Dataset Information

Regenerative Adaptation to Electrochemical Perturbation in Planaria: A Molecular Analysis of Physiological Plasticity.

ABSTRACT: Anatomical homeostasis results from dynamic interactions between gene expression, physiology, and the external environment. Owing to its complexity, this cellular and organism-level phenotypic plasticity is still poorly understood. We establish planarian regeneration as a model for acquired tolerance to environments that alter endogenous physiology. Exposure to barium chloride (BaCl₂) results in a rapid degeneration of anterior tissue in Dugesia japonica. Remarkably, continued exposure to fresh solution of BaCl₂ results in regeneration of heads that are insensitive to BaCl₂. RNA-seq revealed transcriptional changes in BaCl₂-adapted heads that suggests a model of adaptation to excitotoxicity. Loss-of-function experiments confirmed several predictions: blockage of chloride and calcium channels allowed heads to survive initial BaCl₂ exposure, inducing adaptation without prior exposure, whereas blockade of TRPM channels reversed adaptation. Such highly adaptive plasticity may represent an attractive target for biomedical strategies in a wide range of applications beyond its immediate relevance to excitotoxicity preconditioning.

SUBMITTER: Emmons-Bell M

PROVIDER: S-EPMC6881696 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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Regenerative Adaptation to Electrochemical Perturbation in Planaria: A Molecular Analysis of Physiological Plasticity.

Emmons-Bell Maya M Durant Fallon F Tung Angela A Pietak Alexis A Miller Kelsie K Kane Anna A Martyniuk Christopher J CJ Davidian Devon D Morokuma Junji J Levin Michael M

iScience 20191109

Anatomical homeostasis results from dynamic interactions between gene expression, physiology, and the external environment. Owing to its complexity, this cellular and organism-level phenotypic plasticity is still poorly understood. We establish planarian regeneration as a model for acquired tolerance to environments that alter endogenous physiology. Exposure to barium chloride (BaCl<sub>2</sub>) results in a rapid degeneration of anterior tissue in Dugesia japonica. Remarkably, continued exposur ...[more]

PMID: 31765995

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Project description: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.

Project description:Gallic acid (GA) is a model hydroxybenzoic acid that occurs esterified in the lignocellulosic biomass of higher plants. GA displays relevant biological activities including anticancer properties. Owing to its antimicrobial and cellulase-inhibiting activities, GA also imposes constraints to the fermentability of lignocellulosic hydrolysates. In depth-knowledge of the mechanisms used by tolerant microorganisms to adapt to hydroxybenzoic acids would be a step forward to improve the bioavailability of GA or select/engineer production hosts with improved metabolic traits for the bioconversion of pretreated lignocellulosic biomass.Whole genome transcriptional profiling using DNA microarrays was used to characterize the molecular response of Lactobacillus plantarum WCFS1 to GA. Expression levels of 14 and 40 genes were differentially regulated at 1.5 and 15 mM GA, respectively. The transcriptomic analysis identified a marked induction of genes with confirmed or related roles to gastrointestinal survival, the repression of genes coding for certain ABC-type transporters and modulation of genes involved in the control of intracellular ammonia levels, among other responses. Most notably, a core set of genes dedicated to produce GA from polyphenols (tanB Lp ), decarboxylate GA to pyrogallol (lpdB, lpdC and lpdD) and transport functions (lp_2943) was highly overexpressed at both GA concentrations. Correspondingly, resting cells of strain WCFS1 induced by GA, but not their non-induced controls, produced pyrogallol. Gene expression and organization of genes involved in GA metabolism suggested a chemiosmotic mechanism of energy generation. Resting cells of L. plantarum induced by GA generated a membrane potential and a pH gradient across the membrane immediately upon addition of GA. Altogether, transcriptome profiling correlated with physiological observations indicating that a proton motive force could be generated during GA metabolism as a result of electrogenic GA uptake coupled with proton consumption by the intracellular gallate decarboxylase.The combination of transcriptome and physiological analyses revealed versatile molecular mechanisms involved in the adaptation of L. plantarum to GA. These data provide a platform to improve the survival of Lactobacillus in the gut. Our data may also guide the selection/engineering of microorganisms that better tolerate phenolic inhibitors present in pretreated lignocellulosic feedstocks.

Dataset Information

Regenerative Adaptation to Electrochemical Perturbation in Planaria: A Molecular Analysis of Physiological Plasticity.

Publications

Regenerative Adaptation to Electrochemical Perturbation in Planaria: A Molecular Analysis of Physiological Plasticity.

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