Maladaptive innate immune training of myelopoiesis links inflammatory comorbidities
Bone marrow (BM)-mediated trained innate immunity (TII) is a state of heightened immune responsiveness of hematopoietic stem and progenitor cells (HSPC) and their myeloid progeny. We show here that maladaptive BM-mediated TII underlies inflammatory comorbidities, as exemplified by the periodontitis-...
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| Published in | Cell Vol. 185; no. 10; pp. 1709 - 1727.e18 |
|---|---|
| Main Authors | , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
12.05.2022
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Bone marrow (BM)-mediated trained innate immunity (TII) is a state of heightened immune responsiveness of hematopoietic stem and progenitor cells (HSPC) and their myeloid progeny. We show here that maladaptive BM-mediated TII underlies inflammatory comorbidities, as exemplified by the periodontitis-arthritis axis. Experimental-periodontitis-related systemic inflammation in mice induced epigenetic rewiring of HSPC and led to sustained enhancement of production of myeloid cells with increased inflammatory preparedness. The periodontitis-induced trained phenotype was transmissible by BM transplantation to naive recipients, which exhibited increased inflammatory responsiveness and disease severity when subjected to inflammatory arthritis. IL-1 signaling in HSPC was essential for their maladaptive training by periodontitis. Therefore, maladaptive innate immune training of myelopoiesis underlies inflammatory comorbidities and may be pharmacologically targeted to treat them via a holistic approach.
[Display omitted]
•Experimental periodontitis (EP) induces maladaptive trained myelopoiesis•EP-induced trained phenotype is transmissible by bone marrow transplantation•IL-1 signaling in hematopoietic progenitors mediates maladaptive training by EP•Maladaptively trained myelopoiesis links the periodontitis-arthritis comorbidity
Trained innate immune responses contribute to pathology of a comorbid condition, as seen with arthritis after periodontitis in animal models. |
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| AbstractList | Bone marrow (BM)-mediated trained innate immunity (TII) is a state of heightened immune responsiveness of hematopoietic stem and progenitor cells (HSPC) and their myeloid progeny. We show here that maladaptive BM-mediated TII underlies inflammatory comorbidities, as exemplified by the periodontitis-arthritis axis. Experimental-periodontitis-related systemic inflammation in mice induced epigenetic rewiring of HSPC and led to sustained enhancement of production of myeloid cells with increased inflammatory preparedness. The periodontitis-induced trained phenotype was transmissible by BM transplantation to naive recipients, which exhibited increased inflammatory responsiveness and disease severity when subjected to inflammatory arthritis. IL-1 signaling in HSPC was essential for their maladaptive training by periodontitis. Therefore, maladaptive innate immune training of myelopoiesis underlies inflammatory comorbidities and may be pharmacologically targeted to treat them via a holistic approach.Bone marrow (BM)-mediated trained innate immunity (TII) is a state of heightened immune responsiveness of hematopoietic stem and progenitor cells (HSPC) and their myeloid progeny. We show here that maladaptive BM-mediated TII underlies inflammatory comorbidities, as exemplified by the periodontitis-arthritis axis. Experimental-periodontitis-related systemic inflammation in mice induced epigenetic rewiring of HSPC and led to sustained enhancement of production of myeloid cells with increased inflammatory preparedness. The periodontitis-induced trained phenotype was transmissible by BM transplantation to naive recipients, which exhibited increased inflammatory responsiveness and disease severity when subjected to inflammatory arthritis. IL-1 signaling in HSPC was essential for their maladaptive training by periodontitis. Therefore, maladaptive innate immune training of myelopoiesis underlies inflammatory comorbidities and may be pharmacologically targeted to treat them via a holistic approach. Bone marrow (BM)-mediated trained innate immunity (TII) is a state of heightened immune responsiveness of hematopoietic stem and progenitor cells (HSPC) and their myeloid progeny. We show here that maladaptive BM-mediated TII underlies inflammatory comorbidities, as exemplified by the periodontitis-arthritis axis. Experimental-periodontitis-related systemic inflammation in mice induced epigenetic rewiring of HSPC and led to sustained enhancement of production of myeloid cells with increased inflammatory preparedness. The periodontitis-induced trained phenotype was transmissible by BM transplantation to naive recipients, which exhibited increased inflammatory responsiveness and disease severity when subjected to inflammatory arthritis. IL-1 signaling in HSPC was essential for their maladaptive training by periodontitis. Therefore, maladaptive innate immune training of myelopoiesis underlies inflammatory comorbidities and may be pharmacologically targeted to treat them via a holistic approach. Bone marrow (BM)-mediated trained innate immunity (TII) is a state of heightened immune responsiveness of hematopoietic stem and progenitor cells (HSPC) and their myeloid progeny. We show here that maladaptive BM-mediated TII underlies inflammatory comorbidities, as exemplified by the periodontitis-arthritis axis. Experimental periodontitis-related systemic inflammation in mice induced epigenetic rewiring of HSPC and led to sustained enhancement of production of myeloid cells with enhanced inflammatory preparedness. The periodontitis-induced trained phenotype was transmissible by BM transplantation to naïve recipients, which exhibited increased inflammatory responsiveness and disease severity when subjected to inflammatory arthritis. IL-1 signaling in HSPC was essential for their maladaptive training by periodontitis. Therefore, maladaptive innate immune training of myelopoiesis underlies inflammatory comorbidities and may be pharmacologically targeted to treat them via a holistic approach. Trained innate immune responses contribute to pathology of a comorbid condition, as seen with arthritis after periodontitis in animal models. Bone marrow (BM)-mediated trained innate immunity (TII) is a state of heightened immune responsiveness of hematopoietic stem and progenitor cells (HSPC) and their myeloid progeny. We show here that maladaptive BM-mediated TII underlies inflammatory comorbidities, as exemplified by the periodontitis-arthritis axis. Experimental-periodontitis-related systemic inflammation in mice induced epigenetic rewiring of HSPC and led to sustained enhancement of production of myeloid cells with increased inflammatory preparedness. The periodontitis-induced trained phenotype was transmissible by BM transplantation to naive recipients, which exhibited increased inflammatory responsiveness and disease severity when subjected to inflammatory arthritis. IL-1 signaling in HSPC was essential for their maladaptive training by periodontitis. Therefore, maladaptive innate immune training of myelopoiesis underlies inflammatory comorbidities and may be pharmacologically targeted to treat them via a holistic approach. [Display omitted] •Experimental periodontitis (EP) induces maladaptive trained myelopoiesis•EP-induced trained phenotype is transmissible by bone marrow transplantation•IL-1 signaling in hematopoietic progenitors mediates maladaptive training by EP•Maladaptively trained myelopoiesis links the periodontitis-arthritis comorbidity Trained innate immune responses contribute to pathology of a comorbid condition, as seen with arthritis after periodontitis in animal models. |
| Author | Ioannidis, Charalampos Saha, Gundappa Li, Xiaofei Yu, Xiang Mitroulis, Ioannis Chavakis, Triantafyllos Wang, Hui Hajishengallis, George Kalafati, Lydia Netea, Mihai G. |
| AuthorAffiliation | 4 Institute for Clinical Chemistry and Laboratory Medicine, Faculty of Medicine, Technische Universität Dresden, 01307 Dresden, Germany 2 Joint International Research Laboratory of Metabolic and Developmental Sciences, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China 9 These authors contributed equally 6 Department of Internal Medicine and Radboud Center for Infectious Diseases, Radboud University Medical Center, Nijmegen, 6525 XZ, The Netherlands 5 First Department of Internal Medicine and Department of Haematology, Democritus University of Thrace, 681 00 Alexandroupolis, Greece 3 Department of Biology, University of Pennsylvania, Philadelphia, PA 19104, USA 8 Centre for Cardiovascular Science, University of Edinburgh, Edinburgh, EH16 4TJ, UK 1 Department of Basic and Translational Sciences, Laboratory of Innate Immunity and Inflammation, Penn Dental Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA 11 Lead contact 10 Senior autho |
| AuthorAffiliation_xml | – name: 9 These authors contributed equally – name: 11 Lead contact – name: 10 Senior authors – name: 5 First Department of Internal Medicine and Department of Haematology, Democritus University of Thrace, 681 00 Alexandroupolis, Greece – name: 8 Centre for Cardiovascular Science, University of Edinburgh, Edinburgh, EH16 4TJ, UK – name: 2 Joint International Research Laboratory of Metabolic and Developmental Sciences, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China – name: 6 Department of Internal Medicine and Radboud Center for Infectious Diseases, Radboud University Medical Center, Nijmegen, 6525 XZ, The Netherlands – name: 1 Department of Basic and Translational Sciences, Laboratory of Innate Immunity and Inflammation, Penn Dental Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA – name: 4 Institute for Clinical Chemistry and Laboratory Medicine, Faculty of Medicine, Technische Universität Dresden, 01307 Dresden, Germany – name: 3 Department of Biology, University of Pennsylvania, Philadelphia, PA 19104, USA – name: 7 Department of Immunology and Metabolism, Life and Medical Science Institute, University of Bonn, 53115 Bonn, Germany |
| Author_xml | – sequence: 1 givenname: Xiaofei surname: Li fullname: Li, Xiaofei organization: Department of Basic and Translational Sciences, Laboratory of Innate Immunity and Inflammation, Penn Dental Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 2 givenname: Hui orcidid: 0000-0002-0055-7357 surname: Wang fullname: Wang, Hui organization: Department of Basic and Translational Sciences, Laboratory of Innate Immunity and Inflammation, Penn Dental Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 3 givenname: Xiang surname: Yu fullname: Yu, Xiang organization: Joint International Research Laboratory of Metabolic and Developmental Sciences, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China – sequence: 4 givenname: Gundappa surname: Saha fullname: Saha, Gundappa organization: Department of Basic and Translational Sciences, Laboratory of Innate Immunity and Inflammation, Penn Dental Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 5 givenname: Lydia orcidid: 0000-0001-9272-8426 surname: Kalafati fullname: Kalafati, Lydia organization: Institute for Clinical Chemistry and Laboratory Medicine, Faculty of Medicine, Technische Universität Dresden, 01307 Dresden, Germany – sequence: 6 givenname: Charalampos surname: Ioannidis fullname: Ioannidis, Charalampos organization: Institute for Clinical Chemistry and Laboratory Medicine, Faculty of Medicine, Technische Universität Dresden, 01307 Dresden, Germany – sequence: 7 givenname: Ioannis orcidid: 0000-0002-9991-2362 surname: Mitroulis fullname: Mitroulis, Ioannis organization: Institute for Clinical Chemistry and Laboratory Medicine, Faculty of Medicine, Technische Universität Dresden, 01307 Dresden, Germany – sequence: 8 givenname: Mihai G. surname: Netea fullname: Netea, Mihai G. organization: Department of Internal Medicine and Radboud Center for Infectious Diseases, Radboud University Medical Center, Nijmegen 6525 XZ, the Netherlands – sequence: 9 givenname: Triantafyllos surname: Chavakis fullname: Chavakis, Triantafyllos email: triantafyllos.chavakis@uniklinikum-dresden.de organization: Institute for Clinical Chemistry and Laboratory Medicine, Faculty of Medicine, Technische Universität Dresden, 01307 Dresden, Germany – sequence: 10 givenname: George orcidid: 0000-0001-7392-8852 surname: Hajishengallis fullname: Hajishengallis, George email: geoh@upenn.edu organization: Department of Basic and Translational Sciences, Laboratory of Innate Immunity and Inflammation, Penn Dental Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35483374$$D View this record in MEDLINE/PubMed |
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| IngestDate | Thu Aug 21 18:36:45 EDT 2025 Fri Jul 11 07:45:10 EDT 2025 Tue Aug 05 09:26:41 EDT 2025 Mon Jul 21 06:03:48 EDT 2025 Tue Jul 01 02:17:11 EDT 2025 Thu Apr 24 23:13:08 EDT 2025 Sun Apr 06 06:53:59 EDT 2025 |
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| Issue | 10 |
| Keywords | comorbidities arthritis inflammation myelopoiesis periodontitis hematopoietic stem and progenitor cells epigenetic rewiring trained immunity bone marrow transplantation |
| Language | English |
| License | Copyright © 2022 Elsevier Inc. All rights reserved. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Author Contributions X.L. designed and performed research, analyzed and interpreted data, and co-wrote the manuscript; H.W. designed and performed research, analyzed and interpreted data, and contributed to writing; X.Y. performed experiments and analyzed data; G.S. performed experiments; L.K. and I.C. generated critical reagents; I.M. interpreted data; M.G.N. interpreted data and edited the manuscript; T.C. conceived and designed the study, interpreted data and edited the manuscript; G.H. conceived and designed the study, supervised research, interpreted data, and wrote the manuscript. |
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| OpenAccessLink | https://www.ncbi.nlm.nih.gov/pmc/articles/9106933 |
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| PublicationTitle | Cell |
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| PublicationYear | 2022 |
| Publisher | Elsevier Inc |
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| SubjectTerms | Animals Arthritis bone marrow bone marrow transplantation comorbidities disease severity epigenetic rewiring epigenetics hematopoietic stem and progenitor cells Hematopoietic Stem Cells Immunity, Innate inflammation innate immunity interleukin-1 Mice Myelopoiesis Periodontitis phenotype progeny trained immunity |
| Title | Maladaptive innate immune training of myelopoiesis links inflammatory comorbidities |
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