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

Maya Emmons-Bell; Fallon Durant; Angela Tung; Alexis Pietak; Kelsie Miller; Anna Kane; Christopher J Martyniuk; Devon Davidian; Junji Morokuma; Michael Levin

doi:10.1016/j.isci.2019.11.014

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

iScience. 2019 Dec 20:22:147-165. doi: 10.1016/j.isci.2019.11.014. Epub 2019 Nov 9.

Authors

Affiliations

¹ Allen Discovery Center at Tufts University, Medford, MA 02155, USA; Department of Biology, Tufts University, Medford, MA 02155, USA.
² Allen Discovery Center at Tufts University, Medford, MA 02155, USA.
³ Department of Physiological Sciences and Center for Environmental and Human Toxicology, University of Florida Genetics Institute, Interdisciplinary Program in Biomedical Sciences Neuroscience, College of Veterinary Medicine, University of Florida, Gainesville, FL 32611, USA.
⁴ Allen Discovery Center at Tufts University, Medford, MA 02155, USA; Department of Biology, Tufts University, Medford, MA 02155, USA. Electronic address: michael.levin@tufts.edu.

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.

Keywords: Cellular Physiology; Ion Activity; Marine Organism.