovery of reproduction. Measures of the number of cocoons produced at several times after brain removal as well as number of hatchlings from those cocoons indicated that the reproductive output after brain removal was restored faster in worms with a relatively complete coelomocyte complement (Prilocaine treatment) than in coelomocye-depleted animals (electro-shock).

In summary, the results presented here further support the notion that coleomocytes play an important role during brain regeneration in earthworms as well as reproduction in them is controlled by neurosecretions. Further studies should try to determine the exact role that a putative factor(s) from the coelomic fluid has on regeneration either by promoting the proliferation, survival or differentiation of the regenerated brain cells.