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26-04-2024 | Mycobacterium Tuberculosis | REVIEW

Bacillus Calmette-Guérin (BCG)-Induced Protection in Brain Disorders

Authors: Khiany Mathias, Richard Simon Machado, Solange Stork, Carla Damasio Martins, Amanda Christine da Silva Kursancew, Victória Linden de Rezende, Cinara Ludvig Gonçalves, Tatiana Barichello, Josiane Somariva Prophiro, Fabricia Petronilho

Published in: Inflammation

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Abstract

The Bacille Calmette-Guerin (BCG) vaccine is one of the most widely used vaccines in the world for the prevention of tuberculosis. Its immunological capacity also includes epigenetic reprogramming, activation of T cells and inflammatory responses. Although the main usage of the vaccine is the prevention of tuberculosis, different works have shown that the effect of BCG can go beyond the peripheral immune response and be linked to the central nervous system by modulating the immune system at the level of the brain. This review therefore aims to describe the BCG vaccine, its origin, its relationship with the immune system, and its involvement at the brain level.
Literature
1.
go back to reference Andersen, P., and T.M. Doherty. 2005. The success and failure of BCG — implications for a novel tuberculosis vaccine. Nature Reviews. Microbiology 3 (8): 656–662.PubMedCrossRef Andersen, P., and T.M. Doherty. 2005. The success and failure of BCG — implications for a novel tuberculosis vaccine. Nature Reviews. Microbiology 3 (8): 656–662.PubMedCrossRef
2.
go back to reference Fatima, S., A. Kumari, G. Das, and V.P. Dwivedi. 2020. Tuberculosis vaccine: a journey from BCG to present. Life Sciences 252: 117594.PubMedCrossRef Fatima, S., A. Kumari, G. Das, and V.P. Dwivedi. 2020. Tuberculosis vaccine: a journey from BCG to present. Life Sciences 252: 117594.PubMedCrossRef
3.
go back to reference Moreo, E., A. Jarit-Cabanillas, I. Robles-Vera, S. Uranga, C. Guerrero, A.B. Gómez, et al. 2023. Intravenous administration of BCG in mice promotes natural killer and T cell-mediated antitumor immunity in the lung. Nature Communications 14 (1): 6090.PubMedPubMedCentralCrossRef Moreo, E., A. Jarit-Cabanillas, I. Robles-Vera, S. Uranga, C. Guerrero, A.B. Gómez, et al. 2023. Intravenous administration of BCG in mice promotes natural killer and T cell-mediated antitumor immunity in the lung. Nature Communications 14 (1): 6090.PubMedPubMedCentralCrossRef
4.
go back to reference Tran, Kim A., E. Pernet, M. Sadeghi, J. Downey, J. Chronopoulos, E. Lapshina, O. Tsai, E. Kaufmann, J. Ding, and M. Divangahi. 2024. BCG immunization induces CX3CR1hi effector memory T cells to provide cross-protection via IFN-γ-mediated trained immunity. Nature Immunology 25: 418–431 Tran, Kim A., E. Pernet, M. Sadeghi, J. Downey, J. Chronopoulos, E. Lapshina, O. Tsai, E. Kaufmann, J. Ding, and M. Divangahi. 2024. BCG immunization induces CX3CR1hi effector memory T cells to provide cross-protection via IFN-γ-mediated trained immunity. Nature Immunology 25: 418–431
5.
go back to reference Jeyanathan, M., M. Vaseghi-Shanjani, S. Afkhami, J.A. Grondin, A. Kang, M.R. D’Agostino, et al. 2022. Parenteral BCG vaccine induces lung-resident memory macrophages and trained immunity via the gut–lung axis. Nature Immunology 23 (12): 1687–1702.PubMedPubMedCentralCrossRef Jeyanathan, M., M. Vaseghi-Shanjani, S. Afkhami, J.A. Grondin, A. Kang, M.R. D’Agostino, et al. 2022. Parenteral BCG vaccine induces lung-resident memory macrophages and trained immunity via the gut–lung axis. Nature Immunology 23 (12): 1687–1702.PubMedPubMedCentralCrossRef
6.
go back to reference Singh, Alok K., R. Wang, K.A Lombardo, M. Praharaj, C.K. Bullen, P. Um, S. Davis, et al. 2022. Dynamic single-cell RNA sequencing reveals BCG vaccination curtails SARS-CoV-2 induced disease severity and lung inflammation. biorxiv: the Preprint Server for Biology. Mar 15. https://doi.org/10.1101/2022.03.15.484018 Singh, Alok K., R. Wang, K.A Lombardo, M. Praharaj, C.K. Bullen, P. Um, S. Davis, et al. 2022. Dynamic single-cell RNA sequencing reveals BCG vaccination curtails SARS-CoV-2 induced disease severity and lung inflammation. biorxiv: the Preprint Server for Biology. Mar 15. https://​doi.​org/​10.​1101/​2022.​03.​15.​484018
7.
go back to reference Rakshit, S., V. Adiga, A. Ahmed, C. Parthiban, N.C. Kumar, P. Dwarkanath, S. Shivalingaiah, et al. 2022. BCG revaccination qualitatively and quantitatively enhances SARS-CoV-2 spike-specific neutralizing antibody and T cell responses induced by the COVISHIELDTM vaccine in SARS-CoV-2 seronegative young Indian adults. Research Square. Mar 2. https://doi.org/10.21203/rs.3.rs-1395683/v1 Rakshit, S., V. Adiga, A. Ahmed, C. Parthiban, N.C. Kumar, P. Dwarkanath, S. Shivalingaiah, et al. 2022. BCG revaccination qualitatively and quantitatively enhances SARS-CoV-2 spike-specific neutralizing antibody and T cell responses induced by the COVISHIELDTM vaccine in SARS-CoV-2 seronegative young Indian adults. Research Square. Mar 2. https://​doi.​org/​10.​21203/​rs.​3.​rs-1395683/​v1
8.
go back to reference Kowalewicz-Kulbat, M., and C. Locht. 2017. BCG and protection against inflammatory and auto-immune diseases. Expert Review of Vaccines 16 (7): 699–708.CrossRef Kowalewicz-Kulbat, M., and C. Locht. 2017. BCG and protection against inflammatory and auto-immune diseases. Expert Review of Vaccines 16 (7): 699–708.CrossRef
9.
go back to reference Yong, J., G. Lacan, H. Dang, T. Hsieh, B. Middleton, C. Wasserfall, et al. 2011. BCG vaccine-induced neuroprotection in a mouse model of Parkinson’s disease. PLoS One 6 (1): e16610.PubMedPubMedCentralCrossRef Yong, J., G. Lacan, H. Dang, T. Hsieh, B. Middleton, C. Wasserfall, et al. 2011. BCG vaccine-induced neuroprotection in a mouse model of Parkinson’s disease. PLoS One 6 (1): e16610.PubMedPubMedCentralCrossRef
10.
go back to reference Li, Q., Y. Zhang, J. Zou, F. Qi, J. Yang, Q. Yuan, et al. 2016. Neonatal vaccination with bacille Calmette-Guérin promotes the dendritic development of hippocampal neurons. Human Vaccines & Immunotherapeutics 12 (1): 140–149.CrossRef Li, Q., Y. Zhang, J. Zou, F. Qi, J. Yang, Q. Yuan, et al. 2016. Neonatal vaccination with bacille Calmette-Guérin promotes the dendritic development of hippocampal neurons. Human Vaccines & Immunotherapeutics 12 (1): 140–149.CrossRef
11.
go back to reference Han, J., X. Gu, Y. Li, and Q. Wu. 2020. Mechanisms of BCG in the treatment of bladder cancer-current understanding and the prospect. Biomedicine & Pharmacotherapy 129: 110393.CrossRef Han, J., X. Gu, Y. Li, and Q. Wu. 2020. Mechanisms of BCG in the treatment of bladder cancer-current understanding and the prospect. Biomedicine & Pharmacotherapy 129: 110393.CrossRef
12.
go back to reference Radhakrishnan, R.K., R.S. Thandi, D. Tripathi, P. Paidipally, M.K. McAllister, S. Mulik, et al. 2020. BCG vaccination reduces the mortality of Mycobacterium tuberculosis–infected type 2 diabetes mellitus mice. JCI Insight 5 (5). Radhakrishnan, R.K., R.S. Thandi, D. Tripathi, P. Paidipally, M.K. McAllister, S. Mulik, et al.  2020. BCG vaccination reduces the mortality of Mycobacterium tuberculosis–infected type 2 diabetes mellitus mice. JCI Insight 5 (5).
13.
go back to reference Brook, B., D.J. Harbeson, C.P. Shannon, B. Cai, D. He, R. Ben-Othman, et al. 2020. BCG vaccination–induced emergency granulopoiesis provides rapid protection from neonatal sepsis. Science Translational Medicine 12 (542). Brook, B., D.J. Harbeson, C.P. Shannon, B. Cai, D. He, R. Ben-Othman, et al. 2020. BCG vaccination–induced emergency granulopoiesis provides rapid protection from neonatal sepsis. Science Translational Medicine 12 (542).
14.
go back to reference Faustman, D.L., A. Lee, E.R. Hostetter, A. Aristarkhova, N.C. Ng, G.F. Shpilsky, et al. 2022. Multiple BCG vaccinations for the prevention of COVID-19 and other infectious diseases in type 1 diabetes. Cell Reports Medicine 3 (9): 100728.PubMedPubMedCentralCrossRef Faustman, D.L., A. Lee, E.R. Hostetter, A. Aristarkhova, N.C. Ng, G.F. Shpilsky, et al. 2022. Multiple BCG vaccinations for the prevention of COVID-19 and other infectious diseases in type 1 diabetes. Cell Reports Medicine 3 (9): 100728.PubMedPubMedCentralCrossRef
15.
go back to reference Cossu, D., S. Ruberto, K. Yokoyama, N. Hattori, and L.A. Sechi. 2022. Efficacy of BCG vaccine in animal models of neurological disorders. Vaccine 40 (3): 432–436.PubMedCrossRef Cossu, D., S. Ruberto, K. Yokoyama, N. Hattori, and L.A. Sechi. 2022. Efficacy of BCG vaccine in animal models of neurological disorders. Vaccine 40 (3): 432–436.PubMedCrossRef
16.
go back to reference Zuo, Z., F. Qi, Z. Xing, L. Yuan, Y. Yang, Z. He, et al. 2021. Bacille Calmette-Guérin attenuates vascular amyloid pathology and maximizes synaptic preservation in APP/PS1 mice following active amyloid-β immunotherapy. Neurobiology of Aging 101: 94–108.PubMedCrossRef Zuo, Z., F. Qi, Z. Xing, L. Yuan, Y. Yang, Z. He, et al. 2021. Bacille Calmette-Guérin attenuates vascular amyloid pathology and maximizes synaptic preservation in APP/PS1 mice following active amyloid-β immunotherapy. Neurobiology of Aging 101: 94–108.PubMedCrossRef
17.
go back to reference Gofrit, O.N., H. Bercovier, B.Y. Klein, I.R. Cohen, T. Ben-Hur, and C.L. Greenblatt. 2019. Can immunization with Bacillus Calmette-Guérin (BCG) protect against Alzheimer’s disease? Medical Hypotheses 123: 95–97.PubMedCrossRef Gofrit, O.N., H. Bercovier, B.Y. Klein, I.R. Cohen, T. Ben-Hur, and C.L. Greenblatt. 2019. Can immunization with Bacillus Calmette-Guérin (BCG) protect against Alzheimer’s disease? Medical Hypotheses 123: 95–97.PubMedCrossRef
18.
go back to reference Yedke, N.G., D. Soni, and P. Kumar. 2023. Effect of Bacille‐Calmette‐Guerin vaccine against rotenone‐induced Parkinson’s disease: role of neuroinflammation and neurotransmitters. Fundamental & Clinical Pharmacology. Dec 2. https://doi.org/10.1111/fcp.12968 Yedke, N.G., D. Soni, and P. Kumar. 2023. Effect of Bacille‐Calmette‐Guerin vaccine against rotenone‐induced Parkinson’s disease: role of neuroinflammation and neurotransmitters. Fundamental & Clinical Pharmacology. Dec 2. https://​doi.​org/​10.​1111/​fcp.​12968
19.
go back to reference Schaltz-Buchholzer, F., M. Kjær Sørensen, C.S. Benn, and P. Aaby. 2022. The introduction of BCG vaccination to neonates in Northern Sweden, 1927–31: re-analysis of historical data to understand the lower mortality among BCG-vaccinated children. Vaccine 40 (11): 1516–1524.PubMedCrossRef Schaltz-Buchholzer, F., M. Kjær Sørensen, C.S. Benn, and P. Aaby. 2022. The introduction of BCG vaccination to neonates in Northern Sweden, 1927–31: re-analysis of historical data to understand the lower mortality among BCG-vaccinated children. Vaccine 40 (11): 1516–1524.PubMedCrossRef
20.
go back to reference Chen, J., L. Gao, X. Wu, Y. Fan, M. Liu, L. Peng, et al. 2023. BCG-induced trained immunity: history, mechanisms and potential applications. Journal of Translational Medicine 21 (1): 106.PubMedPubMedCentralCrossRef Chen, J., L. Gao, X. Wu, Y. Fan, M. Liu, L. Peng, et al. 2023. BCG-induced trained immunity: history, mechanisms and potential applications. Journal of Translational Medicine 21 (1): 106.PubMedPubMedCentralCrossRef
21.
go back to reference Li, J., J. Lu, G. Wang, A. Zhao, and M. Xu. 2022. Past, present and future of Bacillus Calmette-Guérin vaccine use in China. Vaccines (Basel). 10 (7): 1157.PubMedPubMedCentralCrossRef Li, J., J. Lu, G. Wang, A. Zhao, and M. Xu. 2022. Past, present and future of Bacillus Calmette-Guérin vaccine use in China. Vaccines (Basel). 10 (7): 1157.PubMedPubMedCentralCrossRef
22.
go back to reference Singh, A.K., M.G. Netea, and W.R. Bishai. 2021. BCG turns 100: its nontraditional uses against viruses, cancer, and immunologic diseases. Journal of Clinical Investigation 131 (11). Singh, A.K., M.G. Netea, and W.R. Bishai. 2021. BCG turns 100: its nontraditional uses against viruses, cancer, and immunologic diseases. Journal of Clinical Investigation 131 (11).
23.
go back to reference Calmette, A., C. Guerin, and B. Weill-Halle. 1924. Essai d’immunisation contre l’infection tuberculeuse. Bulletin de l’Académie Nationale de Médecine 91: 787–796. Calmette, A., C. Guerin, and B. Weill-Halle. 1924. Essai d’immunisation contre l’infection tuberculeuse. Bulletin de l’Académie Nationale de Médecine 91: 787–796.
24.
go back to reference Mangtani, P., I. Abubakar, C. Ariti, R. Beynon, L. Pimpin, P.E.M. Fine, et al. 2014. Protection by BCG vaccine against tuberculosis: a systematic review of randomized controlled trials. Clinical Infectious Diseases 58 (4): 470–480.PubMedCrossRef Mangtani, P., I. Abubakar, C. Ariti, R. Beynon, L. Pimpin, P.E.M. Fine, et al. 2014. Protection by BCG vaccine against tuberculosis: a systematic review of randomized controlled trials. Clinical Infectious Diseases 58 (4): 470–480.PubMedCrossRef
25.
go back to reference Corner, L.A.L., B.M. Buddle, D.U. Pfeiffer, and R.S. Morris. 2001. Aerosol vaccination of the brushtail possum (Trichosurus vulpecula) with bacille Calmette–Guérin: the duration of protection. Veterinary Microbiology 81 (2): 181–191.PubMedCrossRef Corner, L.A.L., B.M. Buddle, D.U. Pfeiffer, and R.S. Morris. 2001. Aerosol vaccination of the brushtail possum (Trichosurus vulpecula) with bacille Calmette–Guérin: the duration of protection. Veterinary Microbiology 81 (2): 181–191.PubMedCrossRef
26.
go back to reference Elton, L., S. Kasaragod, H. Donoghue, H.A. Safar, P. Amankwah, A. Zumla, et al. 2023. Mapping the phylogeny and lineage history of geographically distinct BCG vaccine strains. Microbial Genomics 9 (8). Elton, L., S. Kasaragod, H. Donoghue, H.A. Safar, P. Amankwah, A. Zumla, et al. 2023. Mapping the phylogeny and lineage history of geographically distinct BCG vaccine strains. Microbial Genomics 9 (8).
27.
go back to reference Luca, S., and T. Mihaescu. 2013. History of BCG vaccine. Maedica (Bucur) 8 (1): 53–68.PubMed Luca, S., and T. Mihaescu. 2013. History of BCG vaccine. Maedica (Bucur) 8 (1): 53–68.PubMed
28.
go back to reference Tran, V., J. Liu, and M.A. Behr. 2014. BCG vaccines. Molecular Genetics of Mycobacteria 2 (1). Tran, V., J. Liu, and M.A. Behr. 2014. BCG vaccines. Molecular Genetics of Mycobacteria 2 (1).
29.
go back to reference Lobo, N., N.A. Brooks, A.R. Zlotta, J.D. Cirillo, S. Boorjian, P.C. Black, et al. 2021. 100 years of Bacillus Calmette-Guérin immunotherapy: from cattle to COVID-19. Nature Reviews. Urology 18 (10): 611–622.PubMedPubMedCentralCrossRef Lobo, N., N.A. Brooks, A.R. Zlotta, J.D. Cirillo, S. Boorjian, P.C. Black, et al. 2021. 100 years of Bacillus Calmette-Guérin immunotherapy: from cattle to COVID-19. Nature Reviews. Urology 18 (10): 611–622.PubMedPubMedCentralCrossRef
30.
go back to reference Yamazaki-Nakashimada, M.A., A. Unzueta, L. Berenise Gámez-González, N. González-Saldaña, and R.U. Sorensen. 2020. BCG: a vaccine with multiple faces. Human Vaccines & Immunotherapeutics 16 (8): 1841–1850.CrossRef Yamazaki-Nakashimada, M.A., A. Unzueta, L. Berenise Gámez-González, N. González-Saldaña, and R.U. Sorensen. 2020. BCG: a vaccine with multiple faces. Human Vaccines & Immunotherapeutics 16 (8): 1841–1850.CrossRef
31.
go back to reference Rakshit, S., V. Adiga, A. Ahmed, C. Parthiban, N. Chetan Kumar, P. Dwarkanath, et al. 2022. Evidence for the heterologous benefits of prior BCG vaccination on COVISHIELDTM vaccine-induced immune responses in SARS-CoV-2 seronegative young Indian adults. Frontiers in Immunology 4: 13. Rakshit, S., V. Adiga, A. Ahmed, C. Parthiban, N. Chetan Kumar, P. Dwarkanath, et al. 2022. Evidence for the heterologous benefits of prior BCG vaccination on COVISHIELDTM vaccine-induced immune responses in SARS-CoV-2 seronegative young Indian adults. Frontiers in Immunology 4: 13.
32.
go back to reference Kleinnijenhuis, J., J. Quintin, F. Preijers, C.S. Benn, L.A.B. Joosten, C. Jacobs, et al. 2014. Long-lasting effects of BCG vaccination on both heterologous Th1/Th17 responses and innate trained immunity. Journal of Innate Immunity 6 (2): 152–158.PubMedCrossRef Kleinnijenhuis, J., J. Quintin, F. Preijers, C.S. Benn, L.A.B. Joosten, C. Jacobs, et al. 2014. Long-lasting effects of BCG vaccination on both heterologous Th1/Th17 responses and innate trained immunity. Journal of Innate Immunity 6 (2): 152–158.PubMedCrossRef
33.
go back to reference Gela, A., M. Murphy, M. Rodo, K. Hadley, W.A. Hanekom, W.H. Boom, et al. 2022. Effects of BCG vaccination on donor unrestricted T cells in two prospective cohort studies. eBioMedicine 76: 103839.PubMedPubMedCentralCrossRef Gela, A., M. Murphy, M. Rodo, K. Hadley, W.A. Hanekom, W.H. Boom, et al. 2022. Effects of BCG vaccination on donor unrestricted T cells in two prospective cohort studies. eBioMedicine 76: 103839.PubMedPubMedCentralCrossRef
34.
go back to reference Kaufmann, E., J. Sanz, J.L. Dunn, N. Khan, L.E. Mendonça, A. Pacis, et al. 2018. BCG educates hematopoietic stem cells to generate protective innate immunity against tuberculosis. Cell 172 (1–2): 176-190.e19.PubMedCrossRef Kaufmann, E., J. Sanz, J.L. Dunn, N. Khan, L.E. Mendonça, A. Pacis, et al. 2018. BCG educates hematopoietic stem cells to generate protective innate immunity against tuberculosis. Cell 172 (1–2): 176-190.e19.PubMedCrossRef
35.
go back to reference Cirovic, B., L.C.J. de Bree, L. Groh, B.A. Blok, J. Chan, W.J.F.M. van der Velden, et al. 2020. BCG vaccination in humans elicits trained immunity via the hematopoietic progenitor compartment. Cell Host & Microbe 28 (2): 322-334.e5.CrossRef Cirovic, B., L.C.J. de Bree, L. Groh, B.A. Blok, J. Chan, W.J.F.M. van der Velden, et al. 2020. BCG vaccination in humans elicits trained immunity via the hematopoietic progenitor compartment. Cell Host & Microbe 28 (2): 322-334.e5.CrossRef
36.
go back to reference Singh, A.K., M. Praharaj, K.A. Lombardo, T. Yoshida, A. Matoso, A.S. Baras, et al. 2022. Re-engineered BCG overexpressing cyclic di-AMP augments trained immunity and exhibits improved efficacy against bladder cancer. Nature Communications 13 (1): 878.PubMedPubMedCentralCrossRef Singh, A.K., M. Praharaj, K.A. Lombardo, T. Yoshida, A. Matoso, A.S. Baras, et al. 2022. Re-engineered BCG overexpressing cyclic di-AMP augments trained immunity and exhibits improved efficacy against bladder cancer. Nature Communications 13 (1): 878.PubMedPubMedCentralCrossRef
37.
go back to reference Wang, Y., F. Ge, J. Wang, H. Li, B. Zheng, W. Li, et al. 2023. Mycobacterium bovis BCG given at birth followed by inactivated respiratory syncytial virus vaccine prevents vaccine-enhanced disease by promoting trained macrophages and resident memory t cells. Journal of Virology 97 (3). Wang, Y., F. Ge, J. Wang, H. Li, B. Zheng, W. Li, et al. 2023. Mycobacterium bovis BCG given at birth followed by inactivated respiratory syncytial virus vaccine prevents vaccine-enhanced disease by promoting trained macrophages and resident memory t cells. Journal of Virology 97 (3).
38.
go back to reference Koeken, V.A.C.M., A.J. Verrall, M.G. Netea, P.C. Hill, and R. van Crevel. 2019. Trained innate immunity and resistance to Mycobacterium tuberculosis infection. Clinical Microbiology and Infection 25 (12): 1468–1472.PubMedCrossRef Koeken, V.A.C.M., A.J. Verrall, M.G. Netea, P.C. Hill, and R. van Crevel. 2019. Trained innate immunity and resistance to Mycobacterium tuberculosis infection. Clinical Microbiology and Infection 25 (12): 1468–1472.PubMedCrossRef
39.
go back to reference Debisarun, P.A., G. Kilic, L.C.J. de Bree, L.J. Pennings, J. van Ingen, C.S. Benn, et al. 2023. The impact of BCG dose and revaccination on trained immunity. Clinical Immunology 246: 109208.PubMedCrossRef Debisarun, P.A., G. Kilic, L.C.J. de Bree, L.J. Pennings, J. van Ingen, C.S. Benn, et al. 2023. The impact of BCG dose and revaccination on trained immunity. Clinical Immunology 246: 109208.PubMedCrossRef
40.
go back to reference Moorlag, S.J.C.F.M., Y.A. Rodriguez-Rosales, J. Gillard, S. Fanucchi, K. Theunissen, B. Novakovic, et al. 2020. BCG vaccination induces long-term functional reprogramming of human neutrophils. Cell Reports 33 (7): 108387.PubMedCrossRef Moorlag, S.J.C.F.M., Y.A. Rodriguez-Rosales, J. Gillard, S. Fanucchi, K. Theunissen, B. Novakovic, et al. 2020. BCG vaccination induces long-term functional reprogramming of human neutrophils. Cell Reports 33 (7): 108387.PubMedCrossRef
41.
go back to reference Sarfas, C., A.D. White, L. Sibley, A.L. Morrison, J. Gullick, S. Lawrence, et al. 2021. Characterization of the infant immune system and the influence and immunogenicity of BCG vaccination in infant and adult rhesus macaques. Frontiers in Immunology 11: 12. Sarfas, C., A.D. White, L. Sibley, A.L. Morrison, J. Gullick, S. Lawrence, et al. 2021. Characterization of the infant immune system and the influence and immunogenicity of BCG vaccination in infant and adult rhesus macaques. Frontiers in Immunology 11: 12.
42.
go back to reference Kang, A., G. Ye, R. Singh, S. Afkhami, J. Bavananthasivam, X. Luo, et al. 223. Subcutaneous BCG vaccination protects against streptococcal pneumonia via regulating innate immune responses in the lung. EMBO Molecular Medicine 15 (7). Kang, A., G. Ye, R. Singh, S. Afkhami, J. Bavananthasivam, X. Luo, et al. 223. Subcutaneous BCG vaccination protects against streptococcal pneumonia via regulating innate immune responses in the lung. EMBO Molecular Medicine 15 (7).
43.
go back to reference Komine-Aizawa, S., S. Mizuno, A. Kawano, S. Hayakawa, K. Matsuo, and M. Honda. 2023. The induction of antigen 85B-specific CD8+ T cells by recombinant BCG protects against mycobacterial infection in mice. International Journal of Molecular Sciences 24 (2): 966.PubMedPubMedCentralCrossRef Komine-Aizawa, S., S. Mizuno, A. Kawano, S. Hayakawa, K. Matsuo, and M. Honda. 2023. The induction of antigen 85B-specific CD8+ T cells by recombinant BCG protects against mycobacterial infection in mice. International Journal of Molecular Sciences 24 (2): 966.PubMedPubMedCentralCrossRef
44.
go back to reference Aagaard, C., N.P.H. Knudsen, I. Sohn, A.A. Izzo, H. Kim, E.H. Kristiansen, et al. 2020. Immunization with Mycobacterium tuberculosis–specific antigens bypasses T cell differentiation from prior Bacillus Calmette-Guérin vaccination and improves protection in mice. The Journal of Immunology 205 (8): 2146–2155.PubMedPubMedCentralCrossRef Aagaard, C., N.P.H. Knudsen, I. Sohn, A.A. Izzo, H. Kim, E.H. Kristiansen, et al. 2020. Immunization with Mycobacterium tuberculosis–specific antigens bypasses T cell differentiation from prior Bacillus Calmette-Guérin vaccination and improves protection in mice. The Journal of Immunology 205 (8): 2146–2155.PubMedPubMedCentralCrossRef
45.
go back to reference Mathurin, K.S., G.W. Martens, H. Kornfeld, and R.M. Welsh. 2009. CD4 T-cell-mediated heterologous immunity between mycobacteria and poxviruses. Journal of Virology 83 (8): 3528–3539.PubMedPubMedCentralCrossRef Mathurin, K.S., G.W. Martens, H. Kornfeld, and R.M. Welsh. 2009. CD4 T-cell-mediated heterologous immunity between mycobacteria and poxviruses. Journal of Virology 83 (8): 3528–3539.PubMedPubMedCentralCrossRef
46.
go back to reference Triglia, D., K.M. Gogan, J. Keane, and M.P. O’Sullivan. 2023. Glucose metabolism and its role in the maturation and migration of human CD1c+ dendritic cells following exposure to BCG. Frontiers in Cellular and Infection Microbiology 5: 13. Triglia, D., K.M. Gogan, J. Keane, and M.P. O’Sullivan. 2023. Glucose metabolism and its role in the maturation and migration of human CD1c+ dendritic cells following exposure to BCG. Frontiers in Cellular and Infection Microbiology 5: 13.
47.
go back to reference Gonciarz, W., M. Chyb, and M. Chmiela. 2023. Mycobacterium bovis BCG increase the selected determinants of monocyte/macrophage activity, which were diminished in response to gastric pathogen Helicobacter pylori. Scientific Reports 13 (1): 3107.PubMedPubMedCentralCrossRef Gonciarz, W., M. Chyb, and M. Chmiela. 2023. Mycobacterium bovis BCG increase the selected determinants of monocyte/macrophage activity, which were diminished in response to gastric pathogen Helicobacter pylori. Scientific Reports 13 (1): 3107.PubMedPubMedCentralCrossRef
48.
go back to reference Peng, X., Y. Zhou, B. Zhang, X. Liang, J. Feng, Y. Huang, et al. 2024. Mucosal recombinant BCG vaccine induces lung-resident memory macrophages and enhances trained immunity via mTORC2/HK1-mediated metabolic rewiring. Journal of Biological Chemistry 300 (1): 105518.PubMedCrossRef Peng, X., Y. Zhou, B. Zhang, X. Liang, J. Feng, Y. Huang, et al. 2024. Mucosal recombinant BCG vaccine induces lung-resident memory macrophages and enhances trained immunity via mTORC2/HK1-mediated metabolic rewiring. Journal of Biological Chemistry 300 (1): 105518.PubMedCrossRef
49.
go back to reference Ahmed, A., H. Tripathi, K.E. van Meijgaarden, N.C. Kumar, v Adiga, S. Rakshit, et al. 2023. BCG revaccination in adults enhances pro-inflammatory markers of trained immunity along with anti-inflammatory pathways. iScience 26 (10): 107889.PubMedPubMedCentralCrossRef Ahmed, A., H. Tripathi, K.E. van Meijgaarden, N.C. Kumar, v Adiga, S. Rakshit, et al. 2023. BCG revaccination in adults enhances pro-inflammatory markers of trained immunity along with anti-inflammatory pathways. iScience 26 (10): 107889.PubMedPubMedCentralCrossRef
50.
go back to reference Narinyan, W., N. Poladian, D. Orujyan, A. Gargaloyan, and V. Venketaraman. 2022. Immunologic role of innate lymphoid cells against Mycobacterial tuberculosis Infection. Biomedicines. 10 (11): 2828.PubMedPubMedCentralCrossRef Narinyan, W., N. Poladian, D. Orujyan, A. Gargaloyan, and V. Venketaraman. 2022. Immunologic role of innate lymphoid cells against Mycobacterial tuberculosis Infection. Biomedicines. 10 (11): 2828.PubMedPubMedCentralCrossRef
51.
go back to reference Kumar, N.P., C. Padmapriyadarsini, A. Rajamanickam, P.K. Bhavani, A. Nancy, B. Jayadeepa, et al. 2021. BCG vaccination induces enhanced frequencies of memory T cells and altered plasma levels of common γc cytokines in elderly individuals. PLoS One 16 (11): :e0258743.PubMedCrossRef Kumar, N.P., C. Padmapriyadarsini, A. Rajamanickam, P.K. Bhavani, A. Nancy, B. Jayadeepa, et al. 2021. BCG vaccination induces enhanced frequencies of memory T cells and altered plasma levels of common γc cytokines in elderly individuals. PLoS One 16 (11): :e0258743.PubMedCrossRef
52.
go back to reference Gerosa, F., B. Baldani-Guerra, C. Nisii, V. Marchesini, G. Carra, and G. Trinchieri. 2002. Reciprocal activating interaction between natural killer cells and dendritic cells. The Journal of Experimental Medicine 195 (3): 327–333.PubMedPubMedCentralCrossRef Gerosa, F., B. Baldani-Guerra, C. Nisii, V. Marchesini, G. Carra, and G. Trinchieri. 2002. Reciprocal activating interaction between natural killer cells and dendritic cells. The Journal of Experimental Medicine 195 (3): 327–333.PubMedPubMedCentralCrossRef
53.
go back to reference Feinberg, J., C. Fieschi, R. Doffinger, M. Feinberg, T. Leclerc, S. Boisson-Dupuis, et al. 2004. Bacillus Calmette Guérin triggers the IL-12/IFN-γ axis by an IRAK-4- and NEMO-dependent, non-cognate interaction between monocytes, NK, and T lymphocytes. European Journal of Immunology 34 (11): 3276–3284.PubMedCrossRef Feinberg, J., C. Fieschi, R. Doffinger, M. Feinberg, T. Leclerc, S. Boisson-Dupuis, et al. 2004. Bacillus Calmette Guérin triggers the IL-12/IFN-γ axis by an IRAK-4- and NEMO-dependent, non-cognate interaction between monocytes, NK, and T lymphocytes. European Journal of Immunology 34 (11): 3276–3284.PubMedCrossRef
54.
go back to reference Perdomo, C., U. Zedler, A.A. Kühl, L. Lozza, P. Saikali, L.E. Sander, et al. 2016. Mucosal BCG vaccination induces protective lung-resident memory T cell populations against tuberculosis. mBio 7 (6). Perdomo, C., U. Zedler, A.A. Kühl, L. Lozza, P. Saikali, L.E. Sander, et al. 2016. Mucosal BCG vaccination induces protective lung-resident memory T cell populations against tuberculosis. mBio 7 (6).
55.
go back to reference Li, Q., and H.-H. Shen. 2009. Neonatal bacillus Calmette-Guérin vaccination inhibits de novo allergic inflammatory response in mice via alteration of CD4+CD25+ T-regulatory cells. Acta Pharmacologica Sinica 30 (1): 125–133.PubMedCrossRef Li, Q., and H.-H. Shen. 2009. Neonatal bacillus Calmette-Guérin vaccination inhibits de novo allergic inflammatory response in mice via alteration of CD4+CD25+ T-regulatory cells. Acta Pharmacologica Sinica 30 (1): 125–133.PubMedCrossRef
56.
go back to reference Aaby, P., A. Roth, H. Ravn, B.M. Napirna, A. Rodrigues, I.M. Lisse, et al. 2011. Randomized trial of BCG vaccination at birth to low-birth-weight children: beneficial nonspecific effects in the neonatal period? The Journal of Infectious Diseases 204 (2): 245–252.PubMedCrossRef Aaby, P., A. Roth, H. Ravn, B.M. Napirna, A. Rodrigues, I.M. Lisse, et al. 2011. Randomized trial of BCG vaccination at birth to low-birth-weight children: beneficial nonspecific effects in the neonatal period? The Journal of Infectious Diseases 204 (2): 245–252.PubMedCrossRef
57.
go back to reference Cancelier, A.C., F. Petronilho, A. Reinke, L. Constantino, R. Machado, C. Ritter, et al. 2009. Inflammatory and oxidative parameters in cord blood as diagnostic of early-onset neonatal sepsis: a case-control study. Pediatric Critical Care Medicine. 10 (4): 467–71.PubMedCrossRef Cancelier, A.C., F. Petronilho, A. Reinke, L. Constantino, R. Machado, C. Ritter, et al. 2009. Inflammatory and oxidative parameters in cord blood as diagnostic of early-onset neonatal sepsis: a case-control study. Pediatric Critical Care Medicine. 10 (4): 467–71.PubMedCrossRef
58.
go back to reference Moorlag, S.J.C.F.M., R.J.W. Arts, R. van Crevel, and M.G. Netea. 2019. Non-specific effects of BCG vaccine on viral infections. Clinical Microbiology and Infection 25 (12): 1473–1478.PubMedCrossRef Moorlag, S.J.C.F.M., R.J.W. Arts, R. van Crevel, and M.G. Netea. 2019. Non-specific effects of BCG vaccine on viral infections. Clinical Microbiology and Infection 25 (12): 1473–1478.PubMedCrossRef
59.
go back to reference Sylvester, R.J., A.P.M. van der Meijden, J.A. Witjes, and K. Kurth. 2005. Bacillus Calmette-Guerin versus chemotherapy for the intravesical treatment of patients with carcinoma in situ of the bladder: a meta-analysis of the published results of randomized clinical trials. Journal of Urology. 174 (1): 86–91.PubMedCrossRef Sylvester, R.J., A.P.M. van der Meijden, J.A. Witjes, and K. Kurth. 2005. Bacillus Calmette-Guerin versus chemotherapy for the intravesical treatment of patients with carcinoma in situ of the bladder: a meta-analysis of the published results of randomized clinical trials. Journal of Urology. 174 (1): 86–91.PubMedCrossRef
60.
go back to reference Lamm, D.L., B.A. Blumenstein, J.D. Crissman, J.E. Montie, J.E. Gottesman, B.A. Lowe, et al. 2000. Maintenance Bacillus Calmette-Guerin immunotherapy for recurrent TA, T1 and carcinoma in situ transitional cell carcinoma of the bladder: a randomized Southwest Oncology Group study. Journal of Urology 163 (4): 1124–1129.PubMedCrossRef Lamm, D.L., B.A. Blumenstein, J.D. Crissman, J.E. Montie, J.E. Gottesman, B.A. Lowe, et al. 2000. Maintenance Bacillus Calmette-Guerin immunotherapy for recurrent TA, T1 and carcinoma in situ transitional cell carcinoma of the bladder: a randomized Southwest Oncology Group study. Journal of Urology 163 (4): 1124–1129.PubMedCrossRef
61.
go back to reference Kleinnijenhuis, J., J. Quintin, F. Preijers, L.A.B. Joosten, D.C. Ifrim, S. Saeed, et al. 2012. Bacille Calmette-Guérin induces NOD2-dependent nonspecific protection from reinfection via epigenetic reprogramming of monocytes. Proceedings of the National Academy of Sciences. 109 (43): 17537–17542.CrossRef Kleinnijenhuis, J., J. Quintin, F. Preijers, L.A.B. Joosten, D.C. Ifrim, S. Saeed, et al. 2012. Bacille Calmette-Guérin induces NOD2-dependent nonspecific protection from reinfection via epigenetic reprogramming of monocytes. Proceedings of the National Academy of Sciences. 109 (43): 17537–17542.CrossRef
62.
go back to reference Méndez-Samperio, P., A. Pérez, and L. Alba. 2010. Reactive oxygen species-activated p38/ERK 1/2 MAPK signaling pathway in the Mycobacterium bovis Bacillus Calmette Guérin (BCG)-induced CCL2 secretion in human monocytic cell line THP-1. Archives of Medical Research 41 (8): 579–585.PubMedCrossRef Méndez-Samperio, P., A. Pérez, and L. Alba. 2010. Reactive oxygen species-activated p38/ERK 1/2 MAPK signaling pathway in the Mycobacterium bovis Bacillus Calmette Guérin (BCG)-induced CCL2 secretion in human monocytic cell line THP-1. Archives of Medical Research 41 (8): 579–585.PubMedCrossRef
63.
go back to reference Méndez-Samperio, P., A. Pérez, and L. Torres. 2009. Role of reactive oxygen species (ROS) in Mycobacterium bovis Bacillus Calmette Guérin-mediated up-regulation of the human cathelicidin LL-37 in A549 cells. Microbial Pathogenesis 47 (5): 252–257.PubMedCrossRef Méndez-Samperio, P., A. Pérez, and L. Torres. 2009. Role of reactive oxygen species (ROS) in Mycobacterium bovis Bacillus Calmette Guérin-mediated up-regulation of the human cathelicidin LL-37 in A549 cells. Microbial Pathogenesis 47 (5): 252–257.PubMedCrossRef
64.
go back to reference Al-Humairi, R.M.A., T. Hashim Mohammad, S. Thanoon Ahmed, and Ad’hiah AH. 2023. Systemic interleukin-6 response after intravesical instillation of Bacillus Calmette-Guérin and mitomycin C in superficial bladder cancer. Archives of Razi Institute 78 (1): 353–360.PubMedPubMedCentral Al-Humairi, R.M.A., T. Hashim Mohammad, S. Thanoon Ahmed, and Ad’hiah AH. 2023. Systemic interleukin-6 response after intravesical instillation of Bacillus Calmette-Guérin and mitomycin C in superficial bladder cancer. Archives of Razi Institute 78 (1): 353–360.PubMedPubMedCentral
65.
go back to reference Koeken, V.A.C.M. 2021. Controlling inflammation in the elderly with BCG vaccination. Science Advances 7 (32). Koeken, V.A.C.M. 2021. Controlling inflammation in the elderly with BCG vaccination. Science Advances 7 (32).
66.
go back to reference Koeken, V.A.C.M., L.C.J. de Bree, V.P. Mourits, S.J.C.F.M. Moorlag, J. Walk, B. Cirovic, et al. 2020. BCG vaccination in humans inhibits systemic inflammation in a sex-dependent manner. Journal of Clinical Investigation 130 (10): 5591–5602.PubMedPubMedCentralCrossRef Koeken, V.A.C.M., L.C.J. de Bree, V.P. Mourits, S.J.C.F.M. Moorlag, J. Walk, B. Cirovic, et al. 2020. BCG vaccination in humans inhibits systemic inflammation in a sex-dependent manner. Journal of Clinical Investigation 130 (10): 5591–5602.PubMedPubMedCentralCrossRef
67.
go back to reference Yang, W., Z. Dong, Y. Li, Y. Zhang, H. Fu, and Y. Xie. 2021. Therapeutic efficacy of chitosan nanoparticles loaded with BCG-polysaccharide nucleic acid and ovalbumin on airway inflammation in asthmatic mice. European Journal of Clinical Microbiology & Infectious Diseases. 40 (8): 1623–1631.CrossRef Yang, W., Z. Dong, Y. Li, Y. Zhang, H. Fu, and Y. Xie. 2021. Therapeutic efficacy of chitosan nanoparticles loaded with BCG-polysaccharide nucleic acid and ovalbumin on airway inflammation in asthmatic mice. European Journal of Clinical Microbiology & Infectious Diseases. 40 (8): 1623–1631.CrossRef
68.
go back to reference Simon Machado, R., K. Mathias, L. Joaquim, R. Willig de Quadros, F. Petronilho, and G.T. Rezin. 2023. From diabetic hyperglycemia to cerebrovascular damage: a narrative review. Brain Research 1821: 148611.PubMedCrossRef Simon Machado, R., K. Mathias, L. Joaquim, R. Willig de Quadros, F. Petronilho, and G.T. Rezin. 2023. From diabetic hyperglycemia to cerebrovascular damage: a narrative review. Brain Research 1821: 148611.PubMedCrossRef
69.
go back to reference Yedke, N.G., S. Upadhayay, R. Singh, S. Jamwal, S.F. Ahmad, and P. Kumar. 2023. Bacillus Calmette-Guérin vaccine attenuates haloperidol-induced TD-like behavioral and neurochemical alteration in experimental rats. Biomolecules 13 (11): 1667.PubMedPubMedCentralCrossRef Yedke, N.G., S. Upadhayay, R. Singh, S. Jamwal, S.F. Ahmad, and P. Kumar. 2023. Bacillus Calmette-Guérin vaccine attenuates haloperidol-induced TD-like behavioral and neurochemical alteration in experimental rats. Biomolecules 13 (11): 1667.PubMedPubMedCentralCrossRef
70.
go back to reference Dow, C.T., C.L. Greenblatt, E.D. Chan, and J.F. Dow. 2022. Evaluation of BCG vaccination and plasma amyloid: a prospective, pilot study with implications for Alzheimer’s disease. Microorganisms. 10 (2): 424.PubMedPubMedCentralCrossRef Dow, C.T., C.L. Greenblatt, E.D. Chan, and J.F. Dow. 2022. Evaluation of BCG vaccination and plasma amyloid: a prospective, pilot study with implications for Alzheimer’s disease. Microorganisms. 10 (2): 424.PubMedPubMedCentralCrossRef
71.
go back to reference Klein, B.Y., C.L. Greenblatt, O.N. Gofrit, and H. Bercovier. 2022. Bacillus Calmette-Guérin in immuno-regulation of Alzheimer’s disease. Front Aging Neurosci. 27: 14. Klein, B.Y., C.L. Greenblatt, O.N. Gofrit, and H. Bercovier. 2022. Bacillus Calmette-Guérin in immuno-regulation of Alzheimer’s disease. Front Aging Neurosci. 27: 14.
72.
go back to reference Klinger, D., B.L. Hill, N. Barda, E. Halperin, O.N. Gofrit, C.L. Greenblatt, et al. 2021. Bladder cancer immunotherapy by BCG is associated with a significantly reduced risk of Alzheimer’s disease and Parkinson’s disease. Vaccines (Basel). 9 (5): 491.PubMedPubMedCentralCrossRef Klinger, D., B.L. Hill, N. Barda, E. Halperin, O.N. Gofrit, C.L. Greenblatt, et al. 2021. Bladder cancer immunotherapy by BCG is associated with a significantly reduced risk of Alzheimer’s disease and Parkinson’s disease. Vaccines (Basel). 9 (5): 491.PubMedPubMedCentralCrossRef
73.
go back to reference Li, Q., X. Wang, Z.H. Wang, Z. Lin, J. Yang, J. Chen, et al. 2022. Changes in dendritic complexity and spine morphology following BCG immunization in APP/PS1 mice. Human Vaccines & Immunotherapeutics 18 (6). Li, Q., X. Wang, Z.H. Wang, Z. Lin, J. Yang, J. Chen, et al. 2022. Changes in dendritic complexity and spine morphology following BCG immunization in APP/PS1 mice. Human Vaccines & Immunotherapeutics 18 (6).
74.
go back to reference Zuo, Z., F. Qi, J. Yang, X. Wang, Y. Wu, Y. Wen, et al. 2017. Immunization with Bacillus Calmette-Guérin (BCG) alleviates neuroinflammation and cognitive deficits in APP/PS1 mice via the recruitment of inflammation-resolving monocytes to the brain. Neurobiology of Diseases 101: 27–39.CrossRef Zuo, Z., F. Qi, J. Yang, X. Wang, Y. Wu, Y. Wen, et al. 2017. Immunization with Bacillus Calmette-Guérin (BCG) alleviates neuroinflammation and cognitive deficits in APP/PS1 mice via the recruitment of inflammation-resolving monocytes to the brain. Neurobiology of Diseases 101: 27–39.CrossRef
75.
go back to reference Barichello, T., J.S. Generoso, L.R. Simões, J.A. Goularte, F. Petronilho, P. Saigal, et al. 2016. Role of microglial activation in the pathophysiology of bacterial meningitis. Molecular Neurobiology 53 (3): 1770–1781.PubMedCrossRef Barichello, T., J.S. Generoso, L.R. Simões, J.A. Goularte, F. Petronilho, P. Saigal, et al. 2016. Role of microglial activation in the pathophysiology of bacterial meningitis. Molecular Neurobiology 53 (3): 1770–1781.PubMedCrossRef
76.
go back to reference Laćan, G., H. Dang, B. Middleton, M.A. Horwitz, J. Tian, W.P. Melega, et al. 2013. Bacillus Calmette-Guerin vaccine-mediated neuroprotection is associated with regulatory T-cell induction in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson’s disease. Journal of Neuroscience Research 91 (10): 1292–1302.PubMedPubMedCentralCrossRef Laćan, G., H. Dang, B. Middleton, M.A. Horwitz, J. Tian, W.P. Melega, et al. 2013. Bacillus Calmette-Guerin vaccine-mediated neuroprotection is associated with regulatory T-cell induction in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson’s disease. Journal of Neuroscience Research 91 (10): 1292–1302.PubMedPubMedCentralCrossRef
77.
go back to reference Witschkowski, J., J. Behrends, R. Frank, L. Eggers, L. von Borstel, D. Hertz, et al. 2020. BCG Provides short-term protection from experimental cerebral malaria in mice. Vaccines (Basel). 8 (4): 745.PubMedPubMedCentralCrossRef Witschkowski, J., J. Behrends, R. Frank, L. Eggers, L. von Borstel, D. Hertz, et al. 2020. BCG Provides short-term protection from experimental cerebral malaria in mice. Vaccines (Basel). 8 (4): 745.PubMedPubMedCentralCrossRef
78.
go back to reference Kulkarni, S., S. Mukherjee, A. Pandey, R. Dahake, U. Padmanabhan, and A.S. Chowdhary. 2016. Bacillus Calmette-Guérin Confers neuroprotection in a murine model of Japanese encephalitis. NeuroImmunoModulation 23 (5–6): 278–286.PubMedCrossRef Kulkarni, S., S. Mukherjee, A. Pandey, R. Dahake, U. Padmanabhan, and A.S. Chowdhary. 2016. Bacillus Calmette-Guérin Confers neuroprotection in a murine model of Japanese encephalitis. NeuroImmunoModulation 23 (5–6): 278–286.PubMedCrossRef
79.
go back to reference Yang, J., F. Qi, and Z. Yao. 2016. Neonatal Bacillus Calmette-Guérin vaccination alleviates lipopolysaccharide-induced neurobehavioral impairments and neuroinflammation in adult mice. Molecular Medicine Reports 14 (2): 1574–1586.PubMedPubMedCentralCrossRef Yang, J., F. Qi, and Z. Yao. 2016. Neonatal Bacillus Calmette-Guérin vaccination alleviates lipopolysaccharide-induced neurobehavioral impairments and neuroinflammation in adult mice. Molecular Medicine Reports 14 (2): 1574–1586.PubMedPubMedCentralCrossRef
80.
go back to reference Yang, J., F. Qi, H. Gu, J. Zou, Y. Yang, Q. Yuan, et al. 2016. Neonatal BCG vaccination of mice improves neurogenesis and behavior in early life. Brain Research Bulletin 120: 25–33.PubMedCrossRef Yang, J., F. Qi, H. Gu, J. Zou, Y. Yang, Q. Yuan, et al. 2016. Neonatal BCG vaccination of mice improves neurogenesis and behavior in early life. Brain Research Bulletin 120: 25–33.PubMedCrossRef
81.
go back to reference Cossu, D., K. Yokoyama, Y. Tomizawa, E. Momotani, and N. Hattori. 2017. Altered humoral immunity to mycobacterial antigens in Japanese patients affected by inflammatory demyelinating diseases of the central nervous system. Scientific Reports 7 (1): 3179.PubMedPubMedCentralCrossRef Cossu, D., K. Yokoyama, Y. Tomizawa, E. Momotani, and N. Hattori. 2017. Altered humoral immunity to mycobacterial antigens in Japanese patients affected by inflammatory demyelinating diseases of the central nervous system. Scientific Reports 7 (1): 3179.PubMedPubMedCentralCrossRef
82.
go back to reference Ristori, G., M.G. Buzzi, U. Sabatini, E. Giugni, S. Bastianello, F. Viselli, et al. 1999. Use of Bacille Calmette-Guèrin (BCG) in multiple sclerosis. Neurology 53 (7): 1588–1588.PubMedCrossRef Ristori, G., M.G. Buzzi, U. Sabatini, E. Giugni, S. Bastianello, F. Viselli, et al. 1999. Use of Bacille Calmette-Guèrin (BCG) in multiple sclerosis. Neurology 53 (7): 1588–1588.PubMedCrossRef
83.
go back to reference Paolillo, A., M.G. Buzzi, E. Giugni, U. Sabatini, S. Bastianello, C. Pozzilli, et al. 2003. The effect of Bacille Calmette-Guérin on the evolution of new enhancing lesions to hypointense T1 lesions in relapsing remitting MS. Journal of Neurology 250 (2): 247–248.PubMedCrossRef Paolillo, A., M.G. Buzzi, E. Giugni, U. Sabatini, S. Bastianello, C. Pozzilli, et al. 2003. The effect of Bacille Calmette-Guérin on the evolution of new enhancing lesions to hypointense T1 lesions in relapsing remitting MS. Journal of Neurology 250 (2): 247–248.PubMedCrossRef
84.
go back to reference Cossu, D., K. Yokoyama, T. Sakanishi, L.A. Sechi, and N. Hattori. 2023. Bacillus Calmette-Guérin Tokyo-172 vaccine provides age-related neuroprotection in actively induced and spontaneous experimental autoimmune encephalomyelitis models. Clinical and Experimental Immunology 212 (1): 70–80.PubMedPubMedCentralCrossRef Cossu, D., K. Yokoyama, T. Sakanishi, L.A. Sechi, and N. Hattori. 2023. Bacillus Calmette-Guérin Tokyo-172 vaccine provides age-related neuroprotection in actively induced and spontaneous experimental autoimmune encephalomyelitis models. Clinical and Experimental Immunology 212 (1): 70–80.PubMedPubMedCentralCrossRef
85.
go back to reference Keefe, R.C., H. Takahashi, L. Tran, K. Nelson, N. Ng, W.M. Kühtreiber, et al. 2021. BCG therapy is associated with long-term, durable induction of Treg signature genes by epigenetic modulation. Scientific Reports 11 (1): 14933.PubMedPubMedCentralCrossRef Keefe, R.C., H. Takahashi, L. Tran, K. Nelson, N. Ng, W.M. Kühtreiber, et al. 2021. BCG therapy is associated with long-term, durable induction of Treg signature genes by epigenetic modulation. Scientific Reports 11 (1): 14933.PubMedPubMedCentralCrossRef
86.
go back to reference Ristori, G., D. Faustman, G. Matarese, S. Romano, and M. Salvetti. 2018. Bridging the gap between vaccination with Bacille Calmette-Guérin (BCG) and immunological tolerance: the cases of type 1 diabetes and multiple sclerosis. Current Opinion in Immunology 55: 89–96.PubMedCrossRef Ristori, G., D. Faustman, G. Matarese, S. Romano, and M. Salvetti. 2018. Bridging the gap between vaccination with Bacille Calmette-Guérin (BCG) and immunological tolerance: the cases of type 1 diabetes and multiple sclerosis. Current Opinion in Immunology 55: 89–96.PubMedCrossRef
87.
go back to reference Gonzalez-Pena, D., S.E. Nixon, J.C. O’Connor, B.R. Southey, M.A. Lawson, R.H. McCusker, et al. 2016. Microglia transcriptome changes in a model of depressive behavior after immune challenge. PLoS One1 11 (3).CrossRef Gonzalez-Pena, D., S.E. Nixon, J.C. O’Connor, B.R. Southey, M.A. Lawson, R.H. McCusker, et al. 2016. Microglia transcriptome changes in a model of depressive behavior after immune challenge. PLoS One1 11 (3).CrossRef
88.
go back to reference Cao, D.H., J.C. Wang, J. Liu, Y.T. Du, L.W. Cui, and Y.M. Cao. 2016. Bacillus Calmette-Guerin-inoculation at different time points influences the outcome of C57BL/6 mice infected with Plasmodium chabaudi chabaudi AS. Folia Parasitol (Praha). 1: 63. Cao, D.H., J.C. Wang, J. Liu, Y.T. Du, L.W. Cui, and Y.M. Cao. 2016. Bacillus Calmette-Guerin-inoculation at different time points influences the outcome of C57BL/6 mice infected with Plasmodium chabaudi chabaudi AS. Folia Parasitol (Praha). 1: 63.
89.
go back to reference Elvang, T., J.P. Christensen, R. Billeskov, T. Thi Kim Thanh, P. Holst, A.R. Thomsen, et al. 2009. CD4 and CD8 T cell responses to the M. tuberculosis Ag85B-TB10.4 promoted by adjuvanted subunit, adenovector or heterologous prime boost vaccination. PLoS One 4 (4): e5139.PubMedPubMedCentralCrossRef Elvang, T., J.P. Christensen, R. Billeskov, T. Thi Kim Thanh, P. Holst, A.R. Thomsen, et al. 2009. CD4 and CD8 T cell responses to the M. tuberculosis Ag85B-TB10.4 promoted by adjuvanted subunit, adenovector or heterologous prime boost vaccination. PLoS One 4 (4): e5139.PubMedPubMedCentralCrossRef
90.
go back to reference Falke, J., J. Parkkinen, L. Vaahtera, C.A. Hulsbergen-van de Kaa, E. Oosterwijk, and J.A. Witjes. 2018. Curcumin as treatment for bladder cancer: a preclinical study of cyclodextrin-curcumin complex and BCG as intravesical treatment in an orthotopic bladder cancer rat model. BioMed Research International 2018: 1–7.CrossRef Falke, J., J. Parkkinen, L. Vaahtera, C.A. Hulsbergen-van de Kaa, E. Oosterwijk, and J.A. Witjes. 2018. Curcumin as treatment for bladder cancer: a preclinical study of cyclodextrin-curcumin complex and BCG as intravesical treatment in an orthotopic bladder cancer rat model. BioMed Research International 2018: 1–7.CrossRef
91.
go back to reference Ferraz, J.C., E. Stavropoulos, M. Yang, S. Coade, C. Espitia, D.B. Lowrie, et al. 2004. A heterologous DNA priming-Mycobacterium bovis BCG boosting immunization strategy using mycobacterial Hsp70, Hsp65, and Apa antigens improves protection against tuberculosis in mice. Infection and Immunity 72 (12): 6945–6950.PubMedPubMedCentralCrossRef Ferraz, J.C., E. Stavropoulos, M. Yang, S. Coade, C. Espitia, D.B. Lowrie, et al. 2004. A heterologous DNA priming-Mycobacterium bovis BCG boosting immunization strategy using mycobacterial Hsp70, Hsp65, and Apa antigens improves protection against tuberculosis in mice. Infection and Immunity 72 (12): 6945–6950.PubMedPubMedCentralCrossRef
92.
go back to reference Fitzpatrick, M., M.M. Ho, S. Clark, B. Dagg, B. Khatri, F. Lanni, et al. 2019. Comparison of pellicle and shake flask-grown BCG strains by quality control assays and protection studies. Tuberculosis 114: 47–53.PubMedCrossRef Fitzpatrick, M., M.M. Ho, S. Clark, B. Dagg, B. Khatri, F. Lanni, et al. 2019. Comparison of pellicle and shake flask-grown BCG strains by quality control assays and protection studies. Tuberculosis 114: 47–53.PubMedCrossRef
93.
go back to reference Gomes-Giacoia, E., M. Miyake, S. Goodison, A. Sriharan, G. Zhang, L. You, et al. 2014. Intravesical ALT-803 and BCG treatment reduces tumor burden in a carcinogen induced bladder cancer rat model; a role for cytokine production and NK cell expansion. PLoS One1 9 (6): e96705.CrossRef Gomes-Giacoia, E., M. Miyake, S. Goodison, A. Sriharan, G. Zhang, L. You, et al. 2014. Intravesical ALT-803 and BCG treatment reduces tumor burden in a carcinogen induced bladder cancer rat model; a role for cytokine production and NK cell expansion. PLoS One1 9 (6): e96705.CrossRef
94.
go back to reference Hogarth, P.J., K.E. Logan, J.C. Ferraz, R.G. Hewinson, and M.A. Chambers. 2006. Protective efficacy induced by Mycobacterium bovis bacille Calmette-Guèrin can be augmented in an antigen independent manner by use of non-coding plasmid DNA. Vaccine. 24 (1): 95–101.PubMedCrossRef Hogarth, P.J., K.E. Logan, J.C. Ferraz, R.G. Hewinson, and M.A. Chambers. 2006. Protective efficacy induced by Mycobacterium bovis bacille Calmette-Guèrin can be augmented in an antigen independent manner by use of non-coding plasmid DNA. Vaccine. 24 (1): 95–101.PubMedCrossRef
95.
go back to reference Huang, P., C. Ma, P. Xu, K. Guo, A. Xu, and C. Liu. 2015. Efficacy of intravesical Bacillus Calmette-Guérin therapy against tumor immune escape in an orthotopic model of bladder cancer. Experimental and Therapeutic Medicine 9 (1): 162–166.PubMedCrossRef Huang, P., C. Ma, P. Xu, K. Guo, A. Xu, and C. Liu. 2015. Efficacy of intravesical Bacillus Calmette-Guérin therapy against tumor immune escape in an orthotopic model of bladder cancer. Experimental and Therapeutic Medicine 9 (1): 162–166.PubMedCrossRef
96.
go back to reference Kolibab, K., A. Yang, S.C. Derrick, T.A. Waldmann, L.P. Perera, and S.L. Morris. 2010. Highly persistent and effective prime/boost regimens against tuberculosis that use a multivalent modified vaccine virus Ankara-based tuberculosis vaccine with interleukin-15 as a molecular adjuvant. Clinical and Vaccine Immunology. 17 (5): 793–801.PubMedPubMedCentralCrossRef Kolibab, K., A. Yang, S.C. Derrick, T.A. Waldmann, L.P. Perera, and S.L. Morris. 2010. Highly persistent and effective prime/boost regimens against tuberculosis that use a multivalent modified vaccine virus Ankara-based tuberculosis vaccine with interleukin-15 as a molecular adjuvant. Clinical and Vaccine Immunology. 17 (5): 793–801.PubMedPubMedCentralCrossRef
97.
go back to reference Lombardo, K.A., A. Obradovic, A.K. Singh, J.L. Liu, G. Joice, M. Kates, et al. 2022. BCG invokes superior STING-mediated innate immune response over radiotherapy in a carcinogen murine model of urothelial cancer. The Journal of Pathology 256 (2): 223–234.PubMedCrossRef Lombardo, K.A., A. Obradovic, A.K. Singh, J.L. Liu, G. Joice, M. Kates, et al. 2022. BCG invokes superior STING-mediated innate immune response over radiotherapy in a carcinogen murine model of urothelial cancer. The Journal of Pathology 256 (2): 223–234.PubMedCrossRef
98.
go back to reference McShane, H., R. Brookes, S.C. Gilbert, and A.V.S. Hill. 2001. Enhanced immunogenicity of CD4(+) t-cell responses and protective efficacy of a DNA-modified vaccinia virus Ankara prime-boost vaccination regimen for murine tuberculosis. Infection and Immunity 69 (2): 681–686.PubMedPubMedCentralCrossRef McShane, H., R. Brookes, S.C. Gilbert, and A.V.S. Hill. 2001. Enhanced immunogenicity of CD4(+) t-cell responses and protective efficacy of a DNA-modified vaccinia virus Ankara prime-boost vaccination regimen for murine tuberculosis. Infection and Immunity 69 (2): 681–686.PubMedPubMedCentralCrossRef
99.
go back to reference Romano, M., S. Dsouza, P. Adnet, R. Laali, F. Jurion, K. Palfliet, et al. 2006. Priming but not boosting with plasmid DNA encoding mycolyl-transferase Ag85A from Mycobacterium tuberculosis increases the survival time of Mycobacterium bovis BCG vaccinated mice against low dose intravenous challenge with M. tuberculosis H37Rv. Vaccine. 24 (16): 3353–3364.PubMedCrossRef Romano, M., S. Dsouza, P. Adnet, R. Laali, F. Jurion, K. Palfliet, et al. 2006. Priming but not boosting with plasmid DNA encoding mycolyl-transferase Ag85A from Mycobacterium tuberculosis increases the survival time of Mycobacterium bovis BCG vaccinated mice against low dose intravenous challenge with M. tuberculosis H37Rv. Vaccine. 24 (16): 3353–3364.PubMedCrossRef
100.
go back to reference Skinner, M.A., A.J. Ramsay, G.S. Buchan, D.L. Keen, C. Ranasinghe, L. Slobbe, et al. 2003. A DNA prime-live vaccine boost strategy in mice can augment IFN-γ responses to mycobacterial antigens but does not increase the protective efficacy of two attenuated strains of Mycobacterium bovis against bovine tuberculosis. Immunology 108 (4): 548–555.PubMedPubMedCentralCrossRef Skinner, M.A., A.J. Ramsay, G.S. Buchan, D.L. Keen, C. Ranasinghe, L. Slobbe, et al. 2003. A DNA prime-live vaccine boost strategy in mice can augment IFN-γ responses to mycobacterial antigens but does not increase the protective efficacy of two attenuated strains of Mycobacterium bovis against bovine tuberculosis. Immunology 108 (4): 548–555.PubMedPubMedCentralCrossRef
101.
go back to reference Song, D., F. Qi, S. Liu, Z. Tang, J. Duan, and Z. Yao. 2020. The adoptive transfer of BCG-induced T lymphocytes contributes to hippocampal cell proliferation and tempers anxiety-like behavior in immune deficient mice. PLoS One 15 (4): e0225874.PubMedPubMedCentralCrossRef Song, D., F. Qi, S. Liu, Z. Tang, J. Duan, and Z. Yao. 2020. The adoptive transfer of BCG-induced T lymphocytes contributes to hippocampal cell proliferation and tempers anxiety-like behavior in immune deficient mice. PLoS One 15 (4): e0225874.PubMedPubMedCentralCrossRef
102.
go back to reference Tkachuk, A.P., V.A. Gushchin, V.D. Potapov, A.V. Demidenko, V.G. Lunin, and A.L. Gintsburg. 2017. Multi-subunit BCG booster vaccine GamTBvac: assessment of immunogenicity and protective efficacy in murine and guinea pig TB models. PLoS One 12 (4): e0176784.PubMedPubMedCentralCrossRef Tkachuk, A.P., V.A. Gushchin, V.D. Potapov, A.V. Demidenko, V.G. Lunin, and A.L. Gintsburg. 2017. Multi-subunit BCG booster vaccine GamTBvac: assessment of immunogenicity and protective efficacy in murine and guinea pig TB models. PLoS One 12 (4): e0176784.PubMedPubMedCentralCrossRef
103.
go back to reference Uranga, S., D. Marinova, C. Martin, and N. Aguilo. 2016. Protective efficacy and pulmonary immune response following subcutaneous and intranasal BCG administration in mice. Journal of Visualized Experiments (115). Uranga, S., D. Marinova, C. Martin, and N. Aguilo. 2016. Protective efficacy and pulmonary immune response following subcutaneous and intranasal BCG administration in mice. Journal of Visualized Experiments (115).
104.
go back to reference Pedras-Vasconcelos, J.A., Y. Chapdelaine, R. Dudani, H. van Faassen, D.K. Smith, and S. Sad. 2002. Mycobacterium bovis BCG-infected mice are more susceptible to staphylococcal enterotoxin B-mediated toxic shock than uninfected mice despite reduced in vitro splenocyte responses to superantigens. Infection and Immunity 70 (8): 4148–4157.PubMedPubMedCentralCrossRef Pedras-Vasconcelos, J.A., Y. Chapdelaine, R. Dudani, H. van Faassen, D.K. Smith, and S. Sad. 2002. Mycobacterium bovis BCG-infected mice are more susceptible to staphylococcal enterotoxin B-mediated toxic shock than uninfected mice despite reduced in vitro splenocyte responses to superantigens. Infection and Immunity 70 (8): 4148–4157.PubMedPubMedCentralCrossRef
105.
go back to reference Xu, H., Y. Jia, Y. Li, C. Wei, W. Wang, R. Guo, et al. 2019. IL-10 Dampens the Th1 and Tc activation through modulating DC functions in BCG vaccination. Mediators of Inflammation 12 (2019): 1–10. Xu, H., Y. Jia, Y. Li, C. Wei, W. Wang, R. Guo, et al. 2019. IL-10 Dampens the Th1 and Tc activation through modulating DC functions in BCG vaccination. Mediators of Inflammation 12 (2019): 1–10.
106.
go back to reference Zhou, H., X. Lu, J. Huang, P. Jordan, S. Ma, L. Xu, et al. 2022. Induction of trained immunity protects neonatal mice against microbial sepsis by boosting both the inflammatory response and antimicrobial activity. Journal of Inflammation Research 15: 3829–3845.PubMedPubMedCentralCrossRef Zhou, H., X. Lu, J. Huang, P. Jordan, S. Ma, L. Xu, et al. 2022. Induction of trained immunity protects neonatal mice against microbial sepsis by boosting both the inflammatory response and antimicrobial activity. Journal of Inflammation Research 15: 3829–3845.PubMedPubMedCentralCrossRef
Metadata
Title
Bacillus Calmette-Guérin (BCG)-Induced Protection in Brain Disorders
Authors
Khiany Mathias
Richard Simon Machado
Solange Stork
Carla Damasio Martins
Amanda Christine da Silva Kursancew
Victória Linden de Rezende
Cinara Ludvig Gonçalves
Tatiana Barichello
Josiane Somariva Prophiro
Fabricia Petronilho
Publication date
26-04-2024
Publisher
Springer US
Published in
Inflammation
Print ISSN: 0360-3997
Electronic ISSN: 1573-2576
DOI
https://doi.org/10.1007/s10753-024-02018-1
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