Contributions of edema factor and protective antigen to the induction of protective immunity by Bacillus anthracis edema toxin as an intranasal adjuvant

Journal of Immunology

Volumn 185, Issue 10, 2010, Pages 5943-5952

  Duverger, Alexandra ^a,g   Carré, Jeanne Marie ^a,b   Jee, Junbae ^a   Leppla, Stephen H ^c   Cormet Boyaka, Estelle ^d   Tang, Wei Jen ^e   Tomé, Daniel ^a   Boyaka, Prosper N ^a,d,f  

^a Department of Veterinary Biosciences ^*  (Australia)

^b Internal Medicine   (Australia)

^c OHIO STATE UNIVERSITY   (United States)

^d AGROPARISTECH   (France)

^e NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^f UNIVERSITY OF CHICAGO   (United States)

^g UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; ADJUVANT; ANTIGEN; BACILLUS ANTHRACIS EDEMA FACTOR S414N; BACILLUS ANTHRACIS EDEMA TOXIN; BACILLUS ANTHRACIS PROTECTIVE ANTIGEN; DFF ANTIGEN; F1 V FUSION PROTEIN; HYBRID PROTEIN; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 6; MUTANT PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; U7 ANTIGEN; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ADJUVANT THERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ANTIGEN BINDING; ARTICLE; B LYMPHOCYTE; CERVICAL LYMPH NODE; CONTROLLED STUDY; CYTOKINE RESPONSE; CYTOSOL; DRUG UPTAKE; ENZYME ACTIVITY; FEMALE; IMMUNIZATION; IN VITRO STUDY; LYMPH NODE CELL; MACROPHAGE; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; WILD TYPE; YERSINIA PESTIS;

ADENYLATE CYCLASE; ADJUVANTS, IMMUNOLOGIC; ADMINISTRATION, INTRANASAL; ANIMALS; ANTHRAX; ANTHRAX VACCINES; ANTIGENS, BACTERIAL; BACILLUS ANTHRACIS; BACTERIAL TOXINS; CELL SEPARATION; FEMALE; FLOW CYTOMETRY; IMMUNITY, MUCOSAL; MICE; MICE, INBRED C57BL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 78650663116     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902795     Document Type: Article

References (44)

1. Young, J. A., and R. J. Collier. 2007. Anthrax toxin: receptor binding, internalization, pore formation, and translocation. Annu. Rev. Biochem. 76:243-265.
2. Tang, W. J., and Q. Guo. 2009. The adenylyl cyclase activity of anthrax edema factor. Mol. Aspects Med. 30:423-430.
3. Duverger, A., R. J. Jackson, F. W. van Ginkel, R. Fischer, A. Tafaro, S. H. Leppla, K. Fujihashi, H. Kiyono, J. R. McGhee, and P. N. Boyaka. 2006. Bacillus anthracis edema toxin acts as an adjuvant for mucosal immune responses to nasally administered vaccine antigens. J. Immunol. 176:1776-1783.
4. Gill, D. M., and C. A. King. 1975. The mechanism of action of cholera toxin in pigeon erythrocyte lysates. J. Biol. Chem. 250:6424-6432.
5. van Heyningen, S. 1974. Cholera toxin: interaction of subunits with ganglioside GM1. Science 183:656-657.
6. Holmgren, J., M. Lindblad, P. Fredman, L. Svennerholm, and H. Myrvold. 1985. Comparison of receptors for cholera and Escherichia coli enterotoxins in human intestine. Gastroenterology 89:27-35.
7. Griffiths, S. L., R. A. Finkelstein, and D. R. Critchley. 1986. Characterization of the receptor for cholera toxin and Escherichia coli heat-labile toxin in rabbit intestinal brush borders. Biochem. J. 238:313-322.
8. Fukuta, S., J. L. Magnani, E. M. Twiddy, R. K. Holmes, and V. Ginsburg. 1988. Comparison of the carbohydrate-binding specificities of cholera toxin and Escherichia coli heat-labile enterotoxins LTh-I, LT-IIa, and LT-IIb. Infect. Immun. 56:1748-1753.
9. Douce, G., C. Turcotte, I. Cropley, M. Roberts, M. Pizza, M. Domenghini, R. Rappuoli, and G. Dougan. 1995. Mutants of Escherichia coli heat-labile toxin lacking ADP-ribosyltransferase activity act as nontoxic, mucosal adjuvants. Proc. Natl. Acad. Sci. USA 92:1644-1648.
10. Dickinson, B. L., and J. D. Clements. 1995. Dissociation of Escherichia coli heat-labile enterotoxin adjuvanticity from ADP-ribosyltransferase activity. Infect. Immun. 63:1617-1623.
11. Yamamoto, S., H. Kiyono, M. Yamamoto, K. Imaoka, K. Fujihashi, F. W. Van Ginkel, M. Noda, Y. Takeda, and J. R. McGhee. 1997. A nontoxic mutant of cholera toxin elicits Th2-type responses for enhanced mucosal immunity. Proc. Natl. Acad. Sci. USA 94:5267-5272.
12. Hagiwara, Y., Y. I. Kawamura, K. Kataoka, B. Rahima, R. J. Jackson, K. Komase, T. Dohi, P. N. Boyaka, Y. Takeda, H. Kiyono, et al. 2006. A second generation of double mutant cholera toxin adjuvants: enhanced immunity without intracellular trafficking. J. Immunol. 177:3045-3054.
13. Williams, N. A. 2000. Immune modulation by the cholera-like enterotoxin B-subunits: from adjuvant to immunotherapeutic. Int. J. Med. Microbiol. 290:447-453.
14. Agren, L., B. Löwenadler, and N. Lycke. 1998. A novel concept in mucosal adjuvanticity: the CTA1-DD adjuvant is a B cell-targeted fusion protein that incorporates the enzymatically active cholera toxin A1 subunit. Immunol. Cell Biol. 76:280-287.
15. Bowman, C. C., and J. D. Clements. 2001. Differential biological and adjuvant activities of cholera toxin and Escherichia coli heat-labile enterotoxin hybrids. Infect. Immun. 69:1528-1535.
16. Boyaka, P. N., M. Ohmura, K. Fujihashi, T. Koga, M. Yamamoto, M. N. Kweon, Y. Takeda, R. J. Jackson, H. Kiyono, Y. Yuki, and J. R. McGhee. 2003. Chimeras of labile toxin one and cholera toxin retain mucosal adjuvanticity and direct Th cell subsets via their B subunit. J. Immunol. 170:454-462.
17. Ramirez, D. M., S. H. Leppla, R. Schneerson, and J. Shiloach. 2002. Production, recovery and immunogenicity of the protective antigen from a recombinant strain of Bacillus anthracis. J. Ind. Microbiol. Biotechnol. 28:232-238.
18. Cooksey, B. A., G. C. Sampey, J. L. Pierre, X. Zhang, J. D. Karwoski, G. H. Choi, and M. W. Laird. 2004. Production of biologically active Bacillus anthracis edema factor in Escherichia coli. Biotechnol. Prog. 20:1651-1659.
19. Drum, C. L., S. Z. Yan, J. Bard, Y. Q. Shen, D. Lu, S. Soelaiman, Z. Grabarek, A. Bohm, and W. J. Tang. 2002. Structural basis for the activation of anthrax adenylyl cyclase exotoxin by calmodulin. Nature 415:396-402.
20. Soelaiman, S., B. Q. Wei, P. Bergson, Y. S. Lee, Y. Shen, M. Mrksich, B. K. Shoichet, and W. J. Tang. 2003. Structure-based inhibitor discovery against adenylyl cyclase toxins from pathogenic bacteria that cause anthrax and whooping cough. J. Biol. Chem. 278:25990-25997.
21. Fischer, R., J. R. McGhee, H. L. Vu, T. P. Atkinson, R. J. Jackson, D. Tomé, and P. N. Boyaka. 2005. Oral and nasal sensitization promote distinct immune responses and lung reactivity in a mouse model of peanut allergy. Am. J. Pathol. 167:1621-1630.
22. Boyaka, P. N., A. Tafaro, R. Fischer, S. H. Leppla, K. Fujihashi, and J. R. McGhee. 2003. Effective mucosal immunity to anthrax: neutralizing antibodies and Th cell responses following nasal immunization with protective antigen. J. Immunol. 170:5636-5643.
23. Mosmann, T. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65:55-63.
24. Bromander, A. K., M. Kjerrulf, J. Holmgren, and N. Lycke. 1993. Cholera toxin enhances alloantigen presentation by cultured intestinal epithelial cells. Scand. J. Immunol. 37:452-458.
25. Lycke, N., A. K. Bromander, L. Ekman, U. Karlsson, and J. Holmgren. 1989. Cellular basis of immunomodulation by cholera toxin in vitro with possible association to the adjuvant function in vivo. J. Immunol. 142:20-27.
26. Boyaka, P. N., M. Marinaro, R. J. Jackson, S. Menon, H. Kiyono, E. Jirillo, and J. R. McGhee. 1999. IL-12 is an effective adjuvant for induction of mucosal immunity. J. Immunol. 162:122-128.
27. Staats, H. F., and F. A. Ennis, Jr. 1999. IL-1 is an effective adjuvant for mucosal and systemic immune responses when coadministered with protein immunogens. J. Immunol. 162:6141-6147.
28. Hong, J., J. Beeler, N. L. Zhukovskaya, W. He, W. J. Tang, and M. R. Rosner. 2005. Anthrax edema factor potency depends on mode of cell entry. Biochem. Biophys. Res. Commun. 335:850-857.
29. Cao, H., D. Agrawal, N. Kushner, N. Touzjian, M. Essex, and Y. Lu. 2002. Delivery of exogenous protein antigens to major histocompatibility complex class I pathway in cytosol. J. Infect. Dis. 185:244-251.
30. Kushner, N., D. Zhang, N. Touzjian, M. Essex, J. Lieberman, and Y. Lu. 2003. A fragment of anthrax lethal factor delivers proteins to the cytosol without requiring protective antigen. Proc. Natl. Acad. Sci. USA 100:6652-6657.
31. Finkelman, F. D., J. Holmes, I. M. Katona, J. F. Urban, Jr., M. P. Beckmann, L. S. Park, K. A. Schooley, R. L. Coffman, T. R. Mosmann, and W. E. Paul. 1990. Lymphokine control of in vivo immunoglobulin isotype selection. Annu. Rev. Immunol. 8:303-333.
32. Mock, M., and A. Fouet. 2001. Anthrax. Annu. Rev. Microbiol. 55:647-671.
33. Goletz, T. J., K. R. Klimpel, N. Arora, S. H. Leppla, J. M. Keith, and J. A. Berzofsky. 1997. Targeting HIV proteins to the major histocompatibility complex class I processing pathway with a novel gp120-anthrax toxin fusion protein. Proc. Natl. Acad. Sci. USA 94:12059-12064.
34. Ballard, J. D., R. J. Collier, and M. N. Starnbach. 1996. Anthrax toxin-mediated delivery of a cytotoxic T-cell epitope in vivo. Proc. Natl. Acad. Sci. USA 93:12531-12534.
35. Zhang, Y., Y. Kida, K. Kuwano, Y. Misumi, Y. Ikehara, and S. Arai. 2001. Role of furin in delivery of a CTL epitope of an anthrax toxin-fusion protein. Microbiol. Immunol. 45:119-125.
36. Doling, A. M., J. D. Ballard, H. Shen, K. M. Krishna, R. Ahmed, R. J. Collier, and M. N. Starnbach. 1999. Cytotoxic T-lymphocyte epitopes fused to anthrax toxin induce protective antiviral immunity. Infect. Immun. 67:3290-3296.
37. Moriya, O., M. Matsui, M. Osorio, H. Miyazawa, C. M. Rice, S. M. Feinstone, S. H. Leppla, J. M. Keith, and T. Akatsuka. 2001. Induction of hepatitis C virusspecific cytotoxic T lymphocytes in mice by immunization with dendritic cells treated with an anthrax toxin fusion protein. Vaccine 20:789-796.
38. Dal Molin, F., F. Tonello, D. Ladant, I. Zornetta, I. Zamparo, G. Di Benedetto, M. Zaccolo, and C. Montecucco. 2006. Cell entry and cAMP imaging of anthrax edema toxin. EMBO J. 25:5405-5413.
39. Tournier, J. N., S. Rossi Paccani, A. Quesnel-Hellmann, and C. T. Baldari. 2009. Anthrax toxins: a weapon to systematically dismantle the host immune defenses. Mol. Aspects Med. 30:456-466.
40. Maldonado-Arocho, F. J., and K. A. Bradley. 2009. Anthrax edema toxin induces maturation of dendritic cells and enhances chemotaxis towards macrophage inflammatory protein 3beta. Infect. Immun. 77:2036-2042.
41. Firoved, A. M., G. F. Miller, M. Moayeri, R. Kakkar, Y. Shen, J. F. Wiggins, E. M. McNally, W. J. Tang, and S. H. Leppla. 2005. Bacillus anthracis edema toxin causes extensive tissue lesions and rapid lethality in mice. Am. J. Pathol. 167:1309-1320.
42. Chen, K. H., S. Liu, L. A. Bankston, R. C. Liddington, and S. H. Leppla. 2007. Selection of anthrax toxin protective antigen variants that discriminate between the cellular receptors TEM8 and CMG2 and achieve targeting of tumor cells. J. Biol. Chem. 282:9834-9845.
43. Singh, Y., K. R. Klimpel, N. Arora, M. Sharma, and S. H. Leppla. 1994. The chymotrypsin-sensitive site, FFD315, in anthrax toxin protective antigen is required for translocation of lethal factor. J. Biol. Chem. 269:29039-29046.
44. Liu, S., T. H. Bugge, and S. H. Leppla. 2001. Targeting of tumor cells by cell surface urokinase plasminogen activator-dependent anthrax toxin. J. Biol. Chem. 276:17976-17984.