Intranodal vaccination with naked antigen-encoding RNA elicits potent prophylactic and therapeutic antitumoral immunity

Cancer Research

Volumn 70, Issue 22, 2010, Pages 9031-9040

  Kreiter, Sebastian ^a   Selmi, Abderraouf ^a   Diken, Mustafa ^a   Koslowski, Michael ^a   Britten, Cedrik M ^a   Huber, Christoph ^a   Türeci, Özlem ^a   Sahin, Ugur ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN ENCODING RNA; PLASMID VECTOR; RNA VACCINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER IMMUNIZATION; CANCER PREVENTION; CANCER SURVIVAL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELLULAR IMMUNITY; CONTROLLED STUDY; DENDRITIC CELL; IMMUNE RESPONSE; IN VITRO GENE TRANSFER; MEMORY T LYMPHOCYTE; MOUSE; NEOPLASM; NONHUMAN; PLASMID; PRIORITY JOURNAL; TH1 CELL; TUMOR IMMUNITY;

ANIMALS; ANTIGENS; CANCER VACCINES; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CELL PROLIFERATION; CYTOTOXICITY, IMMUNOLOGIC; DENDRITIC CELLS; FLOW CYTOMETRY; IMMUNIZATION; LYMPH NODES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NEOPLASMS, EXPERIMENTAL; RNA; SURVIVAL ANALYSIS;

EID: 78549283854     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-0699     Document Type: Article

References (33)

1. Weide B, Garbe C, Rammensee HG, Pascolo S. Plasmid DNA- and messenger RNA-based anti-cancer vaccination. Immunol Lett 2008;115:33-42.
2. Pascolo S. Messenger RNA-based vaccines. Expert Opin Biol Ther 2004;4:1285-94.
3. Gilboa E, Vieweg J. Cancer immunotherapy with mRNA-transfected dendritic cells. Immunol Rev 2004;199:251-63.
4. Michiels A, Tuyaerts S, Bonehill A, et al. Electroporation of immature and mature dendritic cells: implications for dendritic cell-based vaccines. Gene Ther 2005;12:772-82.
5. Carralot JP, Probst J, Hoerr I, et al. Polarization of immunity induced by direct injection of naked sequence-stabilized mRNA vaccines. Cell Mol Life Sci 2004;61:2418-24.
6. Scheel B, Aulwurm S, Probst J, et al. Therapeutic anti-tumor immunity triggered by injections of immunostimulating single-stranded RNA. Eur J Immunol 2006;36:2807-16.
7. Weide B, Carralot JP, Reese A, et al. Results of the first phase I/II clinical vaccination trial with direct injection of mRNA. J Immunother 2008;31:180-8.
8. Weide B, Pascolo S, Scheel B, et al. Direct injection of protamine-protected mRNA: results of a phase 1/2 vaccination trial in metastatic melanoma patients. J Immunother 2009;32:498-507.
9. Holtkamp S, Kreiter S, Selmi A, et al. Modification of antigen encoding RNA increases stability, translational efficacy and T-cell stimulatory capacity of dendritic cells. Blood 2006;108:4009-17.
10. Kreiter S, Selmi A, Diken M, et al. Increased antigen presentation efficiency by coupling antigens to MHC class I trafficking signals. J Immunol 2008;180:309-18.
11. Kirberg J, Baron A, Jakob S, Rolink A, Karjalainen K, von Boehmer H. Thymic selection of CD8+ single positive cells with a class II major histocompatibility complex-restricted receptor. J Exp Med 1994;180:25-34.
12. Hernandez J, Aung S, Redmond WL, Sherman LA. Phenotypic and functional analysis of CD8(+) T cells undergoing peripheral deletion in response to cross-presentation of self-antigen. J Exp Med 2001;194:707-17.
13. Lutz MB, Kukutsch N, Ogilvie AL, et al. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods 1999;223:77-92.
14. Naik SH, Proietto AI, Wilson NS, et al. Cutting edge: generation of splenic CD8+ and CD8- dendritic cell equivalents in Fms-like tyrosine kinase 3 ligand bone marrow cultures. J Immunol 2005;174:6592-7.
15. Kuhn AN, Diken M, Kreiter S, et al. Phosphorothioate cap analogs increase stability and translational efficiency of RNA vaccines in immature dendritic cells and induce superior immune responses in vivo. Gene Ther 2010;17:961-71.
16. Kreiter S, Konrad T, Sester M, Huber C, Tureci O, Sahin U. Simultaneous ex vivo quantification of antigen-specific CD4 and CD8(+) T cell responses using in vitro transcribed RNA. Cancer Immunol Immunother 2007;56:1577-87.
17. Herr W, Linn B, Leister N, Wandel E, Meyer zum Buschenfelde KH, Wolfel T. The use of computer-assisted video image analysis for the quantification of CD8+ T lymphocytes producing tumor necrosis factor alpha spots in response to peptide antigens. J Immunol Methods 1997;203:141-52.
18. Koslowski M, Sahin U, Huber C, Tureci O. The human X chromosome is enriched for germline genes expressed in premeiotic germ cells of both sexes. Hum Mol Genet 2006;15:2392-9.
19. Bins AD, Jorritsma A, Wolkers MC, et al. A rapid and potent DNA vaccination strategy defined by in vivo monitoring of antigen expression. Nat Med 2005;11:899-904.
20. Heinzerling L, Basch V, Maloy K, et al. Critical role for DNA vaccination frequency in induction of antigen-specific cytotoxic responses. Vaccine 2006;24:1389-94.
21. Smith KA, Tam VL, Wong RM, et al. Enhancing DNA vaccination by sequential injection of lymph nodes with plasmid vectors and peptides. Vaccine 2009;27:2603-15.
22. Banchereau J, Briere F, Caux C, et al. Immunobiology of dendritic cells. Annu Rev Immunol 2000;18:767-811.
23. Boczkowski D, Nair SK, Snyder D, Gilboa E. Dendritic cells pulsed with RNA are potent antigen-presenting cells in vitro and in vivo. J Exp Med 1996;184:465-72.
24. Azuma M, Ito D, Yagita H, et al. B70 antigen is a second ligand for CTLA-4 and CD28. Nature 1993;366:76-9.
25. Curtsinger JM, Schmidt CS, Mondino A, et al. Inflammatory cytokines provide a third signal for activation of naive CD4(+) and CD8 (+) T cells. J Immunol 1999;162:3256-62.
26. Rochman I, Paul WE, Ben Sasson SZ. IL-6 increases primed cell expansion and survival. J Immunol 2005;174:4761-7.
27. Sepulveda H, Cerwenka A, Morgan T, Dutton RW. CD28, IL-2-independent costimulatory pathways for CD8 T lymphocyte activation. J Immunol 1999;163:1133-42.
28. Chen ZM, O'Shaughnessy MJ, Gramaglia I, et al. IL-10 and TGF-β induce alloreactive CD4+CD25- T cells to acquire regulatory cell function. Blood 2003;101:5076-83.
29. Tedla N, Wang HW, Mcneil HP, et al. Regulation of T lymphocyte trafficking into lymph nodes during an immune response by the chemokines macrophage inflammatory protein (MIP)-1 α and MIP-1 β. J Immunol 1998;161:5663-72.
30. Castellino F, Huang AY, Altan-Bonnet G, Stoll S, Scheinecker C, Germain RN. Chemokines enhance immunity by guiding naive CD8 (+) T cells to sites of CD4 T cell-dendritic cell interaction. Nature 2006;440:890-5.
31. Gustafsson K, Ingelsten M, Bergqvist L, Nystrom J, Andersson B, Karlsson-Parra A. Recruitment and activation of natural killer cells in vitro by a human dendritic cell vaccine. Cancer Res 2008;68:5965-71.
32. Diebold SS, Kaisho T, Hemmi H, Akira S, Sousa CRE. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 2004;303:1529-31.
33. Kariko K, Ni H, Capodici J, Lamphier M, Weissman D. mRNA is an endogenous ligand for Toll-like receptor 3. J Biol Chem 2004;279:12542-50.