An Integrated Transcriptome Atlas of Embryonic Hair Follicle Progenitors, Their Niche, and the Developing Skin

Overview

Journal Dev Cell

Publisher Cell Press

Specialties Cell Biology
Reproductive Medicine

Date 2015 Aug 11

PMID 26256211

Citations 111

Authors

Rachel Sennett

Zichen Wang

Amelie Rezza

Laura Grisanti

Nataly Roitershtein

Cristina Sicchio

Ka Wai Mok

Nicholas J Heitman

Carlos Clavel

Avi Maayan

Michael Rendl

Affiliations

Soon will be listed here.

Abstract

Defining the unique molecular features of progenitors and their niche requires a genome-wide, whole-tissue approach with cellular resolution. Here, we co-isolate embryonic hair follicle (HF) placode and dermal condensate cells, precursors of adult HF stem cells and the dermal papilla/sheath niche, along with lineage-related keratinocytes and fibroblasts, Schwann cells, melanocytes, and a population inclusive of all remaining skin cells. With next-generation RNA sequencing, we define gene expression patterns in the context of the entire embryonic skin, and through transcriptome cross-comparisons, we uncover hundreds of enriched genes in cell-type-specific signatures. Axon guidance signaling and many other pathway genes are enriched in multiple signatures, implicating these factors in driving the large-scale cellular rearrangements necessary for HF formation. Finally, we share all data in an interactive, searchable companion website. Our study provides an overarching view of signaling within the entire embryonic skin and captures a molecular snapshot of HF progenitors and their niche.

Citing Articles

-Methyladenosine (mA)-Circular RNA Pappalysin 1 (circPAPPA) from Cashmere Goats: Identification, Regulatory Network and Expression Potentially Regulated by Methylation in Secondary Hair Follicles Within the First Intron of Its Host Gene.

Bai M, Shen J, Fan Y, Xu R, Hui T, Zhu Y Animals (Basel). 2025; 15(4).

PMID: 40003062 PMC: 11851913. DOI: 10.3390/ani15040581.

Combined ADAMTS10 and ADAMTS17 inactivation exacerbates bone shortening and compromises extracellular matrix formation.

Taye N, Karoulias S, Balic Z, Wang L, Willard B, Martin D bioRxiv. 2025; .

PMID: 39896540 PMC: 11785165. DOI: 10.1101/2025.01.23.634616.

Gpr54 deletion accelerates hair cycle and hair regeneration.

Xia W, Wang C, Guo B, Tang Z, Ye X, Dang Y EMBO Rep. 2024; 26(1):200-217.

PMID: 39587329 PMC: 11724127. DOI: 10.1038/s44319-024-00327-y.

A lineage-specific nascent RNA assay unveils principles of gene regulation in tissue biology.

Chovatiya G, Wang A, Versluis P, Bai C, Huang S, DeBerardine M bioRxiv. 2024; .

PMID: 39464031 PMC: 11507779. DOI: 10.1101/2024.10.15.618417.

Dermal Papilla Cells: From Basic Research to Translational Applications.

Zhang H, Qiu X, Liao X Biology (Basel). 2024; 13(10).

PMID: 39452150 PMC: 11504027. DOI: 10.3390/biology13100842.

References

Rezza A, Sennett R, Tanguy M, Clavel C, Rendl M . PDGF signalling in the dermis and in dermal condensates is dispensable for hair follicle induction and formation. Exp Dermatol. 2015; 24(6):468-70. PMC: 4943754. DOI: 10.1111/exd.12672. View

Kanehisa M, Goto S . KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 1999; 28(1):27-30. PMC: 102409. DOI: 10.1093/nar/28.1.27. View

Suzuki K, Yamanishi K, Mori O, Kamikawa M, Andersen B, Kato S . Defective terminal differentiation and hypoplasia of the epidermis in mice lacking the Fgf10 gene. FEBS Lett. 2000; 481(1):53-6. DOI: 10.1016/s0014-5793(00)01968-2. View

Reddy S, Andl T, Bagasra A, Lu M, Epstein D, Morrisey E . Characterization of Wnt gene expression in developing and postnatal hair follicles and identification of Wnt5a as a target of Sonic hedgehog in hair follicle morphogenesis. Mech Dev. 2001; 107(1-2):69-82. DOI: 10.1016/s0925-4773(01)00452-x. View

Millar S . Molecular mechanisms regulating hair follicle development. J Invest Dermatol. 2002; 118(2):216-25. DOI: 10.1046/j.0022-202x.2001.01670.x. View

Laurikkala J, Pispa J, Jung H, Nieminen P, Mikkola M, Wang X . Regulation of hair follicle development by the TNF signal ectodysplasin and its receptor Edar. Development. 2002; 129(10):2541-53. DOI: 10.1242/dev.129.10.2541. View

Andl T, Reddy S, Gaddapara T, Millar S . WNT signals are required for the initiation of hair follicle development. Dev Cell. 2002; 2(5):643-53. DOI: 10.1016/s1534-5807(02)00167-3. View

Jamora C, DasGupta R, Kocieniewski P, Fuchs E . Links between signal transduction, transcription and adhesion in epithelial bud development. Nature. 2003; 422(6929):317-22. PMC: 2424170. DOI: 10.1038/nature01458. View

Tumbar T, Guasch G, Greco V, Blanpain C, Lowry W, Rendl M . Defining the epithelial stem cell niche in skin. Science. 2003; 303(5656):359-63. PMC: 2405920. DOI: 10.1126/science.1092436. View

10.

Morris R, Liu Y, Marles L, Yang Z, Trempus C, Li S . Capturing and profiling adult hair follicle stem cells. Nat Biotechnol. 2004; 22(4):411-7. DOI: 10.1038/nbt950. View

11.

Blanpain C, Lowry W, Geoghegan A, Polak L, Fuchs E . Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell. 2004; 118(5):635-48. DOI: 10.1016/j.cell.2004.08.012. View

12.

Jonsson M, Mark E, Brantsing C, Brandner J, Lindahl A, Asp J . Hash4, a novel human achaete-scute homologue found in fetal skin. Genomics. 2004; 84(5):859-66. DOI: 10.1016/j.ygeno.2004.07.004. View

13.

Philbrick W, Dreyer B, Nakchbandi I, Karaplis A . Parathyroid hormone-related protein is required for tooth eruption. Proc Natl Acad Sci U S A. 1998; 95(20):11846-51. PMC: 21728. DOI: 10.1073/pnas.95.20.11846. View

14.

St-Jacques B, Dassule H, Karavanova I, Botchkarev V, Li J, Danielian P . Sonic hedgehog signaling is essential for hair development. Curr Biol. 1998; 8(19):1058-68. DOI: 10.1016/s0960-9822(98)70443-9. View

15.

Chiang C, Swan R, Grachtchouk M, Bolinger M, Litingtung Y, Robertson E . Essential role for Sonic hedgehog during hair follicle morphogenesis. Dev Biol. 1999; 205(1):1-9. DOI: 10.1006/dbio.1998.9103. View

16.

Botchkarev V, Sharov A . BMP signaling in the control of skin development and hair follicle growth. Differentiation. 2004; 72(9-10):512-26. DOI: 10.1111/j.1432-0436.2004.07209005.x. View

17.

Ellis P, Fagan B, Magness S, Hutton S, Taranova O, Hayashi S . SOX2, a persistent marker for multipotential neural stem cells derived from embryonic stem cells, the embryo or the adult. Dev Neurosci. 2005; 26(2-4):148-65. DOI: 10.1159/000082134. View

18.

Jessen K, Mirsky R . The origin and development of glial cells in peripheral nerves. Nat Rev Neurosci. 2005; 6(9):671-82. DOI: 10.1038/nrn1746. View

19.

Rendl M, Lewis L, Fuchs E . Molecular dissection of mesenchymal-epithelial interactions in the hair follicle. PLoS Biol. 2005; 3(11):e331. PMC: 1216328. DOI: 10.1371/journal.pbio.0030331. View

20.

Levy V, Lindon C, Harfe B, Morgan B . Distinct stem cell populations regenerate the follicle and interfollicular epidermis. Dev Cell. 2005; 9(6):855-61. DOI: 10.1016/j.devcel.2005.11.003. View