Platelets modulate multiple markers of neutrophil function in response to in vitro Toll-like receptor stimulation
Identifieur interne : 000776 ( Pmc/Curation ); précédent : 000775; suivant : 000777Platelets modulate multiple markers of neutrophil function in response to in vitro Toll-like receptor stimulation
Auteurs : Kathryn E. Hally [Nouvelle-Zélande] ; Georgina K. Bird [Nouvelle-Zélande] ; Anne C. La Flamme [Nouvelle-Zélande] ; Scott A. Harding [Nouvelle-Zélande] ; Peter D. Larsen [Nouvelle-Zélande]Source :
- PLoS ONE [ 1932-6203 ] ; 2019.
Abstract
In addition to their role in facilitating leukocyte-mediated inflammation, platelets can dampen leukocyte pro-inflammatory responses in some contexts. Consequently, platelets are increasingly appreciated as regulators of inflammation. Together, platelets and neutrophils play a role in inflammation through Toll-like receptor (TLR) expression, although we do not fully understand how platelets shape neutrophil responses to TLR stimulation. Here, we aimed to determine the extent to which platelets can modulate neutrophil function in response to
Neutrophils from 10 healthy individuals were cultured alone or with autologous platelets. Neutrophils ± platelets were left unstimulated or were stimulated with 1 or 100 ng/mL lipopolysaccharide (LPS; a TLR4 agonist), Pam3CSK4 (a TLR2/1 agonist) and fibroblast-stimulating lipopeptide (FSL)-1 (a TLR2/6 agonist). Neutrophil activation and phagocytic activity were assessed by flow cytometry, and elastase and interleukin-8 secretion were assessed by ELISA.
The addition of platelets attenuated neutrophil CD66b and CD11b expression in response to various doses of Pam3CSK4 and FSL-1. Furthermore, platelet co-culture was associated with higher CD62L expression (indicating reduced CD62L shedding) in response to these TLR agonists. Platelets also reduced elastase secretion in unstimulated cultures and in response to low-dose TLR stimulation. Conversely, platelet co-culture increased neutrophil phagocytosis in unstimulated cultures and in response to low-dose Pam3CSK4 and FSL-1. Platelets also increased IL-8 secretion in response to low-dose LPS.
Platelets are complex immunomodulators that can attenuate some, and simultaneously augment other, neutrophil functions. This modulation can occur both in the absence and presence of TLR stimulation.
Url:
DOI: 10.1371/journal.pone.0223444
PubMed: 31581214
PubMed Central: 6776355
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<front><div type="abstract" xml:lang="en"><sec id="sec001"><title>Introduction</title>
<p>In addition to their role in facilitating leukocyte-mediated inflammation, platelets can dampen leukocyte pro-inflammatory responses in some contexts. Consequently, platelets are increasingly appreciated as regulators of inflammation. Together, platelets and neutrophils play a role in inflammation through Toll-like receptor (TLR) expression, although we do not fully understand how platelets shape neutrophil responses to TLR stimulation. Here, we aimed to determine the extent to which platelets can modulate neutrophil function in response to <italic>in vitro</italic>
stimulation with TLR4, TLR2/1, and TLR2/6 agonists.</p>
</sec>
<sec id="sec002"><title>Methods</title>
<p>Neutrophils from 10 healthy individuals were cultured alone or with autologous platelets. Neutrophils ± platelets were left unstimulated or were stimulated with 1 or 100 ng/mL lipopolysaccharide (LPS; a TLR4 agonist), Pam3CSK4 (a TLR2/1 agonist) and fibroblast-stimulating lipopeptide (FSL)-1 (a TLR2/6 agonist). Neutrophil activation and phagocytic activity were assessed by flow cytometry, and elastase and interleukin-8 secretion were assessed by ELISA.</p>
</sec>
<sec id="sec003"><title>Results</title>
<p>The addition of platelets attenuated neutrophil CD66b and CD11b expression in response to various doses of Pam3CSK4 and FSL-1. Furthermore, platelet co-culture was associated with higher CD62L expression (indicating reduced CD62L shedding) in response to these TLR agonists. Platelets also reduced elastase secretion in unstimulated cultures and in response to low-dose TLR stimulation. Conversely, platelet co-culture increased neutrophil phagocytosis in unstimulated cultures and in response to low-dose Pam3CSK4 and FSL-1. Platelets also increased IL-8 secretion in response to low-dose LPS.</p>
</sec>
<sec id="sec004"><title>Conclusion</title>
<p>Platelets are complex immunomodulators that can attenuate some, and simultaneously augment other, neutrophil functions. This modulation can occur both in the absence and presence of TLR stimulation.</p>
</sec>
</div>
</front>
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<author><name sortKey="Jiang, L" uniqKey="Jiang L">L Jiang</name>
</author>
<author><name sortKey="Hultenby, K" uniqKey="Hultenby K">K Hultenby</name>
</author>
<author><name sortKey="Zhu, L" uniqKey="Zhu L">L Zhu</name>
</author>
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<biblStruct><analytic><author><name sortKey="Pokrovskaya, Id" uniqKey="Pokrovskaya I">ID Pokrovskaya</name>
</author>
<author><name sortKey="Aronova, Ma" uniqKey="Aronova M">MA Aronova</name>
</author>
<author><name sortKey="Kamykowski, Ja" uniqKey="Kamykowski J">JA Kamykowski</name>
</author>
<author><name sortKey="Prince, Aa" uniqKey="Prince A">AA Prince</name>
</author>
<author><name sortKey="Hoyne, Jd" uniqKey="Hoyne J">JD Hoyne</name>
</author>
<author><name sortKey="Calco, Gn" uniqKey="Calco G">GN Calco</name>
</author>
</analytic>
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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plosone</journal-id>
<journal-title-group><journal-title>PLoS ONE</journal-title>
</journal-title-group>
<issn pub-type="epub">1932-6203</issn>
<publisher><publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, CA USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">31581214</article-id>
<article-id pub-id-type="pmc">6776355</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0223444</article-id>
<article-id pub-id-type="publisher-id">PONE-D-19-17079</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Cell Biology</subject>
<subj-group><subject>Cellular Types</subject>
<subj-group><subject>Animal Cells</subject>
<subj-group><subject>Blood Cells</subject>
<subj-group><subject>White Blood Cells</subject>
<subj-group><subject>Neutrophils</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Cell Biology</subject>
<subj-group><subject>Cellular Types</subject>
<subj-group><subject>Animal Cells</subject>
<subj-group><subject>Immune Cells</subject>
<subj-group><subject>White Blood Cells</subject>
<subj-group><subject>Neutrophils</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Immunology</subject>
<subj-group><subject>Immune Cells</subject>
<subj-group><subject>White Blood Cells</subject>
<subj-group><subject>Neutrophils</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject>
<subj-group><subject>Immunology</subject>
<subj-group><subject>Immune Cells</subject>
<subj-group><subject>White Blood Cells</subject>
<subj-group><subject>Neutrophils</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Anatomy</subject>
<subj-group><subject>Body Fluids</subject>
<subj-group><subject>Blood</subject>
<subj-group><subject>Platelets</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject>
<subj-group><subject>Anatomy</subject>
<subj-group><subject>Body Fluids</subject>
<subj-group><subject>Blood</subject>
<subj-group><subject>Platelets</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Physiology</subject>
<subj-group><subject>Body Fluids</subject>
<subj-group><subject>Blood</subject>
<subj-group><subject>Platelets</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject>
<subj-group><subject>Physiology</subject>
<subj-group><subject>Body Fluids</subject>
<subj-group><subject>Blood</subject>
<subj-group><subject>Platelets</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Cell Biology</subject>
<subj-group><subject>Cellular Types</subject>
<subj-group><subject>Animal Cells</subject>
<subj-group><subject>Blood Cells</subject>
<subj-group><subject>Platelets</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Cell Biology</subject>
<subj-group><subject>Cell Processes</subject>
<subj-group><subject>Phagocytosis</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject>
<subj-group><subject>Hematology</subject>
<subj-group><subject>Blood Coagulation</subject>
<subj-group><subject>Platelet Activation</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Immunology</subject>
<subj-group><subject>Immune Response</subject>
<subj-group><subject>Inflammation</subject>
</subj-group>
</subj-group>
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<subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject>
<subj-group><subject>Immunology</subject>
<subj-group><subject>Immune Response</subject>
<subj-group><subject>Inflammation</subject>
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<subj-group><subject>Diagnostic Medicine</subject>
<subj-group><subject>Signs and Symptoms</subject>
<subj-group><subject>Inflammation</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject>
<subj-group><subject>Pathology and Laboratory Medicine</subject>
<subj-group><subject>Signs and Symptoms</subject>
<subj-group><subject>Inflammation</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Physiology</subject>
<subj-group><subject>Physiological Processes</subject>
<subj-group><subject>Secretion</subject>
</subj-group>
</subj-group>
</subj-group>
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<subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject>
<subj-group><subject>Physiology</subject>
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<subj-group><subject>Secretion</subject>
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<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Immunology</subject>
<subj-group><subject>Immune System Proteins</subject>
<subj-group><subject>Immune Receptors</subject>
<subj-group><subject>Toll-like Receptors</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject>
<subj-group><subject>Immunology</subject>
<subj-group><subject>Immune System Proteins</subject>
<subj-group><subject>Immune Receptors</subject>
<subj-group><subject>Toll-like Receptors</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Biochemistry</subject>
<subj-group><subject>Proteins</subject>
<subj-group><subject>Immune System Proteins</subject>
<subj-group><subject>Immune Receptors</subject>
<subj-group><subject>Toll-like Receptors</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Cell Biology</subject>
<subj-group><subject>Signal Transduction</subject>
<subj-group><subject>Immune Receptors</subject>
<subj-group><subject>Toll-like Receptors</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject>
<subj-group><subject>Inflammatory Diseases</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Platelets modulate multiple markers of neutrophil function in response to <italic>in vitro</italic>
Toll-like receptor stimulation</article-title>
<alt-title alt-title-type="running-head">Platelets modulate neutrophil function</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-3608-3795</contrib-id>
<name><surname>Hally</surname>
<given-names>Kathryn E.</given-names>
</name>
<role content-type="http://credit.casrai.org/">Conceptualization</role>
<role content-type="http://credit.casrai.org/">Data curation</role>
<role content-type="http://credit.casrai.org/">Formal analysis</role>
<role content-type="http://credit.casrai.org/">Funding acquisition</role>
<role content-type="http://credit.casrai.org/">Writing – original draft</role>
<role content-type="http://credit.casrai.org/">Writing – review & editing</role>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff003"><sup>3</sup>
</xref>
<xref ref-type="corresp" rid="cor001">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Bird</surname>
<given-names>Georgina K.</given-names>
</name>
<role content-type="http://credit.casrai.org/">Data curation</role>
<role content-type="http://credit.casrai.org/">Writing – review & editing</role>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff003"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-2344-7281</contrib-id>
<name><surname>La Flamme</surname>
<given-names>Anne C.</given-names>
</name>
<role content-type="http://credit.casrai.org/">Conceptualization</role>
<role content-type="http://credit.casrai.org/">Funding acquisition</role>
<role content-type="http://credit.casrai.org/">Supervision</role>
<role content-type="http://credit.casrai.org/">Writing – review & editing</role>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff003"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Harding</surname>
<given-names>Scott A.</given-names>
</name>
<role content-type="http://credit.casrai.org/">Conceptualization</role>
<role content-type="http://credit.casrai.org/">Funding acquisition</role>
<role content-type="http://credit.casrai.org/">Supervision</role>
<role content-type="http://credit.casrai.org/">Writing – review & editing</role>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff003"><sup>3</sup>
</xref>
<xref ref-type="aff" rid="aff004"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Larsen</surname>
<given-names>Peter D.</given-names>
</name>
<role content-type="http://credit.casrai.org/">Conceptualization</role>
<role content-type="http://credit.casrai.org/">Formal analysis</role>
<role content-type="http://credit.casrai.org/">Funding acquisition</role>
<role content-type="http://credit.casrai.org/">Supervision</role>
<role content-type="http://credit.casrai.org/">Writing – review & editing</role>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff003"><sup>3</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff001"><label>1</label>
<addr-line>Department of Surgery and Anaesthesia, University of Otago, Wellington, New Zealand</addr-line>
</aff>
<aff id="aff002"><label>2</label>
<addr-line>School of Biological Sciences, Victoria University of Wellington, Wellington, New Zealand</addr-line>
</aff>
<aff id="aff003"><label>3</label>
<addr-line>Wellington Cardiovascular Research Group, Wellington, New Zealand</addr-line>
</aff>
<aff id="aff004"><label>4</label>
<addr-line>Department of Cardiology, Wellington Hospital, Wellington, New Zealand</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Gay</surname>
<given-names>Nick</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1"><addr-line>University of Cambridge, UNITED KINGDOM</addr-line>
</aff>
<author-notes><fn fn-type="COI-statement" id="coi001"><p><bold>Competing Interests: </bold>
The authors have declared that no competing interests exist.</p>
</fn>
<corresp id="cor001">* E-mail: <email>kathryn.hally@otago.ac.nz</email>
</corresp>
</author-notes>
<pub-date pub-type="epub"><day>3</day>
<month>10</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="collection"><year>2019</year>
</pub-date>
<volume>14</volume>
<issue>10</issue>
<elocation-id>e0223444</elocation-id>
<history><date date-type="received"><day>18</day>
<month>6</month>
<year>2019</year>
</date>
<date date-type="accepted"><day>20</day>
<month>9</month>
<year>2019</year>
</date>
</history>
<permissions><copyright-statement>© 2019 Hally et al</copyright-statement>
<copyright-year>2019</copyright-year>
<copyright-holder>Hally et al</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>
, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:href="pone.0223444.pdf"></self-uri>
<abstract><sec id="sec001"><title>Introduction</title>
<p>In addition to their role in facilitating leukocyte-mediated inflammation, platelets can dampen leukocyte pro-inflammatory responses in some contexts. Consequently, platelets are increasingly appreciated as regulators of inflammation. Together, platelets and neutrophils play a role in inflammation through Toll-like receptor (TLR) expression, although we do not fully understand how platelets shape neutrophil responses to TLR stimulation. Here, we aimed to determine the extent to which platelets can modulate neutrophil function in response to <italic>in vitro</italic>
stimulation with TLR4, TLR2/1, and TLR2/6 agonists.</p>
</sec>
<sec id="sec002"><title>Methods</title>
<p>Neutrophils from 10 healthy individuals were cultured alone or with autologous platelets. Neutrophils ± platelets were left unstimulated or were stimulated with 1 or 100 ng/mL lipopolysaccharide (LPS; a TLR4 agonist), Pam3CSK4 (a TLR2/1 agonist) and fibroblast-stimulating lipopeptide (FSL)-1 (a TLR2/6 agonist). Neutrophil activation and phagocytic activity were assessed by flow cytometry, and elastase and interleukin-8 secretion were assessed by ELISA.</p>
</sec>
<sec id="sec003"><title>Results</title>
<p>The addition of platelets attenuated neutrophil CD66b and CD11b expression in response to various doses of Pam3CSK4 and FSL-1. Furthermore, platelet co-culture was associated with higher CD62L expression (indicating reduced CD62L shedding) in response to these TLR agonists. Platelets also reduced elastase secretion in unstimulated cultures and in response to low-dose TLR stimulation. Conversely, platelet co-culture increased neutrophil phagocytosis in unstimulated cultures and in response to low-dose Pam3CSK4 and FSL-1. Platelets also increased IL-8 secretion in response to low-dose LPS.</p>
</sec>
<sec id="sec004"><title>Conclusion</title>
<p>Platelets are complex immunomodulators that can attenuate some, and simultaneously augment other, neutrophil functions. This modulation can occur both in the absence and presence of TLR stimulation.</p>
</sec>
</abstract>
<funding-group><funding-statement>K.E.H. was supported by a Doctoral Scholarship from Victoria University of Wellington, New Zealand (<ext-link ext-link-type="uri" xlink:href="http://www.victoria.ac.nz">www.victoria.ac.nz</ext-link>
) and is currently supported by a Postdoctoral Fellowship from the Heart Foundation, New Zealand (<ext-link ext-link-type="uri" xlink:href="http://www.heartfoundation.org.nz">www.heartfoundation.org.nz</ext-link>
). G.K.B. is currently supported by a Doctoral Scholarship from Victoria University of Wellington. This study was funded by the Wellington Medical Research Foundation, Research For Life (2016/279; <ext-link ext-link-type="uri" xlink:href="http://www.researchforlife.org.nz">www.researchforlife.org.nz</ext-link>
). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement>
</funding-group>
<counts><fig-count count="8"></fig-count>
<table-count count="3"></table-count>
<page-count count="18"></page-count>
</counts>
<custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name>
<meta-value>All relevant data are within the manuscript and its Supporting Information files.</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
<notes><title>Data Availability</title>
<p>All relevant data are within the manuscript and its Supporting Information files.</p>
</notes>
</front>
</pmc>
</record>
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