Self-organization process in newborn skin organoid formation inspires strategy to restore hair regeneration of adult cells
Open accessAbstract
Significance: This study opens avenues to improve the ability of adult skin cells to form a fully functional skin, with clinical applications. Our investigation elucidates a relay of molecular events and biophysical processes at the core of the self-organization process during tissue morphogenesis. Molecules key to the multistage morphological transition are identified and can be added or inhibited to restore the stalled process in adult cells. The principles uncovered here are likely to function in other organ systems and will inspire us to view organoid morphogenesis, embryogenesis, and regeneration differently. The application of these findings will enable rescue of robust hair formation in adult skin cells, thus eventually helping patients in the context of regenerative medicine.
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It remains challenging to induce hair neogenesis in in vitro culture, including the generation of matured hair follicles and the extension of long hair shafts.
“However, it remains challenging to induce hair neogenesis in in vitro culture, including the generation of matured hair follicles (e.g., dermal papilla and the bulge region) and the extension of long hair shafts (11).”
From Reprogramming of three-dimensional microenvironments for in vitro hair follicle induction (2022) · cites this paper as [11]
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Modeling of solar UV-induced photodamage on the hair follicles in human skin organoids
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“14,48 This system allowed us to obtain planar skin organoids with high structural maturity in which the epidermis, dermis, and hair follicles are stratified, akin to real skin.”
BackgroundBuilding Complex Life Through Self-Organization
Sthijns, M. M. J. P. E., LaPointe, V. L. S., & van Blitterswijk, C. (2019) · Tissue Engineering Part A · doi:10.1089/ten.tea.2019.0208 · Cited by 29 · see citing works
“been widely used with success, for example, in the selforganization of skin or the optic cup organoids.(33,40,41) Examples abound on the use of growth factors in directed differentiation of stem or progenitor cells to functioning and specified cell types, and by identifying these factors, selforganization can be impro…”
MethodEpithelial-Mesenchymal Interaction in Hair Regeneration and Skin Wound Healing
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Advances in organoid technology for veterinary disease modeling
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Functional regeneration strategies of hair follicles: advances and challenges
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“The restoration of trichogenicity in mature cells has been achieved through environmental signals like VEGF and PKC inhibition, although the durability of resulting HFs remains unexplored [47, 48].”
InfluentialLuo, J., Chen, M., Liu, Y., Xie, H., Yuan, J., Zhou, Y., Ding, J., Deng, Z., & Li, J. (2018) · PeerJ · doi:10.7717/peerj.4737 · Cited by 24 · see citing works
“Several signaling pathways, particularly Wnt/β-catenin signaling, have been shown to play a key role in the development of new hair follicles and initiation of hair growth (Kandyba et al., 2013; Chu et al., 2004; Lim & Nusse, 2013; Lei et al., 2017; Lei & Chuong, 2016; Lei, Yang & Chuong, 2017).”
BackgroundRevolutionizing healthcare: Emerging frontiers in 3D bioprinting of tissues and organs
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New Scenarios in Pharmacological Treatments of Head and Neck Squamous Cell Carcinomas
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“…con fi gurations and molecular pathways are used to achieve morphogenetic competence in developing skin, wound-induced hair neogenesis, and reconstituted explant cultures 14 , we need to learn more about how the morphogenetic processes progress in these reconstituted skin or organoids.”
BackgroundInfluentialSelf-citationSingle-cell transcriptomics identifies chondrocyte differentiation dynamics in vivo and in vitro
Lawrence, J. E. G., Woods Jon, S., Roberts, K., Sumanaweera, D., Balogh, P., Li, T., Predeus, A. V., He, P., Polański, K., Prigmore, E., et al. (2025) · Developmental Cell · doi:10.1016/j.devcel.2025.06.031 · Cited by 19 · see citing works
Wnt/β-catenin signaling promotes aging-associated hair graying in mice
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“Mesenchymal cells may constitute micro-niches with different epithelial cell lineages, resulting in different epithelial-mesenchymal interactions [34].”
BackgroundSelf-citationWeber, E. L., Lai, Y., Lei, M., Jiang, T., & Chuong, C. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.583434 · Cited by 20 · see citing works
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Organoids/organs-on-chips towards biomimetic human artificial skin
Huang, Y., Wu, X., Xu, Y., Yang, N., Xi, P., Wang, Y., Zhu, Y., & Chen, X. (2025) · Burns & Trauma · doi:10.1093/burnst/tkaf029 · Cited by 20 · see citing works
“When transplanted onto the backs of nude mice, these engineered tissues developed into structurally intact skin, and hair follicles, in which the hair follicles displayed structural and cyclic growth characteristics consistent with those of native hair follicles [128].”
Biomaterials and bioengineering to guide tissue morphogenesis in epithelial organoids
Jeon, E. Y., Sorrells, L., & Abaci, H. E. (2022) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2022.1038277 · Cited by 19 · see citing works
“The preceding approaches to produce multilayered skin have focused on the coculture of dissociated epidermal and dermal cells from newborn skin (Lei et al., 2017; Weber et al., 2019).”
BackgroundPeng, X., Wang, B., Yang, Y., Zhang, Y., Liu, Y., He, Y., Zhang, C., & Fan, H. (2019) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.8b01630 · Cited by 20 · see citing works
What gastroenterologists and hepatologists should know about organoids in 2019
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“[12] Lei M, Schumacher LJ, Lai YC, et al.”
BackgroundEngineered organoids in oral and maxillofacial regeneration
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“In general, the behavior and fate of cells in the process of organoid formation involve proliferation, differentiation, and self-organization, which contains cell sorting and architectural rearrangement.(34) Therefore, the characteristics of organoids partly rely on the starting cell type.”
BackgroundExpansion Culture of Hair Follicle Stem Cells through Uniform Aggregation in Microwell Array Devices
Hirano, S., Kageyama, T., Yamanouchi, M., Yan, L., Suzuki, K., Ebisawa, K., Kasai, K., & Fukuda, J. (2023) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.2c01141 · Cited by 18 · see citing works
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Organoids as Tools for Investigating Skin Aging: Mechanisms, Applications, and Insights
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“ASCs, such as melanocyte and epidermal stem cells, are critical for tissue repair and regeneration, enabling the formation of organoids that closely resemble natural skin, including structures like hair follicles [48].”
Advances in engineered organoid models of skin for biomedical research
Zeng, D., Li, S., Du, F., Xia, Y., Zhang, J., Yu, S., & Qin, J. (2025) · Burns & Trauma · doi:10.1093/burnst/tkaf016 · Cited by 20 · see citing works
“In an epithelial–mesenchymal coculture model [155], mesenchymal cells derived from neonatal mice generated significantly more HFs than those from older ( > 2 months) mice.”
Pandamooz, S., Jurek, B., Dianatpour, M., Haerteis, S., Limm, K., Oefner, P. J., Dargahi, L., Borhani‐Haghighi, A., Miyan, J. A., & Salehi, M. S. (2023) · Cell Proliferation · doi:10.1111/cpr.13397 · Cited by 16 · see citing works
Mechanical stimuli-induced CCL2 restores adult mouse cells to regenerate hair follicles
Wu, W., Zhou, W., Jiang, J., Wang, M., Zhang, J., Yang, J., Tang, Q., Liu, H., Liu, D., Xu, W., et al. (2023) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2023.03.002 · Cited by 19 · see citing works
Self-citationOrganizational principles of integumentary organs: Maximizing variations for effective adaptation
Chuong, C., Wu, P., Zhou, Y., Liang, Y. C., & Widelitz, R. B. (2025) · Developmental Biology · doi:10.1016/j.ydbio.2025.03.011 · Cited by 19 · see citing works
Self-citationThe dermal papilla dilemma and potential breakthroughs in bioengineering hair follicles
Andl, T., Zhou, L., & Zhang, Y. (2022) · Cell and Tissue Research · doi:10.1007/s00441-022-03730-w · Cited by 16 · see citing works
“Such mixtures of keratinocytes and fibroblasts isolated from embryonic or adult rodent skin can form aggregates using either the hanging drop method or lowattachment plates and retain their ability to induce hair follicle neogenesis (Asakawa et al. 2012; Balana et al. 2015; Guo et al. 2019; Lei et al. 2017; Qiao et al…”
MethodImpacts of manipulating cell sorting on in vitro hair follicle regeneration
Kageyama, T., Anakama, R., Togashi, H., & Fukuda, J. (2022) · Journal of Bioscience and Bioengineering · doi:10.1016/j.jbiosc.2022.09.004 · Cited by 15 · see citing works
Choudhury, S., Dhoke, N. R., Chawla, S., & Das, A. (2024) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-023-05057-3 · Cited by 15 · see citing works
“Furthermore, we utilized air–liquid interface culture in our study settings to generate a 3D stratified skin organoid as reported earlier by layered co-culture of fibroblasts and keratinocytes that successfully generates 3D stratified skin structures [21, 45, 46].”
BackgroundMethodTherapeutic potential of endogenous stem cells and cellular factors for scar-free skin regeneration
Giri, S., Machens, H., & Bader, A. (2018) · Drug Discovery Today · doi:10.1016/j.drudis.2018.10.014 · Cited by 15 · see citing works
STIMULATING HAIR GROWTH VIA HORMESIS: Experimental Foundations and Clinical Implications.
Calabrese, E. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2019.104599 · Cited by 15 · see citing works
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Reverse-engineering organogenesis through feedback loops between model systems
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RANKL Reduces Body Weight and Food Intake via the Modulation of Hypothalamic NPY/CART Expression
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“After sacrificing mice with the same procedure stated above, we cut 20μm coronal slices and prepared them as described in previous study [26, 27].”
MethodEnvironmental Regulation of Skin Pigmentation and Hair Regeneration
Wu, W., Yang, J., Tao, H., & Lei, M. (2022) · Stem Cells and Development · doi:10.1089/scd.2022.29011.wwu · Cited by 14 · see citing works
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“Two-Cell Assemblage” Assay: A Simple in vitro Method for Screening Hair Growth-Promoting Compounds
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THSD4 promotes hair growth by facilitating dermal papilla and hair matrix interactions
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“The mouse skin organoid culture was generated as described before [37].”
Self-citationWnt10b Regulation of Hair Follicle Development, Regeneration, and Skin Diseases
Zou, Y. Z., Tang, F., Li, P., Qiu, W., & Lei, M. (2025) · Stem Cell Reviews and Reports · doi:10.1007/s12015-025-10898-5 · Cited by 14 · see citing works
“Interestingly, our skin organoid studies also demonstrate that the addition of Wnt10b can restore the adult skin cells which lose their regenerative ability to regenerate hair follicles [53 – 55].”
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“It includes both epithelial tissues and a group of specified mesenchymal cells known as dermal papilla (DP) [2].”
BackgroundSelf-citationStem Cell Applications in Human Hair Growth: A Literature Review
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“[24] observed the key molecules in multistage morphogenesis of tissues.”
BackgroundPolyethylene-Glycol-Ornamented Small Intestinal Submucosa Biosponge for Skin Tissue Engineering
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The global regulatory logic of organ regeneration: circuitry lessons from skin and its appendages
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“, 2018); and (v) tissue engineering (Higgins et al., 2013; Lei et al., 2017; Abaci et al., 2018).”
BackgroundSelf-citationXie, S., Chen, L., Zhang, M., et al. (2022) · Annals of Translational Medicine · doi:10.21037/atm-22-3252 · Cited by 11 · see citing works
“showed that mouse neonatal epidermis and dermis cells self-organized into planar hair-bearing skin via an early organoid-like aggregation state using a 3D droplet culture method (7).”
MethodPaik, S. H., Choi, S., Jang, S., Jo, S. J., Kim, K. H., & Kwon, O. (2019) · Experimental Dermatology · doi:10.1111/exd.13897 · Cited by 11 · see citing works
Editorial: Hair Follicle Stem Cell Regeneration in Aging
Lei, M., Lin, S., & Chuong, C. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.799268 · Cited by 10 · see citing works
“Epithelialmesenchymal interaction also leads to the formation of a skin cyst when mouse epidermal and dermal cells were mixed and 3dimensionally cultured on a transwell insert, namely organoid culture (Lei et al., 2017).”
BackgroundSelf-citationInhibition of class I HDACs preserves hair follicle inductivity in postnatal dermal cells
Park, M., Jang, S., Chung, J. H., Kwon, O., & Jo, S. J. (2021) · Scientific Reports · doi:10.1038/s41598-021-03508-0 · Cited by 9 · see citing works
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“They found that enhancing specific gene expressions may provide more robust hair follicles and improve the efficacy of HT. Lei et al. [62] isolated cells from newborn mice, remixed them, and cultured them to form organ tissues containing hair primordia.”
Li, Y. E., Wang, J., Wang, Y.-H., Shao, H., Young, L.-C., & Young, T. (2020) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.0c00304 · Cited by 8 · see citing works
Skin Cyst: A Pathological Dead-End With a New Twist of Morphogenetic Potentials in Organoid Cultures
Qiu, W., Gu, P.-R., Chuong, C., & Lei, M. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.628114 · Cited by 8 · see citing works
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“, 2014; Plikus & Chuong, 2014), whose activity in DP cells promotes the activation of HFSCs, thus triggering the growth of hair follicles (Morgan, 2014; Enshell-Seijffers et al., 2010; Lei et al., 2017; Lei & Chuong, 2016).”
BackgroundInnovative approaches in skin therapy: The rise of organoid cultivation
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Self-citationSpheroid formation of human keratinocyte: Balancing between cell-substrate and cell-cell interaction
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“In spheroid culture, the dissociated skin progenitor cells underwent stepwise morphological transitions similar to the morphogenesis process of native skin development, including aggregation, polarization as well as coalescence, and could at the end form the hair-bearing skin [13].”
BackgroundEditorial: Inflammation, stem cells and wound healing in skin aging
Lei, M., Lien, W., & Li, J. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.1046022 · Cited by 6 · see citing works
“HFSCs and hair follicle organoids are major models for studying hair-related diseases and skin aging (Lei and Chuong 2016; Lei et al., 2017).”
BackgroundSelf-citation
- Authors
- Lei, M., Schumacher, L. J., Lai, Y.-C., Juan, W.-T., Yeh, C.-Y., Wu, P., Jiang, T.-X., Baker, R. E., Widelitz, R. B., Yang, L., & Chuong, C.-M.
- Affiliations
- University of Southern California (US)
- University of Oxford (GB)
- China Medical University (TW)
- Chongqing University (CN)
- Corresponding author
- Chuong, Cheng-Ming
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2017-08-10
- Volume
- 114
- Issue
- 34
- Pages
- E7101-E7110
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC5576784
- OpenAlex
- W2742248339
- Cited by
- 142
- References
- 44
- Citations by year
- 2026: 13 · 2025: 18 · 2024: 13 · 2023: 13 · 2022: 14 · 2021: 19 · 2020: 17 · 2019: 13 · 2018: 18 · 2017: 4
- FWCI
- 17.19
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (submittedVersion)
- Spiral (Imperial College London) (submittedVersion)
- Funders
- HHS | NIH | National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR42177, AR60306)
- 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 organoids, self-organization, hair regrowth, hair follicle morphogenesis, tissue morphogenesis, biophysical processes, molecular signaling, regenerative medicine, organoid formation
- MeSH terms
- Animals, Animals, Newborn, Female, Hair, Male, Mice, Nude, Morphogenesis, Organoids, Regeneration, Skin, Skin Physiological Phenomena, Stem Cells, Matrix Metalloproteinases, Mice
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