Coupled response of membrane hydration with oscillating metabolism in live cells: An alternative way to modulate structural aspects of biological membranes?

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

*Corresponding author for this work

Research output: Contribution to journalJournal articleResearchpeer-review

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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.

Original languageEnglish
Article number687
JournalBiomolecules
Volume9
Issue number11
Number of pages13
ISSN2218-273X
DOIs
Publication statusPublished - Nov 2019

Fingerprint

Biological membranes
Metabolism
Hydration
Membranes
Water
Adenosine Triphosphate
Polarization
Exocytosis
Cellular Structures
Metabolites
NAD
Cytosol
Yeast
Cells
Association reactions

Keywords

  • 6-acyl-2-(dimethylamino)naphtalenes fluorescence probes
  • Association-induction hypothesis (AIH)
  • ATP
  • Biological membranes
  • Crowding
  • Cytoskeletal proteins
  • Lyotropic mesomorphism
  • Mesophases
  • Water activity

Cite this

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title = "Coupled response of membrane hydration with oscillating metabolism in live cells: An alternative way to modulate structural aspects of biological membranes?",
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.",
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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? / Bagatolli, Luis A.; Stock, Roberto P.; Olsen, Lars F.

In: Biomolecules, Vol. 9, No. 11, 687, 11.2019.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Coupled response of membrane hydration with oscillating metabolism in live cells

T2 - An alternative way to modulate structural aspects of biological membranes?

AU - Bagatolli, Luis A.

AU - Stock, Roberto P.

AU - Olsen, Lars F.

PY - 2019/11

Y1 - 2019/11

N2 - 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.

AB - 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.

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KW - Crowding

KW - Cytoskeletal proteins

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KW - Mesophases

KW - Water activity

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