ATP-Mediated Compositional Change in Peripheral Myelin Membranes: A Comparative Raman Spectroscopy and Time-Of-Flight Secondary Ion Mass Spectrometry Study

In the present paper we addressed a mechanism of the myelin reorganization initiated by extracellular ATP and adenosine in sciatic nerves of the frog Rana temporaria. In combination with Raman microspectroscopy, allowing noninvasive live-cell measurements, we employed time-of-flight secondary ion mass spectrometry (TOF-SIMS) to follow the underlying changes in chemical composition of myelin membranes triggered by the purinergic agents. The simultaneous increase in lipid ordering degree, decrease in membrane fluidity and the degree of fatty acid unsaturation were induced by both ATP and adenosine. Mass spectrometry measurements revealed that ATP administration also led to the marked elevation of membrane cholesterol and decrease of phosphotidylcholine amounts. Vesicular lipid transport pathways are considered as possible mechanisms of compositional and structural changes of myelin.

• Publication year

  2015

• Venue

  PLoS ONE

• Publication date

  2015-11-06

• Fields of study

  Biology, Medicine, Chemistry

• Identifiers
  DOI 10.1371/journal.pone.0142084PMID 26544552PMCID 4636249
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

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  2014cited by this paper
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  2013cited by this paper
• Secondary ion mass spectrometry: characterizing complex samples in two and three dimensions.

  2013cited by this paper
• Time-of-flight secondary ion mass spectrometry (TOF-SIMS) imaging reveals cholesterol overload in the cerebral cortex of Alzheimer disease patients

  2012cited by this paper
• AMP Is an Adenosine A1 Receptor Agonist*

  2012cited by this paper
• Purinergic signalling

  2012influential reference
• Visualization by mass spectrometry of 2‐dimensional changes in rat brain lipids, including N‐acylphosphatidylethanolamines, during neonatal brain ischemia

  2012cited by this paper
• Adenosine receptors and brain diseases: neuroprotection and neurodegeneration.

  2011cited by this paper
• Imaging mass spectrometry for lipidomics.

  2011cited by this paper
• Lipid metabolism in myelinating glial cells: lessons from human inherited disorders and mouse models

  2011cited by this paper
• Micrometric molecular histology of lipids by mass spectrometry imaging.

  2011cited by this paper
• Adenosine signaling and function in glial cells

  2010cited by this paper
• In vivo lipidomics using single-cell Raman spectroscopy

  2010influential reference
• Roles of membrane trafficking in nerve repair and regeneration

  2010cited by this paper
• Transcardial perfusion versus immersion fixation for assessment of peripheral nerve regeneration.

  2009influential reference
• P2X7 receptor and macrophage function

  2009cited by this paper
• Purinergic signalling: past, present and future.

  2008cited by this paper
• Suppression and enhancement of secondary ion formation due to the chemical environment in static-secondary ion mass spectrometry

  2007cited by this paper
• Kinetics of ATP release following compression injury of a peripheral nerve trunk

  2006cited by this paper
• The E-NTPDase family of ectonucleotidases: Structure function relationships and pathophysiological significance

  2006cited by this paper
• Non‐targeted profiling of lipids during kainate‐induced neuronal injury

  2006cited by this paper
• Purinergic signalling

  2006cited by this paper
• Neuroprotection by adenosine in the brain: From A1 receptor activation to A2A receptor blockade

  2005cited by this paper
• Biological tissue imaging with time-of-flight secondary ion mass spectrometry and cluster ion sources.

  2005cited by this paper
• Intracellular Cholesterol Transport

  2004cited by this paper
• The basis of anisotropic water diffusion in the nervous system – a technical review

  2002cited by this paper
• Intracellular cholesterol transport

  2002cited by this paper
• Adenosine: a neuron-glial transmitter promoting myelination in the CNS in response to action potentials.

  2002cited by this paper
• Adenosine in the central nervous system: release mechanisms and extracellular concentrations

  2001cited by this paper
• Cholesterol-dependent Localization of NAP-22 on a Neuronal Membrane Microdomain (Raft)*

  1999cited by this paper
• Signalling via ATP in the nervous system.

  1994cited by this paper
• Raman spectroscopy of nerve fibers. A study of membrane lipids under steady state conditions.

  1985cited by this paper
• Comment on the carbon-hydrogen stretching region of vibrational Raman spectra of phospholipids.

  1977cited by this paper
• The analysis of collagen in glutaraldehyde-fixed, osmicated peripheral nerve

  1977influential reference
• Changes in the Raman spectrum of frog sciatic nerve during action potential propagation.

  1977cited by this paper
• Published online in Wiley InterScience (www.interscience.wiley.com). DOI:10.1002/nbm.782 Review Article

  year unknowncited by this paper

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