Enhanced cancer immunotherapy using STAT3-depleted dendritic cells with high Th1-inducing ability and resistance to cancer cell-derived inhibitory factors

Journal of Immunology

Volumn 187, Issue 1, 2011, Pages 27-36

  Iwata Kajihara, Tomoko ^a   Sumimoto, Hidetoshi ^a   Kawamura, Naoshi ^a   Ueda, Ryo ^a   Takahashi, Tomomi ^a   Mizuguchi, Hiroyuki ^b   Miyagishi, Makoto ^c   Takeda, Kiyoshi ^b   Kawakami, Yutaka ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; DENDRITIC CELL VACCINE; GLYCOPROTEIN; GLYCOPROTEIN 70; INTERLEUKIN 10; INTERLEUKIN 12; SHORT HAIRPIN RNA; STAT3 PROTEIN; TOLL LIKE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1; TUMOR ANTIGEN; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CANCER IMMUNOTHERAPY; CANCER INHIBITION; COLON CARCINOMA; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TH1 CELL;

ANIMALS; CANCER VACCINES; CELL LINE, TUMOR; CELLS, CULTURED; COLONIC NEOPLASMS; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; HUMANS; IMMUNITY, INNATE; INJECTIONS, INTRALESIONAL; LYMPHOCYTE ACTIVATION; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NEOPLASM PROTEINS; STAT3 TRANSCRIPTION FACTOR; TH1 CELLS;

EID: 79960409792     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1002067     Document Type: Article

References (31)

1. Steinman, R. M., and J. Banchereau. 2007. Taking dendritic cells into medicine. Nature 449: 419-426. (Pubitemid 47509552)
2. Figdor, C. G., I. J. de Vries, W. J. Lesterhuis, and C. J. Melief. 2004. Dendritic cell immunotherapy: mapping the way. Nat. Med. 10: 475-480.
3. Palucka, A. K., H. Ueno, J. W. Fay, and J. Banchereau. 2007. Taming cancer by inducing immunity via dendritic cells. Immunol. Rev. 220: 129-150.
4. Melief, C. J. 2008. Cancer immunotherapy by dendritic cells. Immunity 29: 372-383.
5. Kawakami, Y., T. Fujita, C. Kudo, T. Sakurai, M. Udagawa, T. Yaguchi, G. Hasegawa, E. Hayashi, Y. Ueda, T. Iwata, et al. 2008. Dendritic cell based personalized immunotherapy based on cancer antigen research. Front. Biosci. 13: 1952-1958.
6. Rabinovich, G. A., D. Gabrilovich, and E. M. Sotomayor. 2007. Immunosuppressive strategies that are mediated by tumor cells. Annu. Rev. Immunol. 25: 267-296.
7. Zou, W. 2005. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat. Rev. Cancer 5: 263-274.
8. Wang, T., G. Niu, M. Kortylewski, L. Burdelya, K. Shain, S. Zhang, R. Bhattacharya, D. Gabrilovich, R. Heller, D. Coppola, et al. 2004. Regulation of the innate and adaptive immune responses by Stat-3 signaling in tumor cells. Nat. Med. 10: 48-54.
9. Yu, H., M. Kortylewski, and D. Pardoll. 2007. Crosstalk between cancer and immune cells: role of STAT3 in the tumour microenvironment. Nat. Rev. Immunol. 7: 41-51.
10. Nefedova, Y., M. Huang, S. Kusmartsev, R. Bhattacharya, P. Cheng, R. Salup, R. Jove, and D. Gabrilovich. 2004. Hyperactivation of STAT3 is involved in abnormal differentiation of dendritic cells in cancer. J. Immunol. 172: 464-474. (Pubitemid 38020502)
11. Kortylewski, M., M. Kujawski, T. Wang, S. Wei, S. Zhang, S. Pilon-Thomas, G. Niu, H. Kay, J. Mulé, W. G. Kerr, et al. 2005. Inhibiting Stat3 signaling in the hematopoietic system elicits multicomponent antitumor immunity. Nat. Med. 11: 1314-1321.
12. Nefedova, Y., P. Cheng, D. Gilkes, M. Blaskovich, A. A. Beg, S. M. Sebti, and D. I. Gabrilovich. 2005. Activation of dendritic cells via inhibition of Jak2/STAT3 signaling. J. Immunol. 175: 4338-4346.
13. Yoshimura, A., T. Naka, and M. Kubo. 2007. SOCS proteins, cytokine signalling and immune regulation. Nat. Rev. Immunol. 7: 454-465.
14. Takeda, K., B. E. Clausen, T. Kaisho, T. Tsujimura, N. Terada, I. Förster, and S. Akira. 1999. Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils. Immunity 10: 39-49. (Pubitemid 29077382)
15. Fukao, T., M. Tanabe, Y. Terauchi, T. Ota, S. Matsuda, T. Asano, T. Kadowaki, T. Takeuchi, and S. Koyasu. 2002. PI3K-mediated negative feedback regulation of IL-12 production in DCs. Nat. Immunol. 3: 875-881.
16. Marine, J. C., D. J. Topham, C. McKay, D. Wang, E. Parganas, D. Stravopodis, A. Yoshimura, and J. N. Ihle. 1999. SOCS1 deficiency causes a lymphocytedependent perinatal lethality. Cell 98: 609-616.
17. Alexander, W. S., R. Starr, J. E. Fenner, C. L. Scott, E. Handman, N. S. Sprigg, J. E. Corbin, A. L. Cornish, R. Darwiche, C. M. Owczarek, et al. 1999. SOCS1 is a critical inhibitor of interferon gamma signaling and prevents the potentially fatal neonatal actions of this cytokine. Cell 98: 597-608. (Pubitemid 29418951)
18. Hanada, T., K. Tanaka, Y. Matsumura, M. Yamauchi, H. Nishinakamura, H. Aburatani, R. Mashima, M. Kubo, T. Kobayashi, and A. Yoshimura. 2005. Induction of hyper Th1 cell-type immune responses by dendritic cells lacking the suppressor of cytokine signaling-1 gene. J. Immunol. 174: 4325-4332. (Pubitemid 40396015)
19. Shen, L., K. Evel-Kabler, R. Strube, and S. Y. Chen. 2004. Silencing of SOCS1 enhances antigen presentation by dendritic cells and antigen-specific anti-tumor immunity. Nat. Biotechnol. 22: 1546-1553.
20. Cheng, F., H. W. Wang, A. Cuenca, M. Huang, T. Ghansah, J. Brayer, W. G. Kerr, K. Takeda, S. Akira, S. P. Schoenberger, et al. 2003. A critical role for Stat3 signaling in immune tolerance. Immunity 19: 425-436. (Pubitemid 37153418)
21. Staveley-O'Carroll, K., E. Sotomayor, J. Montgomery, I. Borrello, L. Hwang, S. Fein, D. Pardoll, and H. Levitsky. 1998. Induction of antigen-specific T cell anergy: An early event in the course of tumor progression. Proc. Natl. Acad. Sci. USA 95: 1178-1183.
22. Bogen, B. 1996. Peripheral T cell tolerance as a tumor escape mechanism: deletion of CD4+ T cells specific for a monoclonal immunoglobulin idiotype secreted by a plasmacytoma. Eur. J. Immunol. 26: 2671-2679.
23. Sinha, P., V. K. Clements, S. K. Bunt, S. M. Albelda, and S. Ostrand-Rosenberg. 2007. Cross-talk between myeloid-derived suppressor cells and macrophages subverts tumor immunity toward a type 2 response. J. Immunol. 179: 977-983.
24. Sumimoto, H., S. Yamagata, A. Shimizu, H. Miyoshi, H. Mizuguchi, T. Hayakawa, M. Miyagishi, K. Taira, and Y. Kawakami. 2005. Gene therapy for human small-cell lung carcinoma by inactivation of Skp-2 with virally mediated RNA interference. Gene Ther. 12: 95-100. (Pubitemid 40090049)
25. Mizuguchi, H., and M. A. Kay. 1998. Efficient construction of a recombinant adenovirus vector by an improved in vitro ligation method. Hum. Gene Ther. 9: 2577-2583.
26. Hoentjen, F., R.B. Sartor, M. Ozaki, and C. Jobin. 2005. STAT3 regulates NF-kappaB recruitment to the IL-12p40 promoter in dendritic cells. Blood 105: 689-696. (Pubitemid 40070754)
27. Mizuguchi, H., and T. Hayakawa. 2002. Adenovirus vectors containing chimeric type 5 and type 35 fiber proteins exhibit altered and expanded tropism and increase the size limit of foreign genes. Gene 285: 69-77. (Pubitemid 34246322)
28. Sumimoto, H., F. Imabayashi, T. Iwata, and Y. Kawakami. 2006. The BRAFMAPK signaling pathway is essential for cancer-immune evasion in human melanoma cells. J. Exp. Med. 203: 1651-1656.
29. Clausen, B. E., C. Burkhardt, W. Reith, R. Renkawitz, and I. Förster. 1999. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 8: 265-277. (Pubitemid 29523965)
30. Udagawa, M., C. Kudo-Saito, G. Hasegawa, K. Yano, A. Yamamoto, M. Yaguchi, M. Toda, I. Azuma, T. Iwai, and Y. Kawakami. 2006. Enhancement of immunologic tumor regression by intratumoral administration of dendritic cells in combination with cryoablative tumor pretreatment and Bacillus Calmette-Guerin cell wall skeleton stimulation. Clin. Cancer Res. 12: 7465-7475.
31. Tacken, P. J., I. J. de Vries, K. Gijzen, B. Joosten, D. Wu, R. P. Rother, S. J. Faas, C. J. A. Punt, R. Torensma, G. J. Adema, and C. G. Figdor. 2005. Effective induction of naive and recall T-cell responses by targeting antigen to human dendritic cells via a humanized anti-DC-SIGN antibody. Blood 106: 1278-1285.