Abstract Background The ability to regenerate body parts is a feature of metazoan organisms and the focus of intense research aiming to understand its basis. A number of mechanisms involved in regeneration, such as proliferation and tissue remodeling, affect whole tissues; however, little is known on how distinctively different constituent cell types respond to the dynamics of regenerating tissues. Preliminary studies suggest that a number of organisms alter neuronal numbers to scale with changes in body size. In some species with the ability of whole-body axis regeneration, it has additionally been observed that regenerates are smaller than their pre-amputated parent, but maintain the correct morphological proportionality, suggesting that scaling of tissue and neuronal numbers also occurs. However, the cell dynamics and responses of neuronal subtypes during nervous system regeneration, scaling, and whole-body axis regeneration are not well understood in any system. The cnidarian sea anemone Nematostella vectensis is capable of whole-body axis regeneration, with a number of observations suggesting the ability to alter its size in response to changes in feeding. We took advantage of Nematostella ’s transparent and “simple” body plan and the NvLWamide-like mCherry fluorescent reporter transgenic line to probe the response of neuron populations to variations in body size in vivo in adult animals during body scaling and regeneration. Results We utilized the previously characterized NvLWamide-like::mCherry transgenic reporter line to determine the in vivo response of neuronal subtypes during growth, degrowth, and regeneration. Nematostella alters its size in response to caloric intake, and the nervous system responds by altering neuronal number to scale as the animal changes in size. Neuronal numbers in both the endodermal and ectodermal nerve nets decreased as animals shrunk, increased as they grew, and these changes were reversible. Whole-body axis regeneration resulted in regenerates that were smaller than their pre-amputated size, and the regenerated nerve nets were reduced in neuronal number. Different neuronal subtypes had distinct responses during regeneration, including consistent, not consistent, and conditional increases in number. Conditional responses were regulated, in part, by the size of the remnant fragment and the position of the amputation site. Regenerates and adults with reduced nerve nets displayed normal behaviors, indicating that the nerve net retains functionality as it scales. Conclusion These data suggest that the Nematostella nerve net is dynamic, capable of scaling with changes in body size, and that neuronal subtypes display differential regenerative responses, which we propose may be linked to the scale state of the regenerating animals.
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Whole-Body Regeneration in the Lobate Ctenophore Mnemiopsis leidyi
Ctenophores (a.k.a. comb jellies) are one of the earliest branching extant metazoan phyla. Adult regenerative ability varies greatly within the group, with platyctenes undergoing both sexual and asexual reproduction by fission while others in the genus Beroe having completely lost the ability to replace missing body parts. We focus on the unique regenerative aspects of the lobate ctenophore, Mnemiopsis leidyi, which has become a popular model for its rapid wound healing and tissue replacement, optical clarity, and sequenced genome. M. leidyi’s highly mosaic, stereotyped development has been leveraged to reveal the polar coordinate system that directs whole-body regeneration as well as lineage restriction of replacement cells in various regenerating organs. Several cell signaling pathways known to function in regeneration in other animals are absent from the ctenophore’s genome. Further research will either reveal ancient principles of the regenerative process common to all animals or reveal novel solutions to the stability of cell fates and whole-body regeneration.
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- NSF-PAR ID:
- 10317780
- Date Published:
- Journal Name:
- Genes
- Volume:
- 12
- Issue:
- 6
- ISSN:
- 2073-4425
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Regenerative potential is widespread but unevenly distributed across animals. However, our understanding of the molecular mechanisms underlying regenerative processes is limited to a handful of model organisms, restricting robust comparative analyses. Here, we conduct a time course of RNA-seq during whole body regeneration in
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3390/genes12060867
