Immunological biomarkers of tuberculosis (original) (raw)
World Health Organisation. Multidrug and extensively drug-resistant TB (M/XDR-TB): 2010 global report on surveillance and response. WHO[online], (2010).
Corbett, E. L. et al. The growing burden of tuberculosis: global trends and interactions with the HIV epidemic. Arch. Intern. Med.163, 1009–1021 (2003). ArticlePubMed Google Scholar
Abu-Raddad, L. J. et al. Epidemiological benefits of more-effective tuberculosis vaccines, drugs, and diagnostics. Proc. Natl Acad. Sci. USA106, 13980–13985 (2009). ArticlePubMedPubMed Central Google Scholar
Davies, P. D. & Pai, M. The diagnosis and misdiagnosis of tuberculosis. Int. J. Tuberc. Lung Dis.12, 1226–1234 (2008). CASPubMed Google Scholar
Boehme, C. C. et al. Rapid molecular detection of tuberculosis and rifampin resistance. N. Engl. J. Med.363, 1005–1015 (2010). This paper describes the biggest breakthrough in tuberculosis diagnostics in decades: a directex vivo M. tuberculosisgene amplification test for the diagnosis and detection of rifampicin resistance. ArticleCASPubMedPubMed Central Google Scholar
Black, G. F. et al. BCG-induced increase in interferon-γ response to mycobacterial antigens and efficacy of BCG vaccination in Malawi and the UK: two randomised controlled studies. Lancet359, 1393–1401 (2002). ArticlePubMed Google Scholar
Barry, C. E. et al. The spectrum of latent tuberculosis: rethinking the biology and intervention strategies. Nature Rev. Microbiol.7, 845–855 (2009). ArticleCAS Google Scholar
Sudre, P., ten Dam, G. & Kochi, A. Tuberculosis: a global overview of the situation today. Bull. World Health Organ.70, 149–159 (1992). CASPubMedPubMed Central Google Scholar
Ottenhoff, T. H., Verreck, F. A., Hoeve, M. A. & van deVosse, E. Control of human host immunity to mycobacteria. Tuberculosis85, 53–64 (2005). ArticleCASPubMed Google Scholar
Lawn, S. D., Myer, L., Edwards, D., Bekker, L. G. & Wood, R. Short-term and long-term risk of tuberculosis associated with CD4 cell recovery during antiretroviral therapy in South Africa. AIDS23, 1717–1725 (2009). ArticlePubMed Google Scholar
Khader, S. A. et al. IL-23 and IL-17 in the establishment of protective pulmonary CD4+ T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nature Immunol.8, 369–377 (2007). ArticleCAS Google Scholar
Vordermeier, H. M. et al. Viral booster vaccines improve Mycobacterium bovis BCG-induced protection against bovine tuberculosis. Infect. Immun.77, 3364–3373 (2009). ArticleCASPubMedPubMed Central Google Scholar
Green, A. M. et al. CD4+ regulatory T cells in a cynomolgus macaque model of Mycobacterium tuberculosis infection. J. Infect. Dis.202, 533–541 (2010). ArticleCASPubMed Google Scholar
Lazar-Molnar, E. et al. Programmed death-1 (PD-1)-deficient mice are extraordinarily sensitive to tuberculosis. Proc. Natl Acad. Sci. USA107, 13402–13407 (2010). ArticlePubMedPubMed Central Google Scholar
Bruns, H. et al. Anti-TNF immunotherapy reduces CD8+ T cell-mediated antimicrobial activity against Mycobacterium tuberculosis in humans. J. Clin. Invest.119, 1167–1177 (2009). ArticleCASPubMedPubMed Central Google Scholar
Stenger, S. et al. An antimicrobial activity of cytolytic T cells mediated by granulysin. Science282, 121–125 (1998). ArticleCASPubMed Google Scholar
Gallegos, A. M., Pamer, E. G. & Glickman, M. S. Delayed protection by ESAT-6-specific effector CD4+ T cells after airborne M. tuberculosis infection. J. Exp. Med.205, 2359–2368 (2008). ArticleCASPubMedPubMed Central Google Scholar
Gonzalez-Juarrero, M. et al. Temporal and spatial arrangement of lymphocytes within lung granulomas induced by aerosol infection with Mycobacterium tuberculosis. Infect. Immun.69, 1722–1728 (2001). ArticleCASPubMedPubMed Central Google Scholar
Qin, L., Gilbert, P. B., Corey, L., McElrath, M. J. & Self, S. G. A framework for assessing immunological correlates of protection in vaccine trials. J. Infect. Dis.196, 1304–1312 (2007). ArticlePubMed Google Scholar
Comstock, G. W. Field trials of tuberculosis vaccines: how could we have done them better? Control. Clin. Trials15, 247–276 (1994). ArticleCASPubMed Google Scholar
Kagina, B. M. 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.182, 1073–1079 (2010). This study shows that polyfunctional T cells and cytokine expression do not correlate with BCG-induced protection against tuberculosis. ArticleCASPubMedPubMed Central Google Scholar
Darrah, P. A. et al. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nature Med.13, 843–850 (2007). ArticleCASPubMed Google Scholar
Giri, P. K., Verma, I. & Khuller, G. K. Enhanced immunoprotective potential of Mycobacterium tuberculosis Ag85 complex protein based vaccine against airway Mycobacterium tuberculosis challenge following intranasal administration. FEMS Immunol. Med. Microbiol.47, 233–241 (2006). ArticleCASPubMed Google Scholar
Agger, E. M. et al. Protective immunity to tuberculosis with Ag85B-ESAT-6 in a synthetic cationic adjuvant system IC31. Vaccine24, 5452–5460 (2006). ArticleCASPubMed Google Scholar
Bennekov, T. et al. Alteration of epitope recognition pattern in Ag85B and ESAT-6 has a profound influence on vaccine-induced protection against Mycobacterium tuberculosis. Eur. J. Immunol.36, 3346–3355 (2006). ArticleCASPubMed Google Scholar
Hoft, D. F. et al. Investigation of the relationships between immune-mediated inhibition of mycobacterial growth and other potential surrogate markers of protective Mycobacterium tuberculosis immunity. J. Infect. Dis.186, 1448–1457 (2002). ArticleCASPubMed Google Scholar
Cheon, S. H. et al. Bactericidal activity in whole blood as a potential surrogate marker of immunity after vaccination against tuberculosis. Clin. Diagn. Lab. Immunol.9, 901–907 (2002). PubMedPubMed Central Google Scholar
Spencer, C. T., Abate, G., Blazevic, A. & Hoft, D. F. Only a subset of phosphoantigen-responsive γ9δ2 T cells mediate protective tuberculosis immunity. J. Immunol.181, 4471–4484 (2008). ArticleCASPubMed Google Scholar
Wallis, R. S. et al. Biomarkers and diagnostics for tuberculosis: progress, needs, and translation into practice. Lancet375, 1920–1937 (2010). This is a comprehensive review of diagnostic and other biomarkers for tuberculosis. ArticleCASPubMed Google Scholar
Lalvani, A. et al. Enhanced contact tracing and spatial tracking of Mycobacterium tuberculosis infection by enumeration of antigen-specific T cells. Lancet357, 2017–2021 (2001). ArticleCASPubMed Google Scholar
Mori, T. et al. Specific detection of tuberculosis infection: an interferon-γ-based assay using new antigens. Am. J. Respir. Crit. Care Med.170, 59–64 (2004). ArticlePubMed Google Scholar
Ferrara, G. et al. Exploring the immune response against Mycobacterium tuberculosis for a better diagnosis of the infection. Arch. Immunol. Ther. Exp.57, 425–433 (2009). Article Google Scholar
Pai, M., Zwerling, A. & Menzies, D. Systematic review: T-cell-based assays for the diagnosis of latent tuberculosis infection: an update. Ann. Intern. Med.149, 177–184 (2008). ArticlePubMedPubMed Central Google Scholar
Mazurek, G. H. et al. Prospective comparison of the tuberculin skin test and 2 whole-blood interferon-γ release assays in persons with suspected tuberculosis. Clin. Infect. Dis.45, 837–845 (2007). ArticleCASPubMed Google Scholar
Janssens, J. P. Interferon-γ release assay tests to rule out active tuberculosis. Eur. Respir. J.30, 183–184 (2007). ArticlePubMed Google Scholar
Losi, M. et al. Use of a T-cell interferon-γ release assay for the diagnosis of tuberculous pleurisy. Eur. Respir. J.30, 1173–1179 (2007). ArticleCASPubMed Google Scholar
Thomas, M. M. et al. Rapid diagnosis of Mycobacterium tuberculosis meningitis by enumeration of cerebrospinal fluid antigen-specific T-cells. Int. J. Tuberc. Lung Dis.12, 651–657 (2008). CASPubMed Google Scholar
Chegou, N. N., Black, G. F., Kidd, M., van Helden, P. D. & Walzl, G. Host markers in QuantiFERON supernatants differentiate active TB from latent TB infection: preliminary report. BMC Pulm. Med.9, 21 (2009). ArticleCASPubMedPubMed Central Google Scholar
Wu, B. et al. Messenger RNA expression of IL-8, FOXP3, and IL-12β differentiates latent tuberculosis infection from disease. J. Immunol.178, 3688–3694 (2007). ArticleCASPubMed Google Scholar
Djoba Siawaya, J. F. et al. Differential cytokine/chemokines and KL-6 profiles in patients with different forms of tuberculosis. Cytokine47, 132–136 (2009). ArticleCASPubMed Google Scholar
Caccamo, N. et al. Multifunctional CD4+ T cells correlate with active Mycobacterium tuberculosis infection. Eur. J. Immunol.40, 2211–2220 (2010). ArticleCASPubMed Google Scholar
Casey, R. et al. Enumeration of functional T-cell subsets by fluorescence-immunospot defines signatures of pathogen burden in tuberculosis. PLoS ONE5, e15619 (2010). ArticleCASPubMedPubMed Central Google Scholar
Harari, A. et al. Dominant TNF-α+_Mycobacterium tuberculosis_-specific CD4+ T cell responses discriminate between latent infection and active disease. Nature Med.17, 372–376 (2011). ArticleCASPubMed Google Scholar
Steingart, K. R. et al. A systematic review of commercial serological antibody detection tests for the diagnosis of extrapulmonary tuberculosis. Thorax62, 911–918 (2007). PubMedPubMed Central Google Scholar
Steingart, K. R. et al. Performance of purified antigens for serodiagnosis of pulmonary tuberculosis: a meta-analysis. Clin. Vaccine Immunol.16, 260–276 (2009). ArticleCASPubMed Google Scholar
Kunnath-Velayudhan, S. et al. Dynamic antibody responses to the Mycobacterium tuberculosis proteome. Proc. Natl Acad. Sci. USA107, 14703–14708 (2010). ArticlePubMedPubMed Central Google Scholar
Hesseling, A. C. et al. Baseline sputum time to detection predicts month two culture conversion and relapse in non-HIV-infected patients. Int. J. Tuberc. Lung Dis.14, 560–570 (2010). CASPubMed Google Scholar
Johnson, J. L. et al. Shortening treatment in adults with noncavitary tuberculosis and 2-month culture conversion. Am. J. Respir. Crit. Care Med.180, 558–563 (2009). ArticlePubMedPubMed Central Google Scholar
Chee, C. B. et al. Tuberculosis treatment effect on T-cell interferon-γ responses to _Mycobacterium tuberculosis_-specific antigens. Eur. Respir. J.36, 355–361 (2010). ArticleCASPubMed Google Scholar
Sai Priya, V. H., Latha, G. S., Hasnain, S. E., Murthy, K. J. & Valluri, V. L. Enhanced T cell responsiveness to Mycobacterium bovis BCG r32-kDa Ag correlates with successful anti-tuberculosis treatment in humans. Cytokine52, 190–193 (2010). ArticleCASPubMed Google Scholar
Wassie, L. et al. Ex vivo cytokine mRNA levels correlate with changing clinical status of Ethiopian TB patients and their contacts over time. PLoS ONE3, e1522 (2008). ArticleCASPubMedPubMed Central Google Scholar
Millington, K. A. et al. Dynamic relationship between IFN-γ and IL-2 profile of _Mycobacterium tuberculosis_-specific T cells and antigen load. J. Immunol.178, 5217–5226 (2007). ArticleCASPubMed Google Scholar
Millington, K. A., Gooding, S., Hinks, T. S., Reynolds, D. J. & Lalvani, A. _Mycobacterium tuberculosis_-specific cellular immune profiles suggest bacillary persistence decades after spontaneous cure in untreated tuberculosis. J. Infect. Dis.202, 1685–1689 (2010). This paper demonstrates that in some individuals TEMcells persist more than 50 years after spontaneous clinical cure of tuberculosis, suggesting the persistence of antigen. In some cured patients, however, only TCMcells are present, and this is consistent with sterilizing cure. ArticleCASPubMed Google Scholar
Bahk, Y. Y. et al. Antigens secreted from Mycobacterium tuberculosis: identification by proteomics approach and test for diagnostic marker. Proteomics4, 3299–3307 (2004). ArticleCASPubMed Google Scholar
Berry, M. P. et al. An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature466, 973–977 (2010). This work illustrates a role for neutrophil-driven type I IFN signalling inM. tuberculosispathogenesis and the importance of cell-specific transcriptome analysis. ArticleCASPubMedPubMed Central Google Scholar
Jacobsen, M. et al. Candidate biomarkers for discrimination between infection and disease caused by Mycobacterium tuberculosis. J. Mol. Med.85, 613–621 (2007). ArticleCASPubMed Google Scholar
Mistry, R. et al. Gene-expression patterns in whole blood identify subjects at risk for recurrent tuberculosis. J. Infect. Dis.195, 357–365 (2007). ArticleCASPubMed Google Scholar
Maertzdorf, J. et al. Human gene expression profiles of susceptibility and resistance in tuberculosis. Genes Immun.12, 15–22 (2011). ArticleCASPubMed Google Scholar
Repsilber, D. et al. Biomarker discovery in heterogeneous tissue samples – taking the in-silico deconfounding approach. BMC Bioinformatics11, 27 (2010). ArticleCASPubMedPubMed Central Google Scholar
Sartain, M. J., Slayden, R. A., Singh, K. K., Laal, S. & Belisle, J. T. Disease state differentiation and identification of tuberculosis biomarkers via native antigen array profiling. Mol. Cell. Proteomics5, 2102–2113 (2006). ArticleCASPubMed Google Scholar
O'Connell, R. M., Rao, D. S., Chaudhuri, A. A. & Baltimore, D. Physiological and pathological roles for microRNAs in the immune system. Nature Rev. Immunol.10, 111–122 (2010). ArticleCAS Google Scholar
Liu, Q. et al. Serum protein profiling of smear-positive and smear-negative pulmonary tuberculosis using SELDI-TOF mass spectrometry. Lung188, 15–23 (2010). ArticleCASPubMed Google Scholar
Agranoff, D. et al. Identification of diagnostic markers for tuberculosis by proteomic fingerprinting of serum. Lancet368, 1012–1021 (2006). ArticleCASPubMedPubMed Central Google Scholar
de Carvalho, L. P. et al. Activity-based metabolomic profiling of enzymatic function: identification of Rv1248c as a mycobacterial 2-hydroxy-3-oxoadipate synthase. Chem. Biol.17, 323–332 (2010). ArticleCASPubMedPubMed Central Google Scholar
Koulman, A., Lane, G. A., Harrison, S. J. & Volmer, D. A. From differentiating metabolites to biomarkers. Anal. Bioanal. Chem.394, 663–670 (2009). ArticleCASPubMedPubMed Central Google Scholar
World Health Organisation. Treatment of tuberculosis: guidelines 4th edn. WHO[online], (2010).
Diel, R., Loddenkemper, R., Meywald-Walter, K., Niemann, S. & Nienhaus, A. Predictive value of a whole blood IFN-γ assay for the development of active tuberculosis disease after recent infection with Mycobacterium tuberculosis. Am. J. Respir. Crit. Care Med.177, 1164–1170 (2008). ArticlePubMed Google Scholar
Doherty, T. M. et al. Immune responses to the _Mycobacterium tuberculosis_-specific antigen ESAT-6 signal subclinical infection among contacts of tuberculosis patients. J. Clin. Microbiol.40, 704–706 (2002). ArticleCASPubMedPubMed Central Google Scholar
Mattos, A. M. et al. Increased IgG1, IFN-γ, TNF-α and IL-6 responses to Mycobacterium tuberculosis antigens in patients with tuberculosis are lower after chemotherapy. Int. Immunol.22, 775–782 (2010). ArticleCASPubMed Google Scholar
Veenstra, H. et al. Changes in the kinetics of intracellular IFN-γ production in TB patients during treatment. Clin. Immunol.124, 336–344 (2007). ArticleCASPubMed Google Scholar
Goletti, D. et al. Is IP-10 an accurate marker for detecting _M. tuberculosis_-specific response in HIV-infected persons? PLoS ONE5, e12577 (2010). ArticleCASPubMedPubMed Central Google Scholar
Ruhwald, M. et al. Evaluating the potential of IP-10 and MCP-2 as biomarkers for the diagnosis of tuberculosis. Eur. Respir. J.32, 1607–1615 (2008). ArticleCASPubMed Google Scholar
Ruhwald, M., Bjerregaard-Andersen, M., Rabna, P., Eugen-Olsen, J. & Ravn, P. IP-10, MCP-1, MCP-2, MCP-3, and IL-1RA hold promise as biomarkers for infection with M. tuberculosis in a whole blood based T-cell assay. BMC Res. Notes2, 19 (2009). ArticleCASPubMedPubMed Central Google Scholar
Smith, S. G. et al. Mycobacterium tuberculosis PPD-induced immune biomarkers measurable in vitro following BCG vaccination of UK adolescents by multiplex bead array and intracellular cytokine staining. BMC Immunol.11, 35 (2010). ArticleCASPubMedPubMed Central Google Scholar
Demissie, A. et al. Healthy individuals that control a latent infection with Mycobacterium tuberculosis express high levels of Th1 cytokines and the IL-4 antagonist IL-4δ2. J. Immunol.172, 6938–6943 (2004). ArticleCASPubMed Google Scholar
Ordway, D. J. et al. Increased Interleukin-4 production by CD8 and γδ T cells in health-care workers is associated with the subsequent development of active tuberculosis. J. Infect. Dis.190, 756–766 (2004). ArticleCASPubMed Google Scholar
Lee, J. H. & Chang, J. H. Changes of plasma interleukin-1 receptor antagonist, interleukin-8 and other serologic markers during chemotherapy in patients with active pulmonary tuberculosis. Korean J. Intern. Med.18, 138–145 (2003). ArticleCASPubMedPubMed Central Google Scholar
Sutherland, J. S., de Jong, B. C., Jeffries, D. J., Adetifa, I. M. & Ota, M. O. Production of TNF-α, IL-12(p40) and IL-17 can discriminate between active TB disease and latent infection in a West African cohort. PLoS ONE5, e12365 (2010). ArticleCASPubMedPubMed Central Google Scholar
Djoba Siawaya, J. F. et al. Differential expression of interleukin-4 (IL-4) and IL-4δ2 mRNA, but not transforming growth factor beta (TGF-β), TGF-βRII, Foxp3, gamma interferon, T-bet, or GATA-3 mRNA, in patients with fast and slow responses to antituberculosis treatment. Clin. Vaccine Immunol.15, 1165–1170 (2008). ArticleCASPubMedPubMed Central Google Scholar
Djoba Siawaya, J. F. et al. Immune parameters as markers of tuberculosis extent of disease and early prediction of anti-tuberculosis chemotherapy response. J. Infect.56, 340–347 (2008). ArticlePubMed Google Scholar
Eugen-Olsen, J. et al. The serum level of soluble urokinase receptor is elevated in tuberculosis patients and predicts mortality during treatment: a community study from Guinea-Bissau. Int. J. Tuberc. Lung Dis.6, 686–692 (2002). CASPubMed Google Scholar
Demir, T., Yalcinoz, C., Keskinel, I., Demiroz, F. & Yildirim, N. sICAM-1 as a serum marker in the diagnosis and follow-up of treatment of pulmonary tuberculosis. Int. J. Tuberc. Lung Dis.6, 155–159 (2002). CASPubMed Google Scholar
Mukae, H. et al. Elevated levels of circulating adhesion molecules in patients with active pulmonary tuberculosis. Respirology8, 326–331 (2003). ArticlePubMed Google Scholar
Chan, C. H., Lai, C. K., Leung, J. C., Ho, A. S. & Lai, K. N. Elevated interleukin-2 receptor level in patients with active pulmonary tuberculosis and the changes following anti-tuberculosis chemotherapy. Eur. Respir. J.8, 70–73 (1995). ArticleCASPubMed Google Scholar
Tsao, T. C. et al. Imbalances between tumor necrosis factor-α and its soluble receptor forms, and interleukin-1β and interleukin-1 receptor antagonist in BAL fluid of cavitary pulmonary tuberculosis. Chest117, 103–109 (2000). ArticleCASPubMed Google Scholar
Djoba Siawaya, J. F., Ruhwald, M., Eugen-Olsen, J. & Walzl, G. Correlates for disease progression and prognosis during concurrent HIV/TB infection. Int. J. Infect. Dis.11, 289–299 (2007). ArticleCASPubMed Google Scholar
Rosas-Taraco, A. G. et al. Expression of CDllc in blood monocytes as biomarker for favorable response to antituberculosis treatment. Arch. Med. Res.40, 128–131 (2009). ArticleCASPubMed Google Scholar
Wolday, D. et al. Expression of chemokine receptors CCR5 and CXCR4 on CD4+ T cells and plasma chemokine levels during treatment of active tuberculosis in HIV-1-coinfected patients. J. Acquir. Immune Defic. Syndr.39, 265–271 (2005). ArticleCASPubMed Google Scholar
Hosp, M. et al. Neopterin, β2-microglobulin, and acute phase proteins in HIV-1-seropositive and -seronegative Zambian patients with tuberculosis. Lung175, 265–275 (1997). ArticleCASPubMed Google Scholar
Schleicher, G. K. et al. Procalcitonin and C-reactive protein levels in HIV-positive subjects with tuberculosis and pneumonia. Eur. Respir. J.25, 688–692 (2005). ArticleCASPubMed Google Scholar
Krenke, R. & Korczynski, P. Use of pleural fluid levels of adenosine deaminase and interferon γ in the diagnosis of tuberculous pleuritis. Curr. Opin. Pulm. Med.16, 367–375 (2010). ArticleCASPubMed Google Scholar
Abel, B. et al. The novel tuberculosis vaccine, AERAS-402, induces robust and polyfunctional CD4+ and CD8+ T cells in adults. Am. J. Respir. Crit. Care Med.181, 1407–1417 (2010). ArticleCASPubMedPubMed Central Google Scholar
Hohn, H. et al. MHC class II tetramer guided detection of _Mycobacterium tuberculosis_-specific CD4+ T cells in peripheral blood from patients with pulmonary tuberculosis. Scand. J. Immunol.65, 467–478 (2007). ArticleCASPubMed Google Scholar
Axelsson-Robertson, R. et al. Extensive major histocompatibility complex class I binding promiscuity for Mycobacterium tuberculosis TB10.4 peptides and immune dominance of human leucocyte antigen (HLA)-B*0702 and HLA-B*0801 alleles in TB10.4 CD8 T-cell responses. Immunology129, 496–505 (2010). ArticleCASPubMedPubMed Central Google Scholar
Veenstra, H. et al. Changes in leucocyte and lymphocyte subsets during tuberculosis treatment; prominence of CD3dimCD56+ natural killer T cells in fast treatment responders. Clin. Exp. Immunol.145, 252–260 (2006). ArticleCASPubMedPubMed Central Google Scholar
Azzurri, A. et al. Serological markers of pulmonary tuberculosis and of response to anti-tuberculosis treatment in a patient population in Guinea. Int. J. Immunopathol. Pharmacol.19, 199–208 (2006). ArticleCASPubMed Google Scholar
Esquivel-Valerio, J. A. et al. Antineutrophil cytoplasm autoantibodies in patients with tuberculosis are directed against bactericidal/permeability increasing protein and are detected after treatment initiation. Clin. Exp. Rheumatol.28, 35–39 (2010). PubMed Google Scholar
Jacobsen, M. et al. Suppressor of cytokine signaling (SOCS)-3 is affected in T cells from TB patients. Clin. Microbiol. Infect. 29 Jul 2010 (doi:10.1111/j.1469-0691.2010.03326.x).