Inflammatory exposure drives long-lived impairment of hematopoietic stem cell self-renewal activity and accelerated aging.

HSCs accelerated aging aging clonal hematopoiesis hematopoietic stem cells inflammaging inflammation self-renewal stem cell exhaustion stress hematopoiesis

Journal

Cell stem cell
ISSN: 1875-9777
Titre abrégé: Cell Stem Cell
Pays: United States
ID NLM: 101311472

Informations de publication

Date de publication:
04 08 2022
Historique:
received: 19 04 2022
revised: 08 06 2022
accepted: 21 06 2022
pubmed: 21 7 2022
medline: 10 8 2022
entrez: 20 7 2022
Statut: ppublish

Résumé

Hematopoietic stem cells (HSCs) mediate regeneration of the hematopoietic system following injury, such as following infection or inflammation. These challenges impair HSC function, but whether this functional impairment extends beyond the duration of inflammatory exposure is unknown. Unexpectedly, we observed an irreversible depletion of functional HSCs following challenge with inflammation or bacterial infection, with no evidence of any recovery up to 1 year afterward. HSCs from challenged mice demonstrated multiple cellular and molecular features of accelerated aging and developed clinically relevant blood and bone marrow phenotypes not normally observed in aged laboratory mice but commonly seen in elderly humans. In vivo HSC self-renewal divisions were absent or extremely rare during both challenge and recovery periods. The progressive, irreversible attrition of HSC function demonstrates that temporally discrete inflammatory events elicit a cumulative inhibitory effect on HSCs. This work positions early/mid-life inflammation as a mediator of lifelong defects in tissue maintenance and regeneration.

Identifiants

pubmed: 35858618
pii: S1934-5909(22)00261-2
doi: 10.1016/j.stem.2022.06.012
pmc: PMC9357150
mid: NIHMS1824968
pii:
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1273-1284.e8

Subventions

Organisme : NHLBI NIH HHS
ID : F31 HL154661
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK112976
Pays : United States
Organisme : NHLBI NIH HHS
ID : R35 HL155672
Pays : United States
Organisme : NIEHS NIH HHS
ID : P30 ES030285
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK056638
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2022 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

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Auteurs

Ruzhica Bogeska (R)

Division of Experimental Hematology, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany; Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM), 69120 Heidelberg, Germany.

Ana-Matea Mikecin (AM)

Division of Experimental Hematology, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany; Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM), 69120 Heidelberg, Germany.

Paul Kaschutnig (P)

Division of Experimental Hematology, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany; Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM), 69120 Heidelberg, Germany; Faculty of Biosciences, University of Heidelberg, 69120 Heidelberg, Germany.

Malak Fawaz (M)

Department of Medicine, Hematology/Oncology, Goethe University Hospital Frankfurt, 60590 Frankfurt, Germany.

Marleen Büchler-Schäff (M)

Division of Experimental Hematology, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany; Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM), 69120 Heidelberg, Germany; Faculty of Biosciences, University of Heidelberg, 69120 Heidelberg, Germany.

Duy Le (D)

Program in Immunology, Graduate School of Biomedical Sciences, Baylor College of Medicine, Houston, TX 77030, USA.

Miguel Ganuza (M)

Department of Hematology, St. Jude Children's Research Hospital, Memphis, TN 38105, USA; Centre for Haemato-Oncology, Barts Cancer Institute, Queen Mary University of London London EC1M 6BQ, UK.

Angelika Vollmer (A)

Institute of Molecular Medicine, Stem Cells and Aging, Aging Research Center, Ulm University, 89081 Ulm, Germany.

Stella V Paffenholz (SV)

Division of Experimental Hematology, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany; Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM), 69120 Heidelberg, Germany; Faculty of Biosciences, University of Heidelberg, 69120 Heidelberg, Germany.

Noboru Asada (N)

Ruth L. and David S. Gottesman Institute for Stem Cell and Regenerative Medicine Research, Albert Einstein College of Medicine, Bronx, NY 10461, USA.

Esther Rodriguez-Correa (E)

Division of Experimental Hematology, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany; Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM), 69120 Heidelberg, Germany; Faculty of Biosciences, University of Heidelberg, 69120 Heidelberg, Germany.

Felix Frauhammer (F)

Faculty of Biosciences, University of Heidelberg, 69120 Heidelberg, Germany; Division of Applied Bioinformatics, DKFZ, 69120 Heidelberg, Germany.

Florian Buettner (F)

Department of Medicine, Hematology/Oncology, Goethe University Hospital Frankfurt, 60590 Frankfurt, Germany; The German Cancer Consortium (DKTK), 69120 Heidelberg, Germany; Frankfurt Cancer Institute, 60590 Frankfurt, Germany.

Melanie Ball (M)

Division of Experimental Hematology, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany; Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM), 69120 Heidelberg, Germany.

Julia Knoch (J)

Division of Experimental Hematology, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany; Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM), 69120 Heidelberg, Germany.

Sina Stäble (S)

Division of Experimental Hematology, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany; Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM), 69120 Heidelberg, Germany; Faculty of Biosciences, University of Heidelberg, 69120 Heidelberg, Germany; Section Translational Cancer Epigenomics, Division of Translational Medical Oncology, DKFZ, 69120 Heidelberg, Germany.

Dagmar Walter (D)

Division of Experimental Hematology, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany; Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM), 69120 Heidelberg, Germany.

Amelie Petri (A)

Division of Experimental Hematology, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany; Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM), 69120 Heidelberg, Germany.

Martha J Carreño-Gonzalez (MJ)

Division of Experimental Hematology, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany; Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM), 69120 Heidelberg, Germany; Faculty of Biosciences, University of Heidelberg, 69120 Heidelberg, Germany.

Vinona Wagner (V)

Division of Experimental Hematology, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany; Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM), 69120 Heidelberg, Germany; Faculty of Biosciences, University of Heidelberg, 69120 Heidelberg, Germany.

Benedikt Brors (B)

Division of Applied Bioinformatics, DKFZ, 69120 Heidelberg, Germany.

Simon Haas (S)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM), 69120 Heidelberg, Germany; The German Cancer Consortium (DKTK), 69120 Heidelberg, Germany; Division of Stem Cells and Cancer, DKFZ, 69120 Heidelberg, Germany; DKFZ-ZMBH Alliance, Heidelberg, Germany; Berlin Institute of Health (BIH), Charité Universitätsmedizin, 10178 Berlin, Germany; Max Delbrück Center for Molecular Medicine, 13125 Berlin, Germany.

Daniel B Lipka (DB)

The German Cancer Consortium (DKTK), 69120 Heidelberg, Germany; Section Translational Cancer Epigenomics, Division of Translational Medical Oncology, DKFZ, 69120 Heidelberg, Germany; National Center for Tumor Diseases (NCT), 69120 Heidelberg, Germany; Faculty of Medicine, Otto-von-Guericke University, 39120 Magdeburg, Germany.

Marieke A G Essers (MAG)

Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM), 69120 Heidelberg, Germany; DKFZ-ZMBH Alliance, Heidelberg, Germany; Division of Inflammatory Stress in Stem Cells, DKFZ, 69120 Heidelberg, Germany.

Vivienn Weru (V)

Division of Biostatistics, DKFZ, 69120 Heidelberg, Germany.

Tim Holland-Letz (T)

Division of Biostatistics, DKFZ, 69120 Heidelberg, Germany.

Jan-Philipp Mallm (JP)

Division of Chromatin Networks, DKFZ, 69120 Heidelberg, Germany.

Karsten Rippe (K)

Division of Chromatin Networks, DKFZ, 69120 Heidelberg, Germany.

Stephan Krämer (S)

Faculty of Biosciences, University of Heidelberg, 69120 Heidelberg, Germany; Section Translational Cancer Epigenomics, Division of Translational Medical Oncology, DKFZ, 69120 Heidelberg, Germany; Biomedical Informatics, Data Mining and Data Analytics, Faculty of Applied Computer Science and Medical Faculty, University of Augsburg, 86159 Augsburg, Germany; Bioinformatics and Omics Data Analysis, DKFZ, 69120 Heidelberg, Germany.

Matthias Schlesner (M)

Biomedical Informatics, Data Mining and Data Analytics, Faculty of Applied Computer Science and Medical Faculty, University of Augsburg, 86159 Augsburg, Germany; Bioinformatics and Omics Data Analysis, DKFZ, 69120 Heidelberg, Germany.

Shannon McKinney Freeman (S)

Department of Hematology, St. Jude Children's Research Hospital, Memphis, TN 38105, USA.

Maria Carolina Florian (MC)

Stem Cell Aging Group, Regenerative Medicine Program, The Bellvitge Institute for Biomedical Research (IDIBELL), L'Hospitalet de Llobregat, Barcelona, Spain.

Katherine Y King (KY)

Program in Immunology, Graduate School of Biomedical Sciences, Baylor College of Medicine, Houston, TX 77030, USA; Department of Pediatrics, Division of Infectious Diseases, Baylor College of Medicine, Houston, TX 77030, USA.

Paul S Frenette (PS)

Ruth L. and David S. Gottesman Institute for Stem Cell and Regenerative Medicine Research, Albert Einstein College of Medicine, Bronx, NY 10461, USA.

Michael A Rieger (MA)

Department of Medicine, Hematology/Oncology, Goethe University Hospital Frankfurt, 60590 Frankfurt, Germany; The German Cancer Consortium (DKTK), 69120 Heidelberg, Germany; Frankfurt Cancer Institute, 60590 Frankfurt, Germany; Cardio-Pulmonary Institute, 60590 Frankfurt, Germany.

Michael D Milsom (MD)

Division of Experimental Hematology, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany; Heidelberg Institute for Stem Cell Technology and Experimental Medicine (HI-STEM), 69120 Heidelberg, Germany; DKFZ-ZMBH Alliance, Heidelberg, Germany. Electronic address: michael.milsom@dkfz.de.

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