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Abstract
Glioblastoma (GBM) remains uniformly lethal, and despite a large accumulation of immune cells in the microenvironment, there is limited antitumor immune response. To overcome these challenges, a comprehensive understanding of GBM systemic immune response during disease progression is required. Here, we integrated multiparameter flow cytometry and mass cytometry TOF (CyTOF) analysis of patient blood to determine changes in the immune system among tumor types and over disease progression. Utilizing flow cytometry analysis in a cohort of 259 patients ranging from benign to malignant primary and metastatic brain tumors, we found that GBM patients had a significant elevation in myeloid-derived suppressor cells (MDSCs) in peripheral blood but not immunosuppressive Tregs. In GBM patient tissue, we found that increased MDSC levels in recurrent GBM portended poor prognosis. CyTOF analysis of peripheral blood from newly diagnosed GBM patients revealed that reduced MDSCs over time were accompanied by a concomitant increase in DCs. GBM patients with extended survival also had reduced MDSCs, similar to the levels of low-grade glioma (LGG) patients. Our findings provide a rationale for developing strategies to target MDSCs, which are elevated in GBM patients and predict poor prognosis.
Authors
Tyler J. Alban, Alvaro G. Alvarado, Mia D. Sorensen, Defne Bayik, Josephine Volovetz, Emily Serbinowski, Erin E. Mulkearns-Hubert, Maksim Sinyuk, James S. Hale, Giovana R. Onzi, Mary McGraw, Pengjing Huang, Matthew M. Grabowski, Connor A. Wathen, Manmeet S. Ahluwalia, Tomas Radivoyevitch, Harley I. Kornblum, Bjarne W. Kristensen, Michael A. Vogelbaum, Justin D. Lathia
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Citations to this article (122)
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AR Antunes, I Scheyltjens, J Duerinck, B Neyns, K Movahedi, JA Ginderachter |
eLife | 2020 |
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Myeloid Cells in Glioblastoma Microenvironment
AD Leo, A Ugolini, F Veglia |
Cells | 2020 |
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Considering the Experimental Use of Temozolomide in Glioblastoma Research
VJ Herbener, T Burster, A Goreth, M Pruss, H von Bandemer, T Baisch, R Fitzel, MD Siegelin, G Karpel-Massler, KM Debatin, MA Westhoff, H Strobel |
Biomedicines | 2020 |
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Revealing and Harnessing Tumour-Associated Microglia/Macrophage Heterogeneity in Glioblastoma
Y Pires-Afonso, SP Niclou, A Michelucci |
International journal of molecular sciences | 2020 |
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Myeloid-Derived Suppressor Cell Subsets Drive Glioblastoma Growth in a Sex-Specific Manner
D Bayik, Y Zhou, C Park, C Hong, D Vail, DJ Silver, A Lauko, G Roversi, DC Watson, A Lo, TJ Alban, M McGraw, M Sorensen, MM Grabowski, B Otvos, MA Vogelbaum, C Horbinski, BW Kristensen, AM Khalil, TH Hwang, MS Ahluwalia, F Cheng, JD Lathia |
Cancer Discovery | 2020 |
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Immune involvement of the contralateral hemisphere in a glioblastoma mouse model
MH Crommentuijn, ST Schetters, SA Dusoswa, LJ Kruijssen, JJ Garcia-Vallejo, Y van Kooyk |
Journal for ImmunoTherapy of Cancer | 2020 |
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Cellular Plasticity and Tumor Microenvironment in Gliomas: The Struggle to Hit a Moving Target
R Gargini, B Segura-Collar, P Sánchez-Gómez |
Cancers | 2020 |
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Inflammation and lymphocyte infiltration are associated with shorter survival in patients with high-grade glioma
E Marinari, M Allard, R Gustave, V Widmer, G Philippin, D Merkler, P Tsantoulis, V Dutoit, PY Dietrich |
OncoImmunology | 2020 |
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Convection-enhanced delivery of temozolomide and whole cell tumor immunizations in GL261 and KR158 experimental mouse gliomas
JE Pérez, J Kopecky, E Visse, A Darabi, P Siesjö |
BMC Cancer | 2020 |
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Effective Treatment of Glioblastoma Multiforme With Oncolytic Virotherapy: A Case-Series
B Gesundheit, E Ben-David, Y Posen, R Ellis, G Wollmann, EM Schneider, K Aigner, L Brauns, T Nesselhut, I Ackva, C Weisslein, A Thaller |
Frontiers in Oncology | 2020 |
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Glioblastoma Myeloid-Derived Suppressor Cell Subsets Express Differential Macrophage Migration Inhibitory Factor Receptor Profiles That Can Be Targeted to Reduce Immune Suppression
TJ Alban, D Bayik, B Otvos, A Rabljenovic, L Leng, L Jia-Shiun, G Roversi, A Lauko, AA Momin, AM Mohammadi, DM Peereboom, MS Ahluwalia, K Matsuda, K Yun, R Bucala, MA Vogelbaum, JD Lathia |
Frontiers in immunology | 2020 |
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Therapeutic Strategies for Overcoming Immunotherapy Resistance Mediated by Immunosuppressive Factors of the Glioblastoma Microenvironment
T Miyazaki, E Ishikawa, N Sugii, M Matsuda |
Cancers | 2020 |
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Inflammatory Mediators in Glioma Microenvironment Play a Dual Role in Gliomagenesis and Mesenchymal Stem Cell Homing: Implication for Cellular Therapy
R Al-kharboosh, K ReFaey, M Lara-Velazquez, SS Grewal, J Imitola, A Quiñones-Hinojosa |
2020 | |
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Progress and applications of mass cytometry in sketching immune landscapes
T Zhang, AR Warden, Y Li, X Ding |
Clinical and Translational Medicine | 2020 |
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Radiomic Immunophenotyping of GSEA-Assessed Immunophenotypes of Glioblastoma and Its Implications for Prognosis: A Feasibility Study
JB Hsu, GA Lee, TH Chang, SW Huang, NQ Le, YC Chen, DP Kuo, YT Li, CY Chen |
Cancers | 2020 |
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Hepatitis B virus reactivation during temozolomide administration for malignant glioma
T Shoji, M Kanamori, J Inoue, R Saito, Y Osada, Y Shimoda, M Chonan, H Uenohara, A Masamune, T Tominaga |
International Journal of Clinical Oncology | 2020 |
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Glioblastoma Organoids: Pre-Clinical Applications and Challenges in the Context of Immunotherapy
E Klein, AC Hau, A Oudin, A Golebiewska, SP Niclou |
Frontiers in Oncology | 2020 |
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Importance of myeloid derived suppressor cells in cancer from a biomarker perspective
Kalathil SG, Thanavala Y |
Cellular Immunology | 2020 |
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Metronomic capecitabine as an immune modulator in glioblastoma patients reduces myeloid-derived suppressor cells
David M Peereboom, Tyler J Alban, Mathew M. Grabowski, Alvaro G Alvarado, Balint Otvos, Defne Bayik, Gustavo Roversi, Mary McGraw, Pengjing Huang, Alireza M. Mohammadi, Harley I. Kornblum, Tomas Radivoyevitch, Manmeet S. Ahluwalia, Michael A Vogelbaum, Justin Lathia |
JCI Insight | 2019 |
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Targeting the Post-Irradiation Tumor Microenvironment in Glioblastoma via Inhibition of CXCL12
F Giordano, B Link, M Glas, U Herrlinger, F Wenz, V Umansky, J Brown, C Herskind |
Cancers | 2019 |
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CCR2 inhibition reduces tumor myeloid cells and unmasks a checkpoint inhibitor effect to slow progression of resistant murine gliomas
JA Flores-Toro, D Luo, A Gopinath, MR Sarkisian, JJ Campbell, IF Charo, R Singh, TJ Schall, M Datta, RK Jain, DA Mitchell, JK Harrison |
Proceedings of the National Academy of Sciences | 2019 |
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Single-Cell High-Throughput Technologies in Cerebrospinal Fluid Research and Diagnostics
TV Lanz, AK Pröbstel, I Mildenberger, M Platten, L Schirmer |
Frontiers in immunology | 2019 |
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Therapeutic targeting of tumor-associated myeloid cells synergizes with radiation therapy for glioblastoma
P Zhang, J Miska, C Lee-Chang, A Rashidi, WK Panek, S An, M Zannikou, A Lopez-Rosas, Y Han, T Xiao, KC Pituch, D Kanojia, IV Balyasnikova, MS Lesniak |
Proceedings of the National Academy of Sciences | 2019 |
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Targeting Myeloid Cells in Combination Treatments for Glioma and Other Tumors
AS Ding, D Routkevitch, C Jackson, M Lim |
Frontiers in immunology | 2019 |
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Accurate expression of PD‐L1/L2 in lung adenocarcinoma cells: A retrospective study by double immunohistochemistry
Y Shinchi, Y Komohara, K Yonemitsu, K Sato, K Ohnishi, Y Saito, Y Fujiwara, T Mori, K Shiraishi, K Ikeda, M Suzuki |
Cancer Science | 2019 |
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Pulmonary surfactant: an immunological perspective
ZC Chroneos, Z Sever-Chroneos, VL Shepherd |
Cellular physiology and biochemistry : international journal of experimental cellular physiology, biochemistry, and pharmacology | 2009 |
