DNA augments antigenicity of mycobacterial DNA-binding protein 1 and confers protection against Mycobacterium tuberculosis infection in mice

Journal of Immunology

Volumn 175, Issue 1, 2005, Pages 441-449

  Matsumoto, Sohkichi ^a   Matsumoto, Makoto ^b   Umemori, Kiyoko ^c   Ozeki, Yuriko ^a,d   Furugen, Makoto ^e   Tatsuo, Tomishige ^b   Hirayama, Yukio ^a   Yamamoto, Saburo ^c   Yamada, Takeshi ^e   Kobayashi, Kazuo ^a  

^a OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b OTSUKA PHARMACEUTICAL CO LTD   (Japan)

^c NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^d Department of Child Care Studies   (Japan)

^e NAGASAKI UNIVERSITY GRADUATE SCHOOL OF BIOMEDICAL SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BCG VACCINE; DNA; DNA BINDING PROTEIN; DNA BINDING PROTEIN 1; EPITOPE; GAMMA INTERFERON; IMMUNOGLOBULIN G ANTIBODY; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGENICITY; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; CPG ISLAND; CYTOKINE PRODUCTION; FEMALE; IMMUNE RESPONSE; IMMUNOSTIMULATION; IN VITRO STUDY; MOUSE; MYCOBACTERIUM; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; TUBERCULOSIS;

EID: 21244464634     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.175.1.441     Document Type: Article

References (69)

1. Wayne, L. G., and C. D. Sohaskey. 2001. Nonreplicating persistence of Mycobacterium tuberculosis. Annu. Rev. Microbiol. 55: 139-163.
2. Schwartzman, K. 2002. Latent tuberculosis infection: old problem, new priorities. CMAJ 166: 759-761.
3. Manabe, Y. C., and W. R. Bishai. 2000. Latent Mycobacterium tuberculosis-persistence, patience, and winning by waiting. Nat. Med. 6: 1327-1329.
4. Bloom, B. R. 2002. Tuberculosis: the global view. N. Engl. J. Med. 346: 1434-1435.
5. Horsburgh, C. R., Jr. 2004. Priorities for the treatment of latent tuberculosis infection in the United States. N. Engl. J. Med. 350: 2060-2067.
6. Colditz, G. A., T. F. Brewer, C. S. Berkey, M. E. Wilson, E. Burdick, H. V. Fineberg, and F. Mosteller. 1994. Efficacy of BCG vaccine in the prevention of tuberculosis: meta-analysis of the published literature. J. Am. Med. Assoc. 271: 698-702.
7. Collins, H. L., and S. H. Kaufmann. 2001. Prospects for better tuberculosis vaccines. Lancet Infect. Dis. 1: 21-28.
8. Roche, P. W., J. A. Triccas, and N. Winter. 1995. BCG vaccination against tuberculosis: past disappointments and future hopes. Trends Microbiol. 3: 397-401.
9. Milstien, J. B., and J. J. Gibson. 1990. Quality control of BCG vaccine by WHO: a review of factors that may influence vaccine effectiveness and safety. Bull. World Health Organ. 68: 93-108.
10. Sorensen, A. L., S. Nagai, G. Houen, P. Andersen, and A. B. Andersen. 1995. Purification and characterization of a low-molecular-mass T-cell antigen secreted by Mycobacterium tuberculosis. Infect. Immun. 63: 1710-1717.
11. Horwitz, M. A., B. W. Lee, B. J. Dillon, and G. Harth. 1995. Protective immunity against tuberculosis induced by vaccination with major extracellular proteins of Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 92: 1530-1534.
12. Skeiky, Y. A., M. R. Alderson, P. J. Ovendale, J. A. Guderian, L. Brandt, D. C. Dillon, A. Campos-Neto, Y. Lobet, W. Dalemans, I. M. Orme, et al. 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.
13. Tascon, R. E., M. J. Colston, S. Ragno, E. Stavropoulos, D. Gregory, and D. B. Lowrie. 1996. Vaccination against tuberculosis by DNA injection. Nat. Med. 2: 888-892.
14. Matsumoto, S., H. Yukitake, M. Furugen, T. Matsuo, T. Mineta, and T. Yamada. 1999. Identification of a novel DNA-binding protein from Mycobacterium bovis bacillus Calmette-Guérin. Microbiol. Immunol. 43: 1027-1036.
15. Furugen, M., S. Matsumoto, T. Matsuo, M. Matsumoto, and T. Yamada. 2001. Identification of the mycobacterial DNA-binding protein 1 region which suppresses transcription in vitro. Microb. Pathog. 30: 129-138.
16. Aoki, K., S. Matsumoto, Y. Hirayama, T. Wada, Y. Ozeki, M. Niki, P. Domenech, K. Umemori, S. Yamamoto, A. Mineda, et al. 2004. Extracellular mycobacterial DNA-binding protein 1 participates in Mycobacterium-lung epithelial cell interaction through hyaluronic acid. J. Biol. Chem. 279: 39798-39806.
17. Lee, B. H., B. Murugasu-Oei, and T. Dick. 1998. Upregulation of a histone-like protein in dormant Mycobacterium smegmatis. Mol. Gen. Genet. 260: 475-479.
18. Matsumoto, S., M. Furugen, H. Yukitake, and T. Yamada. 2000. The gene encoding mycobacterial DNA-binding protein 1 (MDP1) transformed rapidly growing bacteria to slowly growing bacteria. FEMS Microbiol. Lett. 182: 297-301.
19. Pethe, K., V. Puech, M. Daffe, C. Josenhans, H. Drobecq, C. Locht, and F. D. Menozzi. 2001. Mycobacterium smegmatis laminin-binding glycoprotein shares epitopes with Mycobacterium tuberculosis heparin-binding haemagglutinin. Mol. Microbiol. 39: 89-99.
20. Shimoji, Y., V. Ng, K. Matsumura, V. A. Fischetti, and A. Rambukkana. 1999. A 21-kDa surface protein of Mycobacterium leprae binds peripheral nerve laminin-2 and mediates Schwann cell invasion. Proc. Natl. Acad. Sci. USA 96: 9857-9862.
21. Rambukkana, A., J. L. Salzer, P. D. Yurchenco, and E. I. Tuomanen. 1997. Neural targeting of Mycobacterium leprae mediated by the G domain of the laminin-α2 chain. Cell 88: 811-821.
22. Ng, V., G. Zanazzi, R. Timpl, J. F. Tilts, J. L. Salzer, P. J. Brennan, and A. Rambukkana. 2000. Role of the cell wall phenolic glycolipid-1 in the peripheral nerve predilection of Mycobacterium leprae. Cell 103: 511-524.
23. Menozzi, F. D., J. H. Rouse, M. Alavi, M. Laude-Sharp, J. Muller, R. Bischoff, M. J. Brennan, and C. Locht. 1996. Identification of a heparin-binding hemagglutinin present in mycobacteria. J. Exp. Med. 184: 993-1001.
24. Hernandez-Pando, R., M. Jeyanathan, G. Mengistu, D. Aguilar, H. Orozco, M. Harboe, G. A. Rook, and G. Bjune. 2000. Persistence of DNA from Mycobacterium tuberculosis in superficially normal lung tissue during latent infection. Lancet 356: 2133-2138.
25. Prabhakar, S., P. S. Annapurna, N. K. Jain, A. B. Dey, J. S. Tyagi, and H. K. Prasad. 1998. Identification of an immunogenic histone-like protein (HLPMt) of Mycobacterium tuberculosis. Tuber. Lung Dis. 79: 43-53.
26. Yamamoto, S., T. Yamamoto, T. Kataoka, E. Kuramoto, O. Yano, and T. Tokunaga. 1992. Unique palindromic sequences in synthetic oligonucleotides are required to induce IFN and augment IFN-mediated natural killer activity. J. Immunol. 148: 4072-4076.
27. Krieg, A. M., A. K. Yi, S. Matson, T. J. Waldschmidt, G. A. Bishop, R. Teasdale, G. A. Koretzky, and D. M. Klinman. 1995. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 374: 546-549.
28. Hemmi, H., O. Takeuchi, T. Kawai, T. Kaisho, S. Sato, H. Sanjo, M. Matsumoto, K. Hoshino, H. Wagner, K. Takeda, and S. Akira. 2000. A Toll-like receptor recognizes bacterial DNA. Nature 408: 740-745.
29. Nagai, S., H. G. Wiker, M. Harboe, and M. Kinomoto. 1991. Isolation and partial characterization of major protein antigens in the culture fluid of Mycobacterium tuberculosis. Infect. Immun. 59: 372-382.
30. Tabira, Y., N. Ohara, and T. Yamada. 2000. Identification and characterization of the ribosome-associated protein, HrpA, of bacillus Calmette-Guerin. Microb. Pathog. 29: 213-222.
31. Belisle J. T., and M. G. Sonnenberg. 1998. Mycobacteria Protocol. Humana Press, Totowa.
32. Gursel, I., M. Gursel, K. J. Ishii, and D. M. Klinman. 2001. Sterically stabilized cationic liposomes improve the uptake and immunostimulatory activity of CpG oligonucleotides. J. Immunol. 167: 3324-3328.
33. Davis, H. L., R. Weeratna, T. J. Waldschmidt, L. Tygrett, J. Schorr, A. M. Krieg, and R. Weeranta. 1998. CpG DNA is a potent enhancer of specific immunity in mice immunized with recombinant hepatitis B surface antigen. J. Immunol. 160: 870-876.
34. Walker, P. S., T. Scharton-Kersten, A. M. Krieg, L. Love-Homan, E. D. Rowton, M. C. Udey, and J. C. Vogel. 1999. Immunostimulatory oligodeoxynucleotides promote protective immunity and provide systemic therapy for leishmaniasis via 1L-12- and IFN-γ-dependent mechanisms. Proc. Natl. Acad. Sci. USA 96: 6970-6975.
35. Pyles, R. B., D. Higgins, C. Chalk, A. Zalar, J. Eiden, C. Brown, G. Van Nest, and L. R. Stanberry. 2002. Use of immunostimulatory sequence-containing oligonucleotides as topical therapy for genital herpes simplex virus type 2 infection. J. Virol. 76: 11387-11396.
36. Klinman, D. M., I. Conover, and C. Coban. 1999. Repeated administration of synthetic oligodeoxynucleotides expressing CpG motifs provides long-term protection against bacterial infection. Infect. Immun. 67: 5658-5663.
37. Krieg, A. M., L. Love-Homan, A. K. Yi, and J. T. Harty. 1998. CpG DNA induces sustained IL-12 expression in vivo and resistance to Listeria monocytogenes challenge. J. Immunol. 161: 2428-2434.
38. Zimmermann, S., O. Egeter, S. Hausmann, G. B. Lipford, M. Rocken, H. Wagner, and K. Heeg. 1998. CpG oligodeoxynucleotides trigger protective and curative Th1 responses in lethal murine leishmaniasis. J. Immunol. 160: 3627-3630.
39. Ohara, N., M. Naito, C. Miyazaki, S. Matsumoto, Y. Tabira, and T. Yamada. 1997. HrpA, a new ribosome-associated protein which appears in heat-stressed Mycobacterium bovis bacillus Calmette-Guérin. J. Bacteriol. 179: 6495-6498.
40. Flynn, I. L., and I. Chan, 2001. Immunology of tuberculosis. Annu. Rev. Immunol. 19: 93-129.
41. Kaufmann, S. H. 2001. How can immunology contribute to the control of tuberculosis? Nat. Rev. Immunol. 1: 20-30.
42. Flynn, J. L., J. Chan, K. J. Triebold, D. K. Dalton, T. A. Stewart, and B. R. Bloom. 1993. An essential role for interferon γ in resistance to Mycobacterium tuberculosis infection. J. Exp. Med. 178: 2249-2254.
43. Cooper, A. M., D. K. Dalton, T. A. Stewart, J. P. Griffin, D. G. Russell, and I. M. Orme. 1993. Disseminated tuberculosis in interferon γ gene-disrupted mice. J. Exp. Med. 178: 2243-2247.
44. Coffman, R. L., B. W. Seymour, D. A. Lebman, D. D. Hiraki, J. A. Christiansen, B. Shrader, H. M. Cherwinski, H. F. Savelkoul, F. D. Finkelman, M. W. Bond, et al. 1988. The role of helper T cell products in mouse B cell differentiation and isotype regulation. Immunol. Rev. 102: 5-28.
45. Faquim-Mauro, E. L., R. L. Coffman, I. A. Abrahamsohn, and M. S. Macedo. 1999. Cutting edge: mouse IgG1 antibodies comprise two functionally distinct types that are differentially regulated by IL-4 and IL-12. J. Immunol. 163: 3572-3576.
46. + T cells provide help for B cell clonal expansion and antibody synthesis in a similar manner in vivo. J. Immunol. 165: 3136-3144.
47. Poltorak, A., X. He, I. Smirnova, M. Y. Liu, C. Van Huffel, X. Du, D. Birdwell, E. Alejos, M. Silva, C. Galanos, et al. 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282: 2085-2088.
48. Qureshi, S. T., L. Lariviere, G. Leveque, S. Clermont, K. J. Moore, P. Gros, and D. Malo. 1999. Endotoxin-tolerant mice have mutations in Toll-like receptor 4 (Tlr4). J. Exp. Med. 189: 615-625.
49. Yamamoto, T., S. Yamamoto, T. Kataoka, and T. Tokunaga. 1994. Lipofection of synthetic oligodeoxyribonucleotide having a palindromic sequence of AACGTT to murine splenocytes enhances interferon production and natural killer activity. Microbiol. Immunol. 38: 831-836.
50. Krieg, A. M. 2002. CpG motifs in bacterial DNA and their immune effects. Annu. Rev. Immunol. 20: 709-760.
51. Hacker, H., H. Mischak, T. Miethke, S. Liptay, R. Schmid, T. Sparwasser, K. Heeg, G. B. Lipford, and H. Wagner. 1998. CpG-DNA-specific activation of antigen-presenting cells requires stress kinase activity and is preceded by non-specific endocytosis and endosomal maturation. EMBO J. 17: 6230-6240.
52. Mueller-Ortiz, S. L., E. Sepulveda, M. R. Olsen, C. Jagannath, A. R. Wanger, and S. J. Norris. 2002. Decreased infectivity despite unaltered C3 binding by a DeltahbhA mutant of Mycobacterium tuberculosis. Infect. Immun. 70: 6751-6760.
53. Hirsch, C. S., J. J. Ellner, D. G. Russell, and E. A. Rich. 1994. Complement receptor-mediated uptake and tumor necrosis factor-α-mediated growth inhibition of Mycobacterium tuberculosis by human alveolar macrophages. J. Immunol. 152: 743-753.
54. Schlesinger, L. S., C. G. Bellinger-Kawahara, N. R. Payne, and M. A. Horwitz. 1990. Phagocytosis Mycobacterium tuberculosis is mediated by human monocyte complement receptors and complement component C3. J. Immunol. 144: 2771-2780.
55. Huygen, K., J. Content, O. Denis, D. L. Montgomery, A. M. Yawman, R. R. Deck, C. M. DeWitt, I. M. Orme, S. Baldwin, C. D'Souza, et al. 1996. Immunogenicity and protective efficacy of a tuberculosis DNA vaccine. Nat. Med. 2: 893-898.
56. Lozes, E., K. Huygen, J. Content, O. Denis, D. L. Montgomery, A. M. Yawman, P. Vandenbussche, J. P. Van Vooren, A. Drowart, J. B. Ulmer, et al. 1997. Immunogenicity and efficacy of a tuberculosis DNA vaccine encoding the components of the secreted antigen 85 complex. Vaccine 15: 830-833.
57. Riley, R. L., C. C. Mills, W. Nyka, N. Weinstock, P. B. Storey, L. U. Sultan, M. C. Riley, and W. F. Wells. 1959. Aerial dissemination of pulmonary tuberculosis: a two year study of contagion in a tuberculosis ward. Am. J. Hyg. 70: 185-196.
58. Smith, D. W., D. N. McMurray, E. H. Wiegeshaus, A. A. Grover, and G. E. Harding. 1970. Host-parasite relationships in experimental airborne tuberculosis. IV. Early events in the course of infection in vaccinated and nonvaccinated guinea pigs. Am. Rev. Respir. Dis. 102: 937-949.
59. Hacker, H., R. M. Vabulas, O. Takeuchi, K. Hoshino, S. Akira, and H. Wagner. 2000. Immune cell activation by bacterial CpG-DNA through myeloid differentiation marker 88 and tumor necrosis factor receptor-associated factor (TRAF)6. J. Exp. Med. 192: 595-600.
60. Schnare, M., A. C. Holt, K. Takeda, S. Akira, and R. Medzhitov. 2000. Recognition of CpG DNA is mediated by signaling pathways dependent on the adaptor protein MyD88. Curr. Biol. 10: 1139-1142.
61. Scanga, C. A., A. Bafica, C. G. Feng, A. W. Cheever, S. Hieny, and A. Sher. 2004. MyD88-deficient mice display a profound loss in resistance to Mycobacterium tuberculosis associated with partially impaired Th1 cytokine and nitric oxide synthase 2 expression. Infect. Immun. 72: 2400-2404.
62. Feng, C. G., C. A. Scanga, C. M. Collazo-Custodio, A. W. Cheever, S. Hieny, P. Caspar, and A. Sher. 2003. Mice lacking myeloid differentiation factor 88 display profound defects in host resistance and immune responses to Mycobacterium avium infection not exhibited by Toll-like receptor 2 (TLR2)- and TLR4-deficient animals. J. Immunol. 171: 4758-4764.
63. Reiling, N., C. Holscher, A. Fehrenbach, S. Kroger, C. J. Kirschning, S. Goyert, and S. Ehlers. 2002. Cutting edge: Toll-like receptor (TLR)2- and TLR4-mediated pathogen recognition in resistance to airborne infection with Mycobacterium tuberculosis. J. Immunol. 169: 3480-3484.
64. Thoma-Uszynski, S., S. Stenger, O. Takeuchi, M. T. Ochoa, M. Engele, P. A. Sieling, P. F. Barnes, M. Rollinghoff, P. L. Bolcskei, M. Wagner, et al. 2001. Induction of direct antimicrobial activity through mammalian Toll-like receptors. Science 291: 1544-1547.
65. Tokunaga, T., H. Yamamoto, S. Shimada, H. Abe, T. Fukuda, Y. Fujisawa, Y. Furutani, O. Yano, T. Kataoka, T. Sudo, et al. 1984. Antitumor activity of deoxyribonucleic acid fraction from Mycobacterium bovis BCG. I. Isolation, physicochemical characterization, and antitumor activity. J. Natl. Cancer Inst. 72: 955-962.
66. Shimada, S., O. Yano, H. Inoue, E. Kuramoto, T. Fukuda, H. Yamamoto, T. Kataoka, and T. Tokunaga. 1985. Antitumor activity of the DNA fraction from Mycobacterium bovis BCG. II. Effects on various syngeneic mouse tumors. J. Natl. Cancer Inst. 74: 681-688.
67. Halperin, S. A., G. Van Nest, B. Smith, S. Abtahi, H. Whiley, and J. J. Eiden. 2003. A phase I study of the safety and immunogenicity of recombinant hepatitis B surface antigen co-administered with an immunostimulatory phosphorothioate oligonucleotide adjuvant. Vaccine 21: 2461-2467.
68. Jahrsdorfer, B., and G. J. Weiner. 2003. CpG oligodeoxynucleotides for immune stimulation in cancer immunotherapy. Curr. Opin. Investig. Drugs. 4: 686-690.
69. Klinman, D. M. 2004. Immunotherapeutic uses of CpG oligodeoxynucleotides. Nat. Rev. Immunol. 4: 249-258.