Phylogeny, Regeneration, Ageing and Cancer: Role of Microenvironment and Possibility of Its Therapeutic Manipulation

Nervous systems are traditionally thought of as providing sensing and behavioral coordination functions at the level of the whole organism. What is the evolutionary origin of the mechanisms enabling the nervous systems’ information processing ability? Here, we review evidence from evolutionary, developmental, and regenerative biology suggesting a deeper, ancestral function of both pre-neural and neural cell-cell communication systems: the long-distance coordination of cell division and differentiation required to create and maintain body-axis symmetries. This conceptualization of the function of nervous system activity sheds new light on the evolutionary transition from the morphologically rudimentary, non-neural Porifera and Placazoa to the complex morphologies of Ctenophores, Cnidarians, and Bilaterians. It further allows a sharp formulation of the distinction between long-distance axis-symmetry coordination based on external coordinates, e.g., by whole-organism scale trophisms as employed by plants and sessile animals, and coordination based on body-centered coordinates as employed by motile animals. Thus we suggest that the systems that control animal behavior evolved from ancient mechanisms adapting preexisting ionic and neurotransmitter mechanisms to regulate individual cell behaviors during morphogenesis. An appreciation of the ancient, non-neural origins of bioelectrically mediated computation suggests new approaches to the study of embryological development, including embryological dysregulation, cancer, regenerative medicine, and synthetic bioengineering.

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Characterization of regeneration initiating cells during Xenopus laevis tail regeneration

Sindelka,

Naraine,

Abaffy

et al. 2024

Genome Biol

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Background Embryos are regeneration and wound healing masters. They rapidly close wounds and scarlessly remodel and regenerate injured tissue. Regeneration has been extensively studied in many animal models using new tools such as single-cell analysis. However, until now, they have been based primarily on experiments assessing from 1 day post injury. Results In this paper, we reveal that critical steps initiating regeneration occur within hours after injury. We discovered the regeneration initiating cells (RICs) using single-cell and spatial transcriptomics of the regenerating Xenopus laevis tail. RICs are formed transiently from the basal epidermal cells, and their expression signature suggests they are important for modifying the surrounding extracellular matrix thus regulating development. The absence or deregulation of RICs leads to excessive extracellular matrix deposition and defective regeneration. Conclusion RICs represent a newly discovered transient cell state involved in the initiation of the regeneration process. Supplementary Information The online version contains supplementary material available at 10.1186/s13059-024-03396-3.

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Phylogeny, Regeneration, Ageing and Cancer: Role of Microenvironment and Possibility of Its Therapeutic Manipulation

Cited by 4 publications

References 103 publications

The Prospects of RNAs and Common Significant Pathways in Cancer Therapy and Regenerative Medicine

The Prospects of RNAs and Common Significant Pathways in Cancer Therapy and Regenerative Medicine

Morphological Coordination: A Common Ancestral Function Unifying Neural and Non-Neural Signaling

Characterization of regeneration initiating cells during Xenopus laevis tail regeneration

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