Early alveolar macrophage response and IL-1R-dependent T cell priming determine transmissibility of Mycobacterium tuberculosis strains.
Animals
Cell Movement
/ immunology
Dendritic Cells
/ immunology
Female
Lymph Nodes
/ immunology
Lymphocyte Activation
/ immunology
Macrophages, Alveolar
/ immunology
Mice
Mice, Inbred C3H
Mycobacterium tuberculosis
/ immunology
Pulmonary Alveoli
/ cytology
Receptors, Interleukin-1 Type I
/ metabolism
Signal Transduction
/ immunology
Th1 Cells
/ immunology
Th17 Cells
/ immunology
Tuberculosis, Pulmonary
/ immunology
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
16 02 2022
16 02 2022
Historique:
received:
28
06
2021
accepted:
28
01
2022
entrez:
17
2
2022
pubmed:
18
2
2022
medline:
3
3
2022
Statut:
epublish
Résumé
Mechanisms underlying variability in transmission of Mycobacterium tuberculosis strains remain undefined. By characterizing high and low transmission strains of M.tuberculosis in mice, we show here that high transmission M.tuberculosis strain induce rapid IL-1R-dependent alveolar macrophage migration from the alveolar space into the interstitium and that this action is key to subsequent temporal events of early dissemination of bacteria to the lymph nodes, Th1 priming, granulomatous response and bacterial control. In contrast, IL-1R-dependent alveolar macrophage migration and early dissemination of bacteria to lymph nodes is significantly impeded in infection with low transmission M.tuberculosis strain; these events promote the development of Th17 immunity, fostering neutrophilic inflammation and increased bacterial replication. Our results suggest that by inducing granulomas with the potential to develop into cavitary lesions that aids bacterial escape into the airways, high transmission M.tuberculosis strain is poised for greater transmissibility. These findings implicate bacterial heterogeneity as an important modifier of TB disease manifestations and transmission.
Identifiants
pubmed: 35173157
doi: 10.1038/s41467-022-28506-2
pii: 10.1038/s41467-022-28506-2
pmc: PMC8850437
doi:
Substances chimiques
IL1R1 protein, mouse
0
Receptors, Interleukin-1 Type I
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
884Subventions
Organisme : NIAID NIH HHS
ID : T32 AI125185
Pays : United States
Organisme : NIAID NIH HHS
ID : U01 AI065663
Pays : United States
Organisme : NIAID NIH HHS
ID : U19 AI111276
Pays : United States
Informations de copyright
© 2022. The Author(s).
Références
World Health Organisation. Global tuberculosis Report 2020 1–232 (World Health Organisation, 2020).
Riley, R. L., Wells, W. F., Mills, C. C., Nyka, W. & McLean, R. L. Air hygiene in tuberculosis: Quantitative studies of infectivity and control in a pilot ward. Am. Rev. Tuberc. 75, 420–431 (1957).
pubmed: 13403171
Riley, R. L. Aerial dissemination of pulmonary tuberculosis. Am. Rev. Tuberc. 76, 931–941 (1957).
pubmed: 13488004
Riley, R. L. et al. Aerial dissemination of pulmonary tuberculosis. A two-year study of contagion in a tuberculosis ward. 1959. Am. J. Epidemiol. 142, 3–14 (1995).
pubmed: 7785671
doi: 10.1093/oxfordjournals.aje.a117542
Dharmadhikari, A. S. et al. Natural infection of guinea pigs exposed to patients with highly drug-resistant tuberculosis. Tuberculosis 91, 329–338 (2011).
pubmed: 21478054
doi: 10.1016/j.tube.2011.03.002
Acuna-Villaorduna, C. et al. Cough-aerosol cultures of Mycobacterium tuberculosis in the prediction of outcomes after exposure. A household contact study in Brazil. PLoS One 13, e0206384 (2018).
pubmed: 30372480
pmcid: 6205616
doi: 10.1371/journal.pone.0206384
Fennelly, K. P. et al. Cough-generated aerosols of Mycobacterium tuberculosis: A new method to study infectiousness. Am. J. Respir. Crit. Care Med. 169, 604–609 (2004).
pubmed: 14656754
doi: 10.1164/rccm.200308-1101OC
Godfrey-Faussett, P. et al. Tuberculosis control and molecular epidemiology in a South African gold-mining community. Lancet 356, 1066–1071 (2000).
pubmed: 11009142
doi: 10.1016/S0140-6736(00)02730-6
Ypma, R. J., Altes, H. K., van Soolingen, D., Wallinga, J. & van Ballegooijen, W. M. A sign of superspreading in tuberculosis: Highly skewed distribution of genotypic cluster sizes. Epidemiology 24, 395–400 (2013).
pubmed: 23446314
doi: 10.1097/EDE.0b013e3182878e19
Walker, T. M. et al. Whole-genome sequencing to delineate Mycobacterium tuberculosis outbreaks: A retrospective observational study. Lancet Infect. Dis. 13, 137–146 (2013).
pubmed: 23158499
pmcid: 3556524
doi: 10.1016/S1473-3099(12)70277-3
Coscolla, M. & Gagneux, S. Consequences of genomic diversity in Mycobacterium tuberculosis. Semin. Immunol. 26, 431–444 (2014).
pubmed: 25453224
pmcid: 4314449
doi: 10.1016/j.smim.2014.09.012
Nicol, M. P. & Wilkinson, R. J. The clinical consequences of strain diversity in Mycobacterium tuberculosis. Trans. R. Soc. Trop. Med. Hyg. 102, 955–965 (2008).
pubmed: 18513773
doi: 10.1016/j.trstmh.2008.03.025
van Laarhoven, A. et al. Low induction of proinflammatory cytokines parallels evolutionary success of modern strains within the Mycobacterium tuberculosis Beijing genotype. Infect. Immun. 81, 3750–3756 (2013).
pubmed: 23897611
pmcid: 3811744
doi: 10.1128/IAI.00282-13
Sarkar, R., Lenders, L., Wilkinson, K. A., Wilkinson, R. J. & Nicol, M. P. Modern lineages of Mycobacterium tuberculosis exhibit lineage-specific patterns of growth and cytokine induction in human monocyte-derived macrophages. PLoS One 7, e43170 (2012).
pubmed: 22916219
pmcid: 3420893
doi: 10.1371/journal.pone.0043170
Portevin, D., Gagneux, S., Comas, I. & Young, D. Human macrophage responses to clinical isolates from the Mycobacterium tuberculosis complex discriminate between ancient and modern lineages. PLoS Pathog. 7, e1001307 (2011).
pubmed: 21408618
pmcid: 3048359
doi: 10.1371/journal.ppat.1001307
Reiling, N. et al. Clade-specific virulence patterns of Mycobacterium tuberculosis complex strains in human primary macrophages and aerogenically infected mice. MBio 4, e00250–13 (2013).
Reed, M. B. et al. A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. Nature 431, 84–87 (2004).
pubmed: 15343336
doi: 10.1038/nature02837
Lopez, B. et al. A marked difference in pathogenesis and immune response induced by different Mycobacterium tuberculosis genotypes. Clin. Exp. Immunol. 133, 30–37 (2003).
pubmed: 12823275
pmcid: 1808750
doi: 10.1046/j.1365-2249.2003.02171.x
Newton, S. M. et al. A deletion defining a common Asian lineage of Mycobacterium tuberculosis associates with immune subversion. Proc. Natl Acad. Sci. USA 103, 15594–15598 (2006).
pubmed: 17028173
pmcid: 1622867
doi: 10.1073/pnas.0604283103
Valway, S. E. et al. An outbreak involving extensive transmission of a virulent strain of Mycobacterium tuberculosis. N. Engl. J. Med. 338, 633–639 (1998).
pubmed: 9486991
doi: 10.1056/NEJM199803053381001
Ribeiro, S. C. et al. Mycobacterium tuberculosis strains of the modern sublineage of the Beijing family are more likely to display increased virulence than strains of the ancient sublineage. J. Clin. Microbiol. 52, 2615–2624 (2014).
pubmed: 24829250
pmcid: 4097719
doi: 10.1128/JCM.00498-14
Jones-Lopez, E. C. et al. Importance of cough and M. tuberculosis strain type as risks for increased transmission within households. PLoS One 9, e100984 (2014).
pubmed: 24988000
pmcid: 4079704
doi: 10.1371/journal.pone.0100984
Kaplan, G. et al. Mycobacterium tuberculosis growth at the cavity surface: a microenvironment with failed immunity. Infect. Immun. 71, 7099–7108 (2003).
pubmed: 14638800
pmcid: 308931
doi: 10.1128/IAI.71.12.7099-7108.2003
Verma, S. et al. Transmission phenotype of Mycobacterium tuberculosis strains is mechanistically linked to induction of distinct pulmonary pathology. PLoS Pathog. 15, e1007613 (2019).
pubmed: 30840702
pmcid: 6422314
doi: 10.1371/journal.ppat.1007613
Niemann, S. et al. Genomic diversity among drug sensitive and multidrug resistant isolates of Mycobacterium tuberculosis with identical DNA fingerprints. PLoS One 4, e7407 (2009).
pubmed: 19823582
pmcid: 2756628
doi: 10.1371/journal.pone.0007407
Chackerian, A. A., Alt, J. M., Perera, T. V., Dascher, C. C. & Behar, S. M. Dissemination of Mycobacterium tuberculosis is influenced by host factors and precedes the initiation of T-cell immunity. Infect. Immun. 70, 4501–4509 (2002).
pubmed: 12117962
pmcid: 128141
doi: 10.1128/IAI.70.8.4501-4509.2002
Wolf, A. J. et al. Initiation of the adaptive immune response to Mycobacterium tuberculosis depends on antigen production in the local lymph node, not the lungs. J. Exp. Med. 205, 105–115 (2008).
pubmed: 18158321
pmcid: 2234384
doi: 10.1084/jem.20071367
Cohen, S. B. et al. Alveolar macrophages provide an early Mycobacterium tuberculosis niche and initiate dissemination. Cell Host Microbe 24, 439–446 e434 (2018).
pubmed: 30146391
pmcid: 6152889
doi: 10.1016/j.chom.2018.08.001
Lavin, Y. et al. Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell 159, 1312–1326 (2014).
pubmed: 25480296
pmcid: 4437213
doi: 10.1016/j.cell.2014.11.018
Allard, B., Panariti, A. & Martin, J. G. Alveolar macrophages in the resolution of inflammation, tissue repair, and tolerance to infection. Front. Immunol. 9, 1777 (2018).
Snelgrove, R. J. et al. A critical function for CD200 in lung immune homeostasis and the severity of influenza infection. Nat. Immunol. 9, 1074–1083 (2008).
pubmed: 18660812
doi: 10.1038/ni.1637
Huang, L., Nazarova, E. V., Tan, S., Liu, Y. & Russell, D. G. Growth of Mycobacterium tuberculosis in vivo segregates with host macrophage metabolism and ontogeny. J. Exp. Med. 215, 1135–1152 (2018).
pubmed: 29500179
pmcid: 5881470
doi: 10.1084/jem.20172020
Rothchild, A. C. et al. Alveolar macrophages generate a noncanonical NRF2-driven transcriptional response to Mycobacterium tuberculosis in vivo. Sci. Immunol. 4 (2019).
Khader, S. A. et al. Interleukin 12p40 is required for dendritic cell migration and T cell priming after Mycobacterium tuberculosis infection. J. Exp. Med. 203, 1805–1815 (2006).
pubmed: 16818672
pmcid: 2118335
doi: 10.1084/jem.20052545
Wolf, A. J. et al. Mycobacterium tuberculosis infects dendritic cells with high frequency and impairs their function in vivo. J. Immunol. 179, 2509–2519 (2007).
pubmed: 17675513
doi: 10.4049/jimmunol.179.4.2509
Hinchey, J. et al. Enhanced priming of adaptive immunity by a proapoptotic mutant of Mycobacterium tuberculosis. J. Clin. Investig. 117, 2279–2288 (2007).
pubmed: 17671656
pmcid: 1934588
doi: 10.1172/JCI31947
Chen, M. et al. Lipid mediators in innate immunity against tuberculosis: Opposing roles of PGE2 and LXA4 in the induction of macrophage death. J. Exp. Med. 205, 2791–2801 (2008).
pubmed: 18955568
pmcid: 2585850
doi: 10.1084/jem.20080767
Divangahi, M. et al. Mycobacterium tuberculosis evades macrophage defenses by inhibiting plasma membrane repair. Nat. Immunol. 10, 899–906 (2009).
pubmed: 19561612
pmcid: 2730354
doi: 10.1038/ni.1758
Schaible, U. E. et al. Apoptosis facilitates antigen presentation to T lymphocytes through MHC-I and CD1 in tuberculosis. Nat. Med. 9, 1039–1046 (2003).
pubmed: 12872166
doi: 10.1038/nm906
Winau, F., Kaufmann, S. H. & Schaible, U. E. Apoptosis paves the detour path for CD8 T cell activation against intracellular bacteria. Cell Microbiol. 6, 599–607 (2004).
pubmed: 15186397
doi: 10.1111/j.1462-5822.2004.00408.x
Xu, W. et al. Early innate and adaptive immune perturbations determine long-term severity of chronic virus and Mycobacterium tuberculosis coinfection. Immunity 54, 526–541 e527 (2021).
pubmed: 33515487
doi: 10.1016/j.immuni.2021.01.003
Desvignes, L. & Ernst, J. D. Interferon-gamma-responsive nonhematopoietic cells regulate the immune response to Mycobacterium tuberculosis. Immunity 31, 974–985 (2009).
pubmed: 20064452
pmcid: 2807991
doi: 10.1016/j.immuni.2009.10.007
Mishra, B. B. et al. Nitric oxide prevents a pathogen-permissive granulocytic inflammation during tuberculosis. Nat. Microbiol. 2, 17072 (2017).
pubmed: 28504669
pmcid: 5461879
doi: 10.1038/nmicrobiol.2017.72
Mishra, B. B. et al. Nitric oxide controls the immunopathology of tuberculosis by inhibiting NLRP3 inflammasome-dependent processing of IL-1beta. Nat. Immunol. 14, 52–60 (2013).
pubmed: 23160153
doi: 10.1038/ni.2474
Zhang, G. et al. Allele-specific induction of IL-1beta expression by C/EBPbeta and PU.1 contributes to increased tuberculosis susceptibility. PLoS Pathog. 10, e1004426 (2014).
pubmed: 25329476
pmcid: 4199770
doi: 10.1371/journal.ppat.1004426
Winchell, C. G. et al. Evaluation of IL-1 blockade as an adjunct to linezolid therapy for tuberculosis in mice and macaques. Front. Immunol. 11, 891 (2020).
pubmed: 32477361
pmcid: 7235418
doi: 10.3389/fimmu.2020.00891
Juffermans, N. P. et al. Interleukin-1 signaling is essential for host defense during murine pulmonary tuberculosis. J. Infect. Dis. 182, 902–908 (2000).
pubmed: 10950787
doi: 10.1086/315771
Mayer-Barber, K. D. et al. Innate and adaptive interferons suppress IL-1alpha and IL-1beta production by distinct pulmonary myeloid subsets during Mycobacterium tuberculosis infection. Immunity 35, 1023–1034 (2011).
pubmed: 22195750
pmcid: 3246221
doi: 10.1016/j.immuni.2011.12.002
Mayer-Barber, K. D. et al. Caspase-1 independent IL-1beta production is critical for host resistance to mycobacterium tuberculosis and does not require TLR signaling in vivo. J. Immunol. 184, 3326–3330 (2010).
pubmed: 20200276
doi: 10.4049/jimmunol.0904189
Yamada, H., Mizumo, S., Horai, R., Iwakura, Y. & Sugawara, I. Protective role of interleukin-1 in mycobacterial infection in IL-1 alpha/beta double-knockout mice. Lab. Investig. 80, 759–767 (2000).
pubmed: 10830786
doi: 10.1038/labinvest.3780079
Bohrer, A. C., Tocheny, C., Assmann, M., Ganusov, V. V. & Mayer-Barber, K. D. Cutting Edge: IL-1R1 mediates host resistance to Mycobacterium tuberculosis by trans-protection of infected cells. J. Immunol. 201, 1645–1650 (2018).
pubmed: 30068597
doi: 10.4049/jimmunol.1800438
Manca, C. et al. Hypervirulent M. tuberculosis W/Beijing strains upregulate type I IFNs and increase expression of negative regulators of the Jak-Stat pathway. J. Interferon Cytokine Res. 25, 694–701 (2005).
pubmed: 16318583
doi: 10.1089/jir.2005.25.694
Manca, C. et al. Virulence of a Mycobacterium tuberculosis clinical isolate in mice is determined by failure to induce Th1 type immunity and is associated with induction of IFN-alpha /beta. Proc. Natl Acad. Sci. USA 98, 5752–5757 (2001).
pubmed: 11320211
pmcid: 33285
doi: 10.1073/pnas.091096998
Antonelli, L. R. et al. Intranasal Poly-IC treatment exacerbates tuberculosis in mice through the pulmonary recruitment of a pathogen-permissive monocyte/macrophage population. J. Clin. Investig. 120, 1674–1682 (2010).
pubmed: 20389020
pmcid: 2860920
doi: 10.1172/JCI40817
McNab, F. W. et al. TPL-2-ERK1/2 signaling promotes host resistance against intracellular bacterial infection by negative regulation of type I IFN production. J. Immunol. 191, 1732–1743 (2013).
pubmed: 23842752
doi: 10.4049/jimmunol.1300146
Di Paolo, N. C. et al. Interdependence between interleukin-1 and tumor necrosis factor regulates TNF-dependent control of Mycobacterium tuberculosis infection. Immunity 43, 1125–1136 (2015).
pubmed: 26682985
pmcid: 4685953
doi: 10.1016/j.immuni.2015.11.016
Hnizdo, E., Singh, T., & Churchyard, G. Chronic pulmonary function impairment caused by initial and recurrent pulmonary tuberculosis following treatment. Thorax 55, 32–38 (2000).
pubmed: 10607799
pmcid: 1745584
doi: 10.1136/thorax.55.1.32
Plit, M. L. et al. Influence of antimicrobial chemotherapy on spirometric parameters and pro-inflammatory indices in severe pulmonary tuberculosis. Eur. Respir. J. 12, 351–356 (1998).
pubmed: 9727784
doi: 10.1183/09031936.98.12020351
Ross, J., Ehrlich, R. I., Hnizdo, E., White, N. & Churchyard, G. J. Excess lung function decline in gold miners following pulmonary tuberculosis. Thorax 65, 1010–1015 (2010).
pubmed: 20871124
doi: 10.1136/thx.2009.129999
Pasipanodya, J. G. et al. Pulmonary impairment after tuberculosis. Chest 131, 1817–1824 (2007).
pubmed: 17400690
doi: 10.1378/chest.06-2949
Anderson, J. et al. Sublineages of lineage 4 (Euro-American) Mycobacterium tuberculosis differ in genotypic clustering. Int. J. Tuberc. Lung Dis. 17, 885–891 (2013).
pubmed: 23743309
doi: 10.5588/ijtld.12.0960
Mekonnen, D. et al. Genomic diversity and transmission dynamics of M. tuberculosis in Africa: a systematic review and meta-analysis. Int. J. Tuberc. Lung Dis. 23, 1314–1326 (2019).
pubmed: 31931916
doi: 10.5588/ijtld.19.0127
Talarico, S. et al. Association of Mycobacterium tuberculosis PE PGRS33 polymorphism with clinical and epidemiological characteristics. Tuberculosis 87, 338–346 (2007).
pubmed: 17475562
doi: 10.1016/j.tube.2007.03.003
Talarico, S. et al. Variation of the Mycobacterium tuberculosis PE_PGRS 33 gene among clinical isolates. J. Clin. Microbiol. 43, 4954–4960 (2005).
pubmed: 16207947
pmcid: 1248487
doi: 10.1128/JCM.43.10.4954-4960.2005
Wang, J. et al. DNA polymorphism of Mycobacterium tuberculosis PE_PGRS33 gene among clinical isolates of pediatric TB patients and its associations with clinical presentation. Tuberculosis 91, 287–292 (2011).
pubmed: 21664871
doi: 10.1016/j.tube.2011.05.001
McEvoy, C. R. et al. Comparative analysis of Mycobacterium tuberculosis pe and ppe genes reveals high sequence variation and an apparent absence of selective constraints. PLoS One 7, e30593 (2012).
pubmed: 22496726
pmcid: 3319526
doi: 10.1371/journal.pone.0030593
Krishnan, N. et al. Mycobacterium tuberculosis lineage influences innate immune response and virulence and is associated with distinct cell envelope lipid profiles. PLoS One 6, e23870 (2011).
pubmed: 21931620
pmcid: 3169546
doi: 10.1371/journal.pone.0023870
Domenech, P. et al. The role of MmpL8 in sulfatide biogenesis and virulence of Mycobacterium tuberculosis. J. Biol. Chem. 279, 21257–21265 (2004).
pubmed: 15001577
doi: 10.1074/jbc.M400324200
Converse, S. E. et al. MmpL8 is required for sulfolipid-1 biosynthesis and Mycobacterium tuberculosis virulence. Proc. Natl Acad. Sci. USA 100, 6121–6126 (2003).
pubmed: 12724526
pmcid: 156336
doi: 10.1073/pnas.1030024100
Ruhl, C. R. et al. Mycobacterium tuberculosis sulfolipid-1 activates nociceptive neurons and induces cough. Cell 181, 293–305 e211 (2020).
pubmed: 32142653
pmcid: 7102531
doi: 10.1016/j.cell.2020.02.026
Gomez-Gonzalez, P. J. et al. An integrated whole genome analysis of Mycobacterium tuberculosis reveals insights into relationship between its genome, transcriptome, and methylome. Sci. Rep. 9, 5204 (2019).
pubmed: 30914757
pmcid: 6435705
doi: 10.1038/s41598-019-41692-2
Shell, S. S. et al. DNA methylation impacts gene expression and ensures hypoxic survival of Mycobacterium tuberculosis. PLoS Pathog. 9, e1003419 (2013).
pubmed: 23853579
pmcid: 3701705
doi: 10.1371/journal.ppat.1003419
Phelan, J. et al. Methylation in Mycobacterium tuberculosis is lineage specific with associated mutations present globally. Sci. Rep. 8, 160 (2018).
pubmed: 29317751
pmcid: 5760664
doi: 10.1038/s41598-017-18188-y
Coll, F. et al. A robust SNP barcode for typing Mycobacterium tuberculosis complex strains. Nat. Commun. 5, 4812 (2014).
pubmed: 25176035
doi: 10.1038/ncomms5812
Russell, J. N., Clements, J. E. & Gama, L. Quantitation of gene expression in formaldehyde-fixed and fluorescence-activated sorted cells. PLoS One 8, e73849 (2013).
pubmed: 24023909
pmcid: 3759445
doi: 10.1371/journal.pone.0073849
Wang, H., Zhai, T. & Wang, C. NanoStringDiff: Differential Expression Analysis of NanoString nCounter Data. R package version 1.22.0. https://bioconductor.org/packages/NanoStringDiff/ (2021).
Wang, H. et al. NanoStringDiff: A novel statistical method for differential expression analysis based on NanoString nCounter data. Nucleic Acids Res. 44, e151 (2016).
pubmed: 27471031
pmcid: 5175344