A prenatal skin atlas reveals immune regulation of human skin morphogenesis
Open accessAbstract
. The SkO model closely recapitulated in vivo skin epidermal and dermal cell types during hair follicle development and expression of genes implicated in the pathogenesis of genetic hair and skin disorders. However, the SkO model lacked immune cells and had markedly reduced endothelial cell heterogeneity and quantity. Our in vivo prenatal skin cell atlas indicated that macrophages and macrophage-derived growth factors have a role in driving endothelial development. Indeed, vascular network remodelling was enhanced following transfer of autologous macrophages derived from induced pluripotent stem cells into SkO cultures. Innate immune cells are therefore key players in skin morphogenesis beyond their conventional role in immunity, a function they achieve through crosstalk with non-immune cells.
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The dataset, collected by Jin et al., consists of scratch assays performed on PC-3 prostate cancer cells with varying initial confluence prior to the scratch.
“The dataset, collected by Jin et al.,8 consists of scratch assays performed on PC-3 prostate cancer cells with varying initial confluence prior to the scratch.”
From Inference of weak-form partial differential equations describing migration and proliferation mechanisms in wound healing experiments on cancer cells (2025) · cites this paper as [8]
The Methods section, “Scratch wound assay of fibroblasts in co-culture with macrophages” (page unavailable), describes assays using skin-organoid-derived fibroblasts and macrophages, not PC-3 prostate cancer cells. It specifies a 5:1 seeding ratio and does not describe varying initial confluence. (LLM, conf=0.89)
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measuredBy estimating parameters for these models, past work has helped identify quantitative effects of biological perturbations in scratch assays.
“By estimating parameters for these models, past work has helped identify quantitative effects of biological perturbations in scratch assays8,10,11.”
From Inference of weak-form partial differential equations describing migration and proliferation mechanisms in wound healing experiments on cancer cells (2025) · cites this paper as [8]
The ‘Scarless healing and potential macrophage contribution’ section reports that macrophage co-culture improved scratch wound-width closure over 72 hours, supporting a measured effect of a biological perturbation. The Methods section says the scratch images were analysed with an ImageJ macro and two-way ANOVA; it does not describe estimating parameters of a scratch-assay model to identify that effect. Page numbers are unavailable in our copy. (LLM, conf=0.85)
Experimental — accuracy not yet measuredVascular-immune interactions were primarily inferred from histological proximity, flow cytometry and gene-expression patterns.
“Moreover, vascular-immune interactions were primarily inferred from histological proximity, flow cytometry and gene-expression patterns; spatial transcriptomics and single-cell multiomics approaches will be valuable for elucidating cell-type-specific crosstalk at single-cell resolution 54,55 .”
From Vascularized human skin assembloids model compartmental skin organization and immune responsiveness in vitro (2026) · cites this paper as [55]
In “Macrophages support prenatal skin angiogenesis” (page unavailable), the paper uses staining to show macrophages near endothelial cells and gene-expression analyses to predict interactions. But it also reports spatial transcriptomic analysis and co-culture angiogenesis experiments; the Methods describe flow cytometry as phenotyping macrophages before co-culture, not as the primary basis for inferring vascular–immune interactions. The claim therefore omits important evidence and mischaracterizes flow cytometry’s role. (LLM, conf=0.86)
Experimental — accuracy not yet measuredhiPSC-derived skin organoids have hair follicles, pigmentation, dermal stratification, appendage patterning, and innervation.
“Recent advances in human induced pluripotent stem cell (hiPSC) technology have enabled the generation of skin organoids (SKO) with hair follicles, pigmentation, dermal stratification, appendage patterning, and innervation.[ 25 , 26 , 28 , 29 , 30 , 31 , 32 , 33 , 34 , 35 ]”
From Coordinated Development of Immune Cell Populations in Vascularized Skin Organoids from Human Induced Pluripotent Stem Cells (2025) · cites this paper as [35]
The Single-cell atlas of human prenatal skin section (page not supplied) says the stem-cell-derived skin organoid model recapitulates prenatal hair-follicle components, neural cells and dermal fibroblasts, and contains melanocytes. The paper does not establish pigmentation, dermal stratification, appendage patterning or innervation as organoid features; neural cells and melanocytes alone do not demonstrate innervation or pigmentation. (LLM, conf=0.86)
Experimental — accuracy not yet measuredPrevious human SKO models were devoid of vascularization and immune cells.
“Previous human SKO models were devoid of vascularization and immune cells.[ 25 , 26 , 28 , 29 , 30 , 31 , 32 , 33 , 34 , 35 , 36 , 37 , 38 , 59 ]”
From Coordinated Development of Immune Cell Populations in Vascularized Skin Organoids from Human Induced Pluripotent Stem Cells (2025) · cites this paper as [35]
The Single-cell atlas of human prenatal skin section says the SkO model lacked immune cells, supporting that part of the claim. It says endothelial cells were markedly reduced, not absent; the Macrophages support prenatal skin angiogenesis section also describes SkO endothelial cells. The source therefore does not support saying these models were devoid of vascularization. (LLM, conf=0.91)
Experimental — accuracy not yet measured
Although macrophage co-culture with SKOs has been reported, a physiologically relevant vascularized hiPSC-derived SKO has yet to be achieved.
“Although macrophage co‐culture with SKOs has been reported,[ 35 ] a physiologically relevant vascularized hiPSC‐derived SKO has yet to be achieved.[ 36 , 37 , 38 ]”
From Coordinated Development of Immune Cell Populations in Vascularized Skin Organoids from Human Induced Pluripotent Stem Cells (2025) · cites this paper as [35]
Currently, SKOs lack vasculature and immune cells in a physiologically relevant context.
“Currently, SKOs lack vasculature and immune cells in a physiologically relevant context.[ 25 , 35 , 36 , 37 , 38 ]”
From Coordinated Development of Immune Cell Populations in Vascularized Skin Organoids from Human Induced Pluripotent Stem Cells (2025) · cites this paper as [35]
First-principles modeling has established a variety of PDE models that accurately represent the behavior of scratch assays with a high density of cells and under a variety of conditions.
“First-principles modeling has established a variety of partial differential equation (PDE) models that accurately represent the behavior of scratch assays with a high density of cells and under a variety of conditions8,9.”
From Inference of weak-form partial differential equations describing migration and proliferation mechanisms in wound healing experiments on cancer cells (2025) · cites this paper as [8]
The Methods section describes a fibroblast–macrophage scratch assay and its image-based analysis, but does not discuss PDE models of scratch assays. Searches for first-principles PDE modeling and cell-density-dependent scratch-assay models found no passage addressing the claimed modeling results. (LLM, conf=0.76)
Experimental — accuracy not yet measuredThere exist models that have considered density-dependent effects on migration and on cell proliferation.
“There exist models that have considered density-dependent effects on migration, for instance representing cells interacting with each other, and on cell proliferation, for instance, modeling its saturation at high cell density8,27.”
From Inference of weak-form partial differential equations describing migration and proliferation mechanisms in wound healing experiments on cancer cells (2025) · cites this paper as [8]
The Methods sections on spatial data analysis and trajectory analysis describe models for estimating cell abundance and cell-state transitions, not models of density-dependent migration or proliferation. Searches for high-density proliferation saturation and density-dependent migration found no passage addressing either point in our copy. (LLM, conf=0.75)
Experimental — accuracy not yet measuredVariational System Identification rapidly identified an accurate model describing the evolution of cell concentration over time for a variety of initial seeding densities, with accuracy that matched or improved upon results in the literature.
“With it, we were able to rapidly identify an accurate model describing the evolution of cell concentration over time for a variety of initial seeding densities with accuracy that matched or improved upon results in the literature8.”
From Inference of weak-form partial differential equations describing migration and proliferation mechanisms in wound healing experiments on cancer cells (2025) · cites this paper as [8]
Split into 2 atoms — 0 confirmed, 0 partially supported, 0 disputed, 0 misattributed, 2 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredThe cell densities achieved in our MDA-MB-231 scratch assays are comparable to those observed by Jin et al. and admit treatment using continuum advection-diffusion-reaction PDEs.
“As seen in Fig. 6A, the cell densities achieved are comparable to those observed by Jin et al.,8 and admit treatment of the problem using continuum advection-diffusion-reaction PDEs.”
From Inference of weak-form partial differential equations describing migration and proliferation mechanisms in wound healing experiments on cancer cells (2025) · cites this paper as [8]
The Methods section describes scratch assays using skin-organoid-derived fibroblasts and macrophages, but gives no cell densities comparable to the citing paper's MDA-MB-231 assays. Searches for MDA-MB-231, Jin, and advection-diffusion-reaction PDEs found no passage addressing the attributed comparison or modeling rationale; no page number is available in our copy. (LLM, conf=0.77)
Experimental — accuracy not yet measuredLagergren et al. inferred density-dependent reaction-diffusion equations for cell migration and identified non-linear functions of concentration for diffusivity and reaction terms that vary with initial seeding concentration, consistent with our findings.
“Lagergren et al. demonstrated the power of this approach on the Jin et al. dataset8 (also analyzed by Jin et al.), when they inferred density-dependent reaction-diffusion equations for cell migration10. They identified non-linear functions of concentration for diffusivity and reaction terms, and found that these functions vary with initial seeding concentration, consistent with our findings.”
From Inference of weak-form partial differential equations describing migration and proliferation mechanisms in wound healing experiments on cancer cells (2025) · cites this paper as [8]
Split into 2 atoms — 0 confirmed, 0 partially supported, 0 disputed, 0 misattributed, 2 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measured
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The Spectrum of Fibroblast Immune Biology
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Reversing vascular aging by restoring macrophages
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Prenatal Skin Cell Atlas reveals macrophages’ role beyond immunity
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Krüppel-like factor 2 programs early exhausted T cell states and restrains antiviral immunity
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Hair follicle organoids: advances in construction, applications, and translational challenges
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Macrophages in embryonic development
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Macrophages boosting human skin morphogenesis
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The Beauty of Fibroblasts Is Several Skin Layers Deep and Much Deeper
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Senescence-induced reparative fibroblasts enable scarless wound healing in aged murine skinPreprint
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Enhanced differentiation potential of pigmented human epidermal equivalents
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- Authors
- Gopee, N. H., Winheim, E., Olabi, B., Admane, C., Foster, A. R., Huang, N., Botting, R. A., Torabi, F., Sumanaweera, D., Le, A. P., Kim, J., Verger, L., Stephenson, E., Adão, D., Ganier, C., Gim, K. Y., Serdy, S. A., Deakin, C., Goh, I., Steele, L., Annusver, K., Miah, M.-U., Tun, W. M., Moghimi, P., Kwakwa, K. A., Li, T., Basurto Lozada, D., Rumney, B., Tudor, C. L., Roberts, K., Chipampe, N.-J., Sidhpura, K., Englebert, J., Jardine, L., Reynolds, G., Rose, A., Rowe, V., Pritchard, S., Mulas, I., Fletcher, J., Popescu, D.-M., Poyner, E., Dubois, A., Guy, A., Filby, A., Lisgo, S., Barker, R. A., Glass, I. A., Park, J.-E., Vento-Tormo, R., Nikolova, M. T., He, P., Lawrence, J. E. G., Moore, J., Ballereau, S., Hale, C. B., Shanmugiah, V., Horsfall, D., Rajan, N., McGrath, J. A., O’Toole, E. A., Treutlein, B., Bayraktar, O., Kasper, M., Progatzky, F., Mazin, P., Lee, J., Gambardella, L., Koehler, K. R., Teichmann, S. A., & Haniffa, M.
- Affiliations
- Newcastle upon Tyne Hospitals NHS Foundation Trust (GB)
- Wellcome Sanger Institute (GB)
- Newcastle University (GB)
- Boston Children's Hospital (US)
- University of Oxford (GB)
- Karolinska Institutet (SE)
- Guy's Hospital (GB)
- Wellcome/MRC Cambridge Stem Cell Institute (GB)
- University of Washington (US)
- ETH Zurich (CH)
- University of California, San Francisco (US)
- German BioImaging – Gesellschaft für Mikroskopie und Bildanalyse (DE)
- King's College London (GB)
- Queen Mary University of London (GB)
- Corresponding author
- Koehler, Karl R.
- Teichmann, Sarah A.
- Haniffa, Muzlifah
- ORCID
- Gopee, Nusayhah Hudaa
- Winheim, Elena
- Olabi, Bayanne
- Admane, Chloe
- Foster, April Rose
- Huang, Ni
- Botting, Rachel A.
- Torabi, Fereshteh
- Sumanaweera, Dinithi
- Le, Anh Phuong
- Kim, Jin
- Verger, Luca
- Stephenson, Emily
- Adão, Diana
- Gim, Kelly Y.
- Serdy, Sara A.
- Goh, Issac
- Steele, Lloyd
- Annusver, Karl
- Miah, Mohi-Uddin
- Tun, Win Min
- Li, Tong
- Tudor, Catherine L.
- Roberts, Kenny
- Chipampe, Nana-Jane
- Sidhpura, Keval
- Jardine, Laura
- Reynolds, Gary
- Rose, Antony
- Pritchard, Sophie
- Mulas, Ilaria
- Poyner, Elizabeth
- Guy, Alyson
- Filby, Andrew
- Lisgo, Steven
- Barker, Roger A.
- Glass, Ian A.
- Park, Jong-Eun
- Vento-Tormo, Roser
- Nikolova, Marina Tsvetomilova
- He, Peng
- Lawrence, John E. G.
- Moore, Josh
- Hale, Christine B.
- Horsfall, David
- Rajan, Neil
- McGrath, John A.
- O’Toole, Edel A.
- Treutlein, Barbara
- Bayraktar, Omer
- Kasper, Maria
- Progatzky, Fränze
- Mazin, Pavel
- Lee, Jiyoon
- Gambardella, Laure
- Koehler, Karl R.
- Teichmann, Sarah A.
- Haniffa, Muzlifah
- Venue
- Nature
- Published
- 2024-10-16
- Volume
- 635
- Issue
- 8039
- Pages
- 679-689
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC11578897
- OpenAlex
- W4403450831
- Cited by
- 108
- References
- 108
- Citations by year
- 2026: 44 · 2025: 52 · 2024: 11 · 2016: 1
- FWCI
- 50.45
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Nature (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by-nc-nd)
- Queen Mary Research Online (Queen Mary University of London) (submittedVersion, cc-by-nc-nd)
- Apollo (University of Cambridge) (submittedVersion, cc-by-nc-nd)
- Repository for Publications and Research Data (ETH Zurich) (submittedVersion, cc-by-nc-nd)
- ETH Zürich Research Collection
- Funders
- Wellcome Trust
- National Institute for Health and Care Research ((NIHR203312)
- Medical Research Council (MR/W015625/1)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR075018, R01AR083139)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R24HD000836)
- Topics
- Health Sciences › Medicine › Urology › Hair Growth and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Skin and Cellular Biology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- skin morphogenesis, immune regulation, macrophages, endothelial development, hair follicle development, induced pluripotent stem cells, innate immune cells, skin diseases
- MeSH terms
- Human Embryonic Stem Cells, Multiomics, Adult, Atlases as Topic, Female, Fetus, Humans, Immunity, Innate, Macrophages, Morphogenesis, Organoids, Skin, Skin Diseases, Wound Healing, Hair Follicle, Neovascularization, Physiologic, Endothelial Cells, Induced Pluripotent Stem Cells, Single-Cell Analysis, Transcriptome
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