Estrogen Regulates the Satellite Cell Compartment in Females

Summary: Skeletal muscle mass, strength, and regenerative capacity decline with age, with many measures showing a greater deterioration in females around the time estrogen levels decrease at menopause. Here, we show that estrogen deficiency severely compromises the maintenance of muscle stem cells (...

Full description

Bibliographic Details
Main Authors: Brittany C. Collins, Robert W. Arpke, Alexie A. Larson, Cory W. Baumann, Ning Xie, Christine A. Cabelka, Nardina L. Nash, Hanna-Kaarina Juppi, Eija K. Laakkonen, Sarianna Sipilä, Vuokko Kovanen, Espen E. Spangenburg, Michael Kyba, Dawn A. Lowe
Format: Article
Language:English
Published: Elsevier 2019-07-01
Series:Cell Reports
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124719307910
_version_ 1818946825756868608
author Brittany C. Collins
Robert W. Arpke
Alexie A. Larson
Cory W. Baumann
Ning Xie
Christine A. Cabelka
Nardina L. Nash
Hanna-Kaarina Juppi
Eija K. Laakkonen
Sarianna Sipilä
Vuokko Kovanen
Espen E. Spangenburg
Michael Kyba
Dawn A. Lowe
author_facet Brittany C. Collins
Robert W. Arpke
Alexie A. Larson
Cory W. Baumann
Ning Xie
Christine A. Cabelka
Nardina L. Nash
Hanna-Kaarina Juppi
Eija K. Laakkonen
Sarianna Sipilä
Vuokko Kovanen
Espen E. Spangenburg
Michael Kyba
Dawn A. Lowe
author_sort Brittany C. Collins
collection DOAJ
description Summary: Skeletal muscle mass, strength, and regenerative capacity decline with age, with many measures showing a greater deterioration in females around the time estrogen levels decrease at menopause. Here, we show that estrogen deficiency severely compromises the maintenance of muscle stem cells (i.e., satellite cells) as well as impairs self-renewal and differentiation into muscle fibers. Mechanistically, by hormone replacement, use of a selective estrogen-receptor modulator (bazedoxifene), and conditional estrogen receptor knockout, we implicate 17β-estradiol and satellite cell expression of estrogen receptor α and show that estrogen signaling through this receptor is necessary to prevent apoptosis of satellite cells. Early data from a biopsy study of women who transitioned from peri- to post-menopause are consistent with the loss of satellite cells coincident with the decline in estradiol in humans. Together, these results demonstrate an important role for estrogen in satellite cell maintenance and muscle regeneration in females. : Collins et al. show the loss of estrogen in female mice and post-menopausal women leads to a decrease in skeletal muscle stem cells. Using muscle stem cell-specific mutants, it was demonstrated that ERα is necessary for satellite cell maintenance, self-renewal, and protection from apoptosis, thereby promoting optimal muscle regeneration. Keywords: estradiol, muscle stem cells, ovarian hormones, quiescence, skeletal muscle
first_indexed 2024-12-20T08:21:10Z
format Article
id doaj.art-37ec4ce13b9944809954e964e9bbeabf
institution Directory Open Access Journal
issn 2211-1247
language English
last_indexed 2024-12-20T08:21:10Z
publishDate 2019-07-01
publisher Elsevier
record_format Article
series Cell Reports
spelling doaj.art-37ec4ce13b9944809954e964e9bbeabf2022-12-21T19:47:00ZengElsevierCell Reports2211-12472019-07-01282368381.e6Estrogen Regulates the Satellite Cell Compartment in FemalesBrittany C. Collins0Robert W. Arpke1Alexie A. Larson2Cory W. Baumann3Ning Xie4Christine A. Cabelka5Nardina L. Nash6Hanna-Kaarina Juppi7Eija K. Laakkonen8Sarianna Sipilä9Vuokko Kovanen10Espen E. Spangenburg11Michael Kyba12Dawn A. Lowe13Divisions of Rehabilitation Science and Physical Therapy, Department of Rehabilitation Medicine, Medical School, University of Minnesota, Minneapolis, MN, USALillehei Heart Institute and Department of Pediatrics, Medical School, University of Minnesota, Minneapolis, MN, USADepartment of Integrative Biology and Physiology, Medical School, University of Minnesota, Minneapolis, MN, USADivisions of Rehabilitation Science and Physical Therapy, Department of Rehabilitation Medicine, Medical School, University of Minnesota, Minneapolis, MN, USALillehei Heart Institute and Department of Pediatrics, Medical School, University of Minnesota, Minneapolis, MN, USADivisions of Rehabilitation Science and Physical Therapy, Department of Rehabilitation Medicine, Medical School, University of Minnesota, Minneapolis, MN, USADivisions of Rehabilitation Science and Physical Therapy, Department of Rehabilitation Medicine, Medical School, University of Minnesota, Minneapolis, MN, USAGerontology Research Center, Faculty of Sport and Health Sciences, University of Jyväskylä, Jyväskylä, FinlandGerontology Research Center, Faculty of Sport and Health Sciences, University of Jyväskylä, Jyväskylä, FinlandGerontology Research Center, Faculty of Sport and Health Sciences, University of Jyväskylä, Jyväskylä, FinlandGerontology Research Center, Faculty of Sport and Health Sciences, University of Jyväskylä, Jyväskylä, FinlandEast Carolina Diabetes and Obesity Institute, Department of Physiology, Brody School of Medicine, East Carolina University, Greenville, NC, USALillehei Heart Institute and Department of Pediatrics, Medical School, University of Minnesota, Minneapolis, MN, USADivisions of Rehabilitation Science and Physical Therapy, Department of Rehabilitation Medicine, Medical School, University of Minnesota, Minneapolis, MN, USA; Corresponding authorSummary: Skeletal muscle mass, strength, and regenerative capacity decline with age, with many measures showing a greater deterioration in females around the time estrogen levels decrease at menopause. Here, we show that estrogen deficiency severely compromises the maintenance of muscle stem cells (i.e., satellite cells) as well as impairs self-renewal and differentiation into muscle fibers. Mechanistically, by hormone replacement, use of a selective estrogen-receptor modulator (bazedoxifene), and conditional estrogen receptor knockout, we implicate 17β-estradiol and satellite cell expression of estrogen receptor α and show that estrogen signaling through this receptor is necessary to prevent apoptosis of satellite cells. Early data from a biopsy study of women who transitioned from peri- to post-menopause are consistent with the loss of satellite cells coincident with the decline in estradiol in humans. Together, these results demonstrate an important role for estrogen in satellite cell maintenance and muscle regeneration in females. : Collins et al. show the loss of estrogen in female mice and post-menopausal women leads to a decrease in skeletal muscle stem cells. Using muscle stem cell-specific mutants, it was demonstrated that ERα is necessary for satellite cell maintenance, self-renewal, and protection from apoptosis, thereby promoting optimal muscle regeneration. Keywords: estradiol, muscle stem cells, ovarian hormones, quiescence, skeletal musclehttp://www.sciencedirect.com/science/article/pii/S2211124719307910
spellingShingle Brittany C. Collins
Robert W. Arpke
Alexie A. Larson
Cory W. Baumann
Ning Xie
Christine A. Cabelka
Nardina L. Nash
Hanna-Kaarina Juppi
Eija K. Laakkonen
Sarianna Sipilä
Vuokko Kovanen
Espen E. Spangenburg
Michael Kyba
Dawn A. Lowe
Estrogen Regulates the Satellite Cell Compartment in Females
Cell Reports
title Estrogen Regulates the Satellite Cell Compartment in Females
title_full Estrogen Regulates the Satellite Cell Compartment in Females
title_fullStr Estrogen Regulates the Satellite Cell Compartment in Females
title_full_unstemmed Estrogen Regulates the Satellite Cell Compartment in Females
title_short Estrogen Regulates the Satellite Cell Compartment in Females
title_sort estrogen regulates the satellite cell compartment in females
url http://www.sciencedirect.com/science/article/pii/S2211124719307910
work_keys_str_mv AT brittanyccollins estrogenregulatesthesatellitecellcompartmentinfemales
AT robertwarpke estrogenregulatesthesatellitecellcompartmentinfemales
AT alexiealarson estrogenregulatesthesatellitecellcompartmentinfemales
AT corywbaumann estrogenregulatesthesatellitecellcompartmentinfemales
AT ningxie estrogenregulatesthesatellitecellcompartmentinfemales
AT christineacabelka estrogenregulatesthesatellitecellcompartmentinfemales
AT nardinalnash estrogenregulatesthesatellitecellcompartmentinfemales
AT hannakaarinajuppi estrogenregulatesthesatellitecellcompartmentinfemales
AT eijaklaakkonen estrogenregulatesthesatellitecellcompartmentinfemales
AT sariannasipila estrogenregulatesthesatellitecellcompartmentinfemales
AT vuokkokovanen estrogenregulatesthesatellitecellcompartmentinfemales
AT espenespangenburg estrogenregulatesthesatellitecellcompartmentinfemales
AT michaelkyba estrogenregulatesthesatellitecellcompartmentinfemales
AT dawnalowe estrogenregulatesthesatellitecellcompartmentinfemales