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Published in: BMC Cancer 1/2023

Open Access 01-12-2023 | Glioblastoma | Research

Shooting the messenger: a systematic review investigating extracellular vesicle isolation and characterisation methods and their influence on understanding extracellular vesicles-radiotherapy interactions in glioblastoma

Authors: Stephen David Robinson, Mark Samuels, William Jones, Duncan Gilbert, Giles Critchley, Georgios Giamas

Published in: BMC Cancer | Issue 1/2023

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Abstract

Background

Extracellular vesicles (EVs) hold promise for improving our understanding of radiotherapy response in glioblastoma due to their role in intercellular communication within the tumour microenvironment (TME). However, methodologies to study EVs are evolving with significant variation within the EV research community.

Methods

We conducted a systematic review to critically appraise EV isolation and characterisation methodologies and how this influences our understanding of the findings from studies investigating radiotherapy and EV interactions in glioblastoma. 246 articles published up to 24/07/2023 from PubMed and Web of Science were identified using search parameters related to radiotherapy, EVs, and glioblastoma. Two reviewers evaluated study eligibility and abstracted data.

Results

In 26 articles eligible for inclusion (16 investigating the effects of radiotherapy on EVs, five investigating the effect of EVs on radiation response, and five clinical studies), significant heterogeneity and frequent omission of key characterisation steps was identified, reducing confidence that the results are related to EVs and their cargo as opposed to co-isolated bioactive molecules. However, the results are able to clearly identify interactions between EVs and radiotherapy bi-directionally within different cell types within the glioblastoma TME. These interactions facilitate transferable radioresistance and oncogenic signalling, highlighting that EVs are an important component in the variability of glioblastoma radiotherapy response.

Conclusions

Future multi-directional investigations interrogating the whole TME are required to improve subsequent clinical translation, and all studies should incorporate up to date controls and reporting requirements to increase the validity of their findings. This would be facilitated by increased collaboration between less experienced and more experienced EV research groups.
Literature
1.
go back to reference Yáñez-Mó M, Siljander PR, Andreu Z, Zavec AB, Borràs FE, Buzas EI, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles. 2015;4:27066.PubMedCrossRef Yáñez-Mó M, Siljander PR, Andreu Z, Zavec AB, Borràs FE, Buzas EI, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles. 2015;4:27066.PubMedCrossRef
2.
go back to reference Meehan K, Vella LJ. The contribution of tumour-derived exosomes to the hallmarks of cancer. Crit Rev Clin Lab Sci. 2016;53(2):121–31.PubMedCrossRef Meehan K, Vella LJ. The contribution of tumour-derived exosomes to the hallmarks of cancer. Crit Rev Clin Lab Sci. 2016;53(2):121–31.PubMedCrossRef
3.
go back to reference Zhang DX, Vu LT, Ismail NN, Le MTN, Grimson A. Landscape of extracellular vesicles in the tumour microenvironment: interactions with stromal cells and with non-cell components, and impacts on metabolic reprogramming, horizontal transfer of neoplastic traits, and the emergence of therapeutic resistance. Semin Cancer Biol. 2021;74:24–44.PubMedCrossRef Zhang DX, Vu LT, Ismail NN, Le MTN, Grimson A. Landscape of extracellular vesicles in the tumour microenvironment: interactions with stromal cells and with non-cell components, and impacts on metabolic reprogramming, horizontal transfer of neoplastic traits, and the emergence of therapeutic resistance. Semin Cancer Biol. 2021;74:24–44.PubMedCrossRef
4.
go back to reference Simon T, Pinioti S, Schellenberger P, Rajeeve V, Wendler F, Cutillas PR et al. Shedding of bevacizumab in tumour cells-derived extracellular vesicles as a new therapeutic escape mechanism in glioblastoma. Mol Cancer. 17. England2018. p. 132. Simon T, Pinioti S, Schellenberger P, Rajeeve V, Wendler F, Cutillas PR et al. Shedding of bevacizumab in tumour cells-derived extracellular vesicles as a new therapeutic escape mechanism in glioblastoma. Mol Cancer. 17. England2018. p. 132.
5.
go back to reference Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352(10):987–96.PubMedCrossRef Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352(10):987–96.PubMedCrossRef
6.
go back to reference Mann J, Ramakrishna R, Magge R, Wernicke AG. Advances in Radiotherapy for Glioblastoma. Front Neurol. 2017;8:748.PubMedCrossRef Mann J, Ramakrishna R, Magge R, Wernicke AG. Advances in Radiotherapy for Glioblastoma. Front Neurol. 2017;8:748.PubMedCrossRef
7.
go back to reference Tsien CI, Pugh SL, Dicker AP, Raizer JJ, Matuszak MM, Lallana EC, et al. NRG Oncology/RTOG1205: a randomized phase II trial of concurrent Bevacizumab and Reirradiation Versus Bevacizumab alone as treatment for recurrent glioblastoma. J Clin Oncol. 2023;41(6):1285–95.PubMedCrossRef Tsien CI, Pugh SL, Dicker AP, Raizer JJ, Matuszak MM, Lallana EC, et al. NRG Oncology/RTOG1205: a randomized phase II trial of concurrent Bevacizumab and Reirradiation Versus Bevacizumab alone as treatment for recurrent glioblastoma. J Clin Oncol. 2023;41(6):1285–95.PubMedCrossRef
8.
go back to reference Barker HE, Paget JT, Khan AA, Harrington KJ. The tumour microenvironment after radiotherapy: mechanisms of resistance and recurrence. Nat Rev Cancer. 2015;15(7):409–25.PubMedPubMedCentralCrossRef Barker HE, Paget JT, Khan AA, Harrington KJ. The tumour microenvironment after radiotherapy: mechanisms of resistance and recurrence. Nat Rev Cancer. 2015;15(7):409–25.PubMedPubMedCentralCrossRef
10.
go back to reference Wen PY, Macdonald DR, Reardon DA, Cloughesy TF, Sorensen AG, Galanis E, et al. Updated response assessment criteria for high-grade gliomas: response assessment in neuro-oncology working group. J Clin Oncol. 2010;28(11):1963–72.PubMedCrossRef Wen PY, Macdonald DR, Reardon DA, Cloughesy TF, Sorensen AG, Galanis E, et al. Updated response assessment criteria for high-grade gliomas: response assessment in neuro-oncology working group. J Clin Oncol. 2010;28(11):1963–72.PubMedCrossRef
11.
go back to reference Nieuwland R, Siljander PR, Falcón-Pérez JM, Witwer KW. Reproducibility of extracellular vesicle research. Eur J Cell Biol. 2022;101(3):151226.PubMedCrossRef Nieuwland R, Siljander PR, Falcón-Pérez JM, Witwer KW. Reproducibility of extracellular vesicle research. Eur J Cell Biol. 2022;101(3):151226.PubMedCrossRef
12.
go back to reference Théry C, Witwer KW, Aikawa E, Alcaraz MJ, Anderson JD, Andriantsitohaina R, et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular vesicles and update of the MISEV2014 guidelines. J Extracell Vesicles. 2018;7(1):1535750.PubMedPubMedCentralCrossRef Théry C, Witwer KW, Aikawa E, Alcaraz MJ, Anderson JD, Andriantsitohaina R, et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular vesicles and update of the MISEV2014 guidelines. J Extracell Vesicles. 2018;7(1):1535750.PubMedPubMedCentralCrossRef
13.
go back to reference Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71.PubMedPubMedCentralCrossRef Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71.PubMedPubMedCentralCrossRef
14.
go back to reference Jennrich S, Pelzer M, Tertel T, Koska B, Vullings M, Thakur BK, et al. CD9-and CD81-positive extracellular vesicles provide a marker to monitor glioblastoma cell response to photon-based and proton-based radiotherapy. Front Oncol. 2022;12:13.CrossRef Jennrich S, Pelzer M, Tertel T, Koska B, Vullings M, Thakur BK, et al. CD9-and CD81-positive extracellular vesicles provide a marker to monitor glioblastoma cell response to photon-based and proton-based radiotherapy. Front Oncol. 2022;12:13.CrossRef
15.
go back to reference Ramakrishnan V, Xu BB, Akers J, Nguyen T, Ma J, Dhawan S, et al. Radiation-induced extracellular vesicle (EV) release of miR-603 promotes IGF1-mediated stem cell state in glioblastomas. Ebiomedicine. 2020;55:16.CrossRef Ramakrishnan V, Xu BB, Akers J, Nguyen T, Ma J, Dhawan S, et al. Radiation-induced extracellular vesicle (EV) release of miR-603 promotes IGF1-mediated stem cell state in glioblastomas. Ebiomedicine. 2020;55:16.CrossRef
16.
go back to reference Takov K, Yellon DM, Davidson SM. Confounding factors in vesicle uptake studies using fluorescent lipophilic membrane dyes. J Extracell Vesicles. 2017;6(1):1388731.PubMedPubMedCentralCrossRef Takov K, Yellon DM, Davidson SM. Confounding factors in vesicle uptake studies using fluorescent lipophilic membrane dyes. J Extracell Vesicles. 2017;6(1):1388731.PubMedPubMedCentralCrossRef
17.
go back to reference Whitehead CA, Fang HY, Su HQ, Morokoff AP, Kaye AH, Hanssen E et al. Small extracellular vesicles promote invadopodia activity in glioblastoma cells in a therapy-dependent manner. Cell Oncol. 2023:23. Whitehead CA, Fang HY, Su HQ, Morokoff AP, Kaye AH, Hanssen E et al. Small extracellular vesicles promote invadopodia activity in glioblastoma cells in a therapy-dependent manner. Cell Oncol. 2023:23.
18.
go back to reference Arscott WT, Tandle AT, Zhao SP, Shabason JE, Gordon IK, Schlaff CD, et al. Ionizing Radiation and Glioblastoma Exosomes: implications in Tumor Biology and Cell Migration. Transl Oncol. 2013;6(6):638–U254.PubMedPubMedCentralCrossRef Arscott WT, Tandle AT, Zhao SP, Shabason JE, Gordon IK, Schlaff CD, et al. Ionizing Radiation and Glioblastoma Exosomes: implications in Tumor Biology and Cell Migration. Transl Oncol. 2013;6(6):638–U254.PubMedPubMedCentralCrossRef
19.
go back to reference Pavlyukov MS, Yu H, Bastola S, Minata M, Shender VO, Lee Y, et al. Apoptotic cell-derived extracellular vesicles promote malignancy of Glioblastoma Via Intercellular transfer of splicing factors. Cancer Cell. 2018;34(1):119–.PubMedPubMedCentralCrossRef Pavlyukov MS, Yu H, Bastola S, Minata M, Shender VO, Lee Y, et al. Apoptotic cell-derived extracellular vesicles promote malignancy of Glioblastoma Via Intercellular transfer of splicing factors. Cancer Cell. 2018;34(1):119–.PubMedPubMedCentralCrossRef
20.
go back to reference Pineda B, Garcia FJS, Olascoaga NK, de la Cruz VP, Salazar A, Moreno-Jimenez S, et al. Malignant glioma therapy by vaccination with irradiated C6 cell-derived microvesicles promotes an Antitumoral Immune Response. Mol Ther. 2019;27(9):1612–20.PubMedPubMedCentralCrossRef Pineda B, Garcia FJS, Olascoaga NK, de la Cruz VP, Salazar A, Moreno-Jimenez S, et al. Malignant glioma therapy by vaccination with irradiated C6 cell-derived microvesicles promotes an Antitumoral Immune Response. Mol Ther. 2019;27(9):1612–20.PubMedPubMedCentralCrossRef
21.
go back to reference Zhao M, Xu J, Zhong S, Liu Y, Xiao H, Geng L, et al. Expression profiles and potential functions of circular RNAs in extracellular vesicles isolated from radioresistant glioma cells. Oncol Rep. 2019;41(3):1893–900.PubMed Zhao M, Xu J, Zhong S, Liu Y, Xiao H, Geng L, et al. Expression profiles and potential functions of circular RNAs in extracellular vesicles isolated from radioresistant glioma cells. Oncol Rep. 2019;41(3):1893–900.PubMed
22.
go back to reference Baulch JE, Geidzinski E, Tran KK, Yu LP, Zhou YH, Limoli CL. Irradiation of primary human gliomas triggers dynamic and aggressive survival responses involving microvesicle signaling. Environ Mol Mutagen. 2016;57(5):405–15.PubMedCrossRef Baulch JE, Geidzinski E, Tran KK, Yu LP, Zhou YH, Limoli CL. Irradiation of primary human gliomas triggers dynamic and aggressive survival responses involving microvesicle signaling. Environ Mol Mutagen. 2016;57(5):405–15.PubMedCrossRef
23.
go back to reference Mrowczynski OD, Madhankumar AB, Sundstrom JM, Zhao Y, Kawasawa YI, Slagle-Webb B, et al. Exosomes impact survival to radiation exposure in cell line models of nervous system cancer. Oncotarget. 2018;9(90):36083–101.PubMedPubMedCentralCrossRef Mrowczynski OD, Madhankumar AB, Sundstrom JM, Zhao Y, Kawasawa YI, Slagle-Webb B, et al. Exosomes impact survival to radiation exposure in cell line models of nervous system cancer. Oncotarget. 2018;9(90):36083–101.PubMedPubMedCentralCrossRef
24.
go back to reference Wang XX, Cao QN, Shi YG, Wu XL, Mi Y, Liu K, et al. Identification of low-dose radiation-induced exosomal circ- METRN and miR-4709-3p/GRB14/PDGFR alpha pathway as a key regulatory mechanism in Glioblastoma progression and radioresistance: functional validation and clinical theranostic significance. Int J Biol Sci. 2021;17(4):1061–78.PubMedPubMedCentralCrossRef Wang XX, Cao QN, Shi YG, Wu XL, Mi Y, Liu K, et al. Identification of low-dose radiation-induced exosomal circ- METRN and miR-4709-3p/GRB14/PDGFR alpha pathway as a key regulatory mechanism in Glioblastoma progression and radioresistance: functional validation and clinical theranostic significance. Int J Biol Sci. 2021;17(4):1061–78.PubMedPubMedCentralCrossRef
25.
go back to reference Dhondt B, Pinheiro C, Geeurickx E, Tulkens J, Vergauwen G, Van Der Pol E, et al. Benchmarking blood collection tubes and processing intervals for extracellular vesicle performance metrics. J Extracell Vesicles. 2023;12(5):e12315.PubMedPubMedCentralCrossRef Dhondt B, Pinheiro C, Geeurickx E, Tulkens J, Vergauwen G, Van Der Pol E, et al. Benchmarking blood collection tubes and processing intervals for extracellular vesicle performance metrics. J Extracell Vesicles. 2023;12(5):e12315.PubMedPubMedCentralCrossRef
26.
go back to reference Colangelo NW, Azzam EI. Extracellular vesicles originating from glioblastoma cells increase metalloproteinase release by astrocytes: the role of CD147 (EMMPRIN) and ionizing radiation. Cell Commun Signal. 2020;18(1):14.CrossRef Colangelo NW, Azzam EI. Extracellular vesicles originating from glioblastoma cells increase metalloproteinase release by astrocytes: the role of CD147 (EMMPRIN) and ionizing radiation. Cell Commun Signal. 2020;18(1):14.CrossRef
27.
go back to reference Yang XJ, Ma LL, Ye ZJ, Shi WY, Zhang LY, Wang JD, et al. Radiation-induced bystander effects may contribute to radiation-induced cognitive impairment. Int J Radiat Biol. 2021;97(3):329–40.PubMedCrossRef Yang XJ, Ma LL, Ye ZJ, Shi WY, Zhang LY, Wang JD, et al. Radiation-induced bystander effects may contribute to radiation-induced cognitive impairment. Int J Radiat Biol. 2021;97(3):329–40.PubMedCrossRef
28.
go back to reference Briand J, Garnier D, Nadaradjane A, Clement-Colmou K, Potiron V, Supiot S, et al. Radiotherapy-induced overexpression of exosomal miRNA-378a-3p in cancer cells limits natural killer cells cytotoxicity. Epigenomics. 2020;12(5):397–408.PubMedCrossRef Briand J, Garnier D, Nadaradjane A, Clement-Colmou K, Potiron V, Supiot S, et al. Radiotherapy-induced overexpression of exosomal miRNA-378a-3p in cancer cells limits natural killer cells cytotoxicity. Epigenomics. 2020;12(5):397–408.PubMedCrossRef
29.
go back to reference Tian YH, Liu CS, Li ZY, Ai ML, Wang BY, Du KP, et al. Exosomal B7-H4 from irradiated glioblastoma cells contributes to increase FoxP3 expression of differentiating Th1 cells and promotes tumor growth. Redox Biol. 2022;56:15.CrossRef Tian YH, Liu CS, Li ZY, Ai ML, Wang BY, Du KP, et al. Exosomal B7-H4 from irradiated glioblastoma cells contributes to increase FoxP3 expression of differentiating Th1 cells and promotes tumor growth. Redox Biol. 2022;56:15.CrossRef
30.
go back to reference Zhang CZ, Zhou Y, Gao Y, Zhu Z, Zeng XL, Liang WZ, et al. Radiated glioblastoma cell-derived exosomal circ_0012381 induce M2 polarization of microglia to promote the growth of glioblastoma by CCL2/CCR2 axis. J Transl Med. 2022;20(1):13. Zhang CZ, Zhou Y, Gao Y, Zhu Z, Zeng XL, Liang WZ, et al. Radiated glioblastoma cell-derived exosomal circ_0012381 induce M2 polarization of microglia to promote the growth of glioblastoma by CCL2/CCR2 axis. J Transl Med. 2022;20(1):13.
31.
go back to reference Shin E, Kang H, Lee H, Lee S, Jeon J, Seong K, et al. Exosomal plasminogen activator Inhibitor-1 induces Ionizing Radiation-Adaptive Glioblastoma Cachexia. Cells. 2022;11:19.CrossRef Shin E, Kang H, Lee H, Lee S, Jeon J, Seong K, et al. Exosomal plasminogen activator Inhibitor-1 induces Ionizing Radiation-Adaptive Glioblastoma Cachexia. Cells. 2022;11:19.CrossRef
32.
go back to reference Menck K, Sönmezer C, Worst TS, Schulz M, Dihazi GH, Streit F, et al. Neutral sphingomyelinases control extracellular vesicles budding from the plasma membrane. J Extracell Vesicles. 2017;6(1):1378056.PubMedPubMedCentralCrossRef Menck K, Sönmezer C, Worst TS, Schulz M, Dihazi GH, Streit F, et al. Neutral sphingomyelinases control extracellular vesicles budding from the plasma membrane. J Extracell Vesicles. 2017;6(1):1378056.PubMedPubMedCentralCrossRef
33.
go back to reference Dai XJ, Liao KM, Zhuang ZJ, Chen BH, Zhou ZY, Zhou SH, et al. AHIF promotes glioblastoma progression and radioresistance via exosomes. Int J Oncol. 2019;54(1):261–70.PubMed Dai XJ, Liao KM, Zhuang ZJ, Chen BH, Zhou ZY, Zhou SH, et al. AHIF promotes glioblastoma progression and radioresistance via exosomes. Int J Oncol. 2019;54(1):261–70.PubMed
34.
go back to reference Yue X, Lan FM, Xia TY. Hypoxic glioma cell-secreted exosomal miR-301a activates Wnt/beta-catenin signaling and promotes Radiation Resistance by Targeting TCEAL7. Mol Ther. 2019;27(11):1939–49.PubMedPubMedCentralCrossRef Yue X, Lan FM, Xia TY. Hypoxic glioma cell-secreted exosomal miR-301a activates Wnt/beta-catenin signaling and promotes Radiation Resistance by Targeting TCEAL7. Mol Ther. 2019;27(11):1939–49.PubMedPubMedCentralCrossRef
35.
go back to reference Ma CK, Nguyen HPT, Jones JJ, Stylli SS, Whitehead CA, Paradiso L, et al. Extracellular vesicles secreted by glioma stem cells are involved in Radiation Resistance and Glioma Progression. Int J Mol Sci. 2022;23(5):14.CrossRef Ma CK, Nguyen HPT, Jones JJ, Stylli SS, Whitehead CA, Paradiso L, et al. Extracellular vesicles secreted by glioma stem cells are involved in Radiation Resistance and Glioma Progression. Int J Mol Sci. 2022;23(5):14.CrossRef
36.
go back to reference Panizza E, Regalado BD, Wang F, Nakano I, Vacanti NM, Cerione RA et al. Proteomic analysis reveals microvesicles containing NAMPT as mediators of radioresistance in glioma. Life Sci Alliance. 2023;6(6). Panizza E, Regalado BD, Wang F, Nakano I, Vacanti NM, Cerione RA et al. Proteomic analysis reveals microvesicles containing NAMPT as mediators of radioresistance in glioma. Life Sci Alliance. 2023;6(6).
37.
go back to reference Zhang ZP, Xu JY, Chen ZH, Wang HZ, Xue H, Yang CL, et al. Transfer of MicroRNA via macrophage-derived extracellular vesicles promotes Proneural-to-mesenchymal transition in glioma stem cells. Cancer Immunol Res. 2020;8(7):966–81.PubMedCrossRef Zhang ZP, Xu JY, Chen ZH, Wang HZ, Xue H, Yang CL, et al. Transfer of MicroRNA via macrophage-derived extracellular vesicles promotes Proneural-to-mesenchymal transition in glioma stem cells. Cancer Immunol Res. 2020;8(7):966–81.PubMedCrossRef
38.
go back to reference Reynés G, Vila V, Fleitas T, Reganon E, Font de Mora J, Jordá M, et al. Circulating endothelial cells and procoagulant microparticles in patients with glioblastoma: prognostic value. PLoS ONE. 2013;8(7):e69034.PubMedPubMedCentralCrossRef Reynés G, Vila V, Fleitas T, Reganon E, Font de Mora J, Jordá M, et al. Circulating endothelial cells and procoagulant microparticles in patients with glioblastoma: prognostic value. PLoS ONE. 2013;8(7):e69034.PubMedPubMedCentralCrossRef
39.
go back to reference Koch CJ, Lustig RA, Yang XY, Jenkins WT, Wolf RL, Martinez-Lage M, et al. Microvesicles as a Biomarker for Tumor Progression versus Treatment Effect in Radiation/Temozolomide-Treated glioblastoma patients. Transl Oncol. 2014;7(6):752–8.PubMedPubMedCentralCrossRef Koch CJ, Lustig RA, Yang XY, Jenkins WT, Wolf RL, Martinez-Lage M, et al. Microvesicles as a Biomarker for Tumor Progression versus Treatment Effect in Radiation/Temozolomide-Treated glioblastoma patients. Transl Oncol. 2014;7(6):752–8.PubMedPubMedCentralCrossRef
40.
go back to reference Evans SM, Putt M, Yang XY, Lustig RA, Martinez-Lage M, Williams D, et al. Initial evidence that blood-borne microvesicles are biomarkers for recurrence and survival in newly diagnosed glioblastoma patients. J Neuro-Oncol. 2016;127(2):391–400.CrossRef Evans SM, Putt M, Yang XY, Lustig RA, Martinez-Lage M, Williams D, et al. Initial evidence that blood-borne microvesicles are biomarkers for recurrence and survival in newly diagnosed glioblastoma patients. J Neuro-Oncol. 2016;127(2):391–400.CrossRef
41.
go back to reference Li ZH, Ye L, Wang L, Quan RC, Zhou YY, Li XM. Identification of miRNA signatures in serum exosomes as a potential biomarker after radiotherapy treatment in glioma patients. Ann Diagn Pathol. 2020;44:6.CrossRef Li ZH, Ye L, Wang L, Quan RC, Zhou YY, Li XM. Identification of miRNA signatures in serum exosomes as a potential biomarker after radiotherapy treatment in glioma patients. Ann Diagn Pathol. 2020;44:6.CrossRef
42.
go back to reference Tzaridis T, Weller J, Bachurski D, Shakeri F, Schaub C, Hau P, et al. A novel serum extracellular vesicle protein signature to monitor glioblastoma tumor progression. Int J Cancer. 2023;152(2):308–19.PubMedCrossRef Tzaridis T, Weller J, Bachurski D, Shakeri F, Schaub C, Hau P, et al. A novel serum extracellular vesicle protein signature to monitor glioblastoma tumor progression. Int J Cancer. 2023;152(2):308–19.PubMedCrossRef
43.
go back to reference Ansems M, Span PN. The tumor microenvironment and radiotherapy response; a central role for cancer-associated fibroblasts. Clin Transl Radiat Oncol. 2020;22:90–7.PubMedPubMedCentral Ansems M, Span PN. The tumor microenvironment and radiotherapy response; a central role for cancer-associated fibroblasts. Clin Transl Radiat Oncol. 2020;22:90–7.PubMedPubMedCentral
44.
go back to reference Ali MY, Oliva CR, Noman ASM, Allen BG, Goswami PC, Zakharia Y et al. Radioresistance in Glioblastoma and the development of Radiosensitizers. Cancers (Basel). 2020;12(9). Ali MY, Oliva CR, Noman ASM, Allen BG, Goswami PC, Zakharia Y et al. Radioresistance in Glioblastoma and the development of Radiosensitizers. Cancers (Basel). 2020;12(9).
45.
go back to reference Broekman ML, Maas SLN, Abels ER, Mempel TR, Krichevsky AM, Breakefield XO. Multidimensional communication in the microenvirons of glioblastoma. Nat Rev Neurol. 2018;14(8):482–95.PubMedPubMedCentralCrossRef Broekman ML, Maas SLN, Abels ER, Mempel TR, Krichevsky AM, Breakefield XO. Multidimensional communication in the microenvirons of glioblastoma. Nat Rev Neurol. 2018;14(8):482–95.PubMedPubMedCentralCrossRef
46.
go back to reference Steel GG, McMillan TJ, Peacock JH. The 5Rs of radiobiology. Int J Radiat Biol. 1989;56(6):1045–8.PubMedCrossRef Steel GG, McMillan TJ, Peacock JH. The 5Rs of radiobiology. Int J Radiat Biol. 1989;56(6):1045–8.PubMedCrossRef
48.
go back to reference Lawrie TA, Evans J, Gillespie D, Erridge S, Vale L, Kernohan A et al. Long-term side effects of radiotherapy, with or without chemotherapy, for glioma. Cochrane Database Syst Rev. 2018: Copyright © 2018 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.; 2018. Lawrie TA, Evans J, Gillespie D, Erridge S, Vale L, Kernohan A et al. Long-term side effects of radiotherapy, with or without chemotherapy, for glioma. Cochrane Database Syst Rev. 2018: Copyright © 2018 The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.; 2018.
49.
go back to reference Bentzen SM, Constine LS, Deasy JO, Eisbruch A, Jackson A, Marks LB, et al. Quantitative analyses of normal tissue Effects in the clinic (QUANTEC): an introduction to the scientific issues. Int J Radiat Oncol Biol Phys. 2010;76(3 Suppl):3–9.CrossRef Bentzen SM, Constine LS, Deasy JO, Eisbruch A, Jackson A, Marks LB, et al. Quantitative analyses of normal tissue Effects in the clinic (QUANTEC): an introduction to the scientific issues. Int J Radiat Oncol Biol Phys. 2010;76(3 Suppl):3–9.CrossRef
50.
go back to reference Alhaddad L, Osipov AN, Leonov S. The Molecular and Cellular strategies of Glioblastoma and Non-Small-Cell Lung Cancer cells conferring Radioresistance. Int J Mol Sci. 2022;23(21). Alhaddad L, Osipov AN, Leonov S. The Molecular and Cellular strategies of Glioblastoma and Non-Small-Cell Lung Cancer cells conferring Radioresistance. Int J Mol Sci. 2022;23(21).
52.
go back to reference Grabowski MM, Sankey EW, Ryan KJ, Chongsathidkiet P, Lorrey SJ, Wilkinson DS, et al. Immune suppression in gliomas. J Neurooncol. 2021;151(1):3–12.PubMedCrossRef Grabowski MM, Sankey EW, Ryan KJ, Chongsathidkiet P, Lorrey SJ, Wilkinson DS, et al. Immune suppression in gliomas. J Neurooncol. 2021;151(1):3–12.PubMedCrossRef
53.
54.
go back to reference Wilkins AC, Patin EC, Harrington KJ, Melcher AA. The immunological consequences of radiation-induced DNA damage. J Pathol. 2019;247(5):606–14.PubMedCrossRef Wilkins AC, Patin EC, Harrington KJ, Melcher AA. The immunological consequences of radiation-induced DNA damage. J Pathol. 2019;247(5):606–14.PubMedCrossRef
55.
go back to reference Tuomela K, Mukherjee D, Ambrose AR, Harikrishnan A, Mole H, Hurlstone A et al. Radiotherapy transiently reduces the sensitivity of cancer cells to lymphocyte cytotoxicity. Proc Natl Acad Sci U S A. 2022;119(3). Tuomela K, Mukherjee D, Ambrose AR, Harikrishnan A, Mole H, Hurlstone A et al. Radiotherapy transiently reduces the sensitivity of cancer cells to lymphocyte cytotoxicity. Proc Natl Acad Sci U S A. 2022;119(3).
56.
go back to reference Galluzzi L, Aryankalayil MJ, Coleman CN, Formenti SC. Emerging evidence for adapting radiotherapy to immunotherapy. Nat Rev Clin Oncol. 2023. Galluzzi L, Aryankalayil MJ, Coleman CN, Formenti SC. Emerging evidence for adapting radiotherapy to immunotherapy. Nat Rev Clin Oncol. 2023.
57.
go back to reference Antonia SJ, Villegas A, Daniel D, Vicente D, Murakami S, Hui R, et al. Overall survival with Durvalumab after Chemoradiotherapy in Stage III NSCLC. N Engl J Med. 2018;379(24):2342–50.PubMedCrossRef Antonia SJ, Villegas A, Daniel D, Vicente D, Murakami S, Hui R, et al. Overall survival with Durvalumab after Chemoradiotherapy in Stage III NSCLC. N Engl J Med. 2018;379(24):2342–50.PubMedCrossRef
58.
go back to reference Kelly RJ, Ajani JA, Kuzdzal J, Zander T, Van Cutsem E, Piessen G, et al. Adjuvant nivolumab in Resected Esophageal or Gastroesophageal Junction Cancer. N Engl J Med. 2021;384(13):1191–203.PubMedCrossRef Kelly RJ, Ajani JA, Kuzdzal J, Zander T, Van Cutsem E, Piessen G, et al. Adjuvant nivolumab in Resected Esophageal or Gastroesophageal Junction Cancer. N Engl J Med. 2021;384(13):1191–203.PubMedCrossRef
59.
go back to reference Lehrer EJ, Peterson J, Brown PD, Sheehan JP, Quiñones-Hinojosa A, Zaorsky NG, et al. Treatment of brain metastases with stereotactic radiosurgery and immune checkpoint inhibitors: an international meta-analysis of individual patient data. Radiother Oncol. 2019;130:104–12.PubMedCrossRef Lehrer EJ, Peterson J, Brown PD, Sheehan JP, Quiñones-Hinojosa A, Zaorsky NG, et al. Treatment of brain metastases with stereotactic radiosurgery and immune checkpoint inhibitors: an international meta-analysis of individual patient data. Radiother Oncol. 2019;130:104–12.PubMedCrossRef
60.
go back to reference Lee NY, Ferris RL, Psyrri A, Haddad RI, Tahara M, Bourhis J, et al. Avelumab plus standard-of-care chemoradiotherapy versus chemoradiotherapy alone in patients with locally advanced squamous cell carcinoma of the head and neck: a randomised, double-blind, placebo-controlled, multicentre, phase 3 trial. Lancet Oncol. 2021;22(4):450–62.PubMedCrossRef Lee NY, Ferris RL, Psyrri A, Haddad RI, Tahara M, Bourhis J, et al. Avelumab plus standard-of-care chemoradiotherapy versus chemoradiotherapy alone in patients with locally advanced squamous cell carcinoma of the head and neck: a randomised, double-blind, placebo-controlled, multicentre, phase 3 trial. Lancet Oncol. 2021;22(4):450–62.PubMedCrossRef
61.
go back to reference Lim M, Weller M, Idbaih A, Steinbach J, Finocchiaro G, Raval RR, et al. Phase III trial of chemoradiotherapy with temozolomide plus nivolumab or placebo for newly diagnosed glioblastoma with methylated MGMT promoter. Neuro Oncol. 2022;24(11):1935–49.PubMedPubMedCentralCrossRef Lim M, Weller M, Idbaih A, Steinbach J, Finocchiaro G, Raval RR, et al. Phase III trial of chemoradiotherapy with temozolomide plus nivolumab or placebo for newly diagnosed glioblastoma with methylated MGMT promoter. Neuro Oncol. 2022;24(11):1935–49.PubMedPubMedCentralCrossRef
62.
go back to reference Omuro A, Brandes AA, Carpentier AF, Idbaih A, Reardon DA, Cloughesy T, et al. Radiotherapy combined with nivolumab or temozolomide for newly diagnosed glioblastoma with unmethylated MGMT promoter: an international randomized phase III trial. Neuro Oncol. 2023;25(1):123–34.PubMedCrossRef Omuro A, Brandes AA, Carpentier AF, Idbaih A, Reardon DA, Cloughesy T, et al. Radiotherapy combined with nivolumab or temozolomide for newly diagnosed glioblastoma with unmethylated MGMT promoter: an international randomized phase III trial. Neuro Oncol. 2023;25(1):123–34.PubMedCrossRef
63.
go back to reference Reardon DA, Brandes AA, Omuro A, Mulholland P, Lim M, Wick A, et al. Effect of Nivolumab vs Bevacizumab in patients with recurrent glioblastoma: the CheckMate 143 phase 3 Randomized Clinical Trial. JAMA Oncol. 2020;6(7):1003–10.PubMedCrossRef Reardon DA, Brandes AA, Omuro A, Mulholland P, Lim M, Wick A, et al. Effect of Nivolumab vs Bevacizumab in patients with recurrent glioblastoma: the CheckMate 143 phase 3 Randomized Clinical Trial. JAMA Oncol. 2020;6(7):1003–10.PubMedCrossRef
64.
go back to reference Short SC, Noushmehr H. Unmet need for liquid biomarkers and the brain-liquid Biopsy Consortium. Neurooncol Adv. 2022;4(Suppl 2):ii1–ii3.PubMedPubMedCentral Short SC, Noushmehr H. Unmet need for liquid biomarkers and the brain-liquid Biopsy Consortium. Neurooncol Adv. 2022;4(Suppl 2):ii1–ii3.PubMedPubMedCentral
66.
go back to reference van Leeuwen CM, Oei AL, Crezee J, Bel A, Franken NAP, Stalpers LJA, et al. The alfa and beta of tumours: a review of parameters of the linear-quadratic model, derived from clinical radiotherapy studies. Radiat Oncol. 2018;13(1):96.PubMedPubMedCentralCrossRef van Leeuwen CM, Oei AL, Crezee J, Bel A, Franken NAP, Stalpers LJA, et al. The alfa and beta of tumours: a review of parameters of the linear-quadratic model, derived from clinical radiotherapy studies. Radiat Oncol. 2018;13(1):96.PubMedPubMedCentralCrossRef
Metadata
Title
Shooting the messenger: a systematic review investigating extracellular vesicle isolation and characterisation methods and their influence on understanding extracellular vesicles-radiotherapy interactions in glioblastoma
Authors
Stephen David Robinson
Mark Samuels
William Jones
Duncan Gilbert
Giles Critchley
Georgios Giamas
Publication date
01-12-2023
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2023
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/s12885-023-11437-6

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