Combined Treatment of Radiotherapy and Immunotherapy for Urological Malignancies: Current Evidence and Clinical Considerations

References

• Order SE. The effects of therapeutic irradiation on lymphocytes and immunity. Cancer. 1977;39(S2):737–743.300040
   PubMed Web of Science ®Google Scholar
• Jacob VD. The Modern Technology of Radiation Oncology. Madison, WI: Medical Physics Publishing; 2013.
   Google Scholar
• Hall EJ, Giaccia AJ. Radiobiology for the Radiologist. 6th ed. Philadelphia: Lippincott Williams & Wilkins; 2006.
   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):1229–1235.291749
   PubMedGoogle Scholar
• Demaria S, Golden EB, Formenti SC. Role of local radiation therapy in cancer immunotherapy. JAMA Oncol. 2015;1(9):1325–1332. doi:10.1001/jamaoncol.2015.275626270858
   PubMed Web of Science ®Google Scholar
• Formenti SC, Demaria S. Systemic effects of local radiotherapy. Lancet Oncol. 2009;10(7):718–726. doi:10.1016/S1470-2045(09)70082-819573801
   PubMed Web of Science ®Google Scholar
• Salama AK, Postow MA, Salama JK. Irradiation and immunotherapy: from concept to the clinic. Cancer. 2016;122(11):1659–1671. doi:10.1002/cncr.2988926914620
   PubMed Web of Science ®Google Scholar
• Park B, Yee C, Lee KM. The effect of radiation on the immune response to cancers. Int J Mol Sci. 2014;15(1):927–943. doi:10.3390/ijms1501092724434638
   PubMed Web of Science ®Google Scholar
• Brooks ED, Schoenhals JE, Tang C, et al. Stereotactic ablative radiation therapy combined with immunotherapy for solid tumors. Cancer J. 2016;22(4):257–266. doi:10.1097/PPO.000000000000021027441745
   PubMed Web of Science ®Google Scholar
• Formenti SC, Demaria S. Combining radiotherapy and cancer immunotherapy: a paradigm shift. J Natl Cancer Inst. 2013;105(4):256–265. doi:10.1093/jnci/djs62923291374
   PubMed Web of Science ®Google Scholar
• Weichselbaum RR, Liang H, Deng L, Fu Y-X. Radiotherapy and immunotherapy: a beneficial liaison? Nat Rev Clin Oncol. 2017;14(6):365–379.28094262
   PubMed Web of Science ®Google Scholar
• Shabason JE, Minn AJ. Radiation and immune checkpoint blockade: from bench to clinic. Semin Radiat Oncol. 2017;27(3):289–298. doi:10.1016/j.semradonc.2017.03.00228577836
   PubMed Web of Science ®Google Scholar
• Kroemer G, Galluzzi L, Kepp O, Zitvogel L. Immunogenic cell death in cancer therapy. Annu Rev Immunol. 2013;31:51–72. doi:10.1146/annurev-immunol-032712-10000823157435
   PubMed Web of Science ®Google Scholar
• Akashi M, Hachiya M, Koeffler HP, Suzuki G. Irradiation increases levels of GM-CSF through RNA stabilization which requires an AU-rich region in cancer cells. Biochem Biophys Res Commun. 1992;189(2):986–993. doi:10.1016/0006-291X(92)92301-D1472071
   PubMed Web of Science ®Google Scholar
• Demaria S, Pilones KA, Vanpouille-Box C, Golden EB, Formenti SC. The optimal partnership of radiation and immunotherapy: from preclinical studies to clinical translation. Radiat Res. 2014;182(2):170–181. doi:10.1667/RR13500.124937779
   PubMed Web of Science ®Google Scholar
• Gameiro SR, Jammeh ML, Wattenberg MM, Tsang KY, Ferrone S, Hodge JW. Radiation-induced immunogenic modulation of tumor enhances antigen processing and calreticulin exposure, resulting in enhanced T-cell killing. Oncotarget. 2014;5(2):403–416. doi:10.18632/oncotarget.171924480782
   PubMed Web of Science ®Google Scholar
• Rovere-Querini P, Capobianco A, Scaffidi P, et al. HMGB1 is an endogenous immune adjuvant released by necrotic cells. EMBO Rep. 2004;5(8):825–830. doi:10.1038/sj.embor.740020515272298
   PubMed Web of Science ®Google Scholar
• Ganss R, Ryschich E, Klar E, Arnold B, Hämmerling GJ. Combination of T-cell therapy and trigger of inflammation induces remodeling of the vasculature and tumor eradication. J Cancer Research. 2002;62(5):1462–1470.
   Google Scholar
• Matsumura S, Wang B, Kawashima N, et al. Radiation-induced CXCL16 release by breast cancer cells attracts effector T cells. J Immunol. 2008;181(5):3099–3107. doi:10.4049/jimmunol.181.5.309918713980
   PubMed Web of Science ®Google Scholar
• Shahabi V, Postow MA, Tuck D, Wolchok JD. Immune-priming of the tumor microenvironment by radiotherapy: rationale for combination with immunotherapy to improve anticancer efficacy. Am J Clin Oncol. 2015;38(1):90–97. doi:10.1097/COC.0b013e3182868ec825616204
   PubMed Web of Science ®Google Scholar
• Chakraborty M, Abrams SI, Coleman CN, Camphausen K, Hodge JWJCR. External beam radiation of tumors alters phenotype of tumor cells to render them susceptible to vaccine-mediated T-cell killing. Cancer Res. 2004;64(12):4328–4337. doi:10.1158/0008-5472.CAN-04-007315205348
   PubMed Web of Science ®Google Scholar
• Chakraborty M, Abrams SI, Camphausen K, et al. Irradiation of tumor cells up-regulates fas and enhances CTL lytic activity and CTL adoptive immunotherapy. J Immunol. 2003;170(12):6338–6347. doi:10.4049/jimmunol.170.12.633812794167
   PubMed Web of Science ®Google Scholar
• Garnett CT, Palena C, Chakraborty M, Tsang K-Y, Schlom J, Hodge JW. Sublethal irradiation of human tumor cells modulates phenotype resulting in enhanced killing by cytotoxic T lymphocytes. Cancer Res. 2004;64(21):7985–7994. doi:10.1158/0008-5472.CAN-04-152515520206
   PubMed Web of Science ®Google Scholar
• Sharabi AB, Nirschl CJ, Kochel CM, et al. Stereotactic radiation therapy augments antigen-specific PD-1-mediated antitumor immune responses via cross-presentation of tumor antigen. J Cancer Immunol Res. 2016;3(4):345–355. doi:10.1158/2326-6066.CIR-14-0196
   Web of Science ®Google Scholar
• Kachikwu EL, Iwamoto KS, Liao YP, et al. Radiation enhances regulatory T cell representation. Int J Radiat Oncol Biol Phys. 2011;81(4):1128–1135. doi:10.1016/j.ijrobp.2010.09.03421093169
   PubMed Web of Science ®Google Scholar
• Kumar V, Patel S, Tcyganov E, Gabrilovich DI. The nature of myeloid-derived suppressor cells in the tumor microenvironment. J Trends Immunol. 2016;37(3):208–220. doi:10.1016/j.it.2016.01.004
   PubMed Web of Science ®Google Scholar
• Wu CT, Chen WC, Chang YH, Lin WY, Chen MF. The role of PD-L1 in the radiation response and clinical outcome for bladder cancer. Sci Rep. 2016;6:19740. doi:10.1038/srep1974026804478
   PubMed Web of Science ®Google Scholar
• Persa E, Balogh A, Safrany G, Lumniczky K. The effect of ionizing radiation on regulatory T cells in health and disease. Cancer Lett. 2015;368(2):252–261. doi:10.1016/j.canlet.2015.03.00325754816
   PubMed Web of Science ®Google Scholar
• Twyman-Saint Victor C, Rech AJ, Maity A, et al. Radiation and dual checkpoint blockade activate non-redundant immune mechanisms in cancer. Nature. 2015;520(7547):373–377. doi:10.1038/nature1429225754329
   PubMed Web of Science ®Google Scholar
• Mole RH. Whole body irradiation-radiobiology or medicine? Br J Radiol. 1953;26(305):234–241. doi:10.1259/0007-1285-26-305-23413042090
   PubMed Web of Science ®Google Scholar
• Abuodeh Y, Venkat P, Kim S. Systematic review of case reports on the abscopal effect. Curr Probl Cancer. 2016;40(1):25–37. doi:10.1016/j.currproblcancer.2015.10.00126582738
   PubMed Web of Science ®Google Scholar
• Golden EB, Chhabra A, Chachoua A, et al. Local radiotherapy and granulocyte-macrophage colony-stimulating factor to generate abscopal responses in patients with metastatic solid tumours: a proof-of-principle trial. Lancet Oncol. 2015;16(7):795–803. doi:10.1016/S1470-2045(15)00054-626095785
   PubMed Web of Science ®Google Scholar
• Park SS, Dong H, Liu X, et al. PD-1 Restrains radiotherapy-induced abscopal effect. Cancer Immunol Res. 2015;3(6):610–619. doi:10.1158/2326-6066.CIR-14-013825701325
   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-09-026519706802
   PubMed Web of Science ®Google 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-2009-02-20687019349616
   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-14-125825274032
   PubMed Web of Science ®Google Scholar
• Kantoff PW, Higano CS, Shore ND, et al. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med. 2010;363(5):411–422. doi:10.1056/NEJMoa100129420818862
   PubMed Web of Science ®Google Scholar
• Hoos A, Ibrahim R, Korman A, et al. Development of ipilimumab: contribution to a new paradigm for cancer immunotherapy. Semin Oncol. 2010;37(5):533–546. doi:10.1053/j.seminoncol.2010.09.01521074069
   PubMed Web of Science ®Google Scholar
• Demaria S, Formenti SC. Radiation as an immunological adjuvant: current evidence on dose and fractionation. Front Oncol. 2012;2:153. doi:10.3389/fonc.2012.0015323112958
   PubMedGoogle Scholar
• Tsai MH, Cook JA, Chandramouli GV, et al. Gene expression profiling of breast, prostate, and glioma cells following single versus fractionated doses of radiation. Cancer Res. 2007;67(8):3845–3852. doi:10.1158/0008-5472.CAN-06-425017440099
   PubMed Web of Science ®Google Scholar
• John-Aryankalayil M, Palayoor ST, Cerna D, et al. Fractionated radiation therapy can induce a molecular profile for therapeutic targeting. Radiat Res. 2010;174(4):446–458. doi:10.1667/RR2105.120726711
   PubMed Web of Science ®Google Scholar
• Lugade AA, Moran JP, Gerber SA, Rose RC, Frelinger JG, Lord EM. Local radiation therapy of B16 melanoma tumors increases the generation of tumor antigen-specific effector cells that traffic to the tumor. J Immunol. 2005;174(12):7516–7523. doi:10.4049/jimmunol.174.12.751615944250
   PubMed Web of Science ®Google Scholar
• Sharabi AB, Lim M, DeWeese TL, Drake CG. Radiation and checkpoint blockade immunotherapy: radiosensitisation and potential mechanisms of synergy. Lancet Oncol. 2015;16(13):e498–e509. doi:10.1016/S1470-2045(15)00007-826433823
   PubMed Web of Science ®Google Scholar
• Young KH, Baird JR, Savage T, et al. Optimizing timing of immunotherapy improves control of tumors by hypofractionated radiation therapy. PLoS One. 2016;11(6):e0157164. doi:10.1371/journal.pone.015716427281029
   PubMed Web of Science ®Google Scholar
• Tree AC, Jones K, Hafeez S, et al. Dose-limiting urinary toxicity with pembrolizumab combined with weekly hypofractionated radiation therapy in bladder cancer. Int J Radiat Oncol Biol Phys. 2018;101(5):1168–1171. doi:10.1016/j.ijrobp.2018.04.07030012528
   PubMed Web of Science ®Google Scholar
• Kwon ED, Drake CG, Scher HI, et al. Ipilimumab versus placebo after radiotherapy in patients with metastatic castration-resistant prostate cancer that had progressed after docetaxel chemotherapy (CA184-043): a multicentre, randomised, double-blind, Phase 3 trial. Lancet Oncol. 2014;15(7):700–712. doi:10.1016/S1470-2045(14)70189-524831977
   PubMed Web of Science ®Google Scholar
• Cristina M, Cinzia I, Ugo DG, et al. Nivolumab (NIVO) in combination with stereotactic body radiotherapy (SBRT) in pretreated patients (pts) with metastatic renal cell carcinoma (mRCC): first results of phase II NIVES study. J Clin Oncol. 2020;38(abstr):613. doi:10.1200/JCO.2020.38.6_suppl.61331829907
   PubMed Web of Science ®Google Scholar
• Hans H, Dendra VM, Chul A, et al. Combination of dual immune checkpoint inhibition (ICI) with stereotactic radiation (SBRT) in metastatic renal cell carcinoma (mRCC)(RADVAX RCC). J Clin Oncol. 2020;38(abstr):614. doi:10.1200/JCO.2020.38.6_suppl.614
   Google Scholar