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WIREs Syst Biol Med
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Multiscale memory and bioelectric error correction in the cytoplasm–cytoskeleton‐membrane system

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A fundamental aspect of life is the modification of anatomy, physiology, and behavior in the face of changing conditions. This is especially illustrated by the adaptive regulation of growth and form that underlies the ability of most organisms—from single cells to complex large metazoa—to develop, remodel, and regenerate to specific anatomical patterns. What is the relationship of the genome and other cellular components to the robust computations that underlie this remarkable pattern homeostasis? Here we examine the role of constraints defined at the cellular level, especially endogenous bioelectricity, in generating and propagating biological information. We review evidence that the genome is only one of several multi‐generational biological memories. Focusing on the cell membrane and cytoplasm, which is physically continuous across all of life in evolutionary timeframes, we characterize the environment as an interstitial space through which messages are passed via bioelectric and biochemical codes. We argue that biological memory is a fundamental phenomenon that cannot be understood at any one scale, and suggest that functional studies of information propagated in non‐genomic cellular structures will not only strongly impact evolutionary developmental biology, but will also have implications for regenerative medicine and synthetic bioengineering. WIREs Syst Biol Med 2018, 10:e1410. doi: 10.1002/wsbm.1410

This article is categorized under:

  • Developmental Biology > Stem Cell Biology and Regeneration
  • Physiology > Physiology of Model Organisms
  • Models of Systems Properties and Processes > Cellular Models
Phylogenetic diagrams showing membrane (parallel black lines), cytoplasm (area between parallel lines) and DNA genome (red lines) explicitly; LUCA = Last Universal Common Ancestor. (a) An extended RNA world hypothesis in which both bacterial and ‘arkarial’ (sensu Ref ) lineages independently evolve DNA genomes (cf. Ref , Figure 3). (b) A shorter RNA world scenario in which both bacterial and arkarial lineages undergo massive DNA alteration and/or loss. In both cases, membrane and cytoplasm exhibit deeper temporal continuity than DNA. (c) Endosymbiotic scenario for the origin of eukaryotes in which bacterial and archaeal membranes and cytoplasms mix (cf. Ref , Figure 3). This diagram is consistent with the ‘ring of life’ concept proposed by Rivera and Lake; see also Ref . (d) A more classical endosymbiotic scenario in which membranes and cytoplasms do not mix.
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The results of experiments with Xenopus embryos in which gap‐junction communication (GJC) was either inhibited (top panel) or enhanced (bottom panel) in the context of tumor‐like structures induced by injecting mRNA encoding a KRAS mutant in various locations relative to the gap junctional inhibiting protein. The response to KRAS transformation assayed could be explained by assuming that the two halves of the embryo exchange an oscillatory ‘handshaking’ signal that inhibits cell division (adapted from Ref ).
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Symmetric cell division in the desmid alga Micrasterias. (a) Sketch of planar parent and daughter half‐cells immediately following division of the parent cell (adapted from Ref , Figure 2). (b) Initial structuring of the daughter cell wall immediately following the state shown in (a). Arrows show sites of Ca2+ influx as determined by vibrating‐probe electrophysiology. (c) Subsequent ramification of the structure shown in (b); arrows show sites of Ca2+ influx. See Ref Figure 1(d)–(j) for high‐resolution photomicrographs of this process.
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Non‐genomic inheritance of pattern memory in planaria. Pharyngeal fragments of wild‐type (WT) planaria treated briefly post‐amputation with octanol to inhibit electrical synapses (gap‐junction communication) regenerate two‐headed animals that, when cut again in water, continue to regenerate two‐headed animals in perpetuity. The two‐headed phenotype can be rescued back to the single‐headed form by experimentally re‐setting the bioelectric circuit back to wild‐type state. This stable change to the animals’ target morphology is achieved without editing the genomic sequence or transgenesis.
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Simplified phylogeny showing divergence between genetic and morphological diversity, and hence between genome‐dominated and architectome‐dominated evolutionary processes.
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Spatial and temporal scales of CCM‐encoded memories. The smallest to largest spatial scales of CCM‐encoded memories span roughly 10 orders of magnitude (see text for examples); however, the spatial constraints on these memories extend to both smaller and larger scales.
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Markov blankets provide a formal model of the CCM system. The Markov blanket separating a node X in a causal network from its external environment E comprises, by definition, the parents of X (nodes with arrows to X), the children of X (nodes with arrows from X) and any other parents of X's children. (a) example of a Markov blanket. Unlabeled open nodes comprise the external environment E of the ‘blanketed’ node X; nodes within the shaded area comprise the Markov blanket of X. (b) a Markov blanket can be thought of as ‘mediating’ or ‘translating’ between X and E.
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