Cyclophosphamide Potentiates the Antitumor Effect of Immunization with Injection of Immature Dendritic Cells into Irradiated Tumor

REFERENCES

• Asavaroengchai, W., Kotera, Y., Mule, J. J. (2002). Tumor lysate-pulsed dendritic cells can elicit an effective antitumor immune response during early lymphoid recovery. Proc. Natl. Acad. Sci. USA 99:931–936.
   PubMed Web of Science ®Google Scholar
• Askenase, P. W., Hayden, B. J., Gershon, R. K. (1975). Augmentation of delayed-type hypersensitivity by doses of cyclophosphamide which do not affect antibody responses. J. Exp. Med. 141:697–702.
   PubMed Web of Science ®Google Scholar
• Banchereau, J., Palucka, A. K. (2005). Dendritic cells as therapeutic vaccines against cancer. Nat. Rev. Immunol. 5:296–306.
   PubMed Web of Science ®Google Scholar
• Banerjee, D. K., Dhodapkar, M. V., Matayeva, E., Steinman, R. M., Dhodapkar, K. M. (2006). Expansion of FOXP3high regulatory T cells by human dendritic cells (DCs) in vitro and after injection of cytokine-matured DCs in myeloma patients. Blood 108:2655–2661.
   PubMed Web of Science ®Google Scholar
• Berd, D., Maguire, H. C., Jr., Mastrangelo, M. J. (1986). Induction of cell-mediated immunity to autologous melanoma cells and regression of metastases after treatment with a melanoma cell vaccine preceded by cyclophosphamide. Cancer Res. 46:2572–2577.
   PubMed Web of Science ®Google Scholar
• Berd, D., Mastrangelo, M. J. (1988). Effect of low dose cyclophosphamide on the immune system of cancer patients: depletion of CD4+, 2H4+ suppressor-inducer T-cells. Cancer Res. 48:1671–1675.
   PubMed Web of Science ®Google Scholar
• Boissier, M. C., Assier, E., Biton, J., Denys, A., Falgarone, G., Bessis, N. (2009). Regulatory T cells (Treg) in rheumatoid arthritis. Joint Bone Spine 76:10–14.
   PubMed Web of Science ®Google Scholar
• Bracci, L., Moschella, F., Sestili, P., La Sorsa, V., Valentini, M., Canini, I., Baccarini, S., Maccari, S., Ramoni, C., Belardelli, F., and others (2007). Cyclophosphamide enhances the antitumor efficacy of adoptively transferred immune cells through the induction of cytokine expression, B-cell and T-cell homeostatic proliferation, and specific tumor infiltration. Clin. Cancer Res. 13:644–653.
   PubMed Web of Science ®Google Scholar
• Campbell, D. J., Ziegler, S. F. (2007). FOXP3 modifies the phenotypic and functional properties of regulatory T cells. Nat. Rev. Immunol. 7:305–310.
   PubMed Web of Science ®Google Scholar
• Cao, M., Cabrera, R., Xu, Y., Liu, C., Nelson, D. (2009). Gamma irradiation alters the phenotype and function of CD4+CD25+ regulatory T cells. Cell. Biol. Int.33:565–571.
   PubMed Web of Science ®Google Scholar
• Chi, K. H., Liu, S. J., Li, C. P., Kuo, H. P., Wang, Y. S., Chao, Y., Hsieh, S. L. (2005). Combination of conformal radiotherapy and intratumoral injection of adoptive dendritic cell immunotherapy in refractory hepatoma. J. Immunother. 28:129–135.
   PubMed Web of Science ®Google Scholar
• Cools, N., Ponsaerts, P., Van Tendeloo, V. F., Berneman, Z. N. (2007). Regulatory T cells and human disease. Clin. Dev. Immunol. 2007:891–895.
   Google Scholar
• Curiel, T. J., Coukos, G., Zou, L., Alvarez, X., Cheng, P., Mottram, P., Evdemon-Hogan, M., Conejo-Garcia, J. R., Zhang, L., Burow, M., and others (2004). Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med. 10:942–949.
   PubMed Web of Science ®Google Scholar
• Davis, I. D., Jefford, M., Parente, P., Cebon, J. (2003). Rational approaches to human cancer immunotherapy. J. Leukoc. Biol. 73:3–9.
   PubMed Web of Science ®Google Scholar
• Demaria, S., Ng, B., Devitt, M. L., Babb, J. S., Kawashima, N., Liebes, L., Formenti, S. C. (2004). Ionizing radiation inhibition of distant untreated tumors (abscopal effect) is immune mediated. Int. J. Radiat. Oncol. Biol. Phys. 58:862–870.
   PubMed Web of Science ®Google Scholar
• Fong, L. E. E. (2000). Dendritic cells in cancer immunotherapy. Annu. Rev. Immunol 18:245–273.
   PubMed Web of Science ®Google Scholar
• Formenti, S. C., Demaria, S. (2008). Local control by radiotherapy: Is that all there is? Breast Cancer Res. 10:215.
   PubMed Web of Science ®Google Scholar
• Formenti, S. C., Demaria, S. (2009). Systemic effects of local radiotherapy. Lancet Oncol. 10:718–726.
   PubMed Web of Science ®Google Scholar
• Ghiringhelli, F., Menard, C., Puig, P. E., Ladoire, S., Roux, S., Martin, F., Solary, E., Le Cesne, A., Zitvogel, L., Chauffert, B. (2007). Metronomic cyclophosphamide regimen selectively depletes CD4+CD25+ regulatory T cells and restores T and NK effector functions in end stage cancer patients. Cancer Immunol. Immunother. 56:641–648.
   PubMed Web of Science ®Google Scholar
• Gilboa, E., Nair, S. K., Lyerly, H. K. (1998). Immunotherapy of cancer with dendritic-cell-based vaccines. Cancer Immunol. Immunother. 46:82–87.
   PubMed Web of Science ®Google Scholar
• Gochi, A., Orita, K., Fuchimoto, S., Tanaka, N., Ogawa, N. (2001). The prognostic advantage of preoperative intratumoral injection of OK-432 for gastric cancer patients. Br. J. Cancer 84:443–451.
   PubMedGoogle Scholar
• Hegde, U., Chhabra, A., Chattopadhyay, S., Das, R., Ray, S., Chakraborty, N. G. (2008). Presence of low dose of fludarabine in cultures blocks regulatory T cell expansion and maintains tumor-specific cytotoxic T lymphocyte activity generated with peripheral blood lymphocytes. Pathobiology 75:200–208.
   PubMed Web of Science ®Google Scholar
• Holtl, L., Ramoner, R., Zelle-Rieser, C., Gander, H., Putz, T., Papesh, C., Nussbaumer, W., Falkensammer, C., Bartsch, G., Thurnher, M. (2005). Allogeneic dendritic cell vaccination against metastatic renal cell carcinoma with or without cyclophosphamide. Cancer Immunol. Immunother. 54:663–670.
   PubMed Web of Science ®Google Scholar
• Hoon, D. S., Foshag, L. J., Nizze, A. S., Bohman, R., Morton, D. L. (1990). Suppressor cell activity in a randomized trial of patients receiving active specific immunotherapy with melanoma cell vaccine and low dosages of cyclophosphamide. Cancer Res. 50:5358–5364.
   PubMed Web of Science ®Google Scholar
• Huang, J., Wang, Y., Guo, J., Lu, H., Lin, X., Ma, L., Teitz-Tennenbaum, S., Chang, A. E., Li, Q. (2007). Radiation-induced apoptosis along with local and systemic cytokine elaboration is associated with DC plus radiotherapy-mediated renal cell tumor regression. Clin. Immunol. 123:298–310.
   PubMedGoogle Scholar
• Itoh, T., Ueda, Y., Okugawa, K., Fujiwara, H., Fuji, N., Yamashita, T., Fujiki, H., Harada, S., Yoshimura, T., Yamagishi, H (2003). Streptococcal preparation OK432 promotes functional maturation of human monocyte-derived dendritic cells. Cancer Immunol. Immunother. 52:207–214.
   PubMedGoogle Scholar
• Kikkawa, F., Kawai, M., Oguchi, H., Kojima, M., Ishikawa, H., Iwata, M., Maeda, O., Tomoda, Y., Arii, Y., Kuzuya, K., and others (1993) Randomised study of immunotherapy with OK-432 in uterine cervical carcinoma. Eur. J. Cancer 29A:1542–1546.
   Google Scholar
• Kim, K. W. K. S., Shin, J. G., . (2004). Direct injection of immature dendritic cells into irradiated tumor induces efficient antitumor immunity. I. J. Cancer 109:685–690.
   PubMed Web of Science ®Google Scholar
• Kuroki, H., Morisaki, T., Matsumoto, K., Onishi, H., Baba, E., Tanaka, M., Katano, M. (2003). Streptococcal preparation OK-432: A new maturation factor of monocyte-derived dendritic cells for clinical use. Cancer Immunol. Immunother. 52:561–568.
   PubMedGoogle Scholar
• Lissoni, P., Brivio, F., Fumagalli, L., Messina, G., Meregalli, S., Porro, G., Rovelli, F., Vigore, L., Tisi, E., D'Amico, G. (2009). Effects of the conventional antitumor therapies surgery, chemotherapy, radiotherapy and immunotherapy on regulatory T lymphocytes in cancer patients. Anticancer Res. 29:1847–1852.
   PubMed Web of Science ®Google Scholar
• Liu, J. Y., Wu, Y., Zhang, X. S., Yang, J. L., Li, H. L., Mao, Y. Q., Wang, Y., Cheng, X., Li, Y. Q., Xia, J. C., and others (2007). Single administration of low dose cyclophosphamide augments the antitumor effect of dendritic cell vaccine. Cancer Immunol. Immunother. 56:1597–1604.
   PubMed Web of Science ®Google Scholar
• Liyanage, U. K., Moore, T. T., Joo, H. G., Tanaka, Y., Herrmann, V., Doherty, G., Drebin, J. A., Strasberg, S. M., Eberlein, T. J., Goedegebuure, P. S., and others (2002). Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma. J. Immunol. 169:2756–2761.
   PubMed Web of Science ®Google Scholar
• Lizee, G., Radvanyi, L. G., Overwijk, W. W., Hwu, P. (2006). Improving antitumor immune responses by circumventing immunoregulatory cells and mechanisms. Clin Cancer Res. 12:4794–4803.
   PubMed Web of Science ®Google Scholar
• Lutsiak, M. E., Semnani, R. T., De Pascalis, R., Kashmiri, S. V., Schlom, J., Sabzevari, H. (2005). Inhibition of CD4(+)25+ T regulatory cell function implicated in enhanced immune response by low-dose cyclophosphamide. Blood 105:2862–2868.
   PubMed Web of Science ®Google Scholar
• Machiels, J. P., Reilly, R. T., Emens, L. A., Ercolini, A. M., Lei, R. Y., Weintraub, D., Okoye, F. I., Jaffee, E. M. (2001). Cyclophosphamide, doxorubicin, and paclitaxel enhance the antitumor immune response of granulocyte/macrophage-colony stimulating factor-secreting whole-cell vaccines in HER-2/neu tolerized mice. Cancer Res. 61:3689–3697.
   PubMed Web of Science ®Google Scholar
• Marson, A., Kretschmer, K., Frampton, G. M., Jacobsen, E. S., Polansky, J. K., MacIsaac, K. D., Levine, S. S., Fraenkel, E., von Boehmer, H., Young, R. A. (2007). Foxp3 occupancy and regulation of key target genes during T-cell stimulation. Nature 445:931–935.
   PubMed Web of Science ®Google Scholar
• Mitsuoka, A., Baba, M., Morikawa, S. (1976). Enhancement of delayed hypersensitivity by depletion of suppressor T cells with cyclophosphamide in mice. Nature 262:77–78.
   PubMed Web of Science ®Google Scholar
• Motoyoshi, Y., Kaminoda, K., Saitoh, O., Hamasaki, K., Nakao, K., Ishii, N., Nagayama, Y., Eguchi, K (2006). Different mechanisms for anti-tumor effects of low- and high-dose cyclophosphamide. Oncol. Rep. 16:141–146.
   PubMed Web of Science ®Google Scholar
• Nakahara, S., Tsunoda, T., Baba, T., Asabe, S., Tahara, H. (2003). Dendritic cells stimulated with a bacterial product, OK-432, efficiently induce cytotoxic T lymphocytes specific to tumor rejection peptide. Cancer Res. 63:4112–4118.
   PubMed Web of Science ®Google Scholar
• Nakai, N., Katoh, N., Kitagawa, T., Ueda, E., Takenaka, H., Kishimoto, S. (2009). Immunoregulatory T cells in the peripheral blood of melanoma patients treated with melanoma antigen-pulsed mature monocyte-derived dendritic cell vaccination. J. Dermatol. Sci. 54:31–37.
   PubMedGoogle Scholar
• Nakamura, K., Kitani, A., Strober, W. (2001) Cell contact-dependent immunosuppression by CD4(+)CD25(+) regulatory T cells is mediated by cell surface-bound transforming growth factor beta. J. Exp. Med. 194:629–644.
   PubMed Web of Science ®Google Scholar
• Nencioni, A., Brossart, P. (2004). Cellular immunotherapy with dendritic cells in cancer: current status. Stem Cells 22:501–13.
   Google Scholar
• Okamoto, M., Furuichi, S., Nishioka, Y., Oshikawa, T., Tano, T., Ahmed, S. U., Takeda, K., Akira, S., Ryoma, Y., Moriya, Y., and others (2004). Expression of toll-like receptor 4 on dendritic cells is significant for anticancer effect of dendritic cell-based immunotherapy in combination with an active component of OK-432, a streptococcal preparation. Cancer Res. 64:5461–5470.
   PubMedGoogle Scholar
• Ono, T., Harada, M., Yamada, A., Tanaka, M., Takao, Y., Tanaka, Y., Mine, T., Sakamoto, K., Nakashima, T., Itoh, K. (2006). Antitumor effects of systemic and local immunization with a CTL-directed peptide in combination with a local injection of OK-432. Clin. Cancer Res. 12:1325–1332.
   PubMedGoogle Scholar
• Reits, E. A., Hodge, J. W., Herberts, C. A., Groothuis, T. A., Chakraborty, M., Wansley, E. K., Camphausen, K., Luiten, R. M., de Ru, A. H., Neijssen, J., and others (2006). Radiation modulates the peptide repertoire, enhances MHC class I expression, and induces successful antitumor immunotherapy. J. Exp. Med. 203:1259–1271.
   PubMed Web of Science ®Google Scholar
• Schmidtner, J., Distel, L. V., Ott, O. J., Nkenke, E., Sprung, C. N., Fietkau, R., Lubgan, D. (2009). Hyperthermia and irradiation of head and neck squamous cancer cells causes migratory profile changes of tumour infiltrating lymphocytes. Int. J. Hyperthermia 25:347–354.
   PubMed Web of Science ®Google Scholar
• Smyth, M. J., Cretney, E., Kershaw, M. H., Hayakawa, Y. (2004) Cytokines in cancer immunity and immunotherapy. Immunol. Rev. 202:275–293.
   PubMed Web of Science ®Google Scholar
• Taieb, J., Chaput, N., Schartz, N., Roux, S., Novault, S., Menard, C., Ghiringhelli, F., Terme, M., Carpentier, A. F., Darrasse-Jeze, G., and others (2006). Chemoimmunotherapy of tumors: Cyclophosphamide synergizes with exosome based vaccines. J. Immunol. 176:2722–2729.
   PubMed Web of Science ®Google Scholar
• Teitz-Tennenbaum, S., Li, Q., Rynkiewicz, S., Ito, F., Davis, M. A., McGinn, C. J., Chang, A. E. (2003). Radiotherapy potentiates the therapeutic efficacy of intratumoral dendritic cell administration. Cancer Res. 63:8466–8475.
   PubMed Web of Science ®Google Scholar
• van der Vliet, H. J., Koon, H. B., Atkins, M. B., Balk, S. P., Exley, M. A. (2007) Exploiting regulatory T-cell populations for the immunotherapy of cancer. J. Immunother. 30:591–595.
   PubMed Web of Science ®Google Scholar
• Vierboom, M. P., Bos, G. M., Ooms, M., Offringa, R., Melief, C. J. (2000). Cyclophosphamide enhances anti-tumor effect of wild-type p53-specific CTL. Int. J. Cancer 87:253–260.
   PubMed Web of Science ®Google Scholar
• Vignali, D. A., Collison, L. W., Workman, C. J. (2008). How regulatory T cells work. Nat Rev Immunol. 8:523–532.
   PubMed Web of Science ®Google Scholar
• Viguier, M., Lemaitre, F., Verola, O., Cho, M. S., Gorochov, G., Dubertret, L., Bachelez, H., Kourilsky, P., Ferradini, L. (2004). Foxp3 expressing CD4+CD25(high) regulatory T cells are overrepresented in human metastatic melanoma lymph nodes and inhibit the function of infiltrating T cells. J. Immunol. 173:1444–1453.
   PubMed Web of Science ®Google Scholar
• Watanabe, Y., Iwa, T. (1987). Clinical value of immunotherapy with the streptococcal preparation OK-432 in non-small cell lung cancer. J. Biol. Response Mod. 6:169–180.
   PubMedGoogle Scholar
• Woo, E. Y., Chu, C. S., Goletz, T. J., Schlienger, K., Yeh, H., Coukos, G., Rubin, S. C., Kaiser, L. R., June, C. H. (2001). Regulatory CD4(+)CD25(+) T cells in tumors from patients with early-stage non-small cell lung cancer and late-stage ovarian cancer. Cancer Res. 61:4766–4772.
   PubMed Web of Science ®Google Scholar
• Yokokawa, J., Cereda, V., Remondo, C., Gulley, J. L., Arlen, P. M., Schlom, J., Tsang, K. Y. (2008). Enhanced functionality of CD4+CD25(high)FoxP3+ regulatory T cells in the peripheral blood of patients with prostate cancer. Clin. Cancer Res. 14:1032–1040.
   PubMed Web of Science ®Google Scholar
• Zanoni, I., Granucci, F., Foti, M., Ricciardi-Castagnoli, P. (2007). Self-tolerance, dendritic cell (DC)-mediated activation and tissue distribution of natural killer (NK) cells. Immunol. Lett. 110:6–17.
   PubMed Web of Science ®Google Scholar
• Zou, W. (2006). Regulatory T cells, tumour immunity and immunotherapy. Nat. Rev. Immunol. 6:295–307.
   PubMed Web of Science ®Google Scholar