BCG immunization induces CX3CR1
Journal
Nature immunology
ISSN: 1529-2916
Titre abrégé: Nat Immunol
Pays: United States
ID NLM: 100941354
Informations de publication
Date de publication:
15 Jan 2024
15 Jan 2024
Historique:
received:
18
08
2023
accepted:
20
12
2023
medline:
16
1
2024
pubmed:
16
1
2024
entrez:
15
1
2024
Statut:
aheadofprint
Résumé
After a century of using the Bacillus Calmette-Guérin (BCG) vaccine, our understanding of its ability to provide protection against homologous (Mycobacterium tuberculosis) or heterologous (for example, influenza virus) infections remains limited. Here we show that systemic (intravenous) BCG vaccination provides significant protection against subsequent influenza A virus infection in mice. We further demonstrate that the BCG-mediated cross-protection against influenza A virus is largely due to the enrichment of conventional CD4
Identifiants
pubmed: 38225437
doi: 10.1038/s41590-023-01739-z
pii: 10.1038/s41590-023-01739-z
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Gouvernement du Canada | Instituts de Recherche en Santé du Canada | CIHR Skin Research Training Centre (Skin Research Training Centre)
ID : 168884
Organisme : Gouvernement du Canada | Instituts de Recherche en Santé du Canada | CIHR Skin Research Training Centre (Skin Research Training Centre)
ID : 168885
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer Nature America, Inc.
Références
Calmette A. G. C., Boquet A. & Négre L. La vaccination préventive contre la tuberculose par le ‘BCG’. Am. J. Public Health Nations Health 18, 1075 (1928).
Mangtani, P. et al. Protection by BCG vaccine against tuberculosis: a systematic review of randomized controlled trials. Clin. Infect. Dis. 58, 470–480 (2014).
pubmed: 24336911
doi: 10.1093/cid/cit790
Benn, C. S., Netea, M. G., Selin, L. K. & Aaby, P. A small jab - a big effect: nonspecific immunomodulation by vaccines. Trends Immunol. 34, 431–439 (2013).
pubmed: 23680130
doi: 10.1016/j.it.2013.04.004
Garly, M. L. et al. BCG scar and positive tuberculin reaction associated with reduced child mortality in West Africa. A non-specific beneficial effect of BCG? Vaccine 21, 2782–2790 (2003).
pubmed: 12798618
doi: 10.1016/S0264-410X(03)00181-6
Prentice, S. et al. BCG-induced non-specific effects on heterologous infectious disease in Ugandan neonates: an investigator-blind randomised controlled trial. Lancet Infect. Dis. 21, 993–1003 (2021).
pubmed: 33609457
pmcid: 8222005
doi: 10.1016/S1473-3099(20)30653-8
Kleinnijenhuis, J. et al. Bacille Calmette–Guerin induces NOD2-dependent nonspecific protection from reinfection via epigenetic reprogramming of monocytes. Proc. Natl Acad. Sci. USA 109, 17537–17542 (2012).
pubmed: 22988082
pmcid: 3491454
doi: 10.1073/pnas.1202870109
Arts, R. J. W. et al. BCG vaccination protects against experimental viral infection in humans through the induction of cytokines associated with trained immunity. Cell Host Microbe 23, 89–100 (2018).
pubmed: 29324233
doi: 10.1016/j.chom.2017.12.010
van ‘t Wout, J. W., Poell, R. & van Furth, R. The role of BCG/PPD-activated macrophages in resistance against systemic candidiasis in mice. Scand. J. Immunol. 36, 713–719 (1992).
pubmed: 1439583
doi: 10.1111/j.1365-3083.1992.tb03132.x
Tribouley, J., Tribouley-Duret, J. & Appriou, M. Effect of Bacillus Callmette Guerin (BCG) on the receptivity of nude mice to Schistosoma mansoni. C. R. Seances Soc. Biol. Fil. 172, 902–904 (1978).
pubmed: 157204
Hippmann, G., Wekkeli, M., Rosenkranz, A. R., Jarisch, R. & Götz, M.Nonspecific immune stimulation with BCG in Herpes simplex recidivans. Follow-up 5 to 10 years after BCG vaccination.Wien. Klin. Wochenschr. 104, 200–204 (1992).
pubmed: 1523844
Giamarellos-Bourboulis, E. J. et al. Activate: randomized clinical trial of BCG vaccination against infection in the elderly. Cell 183, 315–323 (2020).
pubmed: 32941801
pmcid: 7462457
doi: 10.1016/j.cell.2020.08.051
Stensballe, L. G. et al. Acute lower respiratory tract infections and respiratory syncytial virus in infants in Guinea-Bissau: a beneficial effect of BCG vaccination for girls community based case–control study. Vaccine 23, 1251–1257 (2005).
pubmed: 15652667
doi: 10.1016/j.vaccine.2004.09.006
Wardhana, Datau, E. A., Sultana, A., Mandang, V. V. & Jim, E. The efficacy of Bacillus Calmette–Guerin vaccinations for the prevention of acute upper respiratory tract infection in the elderly. Acta Med Indones. 43, 185–190 (2011).
pubmed: 21979284
Kaufmann, E. et al. BCG educates hematopoietic stem cells to generate protective innate immunity against tuberculosis. Cell 172, 176–190 (2018).
pubmed: 29328912
doi: 10.1016/j.cell.2017.12.031
Khan, N. et al. M. tuberculosis reprograms hematopoietic stem cells to limit myelopoiesis and impair trained immunity. Cell 183, 752–770 (2020).
pubmed: 33125891
pmcid: 7599081
doi: 10.1016/j.cell.2020.09.062
Barclay, W. R., Anacker, R. L., Brehmer, W., Leif, W. & Ribi, E. Aerosol-induced tuberculosis in subhuman primates and the course of the disease after intravenous BCG vaccination. Infect. Immun. 2, 574–582 (1970).
pubmed: 16557880
pmcid: 416053
doi: 10.1128/iai.2.5.574-582.1970
Darrah, P. A. et al. Prevention of tuberculosis in macaques after intravenous BCG immunization. Nature 577, 95–102 (2020).
pubmed: 31894150
pmcid: 7015856
doi: 10.1038/s41586-019-1817-8
Darrah, P. A. et al. Airway T cells are a correlate of i.v. Bacille Calmette–Guerin-mediated protection against tuberculosis in rhesus macaques. Cell Host Microbe 31, 962–977 (2023).
pubmed: 37267955
doi: 10.1016/j.chom.2023.05.006
Selin, L. K., Nahill, S. R. & Welsh, R. M. Cross-reactivities in memory cytotoxic T lymphocyte recognition of heterologous viruses. J. Exp. Med. 179, 1933–1943 (1994).
pubmed: 8195718
doi: 10.1084/jem.179.6.1933
Mason, D. A very high level of crossreactivity is an essential feature of the T-cell receptor. Immunol. Today 19, 395–404 (1998).
pubmed: 9745202
doi: 10.1016/S0167-5699(98)01299-7
Hesslein, D. G. & Schatz, D. G. Factors and forces controlling V(D)J recombination. Adv. Immunol. 78, 169–232 (2001).
pubmed: 11432204
doi: 10.1016/S0065-2776(01)78004-2
Wedemeyer, H., Mizukoshi, E., Davis, A. R., Bennink, J. R. & Rehermann, B. Cross-reactivity between hepatitis C virus and influenza A virus determinant-specific cytotoxic T cells. J. Virol. 75, 11392–11400 (2001).
pubmed: 11689620
pmcid: 114725
doi: 10.1128/JVI.75.23.11392-11400.2001
Pihlgren, M., Dubois, P. M., Tomkowiak, M., Sjögren, T. & Marvel, J. Resting memory CD8
pubmed: 8976170
pmcid: 2196370
doi: 10.1084/jem.184.6.2141
Tough, D. F., Borrow, P. & Sprent, J. Induction of bystander T cell proliferation by viruses and type I interferon in vivo. Science 272, 1947–1950 (1996).
pubmed: 8658169
doi: 10.1126/science.272.5270.1947
Kim, J. et al. Innate-like cytotoxic function of bystander-activated CD8
pubmed: 29305140
doi: 10.1016/j.immuni.2017.11.025
Zhang, X., Sun, S., Hwang, I., Tough, D. F. & Sprent, J. Potent and selective stimulation of memory-phenotype CD8
pubmed: 9620680
doi: 10.1016/S1074-7613(00)80564-6
Berg, R. E., Crossley, E., Murray, S. & Forman, J. Memory CD8
pubmed: 14623912
pmcid: 1592647
doi: 10.1084/jem.20031051
Lertmemongkolchai, G., Cai, G., Hunter, C. A. & Bancroft, G. J. Bystander activation of CD8
pubmed: 11145690
doi: 10.4049/jimmunol.166.2.1097
Olson, J. A., McDonald-Hyman, C., Jameson, S. C. & Hamilton, S. E. Effector-like CD8
pubmed: 23746652
pmcid: 3703254
doi: 10.1016/j.immuni.2013.05.009
Mudd, J. C. et al. Inflammatory function of CX3CR1
pubmed: 27703039
pmcid: 5142088
doi: 10.1093/infdis/jiw463
Nishimura, M. et al. Dual functions of fractalkine/CX3C ligand 1 in trafficking of perforin
pubmed: 12055230
doi: 10.4049/jimmunol.168.12.6173
Böttcher, J. P. et al. Functional classification of memory CD8
pubmed: 26404698
doi: 10.1038/ncomms9306
Gerlach, C. et al. The chemokine receptor CX3CR1 defines three antigen-experienced CD8 T cell subsets with distinct roles in immune surveillance and homeostasis. Immunity 45, 1270–1284 (2016).
pubmed: 27939671
pmcid: 5177508
doi: 10.1016/j.immuni.2016.10.018
Batista, N. V. et al. T cell-intrinsic CX3CR1 marks the most differentiated effector CD4
pubmed: 33172841
doi: 10.4049/immunohorizons.2000059
Weiskopf, D. et al. Dengue virus infection elicits highly polarized CX3CR1
pubmed: 26195744
pmcid: 4534238
doi: 10.1073/pnas.1505956112
Tang, J. et al. Respiratory mucosal immunity against SARS-CoV-2 after mRNA vaccination. Sci. Immunol. 7, eadd4853 (2022).
pubmed: 35857583
doi: 10.1126/sciimmunol.add4853
Kaufmann, E. et al. BCG vaccination provides protection against IAV but not SARS-CoV-2. Cell Rep. 38, 110502 (2022).
pubmed: 35235831
pmcid: 8858710
doi: 10.1016/j.celrep.2022.110502
Divangahi, M., King, I. L. & Pernet, E. Alveolar macrophages and type I IFN in airway homeostasis and immunity. Trends Immunol. 36, 307–314 (2015).
pubmed: 25843635
doi: 10.1016/j.it.2015.03.005
Downey, J. et al. RIPK3 interacts with MAVS to regulate type I IFN-mediated immunity to influenza A virus infection. PLoS Pathog. 13, e1006326 (2017).
pubmed: 28410401
pmcid: 5406035
doi: 10.1371/journal.ppat.1006326
Anacker, R. L. et al. Superiority of intravenously administered BCG and BCG cell walls in protecting rhesus monkeys (Macaca mulatta) against airborne tuberculosis. Z. Immunitatsforsch. Exp. Klin. Immunol. 143, 363–376 (1972).
pubmed: 4282920
Buck, M. D. et al. Mitochondrial dynamics controls T cell fate through metabolic programming. Cell 166, 63–76 (2016).
pubmed: 27293185
pmcid: 4974356
doi: 10.1016/j.cell.2016.05.035
Matza, D. et al. A scaffold protein, AHNAK1, is required for calcium signaling during T cell activation. Immunity 28, 64–74 (2008).
pubmed: 18191595
pmcid: 2350190
doi: 10.1016/j.immuni.2007.11.020
Yu, F. et al. The transcription factor Bhlhe40 is a switch of inflammatory versus antiinflammatory T
pubmed: 29773643
pmcid: 6028509
doi: 10.1084/jem.20170155
Dutta, A. et al. Sterilizing immunity to influenza virus infection requires local antigen-specific T cell response in the lungs. Sci. Rep. 6, 32973 (2016).
pubmed: 27596047
pmcid: 5011745
doi: 10.1038/srep32973
Landsman, L. et al. CX3CR1 is required for monocyte homeostasis and atherogenesis by promoting cell survival. Blood 113, 963–972 (2009).
pubmed: 18971423
doi: 10.1182/blood-2008-07-170787
Hughes, P. M., Botham, M. S., Frentzel, S., Mir, A. & Perry, V. H. Expression of fractalkine (CX3CL1) and its receptor, CX3CR1, during acute and chronic inflammation in the rodent CNS. Glia 37, 314–327 (2002).
pubmed: 11870871
doi: 10.1002/glia.10037
McMichael, A. J., Gotch, F. M., Noble, G. R. & Beare, P. A. Cytotoxic T-cell immunity to influenza. N. Engl. J. Med. 309, 13–17 (1983).
pubmed: 6602294
doi: 10.1056/NEJM198307073090103
Lee, H., Jeong, S. & Shin, E. C. Significance of bystander T cell activation in microbial infection. Nat. Immunol. 23, 13–22 (2022).
pubmed: 34354279
doi: 10.1038/s41590-021-00985-3
Lusty, E. et al. IL-18/IL-15/IL-12 synergy induces elevated and prolonged IFN-γ production by ex vivo expanded NK cells which is not due to enhanced STAT4 activation. Mol. Immunol. 88, 138–147 (2017).
pubmed: 28644973
doi: 10.1016/j.molimm.2017.06.025
Flynn, J. L. et al. An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J. Exp. Med. 178, 2249–2254 (1993).
pubmed: 7504064
doi: 10.1084/jem.178.6.2249
Kamijo, R. et al. Mice that lack the interferon-gamma receptor have profoundly altered responses to infection with Bacillus Calmette–Guérin and subsequent challenge with lipopolysaccharide. J. Exp. Med. 178, 1435–1440 (1993).
pubmed: 8376946
doi: 10.1084/jem.178.4.1435
Misharin, A. V. et al. Monocyte-derived alveolar macrophages drive lung fibrosis and persist in the lung over the life span. J. Exp. Med. 214, 2387–2404 (2017).
pubmed: 28694385
pmcid: 5551573
doi: 10.1084/jem.20162152
Schneider, C. et al. Alveolar macrophages are essential for protection from respiratory failure and associated morbidity following influenza virus infection. PLoS Pathog. 10, e1004053 (2014).
pubmed: 24699679
pmcid: 3974877
doi: 10.1371/journal.ppat.1004053
Liu, Z. et al. Fate mapping via Ms4a3-expression history traces monocyte-derived cells. Cell 178, 1509–1525 (2019).
pubmed: 31491389
doi: 10.1016/j.cell.2019.08.009
Pernet, E. et al. Neonatal imprinting of alveolar macrophages via neutrophil-derived 12-HETE. Nature 614, 530–538 (2023).
pubmed: 36599368
pmcid: 9945843
doi: 10.1038/s41586-022-05660-7
Yao, Y. et al. Induction of autonomous memory alveolar macrophages requires t cell help and is critical to trained immunity. Cell 175, 1634–1650 (2018).
pubmed: 30433869
doi: 10.1016/j.cell.2018.09.042
Kristensen, I., Aaby, P. & Jensen, H. Routine vaccinations and child survival: follow up study in Guinea-Bissau, West Africa. BMJ 321, 1435–1438 (2000).
pubmed: 11110734
pmcid: 27544
doi: 10.1136/bmj.321.7274.1435
Aaby, P. et al. Non-specific effects of standard measles vaccine at 4.5 and 9 months of age on childhood mortality: randomised controlled trial. BMJ 341, c6495 (2010).
pubmed: 21118875
pmcid: 2994348
doi: 10.1136/bmj.c6495
Su, L. F., Kidd, B. A., Han, A., Kotzin, J. J. & Davis, M. M. Virus-specific CD4
pubmed: 23395677
pmcid: 3626102
doi: 10.1016/j.immuni.2012.10.021
Arstila, T. P. et al. A direct estimate of the human alphabeta T cell receptor diversity. Science 286, 958–961 (1999).
pubmed: 10542151
doi: 10.1126/science.286.5441.958
Uthayakumar, D. et al. Non-specific effects of vaccines illustrated through the BCG example: from observations to demonstrations. Front. Immunol. 9, 2869 (2018).
pubmed: 30564249
pmcid: 6288394
doi: 10.3389/fimmu.2018.02869
Jameson, J., Cruz, J. & Ennis, F. A. Human cytotoxic T-lymphocyte repertoire to influenza A viruses. J. Virol. 72, 8682–8689 (1998).
pubmed: 9765409
pmcid: 110281
doi: 10.1128/JVI.72.11.8682-8689.1998
Tabi, Z., Lynch, F., Ceredig, R., Allan, J. E. & Doherty, P. C. Virus-specific memory T cells are Pgp-1
pubmed: 3282677
doi: 10.1016/0008-8749(88)90026-3
Demetriou, M., Granovsky, M., Quaggin, S. & Dennis, J. W. Negative regulation of T-cell activation and autoimmunity by Mgat5 N-glycosylation. Nature 409, 733–739 (2001).
pubmed: 11217864
doi: 10.1038/35055582
Milner, J. J. et al. Heterogenous populations of tissue-resident CD8
pubmed: 32433949
pmcid: 7784612
doi: 10.1016/j.immuni.2020.04.007
Etienne-Manneville, S. & Hall, A. Rho GTPases in cell biology. Nature 420, 629–635 (2002).
pubmed: 12478284
doi: 10.1038/nature01148
Krueger, P. D. et al. Two sequential activation modules control the differentiation of protective T helper-1 (T
pubmed: 33773107
pmcid: 8495663
doi: 10.1016/j.immuni.2021.03.006
Klenerman, P. & Oxenius, A. T cell responses to cytomegalovirus. Nat. Rev. Immunol. 16, 367–377 (2016).
pubmed: 27108521
doi: 10.1038/nri.2016.38
Murray, P. J. et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 41, 14–20 (2014).
pubmed: 25035950
pmcid: 4123412
doi: 10.1016/j.immuni.2014.06.008
Hu, X. & Ivashkiv, L. B. Cross-regulation of signaling pathways by interferon-gamma: implications for immune responses and autoimmune diseases. Immunity 31, 539–550 (2009).
pubmed: 19833085
pmcid: 2774226
doi: 10.1016/j.immuni.2009.09.002
Fong, C. H. et al. Interferon-gamma inhibits influenza A virus cellular attachment by reducing sialic acid cluster size. iScience 25, 104037 (2022).
pubmed: 35330686
pmcid: 8938289
doi: 10.1016/j.isci.2022.104037
Gocher-Demske, A. M. et al. IFNγ-induction of T
pubmed: 36928412
pmcid: 10224582
doi: 10.1038/s41590-023-01453-w
Peters, J. M. et al. Protective intravenous BCG vaccination induces enhanced immune signaling in the airways. Preprint at bioRxiv https://doi.org/10.1101/2023.07.16.549208 (2023).
Jaworska, J. et al. NLRX1 prevents mitochondrial induced apoptosis and enhances macrophage antiviral immunity by interacting with influenza virus PB1-F2 protein. Proc. Natl Acad. Sci. USA 111, 2110–2119 (2014).
doi: 10.1073/pnas.1322118111
Ghoneim, H. E., Thomas, P. G. & McCullers, J. A. Depletion of alveolar macrophages during influenza infection facilitates bacterial superinfections. J. Immunol. 191, 1250–1259 (2013).
pubmed: 23804714
doi: 10.4049/jimmunol.1300014
Benoist, C. & Mathis, D. Autoimmunity provoked by infection: how good is the case for T cell epitope mimicry? Nat. Immunol. 2, 797–801 (2001).
pubmed: 11526389
doi: 10.1038/ni0901-797
Netea, M. G. et al. Innate and adaptive immune memory: an evolutionary continuum in the host’s response to pathogens. Cell Host Microbe https://doi.org/10.1016/j.chom.2018.12.006 (2019).