Impact of curative radiotherapy on the immune status of patients with localized prostate cancer

References

• Perica K, Varela JC, Oelke M, Schneck J. Adoptive T cell immunotherapy for cancer. Rambam Maimonides Med J. 2015;6:e0004. doi:10.5041/RMMJ.20769172.
   PubMed Web of Science ®Google Scholar
• Rizvi NA, Mazieres J, Planchard D, Stinchcombe TE, Dy GK, Antonia SJ, Horn L, Lena H, Minenza E, Mennecier B, et al. Activity and safety of nivolumab, an anti-PD-1 immune checkpoint inhibitor, for patients with advanced, refractory squamous non-small-cell lung cancer (CheckMate 063): a phase 2, single-arm trial. Lancet Oncol. 2015;16:257–265. doi:10.1016/S1470-2045(15)70054-9.
   PubMed Web of Science ®Google Scholar
• Schadendorf D, Hodi FS, Robert C, Weber JS, Margolin K, Hamid O, Patt D, Chen TT, Berman DM, Wolchok JD. Pooled analysis of long-term survival data from phase ii and phase iii trials of ipilimumab in unresectable or metastatic melanoma. J Clin Oncol. 2015;33:1889–1894. doi:10.1200/JCO.2014.56.2736.
   PubMed Web of Science ®Google Scholar
• Singh P, Black P. Emerging role of checkpoint inhibition in localized bladder cancer. Urologic Oncology. 2016;34:548–555. doi:10.1016/j.urolonc.2016.09.004.
   PubMed Web of Science ®Google Scholar
• Adkins DR, DiPersio JF. Total body irradiation before an allogeneic stem cell transplantation: is there a magic dose? Curr Opin Hematol. 2008;15:555–560. doi:10.1097/MOH.0b013e32831188f5.
   PubMed Web of Science ®Google Scholar
• Arenas M, Sabater S, Hernandez V, Rovirosa A, Lara PC, Biete A, Panes J. Anti-inflammatory effects of low-dose radiotherapy. Indications, dose, and radiobiological mechanisms involved. Strahlenther Onkol. 2012;188:975–981. doi:10.1007/s00066-012-0170-8.
   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.2012.00153.
   PubMedGoogle Scholar
• Formenti SC, Demaria S. Combining radiotherapy and cancer immunotherapy: a paradigm shift. J Natl Cancer Inst. 2013;105:256–265. doi:10.1093/jnci/djs629.
   PubMed Web of Science ®Google Scholar
• Golden EB, Apetoh L. Radiotherapy and immunogenic cell death. Semin Radiat Oncol. 2015;25:11–17. doi:10.1016/j.semradonc.2014.07.005.
   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:e498–509. doi:10.1016/S1470-2045(15)00007-8.
   PubMed Web of Science ®Google Scholar
• Weichselbaum RR, Liang H, Deng L, Fu YX. Radiotherapy and immunotherapy: a beneficial liaison? Nat Reviews Clin Oncology. 2017;14:365–379. doi:10.1038/nrclinonc.2016.211.
   PubMed Web of Science ®Google Scholar
• Eckert F, Gaipl US, Niedermann G, Hettich M, Schilbach K, Huber SM, Zips D. Beyond checkpoint inhibition - Immunotherapeutical strategies in combination with radiation. Clin Translational Radiat Oncol. 2017;2:29–35. doi:10.1016/j.ctro.2016.12.006.
   PubMed Web of Science ®Google Scholar
• Eckert F, Jelas I, Oehme M, Huber SM, Sonntag K, Welker C, Gillies SD, Strittmatter W, Zips D, Handgretinger R, et al. Tumor-targeted IL-12 combined with local irradiation leads to systemic tumor control via abscopal effects in vivo. Oncoimmunology. 2017;6:e1323161. doi:10.1080/2162402X.2017.1323161.
   PubMed Web of Science ®Google Scholar
• Postow MA, Callahan MK, Barker CA, Yamada Y, Yuan J, Kitano S, Mu Z, Rasalan T, Adamow M, Ritter E, et al. Immunologic correlates of the abscopal effect in a patient with melanoma. N Engl J Med. 2012;366:925–931. doi:10.1056/NEJMoa1112824.
   PubMed Web of Science ®Google Scholar
• Schoenhals JE, Seyedin SN, Tang C, Cortez MA, Niknam S, Tsouko E, Chang JY, Hahn SM, Welsh JW. Preclinical rationale and clinical considerations for radiotherapy plus immunotherapy: going beyond local control. Cancer J (Sudbury, Mass). 2016;22:130–137. doi:10.1097/PPO.0000000000000181.
   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;38:90–97. doi:10.1097/COC.0b013e3182868ec8.
   PubMed Web of Science ®Google Scholar
• Higano CS, Schellhammer PF, Small EJ, Burch PA, Nemunaitis J, Yuh L, Provost N, Frohlich MW. Integrated data from 2 randomized, double-blind, placebo-controlled, phase 3 trials of active cellular immunotherapy with sipuleucel-T in advanced prostate cancer. Cancer. 2009;115:3670–3679. doi:10.1002/cncr.24429.
   PubMed Web of Science ®Google Scholar
• Kantoff PW, Higano CS, Shore ND, Berger ER, Small EJ, Penson DF, Redfern CH, Ferrari AC, Dreicer R, Sims RB, et al. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med. 2010;363:411–422. doi:10.1056/NEJMoa1001294.
   PubMed Web of Science ®Google Scholar
• Feyerabend S, Stevanovic S, Gouttefangeas C, Wernet D, Hennenlotter J, Bedke J, Dietz K, Pascolo S, Kuczyk M, Rammensee H-G, et al. Novel multi-peptide vaccination in Hla-A2+ hormone sensitive patients with biochemical relapse of prostate cancer. Prostate. 2009;69:917–927. doi:10.1002/pros.20941.
   PubMed Web of Science ®Google Scholar
• Garnett-Benson C, Hodge JW, Gameiro SR. Combination regimens of radiation therapy and therapeutic cancer vaccines: mechanisms and opportunities. Semin Radiat Oncol. 2015;25:46–53. doi:10.1016/j.semradonc.2014.07.002.
   PubMed Web of Science ®Google Scholar
• Widenmeyer M, Griesemann H, Stevanovic S, Feyerabend S, Klein R, Attig S, Hennenlotter J, Wernet D, Kuprash DV, Sazykin AY, et al. Promiscuous survivin peptide induces robust CD4+ T-cell responses in the majority of vaccinated cancer patients. Int J Cancer. 2012;131:140–149. doi:10.1002/ijc.26365.
   PubMed Web of Science ®Google Scholar
• Drake CG. Prostate cancer as a model for tumour immunotherapy. Nat Reviews Immunol. 2010;10:580–593. doi:10.1038/nri2817.
   PubMed Web of Science ®Google Scholar
• McNeel DG, Bander NH, Beer TM, Drake CG, Fong L, Harrelson S, Kantoff PW, Madan RA, Oh WK, Peace DJ, et al. The society for immunotherapy of cancer consensus statement on immunotherapy for the treatment of prostate carcinoma. J Immunother Cancer. 2016;4:92. doi:10.1186/s40425-016-0198-x.
   PubMed Web of Science ®Google Scholar
• Schepisi G, Farolfi A, Conteduca V, Martignano F, De Lisi D, Ravaglia G, Rossi L, Menna C, Bellia SR, Barone D, et al. Immunotherapy for prostate cancer: where we are headed. Int J Mol Sci. 2017;18:2627.
   PubMedGoogle Scholar
• Yarchoan M, Hopkins A, Jaffee EM. Tumor mutational burden and response rate to PD-1 Inhibition. N Engl J Med. 2017;377:2500–2501. doi:10.1056/NEJMc1713444.
   PubMed Web of Science ®Google Scholar
• Kwon ED, Drake CG, Scher HI, Fizazi K, Bossi A, Van Den Eertwegh AJ, Krainer M, Houede N, Santos R, Mahammedi H, 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;15:700–712. doi:10.1016/S1470-2045(14)70189-5.
   PubMed Web of Science ®Google Scholar
• Baxevanis CN, Papamichail M, Perez SA. Prostate cancer vaccines: the long road to clinical application. Cancer Immunology, Immunotherapy: CII. 2015;64:401–408. doi:10.1007/s00262-015-1667-7.
   PubMed Web of Science ®Google Scholar
• Yoshimura K, Minami T, Nozawa M, Kimura T, Egawa S, Fujimoto H, Yamada A, Itoh K, Uemura H. A phase 2 randomized controlled trial of personalized peptide vaccine immunotherapy with low-dose dexamethasone versus dexamethasone alone in chemotherapy-naive castration-resistant prostate cancer. Eur Urol. 2016;70:35–41. doi:10.1016/j.eururo.2015.12.050.
   PubMed Web of Science ®Google Scholar
• McDonald R, Chow E, Lam H, Rowbottom L, Soliman H. International patterns of practice in radiotherapy for bone metastases: A review of the literature. J Bone Joint Surg Am. 2014;3:96–102. doi:10.1016/j.jbo.2014.10.003.
   Google Scholar
• Dirix P, Joniau S, Van Den Bergh L, Isebaert S, Oyen R, Deroose CM, Lerut E, Haustermans K. The role of elective pelvic radiotherapy in clinically node-negative prostate cancer: a systematic review. Radiother Oncol. 2014;110:45–54. doi:10.1016/j.radonc.2013.06.046.
   PubMed Web of Science ®Google Scholar
• Hernandez DJ, Nielsen ME, Han M, Partin AW. Contemporary evaluation of the D’amico risk classification of prostate cancer. Urology. 2007;70:931–935. doi:10.1016/j.urology.2007.08.055.
   PubMed Web of Science ®Google Scholar
• Jones CU, Hunt D, McGowan DG, Amin MB, Chetner MP, Bruner DW, Leibenhaut MH, Husain SM, Rotman M, Souhami L, et al. Radiotherapy and short-term androgen deprivation for localized prostate cancer. N Engl J Med. 2011;365:107–118. doi:10.1056/NEJMoa1012348.
   PubMed Web of Science ®Google Scholar
• Lawton CA, DeSilvio M, Roach M, 3rd, Uhl V, Kirsch R, Seider M, Rotman M, Jones C, Asbell S, Valicenti R, et al. An update of the phase III trial comparing whole pelvic to prostate only radiotherapy and neoadjuvant to adjuvant total androgen suppression: updated analysis of RTOG 94-13, with emphasis on unexpected hormone/radiation interactions. Int J Radiat Oncol Biol Phys. 2007;69:646–655. doi:10.1016/j.ijrobp.2007.04.003.
   PubMed Web of Science ®Google Scholar
• Zelefsky MJ, Pei X, Chou JF, Schechter M, Kollmeier M, Cox B, Yamada Y, Fidaleo A, Sperling D, Happersett L, et al. Dose escalation for prostate cancer radiotherapy: predictors of long-term biochemical tumor control and distant metastases-free survival outcomes. Eur Urol. 2011;60:1133–1139. doi:10.1016/j.eururo.2011.08.029.
   PubMed Web of Science ®Google Scholar
• Grimm P, Billiet I, Bostwick D, Dicker AP, Frank S, Immerzeel J, Keyes M, Kupelian P, Lee WR, Machtens S, et al. Comparative analysis of prostate-specific antigen free survival outcomes for patients with low, intermediate and high risk prostate cancer treatment by radical therapy. Results from the prostate cancer results study group. BJU Int. 2012;109(Suppl 1):22–29. doi:10.1111/j.1464-410X.2011.10827.x.
   PubMed Web of Science ®Google Scholar
• Forsberg O, Carlsson B, Malmstrom PU, Ullenhag G, Totterman TH, Essand M. High frequency of prostate antigen-directed T cells in cancer patients compared to healthy age-matched individuals. Prostate. 2009;69:70–81. doi:10.1002/pros.20858.
   PubMed Web of Science ®Google Scholar
• Kiessling A, Fussel S, Schmitz M, Stevanovic S, Meye A, Weigle B, Klenk U, Wirth MP, Rieber EP. Identification of an HLA-A*0201-restricted T-cell epitope derived from the prostate cancer-associated protein trp-p8. Prostate. 2003;56:270–279. doi:10.1002/pros.10265.
   PubMed Web of Science ®Google Scholar
• Komatsu N, Terasaki Y, Moriya F, Suekane S, Noguchi M, Todo S, Itoh K, Shichijo S. A beta-tubulin 5-derived peptide induces cytotoxic T lymphocytes restricted to the HLA-A24 allele in prostate cancer patients. Exp Ther Med. 2010;1:833–839. doi:10.3892/etm.2010.120.
   PubMed Web of Science ®Google Scholar
• Tabi Z, Spary LK, Coleman S, Clayton A, Mason MD, Staffurth J. Resistance of CD45RA- T cells to apoptosis and functional impairment, and activation of tumor-antigen specific T cells during radiation therapy of prostate cancer. J Immunol (Baltimore, Md. 1950;2010(185):1330–1339.
   Google Scholar
• Bernstein MB, Garnett CT, Zhang H, Velcich A, Wattenberg MM, Gameiro SR, Kalnicki S, Hodge JW, Guha C. Radiation-induced modulation of costimulatory and coinhibitory T-cell signaling molecules on human prostate carcinoma cells promotes productive antitumor immune interactions. Cancer Biother Radiopharm. 2014;29:153–161. doi:10.1089/cbr.2013.1578.
   PubMed Web of Science ®Google Scholar
• Gameiro SR, Malamas AS, Bernstein MB, Tsang KY, Vassantachart A, Sahoo N, Tailor R, Pidikiti R, Guha CP, Hahn SM, et al. Tumor cells surviving exposure to proton or photon radiation share a common immunogenic modulation signature, rendering them more sensitive to T cell-mediated killing. Int J Radiat Oncol Biol Phys. 2016;95:120–130. doi:10.1016/j.ijrobp.2016.02.022.
   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;5:403–416. doi:10.18632/oncotarget.1719.
   PubMed Web of Science ®Google Scholar
• Chaudhary B, Elkord E. Regulatory T cells in the tumor microenvironment and cancer progression: role and therapeutic targeting. Vaccines. 2016;4.
   PubMed Web of Science ®Google Scholar
• Komatsu N, Hori S. Full restoration of peripheral Foxp3+ regulatory T cell pool by radioresistant host cells in scurfy bone marrow chimeras. Proc Natl Acad Sci U S A. 2007;104:8959–8964. doi:10.1073/pnas.0702004104.
   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;368:252–261. doi:10.1016/j.canlet.2015.03.003.
   PubMed Web of Science ®Google Scholar
• Schaue D, Comin-Anduix B, Ribas A, Zhang L, Goodglick L, Sayre JW, Debucquoy A, Haustermans K, McBride WH. T-cell responses to survivin in cancer patients undergoing radiation therapy. Clin Cancer Res. 2008;14:4883–4890. doi:10.1158/1078-0432.CCR-07-4462.
   PubMed Web of Science ®Google Scholar
• Elhilali MM, Paika KD, Brosman S, Fahey JL. Critical evaluation of lymphocyte functions in urological cancer patients. Cancer Res. 1976;36:132–137.
   PubMed Web of Science ®Google Scholar
• El-Saghire H, Vandevoorde C, Ost P, Monsieurs P, Michaux A, De Meerleer G, Baatout S, Thierens H. Intensity modulated radiotherapy induces pro-inflammatory and pro-survival responses in prostate cancer patients. Int J Oncol. 2014;44:1073–1083. doi:10.3892/ijo.2014.2260.
   PubMed Web of Science ®Google Scholar
• Hurwitz MD, Kaur P, Nagaraja GM, Bausero MA, Manola J, Asea A. Radiation therapy induces circulating serum Hsp72 in patients with prostate cancer. Radiother Oncol. 2010;95:350–358. doi:10.1016/j.radonc.2010.03.024.
   PubMed Web of Science ®Google Scholar
• Yang ZR, Zhao N, Meng J, Shi ZL, Li BX, Wu XW, Li P, Zhang Q, Wei XB, Fu S. Peripheral lymphocyte subset variation predicts prostate cancer carbon ion radiotherapy outcomes. Oncotarget. 2016;7:26422–26435. doi:10.18632/oncotarget.8389.
   PubMedGoogle Scholar
• Sage EK, Schmid TE, Geinitz H, Gehrmann M, Sedelmayr M, Duma MN, Combs SE, Multhoff G. Effects of definitive and salvage radiotherapy on the distribution of lymphocyte subpopulations in prostate cancer patients. Strahlenther Onkol. 2017;193:648–655. doi:10.1007/s00066-017-1144-7.
   PubMed Web of Science ®Google Scholar
• Kalina JL, Neilson DS, Comber AP, Rauw JM, Alexander AS, Vergidis J, Lum JJ. Immune modulation by androgen deprivation and radiation therapy: implications for prostate cancer immunotherapy. Cancers. 2017;9.
   PubMed Web of Science ®Google Scholar
• Van Meir H, Nout RA, Welters MJ, Loof NM, De Kam ML, Van Ham JJ, Samuels S, Kenter GG, Cohen AF, Melief CJ, et al. Impact of (chemo)radiotherapy on immune cell composition and function in cervical cancer patients. Oncoimmunology. 2016;6:e1267095. doi:10.1080/2162402X.2016.1267095.
   PubMed Web of Science ®Google Scholar
• Finkelstein SE, Rodriguez F, Dunn M, Farmello MJ, Smilee R, Janssen W, Kang L, Chuang T, Seigne J, Pow-Sang J, et al. Serial assessment of lymphocytes and apoptosis in the prostate during coordinated intraprostatic dendritic cell injection and radiotherapy. Immunotherapy. 2012;4:373–382. doi:10.2217/imt.12.24.
   PubMed Web of Science ®Google Scholar
• Corfield J, Crozier J, Joshua AM, Bolton D, Lawrentschuk N. Understanding the role of new systemic agents in the treatment of prostate cancer. BJU Int. 2016;118(Suppl 3):8–13. doi:10.1111/bju.13633.
   PubMedGoogle Scholar
• Gillessen S, Attard G, Beer TM, Beltran H, Bossi A, Bristow R, Carver B, Castellano D, Chung BH, Clarke N, et al. Management of patients with advanced prostate cancer: the report of the Advanced Prostate Cancer Consensus Conference APCCC 2017. Eur Urol. 2018;73:178–211. doi:10.1016/j.eururo.2017.06.002.
   PubMed Web of Science ®Google Scholar
• Harris TJ, Hipkiss EL, Borzillary S, Wada S, Grosso JF, Yen HR, Getnet D, Bruno TC, Goldberg MV, Pardoll DM, et al. Radiotherapy augments the immune response to prostate cancer in a time-dependent manner. Prostate. 2008;68:1319–1329. doi:10.1002/pros.20794.
   PubMed Web of Science ®Google Scholar
• Gulley JL, Arlen PM, Bastian A, Morin S, Marte J, Beetham P, Tsang KY, Yokokawa J, Hodge JW, Menard C, et al. Combining a recombinant cancer vaccine with standard definitive radiotherapy in patients with localized prostate cancer. Clin Cancer Res. 2005;11:3353–3362. doi:10.1158/1078-0432.CCR-04-2062.
   PubMed Web of Science ®Google Scholar
• Fujita T, Teh BS, Timme TL, Mai WY, Satoh T, Kusaka N, Fattah EA, Aguilar-Cordova E, Butler EB, et al. Sustained long-term immune responses after in situ gene therapy combined with radiotherapy and hormonal therapy in prostate cancer patients. Int J Radiat Oncol Biol Phys. 2006;65:84–90. doi:10.1016/j.ijrobp.2005.11.009.
   PubMed Web of Science ®Google Scholar
• Kang J, Demaria S, Formenti S. Current clinical trials testing the combination of immunotherapy with radiotherapy. J Immunother Cancer. 2016;4:51. doi:10.1186/s40425-016-0156-7.
   PubMed Web of Science ®Google Scholar
• Gandhi SJ, Minn AJ, Vonderheide RH, Wherry EJ, Hahn SM, Maity A. Awakening the immune system with radiation: optimal dose and fractionation. Cancer Lett. 2015;368:185–190. doi:10.1016/j.canlet.2015.03.024.
   PubMed Web of Science ®Google Scholar
• Chandran PA, Laske K, Cazaly A, Rusch E, Schmid-Horch B, Rammensee HG, Ottensmeier CH, Gouttefangeas C. Validation of immunomonitoring methods for application in clinical studies: the HLA-peptide multimer staining assay. Cytometry Part B, Clinical Cytometry. 2018;94:342–353.
   PubMed Web of Science ®Google Scholar
• Hadrup SR, Maurer D, Laske K, Frosig TM, Andersen SR, Britten CM, van der Burg SH, Walter S, Gouttefangeas C. Cryopreservation of MHC multimers: recommendations for quality assurance in detection of antigen specific T cells. Cytometry A: Journal Int Soc Anal Cytol. 2015;87:37–48. doi:10.1002/cyto.a.22575.
   PubMedGoogle Scholar