Therapeutic Tumor Control of HER2 DNA Vaccines Is Achieved by an Alteration of Tumor Cells and Tumor Microenvironment by Gemcitabine and Anti-Gr-1 Ab Treatment in a HER2-Expressing Tumor Model

DNA and Cell Biology

Volumn 36, Issue 9, 2017, Pages 801-811

  Danishmalik, Sayyed Nilofar ^a   Sin, Jeong Im ^a  

^a Kangwon National University   (South Korea)

Author keywords

antitumor immunity

Indexed keywords

ANTIBODY; CANCER VACCINE; CD274 PROTEIN, MOUSE; CHEMOKINE RECEPTOR; DEOXYCYTIDINE; DNA VACCINE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ERBB2 PROTEIN, MOUSE; GEMCITABINE; GR-1 PROTEIN, MOUSE; PROGRAMMED DEATH 1 LIGAND 1;

ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; CYTOTOXIC T LYMPHOCYTE; DRUG EFFECTS; FEMALE; GENETICS; IMMUNOLOGY; METABOLISM; NEOPLASMS, EXPERIMENTAL; PATHOLOGY; TUMOR MICROENVIRONMENT;

ANIMALS; ANTIBODIES; ANTIGENS, CD274; CANCER VACCINES; DEOXYCYTIDINE; FEMALE; MICE, INBRED BALB C; NEOPLASMS, EXPERIMENTAL; RECEPTOR, ERBB-2; RECEPTORS, CHEMOKINE; T-LYMPHOCYTES, CYTOTOXIC; TUMOR MICROENVIRONMENT; VACCINES, DNA;

EID: 85030787203     PISSN: 10445498     EISSN: 15577430     Source Type: Journal    
DOI: 10.1089/dna.2017.3810     Document Type: Article

References (37)

1. Ahn, E., Kim, H., Han, K.T., and Sin J.I. (2015). 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 Lett 356, 676-685.
2. Akiyama, T., Sudo, C., Ogawara, H., Toyoshima, K., and Yamamoto, T. (1986). The product of the human c-erbB-2 gene: A 185-kilodalton glycoprotein with tyrosine kinase activity. Science 232, 1644-1646.
3. Bae, S.H., Park, Y.J., Park, J.B., Choi, Y.S., Kim, M.S., and Sin, J.I. (2007). Therapeutic synergy of human papillomavirus E7 subunit vaccines plus cisplatin in an animal tumor model: causal involvement of increased sensitivity of cisplatintreated tumors to CTL-mediated killing in therapeutic synergy. Clin Cancer Res 13, 341-349.
4. Bargmann, C.I., Hung, M.C., and Weinberg, R.A. (1986). The neu oncogene encodes an epidermal growth factor receptorrelated protein. Nature 319, 226-230.
5. Bauer, C., Hees, C., Sterzik, A., Bauernfeind, F., Mak?Anyengo, R., Duewell, P., Lehr, H.A., Noessner, E., Wank, R., Trauzold, A., Endres, S., Dauer, M., and Schnurr, M. (2015). Proapoptotic and antiapoptotic proteins of the Bcl-2 family regulate sensitivity of pancreatic cancer cells toward gemcitabine and T-cell-mediated cytotoxicity. J Immunother 38, 116-126.
6. Bauer, C., Sterzik, A., Bauernfeind, F., Duewell, P., Conrad, C., Kiefl, R., Endres, S., Eigler, A., Schnurr, M., and Dauer, M. (2014). Concomitant gemcitabine therapy negatively affects DC vaccine-induced CD8(+) T-cell and B-cell responses but improves clinical efficacy in a murine pancreatic carcinoma model. Cancer Immunol Immunother 63, 321-333.
7. Bennett, M.W., O?Connell, J., O?Sullivan, G.C., Brady, C., Roche, D., Collins, J.K., and Shanahan, F. (1998). The Fas counterattack in vivo: Apoptotic depletion of tumor-infiltrating lymphocytes associated with Fas ligand expression by human esophageal carcinoma. J Immunol 160, 5669-5675.
8. Danishmalik, S.N., Lee, S.H., and Sin, J.I. (2017). Tumor regression is mediated by induction of HER263-71-specific CD8+ CTLs in a 4T1.2/HER2 tumor model: no involvement of CD80 in tumor control. Oncotarget 8, 26771-26788.
9. Dong, H., Strome, S.E., Salomao, D.R., Tamura, H., Hirano, F., Flies, D.B., Roche, P.C., Lu, J., Zhu, G., Tamada, K., Lennon, V.A., Celis, E., and Chen, L. (2002). Tumor-Associated B7-H1 promotes T-cell apoptosis: A potential mechanism of immune evasion. Nat Med 8, 793-800.
10. Foy, S.P., Mandl, S.J., Dela Cruz, T., Cote, J.J., Gordon, E.J., Trent, E., Delcayre, A., Breitmeyer, J., Franzusoff, A., and Rountree, R.B. (2016). Poxvirus-based active immunotherapy synergizes with CTLA-4 blockade to increase survival in a murine tumor model by improving the magnitude and quality of cytotoxic T cells. Cancer Immunol Immunother 65, 537-549.
11. Gabrilovich, D.I., and Nagaraj, S. (2009). Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 9, 162-174.
12. Jin, D., Fan, J., Wang, L., Thompson, L.F., Liu, A., Daniel, B.J., Shin, T., Curiel, T.J., and Zhang, B. (2010). CD73 on tumor cells impairs antitumor T-cell responses: A novel mechanism of tumor-induced immune suppression. Cancer Res 70, 2245-2255.
13. Kang, C., Dutta, A., Chang, L.Y., Mahalingam, J., Lin, Y.C., Chiang, J.M., Hsu, C.Y., Huang, C.T., Su, W.T., Chu, Y.Y., and Li, C.Y. (2015). Apoptosis of tumor infiltrating effector TIM-3+CD8+ T cells in colon cancer. Sci Rep 5, 15659.
14. Kim, H., Danishmalik, S.N., Hwang, H., Sin, J.I., Oh, J., Cho, Y., Lee, H., Jeong, M., Kim, S.H., and Hong, H.J. (2016). Gene therapy using plasmid DNA-encoded anti-HER2 antibody for cancers that overexpress HER2. Cancer Gene Ther 23, 341-347.
15. Kim, H., Kwon, B., and Sin, J.I. (2013). 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 8, e83765.
16. Lee, I.H., Park, J.B., Cheong, M., Choi, Y.S., Park, D., and Sin, J.I. (2011). Antitumor therapeutic and antimetastatic activity of electroporation-delivered human papillomavirus 16 E7 DNA vaccines: A possible mechanism for enhanced tumor control. DNA Cell Biol 30, 975-985.
17. Lee, J.Y., Kim, D.H., Chung, Y., Shin, S.U., and Kang, C.Y. (2003). Comparison of the antitumor efficacies of Her-2/neu DNA vaccines inducing contrasting IgG immunity but comparable CTL activity in mice. Vaccine 21, 521-531.
18. Lee, S.H., Danishmalik, S.N., and Sin, J.I. (2015). DNA vaccines, electroporation and their applications in cancer treatment. Hum Vaccin Immunother 11, 1889-1900.
19. Liu, X., Wu, X., Cao, S., Harrington, S.M., Yin, P., Mansfield, A.S., and Dong, H. (2016). B7-H1 antibodies lose antitumor activity due to activation of p38 MAPK that leads to apoptosis of tumor-reactive CD8+ T cells. Sci Rep 6, 36722.
20. Milani, A., Sangiolo, D., Aglietta, M., and Valabrega, G. (2014). Recent advances in the development of breast cancer vaccines. Breast Cancer (Dove Med Press) 6, 159-168.
21. Mundy-Bosse, B.L., Lesinski, G.B., Jaime-Ramirez, A.C., Benninger, K., Khan, M., Kuppusamy, P., Guenterberg, K., Kondadasula, S.V., Chaudhury, A.R., La Perle, K.M., Kreiner, M., Young, G., Guttridge, D.C., and Carson, W.E., 3rd. (2011). Myeloid-derived suppressor cell inhibition of the IFN response in tumor-bearing mice. Cancer Res 71, 5101-5110.
22. Nagaraj, S., Schrum, A.G., Cho, H.I., Celis, E., and Gabrilovich, D.I. (2010). Mechanism of T cell tolerance induced by myeloid-derived suppressor cells. J Immunol 184, 3106-3116.
23. Nagata, Y., Furugen, R., Hiasa, A., Ikeda, H., Ohta, N., Furukawa, K., Nakamura, H., Furukawa, K., Kanematsu, T., and Shiku, H. (1997). Peptides derived from a wild-Type murine proto-oncogene c-erbB-2/HER2/neu can induce CTL and tumor suppression in syngeneic hosts. J Immunol 159, 1336-1343.
24. Natali, P.G., Nicotra, M.R., Bigotti, A., Venturo, I., Slamon, D.J., Fendly, B.M., and Ullrich, A. (1990). Expression of the p185 encoded by HER2 oncogene in normal and transformed human tissues. Int J Cancer 45, 457-461.
25. Nguyen-Hoai, T., Kobelt, D., Hohn, O., Vu, M.D., Schlag, P.M., Dörken, B., Norley, S., Lipp, M., Walther, W., Pezzutto, A., and Westermann, J. (2012). HER2/neu DNA vaccination by intradermal gene delivery in a mouse tumor model: gene gun is superior to jet injector in inducing CTL responses and protective immunity. Oncoimmunol 1, 1537-1545.
26. Penichet, M.L., Challita, P.M., Shin, S.U., Sampogna, S.L., Rosenblatt, J.D., and Morrison, S.L. (1999). In vivo properties of three human HER2/neu-expressing murine cell lines in immunocompetent mice. Lab Anim Sci 49, 179-188.
27. Pilon-Thomas, S., Mackay, A., Vohra, N., and Mulé, J.J. (2010). Blockade of programmed death ligand 1 enhances the therapeutic efficacy of combination immunotherapy against melanoma. J Immunol 184, 3442-3449.
28. Ramakrishnan, R., Assudani, D., Nagaraj, S., Hunter, T., Cho, H.I., Antonia, S., Altiok, S., Celis, E., and Gabrilovich, D.I. (2010). Chemotherapy enhances tumor cell susceptibility to CTL-mediated killing during cancer immunotherapy in mice. J Clin Investig 120, 1111-1124.
29. Sin, J.I., Kim, H., Ahn, E., Jeon, Y.H., Park, W.S., Lee, S.Y., and Kwon, B. (2013). 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 330, 190-199.
30. Sin, J.I., Park, J.B., Lee, I.H., Park, D., Choi, Y.S., Choe, J., and Celis, E. (2012). Intratumoral electroporation of IL-12 cDNA eradicates established melanomas by Trp2180-188-specific CD8+ CTLs in a perforin/granzyme-mediated and IFN-g dependent manner: Application of Trp2180-188 peptides. Cancer Immunol Immunother 61, 1671-1682.
31. Sin, J.I., Sung, J.H., Suh, Y.S., Lee, A.H., Chung, J.H., and Sung, Y.C. (1997). 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 15, 1827-1833.
32. Slamon, D.J., Clark, G.M., Wong, S.G., Levin, W.J., Ullrich, A., and McGuire, W.L. (1987). Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 235, 177-182.
33. Srivastava, M.K., Sinha, P., Clements, V.K., Rodriguez, P., and Ostrand-Rosenberg, S. (2010). Myeloid-derived suppressor cells inhibit T-cell activation by depleting cystine and cysteine. Cancer Res 70, 68-77.
34. Strome, S.E., Dong, H.D., Tamura, H.H., Voss, S.G., Flies, D.B., Tamada, K., Salomao, D., Cheville, J., Hirano, F., Lin, W., Kasperbauer, J.L., Ballman, K.V., and Chen, L. (2003). B7-H1 blockade augments adoptive T-cell immunotherapy for squamous cell carcinoma. Cancer Res 63, 6501-6505.
35. Tseng, C.W., Hung, C.F., Alvarez, R.D., Trimble, C., Huh, W.K., Kim, D., Chuang, C.M., Lin, C.T., Tsai, Y.C., He, L., Monie, A., and Wu, T.C. (2008). Pretreatment with cisplatin enhances E7-specific CD8+ T-cell-mediated antitumor immunity induced by DNA vaccination. Clin Cancer Res 14, 3185-3192.
36. Wang, L., Zhou, X., Zhou, T., Ma, D., Chen, S., Zhi, X., Yin, L., Shao, Z., Ou, Z., and Zhou, P. (2008). Ecto-5?-nucleotidase promotes invasion, migration and adhesion of human breast cancer cells. J Cancer Res Clin Oncol 134, 365-372.
37. Webster, W.S., Thompson, R.H., Harris, K.J., Frigola, X., Kuntz, S., Inman, B.A., and Dong, H. (2007). Targeting molecular and cellular inhibitory mechanisms for improvement of antitumor memory responses reactivated by tumor cell vaccine. J Immunol 179, 2860-2869.