Antigen-containing liposomes engrafted with flagellin-related peptides are effective vaccines that can induce potent antitumor immunity and immunotherapeutic effect

Journal of Immunology

Volumn 185, Issue 3, 2010, Pages 1744-1754

  Faham, Abdus ^a   Altin, Joseph G ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; FLAGELLIN; GAMMA INTERFERON; IMMUNOGLOBULIN G2B; LIPOSOME; MYELOID DIFFERENTIATION FACTOR 88; PEPTIDE VACCINE; TOLL LIKE RECEPTOR 5; AMINE; CANCER VACCINE; DRUG DERIVATIVE; NITRILOTRIACETIC ACID; NITRILOTRIACETIC ACID DITETRADECYLAMINE; PEPTIDE; TUMOR ANTIGEN;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; BONE MARROW; CANCER IMMUNOTHERAPY; CELL MATURATION; CONTROLLED STUDY; CORRELATION ANALYSIS; DENDRITIC CELL; DRUG ACTIVITY; FEMALE; HUMAN; HUMAN CELL; MEMBRANE VESICLE; METASTASIS; MOUSE; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN CELL; T LYMPHOCYTE; TUMOR GROWTH; TUMOR IMMUNITY; TUMOR MODEL; TUMOR REGRESSION; VACCINATION; ANIMAL; C57BL MOUSE; CELL LINE; CELL STRAIN HEPG2; CHO CELL; CRICETULUS; DBA MOUSE; DRUG DELIVERY SYSTEM; EXPERIMENTAL MELANOMA; HAMSTER; IMMUNOLOGY; MASTOCYTOMA; METHODOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; SYNTHESIS; TUMOR CELL LINE;

AMINES; AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, NEOPLASM; CANCER VACCINES; CELL LINE; CELL LINE, TUMOR; CHO CELLS; CONSERVED SEQUENCE; CRICETINAE; CRICETULUS; DRUG DELIVERY SYSTEMS; FLAGELLIN; HEP G2 CELLS; HUMANS; LIPOSOMES; MASTOCYTOMA; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MOLECULAR SEQUENCE DATA; NITRILOTRIACETIC ACID; PEPTIDES;

EID: 77956408001     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1000027     Document Type: Article

References (48)

1. Akira, S., S. Uematsu, and O. Takeuchi. 2006. Pathogen recognition and innate immunity. Cell 124: 783-801.
2. Gordon, S. 2002. Pattern recognition receptors: doubling up for the innate immune response. Cell 111: 927-930. (Pubitemid 36044685)
3. Uematsu, S., and S. Akira. 2006. Toll-like receptors and innate immunity. J. Mol. Med. 84: 712-725.
4. Gay, N. J., and M. Gangloff. 2008. Structure of toll-like receptors. In Handbook Experimental Pharmacology, Vol. 183. Springer Berlin Heidelberg, New York/ Berlin, p. 181-200.
5. Buwitt-Beckmann, U., H. Heine, K. H. Wiesmüller, G. Jung, R. Brock, S. Akira, and A. J. Ulmer. 2006. TLR1- and TLR6-independent recognition of bacterial lipopeptides. J. Biol. Chem. 281: 9049-9057.
6. Hayashi, F., K. D. Smith, A. Ozinsky, T. R. Hawn, E. C. Yi, D. R. Goodlett, J. K. Eng, S. Akira, D. M. Underhill, and A. Aderem. 2001. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410: 1099-1103. (Pubitemid 32391041)
7. Feuillet, V., S. Medjane, I. Mondor, O. Demaria, P. P. Pagni, J. E. Galán, R. A. Flavell, and L. Alexopoulou. 2006. Involvement of Toll-like receptor 5 in the recognition of flagellated bacteria. Proc. Natl. Acad. Sci. USA 103: 12487-12492.
8. Edwards, A. D., S. S. Diebold, E. M. Slack, H. Tomizawa, H. Hemmi, T. Kaisho, S. Akira, and C. Reis e Sousa. 2003. Toll-like receptor expression in murine DC subsets: lack of TLR7 expression by CD8 alpha+ DC correlates with unresponsiveness to imidazoquinolines. Eur. J. Immunol. 33: 827-833.
9. Uematsu, S., M. H. Jang, N. Chevrier, Z. Guo, Y. Kumagai, M. Yamamoto, H. Kato, N. Sougawa, H. Matsui, H. Kuwata, et al. 2006. Detection of pathogenic intestinal bacteria by Toll-like receptor 5 on intestinal CD11c+ lamina propria cells. Nat. Immunol. 7: 868-874.
10. Hawn, T. R., W. R. Berrington, I. A. Smith, S. Uematsu, S. Akira, A. Aderem, K. D. Smith, and S. J. Skerrett. 2007. Altered inflammatory responses in TLR5- deficient mice infected with Legionella pneumophila. J. Immunol. 179: 6981-6987.
11. -/- mice are more susceptible to Escherichia coli urinary tract infection. J. Immunol. 178: 4717-4720.
12. Uematsu, S., K. Fujimoto, M. H. Jang, B. G. Yang, Y. J. Jung, M. Nishiyama, S. Sato, T. Tsujimura, M. Yamamoto, Y. Yokota, et al. 2008. Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5. Nat. Immunol. 9: 769-776.
13. Bagchi, A., E. A. Herrup, H. S. Warren, J. Trigilio, H. S. Shin, C. Valentine, and J. Hellman. 2007. MyD88-dependent and MyD88-independent pathways in synergy, priming, and tolerance between TLR agonists. J. Immunol. 178: 1164-1171. (Pubitemid 46095190)
14. Zaru, R., N. Ronkina, M. Gaestel, J. S. Arthur, and C. Watts. 2007. The MAPK-activated kinase Rsk controls an acute Toll-like receptor signaling response in dendritic cells and is activated through two distinct pathways. Nat. Immunol. 8: 1227-1235.
15. Tallant, T., A. Deb, N. Kar, J. Lupica, M. J. de Veer, and J. A. DiDonato. 2004. Flagellin acting via TLR5 is the major activator of key signaling pathways leading to NF-kappa B and proinflammatory gene program activation in intestinal epithelial cells. BMC Microbiol. 4: 33.
16. Tsujimoto, H., T. Uchida, P. A. Efron, P. O. Scumpia, A. Verma, T. Matsumoto, S. K. Tschoeke, R. F. Ungaro, S. Ono, S. Seki, et al. 2005. Flagellin enhances NK cell proliferation and activation directly and through dendritic cell-NK cell interactions. J. Leukoc. Biol. 78: 888-897.
17. McSorley, S. J., B. T. Cookson, and M. K. Jenkins. 2000. Characterization of CD4+ T cell responses during natural infection with Salmonella typhimurium. J. Immunol. 164: 986-993.
18. McKee, A. S., M. W. Munks, and P. Marrack. 2007. How do adjuvants work? Important considerations for new generation adjuvants. Immunity 27: 687-690.
19. Cuadros, C., F. J. Lopez-Hernandez, A. L. Dominguez, M. McClelland, and J. Lustgarten. 2004. Flagellin fusion proteins as adjuvants or vaccines induce specific immune responses. Infect. Immun. 72: 2810-2816.
20. Huleatt, J. W., A. R. Jacobs, J. Tang, P. Desai, E. B. Kopp, Y. Huang, L. Song, V. Nakaar, and T. J. Powell. 2007. Vaccination with recombinant fusion proteins incorporating Toll-like receptor ligands induces rapid cellular and humoral immunity. Vaccine 25: 763-775.
21. Honko, A. N., N. Sriranganathan, C. J. Lees, and S. B. Mizel. 2006. Flagellin is an effective adjuvant for immunization against lethal respiratory challenge with Yersinia pestis. Infect. Immun. 74: 1113-1120.
22. McDonald, W. F., J. W. Huleatt, H. G. Foellmer, D. Hewitt, J. Tang, P. Desai, A. Price, A. Jacobs, V. N. Takahashi, Y. Huang, et al. 2007. A West Nile virus recombinant protein vaccine that coactivates innate and adaptive immunity. J. Infect. Dis. 195: 1607-1617.
23. Le Moigne, V., G. Robreau, and W. Mahana. 2006. Homologous recombination with linear DNA to insert antigenic protein in the flagellin: improvement of the Th1 immune response. Microbiol. Immunol. 50: 33-43.
24. Huleatt, J. W., V. Nakaar, P. Desai, Y. Huang, D. Hewitt, A. Jacobs, J. Tang, W. McDonald, L. Song, R. K. Evans, et al. 2008. Potent immunogenicity and efficacy of a universal influenza vaccine candidate comprising a recombinant fusion protein linking influenza M2e to the TLR5 ligand flagellin. Vaccine 26: 201-214.
25. Bargieri, D. Y., D. S. Rosa, C. J. Braga, B. O. Carvalho, F. T. Costa, N. M. Espíndola, A. J. Vaz, I. S. Soares, L. C. Ferreira, and M. M. Rodrigues. 2008. New malaria vaccine candidates based on the Plasmodium vivax Merozoite Surface Protein-1 and the TLR-5 agonist Salmonella Typhimurium FliC flagellin. Vaccine 26: 6132-6142.
26. Le Moigne, V., G. Robreau, and W. Mahana. 2008. Flagellin as a good carrier and potent adjuvant for Th1 response: study of mice immune response to the p27 (Rv2108) Mycobacterium tuberculosis antigen. Mol. Immunol. 45: 2499-2507.
27. Altin, J. G., M. G. Banwell, P. A. Coghlan, C. J. Easton, M. R. Nairn, and D. A. Offermann. 2006. Synthesis of NTA3-DTDA - A Chelator-Lipid that Promotes Stable Binding of His-Tagged Proteins to Membranes. Aust. J. Chem. 59: 302-306.
28. van Broekhoven, C. L., C. R. Parish, C. Demangel, W. J. Britton, and J. G. Altin. 2004. Targeting dendritic cells with antigen-containing liposomes: a highly effective procedure for induction of antitumor immunity and for tumor immunotherapy. Cancer Res. 64: 4357-4365.
29. van Broekhoven, C. L., and J. G. Altin. 2005. The novel chelator lipid 3(nitrilotriacetic acid)-ditetradecylamine (NTA(3)-DTDA) promotes stable binding of His-tagged proteins to liposomal membranes: potent anti-tumor responses induced by simultaneously targeting antigen, cytokine and costimulatory signals to T cells. Biochim. Biophys. Acta 1716: 104-116.
30. Herringson, T. P., R. R. Patlolla, and J. G. Altin. 2009. Targeting of plasmid DNA-lipoplexes to cells with molecules anchored via a metal chelator lipid. J. Gene Med. 11: 1048-1063.
31. Inaba, K., M. Inaba, N. Romani, H. Aya, M. Deguchi, S. Ikehara, S. Muramatsu, and R. M. Steinman. 1992. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 176: 1693-1702.
32. Faham, A., D. Bennett, and J. G. Altin. 2009. Liposomal Ag engrafted with peptides of sequence derived from HMGB1 induce potent Ag-specific and anti-tumour immunity. Vaccine 27: 5846-5854.
33. Smith, K. D., E. Andersen-Nissen, F. Hayashi, K. Strobe, M. A. Bergman, S. L. Barrett, B. T. Cookson, and A. Aderem. 2003. Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility. Nat. Immunol. 4: 1247-1253.
34. Reichhart, J. M. 2003. TLR5 takes aim at bacterial propeller. Nat. Immunol. 4: 1159-1160.
35. Murthy, K. G., A. Deb, S. Goonesekera, C. Szabó, and A. L. Salzman. 2004. Identification of conserved domains in Salmonella muenchen flagellin that are essential for its ability to activate TLR5 and to induce an inflammatory response in vitro. J. Biol. Chem. 279: 5667-5675.
36. Nempont, C., D. Cayet, M. Rumbo, C. Bompard, V. Villeret, and J. C. Sirard. 2008. Deletion of flagellin's hypervariable region abrogates antibody-mediated neutralization and systemic activation of TLR5-dependent immunity. J. Immunol. 181: 2036-2043.
37. Andersen-Nissen, E., K. D. Smith, R. Bonneau, R. K. Strong, and A. Aderem. 2007. A conserved surface on Toll-like receptor 5 recognizes bacterial flagellin. J. Exp. Med. 204: 393-403.
38. Andersen-Nissen, E., K. D. Smith, K. L. Strobe, S. L. Barrett, B. T. Cookson, S. M. Logan, and A. Aderem. 2005. Evasion of Toll-like receptor 5 by flagellated bacteria. Proc. Natl. Acad. Sci. USA 102: 9247-9252.
39. Samatey, F. A., K. Imada, S. Nagashima, F. Vonderviszt, T. Kumasaka, M. Yamamoto, and K. Namba. 2001. Structure of the bacterial flagellar proto- filament and implications for a switch for supercoiling. Nature 410: 331-337.
40. Wong, C. K., P. F. Cheung, W. K. Ip, and C. W. Lam. 2007. Intracellular signaling mechanisms regulating toll-like receptor-mediated activation of eosinophils. Am. J. Respir. Cell Mol. Biol. 37: 85-96.
41. Fukata, M., K. Breglio, A. Chen, A. S. Vamadevan, T. Goo, D. Hsu, D. Conduah, R. Xu, and M. T. Abreu. 2008. The myeloid differentiation factor 88 (MyD88) is required for CD4+ T cell effector function in a murine model of inflammatory bowel disease. J. Immunol. 180: 1886-1894.
42. Xia, C., M. Lu, Z. Zhang, Z. Meng, Z. Zhang, and C. Shi. 2008. TLRs antiviral effect on hepatitis B virus in HepG2 cells. J. Appl. Microbiol. 105: 1720-1727.
43. Hawn, T. R., A.Verbon, K. D. Lettinga, L. P. Zhao, S. S. Li, R. J. Laws, S. J. Skerrett, B. Beutler, L. Schroeder, A. Nachman, et al. 2003. A common dominant TLR5 stop codon polymorphism abolishes flagellin signaling and is associated with susceptibility to legionnaires' disease. J. Exp. Med. 198: 1563-1572.
44. Eaves-Pyles, T. D., H. R. Wong, K. Odoms, and R. B. Pyles. 2001. Salmonella flagellin-dependent proinflammatory responses are localized to the conserved amino and carboxyl regions of the protein. J. Immunol. 167: 7009-7016.
45. Van Broekhoven, C. L., and J. G. Altin. 2001. A novel system for convenient detection of low-affinity receptor-ligand interactions: chelator-lipid liposomes engrafted with recombinant CD4 bind to cells expressing MHC class II. Immunol. Cell Biol. 79: 274-284.
46. McNamara, N., M. Gallup, A. Sucher, I. Maltseva, D. McKemy, and C. Basbaum. 2006. AsialoGM1 and TLR5 cooperate in flagellin-induced nucleotide signaling to activate Erk1/2. Am. J. Respir. Cell Mol. Biol. 34: 653-660.
47. Heath, W. R., G. T. Belz, G. M. Behrens, C. M. Smith, S. P. Forehan, I. A. Parish, G. M. Davey, N. S. Wilson, F. R. Carbone, and J. A. Villadangos. 2004. Cross-presentation, dendritic cell subsets, and the generation of immunity to cellular antigens. Immunol. Rev. 199: 9-26.
48. Steinman, R. M., and J. Banchereau. 2007. Taking dendritic cells into medicine. Nature 449: 419-426.