Newly defined ABCB5+ dermal mesenchymal stem cells promote healing of chronic iron overload wounds via secretion of interleukin-1 receptor antagonist

Here we report the beneficial effects of a newly identified dermal cell subpopulation expressing the ATP-binding cassette subfamily B member 5 (ABCB5) for the therapy of non-healing wounds. Local administration of dermal ABCB5 + -derived MSCs attenuated macrophage-dominated inflammation and thereby...

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Published inStem cells (Dayton, Ohio) Vol. 37; no. 8; pp. 1057 - 1074
Main Authors BEKEN, SEPPE VANDER, DE VRIES, JULIANE C., MEIER-SCHIESSER, BARBARA, MEYER, PATRICK, JIANG, DONGSHENG, SINDRILARU, ANCA, FERREIRA, FILIPA F., HAINZL, ADELHEID, SCHATZ, SUSANNE, MUSCHHAMMER, JANA, SCHEURMANN, NATALIE J., KAMPILAFKOS, PANAGIOTIS, SEITZ, ANDREAS M., DÜRSELEN, LUTZ, IGNATIUS, ANITA, KLUTH, MARK A., GANSS, CHRISTOPH, WLASCHEK, MEINHARD, SINGH, KARMVEER, MAITY, PALLAB, FRANK, NATASHA Y., FRANK, MARKUS H., SCHARFFETTER-KOCHANEK, KARIN
Format Journal Article
LanguageEnglish
Published 13.05.2019
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Abstract Here we report the beneficial effects of a newly identified dermal cell subpopulation expressing the ATP-binding cassette subfamily B member 5 (ABCB5) for the therapy of non-healing wounds. Local administration of dermal ABCB5 + -derived MSCs attenuated macrophage-dominated inflammation and thereby accelerated healing of full-thickness excisional wounds in the iron overload mouse model mimicking the non-healing state of human venous leg ulcers. The observed beneficial effects were due to interleukin-1 receptor antagonist (IL-1RA) secreted by ABCB5 + -derived MSCs, which dampened inflammation and shifted the prevalence of unrestrained pro-inflammatory M1 macrophages toward repair promoting anti-inflammatory M2 macrophages at the wound site. The beneficial anti-inflammatory effect of IL-1RA released from ABCB5 + -derived MSCs on human wound macrophages was conserved in humanized NOD- scid IL2rγ null mice. In conclusion, human dermal ABCB5 + cells represent a novel, easy accessible and marker-enriched source of MSCs which holds substantial promise to successfully treat chronic non-healing wounds in humans. In chronic wounds, M1 macrophages and their autocrine amplification of inflammasome-generated IL-1β perpetuates a pro-inflammatory environment impeding the progression through normal phases of wound healing. IL-1RA adaptively secreted by ABCB5 + MSCs when exposed to the M1 macrophage imprinted pro-inflammatory wound environment, attenuates this vicious cycle and leads to a shift from pro-inflammatory M1 toward anti-inflammatory, wound healing-promoting M2 macrophages as observed in normal wound healing.
AbstractList Here we report the beneficial effects of a newly identified dermal cell subpopulation expressing the ATP-binding cassette subfamily B member 5 (ABCB5) for the therapy of non-healing wounds. Local administration of dermal ABCB5 + -derived MSCs attenuated macrophage-dominated inflammation and thereby accelerated healing of full-thickness excisional wounds in the iron overload mouse model mimicking the non-healing state of human venous leg ulcers. The observed beneficial effects were due to interleukin-1 receptor antagonist (IL-1RA) secreted by ABCB5 + -derived MSCs, which dampened inflammation and shifted the prevalence of unrestrained pro-inflammatory M1 macrophages toward repair promoting anti-inflammatory M2 macrophages at the wound site. The beneficial anti-inflammatory effect of IL-1RA released from ABCB5 + -derived MSCs on human wound macrophages was conserved in humanized NOD- scid IL2rγ null mice. In conclusion, human dermal ABCB5 + cells represent a novel, easy accessible and marker-enriched source of MSCs which holds substantial promise to successfully treat chronic non-healing wounds in humans. In chronic wounds, M1 macrophages and their autocrine amplification of inflammasome-generated IL-1β perpetuates a pro-inflammatory environment impeding the progression through normal phases of wound healing. IL-1RA adaptively secreted by ABCB5 + MSCs when exposed to the M1 macrophage imprinted pro-inflammatory wound environment, attenuates this vicious cycle and leads to a shift from pro-inflammatory M1 toward anti-inflammatory, wound healing-promoting M2 macrophages as observed in normal wound healing.
Author DE VRIES, JULIANE C.
SCHEURMANN, NATALIE J.
WLASCHEK, MEINHARD
IGNATIUS, ANITA
SEITZ, ANDREAS M.
SINDRILARU, ANCA
FERREIRA, FILIPA F.
SINGH, KARMVEER
FRANK, NATASHA Y.
FRANK, MARKUS H.
KLUTH, MARK A.
BEKEN, SEPPE VANDER
SCHARFFETTER-KOCHANEK, KARIN
JIANG, DONGSHENG
DÜRSELEN, LUTZ
KAMPILAFKOS, PANAGIOTIS
MAITY, PALLAB
HAINZL, ADELHEID
MEIER-SCHIESSER, BARBARA
GANSS, CHRISTOPH
SCHATZ, SUSANNE
MUSCHHAMMER, JANA
MEYER, PATRICK
AuthorAffiliation b Institute of Orthopaedic Research and Biomechanics, University of Ulm, Ulm, Germany
a Department of Dermatology and Allergic Diseases, University of Ulm, Ulm, Germany
d RHEACELL GmbH & Co. KG, Heidelberg, Germany
e Transplantation Research Center, Boston Children’s Hospital and Brigham and Women’s Hospital, Boston, Massachusetts, USA
f Department of Medicine, Boston VA Healthcare System, West Roxbury, Massachusetts, USA
g Division of Genetics, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, USA
h Harvard Skin Disease Research Center, Department of Dermatology, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts, USA
c TICEBA GmbH, Heidelberg, Germany
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  organization: Department of Dermatology and Allergic Diseases, University of Ulm, Ulm, Germany Institute of Orthopaedic Research and Biomechanics, University of Ulm, Ulm, Germany TICEBA GmbH, Heidelberg, Germany RHEACELL GmbH & Co. KG, Heidelberg, Germany Transplantation Research Center, Boston Children’s Hospital and Brigham and Women’s Hospital, Boston, Massachusetts, USA Department of Medicine, Boston VA Healthcare System, West Roxbury, Massachusetts, USA Division of Genetics, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, USA Harvard Skin Disease Research Center, Department of Dermatology, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts, USA
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  organization: Department of Dermatology and Allergic Diseases, University of Ulm, Ulm, Germany Institute of Orthopaedic Research and Biomechanics, University of Ulm, Ulm, Germany TICEBA GmbH, Heidelberg, Germany RHEACELL GmbH & Co. KG, Heidelberg, Germany Transplantation Research Center, Boston Children’s Hospital and Brigham and Women’s Hospital, Boston, Massachusetts, USA Department of Medicine, Boston VA Healthcare System, West Roxbury, Massachusetts, USA Division of Genetics, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, USA Harvard Skin Disease Research Center, Department of Dermatology, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts, USA
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Notes Current address: Department of Dermatology, University Hospital Zürich, Zürich, Switzerland.
S.V.B., J.C.V., B.M., D.J., P.Me., M.A.K., S.S., A.H., K.S., P.M. and A.M.S. acquired and analyzed data. K.S.-K., S.V.B., J.C.V., M.W., M.H.F., N.Y.F., B.M., D.J., P.Me. A.S., A.I. and L.D. designed the research concept and set up experiments.
Current address: Bredent medical GmbH & Co.KG, Senden, Germany.
Author Contribution
M.A.K., C.G. and P.K. isolated and provided ABCB5+ and ABCB5− cell fractions. M.H.F., N.Y.F and C.G. provided anti-ABCB5 monoclonal antibody. L.D., A.I. and A.M.S. provided critical conceptual, administrative and technical support for the scar tissue breaking strength analysis. Excellent technical assistance was provided by A.H., S.S., J.M., F.F.F. and N.J.S. General administrative support and supervision was given by K.S.-K., M.W., S.V.B., D.J. and A.S. The manuscript was written and revised by K.S.-K., S.V.B., and M.H.F with critical inputs and edits by co-authors.
PMID 31002437
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  year: 2019
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PublicationTitle Stem cells (Dayton, Ohio)
PublicationYear 2019
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Snippet Here we report the beneficial effects of a newly identified dermal cell subpopulation expressing the ATP-binding cassette subfamily B member 5 (ABCB5) for the...
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StartPage 1057
Title Newly defined ABCB5+ dermal mesenchymal stem cells promote healing of chronic iron overload wounds via secretion of interleukin-1 receptor antagonist
URI https://pubmed.ncbi.nlm.nih.gov/PMC6663647
Volume 37
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