Generation and characterization of hair-bearing skin organoids from human pluripotent stem cells

Jiyoon Lee, Wouter H. van der Valk, Sara A. Serdy, CiCi Deakin, Jin Kim, Anh Phuong Le, Karl R. Koehler

Published: 2022-03-22 DOI: 10.1038/s41596-022-00681-y

human pluripotent stem cells

hair-bearing skin organoids

three-dimensional culture

skin tissue regeneration

fetal skin development

AI 解读

暂无数据

Author Correction: Full-length sequencing of circular DNA viruses and extrachromosomal circular DNA using CIDER-Seq

Generation of heart-forming organoids from human pluripotent stem cells

Design and fabrication of wearable electronic textiles using twisted fiber-based threads

Activation of mechanoluminescent nanotransducers by focused ultrasound enables light delivery to deep-seated tissue in vivo

Chromatin accessibility profiling by ATAC-seq

Deoxyfluorination of phenols for chemoselective18F-labeling of peptides

Author Correction: cfSNV: a software tool for the sensitive detection of somatic mutations from cell-free DNA

Human primordial germ cell-like cells specified from resetting precursors develop in human hindgut organoids

An inexpensive semi-automated sample processing pipeline for cell-free RNA extraction

Application of CHyMErA Cas9-Cas12a combinatorial genome-editing platform for genetic interaction mapping and gene fragment deletion screening

查看全部

Sections

Figures

References

Haniffa, M. et al. Human Developmental Cell Atlas: milestones achieved and the roadmap ahead. https://doi.org/10.21203/rs.3.rs-73986/v1 (2020).
Regev, A. et al. The Human Cell Atlas. eLife 6, e27041 (2017).
Dąbrowska, A. K. et al. The relationship between skin function, barrier properties, and body‐dependent factors. Ski. Res. Technol. 24, 165–174 (2018).
Kolarsick, P. A. J., Kolarsick, M. A. & Goodwin, C. Anatomy and physiology of the skin. J. Dermatol. Nurs. Assoc. 3, 203–213 (2011).
Nose, H., Kamijo, Y. & Masuki, S. Chapter 25—interactions between body fluid homeostasis and thermoregulation in humans. Handb. Clin. Neurol. 156, 417–429 (2018).
Woo, S.-H., Lumpkin, E. A. & Patapoutian, A. Merkel cells and neurons keep in touch. Trends Cell Biol. 25, 74–81 (2015).
Zimmerman, A., Bai, L. & Ginty, D. D. The gentle touch receptors of mammalian skin. Science 346, 950–954 (2014).
Sun, B. K., Siprashvili, Z. & Khavari, P. A. Advances in skin grafting and treatment of cutaneous wounds. Science 346, 941–945 (2014).
Karimkhani, C. et al. Global skin disease morbidity and mortality: an update from the Global Burden of Disease Study 2013. JAMA Dermatol. 153, 406–412 (2017).
He, Z. et al. Factors affecting health-related quality of life in patients with skin disease: cross-sectional results from 8,789 patients with 16 skin diseases. Health Qual. Life Outcomes 18, 298 (2020).
Laughter, M. R. et al. The burden of skin and subcutaneous diseases in the United States from 1990 to 2017. JAMA Dermatol. 156, 874–881 (2020).
Laughter, M. R. et al. The global burden of atopic dermatitis: lessons from the Global Burden of Disease Study 1990–2017*. Brit. J. Dermatol. 184, 304–309 (2021).
Mehrmal, S., Uppal, P., Nedley, N., Giesey, R. L. & Delost, G. R. The global, regional, and national burden of psoriasis in 195 countries and territories, 1990 to 2017: a systematic analysis from the Global Burden of Disease Study 2017. J. Am. Acad. Dermatol. 84, 46–52 (2021).
Wu, X., Scott, L., Washenik, K. & Stenn, K. Full-thickness skin with mature hair follicles generated from tissue culture expanded human cells. Tissue Eng. 20, 3314–3321 (2014).
Klicznik, M. M. et al. A novel humanized mouse model to study the function of human cutaneous memory T cells in vivo in human skin. Sci. Rep. 10, 11164 (2020).
Agarwal, Y. et al. Development of humanized mouse and rat models with full-thickness human skin and autologous immune cells. Sci. Rep. 10, 14598 (2020).
Salgado, G., Ng, Y. Z., Koh, L. F., Goh, C. S. M. & Common, J. E. Human reconstructed skin xenografts on mice to model skin physiology. Differentiation 98, 14–24 (2017).
Takagi, R. et al. Bioengineering a 3D integumentary organ system from iPS cells using an in vivo transplantation model. Sci. Adv. 2, e1500887 (2016).
Zheng, Y. et al. Organogenesis from dissociated cells: generation of mature cycling hair follicles from skin-derived cells. J. Invest. Dermatol. 124, 867–876 (2005).
Zomer, H. D. & Trentin, A. G. Skin wound healing in humans and mice: challenges in translational research. J. Dermatol. Sci. 90, 3–12 (2018).
Itoh, M. et al. Generation of 3D skin equivalents fully reconstituted from human induced pluripotent stem cells (iPSCs). PLoS ONE 8, e77673 (2013).
Yang, R. et al. Generation of folliculogenic human epithelial stem cells from induced pluripotent stem cells. Nat. Commun. 5, 3071–3071 (2014).
Gledhill, K. et al. Melanin transfer in human 3D skin equivalents generated exclusively from induced pluripotent stem cells. PLoS ONE 10, e0136713 (2015).
Abaci, H. E. et al. Tissue engineering of human hair follicles using a biomimetic developmental approach. Nat. Commun. 9, 5301 (2018).
Letsiou, S. Tracing skin aging process: a mini-review of in vitro approaches. Biogerontology 22, 261–272 (2021).
Christian, H., Hans & Yves, P. in Skin Disease Models In Vitro and Inflammatory Mechanisms: Predictability for Drug Development 187– 218 (Springer International Publishing, 2021); https://doi.org/10.1007/164_2020_428
Lee, J. et al. Hair-bearing human skin generated entirely from pluripotent stem cells. Nature 582, 399–404 (2020).
Lee, J. & Koehler, K. R. Skin organoids: a new human model for developmental and translational research. Exp. Dermatol. 30, 613–620 (2021).
Biggs, L. C., Kim, C. S., Miroshnikova, Y. A. & Wickström, S. A. Mechanical forces in the skin: roles in tissue architecture, stability, and function. J. Invest. Dermatol. 140, 284–290 (2019).
Wong, R., Geyer, S., Weninger, W., Guimberteau, J. & Wong, J. K. The dynamic anatomy and patterning of skin. Exp. Dermatol. 25, 92–98 (2016).
Lee, J. et al. Hair follicle development in mouse pluripotent stem cell-derived skin organoids. Cell Rep. 22, 242–254 (2018).
Koehler, K. R., Mikosz, A. M., Molosh, A. I., Patel, D. & Hashino, E. Generation of inner ear sensory epithelia from pluripotent stem cells in 3D culture. Nature 500, 217–221 (2013).
Eiraku, M. et al. Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell 3, 519–532 (2008).
Eiraku, M. et al. Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 472, 51–56 (2011).
Koehler, K. R. et al. Generation of inner ear organoids containing functional hair cells from human pluripotent stem cells. Nat. Biotechnol. 35, 583–589 (2017).
Prummel, K. D., Nieuwenhuize, S. & Mosimann, C. The lateral plate mesoderm. Development 147, dev175059 (2020).
Guibentif, C. et al. Diverse routes toward early somites in the mouse embryo. Dev. Cell 56, 141–153.e6 (2021).
Wilson, P. A. & Hemmati-Brivanlou, A. Induction of epidermis and inhibition of neural fate by Bmp-4. Nature 376, 331–333 (1995).
Duverger, O. & Morasso, M. I. To grow or not to grow: hair morphogenesis and human genetic hair disorders. Semin. Cell Dev. Biol. 25, 22–33 (2014).
McCune, J. M. & Weissman, I. L. The ban on US government funding research using human fetal tissues: how does this fit with the NIH mission to advance medical science for the benefit of the citizenry? Stem Cell Rep. 13, 777–786 (2019).
Haniffa, M. et al. A roadmap for the Human Developmental Cell Atlas. Nature 597, 196–205 (2021).
Yu, Q. et al. Charting human development using a multi-endodermal organ atlas and organoid models. Cell 184, 3281–3298 (2021).
Yucha, S. E. V., Tamamoto, K. A., Nguyen, H., Cairns, D. M. & Kaplan, D. L. Human skin equivalents demonstrate need for neuro-immuno-cutaneous system. Adv. Biosyst. 3, 1800283 (2019).
Meltzer, S., Santiago, C., Sharma, N. & Ginty, D. D. The cellular and molecular basis of somatosensory neuron development. Neuron 109, 3736–3757 (2021).
Andersen, J. et al. Generation of functional human 3D cortico-motor assembloids. Cell 183, 1913–1929.e26 (2020).
Wainger, B. J. et al. Modeling pain in vitro using nociceptor neurons reprogrammed from fibroblasts. Nat. Neurosci. 18, 17–24 (2015).
Oulès, B. et al. Contribution of GATA6 to homeostasis of the human upper pilosebaceous unit and acne pathogenesis. Nat. Commun. 11, 5067 (2020).
Kanwar, I. L. et al. Models for acne: a comprehensive study. Drug Discov. Ther. 12, 329–340 (2018).
Langan, S. M., Irvine, A. D. & Weidinger, S. Atopic dermatitis. Lancet 396, 345–360 (2020).
Condorelli, A. G., Dellambra, E., Logli, E., Zambruno, G. & Castiglia, D. Epidermolysis bullosa-associated squamous cell carcinoma: from pathogenesis to therapeutic perspectives. Int J. Mol. Sci. 20, 5707 (2019).
Kim, D. P., Kus, K. J. B. & Ruiz, E. Basal cell carcinoma review. Hematol. Oncol. Clin. North Am. 33, 13–24 (2019).
Davis, L. E., Shalin, S. C. & Tackett, A. J. Current state of melanoma diagnosis and treatment. Cancer Biol. Ther. 20, 1–14 (2019).
Que, S. K. T., Zwald, F. O. & Schmults, C. D. Cutaneous squamous cell carcinoma Incidence, risk factors, diagnosis, and staging. J. Am. Acad. Dermatol. 78, 237–247 (2018).
Waldman, A. & Schmults, C. Cutaneous squamous cell carcinoma. Hematol. Oncol. Clin. North Am. 33, 1–12 (2019).
Hogue, L. & Harvey, V. M. Basal cell carcinoma, squamous cell carcinoma, and cutaneous melanoma in skin of color patients. Dermatol. Clin. 37, 519–526 (2019).
Yum, M. K. et al. Tracing oncogene-driven remodelling of the intestinal stem cell niche. Nature 594, 442–447 (2021).
Yang, L., Mali, P., Kim-Kiselak, C. & Church, G. In Gene Correction. Methods in Molecular Biology (Methods and Protocols) (ed. Storici F.) Vol 1114, 245–267 (Humana Press, 2014); https://doi.org/10.1007/978-1-62703-761-7_16
Hendriks, D., Clevers, H. & Artegiani, B. CRISPR-Cas tools and their application in genetic engineering of human stem cells and organoids. Cell Stem Cell 27, 705–731 (2020).
Wenzel, D. et al. Genetically corrected iPSCs as cell therapy for recessive dystrophic epidermolysis bullosa. Sci. Transl. Med. 6, 264ra165–264ra165 (2014).
Sebastiano, V. et al. Human COL7A1-corrected induced pluripotent stem cells for the treatment of recessive dystrophic epidermolysis bullosa. Sci. Transl. Med. 6, 264ra163–264ra163 (2014).
Tolar, J. et al. Induced pluripotent stem cells from individuals with recessive dystrophic epidermolysis bullosa. J. Invest. Dermatol. 131, 848–856 (2011).
Itoh, M., Kiuru, M., Cairo, M. S. & Christiano, A. M. Generation of keratinocytes from normal and recessive dystrophic epidermolysis bullosa-induced pluripotent stem cells. Proc. Natl Acad. Sci. USA. 108, 8797–8802 (2011).
Candi, E., Schmidt, R. & Melino, G. The cornified envelope: a model of cell death in the skin. Nat. Rev. Mol. Cell Biol. 6, 328–340 (2005).
Langbein, L., Yoshida, H., Praetzel-Wunder, S., Parry, D. A. & Schweizer, J. The keratins of the human beard hair medulla: the riddle in the middle. J. Invest. Dermatol. 130, 55–73 (2010).
Lu, C. & Fuchs, E. Sweat gland progenitors in development, homeostasis, and wound repair. Cold Spring Harb. Perspect. Med. 4, a015222 (2014).
Lu, C. P., Polak, L., Keyes, B. E. & Fuchs, E. Spatiotemporal antagonism in mesenchymal–epithelial signaling in sweat versus hair fate decision. Science 354, aah6102 (2016).
Zhao, X. et al. Review on the vascularization of organoids and organoids-on-a-chip. Front. Bioeng. Biotechnol. 9, 637048 (2021).
Augustin, H. G., Koh, G. Y., Thurston, G. & Alitalo, K. Control of vascular morphogenesis and homeostasis through the angiopoietin–Tie system. Nat. Rev. Mol. Cell Biol. 10, 165–177 (2009).
Holloway, E. M. et al. Differentiation of human intestinal organoids with endogenous vascular endothelial cells. Dev. Cell 54, 516–528.e7 (2020).
Bar-Ephraim, Y. E., Kretzschmar, K. & Clevers, H. Organoids in immunological research. Nat. Rev. Immunol. 20, 279–293 (2020).
Takahashi, K. & Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663–676 (2006).
Tchieu, J. et al. A modular platform for differentiation of human PSCs into all major ectodermal lineages. Cell Stem Cell 21, 399–410.e7 (2017).
Volpato, V. & Webber, C. Addressing variability in iPSC-derived models of human disease: guidelines to promote reproducibility. Dis. Model Mech. 13, dmm042317 (2020).
Vigilante, A. et al. Identifying extrinsic versus intrinsic drivers of variation in cell behavior in human iPSC lines from healthy donors. Cell Rep. 26, 2078–2087.e3 (2019).
Li, W., Germain, R. N. & Gerner, M. Y. High-dimensional cell-level analysis of tissues with Ce3D multiplex volume imaging. Nat. Protoc. 14, 1708–1733 (2019).

Generation and characterization of hair-bearing skin organoids from human pluripotent stem cells

推荐阅读