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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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“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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Self-citationGeneration of Skin Organoids: Potential Opportunities and Challenges
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Self-citationEstablishment and characterization of a canine keratinocyte organoid culture system
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“After the first in vitro step, a second step implying the transplantation of organoid explants in nude mice, resulted in the formation of HFs and a hair shaft.(28) Culture systems enabling the formation of canine IFE and HF organoids have not been described.”
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Self-citationThe mechano-chemical circuit drives skin organoid self-organization
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BackgroundInfluentialOrganoid‐Guided Precision Medicine: From Bench to Bedside
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Self-citationOrganoids of the Female Reproductive Tract: Innovative Tools to Study Desired to Unwelcome Processes
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MethodEpithelial-Mesenchymal Interaction in Hair Regeneration and Skin Wound Healing
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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
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“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
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BackgroundExpansion Culture of Hair Follicle Stem Cells through Uniform Aggregation in Microwell Array Devices
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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 22
“In an epithelial–mesenchymal coculture model [155], mesenchymal cells derived from neonatal mice generated significantly more HFs than those from older ( > 2 months) mice.”
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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 20
“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
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
“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
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
Zhao, H., Chen, Z., Kang, X., Yang, B., Luo, P., Li, H., & He, Q. (2023) · Toxicological Sciences · doi:10.1093/toxsci/kfad093 · Cited by 15
Reverse-engineering organogenesis through feedback loops between model systems
Narciso, C. E., & Zartman, J. J. (2017) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2017.12.009 · Cited by 13
RANKL Reduces Body Weight and Food Intake via the Modulation of Hypothalamic NPY/CART Expression
Zhu, P., Zhang, Z., Huang, X., Liang, S., Khandekar, N., Song, Z.-Y., & Lin, S. (2018) · International Journal of Medical Sciences · doi:10.7150/ijms.24373 · Cited by 14
“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 16
Self-citationPan, Y., Zou, J., Hu, T., Zhu, Z., Zhang, Z., Chen, W., & Lu, Y. (2025) · Molecular Diagnosis & Therapy · doi:10.1007/s40291-025-00776-8 · Cited by 14
“Two-Cell Assemblage” Assay: A Simple in vitro Method for Screening Hair Growth-Promoting Compounds
Jang, S., Ohn, J., Kang, B. M., Park, M., Kim, K. H., & Kwon, O. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.581528 · Cited by 13
THSD4 promotes hair growth by facilitating dermal papilla and hair matrix interactions
Wang, M., Wang, M., Jiang, J., Li, K., Liang, H., Wang, N., Zou, Y., Wang, D., Zhou, S., Tang, Y., et al. (2025) · Theranostics · doi:10.7150/thno.103221 · Cited by 14
“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
“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].”
Self-citationHe, L., Lei, M., Xing, Y., Li, Y., Hu, C., Chen, P., Lian, X., Tian, Y., Liu, W., & Yang, L. (2017) · Oncotarget · doi:10.18632/oncotarget.22212 · Cited by 12
“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
Talebzadeh, A. T., & Talebzadeh, N. (2023) · Cureus · doi:10.7759/cureus.37439 · Cited by 12
“[24] observed the key molecules in multistage morphogenesis of tissues.”
BackgroundPolyethylene-Glycol-Ornamented Small Intestinal Submucosa Biosponge for Skin Tissue Engineering
Dong, Y., Liu, Z., Qi, F., et al. (2019) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.8b01592 · Cited by 12
The global regulatory logic of organ regeneration: circuitry lessons from skin and its appendages
Yue, Z., Lei, M., Paus, R., & Chuong, C. (2021) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12767 · Cited by 13
“, 2018); and (v) tissue engineering (Higgins et al., 2013; Lei et al., 2017; Abaci et al., 2018).”
BackgroundSelf-citationXie, S., Chen, L., Zhang, M., Zhang, C., & Li, H. (2022) · Annals of Translational Medicine · doi:10.21037/atm-22-3252 · Cited by 11
“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
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
“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 10
Zhou, H., Zhang, Y.-X., Lei, Q.-K., Li, Y., & Zheng, Y. (2025) · Stem Cell Research & Therapy · doi:10.1186/s13287-025-04447-7 · Cited by 9
“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
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 9
Self-citationSha, K., Chen, M., Liu, F., Xu, S., Wang, B., Peng, Q., Zhang, Y., Xie, H., Li, J., & Deng, Z. (2020) · PeerJ · doi:10.7717/peerj.9867 · Cited by 7
“, 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
Zhou, R., Luo, X., Chen, S., Jia, K., Yu, H., Huang, Z., Tan, Y., Ma, M., Zhao, J., Xing, J., et al. (2025) · Chemical Engineering Journal · doi:10.1016/j.cej.2025.162248 · Cited by 6
Xu, C., Zhang, Y., Sutrisno, L., et al. (2018) · Connective Tissue Research · doi:10.1080/03008207.2018.1512978 · Cited by 6
Self-citationSpheroid formation of human keratinocyte: Balancing between cell-substrate and cell-cell interaction
Nie, Y. G., Xu, X., Wang, W., et al. (2020) · Clinical Hemorheology and Microcirculation · doi:10.3233/ch-209217 · Cited by 6
“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
“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
Metadata
- 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 › Dermatology › 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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