Pivotal role for skin trans-endothelial radio-resistant anti-inflammatory macrophages in tissue repair

  1. Olga Barreiro
  2. Danay Cibrian
  3. Cristina Clemente
  4. David Alvarez
  5. Vanessa Moreno
  6. Inigo Valiente
  7. Antonio Bernad
  8. Dietmar Vestweber
  9. Alicia G Arroyo
  10. Pilar Martín
  11. Ulrich von Andrian
  12. Francisco Sánchez Madrid  Is a corresponding author
  1. Harvard Medical School, United States
  2. Centro Nacional de Investigaciones Cardiovasculares, Spain
  3. Max Planck Institute of Molecular Biomedicine, Germany

Abstract

Heterogeneity and functional specialization among skin-resident macrophages are incompletely understood. In this study, we describe a novel subset of murine dermal perivascular macrophages that extend protrusions across the endothelial junctions in steady-state and capture blood-borne macromolecules. Unlike other skin-resident macrophages that are reconstituted by bone marrow-derived progenitors after a genotoxic insult, these cells are replenished by an extramedullary radio-resistant and UV-sensitive Bmi1+ progenitor. Furthermore, they possess a distinctive anti-inflammatory transcriptional profile, which cannot be polarized under inflammatory conditions, and are involved in repair and remodeling functions for which other skin-resident macrophages appear dispensable. Based on all their properties, we define these macrophages as Skin Transendothelial Radio-resistant Anti-inflammatory Macrophages (STREAM) and postulate that their preservation is important for skin homeostasis.

Article and author information

Author details

  1. Olga Barreiro

    Department of Microbiology and Immunobiology, Harvard Medical School, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Danay Cibrian

    Department of Vascular Biology and Inflammation, Centro Nacional de Investigaciones Cardiovasculares, Madrid, Spain
    Competing interests
    The authors declare that no competing interests exist.
  3. Cristina Clemente

    Department of Vascular Biology and Inflammation, Centro Nacional de Investigaciones Cardiovasculares, Madrid, Spain
    Competing interests
    The authors declare that no competing interests exist.
  4. David Alvarez

    Department of Microbiology and Immunobiology, Harvard Medical School, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Vanessa Moreno

    Department of Vascular Biology and Inflammation, Centro Nacional de Investigaciones Cardiovasculares, Madrid, Spain
    Competing interests
    The authors declare that no competing interests exist.
  6. Inigo Valiente

    Department of Cardiovascular Development and Repair, Centro Nacional de Investigaciones Cardiovasculares, Madrid, Spain
    Competing interests
    The authors declare that no competing interests exist.
  7. Antonio Bernad

    Department of Cardiovascular Development and Repair, Centro Nacional de Investigaciones Cardiovasculares, Madrid, Spain
    Competing interests
    The authors declare that no competing interests exist.
  8. Dietmar Vestweber

    Max Planck Institute of Molecular Biomedicine, Münster, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Alicia G Arroyo

    Department of Vascular Biology and Inflammation, Centro Nacional de Investigaciones Cardiovasculares, Madrid, Spain
    Competing interests
    The authors declare that no competing interests exist.
  10. Pilar Martín

    Department of Vascular Biology and Inflammation, Centro Nacional de Investigaciones Cardiovasculares, Madrid, Spain
    Competing interests
    The authors declare that no competing interests exist.
  11. Ulrich von Andrian

    Department of Microbiology and Immunobiology, Harvard Medical School, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  12. Francisco Sánchez Madrid

    Department of Vascular Biology and Inflammation, Centro Nacional de Investigaciones Cardiovasculares, Madrid, Spain
    For correspondence
    fsmadrid@salud.madrid.org
    Competing interests
    The authors declare that no competing interests exist.

Ethics

Animal experimentation: Animal studies were approved by the local ethics committee and by the Division of Animal Protection of Comunidad de Madrid (approved protocols PROEX 159/15 and 160/15). All animal procedures conformed to EU Directive 2010/63EU and Recommendation 2007/526/EC regarding the protection of animals used for experimental and other scientific purposes, enforced in Spanish law under Real Decreto 1201/2005

Copyright

© 2016, Barreiro et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Olga Barreiro
  2. Danay Cibrian
  3. Cristina Clemente
  4. David Alvarez
  5. Vanessa Moreno
  6. Inigo Valiente
  7. Antonio Bernad
  8. Dietmar Vestweber
  9. Alicia G Arroyo
  10. Pilar Martín
  11. Ulrich von Andrian
  12. Francisco Sánchez Madrid
(2016)
Pivotal role for skin trans-endothelial radio-resistant anti-inflammatory macrophages in tissue repair
eLife 5:e15251.
https://doi.org/10.7554/eLife.15251

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https://doi.org/10.7554/eLife.15251

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