Systemic blockade of transforming growth factor-β signaling augments the efficacy of immunogene therapy

Cancer Research

Volumn 68, Issue 24, 2008, Pages 10247-10256

  Kim, Samuel ^a   Buchlis, George ^a   Fridlender, Zvi G ^a   Sun, Jing ^a   Kapoor, Veena ^a   Cheng, Guanjun ^a   Haas, Andrew ^a   Hung, Kam Cheung ^b   Zhang, Xiamei ^b   Corbley, Michael ^b   Kaiser, Larry R ^a   Ling, Leona ^b   Albelda, Steven M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b BIOGEN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; ANTINEOPLASTIC AGENT; BETA INTERFERON; INTERCELLULAR ADHESION MOLECULE 1; SM 16; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; WART VIRUS VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNOTHERAPY; CD25+ T LYMPHOCYTE; CONTROLLED STUDY; DRUG POTENTIATION; FEMALE; HISTOPATHOLOGY; HUMAN PAPILLOMAVIRUS TYPE E7; LUNG CANCER; LYMPHOCYTIC INFILTRATION; MALE; MESOTHELIOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR GROWTH;

ADENOVIRIDAE; ANIMALS; AZABICYCLO COMPOUNDS; CANCER VACCINES; CD8-POSITIVE T-LYMPHOCYTES; COMBINED MODALITY THERAPY; CYTOKINES; EPITOPES, T-LYMPHOCYTE; FEMALE; IMMUNOGENETICS; IMMUNOTHERAPY; INTERCELLULAR ADHESION MOLECULE-1; INTERFERON-BETA; LUNG NEOPLASMS; MALE; MESOTHELIOMA; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; ONCOGENE PROTEINS, VIRAL; RNA, MESSENGER; TRANSFORMING GROWTH FACTOR BETA;

EID: 57749107585     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-1494     Document Type: Article

References (54)

1. Mueller MM, Fusenig NE. Friends or foes - bipolar effects of the tumour stroma in cancer. Nat Rev Cancer 2004;4:839-49.
2. Bhowmick NA, Moses HL. Tumor-stroma interactions. Curr Opin Genet Dev 2005;15:97-101.
3. Kim R, Emi M, Tanabe K, Arihiro K. Tumor-driven evolution of immunosuppressive networks during malignant progression. Cancer Res 2006;66:5527-36.
4. Gajewski TF, Meng Y, Harlin H. Immune suppression in the tumor microenvironment. J Immunother 2006;29:233-40.
5. Rodriguez PC, Ochoa AC. T cell dysfunction in cancer: role of myeloid cells and tumor cells regulating amino acid availability and oxidative stress. Semin Cancer Biol 2006;16:66-72.
6. Rabinovich GA, Gabrilovich D, Sotomayer EM. Immunosuppressive strategies that are mediated by tumor cells. Annu Rev Immunol 2007;25:267-96.
7. Lizee G, Radvanyi LG, Overwijk WW, Hwu P. Improving antitumor immune responses by circumventing immunoregulatory cells and mechanisms. Clin Cancer Res 2006;12:4794-803.
8. Whiteside TL. Immune suppression in cancer: effects on immune cells, mechanisms and future therapeutic intervention. Semin Cancer Biol 2006;16:3-15.
9. Elliott RL, Blobe GC. Role of transforming growth factor β in human cancer. J Clin Oncol 2005;23:2078-93.
10. Gorelik L, Flavell RA. Transforming growth factor-β in T-cell biology. Nat Rev Immunol 2002;2:46-53.
11. Li MO, Wan YY, Sanjabi S, Robertson AK, Flavell RA. Transforming growth factor-h regulation of immune responses. Annu Rev Immunol 2006;24:99-146.
12. Ahmadzadeh M, Rosenberg SA. TGF-β 1 attenuates the acquisition and expression of effector function by tumor antigen-specific human memory CD8 T cells. J Immunol 2005;174:5215-23.
13. Thomas DA, Massague J. TGF-β directly targets cytotoxic T cell functions during tumor evasion of immune surveillance. Cancer Cell 2005;8:369-80.
14. + regulatory T cells. J Exp Med 2005;201:1061-7.
15. Liau LM, Prns RM, Liertscher SM, et al. Dendritic cell vaccination in glioblastoma patients induces systemic and intracranial T-cell responses modulated by the local central nervous system tumor microenvironment. Clin Cancer Res 2005;11:5515-25.
16. Ge R, Rajeev V, Ray P, et al. Inhibition of growth and metastasis of mouse mammary carcinoma by selective inhibitor of transforming growth factor-β type I receptor kinase in vivo. Clin Cancer Res 2006;12:4315-30.
17. Nam J-S, Terabe M, Mamura M, et al. An antitransforming growth factorβantibody suppresses metastasis via cooperative effects on multiple cell compartments. Cancer Res 2008;68:3835-43.
18. Suzuki E, Kapoor V, Cheung HK, et al. Soluble type II transforming growth factor-β receptor inhibits both small and large established murine malignant mesothelioma tumor growth by augmenting host anti-tumor immunity. Clin Cancer Res 2004;10:5907-18.
19. Suzuki E, KimS, Cheung HK, et al. A novel small molecule inhibitor of TGF-β type I receptor kinase (SM16) inhibits murine mesothelioma tumor growth in vivo and prevents the extent of tumor recurrence after surgical resection. Cancer Res 2007;67:2351-9.
20. Odaka M, Sterman D, Wiewrodt R, et al. Eradication of intraperitoneal and distant tumor by adenovirus-mediated interferon-β gene therapy due to induction of systemic immunity. Cancer Res 2001;61:6201-12.
21. Wilderman M, Sun J, Khan M, et al. Intrapulmonary interferon-β gene therapy using an adenoviral vector is highly effective in a murine orthotopic model of lung adenocarcinoma via a combination of direct toxicity, NK cell, and CD8 T-cell mediated effects. Cancer Res 2005;65:8379-87.
22. Haas A, Sun J, Vachani A, et al. Cyclooxygenase-2 inhibition augments efficacy of a cancer vaccine. Clin Cancer Res 2006;12:214-22.
23. Davis MR, Manning LS, Whataker D, Garlepp MJ, Robinson BWS. Establishment of a murine model of malignant mesothelioma. Int J Cancer 1992;52:881-6.
24. Lin KY, Guarnieri FG, Staveley-O'Carroll KF, et al. Treatment of established tumors with a novel vaccine that enhances major histocompatibility class II presentation of tumor antigens. Cancer Res 1996;56:21-6.
25. Fu K, Corbley MJ, Sun L, et al. An orally active inhibitor of the TGF-β type I receptor, ALK5, inhibits vascular fibrosis and adventitial myofibroblast induction in the rat carotid balloon injury model. Arterioscler Thromb Vasc Biol 2008;28:665-71.
26. + T-cells are the key mediators of anti-tumor effects of the vascular disrupting agent 5,6-di-methylxanthenone-4-acetic Acid (DMXAA) in murine models of lung cancer and mesothelioma. Cancer Res 2005;65:11752-61.
27. Quezada SA, Peggs KS, Curran MA, Allison JP. CTLA4 blockade and GM-CSF combination immunotherapy alters the intratumor balance of effector and regulatory T cells. J Clin Invest 2006;116:1935-45.
28. Serafini P, Meckel K, Kelso M, et al. Phosphodiesterase-5 inhibition augments endogenous antitumor immunity by reducing myeloid-derived suppressor cell function. J Exp Med 2006;203:2691-702.
29. Vicari AP, Caux C. Chemokines in cancer. Cytokine Growth Factor Rev 2002;13:143-54.
30. Carlos TM. Leukocyte recruitment at sites of tumor: dissonant orchestration. J Leukoc Biol 2001;70:171-84.
31. Boutard V, Havouis R, Fouqueray B, Philippe C, Moulinoux JP, Baud L. Transforming growth factor-β stimulates arginase activity in macrophages. Implications for the regulation of macrophage cytotoxicity. J Immunol 1995;155:2077-84.
32. Bierie B, Stover DG, Abel TW, et al. Transforming growth factor-β regulates mammary carcinoma cell survival and interaction with adjacent microenvironment. Cancer Res 2008;68:1809-19.
33. + myeloid cells that promote metastasis. Cancer Cell 2008;13:23-35.
34. Borczuk AC, Papanikolaou N, Toonkel RL, et al. Lung adenocarcinoma invasion in TGFβRII-deficient cells is mediated by CCL5/RANTES. Oncogene 2007;27:557-64.
35. NamJ-S, Terabe M, Kang M-J, et al. Transforming growth factor-β subverts the immune system into directly promoting tumor growth through interleukin-17. Cancer Res 2008;68:3915-23.
36. Wang FL, Qin WJ, Wen WH, et al. TGF-β insensitive dendritic cells: an efficient vaccine for murine prostate cells. Cancer Immunol Immunother 2007;56:1785-93.
37. Gorelik L, Flavell RA. Immune-mediated eradication of tumors through the blockade of transforming growth factor-β signaling in T cells. Nat Med 2001;7:1118-22.
38. Bollard C, Rossig C, Calonge MJ, et al. Adapting a transforming growth factor-β-related tumor protection strategy to enhance antitumor immunity. Blood 2002;99:3179-87.
39. + T cell tumorigenesis. Cancer Res 2004;64:6524-9.
40. + T cells: eradication of autologous mouse prostate cancer. Cancer Res 2005;65:1761-9.
41. Nemunaitis J, Dillman RO, Scharzenberger PO, et al. Phase II study of belagenpumatucel-L, a transforming growth factor β-2 antisense gene-modified allogeneic tumor cell vaccine in non-small-cell lung cancer. J Clin Oncol 2006;24:4721-30.
42. Arteaga C. Inhibition of TGFβ signaling in cancer therapy. Curr Opin Genet Dev 2006;16:30-7.
43. Yingling JM, Blanchard KL, Sawyer JS. Development of TGF-β signaling inhibitors for cancer therapy. Nat Rev 2004;3:1011-22.
44. Iyer S, Wang ZG, Akhtari M, Zhao W, Seth P. Targeting TGFβ signaling for cancer therapy. Cancer Biol Ther 2005;4:261-6.
45. Liu Y, Want Q, Kleinschmidt-DeMasters BK, et al. TGF-β2 inhibition augments the effect of tumor vaccine and improves the survival of animals with preestablished brain tumors. J Neurooncol 2007;81:149-62.
46. Jia ZC, Zou LY, Ni B, et al. Effective induction of antitumor immunity by immunization with plasmid DNA encoding TRP-2 plus neutralization of TGF-β. Cancer Immunol Immunother 2005;54:446-52.
47. Kobie JJ, Wu RS, Kurt RA, et al. Transforming growth factor h inhibits the antigen-presenting functions and antitumor activity of dendritic cell vaccines. Cancer Res 2003;63:1860-4.
48. + cells unmasks tumor immunogenicity leading to the rejection of late-stage tumors. J Exp Med 2005;201:779-91.
49. + T cells in patients with melanoma. J Immunol 2005;175:6169-76.
50. Frey AB, Monu N. Effector-phase tolerance: another mechanism of how cancer escapes antitumor immune response. J Leukoc Biol 2006;79:652-62.
51. Wallace A, Kapoor V, Sun J, et al. TGF-β receptor blockade augments the effectiveness of adoptive T-cell therapy of established solid tumors. Clin Cancer Res 2008;14:3966-74.
52. Berzofsky JA, Terabe M, Oh S, et al. Progress on new vaccine strategies for the immunotherapy and prevention of cancer. J Clin Invest 2004;113:1515-25.
53. Rosenberg SA, Yang JC, Restifo NP. Cancer immunotherapy: moving beyond current vaccines. Nat Med 2004;9:909-15.
54. Sterman DH, Recio AR, Carroll RG, et al. A phase I clinical trial of single-dose intrapleural interferon-β gene transfer for malignant mesothelioma and metastatic pleural effusions: high rate of anti-tumor immune responses. Clin Cancer Res 2007;13:4456-66.