Enhancement of fibroblast activation protein α-based vaccines and adenovirus boost immunity by cyclophosphamide through inhibiting IL-10 expression in 4T1 tumor bearing mice

Vaccine

Volumn 34, Issue 38, 2016, Pages 4526-4535

  Xia, Qiu ^a   Geng, Fei ^a   Zhang, Fang Fang ^a   Liu, Chen Lu ^a   Xu, Ping ^a   Lu, Zhen Zhen ^a   Zhang, Hai Hong ^a   Kong, Wei ^a   Yu, Xiang Hui ^a  

^a JILIN UNIVERSITY   (China)

Author keywords

Cancer vaccine; Cyclophosphamide; Fibroblast activation protein ; Immunosuppression; Interleukin 10; Prime boost strategy

Indexed keywords

ADENOVIRUS VECTOR; CANCER VACCINE; CYCLOPHOSPHAMIDE; INTERLEUKIN 10; SEPRASE; DNA VACCINE; GELATINASE; MEMBRANE PROTEIN; SERINE PROTEINASE;

ADENOVIRIDAE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BAGG ALBINO MOUSE; BREAST CANCER; CANCER ASSOCIATED FIBROBLAST; CANCER INHIBITION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFECT; DRUG INHIBITION; EMBRYO; FEMALE; FIBROBLAST; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOPOTENTIATION; IMMUNOSUPPRESSIVE TREATMENT; LOW DRUG DOSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SURVIVAL TIME; TUMOR IMMUNITY; VACCINATION; ANIMAL; ANTAGONISTS AND INHIBITORS; GENE VECTOR; IMMUNOLOGY; NEOPLASMS, EXPERIMENTAL; SECONDARY IMMUNIZATION; T LYMPHOCYTE; TUMOR CELL LINE; TUMOR MICROENVIRONMENT;

ADENOVIRIDAE; ANIMALS; CANCER VACCINES; CELL LINE, TUMOR; CYCLOPHOSPHAMIDE; FEMALE; FIBROBLASTS; GELATINASES; GENETIC VECTORS; IMMUNITY, CELLULAR; IMMUNIZATION, SECONDARY; INTERLEUKIN-10; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; NEOPLASMS, EXPERIMENTAL; SERINE ENDOPEPTIDASES; T-LYMPHOCYTES; TUMOR MICROENVIRONMENT; VACCINES, DNA;

EID: 84996526188     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2016.07.054     Document Type: Article

References (34)

1. [1] Micke, P., Tumour-stroma interaction: cancer-associated fibroblasts as novel targets in anti-cancer therapy?. Lung Cancer 45 (2004), S163–S175.
2. [2] Östman, A., Augsten, M., Cancer-associated fibroblasts and tumor growth–bystanders turning into key players. Curr Opin Genet Dev 19:1 (2009), 67–73.
3. [3] Kalluri, R., Zeisberg, M., Fibroblasts in cancer. Nat Rev Cancer 6:5 (2006), 392–401.
4. [4] Ribatti, D., Vacca, A., The role of microenvironment in tumor angiogenesis. Genes Nutr 3:1 (2008), 29–34.
5. [5] Acharya, P.S., Zukas, A., Chandan, V., Katzenstein, A.-L.A., Puré, E., Fibroblast activation protein: a serine protease expressed at the remodeling interface in idiopathic pulmonary fibrosis. Hum Pathol 37:3 (2006), 352–360.
6. [6] Goldstein, L.A., Ghersi, G., Piñeiro-Sánchez, M.L., Salamone, M., Yeh, Y., Flessate, D., et al. Molecular cloning of seprase: a serine integral membrane protease from human melanoma. Biochim Biophys Acta (BBA)-Mol Basis Disease 1361:1 (1997), 11–19.
7. [7] Liu, R., Li, H., Liu, L., Yu, J., Ren, X., Fibroblast activation protein: a potential therapeutic target in cancer. Cancer Biol Ther 13:3 (2012), 123–129.
8. [8] Fearon, D.T., The carcinoma-associated fibroblast expressing fibroblast activation protein and escape from immune surveillance. Cancer Immunol Res 2:3 (2014), 187–193.
9. [9] Fassnacht, M., Lee, J., Milazzo, C., Boczkowski, D., Su, Z., Nair, S., et al. Induction of CD4+ and CD8+ T-cell responses to the human stromal antigen, fibroblast activation protein: implication for cancer immunotherapy. Clin Cancer Res 11:15 (2005), 5566–5571.
10. [10] Nguyen, T., Urban, J., Kalinski, P., Therapeutic cancer vaccines and combination immunotherapies involving vaccination. ImmunoTargets Ther 3 (2014), 135–150.
11. [11] Kraman, M., Bambrough, P.J., Arnold, J.N., Roberts, E.W., Magiera, L., Jones, J.O., et al. Suppression of antitumor immunity by stromal cells expressing fibroblast activation protein–α. Science 330:6005 (2010), 827–830.
12. [12] Prud'homme, G.J., DNA vaccination against tumors. J Gene Med 7:1 (2005), 3–17.
13. [13] Lee, J., Fassnacht, M., Nair, S., Boczkowski, D., Gilboa, E., Tumor immunotherapy targeting fibroblast activation protein, a product expressed in tumor-associated fibroblasts. Cancer Res 65:23 (2005), 11156–11163.
14. [14] Liao, D., Luo, Y., Markowitz, D., Xiang, R., Reisfeld, R.A., Cancer associated fibroblasts promote tumor growth and metastasis by modulating the tumor immune microenvironment in a 4T1 murine breast cancer model. PLoS ONE, 4(11), 2009, e7965.
15. [15] Loeffler, M., Kruger, J.A., Niethammer, A.G., Reisfeld, R.A., Targeting tumor-associated fibroblasts improves cancer chemotherapy by increasing intratumoral drug uptake. J Clin Invest 116:7 (2006 Jul), 1955–1962.
16. [16] Barouch, D.H., Novel adenovirus vector-based vaccines for HIV-1. Curr Opin HIV AIDS 5:5 (2010), 386–390.
17. [17] Johnson, M.J., Petrovas, C., Yamamoto, T., Lindsay, R.W., Loré, K., Gall, J.G., et al. Type I IFN induced by adenovirus serotypes 28 and 35 has multiple effects on T cell immunogenicity. J Immunol 188:12 (2012), 6109–6118.
18. [18] Zhang, H., Wang, Y., Liu, C., Zhang, L., Xia, Q., Zhang, Y., et al. DNA and adenovirus tumor vaccine expressing truncated survivin generates specific immune responses and anti-tumor effects in a murine melanoma model. Cancer Immunol, Immunother 61:10 (2012), 1857–1867.
19. [19] Dennis, K.L., Blatner, N.R., Gounari, F., Khazaie, K., Current status of IL-10 and regulatory T-cells in cancer. Curr Opin Oncol, 25(6), 2013, 637.
20. [20] Joyce, J.A., Fearon, D.T., T cell exclusion, immune privilege, and the tumor microenvironment. Science 348:6230 (2015), 74–80.
21. [21] Sistigu, A., Viaud, S., Chaput, N., Bracci, L., Proietti, E., Zitvogel, L., Immunomodulatory effects of cyclophosphamide and implementations for vaccine design. Semin Immunopathol 33:4 (2011), 369–383.
22. [22] Matar, P., Rozados, V.R., Gervasoni, S.I., Scharovsky, O.G., Down regulation of T-cell-derived IL-10 production by low-dose cyclophosphamide treatment in tumor-bearing rats restores in vitro normal lymphoproliferative response. Int Immunopharmacol 1:2 (2001), 307–319.
23. [23] Son, C.-H., Bae, J.-H., Lee, H.-R., Shin, D.-Y., Yang, K., Park, Y.-S., Enhanced dendritic cell–based immunotherapy using low-dose cyclophosphamide and CD25-targeted antibody for transplanted lewis lung carcinoma cells. J Immunother 38:3 (2015), 107–115.
24. [24] Chen, X., Yang, Y., Zhou, Q., Weiss, J.M., Howard, O.Z., McPherson, J.M., et al. Effective chemoimmunotherapy with anti-TGFβ antibody and cyclophosphamide in a mouse model of breast cancer. PLoS ONE, 9, 2014, e85398.
25. [25] Hofmann, E., Weibel, S., Szalay, A.A., Combination treatment with oncolytic Vaccinia virus and cyclophosphamide results in synergistic antitumor effects in human lung adenocarcinoma bearing mice. J Trans Med, 12(1), 2014, 197.
26. [26] You, Q., Jiang, C., Wu, Y., Yu, X., Chen, Y., Zhang, X., et al. Subcutaneous administration of modified vaccinia virus ankara expressing an Ag85B-ESAT6 fusion protein, but not an adenovirus-based vaccine, protects mice against intravenous challenge with mycobacterium tuberculosis. Scand J Immunol 75:1 (2012), 77–84.
27. [27] Lladser, A., Ljungberg, K., Tufvesson, H., Tazzari, M., Roos, A.-K., Quest, A.F., et al. Intradermal DNA electroporation induces survivin-specific CTLs, suppresses angiogenesis and confers protection against mouse melanoma. Cancer Immunol, Immunother 59:1 (2010), 81–92.
28. [28] Nagaraj, S., Pisarev, V., Kinarsky, L., Sherman, S., Muro-Cacho, C., Altieri, D.C., et al. Dendritic cell-based full-length survivin vaccine in treatment of experimental tumors. J Immunother 30:2 (2007), 169–179.
29. [29] Wang, Y.-Q., Zhang, H.-H., Liu, C.-L., Wu, H., Wang, P., Xia, Q., et al. Enhancement of survivin-specific anti-tumor immunity by adenovirus prime protein-boost immunity strategy with DDA/MPL adjuvant in a murine melanoma model. Int Immunopharmacol 17:1 (2013), 9–17.
30. [30] Chen, M., Xiang, R., Wen, Y., Xu, G., Wang, C., Luo, S., et al. A whole-cell tumor vaccine modified to express fibroblast activation protein induces antitumor immunity against both tumor cells and cancer-associated fibroblasts. Sci Rep, 5, 2015, 14421.
31. [31] Wen, Y., Wang, C.T., Ma, T.T., Li, Z.Y., Zhou, L.N., Mu, B., et al. Immunotherapy targeting fibroblast activation protein inhibits tumor growth and increases survival in a murine colon cancer model. Cancer Sci 101:11 (2010), 2325–2332.
32. [32] Devaud, C., John, L.B., Westwood, J.A., Darcy, P.K., Kershaw, M.H., Immune modulation of the tumor microenvironment for enhancing cancer immunotherapy. Oncoimmunology, 2(8), 2013, e25961.
33. [33] Casey, S.C., Amedei, A., Aquilano, K., Azmi, A.S., Benencia, F., Bhakta, D., et al. Cancer prevention and therapy through the modulation of the tumor microenvironment. Semin Cancer Biol(Suppl), 2015, S199–S223.
34. [34] LeBleu, V.S., Imaging the tumor microenvironment. Cancer J 21:3 (2015), 174–178.