Regenerative adaptation to electrochemical perturbation in planaria: a molecular analysis of physiological plasticity

ABSTRACT: The development and maintenance of organismal form results from dynamic interactions between genome, protein interaction, physiology and the external environment. Bioelectric signaling represents an important epigenetic layer of control over processes of large-scale patterning during development and regeneration. However it is still largely unknown how physiological plasticity and adaptation operate during regenerative processes. Planarian flatworms are an exceptional system in which to study the interplay between genetics and environment, as they are able to regenerate any tissue or organ after traumatic injury. Here, we study acquired tolerance to a bioelectric homeostasis-altering pharmacological treatment. After exposure to the non-selective potassium channel blocker BaCl2, D. japonica flatworms display extreme depolarization of the head and then violently degenerate their anterior tissues via an apoptotic mechanism. Remarkably, when kept in fresh barium solution, they then regenerate a head that displays normal bioelectric state and is non-responsive to the channel blocker. Transcriptomics using RNAseq was used to characterize transcriptional changes that occur during this adaptation process, identifying a number of ion translocators that are differentially expressed with BaCl2, including the BK channel which is resistant to barium blockade. Many of these channels were identified as cation transporters (cation-transporting ATPases, small conductance calcium activated potassium (SK) channels, and sodium/hydrogen exchangers), suggesting that the physiological buffering of a depolarizing treatment is dependent on employing alternative means of transporting cations into and out of anterior cells and tissues. Moreover, pathway enrichment analysis revealed that transcriptional networks related to synaptic plasticity, nervous system development, neurotransmission, and nerve development were increased ~2 to 3-fold. Transcriptome responses were also activated for membrane steady potential, excitatory junction potential, and membrane hyperpolarization, all associated with the modulation of Vmem. The ability to adjust to physiological conditions that are strongly injurious to normal anatomy, by altering the transcriptome is a powerful adaptive capability of physiological circuits. Further studies on this plasticity will shed light on numerous regenerative and patterning mechanisms in the context of evolution, and will contribute to biomedical therapies that exploit this innate robustness.

ORGANISM(S): Dugesia japonica

PROVIDER: GSE98084 | GEO | 2017/08/31

SECONDARY ACCESSION(S): PRJNA383937

REPOSITORIES: GEO