The DOI matches its Crossref record; 44 of the 44 references it cites were found in a registry or an index.
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]
Citations
Cites
STAR: ultrafast universal RNA-seq aligner
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., & Gingeras, T. R. (2013) · Bioinformatics · doi:10.1093/bioinformatics/bts635 · Cited by 51,709
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources
Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009) · Nature Protocols · doi:10.1038/nprot.2008.211 · Cited by 35,890
HTSeq—a Python framework to work with high-throughput sequencing data
Anders, S., Pyl, P. T., & Huber, W. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btu638 · Cited by 21,464
A scaling normalization method for differential expression analysis of RNA-seq data
Robinson, M. D., & Oshlack, A. (2010) · Genome Biology · doi:10.1186/gb-2010-11-3-r25 · Cited by 7,876
Organogenesis in a dish: Modeling development and disease using organoid technologies
Lancaster, M. A., & Knoblich, J. A. (2014) · Science · doi:10.1126/science.1247125 · Cited by 2,931
Defining the Epithelial Stem Cell Niche in Skin
Tumbar, T., Guasch, G., Greco, V., Blanpain, C., Lowry, W. E., Rendl, M., & Fuchs, E. (2004) · Science · doi:10.1126/science.1092436 · Cited by 2,031
Self-organizing optic-cup morphogenesis in three-dimensional culture
Eiraku, M., Takata, N., Ishibashi, H., Kawada, M., Sakakura, E., Okuda, S., Sekiguchi, K., Adachi, T., & Sasai, Y. (2011) · Nature · doi:10.1038/nature09941 · Cited by 2,001
Eiraku, M., Watanabe, K., Matsuo-Takasaki, M., Kawada, M., Yonemura, S., Matsumura, M., Wataya, T., Nishiyama, A., Muguruma, K., & Sasai, Y. (2008) · Cell Stem Cell · doi:10.1016/j.stem.2008.09.002 · Cited by 1,522
Distinct fibroblast lineages determine dermal architecture in skin development and repair
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., et al. (2013) · Nature · doi:10.1038/nature12783 · Cited by 1,291
Small-sample estimation of negative binomial dispersion, with applications to SAGE data
Robinson, M. D., & Smyth, G. K. (2007) · Biostatistics · doi:10.1093/biostatistics/kxm030 · Cited by 1,073
Cited by
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Items 101–142 of 142
Recent progress in the identification and in vitro culture of skin organoids
Huang, Y., Ye, Q., Wang, J., Kaimin, Z., Yang, H., Jiang, X., & Shen, M. (2025) · Regenerative Therapy · doi:10.1016/j.reth.2025.01.001 · Cited by 8
Wang, S., Sun, J., Li, Y., Zhou, Y., Cai, Y., Simayijiang, Z., Gu, Z., & Xie, Z. (2026) · Materials Today Bio · doi:10.1016/j.mtbio.2026.102997 · Cited by 4
Guo, X., Wu, M., Li, Y., et al. (2026) · Antioxidants · doi:10.3390/antiox15040484 · Cited by 4
Zhou, Y., & Chuong, C. (2025) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2025.07.013 · Cited by 4
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Zhang, M., Wang, M., Jiang, J., Liu, W., Zhou, S., Wang, D., Wang, M., Zhao, Z., Xu, Z., Wang, W., et al. (2023) · International Journal of Biological Sciences · doi:10.7150/ijbs.83387 · Cited by 3
“Two available mice skin transcriptome data were downloaded from previous studies [21].”
Self-citationXing, Y., Xiang, F., Guo, H., Gong, H., & Li, Y. (2023) · Experimental Dermatology · doi:10.1111/exd.14999 · Cited by 3
Patient-derived skin tumor organoids with immune cells respond to metformin
Shi, Y., Liu, J., Li, L., Wang, C., Zhang, J., Rong, M., Rao, Y., Zhou, X., Sun, D., Chen, J., et al. (2024) · Cell organoid (Print) · doi:10.26599/co.2024.9410001 · Cited by 3
The role of CTHRC1 in hair follicle regenerative capacity restored by plantar dermis homogenate
Zhang, Y., Enhejirigala, Zhao, L., Song, W., Yao, B., Li, J., Wang, Y., Duan, X., Yuan, X., Huang, S., et al. (2021) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2021.07.056 · Cited by 3
Bioengineering strategies for regeneration of skin integrity: A literature review
Shiraishi, M., Sowa, Y., Sunaga, A., Yamamoto, K., & Okazaki, M. (2024) · Regenerative Therapy · doi:10.1016/j.reth.2024.12.006 · Cited by 2
Silli, E. K., Wang, K., Xiao, Z., Liu, T., Zhang, L., Zhu, J., Song, R., & Lv, H. (2026) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2026.150363 · Cited by 2
Hair Regeneration under Stress
Davidson, J. M. (2018) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2018.02.031 · Cited by 2
Skin Organoid Research Progress and Potential Applications
Li, H., Ren, K., Wang, C., & Bu, W.-B. (2021) · International Journal of Dermatology and Venereology · doi:10.1097/jd9.0000000000000201 · Cited by 5
Regeneration of Mouse Skin Melanocyte Stem Cells In Vivo and In Vitro
Yang, K., Qiu, W., Gu, P.-R., et al. (2018) · Methods in molecular biology · doi:10.1007/7651_2018_143 · Cited by 2
Self-citationSystems of pattern formation within developmental biology
Pas, K. E., Laboy-Segarra, S. L., & Lee, J. (2021) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2021.09.005 · Cited by 3
Intestinal and optic-cup organoids as tools for unveiling mechanics of self-organizing morphogenesis
Nath, S., Toda, S., & Okuda, S. (2022) · Biophysics and Physicobiology · doi:10.2142/biophysico.bppb-v19.0048 · Cited by 2
Molecular aspects governing epidermal stem cell niches
Kuri, P., Rice, G., & Rompolas, P. (2019) · Advances in stem cells and their niches · doi:10.1016/bs.asn.2019.05.001 · Cited by 2
Review of Stem Cell Therapy for Hair Loss
Alkhalaf, H. M. (2024) · Journal of Dermatology Research Reviews & Reports · doi:10.47363/jdmrs/2024(5)159 · Cited by 1
“The success of the future stem cell research depends on our ability to comprehend how cells interact to form three-dimensional structures [14].”
Advances in sweat gland organoids: construction, molecular mechanisms, and challenges
Liu, X., Ye, Y., Chen, J., Tan, Y., Yang, G., Li, L., Liu, H., Liang, Y., Lei, M., & Lei, X. (2025) · Stem Cell Research & Therapy · doi:10.1186/s13287-025-04689-5 · Cited by 2
“Their method shares similarities with our study [15], which assembled hair follicle organoids using epidermal and dermal cells.”
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Chen, Q., & Zernicka‐Goetz, M. (2026) · Nature Biotechnology · doi:10.1038/s41587-026-03161-w · Cited by 2
“A compelling example is the self-organization of skin-derived organoids 36 , where a ‘mechano–chemical circuit’ transforms multiple spheroidal units into a flat epithelial sheet, mirroring in vivo skin architecture.”
In vitro and in vivo models for androgenetic alopecia drug development
Tu, S., Nanmo, A., Migita, Y., Asaba, T., Seo, J., Hamano, S., Kageyama, T., & Fukuda, J. (2026) · Disease Models & Mechanisms · doi:10.1242/dmm.052848 · Cited by 2
“…limitations prevail in vascularization, immune components and overall tissue architecture , particularly, given that HF formation follows an outside – in structure, with mesenchymal cells on the outside and epithelial cells on the inside of the organoid (Kageyama et al., 2022a; Lei et al., 2017).”
Suppression of IGF1R in Melanoma Cells by an Adenovirus-Mediated One-Step Knockdown System
Xin, H., Lei, M., Zhang, Z., Li, J., Zhang, H., Luo, X., Wang, A., & Deng, F. (2018) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2018.08.004 · Cited by 1
“Immunofluorescence Staining Immunofluorescence staining was performed as previously described.(28,29) Briefly, after infection with AdRmIGF1R-OK, AdRhIGF1R-OK, or AdRFP for 72 hr, cells were fixed with methanol for 10 min, permeabilized with 1% nonyl phenoxypolyethoxylethanol-40 (NP-40) for 5 min, and blocked with 10%…”
MethodSelf-citationCutaneous epithelial stem cells
Gay, D. L., Plikus, M. V., Lee, I., Treffeisen, E. R., Wang, A., & Cotsarelis, G. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-818422-6.00071-x · Cited by 1
Khoo, T. C., Moskwa, N. L., Athanassiadis, G. A., et al. (2020) · Label-free Biomedical Imaging and Sensing (LBIS) · doi:10.1117/12.2547636
Capturing Neonatal Cardiomyocyte – Endothelial interactions on-a-ChipPreprint
Tavassoli, H., Kang, Y. C., Rorimpandey, P., Pimanda, J. E., Chandrakanthan, V., & Chan, P. P. Y. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.08.10.243600
Utilizing organoids to study general and tissue-specific adult stem cell profiles
Boonekamp, K. E. (2020) · Utrecht University Repository (Utrecht University) · doi:10.33540/280
Zhou, S., Li, Z., Li, K., et al. (2024) · Research Square · doi:10.21203/rs.3.rs-4772423/v1
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Zheng, K., Yang, Q., & Wu, Y. (2025) · Health engineering. · doi:10.26599/he.2024.9460004
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Hosseini, S. Z. (2018) · Scholars Archive - University at Albany (University at Albany, State University of New York) · doi:10.54014/0gvr-a4kq
Liu, W., Lei, M., Shen, X., et al. (2025) · SSRN Electronic Journal · doi:10.2139/ssrn.5389001
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Chuong, C., Richman, J. M., & Wu, P. (2025) · Developmental Biology · doi:10.1016/j.ydbio.2025.10.019
Self-citationZhao, Y., Xie, T., Yi, Y., Zeng, X., Shao, S.-W., Xu, X., Gao, X., & Lei, M. (2025) · International Journal of Dermatology and Venereology · doi:10.1097/jd9.0000000000000446
Self-citationLiving Organs as Micro‐Factories: Material‐Producing Organoids
Perrin, Q. M., & Miserez, A. (2026) · Wiley Interdisciplinary Reviews Nanomedicine and Nanobiotechnology · doi:10.1002/wnan.70049
Symmetry breaking directs skin appendage fate
Zhou, C., Tang, F., Chen, Y., Zou, Y., Qu, Y., Zhou, X., & Lei, M. (2026) · Genes & Diseases · doi:10.1016/j.gendis.2026.102131
Self-citationDevelopment of a hair follicle reconstitution model utilizing cashmere goat hair follicle stem cells
Zhao, S., Fang, Y., Dong, Z., Ye, S., Yue, L., Liu, Q., Liu, H., Xu, S., Wang, X., Zhang, S., et al. (2026) · Journal of Animal Science · doi:10.1093/jas/skag120
Wang, Y., Nozhat, Z., Duan, T., Chen, S., Ni, Y., Wang, Y., Shen, C., & You, M. (2026) · Cancer Biome and Targeted Therapy · doi:10.66505/cbtt.v1i2.37
Skin organoid diversity and applications in biomedical research: A comprehensive review
Liang, L., Zhou, J., & Leng, L. (2026) · Cell Biomaterials · doi:10.1016/j.celbio.2026.100492 · Cited by 2
Temperature-sensitive IL4Ra signaling regulates skin inflammation and repair after thermal injury
Liu, W., Shen, X., Li, K., et al. (2026) · Genes & Diseases · doi:10.1016/j.gendis.2026.102252
Self-citationAdult stem cell therapy for skin wound healing: A translational perspective from bench to bedside
Lei, R., Li, G., Li, N., Lin, S., Chen, Q., Yu, X., Song, L., Liang, Y., Wang, W. L., Hu, B., et al. (2026) · Regenesis repair rehabilitation. · doi:10.1016/j.rerere.2026.06.003
Tang, Y., Wang, M., Ye, Y., Jiang, J., Huang, W., Zhao, Y., Xie, Q., Lin, J., Xiao, X., Ke, D., et al. (2026) · Research · doi:10.34133/research.1430
“3 A) [ 13 , 25 , 37 , 38 ].”
Self-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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