Next Article in Journal
Nucleotide-Induced Conformational Changes in Escherichia coli DnaA Protein Are Required for Bacterial ORC to Pre-RC Conversion at the Chromosomal Origin
Next Article in Special Issue
Characterization of Morphological and Cellular Events Underlying Oral Regeneration in the Sea Anemone, Nematostella vectensis
Previous Article in Journal
Establishment and Comparison of Two Different Diagnostic Platforms for Detection of DENV1 NS1 Protein
Previous Article in Special Issue
Effect of Human Adipose Tissue Mesenchymal Stem Cells on the Regeneration of Ovine Articular Cartilage
Article Menu
Issue 11 (November) cover image

Export Article

Open AccessArticle
Int. J. Mol. Sci. 2015, 16(11), 27865-27896; doi:10.3390/ijms161126065

Gap Junctional Blockade Stochastically Induces Different Species-Specific Head Anatomies in Genetically Wild-Type Girardia dorotocephala Flatworms

1
Center for Regenerative and Developmental Biology and Department of Biology, Tufts University, 200 Boston Avenue, Suite 4600, Medford, MA 02155, USA
2
Institute of Problems of Mechanical Engineering, Russian Academy of Sciences, Saint Petersburg 199178, Russia
3
Institut Camille Jordan, UMR 5208 CNRS, University Lyon 1, Villeurbanne 69622, France
4
Octane Biotechnology, Kingston, ON K7K 6Z1, Canada
5
Department of Biological Sciences, University of Maryland Baltimore County, 1000 Hilltop Circle, Baltimore, MD 21250, USA
*
Author to whom correspondence should be addressed.
Academic Editor: Francesc Cebrià
Received: 1 August 2015 / Revised: 6 November 2015 / Accepted: 10 November 2015 / Published: 24 November 2015
(This article belongs to the Special Issue Molecular and Cellular Basis of Regeneration and Tissue Repair)
View Full-Text   |   Download PDF [7437 KB, uploaded 24 November 2015]   |  

Abstract

The shape of an animal body plan is constructed from protein components encoded by the genome. However, bioelectric networks composed of many cell types have their own intrinsic dynamics, and can drive distinct morphological outcomes during embryogenesis and regeneration. Planarian flatworms are a popular system for exploring body plan patterning due to their regenerative capacity, but despite considerable molecular information regarding stem cell differentiation and basic axial patterning, very little is known about how distinct head shapes are produced. Here, we show that after decapitation in G. dorotocephala, a transient perturbation of physiological connectivity among cells (using the gap junction blocker octanol) can result in regenerated heads with quite different shapes, stochastically matching other known species of planaria (S. mediterranea, D. japonica, and P. felina). We use morphometric analysis to quantify the ability of physiological network perturbations to induce different species-specific head shapes from the same genome. Moreover, we present a computational agent-based model of cell and physical dynamics during regeneration that quantitatively reproduces the observed shape changes. Morphological alterations induced in a genomically wild-type G. dorotocephala during regeneration include not only the shape of the head but also the morphology of the brain, the characteristic distribution of adult stem cells (neoblasts), and the bioelectric gradients of resting potential within the anterior tissues. Interestingly, the shape change is not permanent; after regeneration is complete, intact animals remodel back to G. dorotocephala-appropriate head shape within several weeks in a secondary phase of remodeling following initial complete regeneration. We present a conceptual model to guide future work to delineate the molecular mechanisms by which bioelectric networks stochastically select among a small set of discrete head morphologies. Taken together, these data and analyses shed light on important physiological modifiers of morphological information in dictating species-specific shape, and reveal them to be a novel instructive input into head patterning in regenerating planaria.
Keywords: regeneration; planaria; morphology; head; shape; species regeneration; planaria; morphology; head; shape; species
Figures

This is an open access article distributed under the Creative Commons Attribution License (CC BY 4.0).

Supplementary material

Scifeed alert for new publications

Never miss any articles matching your research from any publisher
  • Get alerts for new papers matching your research
  • Find out the new papers from selected authors
  • Updated daily for 49'000+ journals and 6000+ publishers
  • Define your Scifeed now

SciFeed Share & Cite This Article

MDPI and ACS Style

Emmons-Bell, M.; Durant, F.; Hammelman, J.; Bessonov, N.; Volpert, V.; Morokuma, J.; Pinet, K.; Adams, D.S.; Pietak, A.; Lobo, D.; Levin, M. Gap Junctional Blockade Stochastically Induces Different Species-Specific Head Anatomies in Genetically Wild-Type Girardia dorotocephala Flatworms. Int. J. Mol. Sci. 2015, 16, 27865-27896.

Show more citation formats Show less citations formats

Related Articles

Article Metrics

Article Access Statistics

1

Comments

[Return to top]
Int. J. Mol. Sci. EISSN 1422-0067 Published by MDPI AG, Basel, Switzerland RSS E-Mail Table of Contents Alert
Back to Top