Cell Reports (Jul 2022)
Rapid GPR183-mediated recruitment of eosinophils to the lung after Mycobacterium tuberculosis infection
- 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
Affiliations
- Andrea C. Bohrer
- Inflammation 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
- Ehydel Castro
- Inflammation 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
- Claire E. Tocheny
- Inflammation 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
- Maike Assmann
- Inflammation 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
- Benjamin Schwarz
- Immunity to Pulmonary Pathogens Section, Laboratory of Bacteriology, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Hamilton, MT 59840, USA
- Eric Bohrnsen
- Immunity to Pulmonary Pathogens Section, Laboratory of Bacteriology, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Hamilton, MT 59840, USA
- Michelle A. Makiya
- Human Eosinophil Section, Laboratory of Parasitic Diseases, NIAID, NIH, Bethesda, MD 20892, USA
- Fanny Legrand
- Human Eosinophil Section, Laboratory of Parasitic Diseases, NIAID, NIH, Bethesda, MD 20892, USA
- Kerry L. Hilligan
- Immunobiology Section, Laboratory of Parasitic Diseases, NIAID, NIH, Bethesda, MD 20892, USA
- Paul J. Baker
- Inflammation 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
- Flor Torres-Juarez
- Inflammation 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
- Zhidong Hu
- Department 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, China
- Hui Ma
- Department 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, China
- Lin Wang
- TB 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, China
- Liangfei Niu
- Department 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, China
- Zilu Wen
- TB 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, China
- Sang H. Lee
- Intracellular Parasite Biology Section, Laboratory of Parasitic Diseases, NIAID, NIH, Bethesda, MD 20892, USA
- Olena Kamenyeva
- Biological Imaging Section, Research Technologies Branch, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Bethesda, MD 20892, USA
- Keith D. Kauffman
- T Lymphocyte Biology Section, Laboratory of Parasitic Disease, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Bethesda, MD 20892, USA
- Michele Donato
- Institute 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, USA
- Alan Sher
- Immunobiology Section, Laboratory of Parasitic Diseases, NIAID, NIH, Bethesda, MD 20892, USA
- Daniel L. Barber
- T Lymphocyte Biology Section, Laboratory of Parasitic Disease, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Bethesda, MD 20892, USA
- Laura E. Via
- Tuberculosis 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, USA
- Thomas J. Scriba
- South African Tuberculosis Vaccine Initiative, Institute of Infectious Disease & Molecular Medicine and Division of Immunology, Department of Pathology, University of Cape Town, Observatory, 7925, South Africa
- Purvesh Khatri
- Institute 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, USA
- Yanzheng Song
- TB 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, China
- Ka-Wing Wong
- Department 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, China
- Catharine M. Bosio
- Immunity to Pulmonary Pathogens Section, Laboratory of Bacteriology, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Hamilton, MT 59840, USA
- Amy D. Klion
- Human Eosinophil Section, Laboratory of Parasitic Diseases, NIAID, NIH, Bethesda, MD 20892, USA
- Katrin D. Mayer-Barber
- Inflammation 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 author
- Journal volume & issue
-
Vol. 40,
no. 4
p. 111144
Abstract
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.
