SIRT1 regulates macrophage self‐renewal

Mature differentiated macrophages can self‐maintain by local proliferation in tissues and can be extensively expanded in culture under specific conditions, but the mechanisms of this phenomenon remain only partially defined. Here, we show that SIRT1, an evolutionary conserved regulator of life span,...

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Published inThe EMBO journal Vol. 36; no. 16; pp. 2353 - 2372
Main Authors Imperatore, Francesco, Maurizio, Julien, Vargas Aguilar, Stephanie, Busch, Clara J, Favret, Jérémy, Kowenz‐Leutz, Elisabeth, Cathou, Wilfried, Gentek, Rebecca, Perrin, Pierre, Leutz, Achim, Berruyer, Carole, Sieweke, Michael H
Format Journal Article
LanguageEnglish
Published England Blackwell Publishing Ltd 15.08.2017
EMBO Press
John Wiley and Sons Inc
Subjects
Animals
Bone marrow
Cell culture
Cell Cycle
cell cycle regulation
Cell Proliferation
Cell Self Renewal
Clonal deletion
CRISPR
Deactivation
Differentiation
Evolutionary conservation
FOXO1 protein
Gene Expression
Gene Knockdown Techniques
Gene Knockout Techniques
Genes
Homology
Immunology
In vitro methods and tests
Inactivation
Inhibition
Life Sciences
Life span
Longevity
macrophage
Macrophages
Macrophages - physiology
Mice
Myc protein
Nicotinamide
Peritoneum
Pharmacology
replicative life span
self‐renewal
SIRT1 protein
Sirtuin 1 - genetics
Sirtuin 1 - metabolism
sirtuins
Steady state
Stress response
Yeast
Yeasts
self‐renewal
macrophage
cell cycle regulation
sirtuins
replicative life span
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Abstract Mature differentiated macrophages can self‐maintain by local proliferation in tissues and can be extensively expanded in culture under specific conditions, but the mechanisms of this phenomenon remain only partially defined. Here, we show that SIRT1, an evolutionary conserved regulator of life span, positively affects macrophage self‐renewal ability in vitro and in vivo. Overexpression of SIRT1 during bone marrow‐derived macrophage differentiation increased their proliferative capacity. Conversely, decrease of SIRT1 expression by shRNA inactivation, CRISPR/Cas9 mediated deletion and pharmacological inhibition restricted macrophage self‐renewal in culture. Furthermore, pharmacological SIRT1 inhibition in vivo reduced steady state and cytokine‐induced proliferation of alveolar and peritoneal macrophages. Mechanistically, SIRT1 inhibition negatively regulated G1/S transition, cell cycle progression and a network of self‐renewal genes. This included inhibition of E2F1 and Myc and concomitant activation of FoxO1, SIRT1 targets mediating cell cycle progression and stress response, respectively. Our findings indicate that SIRT1 is a key regulator of macrophage self‐renewal that integrates cell cycle and longevity pathways. This suggests that macrophage self‐renewal might be a relevant parameter of ageing. Synopsis Sirtuin1 (SIRT1), a mammalian homolog of yeast Silent Information Regulator 2 (Sir2) and evolutionary conserved regulator of life span, positively affects self‐renewal ability of macrophages in vitro and in vivo. SIRT1 is a key regulator of macrophage self‐renewal that integrates cell cycle and longevity pathways. Overexpression of SIRT1 in bone‐marrow derived macrophages increases their proliferative capacity. Decrease of SIRT1 expression by shRNA inactivation, CRISPR/Cas9 mediated deletion and pharmacological inhibition by nicotinamide or inauhzin, restricts macrophage self‐renewal. SIRT1 inhibition limits alveolar and peritoneal macrophages proliferation in vivo. In macrophages, SIRT1 is required for cell cycle progression and self renewal gene activity, like E2F1 and Myc, but inhibits stress response genes like FOXO1. The life span regulator SIRT1 controls a transcriptional network for macrophage cell cycle progression and stress responses, implying macrophage self‐renewal as a potential parameter of aging.
AbstractList Mature differentiated macrophages can self-maintain by local proliferation in tissues and can be extensively expanded in culture under specific conditions, but the mechanisms of this phenomenon remain only partially defined. Here, we show that SIRT1, an evolutionary conserved regulator of life span, positively affects macrophage self-renewal ability in vitro and in vivo. Overexpression of SIRT1 during bone marrow-derived macrophage differentiation increased their proliferative capacity. Conversely, decrease of SIRT1 expression by shRNA inactivation, CRISPR/Cas9 mediated deletion and pharmacological inhibition restricted macrophage self-renewal in culture. Furthermore, pharmacological SIRT1 inhibition in vivo reduced steady state and cytokine-induced proliferation of alveolar and peritoneal macrophages. Mechanistically, SIRT1 inhibition negatively regulated G1/S transition, cell cycle progression and a network of self-renewal genes. This included inhibition of E2F1 and Myc and concomitant activation of FoxO1, SIRT1 targets mediating cell cycle progression and stress response, respectively. Our findings indicate that SIRT1 is a key regulator of macrophage self-renewal that integrates cell cycle and longevity pathways. This suggests that macrophage self-renewal might be a relevant parameter of ageing. Synopsis Sirtuin1 (SIRT1), a mammalian homolog of yeast Silent Information Regulator 2 (Sir2) and evolutionary conserved regulator of life span, positively affects self-renewal ability of macrophages in vitro and in vivo. SIRT1 is a key regulator of macrophage self-renewal that integrates cell cycle and longevity pathways. Overexpression of SIRT1 in bone-marrow derived macrophages increases their proliferative capacity. Decrease of SIRT1 expression by shRNA inactivation, CRISPR/Cas9 mediated deletion and pharmacological inhibition by nicotinamide or inauhzin, restricts macrophage self-renewal. SIRT1 inhibition limits alveolar and peritoneal macrophages proliferation in vivo. In macrophages, SIRT1 is required for cell cycle progression and self renewal gene activity, like E2F1 and Myc, but inhibits stress response genes like FOXO1.
Mature differentiated macrophages can self-maintain by local proliferation in tissues and can be extensively expanded in culture under specific conditions, but the mechanisms of this phenomenon remain only partially defined. Here, we show that SIRT1, an evolutionary conserved regulator of life span, positively affects macrophage self-renewal ability and Overexpression of SIRT1 during bone marrow-derived macrophage differentiation increased their proliferative capacity. Conversely, decrease of SIRT1 expression by shRNA inactivation, CRISPR/Cas9 mediated deletion and pharmacological inhibition restricted macrophage self-renewal in culture. Furthermore, pharmacological SIRT1 inhibition reduced steady state and cytokine-induced proliferation of alveolar and peritoneal macrophages. Mechanistically, SIRT1 inhibition negatively regulated G1/S transition, cell cycle progression and a network of self-renewal genes. This included inhibition of E2F1 and Myc and concomitant activation of FoxO1, SIRT1 targets mediating cell cycle progression and stress response, respectively. Our findings indicate that SIRT1 is a key regulator of macrophage self-renewal that integrates cell cycle and longevity pathways. This suggests that macrophage self-renewal might be a relevant parameter of ageing.
Mature differentiated macrophages can self-maintain by local proliferation in tissues and can be extensively expanded in culture under specific conditions, but the mechanisms of this phenomenon remain only partially defined. Here, we show that SIRT1, an evolutionary conserved regulator of life span, positively affects macrophage self-renewal ability in vitro and in vivo. Overexpression of SIRT1 during bone marrow-derived macrophage differentiation increased their proliferative capacity. Conversely, decrease of SIRT1 expression by shRNA inactivation, CRISPR/Cas9 mediated deletion and pharmacological inhibition restricted macrophage self-renewal in culture. Furthermore, pharmacological SIRT1 inhibition in vivo reduced steady state and cytokine-induced proliferation of alveolar and peritoneal macrophages. Mechanistically, SIRT1 inhibition negatively regulated G1/S transition, cell cycle progression and a network of self-renewal genes. This included inhibition of E2F1 and Myc and concomitant activation of FoxO1, SIRT1 targets mediating cell cycle progression and stress response, respectively. Our findings indicate that SIRT1 is a key regulator of macrophage self-renewal that integrates cell cycle and longevity pathways. This suggests that macrophage self-renewal might be a relevant parameter of ageing.
Mature differentiated macrophages can self‐maintain by local proliferation in tissues and can be extensively expanded in culture under specific conditions, but the mechanisms of this phenomenon remain only partially defined. Here, we show that SIRT1, an evolutionary conserved regulator of life span, positively affects macrophage self‐renewal ability in vitro and in vivo . Overexpression of SIRT1 during bone marrow‐derived macrophage differentiation increased their proliferative capacity. Conversely, decrease of SIRT1 expression by shRNA inactivation, CRISPR/Cas9 mediated deletion and pharmacological inhibition restricted macrophage self‐renewal in culture. Furthermore, pharmacological SIRT1 inhibition in vivo reduced steady state and cytokine‐induced proliferation of alveolar and peritoneal macrophages. Mechanistically, SIRT1 inhibition negatively regulated G1/S transition, cell cycle progression and a network of self‐renewal genes. This included inhibition of E2F1 and Myc and concomitant activation of FoxO1, SIRT1 targets mediating cell cycle progression and stress response, respectively. Our findings indicate that SIRT1 is a key regulator of macrophage self‐renewal that integrates cell cycle and longevity pathways. This suggests that macrophage self‐renewal might be a relevant parameter of ageing.
Mature differentiated macrophages can self‐maintain by local proliferation in tissues and can be extensively expanded in culture under specific conditions, but the mechanisms of this phenomenon remain only partially defined. Here, we show that SIRT1, an evolutionary conserved regulator of life span, positively affects macrophage self‐renewal ability in vitro and in vivo. Overexpression of SIRT1 during bone marrow‐derived macrophage differentiation increased their proliferative capacity. Conversely, decrease of SIRT1 expression by shRNA inactivation, CRISPR/Cas9 mediated deletion and pharmacological inhibition restricted macrophage self‐renewal in culture. Furthermore, pharmacological SIRT1 inhibition in vivo reduced steady state and cytokine‐induced proliferation of alveolar and peritoneal macrophages. Mechanistically, SIRT1 inhibition negatively regulated G1/S transition, cell cycle progression and a network of self‐renewal genes. This included inhibition of E2F1 and Myc and concomitant activation of FoxO1, SIRT1 targets mediating cell cycle progression and stress response, respectively. Our findings indicate that SIRT1 is a key regulator of macrophage self‐renewal that integrates cell cycle and longevity pathways. This suggests that macrophage self‐renewal might be a relevant parameter of ageing. Synopsis Sirtuin1 (SIRT1), a mammalian homolog of yeast Silent Information Regulator 2 (Sir2) and evolutionary conserved regulator of life span, positively affects self‐renewal ability of macrophages in vitro and in vivo. SIRT1 is a key regulator of macrophage self‐renewal that integrates cell cycle and longevity pathways. Overexpression of SIRT1 in bone‐marrow derived macrophages increases their proliferative capacity. Decrease of SIRT1 expression by shRNA inactivation, CRISPR/Cas9 mediated deletion and pharmacological inhibition by nicotinamide or inauhzin, restricts macrophage self‐renewal. SIRT1 inhibition limits alveolar and peritoneal macrophages proliferation in vivo. In macrophages, SIRT1 is required for cell cycle progression and self renewal gene activity, like E2F1 and Myc, but inhibits stress response genes like FOXO1. The life span regulator SIRT1 controls a transcriptional network for macrophage cell cycle progression and stress responses, implying macrophage self‐renewal as a potential parameter of aging.
Author Favret, Jérémy
Kowenz‐Leutz, Elisabeth
Vargas Aguilar, Stephanie
Gentek, Rebecca
Imperatore, Francesco
Perrin, Pierre
Sieweke, Michael H
Cathou, Wilfried
Leutz, Achim
Berruyer, Carole
Maurizio, Julien
Busch, Clara J
AuthorAffiliation 1 Aix Marseille Université CNRS, INSERM, CIML Marseille France
2 Max‐Delbrück‐Centrum für Molekulare Medizin in der Helmholtzgemeinschaft (MDC) Berlin Germany
AuthorAffiliation_xml – name: 1 Aix Marseille Université CNRS, INSERM, CIML Marseille France
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  organization: Max‐Delbrück‐Centrum für Molekulare Medizin in der Helmholtzgemeinschaft (MDC)
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  organization: Max‐Delbrück‐Centrum für Molekulare Medizin in der Helmholtzgemeinschaft (MDC)
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  givenname: Jérémy
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  orcidid: 0000-0002-3228-9537
  surname: Sieweke
  fullname: Sieweke, Michael H
  email: sieweke@ciml.univ-mrs.fr
  organization: Max‐Delbrück‐Centrum für Molekulare Medizin in der Helmholtzgemeinschaft (MDC)
BackLink https://www.ncbi.nlm.nih.gov/pubmed/28701484$$D View this record in MEDLINE/PubMed
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Issue 16
Keywords self‐renewal
macrophage
cell cycle regulation
sirtuins
replicative life span
Language English
License 2017 The Authors.
Distributed under a Creative Commons Attribution 4.0 International License: http://creativecommons.org/licenses/by/4.0
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PMCID: PMC5556267
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Snippet Mature differentiated macrophages can self‐maintain by local proliferation in tissues and can be extensively expanded in culture under specific conditions, but...
Mature differentiated macrophages can self-maintain by local proliferation in tissues and can be extensively expanded in culture under specific conditions, but...
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SubjectTerms Animals
Bone marrow
Cell culture
Cell Cycle
cell cycle regulation
Cell Proliferation
Cell Self Renewal
Clonal deletion
CRISPR
Deactivation
Differentiation
Evolutionary conservation
FOXO1 protein
Gene Expression
Gene Knockdown Techniques
Gene Knockout Techniques
Genes
Homology
Immunology
In vitro methods and tests
Inactivation
Inhibition
Life Sciences
Life span
Longevity
macrophage
Macrophages
Macrophages - physiology
Mice
Myc protein
Nicotinamide
Peritoneum
Pharmacology
replicative life span
self‐renewal
SIRT1 protein
Sirtuin 1 - genetics
Sirtuin 1 - metabolism
sirtuins
Steady state
Stress response
Yeast
Yeasts
Title SIRT1 regulates macrophage self‐renewal
URI https://onlinelibrary.wiley.com/doi/abs/10.15252%2Fembj.201695737
https://www.ncbi.nlm.nih.gov/pubmed/28701484
https://www.proquest.com/docview/1928613220/abstract/
https://search.proquest.com/docview/1918852727
https://amu.hal.science/hal-01765090
https://pubmed.ncbi.nlm.nih.gov/PMC5556267
Volume 36
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