NK cell-macrophage interactions in granulomas correlate with limited tuberculosis pathology

Development of novel vaccines and treatment approaches against tuberculosis are hampered by limited knowledge of what constitutes a protective immune response against Mycobacterium tuberculosis ( Mtb ). Granulomas are organized immune aggregates that form in the lung in response to mycobacterial inf...

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Veröffentlicht in:	PLoS pathogens Jg. 21; H. 8; S. e1012980
Hauptverfasser:	Niewold, Paula, IJsselsteijn, Marieke E., Dijkman, Karin, de Miranda, Noel, Ottenhoff, Tom H. M., Verreck, Frank A. W., Joosten, Simone A.
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	United States Public Library of Science 01.08.2025 Public Library of Science (PLoS)
Schlagworte:	Animal pathology Animals Antibiotics Biology and Life Sciences Cell Communication - immunology Cells Composition Correlation Cytometry Granuloma Granuloma - immunology Granuloma - microbiology Granuloma - pathology Granulomas Host-Pathogen Interactions - immunology Immune response Immune system Infections Killer Cells, Natural - immunology Killer Cells, Natural - pathology Lung - immunology Lung - microbiology Lung - pathology Lungs Lymphocytes Macaca mulatta Macrophages Macrophages - immunology Macrophages - pathology Medicine and Health Sciences Microenvironments Mycobacterium tuberculosis - immunology Natural killer cells Neutrophils Pathology Research and Analysis Methods Tuberculosis Tuberculosis - immunology Tuberculosis - pathology Tuberculosis, Pulmonary - immunology Tuberculosis, Pulmonary - pathology Vaccines
ISSN:	1553-7374, 1553-7366, 1553-7374
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Abstract	Development of novel vaccines and treatment approaches against tuberculosis are hampered by limited knowledge of what constitutes a protective immune response against Mycobacterium tuberculosis ( Mtb ). Granulomas are organized immune aggregates that form in the lung in response to mycobacterial infection and are an important site of pathogen-host interaction. The composition and cellular microenvironment within the granuloma impacts the bacterial control capacity. To identify protective responses in granulomas, imaging mass cytometry was used to study archived lung tissue from low dose Mtb -infected non-human primates presenting with various levels of disease. This approach revealed that granuloma composition is correlated with the severity of lung pathology. Granulomas of animals with limited lung pathology were enriched for NK cells showing increased interactions with tissue macrophages. This work improves our understanding of local immune interactions in the lung and how these correlate with severity of tuberculosis disease.
AbstractList	Development of novel vaccines and treatment approaches against tuberculosis are hampered by limited knowledge of what constitutes a protective immune response against Mycobacterium tuberculosis (Mtb). Granulomas are organized immune aggregates that form in the lung in response to mycobacterial infection and are an important site of pathogen-host interaction. The composition and cellular microenvironment within the granuloma impacts the bacterial control capacity. To identify protective responses in granulomas, imaging mass cytometry was used to study archived lung tissue from low dose Mtb-infected non-human primates presenting with various levels of disease. This approach revealed that granuloma composition is correlated with the severity of lung pathology. Granulomas of animals with limited lung pathology were enriched for NK cells showing increased interactions with tissue macrophages. This work improves our understanding of local immune interactions in the lung and how these correlate with severity of tuberculosis disease. Development of novel vaccines and treatment approaches against tuberculosis are hampered by limited knowledge of what constitutes a protective immune response against Mycobacterium tuberculosis (Mtb). Granulomas are organized immune aggregates that form in the lung in response to mycobacterial infection and are an important site of pathogen-host interaction. The composition and cellular microenvironment within the granuloma impacts the bacterial control capacity. To identify protective responses in granulomas, imaging mass cytometry was used to study archived lung tissue from low dose Mtb-infected non-human primates presenting with various levels of disease. This approach revealed that granuloma composition is correlated with the severity of lung pathology. Granulomas of animals with limited lung pathology were enriched for NK cells showing increased interactions with tissue macrophages. This work improves our understanding of local immune interactions in the lung and how these correlate with severity of tuberculosis disease.Development of novel vaccines and treatment approaches against tuberculosis are hampered by limited knowledge of what constitutes a protective immune response against Mycobacterium tuberculosis (Mtb). Granulomas are organized immune aggregates that form in the lung in response to mycobacterial infection and are an important site of pathogen-host interaction. The composition and cellular microenvironment within the granuloma impacts the bacterial control capacity. To identify protective responses in granulomas, imaging mass cytometry was used to study archived lung tissue from low dose Mtb-infected non-human primates presenting with various levels of disease. This approach revealed that granuloma composition is correlated with the severity of lung pathology. Granulomas of animals with limited lung pathology were enriched for NK cells showing increased interactions with tissue macrophages. This work improves our understanding of local immune interactions in the lung and how these correlate with severity of tuberculosis disease. Development of novel vaccines and treatment approaches against tuberculosis are hampered by limited knowledge of what constitutes a protective immune response against Mycobacterium tuberculosis (Mtb). Granulomas are organized immune aggregates that form in the lung in response to mycobacterial infection and are an important site of pathogen-host interaction. The composition and cellular microenvironment within the granuloma impacts the bacterial control capacity. To identify protective responses in granulomas, imaging mass cytometry was used to study archived lung tissue from low dose Mtb-infected non-human primates presenting with various levels of disease. This approach revealed that granuloma composition is correlated with the severity of lung pathology. Granulomas of animals with limited lung pathology were enriched for NK cells showing increased interactions with tissue macrophages. This work improves our understanding of local immune interactions in the lung and how these correlate with severity of tuberculosis disease. Tuberculosis remains the deadliest infectious disease in the world with 10 million new infections and 1.5 million deaths annually. The existing vaccine is not effective enough to halt the tuberculosis epidemic. In order to develop an improved vaccine, more complete and detailed knowledge on the immune responses that can successfully protect against tuberculosis is required. Individuals that are exposed to Mycobacterium tuberculosis, the pathogen that causes tuberculosis disease, fall along a spectrum, with some individuals showing a strong innate capacity to protect against disease, while others fall ill. By studying these differences in a model organism, namely non-human primates, we can learn about protective immune responses. In primates with limited disease, the immune cell aggregates surrounding the bacteria in the lung contained more NK cells than were found in severe disease. In addition, interactions between NK cells and macrophages, cells that can eat bacteria, were seen a lot more in protected animals. This suggests that the interaction between NK cell and macrophages contributes to controlling tuberculosis disease, this knowledge can contribute to improved vaccine strategies.
Author	de Miranda, Noel IJsselsteijn, Marieke E. Dijkman, Karin Ottenhoff, Tom H. M. Joosten, Simone A. Verreck, Frank A. W. Niewold, Paula
AuthorAffiliation	2 Department of Pathology, Leiden University Medical Center, Leiden, The Netherlands 1 Leiden University Center for Infectious Diseases, Leiden University Medical Center, Leiden, The Netherlands 4 Section of TB Research and Immunology, Department of Parasitology, Biomedical Primate Research Center (BPRC), Rijswijk, The Netherlands 3 Department of Immunology, Leiden University Medical Center, Leiden, The Netherlands Portland VA Medical Center, Oregon Health and Science University, UNITED STATES OF AMERICA
AuthorAffiliation_xml	– name: 3 Department of Immunology, Leiden University Medical Center, Leiden, The Netherlands – name: 4 Section of TB Research and Immunology, Department of Parasitology, Biomedical Primate Research Center (BPRC), Rijswijk, The Netherlands – name: 2 Department of Pathology, Leiden University Medical Center, Leiden, The Netherlands – name: Portland VA Medical Center, Oregon Health and Science University, UNITED STATES OF AMERICA – name: 1 Leiden University Center for Infectious Diseases, Leiden University Medical Center, Leiden, The Netherlands
Author_xml	– sequence: 1 givenname: Paula orcidid: 0000-0002-9614-4601 surname: Niewold fullname: Niewold, Paula – sequence: 2 givenname: Marieke E. surname: IJsselsteijn fullname: IJsselsteijn, Marieke E. – sequence: 3 givenname: Karin surname: Dijkman fullname: Dijkman, Karin – sequence: 4 givenname: Noel surname: de Miranda fullname: de Miranda, Noel – sequence: 5 givenname: Tom H. M. surname: Ottenhoff fullname: Ottenhoff, Tom H. M. – sequence: 6 givenname: Frank A. W. surname: Verreck fullname: Verreck, Frank A. W. – sequence: 7 givenname: Simone A. orcidid: 0000-0002-9878-0863 surname: Joosten fullname: Joosten, Simone A.
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/40749077$$D View this record in MEDLINE/PubMed
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SubjectTerms	Animal pathology Animals Antibiotics Biology and Life Sciences Cell Communication - immunology Cells Composition Correlation Cytometry Granuloma Granuloma - immunology Granuloma - microbiology Granuloma - pathology Granulomas Host-Pathogen Interactions - immunology Immune response Immune system Infections Killer Cells, Natural - immunology Killer Cells, Natural - pathology Lung - immunology Lung - microbiology Lung - pathology Lungs Lymphocytes Macaca mulatta Macrophages Macrophages - immunology Macrophages - pathology Medicine and Health Sciences Microenvironments Mycobacterium tuberculosis - immunology Natural killer cells Neutrophils Pathology Research and Analysis Methods Tuberculosis Tuberculosis - immunology Tuberculosis - pathology Tuberculosis, Pulmonary - immunology Tuberculosis, Pulmonary - pathology Vaccines
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Title	NK cell-macrophage interactions in granulomas correlate with limited tuberculosis pathology
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