Macrophage Epithelial Reprogramming Underlies Mycobacterial Granuloma Formation and Promotes Infection
Mycobacterium tuberculosis infection in humans triggers formation of granulomas, which are tightly organized immune cell aggregates that are the central structure of tuberculosis. Infected and uninfected macrophages interdigitate, assuming an altered, flattened appearance. Although pathologists have...
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Published in | Immunity (Cambridge, Mass.) Vol. 45; no. 4; pp. 861 - 876 |
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Main Authors | , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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United States
Elsevier Inc
18.10.2016
Elsevier Limited |
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Abstract | Mycobacterium tuberculosis infection in humans triggers formation of granulomas, which are tightly organized immune cell aggregates that are the central structure of tuberculosis. Infected and uninfected macrophages interdigitate, assuming an altered, flattened appearance. Although pathologists have described these changes for over a century, the molecular and cellular programs underlying this transition are unclear. Here, using the zebrafish-Mycobacterium marinum model, we found that mycobacterial granuloma formation is accompanied by macrophage induction of canonical epithelial molecules and structures. We identified fundamental macrophage reprogramming events that parallel E-cadherin-dependent mesenchymal-epithelial transitions. Macrophage-specific disruption of E-cadherin function resulted in disordered granuloma formation, enhanced immune cell access, decreased bacterial burden, and increased host survival, suggesting that the granuloma can also serve a bacteria-protective role. Granuloma macrophages in humans with tuberculosis were similarly transformed. Thus, during mycobacterial infection, granuloma macrophages are broadly reprogrammed by epithelial modules, and this reprogramming alters the trajectory of infection and the associated immune response.
[Display omitted]
•Macrophages mobilize classical epithelial modules during granuloma formation•Macrophage reprogramming shares features of mesenchymal-epithelial transitions•Inhibition of macrophage epithelialization leads to disordered granulomas•Granuloma disruption increases immune access and promotes host survival
A hallmark of tuberculosis is aggregation of macrophages into a structure termed the granuloma. Cronan et al. show that macrophages deploy classical epithelialization pathways to construct mycobacterial granulomas. This reprogramming is host detrimental, as macrophage-specific inhibition of the process enhances host survival and immune cell access and reduces bacterial burden. |
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AbstractList | Mycobacterium tuberculosis
infection in humans triggers formation of granulomas, tightly organized immune cell aggregates that are the central structure of tuberculosis. Infected and uninfected macrophages interdigitate, assuming an altered, flattened appearance. Although pathologists have described these changes for over a century, the molecular and cellular programs underlying this transition are unclear. Here, using the zebrafish-
Mycobacterium marinum
model, we found that mycobacterial granuloma formation is accompanied by macrophage induction of canonical epithelial molecules and structures. We identified fundamental macrophage reprogramming events that parallel E-cadherin-dependent mesenchymal-epithelial transitions. Macrophage-specific disruption of E-cadherin function resulted in disordered granuloma formation, enhanced immune cell access, decreased bacterial burden and increased host survival, suggesting that the granuloma can also serve a bacteria-protective role. Granuloma macrophages in humans with tuberculosis were similarly transformed. Thus, during mycobacterial infection, granuloma macrophages are broadly reprogrammed by epithelial modules, and this reprogramming alters the trajectory of infection and the associated immune response. Mycobacterium tuberculosis infection in humans triggers formation of granulomas, which are tightly organized immune cell aggregates that are the central structure of tuberculosis. Infected and uninfected macrophages interdigitate, assuming an altered, flattened appearance. Although pathologists have described these changes for over a century, the molecular and cellular programs underlying this transition are unclear. Here, using the zebrafish-Mycobacterium marinum model, we found that mycobacterial granuloma formation is accompanied by macrophage induction of canonical epithelial molecules and structures. We identified fundamental macrophage reprogramming events that parallel E-cadherin-dependent mesenchymal-epithelial transitions. Macrophage-specific disruption of E-cadherin function resulted in disordered granuloma formation, enhanced immune cell access, decreased bacterial burden, and increased host survival, suggesting that the granuloma can also serve a bacteria-protective role. Granuloma macrophages in humans with tuberculosis were similarly transformed. Thus, during mycobacterial infection, granuloma macrophages are broadly reprogrammed by epithelial modules, and this reprogramming alters the trajectory of infection and the associated immune response. Mycobacterium tuberculosis infection in humans triggers formation of granulomas, which are tightly organized immune cell aggregates that are the central structure of tuberculosis. Infected and uninfected macrophages interdigitate, assuming an altered, flattened appearance. Although pathologists have described these changes for over a century, the molecular and cellular programs underlying this transition are unclear. Here, using the zebrafish-Mycobacterium marinum model, we found that mycobacterial granuloma formation is accompanied by macrophage induction of canonical epithelial molecules and structures. We identified fundamental macrophage reprogramming events that parallel E-cadherin-dependent mesenchymal-epithelial transitions. Macrophage-specific disruption of E-cadherin function resulted in disordered granuloma formation, enhanced immune cell access, decreased bacterial burden, and increased host survival, suggesting that the granuloma can also serve a bacteria-protective role. Granuloma macrophages in humans with tuberculosis were similarly transformed. Thus, during mycobacterial infection, granuloma macrophages are broadly reprogrammed by epithelial modules, and this reprogramming alters the trajectory of infection and the associated immune response. [Display omitted] •Macrophages mobilize classical epithelial modules during granuloma formation•Macrophage reprogramming shares features of mesenchymal-epithelial transitions•Inhibition of macrophage epithelialization leads to disordered granulomas•Granuloma disruption increases immune access and promotes host survival A hallmark of tuberculosis is aggregation of macrophages into a structure termed the granuloma. Cronan et al. show that macrophages deploy classical epithelialization pathways to construct mycobacterial granulomas. This reprogramming is host detrimental, as macrophage-specific inhibition of the process enhances host survival and immune cell access and reduces bacterial burden. Mycobacterium tuberculosisinfection in humans triggers formation of granulomas, which are tightly organized immune cell aggregates that are the central structure of tuberculosis. Infected and uninfected macrophages interdigitate, assuming an altered, flattened appearance. Although pathologists have described these changes for over a century, the molecular and cellular programs underlying this transition are unclear. Here, using the zebrafish-Mycobacterium marinummodel, we found that mycobacterial granuloma formation is accompanied by macrophage induction of canonical epithelial molecules and structures. We identified fundamental macrophage reprogramming events that parallel E-cadherin-dependent mesenchymal-epithelial transitions. Macrophage-specific disruption of E-cadherin function resulted in disordered granuloma formation, enhanced immune cell access, decreased bacterial burden, and increased host survival, suggesting that the granuloma can also serve a bacteria-protective role. Granuloma macrophages in humans with tuberculosis were similarly transformed. Thus, during mycobacterial infection, granuloma macrophages are broadly reprogrammed by epithelial modules, and this reprogramming alters the trajectory of infection and the associated immune response. |
Author | Turner, Joanne Medvitz, Neil A. Jurcic Smith, Kristen L. Rosenberg, Allison F. Miller, Sara E. Johnson, Matthew G. Tobin, David M. Fraser, Scott E. Oehlers, Stefan H. Cronan, Mark R. Trinh, Le A. Saelens, Joseph W. Sisk, Dana M. Lee, Sunhee Stout, Jason E. Madden, John F. Beerman, Rebecca W. |
AuthorAffiliation | 3 Department of Medicine, Duke University School of Medicine, Durham, NC 27710, USA 6 Molecular and Computational Biology and Translational Imaging Center, University of Southern California, Los Angeles, CA 90089, USA 7 Department of Microbial Infection and Immunity, The Ohio State University, Columbus, OH 43210 5 Department of Immunology, Duke University School of Medicine, Durham, NC 27710, USA 4 Department of Pathology, Duke University School of Medicine, Durham, NC 27710, USA 8 Center for Microbial Interface Biology, The Ohio State University, Columbus, OH 43210 1 Department of Molecular Genetics and Microbiologym, Duke University School of Medicine, Durham, NC 27710, USA 2 Division of Infectious Diseases, Duke University School of Medicine, Durham, NC 27710, USA |
AuthorAffiliation_xml | – name: 4 Department of Pathology, Duke University School of Medicine, Durham, NC 27710, USA – name: 5 Department of Immunology, Duke University School of Medicine, Durham, NC 27710, USA – name: 7 Department of Microbial Infection and Immunity, The Ohio State University, Columbus, OH 43210 – name: 1 Department of Molecular Genetics and Microbiologym, Duke University School of Medicine, Durham, NC 27710, USA – name: 3 Department of Medicine, Duke University School of Medicine, Durham, NC 27710, USA – name: 6 Molecular and Computational Biology and Translational Imaging Center, University of Southern California, Los Angeles, CA 90089, USA – name: 2 Division of Infectious Diseases, Duke University School of Medicine, Durham, NC 27710, USA – name: 8 Center for Microbial Interface Biology, The Ohio State University, Columbus, OH 43210 |
Author_xml | – sequence: 1 givenname: Mark R. surname: Cronan fullname: Cronan, Mark R. organization: Department of Molecular Genetics and Microbiology, Duke University School of Medicine, Durham, NC 27710, USA – sequence: 2 givenname: Rebecca W. surname: Beerman fullname: Beerman, Rebecca W. organization: Department of Molecular Genetics and Microbiology, Duke University School of Medicine, Durham, NC 27710, USA – sequence: 3 givenname: Allison F. surname: Rosenberg fullname: Rosenberg, Allison F. organization: Department of Molecular Genetics and Microbiology, Duke University School of Medicine, Durham, NC 27710, USA – sequence: 4 givenname: Joseph W. surname: Saelens fullname: Saelens, Joseph W. organization: Department of Molecular Genetics and Microbiology, Duke University School of Medicine, Durham, NC 27710, USA – sequence: 5 givenname: Matthew G. surname: Johnson fullname: Johnson, Matthew G. organization: Division of Infectious Diseases, Duke University School of Medicine, Durham, NC 27710, USA – sequence: 6 givenname: Stefan H. surname: Oehlers fullname: Oehlers, Stefan H. organization: Department of Molecular Genetics and Microbiology, Duke University School of Medicine, Durham, NC 27710, USA – sequence: 7 givenname: Dana M. surname: Sisk fullname: Sisk, Dana M. organization: Department of Molecular Genetics and Microbiology, Duke University School of Medicine, Durham, NC 27710, USA – sequence: 8 givenname: Kristen L. surname: Jurcic Smith fullname: Jurcic Smith, Kristen L. organization: Department of Molecular Genetics and Microbiology, Duke University School of Medicine, Durham, NC 27710, USA – sequence: 9 givenname: Neil A. surname: Medvitz fullname: Medvitz, Neil A. organization: Department of Pathology, Duke University School of Medicine, Durham, NC 27710, USA – sequence: 10 givenname: Sara E. surname: Miller fullname: Miller, Sara E. organization: Department of Pathology, Duke University School of Medicine, Durham, NC 27710, USA – sequence: 11 givenname: Le A. surname: Trinh fullname: Trinh, Le A. organization: Molecular and Computational Biology and Translational Imaging Center, University of Southern California, Los Angeles, CA 90089, USA – sequence: 12 givenname: Scott E. surname: Fraser fullname: Fraser, Scott E. organization: Molecular and Computational Biology and Translational Imaging Center, University of Southern California, Los Angeles, CA 90089, USA – sequence: 13 givenname: John F. surname: Madden fullname: Madden, John F. organization: Department of Pathology, Duke University School of Medicine, Durham, NC 27710, USA – sequence: 14 givenname: Joanne surname: Turner fullname: Turner, Joanne organization: Department of Microbial Infection and Immunity, The Ohio State University, Columbus, OH 43210, USA – sequence: 15 givenname: Jason E. surname: Stout fullname: Stout, Jason E. organization: Division of Infectious Diseases, Duke University School of Medicine, Durham, NC 27710, USA – sequence: 16 givenname: Sunhee surname: Lee fullname: Lee, Sunhee organization: Department of Molecular Genetics and Microbiology, Duke University School of Medicine, Durham, NC 27710, USA – sequence: 17 givenname: David M. surname: Tobin fullname: Tobin, David M. email: david.tobin@duke.edu organization: Department of Molecular Genetics and Microbiology, Duke University School of Medicine, Durham, NC 27710, USA |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27760340$$D View this record in MEDLINE/PubMed |
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Snippet | Mycobacterium tuberculosis infection in humans triggers formation of granulomas, which are tightly organized immune cell aggregates that are the central... Mycobacterium tuberculosisinfection in humans triggers formation of granulomas, which are tightly organized immune cell aggregates that are the central... Mycobacterium tuberculosis infection in humans triggers formation of granulomas, tightly organized immune cell aggregates that are the central structure of... |
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SubjectTerms | Animals Cadherins - immunology Epithelium - immunology Epithelium - microbiology Experiments Granuloma - immunology Granuloma - microbiology Histology Immunoglobulins Infections Keratin Laboratories Macrophages - immunology Macrophages - microbiology Microscopy Mycobacterium marinum - immunology Mycobacterium tuberculosis Mycobacterium tuberculosis - immunology Pathology Tuberculosis Zebrafish |
Title | Macrophage Epithelial Reprogramming Underlies Mycobacterial Granuloma Formation and Promotes Infection |
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