Radiotherapy of human sarcoma promotes an intratumoral immune effector signature

Clinical Cancer Research

Volumn 19, Issue 17, 2013, Pages 4843-4853

  Sharma, Anu ^a   Bode, Beata ^a   Studer, Gabriela ^a   Moch, Holger ^a   Okoniewski, Michal ^b   Knuth, Alexander ^a   Von Boehmer, Lotta ^a   Van Den Broek, Maries ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER TESTIS ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

ARTICLE; CANCER RADIOTHERAPY; CLINICAL ARTICLE; DOWN REGULATION; HUMAN; HUMAN TISSUE; IMMUNOMODULATION; PRIORITY JOURNAL; RETROSPECTIVE STUDY; SARCOMA; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; UPREGULATION;

ADULT; ANTIGENS, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, MHC CLASS I; HUMANS; IMMUNOHISTOCHEMISTRY; PARAFFIN EMBEDDING; SARCOMA; SOFT TISSUE NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84883470832     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-13-0352     Document Type: Article

References (50)

1. Martin Liberal J, Lagares-Tena L, Sainz-Jaspeado M, Mateo-Lozano S, Garcia Del Muro X, Tirado OM. Targeted therapies in sarcomas: challenging the challenge. Sarcoma 2012;2012:626094.
2. Howlader N, Noone AM, Krapcho M, Neyman N, Aminou R, Altekruse SF, et al. (eds). SEER cancer statistics review, 1975-2009 (vintage 2009 populations). Bethesda, MD: National Cancer Institute. Available from http://seer.cancer.gov/ csr/1975-2009-pops09/sections.html, based on November 2011 SEER data submission, posted to the SEER web site; April 2012.
3. Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 2011;331:1565-70.
4. Knuth A, Danowski B, Oettgen HF, Old LJ. T-cell-mediated cytotoxicity against autologous malignant melanoma: analysis with interleukin 2-dependent T-cell cultures. Proc Natl Acad Sci U S A 1984;81:3511-5. (Pubitemid 14122704)
5. van der Bruggen P, Traversari C, Chomez P, Lurquin C, De Plaen E, Van den Eynde B, et al. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science 1991;254:1643-7. (Pubitemid 21917508)
6. Parmigiani RB, Bettoni F, Vibranovski MD, Lopes MH, Martins WK, Cunha IW, et al. Characterization of a cancer/testis (CT) antigen gene family capable of eliciting humoral response in cancer patients. Proc Natl Acad Sci U S A 2006;103:18066-71. (Pubitemid 44871613)
7. Hofmann O, Caballero OL, Stevenson BJ, Chen YT, Cohen T, Chua R, et al. Genome-wide analysis of cancer/testis gene expression. Proc Natl Acad Sci U S A 2008;105:20422-7.
8. Scanlan MJ, Simpson AJ, Old LJ. The cancer/testis genes: review, standardization, and commentary. Cancer Immun 2004;4:1.
9. Parish IA, Kaech SM. Diversity in CD8(+) T cell differentiation. Curr Opin Immunol 2009;21:291-7.
10. Lanier LL. NK cell recognition. Annu Rev Immunol 2005;23:225-74. (Pubitemid 40563170)
11. Marigo I, Dolcetti L, Serafini P, Zanovello P, Bronte V. Tumor-induced tolerance and immune suppression by myeloid derived suppressor cells. Immunol Rev 2008;222:162-79. (Pubitemid 351430364)
12. Bilate AM, Lafaille JJ. Induced CD4+Foxp3+ regulatory T cells in immune tolerance. Annu Rev Immunol 2012;30:733-58.
13. Fan H, Wang J, Zhou X, Liu Z, Zheng SG. Induction of antigen-specific immune tolerance by TGF-beta-induced CD4+Foxp3+ regulatory T cells. Int J Clin Exp Med 2009;2:212-20.
14. Tan PH, Lota AS. Interaction of current cancer treatments and the immune system: implications for breast cancer therapeutics. Expert Opin Pharmacother 2008;9:2639-60.
15. Zitvogel L, Apetoh L, Ghiringhelli F, Kroemer G. Immunological aspects of cancer chemotherapy. Nat Rev Immunol 2008;8:59-73.
16. Van De Voorde L, Delrue L, van Eijkeren M, De Meerleer G. Radiotherapy and surgery-an indispensable duo in the treatment of retroperitoneal sarcoma. Cancer 2011;117:4355-64.
17. Sharma A, Bode B, Wenger RH, Lehmann K, Sartori AA, Moch H, et al. gamma-Radiation promotes immunological recognition of cancer cells through increased expression of cancer-testis antigens in vitro and in vivo. PLoS One 2011;6:e28217.
18. Gupta A, Probst HC, Vuong V, Landshammer A, Muth S, Yagita H, et al. Radiotherapy promotes tumor-specific effector CD8+ T cells via dendritic cell activation. J Immunol 2012;189:558-66.
19. Gupta A SA, von Boehmer L, Surace L, Knuth A, van den Broek M. Radiotherapy supports protective tumor-specific immunity. Oncoimmunology 2012;1:21-2.
20. Merrick A, Errington F, Milward K, O'Donnell D, Harrington K, Bateman A, et al. Immunosuppressive effects of radiation on human dendritic cells: reduced IL-12 production on activation and impairment of naive T-cell priming. Br J Cancer 2005;92:1450-8. (Pubitemid 40705012)
21. Demaria S, Bhardwaj N, McBride WH, Formenti SC. Combining radiotherapy and immunotherapy: a revived partnership. Int J Radiat Oncol Biol Phys 2005;63:655-66. (Pubitemid 41400049)
22. Lugade AA, Sorensen EW, Gerber SA, Moran PJ, Frelinger JG, Lord EM. Radiation-induced IFN-g production within the tumor microenvironment influences antitumor immunity. J Immunol 2008;180:3132-9.
23. Takeshima T, Chamoto K, Wakita D, Ohkuri T, Togashi Y, Shirato H, et al. Local radiation therapy inhibits tumor growth through the generation of tumor-specific CTL: its potentiation by combination with Th1 cell therapy. Cancer Res 2010;70:2697-706.
24. Gerloni M, Zanetti M. CD4 T cells in tumor immunity. Springer Semin Immunopathol 2005;27:37-48. (Pubitemid 40905061)
25. Rubner Y, Wunderlich R, Rühle PF, Kulzer L, Werthmöller N, Frey B, et al. How does ionizing irradiation contribute to the induction of antitumor immunity? Front Oncol 2012;2:75.
26. Burnette BC, Liang H, Lee Y, Chlewicki L, Khodarev NN, Weichselbaum RR, et al. The efficacy of radiotherapy relies upon induction of type I interferon-dependent innate and adaptive immunity. Cancer Res 2011;71:2488-96.
27. Schulz TF. Cancer and viral infections in immunocompromised individuals. Int J Cancer 2009;125:1755-63.
28. Reits EA, Hodge JW, Herberts CA, Groothuis TA, Chakraborty M, Wansley EK, et al. Radiation modulates the peptide repertoire, enhances MHC class I expression, and induces successful antitumor immunotherapy. J Exp Med 2006;203:1259-71. (Pubitemid 43736595)
29. Jager E, Ringhoffer M, Altmannsberger M, Arand M, Karbach J, Jager D, et al. Immunoselection in vivo: independent loss of MHC class I and melanocyte differentiation antigen expression in metastatic melanoma. Int J Cancer 1997;71:142-7. (Pubitemid 27252981)
30. Kim R, Emi M, Tanabe K. Cancer immunoediting from immune surveillance to immune escape. Immunology 2007;121:1-14. (Pubitemid 46537674)
31. Leroy P, Slos P, Homann H, Erbs P, Poitevin Y, Regulier E, et al. Cancer immunotherapy by direct in vivo transfer of immunomodulatory genes. Res Immunol 1998;149:681-4. (Pubitemid 29487162)
32. Joshi A, Cao D. TGF-beta signaling, tumor microenvironment and tumor progression: the butterfly effect. Front Biosci 2010;15:180-94.
33. Wang R, Lu M, Zhang J, Chen S, Luo X, Qin Y, et al. Increased IL-10 mRNA expression in tumor-associated macrophage correlated with late stage of lung cancer. J Exp Clin Cancer Res 2011;30:62.
34. van Horssen R, Ten Hagen TL, Eggermont AM. TNF-alpha in cancer treatment: molecular insights, antitumor effects, and clinical utility. Oncologist 2006;11:397-408.
35. BarthRJ Jr,Mulé JJ, Spiess PJ,Rosenberg SA. Interferon gammaand tumor necrosis factor have a role in tumor regressions mediated by murine CD8+ tumor-infiltrating lymphocytes. J Exp Med 1991;173:647-58.
36. Papatriantafyllou M. Tumour immunology: how does IL-12 enhance antitumour responses? Nat Rev Immunol 2011;11:801.
37. Dewan MZ, Galloway AE, Kawashima N, Dewyngaert JK, Babb JS, Formenti SC, et al. Fractionated but not single-dose radiotherapy induces an immune-mediated abscopal effect when combined with anti-CTLA-4 antibody. Clin Cancer Res 2009;15:5379-88.
38. Stamell EF, Wolchok JD, Gnjatic S, Lee NY, Brownell I. The abscopal effect associated with a systemic anti-melanoma immune response. Int J Radiat Oncol Biol Phys 2013;85:293-95.
39. Wu YL, Liang J, Zhang W, Tanaka Y, Sugiyama H. Immunotherapies: the blockade of inhibitory signals. Int J Biol Sci 2012;8:1420-30.
40. Sierro SR, Donda A, Perret R, Guillaume P, Yagita H, Levy F, et al. Combination of lentivector immunization and low-dose chemotherapy or PD-1/PD-L1 blocking primes self-reactive T cells and induces antitumor immunity. Eur J Immunol 2011;41:2217-28.
41. Ngiow SF, von Scheidt B, Akiba H, Yagita H, Teng MW, Smyth MJ. Anti-TIM3 antibody promotes T cell IFN-gamma-mediated antitumor immunity and suppresses established tumors. Cancer Res 2011;71:3540-51.
42. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012;366:2443-54.
43. Moschetta M, Pretto F, Berndt A, Galler K, Richter P, Bassi A, et al. Paclitaxel enhances therapeutic efficacy of the F8-IL2 immunocytokine to EDA-fibronectin-positive metastatic human melanoma xenografts. Cancer Res 2012;72:1814-24.
44. Steiner M, Neri D. Antibody-radionuclide conjugates for cancer therapy: historical considerations and new trends. Clin Cancer Res 2011;17:6406-16.
45. Seetharam S, Staba MJ, Schumm LP, Schreiber K, Schreiber H, Kufe DW, et al. Enhanced eradication of local and distant tumors by genetically produced interleukin-12 and radiation. Int J Oncol 1999;15:769-73.
46. Berrien-Elliott MM, Jackson SR, Meyer JM, Rouskey CJ, Nguyen TL, Yagita H, et al. Durable adoptive immunotherapy for leukemia produced by manipulation of multiple regulatory pathways of CD8+ T cell tolerance. Cancer Res 2013;73:605-16.
47. Chakraborty M, Abrams SI, Coleman CN, Camphausen K, Schlom J, Hodge JW. External beam radiation of tumors alters phenotype of tumor cells to render them susceptible to vaccine-mediated T-cell killing. Cancer Res 2004;64:4328-37. (Pubitemid 38802440)
48. Gnjatic S, Altorki NK, Tang DN, Tu SM, Kundra V, Ritter G, et al. NY-ESO-1 DNA vaccine induces T-cell responses that are suppressed by regulatory T cells. Clin Cancer Res 2009;15:2130-9.
49. Sabbatini P, Tsuji T, Ferran L, Ritter E, Sedrak C, Tuballes K, et al. Phase I trial of overlapping long peptides from a tumor self-antigen and poly-ICLC shows rapid induction of integrated immune response in ovarian cancer patients. Clin Cancer Res 2012;18:6497-508.
50. Gajewski TF, Fallarino F, Ashikari A, Sherman M. Immunization of HLA-A2+ melanoma patients with MAGE-3 or MelanA peptide-pulsed autologous peripheral blood mononuclear cells plus recombinant human interleukin 12. Clin Cancer Res 2001;7:895s-901s. (Pubitemid 33600943)