Beyond Neurons: Long Distance Communication in Development and Cancer

McMillen, Patrick; Oudin, Madeleine J.; Levin, Michael; Payne, Samantha L.

doi:10.3389/fcell.2021.739024

Cited by 27 publications

(25 citation statements)

References 135 publications

(196 reference statements)

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“…Indeed, in most cell networks, cells are only connected to their near neighbours. The stress system can be seen as another communication system and could play a role in changing the network structure to a flat (fully-connected) structure, at least for some part of the network and thus facilitating information aggregation (see [62] for a review of non-local cell communication modalities).…”

Section: Experimental Results On Repatterning Of Planariamentioning

confidence: 99%

The scaling of goals via homeostasis: an evolutionary simulation, experiment and analysis

Pio-Lopez¹,

Bischof²,

LaPalme³

et al. 2022

Preprint

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All cognitive agents are composite beings. Specifically, complex living agents consist of cells, which are themselves competent sub-agents navigating physiological and metabolic spaces. Behavior science, evolutionary developmental biology, and the field of machine intelligence all seek an answer to the scaling of biological cognition: what evolutionary dynamics enable individual cells to integrate their activities to result in the emergence of a novel, higher-level intelligence that has goals and competencies that belong to it and not to its parts? Here, we report the results of simulations based on the TAME framework, which proposes that evolution pivoted the collective intelligence of cells during morphogenesis of the body into traditional behavioral intelligence by scaling up the goal states at the center of homeostatic processes. We tested the hypothesis that a minimal evolutionary framework is sufficient for small, low-level setpoints of metabolic homeostasis in cells to scale up into collectives (tissues) which solve a problem in morphospace: the organization of a body-wide positional information axis (the classic French Flag problem). We found that these emergent morphogenetic agents exhibit a number of predicted features, including the use of stress propagation dynamics to achieve its target morphology as well as the ability to recover from perturbation (robustness) and long-term stability (even though neither of these was directly selected for). Moreover, we observed unexpected behavior of sudden remodeling long after the system stabilizes. We tested this prediction in a biological system -regenerating planaria -and observed a very similar phenomenon. We propose that this system is a first step toward a quantitative understanding of how evolution scales minimal goal-directed behavior (homeostatic loops) into higher-level problem-solving agents in morphogenetic and other spaces.

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Section: Experimental Results On Repatterning Of Planariamentioning

confidence: 99%

The scaling of goals via homeostasis: an evolutionary simulation, experiment and analysis

Pio-Lopez¹,

Bischof²,

LaPalme³

et al. 2022

Preprint

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“…Bioelectric signaling is also relevant to the "disease of geometry" known as cancer [196]. Cells are normally bound to large-scale morphogenetic goals (such as organbuilding or maintenance) by a collection of electrochemical cues that bind them into a network which maintains anatomical homeostasis [197,198]. Disruptions in this system can induce cancer phenotypes [181,182], even in the absence of mutation or DNA damage, because the society of the body is a dynamical type of order that must be continually and actively maintained [199][200][201].…”

Section: Discussion: Toward a Biomedicine Of Reprogrammable Tissuesmentioning

confidence: 99%

Cellular Signaling Pathways as Plastic, Proto-cognitive Systems: Implications for Biomedicine

Mathews¹,

Chang²,

Devlin³

et al. 2022

Preprint

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Many aspects of health and disease are modeled using the abstraction of a “pathway” – a set of protein or other subcellular activities with specified functional linkages between them. This metaphor is a paradigmatic case of a deterministic, mechanistic framework that focuses biomedical intervention strategies on altering the members of this network or the up/down-regulation links between them – rewiring the molecular hardware. However, protein pathways and transcriptional networks share important properties with neural networks and related dynamical systems, which implies that they can exhibit interesting and unexpected capabilities such as trainability (memory) and information processing in a context-sensitive manner. Specifically, they may be amenable to manipulation via their history of stimuli (equivalent to experiences, in behavioral science). If true, this would enable a new class of biomedical interventions that targets aspects of the dynamic physiological “software” implemented by pathways and gene-regulatory networks. Here, we propose an expanded view of pathways from the perspective of basal cognition. We review clinical and laboratory data supporting the idea that a broader understanding of pathways (and how they process contextual information across scales) is a limiting factor for progress in many areas of physiology and neurobiology. We argue that a fuller understanding of the functionality and tractability of pathways must go beyond a focus on the mechanistic details of their structure, to encompass their physiological history and embedding within higher levels of organization in the organism, with numerous implications for data science addressing health and disease. Exploiting tools and concepts from behavioral and cognitive sciences is not just a philosophical stance on biochemical processes; at stake is a new roadmap for overcoming the limitations of today’s pharmacological strategies and for the inference of future therapeutic interventions impacting a wide range of disease states.

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“…Currently, there are few examples of TNT in vivo, including in HIV animal models [ 77 ] and glioblastoma tumors [ 61 , 82 , 181 ]. However, observation of TNT processes in clinical samples has been proposed but not examined [ 182 , 183 ], though several laboratories are working on similar microtentacle (well-defined tubulin content) processes. Microtentacles are microtubule-based protrusions with high actin and vimentin content, as originally observed in detached breast cancer cells [ 184 ].…”

Section: Tnt or Cytonemes A New Concept For A Novel Long-rangementioning

confidence: 99%

Direct Cell-Cell Communication via Membrane Pores, Gap Junction Channels, and Tunneling Nanotubes: Medical Relevance of Mitochondrial Exchange

Eugenin

Camporesi

Peracchia

2022

IJMS

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The history of direct cell-cell communication has evolved in several small steps. First discovered in the 1930s in invertebrate nervous systems, it was thought at first to be an exception to the “cell theory”, restricted to invertebrates. Surprisingly, however, in the 1950s, electrical cell-cell communication was also reported in vertebrates. Once more, it was thought to be an exception restricted to excitable cells. In contrast, in the mid-1960s, two startling publications proved that virtually all cells freely exchange small neutral and charged molecules. Soon after, cell-cell communication by gap junction channels was reported. While gap junctions are the major means of cell-cell communication, in the early 1980s, evidence surfaced that some cells might also communicate via membrane pores. Questions were raised about the possible artifactual nature of the pores. However, early in this century, we learned that communication via membrane pores exists and plays a major role in medicine, as the structures involved, “tunneling nanotubes”, can rescue diseased cells by directly transferring healthy mitochondria into compromised cells and tissues. On the other hand, pathogens/cancer could also use these communication systems to amplify pathogenesis. Here, we describe the evolution of the discovery of these new communication systems and the potential therapeutic impact on several uncurable diseases.

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Beyond Neurons: Long Distance Communication in Development and Cancer

Cited by 27 publications

References 135 publications

The scaling of goals via homeostasis: an evolutionary simulation, experiment and analysis

The scaling of goals via homeostasis: an evolutionary simulation, experiment and analysis

Cellular Signaling Pathways as Plastic, Proto-cognitive Systems: Implications for Biomedicine

Direct Cell-Cell Communication via Membrane Pores, Gap Junction Channels, and Tunneling Nanotubes: Medical Relevance of Mitochondrial Exchange

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