Messenger RNA-electroporated dendritic cells presenting MAGE-A3 simultaneously in HLA class I and class II molecules

Journal of Immunology

Volumn 172, Issue 11, 2004, Pages 6649-6657

  Bonehill, Aude ^a   Heirman, Carlo ^a   Tuyaerts, Sandra ^a   Michiels, Annelies ^a   Breckpot, Karine ^a   Brasseur, Francis ^b   Zhang, Yi ^b   Van Der Bruggen, Pierre ^b   Thielemans, Kris ^a  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b LUDWIG INSTITUTE FOR CANCER RESEARCH   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER VACCINE; CELL PROTEIN; CHLOROQUINE; EPITOPE; GREEN FLUORESCENT PROTEIN; HLA ANTIGEN CLASS 1; HLA ANTIGEN CLASS 2; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MELANOMA ANTIGEN A3; MESSENGER RNA; TUMOR ANTIGEN; UNCLASSIFIED DRUG;

ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; CANCER IMMUNOTHERAPY; CELL MATURATION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; DNA MODIFICATION; ELECTROPORATION; HELPER CELL; HLA SYSTEM; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION;

EID: 2442689202     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.172.11.6649     Document Type: Article

References (68)

1. Rosenberg, S. A., B. S. Packard, P. M. Aebersold, D. Solomon, S. L. Topalian, S. T. Toy, P. Simon, M. T. Lotze, J. C. Yang, C. A. Seipp, et al. 1988. Use of tumor-infiltrating lymphocytes and interleukin-2 in the immunotherapy of patients with metastatic melanoma: a preliminary report. N. Engl. J. Med. 319:1676.
2. Dudley, M. E., J. R. Wunderlich, P. F. Robbins, J. C. Yang, P. Hwu, D. J. Schwartzentruber, S. L. Topalian, R. Sherry, N. P. Restifo, A. M. Hubicki, et al. 2002. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes, Science 298:850.
3. Rosenberg, S. A., J. C. Yang, D. J. Schwartzentruber, P. Hwu, F. M. Marincola, S. L. Topalian, N. P. Restifo, M. E. Dudley, S. L. Schwarz, P. J. Spiess, et al. 1998. Immunologic and therapeutic evaluation of a synthetic peptide vaccine for the treatment of patients with metastatic melanoma. Nat. Med. 4:321.
4. Nestle, F. O., S. Alijagic, M. Gilliet, Y. Sun, S. Grabbe, R. Dummer, G. Burg, and D. Schadendorf. 1998. Vaccination of melanoma patients with peptide- or tumor lysate-pulsed dendritic cells. Nat. Med. 4:328.
5. Marchand, M., N. van Baren, P. Weynants, V. Brichard, B. Dreno, M. H. Tessier, E. Rankin, G. Parmiani, F. Arienti, Y. Humblet, et al. 1999. Tumor regressions observed in patients with metastatic melanoma treated with an antigenic peptide encoded by gene MAGE-3 and presented by HLA-A1. Int. J. Cancer. 80:219.
6. + T cell responses in antitumor immunity. Curr. Opin. Immunol. 10:588.
7. Ossendorp, F., E. Mengede, M. Camps, R. Filius, and C. J. Melief. 1998, Specific T helper cell requirement for optimal induction of cytotoxic T lymphocytes against major histocompatibility complex class II negative tumors. J. Exp. Med. 187:693.
8. + T cells in the antitumor immune response. J. Exp. Med. 188:2357.
9. + T-helper and a T-killer cell. Nature 393:474.
10. Bennett, S. R., F. R. Carbone, F. Karamalis, R. A. Flavell, J. F. Miller, and W. R. Heath. 1998. Help for cytotoxic-T-cell responses is mediated by CD40 signalling. Nature 393:478.
11. Schoenberger, S. P., R. E. Toes, E. I. van der Voort, R. Offringa, and C. J. Melief. 1998. T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature 393:480.
12. + T cells have a major "post-licensing" role in CTL mediated anti-tumor immunity. J. Immunol. 165:6047.
13. + T cell-mediated tumor rejection involves inhibition of angiogenesis that is dependent on IFNγ receptor expression by nonhematopoietic cells. Immunity 12:677.
14. + T cell memory. Science 297:2060.
15. + T lymphocytes. Nature 421:852.
16. + T cell memory. Science 300:337.
17. Sun, J. C., and M. J. Bevan. 2003. Defective CD8 T cell memory following acute infection without CD4 T cell help. Science 300:339.
18. Grakoui, A., N. H. Shoukry, D. J. Woollard, J. H. Han, H. L. Hanson, J. Ghrayeb, K. K. Murthy, C. M. Rice, and C. M. Walker. 2003. HCV persistence and immune evasion in the absence of memory T cell help. Science 302:659.
19. + T cells recognize nonmutated HLA-DR-restricted tyrosinase epitopes. J. Exp. Med. 183:1965.
20. Li, K., M. Adibzadeh, T. Halder, H. Kalbacher, S. Heinzel, C. Muller, J. Zeuthen, and G. Pawelec. 1998. Tumour-specific MHC-class-II-restricted responses after in vitro sensitization to synthetic peptides corresponding to gp100 and Annexin II eluted from melanoma cells. Cancer Immunol. Immunother. 47:32.
21. + T lymphocytes. J. Exp. Med. 189:767.
22. + cytotoxic T cells in association with histocompatibility leukocyte antigen DR11. J. Exp. Med. 189:871.
23. + cytolytic T lymphocytes. Cancer Res. 60:6272.
24. + T cells. Proc. Natl. Acad. Sci. USA 97:400.
25. Touloukian, C. E., W. W. Leitner, S. L. Topalian, Y. F. Li, P. F. Robbins, S. A. Rosenberg, and N. P. Restifo. 2000. Identification of a MHC class II-restricted human gp100 epitope using DR4-IE transgenic mice. J. Immunol. 164:3535.
26. + T cells. Eur. J. Immunol. 31:1910.
27. + T cells that were isolated from a melanoma patient vaccinated with a MAGE-3 protein. J. Immunol. 171: 219.
28. Banchereau, J., F. Briere, C. Caux, J. Davoust, S. Lebecque, Y. J. Liu, B. Pulendran, and K. Palucka. 2000. Immunobiology of dendritic cells. Annu. Rev. Immunol. 18:767.
29. Fong, L., and E. G. Engleman. 2000. Dendritic cells in cancer immunotherapy. Annu. Rev. Immunol. 18:245.
30. Steinman, R. M., and M. Dhodapkar. 2001. Active immunization against cancer with dendritic cells: the near future. Int. J. Cancer. 94:459.
31. Guermonprez, P., J. Valladeau, L. Zitvogel, C. Thery, and S. Amigorena. 2002. Antigen presentation and T cell stimulation by dendritic cells. Annu. Rev. Immunol. 20:621.
32. Jager, E., Y. T. Chen, J. W. Drijfhout, J. Karbach, M. Ringhoffer, D. Jager, M. Arand, H. Wada, Y. Noguchi, E. Stockert, et al. 1998. Simultaneous humoral and cellular immune response against cancer-testis antigen NY-ESO-1: definition of human histocompatibility leukocyte antigen (HLA)-A2-binding peptide epitopes. J. Exp. Med. 187:265.
33. + T lymphocytes of patients with NY-ESO-1-expressing melanoma. J. Exp. Med. 191:625.
34. Schuler-Thurner, B., E. S. Schultz, T. G. Berger, G. Weinlich, S. Ebner, P. Woerl, A. Bender, B. Feuerstein, P. O. Fritsch, N. Romani, et al. 2002. Rapid induction of tumor-specific type 1 T helper cells in metastatic melanoma patients by vaccination with mature, cryopreserved, peptide-loaded monocyte-derived dendritic cells. J. Exp. Med. 195:1279.
35. Geuze, H. J. 1998. The role of endosomes and lysosomes in MHC class II functioning. Immunol. Today 19:282.
36. Hiltbold, E. M., and P. A. Roche. 2002. Trafficking of MHC class 11 molecules in the late secretory pathway. Curr. Opin. Immunol. 14:30.
37. Sanderson, S., K. Frauwirth, and N. Shastri. 1995. Expression of endogenous peptide-major histocompatibility complex class II complexes derived from invariant chain-antigen fusion proteins. Proc. Natl. Acad. Sci. USA 92:7217.
38. + cytotoxic T lymphocytes: a novel approach to vaccine design. J. Virol. 72:2246.
39. Diebold, S. S., M. Cotten, N. Koch, and M. Zenke. 2001. MHC class II presentation of endogenously expressed antigens by transfected dendritic cells. Gene Ther. 8:487.
40. Rowell, J. F., A. L. Ruff, F. G. Guarnieri, K. Staveley-O'Carroll, X. Lin, J. Tang, J. T. August, and R. F. Siliciano. 1995. Lysosome-associated membrane protein-1-mediated targeting of the HIV-1 envelope protein to an endosomal/lysosomal compartment enhances its presentation to MHC class II-restricted T cells. J. Immunol. 155:1818.
41. Wu, T. C., F. G. Guarnieri, K. F. Staveley-O'Carroll, R. P. Viscidi, H. I. Levitsky, L. Hedrick, K. R. Cho, J. T. August, and D. M. Pardoll. 1995. Engineering an intracellular pathway for major histocompatibility complex class II presentation of antigens. Proc. Natl. Acad. Sci. USA 92:11671.
42. + T cells. J. Immunol. 166:5250.
43. Van Tendeloo, V. F., P. Ponsaerts, F. Lardon, G. Nijs, M. Lenjou, C. Van Broeckhoven, D. R. Van Bockstaele, and Z. N. Berneman. 2001. Highly efficient gene delivery by mRNA electroporation in human hematopoietic cells: superiority to lipofection and passive pulsing of mRNA and to electroporation of plasmid cDNA for tumor antigen loading of dendritic cells. Blood 98:49.
44. Van Meirvenne, S., L. Straetman, C. Heirman, M. Dullaers, C. De Greef, V. Van Tendeloo, and K. Thielemans. 2002. Efficient genetic modification of murine dendritic cells by electroporation with mRNA. Cancer Gene Ther. 9:787.
45. Tuyaerts, S., A. Michiels, J. Corthals, A. Bonehill, C. Heirman, C. D. Greef, S. M. Noppe, and K. Thielemans. 2003. Induction of influenza matrix protein 1 and melanA-specific T lymphocytes in vitro using mRNA-electroporated dendritic cells. Cancer Gene Ther. 10:696.
46. Bonehill, A., C. Heirman, S. Tuyaerts, A. Michiels, Y. Zhang, P. Van Der Bruggen, and K. Thielemans. 2003. Efficient presentation of known HLA class II-restricted MAGE-A3 epitopes by dendritic cells electroporated with messenger RNA encoding an invariant chain with genetic exchange of class II-associated invariant chain peptide. Cancer Res. 63:5587.
47. Nair, S. K., D. Boczkowski, M. Morse, R. I. Cumming, H. K. Lyerly, and E. Gilboa. 1998. Induction of primary carcinoembryonic antigen (CEA)-specific cytotoxic T lymphocytes in vitro using human dendritic cells transfected with RNA. Nat. Biotechnol. 16:364.
48. Heiser, A., P. Dahm, D. R. Yancey, M. A. Maurice, D. Boczkowski, S. K. Nair, E. Gilboa, and J. Vieweg. 2000. Human dendritic cells transfected with RNA encoding prostate-specific antigen stimulate prostate-specific CTL responses in vitro. J. Immunol. 164:5508.
49. Heiser, A., D. Coleman, J. Dannull, D. Yancey, M. A. Maurice, C. D. Lallas, P. Dahm, D. Niedzwiecki, E. Gilboa, and J. Vieweg. 2002. Autologous dendritic cells transfected with prostate-specific antigen RNA stimulate CTL responses against metastatic prostate tumors. J. Clin. Invest. 109:409.
50. Saeboe-Larssen, S., E. Fossberg, and G. Gaudernack. 2002. mRNA-based electrotransfection of human dendritic cells and induction of cytotoxic T lymphocyte responses against the telomerase catalytic subunit (hTERT). J. Immunol. Methods 259:191.
51. + T cells using dendritic cells transfected with RNA encoding a chimeric gene product. Cancer Res. 62:5041.
52. Mitchell, D. A., and S. K. Nair. 2000. RNA transfected dendritic cells as cancer vaccines. Curr. Opin. Mol. Ther. 2:176.
53. Mitchell, D. A., and S. K. Nair. 2000. RNA-transfected dendritic cells in cancer immunotherapy. J. Clin. Invest. 106:1065.
54. de Saint-Vis, B., J. Vincent, S. Vandenabeele, B. Vanbervliet, J.-J. Pin, S. Aït-Yahia, S. Patel, M.-G. Mattei, J. Banchereau, S. Zurawski, et al. 1998. A novel lysosome-associated membrane glycoprotein, DC-LAMP, induced upon DC maturation, is transiently expressed in MHC class II compartment. Immunity 9:325.
55. Boczkowski, D., S. K. Nair, D. Snyder, and E. Gilboa. 1996. Dendritic cells pulsed with RNA are potent antigen-presenting cells in vitro and in vivo. J. Exp. Med. 184:465.
56. Tuyaerts, S., S. M. Noppe, J. Corthals, K. Breckpot, C. Heirman, C. De Greef, I. Van Riet, and K. Thielemans. 2002. Generation of large numbers of dendritic cells in a closed system using cell factories. J. Immunol. Methods 264:135.
57. Gaugler, B., B. Van den Eynde, P. van der Bruggen, P. Romero, J. J. Gaforio, E. De Plaen, B. Lethe, F. Brasseur, and T. Boon. 1994. Human gene MAGE-3 codes for an antigen recognized on a melanoma by autologous cytolytic T lymphocytes. J. Exp. Med. 179:921.
58. Pieters, J., O. Bakke, and B. Dobberstein. 1993. The MHC class II-associated invariant chain contains two endosomal targeting signals within its cytoplasmic tail. J. Cell Sci. 106:831.
59. Odorizzi, C. G., I. S. Trowbridge, L. Xue, C. R. Hopkins, C. D. Davis, and J. F. Collawn. 1994. Sorting signals in the MHC class II invariant chain cytoplasmic tail and transmembrane region determine trafficking to an endocytic processing compartment. J. Cell Biol. 126:317.
60. Breckpot, K., M. Dullaers, A. Bonehill, S. Van Meirvenne, C. Heirman, C. De Greef, P. Van Der Bruggen, and K. Thielemans. 2003. Lentivirally transduced dendritic cells as a tool for cancer immunotherapy. J. Gene Med. 5:654.
61. Breitfeld, P. P., J. E. Casanova, W. C. McKinnon, and K. E. Mostov. 1990. Deletions in the cytoplasmic domain of the polymeric immunoglobulin receptor differentially affect endocytotic rate and postendocytotic traffic. J. Biol. Chem. 265:13750.
62. Chen, W. J., J. L. Goldstein, and M. S. Brown. 1990. NPXY, a sequence often found in cytoplasmic tails, is required for coated pit-mediated internalization of the low density lipoprotein receptor. J. Biol. Chem. 265:3116.
63. Williams, M. A., and M. Fukuda. 1990. Accumulation of membrane glycoproteins in lysosomes requires a tyrosine residue at a particular position in the cytoplasmic tail. J. Cell Biol. 111:955.
64. Guarnieri, F. G., L. M. Arterbum, M. B. Penno, Y. Cha, and J. T. August. 1993. The motif Tyr-X-X-hydrophobic residue mediates lysosomal membrane targeting of lysosome-associated membrane protein 1. J. Biol. Chem. 268:1941.
65. Yewdell, J. W., L. C. Anton, and J. R. Bennink. 1996. Defective ribosomal products (DRiPs): a major source of antigenic peptides for MHC class I molecules? J. Immunol. 157:1823.
66. Gromme, M., F. G. Uytdehaag, H. Janssen, J. Calafat, R. S. van Binnendijk, M. J. Kenter, A. Tulp, D. Verwoerd, and J. Neefjes. 1999. Recycling MHC class I molecules and endosomal peptide loading. Proc. Natl. Acad. Sci. USA 96:10326.
67. Kleijmeer, M. J., J. M. Escola, F. G. UytdeHaag, E. Jakobson, J. M. Griffith, A. D. Osterhaus, W. Stoorvogel, C. J. Melief, C. Rabouille, and H. J. Geuze. 2001. Antigen loading of MHC class I molecules in the endocytic tract. Traffic 2:124.
68. Yewdell, J. W., E. Reits, and J. Neefjes. 2003. Making sense of mass destruction: quantitating MHC class I antigen presentation. Nat. Rev. Immunol. 3:952.