CD24 induces changes to the surface receptors of B cell microvesicles with variable effects on their RNA and protein cargo

Abstract The CD24 cell surface receptor promotes apoptosis in developing B cells, and we recently found that it induces B cells to release plasma membrane-derived, CD24-bearing microvesicles (MVs). Here we have performed a systematic characterization of B cell MVs released from WEHI-231 B lymphoma c...

Full description

Bibliographic Details
Main Authors: D. Craig Ayre, Ian C. Chute, Andrew P. Joy, David A. Barnett, Andrew M. Hogan, Marc P. Grüll, Lourdes Peña-Castillo, Andrew S. Lang, Stephen M. Lewis, Sherri L. Christian
Format: Article
Language:English
Published: Nature Portfolio 2017-08-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-017-08094-8
_version_ 1818343996701802496
author D. Craig Ayre
Ian C. Chute
Andrew P. Joy
David A. Barnett
Andrew M. Hogan
Marc P. Grüll
Lourdes Peña-Castillo
Andrew S. Lang
Stephen M. Lewis
Sherri L. Christian
author_facet D. Craig Ayre
Ian C. Chute
Andrew P. Joy
David A. Barnett
Andrew M. Hogan
Marc P. Grüll
Lourdes Peña-Castillo
Andrew S. Lang
Stephen M. Lewis
Sherri L. Christian
author_sort D. Craig Ayre
collection DOAJ
description Abstract The CD24 cell surface receptor promotes apoptosis in developing B cells, and we recently found that it induces B cells to release plasma membrane-derived, CD24-bearing microvesicles (MVs). Here we have performed a systematic characterization of B cell MVs released from WEHI-231 B lymphoma cells in response to CD24 stimulation. We found that B cells constitutively release MVs of approximately 120 nm, and that CD24 induces an increase in phosphatidylserine-positive MV release. RNA cargo is predominantly comprised of 5S rRNA, regardless of stimulation; however, CD24 causes a decrease in the incorporation of protein coding transcripts. The MV proteome is enriched with mitochondrial and metabolism-related proteins after CD24 stimulation; however, these changes were variable and could not be fully validated by Western blotting. CD24-bearing MVs carry Siglec-2, CD63, IgM, and, unexpectedly, Ter119, but not Siglec-G or MHC-II despite their presence on the cell surface. CD24 stimulation also induces changes in CD63 and IgM expression on MVs that is not mirrored by the changes in cell surface expression. Overall, the composition of these MVs suggests that they may be involved in releasing mitochondrial components in response to pro-apoptotic stress with changes to the surface receptors potentially altering the cell type(s) that interact with the MVs.
first_indexed 2024-12-13T16:39:28Z
format Article
id doaj.art-5fdc4db9bd1d46f7b03db8910ae362c7
institution Directory Open Access Journal
issn 2045-2322
language English
last_indexed 2024-12-13T16:39:28Z
publishDate 2017-08-01
publisher Nature Portfolio
record_format Article
series Scientific Reports
spelling doaj.art-5fdc4db9bd1d46f7b03db8910ae362c72022-12-21T23:38:19ZengNature PortfolioScientific Reports2045-23222017-08-017111610.1038/s41598-017-08094-8CD24 induces changes to the surface receptors of B cell microvesicles with variable effects on their RNA and protein cargoD. Craig Ayre0Ian C. Chute1Andrew P. Joy2David A. Barnett3Andrew M. Hogan4Marc P. Grüll5Lourdes Peña-Castillo6Andrew S. Lang7Stephen M. Lewis8Sherri L. Christian9Department of Biochemistry, Memorial University of NewfoundlandAtlantic Cancer Research InstituteAtlantic Cancer Research InstituteAtlantic Cancer Research InstituteDepartment of Biochemistry, Memorial University of NewfoundlandDepartments of Biology, Memorial University of NewfoundlandDepartments of Biology, Memorial University of NewfoundlandDepartments of Biology, Memorial University of NewfoundlandAtlantic Cancer Research InstituteDepartment of Biochemistry, Memorial University of NewfoundlandAbstract The CD24 cell surface receptor promotes apoptosis in developing B cells, and we recently found that it induces B cells to release plasma membrane-derived, CD24-bearing microvesicles (MVs). Here we have performed a systematic characterization of B cell MVs released from WEHI-231 B lymphoma cells in response to CD24 stimulation. We found that B cells constitutively release MVs of approximately 120 nm, and that CD24 induces an increase in phosphatidylserine-positive MV release. RNA cargo is predominantly comprised of 5S rRNA, regardless of stimulation; however, CD24 causes a decrease in the incorporation of protein coding transcripts. The MV proteome is enriched with mitochondrial and metabolism-related proteins after CD24 stimulation; however, these changes were variable and could not be fully validated by Western blotting. CD24-bearing MVs carry Siglec-2, CD63, IgM, and, unexpectedly, Ter119, but not Siglec-G or MHC-II despite their presence on the cell surface. CD24 stimulation also induces changes in CD63 and IgM expression on MVs that is not mirrored by the changes in cell surface expression. Overall, the composition of these MVs suggests that they may be involved in releasing mitochondrial components in response to pro-apoptotic stress with changes to the surface receptors potentially altering the cell type(s) that interact with the MVs.https://doi.org/10.1038/s41598-017-08094-8
spellingShingle D. Craig Ayre
Ian C. Chute
Andrew P. Joy
David A. Barnett
Andrew M. Hogan
Marc P. Grüll
Lourdes Peña-Castillo
Andrew S. Lang
Stephen M. Lewis
Sherri L. Christian
CD24 induces changes to the surface receptors of B cell microvesicles with variable effects on their RNA and protein cargo
Scientific Reports
title CD24 induces changes to the surface receptors of B cell microvesicles with variable effects on their RNA and protein cargo
title_full CD24 induces changes to the surface receptors of B cell microvesicles with variable effects on their RNA and protein cargo
title_fullStr CD24 induces changes to the surface receptors of B cell microvesicles with variable effects on their RNA and protein cargo
title_full_unstemmed CD24 induces changes to the surface receptors of B cell microvesicles with variable effects on their RNA and protein cargo
title_short CD24 induces changes to the surface receptors of B cell microvesicles with variable effects on their RNA and protein cargo
title_sort cd24 induces changes to the surface receptors of b cell microvesicles with variable effects on their rna and protein cargo
url https://doi.org/10.1038/s41598-017-08094-8
work_keys_str_mv AT dcraigayre cd24induceschangestothesurfacereceptorsofbcellmicrovesicleswithvariableeffectsontheirrnaandproteincargo
AT iancchute cd24induceschangestothesurfacereceptorsofbcellmicrovesicleswithvariableeffectsontheirrnaandproteincargo
AT andrewpjoy cd24induceschangestothesurfacereceptorsofbcellmicrovesicleswithvariableeffectsontheirrnaandproteincargo
AT davidabarnett cd24induceschangestothesurfacereceptorsofbcellmicrovesicleswithvariableeffectsontheirrnaandproteincargo
AT andrewmhogan cd24induceschangestothesurfacereceptorsofbcellmicrovesicleswithvariableeffectsontheirrnaandproteincargo
AT marcpgrull cd24induceschangestothesurfacereceptorsofbcellmicrovesicleswithvariableeffectsontheirrnaandproteincargo
AT lourdespenacastillo cd24induceschangestothesurfacereceptorsofbcellmicrovesicleswithvariableeffectsontheirrnaandproteincargo
AT andrewslang cd24induceschangestothesurfacereceptorsofbcellmicrovesicleswithvariableeffectsontheirrnaandproteincargo
AT stephenmlewis cd24induceschangestothesurfacereceptorsofbcellmicrovesicleswithvariableeffectsontheirrnaandproteincargo
AT sherrilchristian cd24induceschangestothesurfacereceptorsofbcellmicrovesicleswithvariableeffectsontheirrnaandproteincargo