Immunodiagnosis of tuberculosis: A dynamic view of biomarker discovery

Clinical Microbiology Reviews

Volumn 24, Issue 4, 2011, Pages 792-805

  Kunnath Velayudhan, Shajo ^a   Gennaro, Maria Laura ^a  

^a PUBLIC HEALTH RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA CRYSTALLIN; BIOLOGICAL MARKER; CD40 LIGAND; CULTURE FILTRATE PROTEIN 10; EARLY SECRETORY ANTIGENIC TARGET 6; EPIDERMAL GROWTH FACTOR; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GAMMA INTERFERON RECEPTOR; HLA A ANTIGEN; HLA B ANTIGEN; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN G2; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 17F; INTERLEUKIN 1ALPHA; INTERLEUKIN 2; INTERLEUKIN 21; INTERLEUKIN 22; INTERLEUKIN 4; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; T LYMPHOCYTE ANTIGEN; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN; TRANSFORMING GROWTH FACTOR ALPHA; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

ANTIBODY RESPONSE; ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; B LYMPHOCYTE; BACTERIAL LOAD; BACTERIAL METABOLISM; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; DIAGNOSTIC ACCURACY; DISEASE COURSE; GRANULOMA; HISTOPATHOLOGY; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; INTERFERON GAMMA RELEASE ASSAY; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NOTE; PHENOTYPE; SERODIAGNOSIS; TUBERCULOSIS; TUBERCULOUS GRANULOMA;

ANIMALS; BIOLOGICAL MARKERS; HUMANS; MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSIS;

EID: 80053577116     PISSN: 08938512     EISSN: 10986618     Source Type: Journal    
DOI: 10.1128/CMR.00014-11     Document Type: Note

References (191)

1. Abebe, F., C. Holm-Hansen, H. G. Wiker, and G. Bjune. 2007. Progress in serodiagnosis of Mycobacterium tuberculosis infection. Scand. J. Immunol. 66:176-191.
2. American Thoracic Society. 2000. Diagnostic standards and classification of tuberculosis in adults and children. Am. J. Respir. Crit. Care Med. 161: 1376-1395.
3. American Thoracic Society. 2000. Targeted tuberculin testing and treatment of latent tuberculosis infection. MMWR Recommend. Rep. 49:1-51.
4. Andersen, P., D. Askgaard, L. Ljungqvist, J. Bennedsen, and I. Heron. 1991. Proteins released from Mycobacterium tuberculosis during growth. Infect. Immun. 59:1905-1910.
5. Andersen, P., T. M. Doherty, M. Pai, and K. Weldingh. 2007. The prognosis of latent tuberculosis: can disease be predicted? Trends Mol. Med. 13:175182.
6. Barry, C. E., III, et al. 2009. The spectrum of latent tuberculosis: rethinking the biology and intervention strategies. Nat. Rev. Microbiol. 7:845-855.
7. Barry, S., R. Breen, M. Lipman, M. Johnson, and G. Janossy. 2009. Impaired antigen-specific CD4(+) T lymphocyte responses in cavitary tuberculosis. Tuberculosis (Edinb.) 89:48-53.
8. Beatty, W. L., et al. 2000. Trafficking and release of mycobacterial lipids from infected macrophages. Traffic 1:235-247.
9. Belisle, J. T., et al. 1997. Role of the major antigen of Mycobacterium tuberculosis in cell wall biogenesis. Science 276:1420-1422.
10. Bhatnagar, S., K. Shinagawa, F. J. Castellino, and J. S. Schorey. 2007. Exosomes released from macrophages infected with intracellular pathogens stimulate a proinflammatory response in vitro and in vivo. Blood 110:32343244.
11. Biselli, R., et al. 2010. Detection of interleukin-2 in addition to interferon-gamma discriminates active tuberculosis patients, latently infected individuals, and controls. Clin. Microbiol. Infect. 16:1282-1284.
12. Boom, W. H. 1999. Gammadelta T cells and Mycobacterium tuberculosis. Microbes Infect. 1:187-195.
13. Bothamley, G. H., G. M. Schreuder, R. R. de Vries, and J. Ivanyi. 1993. Association of antibody responses to the 19-kDa antigen of Mycobacterium tuberculosis and the HLA-DQ locus. J. Infect. Dis. 167:992-993.
14. Bothamley, G. H., R. Rudd, F. Festenstein, and J. Ivanyi. 1992. Clinical value of the measurement of Mycobacterium tuberculosis specific antibody in pulmonary tuberculosis. Thorax 47:270-275.
15. Bothamley, G. H., et al. 1989. Association of tuberculosis and M. tuberculosis-specific antibody levels with HLA. J. Infect. Dis. 159:549-555.
16. Caccamo, N., et al. 2010. Multifunctional CD4(+) T cells correlate with active Mycobacterium tuberculosis infection. Eur. J. Immunol. 40:22112220.
17. Capuano, S. V., III, et al. 2003. Experimental Mycobacterium tuberculosis infection of cynomolgus macaques closely resembles the various manifestations of human M. tuberculosis infection. Infect. Immun. 71:5831-5844.
18. Casey, R., et al. 2010. Enumeration of functional T-cell subsets by fluores-cence-immunospot defines signatures of pathogen burden in tuberculosis. PLoS One 5:e15619.
19. Cavalcante, S., et al. 1997. Association between an early humoral response to Mycobacterium tuberculosis antigens and later development of tuberculosis in human immunodeficiency virus-infected individuals. Int. J. Tuberc. Lung Dis. 1:170-174.
20. Chee, C. B., T. M. Barkham, K. W. Khinmar, S. H. Gan, and Y. T. Wang. 2009. Quantitative T-cell interferon-gamma responses to Mycobacterium tuberculosis-specific antigens in active and latent tuberculosis. Eur. J. Clin. Microbiol. Infect. Dis. 28:667-670.
21. Chee, C. B., et al. 2008. Comparison of sensitivities of two commercial gamma interferon release assays for pulmonary tuberculosis. J. Clin. Mi-crobiol. 46:1935-1940.
22. Chegou, N. N., G. F. Black, M. Kidd, P. D. van Helden, and G. Walzl. 2009. Host markers in QuantiFERON supernatants differentiate active TB from latent TB infection: preliminary report. BMC Pulm. Med. 9:21.
23. Chen, J., et al. 2009. Novel recombinant RD2- and RD11-encoded Myco-bacterium tuberculosis antigens are potential candidates for diagnosis of tuberculosis infections in BCG-vaccinated individuals. Microbes Infect. 11: 876-885.
24. Clemens, D. L., B. Y. Lee, and M. A. Horwitz. 2002. The Mycobacterium tuberculosis phagosome in human macrophages is isolated from the host cell cytoplasm. Infect. Immun. 70:5800-5807.
25. Comas, I., et al. 2010. Human T cell epitopes of Mycobacterium tuberculosis are evolutionarily hyperconserved. Nat. Genet. 42:498-503.
26. Comstock, G. W., C. Baum, and D. E. Snider, Jr. 1979. Isoniazid prophylaxis among Alaskan Eskimos: a final report of the bethel isoniazid studies. Am. Rev. Respir. Dis. 119:827-830.
27. Connolly, L. E., P. H. Edelstein, and L. Ramakrishnan. 2007. Why is long-term therapy required to cure tuberculosis? PLoS Med. 4:e120.
28. Cooper, A. M. 2009. Cell-mediated immune responses in tuberculosis. Annu. Rev. Immunol. 27:393-422.
29. Covert, B. A., J. S. Spencer, I. M. Orme, and J. T. Belisle. 2001. The application of proteomics in defining the T cell antigens of Mycobacterium tuberculosis. Proteomics 1:574-586.
30. Cruz, A. T., and J. R. Starke. 2010. Pediatric tuberculosis. Pediatr. Rev. 31:13-26.
31. Cunningham, A. F., and C. L. Spreadbury. 1998. Mycobacterial stationary phase induced by low oxygen tension: cell wall thickening and localization of the 16-kilodalton alpha-crystallin homolog. J. Bacteriol. 180:801-808.
32. Daniel, T. M., M. J. Oxtoby, E. Pinto, and E. Moreno. 1981. The immune spectrum in patients with pulmonary tuberculosis. Am. Rev. Respir. Dis. 123:556-559.
33. Davidow, A., et al. 2005. Antibody profiles characteristic of Mycobacterium tuberculosis infection state. Infect. Immun. 73:6846-6851.
34. Deb, C., et al. 2009. A novel in vitro multiple-stress dormancy model for Mycobacterium tuberculosis generates a lipid-loaded, drug-tolerant, dormant pathogen. PLoS One 4:e6077.
35. del Corral, H., et al. 2009. IFNgamma response to Mycobacterium tuberculosis, risk of infection and disease in household contacts of tuberculosis patients in Colombia. PLoS One 4:e8257.
36. Delves, P., S. Martin, D. Burton, and I. Roitt (ed.). 2006. Roitt's essential immunology. Blackwell Publishing, Malden, MA.
37. Demissie, A., et al. 2006. Recognition of stage-specific mycobacterial antigens differentiates between acute and latent infections with Mycobacterium tuberculosis. Clin. Vaccine Immunol. 13:179-186.
38. Derrick, S. C., I. M. Yabe, A. Yang, and S. L. Morris. 2011. Vaccine-induced anti-tuberculosis protective immunity in mice correlates with the magnitude and quality of multifunctional CD4 T cells. Vaccine 29:29022909.
39. Dheda, K., et al. 2008. Gene expression of IL17 and IL23 in the lungs of patients with active tuberculosis. Thorax 63:566-568.
40. Diel, R., et al. 2011. Interferon-gamma release assays for the diagnosis of latent ycobacterium tuberculosis infection: a systematic review and metaanalysis. Eur. Respir. J. 37:88-99.
41. Diel, R., R. Loddenkemper, S. Niemann, K. Meywald-Walter, and A. Nien-haus. 2011. Negative and positive predictive value of a whole-blood inter-feron-7 release assay for developing active tuberculosis: an update. Am. J. Respir. Crit. Care Med. 183:88-95.
42. Diel, R., R. Loddenkemper, and A. Nienhaus. 2010. Evidence-based comparison of commercial interferon-gamma release assays for detecting active TB: a metaanalysis. Chest 137:952-968.
43. Doherty, M., R. S. Wallis, A. Zumia, and the WHO-Tropical Disease Research/European Commission Joint Expert Consultation Group. 2009. Bio-markers for tuberculosis disease status and diagnosis. Curr. Opin. Pulm. Med. 15:181-187.
44. Dominguez, J., et al. 2009. T-cell responses to the Mycobacterium tuberculosis-specific antigens in active tuberculosis patients at the beginning, during, and after antituberculosis treatment. Diagn. Microbiol. Infect. Dis. 63:43-51.
45. Dominguez, J., et al. 2008. Comparison of two commercially available gamma interferon blood tests for immunodiagnosis of tuberculosis. Clin. Vaccine Immunol. 15:168-171.
46. Dorhoi, A., S. T. Reece, and S. H. Kaufmann. 2011. For better or for worse: the immune response against Mycobacterium tuberculosis balances pathology and protection. Immunol. Rev. 240:235-251.
47. Dye, C., C. J. Watt, D. M. Bleed, S. M. Hosseini, and M. C. Raviglione. 2005. Evolution of tuberculosis control and prospects for reducing tuberculosis incidence, prevalence, and deaths globally. JAMA 293:2767-2775.
48. Ehlers, S. 2009. Lazy, dynamic or minimally recrudescent? On the elusive nature and location of the mycobacterium responsible for latent tuberculosis. Infection 37:87-95.
49. Eichbaum, Q., and E. J. Rubin. 2002. Tuberculosis. Advances in laboratory diagnosis and drug susceptibility testing. Am. J. Clin. Pathol. 118(Suppl.): S3-S17.
50. Fenhalls, G., et al. 2002. Localisation of mycobacterial DNA and mRNA in human tuberculous granulomas. J. Microbiol. Methods 51:197-208.
51. Fenhalls, G., et al. 2002. Distribution of IFN-gamma, IL-4 and TNF-alpha protein and CD8 T cells producing IL-12p40 mRNA in human lung tuberculous granulomas. Immunology 105:325-335.
52. Fenhalls, G., et al. 2002. In situ detection of Mycobacterium tuberculosis transcripts in human lung granulomas reveals differential gene expression in necrotic lesions. Infect. Immun. 70:6330-6338.
53. Flynn, J. L., and J. Chan. 2001. Immunology of tuberculosis. Annu. Rev. Immunol. 19:93-129.
54. Gao, Q., et al. 2005. Gene expression diversity among Mycobacterium tuberculosis clinical isolates. Microbiology 151:5-14.
55. Garton, N. J., et al. 2008. Cytological and transcript analyses reveal fat and lazy persister-like bacilli in tuberculous sputum. PLoS Med. 5:e75.
56. Gennaro, M. L., and T. M. Doherty (ed.). 2010. Immunodiagnosis of Tuberculosis: New questions, New Tools conference, 2008. Proceedings. BMC Proc. 4 (Suppl. 3). http://www.tb-conference.com.
57. Gennaro, M. L., et al. 2007. Antibody markers of incident tuberculosis among HIV-infected adults in the USA: a historical prospective study. Int. J. Tuberc. Lung Dis. 11:624-631.
58. Giri, P. K., and J. S. Schorey. 2008. Exosomes derived from M. Bovis BCG infected macrophages activate antigen-specific CD4+ and CD8+ T cells in vitro and in vivo. PLoS One 3:e2461.
59. Goletti, D., et al. 2010. Response to Rv2628 latency antigen associates with cured tuberculosis and remote infection. Eur. Respir. J. 36:135-142.
60. Goletti, D., et al. 2006. Accuracy of an immune diagnostic assay based on RD1 selected epitopes for active tuberculosis in a clinical setting: a pilot study. Clin. Microbiol. Infect. 12:544-550.
61. Goletti, D., et al. 2010. IFN-gamma, but not IP-10, MCP-2 or IL-2 response to RD1 selected peptides associates to active tuberculosis. J. Infect. 61:133143.
62. Goletti, D., et al. 2010. Is IP-10 an accurate marker for detecting M. tuberculosis-specific response in HIV-infected persons? PLoS One 5:e12577.
63. Goletti, D., et al. 2005. Selected RD1 peptides for active tuberculosis diagnosis: comparison of a gamma interferon whole-blood enzyme-linked im-munosorbent assay and an enzyme-linked immunospot assay. Clin. Diagn. Lab. Immunol. 12:1311-1316.
64. Govender, L., et al. 2010. Higher human CD4 T cell response to novel Mycobacterium tuberculosis latency associated antigens Rv2660 and Rv2659 in latent infection compared with tuberculosis disease. Vaccine 29:51-57.
65. Green, A. M., et al. 2010. CD4(+) regulatory T cells in a cynomolgus macaque model of Mycobacterium tuberculosis infection. J. Infect. Dis. 202:533-541.
66. Grzybowski, S. H. Fishaut, J. Rowe, and A. Brown. 1971. Tuberculosis among patients with various radiologic abnormalities, followed by the chest clinic service. Am. Rev. Respir. Dis. 104:605-608.
67. Hadrup, S. R., et al. 2009. Parallel detection of antigen-specific T-cell responses by multidimensional encoding of MHC multimers. Nat. Methods 6:520-526.
68. Harari, A., et al. 2011. Dominant TNF-alpha(+) Mycobacterium tuberculosis-specific CD4(+) T cell responses discriminate between latent infection and active disease. Nat. Med. 17:372-376.
69. Hasan, Z., et al. 2009. Differential live Mycobacterium tuberculosis-, M. bovis BCG-, recombinant ESAT6-, and culture filtrate protein 10-induced immunity in tuberculosis. Clin. Vaccine Immunol. 16:991-998.
70. Hegazy, A. N., et al. 2010. Interferons direct Th2 cell reprogramming to generate a stable GATA-3(+)T-bet(+) cell subset with combined Th2 and Th1 cell functions. Immunity 32:116-128.
71. Hernandez-Pando, R., et al. 2000. Persistence of DNA from Mycobacterium tuberculosis in superficially normal lung tissue during latent infection. Lancet 356:2133-2138.
72. Higuchi, K., N. Harada, K. Fukazawa, and T. Mori. 2008. Relationship between whole-blood interferon-gamma responses and the risk of active tuberculosis. Tuberculosis (Edinb.) 88:244-248.
73. Hinks, T. S., et al. 2009. Frequencies of region of difference 1 antigen-specific but not purified protein derivative-specific gamma interferon-se-creting T cells correlate with the presence of tuberculosis disease but do not distinguish recent from remote latent infections. Infect. Immun. 77:54865495.
74. Hrabec, E., M. Strek, M. Zieba, S. Kwiatkowska, and Z. Hrabec. 2002. Circulation level of matrix metalloproteinase-9 is correlated with disease severity in tuberculosis patients. Int. J. Tuberc. Lung Dis. 6:713-719.
75. Humphrey, D. M., and M. H. Weiner. 1987. Mycobacterial antigen detection by immunohistochemistry in pulmonary tuberculosis. Hum. Pathol. 18:701-708.
76. Hussain, R., F. Shahid, S. Zafar, M. Dojki, and H. M. Dockrell. 2004. Immune profiling of leprosy and tuberculosis patients to 15-mer peptides of Mycobacterium leprae and M. tuberculosis GroES in a BCG vaccinated area: implications for development of vaccine and diagnostic reagents. Immunology 111:462-471.
77. Hussain, R., N. Talat, F. Shahid, and G. Dawood. 2007. Longitudinal tracking of cytokines after acute exposure to tuberculosis: association of distinct cytokine patterns with protection and disease development. Clin. Vaccine Immunol. 14:1578-1586.
78. Huygen, K., et al. 1993. Influence of genes from the major histocompatibility complex on the antibody repertoire against culture filtrate antigens in mice infected with live Mycobacterium bovis BCG. Infect. Immun. 61:26872693.
79. Jafari, C., et al. 2006. Rapid diagnosis of smear-negative tuberculosis by bronchoalveolar lavage enzyme-linked immunospot. Am. J. Respir. Crit. Care Med. 174:1048-1054.
80. Jafari, C., et al. 2008. Local immunodiagnosis of pulmonary tuberculosis by enzyme-linked immunospot. Eur. Respir. J. 31:261-265.
81. Jafari, C., and C. Lange. 2008. Suttons's law: local immunodiagnosis of tuberculosis. Infection 36:510-514.
82. Janssens, J. P., et al. 2007. Quantitative scoring of an interferon-gamma assay for differentiating active from latent tuberculosis. Eur. Respir. J. 30:722-728.
83. Kanunfre, K. A., O. H. Leite, M. I. Lopes, M. Litvoc, and A. W. Ferreira. 2008. Enhancement of diagnostic efficiency by a gamma interferon release assay for pulmonary tuberculosis. Clin. Vaccine Immunol. 15:1028-1030.
84. Kaplan, G., et al. 2003. Mycobacterium tuberculosis growth at the cavity surface: a microenvironment with failed immunity. Infect. Immun. 71:70997108.
85. Kumar, G., et al. 2008. Diagnostic potential of Ag85C in comparison to various secretory antigens for childhood tuberculosis. Scand. J. Immunol. 68:177-183.
86. Kunnath-Velayudhan, S., et al. 2010. Dynamic antibody responses to the Mycobacterium tuberculosis proteome. Proc. Natl. Acad. Sci. U. S. A. 107:14703-14708.
87. Laal, S., et al. 1997. Surrogate marker of preclinical tuberculosis in human immunodeficiency virus infection: antibodies to an 88-kDa secreted antigen of Mycobacterium tuberculosis. J. Infect. Dis. 176:133-143.
88. Lalvani, A., and M. Pareek. 2010. A 100 year update on diagnosis of tuberculosis infection. Br. Med. Bull. 93:69-84.
89. Lange, C., M. Pai, F. Drobniewski, and G. B. Migliori. 2009. Interferon-gamma release assays for the diagnosis of active tuberculosis: sensible or silly? Eur. Respir. J. 33:1250-1253.
90. Latorre, I., et al. 2009. Quantitative evaluation of T-cell response after specific antigen stimulation in active and latent tuberculosis infection in adults and children. Diagn. Microbiol. Infect. Dis. 65:236-246.
91. Lee, J. Y., et al. 2006. Comparison of two commercial interferon-gamma assays for diagnosing Mycobacterium tuberculosis infection. Eur. Respir. J. 28:24-30.
92. Lenzini, L., P. Rottoli, and L. Rottoli. 1977. The spectrum of human tuberculosis. Clin. Exp. Immunol. 27:230-237.
93. Lewinsohn, D. A., M. L. Gennaro, L. Scholvinck, and D. M. Lewinsohn. 2004. Tuberculosis immunology in children: diagnostic and therapeutic challenges and opportunities. Int. J. Tuberc. Lung Dis. 8:658-674.
94. Leyten, E. M., et al. 2006. Human T-cell responses to 25 novel antigens encoded by genes of the dormancy regulon of Mycobacterium tuberculosis. Microbes Infect. 8:2052-2060.
95. Lienhardt, C., et al. 2010. Evaluationof the prognostic value of IFN-gamma release assay and tuberculin skin test in household contacts of infectious tuberculosis cases in Senegal. PLoS One 5:e10508.
96. Lighter, J., M. Rigaud, M. Huie, C. H. Peng, and H. Pollack. 2009. Chemo-kine IP-10: an adjunct marker for latent tuberculosis infection in children. Int. J. Tuberc. Lung Dis. 13:731-736.
97. Lin, P. L., et al. 2009. Quantitative comparison of active and latent tuberculosis in the cynomolgus macaque model. Infect. Immun. 77:4631-4642.
98. Ling, D. I., L. L. Flores, L. W. Riley, and M. Pai. 2008. Commercial nucleic-acid amplification tests for diagnosis of pulmonary tuberculosis in respiratory specimens: meta-analysis and meta-regression. PLoS One 3:e1536.
99. Ling, D. I., A. A. Zwerling, and M. Pai. 2008. GenoType MTBDR assays for the diagnosis of multidrug-resistant tuberculosis: a meta-analysis. Eur. Re-spir. J. 32:1165-1174.
100. Macedo, G. C., A. Bozzi, H. R. Weinreich, A. Bafica, H. C. Teixeira, and S. C. Oliveira. 2011. HumanT cell and antibody-mediated responses to the Mycobacterium tuberculosis recombinant 85A, 85B, and ESAT-6 antigens. Clin. Dev. Immunol. 2011:351573.
101. Maglione, P. J., and J. Chan. 2009. How B cells shape the immune response against Mycobacterium tuberculosis. Eur. J. Immunol. 39:676-686.
102. Mase, S. R., et al. 2007. Yield of serial sputum specimen examinations in the diagnosis of pulmonary tuberculosis: a systematic review. Int. J. Tuberc. Lung Dis. 11:485-495.
103. Masungi, C., et al. 2002. Differential T and B cell responses against My-cobacterium tuberculosis heparin-binding hemagglutinin adhesin in infected healthy individuals and patients with tuberculosis. J. Infect. Dis. 185:513-520.
104. McDonough, K. A., Y. Kress, and B. R. Bloom. 1993. Pathogenesis of tuberculosis: interaction of Mycobacterium tuberculosis with macrophages. Infect. Immun. 61:2763-2773.
105. Mendez, A., R. Hernandez-Pando, S. Contreras, D. Aguilar, and G. A. Rook. 2011. CCL2, CCL18 and sIL-4R in renal, meningeal and pulmonary TB; a 2 year study of patients and contacts. Tuberculosis (Edinb.) 91:140145.
106. Menzies, D. 2008. Using tests for latent tuberculous infection to diagnose active tuberculosis: can we eat our cake and have it too? Ann. Intern. Med. 148:398-399.
107. Menzies, D., G. Gardiner, M. Farhat, C. Greenaway, and M. Pai. 2008. Thinking in three dimensions: a web-based algorithm to aid the interpretation of tuberculin skin test results. Int. J. Tuberc. Lung Dis. 12:498-505.
108. Menzies, D., M. Pai, and G. Comstock. 2007. Meta-analysis: new tests for the diagnosis of latent tuberculosis infection: areas of uncertainty and recommendations for research. Ann. Intern. Med. 146:340-354.
109. Metcalfe, J. Z., et al. 2010. Evaluation of quantitative IFN-gamma response for risk stratification of active tuberculosis suspects. Am. J. Respir. Crit. Care Med. 181:87-93.
110. Millington, K. A., et al. 2007. Dynamic relationship between IFN-gamma and IL-2 profile of Mycobacterium tuberculosis-specific T cells and antigen load. J. Immunol. 178:5217-5226.
111. Montoya, D., and R. L. Modlin. 2010. Learning from leprosy: insight into the human innate immune response. Adv. Immunol. 105:1-24.
112. Mukamolova, G. V., O. Turapov, J. Malkin, G. Woltmann, and M. R. Barer. 2010. Resuscitation-promoting factors reveal an occult population of tubercle bacilli in sputum. Am. J. Respir. Crit. Care Med. 181:174-180.
113. Musser, J. M., A. Amin, and S. Ramaswamy. 2000. Negligible genetic diversity of mycobacterium tuberculosis host immune system protein targets: evidence of limited selective pressure. Genetics 155:7-16.
114. Nemeth, J., et al. 2009. Recruitment of Mycobacterium tuberculosis specific CD4+ T cells to the site of infection for diagnosis of active tuberculosis. J. Intern. Med. 265:163-168.
115. Newell, E. W., L. O. Klein, W. Yu, and M. M. Davis. 2009. Simultaneous detection of many T-cell specificities using combinatorial tetramer staining. Nat. Methods 6:497-499.
116. Nolan, C. M., and A. M. Elarth. 1988. Tuberculosis in a cohort of Southeast Asian refugees. A five-year surveillance study. Am. Rev. Respir. Dis. 137: 805-809.
117. North, R. J., and Y. J. Jung. 2004. Immunity to tuberculosis. Annu. Rev. Immunol. 22:599-623.
118. Ordway, D. J., et al. 2004. Increased interleukin-4 production by CD8 and gammadelta T cells in health-care workers is associated with the subsequent development of active tuberculosis. J. Infect. Dis. 190:756-766.
119. Ottenhoff, T. H. M., D. A. Lewinsohn, and D. M. Lewinsohn. 2008. Human CD4 and CD8 T cell responses to Mycobacterium tuberculosis: antigen specificity, function, implications and applications, p. 119-155. In S. H. E. Kaufmann and W. J. Britton (ed.), Handbook of tuberculosis: immunology and cell biology. Wiley-VCH Verlag GmbH & co KGaA, Weinheim, Germany.
120. Pai, M. 2010. Spectrum of latent tuberculosis-existing tests cannot resolve the underlying phenotypes. Nat. Rev. Microbiol. 8:242. (Author reply, 8:242.)
121. Pai, M., K. Dheda, J. Cunningham, F. Scano, and R. O'Brien. 2007. T-cell assays for the diagnosis of latent tuberculosis infection: moving the research agenda forward. Lancet Infect. Dis. 7:428-438.
122. Pai, M., L. W. Riley, and J. M. Colford, Jr. 2004. Interferon-gamma assays in the immunodiagnosis of tuberculosis: a systematic review. Lancet Infect. Dis. 4:761-776.
123. Pai, M., A. Zwerling, and D. Menzies. 2008. Systematic review: T-cell-based assays for the diagnosis of latent tuberculosis infection: an update. Ann. Intern. Med. 149:177-184.
124. Pantaleo, G., and A. Harari. 2006. Functional signatures in antiviral T-cell immunity for monitoring virus-associated diseases. Nat. Rev. Immunol. 6:417-423.
125. Parkash, O., B. P. Singh, and M. Pai. 2009. Regions of differences encoded antigens as targets for immunodiagnosis of tuberculosis in humans. Scand. J. Immunol. 70:345-357.
126. Pathan, A. A., et al. 2001. Direct ex vivo analysis of antigen-specific IFN-gamma-secreting CD4 T cells in Mycobacterium tuberculosis-infected individuals: associations with clinical disease state and effect of treatment. J. Immunol. 167:5217-5225.
127. Pheiffer, C., J. C. Betts, H. R. Flynn, P. T. Lukey, and P. van Helden. 2005. Protein expression by a Beijing strain differs from that of another clinical isolate and Mycobacterium tuberculosis H37Rv. Microbiology 151:11391150.
128. Pollock, J. M., and P. Andersen. 1997. The potential of the ESAT-6 antigen secreted by virulent mycobacteria for specific diagnosis of tuberculosis. J. Infect. Dis. 175:1251-1254.
129. Price, N. M., R. H. Gilman, J. Uddin, S. Recavarren, and J. S. Friedland. 2003. Unopposed matrix metalloproteinase-9 expression in human tuberculous granuloma and the role of TNF-alpha-dependent monocyte networks. J. Immunol. 171:5579-5586.
130. Rachman, H., et al. 2006. Unique transcriptome signature of Mycobacte-rium tuberculosis in pulmonary tuberculosis. Infect. Immun. 74:1233-1242.
131. Ravn, P., et al. 1999. Human T cell responses to the ESAT-6 antigen from Mycobacterium tuberculosis. J. Infect. Dis. 179:637-645.
132. Ravn, P., et al. 2005. Prospective evaluation of a whole-blood test using Mycobacterium tuberculosis-specific antigens ESAT-6 and CFP-10 for diagnosis of active tuberculosis. Clin. Diagn. Lab Immunol. 12:491-496.
133. Ribeiro, S., et al. 2009. T-SPOT.TB responses during treatment of pulmonary tuberculosis. BMC Infect. Dis. 9:23.
134. Ridley, D. S. 1974. Histological classification and the immunological spectrum of leprosy. Bull. World Health Organ. 51:451-465.
135. Roberts, D. M., R. P. Liao, G. Wisedchaisri, W. G. Hol, and D. R. Sherman. 2004. Two sensor kinases contribute to the hypoxic response of Mycobacterium tuberculosis. J. Biol. Chem. 279:23082-23087.
136. Roberts, T., N. Beyers, A. Aguirre, and G. Walzl. 2007. Immunosuppression during active tuberculosis is characterized by decreased interferon-gamma production and CD25 expression with elevated forkhead box P3, transforming growth factor-beta, and interleukin-4 mRNA levels. J. Infect. Dis. 195: 870-888.
137. Rogerson, B. J., et al. 2006. Expression levels of Mycobacterium tuberculosis antigen-encoding genes versus production levels of antigen-specific T cells during stationary level lung infection in mice. Immunology 118:195201.
138. Rook, G. A. 2007. Th2 cytokines in susceptibility to tuberculosis. Curr. Mol. Med. 7:327-337.
139. Rueda, C. M., N. D. Marin, L. F. Garcia, and M. Rojas. 2010. Characterization of CD4 and CD8 T cells producing IFN-gamma in human latent and active tuberculosis. Tuberculosis (Edinb.) 90:346-353.
140. Ruhwald, M., M. Bjerregaard-Andersen, P. Rabna, J. Eugen-Olsen, and P. Ravn. 2009. 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. Notes 2:19.
141. Ruhwald, M., et al. 2007. CXCL10/IP-10 release is induced by incubation of whole blood from tuberculosis patients with ESAT-6, CFP10 and TB7.7. Microbes Infect. 9:806-812.
142. Russell, D. G. 2007. Who puts the tubercle in tuberculosis? Nat. Rev. Microbiol. 5:39-47.
143. Russell, D. G., P. J. Cardona, M. J. Kim, S. Allain, and F. Altare. 2009. Foamy macrophages and the progression of the human tuberculosis gran-uloma. Nat. Immunol. 10:943-948.
144. Samanich, K., J. T. Belisle, and S. Laal. 2001. Homogeneity of antibody responses in tuberculosis patients. Infect. Immun. 69:4600-4609.
145. Sargentini, V., et al. 2009. Cytometric detection of antigen-specific IFN-gamma/IL-2 secreting cells in the diagnosis of tuberculosis. BMC Infect. Dis. 9:99.
146. Schaible, U. E., et al. 2003. Apoptosis facilitates antigen presentation to T lymphocytes through MHC-I and CD1 in tuberculosis. Nat. Med. 9:10391046.
147. Schuck, S. D., et al. 2009. Identification of T-cell antigens specific for latent Mycobacterium tuberculosis infection. PLoS One 4:e5590.
148. Schwander, S., and K. Dheda. 2011. Human lung immunity against Myco-bacterium tuberculosis: insights into pathogenesis and protection. Am. J. Respir. Crit. Care Med. 183:696-707.
149. Seder, R. A., P. A. Darrah, and M. Roederer. 2008. T-cell quality in memory and protection: implications for vaccine design. Nat. Rev. Immunol. 8:247258.
150. Sester, M., et al. 2011. Interferon-gamma release assays for the diagnosis of active tuberculosis: a systematic review and meta-analysis. Eur. Respir. J. 37:100-111.
151. Shi, L., Y. J. Jung, S. Tyagi, M. L. Gennaro, and R. J. North. 2003. Expression of Th1-mediated immunity in mouse lungs induces a Mycobac-terium tuberculosis transcription pattern characteristic of nonreplicating persistence. Proc. Natl. Acad. Sci. U. S. A. 100:241-246.
152. Shi, L., R. North, and M. L. Gennaro. 2004. Effect of growth state on transcription levels of genes encoding major secreted antigens of Mycobac-terium tuberculosis in the mouse lung. Infect. Immun. 72:2420-2424.
153. Shi, L., et al. 2005. Changes in energy metabolism of Mycobacterium tuberculosis in mouse lung and under in vitro conditions affecting aerobic respiration. Proc. Natl. Acad. Sci. U. S. A. 102:15629-15634.
154. Silva, V. M., G. Kanaujia, M. L. Gennaro, and D. Menzies. 2003. Factors associated with humoral response to ESAT-6, 38 kDa and 14 kDa in patients with a spectrum of tuberculosis. Int. J. Tuberc. Lung Dis. 7:478484.
155. Simonney, N., et al. 2007. B-cell immune responses in HIV positive and HIV negative patients with tuberculosis evaluated with an ELISA using a glycolipid antigen. Tuberculosis (Edinb.) 87:109-122.
156. Sodhi, A., J. Gong, C. Silva, D. Qian, and P. F. Barnes. 1997. Clinical correlates of interferon gamma production in patients with tuberculosis. Clin. Infect. Dis. 25:617-620.
157. Sonnenberg, M. G., and J. T. Belisle. 1997. Definition of Mycobacterium tuberculosis culture filtrate proteins by two-dimensional polyacrylamide gel electrophoresis, N-terminal amino acid sequencing, and electrospray mass spectrometry. Infect. Immun. 65:4515-4524.
158. Sousa, A. O., et al. 1998. IgG subclass distribution of antibodyresponses to protein and polysaccharide mycobacterial antigens in leprosy and tuberculosis patients. Clin. Exp. Immunol. 111:48-55.
159. Starke, J. R. 2007. New concepts in childhood tuberculosis. Curr. Opin. Pediatr. 19:306-313.
160. Steingart, K. R., et al. 2009. Performance of purified antigens for serodi-agnosis of pulmonary tuberculosis: a meta-analysis. Clin. Vaccine Immunol. 16:260-276.
161. Steingart, K. R., et al. 2007. Commercial serological antibody detection tests for the diagnosis of pulmonary tuberculosis: a systematic review. PLoS Med. 4:e202.
162. Steingart, K. R., et al. 2006. Fluorescence versus conventional sputum smear microscopy for tuberculosis: a systematic review. Lancet Infect. Dis. 6:570-581.
163. Steingart, K. R., et al. 2006. Sputum processing methods to improve the sensitivity of smear microscopy for tuberculosis: a systematic review. Lancet Infect. Dis. 6:664-674.
164. Strassburg, A., C. Jafari, M. Ernst, W. Lotz, and C. Lange. 2008. Rapid diagnosis of pulmonary TB by BAL enzyme-linked immunospot assay in an immunocompromised host. Eur. Respir. J. 31:1132-1135.
165. Sutherland, J. S., I. M. Adetifa, P. C. Hill, R. A. Adegbola, and M. O. Ota. 2009. Pattern and diversity of cytokine production differentiates between Mycobacterium tuberculosis infection and disease. Eur. J. Immunol. 39: 723-729.
166. Sutherland, J. S., B. C. de Jong, D. J. Jeffries, I. M. Adetifa, and M. O. Ota. 2010. Production of TNF-alpha, IL-12(p40) and IL-17 can discriminate between active TB disease and latent infection in a West African cohort. PLoS One 5:e12365.
167. Syed Ahamed Kabeer, B., B. Raman, A. Thomas, V. Perumal, and A. Raja. 2010. Role of QuantiFERON-TB gold, interferon gamma inducible pro-tein-10 and tuberculin skin test in active tuberculosis diagnosis. PLoS One 5:e9051.
168. Teitelbaum, R., et al. 1999. Mycobacterial infection of macrophages results in membrane-permeable phagosomes. Proc. Natl. Acad. Sci. U. S. A. 96: 15190-15195.
169. Teitelbaum, R., et al. 1998. A mAb recognizing a surface antigen of My-cobacterium tuberculosis enhances host survival. Proc. Natl. Acad. Sci. U. S. A. 95:15688-15693.
170. Timm, J., et al. 2003. Differential expression of iron-, carbon-, and oxygen-responsive mycobacterial genes in the lungs of chronically infected mice and tuberculosis patients. Proc. Natl. Acad. Sci. U. S. A. 100:14321-14326.
171. Torrado, E., and A. M. Cooper. 2010. IL-17 and Th17 cells intuberculosis. Cytokine Growth Factor Rev. 21:455-462.
172. Tsao, T. C., et al. 2002. Shifts of T4/T8 T lymphocytes from BAL fluid and peripheral blood by clinical grade in patients with pulmonary tuberculosis. Chest 122:1285-1291.
173. Tully, G., et al. 2005. Highly focused T cell responses in latent human pulmonary Mycobacterium tuberculosis infection. J. Immunol. 174:21742184.
174. Ulrichs, T., and S. H. Kaufmann. 2006. New insights into the function of granulomas in human tuberculosis. J. Pathol. 208:261-269.
175. Ulrichs, T., et al. 2005. Differential organization of the local immune response in patients with active cavitary tuberculosis or with nonprogressive tuberculoma. J. Infect. Dis. 192:89-97.
176. Ulrichs, T., et al. 2004. Human tuberculous granulomas induce peripheral lymphoid follicle-like structures to orchestrate local host defence in the lung. J. Pathol. 204:217-228.
177. van der Wel, N., et al. 2007. M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 129:1287-1298.
178. Voskuil, M. I., et al. 2003. Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J. Exp. Med. 198:705713.
179. Voskuil, M. I., K. C. Visconti, and G. K. Schoolnik. 2004. Mycobacterium tuberculosis gene expression during adaptation to stationary phase and low-oxygen dormancy. Tuberculosis (Edinb.) 84:218-227.
180. Wallis, R. S., et al. 2010. Biomarkers and diagnostics for tuberculosis: progress, needs, and translation into practice. Lancet 375:1920-1937.
181. Walzl, G., K. Ronacher, W. Hanekom, T. J. Scriba, and A. Zumla. 2011. Immunological biomarkers of tuberculosis. Nat. Rev. Immunol. 11:343354.
182. Wang, B. L., et al. 2005. Antibody response to four secretory proteins from Mycobacterium tuberculosis and their complex antigen in TB patients. Int. J. Tuberc. Lung Dis. 9:1327-1334.
183. Wang, J. Y., et al. 2007. Diagnosis of tuberculosis by an enzyme-linked immunospot assay for interferon-gamma. Emerg. Infect. Dis. 13:553-558.
184. Wassie, L., et al. 2008. Ex vivo cytokine mRNA levels correlate with changing clinical status of Ethiopian TB patients and their contacts over time. PLoS One 3:e1522.
185. Wayne, L. G., and C. D. Sohaskey. 2001. Nonreplicating persistence of Mycobacterium tuberculosis. Annu. Rev. Microbiol. 55:139-163.
186. Whittaker, E., A. Gordon, and B. Kampmann. 2008. Is IP-10 a better biomarker for active and latent tuberculosis in children than IFNgamma? PLoS One 3:e3901.
187. Wiker, H. G., and M. Harboe. 1992. The antigen 85 complex: a major secretion product of Mycobacterium tuberculosis. Microbiol. Rev. 56:648-661.
188. Wilkinson, K. A., et al. 2005. Ex vivo characterization of early secretory antigenic target 6-specific T cells at sites of active disease in pleural tuberculosis. Clin. Infect. Dis. 40:184-187.
189. Wolf, A. J., et al. 2008. 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.
190. Yoshiyama, T., N. Harada, K. Higuchi, Y. Sekiya, and K. Uchimura. 2010. Use of the QuantiFERON-TB Gold test for screening tuberculosis contacts and predicting active disease. Int. J. Tuberc. Lung Dis. 14:819827.
191. Young, J. M., I. M. Adetifa, M. O. Ota, and J. S. Sutherland. 2010. Expanded polyfunctional T cell response to mycobacterial antigens in TB disease and contraction post-treatment. PLoS One 5:e11237.