Bacillus subtilis spores: A novel microparticle adjuvant which can instruct balanced Th1 and Th2 immune response to specific antigen

European Journal of Immunology

Volumn 37, Issue 6, 2007, Pages 1538-1547

  Barnes, Andrew G C ^a   Cerovic, Vuk ^a   Hobson, Philip S ^a   Klavinskis, Linda S ^a  

^a GUY S HOSPITAL   (United Kingdom)

Author keywords

Adaptive immune response; Anjuvant; Bacillus subtilis; Polyvalent; Spore

Indexed keywords

ANTIBODY; ANTIGEN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G ANTIBODY; IMMUNOLOGICAL ADJUVANT; OVALBUMIN; PROBIOTIC AGENT; TETANUS TOXOID;

ANIMAL EXPERIMENT; ARTICLE; BACILLUS SUBTILIS; BACTERIAL SPORE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; DRUG SAFETY; DRUG TOLERABILITY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; IMMUNIZATION; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY TRACT MUCOSA; TH1 CELL; TH2 CELL; VAGINA MUCOSA;

ADJUVANTS, IMMUNOLOGIC; ADMINISTRATION, INTRANASAL; ANIMALS; BACILLUS SUBTILIS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CERVIX UTERI; CYTOKINES; EGG PROTEINS; FEMALE; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; LYMPHOCYTES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; OVALBUMIN; SPLEEN; SPORES, BACTERIAL; TETANUS TOXOID; TH1 CELLS; TH2 CELLS; VACCINATION; VAGINA;

EID: 34250647034     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200636875     Document Type: Article

References (48)

1. Trollfors, B., Knutsson, N., Taranger, J., Mark A., Bergfors, E., Sundh, V. and Lagergard, T., Diphtheria, tetanus and pertussis antibodies in 10-year-old children before and after a booster dose of three toxoids: implications for the timing of a booster dose. Eur. J. Pediatr. 2006. 165: 14-18.
2. Storsaeter, J. and Wolter, J., Is there a need for a new generation of vaccines against pertussis? Expert Opin. Emerg. Drugs 2006. 11: 195-205.
3. Skowera, A., de Jong, E. C., Schuitemaker, J. H., Allen, J. S., Wessely, S. C., Griffiths, G., Kapsenberg, M. and Peakman, M., Analysis of anthrax and plague biowarfare vaccine interactions with human monocyte-derived dendritic cells. J. Immunol. 2005. 175: 7235-7243.
4. McMichael, A. J., HIV vaccines. Annu. Rev. Immunol. 2006. 24: 227-255.
5. Kaufmann, S. H., Tuberculosis: back on the immunologists' agenda. Immunity 2006. 24: 351-357.
6. Hill, A. V., Pre-erythrocytic malaria vaccines: towards greater efficacy. Nat. Rev. Immunol. 2006. 6: 21-32.
7. Medzhitov, R. and Janeway, C., Jr., Innate immune recognition: mechanisms and pathways. Immunol. Rev. 2000. 173: 89-97.
8. Luft, T., Rodionova, E., Maraskovsky, E., Kirsch, M., Hess, M., Buchholtz, C., Goerner, M. et al., Adaptive functional differentiation of dendritic cells: integrating the network of extra-and intracellular signals. Blood 2006. 107: 4763-4769.
9. Akira, S., Toll-like receptors and innate immunity. Adv. Immunol. 2001. 78: 1-56.
10. Iwasaki, A. and Medzhitov, R., Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 2004. 5: 987-995.
11. Weiner, G. J., Liu, H. M., Wooldridge, J. E., Dahle, C. E. and Krieg, A. M., Immunostimulatory oligodeoxynucleotides containing the CpG motif are effective as immune adjuvants in tumor antigen immunization. Proc. Natl. Acad. Sci. USA 1997 94: 10833-10837.
12. Gorden, K. B., Gorski, K. S., Gibson, S. J., Kedl, R. M., Kieper, W. C., Qiu, X., Tomai, M. A. et al., Synthetic TLR agonists reveal functional differences between human TLR7 and TLR8. J. Immunol. 2005. 174: 1259-1268.
13. Wille-Reece, U., Flynn, B. J., Lore, K., Koup, R. A., Miles, A. P., Saul, A., Kedl, R. M. et al., Toll-like receptor agonists influence the magnitude and quality of memory T cell responses after prime-boost immunization in nonhuman primates. J. Exp. Med. 2006. 203: 1249-1258.
14. Gursel, I., Gursel, M., Ishii, K. J. and Klinman, D. M., Sterically stabilized cationic liposomes improve the uptake and immunostimulatory activity of CpG oligonucleotides. J. Immunol. 2001. 167: 3324-3328.
15. Querec, T., Bennouna, S., Alkan, S., Laouar, Y., Gorden, K., Flavell, R., Akira, S. et al., Yellow fever vaccine YF-17D activates multiple dendritic cell subsets via TLR2, 7, 8, and 9 to stimulate polyvalent immunity. J. Exp. Med. 2006, 203: 413-424.
16. Pulendran, B. and Ahmed, R., Translating innate immunity into immunological memory: implications for vaccine development. Cell 2006. 124: 849-863.
17. Napolitani, G., Rinaldi, A., Bertoni, F., Sallusto, F. and Lanzavecchia, A., Selected Toll-like receptor agonist combinations synergistically trigger a T helper type 1-polarizing program in dendritic cells. Nat. Immunol. 2005. 6: 769-776.
18. Mazza, P., The use of Bacillus subtilis as an antidiarrhoeal microorganism. Boll. Chim. Farm. 1994. 133: 3-18.
19. Bonomo, R., Luzi, G., Frielingsdorf, A. and Aiuti, F., Ruolo delle IgA secretorie nelle functioni dell' immunita locale dell' apparato digerente. Impiego di spore di B.subtilis in alcune forme morbose con dejicit di IgA e impogammaglobulinaemia. Chemioter. Antimicrob. 1980. 3: 237-240.
20. Vacca, A., Pantaleo, G., Ronco, M. and Dammacco, F., Chemotherapy for multiple myeloma using an intermitenet combination drug schedule (melphalon + prednisone) and alternating course of B. subtillis spores. Chemioterapia 1983. 2: 300-305.
21. Novelli, A., Ulivelli, A., Reali, E. F., Mannelli, F., Trombi Belcari, L., Spezia, R. and Periti, P., Bacillus subtilis spores as a natural pro-host oral agent. Preliminary data in children. Chemioterapia 1984. 3: 152-155.
22. Green, D. H., Wakeley, P. R., Page, A., Barnes, A., Baccigalupi, L., Ricca, E. and Cutting, S. M., Characterization of two Bacillus probiotics. Appl. Environ. Microbiol. 1999. 65: 4288-4291.
23. Driks, A., Bacillus subtilis spore coat. Microbiol. Mol. Biol. Rev. 1999. 63: 1-20.
24. Gilmore, M. E., Bandyopadhyay, D., Dean, A. M., Linnstaedt, S. D. and Popham, D. L., Production of muramic delta-lactam in Bacillus subtilis spore peptidoglycan. J. Bacteriol. 2004. 186: 80-89.
25. Pandey, N. K. and Aronson, A. I., Properties of the Bacillus subtilis spore coat. J. Bacteriol. 1979. 137: 1208-1218.
26. Henriques, A. O., Beall, B. W. and Moran, C. P., Jr., CotM of Bacillus subtilis, a member of the alpha-crystallin family of stress proteins, is induced during development and participates in spore outer coat formation. J. Bacteriol. 1997 179: 1887-1897.
27. Reischl, S., Thake, S., Homuth, G. and Schumann, W., Transcriptional analysis of three Bacillus subtilis genes coding for proteins with the alpha-crystallin domain characteristic of small heat shock proteins. FEMS Microbiol. Lett. 2001. 194: 99-103.
28. Roelofs, M. F., Boelens, W. C., Joosten, L. A., Abdollahi-Roodsaz, S., Geurts, J., Wunderink, L. U., Schreurs, B. W. et al., Identification of small heat shock protein B8 (HSP22) as a novel TLR4 ligand and potential involvement in the pathogenesis of rheumatoid arthritis. J. Immunol. 2006. 176: 7021-7027.
29. Marinaro, M., Staats, H. F., Hiroi, T., Jackson, R. J., Coste, M., Boyaka, P. N., Okahashi, N. et al., Mucosal adjuvant effect of cholera toxin in mice results from induction of T helper 2 (Th2) cells and IL-4. J. Immunol. 1995. 155: 4621-4629.
30. Theiler, M. and Smith, H., The use of yellow fever virus modified by in vitro cultivation for human immunization. J. Exp. Med. 1937 65: 787-800.
31. Sabin, A. B., Oral, live poliovirus vaccine for elimination of poliomyelitis. Arch. Intern. Med. 1960. 106: 5-9.
32. Oggioni, M. R., Ciabattini, A., Cuppone, A. M. and Pozzi, G., Bacillus spores for vaccine delivery. Vaccine 2003. 21 Suppl 2: S96-101.
33. Paccez, J. D., Luiz, W. B., Sbrogio-Almeida, M. E., Ferreira, R. C., Schumann, W. and Ferreira, L. C., Stable episomal expression system under control of a stress inducible promoter enhances the immunogenicity of Bacillus subtilis as a vector for antigen delivery. Vaccine 2006. 24: 2935-2943.
34. Ciabattini, A., Parigi, R., Isticato, R., Oggioni, M. R. and Pozzi, G., Oral priming of mice by recombinant spores of Bacillus subtilis. Vaccine 2004. 22: 4139-4143.
35. Mauriello, E. M., Duc le, H., Isticato, R., Cangiano, G., Hong, H. A., De Felice, M., Ricca, E. and Cutting, S. M., Display of heterologous antigens on the Bacillus subtilis spore coat using CotC as a fusion partner. Vaccine 2004. 22: 1177-1187.
36. Chada, V. G., Sanstad, E. A., Wang, R. and Driks, A., Morphogenesis of bacillus spore surfaces. J. Bacteriol. 2003. 185: 6255-6261.
37. Singh, M., Chesko, J., Kazzaz, J., Ugozzoli, M., Kan, E., Srivastava, I. and O'Hagan, D. T., Adsorption of a novel recombinant glycoprotein from HIV (Env gp120dV2 SF162) to anionic PLG microparticles retains the structural integrity of the protein, whereas encapsulation in PLG microparticles does not. Pharm. Res. 2004. 21: 2148-2152.
38. Chesko, J., Kazzaz, J., Ugozzoli, M., O'Hagan D, T. and Singh, M., An investigation of the factors controlling the adsorption of protein antigens to anionic PLG microparticles. J. Pharm. Sci. 2005. 94: 2510-2519.
39. Peter, K., Men, Y., Pantaleo, G., Gander, B. and Corradin, G., Induction of a cytotoxic T-cell response to HIV-1 proteins with short synthetic peptides and human compatible adjuvants. Vaccine 2001. 19: 4121-4129.
40. Yan, M., Peng, J., Jabbar, I. A., Liu, X., Filgueira, L., Frazer, I. H. and Thomas, R., Despite differences between dendritic cells and Langerhans cells in the mechanism of papillomavirus-like particle antigen uptake, both cells cross-prime T cells. Virology 2004. 324: 297-310.
41. Sanders, M. T., Brown, L. E., Deliyannis, G. and Pearse, M. J., ISCOM-based vaccines: the second decade. Immunol. Cell. Biol. 2005. 83: 119-128.
42. Raychaudhuri, S. and Rock, K. L., Fully mobilizing host defense: building better vaccines. Nat. Biotechnol. 1998. 16: 1025-1031.
43. Bafica, A., Scanga, C. A., Feng, C. G., Leifer, C., Cheever, A. and Sher, A., TLR9 regulates Th1 responses and cooperates with TLR2 in mediating optimal resistance to Mycobacterium tuberculosis. J. Exp. Med. 2005. 202: 1715-1724.
44. Bafica, A., Santiago, H. C., Goldszmid, R., Ropert, C., Gazzinelli, R. T. and Sher, A., Cutting edge: TLR9 and TLR2 signaling together account for MyD88-dependent control of parasitemia in Trypanosoma cruzi infection. J. Immunol. 2006. 177: 3515-3519.
45. + T cells engaging class II molecules in cholesterol-rich domains. J. Immunol. 2002. 168: 1172-1180.
46. Rescigno, M., Citterio, S., Thery, C., Rittig, M., Medaglini, D., Pozzi, G., Amigorena, S. and Ricciardi-Castagnoli, P., Bacteria-induced neo-biosynthesis, stabilization, and surface expression of functional class I molecules in mouse dendritic cells. Proc. Natl. Acad. Sci. USA 1998. 95: 5229-5234.
47. Klavinskis, L. S., Barnfield, C., Gao, L. and Parker, S., Intranasal immunization with plasmid DNA-lipid complexes elicits mucosal immunity in the female genital and rectal tracts. J. Immunol. 1999. 162: 254-262.
48. + T lymphocytes by immunostimulatory DNA-based vaccines. J. Immunol. 2002. 168: 4907-4913.