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CXCR4 identifies transitional bone marrow premonocytes that replenish the mature monocyte pool for peripheral responses

Identifieur interne : 002521 ( Pmc/Curation ); précédent : 002520; suivant : 002522

CXCR4 identifies transitional bone marrow premonocytes that replenish the mature monocyte pool for peripheral responses

Auteurs : Shu Zhen Chong ; Maximilien Evrard ; Sapna Devi ; Jinmiao Chen ; Jyue Yuan Lim ; Peter See ; Yiru Zhang ; José M. Adrover ; Bernett Lee ; Leonard Tan ; Jackson L. Y. Li ; Ka Hang Liong ; Cindy Phua ; Akhila Balachander ; Adrian Boey ; David Liebl ; Suet Mien Tan ; Jerry K. Y. Chan ; Karl Balabanian ; John E. Harris ; Mariaelvy Bianchini ; Christian Weber ; Johan Duchene ; Josephine Lum ; Michael Poidinger ; Qingfeng Chen ; Laurent Rénia ; Cheng-I Wang ; Anis Larbi ; Gwendalyn J. Randolph ; Wolfgang Weninger ; Mark R. Looney ; Matthew F. Krummel ; Subhra K. Biswas ; Florent Ginhoux ; Andrés Hidalgo ; Françoise Bachelerie ; Lai Guan Ng

Source :

RBID : PMC:5068243

Abstract

CXCR4 identifies an immobilized BM precursor (i.e., transitional premonocyte [TpMo]) that proliferates and replenishes mature Ly6Chi monocytes in mice and humans. Upon entering the circulation, CXCR4 governs monocyte margination in the lung vasculature.


Url:
DOI: 10.1084/jem.20160800
PubMed: 27811056
PubMed Central: 5068243

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PMC:5068243

Le document en format XML

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<name sortKey="Tan, Suet Mien" sort="Tan, Suet Mien" uniqKey="Tan S" first="Suet Mien" last="Tan">Suet Mien Tan</name>
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<name sortKey="Weber, Christian" sort="Weber, Christian" uniqKey="Weber C" first="Christian" last="Weber">Christian Weber</name>
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<name sortKey="Duchene, Johan" sort="Duchene, Johan" uniqKey="Duchene J" first="Johan" last="Duchene">Johan Duchene</name>
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<name sortKey="Lum, Josephine" sort="Lum, Josephine" uniqKey="Lum J" first="Josephine" last="Lum">Josephine Lum</name>
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<name sortKey="Chen, Qingfeng" sort="Chen, Qingfeng" uniqKey="Chen Q" first="Qingfeng" last="Chen">Qingfeng Chen</name>
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<name sortKey="Looney, Mark R" sort="Looney, Mark R" uniqKey="Looney M" first="Mark R." last="Looney">Mark R. Looney</name>
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<name sortKey="Krummel, Matthew F" sort="Krummel, Matthew F" uniqKey="Krummel M" first="Matthew F." last="Krummel">Matthew F. Krummel</name>
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<name sortKey="Biswas, Subhra K" sort="Biswas, Subhra K" uniqKey="Biswas S" first="Subhra K." last="Biswas">Subhra K. Biswas</name>
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<name sortKey="Ginhoux, Florent" sort="Ginhoux, Florent" uniqKey="Ginhoux F" first="Florent" last="Ginhoux">Florent Ginhoux</name>
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<name sortKey="Hidalgo, Andres" sort="Hidalgo, Andres" uniqKey="Hidalgo A" first="Andrés" last="Hidalgo">Andrés Hidalgo</name>
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<name sortKey="Bachelerie, Francoise" sort="Bachelerie, Francoise" uniqKey="Bachelerie F" first="Françoise" last="Bachelerie">Françoise Bachelerie</name>
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<name sortKey="Ng, Lai Guan" sort="Ng, Lai Guan" uniqKey="Ng L" first="Lai Guan" last="Ng">Lai Guan Ng</name>
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<title xml:lang="en" level="a" type="main">CXCR4 identifies transitional bone marrow premonocytes that replenish the mature monocyte pool for peripheral responses</title>
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<name sortKey="Chen, Jinmiao" sort="Chen, Jinmiao" uniqKey="Chen J" first="Jinmiao" last="Chen">Jinmiao Chen</name>
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<name sortKey="Lim, Jyue Yuan" sort="Lim, Jyue Yuan" uniqKey="Lim J" first="Jyue Yuan" last="Lim">Jyue Yuan Lim</name>
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<name sortKey="Zhang, Yiru" sort="Zhang, Yiru" uniqKey="Zhang Y" first="Yiru" last="Zhang">Yiru Zhang</name>
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<name sortKey="Adrover, Jose M" sort="Adrover, Jose M" uniqKey="Adrover J" first="José M." last="Adrover">José M. Adrover</name>
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<name sortKey="Lee, Bernett" sort="Lee, Bernett" uniqKey="Lee B" first="Bernett" last="Lee">Bernett Lee</name>
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<name sortKey="Tan, Leonard" sort="Tan, Leonard" uniqKey="Tan L" first="Leonard" last="Tan">Leonard Tan</name>
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<name sortKey="Li, Jackson L Y" sort="Li, Jackson L Y" uniqKey="Li J" first="Jackson L. Y." last="Li">Jackson L. Y. Li</name>
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<name sortKey="Liong, Ka Hang" sort="Liong, Ka Hang" uniqKey="Liong K" first="Ka Hang" last="Liong">Ka Hang Liong</name>
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<name sortKey="Phua, Cindy" sort="Phua, Cindy" uniqKey="Phua C" first="Cindy" last="Phua">Cindy Phua</name>
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<nlm:aff id="aff1">
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</nlm:aff>
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<author>
<name sortKey="Balachander, Akhila" sort="Balachander, Akhila" uniqKey="Balachander A" first="Akhila" last="Balachander">Akhila Balachander</name>
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</nlm:aff>
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<name sortKey="Boey, Adrian" sort="Boey, Adrian" uniqKey="Boey A" first="Adrian" last="Boey">Adrian Boey</name>
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<name sortKey="Liebl, David" sort="Liebl, David" uniqKey="Liebl D" first="David" last="Liebl">David Liebl</name>
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<nlm:aff id="aff5">
<institution>Institute of Medical Biology (IMB)-Institute of Molecular and Cell Biology (IMCB) Electron Microscopy Suite, A*STAR (Agency for Science, Technology and Research), Biopolis, 138671 Singapore</institution>
</nlm:aff>
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<institution>School of Biological Sciences, Nanyang Technological University, 637551 Singapore</institution>
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<name sortKey="Chan, Jerry K Y" sort="Chan, Jerry K Y" uniqKey="Chan J" first="Jerry K. Y." last="Chan">Jerry K. Y. Chan</name>
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<institution>Experimental Fetal Medicine Group, Yong Loo Lin School of Medicine, National University of Singapore, 119228 Singapore</institution>
</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="aff7">
<institution>Department of Reproductive Medicine, KK Women’s and Children’s Hospital, 229899 Singapore</institution>
</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="aff8">
<institution>Cancer and Stem Cell Biology Program, Duke-NUS Graduate Medical School, 169857 Singapore</institution>
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<name sortKey="Harris, John E" sort="Harris, John E" uniqKey="Harris J" first="John E." last="Harris">John E. Harris</name>
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<nlm:aff id="aff10">
<institution>Department of Medicine, University of Massachusetts Medical School, Worcester, MA 01605</institution>
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<author>
<name sortKey="Bianchini, Mariaelvy" sort="Bianchini, Mariaelvy" uniqKey="Bianchini M" first="Mariaelvy" last="Bianchini">Mariaelvy Bianchini</name>
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<institution>Institute for Cardiovascular Prevention, Ludwig-Maximilians-University Munich, Munich 80336, Germany</institution>
</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Weber, Christian" sort="Weber, Christian" uniqKey="Weber C" first="Christian" last="Weber">Christian Weber</name>
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<nlm:aff id="aff11">
<institution>Institute for Cardiovascular Prevention, Ludwig-Maximilians-University Munich, Munich 80336, Germany</institution>
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<institution>Institute for Cardiovascular Prevention, Ludwig-Maximilians-University Munich, Munich 80336, Germany</institution>
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<institution>Singapore Immunology Network (SIgN), A*STAR (Agency for Science, Technology and Research), Biopolis, 138648 Singapore</institution>
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<institution>Singapore Immunology Network (SIgN), A*STAR (Agency for Science, Technology and Research), Biopolis, 138648 Singapore</institution>
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</affiliation>
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<nlm:aff id="aff11">
<institution>Institute for Cardiovascular Prevention, Ludwig-Maximilians-University Munich, Munich 80336, Germany</institution>
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<name sortKey="Bachelerie, Francoise" sort="Bachelerie, Francoise" uniqKey="Bachelerie F" first="Françoise" last="Bachelerie">Françoise Bachelerie</name>
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<institution>School of Biological Sciences, Nanyang Technological University, 637551 Singapore</institution>
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</analytic>
<series>
<title level="j">The Journal of Experimental Medicine</title>
<idno type="ISSN">0022-1007</idno>
<idno type="eISSN">1540-9538</idno>
<imprint>
<date when="2016">2016</date>
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</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc>
<textClass></textClass>
</profileDesc>
</teiHeader>
<front>
<div type="abstract" xml:lang="en">
<p>CXCR4 identifies an immobilized BM precursor (i.e., transitional premonocyte [TpMo]) that proliferates and replenishes mature Ly6C
<sup>hi</sup>
monocytes in mice and humans. Upon entering the circulation, CXCR4 governs monocyte margination in the lung vasculature.</p>
</div>
</front>
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<pmc article-type="research-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">J Exp Med</journal-id>
<journal-id journal-id-type="iso-abbrev">J. Exp. Med</journal-id>
<journal-id journal-id-type="publisher-id">jem</journal-id>
<journal-id journal-id-type="hwp">jem</journal-id>
<journal-title-group>
<journal-title>The Journal of Experimental Medicine</journal-title>
</journal-title-group>
<issn pub-type="ppub">0022-1007</issn>
<issn pub-type="epub">1540-9538</issn>
<publisher>
<publisher-name>The Rockefeller University Press</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">27811056</article-id>
<article-id pub-id-type="pmc">5068243</article-id>
<article-id pub-id-type="publisher-id">20160800</article-id>
<article-id pub-id-type="doi">10.1084/jem.20160800</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Research Articles</subject>
<subj-group>
<subject>Article</subject>
</subj-group>
</subj-group>
<subj-group subj-group-type="hwp-journal-coll">
<subject>311</subject>
<subject>315</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>CXCR4 identifies transitional bone marrow premonocytes that replenish the mature monocyte pool for peripheral responses</article-title>
<alt-title alt-title-type="short">CXCR4 in monocyte development and lung margination</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Chong</surname>
<given-names>Shu Zhen</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="author-notes" rid="afn16">*</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Evrard</surname>
<given-names>Maximilien</given-names>
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</contrib>
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</contrib>
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<given-names>Peter</given-names>
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<given-names>Ka Hang</given-names>
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<surname>Larbi</surname>
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<given-names>Gwendalyn J.</given-names>
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<given-names>Wolfgang</given-names>
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<given-names>Mark R.</given-names>
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<name>
<surname>Krummel</surname>
<given-names>Matthew F.</given-names>
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</contrib>
<contrib contrib-type="author">
<name>
<surname>Biswas</surname>
<given-names>Subhra K.</given-names>
</name>
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<given-names>Florent</given-names>
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<name>
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<given-names>Andrés</given-names>
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<name>
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<name>
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<given-names>Lai Guan</given-names>
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<xref ref-type="aff" rid="aff2">2</xref>
</contrib>
</contrib-group>
<aff id="aff1">
<label>1</label>
<institution>Singapore Immunology Network (SIgN), A*STAR (Agency for Science, Technology and Research), Biopolis, 138648 Singapore</institution>
</aff>
<aff id="aff2">
<label>2</label>
<institution>School of Biological Sciences, Nanyang Technological University, 637551 Singapore</institution>
</aff>
<aff id="aff3">
<label>3</label>
<institution>Institute of Molecular and Cell Biology (IMCB), A*STAR (Agency for Science, Technology and Research), Biopolis, 138673 Singapore</institution>
</aff>
<aff id="aff4">
<label>4</label>
<institution>Area of Cell and Developmental Biology, Fundación Centro Nacional de Investigaciones Cardiovasculares (CNIC), Madrid 28029, Spain</institution>
</aff>
<aff id="aff5">
<label>5</label>
<institution>Institute of Medical Biology (IMB)-Institute of Molecular and Cell Biology (IMCB) Electron Microscopy Suite, A*STAR (Agency for Science, Technology and Research), Biopolis, 138671 Singapore</institution>
</aff>
<aff id="aff6">
<label>6</label>
<institution>Experimental Fetal Medicine Group, Yong Loo Lin School of Medicine, National University of Singapore, 119228 Singapore</institution>
</aff>
<aff id="aff7">
<label>7</label>
<institution>Department of Reproductive Medicine, KK Women’s and Children’s Hospital, 229899 Singapore</institution>
</aff>
<aff id="aff8">
<label>8</label>
<institution>Cancer and Stem Cell Biology Program, Duke-NUS Graduate Medical School, 169857 Singapore</institution>
</aff>
<aff id="aff9">
<label>9</label>
<institution>INSERM UMR-S996, Laboratory of Excellence in Research on Medication and Innovative Therapeutics, Université Paris-Sud, 92140 Clamart, France</institution>
</aff>
<aff id="aff10">
<label>10</label>
<institution>Department of Medicine, University of Massachusetts Medical School, Worcester, MA 01605</institution>
</aff>
<aff id="aff11">
<label>11</label>
<institution>Institute for Cardiovascular Prevention, Ludwig-Maximilians-University Munich, Munich 80336, Germany</institution>
</aff>
<aff id="aff12">
<label>12</label>
<institution>Division of Immunobiology, Washington University, St. Louis, MO 63110</institution>
</aff>
<aff id="aff13">
<label>13</label>
<institution>Centenary Institute for Cancer Medicine and Cell Biology, Newton, New South Wales 2042, Australia</institution>
</aff>
<aff id="aff14">
<label>14</label>
<institution>Department of Medicine and Pathology, Cardiovascular Research Institute, University of California, San Francisco, San Francisco, CA 94143</institution>
</aff>
<author-notes>
<corresp id="cor15">Correspondence to Lai Guan Ng:
<email>Ng_Lai_Guan@immunol.a-star.edu.sg</email>
; or Shu Zhen Chong:
<email>Chong_Shu_Zhen@immunol.a-star.edu.sg</email>
</corresp>
<fn id="afn16" fn-type="equal" specific-use="equal">
<label>*</label>
<p>S.Z. Chong and M. Evrard contributed equally to this paper.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub">
<day>17</day>
<month>10</month>
<year>2016</year>
</pub-date>
<volume>213</volume>
<issue>11</issue>
<fpage>2293</fpage>
<lpage>2314</lpage>
<history>
<date date-type="received">
<day>30</day>
<month>5</month>
<year>2016</year>
</date>
<date date-type="accepted">
<day>01</day>
<month>9</month>
<year>2016</year>
</date>
</history>
<permissions>
<copyright-statement>© 2016 Chong et al.</copyright-statement>
<copyright-year>2016</copyright-year>
<license license-type="openaccess">
<license-p>This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see
<ext-link ext-link-type="uri" xlink:href="http://www.rupress.org/terms">http://www.rupress.org/terms</ext-link>
). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 3.0 Unported license, as described at
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc-sa/3.0/">http://creativecommons.org/licenses/by-nc-sa/3.0/</ext-link>
).</license-p>
</license>
</permissions>
<self-uri xlink:role="icon" xlink:href="JEM_20160800_thumb.gif"></self-uri>
<abstract abstract-type="precis">
<p>CXCR4 identifies an immobilized BM precursor (i.e., transitional premonocyte [TpMo]) that proliferates and replenishes mature Ly6C
<sup>hi</sup>
monocytes in mice and humans. Upon entering the circulation, CXCR4 governs monocyte margination in the lung vasculature.</p>
</abstract>
<abstract>
<p>It is well established that Ly6C
<sup>hi</sup>
monocytes develop from common monocyte progenitors (cMoPs) and reside in the bone marrow (BM) until they are mobilized into the circulation. In our study, we found that BM Ly6C
<sup>hi</sup>
monocytes are not a homogenous population, as current data would suggest. Using computational analysis approaches to interpret multidimensional datasets, we demonstrate that BM Ly6C
<sup>hi</sup>
monocytes consist of two distinct subpopulations (CXCR4
<sup>hi</sup>
and CXCR4
<sup>lo</sup>
subpopulations) in both mice and humans. Transcriptome studies and in vivo assays revealed functional differences between the two subpopulations. Notably, the CXCR4
<sup>hi</sup>
subset proliferates and is immobilized in the BM for the replenishment of functionally mature CXCR4
<sup>lo</sup>
monocytes. We propose that the CXCR4
<sup>hi</sup>
subset represents a transitional premonocyte population, and that this sequential step of maturation from cMoPs serves to maintain a stable pool of BM monocytes. Additionally, reduced CXCR4 expression on monocytes, upon their exit into the circulation, does not reflect its diminished role in monocyte biology. Specifically, CXCR4 regulates monocyte peripheral cellular activities by governing their circadian oscillations and pulmonary margination, which contributes toward lung injury and sepsis mortality. Together, our study demonstrates the multifaceted role of CXCR4 in defining BM monocyte heterogeneity and in regulating their function in peripheral tissues.</p>
</abstract>
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<funding-source>A*STAR
<named-content content-type="funder-id">10.13039/501100001348</named-content>
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<funding-source>Deutsche Forschungsgemeinschaft
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</article-meta>
</front>
</pmc>
</record>

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