Neutrophils induce paracrine telomere dysfunction and senescence in ROS-dependent manner.


Journal

The EMBO journal
ISSN: 1460-2075
Titre abrégé: EMBO J
Pays: England
ID NLM: 8208664

Informations de publication

Date de publication:
03 05 2021
Historique:
revised: 09 02 2021
received: 24 06 2020
accepted: 15 02 2021
pubmed: 26 3 2021
medline: 5 11 2021
entrez: 25 3 2021
Statut: ppublish

Résumé

Cellular senescence is characterized by an irreversible cell cycle arrest as well as a pro-inflammatory phenotype, thought to contribute to aging and age-related diseases. Neutrophils have essential roles in inflammatory responses; however, in certain contexts their abundance is associated with a number of age-related diseases, including liver disease. The relationship between neutrophils and cellular senescence is not well understood. Here, we show that telomeres in non-immune cells are highly susceptible to oxidative damage caused by neighboring neutrophils. Neutrophils cause telomere dysfunction both in vitro and ex vivo in a ROS-dependent manner. In a mouse model of acute liver injury, depletion of neutrophils reduces telomere dysfunction and senescence. Finally, we show that senescent cells mediate the recruitment of neutrophils to the aged liver and propose that this may be a mechanism by which senescence spreads to surrounding cells. Our results suggest that interventions that counteract neutrophil-induced senescence may be beneficial during aging and age-related disease.

Identifiants

pubmed: 33764576
doi: 10.15252/embj.2020106048
pmc: PMC8090854
doi:

Substances chimiques

Reactive Oxygen Species 0
Carbon Tetrachloride CL2T97X0V0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e106048

Subventions

Organisme : Medical Research Council
ID : MR/K001949/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : G0900535
Pays : United Kingdom
Organisme : NIA NIH HHS
ID : R01 AG050582
Pays : United States
Organisme : NIA NIH HHS
ID : R37 AG013925
Pays : United States
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/K017314/1
Pays : United Kingdom
Organisme : NIA NIH HHS
ID : R01 AG068182
Pays : United States
Organisme : Medical Research Council
ID : MR/K0019494/1
Pays : United Kingdom
Organisme : Cancer Research UK
ID : 26813
Pays : United Kingdom
Organisme : NIA NIH HHS
ID : T32 AG049672
Pays : United States
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/L502066/1
Pays : United Kingdom
Organisme : NIA NIH HHS
ID : P01 AG062413
Pays : United States
Organisme : National Centre for the Replacement, Refinement and Reduction of Animals in Research
ID : NC/K000748/1
Pays : United Kingdom
Organisme : Cancer Research UK
ID : C18342/A23390
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/R023026/1
Pays : United Kingdom
Organisme : NIA NIH HHS
ID : R01 AG068048
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK084567
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

© 2021 The Authors. Published under the terms of the CC BY 4.0 license.

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Auteurs

Anthony Lagnado (A)

Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, USA.
Robert and Arlene Kogod Center on Aging, Mayo Clinic, Rochester, MN, USA.

Jack Leslie (J)

Newcastle Fibrosis Research Group, Biosciences Institute, Newcastle University, Newcastle upon Tyne, UK.

Marie-Helene Ruchaud-Sparagano (MH)

Translational Research Institute, Newcastle University, Newcastle upon Tyne, UK.

Stella Victorelli (S)

Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, USA.
Robert and Arlene Kogod Center on Aging, Mayo Clinic, Rochester, MN, USA.

Petra Hirsova (P)

Division of Gastroenterology and Hepatology, Mayo Clinic, Rochester, MN, USA.

Mikolaj Ogrodnik (M)

Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, USA.
Robert and Arlene Kogod Center on Aging, Mayo Clinic, Rochester, MN, USA.

Amy L Collins (AL)

Newcastle Fibrosis Research Group, Biosciences Institute, Newcastle University, Newcastle upon Tyne, UK.

Maria Grazia Vizioli (MG)

Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, USA.
Robert and Arlene Kogod Center on Aging, Mayo Clinic, Rochester, MN, USA.

Leena Habiballa (L)

Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, USA.
Robert and Arlene Kogod Center on Aging, Mayo Clinic, Rochester, MN, USA.
NIHR Newcastle Biomedical Research Centre, Newcastle University and Newcastle Upon Tyne Hospitals NHS Foundation Trust, Newcastle upon Tyne, UK.

Gabriele Saretzki (G)

Ageing Research Laboratories, Faculty of Medical Sciences, Biosciences Institute, Newcastle University, Newcastle upon Tyne, UK.

Shane A Evans (SA)

Department of Molecular Biology, Cell Biology and Biochemistry, Brown University, Providence, RI, USA.

Hanna Salmonowicz (H)

Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, USA.
Robert and Arlene Kogod Center on Aging, Mayo Clinic, Rochester, MN, USA.
Ageing Research Laboratories, Faculty of Medical Sciences, Biosciences Institute, Newcastle University, Newcastle upon Tyne, UK.

Adam Hruby (A)

Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, USA.
Robert and Arlene Kogod Center on Aging, Mayo Clinic, Rochester, MN, USA.

Daniel Geh (D)

Newcastle Fibrosis Research Group, Biosciences Institute, Newcastle University, Newcastle upon Tyne, UK.

Kevin D Pavelko (KD)

Department of Immunology and Immune Monitoring Core, Mayo Clinic, Rochester, MN, USA.

David Dolan (D)

Computational Biology Unit, University of Bergen, Bergen, Norway.

Helen L Reeves (HL)

Newcastle University Translational and Clinical Research Institute, Liver Unit, Newcastle upon Tyne NHS Foundation Trust, Newcastle upon Tyne, UK.

Sushma Grellscheid (S)

Computational Biology Unit, University of Bergen, Bergen, Norway.
Department of Biosciences, Durham University, Durham, UK.

Colin H Wilson (CH)

Department of Hepatobiliary Surgery, Newcastle upon Tyne Hospitals NHS Foundation Trust, Newcastle upon Tyne, UK.

Sanjay Pandanaboyana (S)

Department of Hepatobiliary Surgery, Newcastle upon Tyne Hospitals NHS Foundation Trust, Newcastle upon Tyne, UK.

Madison Doolittle (M)

Robert and Arlene Kogod Center on Aging, Mayo Clinic, Rochester, MN, USA.

Thomas von Zglinicki (T)

Ageing Research Laboratories, Faculty of Medical Sciences, Biosciences Institute, Newcastle University, Newcastle upon Tyne, UK.

Fiona Oakley (F)

Newcastle Fibrosis Research Group, Biosciences Institute, Newcastle University, Newcastle upon Tyne, UK.

Suchira Gallage (S)

Division of Chronic Inflammation and Cancer, German Cancer Research Center (DKFZ), Heidelberg, Germany.

Caroline L Wilson (CL)

Newcastle Fibrosis Research Group, Biosciences Institute, Newcastle University, Newcastle upon Tyne, UK.

Jodie Birch (J)

Ageing Research Laboratories, Faculty of Medical Sciences, Biosciences Institute, Newcastle University, Newcastle upon Tyne, UK.

Bernadette Carroll (B)

School of Biochemistry, University of Bristol, Bristol, UK.

James Chapman (J)

Ageing Research Laboratories, Faculty of Medical Sciences, Biosciences Institute, Newcastle University, Newcastle upon Tyne, UK.

Mathias Heikenwalder (M)

Division of Chronic Inflammation and Cancer, German Cancer Research Center (DKFZ), Heidelberg, Germany.

Nicola Neretti (N)

Department of Molecular Biology, Cell Biology and Biochemistry, Brown University, Providence, RI, USA.

Sundeep Khosla (S)

Robert and Arlene Kogod Center on Aging, Mayo Clinic, Rochester, MN, USA.

Claudio Akio Masuda (CA)

Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, USA.
Robert and Arlene Kogod Center on Aging, Mayo Clinic, Rochester, MN, USA.
Instituto de Bioquímica Médica Leopoldo de Meis, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil.

Tamar Tchkonia (T)

Robert and Arlene Kogod Center on Aging, Mayo Clinic, Rochester, MN, USA.

James L Kirkland (JL)

Robert and Arlene Kogod Center on Aging, Mayo Clinic, Rochester, MN, USA.

Diana Jurk (D)

Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, USA.
Robert and Arlene Kogod Center on Aging, Mayo Clinic, Rochester, MN, USA.

Derek A Mann (DA)

Newcastle Fibrosis Research Group, Biosciences Institute, Newcastle University, Newcastle upon Tyne, UK.

João F Passos (JF)

Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, USA.
Robert and Arlene Kogod Center on Aging, Mayo Clinic, Rochester, MN, USA.

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