Coupled Response of Membrane Hydration with Oscillating Metabolism in Live Cells: An Alternative Way to Modulate Structural Aspects of Biological Membranes?

Roberto P. Stock,Luis A. Bagatolli,Lars F. Olsen

doi:10.3390/biom9110687

Roberto P. Stock, Luis A. Bagatolli + Show 1 more

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https://doi.org/10.3390/biom9110687

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Journal: Biomolecules	Publication Date: Nov 2, 2019
Citations: 12	License type: CC BY 4.0

Affiliation: University of Southern Denmark

Abstract

We propose that active metabolic processes may regulate structural changes in biological membranes via the physical state of cell water. This proposition is based on recent results obtained from our group in yeast cells displaying glycolytic oscillations, where we demonstrated that there is a tight coupling between the oscillatory behavior of glycolytic metabolites (ATP, NADH) and the extent of the dipolar relaxation of intracellular water, which oscillates synchronously. The mechanism we suggest involves the active participation of a polarized intracellular water network whose degree of polarization is dynamically modulated by temporal ATP fluctuations caused by metabolism with intervention of a functional cytoskeleton, as conceived in the long overlooked association-induction hypothesis (AIH) of Gilbert Ling. Our results show that the polarized state of intracellular water can be propagated from the cytosol to regions containing membranes. Since changes in the extent of the polarization of water impinge on its chemical activity, we hypothesize that metabolism dynamically controls the local structure of cellular membranes via lyotropic effects. This hypothesis offers an alternative way to interpret membrane related phenomena (e.g., changes in local curvature pertinent to endo/exocytosis or dynamical changes in membranous organelle structure, among others) by integrating relevant but mostly overlooked physicochemical characteristics of the cellular milieu.

Highlights

In the last five years, we have studied distinct physicochemical aspects of a well-known biological oscillator, namely, oscillating glycolysis, in the yeast Saccharomyces cerevisiae
Of marked importance for the content of this article was the tight coupling observed between intracellular Adenosine Triphosphate (ATP) levels and the dynamic state of intracellular water [12,13,15]
Considering the experimental results obtained by our group [12,13,14,15] and the interpretative framework provided by the association-induction hypothesis (AIH), we propose that active metabolic changes, reflected, for example, in the intracellular activity of ATP, regulate dynamical changes in the structure of biological membranes via the physical state of cell water

Summary

Introduction

In the last five years, we have studied distinct physicochemical aspects of a well-known biological oscillator, namely, oscillating glycolysis, in the yeast Saccharomyces cerevisiae When these cells are starved and respiration is blocked, they will use externally added glucose in such a way that the chemical activity of essential central metabolites such as reduced Nicotinamide Adenine dinucleotide (NADH) and Adenosine Triphosphate (ATP) will follow a well-established temporal waveform. It considers the intracellular environment as an isotropic aqueous solution where enzymes and metabolites react and diffuse according to principles of mass action kinetics and dilute solution theory (van’t Hoff) This interpretation exerts a robust influence on the way we currently grasp and think about biological systems, it has been repeatedly challenged when consideration is given to well-accepted ( largely ignored) features of the cellular milieu such as molecular crowding and spatial confinement that are likely to strongly influence the way that the cellular machinery operates. Due to the high concentration of macromolecules, estimated to be around

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