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; Tuberculosis Imaging Program; 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

doi:10.1016/j.celrep.2022.111144

Rapid GPR183-mediated recruitment of eosinophils to the lung after Mycobacterium tuberculosis infection

Cell Rep. 2022 Jul 26;40(4):111144. doi: 10.1016/j.celrep.2022.111144.

Authors

Andrea C Bohrer¹, Ehydel Castro¹, Claire E Tocheny¹, Maike Assmann¹, Benjamin Schwarz², Eric Bohrnsen², Michelle A Makiya³, Fanny Legrand³, Kerry L Hilligan⁴, Paul J Baker¹, Flor Torres-Juarez¹, Zhidong Hu⁵, Hui Ma⁵, Lin Wang⁶, Liangfei Niu⁵, Zilu Wen⁶, Sang H Lee⁷, Olena Kamenyeva⁸; Tuberculosis Imaging Program⁹; Keith D Kauffman¹⁰, Michele Donato¹¹, Alan Sher⁴, Daniel L Barber¹⁰, Laura E Via¹², Thomas J Scriba¹³, Purvesh Khatri¹¹, Yanzheng Song⁶, Ka-Wing Wong⁵, Catharine M Bosio², Amy D Klion³, Katrin D Mayer-Barber¹⁴

Affiliations

¹ 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.
² 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.
³ Human Eosinophil Section, Laboratory of Parasitic Diseases, NIAID, NIH, Bethesda, MD 20892, USA.
⁴ Immunobiology Section, Laboratory of Parasitic Diseases, NIAID, NIH, Bethesda, MD 20892, USA.
⁵ 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.
⁶ 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.
⁷ Intracellular Parasite Biology Section, Laboratory of Parasitic Diseases, NIAID, NIH, Bethesda, MD 20892, USA.
⁸ Biological Imaging Section, Research Technologies Branch, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Bethesda, MD 20892, USA.
⁹ 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.
¹⁰ 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.
¹¹ 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.
¹² 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.
¹³ 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.
¹⁴ 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. Electronic address: mayerk@niaid.nih.gov.

Abstract

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.

Keywords: CCR3; CP: Immunology; CP: Microbiology; Ch25h; GPR183; Mycobacterium tuberculosis; NHP; alveolar macrophages; bacterial infection; eosinophils; eotaxin; granulocytes; lung; neutrophils; nonhuman primate; oxysterols; rhesus macaque.

Publication types

Research Support, Non-U.S. Gov't
Research Support, N.I.H., Intramural

MeSH terms

Animals
Eosinophils / metabolism
Humans
Lung / pathology
Macrophages, Alveolar
Mice
Mycobacterium tuberculosis* / physiology
Receptors, G-Protein-Coupled / metabolism
Tuberculosis* / pathology

Substances

GPR183 protein, human
Gpr183 protein, mouse
Receptors, G-Protein-Coupled

Abstract

Publication types

MeSH terms

Substances

Grants and funding