A tuberculosis vaccine base on phosphoantigens and fusion proteins induces distinct γδ and αβ T cell responses in primates

European Journal of Immunology

Volumn 37, Issue 2, 2007, Pages 549-565

  Cendron, Delphine ^a   Ingoure, Sophie ^b   Martino, Angelo ^c   Casetti, Rita ^c   Horand, Françoise ^d   Romagné, François ^b   Sicard, Hélène ^b   Fournié, Jean Jacques ^a   Poccia, Fabrizio ^c  

^a INSERM   (France)

^b INNATE PHARMA   (France)

^c NATIONAL INSTITUTE FOR INFECTIOUS DISEASES L SPALLANZANI   (Italy)

^d MDS Pharma Services   (France)

Author keywords

Primates; T cells; Tuberculosis; Vaccine

Indexed keywords

BCG VACCINE; EARLY SECRETORY ANTIGENIC TARGET 6 MUCOLYLTRANSFERASE COMPLEX ANTIGEN 85B FUSION PROTEIN; GAMMA INTERFERON; HYBRID PROTEIN; INTERLEUKIN 2; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; BACTERIAL ANTIGEN; BACTERIAL PROTEIN; BROMOHYDRIN PYROPHOSPHATE; CYTOKINE; ESAT 6 PROTEIN, MYCOBACTERIUM TUBERCULOSIS; ESAT-6 PROTEIN, MYCOBACTERIUM TUBERCULOSIS; LYMPHOCYTE ANTIGEN RECEPTOR; PYROPHOSPHATE;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; BCG VACCINATION; CELLULAR IMMUNITY; CLONAL ANERGY; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXIC T LYMPHOCYTE; DRUG SAFETY; DRUG TOLERABILITY; FEMALE; IMMUNOGENICITY; MACACA; MALE; MEMORY T LYMPHOCYTE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; T LYMPHOCYTE; TH1 CELL; TUBERCULOSIS; ANIMAL; FLOW CYTOMETRY; IMMUNOLOGY; LUNG TUBERCULOSIS; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CYTOKINES; DIPHOSPHATES; FEMALE; FLOW CYTOMETRY; MACACA FASCICULARIS; MALE; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECOMBINANT FUSION PROTEINS; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES; TUBERCULOSIS VACCINES; TUBERCULOSIS, PULMONARY;

EID: 33947718052     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200636343     Document Type: Article

References (76)

1. Ellner, J. J., Hirsch, C. S. and Whalen, C. C., Correlates of protective immunity to Mycobacterium tuberculosis in humans. Clin. Infect. Dis. 2000. 30 Suppl 3: S279-282.
2. Black, G. F., Weir, R. E., Floyd, S., Bliss, L., Warndorff, D. K., Crampin, A. C., Ngwira, B. et al., BCG-induced increase in interferon-gamma response to mycobacterial antigens and efficacy of BCG vaccination in Malawi and the UK: Two randomised controlled studies. Lancet 2002. 359: 1393-1401.
3. Hess, J., Miko, D., Catic, A., Lehmensiek, V., Russell, D. G. and Kaufmann, S. H., Mycobacterium bovis Bacille Calmette-Guerin strains secreting listeriolysin of Listeria monocytogenes. Proc. Natl. Acad. Sci. USA 1998. 95: 5299-5304.
4. Horwitz, M. A., Harth, G., Dillon, B. J. and Maslesa-Galic, S., Recombinant bacillus calmette-guerin (BCG) vaccines expressing the Mycobacterium tuberculosis 30-kDa major secretory protein induce greater protective immunity against tuberculosis than conventional BCG vaccines in a highly susceptible animal model. Proc. Natl. Acad. Sci. USA 2000. 97: 13853-13858.
5. Pym, A. S., Brodin, P., Majlessi, L., Brosch, R., Demangel, C., Williams, A., Griffiths, K. E. et al., Recombinant BCG exporting ESAT-6 confers enhanced protection against tuberculosis. Nat. Med. 2003. 9: 533-539.
6. Guleria, I., Teitelbaum, R., McAdam, R. A., Kalpana, G., Jacobs, W. R., Jr. and Bloom, B. R., Auxotrophic vaccines for tuberculosis. Nat. Med. 1996. 2: 334-337.
7. Jackson, M., Phalen, S. W., Lagranderie, M., Ensergueix, D., Chavarot, P., Marchal, G., McMurray, D. N. et al., Persistence and protective efficacy of a Mycobacterium tuberculosis auxotroph vaccine. Infect. Immun. 1999. 67: 2867-2873.
8. Smith, D. A., Parish, T., Stoker, N. G. and Bancroft, G. J., Characterization of auxotrophic mutants of Mycobacterium tuberculosis and their potential as vaccine candidates. Infect. Immun. 2001. 69: 1142-1150.
9. McShane, H., Brookes, R., Gilbert, S. C. and Hill, A. V., Enhanced immunogenicity of CD4(+) t-cell responses and protective efficacy of a DNA-modified vaccinia virus Ankara prime-boost vaccination regimen for murine tuberculosis. Infect. Immun. 2001. 69: 681-686.
10. Huygen, K., Content, J., Denis, O., Montgomery, D. L., Yawman, A. M., Deck, R. R., DeWitt, C. M. et al., Immunogenicity and protective efficacy of a tuberculosis DNA vaccine. Nat. Med. 1996. 2: 893-898.
11. Mollenkopf, H. J., Groine-Triebkorn, D., Andersen, P., Hess, J. and Kaufmann, S. H., Protective efficacy against tuberculosis of ESAT-6 secreted by a live Salmonella typhimurium vaccine carrier strain and expressed by naked DNA. Vaccine 2001. 19: 4028-4035.
12. Skeiky, Y. A. and Sadoff, J. C., Advances in tuberculosis vaccine strategies. Nat. Rev. Microbiol. 2006. 4: 469-476.
13. Kaufmann, S. H., Envisioning future strategies for vaccination against tuberculosis. Nat. Rev. Immunol. 2006. 6: 699-704.
14. McShane, H., Pathan, A. A., Sander, C. R., Keating, S. M., Gilbert, S. C., Huygen, K., Fletcher, H. A. and Hill, A. V., Recombinant modified vaccinia virus Ankara expressing antigen 85A boosts BCG-primed and naturally acquired antimycobacterial immunity in humans. Nat. Med. 2004. 10: 1240-1244.
15. Alderson, M. R., Bement, T., Day, C. H., Zhu, L., Molesh, D., Skeiky, Y. A., Coler, R. et al., Expression cloning of an immunodominant family of Mycobacterium tuberculosis antigens using human CD4(+) T cells. J. Exp. Med. 2000. 191: 551-560.
16. Skeiky, Y. A., Ovendale, P. J., Jen, S., Alderson, M. R., Dillon, D. C., Smith, S., Wilson, C. B. et al., T cell expression cloning of a Mycobacterium tuberculosis gene encoding a protective antigen associated with the early control of infection. J. Immunol. 2000. 165: 7140-7149.
17. 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. Immun. 2002. 70: 5446-5453.
18. Andersen, P., Andersen, A. B., Sorensen, A. L. and Nagai, S., Recall of long-lived immunity to Mycobacterium tuberculosis infection in mice. J. Immunol. 1995. 154: 3359-3372.
19. Huygen, K., Van Vooren, J. P., Turneer, M., Bosmans, R., Dierckx, P. and De Bruyn, J., Specific lymphoproliferation, gamma interferon production, and serum immunoglobulin G directed against a purified 32 kDa mycobacterial protein antigen (P32) in patients with active tuberculosis. Scand. J. Immunol. 1988. 27: 187-194.
20. 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.
21. Weinrich Olsen, A., van Pinxteren, L. A., Meng Okkels, L., Birk Rasmussen, P. and Andersen, P., Protection of mice with a tuberculosis subunit vaccine based on a fusion protein of antigen 85b and esat-6. Infect. Immun. 2001. 69: 2773-2778.
22. Brandt, L., Elhay, M., Rosenkrands, I., Lindblad, E. B. and Andersen, P., ESAT-6 subunit vaccination against Mycobacterium tuberculosis. Infect. Immun. 2000. 68: 791-795.
23. Davidsen, J., Rosenkrands, I., Christensen, D., Vangala, A., Kirby, D., Perrie, Y., Agger, E. M. and Andersen, P., Characterization of cationic liposomes based on dimethyldioctadecylammonium and synthetic cord factor from M. tuberculosis (trehalose 6,6′-dibehenate)-a novel adjuvant inducing both strong CMI and antibody responses. Biochim. Biophys. Acta 2005. 1718: 22-31.
24. Langermans, J. A., Doherty, T. M., Vervenne, R. A., van der Laan, T., Lyashchenko, K., Greenwald, R., Agger, E. M. et al., Protection of macaques against Mycobacterium tuberculosis infection by a subunit vaccine based on a fusion protein of antigen 85B and ESAT-6. Vaccine 2005. 23: 2740-2750.
25. Olsen, A. W., Williams, A., Okkels, L. M., Hatch, G. and Andersen, P., Protective effect of a tuberculosis subunit vaccine based on a fusion of antigen 85B and ESAT-6 in the aerosol guinea pig model. Infect. Immun. 2004. 72: 6148-6150.
26. Langermans, J. A., Andersen, P., van Soolingen, D., Vervenne, R. A., Frost, P. A., van der Laan, T., van Pinxteren, L. A. et al., Divergent effect of bacillus Calmette-Guerin (BCG) vaccination on Mycobacterium tuberculosis infection in highly related macaque species: Implications for primate models in tuberculosis vaccine research. Proc. Natl. Acad. Sci. USA 2001. 98: 11497-11502.
27. Poupot, M. and Fournie, J. J., Non-peptide antigens activating human Vgamma9/Vdelta2 T lymphocytes. Immunol. Lett. 2004. 95: 129-138.
28. Brigl, M. and Brenner, M. B., CD1: Antigen presentation and T cell function. Annu. Rev. Immunol. 2004. 22: 817-890.
29. Wang, H., Lee, H. K., Bukowski, J. F., Li, H., Mariuzza, R. A., Chen, Z. W., Nam, K. H. and Morita, C. T., Conservation of nonpeptide antigen recognition by rhesus monkey V gamma 2V delta 2 T cells. J. Immunol. 2003. 170: 3696-3706.
30. Poccia, F., Malkovsky, M., Pollak, A., Colizzi, V., Sireci, G., Salerno, A. and Dieli, F., In vivo gammadelta T cell priming to mycobacterial antigens by primary Mycobacterium tuberculosis infection and exposure to nonpeptidic ligands. Mol. Med. 1999. 5: 471-476.
31. Rakasz, E., MacDougall, A. V., Zayas, M. T., Helgelund, J. L., Ruckward, T. J., Hatfield, G., Dykhuizen, M. et al., Gammadelta T cell receptor repertoire in blood and colonic mucosa of rhesus macaques. J. Med. Primatol. 2000. 29: 387-396.
32. + T cells during mycobacterial infections. Science 2002. 295: 2255-2258.
33. Constant, P., Davodeau, F., Peyrat, M. A., Poquet, Y., Puzo, G., Bonneville, M. and Fournie, J. J., Stimulation of human gamma delta T cells by nonpeptidic mycobacterial ligands. Science 1994. 264: 267-270.
34. Constant, P., Poquet, Y., Peyrat, M. A., Davodeau, F., Bonneville, M. and Fournie, J. J., The antituberculous Mycobacterium bovis BCG vaccine is an attenuated mycobacterial producer of phosphorylated nonpeptidic antigens for human gamma delta T cells. Infect. Immun. 1995. 63: 4628-4633.
35. Espinosa, E., Belmant, C., Pont, F., Luciani, B., Poupot, R., Romagne, F., Brailly, H. et al., Chemical synthesis and biological activity of bromohydrin pyrophosphate, a potent stimulator of human gamma delta T cells. J. Biol. Chem. 2001. 276: 18337-18344.
36. Bennouna, J., Medioni, J., Rolland, F., Misset, J., Campone, M., Sicard, H., Tiollier, J. et al., Phase I clinical trial of Bromohydrin Pyrophosphate BrHPP (Phosphostim) a Vg9Vd2 T lymphocytes agonistin combination with low-dose interleukin-2 in patients with solid tumors. (abstract # 2536). J. Clin. Oncol. 2005. 23: 174s.
37. Casetti, R., Perretta, G., Taglioni, A., Mattei, M., Colizzi, V., Dieli, F., D'Offizi, G. et al., Drug-induced expansion and differentiation of V gamma 9V delta 2 T cells in vivo: The role of exogenous IL-2. J. Immunol. 2005. 175: 1593-1598.
38. Sicard, H., Ingoure, S., Luciani, B., Serraz, C., Fournie, J. J., Bonneville, M., Tiollier, J. and Romagne, F., In vivo immunomanipulation of V gamma 9V delta 2 T cells with a synthetic phosphoantigen in a preclinical nonhuman primate model. J. Immunol. 2005. 175: 5471-5480.
39. Ismaili, J., Olislagers, V., Poupot, R., Fournie, J. J. and Goldman, M., Human gamma delta T cells induce dendritic cell maturation. Clin. Immunol. 2002. 103: 296-302.
40. Martino, A., Casetti, R., D'Alessandri, A., Sacchi, A. and Poccia, F., Complementary function of gamma delta T-lymphocytes and dendritic cells in the response to isopentenyl-pyrophosphate and lipopolysaccharide antigens. J. Clin. Immunol. 2005. 25: 230-237.
41. Conti, L., Casetti, R., Cardone, M., Varano, B., Martino, A., Belardelli, F., Poccia, F. and Gessani, S., Reciprocal activating interaction between dendritic cells and pamidronate-stimulated gammadelta T cells: Role of CD86 and inflammatory cytokines. J. Immunol. 2005. 174: 252-260.
42. Devilder, M. C., Maillet, S., Bouyge-Moreau, I., Donnadieu, E., Bonneville, M. and Scotet, E., Potentiation of antigen-stimulated V gamma 9V delta 2 T cell cytokine production by immature dendritic cells (DC) and reciprocal effect on DC maturation. J. Immunol. 2006. 176: 1386-1393.
43. Brandes, M., Willimann, K. and Moser, B., Professional antigen-presentation function by human gammadelta T Cells. Science 2005. 309: 264-268.
44. Dieli, F., Troye-Blomberg, M., Ivanyi, J., Fournie, J. J., Krensky, A. M., Bonneville, M., Peyrat, M. A. et al., Granulysin-dependent killing of intracellular and extracellular Mycobacterium tuberculosis by Vgamma9/Vdelta2 T lymphocytes. J. Infect. Dis. 2001. 184: 1082-1085.
45. Dieli, F., Sireci, G., Caccamo, N., Di Sano, C., Titone, L., Romano, A., Di Carlo, P. et al., Selective depression of interferon-gamma and granulysin production with increase of proliferative response by Vgamma9/Vdelta2 T cells in children with tuberculosis. J. Infect. Dis. 2002. 186: 1835-1839.
46. + T cell effectors in immunocompromised hosts and during active pulmonary tuberculosis. J. Immunol. 2002. 168: 1484-1489.
47. Caccamo, N., Dieli, F., Wesch, D., Jomaa, H. and Eberl, M., Sex-specific phenotypical and functional differences in peripheral human Vgamma9/Vdelta2 T cells. J. Leukoc. Biol. 2006. 79: 663-666.
48. + Tcells in HLA-transgenic mice and humans. J. Immunol. 2000. 165: 6463-6471.
49. Lozes, E., Huygen, K., Content, J., Denis, O., Montgomery, D. L., Yawman, A. M., Vandenbussche, P. et al., Immunogenicity and efficacy of a tuberculosis DNA vaccine encoding the components of the secreted antigen 85 complex. Vaccine 1997. 15: 830-833.
50. Dieli, F., Poccia, F., Lipp, M., Sireci, G., Caccamo, N., Di Sano, C. and Salerno, A., Differentiation of effector/memory Vdelta2 T cells and migratory routes in lymph nodes or inflammatory sites. J. Exp. Med. 2003. 198: 391-397.
51. + T-cell subsets in the peripheral blood of patients with active pulmonary tuberculosis. Int. J. Immunopathol. Pharmacol 2003. 16: 247-252.
52. Cipriani, B., Borsellino, G., Poccia, F., Placido, R., Tramonti, D., Bach, S., Battistini, L. and Brosnan, C. F., Activation of C-C beta-chemokines in human peripheral blood gammadelta T cells by isopentenyl pyrophosphate and regulation by cytokines. Blood 2000. 95: 39-47.
53. Eberl, M., Engel, R., Beck, E. and Jomaa, H., Differentiation of human gamma-delta T cells towards distinct memory phenotypes. Cell. Immunol. 2002. 218: 1-6.
54. Glatzel, A., Wesch, D., Schiemann, F., Brandt, E., Janssen, O. and Kabelitz, D., Patterns of chemokine receptor expression on peripheral blood gamma delta T lymphocytes: Strong expression of CCR5 is a selective feature of V delta 2/V gamma 9 gamma delta T cells. J. Immunol. 2002. 168: 4920-4929.
55. Kabelitz, D. and Wesch, D., Features and functions of gamma delta T lymphocytes: Focus on chemokines and their receptors. Crit. Rev. Immunol. 2003. 23: 339-370.
56. Coudert, J. D., Zimmer, J., Tomasello, E., Cebecauer, M., Colonna, M., Vivier, E. and Held, W., Altered NKG2D function in NK cells induced by chronic exposure to NKG2D ligand-expressing tumor cells. Blood 2005. 106: 1711-1717.
57. Groh, V., Bruhl, A., El-Gabalawy, H., Nelson, J. L. and Spies, T., Stimulation of T cell autoreactivity by anomalous expression of NKG2D and its MIC ligands in rheumatoid arthritis. Proc. Natl. Acad. Sci. USA 2003. 100: 9452-9457.
58. + T lymphocytes from healthy donors and multiple sclerosis patients: Involvement of phosphatidylinositol 3 kinase and calcium calmodulin-dependent kinase II. J. Immunol. 2002. 168: 6071-6077.
59. Bonneville, M. and Fournie, J. J., Sensing cell stress and transformation through Vgamma9Vdelta2 T cell-mediated recognition of the isoprenoid pathway metabolites. Microbes Infect. 2005. 7: 503-509.
60. Pechhold, K., Wesch, D., Schondelmaier, S. and Kabelitz, D., Primary activation of V gamma 9-expressing gamma delta T cells by Mycobacterium tuberculosis. Requirement for Th1-type CD4 T cell help and inhibition by IL- 10. J. Immunol. 1994. 152: 4984-4992.
61. Caccamo, N., Battistini, L., Bonneville, M., Poccia, F., Fournie, J. J., Meraviglia, S., Borsellino, G. et al., CXCR5 identifies a subset of V{gamma}9V{delta}2 T cells which secrete IL-4 and IL-10 and help B cells for antibody production. J. Immunol. 2006. 177: 5290-5295.
62. Caccamo, N., Meraviglia, S., Ferlazzo, V., Angelini, D., Borsellino, G., Poccia, F., Battistini, L. et al., Differential requirements for antigen or homeostatic cytokines for proliferation and differentiation of human Vgamma9Vdelta2 naive, memory and effector T cell subsets. Eur. J. Immunol. 2005. 35: 1764-1772.
63. Dieli, F., Caccamo, N., Meraviglia, S., Ivanyi, J., Sireci, G., Bonanno, C. T., Ferlazzo, V. et al., Reciprocal stimulation of gammadelta T cells and dendritic cells during the anti-mycobacterial immune response. Eur. J. Immunol. 2004. 34: 3227-3235.
64. Leslie, D. S., Vincent, M. S., Spada, F. M., Das, H., Sugita, M., Morita, C. T. and Brenner, M. B., CD1-mediated gamma/delta T cell maturation of dendritic cells. J. Exp. Med. 2002. 196: 1575-1584.
65. Doherty, T. M., Demissie, A., Olobo, J., Wolday, D., Britton, S., Eguale, T., Ravn, P. and Andersen, P., Immune responses to the Mycobacterium tuberculosis-specific antigen ESAT-6 signal subclinical infection among contacts of tuberculosis patients. J. Clin. Microbiol. 2002. 40: 704-706.
66. Vordermeier, H. M., Chambers, M. A., Cockle, P. J., Whelan, A. O., Simmons, J. and Hewinson, R. G., Correlation of ESAT-6-specific gamma interferon production with pathology in cattle following Mycobacterium bovis BCG vaccination against experimental bovine tuberculosis. Infect. Immun. 2002. 70: 3026-3032.
67. Wilson, M. T. and Van Kaer, L., Natural killer T cells as targets for therapeutic intervention in autoimmune diseases. Curr. Pharm. Des. 2003. 9: 201-220.
68. Harada, M., Seino, K., Wakao, H., Sakata, S., Ishizuka, Y., Ito, T., Kojo, S. et al., Down-regulation of the invariant Valpha14 antigen receptor in NKT cells upon activation. Int. Immunol. 2004. 16: 241-247.
69. Leite-de-Moraes, M. C., Herbelin, A., Gouarin, C., Koezuka, Y., Schneider, E. and Dy, M., Fas/Fas ligand interactions promote activation-induced cell death of NK T lymphocytes. J. Immunol. 2000. 165: 4367-4371.
70. Eberl, G. and MacDonald, H. R., Rapid death and regeneration of NKT cells in anti-CD3epsilon- or IL-12-treated mice: A major role for bone marrow in NKT cell homeostasis. Immunity 1998. 9: 345-353.
71. Hayakawa, Y., Godfrey, D. I. and Smyth, M. J., Alpha-galactosylceramide: Potential immunomodulatory activity and future application. Curr. Med. Chem. 2004. 11: 241-252.
72. Parekh, V. V., Wilson, M. T., Olivares-Villagomez, D., Singh, A. K., Wu, L., Wang, C. R., Joyce, S. and Van Kaer, L., Glycolipid antigen induces long-term natural killer T cell anergy in mice. J. Clin. Invest. 2005. 115: 2572-2583.
73. Hoft, D. F., Brown, R. M. and Roodman, S. T., Bacille Calmette-Guerin vaccination enhances human gamma delta T cell responsiveness to mycobacteria suggestive of a memory-like phenotype. J. Immunol. 1998. 161: 1045-1054.
74. Fischer, K., Scotet, E., Niemeyer, M., Koebernick, H., Zerrahn, J., Maillet, S., Hurwitz, R. et al., Mycobacterial phosphatidylinositol mannoside is a natural antigen for CD1d-restricted T cells. Proc. Natl. Acad. Sci. USA 2004. 101: 10685-10690.
75. Gilleron, M., Ronet, C., Mempel, M., Monsarrat, B., Gachelin, G. and Puzo, G., Acylation state of the phosphatidylinositol mannosides from Mycobacterium bovis bacillus Calmette Guerin and ability to induce granuloma and recruit natural killer T cells. J. Biol, Chem. 2001. 276: 34896-34904.
76. Gilleron, M., Quesniaux, V. F. and Puzo, G., Acylation state of the phosphatidylinositol hexamannosides from Mycobacterium bovis bacillus Calmette Guerin and mycobacterium tuberculosis H37Rv and its implication in Toll-like receptor response. J. Biol. Chem. 2003. 278: 29880-29889.