A transcriptional analysis of cattle immune cells reveals a central role of type 1 interferon in the In vitro innate immune response against Mycobacterium bovis
Bovine tuberculosis is a chronic infectious disease primarily caused by Mycobacterium bovis, a bacterium that affects cattle and other mammals, including humans. Despite the availability of vast research about the immune response mechanisms of human tuberculosis caused by Mycobacterium tuberculosis, the knowledge of bovine tuberculosis’s immunology, particularly regarding the innate immune response, still remains scarce. In this study, we compared the transcriptome of cell cultures containing lymphocytes and M. bovis infected-macrophages with two strains of variable virulence, the virulent Mb04-303 strain and the attenuated Mb534. To that end, we infected bovine macrophages at a multiplicity of infection of one, and co-cultured the infections with autologous lymphocytes. RNA obtained from the co-cultures was sequenced to identify differentially expressed gene pathways by using the database Reactome. The RNA-seq analysis showed that the Mb04-303 infection upregulated the type 1 interferon signalling pathway, while it downregulated the KEAP1-NFE2L2 pathway. According to the literature, this last pathway is involved in the activation of antioxidant genes and inflammasome. In addition, the macrophages infected with Mb04-303 recruited more Galectin 8 than those infected with Mb534. This result indicates that Mb04-303 induced higher phagosome membrane damage, with the possible concomitant release of bacterial compounds into the cytoplasm that activates the type I signalling pathway. Altogether, Mb04-303 repressed the antioxidant and anti-inflammatory responses, likely impairing interleukin-1β activation, and trigged the canonical type 1 interferon signalling. Although these responses led to the control of bacterial replication during early infection, the virulent strain eventually managed to establish a successful infection.
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MDPI
2023-09
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Subjects: | Bovine Tuberculosis, Interferons, Macrophages, Cattle, Natural Immunity, Immune Response, In vitro, Tuberculosis Bovina, Mycobacterium bovis, Interferonas, Macrofagos, Ganado Bovino, Inmunidad Natural, Respuesta Inmunológica, |
Online Access: | http://hdl.handle.net/20.500.12123/15303 https://www.mdpi.com/2076-0817/12/9/1159 https://doi.org/10.3390/pathogens12091159 |
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Bovine Tuberculosis Interferons Macrophages Cattle Natural Immunity Immune Response In vitro Tuberculosis Bovina Mycobacterium bovis Interferonas Macrofagos Ganado Bovino Inmunidad Natural Respuesta Inmunológica Bovine Tuberculosis Interferons Macrophages Cattle Natural Immunity Immune Response In vitro Tuberculosis Bovina Mycobacterium bovis Interferonas Macrofagos Ganado Bovino Inmunidad Natural Respuesta Inmunológica |
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Bovine Tuberculosis Interferons Macrophages Cattle Natural Immunity Immune Response In vitro Tuberculosis Bovina Mycobacterium bovis Interferonas Macrofagos Ganado Bovino Inmunidad Natural Respuesta Inmunológica Bovine Tuberculosis Interferons Macrophages Cattle Natural Immunity Immune Response In vitro Tuberculosis Bovina Mycobacterium bovis Interferonas Macrofagos Ganado Bovino Inmunidad Natural Respuesta Inmunológica Blanco, Federico Carlos Bigi, María Mercedes Garcia, Elizabeth Andrea Elola, María Teresa Vazquez, Cristina Lourdes Bigi, Fabiana A transcriptional analysis of cattle immune cells reveals a central role of type 1 interferon in the In vitro innate immune response against Mycobacterium bovis |
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Bovine tuberculosis is a chronic infectious disease primarily caused by Mycobacterium bovis, a bacterium that affects cattle and other mammals, including humans. Despite the availability of vast research about the immune response mechanisms of human tuberculosis caused by Mycobacterium tuberculosis, the knowledge of bovine tuberculosis’s immunology, particularly regarding the innate immune response, still remains scarce. In this study, we compared the transcriptome of cell cultures containing lymphocytes and M. bovis infected-macrophages with two strains of variable virulence, the virulent Mb04-303 strain and the attenuated Mb534. To that end, we infected bovine macrophages at a multiplicity of infection of one, and co-cultured the infections with autologous lymphocytes. RNA obtained from the co-cultures was sequenced to identify differentially expressed gene pathways by using the database Reactome. The RNA-seq analysis showed that the Mb04-303 infection upregulated the type 1 interferon signalling pathway, while it downregulated the KEAP1-NFE2L2 pathway. According to the literature, this last pathway is involved in the activation of antioxidant genes and inflammasome. In addition, the macrophages infected with Mb04-303 recruited more Galectin 8 than those infected with Mb534. This result indicates that Mb04-303 induced higher phagosome membrane damage, with the possible concomitant release of bacterial compounds into the cytoplasm that activates the type I signalling pathway. Altogether, Mb04-303 repressed the antioxidant and anti-inflammatory responses, likely impairing interleukin-1β activation, and trigged the canonical type 1 interferon signalling. Although these responses led to the control of bacterial replication during early infection, the virulent strain eventually managed to establish a successful infection. |
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info:ar-repo/semantics/artículo |
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Bovine Tuberculosis Interferons Macrophages Cattle Natural Immunity Immune Response In vitro Tuberculosis Bovina Mycobacterium bovis Interferonas Macrofagos Ganado Bovino Inmunidad Natural Respuesta Inmunológica |
author |
Blanco, Federico Carlos Bigi, María Mercedes Garcia, Elizabeth Andrea Elola, María Teresa Vazquez, Cristina Lourdes Bigi, Fabiana |
author_facet |
Blanco, Federico Carlos Bigi, María Mercedes Garcia, Elizabeth Andrea Elola, María Teresa Vazquez, Cristina Lourdes Bigi, Fabiana |
author_sort |
Blanco, Federico Carlos |
title |
A transcriptional analysis of cattle immune cells reveals a central role of type 1 interferon in the In vitro innate immune response against Mycobacterium bovis |
title_short |
A transcriptional analysis of cattle immune cells reveals a central role of type 1 interferon in the In vitro innate immune response against Mycobacterium bovis |
title_full |
A transcriptional analysis of cattle immune cells reveals a central role of type 1 interferon in the In vitro innate immune response against Mycobacterium bovis |
title_fullStr |
A transcriptional analysis of cattle immune cells reveals a central role of type 1 interferon in the In vitro innate immune response against Mycobacterium bovis |
title_full_unstemmed |
A transcriptional analysis of cattle immune cells reveals a central role of type 1 interferon in the In vitro innate immune response against Mycobacterium bovis |
title_sort |
transcriptional analysis of cattle immune cells reveals a central role of type 1 interferon in the in vitro innate immune response against mycobacterium bovis |
publisher |
MDPI |
publishDate |
2023-09 |
url |
http://hdl.handle.net/20.500.12123/15303 https://www.mdpi.com/2076-0817/12/9/1159 https://doi.org/10.3390/pathogens12091159 |
work_keys_str_mv |
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oai:localhost:20.500.12123-153032023-09-25T15:02:17Z A transcriptional analysis of cattle immune cells reveals a central role of type 1 interferon in the In vitro innate immune response against Mycobacterium bovis Blanco, Federico Carlos Bigi, María Mercedes Garcia, Elizabeth Andrea Elola, María Teresa Vazquez, Cristina Lourdes Bigi, Fabiana Bovine Tuberculosis Interferons Macrophages Cattle Natural Immunity Immune Response In vitro Tuberculosis Bovina Mycobacterium bovis Interferonas Macrofagos Ganado Bovino Inmunidad Natural Respuesta Inmunológica Bovine tuberculosis is a chronic infectious disease primarily caused by Mycobacterium bovis, a bacterium that affects cattle and other mammals, including humans. Despite the availability of vast research about the immune response mechanisms of human tuberculosis caused by Mycobacterium tuberculosis, the knowledge of bovine tuberculosis’s immunology, particularly regarding the innate immune response, still remains scarce. In this study, we compared the transcriptome of cell cultures containing lymphocytes and M. bovis infected-macrophages with two strains of variable virulence, the virulent Mb04-303 strain and the attenuated Mb534. To that end, we infected bovine macrophages at a multiplicity of infection of one, and co-cultured the infections with autologous lymphocytes. RNA obtained from the co-cultures was sequenced to identify differentially expressed gene pathways by using the database Reactome. The RNA-seq analysis showed that the Mb04-303 infection upregulated the type 1 interferon signalling pathway, while it downregulated the KEAP1-NFE2L2 pathway. According to the literature, this last pathway is involved in the activation of antioxidant genes and inflammasome. In addition, the macrophages infected with Mb04-303 recruited more Galectin 8 than those infected with Mb534. This result indicates that Mb04-303 induced higher phagosome membrane damage, with the possible concomitant release of bacterial compounds into the cytoplasm that activates the type I signalling pathway. Altogether, Mb04-303 repressed the antioxidant and anti-inflammatory responses, likely impairing interleukin-1β activation, and trigged the canonical type 1 interferon signalling. Although these responses led to the control of bacterial replication during early infection, the virulent strain eventually managed to establish a successful infection. Instituto de Biotecnología Fil: Blanco, Federico Carlos. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina Fil: Blanco, Federico Carlos. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina Fil: Bigi, María Mercedes. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Biomédicas; Argentina Fil: Bigi, María Mercedes. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina Fil: Garcia, Elizabeth Andrea. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina Fil: Garcia, Elizabeth Andrea. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina Fil: Elola, María Teresa. Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Instituto de Química y Fisicoquímica Biológicas Prof. Dr. Alejandro Paladini; Argentina Fil: Vazquez, Cristina Lourdes. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina Fil: Vazquez, Cristina Lourdes. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina Fil: Bigi, Fabiana. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina Fil: Bigi, Fabiana. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina 2023-09-25T14:55:28Z 2023-09-25T14:55:28Z 2023-09 info:ar-repo/semantics/artículo info:eu-repo/semantics/article info:eu-repo/semantics/publishedVersion http://hdl.handle.net/20.500.12123/15303 https://www.mdpi.com/2076-0817/12/9/1159 2076-0817 https://doi.org/10.3390/pathogens12091159 eng info:eu-repograntAgreement/INTA/2019-PD-E6-I116-001, Identificación y análisis funcional de genes o redes génicas de interés biotecnológico con fin agropecuario, forestal, agroalimentario y/o agroindustrial. info:eu-repo/semantics/openAccess http://creativecommons.org/licenses/by-nc-sa/4.0/ Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0) application/pdf MDPI Pathogens 12 (9) : 1159 (Septiembre 2023) |