Difference in TB10.4 T-cell epitope recognition following immunization with recombinant TB10.4, BCG or infection with Mycobacterium tuberculosis

European Journal of Immunology

Volumn 40, Issue 5, 2010, Pages 1342-1354

  Billeskov, Rolf ^a,b   Grandal, Michael V ^b   Poulsen, Christian ^c   Christensen, Jan P ^b   Winter, Nathalie ^d   Vingsbo Lundberg, Carina ^a   Hoang, Truc T K T ^a   Van Deurs, Bo ^b   Song, Young Hwa ^c   Aagaard, Claus ^a   Andersen, Peter ^a   Dietrich, Jes ^a  

^a STATENS SERUM INSTITUT   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^d INSTITUT PASTEUR   (France)

Author keywords

Epitopes; Intracellular localization; Subdominant; T cells; Vaccine uptake

Indexed keywords

BCG VACCINE; RECOMBINANT VACCINE; TB10.4 VACCINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; MACROPHAGE; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; TUBERCULOSIS;

ANIMALS; ANTIGENS, BACTERIAL; BCG VACCINE; CARRIER PROTEINS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CROSSES, GENETIC; EPITOPES, T-LYMPHOCYTE; FEMALE; IMMUNITY, INNATE; IMMUNIZATION; INTERFERON-GAMMA; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MYCOBACTERIUM TUBERCULOSIS; NEUTROPHILS; OLIGOPEPTIDES; RECOMBINANT FUSION PROTEINS; T-LYMPHOCYTE SUBSETS; TUBERCULOSIS; TUBERCULOSIS VACCINES; VACCINES, SYNTHETIC;

EID: 77951757844     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200939830     Document Type: Article

References (38)

1. Xiang, S. D., Scholzen, A., Minigo, G., David, C., Apostolopoulos, V., Mottram, P. L. and Plebanski, M., Pathogen recognition and development of particulate vaccines: does size matter? Methods 2006. 40: 1-9.
2. Gamvrellis, A., Leong, D., Hanley, J. C., Xiang, S. D., Mottram, P. and Plebanski, M., Vaccines that facilitate antigen entry into dendritic cells. Immunol. Cell Biol. 2004. 82: 506-516.
3. Champion, J. A. and Mitragotri, S., Role of target geometry in phagocytosis. Proc. Natl. Acad. Sci. USA 2006. 103: 4930-4934.
4. Koch, R., Die Aetiologie der Tuberkulose. Berliner Klinische Wochenschrift 1882. 19: 221-230.
5. Abadie, V., Badell, E., Douillard, P., Ensergueix, D., Leenen, P. J., Tanguy, M., Fiette, L. et al., Neutrophils rapidly migrate via lymphatics after Mycobacterium bovis BCG intradermal vaccination and shuttle live bacilli to the draining lymph nodes. Blood 2005. 106: 1843-1850. (Pubitemid 41208603)
6. McDonough, K. A. and Kress, Y., Cytotoxicity for lung epithelial cells is a virulence-associated phenotype of Mycobacterium tuberculosis. Infect. Immun. 1995. 63: 4802-4811.
7. Korsholm, K. S., Agger, E. M., Foged, C., Christensen, D., Dietrich, J., Andersen, C. S., Geisler, C. et al., The adjuvant mechanism of cationic dimethyldioctadecylammonium liposomes. Immunology 2007. 121: 216-226. (Pubitemid 46663090)
8. Kamath, A. T., Valenti, M. P., Rochat, A. F., Agger, E. M., Lingnau, K., von Gabain, A., Andersen, P. et al., Protective anti-mycobacterial T cell responses through exquisite in vivo activation of vaccine-targeted dendritic cells. Eur. J. Immunol. 2008. 38: 1247-1256.
9. Savina, A. and Amigorena, S., Phagocytosis and antigen presentation in dendritic cells. Immunol. Rev. 2007. 219: 143-156.
10. Delvig, A. A. and Robinson, J. H., Different endosomal proteolysis requirements for antigen processing of two T-cell epitopes of the M5 protein from viable Streptococcus pyogenes. J. Biol. Chem. 1998. 273: 3291-3295.
11. Skeiky, Y. A., Alderson, M. R., Ovendale, P. J., Guderian, J. A., Brandt, L., Dillon, D. C., Campos-Neto, A. et al., Differential immune responses and protective efficacy induced by components of a tuberculosis polyprotein vaccine, Mtb72F, delivered as naked DNA or recombinant protein. J. Immunol. 2004. 172: 7618-7628. (Pubitemid 38747626)
12. D'Souza, S., Rosseels, V., Romano, M., Tanghe, A., Denis, O., Jurion, F., Castiglione, N. et al., Mapping of murine Th1 helper T-Cell epitopes of mycolyl transferases Ag85A, Ag85B, and Ag85C from Mycobacterium tuberculosis. Infect. Immun. 2003. 71: 483-493.
13. Radosevic, K.,Wieland, C.W., Rodriguez, A.,Weverling, G. J., Mintardjo, R., Gillissen, G., Vogels, R. et al., Protective immune responses to a recombinant adenovirus type 35 tuberculosis vaccine in two mouse strains: CD4 and CD8 T-cell epitope mapping and role of gamma interferon. Infect. Immun. 2007. 75: 4105-4115.
14. Brandt, L., Oettinger, T., Holm, A. and Andersen, P., Key epitopes on the ESAT-6 antigen recognized in mice during the recall of protective immunity to Mycobacterium tuberculosis. J. Immunol. 1996. 157: 3527-3533. (Pubitemid 126449166)
15. Dietrich, J., Aagaard, C., Leah, R., Olsen, A. W., Stryhn, A., Doherty, T. M. and Andersen, P., Exchanging ESAT6 with TB10.4 in an Ag85B fusion molecule-based tuberculosis subunit vaccine: efficient protection and ESAT6-based sensitive monitoring of vaccine efficacy. J. Immunol. 2005. 174: 6332-6339. (Pubitemid 40663826)
16. Bennekow, T., Dietrich, J., Rosenkrands, I., Stryhn, A., Doherty, T. M. and Andersen, P., Alteration in epitope recognition pattern in Ag85B and ESAT-6 has profound influence on vaccine-induced protection against in Mycobacterium tuberculosis. Eur. J. Immunol. 2006. 36: 3346-3355.
17. Davidsen, J., Rosenkrands, I., Christensen, D., Vangala, A., Kirby, D., Perrie, Y., Agger, E. M. et al., Characterization of cationic liposomes based on dimethyldioctadecylammonium and synthetic cord factor from M. tuberculosis (trehalose 6,60-dibehenate)-a novel adjuvant inducing both strong CMI and antibody responses. Biochim. Biophys. Acta 2005. 1718: 22-31.
18. Aagaard, C., Hoang, T. T., Izzo, A., Billeskov, R., Troudt, J., Arnett, K., Keyser, A. et al., Protection and polyfunctional T cells induced by Ag85B-TB104/IC31 against Mycobacterium tuberculosis is highly dependent on the antigen dose. PloS One 2009. 4: e5930.
19. Okkels, L. M. and Andersen, P., Protein-protein interactions of proteins from the ESAT-6 family of Mycobacterium tuberculosis. J. Bacteriol. 2004. 186: 2487-2491. (Pubitemid 38451853)
20. Lightbody, K. L., Renshaw, P. S., Collins, M. L., Wright, R. L., Hunt, D. M., Gordon, S. V., Hewinson, R. G. et al., Characterisation of complex formation between members of the Mycobacterium tuberculosis complex CFP-10/ESAT-6 protein family: towards an understanding of the rules governing complex formation and thereby functional flexibility. FEMS Microbiol. Lett. 2004. 238: 255-262.
21. Lightbody, K. L., Ilghari, D.,Waters, L. C., Carey, G., Bailey, M. A.,Williamson, R. A., Renshaw, P. S. et al., Molecular features governing the stability and specificity of functional complex formation by Mycobacterium tuberculosis CFP-10/ESAT-6 family proteins. J. Biol. Chem. 2008. 283: 17681-17690.
22. Peachman, K. K., Rao, M., Alving, C. R., Palmer, D. R., Sun, W. and Rothwell, S.W., Human dendritic cells and macrophages exhibit different intracellular processing pathways for soluble and liposome-encapsulated antigens. Immunobiology 2005. 210: 321-333. (Pubitemid 41102640)
23. Denis, O., Tanghe, A., Palfliet, K., Jurion, F., van den Berg, T. P., Vanonckelen, A., Ooms, J. et al., Vaccination with plasmid DNA encoding mycobacterial antigen 85A stimulates a CD4+and CD8+T-cell epitopic repertoire broader than that stimulated by Mycobacterium tuberculosis H37Rv infection. Infect. Immun. 1998. 66: 1527-1533.
24. Billeskov, R., Vingsbo-Lundberg, C., Andersen, P. and Dietrich, J., Induction of CD8 T cells against a novel epitope in TB10.4: correlation with mycobacterial virulence and the presence of a functional region of difference-1. J. Immunol. 2007. 179: 3973-3981.
25. Dietrich, J., Billeskov, R., Doherty, T. M. and Andersen, P., Synergistic effect of bacillus calmette guerin and a tuberculosis subunit vaccine in cationic liposomes: increased immunogenicity and protection. J. Immunol. 2007. 178: 3721-3730. (Pubitemid 46417640)
26. Majlessi, L., Rojas, M. J., Brodin, P. and Leclerc, C., CD8+-T-cell responses of Mycobacterium-infected mice to a newly identified major histocompatibility complex class I-restricted epitope shared by proteins of the ESAT-6 family. Infect. Immun. 2003. 71: 7173-7177.
27. Hervas-Stubbs, S., Majlessi, L., Simsova, M., Morova, J., Rojas, M. J., Nouze, C., Brodin, P. et al., High frequency of CD4+T cells specific for the TB10.4 protein correlates with protection against Mycobacterium tuberculosis infection. Infect. Immun. 2006. 74: 3396-3407.
28. van der Wel, N., Hava, D., Houben, D., Fluitsma, D., van Zon, M., Pierson, J., Brenner, M. et al., M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 2007. 129: 1287-1298. (Pubitemid 46962098)
29. Sable, S. B., Plikaytis, B. B. and Shinnick, T. M., Tuberculosis subunit vaccine development: impact of physicochemical properties of mycobacterial test antigens. Vaccine 2007. 25: 1553-1566.
30. Pethe, K., Bifani, P., Drobecq, H., Sergheraert, C., Debrie, A. S., Locht, C. and Menozzi, F. D., Mycobacterial heparin-binding hemagglutinin and laminin-binding protein share antigenic methyllysines that confer resistance to proteolysis. Proc. Natl. Acad. Sci. USA 2002. 99: 10759-10764.
31. Meher, A. K., Bal, N. C., Chary, K. V. and Arora, A., Mycobacterium tuberculosis H37Rv ESAT-6-CFP-10 complex formation confers thermodynamic and biochemical stability. FEBS J. 2006. 273: 1445-1462. (Pubitemid 44029108)
32. Marei, A., Ghaemmaghami, A., Renshaw, P., Wiselka, M., Barer, M., Carr, M. and Ziegler-Heitbrock, L., Superior T cell activation by ESAT-6 as compared with the ESAT-6-CFP-10 complex. Int. Immunol. 2005. 17: 1439-1446.
33. Meher, A. K., Lella, R. K., Sharma, C. and Arora, A., Analysis of complex formation and immune response of CFP-10 and ESAT-6 mutants. Vaccine 2007. 25: 6098-6106. (Pubitemid 47077544)
34. Skjot, R. L., Brock, I., Arend, S. M., Munk, M. E., Theisen, M., Ottenhoff, T. H. and Andersen, P., Epitope mapping of the immunodominant antigen TB10.4 and the two homologous proteins TB10.3 and TB12.9, which constitute a subfamily of the esat-6 gene family. Infect. Immunol. 2002. 70: 5446-5453.
35. Reche, P. A., Glutting, J. P., Zhang, H. and Reinherz, E. L., Enhancement to the RANKPEP resource for the prediction of peptide binding to MHC molecules using profiles. Immunogenetics 2004. 56: 405-419. (Pubitemid 39359226)
36. Morel, C., Badell, E., Abadie, V., Robledo, M., Setterblad, N., Gluckman, J. C., Gicquel, B. et al., Mycobacterium bovis BCG-infected neutrophils and dendritic cells cooperate to induce specific T cell responses in humans and mice. Eur. J. Immunol. 2008. 38: 437-447.
37. Schuller, S., Neefjes, J., Ottenhoff, T., Thole, J. and Young, D., Coronin is involved in uptake of Mycobacterium bovis BCG in human macrophages but not in phagosome maintenance. Cell Microbiol. 2001. 3: 785-793. (Pubitemid 33133475)
38. Ramachandra, L., Chu, R. S., Askew, D., Noss, E. H., Canaday, D. H., Potter, N. S. Johnsen, A. et al., Phagocytic antigen processing and effects of microbial products on antigen processing and T-cell responses. Immunol. Rev. 1999. 168: 217-239.