Influence of the Immune Microenvironment Provided by Implanted Biomaterials on the Biological Properties of Masquelet-Induced Membranes in Rats: Metakaolin as an Alternative Spacer

Macrophages play a key role in the inflammatory phase of wound repair and foreign body reactions—two important processes in the Masquelet-induced membrane technique for extremity reconstruction. The macrophage response depends largely on the nature of the biomaterials implanted. However, little is k...

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Main Authors: Marjorie Durand, Myriam Oger, Krisztina Nikovics, Julien Venant, Anne-Cecile Guillope, Eugénie Jouve, Laure Barbier, Laurent Bégot, Florence Poirier, Catherine Rousseau, Olivier Pitois, Laurent Mathieu, Anne-Laure Favier, Didier Lutomski, Jean-Marc Collombet
Format: Article
Language:English
Published: MDPI AG 2022-11-01
Series:Biomedicines
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Online Access:https://www.mdpi.com/2227-9059/10/12/3017
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author Marjorie Durand
Myriam Oger
Krisztina Nikovics
Julien Venant
Anne-Cecile Guillope
Eugénie Jouve
Laure Barbier
Laurent Bégot
Florence Poirier
Catherine Rousseau
Olivier Pitois
Laurent Mathieu
Anne-Laure Favier
Didier Lutomski
Jean-Marc Collombet
author_facet Marjorie Durand
Myriam Oger
Krisztina Nikovics
Julien Venant
Anne-Cecile Guillope
Eugénie Jouve
Laure Barbier
Laurent Bégot
Florence Poirier
Catherine Rousseau
Olivier Pitois
Laurent Mathieu
Anne-Laure Favier
Didier Lutomski
Jean-Marc Collombet
author_sort Marjorie Durand
collection DOAJ
description Macrophages play a key role in the inflammatory phase of wound repair and foreign body reactions—two important processes in the Masquelet-induced membrane technique for extremity reconstruction. The macrophage response depends largely on the nature of the biomaterials implanted. However, little is known about the influence of the macrophage microenvironment on the osteogenic properties of the induced membrane or subsequent bone regeneration. We used metakaolin, an immunogenic material, as an alternative spacer to standard polymethylmethacrylate (PMMA) in a Masquelet model in rats. Four weeks after implantation, the PMMA- and metakaolin-induced membranes were harvested, and their osteogenic properties and macrophage microenvironments were investigated by histology, immunohistochemistry, mass spectroscopy and gene expression analysis. The metakaolin spacer induced membranes with higher levels of two potent pro-osteogenic factors, transforming growth factor-β (TGF-β) and bone morphogenic protein-2 (BMP-2). These alternative membranes thus had greater osteogenic activity, which was accompanied by a significant expansion of the total macrophage population, including both the M1-like and M2-like subtypes. Microcomputed tomographic analysis showed that metakaolin-induced membranes supported bone regeneration more effectively than PMMA-induced membranes through better callus properties (+58%), although this difference was not significant. This study provides the first evidence of the influence of the immune microenvironment on the osteogenic properties of the induced membranes.
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spelling doaj.art-141b90b25ff14a8cb800bef5a1bad75a2023-11-24T13:25:17ZengMDPI AGBiomedicines2227-90592022-11-011012301710.3390/biomedicines10123017Influence of the Immune Microenvironment Provided by Implanted Biomaterials on the Biological Properties of Masquelet-Induced Membranes in Rats: Metakaolin as an Alternative SpacerMarjorie Durand0Myriam Oger1Krisztina Nikovics2Julien Venant3Anne-Cecile Guillope4Eugénie Jouve5Laure Barbier6Laurent Bégot7Florence Poirier8Catherine Rousseau9Olivier Pitois10Laurent Mathieu11Anne-Laure Favier12Didier Lutomski13Jean-Marc Collombet14Osteo-Articulary Biotherapy Unit, Department of Medical and Surgical Assistance to the Armed Forces, French Armed Forces Biomedical Research Institute, 91223 Brétigny-sur-Orge, FranceImaging Unit, Department of Platforms and Technology Research, French Armed Forces Biomedical Research Institute, 91223 Brétigny-sur-Orge, FranceImaging Unit, Department of Platforms and Technology Research, French Armed Forces Biomedical Research Institute, 91223 Brétigny-sur-Orge, FranceOsteo-Articulary Biotherapy Unit, Department of Medical and Surgical Assistance to the Armed Forces, French Armed Forces Biomedical Research Institute, 91223 Brétigny-sur-Orge, FranceOsteo-Articulary Biotherapy Unit, Department of Medical and Surgical Assistance to the Armed Forces, French Armed Forces Biomedical Research Institute, 91223 Brétigny-sur-Orge, FranceOsteo-Articulary Biotherapy Unit, Department of Medical and Surgical Assistance to the Armed Forces, French Armed Forces Biomedical Research Institute, 91223 Brétigny-sur-Orge, FranceMolecular Biology Unit, Department of Platforms and Technology Research, French Armed Forces Biomedical Research Institute, 91223 Brétigny-sur-Orge, FranceImaging Unit, Department of Platforms and Technology Research, French Armed Forces Biomedical Research Institute, 91223 Brétigny-sur-Orge, FranceTissue Engineering Research Unit-URIT, Sorbonne Paris Nord University, 93000 Bobigny, FranceMolecular Biology Unit, Department of Platforms and Technology Research, French Armed Forces Biomedical Research Institute, 91223 Brétigny-sur-Orge, FranceLaboratoire Navier, Gustave Eiffel University, Ecole des Ponts ParisTech, CNRS, 77447 Marne-la-Vallée, FranceOsteo-Articulary Biotherapy Unit, Department of Medical and Surgical Assistance to the Armed Forces, French Armed Forces Biomedical Research Institute, 91223 Brétigny-sur-Orge, FranceImaging Unit, Department of Platforms and Technology Research, French Armed Forces Biomedical Research Institute, 91223 Brétigny-sur-Orge, FranceTissue Engineering Research Unit-URIT, Sorbonne Paris Nord University, 93000 Bobigny, FranceOsteo-Articulary Biotherapy Unit, Department of Medical and Surgical Assistance to the Armed Forces, French Armed Forces Biomedical Research Institute, 91223 Brétigny-sur-Orge, FranceMacrophages play a key role in the inflammatory phase of wound repair and foreign body reactions—two important processes in the Masquelet-induced membrane technique for extremity reconstruction. The macrophage response depends largely on the nature of the biomaterials implanted. However, little is known about the influence of the macrophage microenvironment on the osteogenic properties of the induced membrane or subsequent bone regeneration. We used metakaolin, an immunogenic material, as an alternative spacer to standard polymethylmethacrylate (PMMA) in a Masquelet model in rats. Four weeks after implantation, the PMMA- and metakaolin-induced membranes were harvested, and their osteogenic properties and macrophage microenvironments were investigated by histology, immunohistochemistry, mass spectroscopy and gene expression analysis. The metakaolin spacer induced membranes with higher levels of two potent pro-osteogenic factors, transforming growth factor-β (TGF-β) and bone morphogenic protein-2 (BMP-2). These alternative membranes thus had greater osteogenic activity, which was accompanied by a significant expansion of the total macrophage population, including both the M1-like and M2-like subtypes. Microcomputed tomographic analysis showed that metakaolin-induced membranes supported bone regeneration more effectively than PMMA-induced membranes through better callus properties (+58%), although this difference was not significant. This study provides the first evidence of the influence of the immune microenvironment on the osteogenic properties of the induced membranes.https://www.mdpi.com/2227-9059/10/12/3017Masquelet-induced membranemacrophagesPMMAmetakaolin
spellingShingle Marjorie Durand
Myriam Oger
Krisztina Nikovics
Julien Venant
Anne-Cecile Guillope
Eugénie Jouve
Laure Barbier
Laurent Bégot
Florence Poirier
Catherine Rousseau
Olivier Pitois
Laurent Mathieu
Anne-Laure Favier
Didier Lutomski
Jean-Marc Collombet
Influence of the Immune Microenvironment Provided by Implanted Biomaterials on the Biological Properties of Masquelet-Induced Membranes in Rats: Metakaolin as an Alternative Spacer
Biomedicines
Masquelet-induced membrane
macrophages
PMMA
metakaolin
title Influence of the Immune Microenvironment Provided by Implanted Biomaterials on the Biological Properties of Masquelet-Induced Membranes in Rats: Metakaolin as an Alternative Spacer
title_full Influence of the Immune Microenvironment Provided by Implanted Biomaterials on the Biological Properties of Masquelet-Induced Membranes in Rats: Metakaolin as an Alternative Spacer
title_fullStr Influence of the Immune Microenvironment Provided by Implanted Biomaterials on the Biological Properties of Masquelet-Induced Membranes in Rats: Metakaolin as an Alternative Spacer
title_full_unstemmed Influence of the Immune Microenvironment Provided by Implanted Biomaterials on the Biological Properties of Masquelet-Induced Membranes in Rats: Metakaolin as an Alternative Spacer
title_short Influence of the Immune Microenvironment Provided by Implanted Biomaterials on the Biological Properties of Masquelet-Induced Membranes in Rats: Metakaolin as an Alternative Spacer
title_sort influence of the immune microenvironment provided by implanted biomaterials on the biological properties of masquelet induced membranes in rats metakaolin as an alternative spacer
topic Masquelet-induced membrane
macrophages
PMMA
metakaolin
url https://www.mdpi.com/2227-9059/10/12/3017
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