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Fibroblast inflammatory priming determines regenerative versus fibrotic skin repair in reindeer. 2022
Sarthak Sinha, and
Holly D Sparks, and
Elodie Labit, and
Hayley N Robbins, and
Kevin Gowing, and
Arzina Jaffer, and
Eren Kutluberk, and
Rohit Arora, and
Micha Sam Brickman Raredon, and
Leslie Cao, and
Scott Swanson, and
Peng Jiang, and
Olivia Hee, and
Hannah Pope, and
Matt Workentine, and
Kiran Todkar, and
Nilesh Sharma, and
Shyla Bharadia, and
Keerthana Chockalingam, and
Luiz G N de Almeida, and
Mike Adam, and
Laura Niklason, and
S Steven Potter, and
Ashley W Seifert, and
Antoine Dufour, and
Vincent Gabriel, and
Nicole L Rosin, and
Ron Stewart, and
Greg Muench, and
Robert McCorkell, and
John Matyas, and
Jeff Biernaskie
Faculty of Veterinary Medicine, University of Calgary, Calgary, AB, Canada.
Adult mammalian skin wounds heal by forming fibrotic scars. We report that full-thickness injuries of reindeer antler skin (velvet) regenerate, whereas back skin forms fibrotic scar. Single-cell multi-omics reveal that uninjured velvet fibroblasts resemble human fetal fibroblasts, whereas back skin fibroblasts express inflammatory mediators mimicking pro-fibrotic adult human and rodent fibroblasts. Consequently, injury elicits site-specific immune responses: back skin fibroblasts amplify myeloid infiltration and maturation during repair, whereas velvet fibroblasts adopt an immunosuppressive phenotype that restricts leukocyte recruitment and hastens immune resolution. Ectopic transplantation of velvet to scar-forming back skin is initially regenerative, but progressively transitions to a fibrotic phenotype akin to the scarless fetal-to-scar-forming transition reported in humans. Skin regeneration is diminished by intensifying, or enhanced by neutralizing, these pathologic fibroblast-immune interactions. Reindeer represent a powerful comparative model for interrogating divergent wound healing outcomes, and our results nominate decoupling of fibroblast-immune interactions as a promising approach to mitigate scar.
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