Rapid GPR183-mediated recruitment of eosinophils to the lung after Mycobacterium tuberculosis infection
Summary: Influx of eosinophils into the lungs is typically associated with type II responses during allergy and fungal and parasitic infections. However, we previously reported that eosinophils accumulate in lung lesions during type I inflammatory responses to Mycobacterium tuberculosis (Mtb) in hum...
| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2022-07-01
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| Series: | Cell Reports |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124722009536 |
| _version_ | 1818017687828168704 |
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| author | Andrea C. Bohrer Ehydel Castro Claire E. Tocheny Maike Assmann Benjamin Schwarz Eric Bohrnsen Michelle A. Makiya Fanny Legrand Kerry L. Hilligan Paul J. Baker Flor Torres-Juarez Zhidong Hu Hui Ma Lin Wang Liangfei Niu Zilu Wen Sang H. Lee Olena Kamenyeva Keith D. Kauffman Michele Donato Alan Sher Daniel L. Barber Laura E. Via Thomas J. Scriba Purvesh Khatri Yanzheng Song Ka-Wing Wong Catharine M. Bosio Amy D. Klion Katrin D. Mayer-Barber |
| author_facet | Andrea C. Bohrer Ehydel Castro Claire E. Tocheny Maike Assmann Benjamin Schwarz Eric Bohrnsen Michelle A. Makiya Fanny Legrand Kerry L. Hilligan Paul J. Baker Flor Torres-Juarez Zhidong Hu Hui Ma Lin Wang Liangfei Niu Zilu Wen Sang H. Lee Olena Kamenyeva Keith D. Kauffman Michele Donato Alan Sher Daniel L. Barber Laura E. Via Thomas J. Scriba Purvesh Khatri Yanzheng Song Ka-Wing Wong Catharine M. Bosio Amy D. Klion Katrin D. Mayer-Barber |
| author_sort | Andrea C. Bohrer |
| collection | DOAJ |
| description | Summary: Influx of eosinophils into the lungs is typically associated with type II responses during allergy and fungal and parasitic infections. However, we previously reported that eosinophils accumulate in lung lesions during type I inflammatory responses to Mycobacterium tuberculosis (Mtb) in humans, macaques, and mice, in which they support host resistance. Here we show eosinophils migrate into the lungs of macaques and mice as early as one week after Mtb exposure. In mice this influx is CCR3 independent and instead requires cell-intrinsic expression of the oxysterol receptor GPR183, which is highly expressed on human and macaque eosinophils. Murine eosinophils interact directly with bacilli-laden alveolar macrophages, which upregulate the oxysterol-synthesizing enzyme Ch25h, and eosinophil recruitment is impaired in Ch25h-deficient mice. Our findings show that eosinophils are among the earliest cells from circulation to sense and respond to Mtb infection of alveolar macrophages and reveal a role for GPR183 in the migration of eosinophils into lung tissue. |
| first_indexed | 2024-04-14T07:30:03Z |
| format | Article |
| id | doaj.art-4cc9d670630f4c0ab39dbfc2f415fe75 |
| institution | Directory Open Access Journal |
| issn | 2211-1247 |
| language | English |
| last_indexed | 2024-04-14T07:30:03Z |
| publishDate | 2022-07-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj.art-4cc9d670630f4c0ab39dbfc2f415fe752022-12-22T02:05:53ZengElsevierCell Reports2211-12472022-07-01404111144Rapid GPR183-mediated recruitment of eosinophils to the lung after Mycobacterium tuberculosis infectionAndrea C. Bohrer0Ehydel Castro1Claire E. Tocheny2Maike Assmann3Benjamin Schwarz4Eric Bohrnsen5Michelle A. Makiya6Fanny Legrand7Kerry L. Hilligan8Paul J. Baker9Flor Torres-Juarez10Zhidong Hu11Hui Ma12Lin Wang13Liangfei Niu14Zilu Wen15Sang H. Lee16Olena Kamenyeva17Keith D. Kauffman18Michele Donato19Alan Sher20Daniel L. Barber21Laura E. Via22Thomas J. Scriba23Purvesh Khatri24Yanzheng Song25Ka-Wing Wong26Catharine M. Bosio27Amy D. Klion28Katrin D. Mayer-Barber29Inflammation and Innate Immunity Unit, Laboratory of Clinical Immunology and Microbiology, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Bethesda, MD 20892, USAInflammation and Innate Immunity Unit, Laboratory of Clinical Immunology and Microbiology, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Bethesda, MD 20892, USAInflammation and Innate Immunity Unit, Laboratory of Clinical Immunology and Microbiology, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Bethesda, MD 20892, USAInflammation and Innate Immunity Unit, Laboratory of Clinical Immunology and Microbiology, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Bethesda, MD 20892, USAImmunity to Pulmonary Pathogens Section, Laboratory of Bacteriology, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Hamilton, MT 59840, USAImmunity to Pulmonary Pathogens Section, Laboratory of Bacteriology, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Hamilton, MT 59840, USAHuman Eosinophil Section, Laboratory of Parasitic Diseases, NIAID, NIH, Bethesda, MD 20892, USAHuman Eosinophil Section, Laboratory of Parasitic Diseases, NIAID, NIH, Bethesda, MD 20892, USAImmunobiology Section, Laboratory of Parasitic Diseases, NIAID, NIH, Bethesda, MD 20892, USAInflammation and Innate Immunity Unit, Laboratory of Clinical Immunology and Microbiology, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Bethesda, MD 20892, USAInflammation and Innate Immunity Unit, Laboratory of Clinical Immunology and Microbiology, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Bethesda, MD 20892, USADepartment of Scientific Research, Shanghai Public Health Clinical Center (SPHCC), Fudan University, Shanghai 201508, China; TB Center, Shanghai Emerging and Re-Emerging Infectious Disease Institute, Fudan University, Shanghai 201508, ChinaDepartment of Scientific Research, Shanghai Public Health Clinical Center (SPHCC), Fudan University, Shanghai 201508, China; TB Center, Shanghai Emerging and Re-Emerging Infectious Disease Institute, Fudan University, Shanghai 201508, ChinaTB Center, Shanghai Emerging and Re-Emerging Infectious Disease Institute, Fudan University, Shanghai 201508, China; Department of Thoracic Surgery, Shanghai Public Health Clinical Center (SPHCC), Fudan University, Shanghai 201508, ChinaDepartment of Scientific Research, Shanghai Public Health Clinical Center (SPHCC), Fudan University, Shanghai 201508, China; TB Center, Shanghai Emerging and Re-Emerging Infectious Disease Institute, Fudan University, Shanghai 201508, ChinaTB Center, Shanghai Emerging and Re-Emerging Infectious Disease Institute, Fudan University, Shanghai 201508, China; Department of Thoracic Surgery, Shanghai Public Health Clinical Center (SPHCC), Fudan University, Shanghai 201508, ChinaIntracellular Parasite Biology Section, Laboratory of Parasitic Diseases, NIAID, NIH, Bethesda, MD 20892, USABiological Imaging Section, Research Technologies Branch, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Bethesda, MD 20892, USAT Lymphocyte Biology Section, Laboratory of Parasitic Disease, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Bethesda, MD 20892, USAInstitute for Immunity, Transplantation and Infection, School of Medicine, Stanford University, Stanford, CA 94305, USA; Center for Biomedical Informatics Research, Department of Medicine, Stanford University, Stanford, CA 94305, USAImmunobiology Section, Laboratory of Parasitic Diseases, NIAID, NIH, Bethesda, MD 20892, USAT Lymphocyte Biology Section, Laboratory of Parasitic Disease, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Bethesda, MD 20892, USATuberculosis Imaging Program (TBIP), Division of Intramural Research, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Bethesda, MD 20892, USA; Tuberculosis Research Section, LCIM, NIAID, NIH, Bethesda, MD 20892, USASouth African Tuberculosis Vaccine Initiative, Institute of Infectious Disease & Molecular Medicine and Division of Immunology, Department of Pathology, University of Cape Town, Observatory, 7925, South AfricaInstitute for Immunity, Transplantation and Infection, School of Medicine, Stanford University, Stanford, CA 94305, USA; Center for Biomedical Informatics Research, Department of Medicine, Stanford University, Stanford, CA 94305, USATB Center, Shanghai Emerging and Re-Emerging Infectious Disease Institute, Fudan University, Shanghai 201508, China; Department of Thoracic Surgery, Shanghai Public Health Clinical Center (SPHCC), Fudan University, Shanghai 201508, ChinaDepartment of Scientific Research, Shanghai Public Health Clinical Center (SPHCC), Fudan University, Shanghai 201508, China; TB Center, Shanghai Emerging and Re-Emerging Infectious Disease Institute, Fudan University, Shanghai 201508, ChinaImmunity to Pulmonary Pathogens Section, Laboratory of Bacteriology, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Hamilton, MT 59840, USAHuman Eosinophil Section, Laboratory of Parasitic Diseases, NIAID, NIH, Bethesda, MD 20892, USAInflammation and Innate Immunity Unit, Laboratory of Clinical Immunology and Microbiology, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Bethesda, MD 20892, USA; Corresponding authorSummary: Influx of eosinophils into the lungs is typically associated with type II responses during allergy and fungal and parasitic infections. However, we previously reported that eosinophils accumulate in lung lesions during type I inflammatory responses to Mycobacterium tuberculosis (Mtb) in humans, macaques, and mice, in which they support host resistance. Here we show eosinophils migrate into the lungs of macaques and mice as early as one week after Mtb exposure. In mice this influx is CCR3 independent and instead requires cell-intrinsic expression of the oxysterol receptor GPR183, which is highly expressed on human and macaque eosinophils. Murine eosinophils interact directly with bacilli-laden alveolar macrophages, which upregulate the oxysterol-synthesizing enzyme Ch25h, and eosinophil recruitment is impaired in Ch25h-deficient mice. Our findings show that eosinophils are among the earliest cells from circulation to sense and respond to Mtb infection of alveolar macrophages and reveal a role for GPR183 in the migration of eosinophils into lung tissue.http://www.sciencedirect.com/science/article/pii/S2211124722009536CP: ImmunologyCP: Microbiology |
| spellingShingle | Andrea C. Bohrer Ehydel Castro Claire E. Tocheny Maike Assmann Benjamin Schwarz Eric Bohrnsen Michelle A. Makiya Fanny Legrand Kerry L. Hilligan Paul J. Baker Flor Torres-Juarez Zhidong Hu Hui Ma Lin Wang Liangfei Niu Zilu Wen Sang H. Lee Olena Kamenyeva Keith D. Kauffman Michele Donato Alan Sher Daniel L. Barber Laura E. Via Thomas J. Scriba Purvesh Khatri Yanzheng Song Ka-Wing Wong Catharine M. Bosio Amy D. Klion Katrin D. Mayer-Barber Rapid GPR183-mediated recruitment of eosinophils to the lung after Mycobacterium tuberculosis infection Cell Reports CP: Immunology CP: Microbiology |
| title | Rapid GPR183-mediated recruitment of eosinophils to the lung after Mycobacterium tuberculosis infection |
| title_full | Rapid GPR183-mediated recruitment of eosinophils to the lung after Mycobacterium tuberculosis infection |
| title_fullStr | Rapid GPR183-mediated recruitment of eosinophils to the lung after Mycobacterium tuberculosis infection |
| title_full_unstemmed | Rapid GPR183-mediated recruitment of eosinophils to the lung after Mycobacterium tuberculosis infection |
| title_short | Rapid GPR183-mediated recruitment of eosinophils to the lung after Mycobacterium tuberculosis infection |
| title_sort | rapid gpr183 mediated recruitment of eosinophils to the lung after mycobacterium tuberculosis infection |
| topic | CP: Immunology CP: Microbiology |
| url | http://www.sciencedirect.com/science/article/pii/S2211124722009536 |
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