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n3:pmcid: PMC0
bibo:doi: 10.1038%2Fonc.2017.261
n5:contains: _:vb66258816 _:vb66258832 _:vb66258808 _:vb66258782

Subject Item: _:vb66258782
rdf:type: n5:Section
dc:title: introduction
n5:contains: _:vb66258783 _:vb66258804 _:vb66258805 _:vb66258806 _:vb66258807 _:vb66258800 _:vb66258801 _:vb66258802 _:vb66258803 _:vb66258796 _:vb66258797 _:vb66258798 _:vb66258799 _:vb66258792 _:vb66258793 _:vb66258794 _:vb66258795 _:vb66258788 _:vb66258789 _:vb66258790 _:vb66258791 _:vb66258784 _:vb66258785 _:vb66258786 _:vb66258787

Subject Item: _:vb66258783
rdf:type: n3:Context
rdf:value: Glioblastomas are the most aggressive type of glioma and are associated with a poor patient prognosis across all molecular subtypes.>>1<<, 2 Despite some progress in neurosurgery, radiotherapy and chemotherapy treatment options, patient survival has improved only marginally during the past three decades.
n3:mentions: n2:15758009

Subject Item: _:vb66258784
rdf:type: n3:Context
rdf:value: Glioblastomas are the most aggressive type of glioma and are associated with a poor patient prognosis across all molecular subtypes.1, >>2<< Despite some progress in neurosurgery, radiotherapy and chemotherapy treatment options, patient survival has improved only marginally during the past three decades.
n3:mentions: n2:20129251

Subject Item: _:vb66258785
rdf:type: n3:Context
rdf:value: three decades. Under the current standard of care regimen, which consists of surgery, radiation and chemotherapy with the alkylating agent temozolomide, the median survival for patients diagnosed with glioblastoma is just 14.6 months.>>1<< Therefore, this disease poses a significant challenge for contemporary healthcare, and novel therapeutics are urgently required to address the unmet medical needs.
n3:mentions: n2:15758009

Subject Item: _:vb66258786
rdf:type: n3:Context
rdf:value: The aggressiveness of glioblastoma is driven both by genetic aberrations in glioma cells and alterations to the tumor microenvironment (TME).>>3<<, 4 Genetic changes such as PDGFRA amplification, TP53 loss, NF1 loss and EGFR mutation activate mitogenic pathways, causing tumor cells to rapidly proliferate.
n3:mentions: n2:22508724

Subject Item: _:vb66258787
rdf:type: n3:Context
rdf:value: The aggressiveness of glioblastoma is driven both by genetic aberrations in glioma cells and alterations to the tumor microenvironment (TME).3, >>4<< Genetic changes such as PDGFRA amplification, TP53 loss, NF1 loss and EGFR mutation activate mitogenic pathways, causing tumor cells to rapidly proliferate.
n3:mentions: n2:28292436

Subject Item: _:vb66258788
rdf:type: n3:Context
rdf:value: in glioma cells and alterations to the tumor microenvironment (TME).3, 4 Genetic changes such as PDGFRA amplification, TP53 loss, NF1 loss and EGFR mutation activate mitogenic pathways, causing tumor cells to rapidly proliferate.>>5<< Although considerable effort has been directed towards inhibiting aberrantly activated signaling pathways in glioma cells,6 success remains limited.
n3:mentions: n2:19915670

Subject Item: _:vb66258789
rdf:type: n3:Context
rdf:value: 5 Although considerable effort has been directed towards inhibiting aberrantly activated signaling pathways in glioma cells,>>6<< success remains limited.
n3:mentions: n2:22015553

Subject Item: _:vb66258790
rdf:type: n3:Context
rdf:value: from insufficient clinical activity. For example, the PDGFR inhibitor imatinib showed promising anti-tumor activities in preclinical studies but failed to deliver significant survival improvement in patients with recurrent glioblastoma.>>7<<, 8 The failure of these trials can likely be attributed to the fact that multiple mechanisms are employed in glioblastoma to achieve primary and acquired drug resistance.
n3:mentions: n2:16274936

Subject Item: _:vb66258791
rdf:type: n3:Context
rdf:value: insufficient clinical activity. For example, the PDGFR inhibitor imatinib showed promising anti-tumor activities in preclinical studies but failed to deliver significant survival improvement in patients with recurrent glioblastoma.7, >>8<< The failure of these trials can likely be attributed to the fact that multiple mechanisms are employed in glioblastoma to achieve primary and acquired drug resistance.
n3:mentions: n2:16914578

Subject Item: _:vb66258792
rdf:type: n3:Context
rdf:value: Several tumor cell-intrinsic processes that mediate unresponsiveness to different treatments have been identified to date, including activation of anti-apoptosis pathways,>>9<< bypass signaling,10 enrichment of glioma-initiating cells11, 12 and drug efflux machinery,13 among others.
n3:mentions: n2:18677408

Subject Item: _:vb66258793
rdf:type: n3:Context
rdf:value: Several tumor cell-intrinsic processes that mediate unresponsiveness to different treatments have been identified to date, including activation of anti-apoptosis pathways,9 bypass signaling,>>10<< enrichment of glioma-initiating cells11, 12 and drug efflux machinery,13 among others.
n3:mentions: n2:24386505

Subject Item: _:vb66258794
rdf:type: n3:Context
rdf:value: Several tumor cell-intrinsic processes that mediate unresponsiveness to different treatments have been identified to date, including activation of anti-apoptosis pathways,9 bypass signaling,10 enrichment of glioma-initiating cells>>11<<, 12 and drug efflux machinery,13 among others. A glioma cell-centric therapy thus needs to evade or overcome numerous such processes in order to achieve a durable response, which is challenging from a drug development perspective.
n3:mentions: n2:21988793

Subject Item: _:vb66258795
rdf:type: n3:Context
rdf:value: Several tumor cell-intrinsic processes that mediate unresponsiveness to different treatments have been identified to date, including activation of anti-apoptosis pathways,9 bypass signaling,10 enrichment of glioma-initiating cells11, >>12<< and drug efflux machinery,13 among others. A glioma cell-centric therapy thus needs to evade or overcome numerous such processes in order to achieve a durable response, which is challenging from a drug development perspective.
n3:mentions: n2:22854781

Subject Item: _:vb66258796
rdf:type: n3:Context
rdf:value: processes that mediate unresponsiveness to different treatments have been identified to date, including activation of anti-apoptosis pathways,9 bypass signaling,10 enrichment of glioma-initiating cells11, 12 and drug efflux machinery,>>13<< among others. A glioma cell-centric therapy thus needs to evade or overcome numerous such processes in order to achieve a durable response, which is challenging from a drug development perspective.
n3:mentions: n2:22891038

Subject Item: _:vb66258797
rdf:type: n3:Context
rdf:value: Compared with tumor cells, non-neoplastic stromal and immune cells are genomically stable, and are thus less prone to the development of resistance and subsequent rapid clonal evolution, a phenomenon linked to therapeutic failure.>>14<< The glioblastoma TME contains diverse populations of non-cancerous cells, including resident microglia, recruited macrophages, immature myeloid cells, astrocytes, T cells, and endothelial cells, among others.
n3:mentions: n2:24265155

Subject Item: _:vb66258798
rdf:type: n3:Context
rdf:value: to therapeutic failure.14 The glioblastoma TME contains diverse populations of non-cancerous cells, including resident microglia, recruited macrophages, immature myeloid cells, astrocytes, T cells, and endothelial cells, among others.>>4<<, 15, 16 These cells are either inhibited in the immunosuppressive TME or actively engage in pro-tumorigenic activities.
n3:mentions: n2:28292436

Subject Item: _:vb66258799
rdf:type: n3:Context
rdf:value: to therapeutic failure.14 The glioblastoma TME contains diverse populations of non-cancerous cells, including resident microglia, recruited macrophages, immature myeloid cells, astrocytes, T cells, and endothelial cells, among others.4, >>15<<, 16 These cells are either inhibited in the immunosuppressive TME or actively engage in pro-tumorigenic activities.
n3:mentions: n2:27840052

Subject Item: _:vb66258800
rdf:type: n3:Context
rdf:value: failure.14 The glioblastoma TME contains diverse populations of non-cancerous cells, including resident microglia, recruited macrophages, immature myeloid cells, astrocytes, T cells, and endothelial cells, among others.4, 15, >>16<< These cells are either inhibited in the immunosuppressive TME or actively engage in pro-tumorigenic activities.
n3:mentions: n2:22379614

Subject Item: _:vb66258801
rdf:type: n3:Context
rdf:value: microglia, recruited macrophages, immature myeloid cells, astrocytes, T cells, and endothelial cells, among others.4, 15, 16 These cells are either inhibited in the immunosuppressive TME or actively engage in pro-tumorigenic activities.>>17<< Notably, increasing evidence has demonstrated that tumor-associated microglia and macrophages (TAMs) contribute to glioma progression by enforcing immunosuppression and enhancing proliferation, invasion and angiogenesis.
n3:mentions: n2:25190673

Subject Item: _:vb66258802
rdf:type: n3:Context
rdf:value: activities.17 Notably, increasing evidence has demonstrated that tumor-associated microglia and macrophages (TAMs) contribute to glioma progression by enforcing immunosuppression and enhancing proliferation, invasion and angiogenesis.>>4<<, 18 Moreover, TAMs can represent up to 30% of the glioblastoma mass,19, 20 and TAM-associated gene expression is significantly associated with reduced patient survival.
n3:mentions: n2:28292436

Subject Item: _:vb66258803
rdf:type: n3:Context
rdf:value: activities.17 Notably, increasing evidence has demonstrated that tumor-associated microglia and macrophages (TAMs) contribute to glioma progression by enforcing immunosuppression and enhancing proliferation, invasion and angiogenesis.4, >>18<< Moreover, TAMs can represent up to 30% of the glioblastoma mass,19, 20 and TAM-associated gene expression is significantly associated with reduced patient survival.
n3:mentions: n2:23737783

Subject Item: _:vb66258804
rdf:type: n3:Context
rdf:value: 4, 18 Moreover, TAMs can represent up to 30% of the glioblastoma mass,>>19<<, 20 and TAM-associated gene expression is significantly associated with reduced patient survival.
n3:mentions: n2:18553315

Subject Item: _:vb66258805
rdf:type: n3:Context
rdf:value: 4, 18 Moreover, TAMs can represent up to 30% of the glioblastoma mass,19, >>20<< and TAM-associated gene expression is significantly associated with reduced patient survival.
n3:mentions: n2:16775224

Subject Item: _:vb66258806
rdf:type: n3:Context
rdf:value: and enhancing proliferation, invasion and angiogenesis.4, 18 Moreover, TAMs can represent up to 30% of the glioblastoma mass,19, 20 and TAM-associated gene expression is significantly associated with reduced patient survival.>>21<< These findings underscore the importance of TAM functions in glioblastoma, and provide a strong rationale for therapeutically targeting this cell population.
n3:mentions: n2:22937035

Subject Item: _:vb66258807
rdf:type: n3:Context
rdf:value: Previously, we reported that inhibition of colony stimulating factor-1 receptor (CSF-1R), using the small molecule BLZ945, alters the functions of TAMs and thus blocks proneural glioblastoma progression.>>22<< These data indicate that re-education of TAMs is a potent therapeutic strategy against glioblastoma and should be further assessed in single-agent or adjuvant/ neoadjuvant settings.
n3:mentions: n2:24056773

Subject Item: _:vb66258808
rdf:type: n5:Section
dc:title: materials and methods
n5:contains: _:vb66258812 _:vb66258813 _:vb66258814 _:vb66258815 _:vb66258809 _:vb66258810 _:vb66258811

Subject Item: _:vb66258809
rdf:type: n3:Context
rdf:value: The Nestin-Tv-a Ink4a/Arf−/− mouse line has been described previously>>27<< and was generously provided by Dr Eric Holland.
n3:mentions: n2:11485986

Subject Item: _:vb66258810
rdf:type: n3:Context
rdf:value: The injection was performed at a depth of 2 mm into the right front cortex, using a coordinate that was 1.5 mm lateral and 1 mm caudal from bregma, as previously described.>>22<<,
n3:mentions: n2:24056773

Subject Item: _:vb66258811
rdf:type: n3:Context
rdf:value: The size of cohorts was estimated based on our previous experience with the genetically engineered PDG mouse model.>>22<<, 36 All the experimental animals enrolled were included in the tumor burden analyses, which were conducted in a non-blinded manner.
n3:mentions: n2:24056773

Subject Item: _:vb66258812
rdf:type: n3:Context
rdf:value: 10 μm frozen sections were used for all analyses. For histological assessment, hematoxylin and eosin staining was performed, and histopathology was blindly scored by a neuropathologist (Dr Jason Huse) based on the 2007 WHO criteria.>>37<< For immunofluorescence analyses, dried frozen sections were rehydrated in PBS, permeabilized in 0.2% Triton X-100, and blocked in 0.5% PNB (PerkinElmer, Waltham, MA, USA) for 1 h at room temperature.
n3:mentions: n2:17618441

Subject Item: _:vb66258813
rdf:type: n3:Context
rdf:value: Quantification of intratumoral changes was performed using TissueQuest and StrataQuest software (TissueGnostics), as previously described.>>22<<
n3:mentions: n2:24056773

Subject Item: _:vb66258814
rdf:type: n3:Context
rdf:value: The generation and characterization of the PDGC23 glioma cell line has been previously described.>>22<< The U-87MG cell line was provided by Prof. Monika Hegi’s lab (University of Lausanne, Switzerland).
n3:mentions: n2:24056773

Subject Item: _:vb66258815
rdf:type: n3:Context
rdf:value: MDMs and U-87MG cells was performed with RIPA buffer (Sigma) containing protease and phosphatase inhibitors (Thermo Scientific). To extract protein from dissected gliomas, a pre-established biochemical fractionation protocol was used.>>22<<, 38 The resultant synaptosomal membrane fraction was lysed in NP-40 buffer as described above.
n3:mentions: n2:24056773

Subject Item: _:vb66258816
rdf:type: n5:Section
dc:title: results
n5:contains: _:vb66258820 _:vb66258821 _:vb66258822 _:vb66258823 _:vb66258817 _:vb66258818 _:vb66258819 _:vb66258828 _:vb66258829 _:vb66258830 _:vb66258831 _:vb66258824 _:vb66258825 _:vb66258826 _:vb66258827

Subject Item: _:vb66258817
rdf:type: n3:Context
rdf:value: To directly compare the therapeutic efficacy of CSF-1R inhibitors with multi-targeted tyrosine kinase inhibitors, we selected PLX3397, a potent CSF-1R and c-Kit inhibitor>>23<< with demonstrated clinical benefit in synovial diffuse-type giant cell tumors,24 as well as vatalanib and dovitinib, two inhibitors targeting multiple RTKs.
n3:mentions: n2:22039576

Subject Item: _:vb66258818
rdf:type: n3:Context
rdf:value: the therapeutic efficacy of CSF-1R inhibitors with multi-targeted tyrosine kinase inhibitors, we selected PLX3397, a potent CSF-1R and c-Kit inhibitor23 with demonstrated clinical benefit in synovial diffuse-type giant cell tumors,>>24<< as well as vatalanib and dovitinib, two inhibitors targeting multiple RTKs.
n3:mentions: n2:26222558

Subject Item: _:vb66258819
rdf:type: n3:Context
rdf:value: Vatalanib inhibits PDGFR-β, VEGFR1/2/3, c-Kit and CSF-1R to varying degrees of efficacy,>>25<< and dovitinib inhibits Flt3, c-Kit, FGFR1/3, VEGFR1/2/3, PDGFR-β and CSF-1R to different extents.
n3:mentions: n2:10786682

Subject Item: _:vb66258820
rdf:type: n3:Context
rdf:value: two inhibitors targeting multiple RTKs. Vatalanib inhibits PDGFR-β, VEGFR1/2/3, c-Kit and CSF-1R to varying degrees of efficacy,25 and dovitinib inhibits Flt3, c-Kit, FGFR1/3, VEGFR1/2/3, PDGFR-β and CSF-1R to different extents.>>26<< For both drugs, substantially higher effective concentrations are required for effective CSF-1R inhibition compared with their other RTK targets.
n3:mentions: n2:15598814

Subject Item: _:vb66258821
rdf:type: n3:Context
rdf:value: In these mice, Nestin+ glioma-initiating cells express the receptor for the replication-competent avian retrovirus, thus allowing cell type-specific delivery of the oncogene PDGF-B>>27<< in an Ink4a/Arf-deficient background.
n3:mentions: n2:11485986

Subject Item: _:vb66258822
rdf:type: n3:Context
rdf:value: avian retrovirus, thus allowing cell type-specific delivery of the oncogene PDGF-B27 in an Ink4a/Arf-deficient background. We previously showed that CSF-1R expression is restricted to TAMs, and PDGFR-α expression is glioma cell-specific.>>22<< Further analysis of the TME by immunostaining of PDG tumors herein revealed that a small proportion of CD31+ endothelial cells express VEGFR2 (Supplementary Figure S1A) and low levels of c-Kit (Supplementary Figure S1B).
n3:mentions: n2:24056773

Subject Item: _:vb66258823
rdf:type: n3:Context
rdf:value: Consistent with the scarcity of evident c-Kit expression in glioma cells in vivo, we did not detect Kit expression in PDGC23, a representative glioma cell line derived from the PDG model>>22<< nor the human glioma cell line U-87MG (data not shown).
n3:mentions: n2:24056773

Subject Item: _:vb66258824
rdf:type: n3:Context
rdf:value: of drugs should be administered to allow for fair comparison of their efficacy; (ii) therapeutic responses had been documented in preclinical models of other tumor types using similar dosages; and (iii) toxicity must be minimal.>>28<<, 29, 30 Pharmacokinetic analyses showed that all three compounds readily entered the systemic circulation and were detectable in the brain parenchyma 2 h following oral administration (Supplementary Figure S1C).
n3:mentions: n2:15256447

Subject Item: _:vb66258825
rdf:type: n3:Context
rdf:value: of drugs should be administered to allow for fair comparison of their efficacy; (ii) therapeutic responses had been documented in preclinical models of other tumor types using similar dosages; and (iii) toxicity must be minimal.28, >>29<<, 30 Pharmacokinetic analyses showed that all three compounds readily entered the systemic circulation and were detectable in the brain parenchyma 2 h following oral administration (Supplementary Figure S1C).
n3:mentions: n2:15502845

Subject Item: _:vb66258826
rdf:type: n3:Context
rdf:value: of drugs should be administered to allow for fair comparison of their efficacy; (ii) therapeutic responses had been documented in preclinical models of other tumor types using similar dosages; and (iii) toxicity must be minimal.28, 29, >>30<< Pharmacokinetic analyses showed that all three compounds readily entered the systemic circulation and were detectable in the brain parenchyma 2 h following oral administration (Supplementary Figure S1C).
n3:mentions: n2:15897558

Subject Item: _:vb66258827
rdf:type: n3:Context
rdf:value: In the context of CSF-1R blockade using a chemically distinct small molecule inhibitor, BLZ945,>>22<< we previously reported that TAMs survive (due to the presence of survival factors including GM-CSF and IFNγ in the proneural glioma microenvironment) but are ‘re-educated’, concomitant with reduced expression of M2-like macrophage genes.
n3:mentions: n2:24056773

Subject Item: _:vb66258828
rdf:type: n3:Context
rdf:value: expected (Supplementary Figure S6A, bottom row), indicating that the glioma microenvironment specifically promotes TAM survival in the context of CSF-1R blockade, as we have also demonstrated with an independent small molecule inhibitor.>>22<< Interestingly, TAM density was similarly unchanged in vatalanib-treated and dovitinib-treated gliomas compared to vehicle, while microglia depletion was observed in the adjacent normal brain of these treatment groups (Figure 2d and
n3:mentions: n2:24056773

Subject Item: _:vb66258829
rdf:type: n3:Context
rdf:value: by glioma cells can render TAMs resistant to RTK inhibitor-mediated cytocidal effects. Indeed, we previously identified GM-CSF, IFN-γ and CXCL10 as glioma cell-secreted factors that keep TAMs alive in the context of BLZ945 treatment.>>22<< It is possible that these same factors also protect macrophages from killing induced by the different RTK inhibitors assessed here, which will be an interesting point to investigate in future studies.
n3:mentions: n2:24056773

Subject Item: _:vb66258830
rdf:type: n3:Context
rdf:value: Specifically, we quantified Adm, Arg1, Mrc1, F13a1, Il10, Cd163, Stab1 and Chil3, several of which had been successfully used to capture TAM-related expression changes in whole gliomas previously.>>22<< Indeed, PLX3397 led to depolarization of TAMs from their original M2-like state, as indicated by significant downregulation of Adm (P<0.001), Arg1 (P<0.05), F13a1 (P<0.01), Il10 (P<0.01) and Chil3 (P<0.05), compared with the vehicle group
n3:mentions: n2:24056773

Subject Item: _:vb66258831
rdf:type: n3:Context
rdf:value: TAM depolarization can be accompanied by important changes in cellular functions.>>22<< To determine whether PLX3397 alters the pro-proliferative function of educated macrophages, we performed conditioned media culture experiments that mimic the heterotypic interactions between tumor cells and macrophages.
n3:mentions: n2:24056773

Subject Item: _:vb66258832
rdf:type: n5:Section
dc:title: discussion
n5:contains: _:vb66258836 _:vb66258837 _:vb66258838 _:vb66258833 _:vb66258834 _:vb66258835

Subject Item: _:vb66258833
rdf:type: n3:Context
rdf:value: Specifically, we observed that PLX3397 induces TAM depolarization from an M2-like state, which is similar to our previous finding using the chemically distinct CSF-1R inhibitor, BLZ945.>>22<< Furthermore, we found that PLX3397 effectively improves the efficacy of the multi-targeted kinase inhibitors vatalanib and dovitinib in vivo, resulting in pronounced glioma regression following combination treatments.
n3:mentions: n2:24056773

Subject Item: _:vb66258834
rdf:type: n3:Context
rdf:value: Underlying this phenotypic switch is the downregulation of a subset of genes that are associated with the M2-like state of TAMs. Genes such as Arg1, Il10 and Chil3 have been implicated in TAM M2 polarization across multiple cancers.>>31<< The phenotypic alteration of TAMs consequently renders glioma cells more susceptible to pharmacological inhibition of mitogenic RTKs, which provides an opportunity to maximize therapeutic outcomes via combination therapies.
n3:mentions: n2:20856220

Subject Item: _:vb66258835
rdf:type: n3:Context
rdf:value: death in a monoculture setting, thus indicating the presence of a cell-extrinsic resistance mechanism in vivo. Because TAMs have been shown to interfere with the efficacy of chemotherapy and radiotherapy (reviewed in De Palma et al.,>>32<< Ruffell et al.,33), it would be of interest to determine whether TAMs also exert such an effect against RTK inhibitors in other tumor types.
n3:mentions: n2:23518347

Subject Item: _:vb66258836
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rdf:value: setting, thus indicating the presence of a cell-extrinsic resistance mechanism in vivo. Because TAMs have been shown to interfere with the efficacy of chemotherapy and radiotherapy (reviewed in De Palma et al.,32 Ruffell et al.,>>33<<), it would be of interest to determine whether TAMs also exert such an effect against RTK inhibitors in other tumor types.
n3:mentions: n2:25858805

Subject Item: _:vb66258837
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rdf:value: Because PLX3397 and some multi-targeted inhibitors, such as dovitinib, have advanced through phase I clinical trials in recurrent glioblastoma patients,>>34<<, 35 it would be timely to explore whether such combination therapies can improve clinical outcomes in patients with newly diagnosed or recurrent glioblastoma.
n3:mentions: n2:26449250

Subject Item: _:vb66258838
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rdf:value: Because PLX3397 and some multi-targeted inhibitors, such as dovitinib, have advanced through phase I clinical trials in recurrent glioblastoma patients,34, >>35<< it would be timely to explore whether such combination therapies can improve clinical outcomes in patients with newly diagnosed or recurrent glioblastoma.
n3:mentions: n2:27100354

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