BCG∆BCG1419c and BCG differ in induction of autophagy, c-di-GMP content, proteome, and progression of lung pathology in Mycobacterium tuberculosis HN878-infected male BALB/c mice
•BCG△BCG1419c increased autophagy in murine macrophages compared with BCG.•BCG△BCG1419c differs in c-di-GMP content compared with BCG.•BCG△BCG1419c has a different proteome compared with BCG.•BCG△BCG1419c delayed progression of lung pathology in Mtb HN878-infected mice. The efficacy of BCG vaccines...
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| Veröffentlicht in: | Vaccine 2023-06, Vol.41 (26), p.3824-3835 |
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| container_title | Vaccine |
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| creator | Aceves-Sánchez, Michel de Jesús Barrios-Payán, Jorge Alberto Segura-Cerda, Cristian Alfredo Flores-Valdez, Mario Alberto Mata-Espinosa, Dulce Pedroza-Roldán, César Yadav, Rahul Saini, Deepak Kumar de la Cruz, Miguel Angel Ares, Miguel A. Bielefeldt-Ohmann, Helle Baay-Guzmán, Guillermina Vergne, Isabelle Velázquez-Fernández, Jesús Bernardino Barba León, Jeannette Hernández-Pando, Rogelio |
| description | •BCG△BCG1419c increased autophagy in murine macrophages compared with BCG.•BCG△BCG1419c differs in c-di-GMP content compared with BCG.•BCG△BCG1419c has a different proteome compared with BCG.•BCG△BCG1419c delayed progression of lung pathology in Mtb HN878-infected mice.
The efficacy of BCG vaccines against Mycobacterium tuberculosis (Mtb) strains of lineage 2 (Beijing) in preclinical models and humans has been questioned. We have developed BCG∆BCG1419c, by deletion of BCG1419c in BCG Pasteur, which improved control of tuberculosis (TB) in preclinical models. Here, we compared the capacity of BCG and BCG∆BCG1419c to induce autophagy in murine macrophages, modify c-di-GMP content and transcript levels of BCG1416c, encoding the enzyme responsible for c-di-GMP synthesis/degradation, and of BCG1419c, encoding the phosphodiesterase involved in c-di-GMP degradation. Furthermore, we evaluated proteomic differences in vitro and compared protection against TB produced by a low dose of the HN878-Beijing strain at 3- and 6-months post-infection. We found that BCG∆BCG1419c induced more autophagy and produced different levels of c-di-GMP as well as different transcription of BCG1416c with no expression of BCG1419c. BCG∆BCG1419c differentially produced several proteins, including some involved in interaction with host cells. Vaccination with either BCG strain led to control of bacillary burden in lungs and spleen at 3- but not 6-months post-infection, whereas it reduced pneumonic areas compared with unvaccinated controls at 6 months post-infection. Vaccination with BCG∆BCG1419c delayed progression of lung necrosis as this was observed only at 6 months post-infection. Taken together, compared with BCG, BCG∆BCG1419c increased autophagy, presented different levels of c-di-GMP and transcription of BCG1416c in vitro in a growth-phase dependent manner, modified its proteome and delayed progression of lung pathology produced by a highly virulent Beijing strain. |
| doi_str_mv | 10.1016/j.vaccine.2023.04.065 |
| format | Article |
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The efficacy of BCG vaccines against Mycobacterium tuberculosis (Mtb) strains of lineage 2 (Beijing) in preclinical models and humans has been questioned. We have developed BCG∆BCG1419c, by deletion of BCG1419c in BCG Pasteur, which improved control of tuberculosis (TB) in preclinical models. Here, we compared the capacity of BCG and BCG∆BCG1419c to induce autophagy in murine macrophages, modify c-di-GMP content and transcript levels of BCG1416c, encoding the enzyme responsible for c-di-GMP synthesis/degradation, and of BCG1419c, encoding the phosphodiesterase involved in c-di-GMP degradation. Furthermore, we evaluated proteomic differences in vitro and compared protection against TB produced by a low dose of the HN878-Beijing strain at 3- and 6-months post-infection. We found that BCG∆BCG1419c induced more autophagy and produced different levels of c-di-GMP as well as different transcription of BCG1416c with no expression of BCG1419c. BCG∆BCG1419c differentially produced several proteins, including some involved in interaction with host cells. Vaccination with either BCG strain led to control of bacillary burden in lungs and spleen at 3- but not 6-months post-infection, whereas it reduced pneumonic areas compared with unvaccinated controls at 6 months post-infection. Vaccination with BCG∆BCG1419c delayed progression of lung necrosis as this was observed only at 6 months post-infection. Taken together, compared with BCG, BCG∆BCG1419c increased autophagy, presented different levels of c-di-GMP and transcription of BCG1416c in vitro in a growth-phase dependent manner, modified its proteome and delayed progression of lung pathology produced by a highly virulent Beijing strain.</description><identifier>ISSN: 0264-410X</identifier><identifier>EISSN: 1873-2518</identifier><identifier>EISSN: 0264-410X</identifier><identifier>DOI: 10.1016/j.vaccine.2023.04.065</identifier><identifier>PMID: 37164819</identifier><language>eng</language><publisher>Netherlands: Elsevier Ltd</publisher><subject>Animals ; Autophagy ; Bacteria ; Bacteriology ; BCG ; BCG Vaccine ; BCG∆BCG1419c ; Beijing ; Biofilms ; Biosensors ; Coding ; Degradation ; Glycerol ; HN878 ; Human health and pathology ; Humans ; Hypotheses ; Immunization ; Immunology ; Infections ; Infectious diseases ; Life Sciences ; Lung ; Lungs ; Macrophages ; Male ; Mice ; Mice, Inbred BALB C ; Microbiology and Parasitology ; Mycobacterium bovis ; Mycobacterium tuberculosis ; Necrosis ; Pathology ; Proteins ; Proteome ; Proteomes ; Proteomics ; Tuberculosis ; Tuberculosis - prevention & control ; Vaccines ; Vaccinology</subject><ispartof>Vaccine, 2023-06, Vol.41 (26), p.3824-3835</ispartof><rights>2023 Elsevier Ltd</rights><rights>Copyright © 2023 Elsevier Ltd. All rights reserved.</rights><rights>2023. Elsevier Ltd</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c342t-cc970e0395c89e938545d9a70a588a015d86587d11de7cd27705e96f8defd4643</citedby><cites>FETCH-LOGICAL-c342t-cc970e0395c89e938545d9a70a588a015d86587d11de7cd27705e96f8defd4643</cites><orcidid>0000-0003-1924-9474</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.proquest.com/docview/2824486146?pq-origsite=primo$$EHTML$$P50$$Gproquest$$H</linktohtml><link.rule.ids>230,314,780,784,885,3550,27924,27925,45995,64385,64387,64389,72469</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37164819$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-04117714$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Aceves-Sánchez, Michel de Jesús</creatorcontrib><creatorcontrib>Barrios-Payán, Jorge Alberto</creatorcontrib><creatorcontrib>Segura-Cerda, Cristian Alfredo</creatorcontrib><creatorcontrib>Flores-Valdez, Mario Alberto</creatorcontrib><creatorcontrib>Mata-Espinosa, Dulce</creatorcontrib><creatorcontrib>Pedroza-Roldán, César</creatorcontrib><creatorcontrib>Yadav, Rahul</creatorcontrib><creatorcontrib>Saini, Deepak Kumar</creatorcontrib><creatorcontrib>de la Cruz, Miguel Angel</creatorcontrib><creatorcontrib>Ares, Miguel A.</creatorcontrib><creatorcontrib>Bielefeldt-Ohmann, Helle</creatorcontrib><creatorcontrib>Baay-Guzmán, Guillermina</creatorcontrib><creatorcontrib>Vergne, Isabelle</creatorcontrib><creatorcontrib>Velázquez-Fernández, Jesús Bernardino</creatorcontrib><creatorcontrib>Barba León, Jeannette</creatorcontrib><creatorcontrib>Hernández-Pando, Rogelio</creatorcontrib><title>BCG∆BCG1419c and BCG differ in induction of autophagy, c-di-GMP content, proteome, and progression of lung pathology in Mycobacterium tuberculosis HN878-infected male BALB/c mice</title><title>Vaccine</title><addtitle>Vaccine</addtitle><description>•BCG△BCG1419c increased autophagy in murine macrophages compared with BCG.•BCG△BCG1419c differs in c-di-GMP content compared with BCG.•BCG△BCG1419c has a different proteome compared with BCG.•BCG△BCG1419c delayed progression of lung pathology in Mtb HN878-infected mice.
The efficacy of BCG vaccines against Mycobacterium tuberculosis (Mtb) strains of lineage 2 (Beijing) in preclinical models and humans has been questioned. We have developed BCG∆BCG1419c, by deletion of BCG1419c in BCG Pasteur, which improved control of tuberculosis (TB) in preclinical models. Here, we compared the capacity of BCG and BCG∆BCG1419c to induce autophagy in murine macrophages, modify c-di-GMP content and transcript levels of BCG1416c, encoding the enzyme responsible for c-di-GMP synthesis/degradation, and of BCG1419c, encoding the phosphodiesterase involved in c-di-GMP degradation. Furthermore, we evaluated proteomic differences in vitro and compared protection against TB produced by a low dose of the HN878-Beijing strain at 3- and 6-months post-infection. We found that BCG∆BCG1419c induced more autophagy and produced different levels of c-di-GMP as well as different transcription of BCG1416c with no expression of BCG1419c. BCG∆BCG1419c differentially produced several proteins, including some involved in interaction with host cells. Vaccination with either BCG strain led to control of bacillary burden in lungs and spleen at 3- but not 6-months post-infection, whereas it reduced pneumonic areas compared with unvaccinated controls at 6 months post-infection. Vaccination with BCG∆BCG1419c delayed progression of lung necrosis as this was observed only at 6 months post-infection. Taken together, compared with BCG, BCG∆BCG1419c increased autophagy, presented different levels of c-di-GMP and transcription of BCG1416c in vitro in a growth-phase dependent manner, modified its proteome and delayed progression of lung pathology produced by a highly virulent Beijing strain.</description><subject>Animals</subject><subject>Autophagy</subject><subject>Bacteria</subject><subject>Bacteriology</subject><subject>BCG</subject><subject>BCG Vaccine</subject><subject>BCG∆BCG1419c</subject><subject>Beijing</subject><subject>Biofilms</subject><subject>Biosensors</subject><subject>Coding</subject><subject>Degradation</subject><subject>Glycerol</subject><subject>HN878</subject><subject>Human health and pathology</subject><subject>Humans</subject><subject>Hypotheses</subject><subject>Immunization</subject><subject>Immunology</subject><subject>Infections</subject><subject>Infectious diseases</subject><subject>Life Sciences</subject><subject>Lung</subject><subject>Lungs</subject><subject>Macrophages</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Microbiology and Parasitology</subject><subject>Mycobacterium bovis</subject><subject>Mycobacterium tuberculosis</subject><subject>Necrosis</subject><subject>Pathology</subject><subject>Proteins</subject><subject>Proteome</subject><subject>Proteomes</subject><subject>Proteomics</subject><subject>Tuberculosis</subject><subject>Tuberculosis - prevention & 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Alberto</au><au>Mata-Espinosa, Dulce</au><au>Pedroza-Roldán, César</au><au>Yadav, Rahul</au><au>Saini, Deepak Kumar</au><au>de la Cruz, Miguel Angel</au><au>Ares, Miguel A.</au><au>Bielefeldt-Ohmann, Helle</au><au>Baay-Guzmán, Guillermina</au><au>Vergne, Isabelle</au><au>Velázquez-Fernández, Jesús Bernardino</au><au>Barba León, Jeannette</au><au>Hernández-Pando, Rogelio</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>BCG∆BCG1419c and BCG differ in induction of autophagy, c-di-GMP content, proteome, and progression of lung pathology in Mycobacterium tuberculosis HN878-infected male BALB/c mice</atitle><jtitle>Vaccine</jtitle><addtitle>Vaccine</addtitle><date>2023-06-13</date><risdate>2023</risdate><volume>41</volume><issue>26</issue><spage>3824</spage><epage>3835</epage><pages>3824-3835</pages><issn>0264-410X</issn><eissn>1873-2518</eissn><eissn>0264-410X</eissn><abstract>•BCG△BCG1419c increased autophagy in murine macrophages compared with BCG.•BCG△BCG1419c differs in c-di-GMP content compared with BCG.•BCG△BCG1419c has a different proteome compared with BCG.•BCG△BCG1419c delayed progression of lung pathology in Mtb HN878-infected mice.
The efficacy of BCG vaccines against Mycobacterium tuberculosis (Mtb) strains of lineage 2 (Beijing) in preclinical models and humans has been questioned. We have developed BCG∆BCG1419c, by deletion of BCG1419c in BCG Pasteur, which improved control of tuberculosis (TB) in preclinical models. Here, we compared the capacity of BCG and BCG∆BCG1419c to induce autophagy in murine macrophages, modify c-di-GMP content and transcript levels of BCG1416c, encoding the enzyme responsible for c-di-GMP synthesis/degradation, and of BCG1419c, encoding the phosphodiesterase involved in c-di-GMP degradation. Furthermore, we evaluated proteomic differences in vitro and compared protection against TB produced by a low dose of the HN878-Beijing strain at 3- and 6-months post-infection. We found that BCG∆BCG1419c induced more autophagy and produced different levels of c-di-GMP as well as different transcription of BCG1416c with no expression of BCG1419c. BCG∆BCG1419c differentially produced several proteins, including some involved in interaction with host cells. Vaccination with either BCG strain led to control of bacillary burden in lungs and spleen at 3- but not 6-months post-infection, whereas it reduced pneumonic areas compared with unvaccinated controls at 6 months post-infection. Vaccination with BCG∆BCG1419c delayed progression of lung necrosis as this was observed only at 6 months post-infection. Taken together, compared with BCG, BCG∆BCG1419c increased autophagy, presented different levels of c-di-GMP and transcription of BCG1416c in vitro in a growth-phase dependent manner, modified its proteome and delayed progression of lung pathology produced by a highly virulent Beijing strain.</abstract><cop>Netherlands</cop><pub>Elsevier Ltd</pub><pmid>37164819</pmid><doi>10.1016/j.vaccine.2023.04.065</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0003-1924-9474</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0264-410X |
| ispartof | Vaccine, 2023-06, Vol.41 (26), p.3824-3835 |
| issn | 0264-410X 1873-2518 0264-410X |
| language | eng |
| recordid | cdi_hal_primary_oai_HAL_hal_04117714v1 |
| source | MEDLINE; Elsevier ScienceDirect Journals Complete; ProQuest Central UK/Ireland |
| subjects | Animals Autophagy Bacteria Bacteriology BCG BCG Vaccine BCG∆BCG1419c Beijing Biofilms Biosensors Coding Degradation Glycerol HN878 Human health and pathology Humans Hypotheses Immunization Immunology Infections Infectious diseases Life Sciences Lung Lungs Macrophages Male Mice Mice, Inbred BALB C Microbiology and Parasitology Mycobacterium bovis Mycobacterium tuberculosis Necrosis Pathology Proteins Proteome Proteomes Proteomics Tuberculosis Tuberculosis - prevention & control Vaccines Vaccinology |
| title | BCG∆BCG1419c and BCG differ in induction of autophagy, c-di-GMP content, proteome, and progression of lung pathology in Mycobacterium tuberculosis HN878-infected male BALB/c mice |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-26T09%3A08%3A31IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_hal_p&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=BCG%E2%88%86BCG1419c%20and%20BCG%20differ%20in%20induction%20of%20autophagy,%20c-di-GMP%20content,%20proteome,%20and%20progression%20of%20lung%20pathology%20in%20Mycobacterium%20tuberculosis%20HN878-infected%20male%20BALB/c%20mice&rft.jtitle=Vaccine&rft.au=Aceves-S%C3%A1nchez,%20Michel%20de%20Jes%C3%BAs&rft.date=2023-06-13&rft.volume=41&rft.issue=26&rft.spage=3824&rft.epage=3835&rft.pages=3824-3835&rft.issn=0264-410X&rft.eissn=1873-2518&rft_id=info:doi/10.1016/j.vaccine.2023.04.065&rft_dat=%3Cproquest_hal_p%3E2824486146%3C/proquest_hal_p%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2824486146&rft_id=info:pmid/37164819&rft_els_id=S0264410X23004899&rfr_iscdi=true |