Interferon-gamma-activated macrophages infected with Burkholderia cenocepacia process and present bacterial antigens to T-cells by class I and II major histocompatibility complex molecules
Burkholderia cenocepacia is an emerging opportunistic pathogen for people with cystic fibrosis and chronic granulomatous disease. Intracellular survival in macrophages within a membrane-bound vacuole (BcCV) that delays acidification and maturation into lysosomes is a hallmark of B. cenocepacia infec...
Saved in:
| Main Authors: | , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Taylor & Francis Group
2020-01-01
|
| Series: | Emerging Microbes and Infections |
| Subjects: | |
| Online Access: | https://www.tandfonline.com/doi/10.1080/22221751.2020.1818632 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1850150281705160704 |
|---|---|
| author | Roberto Rosales-Reyes Paola Garza-Villafuerte Daniela Vences-Vences Daniel F. Aubert Rubi Aca-Teutle Vianney F. Ortiz-Navarrete Laura C. Bonifaz Julio Cesar Carrero-Sánchez Alfonso Olivos-García Miguel A. Valvano José Ignacio Santos-Preciado |
| author_facet | Roberto Rosales-Reyes Paola Garza-Villafuerte Daniela Vences-Vences Daniel F. Aubert Rubi Aca-Teutle Vianney F. Ortiz-Navarrete Laura C. Bonifaz Julio Cesar Carrero-Sánchez Alfonso Olivos-García Miguel A. Valvano José Ignacio Santos-Preciado |
| author_sort | Roberto Rosales-Reyes |
| collection | DOAJ |
| description | Burkholderia cenocepacia is an emerging opportunistic pathogen for people with cystic fibrosis and chronic granulomatous disease. Intracellular survival in macrophages within a membrane-bound vacuole (BcCV) that delays acidification and maturation into lysosomes is a hallmark of B. cenocepacia infection. Intracellular B. cenocepacia induce an inflammatory response leading to macrophage cell death by pyroptosis through the secretion of a bacterial deamidase that results in the activation of the pyrin inflammasome. However, how or whether infected macrophages can process and present B. cenocepacia antigens to activate T-cells has not been explored. Engulfed bacterial protein antigens are cleaved into small peptides in the late endosomal major histocompatibility class II complex (MHC) compartment (MIIC). Here, we demonstrate that BcCVs and MIICs have overlapping features and that interferon-gamma-activated macrophages infected with B. cenocepacia can process bacterial antigens for presentation by class II MHC molecules to CD4+ T-cells and by class I MHC molecules to CD8+ T-cells. Infected macrophages also release processed bacterial peptides into the extracellular medium, stabilizing empty class I MHC molecules of bystander cells. Together, we conclude that BcCVs acquire MIIC characteristics, supporting the notion that macrophages infected with B. cenocepacia contribute to establishing an adaptive immune response against the pathogen. |
| format | Article |
| id | doaj-art-45e072e3a63d438f9918edc68a695a6b |
| institution | OA Journals |
| issn | 2222-1751 |
| language | English |
| publishDate | 2020-01-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | Emerging Microbes and Infections |
| spelling | doaj-art-45e072e3a63d438f9918edc68a695a6b2025-08-20T02:26:36ZengTaylor & Francis GroupEmerging Microbes and Infections2222-17512020-01-01912000201210.1080/22221751.2020.1818632Interferon-gamma-activated macrophages infected with Burkholderia cenocepacia process and present bacterial antigens to T-cells by class I and II major histocompatibility complex moleculesRoberto Rosales-Reyes0Paola Garza-Villafuerte1Daniela Vences-Vences2Daniel F. Aubert3Rubi Aca-Teutle4Vianney F. Ortiz-Navarrete5Laura C. Bonifaz6Julio Cesar Carrero-Sánchez7Alfonso Olivos-García8Miguel A. Valvano9José Ignacio Santos-Preciado10Facultad de Medicina, Unidad de Investigación en Medicina Experimental, Universidad Nacional Autónoma de México, Mexico City, MéxicoFacultad de Medicina, Unidad de Investigación en Medicina Experimental, Universidad Nacional Autónoma de México, Mexico City, MéxicoFacultad de Medicina, Unidad de Investigación en Medicina Experimental, Universidad Nacional Autónoma de México, Mexico City, MéxicoDepartment of Microbiology and Immunology, The University of Western Ontario, London, CanadaFacultad de Medicina, Unidad de Investigación en Medicina Experimental, Universidad Nacional Autónoma de México, Mexico City, MéxicoDepartamento de Biomedicina Molecular, Centro de Investigación y de Estudios Avanzados del IPN, Mexico City, MéxicoUnidad de Investigación Médica en Inmunoquímica Hospital de Especialidades Centro Médico Nacional Siglo XXI, IMSS, Mexico City, MexicoInstituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, Mexico City, MexicoFacultad de Medicina, Unidad de Investigación en Medicina Experimental, Universidad Nacional Autónoma de México, Mexico City, MéxicoDepartment of Microbiology and Immunology, The University of Western Ontario, London, CanadaFacultad de Medicina, Unidad de Investigación en Medicina Experimental, Universidad Nacional Autónoma de México, Mexico City, MéxicoBurkholderia cenocepacia is an emerging opportunistic pathogen for people with cystic fibrosis and chronic granulomatous disease. Intracellular survival in macrophages within a membrane-bound vacuole (BcCV) that delays acidification and maturation into lysosomes is a hallmark of B. cenocepacia infection. Intracellular B. cenocepacia induce an inflammatory response leading to macrophage cell death by pyroptosis through the secretion of a bacterial deamidase that results in the activation of the pyrin inflammasome. However, how or whether infected macrophages can process and present B. cenocepacia antigens to activate T-cells has not been explored. Engulfed bacterial protein antigens are cleaved into small peptides in the late endosomal major histocompatibility class II complex (MHC) compartment (MIIC). Here, we demonstrate that BcCVs and MIICs have overlapping features and that interferon-gamma-activated macrophages infected with B. cenocepacia can process bacterial antigens for presentation by class II MHC molecules to CD4+ T-cells and by class I MHC molecules to CD8+ T-cells. Infected macrophages also release processed bacterial peptides into the extracellular medium, stabilizing empty class I MHC molecules of bystander cells. Together, we conclude that BcCVs acquire MIIC characteristics, supporting the notion that macrophages infected with B. cenocepacia contribute to establishing an adaptive immune response against the pathogen.https://www.tandfonline.com/doi/10.1080/22221751.2020.1818632Burkholderia cepacia complexT-cell activationantigen processingMIICRab7Type 6 secretion |
| spellingShingle | Roberto Rosales-Reyes Paola Garza-Villafuerte Daniela Vences-Vences Daniel F. Aubert Rubi Aca-Teutle Vianney F. Ortiz-Navarrete Laura C. Bonifaz Julio Cesar Carrero-Sánchez Alfonso Olivos-García Miguel A. Valvano José Ignacio Santos-Preciado Interferon-gamma-activated macrophages infected with Burkholderia cenocepacia process and present bacterial antigens to T-cells by class I and II major histocompatibility complex molecules Emerging Microbes and Infections Burkholderia cepacia complex T-cell activation antigen processing MIIC Rab7 Type 6 secretion |
| title | Interferon-gamma-activated macrophages infected with Burkholderia cenocepacia process and present bacterial antigens to T-cells by class I and II major histocompatibility complex molecules |
| title_full | Interferon-gamma-activated macrophages infected with Burkholderia cenocepacia process and present bacterial antigens to T-cells by class I and II major histocompatibility complex molecules |
| title_fullStr | Interferon-gamma-activated macrophages infected with Burkholderia cenocepacia process and present bacterial antigens to T-cells by class I and II major histocompatibility complex molecules |
| title_full_unstemmed | Interferon-gamma-activated macrophages infected with Burkholderia cenocepacia process and present bacterial antigens to T-cells by class I and II major histocompatibility complex molecules |
| title_short | Interferon-gamma-activated macrophages infected with Burkholderia cenocepacia process and present bacterial antigens to T-cells by class I and II major histocompatibility complex molecules |
| title_sort | interferon gamma activated macrophages infected with burkholderia cenocepacia process and present bacterial antigens to t cells by class i and ii major histocompatibility complex molecules |
| topic | Burkholderia cepacia complex T-cell activation antigen processing MIIC Rab7 Type 6 secretion |
| url | https://www.tandfonline.com/doi/10.1080/22221751.2020.1818632 |
| work_keys_str_mv | AT robertorosalesreyes interferongammaactivatedmacrophagesinfectedwithburkholderiacenocepaciaprocessandpresentbacterialantigenstotcellsbyclassiandiimajorhistocompatibilitycomplexmolecules AT paolagarzavillafuerte interferongammaactivatedmacrophagesinfectedwithburkholderiacenocepaciaprocessandpresentbacterialantigenstotcellsbyclassiandiimajorhistocompatibilitycomplexmolecules AT danielavencesvences interferongammaactivatedmacrophagesinfectedwithburkholderiacenocepaciaprocessandpresentbacterialantigenstotcellsbyclassiandiimajorhistocompatibilitycomplexmolecules AT danielfaubert interferongammaactivatedmacrophagesinfectedwithburkholderiacenocepaciaprocessandpresentbacterialantigenstotcellsbyclassiandiimajorhistocompatibilitycomplexmolecules AT rubiacateutle interferongammaactivatedmacrophagesinfectedwithburkholderiacenocepaciaprocessandpresentbacterialantigenstotcellsbyclassiandiimajorhistocompatibilitycomplexmolecules AT vianneyfortiznavarrete interferongammaactivatedmacrophagesinfectedwithburkholderiacenocepaciaprocessandpresentbacterialantigenstotcellsbyclassiandiimajorhistocompatibilitycomplexmolecules AT lauracbonifaz interferongammaactivatedmacrophagesinfectedwithburkholderiacenocepaciaprocessandpresentbacterialantigenstotcellsbyclassiandiimajorhistocompatibilitycomplexmolecules AT juliocesarcarrerosanchez interferongammaactivatedmacrophagesinfectedwithburkholderiacenocepaciaprocessandpresentbacterialantigenstotcellsbyclassiandiimajorhistocompatibilitycomplexmolecules AT alfonsoolivosgarcia interferongammaactivatedmacrophagesinfectedwithburkholderiacenocepaciaprocessandpresentbacterialantigenstotcellsbyclassiandiimajorhistocompatibilitycomplexmolecules AT miguelavalvano interferongammaactivatedmacrophagesinfectedwithburkholderiacenocepaciaprocessandpresentbacterialantigenstotcellsbyclassiandiimajorhistocompatibilitycomplexmolecules AT joseignaciosantospreciado interferongammaactivatedmacrophagesinfectedwithburkholderiacenocepaciaprocessandpresentbacterialantigenstotcellsbyclassiandiimajorhistocompatibilitycomplexmolecules |