Immunogenicity of 60 novel latency-related antigens of Mycobacterium tuberculosis

Frontiers in Microbiology

Volumn 5, Issue SEP, 2014, Pages

  Serra Vidal, M ^a,b,c   Latorre, I ^a,b,c   Franken, K ^f   Diaz J ^a,b,c   de Souza Galvao M ^b,d   Casas, I ^a,b   Maldonado, J ^e   Mila C ^d   Solsona, J ^d   Jimenez Fuentes, M A ^d   Altet, N ^d   Lacoma, A ^a,b,c   Ruiz Manzano, J ^a,b,c   Ausina, V ^a,b,c   Prat, C ^a,b,c   Ottenhoff, T H M ^f   Dominguez J ^a,b,c  

^a HOSPITAL UNIVERSITARI GERMANS TRIAS I PUJOL   (Spain)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^e Barcelona Clinic   (Spain)

^f LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Antigenic stimulation; Immune response; Interferon ; Latent tuberculosis infection; Tuberculosis

Indexed keywords

EARLY SECRETORY ANTIGENIC TARGET 6; GAMMA INTERFERON; HEAT SHOCK PROTEIN; LATENCY ASSOCIATED NUCLEAR ANTIGEN; LATENCY ASSOCIATED PEPTIDE; MEMBRANE PROTEIN; MYCOBACTERIUM ANTIGEN; RECOMBINANT ANTIGEN; THIOREDOXIN REDUCTASE; TUBERCULIN;

ARTICLE; BCG VACCINATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; EXTRAPULMONARY TUBERCULOSIS; FEMALE; HUMAN; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOSTIMULATION; LUNG TUBERCULOSIS; MAJOR CLINICAL STUDY; MALE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PROSPECTIVE STUDY; QUESTIONNAIRE; REGULON; THORAX RADIOGRAPHY; TUBERCULOSIS;

MYCOBACTERIUM TUBERCULOSIS;

EID: 84907845641     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00517     Document Type: Article

References (56)

1. Abubakar, I., Zignol, M., Falzon, D., Raviglione, M., Ditiu, L., Masham, S., Adetifa, I., Ford, N., Cox, H., Lawn, S. D., Marais, B. J., Mchugh, T. D., Mwaba, P., Bates, M., Lipman, M., Zijenah, L., Logan, S., Mcnerney, R., Zumla, A., Sarda, K., Nahid, P., Hoelscher, M., Pletschette, M., Memish, Z. A., Kim, P., Hafner, R., Cole, S., Migliori, G. B., Maeurer, M., Schito, M. and Zumla, A. (2013). Drug-resistant tuberculosis: time for visionary political leadership. Lancet Infect Dis 13, 529-539.
2. Andersen, P., Munk, M. E., Pollock, J. M. and Doherty, T. M. (2000). Specific immunebased diagnosis of tuberculosis. Lancet 356, 1099-1104.
3. Black, G. F., Thiel, B. A., Ota, M. O., Parida, S. K., Adegbola, R., Boom, W. H., Dockrell, H. M., Franken, K. L., Friggen, A. H., Hill, P. C., Klein, M. R., Lalor, M. K., Mayanja, H., Schoolnik, G., Stanley, K., Weldingh, K., Kaufmann, S. H., Walzl, G., Ottenhoff, T. H. and Consortium, G. B. F. T. (2009). Immunogenicity of novel DosR regulon-encoded candidate antigens of Mycobacterium tuberculosis in three highburden populations in Africa. Clin Vaccine Immunol 16, 1203-1212.
4. Brandt, L., Feino Cunha, J., Weinreich Olsen, A., Chilima, B., Hirsch, P., Appelberg, R. and Andersen, P. (2002). Failure of the Mycobacterium bovis BCG vaccine: some species of environmental mycobacteria block multiplication of BCG and induction of protective immunity to tuberculosis. Infect Immun 70, 672-678.
5. Cappelli, G., Volpe, E., Grassi, M., Liseo, B., Colizzi, V. and Mariani, F. (2006). Profiling of Mycobacterium tuberculosis gene expression during human macrophage infection: upregulation of the alternative sigma factor G, a group of transcriptional regulators, and proteins with unknown function. Res Microbiol 157, 445-455.
6. Caws, M., Thwaites, G., Dunstan, S., Hawn, T. R., Lan, N. T., Thuong, N. T., Stepniewska, K., Huyen, M. N., Bang, N. D., Loc, T. H., Gagneux, S., Van Soolingen, D., Kremer, K., Van Der Sande, M., Small, P., Anh, P. T., Chinh, N. T., Quy, H. T., Duyen, N. T., Tho, D. Q., Hieu, N. T., Torok, E., Hien, T. T., Dung, N. H., Nhu, N. T., Duy, P. M., Van Vinh Chau, N. and Farrar, J. (2008). The influence of host and bacterial genotype on the development of disseminated disease with Mycobacterium tuberculosis. PLoS Pathog 4, e1000034.
7. Centers for Disease Control and Prevention (2000). Targeted tuberculin testing and treat- ment of latent tuberculosis infection. MMWR;49(No. RR-6): 23-25.
8. Chegou, N. N., Black, G. F., Loxton, A. G., Stanley, K., Essone, P. N., Klein, M. R., Parida, S. K., Kaufmann, S. H., Doherty, T. M., Friggen, A. H., Franken, K. L., Ottenhoff, T. H. and Walzl, G. (2012). Potential of novel Mycobacterium tuberculosis infection phase-dependent antigens in the diagnosis of TB disease in a high burden setting. BMC Infect Dis 12, 10.
9. Commandeur, S., Van Meijgaarden, K. E., Lin, M. Y., Franken, K. L., Friggen, A. H., Drijfhout, J. W., Oftung, F., Korsvold, G. E., Geluk, A. and Ottenhoff, T. H. (2011). Identification of human T-cell responses to Mycobacterium tuberculosis resuscitationpromoting factors in long-term latently infected individuals. Clin Vaccine Immunol 18, 676-683.
10. Commandeur, S., Van Meijgaarden, K. E., Prins, C., Pichugin, A. V., Dijkman, K., Van Den Eeden, S. J., Friggen, A. H., Franken, K. L., Dolganov, G., Kramnik, I., Schoolnik, G. K., Oftung, F., Korsvold, G. E., Geluk, A. and Ottenhoff, T. H. (2013). An unbiased genome-wide Mycobacterium tuberculosis gene expression approach to discover antigens targeted by human T cells expressed during pulmonary infection. J Immunol 190, 1659-1671.
11. Cooper, A. M., Dalton, D. K., Stewart, T. A., Griffin, J. P., Russell, D. G. and Orme, I. M. (1993). Disseminated tuberculosis in interferon gamma gene-disrupted mice. J Exp Med 178, 2243-2247.
12. Corbett, E. L., Watt, C. J., Walker, N., Maher, D., Williams, B. G., Raviglione, M. C. and Dye, C. (2003). The growing burden of tuberculosis: global trends and interactions with the HIV epidemic. Arch Intern Med 163, 1009-1021.
13. Day, C. L., Abrahams, D. A., Lerumo, L., Janse Van Rensburg, E., Stone, L., O'rie, T., Pienaar, B., De Kock, M., Kaplan, G., Mahomed, H., Dheda, K. and Hanekom, W. A. (2011). Functional capacity of Mycobacterium tuberculosis-specific T cell responses in humans is associated with mycobacterial load. J Immunol 187, 2222-2232.
14. Demissie, A., Leyten, E. M., Abebe, M., Wassie, L., Aseffa, A., Abate, G., Fletcher, H., Owiafe, P., Hill, P. C., Brookes, R., Rook, G., Zumla, A., Arend, S. M., Klein, M., Ottenhoff, T. H., Andersen, P., Doherty, T. M. and Group, V. S. (2006). Recognition of stage-specific mycobacterial antigens differentiates between acute and latent infections with Mycobacterium tuberculosis. Clin Vaccine Immunol 13, 179-186.
15. Dheda, K., Pooran, A., Pai, M., Miller, R. F., Lesley, K., Booth, H. L., Scott, G. M., Akbar, A. N., Zumla, A. and Rook, G. A. (2007). Interpretation of Mycobacterium tuberculosis antigen-specific IFN-gamma release assays (T-SPOT.TB) and factors that may modulate test results. J Infect 55, 169-173.
16. Ernst, J. D. (2012). The immunological life cycle of tuberculosis. Nat Rev Immunol 12, 581-591.
17. Esmail, H., Barry, C. E., 3rd and Wilkinson, R. J. (2012). Understanding latent tuberculosis: the key to improved diagnostic and novel treatment strategies. Drug Discov Today 17, 514-521.
18. Fine, P. E. (1995). Variation in protection by BCG: implications of and for heterologous immunity. Lancet 346, 1339-1345.
19. Flynn, J. L., Chan, J., Triebold, K. J., Dalton, D. K., Stewart, T. A. and Bloom, B. R. (1993). An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J Exp Med 178, 2249-2254.
20. Franken, K. L., Hiemstra, H. S., Van Meijgaarden, K. E., Subronto, Y., Den Hartigh, J., Ottenhoff, T. H. and Drijfhout, J. W. (2000). Purification of his-tagged proteins by immobilized chelate affinity chromatography: the benefits from the use of organic solvent. Protein Expr Purif 18, 95-99.
21. Goldsack, L. and Kirman, J. R. (2007). Half-truths and selective memory: Interferon gamma, CD4(+) T cells and protective memory against tuberculosis. Tuberculosis (Edinb) 87, 465-473.
22. Goletti, D., Butera, O., Vanini, V., Lauria, F. N., Lange, C., Franken, K. L., Angeletti, C., Ottenhoff, T. H. and Girardi, E. (2010). Response to Rv2628 latency antigen associates with cured tuberculosis and remote infection. Eur Respir J 36, 135-142.
23. Homolka, S., Niemann, S., Russell, D. G. and Rohde, K. H. (2010). Functional genetic diversity among Mycobacterium tuberculosis complex clinical isolates: delineation of conserved core and lineage-specific transcriptomes during intracellular survival. PLoS Pathog 6, e1000988.
24. Honaker, R. W., Stewart, A., Schittone, S., Izzo, A., Klein, M. R. and Voskuil, M. I. (2008). Mycobacterium bovis BCG vaccine strains lack narK2 and narX induction and exhibit altered phenotypes during dormancy. Infect Immun 76, 2587-2593.
25. Honer Zu Bentrup, K. and Russell, D. G. (2001). Mycobacterial persistence: adaptation to a changing environment. Trends Microbiol 9, 597-605.
26. Huang, W., Qi, Y., Ren, C., Wen, H., Franken, K. L., Ottenhoff, T. H. and Shen, J. (2013). Interferon-gamma responses to Mycobacterium tuberculosis Rpf proteins in contact investigation. Tuberculosis (Edinb) 93, 612-617.
27. Jabado, N. and Gros, P. (2005). Tuberculosis: the genetics of vulnerability. Nature 434, 709-711.
28. Kaech, S. M., Wherry, E. J. and Ahmed, R. (2002). Effector and memory T-cell differentiation: implications for vaccine development. Nat Rev Immunol 2, 251-262.
29. Karakousis, P. C., Yoshimatsu, T., Lamichhane, G., Woolwine, S. C., Nuermberger, E. L., Grosset, J. and Bishai, W. R. (2004). Dormancy phenotype displayed by extracellular Mycobacterium tuberculosis within artificial granulomas in mice. J Exp Med 200, 647-657.
30. Kassa, D., Ran, L., Geberemeskel, W., Tebeje, M., Alemu, A., Selase, A., Tegbaru, B., Franken, K. L., Friggen, A. H., Van Meijgaarden, K. E., Ottenhoff, T. H., Wolday, D., Messele, T. and Van Baarle, D. (2012). Analysis of immune responses against a wide range of Mycobacterium tuberculosis antigens in patients with active pulmonary tuberculosis. Clin Vaccine Immunol 19, 1907-1915.
31. Kaufmann, S. H. (2001). How can immunology contribute to the control of tuberculosis? Nat Rev Immunol 1, 20-30.
32. Kaufmann, S. H. (2012). Tuberculosis vaccine development: strength lies in tenacity. Trends Immunol 33, 373-379.
33. Latorre, I., De Souza-Galvao, M., Ruiz-Manzano, J., Lacoma, A., Prat, C., Fuenzalida, L., Altet, N., Ausina, V. and Dominguez, J. (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.
34. Leyten, E. M., Lin, M. Y., Franken, K. L., Friggen, A. H., Prins, C., Van Meijgaarden, K. E., Voskuil, M. I., Weldingh, K., Andersen, P., Schoolnik, G. K., Arend, S. M., Ottenhoff, T. H. and Klein, M. R. (2006). Human T-cell responses to 25 novel antigens encoded by genes of the dormancy regulon of Mycobacterium tuberculosis. Microbes Infect 8, 2052-2060.
35. Lin, M. Y., Geluk, A., Smith, S. G., Stewart, A. L., Friggen, A. H., Franken, K. L., Verduyn, M. J., Van Meijgaarden, K. E., Voskuil, M. I., Dockrell, H. M., Huygen, K., Ottenhoff, T. H. and Klein, M. R. (2007). Lack of immune responses to Mycobacterium tuberculosis DosR regulon proteins following Mycobacterium bovis BCG vaccination. Infect Immun 75, 3523-3530.
36. Lin, M. Y., Reddy, T. B., Arend, S. M., Friggen, A. H., Franken, K. L., Van Meijgaarden, K. E., Verduyn, M. J., Schoolnik, G. K., Klein, M. R. and Ottenhoff, T. H. (2009). Cross-reactive immunity to Mycobacterium tuberculosis DosR regulon-encoded antigens in individuals infected with environmental, nontuberculous mycobacteria. Infect Immun 77, 5071-5079.
37. Mukamolova, G. V., Kaprelyants, A. S., Young, D. I., Young, M. and Kell, D. B. (1998). A bacterial cytokine. Proc Natl Acad Sci U S A 95, 8916-8921.
38. Mwaba, P., Mcnerney, R., Grobusch, M. P., O'grady, J., Bates, M., Kapata, N., Maeurer, M. and Zumla, A. (2011). Achieving STOP TB Partnership goals: perspectives on development of new diagnostics, drugs and vaccines for tuberculosis. Trop Med Int Health 16, 819-827.
39. Ottenhoff, T. H. and Kaufmann, S. H. (2012). Vaccines against tuberculosis: where are we and where do we need to go? PLoS Pathog 8, e1002607.
40. Ottenhoff, T. H., Kumararatne, D. and Casanova, J. L. (1998). Novel human immunodeficiencies reveal the essential role of type-I cytokines in immunity to intracellular bacteria. Immunol Today 19, 491-494.
41. Pathan, A. A., Wilkinson, K. A., Klenerman, P., Mcshane, H., Davidson, R. N., Pasvol, G., Hill, A. V. and Lalvani, A. (2001). Direct ex vivo analysis of antigen-specific IFNgamma- secreting CD4 T cells in Mycobacterium tuberculosis-infected individuals: associations with clinical disease state and effect of treatment. J Immunol 167, 5217- 5225.
42. Pollock, L., Basu Roy, R. and Kampmann, B. (2013). How to use: interferon gamma release assays for tuberculosis. Arch Dis Child Educ Pract Ed 98, 99-105.
43. Riaño, F., Arroyo, L., Paris, S., Rojas, M., Friggen, A. H., Van Meijgaarden, K. E., Franken, K. L., Ottenhoff, T. H., Garcia, L. F. and Barrera, L. F. (2012). T cell responses to DosR and Rpf proteins in actively and latently infected individuals from Colombia. Tuberculosis (Edinb) 92, 148-159.
44. Ruiz-Manzano, J., Blanquer, R., Calpe, J. L., Caminero, J. A., Caylà, J., Domínguez, J., García, J. M. and Vidal, R. (2008). SEPAR Guidelines. Diagnostic and treatment of tuberculosis. Arch Bronconeumol 44, 551-566.
45. Rustad, T. R., Harrell, M. I., Liao, R. and Sherman, D. R. (2008). The enduring hypoxic response of Mycobacterium tuberculosis. PLoS One 3, e1502.
46. Rustad, T. R., Sherrid, A. M., Minch, K. J. and Sherman, D. R. (2009). Hypoxia: a window into Mycobacterium tuberculosis latency. Cell Microbiol 11, 1151-1159.
47. Schnappinger, D., Ehrt, S., Voskuil, M. I., Liu, Y., Mangan, J. A., Monahan, I. M., Dolganov, G., Efron, B., Butcher, P. D., Nathan, C. and Schoolnik, G. K. (2003). Transcriptional Adaptation of Mycobacterium tuberculosis within Macrophages: Insights into the Phagosomal Environment. J Exp Med 198, 693-704.
48. Schuck, S. D., Mueller, H., Kunitz, F., Neher, A., Hoffmann, H., Franken, K. L., Repsilber, D., Ottenhoff, T. H., Kaufmann, S. H. and Jacobsen, M. (2009). Identification of T-cell antigens specific for latent Mycobacterium tuberculosis infection. PLoS One 4, e5590.
49. Sutherland, J. S., Lalor, M. K., Black, G. F., Ambrose, L. R., Loxton, A. G., Chegou, N. N., Kassa, D., Mihret, A., Howe, R., Mayanja-Kizza, H., Gomez, M. P., Donkor, S., Franken, K., Hanekom, W., Klein, M. R., Parida, S. K., Boom, W. H., Thiel, B. A., Crampin, A. C., Ota, M., Walzl, G., Ottenhoff, T. H., Dockrell, H. M., Kaufmann, S. H. and Consortium, G. B. F. T. (2013). Analysis of host responses to Mycobacterium tuberculosis antigens in a multi-site study of subjects with different TB and HIV infection states in sub-Saharan Africa. PLoS One 8, e74080.
50. Talaat, A. M., Lyons, R., Howard, S. T. and Johnston, S. A. (2004). The temporal expression profile of Mycobacterium tuberculosis infection in mice. Proc Natl Acad Sci U S A 101, 4602-4607.
51. Tsenova, L., Harbacheuski, R., Sung, N., Ellison, E., Fallows, D. and Kaplan, G. (2007). BCG vaccination confers poor protection against M. tuberculosis HN878- induced central nervous system disease. Vaccine 25, 5126-5132.
52. Vordemeier, H. M., Harris, D. P., Roman, E., Lathigra, R., Moreno, C. and Ivanyi, J. (1991). Identification of T cell stimulatory peptides from the 38-kDa protein of Mycobacterium tuberculosis. J Immunol 147, 1023-1029.
53. Weir, R. E., Fine, P. E., Nazareth, B., Floyd, S., Black, G. F., King, E., Stanley, C., Bliss, L., Branson, K. and Dockrell, H. M. (2003). Interferon-gamma and skin test responses of schoolchildren in southeast England to purified protein derivatives from Mycobacterium tuberculosis and other species of mycobacteria. Clin Exp Immunol 134, 285-294.
54. Winek, J., Rowinska-Zakrzewska, E., Demkow, U., Szopinski, J., Szolkowska, M., Filewska, M., Jagodzinski, J. and Roszkowski-Sliz, K. (2008). Interferon gamma production in the course of Mycobacterium tuberculosis infection. J Physiol Pharmacol 59, 751-759.
55. World Health Organization (2013). Global Tuberculosis Report (WHO/HTM/TB/2013.11), Geneva, Switzerland.
56. Zvi, A., Ariel, N., Fulkerson, J., Sadoff, J. C. and Shafferman, A. (2008). Whole genome identification of Mycobacterium tuberculosis vaccine candidates by comprehensive data mining and bioinformatic analyses. BMC Med Genomics 1, 18.