Regeneration and asexual reproduction share common molecular changes: upregulation of a neural glycoepitope during morphallaxis in Lumbriculus

Neural morphallaxis is a regenerative process characterized by wide-spread anatomical and physiological changes in an adult nervous system. During segmental regeneration of the annelid worm, Lumbriculus variegatus, neural morphallaxis involved a reorganization of sensory, interneuronal, and motor systems as posterior fragments gained a more anterior body position. A monoclonal antibody, Lan 3-2, which labels a neural glyco-domain in the leech, was reactive in Lumbriculus. In the worm, this antibody labeled neural structures, particularly axonal tracts and giant fiber pathways of the central nervous system. A 60 kDa protein, possessing a lumbriculid mannose-rich glycoepitope, was upregulated during neural morphallaxis, peaking in its expression at 3 weeks post-amputation. Peak upregulation of the Lan 3-2 epitope, or the protein possessing it, corresponded to the time of major neurobehavioral plasticity during regeneration. Analyses of asexually reproducing animals also revealed induction of the Lan 3-2 epitope. In this developmental context, Lan 3-2 epitope upregulation was also confined to segments expressing both changes in positional identity and neurobehavioral plasticity, but these molecular and behavioral changes occurred prior to body fragmentation. These results suggest that the lumbriculid Lan 3-2 glycoepitope and proteins that bear them have been co-opted for neural morphallactic programs, induced both in anticipation of reproductive fragmentation and in compensation for injury-induced fragmentation.