Signaling Networks among Stem Cell Precursors, Transit-Amplifying Progenitors, and their Niche in Developing Hair Follicles

Amélie Rezza; Zichen Wang; Rachel Sennett; Wenlian Qiao; Dongmei Wang; Nicholas Heitman; Ka Wai Mok; Carlos Clavel; Rui Yi; Peter Zandstra; Avi Ma'ayan; Michael Rendl

doi:10.1016/j.celrep.2016.02.078

Signaling Networks among Stem Cell Precursors, Transit-Amplifying Progenitors, and their Niche in Developing Hair Follicles

Amélie Rezza, Zichen Wang, Rachel Sennett, Wenlian Qiao, Dongmei Wang, Nicholas Heitman, Ka Wai Mok, Carlos Clavel, Rui Yi, Peter Zandstra, Avi Ma'ayan, Michael Rendl^*

^*Corresponding author for this work

Pathology

Research output: Contribution to journal › Article › peer-review

138 Scopus citations

Abstract

The hair follicle (HF) is a complex miniorgan that serves as an ideal model system to study stem cell (SC) interactions with the niche during growth and regeneration. Dermal papilla (DP) cells are required for SC activation during the adult hair cycle, but signal exchange between niche and SC precursors/transit-amplifying cell (TAC) progenitors that regulates HF morphogenetic growth is largely unknown. Here we use six transgenic reporters to isolate 14 major skin and HF cell populations. With next-generation RNA sequencing, we characterize their transcriptomes and define unique molecular signatures. SC precursors, TACs, and the DP niche express a plethora of ligands and receptors. Signaling interaction network analysis reveals a bird's-eye view of pathways implicated in epithelial-mesenchymal interactions. Using a systematic tissue-wide approach, this work provides a comprehensive platform, linked to an interactive online database, to identify and further explore the SC/TAC/niche crosstalk regulating HF growth.

Original language	English (US)
Pages (from-to)	3001-3018
Number of pages	18
Journal	Cell reports
Volume	14
Issue number	12
DOIs	https://doi.org/10.1016/j.celrep.2016.02.078
State	Published - Mar 29 2016

Funding

We thank Nicole Dubois for valuable comments on the manuscript and Joseph McCarty for providing the ITGB8 antibody. We also thank the personnel of the Flow Cytometry Core Facility and the Microscopy Shared Resource Facility at ISMMS. A.R. was supported by a fellowship from the Fondation pour la Recherche Médicale and the Prix Claude Rozé/CECED. R.S. was supported by fellowship F30AR065847 from NIH/National Institute of Arthritis and Musculoskeletal and Skin Diseases. A.M. was supported by NIH grants R01GM098316, R01DK088541, U54CA189201, and U54HL127624. M.R. was supported by grants from the NIH/NIAMS (R01AR059143 and R01AR063151) and the New York State Department of Health (NYSTEM-C029574) and by a fellowship from the Irma T. Hirschl Trust.

Keywords

Big data
Dermal papilla
Epithelial-mesenchymal interactions
Hair follicle
Hair growth
Progenitors
Signaling networks
Stem cell niche
Stem cells
Systems biology
Transcriptomics

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.celrep.2016.02.078

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title = "Signaling Networks among Stem Cell Precursors, Transit-Amplifying Progenitors, and their Niche in Developing Hair Follicles",

abstract = "The hair follicle (HF) is a complex miniorgan that serves as an ideal model system to study stem cell (SC) interactions with the niche during growth and regeneration. Dermal papilla (DP) cells are required for SC activation during the adult hair cycle, but signal exchange between niche and SC precursors/transit-amplifying cell (TAC) progenitors that regulates HF morphogenetic growth is largely unknown. Here we use six transgenic reporters to isolate 14 major skin and HF cell populations. With next-generation RNA sequencing, we characterize their transcriptomes and define unique molecular signatures. SC precursors, TACs, and the DP niche express a plethora of ligands and receptors. Signaling interaction network analysis reveals a bird's-eye view of pathways implicated in epithelial-mesenchymal interactions. Using a systematic tissue-wide approach, this work provides a comprehensive platform, linked to an interactive online database, to identify and further explore the SC/TAC/niche crosstalk regulating HF growth.",

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AU - Qiao, Wenlian

AU - Wang, Dongmei

AU - Heitman, Nicholas

AU - Mok, Ka Wai

AU - Clavel, Carlos

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AU - Zandstra, Peter

AU - Ma'ayan, Avi

AU - Rendl, Michael

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N2 - The hair follicle (HF) is a complex miniorgan that serves as an ideal model system to study stem cell (SC) interactions with the niche during growth and regeneration. Dermal papilla (DP) cells are required for SC activation during the adult hair cycle, but signal exchange between niche and SC precursors/transit-amplifying cell (TAC) progenitors that regulates HF morphogenetic growth is largely unknown. Here we use six transgenic reporters to isolate 14 major skin and HF cell populations. With next-generation RNA sequencing, we characterize their transcriptomes and define unique molecular signatures. SC precursors, TACs, and the DP niche express a plethora of ligands and receptors. Signaling interaction network analysis reveals a bird's-eye view of pathways implicated in epithelial-mesenchymal interactions. Using a systematic tissue-wide approach, this work provides a comprehensive platform, linked to an interactive online database, to identify and further explore the SC/TAC/niche crosstalk regulating HF growth.

AB - The hair follicle (HF) is a complex miniorgan that serves as an ideal model system to study stem cell (SC) interactions with the niche during growth and regeneration. Dermal papilla (DP) cells are required for SC activation during the adult hair cycle, but signal exchange between niche and SC precursors/transit-amplifying cell (TAC) progenitors that regulates HF morphogenetic growth is largely unknown. Here we use six transgenic reporters to isolate 14 major skin and HF cell populations. With next-generation RNA sequencing, we characterize their transcriptomes and define unique molecular signatures. SC precursors, TACs, and the DP niche express a plethora of ligands and receptors. Signaling interaction network analysis reveals a bird's-eye view of pathways implicated in epithelial-mesenchymal interactions. Using a systematic tissue-wide approach, this work provides a comprehensive platform, linked to an interactive online database, to identify and further explore the SC/TAC/niche crosstalk regulating HF growth.

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Signaling Networks among Stem Cell Precursors, Transit-Amplifying Progenitors, and their Niche in Developing Hair Follicles

Abstract

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Keywords

ASJC Scopus subject areas

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