Login Register Cart 0
Generic placeholder image

Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Targeting Options of Tumor-Associated Macrophages (TAM) Activity in Gliomas

Author(s): Filippos Anagnostakis and Christina Piperi*

Volume 21, Issue 3, 2023

Published on: 01 April, 2022

Page: [457 - 470] Pages: 14

DOI: 10.2174/1570159X20666220120120203

Price: $65

Abstract

Tumor-associated macrophages (TAMs), the most plastic cells of the hematopoietic system, exhibit increased tumor-infiltrating properties and functional heterogeneity depending on tumor type and associated microenvironment. TAMs constitute a major cell type of cancer-related inflammation, commonly enhancing tumor growth. They are profoundly involved in glioma pathogenesis, contributing to many cancer hallmarks such as angiogenesis, survival, metastasis, and immunosuppression. Efficient targeting of TAMs presents a promising approach to tackle glioma progression. Several targeting options involve chemokine signaling axes inhibitors and antibodies, antiangiogenic factors, immunomodulatory molecules, surface immunoglobulins blockers, receptor and transcription factor inhibitors, as well as microRNAs (miRNAs), administered either as standalone or in combination with other conventional therapies. Herein, we provide a critical overview of current therapeutic approaches targeting TAMs in gliomas with the promising outcome.

Keywords: Tumor-associated macrophages, glioma, immunotherapy, CSF-1R, angiogenic factors, CCR2/CCL2, liposomes.

« Previous Next »
Graphical Abstract

[1]
Weller, M.; Wick, W.; Aldape, K.; Brada, M.; Berger, M.; Pfister, S.M.; Nishikawa, R.; Rosenthal, M.; Wen, P.Y.; Stupp, R.; Reifenberger, G. Glioma. Nat. Rev. Dis. Primers, 2015, 1(1), 15017.
[http://dx.doi.org/10.1038/nrdp.2015.17] [PMID: 27188790]
[2]
Ostrom, Q.T.; Bauchet, L.; Davis, F.G.; Deltour, I.; Fisher, J.L.; Langer, C.E.; Pekmezci, M.; Schwartzbaum, J.A.; Turner, M.C.; Walsh, K.M.; Wrensch, M.R.; Barnholtz-Sloan, J.S. The epidemiology of glioma in adults: a “state of the science” review. Neuro-oncol., 2014, 16(7), 896-913.
[http://dx.doi.org/10.1093/neuonc/nou087] [PMID: 24842956]
[3]
Wu, K.; Lin, K.; Li, X.; Yuan, X.; Xu, P.; Ni, P.; Xu, D. Redefining tumor-associated macrophage subpopulations and functions in the tumor microenvironment. Front. Immunol., 2020, 11, 1731.
[http://dx.doi.org/10.3389/fimmu.2020.01731] [PMID: 32849616]
[4]
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]
[5]
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]
[6]
Gargini, R.; Segura-Collar, B.; Sánchez-Gómez, P. Cellular plasticity and tumor microenvironment in gliomas: the struggle to hit a moving target. Cancers (Basel), 2020, 12(6), 1622.
[http://dx.doi.org/10.3390/cancers12061622] [PMID: 32570988]
[7]
Cassetta, L.; Pollard, J.W. Targeting macrophages: therapeutic approaches in cancer. Nat. Rev. Drug Discov., 2018, 17(12), 887-904.
[http://dx.doi.org/10.1038/nrd.2018.169] [PMID: 30361552]
[8]
Petty, A.J.; Yang, Y. Tumor-associated macrophages: implications in cancer immunotherapy. Immunotherapy, 2017, 9(3), 289-302.
[http://dx.doi.org/10.2217/imt-2016-0135] [PMID: 28231720]
[9]
de Groot, A.E.; Pienta, K.J. Epigenetic control of macrophage polarization: implications for targeting tumor-associated macrophages. Oncotarget, 2018, 9(29), 20908-20927.
[http://dx.doi.org/10.18632/oncotarget.24556] [PMID: 29755698]
[10]
Nielsen, S.R.; Schmid, M.C. Macrophages as key drivers of cancer progression and metastasis. Mediators Inflamm., 2017, 2017, 9624760.
[http://dx.doi.org/10.1155/2017/9624760] [PMID: 28210073]
[11]
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]
[12]
Wang, S-C.; Yu, C-F.; Hong, J-H.; Tsai, C-S.; Chiang, C-S. Radiation therapy-induced tumor invasiveness is associated with SDF-1-regulated macrophage mobilization and vasculogenesis. PLoS One, 2013, 8(8), e69182.
[http://dx.doi.org/10.1371/journal.pone.0069182] [PMID: 23940516]
[13]
Zhu, C.; Kros, J.M.; Cheng, C.; Mustafa, D. The contribution of tumor-associated macrophages in glioma neo-angiogenesis and implications for anti-angiogenic strategies. Neuro-oncol., 2017, 19(11), 1435-1446.
[http://dx.doi.org/10.1093/neuonc/nox081] [PMID: 28575312]
[14]
Stafford, J.H.; Hirai, T.; Deng, L.; Chernikova, S.B.; Urata, K.; West, B.L.; Brown, J.M. Colony stimulating factor 1 receptor inhibition delays recurrence of glioblastoma after radiation by altering myeloid cell recruitment and polarization. Neuro-oncol., 2016, 18(6), 797-806.
[http://dx.doi.org/10.1093/neuonc/nov272] [PMID: 26538619]
[15]
Yan, D.; Kowal, J.; Akkari, L.; Schuhmacher, A.J.; Huse, J.T.; West, B.L.; Joyce, J.A. Inhibition of colony stimulating factor-1 receptor abrogates microenvironment-mediated therapeutic resistance in gliomas. Oncogene, 2017, 36(43), 6049-6058.
[http://dx.doi.org/10.1038/onc.2017.261] [PMID: 28759044]
[16]
Coniglio, S.J.; Eugenin, E.; Dobrenis, K.; Stanley, E.R.; West, B.L.; Symons, M.H.; Segall, J.E. Microglial stimulation of glioblastoma invasion involves epidermal growth factor receptor (EGFR) and colony stimulating factor 1 receptor (CSF-1R) signaling. Mol. Med., 2012, 18(3), 519-527.
[http://dx.doi.org/10.2119/molmed.2011.00217] [PMID: 22294205]
[17]
Elmore, M.R.P.; Najafi, A.R.; Koike, M.A.; Dagher, N.N.; Spangenberg, E.E.; Rice, R.A.; Kitazawa, M.; Matusow, B.; Nguyen, H.; West, B.L.; Green, K.N. Colony-stimulating factor 1 receptor signaling is necessary for microglia viability, unmasking a microglia progenitor cell in the adult brain. Neuron, 2014, 82(2), 380-397.
[http://dx.doi.org/10.1016/j.neuron.2014.02.040] [PMID: 24742461]
[18]
Butowski, N.; Colman, H.; De Groot, J.F.; Omuro, A.M.; Nayak, L.; Wen, P.Y.; Cloughesy, T.F.; Marimuthu, A.; Haidar, S.; Perry, A.; Huse, J.; Phillips, J.; West, B.L.; Nolop, K.B.; Hsu, H.H.; Ligon, K.L.; Molinaro, A.M.; Prados, M. Orally administered colony stimulating factor 1 receptor inhibitor PLX3397 in recurrent glioblastoma: an Ivy Foundation Early Phase Clinical Trials Consortium phase II study. Neuro-oncol., 2016, 18(4), 557-564.
[http://dx.doi.org/10.1093/neuonc/nov245] [PMID: 26449250]
[19]
Akkari, L.; Bowman, R.L.; Tessier, J.; Klemm, F.; Handgraaf, S.M.; de Groot, M.; Quail, D.F.; Tillard, L.; Gadiot, J.; Huse, J.T.; Brandsma, D.; Westerga, J.; Watts, C.; Joyce, J.A. Dynamic changes in glioma macrophage populations after radiotherapy reveal CSF-1R inhibition as a strategy to overcome resistance. Sci. Transl. Med., 2020, 12(552), eaaw7843.
[http://dx.doi.org/10.1126/scitranslmed.aaw7843] [PMID: 32669424]
[20]
Dowlati, A.; Harvey, R.D.; Carvajal, R.D.; Hamid, O.; Klempner, S.J.; Kauh, J.S.W.; Peterson, D.A.; Yu, D.; Chapman, S.C.; Szpurka, A.M.; Carlsen, M.; Quinlan, T.; Wesolowski, R. LY3022855, an anti-colony stimulating factor-1 receptor (CSF-1R) monoclonal antibody, in patients with advanced solid tumors refractory to standard therapy: phase 1 dose-escalation trial. Invest. New Drugs, 2021, 39(4), 1057-1071.
[http://dx.doi.org/10.1007/s10637-021-01084-8] [PMID: 33624233]
[21]
Study of Cabiralizumab in Combination With Nivolumab in Patients With Selected Advanced Cancers - Full Text View - ClinicalTrials Available from: https://clinicaltrials.gov/ct2/show/study/ NCT02526017
[22]
Pradel, L.P.; Ooi, C-H.; Romagnoli, S.; Cannarile, M.A.; Sade, H.; Rüttinger, D.; Ries, C.H. Macrophage susceptibility to emactuzumab (RG7155) treatment. Mol. Cancer Ther., 2016, 15(12), 3077-3086.
[http://dx.doi.org/10.1158/1535-7163.MCT-16-0157] [PMID: 27582524]
[23]
Pyonteck, S.M.; Akkari, L.; Schuhmacher, A.J.; Bowman, R.L.; Sevenich, L.; Quail, D.F.; Olson, O.C.; Quick, M.L.; Huse, J.T.; Teijeiro, V.; Setty, M.; Leslie, C.S.; Oei, Y.; Pedraza, A.; Zhang, J.; Brennan, C.W.; Sutton, J.C.; Holland, E.C.; Daniel, D.; Joyce, J.A. CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nat. Med., 2013, 19(10), 1264-1272.
[http://dx.doi.org/10.1038/nm.3337] [PMID: 24056773]
[24]
Gu, G.; Gao, T.; Zhang, L.; Chen, X.; Pang, Q.; Wang, Y.; Wang, D.; Li, J.; Liu, Q. NKAP alters tumor immune microenvironment and promotes glioma growth via Notch1 signaling. J. Exp. Clin. Cancer Res., 2019, 38(1), 291.
[http://dx.doi.org/10.1186/s13046-019-1281-1] [PMID: 31277684]
[25]
Achyut, B.R.; Angara, K.; Jain, M.; Borin, T.F.; Rashid, M.H.; Iskander, A.S.M.; Ara, R.; Kolhe, R.; Howard, S.; Venugopal, N.; Rodriguez, P.C.; Bradford, J.W.; Arbab, A.S. Canonical NFκB signaling in myeloid cells is required for the glioblastoma growth. Sci. Rep., 2017, 7(1), 13754.
[http://dx.doi.org/10.1038/s41598-017-14079-4] [PMID: 29062041]
[26]
Melincovici, C.S.; Boşca, A.B.; Şuşman, S.; Mărginean, M.; Mihu, C.; Istrate, M.; Moldovan, I.M.; Roman, A.L.; Mihu, C.M. Vascular endothelial growth factor (VEGF) - key factor in normal and pathological angiogenesis. Rom. J. Morphol. Embryol., 2018, 59(2), 455-467.
[PMID: 30173249]
[27]
Chen, Z.; Ross, J.L.; Hambardzumyan, D. Intravital 2-photon imaging reveals distinct morphology and infiltrative properties of glioblastoma-associated macrophages. Proc. Natl. Acad. Sci. USA, 2019, 116(28), 14254-14259.
[http://dx.doi.org/10.1073/pnas.1902366116] [PMID: 31235603]
[28]
Peterson, T.E.; Kirkpatrick, N.D.; Huang, Y.; Farrar, C.T.; Marijt, K.A.; Kloepper, J.; Datta, M.; Amoozgar, Z.; Seano, G.; Jung, K.; Kamoun, W.S.; Vardam, T.; Snuderl, M.; Goveia, J.; Chatterjee, S.; Batista, A.; Muzikansky, A.; Leow, C.C.; Xu, L.; Batchelor, T.T.; Duda, D.G.; Fukumura, D.; Jain, R.K. Dual inhibition of Ang-2 and VEGF receptors normalizes tumor vasculature and prolongs survival in glioblastoma by altering macrophages. Proc. Natl. Acad. Sci. USA, 2016, 113(16), 4470-4475.
[http://dx.doi.org/10.1073/pnas.1525349113] [PMID: 27044097]
[29]
Lu-Emerson, C.; Snuderl, M.; Kirkpatrick, N.D.; Goveia, J.; Davidson, C.; Huang, Y.; Riedemann, L.; Taylor, J.; Ivy, P.; Duda, D.G.; Ancukiewicz, M.; Plotkin, S.R.; Chi, A.S.; Gerstner, E.R.; Eichler, A.F.; Dietrich, J.; Stemmer-Rachamimov, A.O.; Batchelor, T.T.; Jain, R.K. Increase in tumor-associated macrophages after antiangiogenic therapy is associated with poor survival among patients with recurrent glioblastoma. Neuro-oncol., 2013, 15(8), 1079-1087.
[http://dx.doi.org/10.1093/neuonc/not082] [PMID: 23828240]
[30]
Pander, J.; Heusinkveld, M.; van der Straaten, T.; Jordanova, E.S.; Baak-Pablo, R.; Gelderblom, H.; Morreau, H.; van der Burg, S.H.; Guchelaar, H-J.; van Hall, T. Activation of tumor-promoting type 2 macrophages by EGFR-targeting antibody cetuximab. Clin. Cancer Res., 2011, 17(17), 5668-5673.
[http://dx.doi.org/10.1158/1078-0432.CCR-11-0239] [PMID: 21788356]
[31]
Rigamonti, N.; Kadioglu, E.; Keklikoglou, I.; Wyser Rmili, C.; Leow, C.C.; De Palma, M. Role of angiopoietin-2 in adaptive tumor resistance to VEGF signaling blockade. Cell Rep., 2014, 8(3), 696-706.
[http://dx.doi.org/10.1016/j.celrep.2014.06.059] [PMID: 25088418]
[32]
Tamura, R.; Tanaka, T.; Ohara, K.; Miyake, K.; Morimoto, Y.; Yamamoto, Y.; Kanai, R.; Akasaki, Y.; Murayama, Y.; Tamiya, T.; Yoshida, K.; Sasaki, H. Persistent restoration to the immunosupportive tumor microenvironment in glioblastoma by bevacizumab. Cancer Sci., 2019, 110(2), 499-508.
[http://dx.doi.org/10.1111/cas.13889] [PMID: 30467920]
[33]
Scholz, A.; Harter, P.N.; Cremer, S.; Yalcin, B.H.; Gurnik, S.; Yamaji, M.; Di Tacchio, M.; Sommer, K.; Baumgarten, P.; Bähr, O.; Steinbach, J.P.; Trojan, J.; Glas, M.; Herrlinger, U.; Krex, D.; Meinhardt, M.; Weyerbrock, A.; Timmer, M.; Goldbrunner, R.; Deckert, M.; Braun, C.; Schittenhelm, J.; Frueh, J.T.; Ullrich, E.; Mittelbronn, M.; Plate, K.H.; Reiss, Y. Endothelial cell-derived angiopoietin-2 is a therapeutic target in treatment-naive and bevacizumab-resistant glioblastoma. EMBO Mol. Med., 2016, 8(1), 39-57.
[http://dx.doi.org/10.15252/emmm.201505505] [PMID: 26666269]
[34]
Castro, B.A.; Flanigan, P.; Jahangiri, A.; Hoffman, D.; Chen, W.; Kuang, R.; De Lay, M.; Yagnik, G.; Wagner, J.R.; Mascharak, S.; Sidorov, M.; Shrivastav, S.; Kohanbash, G.; Okada, H.; Aghi, M.K. Macrophage migration inhibitory factor downregulation: a novel mechanism of resistance to anti-angiogenic therapy. Oncogene, 2017, 36(26), 3749-3759.
[http://dx.doi.org/10.1038/onc.2017.1] [PMID: 28218903]
[35]
Seyfried, T.N.; Flores, R.; Poff, A.M.; D’Agostino, D.P.; Mukherjee, P. Metabolic therapy: a new paradigm for managing malignant brain cancer. Cancer Lett., 2015, 356(2)(2 Pt A), 289-300.
[http://dx.doi.org/10.1016/j.canlet.2014.07.015] [PMID: 25069036]
[36]
Perri, S.R.; Nalbantoglu, J.; Annabi, B.; Koty, Z.; Lejeune, L.; François, M.; Di Falco, M.R.; Béliveau, R.; Galipeau, J. Plasminogen kringle 5-engineered glioma cells block migration of tumor-associated macrophages and suppress tumor vascularization and progression. Cancer Res., 2005, 65(18), 8359-8365.
[http://dx.doi.org/10.1158/0008-5472.CAN-05-0508] [PMID: 16166313]
[37]
Codrici, E.; Enciu, A-M.; Popescu, I-D.; Mihai, S.; Tanase, C. Glioma stem cells and their microenvironments: providers of challenging therapeutic targets. Stem Cells Int., 2016, 2016, 5728438.
[http://dx.doi.org/10.1155/2016/5728438] [PMID: 26977157]
[38]
Guadagno, E.; Presta, I.; Maisano, D.; Donato, A.; Pirrone, C.K.; Cardillo, G.; Corrado, S.D.; Mignogna, C.; Mancuso, T.; Donato, G.; Del Basso De Caro, M.; Malara, N. Role of macrophages in brain tumor growth and progression. Int. J. Mol. Sci., 2018, 19(4), 1005.
[http://dx.doi.org/10.3390/ijms19041005] [PMID: 29584702]
[39]
Deng, L.; Stafford, J.H.; Liu, S-C.; Chernikova, S.B.; Merchant, M.; Recht, L.; Martin, B.J. SDF-1 blockade enhances anti-VEGF therapy of glioblastoma and can be monitored by MRI. Neoplasia, 2017, 19(1), 1-7.
[http://dx.doi.org/10.1016/j.neo.2016.11.010] [PMID: 27940247]
[40]
Wang, C.; Li, Y.; Chen, H.; Zhang, J.; Zhang, J.; Qin, T.; Duan, C.; Chen, X.; Liu, Y.; Zhou, X.; Yang, J. Inhibition of CYP4A by a novel flavonoid FLA-16 prolongs survival and normalizes tumor vasculature in glioma. Cancer Lett., 2017, 402, 131-141.
[http://dx.doi.org/10.1016/j.canlet.2017.05.030] [PMID: 28602979]
[41]
Wang, C.; Li, Y.; Chen, H.; Huang, K.; Liu, X.; Qiu, M.; Liu, Y.; Yang, Y.; Yang, J. CYP4X1 inhibition by flavonoid CH625 normalizes glioma vasculature through reprogramming TAMs via CB2 and EGFR-STAT3 axis. J. Pharmacol. Exp. Ther., 2018, 365(1), 72-83.
[http://dx.doi.org/10.1124/jpet.117.247130] [PMID: 29437915]
[42]
Zhao, T.; Su, Z.; Li, Y.; Zhang, X.; You, Q. Chitinase-3 like-protein-1 function and its role in diseases. Signal Transduct. Target. Ther., 2020, 5(1), 201.
[http://dx.doi.org/10.1038/s41392-020-00303-7] [PMID: 32929074]
[43]
Brana, I.; Calles, A.; LoRusso, P.M.; Yee, L.K.; Puchalski, T.A.; Seetharam, S.; Zhong, B.; de Boer, C.J.; Tabernero, J.; Calvo, E. Carlumab, an anti-C-C chemokine ligand 2 monoclonal antibody, in combination with four chemotherapy regimens for the treatment of patients with solid tumors: an open-label, multicenter phase 1b study. Target. Oncol., 2015, 10(1), 111-123.
[http://dx.doi.org/10.1007/s11523-014-0320-2] [PMID: 24928772]
[44]
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]
[45]
Iwamoto, H.; Izumi, K.; Mizokami, A. Is the C-C motif ligand 2-C-C chemokine receptor 2 axis a promising target for cancer therapy and diagnosis? Int. J. Mol. Sci., 2020, 21(23), 9328.
[http://dx.doi.org/10.3390/ijms21239328] [PMID: 33297571]
[46]
Salacz, M.E.; Kast, R.E.; Saki, N.; Brüning, A.; Karpel-Massler, G.; Halatsch, M-E. Toward a noncytotoxic glioblastoma therapy: blocking MCP-1 with the MTZ Regimen. OncoTargets Ther., 2016, 9, 2535-2545.
[http://dx.doi.org/10.2147/OTT.S100407] [PMID: 27175087]
[47]
Wang, Y.; Long, P.; Wang, Y.; Ma, W. NTRK fusions and TRK inhibitors: potential targeted therapies for adult glioblastoma. Front. Oncol., 2020, 10, 593578.
[http://dx.doi.org/10.3389/fonc.2020.593578] [PMID: 33330081]
[48]
Won, W-J.; Deshane, J.S.; Leavenworth, J.W.; Oliva, C.R.; Griguer, C.E. Metabolic and functional reprogramming of myeloid-derived suppressor cells and their therapeutic control in glioblastoma. Cell Stress, 2019, 3(2), 47-65.
[http://dx.doi.org/10.15698/cst2019.02.176] [PMID: 31225500]
[49]
Wang, H.; Zhang, L.; Zhang, I.Y.; Chen, X.; Da Fonseca, A.; Wu, S.; Ren, H.; Badie, S.; Sadeghi, S.; Ouyang, M.; Warden, C.D.; Badie, B. S100B promotes glioma growth through chemoattraction of myeloid-derived macrophages. Clin. Cancer Res., 2013, 19(14), 3764-3775.
[http://dx.doi.org/10.1158/1078-0432.CCR-12-3725] [PMID: 23719262]
[50]
Gao, H.; Zhang, I.Y.; Zhang, L.; Song, Y.; Liu, S.; Ren, H.; Liu, H.; Zhou, H.; Su, Y.; Yang, Y.; Badie, B. S100B suppression alters polarization of infiltrating myeloid-derived cells in gliomas and inhibits tumor growth. Cancer Lett., 2018, 439, 91-100.
[http://dx.doi.org/10.1016/j.canlet.2018.07.034] [PMID: 30076898]
[51]
Zhu, X.; Fujita, M.; Snyder, L.A.; Okada, H. Systemic delivery of neutralizing antibody targeting CCL2 for glioma therapy. J. Neurooncol., 2011, 104(1), 83-92.
[http://dx.doi.org/10.1007/s11060-010-0473-5] [PMID: 21116835]
[52]
Yoo, J.Y.; Swanner, J.; Otani, Y.; Nair, M.; Park, F.; Banasavadi-Siddegowda, Y.; Liu, J.; Jaime-Ramirez, A.C.; Hong, B.; Geng, F.; Guo, D.; Bystry, D.; Phelphs, M.; Quadri, H.; Lee, T.J.; Kaur, B. Oncolytic HSV therapy increases trametinib access to brain tumors and sensitizes them in vivo. Neuro-oncology, 2019, 21(9), 1131-1140.
[http://dx.doi.org/10.1093/neuonc/noz079] [PMID: 31063549]
[53]
Hu, F.; Huang, Y.; Semtner, M.; Zhao, K.; Tan, Z.; Dzaye, O.; Kettenmann, H.; Shu, K.; Lei, T. Down-regulation of Aquaporin-1 mediates a microglial phenotype switch affecting glioma growth. Exp. Cell Res., 2020, 396(2), 112323.
[http://dx.doi.org/10.1016/j.yexcr.2020.112323] [PMID: 33058832]
[54]
Nakamura, K.; Smyth, M.J. Myeloid immunosuppression and immune checkpoints in the tumor microenvironment. Cell. Mol. Immunol., 2020, 17(1), 1-12.
[http://dx.doi.org/10.1038/s41423-019-0306-1] [PMID: 31611651]
[55]
Yalcin, F.; Dzaye, O.; Xia, S. Tenascin-C function in glioma: immunomodulation and beyond. Adv. Exp. Med. Biol., 2020, 1272, 149-172.
[http://dx.doi.org/10.1007/978-3-030-48457-6_9] [PMID: 32845507]
[56]
Wanderley, C.W.; Colón, D.F.; Luiz, J.P.M.; Oliveira, F.F.; Viacava, P.R.; Leite, C.A.; Pereira, J.A.; Silva, C.M.; Silva, C.R.; Silva, R.L.; Speck-Hernandez, C.A.; Mota, J.M.; Alves-Filho, J.C.; Lima-Junior, R.C.; Cunha, T.M.; Cunha, F.Q. Paclitaxel reduces tumor growth by reprogramming tumor-associated macrophages to an M1 profile in a TLR4-dependent manner. Cancer Res., 2018, 78(20), 5891-5900.
[http://dx.doi.org/10.1158/0008-5472.CAN-17-3480] [PMID: 30104241]
[57]
Smith, D.A.; Conkling, P.; Richards, D.A.; Nemunaitis, J.J.; Boyd, T.E.; Mita, A.C.; de La Bourdonnaye, G.; Wages, D.; Bexon, A.S. Antitumor activity and safety of combination therapy with the Toll-like receptor 9 agonist IMO-2055, erlotinib, and bevacizumab in advanced or metastatic non-small cell lung cancer patients who have progressed following chemotherapy. Cancer Immunol. Immunother., 2014, 63(8), 787-796.
[http://dx.doi.org/10.1007/s00262-014-1547-6] [PMID: 24770667]
[58]
Mercurio, L.; Ajmone-Cat, M.A.; Cecchetti, S.; Ricci, A.; Bozzuto, G.; Molinari, A.; Manni, I.; Pollo, B.; Scala, S.; Carpinelli, G.; Minghetti, L. Targeting CXCR4 by a selective peptide antagonist modulates tumor microenvironment and microglia reactivity in a human glioblastoma model. J. Exp. Clin. Cancer Res., 2016, 35(1), 55.
[http://dx.doi.org/10.1186/s13046-016-0326-y] [PMID: 27015814]
[59]
Pires-Afonso, Y.; Niclou, S.P.; Michelucci, A. Revealing and harnessing tumour-associated microglia/macrophage heterogeneity in glioblastoma. Int. J. Mol. Sci., 2020, 21(3), 689.
[http://dx.doi.org/10.3390/ijms21030689] [PMID: 31973030]
[60]
Logtenberg, M.E.W.; Scheeren, F.A.; Schumacher, T.N. The CD47-SIRPα immune checkpoint. Immunity, 2020, 52(5), 742-752.
[http://dx.doi.org/10.1016/j.immuni.2020.04.011] [PMID: 32433947]
[61]
Hutter, G.; Theruvath, J.; Graef, C.M.; Zhang, M.; Schoen, M.K.; Manz, E.M.; Bennett, M.L.; Olson, A.; Azad, T.D.; Sinha, R.; Chan, C.; Assad Kahn, S.; Gholamin, S.; Wilson, C.; Grant, G.; He, J.; Weissman, I.L.; Mitra, S.S.; Cheshier, S.H. Microglia are effector cells of CD47-SIRPα antiphagocytic axis disruption against glioblastoma. Proc. Natl. Acad. Sci. USA, 2019, 116(3), 997-1006.
[http://dx.doi.org/10.1073/pnas.1721434116] [PMID: 30602457]
[62]
Gholamin, S.; Mitra, S.S.; Feroze, A.H.; Liu, J.; Kahn, S.A.; Zhang, M.; Esparza, R.; Richard, C.; Ramaswamy, V.; Remke, M.; Volkmer, A.K.; Willingham, S.; Ponnuswami, A.; McCarty, A.; Lovelace, P.; Storm, T.A.; Schubert, S.; Hutter, G.; Narayanan, C.; Chu, P.; Raabe, E.H.; Harsh, G., IV; Taylor, M.D.; Monje, M.; Cho, Y-J.; Majeti, R.; Volkmer, J.P.; Fisher, P.G.; Grant, G.; Steinberg, G.K.; Vogel, H.; Edwards, M.; Weissman, I.L.; Cheshier, S.H. Disrupting the CD47-SIRPα anti-phagocytic axis by a humanized anti-CD47 antibody is an efficacious treatment for malignant pediatric brain tumors. Sci. Transl. Med., 2017, 9(381), eaaf2968.
[http://dx.doi.org/10.1126/scitranslmed.aaf2968] [PMID: 28298418]
[63]
Ding, A.S.; Routkevitch, D.; Jackson, C.; Lim, M. Targeting myeloid cells in combination treatments for glioma and other tumors. Front. Immunol., 2019, 10, 1715.
[http://dx.doi.org/10.3389/fimmu.2019.01715] [PMID: 31396227]
[64]
Gholamin, S.; Youssef, O.A.; Rafat, M.; Esparza, R.; Kahn, S.; Shahin, M.; Giaccia, A.J.; Graves, E.E.; Weissman, I.; Mitra, S.; Cheshier, S.H. Irradiation or temozolomide chemotherapy enhances anti-CD47 treatment of glioblastoma. Innate Immun., 2020, 26(2), 130-137.
[http://dx.doi.org/10.1177/1753425919876690] [PMID: 31547758]
[65]
Bastiancich, C.; Bastiat, G.; Lagarce, F. Gemcitabine and glioblastoma: challenges and current perspectives. Drug Discov. Today, 2018, 23(2), 416-423.
[http://dx.doi.org/10.1016/j.drudis.2017.10.010] [PMID: 29074439]
[66]
Fujiwara, Y.; Komohara, Y.; Ikeda, T.; Takeya, M. Corosolic acid inhibits glioblastoma cell proliferation by suppressing the activation of signal transducer and activator of transcription-3 and nuclear factor-kappa B in tumor cells and tumor-associated macrophages. Cancer Sci., 2011, 102(1), 206-211.
[http://dx.doi.org/10.1111/j.1349-7006.2010.01772.x] [PMID: 21073634]
[67]
Iwamaru, A.; Szymanski, S.; Iwado, E.; Aoki, H.; Yokoyama, T.; Fokt, I.; Hess, K.; Conrad, C.; Madden, T.; Sawaya, R.; Kondo, S.; Priebe, W.; Kondo, Y. A novel inhibitor of the STAT3 pathway induces apoptosis in malignant glioma cells both in vitro and in vivo. Oncogene, 2007, 26(17), 2435-2444.
[http://dx.doi.org/10.1038/sj.onc.1210031] [PMID: 17043651]
[68]
Sufit, A.; Lee-Sherick, A.B.; DeRyckere, D.; Rupji, M.; Dwivedi, B.; Varella-Garcia, M.; Pierce, A.M.; Kowalski, J.; Wang, X.; Frye, S.V.; Earp, H.S.; Keating, A.K.; Graham, D.K. MERTK inhibition induces polyploidy and promotes cell death and cellular senescence in glioblastoma multiforme. PLoS One, 2016, 11(10), e0165107.
[http://dx.doi.org/10.1371/journal.pone.0165107] [PMID: 27783662]
[69]
Wu, J.; Frady, L.N.; Bash, R.E.; Cohen, S.M.; Schorzman, A.N.; Su, Y-T.; Irvin, D.M.; Zamboni, W.C.; Wang, X.; Frye, S.V.; Ewend, M.G.; Sulman, E.P.; Gilbert, M.R.; Earp, H.S.; Miller, C.R. MerTK as a therapeutic target in glioblastoma. Neuro-oncol., 2018, 20(1), 92-102.
[http://dx.doi.org/10.1093/neuonc/nox111] [PMID: 28605477]
[70]
Che Mat, M.F.; Abdul Murad, N.A.; Ibrahim, K.; Mohd Mokhtar, N.; Wan Ngah, W.Z.; Harun, R.; Jamal, R. Silencing of PROS1 induces apoptosis and inhibits migration and invasion of glioblastoma multiforme cells. Int. J. Oncol., 2016, 49(6), 2359-2366.
[http://dx.doi.org/10.3892/ijo.2016.3755] [PMID: 27840905]
[71]
Sadahiro, H.; Kang, K-D.; Gibson, J.T.; Minata, M.; Yu, H.; Shi, J.; Chhipa, R.; Chen, Z.; Lu, S.; Simoni, Y.; Furuta, T.; Sabit, H.; Zhang, S.; Bastola, S.; Yamaguchi, S.; Alsheikh, H.; Komarova, S.; Wang, J.; Kim, S-H.; Hambardzumyan, D.; Lu, X.; Newell, E.W.; DasGupta, B.; Nakada, M.; Lee, L.J.; Nabors, B.; Norian, L.A.; Nakano, I. Activation of the receptor tyrosine kinase AXL regulates the immune microenvironment in glioblastoma. Cancer Res., 2018, 78(11), 3002-3013.
[http://dx.doi.org/10.1158/0008-5472.CAN-17-2433] [PMID: 29531161]
[72]
Feng, Y.; Huang, J.; Ding, Y.; Xie, F.; Shen, X. Tamoxifen-induced apoptosis of rat C6 glioma cells via PI3K/Akt, JNK and ERK activation. Oncol. Rep., 2010, 24(6), 1561-1567.
[http://dx.doi.org/10.3892/or_00001018] [PMID: 21042752]
[73]
Liu, Y. Huang, L.; Guan, X.; Li, H.; Zhang, Q-Q.; Han, C.; Wang, Y-J.; Wang, C.; Zhang, Y.; Qu, C.; Liu, J.; Zou, W. ER-α36, a novel variant of ERα is involved in the regulation of Tamoxifen-sensitivity of glioblastoma cells. Steroids, 2016, 111, 127-133.
[http://dx.doi.org/10.1016/j.steroids.2016.02.009] [PMID: 26898538]
[74]
Qu, C.; Ma, J.; Zhang, Y.; Han, C.; Huang, L.; Shen, L.; Li, H.; Wang, X.; Liu, J.; Zou, W. Estrogen receptor variant ER-α36 promotes tamoxifen agonist activity in glioblastoma cells. Cancer Sci., 2019, 110(1), 221-234.
[http://dx.doi.org/10.1111/cas.13868] [PMID: 30417588]
[75]
Du, J.; Lu, W-L.; Ying, X.; Liu, Y.; Du, P.; Tian, W.; Men, Y.; Guo, J.; Zhang, Y.; Li, R-J.; Zhou, J.; Lou, J-N.; Wang, J-C.; Zhang, X.; Zhang, Q. Dual-targeting topotecan liposomes modified with tamoxifen and wheat germ agglutinin significantly improve drug transport across the blood-brain barrier and survival of brain tumor-bearing animals. Mol. Pharm., 2009, 6(3), 905-917.
[http://dx.doi.org/10.1021/mp800218q] [PMID: 19344115]
[76]
Serban, F.; Daianu, O.; Tataranu, L.G.; Artene, S-A.; Emami, G.; Georgescu, A.M.; Alexandru, O.; Purcaru, S.O.; Tache, D.E.; Danciulescu, M.M.; Sfredel, V.; Dricu, A. Silencing of epidermal growth factor, latrophilin and seven transmembrane domain-containing protein 1 (ELTD1) via siRNA-induced cell death in glioblastoma. J. Immunoassay Immunochem., 2017, 38(1), 21-33.
[http://dx.doi.org/10.1080/15321819.2016.1209217] [PMID: 27379831]
[77]
Zhang, H.; Zhang, W.; Sun, X.; Dang, R.; Zhou, R.; Bai, H.; Ben, J.; Zhu, X.; Zhang, Y.; Yang, Q.; Xu, Y.; Chen, Q. Class A1 scavenger receptor modulates glioma progression by regulating M2-like tumor-associated macrophage polarization. Oncotarget, 2016, 7(31), 50099-50116.
[http://dx.doi.org/10.18632/oncotarget.10318] [PMID: 27367025]
[78]
Ye, J.; Yang, Y.; Dong, W.; Gao, Y.; Meng, Y.; Wang, H.; Li, L.; Jin, J.; Ji, M.; Xia, X.; Chen, X.; Jin, Y.; Liu, Y. Drug-free mannosylated liposomes inhibit tumor growth by promoting the polarization of tumor-associated macrophages. Int. J. Nanomedicine, 2019, 14, 3203-3220.
[http://dx.doi.org/10.2147/IJN.S207589] [PMID: 31118632]
[79]
Ye, J.; Yang, Y.; Jin, J.; Ji, M.; Gao, Y.; Feng, Y.; Wang, H.; Chen, X.; Liu, Y. Targeted delivery of chlorogenic acid by mannosylated liposomes to effectively promote the polarization of TAMs for the treatment of glioblastoma. Bioact. Mater., 2020, 5(3), 694-708.
[http://dx.doi.org/10.1016/j.bioactmat.2020.05.001] [PMID: 32478203]
[80]
Xue, N.; Zhou, Q.; Ji, M.; Jin, J.; Lai, F.; Chen, J.; Zhang, M.; Jia, J.; Yang, H.; Zhang, J.; Li, W.; Jiang, J.; Chen, X. Chlorogenic acid inhibits glioblastoma growth through repolarizating macrophage from M2 to M1 phenotype. Sci. Rep., 2017, 7(1), 39011.
[http://dx.doi.org/10.1038/srep39011] [PMID: 28045028]
[81]
Zheng, Z.; Zhang, J.; Jiang, J.; He, Y.; Zhang, W.; Mo, X.; Kang, X.; Xu, Q.; Wang, B.; Huang, Y. Remodeling tumor immune microenvironment (TIME) for glioma therapy using multi-targeting liposomal codelivery. J. Immunother. Cancer, 2020, 8(2), e000207.
[http://dx.doi.org/10.1136/jitc-2019-000207] [PMID: 32817393]
[82]
Chen, T.; Song, X.; Gong, T.; Fu, Y.; Yang, L.; Zhang, Z.; Gong, T. nRGD modified lycobetaine and octreotide combination delivery system to overcome multiple barriers and enhance anti-glioma efficacy. Colloids Surf. B Biointerfaces, 2017, 156, 330-339.
[http://dx.doi.org/10.1016/j.colsurfb.2017.05.038] [PMID: 28544965]
[83]
Zhu, Y.; Liang, J.; Gao, C.; Wang, A.; Xia, J.; Hong, C.; Zhong, Z.; Zuo, Z.; Kim, J.; Ren, H.; Li, S.; Wang, Q.; Zhang, F.; Wang, J. Multifunctional ginsenoside Rg3-based liposomes for glioma targeting therapy. J. Control. Release, 2021, 330, 641-657.
[http://dx.doi.org/10.1016/j.jconrel.2020.12.036] [PMID: 33359582]
[84]
Zou, L.; Tao, Y.; Payne, G.; Do, L.; Thomas, T.; Rodriguez, J.; Dou, H. Targeted delivery of nano-PTX to the brain tumor-associated macrophages. Oncotarget, 2017, 8(4), 6564-6578.
[http://dx.doi.org/10.18632/oncotarget.14169] [PMID: 28036254]
[85]
Madsen, S.J.; Baek, S-K.; Makkouk, A.R.; Krasieva, T.; Hirschberg, H. Macrophages as cell-based delivery systems for nanoshells in photothermal therapy. Ann. Biomed. Eng., 2012, 40(2), 507-515.
[http://dx.doi.org/10.1007/s10439-011-0415-1] [PMID: 21979168]
[86]
Li, T-F.; Li, K.; Wang, C.; Liu, X.; Wen, Y.; Xu, Y-H.; Zhang, Q.; Zhao, Q-Y.; Shao, M.; Li, Y-Z.; Han, M.; Komatsu, N.; Zhao, L.; Chen, X. Harnessing the cross-talk between tumor cells and tumor-associated macrophages with a nano-drug for modulation of glioblastoma immune microenvironment. J. Control. Release, 2017, 268, 128-146.
[http://dx.doi.org/10.1016/j.jconrel.2017.10.024] [PMID: 29051064]
[87]
Zhang, B.; Zhang, Y.; Liao, Z.; Jiang, T.; Zhao, J.; Tuo, Y.; She, X.; Shen, S.; Chen, J.; Zhang, Q.; Jiang, X.; Hu, Y.; Pang, Z. UPA-sensitive ACPP-conjugated nanoparticles for multi-targeting therapy of brain glioma. Biomaterials, 2015, 36, 98-109.
[http://dx.doi.org/10.1016/j.biomaterials.2014.09.008] [PMID: 25443789]
[88]
VanHandel, M.; Alizadeh, D.; Zhang, L.; Kateb, B.; Bronikowski, M.; Manohara, H.; Badie, B. Selective uptake of multi-walled carbon nanotubes by tumor macrophages in a murine glioma model. J. Neuroimmunol., 2009, 208(1-2), 3-9.
[http://dx.doi.org/10.1016/j.jneuroim.2008.12.006] [PMID: 19181390]
[89]
Xu, S.; Wei, J.; Wang, F.; Kong, L-Y.; Ling, X-Y.; Nduom, E.; Gabrusiewicz, K.; Doucette, T.; Yang, Y.; Yaghi, N.K.; Fajt, V.; Levine, J.M.; Qiao, W.; Li, X-G.; Lang, F.F.; Rao, G.; Fuller, G.N.; Calin, G.A.; Heimberger, A.B. Effect of miR-142-3p on the M2 macrophage and therapeutic efficacy against murine glioblastoma. J. Natl. Cancer Inst., 2014, 106(8), dju162.
[http://dx.doi.org/10.1093/jnci/dju162] [PMID: 24974128]
[90]
Qian, M.; Wang, S.; Guo, X.; Wang, J.; Zhang, Z.; Qiu, W.; Gao, X.; Chen, Z.; Xu, J.; Zhao, R.; Xue, H.; Li, G. Hypoxic glioma-derived exosomes deliver microRNA-1246 to induce M2 macrophage polarization by targeting TERF2IP via the STAT3 and NF-κB pathways. Oncogene, 2020, 39(2), 428-442.
[http://dx.doi.org/10.1038/s41388-019-0996-y] [PMID: 31485019]
[91]
Sheng, Y.; Jiang, Q.; Dong, X.; Liu, J.; Liu, L.; Wang, H.; Wang, L.; Li, H.; Yang, X.; Dong, J. 3-Bromopyruvate inhibits the malignant phenotype of malignantly transformed macrophages and dendritic cells induced by glioma stem cells in the glioma microenvironment via miR-449a/MCT1. Biomed. Pharmacother., 2020, 121(109610), 109610.
[http://dx.doi.org/10.1016/j.biopha.2019.109610] [PMID: 31710894]
[92]
Shi, Y.; Zhang, B.; Zhu, J.; Huang, W.; Han, B.; Wang, Q.; Qi, C.; Wang, M.; Liu, F. miR-106b-5p inhibits IRF1/IFN-β signaling to promote M2 macrophage polarization of glioblastoma. OncoTargets Ther., 2020, 13, 7479-7492.
[http://dx.doi.org/10.2147/OTT.S238975] [PMID: 32801770]
[93]
Wang, L.; Lang, B.; Zhou, Y.; Ma, J.; Hu, K. Up-regulation of miR-663a inhibits the cancer stem cell-like properties of glioma via repressing the KDM2A-mediated TGF-β/SMAD signaling pathway. Cell Cycle, 2021, 20(19), 1935-1952.
[http://dx.doi.org/10.1080/15384101.2021.1966962] [PMID: 34424812]
[94]
Wang, Z.; Xue, Y.; Wang, P.; Zhu, J.; Ma, J. MiR-608 inhibits the migration and invasion of glioma stem cells by targeting macrophage migration inhibitory factor. Oncol. Rep., 2016, 35(5), 2733-2742.
[http://dx.doi.org/10.3892/or.2016.4652] [PMID: 26935642]
[95]
Yao, J.; Wang, Z.; Cheng, Y.; Ma, C.; Zhong, Y.; Xiao, Y.; Gao, X.; Li, Z. M2 macrophage-derived exosomal microRNAs inhibit cell migration and invasion in gliomas through PI3K/AKT/mTOR signaling pathway. J. Transl. Med., 2021, 19(1), 99.
[http://dx.doi.org/10.1186/s12967-021-02766-w] [PMID: 33676540]
[96]
Liu, Y.; Li, X.; Zhang, Y.; Wang, H.; Rong, X.; Peng, J.; He, L.; Peng, Y. An miR-340-5p-macrophage feedback loop modulates the progression and tumor microenvironment of glioblastoma multiforme. Oncogene, 2019, 38(49), 7399-7415.
[http://dx.doi.org/10.1038/s41388-019-0952-x] [PMID: 31427735]
[97]
Anand, S.; Coussens, L.M. Manipulating microRNAs to regulate macrophage polarization in gliomas. J. Natl. Cancer Inst., 2014, 106(8), dju230-dju230.
[http://dx.doi.org/10.1093/jnci/dju230] [PMID: 25136034]
[98]
Poli, A.; Wang, J.; Domingues, O.; Planagumà, J.; Yan, T.; Rygh, C.B.; Skaftnesmo, K.O.; Thorsen, F.; McCormack, E.; Hentges, F.; Pedersen, P.H.; Zimmer, J.; Enger, P.Ø.; Chekenya, M. Targeting glioblastoma with NK cells and mAb against NG2/CSPG4 prolongs animal survival. Oncotarget, 2013, 4(9), 1527-1546.
[http://dx.doi.org/10.18632/oncotarget.1291] [PMID: 24127551]
[99]
Taga, T.; Tabu, K. Glioma progression and recurrence involving maintenance and expansion strategies of glioma stem cells by organizing self-advantageous niche microenvironments. Inflamm. Regen., 2020, 40(1), 33.
[http://dx.doi.org/10.1186/s41232-020-00142-7] [PMID: 32952746]
[100]
Guan, X.; Hasan, M.N.; Begum, G.; Kohanbash, G.; Carney, K.E.; Pigott, V.M.; Persson, A.I.; Castro, M.G.; Jia, W.; Sun, D. Blockade of Na/H exchanger stimulates glioma tumor immunogenicity and enhances combinatorial TMZ and anti-PD-1 therapy. Cell Death Dis., 2018, 9(10), 1010.
[http://dx.doi.org/10.1038/s41419-018-1062-3] [PMID: 30262908]
[101]
Shimato, S.; Anderson, L.M.; Asslaber, M.; Bruce, J.N.; Canoll, P.; Anderson, D.E.; Anderson, R.C.E. Inhibition of caveolin-1 restores myeloid cell function in human glioblastoma. PLoS One, 2013, 8(10), e77397.
[http://dx.doi.org/10.1371/journal.pone.0077397] [PMID: 24130882]
[102]
Rose, M.; Duhamel, M.; Aboulouard, S.; Kobeissy, F.; Le Rhun, E.; Desmons, A.; Tierny, D.; Fournier, I.; Rodet, F.; Salzet, M. The role of a proprotein convertase inhibitor in reactivation of tumor-associated macrophages and inhibition of glioma growth. Mol. Ther. Oncolytics, 2020, 17, 31-46.
[http://dx.doi.org/10.1016/j.omto.2020.03.005] [PMID: 32300641]
[103]
Radin, D.P.; Tsirka, S.E. Interactions between tumor cells, neurons, and microglia in the glioma microenvironment. Int. J. Mol. Sci., 2020, 21(22), 8476.
[http://dx.doi.org/10.3390/ijms21228476] [PMID: 33187183]
[104]
Qi, Y.; Deng, G.; Xu, P.; Zhang, H.; Yuan, F.; Geng, R.; Jiang, H.; Liu, B.; Chen, Q. HHLA2 is a novel prognostic predictor and potential therapeutic target in malignant glioma. Oncol. Rep., 2019, 42(6), 2309-2322.
[http://dx.doi.org/10.3892/or.2019.7343] [PMID: 31578594]
[105]
Fujita, M.; Sasada, M.; Iyoda, T.; Fukai, F. Involvement of integrin-activating peptides derived from Tenascin-C in cancer aggression and new anticancer strategy using the fibronectin-derived integrin-inactivating peptide. Molecules, 2020, 25(14), 3239.
[http://dx.doi.org/10.3390/molecules25143239] [PMID: 32708610]
[106]
da Fonseca, A.C.C.; Badie, B. Microglia and macrophages in malignant gliomas: recent discoveries and implications for promising therapies. Clin. Dev. Immunol., 2013, 2013, 264124.
[http://dx.doi.org/10.1155/2013/264124] [PMID: 23864876]
[107]
Kopatz, J.; Beutner, C.; Welle, K.; Bodea, L.G.; Reinhardt, J.; Claude, J.; Linnartz-Gerlach, B.; Neumann, H. Siglec-h on activated microglia for recognition and engulfment of glioma cells. Glia, 2013, 61(7), 1122-1133.
[http://dx.doi.org/10.1002/glia.22501] [PMID: 23633299]
[108]
Wakabayashi, T.; Natsume, A.; Hashizume, Y.; Fujii, M.; Mizuno, M.; Yoshida, J. A phase I clinical trial of interferon-beta gene therapy for high-grade glioma: novel findings from gene expression profiling and autopsy. J. Gene Med., 2008, 10(4), 329-339.
[http://dx.doi.org/10.1002/jgm.1160] [PMID: 18220319]
[109]
A study of ARRY-382 in patients with selected advanced or metastatic cancers - Full Text View – Clinical Trials. Available from: https://clinicaltrials.gov/ct2/show/study/NCT01316822
[110]
A Phase 1, Dose Finding Study of CC-90002 in Subjects With Advanced Solid and Hematologic Cancers - Full Text View - Clinical Trials. Available from: https://clinicaltrials.gov/ct2/show/ NCT02367196
[111]
Trial of Intratumoral Injections of TTI-621 in Subjects With Relapsed and Refractory Solid Tumors and Mycosis Fungoides - Full Text View – Clinical Trials Available from: https://clinicaltrials.gov/ct2/show/ NCT02890368
[112]
Dose Finding Study Of CP-870,893, An Immune System Stimulating Antibody, In Combination With Paclitaxel And Carboplatin For Patients With Metastatic Solid Tumors - Full Text View - Clinical- Trials Available from: https://clinicaltrials.gov/ct2/show/NCT 00607048
[113]
A Study of Selicrelumab (RO7009789) in Combination With Atezolizumab in Participants With Locally Advanced and/or Metastatic Solid Tumors - Full Text View – Clinical Trials Available from: https://clinicaltrials.gov/ct2/show/NCT02304393
[114]
Xie, L.; Yang, Y.; Meng, J.; Wen, T.; Liu, J.; Xu, H. Cationic polysaccharide spermine-pullulan drives tumor associated macrophage towards M1 phenotype to inhibit tumor progression. Int. J. Biol. Macromol., 2019, 123, 1012-1019.
[http://dx.doi.org/10.1016/j.ijbiomac.2018.11.089] [PMID: 30439425]
[115]
Zhang, F.; Parayath, N.N.; Ene, C.I.; Stephan, S.B.; Koehne, A.L.; Coon, M.E.; Holland, E.C.; Stephan, M.T. Genetic programming of macrophages to perform anti-tumor functions using targeted mRNA nanocarriers. Nat. Commun., 2019, 10(1), 3974.
[http://dx.doi.org/10.1038/s41467-019-11911-5] [PMID: 31481662]
[116]
Wurdinger, T.; Deumelandt, K.; van der Vliet, H.J.; Wesseling, P.; de Gruijl, T.D. Mechanisms of intimate and long-distance cross-talk between glioma and myeloid cells: how to break a vicious cycle. Biochim. Biophys. Acta, 2014, 1846(2), 560-575.
[http://dx.doi.org/10.1016/j.bbcan.2014.10.003] [PMID: 25453365]

Rights & Permissions Print Cite
Article Metrics
6
© 2024 Bentham Science Publishers | Privacy Policy