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

作者信息

Emmons-Bell Maya, Durant Fallon, Hammelman Jennifer, Bessonov Nicholas, Volpert Vitaly, Morokuma Junji, Pinet Kaylinnette, Adams Dany S, Pietak Alexis, Lobo Daniel, Levin Michael

机构信息

Center for Regenerative and Developmental Biology and Department of Biology, Tufts University, 200 Boston Avenue, Suite 4600, Medford, MA 02155, USA.

Institute of Problems of Mechanical Engineering, Russian Academy of Sciences, Saint Petersburg 199178, Russia.

出版信息

Int J Mol Sci. 2015 Nov 24;16(11):27865-96. doi: 10.3390/ijms161126065.


DOI:10.3390/ijms161126065
PMID:26610482
原文链接:https://pmc.ncbi.nlm.nih.gov/articles/PMC4661923/
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.

摘要
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0b3a/4661923/7b8e772fa4ae/ijms-16-26065-g009.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0b3a/4661923/9375c0bd69e1/ijms-16-26065-g001.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0b3a/4661923/2f63d66b5878/ijms-16-26065-g002.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0b3a/4661923/7f0e0551d9fe/ijms-16-26065-g003.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0b3a/4661923/7e83079c5b47/ijms-16-26065-g004.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0b3a/4661923/bb12fadde67d/ijms-16-26065-g005.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0b3a/4661923/145312c97ba3/ijms-16-26065-g006.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0b3a/4661923/bb2fc5ce23e4/ijms-16-26065-g007.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0b3a/4661923/6b1940694c4b/ijms-16-26065-g008.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0b3a/4661923/7b8e772fa4ae/ijms-16-26065-g009.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0b3a/4661923/9375c0bd69e1/ijms-16-26065-g001.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0b3a/4661923/2f63d66b5878/ijms-16-26065-g002.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0b3a/4661923/7f0e0551d9fe/ijms-16-26065-g003.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0b3a/4661923/7e83079c5b47/ijms-16-26065-g004.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0b3a/4661923/bb12fadde67d/ijms-16-26065-g005.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0b3a/4661923/145312c97ba3/ijms-16-26065-g006.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0b3a/4661923/bb2fc5ce23e4/ijms-16-26065-g007.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0b3a/4661923/6b1940694c4b/ijms-16-26065-g008.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/0b3a/4661923/7b8e772fa4ae/ijms-16-26065-g009.jpg

相似文献

[1]
Gap Junctional Blockade Stochastically Induces Different Species-Specific Head Anatomies in Genetically Wild-Type Girardia dorotocephala Flatworms.

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[2]
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[3]
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[5]
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[6]
Ethanol exposure induces a delay in the reacquisition of function during head regeneration in Schmidtea mediterranea.

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[7]
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[10]
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本文引用的文献

[1]
Re-membering the body: applications of computational neuroscience to the top-down control of regeneration of limbs and other complex organs.

Integr Biol (Camb). 2015-12

[2]
Bioelectric memory: modeling resting potential bistability in amphibian embryos and mammalian cells.

Theor Biol Med Model. 2015-10-15

[3]
Connexins and pannexins in the integumentary system: the skin and appendages.

Cell Mol Life Sci. 2015-8

[4]
Inferring regulatory networks from experimental morphological phenotypes: a computational method reverse-engineers planarian regeneration.

PLoS Comput Biol. 2015-6-4

[5]
Left-right patterning in Xenopus conjoined twin embryos requires serotonin signaling and gap junctions.

Int J Dev Biol. 2014

[6]
Scaling and regeneration of self-organized patterns.

Phys Rev Lett. 2015-4-3

[7]
A conceptual model of morphogenesis and regeneration.

Acta Biotheor. 2015-9

[8]
Knowing one's place: a free-energy approach to pattern regulation.

J R Soc Interface. 2015-4-6

[9]
Endogenous gradients of resting potential instructively pattern embryonic neural tissue via Notch signaling and regulation of proliferation.

J Neurosci. 2015-3-11

[10]
On a model of pattern regeneration based on cell memory.

PLoS One. 2015-2-19

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