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

1
Instituto de Investigación Médica Mercedes y Martín Ferreyra—INIMEC (CONICET)—Universidad Nacional de Córdoba, Friuli 2434, Córdoba 5016, Argentina
2
Departamento de Química Biológica Ranwel Caputto, Facultad de Ciencias Químicas, Universidad Nacional de Córdoba, Córdoba 5000, Argentina
3
MEMPHYS—International and Interdisciplinary Research Network, 5230 Odense, Denmark
4
University of Southern Denmark, Institute for Biochemistry and Molecular Biology, Campusvej 55, 5230 Odense, Denmark
*
Author to whom correspondence should be addressed.
Biomolecules 2019, 9(11), 687; https://doi.org/10.3390/biom9110687
Received: 1 October 2019 / Revised: 29 October 2019 / Accepted: 30 October 2019 / Published: 2 November 2019
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. View Full-Text
Keywords: water activity; crowding; lyotropic mesomorphism; biological membranes; mesophases; ATP; cytoskeletal proteins; 6-acyl-2-(dimethylamino)naphtalenes fluorescence probes; association-induction hypothesis (AIH) water activity; crowding; lyotropic mesomorphism; biological membranes; mesophases; ATP; cytoskeletal proteins; 6-acyl-2-(dimethylamino)naphtalenes fluorescence probes; association-induction hypothesis (AIH)
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Bagatolli, L.A.; Stock, R.P.; Olsen, L.F. Coupled Response of Membrane Hydration with Oscillating Metabolism in Live Cells: An Alternative Way to Modulate Structural Aspects of Biological Membranes? Biomolecules 2019, 9, 687.

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