Cell Responsiveness to Physical Energies: Paving the Way to Decipher a Morphogenetic Code

Abstract

We discuss emerging views on the complexity of signals controlling the onset of biological shapes and functions, from the nanoarchitectonics arising from supramolecular interactions, to the cellular/multicellular tissue level, and up to the unfolding of complex anatomy. We highlight the fundamental role of physical forces in cellular decisions, stressing the intriguing similarities in early morphogenesis, tissue regeneration, and oncogenic drift. Compelling evidence is presented, showing that biological patterns are strongly embedded in the vibrational nature of the physical energies that permeate the entire universe. We describe biological dynamics as informational processes at which physics and chemistry converge, with nanomechanical motions, and electromagnetic waves, including light, forming an ensemble of vibrations, acting as a sort of control software for molecular patterning. Biomolecular recognition is approached within the establishment of coherent synchronizations among signaling players, whose physical nature can be equated to oscillators tending to the coherent synchronization of their vibrational modes. Cytoskeletal elements are now emerging as senders and receivers of physical signals, “shaping” biological identity from the cellular to the tissue/organ levels. We finally discuss the perspective of exploiting the diffusive features of physical energies to afford in situ stem/somatic cell reprogramming, and tissue regeneration, without stem cell transplantation.

Mechanobiology: A landscape for reinterpreting stem cell heterogeneity and regenerative potential in diseased tissues

“…Spontaneous mechanical vibrations have been theoretically predicted and experimentally demonstrated in virtually all levels of the molecular and subcellular architecture. As we reviewed elsewhere, 29 the repetitive helix–loop–helix domains in single peptide molecules behave as intrinsically oscillatory modules, that owing to the electrically charged features of their composing amino acids, acquire the identity of electromechanical actuators . The hierarchical self-assembly of peptide moieties into larger cytoskeletal structures entails a major outcome of self-organization, implying that the resultant assembly exhibits traits that are way beyond the sum of the features of the composing building blocks ( Figure 1 ).…”

“…Thus, it happens that the nanomechanical (as well as the electric conductivity) characteristics of microtubule are by far different of those exhibited by a tubulin dimer, up to the chance of developing a mechano-electric actuator providing features of mechanical and electromagnetic connectedness with radiation characteristics. 29 , 30 , 31 The spreading of mechanical signals through cells entails particular complexity. In the attempt to elucidate new mechanotransduction pathways, Koch et al.…”

“…We have previously highlighted how nanomechanical and electromagnetic oscillations may coexist in signaling molecules and supramolecular assemblies, owing to their electrically charged nature. 29 Although the mechanical and electric/electromagnetic (including light) oscillations can hardly be separated, as they emerge within the context of the same subcellular structure, it is conceivable that a thorough dissection of the mechanical and electrical components of these oscillations may provide relevant knowledge on how these patterns are generated and on the chance of using mechanical and electric stimulation alone, or in various combinations, to efficiently direct the heterogeneity and rescuing potential of stem cells. A major premise in light of future attempts along this line is establishing whether oscillatory patterns are occurring not only at the subcellular level in cytoskeletal elements, but they are also evident in complex in vitro systems recapitulating relevant developmental pathways, as well as in in vivo settings, and whether, in the affirmative, such oscillatory patterning may have any causal role in morphogenetic decisions.…”