Using immunotherapy to enhance the response of a C3H mammary carcinoma to proton radiation

References

• Salama AKS, Moschos SJ. Next steps in immuno-oncology: enhancing antitumor effects through appropriate patient selection and rationally designed combination strategies. Ann Oncol. 2017;28(1):57–74. doi: 10.1093/annonc/mdw534.
   PubMed Web of Science ®Google Scholar
• Dunn GP, Bruce AT, Ikeda H, et al. Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol. 2002;3(11):991–998. doi: 10.1038/ni1102-991.
   PubMed Web of Science ®Google Scholar
• Callahan MK, Postow MA, Wolchok JP. CTLA-4 and PD-1 pathway blockade: combinations in the clinic. Front Oncol. 2014;4:385. doi: 10.3389/fonc.2014.00385.
   PubMed Web of Science ®Google Scholar
• Antonia SJ, Villegas A, Daniel D, et al. Durvalumab after chemoradiotherapy in stage III non-small-cell lung cancer. N Engl J Med. 2017;377(20):1919–1929. doi: 10.1056/NEJMoa1709937.
   PubMed Web of Science ®Google Scholar
• Syn NL, Teng MWL, Mok TSK, et al. De-novo and acquired resistance to immune checkpoint targeting. Lancet Oncol. 2017;18(12):e731–741–e741. doi: 10.1016/S1470-2045(17)30607-1.
   Web of Science ®Google Scholar
• Postow MA, Callahan MK, Wolchok JD. Immune checkpoint blockade in cancer therapy. J Clin Oncol. 2015;33(17):1974–1982. doi: 10.1200/JCO.2014.59.4358.
   PubMed Web of Science ®Google Scholar
• Chen DS, Mellman I. Oncology meets immunology: the cancer-immunity cycle. Immunity. 2013;39(1):1–10. doi: 10.1016/j.immuni.2013.07.012.
   PubMed Web of Science ®Google Scholar
• Horsman MR, Wittenborn TR, Nielsen PS, et al. Tumors resistant to checkpoint inhibitors can become sensitive after treatment with vascular disrupting agents. Int. J. Mol. Sci. 2020;21:4778. doi: 10.3390/ijms21134778.
   PubMed Web of Science ®Google Scholar
• Lauber K, Brix N, Ernst A, et al. Targeting the heat shock response in combination with radiotherapy: sensitizing cancer cells to irradiation-induced cell death and heating up their immunogenicity. Cancer Lett. 2015;368(2):209–229. doi: 10.1016/j.canlet.2015.02.047.
   PubMed Web of Science ®Google Scholar
• Stone HB, Peters LJ, Milas L. Effect of host immune capability on radiocurability and subsequent transplantability of a murine fibrosarcoma. J Natl Cancer Inst. 1979;63(5):1229–1235.
   PubMedGoogle Scholar
• Lee Y, Auh SL, Wang Y, et al. Therapeutic effects of ablative radiation on local tumor require CD8+ T cells: changing strategies for cancer treatment. Blood. 2009;114(3):589–595. doi: 10.1182/blood-2009-02-206870.
   PubMed Web of Science ®Google Scholar
• Demaria S, Kawashima N, Yang AM, et al. Immune-mediated inhibition of metastases after treatment with local radiation and CTLA-4 blockade in a mouse model of breast cancer. Clin. Cancer Res. 2005;11(2):728–734. doi: 10.1158/1078-0432.728.11.2.
   PubMed Web of Science ®Google Scholar
• Dewan MZ, Galloway AE, Kawashima N, 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(17):5379–5388. doi: 10.1158/1078-0432.CCR-09-0265.
   PubMed Web of Science ®Google Scholar
• Dovedi SJ, Adlard AL, Lipowska-Bhalla G, et al. Acquired resistance to fractionated radiotherapy can be overcome by concurrent PD-L1 blockade. Cancer Res. 2014;74(19):5458–5468. doi: 10.1158/0008-5472.CAN-14-1258.
   PubMed Web of Science ®Google Scholar
• Durante M, Reppingen N, Held KD. Immunologically augmented cancer treatment using modern radiotherapy. Trends Mol Med. 2013;19(9):565–582. doi: 10.1016/j.molmed.2013.05.007.
   PubMed Web of Science ®Google Scholar
• Bernier J. Immuno-oncology: allying forces of radio- and immuno-therapy to enhance cancer cell killing. Crit Rev Oncol Hematol. 2016;108:97–108. doi: 10.1016/j.critrevonc.2016.11.001.
   PubMed Web of Science ®Google Scholar
• Van Limbergen EJ, De Ruysscher DK, Olivo Pimentel V, et al. Combining radiotherapy with immunotherapy: the past, the present and the future. Br J Radiol. 2017;90(1076):20170157. doi: 10.1259/bjr.20170157.
   PubMed Web of Science ®Google Scholar
• Mohan R, Grosshans D. Proton therapy – present and future. Adv Drug Deliv Rev. 2017;109:26–44. doi: 10.1016/j.addr.2016.11.006.
   PubMed Web of Science ®Google Scholar
• Tubin S, Yan W, Mourad WF, et al. The future of radiation-induced abscopal response: beyond conventional radiotherapy approaches. Future Oncol. 2020;16(16):1137–1151. doi: 10.2217/fon-2020-0063.
   PubMed Web of Science ®Google Scholar
• Overgaard J. Simultaneous and sequential hyperthermia and radiation treatment of an experimental tumor and its surrounding normal tissue in vivo. Int J Radiat Oncol Biol Phys. 1980;6(11):1507–1517. doi: 10.1016/0360-3016(80)90008-5.
   PubMed Web of Science ®Google Scholar
• Verbrugge I, Hagekyriakou J, Sharp LL, et al. Radiotherapy increases the permissiveness of established mammary tumors to rejection by immunomodulatory antibodies. Cancer Res. 2012;72(13):3163–3174. doi: 10.1158/0008-5472.CAN-12-0210.
   PubMed Web of Science ®Google Scholar
• Sørensen BS, Bassler N, Nielsen S, et al. Relative biological effectiveness (RBE) and distal edge effects of proton radiation on early damage in vivo. Acta Oncol. 2017;56(11):1387–1391. doi: 10.1080/0284186X.2017.1351621.
   PubMed Web of Science ®Google Scholar
• Horsman MR, Chaplin DJ, Overgaard J. Combination of nicotinamide and hyperthermia to eliminate radioresistant chronically and acutely hypoxic tumour cells. Cancer Res. 1990;50:7430–7436.
   PubMed Web of Science ®Google Scholar
• Baumann M, Krause M, Hill R. Exploring the role of cancer stem cells in radioresistance. Nat Rev Cancer. 2008;8(7):545–554. doi: 10.1038/nrc2419.
   PubMed Web of Science ®Google Scholar
• Paganetti H. Mechanisms and review of clinical evidence of variations in relative biological effectiveness in proton therapy. Int J Radiat Oncol Biol Phys. 2022;112(1):222–236. doi: 10.1016/j.ijrobp.2021.08.015.
   PubMed Web of Science ®Google Scholar
• Mirjolet C, Nicol A, Limagne E, et al. Impact of proton therapy on antitumor immune response. Sci Rep. 2021;11(1):13444. doi: 10.1038/s41598-021-92942-1.
   PubMed Web of Science ®Google Scholar
• Chen M-F, Chen P-T, Hsieh C-C, et al. Effect of proton therapy on tumor cell killing and immune microenvironment for hepatocellular carcinoma. Cells. 2023;12:332. doi: 10.3390/cells12020332.
   PubMed Web of Science ®Google Scholar
• Parry RV, Chemnitz JM, Frauwirth KA, et al. CTLA-4 and PD-1 receptors inhibit T-cell activation by distinct mechanisms. Mol Cell Biol. 2005;25(21):9543–9553. doi: 10.1128/MCB.25.21.9543-9553.2005.
   PubMed Web of Science ®Google Scholar
• Salmon HW, Siemann DW. Effect of the second-generation vascular disrupting agent OXi4503 on tumor vascularity. Clin Cancer Res. 2006;12(13):4090–4094. doi: 10.1158/1078-0432.CCR-06-0163.
   PubMed Web of Science ®Google Scholar
• Folkes LK, Christlieb M, Madej E, et al. Oxidative metabolism of combretastatin A-1 produces quinone intermediates with the potential to bind to nucleophiles and to enhance oxidative stress via free radicals. Chem Res Toxicol. 2007;20(12):1885–1894. doi: 10.1021/tx7002195.
   PubMed Web of Science ®Google Scholar
• Song CW, Glatstein E, Marks LB, et al. Biological principals of stereotactic body radiation therapy (SBRT) and stereotactic radiation surgery (SRS): indirect cell death. Int J Radiat Oncol Biol Phys. 2021;110(1):21–34. doi: 10.1016/j.ijrobp.2019.02.047.
   PubMed Web of Science ®Google Scholar
• Elming PB, Sørensen BS, Oei AL, et al. Hyperthermia: the optimal treatment to overcome radiation resistant hypoxia. Cancers. 2019;11:60. doi: 10.3390/cancers11010060.
   PubMed Web of Science ®Google Scholar
• Thangamathesvaran L, Shah R, Verma R, et al. Immune checkpoint inhibitors and radiotherapy – concept and review of current literature. Ann Transl Med. 2018;6(8):155. doi: 10.21037/atm.2018.03.09.
   PubMed Web of Science ®Google Scholar
• Oei AL, Korangath P, Mulka K, et al. Enhancing the abscopal effect of radiation and immune checkpoint inhibitor therapies with magnetic nanoparticle hyperthermia in a model of metastatic breast cancer. Int J Hyperthermia. 2019;36(sup1):47–63. doi: 10.1080/02656736.2019.1685686.
   PubMed Web of Science ®Google Scholar
• Zhao X, Shao C. Radiotherapy-mediated immunomodulation and anti-tumor abscopal effect combining immune checkpoint blockade. Cancers. 2020;12:2762. doi: 10.3390/cancers12102762.
   PubMed Web of Science ®Google Scholar
• Iversen AB, Busk M, Horsman MR. Induction of hypoxia by vascular disrupting agents and the significance for their combination with radiation therapy. Acta Oncol. 2013;52(7):1320–1326. doi: 10.3109/0284186X.2013.825050.
   PubMed Web of Science ®Google Scholar