Mycobacterial Infection of Precision-Cut Lung Slices Reveals Type 1 Interferon Pathway Is Locally Induced by Mycobacterium bovis but Not M. tuberculosis in a Cattle Breed
Tuberculosis exacts a terrible toll on human and animal health. While Mycobacterium tuberculosis (Mtb) is restricted to humans, Mycobacterium bovis (Mb) is present in a large range of mammalian hosts. In cattle, bovine TB (bTB) is a noticeable disease responsible for important economic losses in dev...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2021-07-01
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| Series: | Frontiers in Veterinary Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fvets.2021.696525/full |
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| author | Aude Remot Florence Carreras Anthony Coupé Émilie Doz-Deblauwe Maria L. Boschiroli John A. Browne Quentin Marquant Delphyne Descamps Fabienne Archer Abraham Aseffa Pierre Germon Stephen V. Gordon Nathalie Winter |
| author_facet | Aude Remot Florence Carreras Anthony Coupé Émilie Doz-Deblauwe Maria L. Boschiroli John A. Browne Quentin Marquant Delphyne Descamps Fabienne Archer Abraham Aseffa Pierre Germon Stephen V. Gordon Nathalie Winter |
| author_sort | Aude Remot |
| collection | DOAJ |
| description | Tuberculosis exacts a terrible toll on human and animal health. While Mycobacterium tuberculosis (Mtb) is restricted to humans, Mycobacterium bovis (Mb) is present in a large range of mammalian hosts. In cattle, bovine TB (bTB) is a noticeable disease responsible for important economic losses in developed countries and underestimated zoonosis in the developing world. Early interactions that take place between mycobacteria and the lung tissue early after aerosol infection govern the outcome of the disease. In cattle, these early steps remain poorly characterized. The precision-cut lung slice (PCLS) model preserves the structure and cell diversity of the lung. We developed this model in cattle in order to study the early lung response to mycobacterial infection. In situ imaging of PCLS infected with fluorescent Mb revealed bacilli in the alveolar compartment, in adjacent or inside alveolar macrophages, and in close contact with pneumocytes. We analyzed the global transcriptional lung inflammation signature following infection of PCLS with Mb and Mtb in two French beef breeds: Blonde d'Aquitaine and Charolaise. Whereas, lungs from the Blonde d'Aquitaine produced high levels of mediators of neutrophil and monocyte recruitment in response to infection, such signatures were not observed in the Charolaise in our study. In the Blonde d'Aquitaine lung, whereas the inflammatory response was highly induced by two Mb strains, AF2122 isolated from cattle in the UK and Mb3601 circulating in France, the response against two Mtb strains, H37Rv, the reference laboratory strain, and BTB1558, isolated from zebu in Ethiopia, was very low. Strikingly, the type I interferon pathway was only induced by Mb but not Mtb strains, indicating that this pathway may be involved in mycobacterial virulence and host tropism. Hence, the PCLS model in cattle is a valuable tool to deepen our understanding of early interactions between lung host cells and mycobacteria. It revealed striking differences between cattle breeds and mycobacterial strains. This model could help in deciphering biomarkers of resistance vs. susceptibility to bTB in cattle as such information is still critically needed for bovine genetic selection programs and would greatly help the global effort to eradicate bTB. |
| first_indexed | 2024-12-19T05:58:41Z |
| format | Article |
| id | doaj.art-23072e77a1e84fc4b1d081293c13084f |
| institution | Directory Open Access Journal |
| issn | 2297-1769 |
| language | English |
| last_indexed | 2024-12-19T05:58:41Z |
| publishDate | 2021-07-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Veterinary Science |
| spelling | doaj.art-23072e77a1e84fc4b1d081293c13084f2022-12-21T20:33:22ZengFrontiers Media S.A.Frontiers in Veterinary Science2297-17692021-07-01810.3389/fvets.2021.696525696525Mycobacterial Infection of Precision-Cut Lung Slices Reveals Type 1 Interferon Pathway Is Locally Induced by Mycobacterium bovis but Not M. tuberculosis in a Cattle BreedAude Remot0Florence Carreras1Anthony Coupé2Émilie Doz-Deblauwe3Maria L. Boschiroli4John A. Browne5Quentin Marquant6Delphyne Descamps7Fabienne Archer8Abraham Aseffa9Pierre Germon10Stephen V. Gordon11Nathalie Winter12INRAE, Université de Tours, Nouzilly, FranceINRAE, Université de Tours, Nouzilly, FranceINRAE, Université de Tours, Nouzilly, FranceINRAE, Université de Tours, Nouzilly, FranceParis-Est University, National Reference Laboratory for Tuberculosis, Animal Health Laboratory, Anses, Maisons-Alfort, FranceUCD School of Agriculture and Food Science, University College Dublin, Dublin, IrelandINRAE, Université Paris-Saclay, UVSQ, Jouy-en-Josas, FranceINRAE, Université Paris-Saclay, UVSQ, Jouy-en-Josas, FranceINRAE, UMR754, Viral Infections and Comparative Pathology, IVPC, Univ Lyon, Université Claude Bernard Lyon 1, EPHE, Lyon, FranceArmauer Hansen Research Institute, Addis Ababa, EthiopiaINRAE, Université de Tours, Nouzilly, FranceUCD School of Veterinary Medicine and UCD Conway Institute, University College Dublin, Dublin, IrelandINRAE, Université de Tours, Nouzilly, FranceTuberculosis exacts a terrible toll on human and animal health. While Mycobacterium tuberculosis (Mtb) is restricted to humans, Mycobacterium bovis (Mb) is present in a large range of mammalian hosts. In cattle, bovine TB (bTB) is a noticeable disease responsible for important economic losses in developed countries and underestimated zoonosis in the developing world. Early interactions that take place between mycobacteria and the lung tissue early after aerosol infection govern the outcome of the disease. In cattle, these early steps remain poorly characterized. The precision-cut lung slice (PCLS) model preserves the structure and cell diversity of the lung. We developed this model in cattle in order to study the early lung response to mycobacterial infection. In situ imaging of PCLS infected with fluorescent Mb revealed bacilli in the alveolar compartment, in adjacent or inside alveolar macrophages, and in close contact with pneumocytes. We analyzed the global transcriptional lung inflammation signature following infection of PCLS with Mb and Mtb in two French beef breeds: Blonde d'Aquitaine and Charolaise. Whereas, lungs from the Blonde d'Aquitaine produced high levels of mediators of neutrophil and monocyte recruitment in response to infection, such signatures were not observed in the Charolaise in our study. In the Blonde d'Aquitaine lung, whereas the inflammatory response was highly induced by two Mb strains, AF2122 isolated from cattle in the UK and Mb3601 circulating in France, the response against two Mtb strains, H37Rv, the reference laboratory strain, and BTB1558, isolated from zebu in Ethiopia, was very low. Strikingly, the type I interferon pathway was only induced by Mb but not Mtb strains, indicating that this pathway may be involved in mycobacterial virulence and host tropism. Hence, the PCLS model in cattle is a valuable tool to deepen our understanding of early interactions between lung host cells and mycobacteria. It revealed striking differences between cattle breeds and mycobacterial strains. This model could help in deciphering biomarkers of resistance vs. susceptibility to bTB in cattle as such information is still critically needed for bovine genetic selection programs and would greatly help the global effort to eradicate bTB.https://www.frontiersin.org/articles/10.3389/fvets.2021.696525/fullcattleMycobacterium bovisex vivoprecision cut lung slicesalveolar macrophagestype I interferon |
| spellingShingle | Aude Remot Florence Carreras Anthony Coupé Émilie Doz-Deblauwe Maria L. Boschiroli John A. Browne Quentin Marquant Delphyne Descamps Fabienne Archer Abraham Aseffa Pierre Germon Stephen V. Gordon Nathalie Winter Mycobacterial Infection of Precision-Cut Lung Slices Reveals Type 1 Interferon Pathway Is Locally Induced by Mycobacterium bovis but Not M. tuberculosis in a Cattle Breed Frontiers in Veterinary Science cattle Mycobacterium bovis ex vivo precision cut lung slices alveolar macrophages type I interferon |
| title | Mycobacterial Infection of Precision-Cut Lung Slices Reveals Type 1 Interferon Pathway Is Locally Induced by Mycobacterium bovis but Not M. tuberculosis in a Cattle Breed |
| title_full | Mycobacterial Infection of Precision-Cut Lung Slices Reveals Type 1 Interferon Pathway Is Locally Induced by Mycobacterium bovis but Not M. tuberculosis in a Cattle Breed |
| title_fullStr | Mycobacterial Infection of Precision-Cut Lung Slices Reveals Type 1 Interferon Pathway Is Locally Induced by Mycobacterium bovis but Not M. tuberculosis in a Cattle Breed |
| title_full_unstemmed | Mycobacterial Infection of Precision-Cut Lung Slices Reveals Type 1 Interferon Pathway Is Locally Induced by Mycobacterium bovis but Not M. tuberculosis in a Cattle Breed |
| title_short | Mycobacterial Infection of Precision-Cut Lung Slices Reveals Type 1 Interferon Pathway Is Locally Induced by Mycobacterium bovis but Not M. tuberculosis in a Cattle Breed |
| title_sort | mycobacterial infection of precision cut lung slices reveals type 1 interferon pathway is locally induced by mycobacterium bovis but not m tuberculosis in a cattle breed |
| topic | cattle Mycobacterium bovis ex vivo precision cut lung slices alveolar macrophages type I interferon |
| url | https://www.frontiersin.org/articles/10.3389/fvets.2021.696525/full |
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