Induction of CD8+ T-cell responses against subunit antigens by the novel cationic liposomal CAF09 adjuvant

Vaccine

Volumn 32, Issue 31, 2014, Pages 3927-3935

  Korsholm, Karen Smith ^a   Hansen, Jon ^a   Karlsen, Kasper ^a   Filskov, Jonathan ^a,b   Mikkelsen, Marianne ^a,c   Lindenstrøm, Thomas ^a   Schmidt, Signe Tandrup ^a,b   Andersen, Peter ^a   Christensen, Dennis ^a  

^a STATENS SERUM INSTITUT   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c GENTOFTE UNIVERSITY HOSPITAL   (Denmark)

Author keywords

Adjuvant; CAF09; Cationic liposome; CTL; Vaccine

Indexed keywords

ADJUVANT; ALUMINUM; ALUMINUM HYDROXIDE; ANTIGEN; CANCER VACCINE; CATIONIC ADJUVANT FORMULATION 01; CATIONIC ADJUVANT FORMULATION 05; CATIONIC ADJUVANT FORMULATION 09; CD44V ANTIGEN; DIMETHYLDIOCTADECYLAMMONIUM BROMIDE; GAG PROTEIN; GAMMA INTERFERON; GLYCEROL; INTERLEUKIN 2; LIPOSOME; MIFAMURTIDE; MONOMYCOLOYL GLYCEROL 1; MONTANIDE ISA720; OVALBUMIN; PHOSPHORYL LIPID A; POLYINOSINIC POLYCYTIDYLIC ACID; PROTEIN E7; TOLL LIKE RECEPTOR 3; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CATION; IMMUNOLOGICAL ADJUVANT; ONCOGENE PROTEIN E7, HUMAN PAPILLOMAVIRUS TYPE 16;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; CANCER INHIBITION; CANCER PREVENTION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXICITY; DRUG EFFICACY; DRUG POTENCY; EFFECTOR CELL; EX VIVO STUDY; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN PAPILLOMAVIRUS TYPE 16; IMMUNE RESPONSE; IMMUNIZATION; IN VITRO STUDY; IN VIVO STUDY; MEMORY CELL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN TUMOR; T LYMPHOCYTE SUBPOPULATION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELLULAR IMMUNITY; CYTOTOXIC T LYMPHOCYTE; DBA MOUSE; IMMUNOLOGY; VIROLOGY;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIGENS; CATIONS; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; IMMUNITY, CELLULAR; LIPOSOMES; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, INBRED DBA; PAPILLOMAVIRUS E7 PROTEINS; POLY I-C; SKIN NEOPLASMS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84901985838     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2014.05.050     Document Type: Article

References (39)

1. Ackerman A.L., Cresswell P. Cellular mechanisms governing cross-presentation of exogenous antigens. Nat Immunol 2004, 5:678-684.
2. Buchbinder S.P., Mehrotra D.V., Duerr A., Fitzgerald D.W., Mogg R., Li D., et al. Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the Step Study): a double-blind, randomised, placebo-controlled, test-of-concept trial. Lancet 2008, 372:1881-1893.
3. Le Bon A., Etchart N., Rossmann C., Ashton M., Hou S., Gewert D., et al. Cross-priming of CD8+ T cells stimulated by virus-induced type I interferon. Nat Immunol 2003, 4:1009-1015.
4. Bevan M.J. Cross-priming for a secondary cytotoxic response to minor H antigens with H-2 congenic cells which do not cross-react in the cytotoxic assay. J Exp Med 1976, 143:1283-1288.
5. Lorenzi S., Mattei F., Sistigu A., Bracci L., Spadaro F., Sanchez M., et al. Type I IFNs control antigen retention and survival of CD8α+ dendritic cells after uptake of tumor apoptotic cells leading to cross-priming. J Immunol 2011, 186:5142-5150.
6. Spadaro F., Lapenta C., Donati S., Abalsamo L., Barnaba V., Belardelli F., et al. IFN-α enhances cross-presentation in human dendritic cells by modulating antigen survival, endocytic routing, and processing. Blood 2012, 119:1407-1417.
7. Foged C., Hansen J., Agger E.M. License to kill: Formulation requirements for optimal priming of CD8(+) CTL responses with particulate vaccine delivery systems. Eur J Pharm Sci 2012, 45:482-491. (official journal of the European Federation for Pharmaceutical Sciences).
8. Fujimoto K., Karuppuchamy T., Takemura N., Shimohigoshi M., Machida T., Haseda Y., et al. A new subset of CD103+CD8alpha+ dendritic cells in the small intestine expresses TLR3, TLR7, and TLR9 and induces Th1 response and CTL activity. J Immunol 2011, 186:6287-6295.
9. Edwards A.D., Diebold S.S., Slack E.M.C., Tomizawa H., Hemmi H., Kaisho T., et al. Toll-like receptor expression in murine DC subsets: lack of TLR7 expression by CD8α+ DC correlates with unresponsiveness to imidazoquinolines. Eur J Immunol 2003, 33:827-833.
10. Hasan M., Ruksznis C., Wang Y., Leifer C.A. Antimicrobial peptides inhibit polyinosinic-polycytidylic acid-induced immune responses. J Immunol 2011, 187:5653-5659.
11. Zaks K., Jordan M., Guth A., Sellins K., Kedl R., Izzo A., et al. Efficient immunization and cross-priming by vaccine adjuvants containing TLR3 or TLR9 agonists complexed to cationic liposomes. J Immunol 2006, 176:7335-7345.
12. Zhu Q., Egelston C., Gagnon S., Sui Y., Belyakov I.M., Klinman D.M., et al. Using 3 TLR ligands as a combination adjuvant induces qualitative changes in T cell responses needed for antiviral protection in mice. J Clin Invest 2010, 120:607-616.
13. Hansen J., Lindenstrom T., Lindberg-Levin J., Aagaard C., Andersen P., Agger E.M. CAF05: cationic liposomes that incorporate synthetic cord factor and poly(I:C) induce CTL immunity and reduce tumor burden in mice. Cancer Immunol Immunother 2012, 61:893-903.
14. Nordly P., Rose F., Christensen D., Nielsen H.M., Andersen P., Agger E.M., et al. Immunity by formulation design: induction of high CD8+ T-cell responses by poly(I:C) incorporated into the CAF01 adjuvant via a double emulsion method. J Control Release 2011, 150:307-317.
15. Andersen C.S., Agger E.M., Rosenkrands I., Gomes J.M., Bhowruth V., Gibson K.J., et al. A simple mycobacterial monomycolated glycerol lipid has potent immunostimulatory activity. J Immunol 2009, 182:424-432.
16. Andersen C.A., Rosenkrands I., Olsen A.W., Nordly P., Christensen D., Lang R., et al. Novel generation mycobacterial adjuvant based on liposome-encapsulated monomycoloyl glycerol from Mycobacterium bovis bacillus Calmette-Guerin. J Immunol 2009, 183:2294-2302.
17. Bhowruth V., Minnikin D.E., Agger E.M., Andersen P., Bramwell V.W., Perrie Y., et al. Adjuvant properties of a simplified C32 monomycolyl glycerol analogue. Bioorg Med Chem Lett 2009, 19:2029-2032.
18. Nordly P., Korsholm K.S., Pedersen E.A., Khilji T.S., Franzyk H., Jorgensen L., et al. Incorporation of a synthetic mycobacterial monomycoloyl glycerol analogue stabilizes dimethyldioctadecylammonium liposomes and potentiates their adjuvant effect in vivo. Eur J Pharm Biopharm 2011, 77:89-98.
19. Martin-Bertelsen B., Korsholm K.S., Rose F., Nordly P., Franzyk H., Andersen P., et al. The supramolecular structure is decisive for the immunostimulatory properties of synthetic analogues of a mycobacterial lipid in vitro. RSC Adv 2013, 3:20673-20683.
20. Davidsen J., Rosenkrands I., Christensen D., Vangala A., Kirby D., Perrie Y., et al. Characterization of cationic liposomes based on dimethyldioctadecylammonium and synthetic cord factor from M. tuberculosis (trehalose 6,6'-dibehenate)-a novel adjuvant inducing both strong CMI and antibody responses. Biochim Biophys Acta 2005, 1718:22-31.
21. Korsholm K.S., Karlsson I., Tang S.T., Brandt L., Agger E.M., Aagaard C., et al. Broadening of the T-cell repertoire to HIV-1 Gag p24 by vaccination of HLA-A2/DR transgenic mice with overlapping peptides in the CAF05 adjuvant. PLoS One 2013, 8:e63575.
22. Aagaard C., Hoang T., Dietrich J., Cardona P.J., Izzo A., Dolganov G., et al. A multistage tuberculosis vaccine that confers efficient protection before and after exposure. Nat Med 2011, 17:189-194.
23. Skjot R.L., Brock I., Arend S.M., Munk M.E., Theisen M., Ottenhoff T.H., et al. Epitope mapping of the immunodominant antigen TB10.4 and the two homologous proteins TB10.3 and TB12.9, which constitute a subfamily of the esat-6 gene family. Infect Immun 2002, 70:5446-5453.
24. Karlsson I., Brandt L., Vinner L., Kromann I., Andreasen L.V., Andersen P., et al. Adjuvanted HLA-supertype restricted subdominant peptides induce new T-cell immunity during untreated HIV-1-infection. Clin Immunol 2013, 146:120-130.
25. Seder R.A., Darrah P.A., Roederer M. T-cell quality in memory and protection: implications for vaccine design. Nat Rev Immunol 2008, 8:247-258.
26. MacLeod M.K., McKee A.S., David A., Wang J., Mason R., Kappler J.W., et al. Vaccine adjuvants aluminum and monophosphoryl lipid A provide distinct signals to generate protective cytotoxic memory CD8 T cells. Proc Nat Acad Sci USA 2011, 108:7914-7919.
27. Heinemann L., Woodfield L., Amer M., Hibma M. Effective induction of type 1 helper IgG2a and cytotoxic T-cell responses in mice following immunization with human papillomavirus type 16 E2 in MF59. Viral Immunol 2008, 21:225-233.
28. Holten-Andersen L., Doherty T.M., Korsholm K.S., Andersen P. Combination of the cationic surfactant dimethyl dioctadecyl ammonium bromide and synthetic mycobacterial cord factor as an efficient adjuvant for tuberculosis subunit vaccines. Infect Immun 2004, 72:1608-1617.
29. Schoenen H., Bodendorfer B., Hitchens K., Manzanero S., Werninghaus K., Nimmerjahn F., et al. Cutting edge: Mincle is essential for recognition and adjuvanticity of the mycobacterial cord factor and its synthetic analog trehalose-dibehenate. J Immunol 2010, 184:2756-2760.
30. Desel C., Werninghaus K., Ritter M., Jozefowski K., Wenzel J., Russkamp N., et al. The Mincle-Activating Adjuvant TDB Induces MyD88-Dependent Th1 and Th17 Responses through IL-1R Signaling. PLoS One 2013, 8:e53531.
31. Shen X., Wong S.B., Buck C.B., Zhang J., Siliciano R.F. Direct priming and cross-priming contribute differentially to the induction of CD8+ CTL following exposure to vaccinia virus via different routes. J Immunol 2002, 169:4222-4229.
32. Berencsi K., Rando R.F., deTaisne C., Paoletti E., Plotkin S.A., Gonczol E. Murine cytotoxic T cell response specific for human cytomegalovirus glycoprotein B (gB) induced by adenovirus and vaccinia virus recombinants expressing gB. J Gen Virol 1993, 74(Pt 11):2507-2512.
33. Barouch D.H., McKay P.F., Sumida S.M., Santra S., Jackson S.S., Gorgone D.A., et al. Plasmid chemokines and colony-stimulating factors enhance the immunogenicity of DNA priming-viral vector boosting human immunodeficiency virus type 1 vaccines. J Virol 2003, 77:8729-8735.
34. Elvang T., Christensen J.P., Billeskov R., Thi Kim Thanh Hoang T., Holst P., Thomsen A.R., et al. CD4 and CD8T cell responses to the M. tuberculosis Ag85B-TB10.4 promoted by adjuvanted subunit, adenovector or heterologous prime boost vaccination. PLoS One 2009, 4:e5139.
35. Johansen P., Häffner A.C., Koch F., Zepter K., Erdmann I., Maloy K., et al. Direct intralymphatic injection of peptide vaccines enhances immunogenicity. Eur J Immunol 2005, 35:568-574.
36. Johansen P., Mohanan D., Martinez-Gomez J.M., Kundig T.M., Gander B. Lympho-geographical concepts in vaccine delivery. J Control Release 2010, 148:56-62.
37. Liu Z., Noh H.S., Chen J., Kim J.H., Falo L.D., You Z. Potent tumor-specific protection ignited by adoptively transferred CD4+ T cells. J Immunol 2008, 181:4363-4370.
38. Liu C., Lou Y., Lizee G., Qin H., Liu S., Rabinovich B., et al. Plasmacytoid dendritic cells induce NK cell-dependent, tumor antigen-specific T cell cross-priming and tumor regression in mice. J Clin Invest 2008, 118:1165-1175.
39. Lindenstrøm T., Aagaard C., Christensen D., Agger E.M., Andersen P. High-frequency vaccine-promoted CD8 T cells specific for an epitope naturally processed during infection with M. tuberculosis do not confer protection. EJI 2014, 10.1002/eji.201344358.