Sequential inflammatory processes define human progression from M. tuberculosis infection to tuberculosis disease

PLoS Pathogens

Volumn 13, Issue 11, 2017, Pages

  Scriba, Thomas J ^a   Penn Nicholson, Adam ^a   Shankar, Smitha ^b   Hraha, Tom ^c   Thompson, Ethan G ^b   Sterling, David ^c   Nemes, Elisa ^a   Darboe, Fatoumatta ^a   Suliman, Sara ^a   Amon, Lynn M ^b   Mahomed, Hassan ^a,d   Erasmus, Mzwandile ^a   Whatney, Wendy ^a   Johnson, John L ^e   Boom, W Henry ^e   Hatherill, Mark ^a   Valvo, Joe ^b   De Groote, Mary Ann ^c   Ochsner, Urs A ^c   Aderem, Alan ^b   Hanekom, Willem A ^a   Zak, Daniel E ^b   more..

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^c SomaLogic Inc   (United States)

^d UNIVERSITY OF STELLENBOSCH   (South Africa)

^e CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BCG VACCINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 17; PROTEOME; STAT1 PROTEIN; VACCINE;

ADOLESCENT; ARTICLE; CD4+ T LYMPHOCYTE; CHILD; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE COURSE; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; INFLAMMATION; KINETICS; LYMPHOPOIESIS; MAJOR CLINICAL STUDY; MALE; MYCOBACTERIUM TUBERCULOSIS; MYELOPOIESIS; PROTEOMICS; REVACCINATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; SCHOOL CHILD; T LYMPHOCYTE ACTIVATION; TH17 CELL; TRANSCRIPTOMICS; TUBERCULOSIS; UPREGULATION; CLINICAL TRIAL; COMPLICATION; DISEASE EXACERBATION; IMMUNOLOGY; MICROBIOLOGY; T LYMPHOCYTE;

ADOLESCENT; CHILD; DISEASE PROGRESSION; HUMANS; INFLAMMATION; MYCOBACTERIUM TUBERCULOSIS; T-LYMPHOCYTES; TUBERCULOSIS; VACCINES;

EID: 85036553506     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1006687     Document Type: Article

References (57)

1. Houben RMGJ, Dodd PJ, The Global Burden of Latent Tuberculosis Infection: A Re-estimation Using Mathematical Modelling. PLoS Med. 2016;13: e1002152. doi: 10.1371/journal.pmed.1002152 27780211
2. Thwaites GE, Nguyen DB, Nguyen HD, Hoang TQ, Do TTO, Nguyen TCT, et al. Dexamethasone for the treatment of tuberculous meningitis in adolescents and adults. N Engl J Med. 2004;351: 1741–1751. doi: 10.1056/NEJMoa040573 15496623
3. Tobin DM, Roca FJ, Oh SF, McFarland R, Vickery TW, Ray JP, et al. Host genotype-specific therapies can optimize the inflammatory response to mycobacterial infections. Cell. 2012;148: 434–446. doi: 10.1016/j.cell.2011.12.023 22304914
4. Barnes PF, Lu S, Abrams JS, Wang E, Yamamura M, Modlin RL, Cytokine production at the site of disease in human tuberculosis. Infection and immunity. 1993;61: 3482–3489. 8335379
5. Wilkinson KA, Wilkinson RJ, Pathan A, Ewer K, Prakash M, Klenerman P, et al. Ex vivo characterization of early secretory antigenic target 6-specific T cells at sites of active disease in pleural tuberculosis. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America. 2005;40: 184–187. doi: 10.1086/426139 15614710
6. Burgess LJ, Reuter H, Carstens ME, Taljaard JJF, Doubell AF, Cytokine production in patients with tuberculous pericarditis. The international journal of tuberculosis and lung disease: the official journal of the International Union against Tuberculosis and Lung Disease. 2002;6: 439–446.
7. Matthews K, Wilkinson KA, Kalsdorf B, Roberts T, Diacon A, Walzl G, et al. Predominance of interleukin-22 over interleukin-17 at the site of disease in human tuberculosis. Tuberculosis (Edinburgh, Scotland). 2011;91: 587–593. doi: 10.1016/j.tube.2011.06.009 21767990
8. Djoba Siawaya JF, Chegou NN, van den Heuvel MM, Diacon AH, Beyers N, van Helden P, et al. Differential cytokine/chemokines and KL-6 profiles in patients with different forms of tuberculosis. Cytokine. 2009;47: 132–136. doi: 10.1016/j.cyto.2009.05.016 19570688
9. Chegou NN, Black GF, Kidd M, van Helden PD, Walzl G, Host markers in QuantiFERON supernatants differentiate active TB from latent TB infection: preliminary report. BMC Pulm Med. 2009;9: 21. doi: 10.1186/1471-2466-9-21 19445695
10. Qiu L, Huang D, Chen CY, Wang R, Shen L, Shen Y, et al. Severe tuberculosis induces unbalanced up-regulation of gene networks and overexpression of IL-22, MIP-1alpha, CCL27, IP-10, CCR4, CCR5, CXCR3, PD1, PDL2, IL-3, IFN-beta, TIM1, and TLR2 but low antigen-specific cellular responses. J Infect Dis. Oxford University Press; 2008;198: 1514–1519. doi: 10.1086/592448 18811584
11. Berry MPR, Graham CM, McNab FW, Xu Z, Bloch SAA, Oni T, et al. An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature. 2010;466: 973–977. doi: 10.1038/nature09247 20725040
12. Maertzdorf J, Weiner J, Mollenkopf H-J, TBornotTB NetworkBauer T, Prasse A, et al. Common patterns and disease-related signatures in tuberculosis and sarcoidosis. Proceedings of the National Academy of Sciences of the United States of America. 2012;109: 7853–7858. doi: 10.1073/pnas.1121072109 22547807
13. Cliff JM, Lee J-S, Constantinou N, Cho J-E, Clark TG, Ronacher K, et al. Distinct phases of blood gene expression pattern through tuberculosis treatment reflect modulation of the humoral immune response. J Infect Dis. 2013;207: 18–29. doi: 10.1093/infdis/jis499 22872737
14. Kaforou M, Wright VJ, Oni T, French N, Anderson ST, Bangani N, Cattamanchi A, et al. Detection of tuberculosis in HIV-infected and -uninfected African adults using whole blood RNA expression signatures: a case-control study. PLoS Med. Public Library of Science; 2013;10: e1001538. doi: 10.1371/journal.pmed.1001538 24167453
15. Zak DE, Penn-Nicholson A, Scriba TJ, Thompson E, Suliman S, Amon LM, et al. A blood RNA signature for tuberculosis disease risk: a prospective cohort study. The Lancet. 2016;387: 2312–2322. doi: 10.1016/S0140-6736(15)01316-1 27017310
16. Barry CE, Boshoff HI, Dartois V, Dick T, Ehrt S, Flynn J, et al. The spectrum of latent tuberculosis: rethinking the biology and intervention strategies. Nat Rev Microbiol. 2009;7: 845–855. doi: 10.1038/nrmicro2236 19855401
17. Suliman S, Geldenhuys H, Johnson JL, Hughes JE, Smit E, Murphy M, et al. Bacillus Calmette-Guérin (BCG) Revaccination of Adults with Latent Mycobacterium tuberculosis Infection Induces Long-Lived BCG-Reactive NK Cell Responses. Journal of Immunology2016;197: 1100–1110. doi: 10.4049/jimmunol.1501996 27412415
18. Obermoser G, Presnell S, Domico K, Xu H, Wang Y, Anguiano E, et al. Systems scale interactive exploration reveals quantitative and qualitative differences in response to influenza and pneumococcal vaccines. Immunity. 2013;38: 831–844. doi: 10.1016/j.immuni.2012.12.008 23601689
19. Li S, Rouphael N, Duraisingham S, Romero-Steiner S, Presnell S, Davis C, et al. Molecular signatures of antibody responses derived from a systems biology study of five human vaccines. Nat Immunol. 2014;15: 195–204. doi: 10.1038/ni.2789 24336226
20. Yang C-S, Shin D-M, Lee H-M, Son JW, Lee SJ, Akira S, et al. ASK1-p38 MAPK-p47phox activation is essential for inflammatory responses during tuberculosis via TLR2-ROS signalling. Cell Microbiol. Blackwell Publishing Ltd; 2008;10: 741–754. doi: 10.1111/j.1462-5822.2007.01081.x 18028450
21. Gold L, Ayers D, Bertino J, Bock C, Bock A, Brody EN, Gelain F, et al. Aptamer-based multiplexed proteomic technology for biomarker discovery. PLoS ONE. 2010;5: e15004. doi: 10.1371/journal.pone.0015004 21165148
22. De Groote MA, Nahid P, Jarlsberg L, Johnson JL, Weiner M, Muzanyi G, et al. Elucidating novel serum biomarkers associated with pulmonary tuberculosis treatment. PLoS ONE. 2013 ed. 2013;8: e61002. doi: 10.1371/journal.pone.0061002 23637781
23. Tobin DM, Vary JC, Ray JP, Walsh GS, Dunstan SJ, Bang ND, et al. The lta4h locus modulates susceptibility to mycobacterial infection in zebrafish and humans. Cell. 2010;140: 717–730. doi: 10.1016/j.cell.2010.02.013 20211140
24. Baldridge MT, King KY, Goodell MA, Inflammatory signals regulate hematopoietic stem cells. Trends Immunol. 2011;32: 57–65. doi: 10.1016/j.it.2010.12.003 21233016
25. O'Garra A, Redford PS, McNab FW, Bloom CI, Wilkinson RJ, Berry MPR, The immune response in tuberculosis. Annu Rev Immunol. 2013;31: 475–527. doi: 10.1146/annurev-immunol-032712-095939 23516984
26. Jasenosky LD, Scriba TJ, Hanekom WA, Goldfeld AE, T cells and adaptive immunity to Mycobacterium tuberculosis in humans. Immunol Rev. 2015;264: 74–87. doi: 10.1111/imr.12274 25703553
27. Teles RMB, Graeber TG, Krutzik SR, Montoya D, Schenk M, Lee DJ, et al. Type I interferon suppresses type II interferon-triggered human anti-mycobacterial responses. Science. 2013;339: 1448–1453. doi: 10.1126/science.1233665 23449998
28. Andrews JR, Nemes E, Tameris M, Landry BS, Mahomed H, McClain JB, et al. Serial QuantiFERON testing and tuberculosis disease risk among young children: an observational cohort study. Lancet Respir Med. 2017;5: 282–290. doi: 10.1016/S2213-2600(17)30060-7 28215501
29. Esmail H, Lai RP, Lesosky M, Wilkinson KA, Graham CM, Coussens AK, et al. Characterization of progressive HIV-associated tuberculosis using 2-deoxy-2-[(18)F]fluoro-D-glucose positron emission and computed tomography. Nature medicine. 2016;22: 1090–1093. doi: 10.1038/nm.4161 27595321
30. Wassermann R, Gulen MF, Sala C, Perin SG, Lou Y, Rybniker J, et al. Mycobacterium tuberculosis Differentially Activates cGAS- and Inflammasome-Dependent Intracellular Immune Responses through ESX-1. Cell Host Microbe. 2015;17: 799–810. doi: 10.1016/j.chom.2015.05.003 26048138
31. Collins AC, Cai H, Li T, Franco LH, Li X-D, Nair VR, et al. Cyclic GMP-AMP Synthase Is an Innate Immune DNA Sensor for Mycobacterium tuberculosis. Cell Host Microbe. 2015;17: 820–828. doi: 10.1016/j.chom.2015.05.005 26048137
32. Watson RO, Bell SL, MacDuff DA, Kimmey JM, Diner EJ, Olivas J, et al. The Cytosolic Sensor cGAS Detects Mycobacterium tuberculosis DNA to Induce Type I Interferons and Activate Autophagy. Cell Host Microbe. 2015;17: 811–819. doi: 10.1016/j.chom.2015.05.004 26048136
33. Wiens KE, Ernst JD, The Mechanism for Type I Interferon Induction by Mycobacterium tuberculosis is Bacterial Strain-Dependent. PLoS pathogens. 2016;12: e1005809. doi: 10.1371/journal.ppat.1005809 27500737
34. Fletcher HA, Snowden MA, Landry B, Rida W, Satti I, Harris SA, et al. T-cell activation is an immune correlate of risk in BCG vaccinated infants. Nat Commun. 2016;7: 11290. doi: 10.1038/ncomms11290 27068708
35. Redford PS, Mayer-Barber KD, McNab FW, Stavropoulos E, Wack A, Sher A, et al. Influenza A virus impairs control of Mycobacterium tuberculosis coinfection through a type I interferon receptor-dependent pathway. J Infect Dis. 2014;209: 270–274. doi: 10.1093/infdis/jit424 23935205
36. Bagheri V, S100A12: Friend or foe in pulmonary tuberculosis?Cytokine. 2017;92: 80–82. doi: 10.1016/j.cyto.2017.01.009 28110121
37. Świerzko AS, Bartłomiejczyk MA, Brzostek A, Łukasiewicz J, Michalski M, Dziadek J, et al. Mycobacterial antigen 85 complex (Ag85) as a target for ficolins and mannose-binding lectin. Int J Med Microbiol. 2016;306: 212–221. doi: 10.1016/j.ijmm.2016.04.004 27141819
38. Volkman HE, Pozos TC, Zheng J, Davis JM, Rawls JF, Ramakrishnan L, Tuberculous granuloma induction via interaction of a bacterial secreted protein with host epithelium. Science. 2010;327: 466–469. doi: 10.1126/science.1179663 20007864
39. Holers VM, Complement and its receptors: new insights into human disease. Annu Rev Immunol. Annual Reviews; 2014;32: 433–459. doi: 10.1146/annurev-immunol-032713-120154 24499275
40. Hirsch CS, Ellner JJ, Russell DG, Rich EA, Complement receptor-mediated uptake and tumor necrosis factor-alpha-mediated growth inhibition of Mycobacterium tuberculosis by human alveolar macrophages. 1994;152: 743–753. 8283049
41. Schlesinger LS, Bellinger-Kawahara CG, Payne NR, Horwitz MA, Phagocytosis of Mycobacterium tuberculosis is mediated by human monocyte complement receptors and complement component C3. 1990;144: 2771–2780. 2108212
42. Carroll MV, Lack N, Sim E, Krarup A, Sim RB, Multiple routes of complement activation by Mycobacterium bovis BCG. Mol Immunol. 2009;46: 3367–3378. doi: 10.1016/j.molimm.2009.07.015 19698993
43. Elkington P, Shiomi T, Breen R, Nuttall RK, Ugarte-Gil CA, Walker NF, et al. MMP-1 drives immunopathology in human tuberculosis and transgenic mice. The Journal of clinical investigation. American Society for Clinical Investigation; 2011;121: 1827–1833. doi: 10.1172/JCI45666 21519144
44. Walker NF, Clark SO, Oni T, Andreu N, Tezera L, Singh S, et al. Doxycycline and HIV infection suppress tuberculosis-induced matrix metalloproteinases. American journal of respiratory and critical care medicine. 2012;185: 989–997. doi: 10.1164/rccm.201110-1769OC 22345579
45. Walzl G, Ronacher K, Hanekom W, Scriba TJ, Zumla A, Immunological biomarkers of tuberculosis. Nat Rev Immunol. 2011 ed. 2011;11: 343–354. doi: 10.1038/nri2960 21475309
46. Gideon HP, Skinner JA, Baldwin N, Flynn JL, Lin PL, Early Whole Blood Transcriptional Signatures Are Associated with Severity of Lung Inflammation in Cynomolgus Macaques with Mycobacterium tuberculosis Infection. Journal of Immunology2016;197: 4817–4828. doi: 10.4049/jimmunol.1601138 27837110
47. Arlehamn CL, Seumois G, Gerasimova A, Huang C, Fu Z, Yue X, et al. Transcriptional profile of tuberculosis antigen-specific T cells reveals novel multifunctional features. 2014;193: 2931–2940. doi: 10.4049/jimmunol.1401151 25092889
48. Yosef N, Shalek AK, Gaublomme JT, Jin H, Lee Y, Awasthi A, et al. Dynamic regulatory network controlling TH17 cell differentiation. Nature. 2013;496: 461–468. doi: 10.1038/nature11981 23467089
49. Ramgolam VS, Sha Y, Jin J, Zhang X, Markovic-Plese S, IFN-beta inhibits human Th17 cell differentiation. Journal of Immunology2009;183: 5418–5427. doi: 10.4049/jimmunol.0803227 19783688
50. Guo B, Chang EY, Cheng G, The type I IFN induction pathway constrains Th17-mediated autoimmune inflammation in mice. The Journal of clinical investigation. 2008;118: 1680–1690. doi: 10.1172/JCI33342 18382764
51. Tilg H, Moschen AR, Kaser A, Suppression of interleukin-17 by type I interferons: a contributing factor in virus-induced immunosuppression?Eur Cytokine Netw. 2009;20: 1–6. doi: 10.1684/ecn.2009.0141 19318313
52. Hatherill M, Geldenhuys H, Pienaar B, Suliman S, Chheng P, Debanne SM, et al. Safety and reactogenicity of BCG revaccination with isoniazid pretreatment in TST positive adults. Vaccine. 2014;32: 3982–3988. doi: 10.1016/j.vaccine.2014.04.084 24814553
53. Wu TD, Nacu S, Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics. 2010;26: 873–881. doi: 10.1093/bioinformatics/btq057 20147302
54. Hoft DF, Blazevic A, Selimovic A, Turan A, Tennant J, Abate G, et al. Safety and Immunogenicity of the Recombinant BCG Vaccine AERAS-422 in Healthy BCG-naïve Adults: A Randomized, Active-controlled, First-in-human Phase 1 Trial. EBioMedicine. 2016;7: 278–286. doi: 10.1016/j.ebiom.2016.04.010 27322481
55. Anders S, Pyl PT, Huber W, HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics. 2015;31: 166–169. doi: 10.1093/bioinformatics/btu638 25260700
56. McCarthy DJ, Chen Y, Smyth GK, Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res. 2012;40: 4288–4297. doi: 10.1093/nar/gks042 22287627
57. Liberzon A, Subramanian A, Pinchback R, Thorvaldsdóttir H, Tamayo P, Mesirov JP, Molecular signatures database (MSigDB) 3.0. Bioinformatics. 2011;27: 1739–1740. doi: 10.1093/bioinformatics/btr260 21546393