Adenovirus expressing both thymidine kinase and soluble PD1 enhances antitumor immunity by strengthening CD8 T-cell response

Molecular Therapy

Volumn 21, Issue 3, 2013, Pages 688-695

  Shin, Seung Pil ^a,b   Seo, Hye Hyun ^a   Shin, Jae Hun ^a   Park, Hyung Bae ^a   Lim, Dong Pyo ^a   Eom, Hyeon Seok ^a   Bae, Yong Soo ^b   Kim, In Hoo ^a   Choi, Kyungho ^a,c   Lee, Sang Jin ^a  

^a National Cancer Center   (South Korea)

^b Sungkyunkwan University   (South Korea)

^c Seoul National University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; PROGRAMMED DEATH 1 RECEPTOR; TELOMERASE REVERSE TRANSCRIPTASE; THYMIDINE KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER GENE THERAPY; CANCER INHIBITION; CANCER REGRESSION; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DENDRITIC CELL; DRUG CYTOTOXICITY; FEMALE; MOUSE; NONHUMAN; PROTEIN DOMAIN; PROTEIN SECRETION; T CELL DEPLETION; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; VIRAL GENE THERAPY; VIRUS EXPRESSION;

ADENOVIRIDAE; MURINAE; MUS; SIMPLEXVIRUS;

EID: 84875214418     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2012.252     Document Type: Article

References (44)

1. Hong, SH, Jeong, JS, Lee, YJ, Jung, HI, Cho, KS, Kim, CM et al. (2008). in vivo reprogramming of hTERT by trans-splicing ribozyme to target tumor cells. Mol Ther 16: 74-80.
2. Jeong, JS, Lee, SW, Hong, SH, Lee, YJ, Jung, HI, Cho, KS et al. (2008). Antitumor effects of systemically delivered adenovirus harboring trans-splicing ribozyme in intrahepatic colon cancer mouse model. Clin Cancer Res 14: 281-290.
3. Abate-Daga, D, Garcia-Rodríguez, L, Sumoy, L and Fillat, C (2010). Cell cycle control pathways act as conditioning factors for TK/GCV sensitivity in pancreatic cancer cells. Biochim Biophys Acta 1803: 1175-1185.
4. Chen, SH, Shine, HD, Goodman, JC, Grossman, RG and Woo, SL (1994). Gene therapy for brain tumors: regression of experimental gliomas by adenovirus-mediated gene transfer in vivo. Proc Natl Acad Sci USA 91: 3054-3057.
5. Smythe, WR, Hwang, HC, Amin, KM, Eck, SL, Davidson, BL, Wilson, JM et al. (1994). Use of recombinant adenovirus to transfer the herpes simplex virus thymidine kinase (HSVtk) gene to thoracic neoplasms: an effective in vitro drug sensitization system. Cancer Res 54: 2055-2059.
6. Tomicic, MT, Thust, R and Kaina, B (2002). Ganciclovir-induced apoptosis in HSV-1 thymidine kinase expressing cells: critical role of DNA breaks, Bcl-2 decline and caspase-9 activation. Oncogene 21: 2141-2153.
7. Barba, D, Hardin, J, Sadelain, M and Gage, FH (1994). Development of anti-tumor immunity following thymidine kinase-mediated killing of experimental brain tumors. Proc Natl Acad Sci USA 91: 4348-4352.
8. Kuriyama, S, Kikukawa, M, Masui, K, Okuda, H, Nakatani, T, Akahane, T et al. (1999). Cancer gene therapy with HSV-tk/GCV system depends on T-cell-mediated immune responses and causes apoptotic death of tumor cells in vivo. Int J Cancer 83: 374-380.
9. Okada, T, Shah, M, Higginbotham, JN, Li, Q, Wildner, O, Walbridge, S et al. (2001). AV.TK-mediated killing of subcutaneous tumors in situ results in effective immunization against established secondary intracranial tumor deposits. Gene Ther 8: 1315-1322.
10. Ghulam Muhammad, AK, Candolfi, M, King, GD, Yagiz, K, Foulad, D, Mineharu, Y et al. (2009). Antiglioma immunological memory in response to conditional cytotoxic/immune-stimulatory gene therapy: humoral and cellular immunity lead to tumor regression. Clin Cancer Res 15: 6113-6127.
11. King, GD, Muhammad, AK, Larocque, D, Kelson, KR, Xiong, W, Liu, C et al. (2011). Combined Flt3L/TK gene therapy induces immunological surveillance which mediates an immune response against a surrogate brain tumor neoantigen. Mol Ther 19: 1793-1801.
12. Brockstedt, DG, Diagana, M, Zhang, Y, Tran, K, Belmar, N, Meier, M et al. (2002). Development of anti-tumor immunity against a non-immunogenic mammary carcinoma through in vivo somatic GM-CSF, IL-2, and HSVtk combination gene therapy. Mol Ther 6: 627-636.
13. Rabinovich, GA, Gabrilovich, D and Sotomayor, EM (2007). Immunosuppressive strategies that are mediated by tumor cells. Annu Rev Immunol 25: 267-296.
14. Li, MO and Flavell, RA (2008). TGF-beta: a master of all T cell trades. Cell 134: 392-404.
15. Phan, GQ, Yang, JC, Sherry, RM, Hwu, P, Topalian, SL, Schwartzentruber, DJ et al. (2003). Cancer regression and autoimmunity induced by cytotoxic T lymphocyteassociated antigen 4 blockade in patients with metastatic melanoma. Proc Natl Acad Sci USA 100: 8372-8377.
16. Cromme, FV, Airey, J, Heemels, MT, Ploegh, HL, Keating, PJ, Stern, PL et al. (1994). Loss of transporter protein, encoded by the TAP-1 gene, is highly correlated with loss of HLA expression in cervical carcinomas. J Exp Med 179: 335-340.
17. Greenwald, RJ, Freeman, GJ and Sharpe, AH (2005). The B7 family revisited. Annu Rev Immunol 23: 515-548.
18. Zou, W and Chen, L (2008). Inhibitory B7-family molecules in the tumour microenvironment. Nat Rev Immunol 8: 467-477.
19. Dong, H, Strome, SE, Salomao, DR, Tamura, H, Hirano, F, Flies, DB et al. (2002). Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med 8: 793-800.
20. Ishida, Y, Agata, Y, Shibahara, K and Honjo, T (1992). Induced expression of PD-1, a novel member of the immunoglobulin gene superfamily, upon programmed cell death. EMBO J 11: 3887-3895.
21. Zha, Y, Blank, C and Gajewski, TF (2004). Negative regulation of T-cell function by PD-1. Crit Rev Immunol 24: 229-237.
22. Keir, ME, Butte, MJ, Freeman, GJ and Sharpe, AH (2008). PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol 26: 677-704.
23. Topalian, SL, Drake, CG and Pardoll, DM (2012). Targeting the PD-1/B7-H1(PD-L1) pathway to activate anti-tumor immunity. Curr Opin Immunol 24: 207-212.
24. Ahmadzadeh, M, Johnson, LA, Heemskerk, B, Wunderlich, JR, Dudley, ME, White, DE et al. (2009). Tumor antigen-specific CD8 T cells infiltrating the tumor express high levels of PD-1 and are functionally impaired. Blood 114: 1537-1544.
25. Iwai, Y, Ishida, M, Tanaka, Y, Okazaki, T, Honjo, T and Minato, N (2002). Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc Natl Acad Sci USA 99: 12293-12297.
26. Strome, SE, Dong, H, Tamura, H, Voss, SG, Flies, DB, Tamada, K et al. (2003). B7-H1 blockade augments adoptive T-cell immunotherapy for squamous cell carcinoma. Cancer Res 63: 6501-6505.
27. Nomi, T, Sho, M, Akahori, T, Hamada, K, Kubo, A, Kanehiro, H et al. (2007). Clinical significance and therapeutic potential of the programmed death-1 ligand/programmed death-1 pathway in human pancreatic cancer. Clin Cancer Res 13: 2151-2157.
28. Brahmer, JR, Drake, CG, Wollner, I, Powderly, JD, Picus, J, Sharfman, WH et al. (2010). Phase I study of single-agent anti-programmed death-1 (MDX-1106) in refractory solid tumors: safety, clinical activity, pharmacodynamics, and immunologic correlates. J Clin Oncol 28: 3167-3175.
29. Attia, P, Phan, GQ, Maker, AV, Robinson, MR, Quezado, MM, Yang, JC et al. (2005). Autoimmunity correlates with tumor regression in patients with metastatic melanoma treated with anti-cytotoxic T-lymphocyte antigen-4. J Clin Oncol 23: 6043-6053.
30. Beck, KE, Blansfield, JA, Tran, KQ, Feldman, AL, Hughes, MS, Royal, RE et al. (2006). Enterocolitis in patients with cancer after antibody blockade of cytotoxic T-lymphocyte-associated antigen 4. J Clin Oncol 24: 2283-2289.
31. Ban, G, Song, MS and Lee, SW (2009). Cancer cell targeting with mouse TERT-specific group I intron of Tetrahymena thermophila. J Microbiol Biotechnol 19: 1070-1076.
32. Gamrekelashvili, J, Krüger, C, von Wasielewski, R, Hoffmann, M, Huster, KM, Busch, DH et al. (2007). Necrotic tumor cell death in vivo impairs tumor-specific immune responses. J Immunol 178: 1573-1580.
33. Iida, N, Nakamoto, Y, Baba, T, Kakinoki, K, Li, YY, Wu, Y et al. (2008). Tumor cell apoptosis induces tumor-specific immunity in a CC chemokine receptor 1- and 5-dependent manner in mice. J Leukoc Biol 84: 1001-1010.
34. Lee, SJ, et al. (2012). Over-expression of miR-145 enhances the effectiveness of HSVtk gene therapy for malignant glioma. Cancer Lett 320: 72-80.
35. McCormick, F (2001). Cancer gene therapy: fringe or cutting edge? Nat Rev Cancer 1: 130-141.
36. Nishimura, H, Nose, M, Hiai, H, Minato, N and Honjo, T (1999). Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity 11: 141-151.
37. Okazaki, T, Tanaka, Y, Nishio, R, Mitsuiye, T, Mizoguchi, A, Wang, J et al. (2003). Autoantibodies against cardiac troponin I are responsible for dilated cardiomyopathy in PD-1-deficient mice. Nat Med 9: 1477-1483.
38. He, YF, Zhang, GM, Wang, XH, Zhang, H, Yuan, Y, Li, D et al. (2004). Blocking programmed death-1 ligand-PD-1 interactions by local gene therapy results in enhancement of antitumor effect of secondary lymphoid tissue chemokine. J Immunol 173: 4919-4928.
39. Song, MY, Park, SH, Nam, HJ, Choi, DH and Sung, YC (2011). Enhancement of vaccine-induced primary and memory CD8(+) T-cell responses by soluble PD-1. J Immunother 34: 297-306.
40. Fridlender, ZG, Sun, J, Singhal, S, Kapoor, V, Cheng, G, Suzuki, E et al. (2010). Chemotherapy delivered after viral immunogene therapy augments antitumor efficacy via multiple immune-mediated mechanisms. Mol Ther 18: 1947-1959.
41. Miles, BJ, Shalev, M, Aguilar-Cordova, E, Timme, TL, Lee, HM, Yang, G et al. (2001). Prostate-specific antigen response and systemic T cell activation after in situ gene therapy in prostate cancer patients failing radiotherapy. Hum Gene Ther 12: 1955-1967.
42. Benson, DM Jr, Bakan, CE, Mishra, A, Hofmeister, CC, Efebera, Y, Becknell, B et al. (2010). The PD-1/PD-L1 axis modulates the natural killer cell versus multiple myeloma effect: a therapeutic target for CT-011, a novel monoclonal anti-PD-1 antibody. Blood 116: 2286-2294.
43. Weiner, LM, Surana, R and Wang, S (2010). Monoclonal antibodies: versatile platforms for cancer immunotherapy. Nat Rev Immunol 10: 317-327.
44. Aguilar, LK, Guzik, BW and Aguilar-Cordova, E (2011). Cytotoxic immunotherapy strategies for cancer: mechanisms and clinical development. J Cell Biochem 112: 1969-1977.