Adoptively transferred immune t cells eradicate established tumors despite cancer-induced immune suppression

Journal of Immunology

Volumn 192, Issue 3, 2014, Pages 1286-1293

  Arina, Ainhoa ^a   Schreiber, Karin ^a   Binder, David C ^a   Karrison, Theodore G ^a   Liu, Rebecca B ^a   Schreiber, Hans ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CANCER CELL; CELL TRANSFER; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EX VIVO STUDY; IMMUNOHISTOCHEMISTRY; IMMUNOSUPPRESSIVE TREATMENT; IN VIVO STUDY; LYMPHOCYTE PROLIFERATION; MOUSE; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; SUPPRESSOR CELL; TUMOR ASSOCIATED LEUKOCYTE; TUMOR CELL DESTRUCTION; TUMOR VASCULARIZATION; TUMOR VOLUME;

ANIMALS; ANTIGENS, CD11B; CANCER VACCINES; DNA-BINDING PROTEINS; HOMEODOMAIN PROTEINS; IMMUNIZATION; IMMUNOLOGIC MEMORY; IMMUNOTHERAPY, ADOPTIVE; MACROPHAGES; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MODELS, BIOLOGICAL; MYELOID CELLS; NEOPLASMS, EXPERIMENTAL; NEOVASCULARIZATION, PATHOLOGIC; RECEPTORS, CHEMOKINE; SKIN WINDOW TECHNIQUE; T-LYMPHOCYTE SUBSETS; TUMOR BURDEN; TUMOR ESCAPE;

EID: 84893429747     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202498     Document Type: Article

References (56)

1. Wen, F. T., R. A. Thisted, D. A. Rowley, and H. Schreiber. 2012. A systematic analysis of experimental immunotherapies on tumors differing in size and duration of growth. OncoImmunology 1: 172-178.
2. Chioda, M., E. Peranzoni, G. Desantis, F. Papalini, E. Falisi, S. Solito, S. Mandruzzato, and V. Bronte. 2011. Myeloid cell diversification and complexity: an old concept with new turns in oncology. Cancer Metastasis Rev. 30: 27-43.
3. Gabrilovich, D. I., V. Bronte, S. H. Chen, M. P. Colombo, A. Ochoa, S. Ostrand-Rosenberg, and H. Schreiber. 2007. The terminology issue for myeloid-derived suppressor cells. Cancer Res. 67: 425.
4. Milas, L., and I. Basic. 1972. Stimulated granulocytopoiesis in mice bearing fibrosarcoma. Eur. J. Cancer 8: 309-313.
5. Balducci, L., and C. Hardy. 1983. High proliferation of granulocyte-macrophage progenitors in tumor-bearing mice. Cancer Res. 43: 4643-4647.
6. Lee, M. Y., K. Kaushansky, S. A. Judkins, J. L. Lottsfeldt, A. Waheed, and R. K. Shadduck. 1989. Mechanisms of tumor-induced neutrophilia: constitutive production of colony-stimulating factors and their synergistic actions. Blood 74: 115-122.
7. DuPre, S. A., and K. W. Hunter, Jr. 2007. Murine mammary carcinoma 4T1 induces a leukemoid reaction with splenomegaly: association with tumor-derived growth factors. Exp. Mol. Pathol. 82: 12-24.
8. Almand, B., J. I. Clark, E. Nikitina, J. van Beynen, N. R. English, S. C. Knight, D. P. Carbone, and D. I. Gabrilovich. 2001. Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer. J. Immunol. 166: 678-689.
9. Delmonte, L., and R. A. Liebelt. 1965. Granulocytosis-promoting extract of mouse tumor tissue: partial purification. Science 148: 521-523.
10. Hibberd, A. D., and D. Metcalf. 1971. Proliferation of macrophage and granulocyte precursors in response to primary and transplanted tumors. Isr. J. Med. Sci. 7: 202-210.
11. Fu, Y. X., G. Watson, J. J. Jimenez, Y. Wang, and D. M. Lopez. 1990. Expansion of immunoregulatory macrophages by granulocyte-macrophage colonystimulating factor derived from a murine mammary tumor. Cancer Res. 50: 227-234.
12. Fu, Y. X., G. A. Watson, M. Kasahara, and D. M. Lopez. 1991. The role of tumor-derived cytokines on the immune system of mice bearing a mammary adenocarcinoma. I. Induction of regulatory macrophages in normal mice by the in vivo administration of rGM-CSF. J. Immunol. 146: 783-789.
13. Jameson, J. L., and B. E. Johnson. 2008. Paraneoplastic syndromes: endocrinologic/hematologic. In Harrison's Principles of Internal Medicine, 17th Ed. A. S. Fauci, ed. McGraw-Hill Medical, New York, p. 617-623.
14. Tepper, R. I., R. L. Coffman, and P. Leder. 1992. An eosinophil-dependent mechanism for the antitumor effect of interleukin-4. Science 257: 548-551.
15. Malek, T. R., G. Ortega, C. Chan, R. A. Kroczek, and E. M. Shevach. 1986. Role of Ly-6 in lymphocyte activation. II. Induction of T cell activation by monoclonal anti-Ly-6 antibodies. J. Exp. Med. 164: 709-722.
16. Wrammert, J., E. Kallberg, W. W. Agace, and T. Leanderson. 2002. Ly6C expression differentiates plasma cells from other B cell subsets in mice. Eur. J. Immunol. 32: 97-103.
17. Movahedi, K., M. Guilliams, J. Van den Bossche, R. Van den Bergh, C. Gysemans, A. Beschin, P. De Baetselier, and J. A. Van Ginderachter. 2008. Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood 111: 4233-4244.
18. Youn, J. I., S. Nagaraj,M. Collazo, and D. I. Gabrilovich. 2008. Subsets of myeloidderived suppressor cells in tumor-bearing mice. J. Immunol. 181: 5791-5802.
19. Movahedi, K., D. Laoui, C. Gysemans, M. Baeten, G. Stangé, J. Van den Bossche, M. Mack, D. Pipeleers, P. In't Veld, P. De Baetselier, and J. A. Van Ginderachter. 2010. Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6Chigh monocytes. Cancer Res. 70: 5728-5739.
20. Dolcetti, L., E. Peranzoni, S. Ugel, I. Marigo, A. Fernandez Gomez, C. Mesa, M. Geilich, G. Winkels, E. Traggiai, A. Casati, et al. 2010. Hierarchy of immunosuppressive strength among myeloid-derived suppressor cell subsets is determined by GM-CSF. Eur. J. Immunol. 40: 22-35.
21. Morales, J. K., M. Kmieciak, K. L. Knutson, H. D. Bear, and M. H. Manjili. 2010. GM-CSF is one of the main breast tumor-derived soluble factors involved in the differentiation of CD11b-Gr12 bone marrow progenitor cells into myeloidderived suppressor cells. Breast Cancer Res. Treat. 123: 39-49.
22. Schmidt, K., S. Zilio, J. C. Schmollinger, V. Bronte, T. Blankenstein, and G. Willimsky. 2013. Differently immunogenic cancers in mice induce immature myeloid cells that suppress CTL in vitro but not in vivo following transfer. Blood 121: 1740-1748.
23. Pekarek, L. A., B. A. Starr, A. Y. Toledano, and H. Schreiber. 1995. Inhibition of tumor growth by elimination of granulocytes. J. Exp. Med. 181: 435-440.
24. Yang, L., L. M. DeBusk, K. Fukuda, B. Fingleton, B. Green-Jarvis, Y. Shyr, L. M. Matrisian, D. P. Carbone, and P. C. Lin. 2004. Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell 6: 409-421.
25. Yang, L., J. Huang, X. Ren, A. E. Gorska, A. Chytil, M. Aakre, D. P. Carbone, L. M. Matrisian, A. Richmond, P. C. Lin, and H. L. Moses. 2008. Abrogation of TGFb signaling in mammary carcinomas recruits Gr-1+CD11b+ myeloid cells that promote metastasis. Cancer Cell 13: 23-35.
26. Mauti, L. A., M. A. Le Bitoux, K. Baumer, J. C. Stehle, D. Golshayan, P. Provero, and I. Stamenkovic. 2011. Myeloid-derived suppressor cells are implicated in regulating permissiveness for tumor metastasis during mouse gestation. J. Clin. Invest. 121: 2794-2807.
27. Bronte, V., E. Apolloni, A. Cabrelle, R. Ronca, P. Serafini, P. Zamboni, N. P. Restifo, and P. Zanovello. 2000. Identification of a CD11b+/Gr-1+/CD31+ myeloid progenitor capable of activating or suppressing CD8+ T cells. Blood 96: 3838-3846.
28. Gabrilovich, D. I., M. P. Velders, E. M. Sotomayor, and W. M. Kast. 2001. Mechanism of immune dysfunction in cancer mediated by immature Gr-1+ myeloid cells. J. Immunol. 166: 5398-5406.
29. Bunt, S. K., P. Sinha, V. K. Clements, J. Leips, and S. Ostrand-Rosenberg. 2006. Inflammation induces myeloid-derived suppressor cells that facilitate tumor progression. J. Immunol. 176: 284-290.
30. Gallina, G., L. Dolcetti, P. Serafini, C. De Santo, I. Marigo, M. P. Colombo, G. Basso, F. Brombacher, I. Borrello, P. Zanovello, et al. 2006. Tumors induce a subset of inflammatory monocytes with immunosuppressive activity on CD8+ T cells. J. Clin. Invest. 116: 2777-2790.
31. Kusmartsev, S., S. Nagaraj, and D. I. Gabrilovich. 2005. Tumor-Associated CD8+ T cell tolerance induced by bone marrow-derived immature myeloid cells. J. Immunol. 175: 4583-4592.
32. Nagaraj, S., A. G. Schrum, H. I. Cho, E. Celis, and D. I. Gabrilovich. 2010. Mechanism of T cell tolerance induced by myeloid-derived suppressor cells. J. Immunol. 184: 3106-3116.
33. Watanabe, S., K. Deguchi, R. Zheng, H. Tamai, L. X. Wang, P. A. Cohen, and S. Shu. 2008. Tumor-induced CD11b+Gr-1+ myeloid cells suppress T cell sensitization in tumor-draining lymph nodes. J. Immunol. 181: 3291-3300.
34. Kusmartsev, S., and D. I. Gabrilovich. 2005. STAT1 signaling regulates tumor-Associated macrophage-mediated T cell deletion. J. Immunol. 174: 4880-4891.
35. Qian, B. Z., and J. W. Pollard. 2010. Macrophage diversity enhances tumor progression and metastasis. Cell 141: 39-51.
36. Sica, A., T. Schioppa, A. Mantovani, and P. Allavena. 2006. Tumour-Associated macrophages are a distinct M2 polarised population promoting tumour progression: potential targets of anti-cancer therapy. Eur. J. Cancer 42: 717-727.
37. Umemura, N., M. Saio, T. Suwa, Y. Kitoh, J. Bai, K. Nonaka, G. F. Ouyang, M. Okada, M. Balazs, R. Adany, et al. 2008. Tumor-infiltrating myeloid-derived suppressor cells are pleiotropic-inflamed monocytes/macrophages that bear M1-And M2-type characteristics. J. Leukoc. Biol. 83: 1136-1144.
38. Schreiber, K., A. Arina, B. Engels, M. T. Spiotto, J. Sidney, A. Sette, T. G. Karrison, R. R. Weichselbaum, D. A. Rowley, and H. Schreiber. 2012. Spleen cells from young but not old immunized mice eradicate large established cancers. Clin. Cancer Res. 18: 2526-2533.
39. Singh, S., S. R. Ross, M. Acena, D. A. Rowley, and H. Schreiber. 1992. Stroma is critical for preventing or permitting immunological destruction of antigenic cancer cells. J. Exp. Med. 175: 139-146.
40. Dubey, P., R. C. Hendrickson, S. C. Meredith, C. T. Siegel, J. Shabanowitz, J. C. Skipper, V. H. Engelhard, D. F. Hunt, and H. Schreiber. 1997. The immunodominant antigen of an ultraviolet-induced regressor tumor is generated by a somatic point mutation in the DEAD box helicase p68. J. Exp. Med. 185: 695-705.
41. Schreiber, K., T. H. Wu, W. M. Kast, and H. Schreiber. 2001. Tracking the common ancestry of antigenically distinct cancer variants. Clin. Cancer Res. 7(3, Suppl)871s-875s.
42. Schietinger, A., A. Arina, R. B. Liu, S. Wells, J. Huang, B. Engels, V. Bindokas, T. Bartkowiak, D. Lee, A. Herrmann, et al. 2013. Longitudinal confocal microscopy imaging of solid tumor destruction following adoptive T cell transfer. OncoImmunology. 2: e26677.
43. Zhang, B., Y. Zhang, N. A. Bowerman, A. Schietinger, Y. X. Fu, D. M. Kranz, D. A. Rowley, and H. Schreiber. 2008. Equilibrium between host and cancer caused by effector T cells killing tumor stroma. Cancer Res. 68: 1563-1571.
44. Garcia-Hernandez, Mde. L., H. Hamada, J. B. Reome, S. K. Misra, M. P. Tighe, and R. W. Dutton. 2010. Adoptive transfer of tumor-specific Tc17 effector T cells controls the growth of B16 melanoma in mice. J. Immunol. 184: 4215-4227.
45. Mullen, C. A., J. L. Urban, C. Van Waes, D. A. Rowley, and H. Schreiber. 1985. Multiple cancers. Tumor burden permits the outgrowth of other cancers. J. Exp. Med. 162: 1665-1682.
46. McAllister, S. S., A. M. Gifford, A. L. Greiner, S. P. Kelleher, M. P. Saelzler, T. A. Ince, F. Reinhardt, L. N. Harris, B. L. Hylander, E. A. Repasky, and R. A. Weinberg. 2008. Systemic endocrine instigation of indolent tumor growth requires osteopontin. Cell 133: 994-1005.
47. Kmieciak, M., D. Basu, K. K. Payne, A. Toor, A. Yacoub, X. Y. Wang, L. Smith, H. D. Bear, and M. H. Manjili. 2011. Activated NKT cells and NK cells render T cells resistant to myeloid-derived suppressor cells and result in an effective adoptive cellular therapy against breast cancer in the FVBN202 transgenic mouse. J. Immunol. 187: 708-717.
48. Bronte, V., M. Wang, W. W. Overwijk, D. R. Surman, F. Pericle, S. A. Rosenberg, and N. P. Restifo. 1998. Apoptotic death of CD8+ T lymphocytes after immunization: induction of a suppressive population of Mac-1+/Gr-1+ cells. J. Immunol. 161: 5313-5320.
49. Seung, L. P., S. K. Seung, and H. Schreiber. 1995. Antigenic cancer cells that escape immune destruction are stimulated by host cells. Cancer Res. 55: 5094-5100.
50. Kaplan, R. N., R. D. Riba, S. Zacharoulis, A. H. Bramley, L. Vincent, C. Costa, D. D. MacDonald, D. K. Jin, K. Shido, S. A. Kerns, et al. 2005. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 438: 820-827.
51. Ibe, S., Z. Qin, T. Schuler, S. Preiss, and T. Blankenstein. 2001. Tumor rejection by disturbing tumor stroma cell interactions. J. Exp. Med. 194: 1549-1559.
52. Zhang, B., T. Karrison, D. A. Rowley, and H. Schreiber. 2008. IFN-g-And TNFdependent bystander eradication of antigen-loss variants in established mouse cancers. J. Clin. Invest. 118: 1398-1404.
53. Beatty, G. L., E. G. Chiorean, M. P. Fishman, B. Saboury, U. R. Teitelbaum, W. Sun, R. D. Huhn, W. Song, D. Li, L. L. Sharp, et al. 2011. CD40 agonists alter tumor stroma and show efficacy against pancreatic carcinoma in mice and humans. Science 331: 1612-1616.
54. Buhtoiarov, I. N., P. M. Sondel, J. M. Wigginton, T. N. Buhtoiarova, E. M. Yanke, D. A. Mahvi, and A. L. Rakhmilevich. 2011. Anti-tumour synergy of cytotoxic chemotherapy and anti-CD40 plus CpG-ODN immunotherapy through repolarization of tumour-Associated macrophages. Immunology 132: 226-239.
55. Medina-Echeverz, J., J. Fioravanti, M. Zabala, N. Ardaiz, J. Prieto, and P. Berraondo. 2011. Successful colon cancer eradication after chemoimmunotherapy is associated with profound phenotypic change of intratumoral myeloid cells. J. Immunol. 186: 807-815.
56. Spiotto, M. T., D. A. Rowley, and H. Schreiber. 2004. Bystander elimination of antigen loss variants in established tumors. Nat. Med. 10: 294-298.