A loss of antitumor therapeutic activity of CEA DNA vaccines is associated with the lack of tumor cells' antigen presentation to Ag-specific CTLs in a colon cancer model

Cancer Letters

Volumn 356, Issue 2, 2015, Pages 676-685

  Ahn, Euri ^a   Kim, Ha ^a   Han, Kyusun Torque ^a   Sin, Jeong Im ^a  

^a Kangwon National University   (South Korea)

Author keywords

Antitumor immunity; CEA; Colon cancer; DNA vaccines; Tumor immune evasion

Indexed keywords

CARCINOEMBRYONIC ANTIGEN; COMPLEMENTARY DNA; DNA VACCINE; GAMMA INTERFERON; INTERLEUKIN 12 ANTIBODY; PLACEBO; PLASMID VECTOR; PROTEIN 4 1BB ANTIBODY; PROTEIN ANTIBODY; UNCLASSIFIED DRUG; ANTIIDIOTYPIC ANTIBODY; CANCER VACCINE; CD137 ANTIGEN; INTERLEUKIN 12;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ANTINEOPLASTIC ACTIVITY; APOPTOSIS ASSAY; ARTICLE; CANCER CELL LINE; CANCER IMMUNIZATION; CANCER RESISTANCE; CD8+ T LYMPHOCYTE; COLON CANCER; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DNA IMMUNIZATION; DRUG EFFICACY; DRUG TREATMENT FAILURE; ELECTROPORATION; EXPRESSION VECTOR; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; IMMUNOGENICITY; IN VITRO STUDY; MOUSE; NONHUMAN; TUMOR MODEL; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CD4+ T LYMPHOCYTE; COLONIC NEOPLASMS; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; PATHOLOGY; TUMOR CELL CULTURE;

ANIMALIA;

ANIMALS; ANTIBODIES, ANTI-IDIOTYPIC; ANTIGEN PRESENTATION; ANTIGENS, CD137; BLOTTING, WESTERN; CANCER VACCINES; CARCINOEMBRYONIC ANTIGEN; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; COLONIC NEOPLASMS; FEMALE; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-12; MICE; MICE, INBRED C57BL; T-LYMPHOCYTES, CYTOTOXIC; TUMOR CELLS, CULTURED; VACCINES, DNA;

EID: 84919460653     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2014.10.019     Document Type: Article

References (35)

1. Thompson J., Zimmermann W. The carcinoembryonic antigen gene family: structure, expression and evolution. Tumor Biol 1988, 9:63-83.
2. Thompson J., Grunert F., Zimmermann W. Carcinoembryonic antigen gene family: molecular biology and clinical perspectives. J. Clin. Lab. Anal 1991, 5:344-366.
3. Kantor J., Irvine K., Abrams S., Kaufman H., DiPietro J., Schlom J. Antitumor activity and immune responses induced by a recombinant carcinoembryonic antigen-vaccinia virus vaccine. J. Natl. Cancer Inst 1992, 84:1084-1091.
4. Hodge J. Carcinoembryonic antigen as a target for cancer vaccines. Cancer Immunol. Immunother 1996, 43:127-134.
5. Conry R., Widera G., LoBuglio A.F., Fuller J.T., Moore S.E., Barlow D.L., et al. Selected strategies to augment polynucleotide immunization. Gene Ther 1996, 3:67-74.
6. Samanci A., Yi Q., Fagerberg J., Strigård K., Smith G., Rudén U., et al. Pharmacological administration of granulocyte/macrophage-colony-stimulating factor is of significant importance for the induction of a strong humoral and cellular response in patients immunized with recombinant carcinoembryonic antigen. Cancer Immunol. Immunother 1998, 47:131-142.
7. Song K., Chang Y., Prud'homme G.J. 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, 7:481-492.
8. Song K., Chang Y., Prud'homme G.J. IL-12 plasmid-enhanced DNA vaccination against carcinoembryonic antigen (CEA) studied in immune-gene knockout mice. Gene Ther 2000, 7:1527-1535.
9. Mennuni C., Calvaruso F., Facciabene A., Aurisicchio L., Storto M., Scarselli E., et al. 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 2005, 117:444-455.
10. Han K.T., Sin J.I. DNA vaccines targeting human papillomavirus-associated diseases: progresses in animal and clinical studies. Clin. Exp. Vaccine Res 2013, 2:106-114.
11. Bagarazzi M.L., Yan J., Morrow M.P., Shen X., Parker R.L., Lee J.C., et al. Immunotherapy against HPV16/18 generates potent TH1 and cytotoxic cellular immune responses. Sci. Transl. Med 2012, 4:155ra138. 10.1126/scitranslmed.3004414.
12. Diaz-Montero C.M., Chiappori A., Aurisicchio L., Bagchi A., Clark J., Dubey S., et al. Phase 1 studies of the safety and immunogenicity of electroporated HER2/CEA DNA vaccine followed by adenoviral boost immunization in patients with solid tumors. J. Transl. Med 2013, 11:62. 10.1186/1479-5876-11-62.
13. Taraban V.Y., Rowley T.F., O'Brien L., Chan H.T., Haswell L.E., Green M.H., et al. Expression and costimulatory effects of the TNF receptor superfamily members CD134 (OX40) and CD137 (4-1BB), and their role in the generation of anti-tumor immune responses. Eur. J. Immunol 2002, 32:3617-3627.
14. Kocak E., Lute K., Chang X., May K.F., Exten K.R., Zhang H., et al. Combination therapy with anti-CTL antigen-4 and anti-4-1BB antibodies enhances cancer immunity and reduces autoimmunity. Cancer Res 2006, 66:7276-7284.
15. Li B., Lin J., Vanroey M., Jure-Kunkel M., Jooss K. Established B16 tumors are rejected following treatment with GM-CSF-secreting tumor cell immunotherapy in combination with anti-4-1BB mAb. Clin. Immunol 2007, 125:76-87.
16. Sin J.I., Kim H., Ahn E., Jeon Y.H., Park W.S., Lee S.Y., et al. Combined stimulation of TLR9 and 4-1BB augments Trp2 peptide vaccine-mediated melanoma rejection by increasing Ag-specific CTLs and their infiltration into tumor sites. Cancer Lett 2013, 330:190-199.
17. Kim H., Kwon B., Sin J.I. Combined stimulation of IL-2 and 4-1BB receptors augments the antitumor activity of E7 DNA vaccines by increasing Ag-specific CTL responses. PLoS ONE 2013, 8:e83765.
18. Sin J.I., Kim J.J., Arnold R.L., Shroff K.E., McCallus D., Pachuk C., et al. 12 gene as a DNA vaccine adjuvant in a herpes mouse model: IL-12 enhances Th1 type CD4+ T cell mediated protective immunity against herpes simplex virus-2 challenge. J. Immunol 1999, 162:2912-2921.
19. Sin J.I., Sung J.H., Suh Y.S., Lee A.H., Chung J.H., Sung Y.C. Protective immunity against heterologous challenge with encephalomyocarditis virus by VP1 DNA vaccination: effect of co-injection with a granulocyte, macrophage-colony stimulating factor gene. Vaccine 1997, 15:1827-1833.
20. Yamaguchi S., Tatsumi T., Takehara T., Sakamori R., Uemura A., Mizushima T., et al. Immunotherapy of murine colon cancer using receptor tyrosine kinase EphA2-derived peptide-pulsed dendritic cell vaccines. Cancer 2007, 110:1469-1477.
21. Ryan M., Abrams S.I. Characterization of CD8+ cytotoxic T lymphocyte/tumor cell interactions reflecting recognition of an endogenously expressed murine wild type p53 determinant. Cancer Immunol. Immunother 2001, 49:603-612.
22. 180-188 peptides. Cancer Immunol. Immunother 2012, 61:1671-1682.
23. Bae S.H., Park Y.J., Park J.B., Choi Y.S., Kim M.S., Sin J.I. Therapeutic synergy of human papillomavirus E7 subunit vaccines plus cisplatin in an animal tumor model: causal involvement of increased sensitivity of cisplatin-treated tumors to CTL-mediated killing in therapeutic synergy. Clin. Cancer Res 2007, 13:341-349.
24. Ye G.W., Park J.B., Park Y.J., Choi Y.S., Sin J.I. Increased sensitivity of radiated murine cervical cancer tumors to E7 subunit vaccine-driven CTL-mediated killing induces synergistic antitumor activity. Mol. Ther 2007, 15:1564-1570.
25. Kim T.Y., Myoung H.J., Kim J.H., Moon I.S., Kim T.G., Ahn W.S., et al. Both E7 and CpG-oligodeoxynucleotide are required for protective immunity against challenge with human papillomavirus 16 (E6/E7)immortalized tumor cells: involvement of CD4+ and CD8+ T cells in protection. Cancer Res 2002, 62:7234-7240.
26. Jang I.K., Lee Z.H., Kim Y.J., Kim S.H., Kwon B.S. Human 4-1BB (CD137) signals are mediated by TRAF2 and activate nuclear factor-κB. Biochem. Biophys. Res. Commun 1998, 242:613-620.
27. Cannons J.L., Choi Y., Watts T.H. Role of TNF receptor-associated factor 2 and p38 mitogen-activated protein kinase activation during 4-1BB-dependent immune response. J. Immunol 2000, 165:6193-6204.
28. Nam K.O., Kang H., Shin S.M., Cho K.H., Kwon B., Kwon B.S., et al. Cross-linking of 4-1BB activates TCR-signaling pathways in CD8+ T lymphocytes. J. Immunol 2005, 174:1898-1905.
29. John L.B., Howland L.J., Flynn J.K., West A.C., Devaud C., Duong C.P., et al. Oncolytic virus and anti-4-1BB combination therapy elicits strong antitumor immunity against established cancer. Cancer Res 2012, 72:1651-1660.
30. Lee I.H., Park J.B., Cheong M., Choi Y.S., Park D., Sin J.I. Antitumor therapeutic and antimetastatic activity of electroporation-delivered human papillomavirus 16 E7 DNA vaccines: a possible mechanism for enhanced tumor control. DNA Cell Biol 2011, 30:975-985.
31. Kim S.G., Park M.Y., Kim C.H., Sohn H.J., Kim H.S., Park J.S., et al. Modification of CEA with both CRT and TAT PTD induces potent anti-tumor immune responses in RNA-pulsed DC vaccination. Vaccine 2008, 26:6433-6440.
32. Park J., Kim H.S., Park H.M., Kim C.H., Kim T.G. Efficient induction of anti-tumor immunity by a TAT-CEA fusion protein vaccine with poly(I:C) in a murine colorectal tumor model. Vaccine 2011, 29:8642-8648.
33. Igney F., Krammer P.H. Immune escape of tumors: apoptosis resistance and tumor counterattack. J. Leukoc. Biol 2002, 71:907-920.
34. Conforti A., Peruzzi D., Giannetti P., Biondo A., Ciliberto G., La Monica N., et al. A novel mouse model for evaluation and prediction of HLA-A2-restricted CEA cancer vaccine responses. J. Immunother 2009, 32:744-754.
35. Palazón A., Teijeira A., Martínez-Forero I., Hervás-Stubbs S., Roncal C., Peñuelas I., et al. Agonist anti-CD137 mAb act on tumor endothelial cells to enhance recruitment of activated T lymphocytes. Cancer Res 2011, 71:801-811.