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While several UVR-induced changes, including extracellular matrix reorganisation and epidermal DNA damage, have been documented, the role of different fibroblast lineages and their communication with immune cells has not been explored. We show that acute and chronic UVR exposure led to selective loss of fibroblasts from the upper dermis in human and mouse skin. Lineage tracing and in vivo live imaging revealed that repair following acute UVR is predominantly mediated by papillary fibroblast proliferation and fibroblast reorganisation occurs with minimal migration. In contrast, chronic UVR exposure led to a permanent loss of papillary fibroblasts, with expansion of fibroblast membrane protrusions partially compensating for the reduction in cell number. Although UVR strongly activated Wnt signalling in skin, stimulation of fibroblast proliferation by epidermal \u03b2-catenin stabilisation did not enhance papillary dermis repair. Acute UVR triggered an infiltrate of neutrophils and T cell subpopulations and increased pro-inflammatory prostaglandin signalling in skin. Depletion of CD4- and CD8-positive cells resulted in increased papillary fibroblast depletion, which correlated with an increase in DNA damage, pro-inflammatory prostaglandins, and reduction in fibroblast proliferation. Conversely, topical COX-2 inhibition prevented fibroblast depletion and neutrophil infiltration after UVR. We conclude that loss of papillary fibroblasts is primarily induced by a deregulated inflammatory response, with infiltrating T cells supporting fibroblast survival upon UVR-induced environmental stress.<\/jats:p>","DOI":"10.7554\/elife.71052","type":"journal-article","created":{"date-parts":[[2021,12,23]],"date-time":"2021-12-23T07:15:19Z","timestamp":1640243719000},"update-policy":"https:\/\/doi.org\/10.7554\/elife.71052","source":"Crossref","is-referenced-by-count":42,"title":["Role of distinct fibroblast lineages and immune cells in dermal repair following UV radiation-induced tissue damage"],"prefix":"10.7554","volume":"10","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6050-2860","authenticated-orcid":true,"given":"Emanuel","family":"Rognoni","sequence":"first","affiliation":[{"name":"Centre for Stem Cells and Regenerative Medicine, King's College London, Guy's Hospital","place":["London, United Kingdom"]},{"name":"Centre for Endocrinology, William Harvey Research Institute, 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