Immuno-phenotyping of IDH-mutant grade 3 astrocytoma and IDH-wildtype glioblastoma reveals specific differences in cells of myeloid origin

References

• Taylor OG, Brzozowski JS, Skelding KA. Glioblastoma Multiforme: an overview of emerging therapeutic targets. Front Oncol. 2019:9. doi:10.3389/fonc.2019.00963.
   PubMed Web of Science ®Google Scholar
• Darmanis S, Sloan SA, Croote D, Mignardi M, Chernikova S, Samghababi P, Zhang Y, Neff N, Kowarsky M, Caneda C, et al. Single-Cell RNA-Seq analysis of infiltrating neoplastic cells at the migrating front of human glioblastoma. Cell Rep. 2017;21(5):1399–11. doi:10.1016/j.celrep.2017.10.030.
   PubMed Web of Science ®Google Scholar
• Jackson CM, Choi J, Lim M. Mechanisms of immunotherapy resistance: lessons from glioblastoma. Nat Immunol. 2019;20(9):1100–1109. doi:10.1038/s41590-019-0433-y.
   PubMed Web of Science ®Google Scholar
• Chen J, Li Y, Yu T-S, McKay RM, Burns DK, Kernie SG, Parada LF. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature. 2012;488(7412):522–526. doi:10.1038/nature11287.
   PubMed Web of Science ®Google Scholar
• Charoentong P, Finotello F, Angelova M, Mayer C, Efremova M, Rieder D, Hackl H, Trajanoski Z. Pan-cancer immunogenomic analyses reveal genotype-immunophenotype relationships and predictors of response to checkpoint blockade. Cell Rep. 2017;18(1):248–262. doi:10.1016/j.celrep.2016.12.019.
   PubMed Web of Science ®Google Scholar
• Schäfer N, Gielen GH, Rauschenbach L, Kebir S, Till A, Reinartz R, Simon M, Niehusmann P, Kleinschnitz C, Herrlinger U, et al. Longitudinal heterogeneity in glioblastoma: moving targets in recurrent versus primary tumors. J Transl Med. 2019;17(1). doi:10.1186/s12967-019-1846-y
   Google Scholar
• Puchalski RB, Shah N, Miller J, Dalley R, Nomura SR, Yoon J-G, Smith KA, Lankerovich M, Bertagnolli D, Bickley K, et al. An anatomic transcriptional atlas of human glioblastoma. Science. 2018;360(6389):660–663. doi:10.1126/science.aaf2666.
   PubMed Web of Science ®Google Scholar
• Zeng J, See AP, Phallen J, Jackson CM, Belcaid Z, Ruzevick J, Durham N, Meyer C, Harris TJ, Albesiano E, et al. Anti-PD-1 blockade and stereotactic radiation produce long-term survival in mice with intracranial gliomas. International Journal of Radiation Oncology*Biology*Physics. 2013;86(2):343–349. doi:10.1016/j.ijrobp.2012.12.025.
   Web of Science ®Google Scholar
• Parney IF, Waldron JS, Parsa AT. Flow cytometry and in vitro analysis of human glioma–associated macrophages. J Neurosurg. 2009;110(3):572–582. doi:10.3171/2008.7.JNS08475.
   PubMed Web of Science ®Google Scholar
• Prosniak M, Harshyne LA, Andrews DW, Kenyon LC, Bedelbaeva K, Apanasovich TV, Heber-Katz E, Curtis MT, Cotzia P, Hooper DC. Glioma grade is associated with the accumulation and activity of cells bearing m2 monocyte markers. Clinical Cancer Research. 2013;19(14):3776–3786. doi:10.1158/1078-0432.CCR-12-1940.
   PubMed Web of Science ®Google Scholar
• Chae M, Peterson TE, Balgeman A, Chen S, Zhang L, Renner DN, Johnson AJ, Parney IF. Increasing glioma-associated monocytes leads to increased intratumoral and systemic myeloid-derived suppressor cells in a murine model. Neuro-Oncology. 2015;17(7):978–991. doi:10.1093/neuonc/nou343.
   PubMed Web of Science ®Google Scholar
• Raychaudhuri B, Rayman P, Ireland J, Ko J, Rini B, Borden EC, Garcia J, Vogelbaum MA, Finke J. Myeloid-derived suppressor cell accumulation and function in patients with newly diagnosed glioblastoma. Neuro-Oncology. 2011;13(6):591–599. doi:10.1093/neuonc/nor042.
   PubMed Web of Science ®Google Scholar
• Raychaudhuri B, Rayman P, Huang P, Grabowski M, Hambardzumyan D, Finke JH, Vogelbaum MA. Myeloid derived suppressor cell infiltration of murine and human gliomas is associated with reduction of tumor infiltrating lymphocytes. J Neurooncol. 2015;122(2):293–301. doi:10.1007/s11060-015-1720-6.
   PubMed Web of Science ®Google Scholar
• Gielen PR, Schulte BM, Kers-Rebel ED, Verrijp K, Petersen-Baltussen HMJM, ter Laan M, Wesseling P, Adema GJ. Increase in both CD14-Positive and CD15-Positive Myeloid-Derived suppressor cell subpopulations in the blood of patients with glioma but predominance of CD15-Positive Myeloid-Derived suppressor cells in glioma tissue. J Neuropathol Exp Neurol. 2015;74(5):390–400. doi:10.1097/NEN.0000000000000183.
   PubMed Web of Science ®Google Scholar
• Gielen PR, Schulte BM, Kers-Rebel ED, Verrijp K, Bossman SAJFH, ter Laan M, Wesseling P, Adema GJ. Elevated levels of polymorphonuclear myeloid-derived suppressor cells in patients with glioblastoma highly express S100A8/9 and arginase and suppress T cell function. Neuro-Oncology. 2016;18(9):1253–1264. doi:10.1093/neuonc/now034.
   PubMed Web of Science ®Google Scholar
• Otvos B, Silver DJ, Mulkearns-Hubert EE, Alvarado AG, Turaga SM, Sorensen MD, Rayman P, Flavahan WA, Hale JS, Stoltz K, et al. Cancer Stem Cell-Secreted Macrophage Migration Inhibitory Factor Stimulates Myeloid Derived Suppressor Cell Function and Facilitates Glioblastoma Immune Evasion: CSC-Secreted MIF and MDSCs in GBM. STEM CELLS. 2016;34(8):2026–2039. doi:10.1002/stem.2393.
   PubMed Web of Science ®Google Scholar
• Alban TJ, Alvarado AG, Sorensen MD, Bayik D, Volovetz J, Serbinowski E, Mulkearns-Hubert EE, Sinyuk M, Hale JS, Onzi GR, et al. Global immune fingerprinting in glioblastoma patient peripheral blood reveals immune-suppression signatures associated with prognosis. JCI Insight. 2018;3(21). doi:10.1172/jci.insight.122264
   PubMed Web of Science ®Google Scholar
• Pereira MB, Barros LRC, Bracco PA, Vigo A, Boroni M, Bonamino MH, Lenz G. Transcriptional characterization of immunological infiltrates and their relation with glioblastoma patients overall survival. OncoImmunology. 2018;7(6):e1431083. doi:10.1080/2162402X.2018.1431083.
   PubMed Web of Science ®Google Scholar
• Gabrusiewicz K, Rodriguez B, Wei J, Hashimoto Y, Healy LM, Maiti SN, Thomas G, Zhou S, Wang Q, Elakkad A, et al. Glioblastoma-infiltrated innate immune cells resemble M0 macrophage phenotype. JCI Insight. 2016;1(2):2. doi:10.1172/jci.insight.85841.
   Web of Science ®Google Scholar
• Quail DF, Bowman RL, Akkari L, Quick ML, Schuhmacher AJ, Huse JT, Holland EC, Sutton JC, Joyce JA. The tumor microenvironment underlies acquired resistance to CSF-1R inhibition in gliomas. Science. 2016;352(6288):aad3018–aad3018. doi:10.1126/science.aad3018.
   PubMed Web of Science ®Google Scholar
• Vidyarthi A, Agnihotri T, Khan N, Singh S, Tewari MK, Radotra BD, Chatterjee D, Agrewala JN. Predominance of M2 macrophages in gliomas leads to the suppression of local and systemic immunity. Cancer Immunology, Immunotherapy. 2019;68(12):1995–2004. doi:10.1007/s00262-019-02423-8.
   PubMed Web of Science ®Google Scholar
• Szulzewsky F, Arora S, de Witte L, Ulas T, Markovic D, Schultze JL, Holland EC, Synowitz M, Wolf SA, Kettenmann H. Human glioblastoma-associated microglia/monocytes express a distinct RNA profile compared to human control and murine samples: human GAMs RNA Sequencing. Glia. 2016;64(8):1416–1436. doi:10.1002/glia.23014.
   PubMed Web of Science ®Google Scholar
• Bowman RL, Klemm F, Akkari L, Pyonteck SM, Sevenich L, Quail DF, Dhara S, Simpson K, Gardner EE, Iacobuzio-Donahue CA, et al. Macrophage ontogeny underlies differences in tumor-specific education in brain malignancies. Cell Rep. 2016;17(9):2445–2459. doi:10.1016/j.celrep.2016.10.052.
   PubMed Web of Science ®Google Scholar
• Friebel E, Kapolou K, Unger S, Núñez NG, Utz S, Rushing EJ, Regli L, Weller M, Greter M, Tugues S, et al. Single-Cell mapping of human brain cancer reveals tumor-specific instruction of tissue-invading leukocytes. Cell. 2020;181(7):1626–1642.e20. doi:10.1016/j.cell.2020.04.055.
   PubMed Web of Science ®Google Scholar
• Klemm F, Maas RR, Bowman RL, Kornete M, Soukup K, Nassiri S, Brouland J-P, Iacobuzio-Donahue CA, Brennan C, Tabar V, et al. Interrogation of the microenvironmental landscape in brain tumors reveals disease-specific alterations of immune cells. Cell. 2020;181(7):1643–1660.e17. doi:10.1016/j.cell.2020.05.007.
   PubMed Web of Science ®Google Scholar
• Liang J, Piao Y, Holmes L, Fuller GN, Henry V, Tiao N, de Groot JF. Neutrophils promote the malignant glioma phenotype through S100A4. Clinical Cancer Research. 2014;20(1):187–198. doi:10.1158/1078-0432.CCR-13-1279.
   PubMed Web of Science ®Google Scholar
• Wang Q, Hu B, Hu X, Kim H, Squatrito M, Scarpace L, deCarvalho AC, Lyu S, Li P, Li Y, et al. Tumor evolution of glioma-intrinsic gene expression subtypes associates with immunological changes in the microenvironment. Cancer Cell. 2017;32(1):42–56.e6. doi:10.1016/j.ccell.2017.06.003.
   PubMed Web of Science ®Google Scholar
• Chai E, Zhang L, Li C. LOX-1+ PMN-MDSC enhances immune suppression which promotes glioblastoma multiforme progression. Cancer Manag Res. 2019;11:7307–7315. doi:10.2147/CMAR.S210545.
   PubMed Web of Science ®Google Scholar
• Jacobs JFM, Idema AJ, Bol KF, Nierkens S, Grauer OM, Wesseling P, Grotenhuis JA, Hoogerbrugge PM, De Vries IJM, Adema GJ. Regulatory T cells and the PD-L1/PD-1 pathway mediate immune suppression in malignant human brain tumors. Neuro-Oncology. 2009;11(4):394–402. doi:10.1215/15228517-2008-104.
   PubMed Web of Science ®Google Scholar
• Shirahata M, Ono T, Stichel D, Schrimpf D, Reuss DE, Sahm F, Koelsche C, Wefers A, Reinhardt A, Huang K, et al. Novel, improved grading system(s) for IDH-mutant astrocytic gliomas. Acta Neuropathol. 2018;136(1):153–166. doi:10.1007/s00401-018-1849-4.
   PubMed Web of Science ®Google Scholar
• Brat DJ, Aldape K, Colman H, Figrarella-Branger D, Fuller GN, Giannini C, Holland EC, Jenkins RB, Kleinschmidt-DeMasters B, Komori T, et al. cIMPACT-NOW update 5: recommended grading criteria and terminologies for IDH-mutant astrocytomas. Acta Neuropathol. 2020;139(3):603–608. doi:10.1007/s00401-020-02127-9.
   PubMed Web of Science ®Google Scholar
• Louis DN, Wesseling P, Aldape K, Brat DJ, Capper D, Cree IA, Eberhart C, Figarella‐Branger D, Fouladi M, Fuller GN, et al. cIMPACT‐NOW update 6: new entity and diagnostic principle recommendations of the cIMPACT‐Utrecht meeting on future CNS tumor classification and grading. Brain Pathol. 2020;30(4):844–856. doi:10.1111/bpa.12832.
   PubMed Web of Science ®Google Scholar
• Dubinski D, Wölfer J, Hasselblatt M, Schneider-Hohendorf T, Bogdahn U, Stummer W, Wiendl H, Grauer OM. CD4+ T effector memory cell dysfunction is associated with the accumulation of granulocytic myeloid-derived suppressor cells in glioblastoma patients. Neuro Oncol. 2016;18(6):807–818. doi:10.1093/neuonc/nov280.
   PubMed Web of Science ®Google Scholar
• Graeber MB, Scheithauer BW, Kreutzberg GW. Microglia in brain tumors. Glia. 2002;40(2):252–259. doi:10.1002/glia.10147.
   PubMed Web of Science ®Google Scholar
• Hambardzumyan D, Gutmann DH, Kettenmann H. The role of microglia and macrophages in glioma maintenance and progression. Nat Neurosci. 2016;19(1):20–27. doi:10.1038/nn.4185.
   PubMed Web of Science ®Google Scholar
• Quail DF, Joyce JA. The microenvironmental landscape of brain tumors. Cancer Cell. 2017;31(3):326–341. doi:10.1016/j.ccell.2017.02.009.
   PubMed Web of Science ®Google Scholar
• Locarno CV, Simonelli M, Carenza C, Capucetti A, Stanzani E, Lorenzi E, Persico P, Della Bella S, Passoni L, Mavilio D, et al. Role of myeloid cells in the immunosuppressive microenvironment in gliomas. Immunobiology. 2020;225(1):151853. doi:10.1016/j.imbio.2019.10.002.
   PubMed Web of Science ®Google Scholar
• gChang Y-Z, Li G-Z, Pang B, Zhang K-N, Zhang X-H, Wang Y-Z, Jiang Z, Chai R-C. Transcriptional CHaracteristics of IDH-Wild type glioma subgroups highlight the biological processes underlying heterogeneity of IDH-Wild Type WHO Grade IV Gliomas. Front Cell Dev Biol. 2020;8:580464. doi:10.3389/fcell.2020.580464.
   PubMed Web of Science ®Google Scholar
• Morantz RA, Wood GW, Foster M, Clark M, Gollahon K. Macrophages in experimental and human brain tumors. J Neurosurg. 1979;50(3):305–311. doi:10.3171/jns.1979.50.3.0305.
   PubMed Web of Science ®Google Scholar
• Rossi ML, Hughes JT, Esiri MM, Coakham HB, Brownell DB. Immunohistological study of mononuclear cell infiltrate in malignant gliomas. Acta Neuropathol. 1987;74(3):269–277. doi:10.1007/BF00688191.
   PubMed Web of Science ®Google Scholar
• Kim AR, Choi KS, Kim M-S, Kim K-M, Kang H, Kim S, Chowdhury T, Yu HJ, Lee CE, Lee JH et al. Absolute quantification of tumor-infiltrating immune cells in high-grade glioma identifies prognostic and radiomics values. Cancer Immunol Immunother. 2021 Jan 8;70(7):1995–2008. doi:10.1007/s00262-020-02836-w.
   PubMed Web of Science ®Google Scholar
• Nicolás-Ávila JÁ, Adrover JM, Hidalgo A. Neutrophils in homeostasis, immunity, and cancer. Immunity. 2017;46(1):15–28. doi:10.1016/j.immuni.2016.12.012.
   PubMed Web of Science ®Google Scholar
• Singhal S, Bhojnagarwala PS, O’Brien S, Moon EK, Garfall AL, Rao AS, Quatromoni JG, Stephen TL, Litzky L, Deshpande C, et al. Origin and role of a subset of tumor-associated neutrophils with antigen-presenting cell features in Early-Stage human lung cancer. Cancer Cell. 2016;30(1):120–135. doi:10.1016/j.ccell.2016.06.001.
   PubMed Web of Science ®Google Scholar
• Gieryng A, Kaminska B. Myeloid-derived suppressor cells in gliomas. wo. 2016;5:345–351. doi:10.5114/wo.2016.64592.
   Google Scholar
• Poon CC, Gordon PMK, Liu K, Yang R, Sarkar S, Mirzaei R, Ahmad ST, Hughes ML, Yong VW, Kelly JJP. Differential microglia and macrophage profiles in human IDH-mutant and -wild type glioblastoma. Oncotarget. 2019;10(33):3129–3143. doi:10.18632/oncotarget.26863.
   PubMedGoogle Scholar