Vaccination with mRNAs encoding tumor-associated antigens and granulocyte-macrophage colony-stimulating factor efficiently primes CTL responses, but is insufficient to overcome tolerance to a model tumor/self antigen

Cancer Immunology, Immunotherapy

Volumn 55, Issue 6, 2006, Pages 672-683

  Hess, Paul R ^a,b   Boczkowski, David ^b   Nair, Smita K ^b   Snyder, David ^b   Gilboa, Eli ^b  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

CTL; GM CSF; mRNA vaccine; SV40 large T antigen; Tolerance

Indexed keywords

1,2 DIOLEOYL 3 TRIMETHYLAMMONIOPROPANE; B7 ANTIGEN; CANCER VACCINE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 2; LIPOSOME; MESSENGER RNA; OVALBUMIN; TUMOR ANTIGEN; VIRUS LARGE T ANTIGEN;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CANCER MODEL; CELL ACTIVITY; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DRUG CYTOTOXICITY; DRUG POTENTIATION; ENCAPSULATION; GENE EXPRESSION; GENE TARGETING; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOLOGICAL TOLERANCE; IMMUNOREACTIVITY; MALE; MOUSE; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; NONVIRAL GENE THERAPY; PRIORITY JOURNAL; PROSTATE ADENOCARCINOMA; SPLEEN CELL; TRANSGENIC MOUSE; TREATMENT RESPONSE; VACCINATION;

ANIMALS; ANTIGENS, NEOPLASM; AUTOANTIGENS; CANCER VACCINES; DISEASE MODELS, ANIMAL; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; IMMUNE TOLERANCE; LIPOSOMES; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; POLYMERASE CHAIN REACTION; PROSTATIC NEOPLASMS; RNA, MESSENGER; T-LYMPHOCYTES, CYTOTOXIC; TRANSFECTION;

EID: 33644591595     PISSN: 03407004     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00262-005-0064-z     Document Type: Article

References (59)

1. Iezzi G, Karjalainen K, Lanzavecchia A (1998) The duration of antigenic stimulation determines the fate of naive and effector T cells. Immunity 8:89-95
2. van Stipdonk MJB, Hardenberg G, Bijker M, Lemmens EE, Droin NM, Green DR, Schoenberger SP (2003) Dynamic programming of CD8+ T lymphocyte responses. Nat Immunol 4:361-365
3. Nair SK, Heiser A, Boczkowski D, Majumdar A, Naoe M, Lebkowski JS, Vieweg J, Gilboa E (2000) Induction of cytotoxic T cell responses and tumor immunity against unrelated tumors using telomerase reverse transcriptase RNA transfected dendritic cells. Nat Med 6:1011-1017
4. Boczkowski D, Nair SK, Synder D, Gilboa E (1996) Dendritic cells pulsed with RNA are potent antigen-presenting cells in vitro and in vivo. J Exp Med 184:465-472
5. Martinon F, Krishnan S, Lenzen G, Magne R, Gomard E, Guillet J-G, Levy J-P, Meulien P (1993) Induction of virus-specific cytotoxic T lymphocytes in vivo by liposome-entrapped mRNA. Eur J Immunol 23:1719-1722
6. Hoerr I, Obst R, Rammensee H-G, Jung G (2000) In vivo application of RNA leads to induction of specific cytotoxic T lymphocytes and antibodies. Eur J Immunol 30:1-7
7. Zhou W-Z, Hoon DSB, Huang SKS, Fujii S, Hashimoto K, Morishita R, Kaneda Y (1999) RNA melanoma vaccine: induction of antitumor immunity by human glycoprotein 100 mRNA immunization. Hum Gene Ther 10:2719-2724
8. Ying H, Zaks TZ, Wang R-F, Irvine KR, Kammula US, Marincola FM, Leitner WW, Restifo NP (1999) Cancer therapy using a self-replicating RNA vaccine. Nat Med 5:823-827
9. Schirrmacher V, Forg P, Dalemans W, Chlichlia K, Zeng Y, Fournier P, von Hoegen P (2000) Intra-pinna anti-tumor vaccination with self-replicating infectious RNA or with DNA encoding a model tumor antigen and a cytokine. Gene Ther 7:1137-1147
10. Colmenero P, Liljestrom P, Jondal M (1999) Induction of P815 tumor immunity by recombinant Semliki Forest virus expressing the P1A gene. Gene Ther 6:1728-1733
11. Cheng WF, Hung CF, Chai CY, Hsu KF, He L, Ling M, Wu TC (2001) Enhancement of sindbis virus self-replicating RNA vaccine potency by linkage of herpes simplex virus type 1 VP22 protein to antigen. J Virol 75:2368-2376
12. Ishii N, Fukushima J, Kaneko T, Okada E, Tani K, Tanaka S-I, Hamajima K, Xin K-Q, Kawamoto S, Koff WC (1997) Cationic liposomes are a strong adjuvant for a DNA vaccine of human immunodeficiency virus type 1. AIDS Res Hum Retrovir 13:1421-1427
13. Li X-L, Boyanapalli M, Weihua X, Kalvakolanu DV, Hassel BA (1998) Induction of interferon synthesis and activation of interferon-stimulated genes by liposomal transfection reagents. J Interferon Cytokine Res 18:947-952
14. Xiang Z, Ertl HC (1995) Manipulation of the immune response to a plasmid-encoded viral antigen by coinoculation with plasmids expressing cytokines. Immunity 2:129-135
15. Iwasaki A, Stiernholm BJ, Chan AK, Berinstein NL, Barber BH (1997) Enhanced CTL responses mediated by plasmid DNA immunogens encoding costimulatory molecules and cytokines. J Immunol 158:4591-4601
16. Geissler M, Gesien A, Tokushige K, Wands JR (1997) Enhancement of cellular and humoral immune responses to hepatitis C virus core protein using DNA-based vaccines augmented with cytokine-expressing plasmids. J Immunol 158:1231-1237
17. Charo J, Ciupitu AM, Le Chevalier De Preville A, Trivedi P, Klein G, Hinkula J, Kiessling R (1999) A long-term memory obtained by genetic immunization results in full protection from a mammary adenocarcinoma expressing an EBV gene. J Immunol 163:5913-5919
18. Bowne WB, Srinivasan R, Wolchok JD, Hawkins WG, Blachere NE, Dyall R, Lewis JJ, Houghton AN (1999) Coupling and uncoupling of tumor immunity and autoimmunity. J Exp Med 190:1711-1722
19. Gabrilovich EI, Ciernik IF, Carbone DP (1996) Dendritic cells in antitumor immune responses. I. Defective antigen presentation in tumor-bearing hosts. Cell Immunol 170:101-110
20. Bronte V, Chappelli DB, Appoloni E, Cabrelle A, Wang M, Hwu P, Restifo NP (1999) Unopposed production of granulocyte-macrophage colony stimulating factor by tumors inhibits CD8+ T cell response by dysregulating antigen-presenting cell maturation. J Immunol 162:5278-5283
21. Mizoguchi H, O'Shea JJ, Longo DL, Loefller CM, McVicar DW, Ochoa AC (1992) Alterations in signal transduction molecules in T lymphocytes from tumor-bearing mice. Science 258:1795-1798
22. Kolenko V, Wang Q, Riedy MC, O'Shea J, Ritz J, Cathcart MK, Rayman P, Tubbs R, Edinger M, Novick A et al. (1997) Tumor-induced suppression of T lymphocyte proliferation coincides with inhibition of Jak3 expression and IL-2 receptor signaling: role of soluble products from human renal cell carcinomas. J Immunol 159:3057-3067
23. Correa MR, Ochoa AC, Ghosh P, Mizoguchi H, Harvey L, Longo DL (1997) Sequential development of structural and functional alterations in T cells from tumor-bearing mice. J Immunol 158:5292-5296
24. Dyall R, Bowne WB, Weber LW, LeMaoult J, Szabo P, Moroi Y, Piskun G, Lewis JJ, Houghton AN, Nikolic-Zugic J (1998) Heteroclitic immunization induces tumor immunity. J Exp Med 188:1553-1561
25. Tsuboi A, Oka Y, Ogawa H, Elisseeva OA, Li H, Kawasaki K, Aozasa K, Kishimoto T, Udaka K, Sugiyama H (2000) Cytotoxic T-lymphocyte responses elicited to Wilms' tumor gene WT1 product by DNA vaccination. J Clin Immunol 20:195-202
26. Bronte V, Apolloni E, Ronca R, Zamboni P, Overwijk WW, Surman DR, Restifo NP, Zanovello P (2000) Genetic vaccination with "self" tyrosinase-related protein 2 causes melanoma eradication but not vitilligo. Canc Res 60:253-258
27. Tuting T, Bambotto A, De Leo A, Lotze MT, Robbins PD, Storkus WJ (1999) Induction of tumor antigen-specific immunity using plasmid DNA immunization in mice. Canc Gene Ther 6:73-80
28. Greenberg NM, DeMayo F, Finegold MH, Medina D, Tilley WD, Aspinal JO, Cunha GR, Donjacour AA, Matusik RJ, Rosen JM (1995) Prostate cancer in a transgenic mouse. Proc Natl Acad Sci USA 92:3439-3443
29. Gingrich JR, Barrios RJ, Morton RA, Boyce BF, DeMayo FJ, Finegold MH, Angelopoulou R, Rosen JM, Greenberg NM (1996) Metastatic prostate cancer in a transgenic mouse. Cane Res 56:4096-4102
30. Granziero L, Krajewski S, Farness P, Yuan L, Courtney MK, Jackson MR, Peterson PA, Vitiello A (1999) Adoptive immunotherapy prevents prostate cancer in a transgenic animal model. Eur J Immunol 29:1127-1138
31. Hurwitz AA, Foster BA, Kwon ED, Truong T, Choi EM, Greenberg NM, Burg MB, Allison JP (2000) Combination immunotherapy of primary prostate cancer in a transgenic mouse model using CTLA-4 blockade. Cane Res 60:2444-2448
32. Mandleboim O, Berke G, Fridkin M, Feldman M, Eisenstein M, Eisenbach L (1994) CTL induction by a tumour-associated antigen octapeptide derived from a murine lung carcinoma. Nature 369:67-71
33. Mylin LM, Deckhut AM, Bonneau RH, Kierstead TD, Tevethia MJ, Simmons DT, Tevethia SS (1995) Cytotoxic T lymphoctye escape variants, induced mutations, and synthetic peptides define a dominant H2-Kb-restricted determinant in simian virus 40 tumor antigen. Virology 208:159-17 2
34. Rock KL, Rothstein L, Gamble S (1990) Generation of class I MHC-restricted T-T hybridomas. J Immunol 145:804-811
35. Gingrich JR, Barrios RJ, Kattan MW, Nahm HS, Finegold MJ, Greenberg NM (1997) Androgen-independent prostate cancer progression in the TRAMP model. Cane Res 57:4687-491
36. Lu D, Benjamin R, Kim M, Conry RM, Curiel DT (1994) Optimization of methods to achieve mRNA-mediated transfection of tumor cells in vitro and in vivo employing cationic liposome vectors. Cane Gene Ther 1:245-252
37. Speiser DE, Miranda R, Zakarian A, Bachman MF, McKall-Faienza K, Odermatt B, Hanahan D, Zinkernagel RM, Ohashi PS (1997) Self antigens expressed by solid tumors do not efficiently stimulate naive or activated T cells: implications for immunotherapy. J Exp Med 186:645-653
38. Grossmann ME, Davila E, Celis E (2001) Avoiding tolerance against prostatic antigens with subdominant peptide epitopes. J Immunother 24:237-241
39. Schell TD, Knowles BB, Tevethia SS (2000) Sequential loss of cytotoxic T lymphocyte responses to simian virus 40 large T antigen epitopes in T antigen transgenic mice developing osteosarcomas. Canc Res 60:3002-3012
40. Mounkes LC, Zhong W, Cipres-Palacin G, Heath TD, Debs RJ (1998) Proteoglycans mediate cationic liposome-DNA complex-based gene delivery in vitro and in vivo. J Biol Chem 273:26164-26170
41. Farhood H, Serbina N, Huang L (1995) The role of dioleoyl phosphatidylethanolamine in cationic liposome mediated gene transfer. Biochem Biophys Acta 1235:289-295
42. Segal AW, Wills EJ, Richmond JE, Slavin G, Black CDV, Gregoriadis G (1974) Morphological observations on the cellular and subcellular destination of intravenously administered liposomes. Brit J Exp Path 55:320-326
43. Haddad D, Ramprakash J, Sedegah M, Charoenvit Y, Baumgartner T, Kumar S, Hoffman SL, Weiss WR (2000) Plasmid vaccine expressing granulocyte-macrophage colony-stimulating factor attracts infiltrates including immature dendritic cells into injected muscles. J Immunol 165:3772-3781
44. Bowne WB, Wolchok JD, Hawkins WG, Srinivasan R, Gregor P, Blachere NE, Moroi Y, Engelhorn ME, Houghton AN, Lewis JJ (1999) Injection of DNA encoding granulocyte-macrophage colony-stimulating factor recruits dendritic cells for immune adjuvant effects. Cytokines Cell Mol Ther 5:217-225
45. Kim JJ, Trivedi NN, Nottingham LK, Morrison L, Tsai A, Hu Y, Mahalingam S, Dang K, Ahn L, Doyle NK, et al. (1998) Modulation of amplitude and direction of in vivo immune responses by co-administration of cytokine gene expression cassettes with DNA immunogens. Eur J Immunol 28:1089-1103
46. Kim JJ, Bagarazzi ML, Trivedi N, Hu Y, Kazahaya K, Wilson DM, Ciccarelli R, Chattergoon MA, Dang K, Mahalingam S et al. (1997) Engineering of in vivo immune responses to DNA immunization via codelivery of costimulatory molecule genes. Nat Biotech 15:641-646
47. Dranoff G, Jaffee E, Lazenby A, Golumbek P, Levitsky H, Brose K, Jackson V, Hamada H, Pardoll D, Mulligan RC (1993) Vaccination with irradiated tumor cells engineered to secrete murine granulocyte-macrophage colony-stimulating factor stimulates potent, specific, and long-lasting anti-tumor immunity. Proc Natl Acad Sci USA 90:3539-3543
48. Soo Hoo W, Lundeen KA, Kohrumel JR, Pham N-L, Brostoff SW, Bartholomew RM, Carlo DJ (1999) Tumor cell surface expression of granulocyte-macrophage colony-stimulating factor elicits antitumor immunity and protects from tumor challenge in the P815 mouse mastocytoma tumor model. J Immunol 162:7343-7349
49. Heiser A, Maurice MA, Yancey DR, Wu NZ, Dahm P, Pruitt SK, Boczkowski D, Nair SK, Ballo MS, Gilboa E, et al. (2001) Induction of polyclonal prostate cancer-specific CTL using dendritic cells transfected with amplified tumor RNA. J Immunol 166:2593-2960
50. Ludewig B, Ochsenbein AF, Odermatt F, Paulin D, Hengartner H, Zinkernagel RM (2000) Immunotherapy with dendritic cells directed against tumor antigen shared with normal host cells results in severe autoimmune disease. J Exp Med 191:795-803
51. Kass E, Schlom J, Thompson J, Guadagni F, Graziano P, Greiner JW (1999) Induction of protective host immunity to carcinoembryonic antigen (CEA), a self-antigen in CEA transgenic mice, by immunizing with a recombinant vaccinia-CEA virus. Canc Res 59:676-683
52. Limmer A, Sacher T, Alferink J, Kretschmar M, Schonrich G, Nichterlein T, Arnold B, Hammerling GJ (1998) Failure to induce organ-specific autoimmunity by breaking of tolerance: importance of the microenvironment. Eur J Immunol 28:2395-2406
53. Morgan DJ, Kreuwel HTC, Fleck S, Levitsky HI, Pardoll DM, Sherman LA (1998) Activation of low avidity CTL specific for a self epitope results in tumor rejection but not autoimmunity. J Immunol 160:643-651
54. Eck SC, Turka LA (2001) Adoptive transfer enables tumor rejection targeted against a self-antigen without the induction of autoimmunity. Canc Res 61:3077-3083
55. Wei C, Willis RA, Tilton BR, Looney RJ, Lord EM, Barth RK, Frelinger JG (1997) Tissue-specific expression of the human prostate-specific antigen gene in transgenic mice: implications for tolerance and immunotherapy. Proc Natl Acad Sci USA 94:6369-6374
56. Heiser A, Dahm P, Yancey DR, Maurice MA, Boczkowski D, Nair SK, Gilboa E, Vieweg J (2000) Human dendritic cells transfected with RNA encoding prostate-specific antigen stimulate prostate-specific CTL responses in vitro. J Immunol 164:5508-5514
57. Zheng X, Gao J-X, Zhang H, Geiger TL, Liu Y, Zheng P (2002) Clonal deletion of simian virus 40 large T antigen-specific T cells in the transgenic adenocarcinoma of mouse prostate mice: an important role for clonal deletion in shaping the repertoire of T cells specific for antigens overexpressed in solid tumors. J Immunol 169:4761-4769
58. Morgan RA, Dudley ME, Yu YYL, Zheng Z, Robbins PF, Theoret MR, Wunderlich JR, Hughes MS, Restifo NP, Rosenberg SA (2003) High efficiency TCR gene transfer into primary human lymphocytes affords avid recognition of melanoma tumor antigen glycoprotein 100 and does not alter the recognition of autologous melanoma antigens. J Immunol 171:3287-3295
59. Kessels HW, Wolkers MC, van den Boom MD, van der Valk MA, Schumacher TN (2001) Immunotherapy through TCR gene transfer. Nat Immunol 2:957-961