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Accelerating metabolism and transmembrane cation flux by distorting red blood cells

Kuchel, Philip William; Shishmarev, Dmitry

Description

Under static conditions, mammalian red blood cells (RBCs) require a continuous supply of energy, typically via glucose, to maintain their biconcave disc shape. Mechanical distortion, in a complementary way, should lead to increased energy demand that is manifest in accelerated glycolysis. The experimental challenge in observing this phenomenon was met by reversibly and reproducibly distorting the cells and noninvasively measuring glycolytic flux. This was done with a gel-distorting device that...[Show more]

dc.contributor.authorKuchel, Philip William
dc.contributor.authorShishmarev, Dmitry
dc.date.accessioned2021-05-05T04:02:32Z
dc.date.available2021-05-05T04:02:32Z
dc.identifier.issn2375-2548
dc.identifier.urihttp://hdl.handle.net/1885/231445
dc.description.abstractUnder static conditions, mammalian red blood cells (RBCs) require a continuous supply of energy, typically via glucose, to maintain their biconcave disc shape. Mechanical distortion, in a complementary way, should lead to increased energy demand that is manifest in accelerated glycolysis. The experimental challenge in observing this phenomenon was met by reversibly and reproducibly distorting the cells and noninvasively measuring glycolytic flux. This was done with a gel-distorting device that was coupled with C-13 nuclear magnetic resonance (NMR) spectroscopy. We measured [3-C-13]L-lactate production from [1,6-C-13]D-glucose in the RBCs suspended in gelatin gels, and up to 90% rate enhancements were recorded. Thus, for the first time, we present experiments that demonstrate the linkage of mechanical distortion to metabolic changes in whole mammalian cells. In seeking a mechanism for the linkage between shape and energy supply, we measured transmembrane cation flux with Cs+ (as a K+ congener) using Cs-133 NMR spectroscopy, and the cation flux was increased up to fivefold. The postulated mechanism for these notable (in terms of whole-body energy consumption) responses is stimulation of Ca-adenosine triphosphatase by increased transmembrane flux of Ca2+ via the channel protein Piezo1 and increased glycolysis because its flux is adenosine triphosphate demand-regulated.
dc.description.sponsorshipAuthor contributions: P.W.K. conceived the experimental designs to study the reciprocity/duality of shape and energy consumption in RBCs. Both authors planned and jointly conducted all experiments and carried out the data analysis. P.W.K. drafted the manuscript and edited, with D.S., the final version. Competing interests: The authors declare that they have no competing interests
dc.format.mimetypeapplication/pdf
dc.language.isoen_AU
dc.publisherAmerican Association for the Advancement of Science
dc.rights© 2017 The Authors
dc.sourceScience Advances
dc.source.urihttps://advances.sciencemag.org/content/3/10/eaao1016
dc.titleAccelerating metabolism and transmembrane cation flux by distorting red blood cells
dc.typeJournal article
local.description.notesImported from ARIES
local.identifier.citationvolume3
dc.date.issued2017
local.identifier.absfor060104 - Cell Metabolism
local.identifier.ariespublicationu4485658xPUB1120
local.publisher.urlhttps://advances.sciencemag.org
local.type.statusPublished Version
local.contributor.affiliationKuchel, Philip William, University of Sydney
local.contributor.affiliationShishmarev, Dmitry, College of Health and Medicine, ANU
dc.relationhttp://purl.org/au-research/grants/arc/DP140102596
local.bibliographicCitation.issue10
local.identifier.doi10.1126/sciadv.aao1016
local.identifier.absseo970106 - Expanding Knowledge in the Biological Sciences
dc.date.updated2020-11-23T10:09:27Z
local.identifier.scopusID2-s2.0-85034848036
local.identifier.thomsonID000417998700050
dcterms.accessRightsOpen Access
dc.provenancehttps://v2.sherpa.ac.uk/id/publication/29739..."Author can archive publisher's version/PDF" from SHERPA/RoMEO site as at 05/05/2021
CollectionsANU Research Publications

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