Stem cells repurpose proliferation to contain a breach in their niche barrier

Abstract
Data availability
Article and author information
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Abstract

Adult stem cells are responsible for life-long tissue maintenance. They reside in and interact with specialized tissue microenvironments (niches). Using murine hair follicle as a model, we show that when junctional perturbations in the niche disrupt barrier function, adjacent stem cells dramatically change their transcriptome independent of bacterial invasion and become capable of directly signaling to and recruiting immune cells. Additionally, these stem cells elevate cell cycle transcripts which reduce their quiescence threshold, enabling them to selectively proliferate within this microenvironment of immune distress cues. However, rather than mobilizing to fuel new tissue regeneration, these ectopically proliferative stem cells remain within their niche to contain the breach. Together, our findings expose a potential communication relay system that operates from the niche to the stem cells to the immune system and back. The repurposing of proliferation by these stem cells patch the breached barrier, stoke the immune response and restore niche integrity.

Data availability

RNA-sequencing data have been deposited in GEO under accession number GSE106767

The following data sets were generated

1. Lay K
2. Yuan S
3. Gur-Cohen S
4. Miao Y
5. Han T
6. Naik S
7. Pasolli HA
8. Larsen SB
9. Elaine Fuchs E
(2018) RNA-sequencing data from Stem cells repurpose proliferation to contain a breach in their niche barrier
Gene Expression Omnibus, GSE106767.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE106767

The following previously published data sets were used

1. Lay K
2. Kume T and Fuchs E
(2016) RNA-seq analysis of hair follicle stem cell transcriptome upon loss of the transcription factor FOXC1
NCBI Gene Expression Omnibus, GSE77256.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi

Article and author information

Author details

Kenneth Lay

Robin Chemers Neustein Laboratory of Mammalian Cell Biology and Development, Howard Hughes Medical Institute, The Rockefeller University, New York, United States

Competing interests
No competing interests declared.
Shaopeng Yuan

Robin Chemers Neustein Laboratory of Mammalian Cell Biology and Development, Howard Hughes Medical Institute, The Rockefeller University, New York, United States

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0001-9554-1325
Shiri Gur-Cohen

Robin Chemers Neustein Laboratory of Mammalian Cell Biology and Development, Howard Hughes Medical Institute, The Rockefeller University, New York, United States

Competing interests
No competing interests declared.
Yuxuan Miao

Robin Chemers Neustein Laboratory of Mammalian Cell Biology and Development, Howard Hughes Medical Institute, The Rockefeller University, New York, United States

Competing interests
No competing interests declared.
Tianxiao Han

Robin Chemers Neustein Laboratory of Mammalian Cell Biology and Development, Howard Hughes Medical Institute, The Rockefeller University, New York, United States

Competing interests
No competing interests declared.
Shruti Naik

Robin Chemers Neustein Laboratory of Mammalian Cell Biology and Development, Howard Hughes Medical Institute, The Rockefeller University, New York, United States

Competing interests
No competing interests declared.
H Amalia Pasolli

Electron Microscopy Shared Resource, Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States

Competing interests
No competing interests declared.
Samantha B Larsen

Robin Chemers Neustein Laboratory of Mammalian Cell Biology and Development, Howard Hughes Medical Institute, The Rockefeller University, New York, United States

Competing interests
No competing interests declared.
Elaine Fuchs

Robin Neustein Laboratory of Mammalian Development and Cell Biology, Howard Hughes Medical Institute, The Rockefeller University, New York, United States

For correspondence
elaine.fuchs@rockefeller.edu

Competing interests
Elaine Fuchs, Reviewing editor, eLife.

"This ORCID iD identifies the author of this article:" 0000-0002-0978-5137

Funding

National Institutes of Health

Elaine Fuchs

L'Oreal USA

Shruti Naik

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 mice were maintained in a facility approved by The Association for Assessment and Accreditation of Laboratory Animal Care (AAALAC), and procedures were performed with protocols approved by Rockefeller University's institutional animal care and use committee (IACUC) members.

Copyright

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.