The human immune response to tuberculosis and its treatment: A view from the blood

Immunological Reviews

Volumn 264, Issue 1, 2015, Pages 88-102

  Cliff, Jacqueline M ^a   Kaufmann, Stefan H E ^b   Mcshane, Helen ^c   van Helden, Paul ^d   O'Garra, Anne ^e,f  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^b MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF STELLENBOSCH   (South Africa)

^e NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^f IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Immune response; Transcriptional signature; Tuberculosis

Indexed keywords

INTERFERON; TRANSCRIPTOME;

ARTICLE; B LYMPHOCYTE; DIAGNOSTIC PROCEDURE; DIAGNOSTIC TEST ACCURACY STUDY; DOWN REGULATION; GENE OVEREXPRESSION; HUMAN; IMMUNE RESPONSE; PATHOGENESIS; PRIORITY JOURNAL; PROGNOSIS; T LYMPHOCYTE; TRANSCRIPTOMICS; TREATMENT OUTCOME; TUBERCULOSIS; ANIMAL; BLOOD; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; MYCOBACTERIUM TUBERCULOSIS;

ANIMALS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HOST-PATHOGEN INTERACTIONS; HUMANS; MYCOBACTERIUM TUBERCULOSIS; PROGNOSIS; TRANSCRIPTOME; TREATMENT OUTCOME; TUBERCULOSIS;

EID: 84923164028     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/imr.12269     Document Type: Article

References (80)

1. O'Garra A, Redford PS, McNab FW, Bloom CI, Wilkinson RJ, Berry MP. The immune response in tuberculosis. Annu Rev Immunol 2013;31:475-527.
2. Barry CE 3rd, et al. The spectrum of latent tuberculosis: rethinking the biology and intervention strategies. Nat Rev Microbiol 2009;7:845-855.
3. Berry MP, Blankley S, Graham CM, Bloom CI, O'Garra A. Systems approaches to studying the immune response in tuberculosis. Curr Opin Immunol 2013;25:579-587.
4. Berry MP, et al. An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature 2010;466:973-977.
5. Blankley S, Berry MP, Graham CM, Bloom CI, Lipman M, O'Garra A. The application of transcriptional blood signatures to enhance our understanding of the host response to infection: the example of tuberculosis. Philos Trans R Soc Lond B Biol Sci 2014;369:20130427.
6. Joosten SA, Fletcher HA, Ottenhoff TH. A helicopter perspective on TB biomarkers: pathway and process based analysis of gene expression data provides new insight into TB pathogenesis. PLoS ONE 2013;8:e73230.
7. Maertzdorf J, et al. Functional correlations of pathogenesis-driven gene expression signatures in tuberculosis. PLoS ONE 2011;6:e26938.
8. Maertzdorf J, et al. Human gene expression profiles of susceptibility and resistance in tuberculosis. Genes Immun 2011;12:15-22.
9. Maertzdorf J, Kaufmann SH, Weiner J. Toward a unified biosignature for tuberculosis. Cold Spring Harb Perspect Med 2014;pii:a018531. doi: 101101/cshperspecta018531.2014.
10. Ottenhoff TH, et al. Genome-wide expression profiling identifies type 1 interferon response pathways in active tuberculosis. PLoS ONE 2012;7:e45839.
11. Bloom CI, et al. Detectable changes in the blood transcriptome are present after two weeks of antituberculosis therapy. PLoS ONE 2012;7:e46191.
12. Cliff JM, 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.
13. Weiner J 3rd, Kaufmann SH. Recent advances towards tuberculosis control: vaccines and biomarkers. J Intern Med 2014;275:467-480.
14. Ottenhoff TH, Ellner JJ, Kaufmann SH. Ten challenges for TB biomarkers. Tuberculosis 2012;92(Suppl 1):S17-S20.
15. Bullinger L, et al. Use of gene-expression profiling to identify prognostic subclasses in adult acute myeloid leukemia. The New England journal of medicine 2004;350:1605-1616.
16. Valk PJ, et al. Prognostically useful gene-expression profiles in acute myeloid leukemia. The New England journal of medicine 2004;350:1617-1628.
17. Alizadeh AA, et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 2000;403:503-511.
18. Golub TR, et al. Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science 1999;286:531-537.
19. Pascual V, Chaussabel D, Banchereau J. A genomic approach to human autoimmune diseases. Annu Rev Immunol 2010;28:535-571.
20. Mejias A, Suarez NM, Ramilo O. Detecting specific infections in children through host responses: a paradigm shift. Curr Opin Infect Dis 2014;27:228-235.
21. Bloom CI, et al. Transcriptional blood signatures distinguish pulmonary tuberculosis, pulmonary sarcoidosis, pneumonias and lung cancers. PLoS ONE 2013;8:e70630.
22. Koth LL, Solberg OD, Peng JC, Bhakta NR, Nguyen CP, Woodruff PG. Sarcoidosis blood transcriptome reflects lung inflammation and overlaps with tuberculosis. Am J Respir Crit Care Med 2011;184:1153-1163.
23. Maertzdorf J, et al. Common patterns and disease-related signatures in tuberculosis and sarcoidosis. Proc Natl Acad Sci USA 2012;109:7853-7858.
24. Teles RM, et al. Type I interferon suppresses type II interferon-triggered human anti-mycobacterial responses. Science 2013;339:1448-1453.
25. Chaussabel D, et al. A modular analysis framework for blood genomics studies: application to systemic lupus erythematosus. Immunity 2008;29:150-164.
26. Pankla R, et al. Genomic transcriptional profiling identifies a candidate blood biomarker signature for the diagnosis of septicemic melioidosis. Genome Biol 2009;10:R127.
27. Jacobsen M, et al. Candidate biomarkers for discrimination between infection and disease caused by Mycobacterium tuberculosis. J Mol Med 2007;85:613-621.
28. Mistry R, et al. Gene-expression patterns in whole blood identify subjects at risk for recurrent tuberculosis. J Infect Dis 2007;195:357-365.
29. Lesho E, et al. Transcriptional responses of host peripheral blood cells to tuberculosis infection. Tuberculosis 2011;91:390-399.
30. Kaforou M, et al. Detection of tuberculosis in HIV-infected and -uninfected African adults using whole blood RNA expression signatures: a case-control study. PLoS Med 2013;10:e1001538.
31. Naranbhai V, et al. Ratio of monocytes to lymphocytes in peripheral blood identifies adults at risk of incident tuberculosis among HIV-infected adults initiating antiretroviral therapy. J Infect Dis 2014;209:500-509.
32. Jacobsen M, et al. Suppressor of cytokine signaling-3 is affected in T-cells from tuberculosisTB patients. Clin Microbiol Infect 2011;17:1323-1331.
33. Koh GC, et al. Host responses to melioidosis and tuberculosis are both dominated by interferon-mediated signaling. PLoS ONE 2013;8:e54961.
34. Getahun H, Gunneberg C, Granich R, Nunn P. HIV infection-associated tuberculosis: the epidemiology and the response. Clin Infect Dis 2010;50(Suppl 3):S201-S207.
35. Perez-Velez CM, Marais BJ. Tuberculosis in children. The New England journal of medicine 2012;367:348-361.
36. Anderson ST, et al. Diagnosis of childhood tuberculosis and host RNA expression in Africa. The New England journal of medicine 2014;370:1712-1723.
37. Chaussabel D, Baldwin N. Democratizing systems immunology with modular transcriptional repertoire analyses. Nat Rev Immunol 2014;14:271-280.
38. Andrade BB, et al. Biomarkers of inflammation and coagulation are associated with mortality and hepatitis flares in persons coinfected with HIV and hepatitis viruses. J Infect Dis 2013;207:1379-1388.
39. Mahomed H, et al. TB incidence in an adolescent cohort in South Africa. PLoS ONE 2013;8:e59652.
40. Mahomed H, et al. Screening for TB in high school adolescents in a high burden setting in South Africa. Tuberculosis 2013;93:357-362.
41. Walzl G, Ronacher K, Hanekom W, Scriba TJ, Zumla A. Immunological biomarkers of tuberculosis. Nat Rev Immunol 2011;11:343-354.
42. Lin PL, et al. Radiologic responses in cynomolgous macaques for assessing tuberculosis chemotherapy regimens. Antimicrob Agents Chemother 2013;[Epub ahead of print].
43. Jeon CY, Murray MB. Diabetes mellitus increases the risk of active tuberculosis: a systematic review of 13 observational studies. PLoS Med 2008;5:e152.
44. Baker MA, et al. The impact of diabetes on tuberculosis treatment outcomes: a systematic review. BMC Med 2011;9:81.
45. Maertzdorf J, Weiner J 3rd, Kaufmann SH. Enabling biomarkers for tuberculosis control. Int J Tuberc Lung Dis 2012;16:1140-1148.
46. Zelante T, Fallarino F, Bistoni F, Puccetti P, Romani L. Indoleamine 2, 3-dioxygenase in infection: the paradox of an evasive strategy that benefits the host. Microbes Infect 2009;11:133-141.
47. Sandhu G, et al. Discriminating active from latent tuberculosis in patients presenting to community clinics. PLoS ONE 2012;7:e38080.
48. Agranoff D, et al. Identification of diagnostic markers for tuberculosis by proteomic fingerprinting of serum. Lancet 2006;368:1012-1021.
49. De Groote MA, et al. Elucidating novel serum biomarkers associated with pulmonary tuberculosis treatment. PLoS ONE 2013;8:e61002.
50. Anderson P. Post-transcriptional control of cytokine production. Nat Immunol 2008;9:353-359.
51. Weiner J, Maertzdorf J, Kaufmann SH. The dual role of biomarkers for understanding basic principles and devising novel intervention strategies in tuberculosis. Ann N Y Acad Sci 2013;1283:22-29.
52. Weiner J 3rd, et al. Biomarkers of inflammation, immunosuppression and stress with active disease are revealed by metabolomic profiling of tuberculosis patients. PLoS ONE 2012;7:e40221.
53. Suzuki Y, et al. Serum indoleamine 2, 3-dioxygenase activity predicts prognosis of pulmonary tuberculosis. Clin Vaccine Immunol 2012;19:436-442.
54. Simon R, Radmacher MD, Dobbin K, McShane LM. Pitfalls in the use of DNA microarray data for diagnostic and prognostic classification. J Natl Cancer Inst 2003;95:14-18.
55. Dorhoi A, et al. MicroRNA-223 controls susceptibility to tuberculosis by regulating lung neutrophil recruitment. J Clin Investig 2013;123:4836-4848.
56. Iannaccone M, Dorhoi A, Kaufmann SH. Host-directed therapy of tuberculosis: what is in it for microRNA? Expert Opin Ther Targets 2014;18:491-494.
57. Esterhuyse MM, Kaufmann SH. Diagnostic biomarkers are hidden in the infected host's epigenome. Expert Rev Mol Diagn 2013;13:625-637.
58. Benn CS, Netea MG, Selin LK, Aaby P. A small jab - a big effect: nonspecific immunomodulation by vaccines. Trends Immunol 2013;34:431-439.
59. Kleinnijenhuis J, et al. Bacille Calmette-Guerin induces NOD2-dependent nonspecific protection from reinfection via epigenetic reprogramming of monocytes. Proc Natl Acad Sci USA 2012;109:17537-17542.
60. Saeed S, et al. Epigenetic programming of monocyte-to-macrophage differentiation and trained innate immunity. Science 2014;345:1251086.
61. Kagina BM, et al. Specific T cell frequency and cytokine expression profile do not correlate with protection against tuberculosis after bacillus Calmette-Guerin vaccination of newborns. Am J Respir Crit Care Med 2010;182:1073-1079.
62. Joosten SA, et al. Identification of biomarkers for tuberculosis disease using a novel dual-color RT-MLPA assay. Genes Immun 2012;13:71-82.
63. 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 2001;98:5752-5757.
64. 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 2005;25:694-701.
65. Ordway D, et al. The hypervirulent Mycobacterium tuberculosis strain HN878 induces a potent TH1 response followed by rapid down-regulation. Journal of immunology 2007;179:522-531.
66. Stanley SA, Johndrow JE, Manzanillo P, Cox JS. The Type I IFN response to infection with Mycobacterium tuberculosis requires ESX-1-mediated secretion and contributes to pathogenesis. Journal of immunology 2007;178:3143-3152.
67. Cooper AM, Pearl JE, Brooks JV, Ehlers S, Orme IM. Expression of the nitric oxide synthase 2 gene is not essential for early control of Mycobacterium tuberculosis in the murine lung. Infect Immun 2000;68:6879-6882.
68. Dorhoi A, et al. Type I IFN signaling triggers immunopathology in tuberculosis-susceptible mice by modulating lung phagocyte dynamics. Eur J Immunol 2014;44:2380-2393.
69. Antonelli LR, et al. Intranasal Poly-IC treatment exacerbates tuberculosis in mice through the pulmonary recruitment of a pathogen-permissive monocyte/macrophage population. J Clin Investig 2010;120:1674-1682.
70. Mayer-Barber KD, et al. Innate and adaptive interferons suppress IL-1alpha and IL-1beta production by distinct pulmonary myeloid subsets during Mycobacterium tuberculosis infection. Immunity 2011;35:1023-1034.
71. Redford PS, 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.
72. McNab FW, et al. TPL-2-ERK1/2 signaling promotes host resistance against intracellular bacterial infection by negative regulation of type I IFN production. Journal of immunology 2013;191:1732-1743.
73. McNab FW, et al. Type I IFN induces IL-10 production in an IL-27-independent manner and blocks responsiveness to IFN-gamma for production of IL-12 and bacterial killing in Mycobacterium tuberculosis-infected macrophages. Journal of immunology 2014;193:3600-3612.
74. Redford PS, Murray PJ, O'Garra A. The role of IL-10 in immune regulation during M. tuberculosis infection. Mucosal Immunol 2011;4:261-270.
75. Knaul JK, et al. Lung-residing myeloid-derived suppressors display dual functionality in murine pulmonary tuberculosis. Am J Respir Crit Care Med 2014;190:1053-1066.
76. Mayer-Barber KD, et al. Host-directed therapy of tuberculosis based on interleukin-1 and type I interferon crosstalk. Nature 2014;511:99-103.
77. Desvignes L, Wolf AJ, Ernst JD. Dynamic roles of type I and type II IFNs in early infection with Mycobacterium tuberculosis. Journal of immunology 2012;188:6205-6215.
78. Bogunovic D, et al. Mycobacterial disease and impaired IFN-gamma immunity in humans with inherited ISG15 deficiency. Science 2012;337:1684-1688.
79. Dorhoi A, Iannaccone M, Maertzdorf J, Nouailles G, Weiner J 3rd, Kaufmann SH. Reverse translation in tuberculosis: neutrophils provide clues for understanding development of active disease. Front Immunol 2014;5:36.
80. O'Garra A. Systems approach to understand the immune response in tuberculosis: an iterative process between mouse models and human disease. Cold Spring Harb Symp Quant Biol 2013;78:173-177.