Hair follicle epidermal stem cells define a niche for tactile sensation
- RIKEN, Japan
- Nagoya University, Japan
- Shigei Medical Research Institute, Japan
- King's College London, United Kingdom
Abstract
The heterogeneity and compartmentalization of stem cells is a common principle in many epithelia, and is known to function in epithelial maintenance, but its other physiological roles remain elusive. Here we show transcriptional and anatomical contributions of compartmentalized epidermal stem cells (EpSCs) in tactile sensory unit formation in the mouse hair follicle (HF). EpSCs in the follicle upper-bulge, where mechanosensory lanceolate complexes (LCs) innervate, express a unique set of extracellular matrix (ECM) and neurogenesis-related genes. These EpSCs deposit an ECM protein called EGFL6 into the collar matrix, a novel ECM that tightly ensheathes LCs. EGFL6 is required for the proper patterning, touch responses, and av integrin-enrichment of LCs. By maintaining a quiescent original EpSC niche, the old bulge, EpSCs provide anatomically stable HF–LC interfaces, irrespective of the stage of follicle regeneration cycle. Thus, compartmentalized EpSCs provide a niche linking the HF and the nervous system throughout the hair cycle.
Data availability
Fastq files of RNA-seq data have been submitted to NCBI SRA, and these data can be accessed through the BioProject ID: PRJNA342736.All data generated or analysed during this study are included in the Source data files.
Article and author information
Author details
Funding
RIKEN (Intramural grant)
- Hironobu Fujiwara
Japan Society for the Promotion of Science (25122720)
- Hironobu Fujiwara
Uehara Memorial Foundation
- Hironobu Fujiwara
Takeda Science Foundation
- Hironobu Fujiwara
Cosmetology Research Foundation
- Hironobu Fujiwara
Medical Research Council
- Fiona M Watt
Biotechnology and Biological Sciences Research Council
- Fiona M Watt
Wellcome
- Fiona M Watt
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: All animal experiments were conducted and performed in accordance with approved Institutional Animal Care and Use Committee protocols (#A2012-03-12).
Copyright
© 2018, Cheng et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Hair follicle epidermal stem cells define a niche for tactile sensation
eLife 7:e38883.
https://doi.org/10.7554/eLife.38883
Further reading
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- Developmental Biology
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Niches are often found in specific positions in tissues relative to the stem cells they support. Consistency of niche position suggests that placement is important for niche function. However, the complexity of most niches has precluded a thorough understanding of how their proper placement is established. To address this, we investigated the formation of a genetically tractable niche, the Drosophila Posterior Signaling Center (PSC), the assembly of which had not been previously explored. This niche controls hematopoietic progenitors of the lymph gland (LG). PSC cells were previously shown to be specified laterally in the embryo, but ultimately reside dorsally, at the LG posterior. Here, using live-imaging, we show that PSC cells migrate as a tight collective and associate with multiple tissues during their trajectory to the LG posterior. We find that Slit emanating from two extrinsic sources, visceral mesoderm and cardioblasts, is required for the PSC to remain a collective, and for its attachment to cardioblasts during migration. Without proper Slit-Robo signaling, PSC cells disperse, form aberrant contacts, and ultimately fail to reach their stereotypical position near progenitors. Our work characterizes a novel example of niche formation and identifies an extrinsic signaling relay that controls precise niche positioning.
