Tumor Immunology

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Efficient induction of T-cell responses to carcinoembryonic antigen by a heterologous prime-boost regimen using DNA and adenovirus vectors carrying a codon usage optimized cDNA

  1. Carmela Mennuni,
  2. Francesco Calvaruso,
  3. Andrea Facciabene,
  4. Luigi Aurisicchio,
  5. Mariangela Storto,
  6. Elisa Scarselli,
  7. Gennaro Ciliberto,
  8. Nicola La Monica†,*

Article first published online: 19 MAY 2005

DOI: 10.1002/ijc.21188

Issue

International Journal of Cancer

International Journal of Cancer

Volume 117, Issue 3, pages 444–455, 10 November 2005

Additional Information

How to Cite

Mennuni, C., Calvaruso, F., Facciabene, A., Aurisicchio, L., Storto, M., Scarselli, E., Ciliberto, G. and La Monica, N. (2005), Efficient induction of T-cell responses to carcinoembryonic antigen by a heterologous prime-boost regimen using DNA and adenovirus vectors carrying a codon usage optimized cDNA. Int. J. Cancer, 117: 444–455. doi: 10.1002/ijc.21188

Author Information

  1. Istituto di Ricerche di Biologia Molecolare (IRBM), Pomezia, Italy

  1. †

    Fax: +39-6-91093-482

*Istituto di Ricerche di Biologia Molecolare (IRBM), Via Pontina km 30,600 Pomezia, 00040 Italy

Publication History

  1. Issue published online: 14 SEP 2005
  2. Article first published online: 19 MAY 2005
  3. Manuscript Accepted: 7 MAR 2005
  4. Manuscript Received: 3 NOV 2004

Funded by

  • Italian MIUR. Grant Number: FIRB RBME017BC4

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References

  • 1
    Gilboa E. The promise of cancer vaccine. Nat Rev Cancer 2004; 4: 401–11.
  • 2
    Finn OJ. Cancer vaccines: between the idea and the reality. Nat Rev Immunol 2003; 3: 630–41.
  • 3
    Thompson JA, Grunert F, Zimmerman W. Carcinoembryonic antigen gene family: molecular biology and clinical perspectives. J Clin Lab Anal 1991; 5: 344–66.
    Direct Link:
  • 4
    Shively JE, Beatty JD. CEA-related antigens: molecular biological and clinical significance. Crit Rev Oncol Hematol 1985; 2: 355–99.
  • 5
    Huang EH, Kaufman HL. CEA-based vaccines. Expert Rev Vaccines 2002; 1: 49–63.
  • 6
    Srivastava IK, Liu MA. Gene vaccines. Ann Intern Med 2003; 138: 550–9.
  • 7
    Gurunthan S, Wu CY, Freidag BL, Seder SA. DNA vaccines: a key for inducing long-term cellular immunity. Curr Opin Immunol 2000; 12: 442–7.
  • 8
    Donnelly JJ, Ulmer JB, Shiver JW, Liu MA. DNA vaccines. Ann Rev Immunol 1997; 15: 617–48.
  • 9
    Fattori E, La Monica N, Ciliberto G, Toniatti C. Electro-gene-transfer: a new approach for muscle gene delivery. Somatic Cell Mol Genet 2003; 27: 75–83.
  • 10
    Scheerlinck JPY, Karlis J, Tjelle TE, Presidente PJA, Mathiesen I, Newton SE. In vivo electroporation improves immune responses to DNA vaccination in sheep. Vaccine 2004; 22: 1820–5.
  • 11
    Zucchelli S, Capone S, Fattori E, Folgori A, Di Marco A, Casimiro D, Simon AJ, Alufer R, La Monica N, Cortese R, Nicosia A. Enhancing B- and T-cell immune response to hepatitis C virus E2 DNA vaccine intramuscular electrical gene transfer. J Virol 2000; 74: 11598–607.
  • 12
    Widera G, Austin M, Rabussay D, Goldbeck C, Barnett SW, Chen M, Leng L, Otten GR, Thudium K, Selby MJ, Ulmer JB. Increased DNA vaccine delivery and immunogenicity by electroporation in vivo. J Immunol 2000; 164: 4635–40.
  • 13
    Babiouk SM, Estrada E, Storms M, Rabussay D, Widera G, Babiuk LA. Electroporation improves efficacy of DNA vaccines in large animals. Vaccine 2002; 20: 3399–408.
  • 14
    Gronevik ES, Tollefsen S, Sikkel LI, Haug T, Tjelle TE, Mathiesen I. DNA transfection of mononuclear cells in muscle tissue. J Gene Med 2003; 5: 909–17.
    Direct Link:
  • 15
    Uno-Furuta S, Tamaki S, Takebe Y, Takamura S, Kamei A, Kim G, Kuromatsu I, Kaito M, Adachi Y, Yasutomi Y. Induction of virus-specific cytotoxic T lymphocytes by in vivo electric administration of peptides. Vaccine 2001; 19: 2190–9.
  • 16
    Babiuk S, Baca-Estrada ME, Foldvari M, Middleton DM, Rabussay D, Widera G, Babiuk LA. Increased gene expression and inflammatory cell infiltration caused by electroporation are both important for improving the efficacy of DNA vaccines. J Biotechnol 2004; 110: 1–10.
  • 17
    Bronte V. Genetic vaccination for the active immunotherapy of Cancer. Curr Gene Therapy 2001; 1: 53–100.
  • 18
    Shiver JW, Fu TM, Chen L, Casimiro DR, Davies ME, Evans RK, Zhang ZQ, Simon AJ, Trigona WL, Dubey SA, Huang L, Harris WA, et al. Replication incompetent adenoviral vector elicits effective anti-immunodeficiency-virus immunity. Nature 2002; 415: 331–5.
  • 19
    Bruna-Romero O, Gonzàlez-Aseguinolaza G, Hafalla JCR, Tsuji M, Nussenweig RS. Complete, long lasting protection against malaria of mice primed and boosted with two distinct viral vectors expressing the same plasmodial antigen. Proc Natl Acad Sci USA 2001; 98: 11491–6.
  • 20
    Casimiro D, Tang A, Chen L, Fu TM, Evans RK, Davies ME, Freed DC, Hurni W, Aste-Amezaga JM, Guam L, Long R, Huang L, et al. Vaccine induced immunity in baboons using DNA and replication-incompetent Adenovirus type 5 vectors expressing a human immunodeficiency virus type I gag gene. J Virol 2003; 77: 7663–8.
  • 21
    Estcourt MJ, Ramsay AJ, Brooks A, Thomson SA, Medveckzy CJ, Ramshaw IA. Prime-boost immunization generates a high frequency, high-avidity, CD8+ cytotoxic T lymphocyte population. Int Immunol 2002; 14: 31–7.
  • 22
    Gonzalo RM, Del Real G, Rodriguez JR, Rodriguez D, Heljasvaara R, Lucas P, Arraga V, Esteban M. A heterologous prime-boost regime using DNA and recombinant vaccinia virus expressing the Leishmania infantum P36/LACK antigen protects BALB/c mice from cutaneous leishmaniasis. Vaccine 2002; 20: 1226–31.
  • 23
    Wierzibicki A, Kiszka I, Kaneko H, Kmieciak D, Wasik TJ, Gzyl J, Kaneko Y, Kozbor D. Immunization strategies to augment oral vaccination with DNA and viral vectors expressing HIV envelope glycoprotein. Vaccine 2002; 20: 1295–307.
  • 24
    Haas J, Park E, Seed B. Codon usage limitations in the expression of the HIV-1 envelope glycoprotein. Curr Biol 1996; 6: 315–24.
  • 25
    Hentze M. Determinants and regulation of cytoplasmic mRNA stability in eukaryotic cells. Biochim Biophys Acta 1991; 1090: 281–92.
  • 26
    Gaucher D, Chadee K. Construction and immunogenicity of a codon-optimized Entamoeba histolytica Gal-lectin-based DNA vaccine. Vaccine 2002; 20: 3244–53.
  • 27
    Liu WJ, Gao F, Zhao KN, Zhao W, Fernando GJ, Thomas R, Frazer IH. Codon modified human papillomavirus type 16 E7 DNA vaccine enhances cytotoxic T-lymphocyte induction and anti-tumor activity. Virology 2002; 301: 43–52.
  • 28
    Demi L, Bojak A, Steck S, Graf M, Wild J, Schirmbeck R, Wolf H, Wagner R. Multiple effects of codon usage optimization on expression and immunogenicity of DNA candidate vaccines encoding the human immunodeficiency virus type 1 gag protein. J Virol 2001; 75: 10991–1001.
  • 29
    André S, Seed B, Eberle J, Schraut W, Bultmann A, Haas J. Increased immune response elicited by DNA vaccination with a synthetic gp120 sequence with optimized codon usage. J Virol 1998; 72: 1497–503.
  • 30
    zur Megede J, Chen MC, Doe B, Schaefer M, Greer CE, Selby M, Otten GR, Barnett SW. Increased expression and immunogenicity of sequence-modified human immunogenicity virus type 1 gag gene. JVirol 2000; 74: 2628–35.
  • 31
    Casimiro DR, Tang A, Parry HC, Long RS, Chen M, Heidecker GJ, Davies ME, Freed DC, Parsaud NV, Dubey S, Smith JG, Havlir D, et al. Vaccine-induced immune responses in rodents and nonhuman primates by use of a humanized human immunodeficiency virus type 1 pol gene. J Virol 2002; 76: 185–94.
  • 32
    Frelin L, Ahlén G, Alheim M, Weiland O, Barnfield C, Liljestrom P, Salberg M. Codon optimization and mRNA amplification effectively enhances the immunogenicity of the hepatitis C virus nonstructural 3/4A gene. Gene Ther 2004; 11: 522.
  • 33
    Montgomery DL, Shiver JW, Leander KR, Perry HC, Friedman A, Martinez D, Ulmer JB, Donnelly JJ, Liu MA. Heterologous and homologous protection against influenza A by DNA vaccination: optimization of DNA vectors. DNA Cell Biol 1993; 129: 777–83.
  • 34
    Song K, Chang Y, Prud'home GJ. Regulation of T-helper-1 versus T-helper-2 activity and enhancement of tumor immunity by combined DNA-based vaccination and nonviral cytokine gene transfer. Gene Ther 2000; 7: 481–92.
  • 35
    Facciabene A, Aurisicchio L, La Monica N. Baculovirus vectors elicit antigen specific immune responses in mice. J Virol 2004; 78: 8663–72.
  • 36
    Clarke P, Mann J, Simpson JF, Rickard-Dickson K, Primus FJ. Mice transgenic for human carcinoembryonic antigen as a model for immunotherapy. Cancer Res 1998; 58: 1469–77.
  • 37
    Rizzuto G, Capelletti M, Maione D, Savino R, Lazzaro D, Costa P, Mathiesen I, Cortese R, Ciliberto G, Laufer R, La Monica N, Fattori E. Efficient and regulated erythropoietin production by naked DNA injection and muscle electroporation. Proc Natl Acad Sci USA 1999; 96: 6417–22.
  • 38
    Park S-H, Yang S-H, Lee CG, Youn J-W, Chan J, Sung YC. Efficient induction of T helper 1 CD4+ T-cell responses to hepatitis C virus core and E2 by a DNA-prime adenovirus boost. Vaccine 2003; 21: 4555–64.
  • 39
    Meng WS, Butterfiled LH, Ribas A, Dissette VR, Heller JH, Miranda GA, Glaspy JA, McBride WH, Economou JS. α-Fetoprotein-specific tumor immunity induced by plasmid prime-adenovirus boost genetic vaccination. Cancer Res 2001; 61: 8782–6.
  • 40
    Gilbert SC, Schneider J, Hannan CM, Hu JT, Plebanski M, Sinden R, Hill AVS. Enhanced CD8 T cell immunogenicity and protective efficacy in a mouse malaria model using a recombinant adenoviral vaccine in heterologous prime-boost immunization regimens. Vaccine 2002; 20: 1039–45.
  • 41
    Rammensee H, Bachmann J, Emmerich NP, Bachor OA, Stevanovic S. SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics 1999; 50: 213–9.
  • 42
    Dunachie SJ, Hill AVS. Prime-boost strategies for malaria vaccine development. J Exp Med 2003; 206: 3771–9.
  • 43
    McShane H, Brookes R, Gilbert SC, Hill AVS. Enhanced immunogenicity of CD4(+) t-cell responses and protective efficacy of a DNA-modified vaccine virus Ankara prime-boost vaccination regimen for murine tuberculosis. Infect Immun 2001; 69: 681–6.
  • 44
    Van der Burg SH, Kwappenberg KM, O'Neill T, Brandt RM, Melief CJ, Hickling JK, Offringa R. Preclinical safety and efficacy of TA-CIN, a recombinant HPV16 L2E6E7 fusion protein vaccine, in homologous and heterologous pirme-boost regimens. Vaccine 2001; 19: 3652–60.
  • 45
    McKelvey T, Tang A, Bett AJ, Casimiro DR, Chastain M. T-cell response to adenovirus hexon and DNA-binding protein in mice. Gene Ther 2004; 11: 791–6.
  • 46
    Fitzgerald JC, Gao GP, Reyes-Sandoval A, Pavlakis GN, Xiang ZQ, Wlazlo AP, Giles-Davis W, Wilson JM, Ertl HCJ. A simian replication defective adenoviral recombinant vaccine to HIV gag. J Immunol 2003; 170: 1416–22.
  • 47
    Casimiro DR, Chen L, Fu TM, Evans RK, Aulfield MJ, Davies ME, Tang A, Chen M, Huang L, Harris V, Freed DC, Wilson KA, et al. Comparative immunogenicity in rhesus monkeys of DNA plasmid recombinant vaccinia virus and replication deficient adenovirus expressing a human immunodeficiency virus type 1 gag gene. J Virol 2003; 77: 6305–13.
  • 48
    Miconnet I, Koenig S, Speiser D, Krieg A, Guillame P, Cerottini JC, Romero P. CpG are efficient adjuvants for specific CTL induction against tumor antigen-derived peptide. J Immunol 2002; 168: 1212–8.
  • 49
    Verthelyi S, Kenney RT, Sedr RA, Gam AA, Friedag B, Klinmann DM. CpG oligodeoxynucleotides as vaccine adjuvants in primates. J Immunol 2002; 15: 1659–63.
  • 50
    Fong L, Hou Y, Rivas A, Benike C, Yuen A, Fisher GA, Davis MM, Engleman EG. Altered peptide ligand vaccination with Flt3 ligand expanded dendritic cells for tumor immunotherapy. Proc Natl Acad Sci USA 2001; 98: 8809–14.
  • 51
    Hodge JW, Grosenbach DW, Aarts WM, Poole DJ, Schlom J. Vaccine therapy of established tumors in the absence of autoimmunity. Clin Can Res 2003; 9: 1837–49.
  • 52
    Schmitz J, Reali E, Hodge JW, Patel A, Davis G, Schlom J, Greiner JW. Identification of an interferon-γ-inducible carcinoembryonic antigen (CEA) CD8+ T cell epitope, which mediates tumor killing in CEA transgenic mice. Cancer Res 2002; 62: 5058–64.
  • 53
    Mizobata S, Tompkins K, Simpson JF, Shyr Y, Primus FJ. Induction of cytotoxic T cells and their antitumor activity in mice transgenic for carcinoembryonic antigen. Cancer Immunol Immunother 2000; 49: 285–95.
  • 54
    Wilkinson RW, Ross EL, Ellison D, Zimmermann W, Snary D, Mather SJ. Evaluation of a transgenic mouse model for anti-human CEA radioimmunotherapeutics. J Nucl Med 2002; 43: 1368–76.
  • 55
    Ullehahg GJ, Fagerberg J, Strigard K, Froding JE, Mellstedt H. Functional HLA-DR T cell epitopes of CEA identified in patients with colorectal carcinoma immunized with the recombinant protein CEA. Cancer Immunol Immunother 2004; 53: 331–7.
  • 56
    Melina Soares M, Mehta V, Finn OJ. Three different vaccines based on the 140-amino acid MUC1 peptide with seven tandemly repeated tumor-specific epitopes elicit distinct immune effector mechanisms in wild type versus MUC1-transgenic mice with different potential for tumor rejection. J Immunol 2001; 166: 6555–63.
  • 57
    Niethammer AG, Primus FJ, Xiang R, Dolman CS, Ruehlmann JM, Ba Y, Gillies SD, Reisfeld RA. An oral DNA vaccine against human carcinoembryonic antigen (CEA) prevents growth and dissemination of Lewis lung carcinoma in CEA transgenic mice. Vaccine 2002; 20: 421–9.
  • 58
    Kass E, Schlom J, Thompson J, Guadagni F, Graziano P, Greiner JW. Induction of protective host immunity to carcinoembryonic antigen (CEA), a self-antigen in CEA transgenic mice, by immunizing with a recombinant vaccinia-CEA virus. Cancer Res 1999; 59: 676–83.
  • 59
    Xiang R, Silletti S, Lode HN, Dolman CS, Ruehlmann JM, Niethammer AG, Pertl U, Gillies SD, Primus JP, Reisfeld RA. Protective immunity against human carcinoembryonic antigen (CEA) induced by an oral DNA vaccine in CEA-transgenic mice. Clin Cancer Res 2001; 7: 856–64.
  • 60
    Luo Y, O'Hagan D, Zhou H, Singh M, Ulmer J, Reisfeld RA, Primus FJ, Xiang R. Plasmid DNA encoding human carcinoembryonic antigen (CEA) adsorbed onto cationic microparticles induces protective immunity against colon cancer in CEA-transgenic mice. Vaccine 2003; 21: 1938–47.
  • 61
    Stevenson FK, Rice J, Ottensmeier CH, Thirdborough SM, Zhu D. DNA fusion gene vaccines against cancer: from the laboratory to the clinic. Immunol Rev 2004; 199: 156–80.
    Direct Link:
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