ABSTRACT
Reconstituting artificial proto-cells capable of transducing extracellular signals into cytoskeletal changes can reveal fundamental principles of how non-equilibrium phenomena in cellular signal transduction affect morphogenesis. Here, we generated a Synthetic Morphogenic Membrane System (SynMMS) by encapsulating a dynamic microtubule (MT) aster and a light-inducible signaling system driven by GTP/ATP chemical potential into cell-sized liposomes. Responding to light cues in analogy to morphogens, this biomimetic design embodies basic principles of localized Rho-GTPase signal transduction that generate an intracellular MT-regulator signaling gradient. Light-induced signaling promotes membrane-deforming growth of MT-filaments by dynamically elevating the membrane-proximal tubulin concentration. The resulting membrane deformations enable recursive coupling of the MT-aster with the signaling system, which generates global self-organized morphologies that reorganize towards local external cues in dependence on prior shape. SynMMS thereby signifies a step towards bio-inspired engineering of self-organized cellular morphogenesis.
Subject(s)
Cues , Liposomes , Morphogenesis/physiology , Artificial Cells , Biophysical Phenomena , Cell Surface Extensions/physiology , Centrosome , Cytoskeleton/metabolism , Humans , Liposomes/chemistry , Microtubules/metabolism , Recombinant Proteins , Signal Transduction , Stathmin/metabolism , Synthetic Biology , Tubulin/metabolism , rho GTP-Binding Proteins/metabolismABSTRACT
How cells utilize surface receptors for chemoreception is a recurrent question spanning between physics and biology over the past few decades. However, the dynamical mechanism for processing time-varying signals is still unclear. Using dynamical systems formalism to describe criticality in non-equilibrium systems, we propose generic principle for temporal information processing through phase space trajectories using dynamic transient memory. In contrast to short-term memory, dynamic memory generated via "ghost" attractor enables signal integration depending on stimulus history and thereby uniquely promotes integrating and interpreting complex temporal growth factor signals. We argue that this is a generic feature of receptor networks, the first layer of the cell that senses the changing environment. Using the experimentally established epidermal growth factor sensing system, we propose how recycling could provide self-organized maintenance of the critical receptor concentration at the plasma membrane through a simple, fluctuation-sensing mechanism. Processing of non-stationary signals, a feature previously attributed only to neural networks, thus uniquely emerges for receptor networks organized at criticality.