The fate and lifespan of human monocyte subsets in steady state and systemic inflammation
In humans, the monocyte pool comprises three subsets (classical, intermediate, and nonclassical) that circulate in dynamic equilibrium. The kinetics underlying their generation, differentiation, and disappearance are critical to understanding both steady-state homeostasis and inflammatory responses....
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| Published in | The Journal of experimental medicine Vol. 214; no. 7; pp. 1913 - 1923 |
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| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Rockefeller University Press
03.07.2017
The Rockefeller University Press |
| Subjects | |
| Online Access | Get full text |
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| Abstract | In humans, the monocyte pool comprises three subsets (classical, intermediate, and nonclassical) that circulate in dynamic equilibrium. The kinetics underlying their generation, differentiation, and disappearance are critical to understanding both steady-state homeostasis and inflammatory responses. Here, using human in vivo deuterium labeling, we demonstrate that classical monocytes emerge first from marrow, after a postmitotic interval of 1.6 d, and circulate for a day. Subsequent labeling of intermediate and nonclassical monocytes is consistent with a model of sequential transition. Intermediate and nonclassical monocytes have longer circulating lifespans (∼4 and ∼7 d, respectively). In a human experimental endotoxemia model, a transient but profound monocytopenia was observed; restoration of circulating monocytes was achieved by the early release of classical monocytes from bone marrow. The sequence of repopulation recapitulated the order of maturation in healthy homeostasis. This developmental relationship between monocyte subsets was verified by fate mapping grafted human classical monocytes into humanized mice, which were able to differentiate sequentially into intermediate and nonclassical cells. |
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| AbstractList | In humans, the monocyte pool comprises three subsets (classical, intermediate, and nonclassical) that circulate in dynamic equilibrium. The kinetics underlying their generation, differentiation, and disappearance are critical to understanding both steady-state homeostasis and inflammatory responses. Here, using human in vivo deuterium labeling, we demonstrate that classical monocytes emerge first from marrow, after a postmitotic interval of 1.6 d, and circulate for a day. Subsequent labeling of intermediate and nonclassical monocytes is consistent with a model of sequential transition. Intermediate and nonclassical monocytes have longer circulating lifespans (∼4 and ∼7 d, respectively). In a human experimental endotoxemia model, a transient but profound monocytopenia was observed; restoration of circulating monocytes was achieved by the early release of classical monocytes from bone marrow. The sequence of repopulation recapitulated the order of maturation in healthy homeostasis. This developmental relationship between monocyte subsets was verified by fate mapping grafted human classical monocytes into humanized mice, which were able to differentiate sequentially into intermediate and nonclassical cells.In humans, the monocyte pool comprises three subsets (classical, intermediate, and nonclassical) that circulate in dynamic equilibrium. The kinetics underlying their generation, differentiation, and disappearance are critical to understanding both steady-state homeostasis and inflammatory responses. Here, using human in vivo deuterium labeling, we demonstrate that classical monocytes emerge first from marrow, after a postmitotic interval of 1.6 d, and circulate for a day. Subsequent labeling of intermediate and nonclassical monocytes is consistent with a model of sequential transition. Intermediate and nonclassical monocytes have longer circulating lifespans (∼4 and ∼7 d, respectively). In a human experimental endotoxemia model, a transient but profound monocytopenia was observed; restoration of circulating monocytes was achieved by the early release of classical monocytes from bone marrow. The sequence of repopulation recapitulated the order of maturation in healthy homeostasis. This developmental relationship between monocyte subsets was verified by fate mapping grafted human classical monocytes into humanized mice, which were able to differentiate sequentially into intermediate and nonclassical cells. In humans, the monocyte pool comprises three subsets (classical, intermediate, and nonclassical) that circulate in dynamic equilibrium. The kinetics underlying their generation, differentiation, and disappearance are critical to understanding both steady-state homeostasis and inflammatory responses. Here, using human in vivo deuterium labeling, we demonstrate that classical monocytes emerge first from marrow, after a postmitotic interval of 1.6 d, and circulate for a day. Subsequent labeling of intermediate and nonclassical monocytes is consistent with a model of sequential transition. Intermediate and nonclassical monocytes have longer circulating lifespans (∼4 and ∼7 d, respectively). In a human experimental endotoxemia model, a transient but profound monocytopenia was observed; restoration of circulating monocytes was achieved by the early release of classical monocytes from bone marrow. The sequence of repopulation recapitulated the order of maturation in healthy homeostasis. This developmental relationship between monocyte subsets was verified by fate mapping grafted human classical monocytes into humanized mice, which were able to differentiate sequentially into intermediate and nonclassical cells. Using stable isotope labeling, Patel et al. establish the lifespan of all three human monocyte subsets that circulate in dynamic equilibrium; in steady state, classical monocytes are short-lived precursors with the potential to become intermediate and nonclassical monocytes. They highlight that systemic inflammation induces an emergency release of classical monocytes into the circulation. In humans, the monocyte pool comprises three subsets (classical, intermediate, and nonclassical) that circulate in dynamic equilibrium. The kinetics underlying their generation, differentiation, and disappearance are critical to understanding both steady-state homeostasis and inflammatory responses. Here, using human in vivo deuterium labeling, we demonstrate that classical monocytes emerge first from marrow, after a postmitotic interval of 1.6 d, and circulate for a day. Subsequent labeling of intermediate and nonclassical monocytes is consistent with a model of sequential transition. Intermediate and nonclassical monocytes have longer circulating lifespans (∼4 and ∼7 d, respectively). In a human experimental endotoxemia model, a transient but profound monocytopenia was observed; restoration of circulating monocytes was achieved by the early release of classical monocytes from bone marrow. The sequence of repopulation recapitulated the order of maturation in healthy homeostasis. This developmental relationship between monocyte subsets was verified by fate mapping grafted human classical monocytes into humanized mice, which were able to differentiate sequentially into intermediate and nonclassical cells. Using stable isotope labeling, Patel et al. establish the lifespan of all three human monocyte subsets that circulate in dynamic equilibrium; in steady state, classical monocytes are short-lived precursors with the potential to become intermediate and nonclassical monocytes. They highlight that systemic inflammation induces an emergency release of classical monocytes into the circulation. In humans, the monocyte pool comprises three subsets (classical, intermediate, and nonclassical) that circulate in dynamic equilibrium. The kinetics underlying their generation, differentiation, and disappearance are critical to understanding both steady-state homeostasis and inflammatory responses. Here, using human in vivo deuterium labeling, we demonstrate that classical monocytes emerge first from marrow, after a postmitotic interval of 1.6 d, and circulate for a day. Subsequent labeling of intermediate and nonclassical monocytes is consistent with a model of sequential transition. Intermediate and nonclassical monocytes have longer circulating lifespans ( similar to 4 and similar to 7 d, respectively). In a human experimental endotoxemia model, a transient but profound monocytopenia was observed; restoration of circulating monocytes was achieved by the early release of classical monocytes from bone marrow. The sequence of repopulation recapitulated the order of maturation in healthy homeostasis. This developmental relationship between monocyte subsets was verified by fate mapping grafted human classical monocytes into humanized mice, which were able to differentiate sequentially into intermediate and nonclassical cells. Using stable isotope labeling, Patel et al. establish the lifespan of all three human monocyte subsets that circulate in dynamic equilibrium; in steady state, classical monocytes are short-lived precursors with the potential to become intermediate and nonclassical monocytes. They highlight that systemic inflammation induces an emergency release of classical monocytes into the circulation.In humans, the monocyte pool comprises three subsets (classical, intermediate, and nonclassical) that circulate in dynamic equilibrium. The kinetics underlying their generation, differentiation, and disappearance are critical to understanding both steady-state homeostasis and inflammatory responses. Here, using human in vivo deuterium labeling, we demonstrate that classical monocytes emerge first from marrow, after a postmitotic interval of 1.6 d, and circulate for a day. Subsequent labeling of intermediate and nonclassical monocytes is consistent with a model of sequential transition. Intermediate and nonclassical monocytes have longer circulating lifespans (∼4 and ∼7 d, respectively). In a human experimental endotoxemia model, a transient but profound monocytopenia was observed; restoration of circulating monocytes was achieved by the early release of classical monocytes from bone marrow. The sequence of repopulation recapitulated the order of maturation in healthy homeostasis. This developmental relationship between monocyte subsets was verified by fate mapping grafted human classical monocytes into humanized mice, which were able to differentiate sequentially into intermediate and nonclassical cells. |
| Author | Gilroy, Derek W. Macallan, Derek Maini, Alexander A. Boelen, Lies Flavell, Richard A. Asquith, Becca Rongvaux, Anthony Bigley, Venetia Zhang, Yan Patel, Amit A. Fullerton, James N. Yona, Simon |
| AuthorAffiliation | 2 Institute for Infection and Immunity, St. George’s, University of London, London, England, UK 4 Department of Immunobiology, Yale University, New Haven, CT 1 Division of Medicine, University College London, University of London, London, England, UK 7 St. George’s University Hospitals NHS Foundation Trust, London, England, UK 6 Newcastle University Medical School, Newcastle University, Newcastle Upon Tyne, England, UK 3 Theoretical Immunology Group, Faculty of Medicine, Imperial College London, London, England, UK 5 Howard Hughes Medical Institute, Yale University, New Haven, CT |
| AuthorAffiliation_xml | – name: 5 Howard Hughes Medical Institute, Yale University, New Haven, CT – name: 1 Division of Medicine, University College London, University of London, London, England, UK – name: 3 Theoretical Immunology Group, Faculty of Medicine, Imperial College London, London, England, UK – name: 2 Institute for Infection and Immunity, St. George’s, University of London, London, England, UK – name: 6 Newcastle University Medical School, Newcastle University, Newcastle Upon Tyne, England, UK – name: 4 Department of Immunobiology, Yale University, New Haven, CT – name: 7 St. George’s University Hospitals NHS Foundation Trust, London, England, UK |
| Author_xml | – sequence: 1 givenname: Amit A. surname: Patel fullname: Patel, Amit A. – sequence: 2 givenname: Yan orcidid: 0000-0001-6054-1309 surname: Zhang fullname: Zhang, Yan – sequence: 3 givenname: James N. orcidid: 0000-0002-4855-9255 surname: Fullerton fullname: Fullerton, James N. – sequence: 4 givenname: Lies orcidid: 0000-0003-3786-5545 surname: Boelen fullname: Boelen, Lies – sequence: 5 givenname: Anthony surname: Rongvaux fullname: Rongvaux, Anthony – sequence: 6 givenname: Alexander A. surname: Maini fullname: Maini, Alexander A. – sequence: 7 givenname: Venetia orcidid: 0000-0002-3017-2474 surname: Bigley fullname: Bigley, Venetia – sequence: 8 givenname: Richard A. orcidid: 0000-0003-4461-0778 surname: Flavell fullname: Flavell, Richard A. – sequence: 9 givenname: Derek W. surname: Gilroy fullname: Gilroy, Derek W. – sequence: 10 givenname: Becca surname: Asquith fullname: Asquith, Becca – sequence: 11 givenname: Derek orcidid: 0000-0002-3014-7148 surname: Macallan fullname: Macallan, Derek – sequence: 12 givenname: Simon orcidid: 0000-0002-3984-2008 surname: Yona fullname: Yona, Simon |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28606987$$D View this record in MEDLINE/PubMed |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 R.A. Flavell, D.W. Gilroy, B. Asquith, and D. Macallan contributed equally to this paper. A. Rongvaux’s present address is Program in Immunology, Clinical Research Division, Fred Hutchinson Cancer Research Center, Seattle, WA. |
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| Snippet | In humans, the monocyte pool comprises three subsets (classical, intermediate, and nonclassical) that circulate in dynamic equilibrium. The kinetics underlying... Using stable isotope labeling, Patel et al. establish the lifespan of all three human monocyte subsets that circulate in dynamic equilibrium; in steady state,... |
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| SubjectTerms | Animals Bone marrow Bone Marrow Cells - immunology Cell Differentiation - immunology Cell fate Cell Survival - immunology Cells, Cultured Deuterium Deuterium - metabolism Endotoxemia Endotoxemia - blood Endotoxemia - immunology Fate maps Flow Cytometry Homeostasis Homeostasis - immunology Human behavior Humans Inflammation Inflammation - blood Inflammation - immunology Isotope Labeling - methods Kinetics Labeling Life span Mice Monocytes Monocytes - immunology Repopulation Restoration Steady state Time Factors |
| Title | The fate and lifespan of human monocyte subsets in steady state and systemic inflammation |
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