Single cell analysis of transcriptome and open chromatin reveals the dynamics of hair follicle stem cell aging

Aging is defined as the functional decline of tissues and organisms, leading to many human conditions, such as cancer, neurodegenerative diseases, and hair loss. Although stem cell exhaustion is widely recognized as a hallmark of aging, our understanding of cell state changes–specifically, the dynam...

Full description

Bibliographic Details
Main Authors: Chi Zhang, Dongmei Wang, Robin Dowell, Rui Yi
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-07-01
Series:Frontiers in Aging
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fragi.2023.1192149/full
_version_ 1797789226645848064
author Chi Zhang
Dongmei Wang
Dongmei Wang
Dongmei Wang
Robin Dowell
Rui Yi
Rui Yi
Rui Yi
author_facet Chi Zhang
Dongmei Wang
Dongmei Wang
Dongmei Wang
Robin Dowell
Rui Yi
Rui Yi
Rui Yi
author_sort Chi Zhang
collection DOAJ
description Aging is defined as the functional decline of tissues and organisms, leading to many human conditions, such as cancer, neurodegenerative diseases, and hair loss. Although stem cell exhaustion is widely recognized as a hallmark of aging, our understanding of cell state changes–specifically, the dynamics of the transcriptome and open chromatin landscape, and their relationship with aging–remains incomplete. Here we present a longitudinal, single-cell atlas of the transcriptome and open chromatin landscape for epithelia cells of the skin across various hair cycle stages and ages in mice. Our findings reveal fluctuating hair follicle stem cell (HF-SC) states, some of which are associated with the progression of the hair cycle during aging. Conversely, inner bulge niche cells display a more linear progression, seemingly less affected by the hair cycle. Further analysis of the open chromatin landscape, determined by single-cell Assay for Transposase-Accessible Chromatin (ATAC) sequencing, demonstrates that reduced open chromatin regions in HF-SCs are associated with differentiation, whereas gained open chromatin regions in HF-SCs are linked to the transcriptional control of quiescence. These findings enhance our understanding of the transcriptional dynamics in HF-SC aging and lay the molecular groundwork for investigating and potentially reversing the aging process in future experimental studies.
first_indexed 2024-03-13T01:47:42Z
format Article
id doaj.art-8c963f1371584994b519ba1cce749750
institution Directory Open Access Journal
issn 2673-6217
language English
last_indexed 2024-03-13T01:47:42Z
publishDate 2023-07-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Aging
spelling doaj.art-8c963f1371584994b519ba1cce7497502023-07-03T06:35:59ZengFrontiers Media S.A.Frontiers in Aging2673-62172023-07-01410.3389/fragi.2023.11921491192149Single cell analysis of transcriptome and open chromatin reveals the dynamics of hair follicle stem cell agingChi Zhang0Dongmei Wang1Dongmei Wang2Dongmei Wang3Robin Dowell4Rui Yi5Rui Yi6Rui Yi7Department of Pathology, Northwestern University Feinberg School of Medicine, Chicago, IL, United StatesDepartment of Pathology, Northwestern University Feinberg School of Medicine, Chicago, IL, United StatesDepartment of Dermatology, Northwestern University Feinberg School of Medicine, Chicago, IL, United StatesRobert H. Lurie Comprehensive Cancer Center, Northwestern University Feinberg School of Medicine, Chicago, IL, United StatesBioFrontiers Institute, University of Colorado Boulder, Boulder, CO, United StatesDepartment of Pathology, Northwestern University Feinberg School of Medicine, Chicago, IL, United StatesDepartment of Dermatology, Northwestern University Feinberg School of Medicine, Chicago, IL, United StatesRobert H. Lurie Comprehensive Cancer Center, Northwestern University Feinberg School of Medicine, Chicago, IL, United StatesAging is defined as the functional decline of tissues and organisms, leading to many human conditions, such as cancer, neurodegenerative diseases, and hair loss. Although stem cell exhaustion is widely recognized as a hallmark of aging, our understanding of cell state changes–specifically, the dynamics of the transcriptome and open chromatin landscape, and their relationship with aging–remains incomplete. Here we present a longitudinal, single-cell atlas of the transcriptome and open chromatin landscape for epithelia cells of the skin across various hair cycle stages and ages in mice. Our findings reveal fluctuating hair follicle stem cell (HF-SC) states, some of which are associated with the progression of the hair cycle during aging. Conversely, inner bulge niche cells display a more linear progression, seemingly less affected by the hair cycle. Further analysis of the open chromatin landscape, determined by single-cell Assay for Transposase-Accessible Chromatin (ATAC) sequencing, demonstrates that reduced open chromatin regions in HF-SCs are associated with differentiation, whereas gained open chromatin regions in HF-SCs are linked to the transcriptional control of quiescence. These findings enhance our understanding of the transcriptional dynamics in HF-SC aging and lay the molecular groundwork for investigating and potentially reversing the aging process in future experimental studies.https://www.frontiersin.org/articles/10.3389/fragi.2023.1192149/fullhair follicle stem cellstem cell exhaustionquiescencecell adhesionsingle cell genomicsscRNAseq
spellingShingle Chi Zhang
Dongmei Wang
Dongmei Wang
Dongmei Wang
Robin Dowell
Rui Yi
Rui Yi
Rui Yi
Single cell analysis of transcriptome and open chromatin reveals the dynamics of hair follicle stem cell aging
Frontiers in Aging
hair follicle stem cell
stem cell exhaustion
quiescence
cell adhesion
single cell genomics
scRNAseq
title Single cell analysis of transcriptome and open chromatin reveals the dynamics of hair follicle stem cell aging
title_full Single cell analysis of transcriptome and open chromatin reveals the dynamics of hair follicle stem cell aging
title_fullStr Single cell analysis of transcriptome and open chromatin reveals the dynamics of hair follicle stem cell aging
title_full_unstemmed Single cell analysis of transcriptome and open chromatin reveals the dynamics of hair follicle stem cell aging
title_short Single cell analysis of transcriptome and open chromatin reveals the dynamics of hair follicle stem cell aging
title_sort single cell analysis of transcriptome and open chromatin reveals the dynamics of hair follicle stem cell aging
topic hair follicle stem cell
stem cell exhaustion
quiescence
cell adhesion
single cell genomics
scRNAseq
url https://www.frontiersin.org/articles/10.3389/fragi.2023.1192149/full
work_keys_str_mv AT chizhang singlecellanalysisoftranscriptomeandopenchromatinrevealsthedynamicsofhairfolliclestemcellaging
AT dongmeiwang singlecellanalysisoftranscriptomeandopenchromatinrevealsthedynamicsofhairfolliclestemcellaging
AT dongmeiwang singlecellanalysisoftranscriptomeandopenchromatinrevealsthedynamicsofhairfolliclestemcellaging
AT dongmeiwang singlecellanalysisoftranscriptomeandopenchromatinrevealsthedynamicsofhairfolliclestemcellaging
AT robindowell singlecellanalysisoftranscriptomeandopenchromatinrevealsthedynamicsofhairfolliclestemcellaging
AT ruiyi singlecellanalysisoftranscriptomeandopenchromatinrevealsthedynamicsofhairfolliclestemcellaging
AT ruiyi singlecellanalysisoftranscriptomeandopenchromatinrevealsthedynamicsofhairfolliclestemcellaging
AT ruiyi singlecellanalysisoftranscriptomeandopenchromatinrevealsthedynamicsofhairfolliclestemcellaging