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Cited by 14Immune cells in cancerWound Healing and TreatmentsMacrophage Migration Inhibitory Factor

Epithelial-Macrophage Crosstalk Initiates Sterile Inflammation in Embryonic Skin

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Bhattacharjee, Oindrila, Ayyangar, Uttkarsh, Kurbet, Ambika S., Lakshmanan, Vairavan, Palakodeti, Dasaradhi, Ginhoux, Florent, Raghavan, Srikala·2021·Frontiers in Immunology
DOI 10.3389/fimmu.2021.718005PMC PMC8553113
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Abstract

Macrophages are highly responsive to the environmental cues and are the primary responders to tissue stress and damage. While much is known about the role of macrophages during inflammatory disease progression; the initial series of events that set up the inflammation remains less understood. In this study, we use next generation sequencing (NGS) of embryonic skin macrophages and the niche cells - skin epithelia and stroma in the epidermis specific knockout of integrin beta 1 (Itgβ1) model to uncover specific roles of each cell type and identify how these cell types communicate to initiate the sterile inflammatory response. We demonstrate that while the embryonic skin fibroblasts in the Itgβ1 knockout skin are relatively inactive, the keratinocytes and macrophages are the critical responders to the sterile inflammatory cues. The epidermis expresses damage associated molecular patterns (DAMPs), stress response genes, pro-inflammatory cytokines, and chemokines that aid in eliciting the inflammatory response. The macrophages, in-turn, respond by acquiring enhanced M2-like characteristics expressing ECM remodeling and matrisome signatures that exacerbate the basement membrane disruption. Depletion of macrophages by blocking the CSF1 receptor (CSF1R) results in improved basement membrane integrity and reduced ECM remodeling activity in the KO skin. Further, blocking the skin inflammation with celecoxib reveals that the acquired fate of macrophages in the KO skin is dependent on its interaction with the epidermal compartment through COX2 dependent cytokine production. Taken together, our study highlights a critical crosstalk between the epithelia and the dermal macrophages that shapes macrophage fate and initiates sterile inflammation in the skin. The insights gained from our study can be extrapolated to other inflammatory disorders to understand the early events that set up the disease.

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Authors
Bhattacharjee, O., Ayyangar, U., Kurbet, A. S., Lakshmanan, V., Palakodeti, D., Ginhoux, F., & Raghavan, S.
Affiliations
  • Institute for Stem Cell Biology and Regenerative Medicine (IN)
  • Agency for Science, Technology and Research (SG)
Corresponding author
Raghavan, Srikala
ORCID
Venue
Frontiers in Immunology
Publisher
Frontiers Media SA
Published
2021-10-14
Volume
12
Pages
718005-718005
ISSN
1664-3224 (ISSN-L)
DOI
10.3389/fimmu.2021.718005
PMC
PMC8553113
OpenAlex
W3205682797
Cited by
14
References
76
Citations by year
2026: 2 · 2025: 4 · 2024: 3 · 2023: 1 · 2022: 4
FWCI
0.75
Type
journal article
Language
en
Open access
Licence
Locations
  • Frontiers in Immunology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, other-oa)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
Department of Biotechnology, Ministry of Science and Technology, India (BT/PR31418/BRB/10/1758/2019)
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
  • Health Sciences › Medicine › Rehabilitation › Wound Healing and Treatments
  • Life Sciences › Immunology and Microbiology › Immunology › Macrophage Migration Inhibitory Factor
Keywords
sterile inflammation, embryonic skin, beta1 integrin, keratinocytes, dermal macrophages, damage-associated molecular patterns, M2 macrophage polarization, basement membrane disruption, extracellular matrix remodeling, CSF1R, celecoxib, cyclooxygenase-2, inflammatory cytokines, epidermis
MeSH terms
Animals, Dermatitis, Disease Susceptibility, Epidermis, Epithelium, Extracellular Matrix, Female, Fetus, Flow Cytometry, Fluorescent Antibody Technique, Immunohistochemistry, Macrophages, Male, Models, Biological, Biomarkers, Mice, Knockout, Mice

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