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In Vivo Imaging Reveals a Pioneer Wave of Monocyte Recruitment into Mouse Skin Wounds

Identifieur interne : 003817 ( Main/Exploration ); précédent : 003816; suivant : 003818

In Vivo Imaging Reveals a Pioneer Wave of Monocyte Recruitment into Mouse Skin Wounds

Auteurs : Mathieu P. Rodero [France] ; Fabrice Licata [France] ; Lucie Poupel [France] ; Pauline Hamon [France] ; Kiarash Khosrotehrani [Australie] ; Christophe Combadiere [France] ; Alexandre Boissonnas [France]

Source :

RBID : PMC:4182700

Descripteurs français

English descriptors

Abstract

The cells of the mononuclear phagocyte system are essential for the correct healing of adult skin wounds, but their specific functions remain ill-defined. The absence of granulation tissue immediately after skin injury makes it challenging to study the role of mononuclear phagocytes at the initiation of this inflammatory stage. To study their recruitment and migratory behavior within the wound bed, we developed a new model for real-time in vivo imaging of the wound, using transgenic mice that express green and cyan fluorescent proteins and specifically target monocytes. Within hours after the scalp injury, monocytes invaded the wound bed. The complete abrogation of this infiltration in monocyte-deficient CCR2−/− mice argues for the involvement of classical monocytes in this process. Monocyte infiltration unexpectedly occurred as early as neutrophil recruitment did and resulted from active release from the bloodstream toward the matrix through microhemorrhages rather than transendothelial migration. Monocytes randomly scouted around the wound bed, progressively slowed down, and stopped. Our approach identified and characterized a rapid and earlier than expected wave of monocyte infiltration and provides a novel framework for investigating the role of these cells during early stages of wound healing.


Url:
DOI: 10.1371/journal.pone.0108212
PubMed: 25272047
PubMed Central: 4182700


Affiliations:


Links toward previous steps (curation, corpus...)


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<nlm:aff id="aff5">
<addr-line>CNRS, ERL, CIMI, 91 Bd de l’hôpital, Paris, France</addr-line>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>CNRS, ERL, CIMI, 91 Bd de l’hôpital, Paris</wicri:regionArea>
<placeName>
<region type="region">Île-de-France</region>
<region type="old region">Île-de-France</region>
<settlement type="city">Paris</settlement>
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</author>
<author>
<name sortKey="Khosrotehrani, Kiarash" sort="Khosrotehrani, Kiarash" uniqKey="Khosrotehrani K" first="Kiarash" last="Khosrotehrani">Kiarash Khosrotehrani</name>
<affiliation wicri:level="1">
<nlm:aff id="aff3">
<addr-line>The University of Queensland, UQ Centre for Clinical Research, Brisbane, QLD, Australia</addr-line>
</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>The University of Queensland, UQ Centre for Clinical Research, Brisbane, QLD</wicri:regionArea>
<wicri:noRegion>QLD</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="aff4">
<addr-line>The University of Queensland, UQ Diamantina Institute, Translational Research Institute, Woolloongabba, QLD, Australia</addr-line>
</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>The University of Queensland, UQ Diamantina Institute, Translational Research Institute, Woolloongabba, QLD</wicri:regionArea>
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</affiliation>
</author>
<author>
<name sortKey="Combadiere, Christophe" sort="Combadiere, Christophe" uniqKey="Combadiere C" first="Christophe" last="Combadiere">Christophe Combadiere</name>
<affiliation wicri:level="3">
<nlm:aff id="aff1">
<addr-line>Sorbonne Universités, UPMC Univ Paris 06, CR7, Centre d’Immunologie et des Maladies Infectieuses (CIMI), 91 Bd de l’hôpital, Paris, France</addr-line>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Sorbonne Universités, UPMC Univ Paris 06, CR7, Centre d’Immunologie et des Maladies Infectieuses (CIMI), 91 Bd de l’hôpital, Paris</wicri:regionArea>
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<region type="region">Île-de-France</region>
<region type="old region">Île-de-France</region>
<settlement type="city">Paris</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3">
<nlm:aff id="aff2">
<addr-line>INSERM, U1135, CIMI, 91 Bd de l’hôpital, Paris, France</addr-line>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>INSERM, U1135, CIMI, 91 Bd de l’hôpital, Paris</wicri:regionArea>
<placeName>
<region type="region">Île-de-France</region>
<region type="old region">Île-de-France</region>
<settlement type="city">Paris</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3">
<nlm:aff id="aff5">
<addr-line>CNRS, ERL, CIMI, 91 Bd de l’hôpital, Paris, France</addr-line>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>CNRS, ERL, CIMI, 91 Bd de l’hôpital, Paris</wicri:regionArea>
<placeName>
<region type="region">Île-de-France</region>
<region type="old region">Île-de-France</region>
<settlement type="city">Paris</settlement>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Boissonnas, Alexandre" sort="Boissonnas, Alexandre" uniqKey="Boissonnas A" first="Alexandre" last="Boissonnas">Alexandre Boissonnas</name>
<affiliation wicri:level="3">
<nlm:aff id="aff1">
<addr-line>Sorbonne Universités, UPMC Univ Paris 06, CR7, Centre d’Immunologie et des Maladies Infectieuses (CIMI), 91 Bd de l’hôpital, Paris, France</addr-line>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Sorbonne Universités, UPMC Univ Paris 06, CR7, Centre d’Immunologie et des Maladies Infectieuses (CIMI), 91 Bd de l’hôpital, Paris</wicri:regionArea>
<placeName>
<region type="region">Île-de-France</region>
<region type="old region">Île-de-France</region>
<settlement type="city">Paris</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3">
<nlm:aff id="aff2">
<addr-line>INSERM, U1135, CIMI, 91 Bd de l’hôpital, Paris, France</addr-line>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>INSERM, U1135, CIMI, 91 Bd de l’hôpital, Paris</wicri:regionArea>
<placeName>
<region type="region">Île-de-France</region>
<region type="old region">Île-de-France</region>
<settlement type="city">Paris</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3">
<nlm:aff id="aff5">
<addr-line>CNRS, ERL, CIMI, 91 Bd de l’hôpital, Paris, France</addr-line>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>CNRS, ERL, CIMI, 91 Bd de l’hôpital, Paris</wicri:regionArea>
<placeName>
<region type="region">Île-de-France</region>
<region type="old region">Île-de-France</region>
<settlement type="city">Paris</settlement>
</placeName>
</affiliation>
</author>
</analytic>
<series>
<title level="j">PLoS ONE</title>
<idno type="eISSN">1932-6203</idno>
<imprint>
<date when="2014">2014</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc>
<textClass>
<keywords scheme="KwdEn" xml:lang="en">
<term>Animals</term>
<term>Chemotaxis, Leukocyte</term>
<term>Disease Models, Animal</term>
<term>Mice</term>
<term>Mice, Knockout</term>
<term>Microscopy, Fluorescence, Multiphoton</term>
<term>Monocytes (immunology)</term>
<term>Monocytes (pathology)</term>
<term>Neutrophil Infiltration</term>
<term>Skin (immunology)</term>
<term>Skin (pathology)</term>
<term>Wound Healing</term>
<term>Wounds and Injuries (immunology)</term>
<term>Wounds and Injuries (pathology)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Animaux</term>
<term>Chimiotaxie des leucocytes</term>
<term>Cicatrisation de plaie</term>
<term>Infiltration par les neutrophiles</term>
<term>Microscopie de fluorescence multiphotonique</term>
<term>Modèles animaux de maladie humaine</term>
<term>Monocytes (anatomopathologie)</term>
<term>Monocytes (immunologie)</term>
<term>Peau (anatomopathologie)</term>
<term>Peau (immunologie)</term>
<term>Plaies et blessures (anatomopathologie)</term>
<term>Plaies et blessures (immunologie)</term>
<term>Souris</term>
<term>Souris knockout</term>
</keywords>
<keywords scheme="MESH" qualifier="anatomopathologie" xml:lang="fr">
<term>Monocytes</term>
<term>Peau</term>
<term>Plaies et blessures</term>
</keywords>
<keywords scheme="MESH" qualifier="immunologie" xml:lang="fr">
<term>Monocytes</term>
<term>Peau</term>
<term>Plaies et blessures</term>
</keywords>
<keywords scheme="MESH" qualifier="immunology" xml:lang="en">
<term>Monocytes</term>
<term>Skin</term>
<term>Wounds and Injuries</term>
</keywords>
<keywords scheme="MESH" qualifier="pathology" xml:lang="en">
<term>Monocytes</term>
<term>Skin</term>
<term>Wounds and Injuries</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Animals</term>
<term>Chemotaxis, Leukocyte</term>
<term>Disease Models, Animal</term>
<term>Mice</term>
<term>Mice, Knockout</term>
<term>Microscopy, Fluorescence, Multiphoton</term>
<term>Neutrophil Infiltration</term>
<term>Wound Healing</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Animaux</term>
<term>Chimiotaxie des leucocytes</term>
<term>Cicatrisation de plaie</term>
<term>Infiltration par les neutrophiles</term>
<term>Microscopie de fluorescence multiphotonique</term>
<term>Modèles animaux de maladie humaine</term>
<term>Souris</term>
<term>Souris knockout</term>
</keywords>
</textClass>
</profileDesc>
</teiHeader>
<front>
<div type="abstract" xml:lang="en">
<p>The cells of the mononuclear phagocyte system are essential for the correct healing of adult skin wounds, but their specific functions remain ill-defined. The absence of granulation tissue immediately after skin injury makes it challenging to study the role of mononuclear phagocytes at the initiation of this inflammatory stage. To study their recruitment and migratory behavior within the wound bed, we developed a new model for real-time in vivo imaging of the wound, using transgenic mice that express green and cyan fluorescent proteins and specifically target monocytes. Within hours after the scalp injury, monocytes invaded the wound bed. The complete abrogation of this infiltration in monocyte-deficient CCR2
<sup>−/−</sup>
mice argues for the involvement of classical monocytes in this process. Monocyte infiltration unexpectedly occurred as early as neutrophil recruitment did and resulted from active release from the bloodstream toward the matrix through microhemorrhages rather than transendothelial migration. Monocytes randomly scouted around the wound bed, progressively slowed down, and stopped. Our approach identified and characterized a rapid and earlier than expected wave of monocyte infiltration and provides a novel framework for investigating the role of these cells during early stages of wound healing.</p>
</div>
</front>
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<name sortKey="Shi, Yq" uniqKey="Shi Y">YQ Shi</name>
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<author>
<name sortKey="Zhang, Wq" uniqKey="Zhang W">WQ Zhang</name>
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<author>
<name sortKey="Wen, Zl" uniqKey="Wen Z">ZL Wen</name>
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<name sortKey="Mantovani, A" uniqKey="Mantovani A">A Mantovani</name>
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<author>
<name sortKey="Cassatella, Ma" uniqKey="Cassatella M">MA Cassatella</name>
</author>
<author>
<name sortKey="Costantini, C" uniqKey="Costantini C">C Costantini</name>
</author>
<author>
<name sortKey="Jaillon, S" uniqKey="Jaillon S">S Jaillon</name>
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</analytic>
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<author>
<name sortKey="Abtin, A" uniqKey="Abtin A">A Abtin</name>
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<author>
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<author>
<name sortKey="Mitchell, Aj" uniqKey="Mitchell A">AJ Mitchell</name>
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<author>
<name sortKey="Roediger, B" uniqKey="Roediger B">B Roediger</name>
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<author>
<name sortKey="Brzoska, Aj" uniqKey="Brzoska A">AJ Brzoska</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Soehnlein, O" uniqKey="Soehnlein O">O Soehnlein</name>
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<author>
<name sortKey="Zernecke, A" uniqKey="Zernecke A">A Zernecke</name>
</author>
<author>
<name sortKey="Weber, C" uniqKey="Weber C">C Weber</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Weber, M" uniqKey="Weber M">M Weber</name>
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<author>
<name sortKey="Hauschild, R" uniqKey="Hauschild R">R Hauschild</name>
</author>
<author>
<name sortKey="Schwarz, J" uniqKey="Schwarz J">J Schwarz</name>
</author>
<author>
<name sortKey="Moussion, C" uniqKey="Moussion C">C Moussion</name>
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<author>
<name sortKey="De Vries, I" uniqKey="De Vries I">I de Vries</name>
</author>
</analytic>
</biblStruct>
<biblStruct>
<analytic>
<author>
<name sortKey="Sarris, M" uniqKey="Sarris M">M Sarris</name>
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<author>
<name sortKey="Masson, Jb" uniqKey="Masson J">JB Masson</name>
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<author>
<name sortKey="Maurin, D" uniqKey="Maurin D">D Maurin</name>
</author>
<author>
<name sortKey="Van Der Aa, Lm" uniqKey="Van Der Aa L">LM Van der Aa</name>
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<author>
<name sortKey="Boudinot, P" uniqKey="Boudinot P">P Boudinot</name>
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<country>
<li>Australie</li>
<li>France</li>
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<li>Île-de-France</li>
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<name sortKey="Rodero, Mathieu P" sort="Rodero, Mathieu P" uniqKey="Rodero M" first="Mathieu P." last="Rodero">Mathieu P. Rodero</name>
</region>
<name sortKey="Boissonnas, Alexandre" sort="Boissonnas, Alexandre" uniqKey="Boissonnas A" first="Alexandre" last="Boissonnas">Alexandre Boissonnas</name>
<name sortKey="Boissonnas, Alexandre" sort="Boissonnas, Alexandre" uniqKey="Boissonnas A" first="Alexandre" last="Boissonnas">Alexandre Boissonnas</name>
<name sortKey="Boissonnas, Alexandre" sort="Boissonnas, Alexandre" uniqKey="Boissonnas A" first="Alexandre" last="Boissonnas">Alexandre Boissonnas</name>
<name sortKey="Combadiere, Christophe" sort="Combadiere, Christophe" uniqKey="Combadiere C" first="Christophe" last="Combadiere">Christophe Combadiere</name>
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<name sortKey="Combadiere, Christophe" sort="Combadiere, Christophe" uniqKey="Combadiere C" first="Christophe" last="Combadiere">Christophe Combadiere</name>
<name sortKey="Hamon, Pauline" sort="Hamon, Pauline" uniqKey="Hamon P" first="Pauline" last="Hamon">Pauline Hamon</name>
<name sortKey="Hamon, Pauline" sort="Hamon, Pauline" uniqKey="Hamon P" first="Pauline" last="Hamon">Pauline Hamon</name>
<name sortKey="Hamon, Pauline" sort="Hamon, Pauline" uniqKey="Hamon P" first="Pauline" last="Hamon">Pauline Hamon</name>
<name sortKey="Licata, Fabrice" sort="Licata, Fabrice" uniqKey="Licata F" first="Fabrice" last="Licata">Fabrice Licata</name>
<name sortKey="Licata, Fabrice" sort="Licata, Fabrice" uniqKey="Licata F" first="Fabrice" last="Licata">Fabrice Licata</name>
<name sortKey="Licata, Fabrice" sort="Licata, Fabrice" uniqKey="Licata F" first="Fabrice" last="Licata">Fabrice Licata</name>
<name sortKey="Poupel, Lucie" sort="Poupel, Lucie" uniqKey="Poupel L" first="Lucie" last="Poupel">Lucie Poupel</name>
<name sortKey="Poupel, Lucie" sort="Poupel, Lucie" uniqKey="Poupel L" first="Lucie" last="Poupel">Lucie Poupel</name>
<name sortKey="Poupel, Lucie" sort="Poupel, Lucie" uniqKey="Poupel L" first="Lucie" last="Poupel">Lucie Poupel</name>
<name sortKey="Rodero, Mathieu P" sort="Rodero, Mathieu P" uniqKey="Rodero M" first="Mathieu P." last="Rodero">Mathieu P. Rodero</name>
<name sortKey="Rodero, Mathieu P" sort="Rodero, Mathieu P" uniqKey="Rodero M" first="Mathieu P." last="Rodero">Mathieu P. Rodero</name>
</country>
<country name="Australie">
<noRegion>
<name sortKey="Khosrotehrani, Kiarash" sort="Khosrotehrani, Kiarash" uniqKey="Khosrotehrani K" first="Kiarash" last="Khosrotehrani">Kiarash Khosrotehrani</name>
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<name sortKey="Khosrotehrani, Kiarash" sort="Khosrotehrani, Kiarash" uniqKey="Khosrotehrani K" first="Kiarash" last="Khosrotehrani">Kiarash Khosrotehrani</name>
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</record>

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