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Neurological heterotopic ossification following spinal cord injury is triggered by macrophage-mediated inflammation in muscle.

Identifieur interne : 002C59 ( PubMed/Curation ); précédent : 002C58; suivant : 002C60

Neurological heterotopic ossification following spinal cord injury is triggered by macrophage-mediated inflammation in muscle.

Auteurs : François Genêt [Australie] ; Irina Kulina [Australie] ; Cedryck Vaquette [Australie] ; Frédéric Torossian [France] ; Susan Millard [Australie] ; Allison R. Pettit [Australie] ; Natalie A. Sims [Australie] ; Adrienne Anginot [France] ; Bernadette Guerton [France] ; Ingrid G. Winkler [Australie] ; Valérie Barbier [Australie] ; Jean-Jacques Lataillade [France] ; Marie-Caroline Le Bousse-Kerdilès [France] ; Dietmar W. Hutmacher [Australie] ; Jean-Pierre Levesque [Australie]

Source :

The Journal of pathology [ 1096-9896 ] ; 2015.

RBID : pubmed:25712044

Descripteurs français

KwdFr :
- Animaux, Cardiotoxines (pharmacologie), Cellules souches (physiologie), Femelle, Humains, Macrophages (physiologie), Modèles animaux de maladie humaine, Muscles squelettiques (cytologie), Muscles squelettiques (physiologie), Myosite (étiologie), Ossification hétérotopique (étiologie), Paraplégie (), Souris de lignée C57BL, Traumatismes de la moelle épinière ().
MESH :
- cytologie : Muscles squelettiques.
- pharmacologie : Cardiotoxines.
- physiologie : Cellules souches, Macrophages, Muscles squelettiques.
- étiologie : Myosite, Ossification hétérotopique.
- Animaux, Femelle, Humains, Modèles animaux de maladie humaine, Paraplégie, Souris de lignée C57BL, Traumatismes de la moelle épinière.

English descriptors

KwdEn :
- Animals, Cardiotoxins (pharmacology), Disease Models, Animal, Female, Humans, Macrophages (physiology), Mice, Inbred C57BL, Muscle, Skeletal (cytology), Muscle, Skeletal (physiology), Myositis (etiology), Ossification, Heterotopic (etiology), Paraplegia (complications), Spinal Cord Injuries (complications), Stem Cells (physiology).
MESH :
- chemical , pharmacology : Cardiotoxins.
- complications : Paraplegia, Spinal Cord Injuries.
- cytology : Muscle, Skeletal.
- etiology : Myositis, Ossification, Heterotopic.
- physiology : Macrophages, Muscle, Skeletal, Stem Cells.
- Animals, Disease Models, Animal, Female, Humans, Mice, Inbred C57BL.

Abstract

Neurological heterotopic ossification (NHO) is the abnormal formation of bone in soft tissues as a consequence of spinal cord or traumatic brain injury. NHO causes pain, ankyloses, vascular and nerve compression and delays rehabilitation in this high-morbidity patient group. The pathological mechanisms leading to NHO remain unknown and consequently there are no therapeutic options to prevent or reduce NHO. Genetically modified mouse models of rare genetic forms of heterotopic ossification (HO) exist, but their relevance to NHO is questionable. Consequently, we developed the first model of spinal cord injury (SCI)-induced NHO in genetically unmodified mice. Formation of NHO, measured by micro-computed tomography, required the combination of both SCI and localized muscular inflammation. Our NHO model faithfully reproduced many clinical features of NHO in SCI patients and both human and mouse NHO tissues contained macrophages. Muscle-derived mesenchymal progenitors underwent osteoblast differentiation in vitro in response to serum from NHO mice without additional exogenous osteogenic stimuli. Substance P was identified as a candidate NHO systemic neuropeptide, as it was significantly elevated in the serum of NHO patients. However, antagonism of substance P receptor in our NHO model only modestly reduced the volume of NHO. In contrast, ablation of phagocytic macrophages with clodronate-loaded liposomes reduced the size of NHO by 90%, supporting the conclusion that NHO is highly dependent on inflammation and phagocytic macrophages in soft tissues. Overall, we have developed the first clinically relevant model of NHO and demonstrated that a combined insult of neurological injury and soft tissue inflammation drives NHO pathophysiology.

DOI: 10.1002/path.4519
PubMed: 25712044

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<term>Cardiotoxins (pharmacology)</term>
<term>Disease Models, Animal</term>
<term>Female</term>
<term>Humans</term>
<term>Macrophages (physiology)</term>
<term>Mice, Inbred C57BL</term>
<term>Muscle, Skeletal (cytology)</term>
<term>Muscle, Skeletal (physiology)</term>
<term>Myositis (etiology)</term>
<term>Ossification, Heterotopic (etiology)</term>
<term>Paraplegia (complications)</term>
<term>Spinal Cord Injuries (complications)</term>
<term>Stem Cells (physiology)</term>
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<keywords scheme="KwdFr" xml:lang="fr"><term>Animaux</term>
<term>Cardiotoxines (pharmacologie)</term>
<term>Cellules souches (physiologie)</term>
<term>Femelle</term>
<term>Humains</term>
<term>Macrophages (physiologie)</term>
<term>Modèles animaux de maladie humaine</term>
<term>Muscles squelettiques (cytologie)</term>
<term>Muscles squelettiques (physiologie)</term>
<term>Myosite (étiologie)</term>
<term>Ossification hétérotopique (étiologie)</term>
<term>Paraplégie ()</term>
<term>Souris de lignée C57BL</term>
<term>Traumatismes de la moelle épinière ()</term>
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<keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en"><term>Cardiotoxins</term>
</keywords>
<keywords scheme="MESH" qualifier="complications" xml:lang="en"><term>Paraplegia</term>
<term>Spinal Cord Injuries</term>
</keywords>
<keywords scheme="MESH" qualifier="cytologie" xml:lang="fr"><term>Muscles squelettiques</term>
</keywords>
<keywords scheme="MESH" qualifier="cytology" xml:lang="en"><term>Muscle, Skeletal</term>
</keywords>
<keywords scheme="MESH" qualifier="etiology" xml:lang="en"><term>Myositis</term>
<term>Ossification, Heterotopic</term>
</keywords>
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</keywords>
<keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Cellules souches</term>
<term>Macrophages</term>
<term>Muscles squelettiques</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Macrophages</term>
<term>Muscle, Skeletal</term>
<term>Stem Cells</term>
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<keywords scheme="MESH" qualifier="étiologie" xml:lang="fr"><term>Myosite</term>
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<term>Femelle</term>
<term>Humains</term>
<term>Modèles animaux de maladie humaine</term>
<term>Paraplégie</term>
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<front><div type="abstract" xml:lang="en">Neurological heterotopic ossification (NHO) is the abnormal formation of bone in soft tissues as a consequence of spinal cord or traumatic brain injury. NHO causes pain, ankyloses, vascular and nerve compression and delays rehabilitation in this high-morbidity patient group. The pathological mechanisms leading to NHO remain unknown and consequently there are no therapeutic options to prevent or reduce NHO. Genetically modified mouse models of rare genetic forms of heterotopic ossification (HO) exist, but their relevance to NHO is questionable. Consequently, we developed the first model of spinal cord injury (SCI)-induced NHO in genetically unmodified mice. Formation of NHO, measured by micro-computed tomography, required the combination of both SCI and localized muscular inflammation. Our NHO model faithfully reproduced many clinical features of NHO in SCI patients and both human and mouse NHO tissues contained macrophages. Muscle-derived mesenchymal progenitors underwent osteoblast differentiation in vitro in response to serum from NHO mice without additional exogenous osteogenic stimuli. Substance P was identified as a candidate NHO systemic neuropeptide, as it was significantly elevated in the serum of NHO patients. However, antagonism of substance P receptor in our NHO model only modestly reduced the volume of NHO. In contrast, ablation of phagocytic macrophages with clodronate-loaded liposomes reduced the size of NHO by 90%, supporting the conclusion that NHO is highly dependent on inflammation and phagocytic macrophages in soft tissues. Overall, we have developed the first clinically relevant model of NHO and demonstrated that a combined insult of neurological injury and soft tissue inflammation drives NHO pathophysiology.</div>
</front>
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<DateRevised><Year>2015</Year>
<Month>05</Month>
<Day>11</Day>
</DateRevised>
<Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1096-9896</ISSN>
<JournalIssue CitedMedium="Internet"><Volume>236</Volume>
<Issue>2</Issue>
<PubDate><Year>2015</Year>
<Month>Jun</Month>
</PubDate>
</JournalIssue>
<Title>The Journal of pathology</Title>
<ISOAbbreviation>J. Pathol.</ISOAbbreviation>
</Journal>
<ArticleTitle>Neurological heterotopic ossification following spinal cord injury is triggered by macrophage-mediated inflammation in muscle.</ArticleTitle>
<Pagination><MedlinePgn>229-40</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1002/path.4519</ELocationID>
<Abstract><AbstractText>Neurological heterotopic ossification (NHO) is the abnormal formation of bone in soft tissues as a consequence of spinal cord or traumatic brain injury. NHO causes pain, ankyloses, vascular and nerve compression and delays rehabilitation in this high-morbidity patient group. The pathological mechanisms leading to NHO remain unknown and consequently there are no therapeutic options to prevent or reduce NHO. Genetically modified mouse models of rare genetic forms of heterotopic ossification (HO) exist, but their relevance to NHO is questionable. Consequently, we developed the first model of spinal cord injury (SCI)-induced NHO in genetically unmodified mice. Formation of NHO, measured by micro-computed tomography, required the combination of both SCI and localized muscular inflammation. Our NHO model faithfully reproduced many clinical features of NHO in SCI patients and both human and mouse NHO tissues contained macrophages. Muscle-derived mesenchymal progenitors underwent osteoblast differentiation in vitro in response to serum from NHO mice without additional exogenous osteogenic stimuli. Substance P was identified as a candidate NHO systemic neuropeptide, as it was significantly elevated in the serum of NHO patients. However, antagonism of substance P receptor in our NHO model only modestly reduced the volume of NHO. In contrast, ablation of phagocytic macrophages with clodronate-loaded liposomes reduced the size of NHO by 90%, supporting the conclusion that NHO is highly dependent on inflammation and phagocytic macrophages in soft tissues. Overall, we have developed the first clinically relevant model of NHO and demonstrated that a combined insult of neurological injury and soft tissue inflammation drives NHO pathophysiology.</AbstractText>
<CopyrightInformation>Copyright © 2015 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Genêt</LastName>
<ForeName>François</ForeName>
<Initials>F</Initials>
<AffiliationInfo><Affiliation>Blood and Bone Diseases Programme, Mater Research Institute, University of Queensland, Woolloongabba, Australia.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Department of Physical Medicine and Rehabilitation, Hôpital Raymond Poincaré, APHP, CIC-IT 1429, Garches, France.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Université Versailles Saint Quentin en Yvelines, END:ICAP U1179 INSERM, UFR des Sciences de la Santé-Simone Veil, Montigny le Bretonneux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Kulina</LastName>
<ForeName>Irina</ForeName>
<Initials>I</Initials>
<AffiliationInfo><Affiliation>Blood and Bone Diseases Programme, Mater Research Institute, University of Queensland, Woolloongabba, Australia.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>School of Medicine, University of Queensland, Herston, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Vaquette</LastName>
<ForeName>Cedryck</ForeName>
<Initials>C</Initials>
<AffiliationInfo><Affiliation>Institute of Health Biomedical Innovation, Queensland University of Technology, Kelvin Grove, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Torossian</LastName>
<ForeName>Frédéric</ForeName>
<Initials>F</Initials>
<AffiliationInfo><Affiliation>Institut National de la Santé et de la Recherche Médicale, Unité 972, Villejuif, France.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Université Paris-Sud, Institut André Lwoff, Paris, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Millard</LastName>
<ForeName>Susan</ForeName>
<Initials>S</Initials>
<AffiliationInfo><Affiliation>Blood and Bone Diseases Programme, Mater Research Institute, University of Queensland, Woolloongabba, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Pettit</LastName>
<ForeName>Allison R</ForeName>
<Initials>AR</Initials>
<AffiliationInfo><Affiliation>Blood and Bone Diseases Programme, Mater Research Institute, University of Queensland, Woolloongabba, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Sims</LastName>
<ForeName>Natalie A</ForeName>
<Initials>NA</Initials>
<AffiliationInfo><Affiliation>St Vincent's Institute of Medical Research, Fitzroy, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Anginot</LastName>
<ForeName>Adrienne</ForeName>
<Initials>A</Initials>
<AffiliationInfo><Affiliation>Institut National de la Santé et de la Recherche Médicale, Unité 972, Villejuif, France.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Université Paris-Sud, Institut André Lwoff, Paris, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Guerton</LastName>
<ForeName>Bernadette</ForeName>
<Initials>B</Initials>
<AffiliationInfo><Affiliation>Institut National de la Santé et de la Recherche Médicale, Unité 972, Villejuif, France.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Université Paris-Sud, Institut André Lwoff, Paris, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Winkler</LastName>
<ForeName>Ingrid G</ForeName>
<Initials>IG</Initials>
<AffiliationInfo><Affiliation>Blood and Bone Diseases Programme, Mater Research Institute, University of Queensland, Woolloongabba, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Barbier</LastName>
<ForeName>Valérie</ForeName>
<Initials>V</Initials>
<AffiliationInfo><Affiliation>Blood and Bone Diseases Programme, Mater Research Institute, University of Queensland, Woolloongabba, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Lataillade</LastName>
<ForeName>Jean-Jacques</ForeName>
<Initials>JJ</Initials>
<AffiliationInfo><Affiliation>Institut National de la Santé et de la Recherche Médicale, Unité 972, Villejuif, France.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Centre de Transfusion Sanguine des Armées, Clamart, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Le Bousse-Kerdilès</LastName>
<ForeName>Marie-Caroline</ForeName>
<Initials>MC</Initials>
<AffiliationInfo><Affiliation>Institut National de la Santé et de la Recherche Médicale, Unité 972, Villejuif, France.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Université Paris-Sud, Institut André Lwoff, Paris, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Hutmacher</LastName>
<ForeName>Dietmar W</ForeName>
<Initials>DW</Initials>
<AffiliationInfo><Affiliation>Blood and Bone Diseases Programme, Mater Research Institute, University of Queensland, Woolloongabba, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Levesque</LastName>
<ForeName>Jean-Pierre</ForeName>
<Initials>JP</Initials>
<AffiliationInfo><Affiliation>Blood and Bone Diseases Programme, Mater Research Institute, University of Queensland, Woolloongabba, Australia.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>School of Medicine, University of Queensland, Herston, Australia.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic"><Year>2015</Year>
<Month>03</Month>
<Day>26</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo><Country>England</Country>
<MedlineTA>J Pathol</MedlineTA>
<NlmUniqueID>0204634</NlmUniqueID>
<ISSNLinking>0022-3417</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList><Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D054715">Cardiotoxins</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList><MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D054715" MajorTopicYN="N">Cardiotoxins</DescriptorName>
<QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D004195" MajorTopicYN="N">Disease Models, Animal</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D005260" MajorTopicYN="N">Female</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D006801" MajorTopicYN="N">Humans</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D008264" MajorTopicYN="N">Macrophages</DescriptorName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D008810" MajorTopicYN="N">Mice, Inbred C57BL</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D018482" MajorTopicYN="N">Muscle, Skeletal</DescriptorName>
<QualifierName UI="Q000166" MajorTopicYN="N">cytology</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D009220" MajorTopicYN="N">Myositis</DescriptorName>
<QualifierName UI="Q000209" MajorTopicYN="Y">etiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D009999" MajorTopicYN="N">Ossification, Heterotopic</DescriptorName>
<QualifierName UI="Q000209" MajorTopicYN="Y">etiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D010264" MajorTopicYN="N">Paraplegia</DescriptorName>
<QualifierName UI="Q000150" MajorTopicYN="N">complications</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D013119" MajorTopicYN="N">Spinal Cord Injuries</DescriptorName>
<QualifierName UI="Q000150" MajorTopicYN="Y">complications</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D013234" MajorTopicYN="N">Stem Cells</DescriptorName>
<QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">heterotopic ossification</Keyword>
<Keyword MajorTopicYN="N">inflammation</Keyword>
<Keyword MajorTopicYN="N">macrophage</Keyword>
<Keyword MajorTopicYN="N">spinal cord injury</Keyword>
</KeywordList>
</MedlineCitation>
<PubmedData><History><PubMedPubDate PubStatus="received"><Year>2015</Year>
<Month>01</Month>
<Day>08</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="revised"><Year>2015</Year>
<Month>02</Month>
<Day>17</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted"><Year>2015</Year>
<Month>02</Month>
<Day>19</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez"><Year>2015</Year>
<Month>2</Month>
<Day>26</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="pubmed"><Year>2015</Year>
<Month>2</Month>
<Day>26</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="medline"><Year>2015</Year>
<Month>7</Month>
<Day>21</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>ppublish</PublicationStatus>
<ArticleIdList><ArticleId IdType="pubmed">25712044</ArticleId>
<ArticleId IdType="doi">10.1002/path.4519</ArticleId>
</ArticleIdList>
</PubmedData>
</pubmed>
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Neurological heterotopic ossification following spinal cord injury is triggered by macrophage-mediated inflammation in muscle.

Neurological heterotopic ossification following spinal cord injury is triggered by macrophage-mediated inflammation in muscle.

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