Frequencies of region of difference 1 antigen-specific but not purified protein derivative-specific gamma interferon-secreting T cells correlate with the presence of tuberculosis disease but do not distinguish recent from remote latent infections

Infection and Immunity

Volumn 77, Issue 12, 2009, Pages 5486-5495

  Hinks, Timothy S C ^a,b   Dosanjh, Davinder P S ^b   Innes, John A ^c   Pasvol, Geoffrey ^d   Hackforth, Sarah ^c   Varia, Hansa ^d   Millington, Kerry A ^b   Liu, Xiao Qing ^e   Bakir, Mustafa ^f   Soysal, Ahmet ^f   Davidson, Robert N ^d   Gunatheesan, Rubamalar ^b   Lalvani, Ajit ^b  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^c BIRMINGHAM HEARTLANDS HOSPITAL   (United Kingdom)

^d NORTHWICK PARK HOSPITAL   (United Kingdom)

^e PEKING UNION MEDICAL COLLEGE HOSPITAL   (China)

^f MARMARA UNIVERSITY SCHOOL OF MEDICINE   (Turkey)

Author keywords

[No Author keywords available]

Indexed keywords

CULTURE FILTRATE PROTEIN 10; EARLY SECRETORY ANTIGENIC TARGET 6; GAMMA INTERFERON; PEPTIDE; TUBERCULIN;

ADOLESCENT; ADULT; ANTIGEN SPECIFICITY; ARTICLE; BACILLUS; CHILD; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE ACTIVITY; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; HUMAN; IMMUNE RESPONSE; LATENT PERIOD; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; SCHOOL CHILD; T LYMPHOCYTE; TUBERCULIN TEST; TUBERCULOSIS;

ADOLESCENT; ADULT; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CHILD; FEMALE; HUMANS; IMMUNOENZYME TECHNIQUES; INTERFERON-GAMMA; MALE; MIDDLE AGED; MYCOBACTERIUM TUBERCULOSIS; T-LYMPHOCYTES; TUBERCULOSIS; YOUNG ADULT;

EID: 72449205452     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01436-08     Document Type: Article

References (42)

1. Andersen, P., A. B. Andersen, A. L. Sorensen, and S. Nagai. 1995. Recall of long-lived immunity to Mycobacterium tuberculosis infection in mice. J. Immunol. 154:3359-3372.
2. Andersen, P., and I. Heron. 1993. Specificity of a protective memory immune response against Mycobacterium tuberculosis. Infect. Immun. 61:844-851.
3. Arend, S. M., A. Geluk, K. E. van Meijgaarden, J. T. van Dissel, M. Theisen, P. Andersen, and T. H. Ottenhoff. 2000. Antigenic equivalence of human T-cell responses to Mycobacterium tuberculosis-specific RD1-encoded protein antigens ESAT-6 and culture filtrate protein 10 and to mixtures of synthetic peptides. Infect. Immun. 68:3314-3321.
4. Badell, E., F. Nicolle, S. Clark, L. Majlessi, F. Boudou, A. Martino, L. Castello-Branco, C. Leclerc, D. J. Lewis, P. D. Marsh, B. Gicquel, and N. Winter. 2009. Protection against tuberculosis induced by oral prime with Mycobacterium bovis BCG and intranasal subunit boost based on the vaccine candidate Ag85B-ESAT-6 does not correlate with circulating IFNgamma producing T-cells. Vaccine 27:28-37.
5. Berthet, F. X., P. B. Rasmussen, I. Rosenkrands, P. Andersen, and B. Gicquel. 1998. A Mycobacterium tuberculosis operon encoding ESAT-6 and a novel low-molecular-mass culture filtrate protein (CFP-10). Microbiology 144:3195-3203.
6. Boussiotis, V. A., E. Y. Tsai, E. J. Yunis, S. Thim, J. C. Delgado, C. C. Dascher, A. Berezovskaya, D. Rousset, J. M. Reynes, and A. E. Goldfeld. 2000. IL-10-producing T cells suppress immune responses in anergic tuberculosis patients. J. Clin. Investig. 105:1317-1325.
7. Brock, I., K. Weldingh, E. M. Leyten, S. M. Arend, P. Ravn, and P. Andersen. 2004. Specific T-cell epitopes for immunoassay-based diagnosis of Mycobacterium tuberculosis infection. J. Clin. Microbiol. 42:2379-2387.
8. Brodin, P., L. Majlessi, R. Brosch, D. Smith, G. Bancroft, S. Clark, A. Williams, C. Leclerc, and S. T. Cole. 2004. Enhanced protection against tuberculosis by vaccination with recombinant Mycobacterium microti vaccine that induces T cell immunity against region of difference 1 antigens. J. Infect. Dis. 190:115-122.
9. Brodin, P., L. Majlessi, L. Marsollier, M. I. de Jonge, D. Bottai, C. Demangel, J. Hinds, O. Neyrolles, P. D. Butcher, C. Leclerc, S. T. Cole, and R. Brosch. 2006. Dissection of ESAT-6 system 1 of Mycobacterium tuberculosis and impact on immunogenicity and virulence. Infect. Immun. 74:88-98.
10. Cockle, P. J., S. V. Gordon, A. Lalvani, B. M. Buddle, R. G. Hewinson, and H. M. Vordermeier. 2002. Identification of novel Mycobacterium tuberculosis antigens with potential as diagnostic reagents or subunit vaccine candidates by comparative genomics. Infect. Immun. 70:6996-7003.
11. Cooper, A. M., D. K. Dalton, T. A. Stewart, J. P. Griffin, D. G. Russell, and I. M. Orme. 1993. Disseminated tuberculosis in interferon gamma gene-disrupted mice. J. Exp. Med. 178:2243-2247.
12. Demissie, A., E. M. Leyten, M. Abebe, L. Wassie, A. Aseffa, G. Abate, H. Fletcher, P. Owiafe, P. C. Hill, R. Brookes, G. Rook, A. Zumla, S. M. Arend, M. Klein, T. H. Ottenhoff, P. Andersen, and T. M. Doherty. 2006. Recognition of stage-specific mycobacterial antigens differentiates between acute and latent infections with Mycobacterium tuberculosis. Clin. Vaccine Immunol. 13:179-186.
13. Dosanjh, D. P., T. S. Hinks, J. A. Innes, J. J. Deeks, G. Pasvol, S. Hackforth, H. Varia, K. A. Millington, R. Gunatheesan, V. Guyot-Revol, and A. Lalvani. 2008. Improved diagnostic evaluation of suspected tuberculosis. Ann. Intern. Med. 148:325-336.
14. Ewer, K., J. Deeks, L. Alvarez, G. Bryant, S. Waller, P. Andersen, P. Monk, and A. Lalvani. 2003. Comparison of T-cell-based assay with tuberculin skin test for diagnosis of Mycobacterium tuberculosis infection in a school tuberculosis outbreak. Lancet 361:1168-1173. (Pubitemid 36398385)
15. Fine, P. E., J. Bruce, J. M. Ponnighaus, P. Nkhosa, A. Harawa, and E. Vynnycky. 1999. Tuberculin sensitivity: conversions and reversions in a rural African population. Int. J. Tuberc. Lung Dis. 3:962-975.
16. Flynn, J. L., and J. Chan. 2001. Immunology of tuberculosis. Annu. Rev. Immunol. 19:93-129.
17. Flynn, J. L., J. Chan, K. J. Triebold, D. K. Dalton, T. A. Stewart, and B. R. Bloom. 1993. An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J. Exp. Med. 178:2249-2254.
18. Goletti, D., S. Carrara, H. Mayanja-Kizza, J. Baseke, M. A. Mugerwa, E. Girardi, and Z. Toossi. 2008. Response to M. tuberculosis selected RD1 peptides in Ugandan HIV-infected patients with smear positive pulmonary tuberculosis: a pilot study. BMC Infect. Dis. 8:11.
19. Guyot-Revol, V., J. A. Innes, S. Hackforth, T. Hinks, and A. Lalvani. 2006. Regulatory T cells are expanded in blood and disease sites in tuberculosis patients. Am. J. Respir. Crit. Care Med. 173:803-810.
20. Health Protection Agency Centre for Infections. 2008. Annual report on tuberculosis surveillance in the UK 2008. Health Protection Agency Centre for Infections, London, United Kingdom.
21. Janssens, J. P., P. Roux-Lombard, T. Perneger, M. Metzger, R. Vivien, and T. Rochat. 2007. Quantitative scoring of an interferon-gamma assay for differentiating active from latent tuberculosis. Eur. Respir. J. 30:722-728.
22. Jo, E. K., J. K. Park, and H. M. Dockrell. 2003. Dynamics of cytokine generation in patients with active pulmonary tuberculosis. Curr. Opin. Infect. Dis. 16:205-210.
23. Joint Tuberculosis Committee of the British Thoracic Society. 2000. Control and prevention of tuberculosis in the United Kingdom: code of practice 2000. Thorax 55:887-901.
24. Kamath, A. T., M. P. Valenti, A. F. Rochat, E. M. Agger, K. Lingnau, A. von Gabain, P. Andersen, P. H. Lambert, and C. A. Siegrist. 2008. Protective anti-mycobacterial T cell responses through exquisite in vivo activation of vaccine-targeted dendritic cells. Eur. J. Immunol. 38:1247-1256.
25. Leyten, E. M., M. Y. Lin, K. L. Franken, A. H. Friggen, C. Prins, K. E. van Meijgaarden, M. I. Voskuil, K. Weldingh, P. Andersen, G. K. Schoolnik, S. M. Arend, T. H. Ottenhoff, and M. R. Klein. 2006. Human T-cell responses to 25 novel antigens encoded by genes of the dormancy regulon of Mycobacterium tuberculosis. Microbes Infect. 8:2052-2060.
26. Liu, X. Q., D. Dosanjh, H. Varia, K. Ewer, P. Cockle, G. Pasvol, and A. Lalvani. 2004. Evaluation of T-cell responses to novel RD1- and RD2- encoded Mycobacterium tuberculosis gene products for specific detection of human tuberculosis infection. Infect. Immun. 72:2574-2581.
27. Majlessi, L., P. Brodin, R. Brosch, M. J. Rojas, H. Khun, M. Huerre, S. T. Cole, and C. Leclerc. 2005. Influence of ESAT-6 secretion system 1 (RD1) of Mycobacterium tuberculosis on the interaction between mycobacteria and the host immune system. J. Immunol. 174:3570-3579. (Pubitemid 40354066)
28. Reference deleted.
29. Millington, K. A., J. A. Innes, S. Hackforth, T. S. Hinks, J. J. Deeks, D. P. Dosanjh, V. Guyot-Revol, R. Gunatheesan, P. Klenerman, and A. Lalvani. 2007. Dynamic relationship between IFN-gamma and IL-2 profile of Mycobacterium tuberculosis-specific T cells and antigen load. J. Immunol. 178: 5217-5226.
30. Olsen, A. W., P. R. Hansen, A. Holm, and P. Andersen. 2000. Efficient protection against Mycobacterium tuberculosis by vaccination with a single subdominant epitope from the ESAT-6 antigen. Eur. J. Immunol. 30:1724-1732.
31. Pathan, A. A., K. A. Wilkinson, P. Klenerman, H. McShane, R. N. Davidson, G. Pasvol, A. V. Hill, and A. Lalvani. 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.
32. Pym, A. S., P. Brodin, L. Majlessi, R. Brosch, C. Demangel, A. Williams, K. E. Griffiths, G. Marchal, C. Leclerc, and S. T. Cole. 2003. Recombinant BCG exporting ESAT-6 confers enhanced protection against tuberculosis. Nat. Med. 9:533-539.
33. Renshaw, P. S., P. Panagiotidou, A. Whelan, S. V. Gordon, R. G. Hewinson, R. A. Williamson, and M. D. Carr. 2002. Conclusive evidence that the major T-cell antigens of the Mycobacterium tuberculosis complex ESAT-6 and CFP-10 form a tight, 1:1 complex and characterization of the structural properties of ESAT-6, CFP-10, and the ESAT-6*CFP-10 complex. Implications for pathogenesis and virulence. J. Biol. Chem. 277:21598-21603.
34. Richeldi, L., K. Ewer, M. Losi, B. M. Bergamini, P. Roversi, J. Deeks, L. M. Fabbri, and A. Lalvani. 2004. T cell-based tracking of multidrug resistant tuberculosis infection after brief exposure. Am. J. Respir. Crit. Care Med. 170:288-295.
35. Schnappinger, D., S. Ehrt, M. I. Voskuil, Y. Liu, J. A. Mangan, I. M. Monahan, G. Dolganov, B. Efron, P. D. Butcher, C. Nathan, and G. K. Schoolnik. 2003. Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J. Exp. Med. 198:693-704.
36. Sepkowitz, K. A. 1996. Tuberculin skin testing and the health care worker: lessons of the Prophit Survey. Tuber. Lung Dis. 77:81-85.
37. + T cells in the context of multiple HLA alleles. J. Immunol. 173:1966-1977.
38. Soysal, A., K. A. Millington, M. Bakir, D. Dosanjh, Y. Aslan, J. J. Deeks, S. Efe, I. Staveley, K. Ewer, and A. Lalvani. 2005. Effect of BCG vaccination on risk of Mycobacterium tuberculosis infection in children with household tuberculosis contact: a prospective community-based study. Lancet 366:1443-1451. (Pubitemid 41483810)
39. Vordermeier, H. M., M. A. Chambers, P. J. Cockle, A. O. Whelan, J. Simmons, and R. G. Hewinson. 2002. Correlation of ESAT-6-specific gamma interferon production with pathology in cattle following Mycobacterium bovis BCG vaccination against experimental bovine tuberculosis. Infect. Immun. 70:3026-3032.
40. Wilkinson, K. A., G. R. Stewart, S. M. Newton, H. M. Vordermeier, J. R. Wain, H. N. Murphy, K. Horner, D. B. Young, and R. J. Wilkinson. 2005. Infection biology of a novel alpha-crystallin of Mycobacterium tuberculosis: Acr2. J. Immunol. 174:4237-4243.
41. Wilkinson, R. J., K. A. Wilkinson, K. A. De Smet, K. Haslov, G. Pasvol, M. Singh, I. Svarcova, and J. Ivanyi. 1998. Human T- and B-cell reactivity to the 16kDa alpha-crystallin protein of Mycobacterium tuberculosis. Scand. J. Immunol. 48:403-409.
42. Wu, B., C. Huang, M. Kato-Maeda, P. C. Hopewell, C. L. Daley, A. M. Krensky, and C. Clayberger. 2007. Messenger RNA expression of IL-8, FOXP3, and IL12beta differentiates latent tuberculosis infection from disease. J. Immunol. 178:3688-3694. (Pubitemid 46417636)