Red Blood Cells Capture and Deliver Bacterial DNA to Drive Host Responses During Polymicrobial Sepsis
Red blood cells (RBCs), traditionally recognized for their role in transporting oxygen, play a pivotal role in the body's immune response by expressing TLR9 and scavenging excess host cell-free DNA. DNA capture by RBCs leads to accelerated RBC clearance and triggers inflammation. Whether RBCs c...
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| Published in | The Journal of clinical investigation Vol. 135; no. 4 |
|---|---|
| Main Authors | , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
American Society for Clinical Investigation
15.02.2025
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| Subjects | |
| Online Access | Get full text |
| ISSN | 1558-8238 0021-9738 1558-8238 |
| DOI | 10.1172/JCI182127 |
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| Abstract | Red blood cells (RBCs), traditionally recognized for their role in transporting oxygen, play a pivotal role in the body's immune response by expressing TLR9 and scavenging excess host cell-free DNA. DNA capture by RBCs leads to accelerated RBC clearance and triggers inflammation. Whether RBCs can also acquire microbial DNA during infections is unknown. Murine RBCs acquire microbial DNA in vitro, and bacterial DNA-induced (bDNA-induced) macrophage activation was augmented by WT, but not Tlr9-deleted, RBCs. In a mouse model of polymicrobial sepsis, RBC-bound bDNA was elevated in WT mice but not in erythroid Tlr9-deleted mice. Plasma cytokine analysis in these mice revealed distinct sepsis clusters characterized by persistent hypothermia and hyperinflammation in the most severely affected mice. RBC Tlr9 deletion attenuated plasma and tissue IL-6 production in the most severely affected group. Parallel findings in humans confirmed that RBCs from patients with sepsis harbored more bDNA than did RBCs from healthy individuals. Further analysis through 16S sequencing of RBC-bound DNA illustrated distinct microbial communities, with RBC-bound DNA composition correlating with plasma IL-6 in patients with sepsis. Collectively, these findings unveil RBCs as overlooked reservoirs and couriers of microbial DNA, capable of influencing host inflammatory responses in sepsis. |
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| AbstractList | Red blood cells (RBCs), traditionally recognized for their role in transporting oxygen, play a pivotal role in the body's immune response by expressing TLR9 and scavenging excess host cell-free DNA. DNA capture by RBCs leads to accelerated RBC clearance and triggers inflammation. Whether RBCs can also acquire microbial DNA during infections is unknown. Murine RBCs acquire microbial DNA in vitro, and bacterial DNA-induced (bDNA-induced) macrophage activation was augmented by WT, but not Tlr9-deleted, RBCs. In a mouse model of polymicrobial sepsis, RBC-bound bDNA was elevated in WT mice but not in erythroid Tlr9-deleted mice. Plasma cytokine analysis in these mice revealed distinct sepsis clusters characterized by persistent hypothermia and hyperinflammation in the most severely affected mice. RBC Tlr9 deletion attenuated plasma and tissue IL-6 production in the most severely affected group. Parallel findings in humans confirmed that RBCs from patients with sepsis harbored more bDNA than did RBCs from healthy individuals. Further analysis through 16S sequencing of RBC-bound DNA illustrated distinct microbial communities, with RBC-bound DNA composition correlating with plasma IL-6 in patients with sepsis. Collectively, these findings unveil RBCs as overlooked reservoirs and couriers of microbial DNA, capable of influencing host inflammatory responses in sepsis.Red blood cells (RBCs), traditionally recognized for their role in transporting oxygen, play a pivotal role in the body's immune response by expressing TLR9 and scavenging excess host cell-free DNA. DNA capture by RBCs leads to accelerated RBC clearance and triggers inflammation. Whether RBCs can also acquire microbial DNA during infections is unknown. Murine RBCs acquire microbial DNA in vitro, and bacterial DNA-induced (bDNA-induced) macrophage activation was augmented by WT, but not Tlr9-deleted, RBCs. In a mouse model of polymicrobial sepsis, RBC-bound bDNA was elevated in WT mice but not in erythroid Tlr9-deleted mice. Plasma cytokine analysis in these mice revealed distinct sepsis clusters characterized by persistent hypothermia and hyperinflammation in the most severely affected mice. RBC Tlr9 deletion attenuated plasma and tissue IL-6 production in the most severely affected group. Parallel findings in humans confirmed that RBCs from patients with sepsis harbored more bDNA than did RBCs from healthy individuals. Further analysis through 16S sequencing of RBC-bound DNA illustrated distinct microbial communities, with RBC-bound DNA composition correlating with plasma IL-6 in patients with sepsis. Collectively, these findings unveil RBCs as overlooked reservoirs and couriers of microbial DNA, capable of influencing host inflammatory responses in sepsis. Red blood cells (RBCs), traditionally recognized for their role in transporting oxygen, play a pivotal role in the body's immune response by expressing TLR9 and scavenging excess host cell-free DNA. DNA capture by RBCs leads to accelerated RBC clearance and triggers inflammation. Whether RBCs can also acquire microbial DNA during infections is unknown. Murine RBCs acquire microbial DNA in vitro, and bacterial DNA-induced (bDNA-induced) macrophage activation was augmented by WT, but not Tlr9-deleted, RBCs. In a mouse model of polymicrobial sepsis, RBC- bound bDNA was elevated in WT mice but not in erythroid Tlr9-deleted mice. Plasma cytokine analysis in these mice revealed distinct sepsis clusters characterized by persistent hypothermia and hyperinflammation in the most severely affected mice. RBC Tlr9 deletion attenuated plasma and tissue IL-6 production in the most severely affected group. Parallel findings in humans confirmed that RBCs from patients with sepsis harbored more bDNA than did RBCs from healthy individuals. Further analysis through 16S sequencing of RBC-bound DNA illustrated distinct microbial communities, with RBC-bound DNA composition correlating with plasma IL-6 in patients with sepsis. Collectively, these findings unveil RBCs as overlooked reservoirs and couriers of microbial DNA, capable of influencing host inflammatory responses in sepsis. Red blood cells (RBCs), traditionally recognized for their role in transporting oxygen, play a pivotal role in the body’s immune response by expressing TLR9 and scavenging excess host cell-free DNA. DNA capture by RBCs leads to accelerated RBC clearance and triggers inflammation. Whether RBCs can also acquire microbial DNA during infections is unknown. Murine RBCs acquire microbial DNA in vitro, and bacterial DNA–induced (bDNA-induced) macrophage activation was augmented by WT, but not Tlr9-deleted, RBCs. In a mouse model of polymicrobial sepsis, RBC-bound bDNA was elevated in WT mice but not in erythroid Tlr9–deleted mice. Plasma cytokine analysis in these mice revealed distinct sepsis clusters characterized by persistent hypothermia and hyperinflammation in the most severely affected mice. RBC Tlr9 deletion attenuated plasma and tissue IL-6 production in the most severely affected group. Parallel findings in humans confirmed that RBCs from patients with sepsis harbored more bDNA than did RBCs from healthy individuals. Further analysis through 16S sequencing of RBC-bound DNA illustrated distinct microbial communities, with RBC-bound DNA composition correlating with plasma IL-6 in patients with sepsis. Collectively, these findings unveil RBCs as overlooked reservoirs and couriers of microbial DNA, capable of influencing host inflammatory responses in sepsis. Red blood cells capture microbial DNA, altering the host response during sepsis. Moreover, human RBCs are a reservoir of microbial DNA. |
| Audience | Academic |
| Author | Yehya, Nadir Oatman, Emily Mangalmurti, Nilam S. Klingensmith, Nathan J. Ranjan, Piyush Sayegh, Layal Lam, LK Metthew McGinnis, John Dickson, Robert P. Eckart, Kaitlyn A. Meyer, Nuala J. Jose, Joshua S. Lanza, Matthew Cosgriff, Christopher V. |
| AuthorAffiliation | 5 Department of Comparative Medicine, Penn State Health Milton S. Hershey Medical Center, Hershey, Pennsylvania, USA 6 Division of Pediatric Critical Care, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pennsylvania, USA 8 Weil Institute for Critical Care Research and Innovation, Ann Arbor, Michigan, USA 1 Division of Pulmonary, Allergy, and Critical Care and 9 Department of Microbiology and Immunology, University of Michigan Medical School, Ann, Arbor, Michigan, USA 4 Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, University of Michigan Health System, Ann Arbor, Michigan, USA 2 Division of Traumatology, Surgical Critical Care and Emergency Surgery, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA 3 Pulmonary and Critical Care Unit, Department of Medicine, Massachusetts General Hospital, Boston, Massachusetts, USA 7 Institute for Immunology, Perelman School of Medicine, University of Penns |
| AuthorAffiliation_xml | – name: 4 Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, University of Michigan Health System, Ann Arbor, Michigan, USA – name: 1 Division of Pulmonary, Allergy, and Critical Care and – name: 6 Division of Pediatric Critical Care, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pennsylvania, USA – name: 2 Division of Traumatology, Surgical Critical Care and Emergency Surgery, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA – name: 5 Department of Comparative Medicine, Penn State Health Milton S. Hershey Medical Center, Hershey, Pennsylvania, USA – name: 9 Department of Microbiology and Immunology, University of Michigan Medical School, Ann, Arbor, Michigan, USA – name: 3 Pulmonary and Critical Care Unit, Department of Medicine, Massachusetts General Hospital, Boston, Massachusetts, USA – name: 7 Institute for Immunology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA – name: 8 Weil Institute for Critical Care Research and Innovation, Ann Arbor, Michigan, USA |
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| Snippet | Red blood cells (RBCs), traditionally recognized for their role in transporting oxygen, play a pivotal role in the body's immune response by expressing TLR9... Red blood cells (RBCs), traditionally recognized for their role in transporting oxygen, play a pivotal role in the body’s immune response by expressing TLR9... |
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| SubjectTerms | Analysis Animals Coinfection - immunology Coinfection - microbiology Development and progression Disease Models, Animal DNA DNA, Bacterial - blood DNA, Bacterial - genetics DNA, Bacterial - immunology Erythrocytes Erythrocytes - immunology Erythrocytes - metabolism Erythrocytes - microbiology Erythrocytes - pathology Female Health aspects Humans Immune response Inflammation Interleukin-6 - blood Interleukin-6 - genetics Interleukin-6 - immunology Male Mice Mice, Knockout Pulmonology Sepsis Sepsis - blood Sepsis - genetics Sepsis - immunology Sepsis - microbiology Sepsis - pathology Toll-Like Receptor 9 - genetics Toll-Like Receptor 9 - immunology |
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| Title | Red Blood Cells Capture and Deliver Bacterial DNA to Drive Host Responses During Polymicrobial Sepsis |
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