Distinct fibroblast lineages determine dermal architecture in skin development and repair
Open accessAbstract
Fibroblasts are the major mesenchymal cell type in connective tissue and deposit the collagen and elastic fibres of the extracellular matrix (ECM). Even within a single tissue, fibroblasts exhibit considerable functional diversity, but it is not known whether this reflects the existence of a differentiation hierarchy or is a response to different environmental factors. Here we show, using transplantation assays and lineage tracing in mice, that the fibroblasts of skin connective tissue arise from two distinct lineages. One forms the upper dermis, including the dermal papilla that regulates hair growth and the arrector pili muscle, which controls piloerection. The other forms the lower dermis, including the reticular fibroblasts that synthesize the bulk of the fibrillar ECM, and the preadipocytes and adipocytes of the hypodermis. The upper lineage is required for hair follicle formation. In wounded adult skin, the initial wave of dermal repair is mediated by the lower lineage and upper dermal fibroblasts are recruited only during re-epithelialization. Epidermal β-catenin activation stimulates the expansion of the upper dermal lineage, rendering wounds permissive for hair follicle formation. Our findings explain why wounding is linked to formation of ECM-rich scar tissue that lacks hair follicles. They also form a platform for discovering fibroblast lineages in other tissues and for examining fibroblast changes in ageing and disease.
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The ITGα8+ αSMA+ muscle-like structures could indicate arrector pili muscle induction.
“Restricting analysis to HFs with normal morphology, we identified ITGα8+ αSMA+ muscle-like structures with elongated nuclei in the organoid dermis (Figure 5C, C′), which could indicate arrector pili muscle induction (Driskell et al., 2013).”
From Hair Follicle Development in Mouse Pluripotent Stem Cell-Derived Skin Organoids (2018) · cites this paper as Driskell et al., 2013
The Abstract (page unavailable) identifies the arrector pili muscle (APM) as a structure formed by the upper dermal fibroblast lineage, supporting the possibility of APM formation. The Methods > Antibodies section lists Itga8 and alpha-smooth muscle actin antibodies, but the passages do not establish that ITGα8+ αSMA+ elongated structures identify APM or demonstrate its induction in organoids. (LLM, conf=0.82)
Experimental — accuracy not yet measuredLipid-rich adipocytes developed around organoid HFs, mimicking the development of hypodermal fat.
“Additionally, lipid-rich adipocytes developed around organoid HFs, mimicking the development of hypodermal fat (Fig. 3b, c, Extended Data Fig. 9)14.”
From Hair-bearing human skin generated entirely from pluripotent stem cells (2020) · cites this paper as [14]
The dermal cell diversity is consistent with late embryonic and early postnatal dermal development.
“Interestingly, by day 16, CD34+ cells were present throughout the dermal layer, while DLK1+ cells were localized to discrete regions, suggesting that a diverse population of dermal cells may emerge in skin organoids (Figure 3F, G), consistent with late embryonic and early postnatal dermal development (Driskell et al., 2013).”
From Hair Follicle Development in Mouse Pluripotent Stem Cell-Derived Skin Organoids (2018) · cites this paper as Driskell et al., 2013
Dermal fibroblasts have two embryonic origins: mesoderm cells (body and scalp skin) and cranial neural crest cells (CNCC; facial skin).
“Dermal fibroblasts have two embryonic origins: mesoderm cells (body and scalp skin) and cranial neural crest cells (CNCC; facial skin)13,14.”
From Hair-bearing human skin generated entirely from pluripotent stem cells (2020) · cites this paper as [14]
The paper’s Abstract describes two dermal fibroblast lineages that form the upper and lower dermis, not two embryonic origins. Searches for mesoderm, cranial neural crest, and the claimed body/scalp versus facial-skin distinction found no passage addressing those origins. (LLM, conf=0.75)
Experimental — accuracy not yet measuredTwo studies demonstrated mesenchymal progenitor hierarchy, diversity in the pathophysiological roles of their progeny, and context-dependent fate determination.
“two studies, focussing on populations of hypermethylated in cancer protein (Hic1)+Pdgfrα+ lymphocyte antigen 6 complex (LY6A)+ MP populations in heart and skeletal muscle, have elegantly demonstrated MP hierarchy, diversity in the pathophysiological roles of their progeny, and how fate determination of MP is context dependent31,32.”
From Fibrosis: from mechanisms to medicines (2020) · cites this paper as [32]
In the heart, Hic1 deficiency in Pdgfrα-expressing cells leads to activation of mesenchymal progenitors and accumulation of cardiac fibroadipogenic progenitor cells, with epicardial thickening, interstitial fibrosis, and fibrofatty depositions that are major pathological features of arrhythmogenic cardiomyopathy.
“In the heart, Hic1 deficiency (in Pdgfrα-expressing cells) led to activation of MPs and accumulation of cardiac fibroadipogenic progenitor cells, with epicardial thickening, interstitial fibrosis and fibrofatty depositions resulting in major pathological features pathognomonic in arrhythmogenic cardiomyopathy32.”
From Fibrosis: from mechanisms to medicines (2020) · cites this paper as [32]
Conditional genetic inactivation of Hic1 in mice leads to activation and expansion of mesenchymal progenitors in both heart and skeletal muscle, demonstrating that Hic1 is required for maintaining mesenchymal progenitor quiescence.
“Conditional genetic inactivation of Hic1 in mice led to activation and expansion of MPs in both heart and skeletal muscle, demonstrating that Hic1 is required for maintaining MP quiescence.”
From Fibrosis: from mechanisms to medicines (2020) · cites this paper as [32]
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Xu, M., Su, X., Xiao, X., Yu, H., Li, X., Keating, A., Wang, S., & Zhao, R. C. (2021) · Aging and disease · doi:10.14336/ad.2020.0624 · Cited by 50 · see citing works
Logan, N. J., Camman, M., Williams, G., & Higgins, C. A. (2018) · Bone · doi:10.1016/j.bone.2018.09.008 · Cited by 21 · see citing works
- Authors
- Driskell, R. R., Lichtenberger, B. M., Hoste, E., Kretzschmar, K., Simons, B. D., Charalambous, M., Ferron, S. R., Herault, Y., Pavlovic, G., Ferguson-Smith, A. C., & Watt, F. M.
- Affiliations
- Guy's Hospital (GB)
- University of Cambridge (GB)
- Phénotypage et ingénierie précliniques des systèmes d’organismes modèles (FR)
- Corresponding author
- Watt, Fiona M.
- ORCID
- Venue
- Nature
- Published
- 2013-12
- Volume
- 504
- Issue
- 7479
- Pages
- 277-281
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC3868929
- OpenAlex
- W2146749615
- Cited by
- 1,291
- References
- 30
- Citations by year
- 2026: 88 · 2025: 96 · 2024: 130 · 2023: 123 · 2022: 136 · 2021: 156 · 2020: 117 · 2019: 101 · 2018: 97 · 2017: 71 · 2016: 77 · 2015: 53 · 2014: 45
- FWCI
- 70.86
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- HAL (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Ghent University Academic Bibliography (Ghent University) (submittedVersion)
- Research Portal (King's College London) (submittedVersion, other-oa)
- Queen Mary Research Online (Queen Mary University of London) (submittedVersion)
- Funders
- Wellcome Trust (079249, 095606, 098357/Z/12/Z, 096540, 98357, 095606/Z/11/Z, 098357, 092096)
- King's College Hospital NHS Foundation Trust
- National Institute for Health and Care Research
- King's College London
- European Commission
- Agence Nationale de la Recherche (ANR-10-INBS-0007)
- Medical Research Council (MR/J001597/1)
- Topics
- Health Sciences › Medicine › Urology › Hair Growth and Disorders
- Health Sciences › Medicine › Rehabilitation › Wound Healing and Treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Skin and Cellular Biology Research
- Keywords
- dermal fibroblasts, fibroblast lineage, dermis, skin development, skin wound healing, hair follicle formation, dermal papilla, arrector pili muscle, reticular fibroblasts, preadipocytes, adipocytes, subcutaneous tissue, smooth muscle cells, extracellular matrix, β-catenin, re-epithelialization
- MeSH terms
- Animals, Female, Fibroblasts, Male, Mice, Inbred CBA, Mice, Inbred C57BL, Mice, Transgenic, Muscle, Smooth, Skin, Wound Healing, Adipocytes, Hair Follicle, Cell Lineage, Dermis, beta Catenin, Mice, In Vitro Techniques
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