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Erschienen in: Clinical and Translational Oncology 12/2020

22.05.2020 | Review Article

Tumor microenvironment, immune response and post-radiotherapy tumor clearance

verfasst von: M. I. Koukourakis, A. Giatromanolaki

Erschienen in: Clinical and Translational Oncology | Ausgabe 12/2020

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Abstract

Radiotherapy is the treatment of choice for many cancer patients. Residual tumor leads to local recurrence after a period of an equilibrium created between proliferating, quiescent and dying cancer cells. The tumor microenvironment is a main obstacle for the efficacy of radiotherapy, as impaired blood flow leads to hypoxia, acidity and reduced accessibility of radiosensitizers. Eradication of remnant disease is an intractable clinical quest. After more than a century of research, anti-tumor immunity has gained a dominant position in oncology research and therapy. Immune cells play a significant role in the eradication of tumors during and after the completion of radiotherapy. The tumor equilibrium reached in the irradiated tumor may shift towards cancer cell eradication if the immune response is appropriately modulated. In the modern immunotherapy era, clinical trials are urged to standardize immunotherapy schemes that could be safely applied to improve clearance of the post-radiotherapy remnant disease.
Literatur
1.
Zurück zum Zitat Grubbe AH (obituary). Br Med J. 1960;2:609. Grubbe AH (obituary). Br Med J. 1960;2:609.
2.
Zurück zum Zitat Moris L, Cumberbatch MG, Van den Broeck T, Gandaglia G, Fossati N, Kelly B, Pal R, Briers E, Cornford P, De Santis M, Fanti S, Gillessen S, Grummet JP, Henry AM, Lam TBL, Lardas M, Liew M, Mason MD, Omar MI, Rouvière O, Schoots IG, Tilki D, van den Bergh RCN, van Der Kwast TH, van Der Poel HG, Willemse PM, Yuan CY, Konety B, Dorff T, Jain S, Mottet N, Wiegel T. Benefits and risks of primary treatments for high-risk localized and locally advanced prostate cancer: an international multidisciplinary systematic review. Eur Urol. 2020;77:614–27.PubMed Moris L, Cumberbatch MG, Van den Broeck T, Gandaglia G, Fossati N, Kelly B, Pal R, Briers E, Cornford P, De Santis M, Fanti S, Gillessen S, Grummet JP, Henry AM, Lam TBL, Lardas M, Liew M, Mason MD, Omar MI, Rouvière O, Schoots IG, Tilki D, van den Bergh RCN, van Der Kwast TH, van Der Poel HG, Willemse PM, Yuan CY, Konety B, Dorff T, Jain S, Mottet N, Wiegel T. Benefits and risks of primary treatments for high-risk localized and locally advanced prostate cancer: an international multidisciplinary systematic review. Eur Urol. 2020;77:614–27.PubMed
3.
Zurück zum Zitat Maier P, Hartmann L, Wenz F, Herskind C. Cellular Pathways in Response to Ionizing Radiation and Their Targetability for Tumor Radiosensitization. Int J Mol Sci. 2016;17(1):E102. Maier P, Hartmann L, Wenz F, Herskind C. Cellular Pathways in Response to Ionizing Radiation and Their Targetability for Tumor Radiosensitization. Int J Mol Sci. 2016;17(1):E102.
4.
Zurück zum Zitat Kim W, Lee S, Seo D, Kim D, Kim K, Kim E, Kang J, Seong KM, Youn H, Youn B. Cellular stress responses in radiotherapy. Cells. 2019;8(9):E1105.PubMed Kim W, Lee S, Seo D, Kim D, Kim K, Kim E, Kang J, Seong KM, Youn H, Youn B. Cellular stress responses in radiotherapy. Cells. 2019;8(9):E1105.PubMed
5.
Zurück zum Zitat Mitrakas AG, Kalamida D, Giatromanolaki A, Pouliliou S, Tsolou A, Kyranas R, Koukourakis MI. Autophagic flux response and glioblastoma sensitivity to radiation. Cancer Biol Med. 2018;15:260–74.PubMedPubMedCentral Mitrakas AG, Kalamida D, Giatromanolaki A, Pouliliou S, Tsolou A, Kyranas R, Koukourakis MI. Autophagic flux response and glioblastoma sensitivity to radiation. Cancer Biol Med. 2018;15:260–74.PubMedPubMedCentral
6.
Zurück zum Zitat Koukourakis MI, Mitrakas AG, Giatromanolaki A. Therapeutic interactions of autophagy with radiation and temozolomide in glioblastoma: evidence and issues to resolve. Br J Cancer. 2016;114:485–96.PubMedPubMedCentral Koukourakis MI, Mitrakas AG, Giatromanolaki A. Therapeutic interactions of autophagy with radiation and temozolomide in glioblastoma: evidence and issues to resolve. Br J Cancer. 2016;114:485–96.PubMedPubMedCentral
7.
Zurück zum Zitat Giatromanolaki A, Sivridis E, Koukourakis MI. The pathology of tumor stromatogenesis. Cancer Biol Ther. 2007;6:639–45.PubMed Giatromanolaki A, Sivridis E, Koukourakis MI. The pathology of tumor stromatogenesis. Cancer Biol Ther. 2007;6:639–45.PubMed
8.
Zurück zum Zitat Koukourakis MI, Giatromanolaki A, Harris AL, Sivridis E. Comparison of metabolic pathways between cancer cells and stromal cells in colorectal carcinomas: a metabolic survival role for tumor-associated stroma. Cancer Res. 2006;15(66):632–7. Koukourakis MI, Giatromanolaki A, Harris AL, Sivridis E. Comparison of metabolic pathways between cancer cells and stromal cells in colorectal carcinomas: a metabolic survival role for tumor-associated stroma. Cancer Res. 2006;15(66):632–7.
9.
Zurück zum Zitat Giatromanolaki A, Sivridis E, Koukourakis MI. Tumour angiogenesis: vascular growth and survival. APMIS. 2004;112:431–40.PubMed Giatromanolaki A, Sivridis E, Koukourakis MI. Tumour angiogenesis: vascular growth and survival. APMIS. 2004;112:431–40.PubMed
10.
Zurück zum Zitat Aboagye EO, Saleem A, Cunningham VJ, Osman S, Price PM. Extraction of 5-fluorouracil by tumor and liver: a noninvasive positron emission tomography study of patients with gastrointestinal cancer. Cancer Res. 2001;61:4937–41.PubMed Aboagye EO, Saleem A, Cunningham VJ, Osman S, Price PM. Extraction of 5-fluorouracil by tumor and liver: a noninvasive positron emission tomography study of patients with gastrointestinal cancer. Cancer Res. 2001;61:4937–41.PubMed
11.
Zurück zum Zitat Burke D, Carnochan P, Glover C, Allen-Mersh TG. Correlation between tumour blood flow and fluorouracil distribution in a hypovascular liver metastasis model. Department of Academic Surgery, Leeds General Infirmary, UK. Clin Exp Metastasis. 2000;18:617–22.PubMed Burke D, Carnochan P, Glover C, Allen-Mersh TG. Correlation between tumour blood flow and fluorouracil distribution in a hypovascular liver metastasis model. Department of Academic Surgery, Leeds General Infirmary, UK. Clin Exp Metastasis. 2000;18:617–22.PubMed
12.
Zurück zum Zitat Koukourakis MI, Giatromanolaki A, Sivridis E, Fezoulidis I. Cancer vascularization: implications in radiotherapy? Int J Radiat Oncol Biol Phys. 2000;48:545–53.PubMed Koukourakis MI, Giatromanolaki A, Sivridis E, Fezoulidis I. Cancer vascularization: implications in radiotherapy? Int J Radiat Oncol Biol Phys. 2000;48:545–53.PubMed
13.
Zurück zum Zitat Giatromanolaki A, Koukourakis MI, Sivridis E, O'Byrne K, Gatter KC, Harris AL. 'Invading edge vs inner' (edvin) patterns of vascularization: an interplay between angiogenic and vascular survival factors defines the clinical behavior of non-small cell lung cancer. J Pathol. 2000;192:140–9.PubMed Giatromanolaki A, Koukourakis MI, Sivridis E, O'Byrne K, Gatter KC, Harris AL. 'Invading edge vs inner' (edvin) patterns of vascularization: an interplay between angiogenic and vascular survival factors defines the clinical behavior of non-small cell lung cancer. J Pathol. 2000;192:140–9.PubMed
14.
Zurück zum Zitat Tharmalingham H, Hoskin P. Clinical trials targeting hypoxia. Br J Radiol. 2018;2018:20170966. Tharmalingham H, Hoskin P. Clinical trials targeting hypoxia. Br J Radiol. 2018;2018:20170966.
15.
Zurück zum Zitat Bishop T, Ratcliffe PJ. Signaling hypoxia by hypoxia-inducible factor protein hydroxylases: a historical overview and future perspectives. Hypoxia (Auckl). 2014;2:197–21313. Bishop T, Ratcliffe PJ. Signaling hypoxia by hypoxia-inducible factor protein hydroxylases: a historical overview and future perspectives. Hypoxia (Auckl). 2014;2:197–21313.
16.
Zurück zum Zitat Samanta D, Semenza GL. Metabolic adaptation of cancer and immune cells mediated by hypoxia-inducible factors. Biochim Biophys Acta Rev Cancer. 2018;1870:15–22.PubMed Samanta D, Semenza GL. Metabolic adaptation of cancer and immune cells mediated by hypoxia-inducible factors. Biochim Biophys Acta Rev Cancer. 2018;1870:15–22.PubMed
17.
Zurück zum Zitat Agani F, Jiang BH. Oxygen-independent regulation of HIF-1: novel involvement of PI3K/AKT/mTOR pathway in cancer. Curr Cancer Drug Targets. 2013;13:245–51.PubMed Agani F, Jiang BH. Oxygen-independent regulation of HIF-1: novel involvement of PI3K/AKT/mTOR pathway in cancer. Curr Cancer Drug Targets. 2013;13:245–51.PubMed
18.
Zurück zum Zitat Crabtree HG, Cramer W. The action of radium on cancer cells. Proc R Soc Lond (Biol). 1933;113:238–50. Crabtree HG, Cramer W. The action of radium on cancer cells. Proc R Soc Lond (Biol). 1933;113:238–50.
19.
Zurück zum Zitat Rey S, Schito L, Koritzinsky M, Wouters BG. Molecular targeting of hypoxia in radiotherapy. Adv Drug Deliv Rev. 2017;109:45–62.PubMed Rey S, Schito L, Koritzinsky M, Wouters BG. Molecular targeting of hypoxia in radiotherapy. Adv Drug Deliv Rev. 2017;109:45–62.PubMed
20.
Zurück zum Zitat Aebersold DM, Burri P, Beer KT, Laissue J, Djonov V, Greiner RH, Semenza GL. Expression of hypoxia-inducible factor-1alpha: a novel predictive and prognostic parameter in the radiotherapy of oropharyngeal cancer. Cancer Res. 2001;61:2911–6.PubMed Aebersold DM, Burri P, Beer KT, Laissue J, Djonov V, Greiner RH, Semenza GL. Expression of hypoxia-inducible factor-1alpha: a novel predictive and prognostic parameter in the radiotherapy of oropharyngeal cancer. Cancer Res. 2001;61:2911–6.PubMed
21.
Zurück zum Zitat Koukourakis MI, Bentzen SM, Giatromanolaki A, Wilson GD, Daley FM, Saunders MI, Dische S, Sivridis E, Harris AL. Endogenous markers of two separate hypoxia response pathways (hypoxia inducible factor 2 alpha and carbonic anhydrase 9) are associated with radiotherapy failure in head and neck cancer patients recruited in the CHART randomized trial. J Clin Oncol. 2006;24:727–35.PubMed Koukourakis MI, Bentzen SM, Giatromanolaki A, Wilson GD, Daley FM, Saunders MI, Dische S, Sivridis E, Harris AL. Endogenous markers of two separate hypoxia response pathways (hypoxia inducible factor 2 alpha and carbonic anhydrase 9) are associated with radiotherapy failure in head and neck cancer patients recruited in the CHART randomized trial. J Clin Oncol. 2006;24:727–35.PubMed
22.
Zurück zum Zitat Koukourakis MI, Giatromanolaki A. Warburg effect, lactate dehydrogenase, and radio/chemo-therapy efficacy. Int J Radiat Biol. 2019;95:408–26.PubMed Koukourakis MI, Giatromanolaki A. Warburg effect, lactate dehydrogenase, and radio/chemo-therapy efficacy. Int J Radiat Biol. 2019;95:408–26.PubMed
23.
Zurück zum Zitat Mahon BP, Pinard MA, McKenna R. Targeting carbonic anhydrase IX activity and expression. Molecules. 2015;20:2323–48.PubMedPubMedCentral Mahon BP, Pinard MA, McKenna R. Targeting carbonic anhydrase IX activity and expression. Molecules. 2015;20:2323–48.PubMedPubMedCentral
24.
Zurück zum Zitat Barker HE, Paget JT, Khan AA, Harrington KJ. The tumour microenvironment after radiotherapy: mechanisms of resistance and recurrence. Nat Rev Cancer. 2015;15:409–25.PubMedPubMedCentral Barker HE, Paget JT, Khan AA, Harrington KJ. The tumour microenvironment after radiotherapy: mechanisms of resistance and recurrence. Nat Rev Cancer. 2015;15:409–25.PubMedPubMedCentral
25.
Zurück zum Zitat Taylor S, Spugnini EP, Assaraf YG, Azzarito T, Rauch C, Fais S. Microenvironment acidity as a major determinant of tumor chemoresistance: Proton pump inhibitors (PPIs) as a novel therapeutic approach. Drug Resist Updat. 2015;23:69–78.PubMed Taylor S, Spugnini EP, Assaraf YG, Azzarito T, Rauch C, Fais S. Microenvironment acidity as a major determinant of tumor chemoresistance: Proton pump inhibitors (PPIs) as a novel therapeutic approach. Drug Resist Updat. 2015;23:69–78.PubMed
26.
Zurück zum Zitat Ou D, Garberis I, Adam J, Blanchard P, Nguyen F, Levy A, Casiraghi O, Gorphe P, Breuskin I, Janot F, Temam S, Scoazec JY, Deutsch E, Tao Y. Prognostic value of tissue necrosis, hypoxia-related markers and correlation with HPV status in head and neck cancer patients treated with bio- or chemo-radiotherapy. Radiother Oncol. 2018;126(1):116–24.PubMed Ou D, Garberis I, Adam J, Blanchard P, Nguyen F, Levy A, Casiraghi O, Gorphe P, Breuskin I, Janot F, Temam S, Scoazec JY, Deutsch E, Tao Y. Prognostic value of tissue necrosis, hypoxia-related markers and correlation with HPV status in head and neck cancer patients treated with bio- or chemo-radiotherapy. Radiother Oncol. 2018;126(1):116–24.PubMed
27.
Zurück zum Zitat Kim JH, Kim JY, Yoon MS, Kim YS, Lee JH, Kim HJ, Kim H, Kim YJ, Yoo CW, Nam BH, Kim TH, Kim SK, Kim SH, Kang S, Seo SS, Lim MC, Park SY. Prophylactic irradiation of para-aortic lymph nodes for patients with locally advanced cervical cancers with and without high CA9 expression (KROG 07–01): A randomized, open-label, multicenter, phase 2 trial. Radiother Oncol. 2016;120:383–9.PubMed Kim JH, Kim JY, Yoon MS, Kim YS, Lee JH, Kim HJ, Kim H, Kim YJ, Yoo CW, Nam BH, Kim TH, Kim SK, Kim SH, Kang S, Seo SS, Lim MC, Park SY. Prophylactic irradiation of para-aortic lymph nodes for patients with locally advanced cervical cancers with and without high CA9 expression (KROG 07–01): A randomized, open-label, multicenter, phase 2 trial. Radiother Oncol. 2016;120:383–9.PubMed
29.
Zurück zum Zitat Koukourakis MI, Koukourakis IM, Arelaki S, Kouroupi M, Domoxoudis S, Giatromanolaki A. Angiogenic regeneration defines loco-regional recurrence following pre-operative radio-chemotherapy for rectal cancer: a pilot study. Mol Biol Rep. 2019;46(2):2147–52.PubMed Koukourakis MI, Koukourakis IM, Arelaki S, Kouroupi M, Domoxoudis S, Giatromanolaki A. Angiogenic regeneration defines loco-regional recurrence following pre-operative radio-chemotherapy for rectal cancer: a pilot study. Mol Biol Rep. 2019;46(2):2147–52.PubMed
30.
Zurück zum Zitat Tsolou A, Lamprou I, Fortosi AO, Liousia M, Giatromanolaki A, Koukourakis MI. 'Stemness' and 'senescence' related escape pathways are dose dependent in lung cancer cells surviving post irradiation. Life Sci. 2019;232:116562.PubMed Tsolou A, Lamprou I, Fortosi AO, Liousia M, Giatromanolaki A, Koukourakis MI. 'Stemness' and 'senescence' related escape pathways are dose dependent in lung cancer cells surviving post irradiation. Life Sci. 2019;232:116562.PubMed
31.
Zurück zum Zitat Mohan R, Held KD, Story MD, Grosshans D, Capala J. Proceedings of the national cancer institute workshop on charged particle radiobiology. Int J Radiat Oncol Biol Phys. 2018;100:816–31.PubMed Mohan R, Held KD, Story MD, Grosshans D, Capala J. Proceedings of the national cancer institute workshop on charged particle radiobiology. Int J Radiat Oncol Biol Phys. 2018;100:816–31.PubMed
32.
Zurück zum Zitat Bhattarai D, Xu X, Lee K. Hypoxia-inducible factor-1 (HIF-1) inhibitors from the last decade (2007 to 2016): a "structure-activity relationship" perspective. Med Res Rev. 2018;38:1404–42.PubMed Bhattarai D, Xu X, Lee K. Hypoxia-inducible factor-1 (HIF-1) inhibitors from the last decade (2007 to 2016): a "structure-activity relationship" perspective. Med Res Rev. 2018;38:1404–42.PubMed
33.
Zurück zum Zitat Bandurska-Luque A, Löck S, Haase R, Richter C, Zöphel K, Abolmaali N, Seidlitz A, Appold S, Krause M, Steinbach J, Kotzerke J, Zips D, Baumann M, Troost EGC. FMISO-PET-based lymph node hypoxia adds to the prognostic value of tumor only hypoxia in HNSCC patients. Radiother Oncol. 2019;130:97–103.PubMed Bandurska-Luque A, Löck S, Haase R, Richter C, Zöphel K, Abolmaali N, Seidlitz A, Appold S, Krause M, Steinbach J, Kotzerke J, Zips D, Baumann M, Troost EGC. FMISO-PET-based lymph node hypoxia adds to the prognostic value of tumor only hypoxia in HNSCC patients. Radiother Oncol. 2019;130:97–103.PubMed
34.
Zurück zum Zitat Golden EB, Apetoh L. Radiotherapy and immunogenic cell death. Semin Radiat Oncol. 2015;25(1):11–7.PubMed Golden EB, Apetoh L. Radiotherapy and immunogenic cell death. Semin Radiat Oncol. 2015;25(1):11–7.PubMed
35.
Zurück zum Zitat 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;63:1229–355.PubMed 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;63:1229–355.PubMed
36.
Zurück zum Zitat Mensah SA, Harding IC, Zhang M, Jaeggli MP, Torchilin VP, Niedre MJ, Ebong EE. Metastatic cancer cell attachment to endothelium is promoted by endothelial glycocalyx sialic acid degradation. AIChE J. 2019;65:8. Mensah SA, Harding IC, Zhang M, Jaeggli MP, Torchilin VP, Niedre MJ, Ebong EE. Metastatic cancer cell attachment to endothelium is promoted by endothelial glycocalyx sialic acid degradation. AIChE J. 2019;65:8.
37.
Zurück zum Zitat Rodrigues E, Macauley MS. Hypersialylation in cancer: modulation of inflammation and therapeutic opportunities. Cancers (Basel). 2018;10:E207.PubMed Rodrigues E, Macauley MS. Hypersialylation in cancer: modulation of inflammation and therapeutic opportunities. Cancers (Basel). 2018;10:E207.PubMed
38.
Zurück zum Zitat Multhoff G, Vaupel P. Hypoxia compromises anti-cancer immune responses. Adv Exp Med Biol. 2020;1232:131–43.PubMed Multhoff G, Vaupel P. Hypoxia compromises anti-cancer immune responses. Adv Exp Med Biol. 2020;1232:131–43.PubMed
39.
Zurück zum Zitat Calcinotto A, Filipazzi P, Grioni M, Iero M, De Milito A, Ricupito A, Cova A, Canese R, Jachetti E, Rossetti M, Huber V, Parmiani G, Generoso L, Santinami M, Borghi M, Fais S, Bellone M, Rivoltini L. Modulation of microenvironment acidity reverses anergy in human and murine tumor-infiltrating T lymphocytes. Cancer Res. 2012;72:2746–56.PubMed Calcinotto A, Filipazzi P, Grioni M, Iero M, De Milito A, Ricupito A, Cova A, Canese R, Jachetti E, Rossetti M, Huber V, Parmiani G, Generoso L, Santinami M, Borghi M, Fais S, Bellone M, Rivoltini L. Modulation of microenvironment acidity reverses anergy in human and murine tumor-infiltrating T lymphocytes. Cancer Res. 2012;72:2746–56.PubMed
40.
Zurück zum Zitat Giatromanolaki A, Koukourakis IM, Balaska K, Mitrakas AG, Harris AL, Koukourakis MI. Programmed death-1 receptor (PD-1) and PD-ligand-1 (PD-L1) expression in non-small cell lung cancer and the immune-suppressive effect of anaerobic glycolysis. Med Oncol. 2019;36:76.PubMed Giatromanolaki A, Koukourakis IM, Balaska K, Mitrakas AG, Harris AL, Koukourakis MI. Programmed death-1 receptor (PD-1) and PD-ligand-1 (PD-L1) expression in non-small cell lung cancer and the immune-suppressive effect of anaerobic glycolysis. Med Oncol. 2019;36:76.PubMed
42.
Zurück zum Zitat Allard B, Longhi MS, Robson SC, Stagg J. The ectonucleotidases CD39 and CD73: novel checkpoint inhibitor targets. Immunol Rev. 2017;276:121–44.PubMedPubMedCentral Allard B, Longhi MS, Robson SC, Stagg J. The ectonucleotidases CD39 and CD73: novel checkpoint inhibitor targets. Immunol Rev. 2017;276:121–44.PubMedPubMedCentral
43.
Zurück zum Zitat Arab S, Hadjati J. Adenosine blockage in tumor microenvironment and improvement of cancer immunotherapy. Immune Netw. 2019;19:e23.PubMedPubMedCentral Arab S, Hadjati J. Adenosine blockage in tumor microenvironment and improvement of cancer immunotherapy. Immune Netw. 2019;19:e23.PubMedPubMedCentral
44.
Zurück zum Zitat Mitra D, Horick NK, Brackett DG, Mouw KW, Hornick JL, Ferrone S, Hong TS, Mamon H, Clark JW, Parikh AR, Allen JN, Ryan DP, Ting DT, Deshpande V, Wo JY. High IDO1 expression is associated with poor outcome in patients with anal cancer treated with definitive chemoradiotherapy. Oncologist. 2019;24:e275–e283283.PubMedPubMedCentral Mitra D, Horick NK, Brackett DG, Mouw KW, Hornick JL, Ferrone S, Hong TS, Mamon H, Clark JW, Parikh AR, Allen JN, Ryan DP, Ting DT, Deshpande V, Wo JY. High IDO1 expression is associated with poor outcome in patients with anal cancer treated with definitive chemoradiotherapy. Oncologist. 2019;24:e275–e283283.PubMedPubMedCentral
45.
Zurück zum Zitat Platten M, Nollen EAA, Röhrig UF, Fallarino F, Opitz CA. Tryptophan metabolism as a common therapeutic target in cancer, neurodegeneration and beyond. Nat Rev Drug Discov. 2019;18:379–401.PubMed Platten M, Nollen EAA, Röhrig UF, Fallarino F, Opitz CA. Tryptophan metabolism as a common therapeutic target in cancer, neurodegeneration and beyond. Nat Rev Drug Discov. 2019;18:379–401.PubMed
46.
Zurück zum Zitat Timosenko E, Hadjinicolaou AV, Cerundolo V. Modulation of cancer-specific immune responses by amino acid degrading enzymes. Immunotherapy. 2017;9:83–97.PubMed Timosenko E, Hadjinicolaou AV, Cerundolo V. Modulation of cancer-specific immune responses by amino acid degrading enzymes. Immunotherapy. 2017;9:83–97.PubMed
47.
Zurück zum Zitat Hui R, Özgüroğlu M, Villegas A, Daniel D, Vicente D, Murakami S, Yokoi T, Chiappori A, Lee KH, de Wit M, Cho BC, Gray JE, Rydén A, Viviers L, Poole L, Zhang Y, Dennis PA, Antonia SJ. Patient-reported outcomes with durvalumab after chemoradiotherapy in stage III, unresectable non-small-cell lung cancer (PACIFIC): a randomised, controlled, phase 3 study. Lancet Oncol. 2019;20:1670–80.PubMed Hui R, Özgüroğlu M, Villegas A, Daniel D, Vicente D, Murakami S, Yokoi T, Chiappori A, Lee KH, de Wit M, Cho BC, Gray JE, Rydén A, Viviers L, Poole L, Zhang Y, Dennis PA, Antonia SJ. Patient-reported outcomes with durvalumab after chemoradiotherapy in stage III, unresectable non-small-cell lung cancer (PACIFIC): a randomised, controlled, phase 3 study. Lancet Oncol. 2019;20:1670–80.PubMed
48.
Zurück zum Zitat Koukourakis GV, Baksevanis CN, Zambatis H, Gritzapis A, Maltezos E, Simopoulos C, Koukourakis MI. Amifostine enhances recovery and expansion of peripheral FAS/CD95+ T- and NK-cell subpopulations during radiotherapy of patients with head-neck cancer. Int J Radiat Biol. 2009;85:96–104.PubMed Koukourakis GV, Baksevanis CN, Zambatis H, Gritzapis A, Maltezos E, Simopoulos C, Koukourakis MI. Amifostine enhances recovery and expansion of peripheral FAS/CD95+ T- and NK-cell subpopulations during radiotherapy of patients with head-neck cancer. Int J Radiat Biol. 2009;85:96–104.PubMed
49.
Zurück zum Zitat Koukourakis MI, Ktenidou-Kartali S, Bourikas G, Kartalis G, Tsatalas C. Amifostine protects lymphocytes during radiotherapy and stimulates expansion of the CD95/Fas and CD31 expressing T-cells, in breast cancer patients. Cancer Immunol Immunother. 2003;52:127–31.PubMed Koukourakis MI, Ktenidou-Kartali S, Bourikas G, Kartalis G, Tsatalas C. Amifostine protects lymphocytes during radiotherapy and stimulates expansion of the CD95/Fas and CD31 expressing T-cells, in breast cancer patients. Cancer Immunol Immunother. 2003;52:127–31.PubMed
50.
Zurück zum Zitat Benna M, Guy JB, Bosacki C, Jmour O, Ben Mrad M, Ogorodniitchouk O, Soltani S, Lan M, Daguenet E, Mery B, Sotton S, Magné N, Vallard A. Chemoradiation and granulocyte-colony or granulocyte macrophage-colony stimulating factors (G-CSF or GM-CSF): time to think out of the box? Br J Radiol. 2020;93:20190147.PubMed Benna M, Guy JB, Bosacki C, Jmour O, Ben Mrad M, Ogorodniitchouk O, Soltani S, Lan M, Daguenet E, Mery B, Sotton S, Magné N, Vallard A. Chemoradiation and granulocyte-colony or granulocyte macrophage-colony stimulating factors (G-CSF or GM-CSF): time to think out of the box? Br J Radiol. 2020;93:20190147.PubMed
51.
Zurück zum Zitat Leary R, Gardner RB, Mockbee C, Roychowdhury DF. Boosting abscopal response to radiotherapy with sargramostim: a review of data and ongoing studies. Cureus. 2019;11:e4276.PubMedPubMedCentral Leary R, Gardner RB, Mockbee C, Roychowdhury DF. Boosting abscopal response to radiotherapy with sargramostim: a review of data and ongoing studies. Cureus. 2019;11:e4276.PubMedPubMedCentral
52.
Zurück zum Zitat Deng L, Liang H, Xu M, Yang X, Burnette B, Arina A, Li XD, Mauceri H, Beckett M, Darga T, Huang X, Gajewski TF, Chen ZJ, Fu YX, Weichselbaum RR. STING-dependent cytosolic DNA sensing promotes radiation-induced type I interferon-dependent antitumor immunity in immunogenic tumors. Immunity. 2014;41:843–52.PubMedPubMedCentral Deng L, Liang H, Xu M, Yang X, Burnette B, Arina A, Li XD, Mauceri H, Beckett M, Darga T, Huang X, Gajewski TF, Chen ZJ, Fu YX, Weichselbaum RR. STING-dependent cytosolic DNA sensing promotes radiation-induced type I interferon-dependent antitumor immunity in immunogenic tumors. Immunity. 2014;41:843–52.PubMedPubMedCentral
53.
Zurück zum Zitat Vanpouille-Box C, Alard A, Aryankalayil MJ, Sarfraz Y, Diamond JM, Schneider RJ, Inghirami G, Coleman CN, Formenti SC, Demaria S. DNA exonuclease Trex1 regulates radiotherapy-induced tumour immunogenicity. Nat Commun. 2017;8:15618.PubMedPubMedCentral Vanpouille-Box C, Alard A, Aryankalayil MJ, Sarfraz Y, Diamond JM, Schneider RJ, Inghirami G, Coleman CN, Formenti SC, Demaria S. DNA exonuclease Trex1 regulates radiotherapy-induced tumour immunogenicity. Nat Commun. 2017;8:15618.PubMedPubMedCentral
54.
Zurück zum Zitat Wang X, Schoenhals JE, Li A, Valdecanas DR, Ye H, Zang F, Tang C, Tang M, Liu CG, Liu X, Krishnan S, Allison JP, Sharma P, Hwu P, Komaki R, Overwijk WW, Gomez DR, Chang JY, Hahn SM, Cortez MA, Welsh JW. Suppression of type I IFN signaling in tumors mediates resistance to anti-PD-1 treatment that can be overcome by radiotherapy. Cancer Res. 2017;77:839–50.PubMed Wang X, Schoenhals JE, Li A, Valdecanas DR, Ye H, Zang F, Tang C, Tang M, Liu CG, Liu X, Krishnan S, Allison JP, Sharma P, Hwu P, Komaki R, Overwijk WW, Gomez DR, Chang JY, Hahn SM, Cortez MA, Welsh JW. Suppression of type I IFN signaling in tumors mediates resistance to anti-PD-1 treatment that can be overcome by radiotherapy. Cancer Res. 2017;77:839–50.PubMed
55.
Zurück zum Zitat Wunderlich R, Ernst A, Rödel F, Fietkau R, Ott O, Lauber K, Frey B, Gaipl US. Low and moderate doses of ionizing radiation up to 2 Gy modulate transmigration and chemotaxis of activated macrophages, provoke an anti-inflammatory cytokine milieu, but do not impact upon viability and phagocytic function. Clin Exp Immunol. 2015;179:50–61.PubMed Wunderlich R, Ernst A, Rödel F, Fietkau R, Ott O, Lauber K, Frey B, Gaipl US. Low and moderate doses of ionizing radiation up to 2 Gy modulate transmigration and chemotaxis of activated macrophages, provoke an anti-inflammatory cytokine milieu, but do not impact upon viability and phagocytic function. Clin Exp Immunol. 2015;179:50–61.PubMed
56.
Zurück zum Zitat Janssens GO, Rademakers SE, Terhaard CH, Doornaert PA, Bijl HP, van den Ende P, Chin A, Takes RP, de Bree R, Hoogsteen IJ, Bussink J, Span PN, Kaanders JH. Improved recurrence-free survival with ARCON for anemic patients with laryngeal cancer. Clin Cancer Res. 2014;20:1345–54.PubMed Janssens GO, Rademakers SE, Terhaard CH, Doornaert PA, Bijl HP, van den Ende P, Chin A, Takes RP, de Bree R, Hoogsteen IJ, Bussink J, Span PN, Kaanders JH. Improved recurrence-free survival with ARCON for anemic patients with laryngeal cancer. Clin Cancer Res. 2014;20:1345–54.PubMed
57.
Zurück zum Zitat Restifo NP, Dudley ME, Rosenberg SA. Adoptive immunotherapy for cancer: harnessing the T cell response. Nat Rev Immunol. 2012;12:269–81.PubMedPubMedCentral Restifo NP, Dudley ME, Rosenberg SA. Adoptive immunotherapy for cancer: harnessing the T cell response. Nat Rev Immunol. 2012;12:269–81.PubMedPubMedCentral
58.
Zurück zum Zitat Zhang YX, Zhao YY, Shen J, Sun X, Liu Y, Liu H, Wang Y, Wang J. Nanoenabled modulation of acidic tumor microenvironment reverses anergy of infiltrating T cells and potentiates anti-PD-1 therapy. Nano Lett. 2019;19:2774–833.PubMed Zhang YX, Zhao YY, Shen J, Sun X, Liu Y, Liu H, Wang Y, Wang J. Nanoenabled modulation of acidic tumor microenvironment reverses anergy of infiltrating T cells and potentiates anti-PD-1 therapy. Nano Lett. 2019;19:2774–833.PubMed
59.
Zurück zum Zitat Shaverdian N, Lisberg AE, Bornazyan K, Veruttipong D, Goldman JW, Formenti SC, Garon EB, Lee P. Previous radiotherapy and the clinical activity and toxicity of pembrolizumab in the treatment of non-small-cell lung cancer: a secondary analysis of the KEYNOTE-001 phase 1 trial. Lancet Oncol. 2017;18:895–903.PubMedPubMedCentral Shaverdian N, Lisberg AE, Bornazyan K, Veruttipong D, Goldman JW, Formenti SC, Garon EB, Lee P. Previous radiotherapy and the clinical activity and toxicity of pembrolizumab in the treatment of non-small-cell lung cancer: a secondary analysis of the KEYNOTE-001 phase 1 trial. Lancet Oncol. 2017;18:895–903.PubMedPubMedCentral
60.
Zurück zum Zitat Yoneda K, Kuwata T, Kanayama M, Mori M, Kawanami T, Yatera K, Ohguri T, Hisaoka M, Nakayama T, Tanaka F. Alteration in tumoural PD-L1 expression and stromal CD8-positive tumour-infiltrating lymphocytes after concurrent chemo-radiotherapy for non-small cell lung cancer. Br J Cancer. 2019;121:490–6.PubMedPubMedCentral Yoneda K, Kuwata T, Kanayama M, Mori M, Kawanami T, Yatera K, Ohguri T, Hisaoka M, Nakayama T, Tanaka F. Alteration in tumoural PD-L1 expression and stromal CD8-positive tumour-infiltrating lymphocytes after concurrent chemo-radiotherapy for non-small cell lung cancer. Br J Cancer. 2019;121:490–6.PubMedPubMedCentral
61.
Zurück zum Zitat Vanpouille-Box C, Formenti SC, Demaria S. Toward precision radiotherapy for use with immune checkpoint blockers. Clin Cancer Res. 2018;24:259–65.PubMed Vanpouille-Box C, Formenti SC, Demaria S. Toward precision radiotherapy for use with immune checkpoint blockers. Clin Cancer Res. 2018;24:259–65.PubMed
62.
63.
Zurück zum Zitat Theodoraki MN, Yerneni SS, Hoffmann TK, Gooding WE, Whiteside TL. Clinical significance of PD-L1(+) Exosomes In Plasma Of Head And Neck Cancer Patients. Clin Cancer Res. 2018;24:896–905.PubMed Theodoraki MN, Yerneni SS, Hoffmann TK, Gooding WE, Whiteside TL. Clinical significance of PD-L1(+) Exosomes In Plasma Of Head And Neck Cancer Patients. Clin Cancer Res. 2018;24:896–905.PubMed
64.
Zurück zum Zitat Li D, Cheng S, Zou S, Zhu D, Zhu T, Wang P, Zhu X. Immuno-PET imaging of (89)Zr labeled anti-PD-L1 domain antibody. Mol Pharm. 2018;15:1674–81.PubMed Li D, Cheng S, Zou S, Zhu D, Zhu T, Wang P, Zhu X. Immuno-PET imaging of (89)Zr labeled anti-PD-L1 domain antibody. Mol Pharm. 2018;15:1674–81.PubMed
65.
Zurück zum Zitat Tavaré R, Escuin-Ordinas H, Mok S, McCracken MN, Zettlitz KA, Salazar FB, Witte ON, Ribas A, Wu AM. An effective immuno-PET imaging method to monitor CD8-Dependent Responses To Immunotherapy. Cancer Res. 2016;76:73–82.PubMed Tavaré R, Escuin-Ordinas H, Mok S, McCracken MN, Zettlitz KA, Salazar FB, Witte ON, Ribas A, Wu AM. An effective immuno-PET imaging method to monitor CD8-Dependent Responses To Immunotherapy. Cancer Res. 2016;76:73–82.PubMed
66.
Zurück zum Zitat Hu M, Xie P, Lee NY, Li M, Ho F, Lian M, Zhao S, Yang G, Fu Z, Zheng J, Ma L, Yu J. Hypoxia with 18F-fluoroerythronitroimidazole integrated positron emission tomography and computed tomography (18F-FETNIM PET/CT) in locoregionally advanced head and neck cancer: Hypoxia changes during chemoradiotherapy and impact on clinical outcome. Med (Baltim). 2019;98(40):e17067. Hu M, Xie P, Lee NY, Li M, Ho F, Lian M, Zhao S, Yang G, Fu Z, Zheng J, Ma L, Yu J. Hypoxia with 18F-fluoroerythronitroimidazole integrated positron emission tomography and computed tomography (18F-FETNIM PET/CT) in locoregionally advanced head and neck cancer: Hypoxia changes during chemoradiotherapy and impact on clinical outcome. Med (Baltim). 2019;98(40):e17067.
67.
Zurück zum Zitat Waller J, Onderdonk B, Flood A, Swartz H, Shah J, Shah A, Aydogan B, Halpern H, Hasan Y. The clinical utility of imaging methods used to measure hypoxia in cervical cancer. Br J Radiol. 2020;2020:20190640. Waller J, Onderdonk B, Flood A, Swartz H, Shah J, Shah A, Aydogan B, Halpern H, Hasan Y. The clinical utility of imaging methods used to measure hypoxia in cervical cancer. Br J Radiol. 2020;2020:20190640.
Metadaten
Titel
Tumor microenvironment, immune response and post-radiotherapy tumor clearance
verfasst von
M. I. Koukourakis
A. Giatromanolaki
Publikationsdatum
22.05.2020
Verlag
Springer International Publishing
Erschienen in
Clinical and Translational Oncology / Ausgabe 12/2020
Print ISSN: 1699-048X
Elektronische ISSN: 1699-3055
DOI
https://doi.org/10.1007/s12094-020-02378-8

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