The quest for a new vaccine against tuberculosis

Journal of Infection in Developing Countries

Volumn 3, Issue 1, 2009, Pages 5-15

  Delogu, Giovanni ^a   Fadda, Giovanni ^a  

^a CATHOLIC UNIVERSITY   (Italy)

Author keywords

DNA vaccines; Mycobacterium; Tuberculosis

Indexed keywords

BCG VACCINE; CULTURE FILTRATE PROTEIN 10; DNA VACCINE; EARLY SECRETORY ANTIGENIC TARGET 6; HEMAGGLUTININ; LIVE VACCINE;

ANTIVIRAL ACTIVITY; BACTERIAL STRAIN; BCG VACCINATION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CLINICAL TRIAL; DRUG EFFICACY; GENE DELETION; GENE DUPLICATION; GENE OVEREXPRESSION; GENETIC ASSOCIATION; GENETIC IMMUNIZATION; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOGENICITY; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PATHOGENESIS; PHENOTYPE; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; TUBERCULOSIS; TUBERCULOUS MENINGITIS; VIRUS ATTENUATION; VIRUS VIRULENCE;

ANIMALIA; MYCOBACTERIUM; MYCOBACTERIUM TUBERCULOSIS;

EID: 66549117134     PISSN: 20366590     EISSN: 19722680     Source Type: Journal    
DOI: 10.3855/jidc.99     Document Type: Review

References (74)

1. Collins, F. M. (1997) Tuberculosis research in a cold climate. Tuber. Lung Dis. 78, 99-107
2. World Health Organization. Global Tuberculosis Control. Surveillance, Planning, Financing. 2007.
3. Moss, A. R., Alland, D., Telzak, E., Hewlett, D., Jr., Sharp, V., Chiliade, P., LaBombardi, V., Kabus, D., Hanna, B., Palumbo, L., Brudney, K., Weltman, A., Stoeckle, K., Chirgwin, K., Simberkoff, M., Moghazeh, S., Eisner, W., Lutfey, M., and Kreiswirth, B. (1997) A city-wide outbreak of a multiple-drugresistant strain of M. tuberculosis in New York. Int. J. Tuberc. Lung Dis. 1, 115-121
4. Singh, J. A., Upshur, R., and Padayatchi, N. (2007) XDR-TB in South Africa: no time for denial or complacency. PLoS. Med. 4, e50
5. Jeon, C. Y., Hwang, S. H., Min, J. H., Prevots, D. R., Goldfeder, L. C., Lee, H., Eum, S. Y., Jeon, D. S., Kang, H. S., Kim, J. H., Kim, B. J., Kim, D. Y., Holland, S. M., Park, S. K., Cho, S. N., Barry, C. E., III, and Via, L. E. (2008) Extensively drug-resistant tuberculosis in South Korea: risk factors and treatment outcomes among patients at a tertiary referral hospital. Clin. Infect. Dis. 46, 42-49
6. Koenig, R. (2008) Drug-resistant tuberculosis. In South Africa, XDR TB and HIV prove a deadly combination. Science 319, 894-897
7. Calmette, A. and Plotz, H. (1929) Protective Inoculation against tuberculosis with BCG. American Review of Tuberculosis 19, 567-572
8. Colditz, G. A., Berkey, C. S., Mosteller, F., Brewer, T. F., Wilson, M. E., Burdick, E., and Fineberg, H. V. (1995) The efficacy of bacillus Calmette-Guerin vaccination of newborns and infants in the prevention of tuberculosis: meta-analyses of the published literature. Pediatrics 96, 29-35
9. Andersen, P. and Doherty, T. M. (2005) The success and failure of BCG - implications for a novel tuberculosis vaccine. Nat. Rev. Microbiol. 3, 656-662
10. Fine, P. E. (1989) The BCG story: lessons from the past and implications for the future. Rev. Infect. Dis. 11 Suppl 2, S353-S359
11. Fine, P. E. (1995) Variation in protection by BCG: implications of and for heterologous immunity. Lancet 346, 1339-1345
12. Rook, G. A., Dheda, K., and Zumla, A. (2005) Immune responses to tuberculosis in developing countries: implications for new vaccines. Nat. Rev. Immunol. 5, 661-667
13. Brandt, L., Feino, C. J., Weinreich, O. 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
14. Behr, M. A., Wilson, M. A., Gill, W. P., Salamon, H., Schoolnik, G. K., Rane, S., and Small, P. M. (1999) Comparative genomics of BCG vaccines by whole-genome DNA microarray. Science 284, 1520-1523
15. Gordon, S. V., Brosch, R., Billault, A., Garnier, T., Eiglmeier, K., and Cole, S. T. (1999) Identification of variable regions in the genomes of tubercle bacilli using bacterial artificial chromosome arrays. Mol. Microbiol. 32, 643-655
16. Giuseppe Champion, P. A. and Cox, J. S. (2007) Protein secretion systems in Mycobacteria. Cell Microbiol. 9, 1376-1384
17. Abdallah, A. M., Gey van Pittius, N. C., Champion, P. A., Cox, J., Luirink, J., Vandenbroucke-Grauls, C. M., Appelmelk, B. J., and Bitter, W. (2007) Type VII secretion - mycobacteria show the way. Nat. Rev. Microbiol. 5, 883-891
18. Pym, A. S., Brodin, P., Majlessi, L., Brosch, R., Demangel, C., Williams, A., Griffiths, K. E., Marchal, G., Leclerc, C., and Cole, S. T. (2003) Recombinant BCG exporting ESAT-6 confers enhanced protection against tuberculosis. Nat. Med. 9, 533-539
19. Brosch, R., Gordon, S. V., Garnier, T., Eiglmeier, K., Frigui, W., Valenti, P., Dos, S. S., Duthoy, S., Lacroix, C., Garcia-Pelayo, C., Inwald, J. K., Golby, P., Garcia, J. N., Hewinson, R. G., Behr, M. A., Quail, M. A., Churcher, C., Barrell, B. G., Parkhill, J., and Cole, S. T. (2007) Genome plasticity of BCG and impact on vaccine efficacy. Proc. Natl. Acad. Sci. U. S. A 104, 5596-5601
20. Russell, D. G. (2007) Who puts the tubercle in tuberculosis? Nat. Rev. Microbiol. 5, 39-47
21. Mittrucker, H. W., Steinhoff, U., Kohler, A., Krause, M., Lazar, D., Mex, P., Miekley, D., and Kaufmann, S. H. (2007) Poor correlation between BCG vaccination-induced T cell responses and protection against tuberculosis. Proc. Natl. Acad. Sci. U. S. A 104, 12434-12439
22. Kaufmann, S. H. (2001) How can immunology contribute to the control of tuberculosis? Nat. Rev. Immunol. 1, 20-30
23. Hondalus, M. K., Bardarov, S., Russell, R., Chan, J., Jacobs, W. R., Jr., and Bloom, B. R. (2000) Attenuation of and protection induced by a leucine auxotroph of Mycobacterium tuberculosis. Infect. Immun. 68, 2888-2898
24. Smith, D. A., Parish, T., Stoker, N. G., and Bancroft, G. J. (2001) Characterization of auxotrophic mutants of M. tuberculosis and their potential as vaccine candidates. Infect. Immun. 69, 1142-1150
25. Tullius, M. V., Harth, G., and Horwitz, M. A. (2003) Glutamine synthetase GlnA1 is essential for growth of M. tuberculosis in human THP-1 macrophages and guinea pigs. Infect. Immun. 71, 3927-3936
26. Pavelka, M. S., Jr., Chen, B., Kelley, C. L., Collins, F. M., and Jacobs, J. W., Jr. (2003) Vaccine efficacy of a lysine auxotroph of M. tuberculosis. Infect. Immun. 71, 4190-4192
27. Jackson, M., Raynaud, C., Laneelle, M. A., Guilhot, C., Laurent-Winter, C., Ensergueix, D., Gicquel, B., and Daffe, M. (1999) Inactivation of the antigen 85C gene profoundly affects the mycolate content and alters the permeability of the M. tuberculosis cell envelope. Mol. Microbiol. 31, 1573-1587
28. Sambandamurthy, V. K. and Jacobs, W. R., Jr. (2005) Live attenuated mutants of M. tuberculosis as candidate vaccines against tuberculosis. Microbes. Infect. 7, 955-961
29. Williams, A., Hatch, G. J., Clark, S. O., Gooch, K. E., Hatch, K. A., Hall, G. A., Huygen, K., Ottenhoff, T. H., Franken, K. L., Andersen, P., Doherty, T. M., Kaufmann, S. H., Grode, L., Seiler, P., Martin, C., Gicquel, B., Cole, S. T., Brodin, P., Pym, A. S., Dalemans, W., Cohen, J., Lobet, Y., Goonetilleke, N., McShane, H., Hill, A., Parish, T., Smith, D., Stoker, N. G., Lowrie, D. B., Kallenius, G., Svenson, S., Pawlowski, A., Blake, K., and Marsh, P. D. (2005) Evaluation of vaccines in the EU TB Vaccine Cluster using a guinea pig aerosol infection model of tuberculosis. Tuberculosis. (Edinb.) 85, 29-38
30. Sambandamurthy, V. K., Wang, X., Chen, B., Russell, R. G., Derrick, S., Collins, F. M., Morris, S. L., and Jacobs, W. R., Jr. (2002) A pantothenate auxotroph of M. tuberculosis is highly attenuated and protects mice against tuberculosis. Nat. Med. 8, 1171-1174
31. Aguilar, L. D., Infante, E., Bianco, M. V., Cataldi, A., Bigi, F., and Pando, R. H. (2006) Immunogenicity and protection induced by M. tuberculosis mce-2 and mce-3 mutants in a Balb/c mouse model of progressive pulmonary tuberculosis. Vaccine 24, 2333-2342
32. Hsu, T., Hingley-Wilson, S. M., Chen, M., Dai, A. Z., Morin, P. M., Marks, C. B., Padiyar, J., Goulding, C., Gingery, M., Eisemberg, D., Russell, R. G., Derrick, S. C., Collins, F. M., Morris, S. L., King, C. H., and Jacobs, W. R., Jr. (2003) The primary mechanism of attenuation of bacillus Calmette-Guerin is a loss of secreted lytic function required for invasion of lung interstitial tissue. Proc. Natl. Acad. Sci. U. S. A 100, 12420-12425
33. Hinchey, J., Lee, S., Jeon, B. Y., Basaraba, R. J., Venkataswamy, M. M., Chen, B., Chan, J., Braunstein, M., Orme, I. M., Derrick, S. C., Morris, S. L., Jacobs, W. R., Jr., and Porcelli, S. A. (2007) Enhanced priming of adaptive immunity by a proapoptotic mutant of M. tuberculosis. J. Clin. Invest 117, 2279-2288
34. Horwitz, M. A., Harth, G., Dillon, B. J., and Maslesa-Galic', S. (2000) Recombinant bacillus calmette-guerin (BCG) vaccines expressing the M. 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. U. S. A 97, 13853-13858
35. Horwitz, M. A. and Harth, G. (2003) A new vaccine against tuberculosis affords greater survival after challenge than the current vaccine in the guinea pig model of pulmonary tuberculosis. Infect. Immun. 71, 1672-1679
36. Flynn, J. L. and Chan, J. (2001) Immunology of tuberculosis. Annu. Rev. Immunol. 19, 93-129
37. Grode, L., Seiler, P., Baumann, S., Hess, J., Brinkmann, V., Nasser, E. A., Mann, P., Goosmann, C., Bandermann, S., Smith, D., Bancroft, G. J., Reyrat, J. M., van, S. D., Raupach, B., and Kaufmann, S. H. (2005) Increased vaccine efficacy against tuberculosis of recombinant M. bovis bacille Calmette-Guerin mutants that secrete listeriolysin. J. Clin. Invest 115, 2472-2479
38. Hess, J., Miko, D., Catic, A., Lehmensiek, V., Russell, D. G., and Kaufmann, S. H. (1998) M. bovis Bacille Calmette-Guerin strains secreting listeriolysin of Listeria monocytogenes. Proc. Natl. Acad. Sci. U.S.A 95, 5299-5304
39. Grode, L., Kursar, M., Fensterle, J., Kaufmann, S. H., and Hess, J. (2002) Cell-mediated immunity induced by recombinant M. bovis Bacille Calmette-Guerin strains against an intracellular bacterial pathogen: importance of antigen secretion or membrane-targeted antigen display as lipoprotein for vaccine efficacy. J. Immunol. 168, 1869-1876
40. Skeiky, Y. A. and Sadoff, J. C. (2006) Advances in tuberculosis vaccine strategies. Nat. Rev. Microbiol. 4, 469-476
41. Pal, P. G. and Horwitz, M. A. (1992) Immunization with extracellular proteins of M. tuberculosis induces cell-mediated immune responses and substantial protective immunity in a guinea pig model of pulmonary tuberculosis. Infect. Immun. 60, 4781-4792
42. Weinrich Olsen A., van Pinxteren, L. A., Meng, O. L., Birk, R. P., and Andersen, P. (2001) Protection of mice with a tuberculosis subunit vaccine based on a fusion protein of antigen 85b and esat-6. Infect. Immun. 69, 2773-2778
43. Skeiky, Y. A., Alderson, M. R., Ovendale, P. J., Guderian, J. A., Brandt, L., Dillon, D. C., Campos-Neto, A., Lobet, Y., Dalemans, W., Orme, I. M., and Reed, S. G. (2004) Differential immune responses and protective efficacy induced by components of a tuberculosis polyprotein vaccine, Mtb72F, delivered as naked DNA or recombinant protein. J. Immunol. 172, 7618-7628
44. Dietrich, J., Aagaard, C., Leah, R., Olsen, A. W., Stryhn, A., Doherty, T. M., and Andersen, P. (2005) 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. 174, 6332-6339
45. Menozzi, F. D., Rouse, J. H., Alavi, M., Laude-Sharp, M., Muller, J., Bischoff, R., Brennan, M. J., and Locht, C. (1996) Identification of a heparin-binding hemagglutinin present in mycobacteria. J. Exp. Med. 184, 993-1001
46. Menozzi, F. D., Bischoff, R., Fort, E., Brennan, M. J., and Locht, C. (1998) Molecular characterization of the mycobacterial heparin-binding hemagglutinin, a mycobacterial adhesin. Proc. Natl. Acad. Sci. U.S.A 95, 12625-12630
47. Pethe, K., Alonso, S., Biet, F., Delogu, G., Brennan, M. J., Locht, C., and Menozzi, F. D. (2001) The heparin-binding haemagglutinin of M. tuberculosis is required for extrapulmonary dissemination. Nature 412, 190-194
48. Masungi, C., Temmerman, S., Van Vooren, J. P., Drowart, A., Pethe, K., Menozzi, F. D., Locht, C., and Mascart, F. (2002) Differential T and B cell responses against M. tuberculosis heparin-binding hemagglutinin adhesin in infected healthy individuals and patients with tuberculosis. J. Infect. Dis. 185, 513-520
49. Parra, M., Pickett, T., Delogu, G., Dheenadhayalan, V., Debrie, A. S., Locht, C., and Brennan, M. J. (2004) The Mycobacterial Heparin-binding Hemagglutinin is a Protective antigen in the Mouse Aerosol Challenge Model of Tuberculosis. Infect. Immun. 72, 6799-6805
50. Temmerman, S., Pethe, K., Parra, M., Alonso, S., Rouanet, C., Pickett, T., Drowart, A., Debrie, A. S., Delogu, G., Menozzi, F. D., Sergheraert, C., Brennan, M. J., Mascart, F., and Locht, C. (2004) Methylation-dependent T cell immunity to M. tuberculosis heparin-binding hemagglutinin. Nat. Med. 10, 935-941
51. Delogu, G., Sanguinetti, M., Posteraro, B., Rocca, S., Zanetti, S., and Fadda, G. (2006) The hbhA gene of M. tuberculosis is specifically upregulated in the lungs but not in the spleens of aerogenically infected mice. Infect. Immun. 74, 3006-3011
52. Tascon, R. E., Colston, M. J., Ragno, S., Stavropoulos, E., Gregory, D., and Lowrie, D. B. (1996) Vaccination against tuberculosis by DNA injection. Nat. Med. 2, 888-892
53. Li, Z., Howard, A., Kelley, C., Delogu, G., Collins, F., and Morris, S. (1999) Immunogenicity of DNA vaccines expressing tuberculosis proteins fused to tissue plasminogen activator signal sequences. Infect. Immun. 67, 4780-4786
54. Parra, M., Cadieux, N., Pickett, T., Dheenadhayalan, V., and Brennan, M. J. (2006) A PE protein expressed by Mycobacterium avium is an effective T-cell immunogen. Infect. Immun. 74, 786-789
55. Dillon, D. C., Alderson, M. R., Day, C. H., Lewinsohn, D. M., Coler, R., Bement, T., Campos-Neto, A., Skeiky, Y. A., Orme, I. M., Roberts, A., Steen, S., Dalemans, W., Badaro, R., and Reed, S. G. (1999) Molecular characterization and human T-cell responses to a member of a novel M. tuberculosis mtb39 gene family. Infect. Immun. 67, 2941-2950
56. Delogu, G., Li, A., Repique, C., Collins, F., and Morris, S. L. (2002) DNA vaccine combinations expressing either tissue plasminogen activator signal sequence fusion proteins or ubiquitin-conjugated antigens induce sustained protective immunity in a mouse model of pulmonary tuberculosis. Infect. Immun. 70, 292-302
57. Denis, O., Tanghe, A., Palfliet, K., Jurion, F., van den Berg, T. P., Vanonckelen, A., Ooms, J., Saman, E., Ulmer, J. B., Content, J., and Huygen, K. (1998) Vaccination with plasmid DNA encoding mycobacterial antigen 85A stimulates a CD4+ and CD8+ T-cell epitopic repertoire broader than that stimulated by M. tuberculosis H37Rv infection. Infect. Immun. 66, 1527-1533
58. Brun, P., Zumbo, A., Castagliuolo, I., Delogu, G., Manfrin, F., Sali, M., Fadda, G., Grillot-Courvalin, C., Palu, G., and Manganelli, R. (2008) Intranasal delivery of DNA encoding antigens of M. tuberculosis by non-pathogenic invasive Escherichia coli. Vaccine 26, 1934-1941
59. Derrick, S. C., Yang, A. L., and Morris, S. L. (2004) A polyvalent DNA vaccine expressing an ESAT6-Ag85B fusion protein protects mice against a primary infection with M. tuberculosis and boosts BCG-induced protective immunity. Vaccine 23, 780-788
60. Derrick, S. C., Repique, C., Snoy, P., Yang, A. L., and Morris, S. (2004) Immunization with a DNA vaccine cocktail protects mice lacking CD4 cells against an aerogenic infection with M. tuberculosis. Infect. Immun. 72, 1685-1692
61. Ulmer, J. B., Wahren, B., and Liu, M. A. (2006) Gene-based vaccines: recent technical and clinical advances. Trends Mol. Med. 12, 216-222
62. Kirman, J. R., Turon, T., Su, H., Li, A., Kraus, C., Polo, J. M., Belisle, J., Morris, S., and Seder, R. A. (2003) Enhanced immunogenicity to M. tuberculosis by vaccination with an alphavirus plasmid replicon expressing antigen 85A. Infect. Immun. 71, 575-579
63. Derrick, S. C., Yang, A. L., and Morris, S. L. (2005) Vaccination with a Sindbis virus-based DNA vaccine expressing antigen 85B induces protective immunity against M. tuberculosis. Infect. Immun. 73, 7727-7735
64. Wang, J., Thorson, L., Stokes, R. W., Santosuosso, M., Huygen, K., Zganiacz, A., Hitt, M., and Xing, Z. (2004) Single mucosal, but not parenteral, immunization with recombinant adenoviral-based vaccine provides potent protection from pulmonary tuberculosis. J. Immunol. 173, 6357-6365
65. McShane, H., Brookes, R., Gilbert, S. C., and Hill, A. V. (2001) 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. 69, 681-686
66. McShane, H., Behboudi, S., Goonetilleke, N., Brookes, R., and Hill, A. V. (2002) Protective immunity against M. tuberculosis induced by dendritic cells pulsed with both CD8(+)- and CD4(+)-T-cell epitopes from antigen 85A. Infect. Immun. 70, 1623-1626
67. McShane, H., Pathan, A. A., Sander, C. R., Keating, S. M., Gilbert, S. C., Huygen, K., Fletcher, H. A., and Hill, A. V. (2004) Recombinant modified vaccinia virus Ankara expressing antigen 85A boosts BCG-primed and naturally acquired antimycobacterial immunity in humans. Nat. Med. 10, 1240-1244
68. Langermans, J. A., Andersen, P., van, S. D., Vervenne, R. A., Frost, P. A., van der, L. T., van Pinxteren, L. A., van den, H. J., Kroon, S., Peekel, I., Florquin, S., and Thomas, A. W. (2001) Divergent effect of bacillus Calmette-Guerin (BCG) vaccination on M. tuberculosis infection in highly related macaque species: implications for primate models in tuberculosis vaccine research. Proc. Natl. Acad. Sci. U.S.A 98, 11497-11502
69. Brennan, M. J., Fruth, U., Milstien, J., Tiernan, R., de Andrade, N. S., and Chocarro, L. (2007) Development of new tuberculosis vaccines: a global perspective on regulatory issues. PLoS. Med. 4, e252
70. Andersen, P. and Kaufmann, S. H. (2008) Novel Vaccination Strategies Against Tuberculosis. Handbook of Tuberculosis. Immunology and Cell Biology (Kaufmann, S. H. and Britton, W. J., eds.) pp. 369-387, WILEY-VCH Verlag GmbH & Co KGaA, Weinheim
71. Lowrie, D. B., Tascon, R. E., Bonato, V. L., Lima, V. M., Faccioli, L. H., Stavropoulos, E., Colston, M. J., Hewinson, R. G., Moelling, K., and Silva, C. L. (1999) Therapy of tuberculosis in mice by DNA vaccination. Nature 400, 269-271
72. Repique, C. J., Li, A., Collins, F. M., and Morris, S. L. (2002) DNA immunization in a mouse model of latent tuberculosis: effect of DNA vaccination on reactivation of disease and on reinfection with a secondary challenge. Infect. Immun. 70, 3318-3323
73. Cole, S. T., Brosch, R., Parkhill, J., Garnier, T., Churcher, C., Harris, D., Gordon, S. V., Eiglmeier, K., Gas, S., Barry, C. E., III, Tekaia, F., Badcock, K., Basham, D., Brown, D., Chillingworth, T., Connor, R., Davies, R., Devlin, K., Feltwell, T., Gentles, S., Hamlin, N., Holroyd, S., Hornsby, T., Jagels, K., and Barrell, B. G. (1998) Deciphering the biology of M. tuberculosis from the complete genome sequence. Nature 393, 537-544
74. Jung, Y. J., Ryan, L., LaCourse, R., and North, R. J. (2005) Properties and protective value of the secondary versus primary T helper type 1 response to airborne M. tuberculosis infection in mice. J. Exp. Med. 201, 1915-1924