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Current Cancer Drug Targets

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ISSN (Print): 1568-0096
ISSN (Online): 1873-5576

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Mini-Review Article

Neuroinflammation in Glioblastoma: The Role of the Microenvironment in Tumour Progression

Author(s): Ana Helena Larangeira Nóbrega, Rafael Sampaio Pimentel, Ana Paula Prado, Jenifer Garcia, Rudimar Luiz Frozza and Andressa Bernardi*

Volume 24, Issue 6, 2024

Published on: 17 January, 2024

Page: [579 - 594] Pages: 16

DOI: 10.2174/0115680096265849231031101449

Price: $65

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Abstract

Glioblastoma (GBM) stands as the most aggressive and lethal among the main types of primary brain tumors. It exhibits malignant growth, infiltrating the brain tissue, and displaying resistance toward treatment. GBM is a complex disease characterized by high degrees of heterogeneity. During tumour growth, microglia and astrocytes, among other cells, infiltrate the tumour microenvironment and contribute extensively to gliomagenesis. Tumour-associated macrophages (TAMs), either of peripheral origin or representing brain-intrinsic microglia, are the most numerous nonneoplastic populations in the tumour microenvironment in GBM. The complex heterogeneous nature of GBM cells is facilitated by the local inflammatory tumour microenvironment, which mostly induces tumour aggressiveness and drug resistance. The immunosuppressive tumour microenvironment of GBM provides multiple pathways for tumour immune evasion, contributing to tumour progression. Additionally, TAMs and astrocytes can contribute to tumour progression through the release of cytokines and activation of signalling pathways. In this review, we summarize the role of the microenvironment in GBM progression, focusing on neuroinflammation. These recent advancements in research of the microenvironment hold the potential to offer a promising approach to the treatment of GBM in the coming times.

Keywords: Glioblastoma, tumour microenvironment, neuroinflammation, TAMs, microglia, astrocytes.

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Graphical Abstract

[1]
Omuro, A.; DeAngelis, L.M. Glioblastoma and other malignant gliomas: A clinical review. JAMA, 2013, 310(17), 1842-1850.
[http://dx.doi.org/10.1001/jama.2013.280319] [PMID: 24193082]
[2]
DeAngelis, L.M. Brain tumors. N. Engl. J. Med., 2001, 344(2), 114-123.
[http://dx.doi.org/10.1056/NEJM200101113440207] [PMID: 11150363]
[3]
Aldoghachi, A.F.; Aldoghachi, A.F.; Breyne, K.; Ling, K.H.; Cheah, P.S. Recent advances in the therapeutic strategies of glioblastoma multiforme. Neuroscience, 2022, 491, 240-270.
[http://dx.doi.org/10.1016/j.neuroscience.2022.03.030] [PMID: 35395355]
[4]
Roberts, J.W.; Powlovich, L.; Sheybani, N.; LeBlang, S. Focused ultrasound for the treatment of glioblastoma. J. Neurooncol., 2022, 157(2), 237-247.
[http://dx.doi.org/10.1007/s11060-022-03974-0] [PMID: 35267132]
[5]
Duzan, A.; Reinken, D.; McGomery, T.L.; Ferencz, N.M.; Plummer, J.M.; Basti, M.M. Endocannabinoids are potential inhibitors of glioblastoma multiforme proliferation. J. Integr. Med., 2023, 21(2), 120-129.
[http://dx.doi.org/10.1016/j.joim.2023.01.005] [PMID: 36805391]
[6]
Ostrom, Q.T.; Gittleman, H.; Truitt, G.; Boscia, A.; Kruchko, C.; Barnholtz-Sloan, J.S. CBTRUS statistical report: Primary brain and other central nervous system tumors diagnosed in the united states in 2011–2015. Neuro-oncol., 2018, 20(S4), iv1-iv86.
[http://dx.doi.org/10.1093/neuonc/noy131] [PMID: 30445539]
[7]
Furnari, F.B.; Fenton, T.; Bachoo, R.M.; Mukasa, A.; Stommel, J.M.; Stegh, A.; Hahn, W.C.; Ligon, K.L.; Louis, D.N.; Brennan, C.; Chin, L.; DePinho, R.A.; Cavenee, W.K. Malignant astrocytic glioma: Genetics, biology, and paths to treatment. Genes Dev., 2007, 21(21), 2683-2710.
[http://dx.doi.org/10.1101/gad.1596707] [PMID: 17974913]
[8]
Delgado-López, P.D.; Corrales-García, E.M. Survival in glioblastoma: A review on the impact of treatment modalities. Clin. Transl. Oncol., 2016, 18(11), 1062-1071.
[http://dx.doi.org/10.1007/s12094-016-1497-x] [PMID: 26960561]
[9]
DeCordova, S.; Shastri, A.; Tsolaki, A.G.; Yasmin, H.; Klein, L.; Singh, S.K.; Kishore, U. Molecular heterogeneity and immunosuppressive microenvironment in glioblastoma. Front. Immunol., 2020, 11, 1402.
[http://dx.doi.org/10.3389/fimmu.2020.01402] [PMID: 32765498]
[10]
Yeo, E.C.F.; Brown, M.P.; Gargett, T.; Ebert, L.M. The role of cytokines and chemokines in shaping the immune microenvironment of glioblastoma: Implications for immunotherapy. Cells, 2021, 10(3), 607.
[http://dx.doi.org/10.3390/cells10030607] [PMID: 33803414]
[11]
Alghamri, M.S.; McClellan, B.L.; Hartlage, C.S.; Haase, S.; Faisal, S.M.; Thalla, R.; Dabaja, A.; Banerjee, K.; Carney, S.V.; Mujeeb, A.A.; Olin, M.R.; Moon, J.J.; Schwendeman, A.; Lowenstein, P.R.; Castro, M.G. Targeting neuroinflammation in brain cancer: Uncovering mechanisms, pharmacological targets, and neuropharmaceutical developments. Front. Pharmacol., 2021, 12, 680021.
[http://dx.doi.org/10.3389/fphar.2021.680021] [PMID: 34084145]
[12]
Catalano, M. Editorial: Brain tumors and neuroinflammation. Front. Cell. Neurosci., 2022, 16, 941263.
[http://dx.doi.org/10.3389/fncel.2022.941263] [PMID: 35722623]
[13]
Río-Hortega, P.; Jiménez de Asúa, F. Sobre la fagocitosis en los tumores y en otros procesos patológicos. Arch Card Y Hemat, 1921, II(5), 161-220.
[14]
Penfield, W. Microglia and the process of phagocytosis in gliomas. Am. J. Pathol., 1925, 1(1), 77-90, 15.
[PMID: 19969634]
[15]
Charles, N.A.; Holland, E.C.; Gilbertson, R.; Glass, R.; Kettenmann, H. The brain tumor microenvironment. Glia, 2011, 59(8), 1169-1180.
[http://dx.doi.org/10.1002/glia.21136] [PMID: 21446047]
[16]
Quail, D.F.; Joyce, J.A. The microenvironmental landscape of brain tumors. Cancer Cell, 2017, 31(3), 326-341.
[http://dx.doi.org/10.1016/j.ccell.2017.02.009] [PMID: 28292436]
[17]
Zhou, W.; Chen, C.; Shi, Y.; Wu, Q.; Gimple, R.C.; Fang, X.; Huang, Z.; Zhai, K.; Ke, S.Q.; Ping, Y.F.; Feng, H.; Rich, J.N.; Yu, J.S.; Bao, S.; Bian, X.W. Targeting glioma stem cell-derived pericytes disrupts the blood-tumor barrier and improves chemotherapeutic efficacy. Cell Stem Cell, 2017, 21(5), 591-603.e4.
[http://dx.doi.org/10.1016/j.stem.2017.10.002] [PMID: 29100012]
[18]
Guan, X.; Hasan, M.N.; Maniar, S.; Jia, W.; Sun, D. Reactive astrocytes in glioblastoma multiforme. Mol. Neurobiol., 2018, 55(8), 6927-6938.
[http://dx.doi.org/10.1007/s12035-018-0880-8] [PMID: 29363044]
[19]
Ma, Q.; Long, W.; Xing, C.; Chu, J.; Luo, M.; Wang, H.Y.; Liu, Q.; Wang, R.F. Cancer stem cells and immunosuppressive microenvironment in glioma. Front. Immunol., 2018, 9, 2924.
[http://dx.doi.org/10.3389/fimmu.2018.02924] [PMID: 30619286]
[20]
Zhang, H.; Zhou, Y.; Cui, B.; Liu, Z.; Shen, H. Novel insights into astrocyte-mediated signaling of proliferation, invasion and tumor immune microenvironment in glioblastoma. Biomed. Pharmacother., 2020, 126, 110086.
[http://dx.doi.org/10.1016/j.biopha.2020.110086] [PMID: 32172060]
[21]
Sokratous, G.; Polyzoidis, S.; Ashkan, K. Immune infiltration of tumor microenvironment following immunotherapy for glioblastoma multiforme. Hum. Vaccin. Immunother., 2017, 13(11), 2575-2582.
[http://dx.doi.org/10.1080/21645515.2017.1303582] [PMID: 28362548]
[22]
Gieryng, A.; Pszczolkowska, D.; Walentynowicz, K.A.; Rajan, W.D.; Kaminska, B. Immune microenvironment of gliomas. Lab. Invest., 2017, 97(5), 498-518.
[http://dx.doi.org/10.1038/labinvest.2017.19] [PMID: 28287634]
[23]
Pachocki, C.J.; Hol, E.M. Current perspectives on diffuse midline glioma and a different role for the immune microenvironment compared to glioblastoma. J. Neuroinflammation, 2022, 19(1), 276.
[http://dx.doi.org/10.1186/s12974-022-02630-8] [PMID: 36403059]
[24]
Tomaszewski, W.; Sanchez-Perez, L.; Gajewski, T.F.; Sampson, J.H. Brain tumor microenvironment and host state: Implications for immunotherapy. Clin. Cancer Res., 2019, 25(14), 4202-4210.
[http://dx.doi.org/10.1158/1078-0432.CCR-18-1627] [PMID: 30804019]
[25]
Codrici, E.; Popescu, I.D.; Tanase, C.; Enciu, A.M. Friends with benefits: Chemokines, glioblastoma-associated microglia/macrophages, and tumor microenvironment. Int. J. Mol. Sci., 2022, 23(5), 2509.
[http://dx.doi.org/10.3390/ijms23052509] [PMID: 35269652]
[26]
Hambardzumyan, D.; Gutmann, D.H.; Kettenmann, H. The role of microglia and macrophages in glioma maintenance and progression. Nat. Neurosci., 2016, 19(1), 20-27.
[http://dx.doi.org/10.1038/nn.4185] [PMID: 26713745]
[27]
Brown, N.F.; Carter, T.J.; Ottaviani, D.; Mulholland, P. Harnessing the immune system in glioblastoma. Br. J. Cancer, 2018, 119(10), 1171-1181.
[http://dx.doi.org/10.1038/s41416-018-0258-8] [PMID: 30393372]
[28]
Kwon, H.S.; Koh, S.H. Neuroinflammation in neurodegenerative disorders: The roles of microglia and astrocytes. Transl. Neurodegener., 2020, 9(1), 42.
[http://dx.doi.org/10.1186/s40035-020-00221-2] [PMID: 33239064]
[29]
Grégoire, H.; Roncali, L.; Rousseau, A.; Chérel, M.; Delneste, Y.; Jeannin, P.; Hindré, F.; Garcion, E. Targeting tumor associated macrophages to overcome conventional treatment resistance in glioblastoma. Front. Pharmacol., 2020, 11, 368.
[http://dx.doi.org/10.3389/fphar.2020.00368] [PMID: 32322199]
[30]
Buonfiglioli, A.; Hambardzumyan, D. Macrophages and microglia: the cerberus of glioblastoma. Acta Neuropathol. Commun., 2021, 9(1), 54.
[http://dx.doi.org/10.1186/s40478-021-01156-z] [PMID: 33766119]
[31]
Mantovani, A.; Biswas, S.K.; Galdiero, M.R.; Sica, A.; Locati, M. Macrophage plasticity and polarization in tissue repair and remodelling. J. Pathol., 2013, 229(2), 176-185.
[http://dx.doi.org/10.1002/path.4133] [PMID: 23096265]
[32]
Virtuoso, A.; Giovannoni, R.; De Luca, C.; Gargano, F.; Cerasuolo, M.; Maggio, N.; Lavitrano, M.; Papa, M. The glioblastoma microenvironment: Morphology, metabolism, and molecular signature of glial dynamics to discover metabolic rewiring sequence. Int. J. Mol. Sci., 2021, 22(7), 3301.
[http://dx.doi.org/10.3390/ijms22073301] [PMID: 33804873]
[33]
Matias, D.; Balça-Silva, J.; da Graça, G.C.; Wanjiru, C.M.; Macharia, L.W.; Nascimento, C.P.; Roque, N.R.; Coelho-Aguiar, J.M.; Pereira, C.M.; Dos Santos, M.F.; Pessoa, L.S.; Lima, F.R.S.; Schanaider, A.; Ferrer, V.P.; Moura-Neto, V. Microglia/astrocytes–glioblastoma crosstalk: Crucial molecular mechanisms and microenvironmental factors. Front. Cell. Neurosci., 2018, 12, 235.
[http://dx.doi.org/10.3389/fncel.2018.00235] [PMID: 30123112]
[34]
Roesch, S.; Rapp, C.; Dettling, S.; Herold-Mende, C. When immune cells turn bad—tumor-associated microglia/macrophages in glioma. Int. J. Mol. Sci., 2018, 19(2), 436.
[http://dx.doi.org/10.3390/ijms19020436] [PMID: 29389898]
[35]
Perelroizen, R.; Philosof, B.; Budick-Harmelin, N.; Chernobylsky, T.; Ron, A.; Katzir, R.; Shimon, D.; Tessler, A.; Adir, O.; Gaoni-Yogev, A.; Meyer, T.; Krivitsky, A.; Shidlovsky, N.; Madi, A.; Ruppin, E.; Mayo, L. Astrocyte immunometabolic regulation of the tumour microenvironment drives glioblastoma pathogenicity. Brain, 2022, 145(9), 3288-3307.
[http://dx.doi.org/10.1093/brain/awac222] [PMID: 35899587]
[36]
Wu, A.; Wei, J.; Kong, L.Y.; Wang, Y.; Priebe, W.; Qiao, W.; Sawaya, R.; Heimberger, A.B. Glioma cancer stem cells induce immunosuppressive macrophages/microglia. Neuro-oncol., 2010, 12(11), 1113-1125.
[http://dx.doi.org/10.1093/neuonc/noq082] [PMID: 20667896]
[37]
Durafourt, B.A.; Moore, C.S.; Zammit, D.A.; Johnson, T.A.; Zaguia, F.; Guiot, M.C.; Bar-Or, A.; Antel, J.P. Comparison of polarization properties of human adult microglia and blood-derived macrophages. Glia, 2012, 60(5), 717-727.
[http://dx.doi.org/10.1002/glia.22298] [PMID: 22290798]
[38]
Iriki, T.; Ohnishi, K.; Fujiwara, Y.; Horlad, H.; Saito, Y.; Pan, C.; Ikeda, K.; Mori, T.; Suzuki, M.; Ichiyasu, H.; Kohrogi, H.; Takeya, M.; Komohara, Y. The cell-cell interaction between tumor-associated macrophages and small cell lung cancer cells is involved in tumor progression via STAT3 activation. Lung Cancer, 2017, 106, 22-32.
[http://dx.doi.org/10.1016/j.lungcan.2017.01.003] [PMID: 28285690]
[39]
Mostofa, A.G.M.; Punganuru, S.R.; Madala, H.R.; Al-Obaide, M.; Srivenugopal, K.S. The process and regulatory components of inflammation in brain oncogenesis. Biomolecules, 2017, 7(4), 34.
[http://dx.doi.org/10.3390/biom7020034] [PMID: 28346397]
[40]
Kai, K.; Komohara, Y.; Esumi, S.; Fujiwara, Y.; Yamamoto, T.; Uekawa, K.; Ohta, K.; Takezaki, T.; Kuroda, J.; Shinojima, N.; Hamasaki, T.; Mukasa, A. Macrophage/microglia-derived IL-1β induces glioblastoma growth via the STAT3/NF-κB pathway. Hum. Cell, 2022, 35(1), 226-237.
[http://dx.doi.org/10.1007/s13577-021-00619-8] [PMID: 34591282]
[41]
Tarassishin, L.; Lim, J.; Weatherly, D.B.; Angeletti, R.H.; Lee, S.C. Interleukin-1-induced changes in the glioblastoma secretome suggest its role in tumor progression. J. Proteomics, 2014, 99, 152-168.
[http://dx.doi.org/10.1016/j.jprot.2014.01.024] [PMID: 24503185]
[42]
Yeung, Y.T.; McDonald, K.L.; Grewal, T.; Munoz, L. Interleukins in glioblastoma pathophysiology: Implications for therapy. Br. J. Pharmacol., 2013, 168(3), 591-606.
[http://dx.doi.org/10.1111/bph.12008] [PMID: 23062197]
[43]
Subhramanyam, C.S.; Wang, C.; Hu, Q.; Dheen, S.T. Microglia-mediated neuroinflammation in neurodegenerative diseases. Semin. Cell Dev. Biol., 2019, 94, 112-120.
[http://dx.doi.org/10.1016/j.semcdb.2019.05.004] [PMID: 31077796]
[44]
Widodo, S.S.; Dinevska, M.; Furst, L.M.; Stylli, S.S.; Mantamadiotis, T. IL-10 in glioma. Br. J. Cancer, 2021, 125(11), 1466-1476.
[http://dx.doi.org/10.1038/s41416-021-01515-6] [PMID: 34349251]
[45]
Allavena, P.; Sica, A.; Garlanda, C.; Mantovani, A. The Yin-Yang of tumor-associated macrophages in neoplastic progression and immune surveillance. Immunol. Rev., 2008, 222(1), 155-161.
[http://dx.doi.org/10.1111/j.1600-065X.2008.00607.x] [PMID: 18364000]
[46]
Bellora, F.; Castriconi, R.; Dondero, A.; Reggiardo, G.; Moretta, L.; Mantovani, A.; Moretta, A.; Bottino, C. The interaction of human natural killer cells with either unpolarized or polarized macrophages results in different functional outcomes. Proc. Natl. Acad. Sci., 2010, 107(50), 21659-21664.
[http://dx.doi.org/10.1073/pnas.1007654108] [PMID: 21118979]
[47]
Galdiero, M.R.; Garlanda, C.; Jaillon, S.; Marone, G.; Mantovani, A. Tumor associated macrophages and neutrophils in tumor progression. J. Cell. Physiol., 2013, 228(7), 1404-1412.
[http://dx.doi.org/10.1002/jcp.24260] [PMID: 23065796]
[48]
Ho, I.A.W.; Shim, W.S.N. Contribution of the microenvironmental niche to glioblastoma heterogeneity. BioMed Res. Int., 2017, 2017, 1-13.
[http://dx.doi.org/10.1155/2017/9634172] [PMID: 28630875]
[49]
Wang, J.; Leavenworth, J.W.; Hjelmeland, A.B.; Smith, R.; Patel, N.; Borg, B.; Si, Y.; King, P.H. Deletion of the RNA regulator HuR in tumor-associated microglia and macrophages stimulates anti-tumor immunity and attenuates glioma growth. Glia, 2019, 67(12), 2424-2439.
[http://dx.doi.org/10.1002/glia.23696] [PMID: 31400163]
[50]
Bejarano, L.; Jordāo, M.J.C.; Joyce, J.A. Therapeutic targeting of the tumor microenvironment. Cancer Discov., 2021, 11(4), 933-959.
[http://dx.doi.org/10.1158/2159-8290.CD-20-1808] [PMID: 33811125]
[51]
Cui, X.; Morales, R.T.T.; Qian, W.; Wang, H.; Gagner, J.P.; Dolgalev, I.; Placantonakis, D.; Zagzag, D.; Cimmino, L.; Snuderl, M.; Lam, R.H.W.; Chen, W. Hacking macrophage-associated immunosuppression for regulating glioblastoma angiogenesis. Biomaterials, 2018, 161, 164-178.
[http://dx.doi.org/10.1016/j.biomaterials.2018.01.053] [PMID: 29421553]
[52]
Lepore, F.; D’Alessandro, G.; Antonangeli, F.; Santoro, A.; Esposito, V.; Limatola, C.; Trettel, F. CXCL16/CXCR6 axis drives microglia/macrophages phenotype in physiological conditions and plays a crucial role in glioma. Front. Immunol., 2018, 9, 2750.
[http://dx.doi.org/10.3389/fimmu.2018.02750] [PMID: 30542347]
[53]
Ni, B.; Huang, G.; Yang, R.; Wang, Z.; Song, H.; Li, K.; Zhang, Y.; Wu, K.; Shi, G.; Wang, X.; Shen, J.; Liu, Y. The short isoform of MS4A7 is a novel player in glioblastoma microenvironment, M2 macrophage polarization, and tumor progression. J. Neuroinflammation, 2023, 20(1), 80.
[http://dx.doi.org/10.1186/s12974-023-02766-1] [PMID: 36944954]
[54]
Zha, C.; Meng, X.; Li, L.; Mi, S.; Qian, D.; Li, Z.; Wu, P.; Hu, S.; Zhao, S.; Cai, J.; Liu, Y. Neutrophil extracellular traps mediate the crosstalk between glioma progression and the tumor microenvironment via the HMGB1/RAGE/IL-8 axis. Cancer Biol. Med., 2020, 17(1), 154-168.
[http://dx.doi.org/10.20892/j.issn.2095-3941.2019.0353] [PMID: 32296583]
[55]
Ma, J.; Chen, C.C.; Li, M. Macrophages/microglia in the glioblastoma tumor microenvironment. Int. J. Mol. Sci., 2021, 22(11), 5775.
[http://dx.doi.org/10.3390/ijms22115775] [PMID: 34071306]
[56]
Zhang, J.; Sarkar, S.; Cua, R.; Zhou, Y.; Hader, W.; Yong, V.W. A dialog between glioma and microglia that promotes tumor invasiveness through the CCL2/CCR2/interleukin-6 axis. Carcinogenesis, 2012, 33(2), 312-319.
[http://dx.doi.org/10.1093/carcin/bgr289] [PMID: 22159219]
[57]
Vakilian, A.; Khorramdelazad, H.; Heidari, P.; Sheikh Rezaei, Z.; Hassanshahi, G. CCL2/CCR2 signaling pathway in glioblastoma multiforme. Neurochem. Int., 2017, 103, 1-7.
[http://dx.doi.org/10.1016/j.neuint.2016.12.013] [PMID: 28025034]
[58]
Henrik Heiland, D.; Ravi, V.M.; Behringer, S.P.; Frenking, J.H.; Wurm, J.; Joseph, K.; Garrelfs, N.W.C.; Strähle, J.; Heynckes, S.; Grauvogel, J.; Franco, P.; Mader, I.; Schneider, M.; Potthoff, A.L.; Delev, D.; Hofmann, U.G.; Fung, C.; Beck, J.; Sankowski, R.; Prinz, M.; Schnell, O. Tumor-associated reactive astrocytes aid the evolution of immunosuppressive environment in glioblastoma. Nat. Commun., 2019, 10(1), 2541.
[http://dx.doi.org/10.1038/s41467-019-10493-6] [PMID: 31186414]
[59]
Gagliano, N.; Costa, F.; Cossetti, C.; Pettinari, L.; Bassi, R.; Chiriva-Internati, M.; Cobos, E.; Gioia, M.; Pluchino, S. Glioma-astrocyte interaction modifies the astrocyte phenotype in a co-culture experimental model. Oncol. Rep., 2009, 22(6), 1349-1356.
[http://dx.doi.org/10.3892/or_00000574] [PMID: 19885586]
[60]
Sin, W.C.; Aftab, Q.; Bechberger, J.F.; Leung, J.H.; Chen, H.; Naus, C.C. Astrocytes promote glioma invasion via the gap junction protein connexin43. Oncogene, 2016, 35(12), 1504-1516.
[http://dx.doi.org/10.1038/onc.2015.210] [PMID: 26165844]
[61]
Di Virgilio, F. Purines, purinergic receptors, and cancer. Cancer Res., 2012, 72(21), 5441-5447.
[http://dx.doi.org/10.1158/0008-5472.CAN-12-1600] [PMID: 23090120]
[62]
Kang, J.; Kang, N.; Lovatt, D.; Torres, A.; Zhao, Z.; Lin, J.; Nedergaard, M. Connexin 43 hemichannels are permeable to ATP. J. Neurosci., 2008, 28(18), 4702-4711.
[http://dx.doi.org/10.1523/JNEUROSCI.5048-07.2008] [PMID: 18448647]
[63]
Sofroniew, M.V. Multiple roles for astrocytes as effectors of cytokines and inflammatory mediators. Neuroscientist, 2014, 20(2), 160-172.
[http://dx.doi.org/10.1177/1073858413504466] [PMID: 24106265]
[64]
Zhu, W.; Carney, K.E.; Pigott, V.M.; Falgoust, L.M.; Clark, P.A.; Kuo, J.S.; Sun, D. Glioma-mediated microglial activation promotes glioma proliferation and migration: Roles of Na + /H + exchanger isoform 1. Carcinogenesis, 2016, 37(9), 839-851.
[http://dx.doi.org/10.1093/carcin/bgw068] [PMID: 27287871]
[65]
Graeber, M.B.; Scheithauer, B.W.; Kreutzberg, G.W. Microglia in brain tumors. Glia, 2002, 40(2), 252-259.
[http://dx.doi.org/10.1002/glia.10147] [PMID: 12379912]
[66]
Li-Rong, L.; Jia-Chen, L.; Jin-Shuang, B.; Qin-Qin, B.; Gai-Qing, W. Interaction of microglia and astrocytes in the neurovascular unit. Front. Immunol., 2020, 11, 1024.
[67]
Liddelow, S.A.; Guttenplan, K.A.; Clarke, L.E.; Bennett, F.C.; Bohlen, C.J.; Schirmer, L.; Bennett, M.L.; Münch, A.E.; Chung, W.S.; Peterson, T.C.; Wilton, D.K.; Frouin, A.; Napier, B.A.; Panicker, N.; Kumar, M.; Buckwalter, M.S.; Rowitch, D.H.; Dawson, V.L.; Dawson, T.M.; Stevens, B.; Barres, B.A. Neurotoxic reactive astrocytes are induced by activated microglia. Nature, 2017, 541(7638), 481-487.
[http://dx.doi.org/10.1038/nature21029] [PMID: 28099414]
[68]
Sriram, K.; O’Callaghan, J.P. Divergent roles for tumor necrosis factor-α in the brain. J. Neuroimmune Pharmacol., 2007, 2(2), 140-153.
[http://dx.doi.org/10.1007/s11481-007-9070-6] [PMID: 18040839]
[69]
Mangogna, A.; Agostinis, C.; Bonazza, D.; Belmonte, B.; Zacchi, P.; Zito, G.; Romano, A.; Zanconati, F.; Ricci, G.; Kishore, U.; Bulla, R. Is the complement protein C1q a pro- or anti-tumorigenic factor? bioinformatics analysis involving human carcinomas. Front. Immunol., 2019, 10, 865.
[http://dx.doi.org/10.3389/fimmu.2019.00865] [PMID: 31130944]
[70]
Oushy, S.; Hellwinkel, J.E.; Wang, M.; Nguyen, G.J.; Gunaydin, D.; Harland, T.A.; Anchordoquy, T.J.; Graner, M.W. Glioblastoma multiforme-derived extracellular vesicles drive normal astrocytes towards a tumour-enhancing phenotype. Philos. Trans. R. Soc. Lond. B Biol. Sci., 2018, 373(1737), 20160477.
[http://dx.doi.org/10.1098/rstb.2016.0477] [PMID: 29158308]
[71]
Sahlender, D.A.; Savtchouk, I.; Volterra, A. What do we know about gliotransmitter release from astrocytes? Philos. Trans. R. Soc. Lond. B Biol. Sci., 2014, 369(1654), 20130592.
[http://dx.doi.org/10.1098/rstb.2013.0592] [PMID: 25225086]
[72]
Huang, J.Y.; Cheng, Y.J.; Lin, Y.P.; Lin, H.C.; Su, C.C.; Juliano, R.; Yang, B.C. Extracellular matrix of glioblastoma inhibits polarization and transmigration of T cells: The role of tenascin-C in immune suppression. J. Immunol., 2010, 185(3), 1450-1459.
[http://dx.doi.org/10.4049/jimmunol.0901352] [PMID: 20622113]
[73]
Swiatek-Machado, K.; Kaminska, B. STAT signaling in glioma cells. Adv. Exp. Med. Biol., 2013, 986, 189-208.
[http://dx.doi.org/10.1007/978-94-007-4719-7_10] [PMID: 22879070]
[74]
Gabrilovich, D.I.; Nagaraj, S. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol., 2009, 9(3), 162-174.
[http://dx.doi.org/10.1038/nri2506] [PMID: 19197294]
[75]
Wei, J.; Barr, J.; Kong, L.Y.; Wang, Y.; Wu, A.; Sharma, A.K.; Gumin, J.; Henry, V.; Colman, H.; Priebe, W.; Sawaya, R.; Lang, F.F.; Heimberger, A.B. Glioblastoma cancer-initiating cells inhibit T-cell proliferation and effector responses by the signal transducers and activators of transcription 3 pathway. Mol. Cancer Ther., 2010, 9(1), 67-78.
[http://dx.doi.org/10.1158/1535-7163.MCT-09-0734] [PMID: 20053772]
[76]
Chautard, E.; Ouédraogo, Z.G.; Biau, J.; Verrelle, P. Role of Akt in human malignant glioma: From oncogenesis to tumor aggressiveness. J. Neurooncol., 2014, 117(2), 205-215.
[http://dx.doi.org/10.1007/s11060-014-1382-9] [PMID: 24477623]
[77]
Kim, J.K.; Jin, X.; Sohn, Y.W.; Jin, X.; Jeon, H.Y.; Kim, E.J.; Ham, S.W.; Jeon, H.M.; Chang, S.Y.; Oh, S.Y.; Yin, J.; Kim, S.H.; Park, J.B.; Nakano, I.; Kim, H. Tumoral RANKL activates astrocytes that promote glioma cell invasion through cytokine signaling. Cancer Lett., 2014, 353(2), 194-200.
[http://dx.doi.org/10.1016/j.canlet.2014.07.034] [PMID: 25079688]
[78]
Li, K.; Li, J.; Zheng, J.; Qin, S. Reactive astrocytes in neurodegenerative diseases. Aging Dis., 2019, 10(3), 664-675.
[http://dx.doi.org/10.14336/AD.2018.0720] [PMID: 31165009]
[79]
Chen, W.; Xia, T.; Wang, D.; Huang, B.; Zhao, P.; Wang, J.; Qu, X.; Li, X. Human astrocytes secrete IL-6 to promote glioma migration and invasion through upregulation of cytomembrane MMP14. Oncotarget, 2016, 7(38), 62425-62438.
[http://dx.doi.org/10.18632/oncotarget.11515] [PMID: 27613828]
[80]
Nicolas, C.S.; Amici, M.; Bortolotto, Z.A.; Doherty, A.; Csaba, Z.; Fafouri, A.; Dournaud, P.; Gressens, P.; Collingridge, G.L.; Peineau, S. The role of JAK-STAT signaling within the CNS. JAK-STAT, 2013, 2(1), e22925.
[http://dx.doi.org/10.4161/jkst.22925] [PMID: 24058789]
[81]
Shabtay-Orbach, A.; Amit, M.; Binenbaum, Y.; Na’ara, S.; Gil, Z. Paracrine regulation of glioma cells invasion by astrocytes is mediated by glial-derived neurotrophic factor. Int. J. Cancer, 2015, 137(5), 1012-1020.
[http://dx.doi.org/10.1002/ijc.29380] [PMID: 25487790]
[82]
Senft, C.; Priester, M.; Polacin, M.; Schröder, K.; Seifert, V.; Kögel, D.; Weissenberger, J. Inhibition of the JAK-2/STAT3 signaling pathway impedes the migratory and invasive potential of human glioblastoma cells. J. Neurooncol., 2011, 101(3), 393-403.
[http://dx.doi.org/10.1007/s11060-010-0273-y] [PMID: 20589525]
[83]
Semenza, G.L. Oxygen sensing, hypoxia-inducible factors, and disease pathophysiology. Annu. Rev. Pathol., 2014, 9(1), 47-71.
[http://dx.doi.org/10.1146/annurev-pathol-012513-104720] [PMID: 23937437]
[84]
Corzo, C.A.; Condamine, T.; Lu, L.; Cotter, M.J.; Youn, J.I.; Cheng, P.; Cho, H.I.; Celis, E.; Quiceno, D.G.; Padhya, T.; McCaffrey, T.V.; McCaffrey, J.C.; Gabrilovich, D.I. HIF-1α regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J. Exp. Med., 2010, 207(11), 2439-2453.
[http://dx.doi.org/10.1084/jem.20100587] [PMID: 20876310]
[85]
Harris, A.J.; Thompson, A.R.; Whyte, M.K.; Walmsley, S.R. HIF-mediated innate immune responses: Cell signaling and therapeutic implications. Hypoxia., 2014, 2, 47-58.
[PMID: 27774466]
[86]
Guo, X.; Xue, H.; Shao, Q.; Wang, J.; Guo, X.; Chen, X.; Zhang, J.; Xu, S.; Li, T.; Zhang, P.; Gao, X.; Qiu, W.; Liu, Q.; Li, G. Hypoxia promotes glioma-associated macrophage infiltration via periostin and subsequent M2 polarization by upregulating TGF-beta and M-CSFR. Oncotarget, 2016, 7(49), 80521-80542.
[http://dx.doi.org/10.18632/oncotarget.11825] [PMID: 27602954]
[87]
Almiron Bonnin, D.A.; Havrda, M.C.; Lee, M.C.; Liu, H.; Zhang, Z.; Nguyen, L.N.; Harrington, L.X.; Hassanpour, S.; Cheng, C.; Israel, M.A. Secretion-mediated STAT3 activation promotes self-renewal of glioma stem-like cells during hypoxia. Oncogene, 2018, 37(8), 1107-1118.
[http://dx.doi.org/10.1038/onc.2017.404] [PMID: 29155422]
[88]
Ooi, Y.C.; Tran, P.; Ung, N.; Thill, K.; Trang, A.; Fong, B.M.; Nagasawa, D.T.; Lim, M.; Yang, I. The role of regulatory T-cells in glioma immunology. Clin. Neurol. Neurosurg., 2014, 119, 125-132.
[http://dx.doi.org/10.1016/j.clineuro.2013.12.004] [PMID: 24582432]
[89]
Yamagiwa, S.; Gray, J.D.; Hashimoto, S.; Horwitz, D.A. A role for TGF-β in the generation and expansion of CD4+CD25+ regulatory T cells from human peripheral blood. J. Immunol., 2001, 166(12), 7282-7289.
[http://dx.doi.org/10.4049/jimmunol.166.12.7282] [PMID: 11390478]
[90]
Liu, S.; Zhang, C.; Wang, B.; Zhang, H.; Qin, G.; Li, C.; Cao, L.; Gao, Q.; Ping, Y.; Zhang, K.; Lian, J.; Zhao, Q.; Wang, D.; Zhang, Z.; Zhao, X.; Yang, L.; Huang, L.; Yang, B.; Zhang, Y. Regulatory T cells promote glioma cell stemness through TGF-β–NF-κB–IL6–STAT3 signaling. Cancer Immunol. Immunother., 2021, 70(9), 2601-2616.
[http://dx.doi.org/10.1007/s00262-021-02872-0] [PMID: 33576874]
[91]
Paluskievicz, C.M.; Cao, X.; Abdi, R.; Zheng, P.; Liu, Y.; Bromberg, J.S. T regulatory cells and priming the suppressive tumor microenvironment. Front. Immunol., 2019, 10, 2453.
[http://dx.doi.org/10.3389/fimmu.2019.02453] [PMID: 31681327]
[92]
Armitage, J.D.; Newnes, H.V.; McDonnell, A.; Bosco, A.; Waithman, J. Fine-tuning the tumour microenvironment: Current perspectives on the mechanisms of tumour immunosuppression. Cells, 2021, 10(1), 56.
[http://dx.doi.org/10.3390/cells10010056] [PMID: 33401460]
[93]
Xu, L.; Xiao, H.; Xu, M.; Zhou, C.; Yi, L.; Liang, H. Glioma-derived T cell immunoglobulin- and mucin domain-containing molecule-4 (TIM4) contributes to tumor tolerance. J. Biol. Chem., 2011, 286(42), 36694-36699.
[http://dx.doi.org/10.1074/jbc.M111.292540] [PMID: 21896488]
[94]
Wang, H.; Zhou, H.; Xu, J.; Lu, Y.; Ji, X.; Yao, Y.; Chao, H.; Zhang, J.; Zhang, X.; Yao, S.; Wu, Y.; Wan, J. Different T-cell subsets in glioblastoma multiforme and targeted immunotherapy. Cancer Lett., 2021, 496, 134-143.
[http://dx.doi.org/10.1016/j.canlet.2020.09.028] [PMID: 33022290]
[95]
Colwell, N.; Larion, M.; Giles, A.J.; Seldomridge, A.N.; Sizdahkhani, S.; Gilbert, M.R.; Park, D.M. Hypoxia in the glioblastoma microenvironment: Shaping the phenotype of cancer stem-like cells. Neuro-oncol., 2017, 19(7), 887-896.
[http://dx.doi.org/10.1093/neuonc/now258] [PMID: 28339582]
[96]
Schaaf, M.B.; Garg, A.D.; Agostinis, P. Defining the role of the tumor vasculature in antitumor immunity and immunotherapy. Cell Death Dis., 2018, 9(2), 115.
[http://dx.doi.org/10.1038/s41419-017-0061-0] [PMID: 29371595]
[97]
Mi, Y.; Guo, N.; Luan, J.; Cheng, J.; Hu, Z.; Jiang, P.; Jin, W.; Gao, X. The emerging role of myeloid-derived suppressor cells in the glioma immune suppressive microenvironment. Front. Immunol., 2020, 11, 737.
[http://dx.doi.org/10.3389/fimmu.2020.00737] [PMID: 32391020]
[98]
Tomić, S.; Joksimović, B.; Bekić, M.; Vasiljević, M.; Milanović, M.; Čolić, M.; Vučević, D. Prostaglanin-E2 potentiates the suppressive functions of human mononuclear myeloid-derived suppressor cells and increases their capacity to expand IL-10-producing regulatory T cell subsets. Front. Immunol., 2019, 10, 475.
[http://dx.doi.org/10.3389/fimmu.2019.00475] [PMID: 30936876]
[99]
Chang, A.L.; Miska, J.; Wainwright, D.A.; Dey, M.; Rivetta, C.V.; Yu, D.; Kanojia, D.; Pituch, K.C.; Qiao, J.; Pytel, P.; Han, Y.; Wu, M.; Zhang, L.; Horbinski, C.M.; Ahmed, A.U.; Lesniak, M.S. CCL2 produced by the glioma microenvironment is essential for the recruitment of regulatory T cells and myeloid-derived suppressor cells. Cancer Res., 2016, 76(19), 5671-5682.
[http://dx.doi.org/10.1158/0008-5472.CAN-16-0144] [PMID: 27530322]
[100]
Otvos, B.; Silver, D.J.; Mulkearns-Hubert, E.E.; Alvarado, A.G.; Turaga, S.M.; Sorensen, M.D.; Rayman, P.; Flavahan, W.A.; Hale, J.S.; Stoltz, K.; Sinyuk, M.; Wu, Q.; Jarrar, A.; Kim, S.H.; Fox, P.L.; Nakano, I.; Rich, J.N.; Ransohoff, R.M.; Finke, J.; Kristensen, B.W.; Vogelbaum, M.A.; Lathia, J.D. Cancer stem cell-secreted macrophage migration inhibitory factor stimulates myeloid derived suppressor cell function and facilitates glioblastoma immune evasion. Stem Cells, 2016, 34(8), 2026-2039.
[http://dx.doi.org/10.1002/stem.2393] [PMID: 27145382]
[101]
Sánchez-León, M.L.; Jiménez-Cortegana, C.; Cabrera, G.; Vermeulen, E.M.; de la Cruz-Merino, L.; Sánchez-Margalet, V. The effects of dendritic cell-based vaccines in the tumor microenvironment: Impact on myeloid-derived suppressor cells. Front. Immunol., 2022, 13, 1050484.
[http://dx.doi.org/10.3389/fimmu.2022.1050484] [PMID: 36458011]
[102]
Martinez, F.O.; Sica, A.; Mantovani, A.; Locati, M. Macrophage activation and polarization. Front. Biosci., 2008, 13(13), 453-461.
[http://dx.doi.org/10.2741/2692] [PMID: 17981560]
[103]
Lapeyre-Prost, A.; Terme, M.; Pernot, S.; Pointet, A.L.; Voron, T.; Tartour, E.; Taieb, J. Immunomodulatory activity of VEGF in cancer. Int. Rev. Cell Mol. Biol., 2017, 330, 295-342.
[http://dx.doi.org/10.1016/bs.ircmb.2016.09.007] [PMID: 28215534]
[104]
Ostrand-Rosenberg, S.; Sinha, P.; Beury, D.W.; Clements, V.K. Cross-talk between myeloid-derived suppressor cells (MDSC), macrophages, and dendritic cells enhances tumor-induced immune suppression. Semin. Cancer Biol., 2012, 22(4), 275-281.
[http://dx.doi.org/10.1016/j.semcancer.2012.01.011] [PMID: 22313874]
[105]
Vallée, A.; Guillevin, R.; Vallée, J.N. Vasculogenesis and angiogenesis initiation under normoxic conditions through Wnt/β-catenin pathway in gliomas. Rev. Neurosci., 2017, 29(1), 71-91.
[http://dx.doi.org/10.1515/revneuro-2017-0032] [PMID: 28822229]
[106]
Samaras, V.; Piperi, C.; Levidou, G.; Zisakis, A.; Kavantzas, N.; Themistocleous, M.S.; Boviatsis, E.I.; Barbatis, C.; Lea, R.W.; Kalofoutis, A.; Korkolopoulou, P. Analysis of interleukin (IL)-8 expression in human astrocytomas: Associations with IL-6, cyclooxygenase-2, vascular endothelial growth factor, and microvessel morphometry. Hum. Immunol., 2009, 70(6), 391-397.
[http://dx.doi.org/10.1016/j.humimm.2009.03.011] [PMID: 19332096]
[107]
Blank, A.; Kremenetskaia, I.; Urbantat, R.M.; Acker, G.; Turkowski, K.; Radke, J.; Schneider, U.C.; Vajkoczy, P.; Brandenburg, S. Microglia/macrophages express alternative proangiogenic factors depending on granulocyte content in human glioblastoma. J. Pathol., 2021, 253(2), 160-173.
[http://dx.doi.org/10.1002/path.5569] [PMID: 33044746]
[108]
Taylor, C.T.; Cummins, E.P. The role of NF-kappaB in hypoxia-induced gene expression. Ann. N. Y. Acad. Sci., 2009, 1177(1), 178-184.
[http://dx.doi.org/10.1111/j.1749-6632.2009.05024.x] [PMID: 19845620]
[109]
Sharma, V.; Dixit, D.; Koul, N.; Mehta, V.S.; Sen, E. Ras regulates interleukin-1β-induced HIF-1α transcriptional activity in glioblastoma. J. Mol. Med., 2011, 89(2), 123-136.
[http://dx.doi.org/10.1007/s00109-010-0683-5] [PMID: 20865400]
[110]
Kaluz, S.; Van Meir, E.G. At the crossroads of cancer and inflammation: Ras rewires an HIF-driven IL-1 autocrine loop. J. Mol. Med., 2011, 89(2), 91-94.
[http://dx.doi.org/10.1007/s00109-010-0706-2] [PMID: 21161499]
[111]
Sun, W.; Depping, R.; Jelkmann, W. Interleukin-1β promotes hypoxia-induced apoptosis of glioblastoma cells by inhibiting hypoxia-inducible factor-1 mediated adrenomedullin production. Cell Death Dis., 2014, 5(1), e1020-e1020.
[http://dx.doi.org/10.1038/cddis.2013.562] [PMID: 24457964]
[112]
Döring, Y.; Pawig, L.; Weber, C.; Noels, H. The CXCL12/CXCR4 chemokine ligand/receptor axis in cardiovascular disease. Front. Physiol., 2014, 5, 212.
[PMID: 24966838]
[113]
Richardson, J.P. CXCR4 and glioblastoma. Anticancer. Agents Med. Chem., 2015, 16(1), 59-74.
[http://dx.doi.org/10.2174/1871520615666150824153032]
[114]
Yadav, V.N.; Zamler, D.; Baker, G.J.; Kadiyala, P.; Erdreich-Epstein, A.; DeCarvalho, A.C.; Mikkelsen, T.; Castro, M.G.; Lowenstein, P.R. CXCR4 increases in-vivo glioma perivascular invasion, and reduces radiation induced apoptosis: A genetic knockdown study. Oncotarget, 2016, 7(50), 83701-83719.
[http://dx.doi.org/10.18632/oncotarget.13295] [PMID: 27863376]
[115]
Stevenson, C.B.; Ehtesham, M.; McMillan, K.M.; Valadez, J.G.; Edgeworth, M.L.; Price, R.R.; Abel, T.W.; Mapara, K.Y.; Thompson, R.C. CXCR4 expression is elevated in glioblastoma multiforme and correlates with an increase in intensity and extent of peritumoral T2-weighted magnetic resonance imaging signal abnormalities. Neurosurgery, 2008, 63(3), 560-570.
[http://dx.doi.org/10.1227/01.NEU.0000324896.26088.EF] [PMID: 18812968]
[116]
Cheng, X.; Wang, H.; Zhang, X.; Zhao, S.; Zhou, Z.; Mu, X.; Zhao, C.; Teng, W. The Role of SDF-1/CXCR4/CXCR7 in Neuronal Regeneration after Cerebral Ischemia. Front. Neurosci., 2017, 11, 590.
[http://dx.doi.org/10.3389/fnins.2017.00590] [PMID: 29123467]
[117]
Chen, L.; Zhu, M.; Yu, S.; Hai, L.; Zhang, L.; Zhang, C.; Zhao, P.; Zhou, H.; Wang, S.; Yang, X. Arg kinase mediates CXCL12/CXCR4-induced invadopodia formation and invasion of glioma cells. Exp. Cell Res., 2020, 389(1), 111893.
[http://dx.doi.org/10.1016/j.yexcr.2020.111893] [PMID: 32035133]
[118]
Ping, Y.; Yao, X.; Jiang, J.; Zhao, L.; Yu, S.; Jiang, T.; Lin, M.C.M.; Chen, J.; Wang, B.; Zhang, R.; Cui, Y.; Qian, C.; Wang, J.M.; Bian, X. The chemokine CXCL12 and its receptor CXCR4 promote glioma stem cell-mediated VEGF production and tumour angiogenesis via PI3K/AKT signalling. J. Pathol., 2011, 224(3), 344-354.
[http://dx.doi.org/10.1002/path.2908] [PMID: 21618540]
[119]
Bao, S.; Wu, Q.; McLendon, R.E.; Hao, Y.; Shi, Q.; Hjelmeland, A.B.; Dewhirst, M.W.; Bigner, D.D.; Rich, J.N. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature, 2006, 444(7120), 756-760.
[http://dx.doi.org/10.1038/nature05236] [PMID: 17051156]
[120]
Ye, X.; Xu, S.; Xin, Y.; Yu, S.; Ping, Y.; Chen, L.; Xiao, H.; Wang, B.; Yi, L.; Wang, Q.; Jiang, X.; Yang, L.; Zhang, P.; Qian, C.; Cui, Y.; Zhang, X.; Bian, X. Tumor-associated microglia/macrophages enhance the invasion of glioma stem-like cells via TGF-β1 signaling pathway. J. Immunol., 2012, 189(1), 444-453.
[http://dx.doi.org/10.4049/jimmunol.1103248] [PMID: 22664874]
[121]
Zhou, W.; Ke, S.Q.; Huang, Z.; Flavahan, W.; Fang, X.; Paul, J.; Wu, L.; Sloan, A.E.; McLendon, R.E.; Li, X.; Rich, J.N.; Bao, S. Periostin secreted by glioblastoma stem cells recruits M2 tumour-associated macrophages and promotes malignant growth. Nat. Cell Biol., 2015, 17(2), 170-182.
[http://dx.doi.org/10.1038/ncb3090] [PMID: 25580734]
[122]
Boyd, N.H.; Tran, A.N.; Bernstock, J.D.; Etminan, T.; Jones, A.B.; Gillespie, G.Y.; Friedman, G.K.; Hjelmeland, A.B. Glioma stem cells and their roles within the hypoxic tumor microenvironment. Theranostics, 2021, 11(2), 665-683.
[http://dx.doi.org/10.7150/thno.41692] [PMID: 33391498]
[123]
Samaras, V.; Piperi, C.; Korkolopoulou, P.; Zisakis, A.; Levidou, G.; Themistocleous, M.S.; Boviatsis, E.I.; Sakas, D.E.; Lea, R.W.; Kalofoutis, A.; Patsouris, E. Application of the ELISPOT method for comparative analysis of interleukin (IL)-6 and IL-10 secretion in peripheral blood of patients with astroglial tumors. Mol. Cell. Biochem., 2007, 304(1-2), 343-351.
[http://dx.doi.org/10.1007/s11010-007-9517-3] [PMID: 17551671]
[124]
Nijaguna, M.B.; Patil, V.; Urbach, S.; Shwetha, S.D.; Sravani, K.; Hegde, A.S.; Chandramouli, B.A.; Arivazhagan, A.; Marin, P.; Santosh, V.; Somasundaram, K. Glioblastoma-derived Macrophage Colony-stimulating Factor (MCSF) induces microglial release of insulin-like growth factor-binding protein 1 (IGFBP1) to promote angiogenesis. J. Biol. Chem., 2015, 290(38), 23401-23415.
[http://dx.doi.org/10.1074/jbc.M115.664037] [PMID: 26245897]
[125]
Noorani, I.; Petty, G.; Grundy, P.L.; Sharpe, G.; Willaime-Morawek, S.; Harris, S.; Thomas, G.J.; Nicoll, J.A.R.; Boche, D. Novel association between microglia and stem cells in human gliomas: A contributor to tumour proliferation? J. Pathol. Clin. Res., 2015, 1(2), 67-75.
[http://dx.doi.org/10.1002/cjp2.7] [PMID: 27499894]
[126]
Abou-Antoun, T.J.; Hale, J.S.; Lathia, J.D.; Dombrowski, S.M. Brain cancer stem cells in adults and children: Cell biology and therapeutic implications. Neurotherapeutics, 2017, 14(2), 372-384.
[http://dx.doi.org/10.1007/s13311-017-0524-0] [PMID: 28374184]
[127]
Yang, I.; Han, S.J.; Kaur, G.; Crane, C.; Parsa, A.T. The role of microglia in central nervous system immunity and glioma immunology. J. Clin. Neurosci., 2010, 17(1), 6-10.
[http://dx.doi.org/10.1016/j.jocn.2009.05.006] [PMID: 19926287]
[128]
Chen, J.; Liu, G.; Wang, X.; Hong, H.; Li, T.; Li, L.; Wang, H.; Xie, J.; Li, B.; Li, T.; Lu, D.; Zhang, Y.; Zhao, H.; Yao, C.; Wen, K.; Li, T.; Chen, J.; Wu, S.; He, K.; Zhang, W.N.; Zhao, J.; Wang, N.; Han, Q.; Xia, Q.; Qi, J.; Chen, J.; Zhou, T.; Man, J.; Zhang, X.M.; Li, A.L.; Pan, X. Glioblastoma stem cell-specific histamine secretion drives pro-angiogenic tumor microenvironment remodeling. Cell Stem Cell, 2022, 29(11), 1531-1546.e7.
[http://dx.doi.org/10.1016/j.stem.2022.09.009] [PMID: 36265493]
[129]
Puebla, M.; Tapia, P.J.; Espinoza, H. Key role of astrocytes in postnatal brain and retinal angiogenesis. Int. J. Mol. Sci., 2022, 23(5), 2646.
[http://dx.doi.org/10.3390/ijms23052646] [PMID: 35269788]
[130]
Vollmann-Zwerenz, A.; Leidgens, V.; Feliciello, G.; Klein, C.A.; Hau, P. Tumor cell invasion in glioblastoma. Int. J. Mol. Sci., 2020, 21(6), 1932.
[http://dx.doi.org/10.3390/ijms21061932] [PMID: 32178267]

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