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n2:pmcid: PMC0
bibo:doi: 10.1155%2F2013%2F264124
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Subject Item: _:vb23859411
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dc:title: introduction
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Subject Item: _:vb23859412
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rdf:value: Malignant gliomas, the most common primary brain tumors that arise from glial cells within the central nervous system (CNS), are among the most fatal human cancers [>>1<<]. Glioblastoma multiforme (GBM), the most aggressive type of malignant glioma, is highly invasive, making tumor recurrence certain even after a complete resection [2].
n2:mentions: n3:23095881

Subject Item: _:vb23859413
rdf:type: n2:Context
rdf:value: Glioblastoma multiforme (GBM), the most aggressive type of malignant glioma, is highly invasive, making tumor recurrence certain even after a complete resection [>>2<<]. Besides, the presence of the blood-brain barrier (BBB) significantly limits the penetration of most chemotherapeutic agents into the CNS [3]. With a median survival of only 14.6 months even after aggressive therapy with surgery,
n2:mentions: n3:22677165

Subject Item: _:vb23859414
rdf:type: n2:Context
rdf:value: Besides, the presence of the blood-brain barrier (BBB) significantly limits the penetration of most chemotherapeutic agents into the CNS [>>3<<]. With a median survival of only 14.6 months even after aggressive therapy with surgery, radiation, and chemotherapy, most patients succumb to their disease within two years of the initial diagnosis [4]. Thus, there is a pressing need for
n2:mentions: n3:17538176

Subject Item: _:vb23859415
rdf:type: n2:Context
rdf:value: With a median survival of only 14.6 months even after aggressive therapy with surgery, radiation, and chemotherapy, most patients succumb to their disease within two years of the initial diagnosis [>>4<<]. Thus, there is a pressing need for discovery of more effective therapies to improve patient outcomes.
n2:mentions: n3:15758009

Subject Item: _:vb23859416
rdf:type: n2:Context
rdf:value: In experimental glioma models, tumor microglia and macrophages can be differentiated by FACS based on CD45 and CD11b staining characteristics [>>6<<], but in human tissue samples, such separation is not as distinct.
n2:mentions: n3:10764271

Subject Item: _:vb23859417
rdf:type: n2:Context
rdf:value: Although both cell types can acquire M1 phenotype and are capable of releasing proinflammatory cytokines, phagocytosis, and antigen presentation [>>7<<], their effector immune function in gliomas appears to be suppressed.
n2:mentions: n3:19926287

Subject Item: _:vb23859418
rdf:type: n2:Context
rdf:value: In fact, increasing new evidence suggests that microglia and macrophages interact with the tumor cells by promoting their growth and migration [>>8<<]. In this review, we briefly summarize recent data that has been reported on microglia/macrophages brain tumor interaction and discuss potential application of these findings to the development of future antiglioma therapies.
n2:mentions: n3:21446047

Subject Item: _:vb23859419
rdf:type: n4:Section
dc:title: immunosuppression
n4:contains: _:vb23859420 _:vb23859421 _:vb23859422 _:vb23859423 _:vb23859424 _:vb23859425 _:vb23859426 _:vb23859427

Subject Item: _:vb23859420
rdf:type: n2:Context
rdf:value: tumor cells establish an immunosuppressed microenvironment, leading GAMs to acquire an alternatively activated (M2) phenotype that further contributes to the local immunosuppression and supports tumor growth and invasion [>>8<<, 21, 22]. Recently, we demonstrated that S100B, a protein that is expressed by most gliomas and activates receptor for advanced glycation end products (RAGE) on microglia/macrophages, can induce signal transducer and activator of
n2:mentions: n3:21446047

Subject Item: _:vb23859421
rdf:type: n2:Context
rdf:value: tumor cells establish an immunosuppressed microenvironment, leading GAMs to acquire an alternatively activated (M2) phenotype that further contributes to the local immunosuppression and supports tumor growth and invasion [8, >>21<<, 22]. Recently, we demonstrated that S100B, a protein that is expressed by most gliomas and activates receptor for advanced glycation end products (RAGE) on microglia/macrophages, can induce signal transducer and activator of
n2:mentions: n3:18553315

Subject Item: _:vb23859422
rdf:type: n2:Context
rdf:value: tumor cells establish an immunosuppressed microenvironment, leading GAMs to acquire an alternatively activated (M2) phenotype that further contributes to the local immunosuppression and supports tumor growth and invasion [8, 21, >>22<<]. Recently, we demonstrated that S100B, a protein that is expressed by most gliomas and activates receptor for advanced glycation end products (RAGE) on microglia/macrophages, can induce signal transducer and activator of transcription 3
n2:mentions: n3:19944963

Subject Item: _:vb23859423
rdf:type: n2:Context
rdf:value: (STAT3) activity, resulting in suppression of microglia and primary monocyte function in vitro, reflected by inhibition of interleukin-1 beta (IL-1β), tumor necrosis factor-alpha (TNF-α) production, and other pro-inflammatory cytokines [>>23<<]. As a signal transducer, STAT3 is a central node for numerous oncogenic signaling pathways involving cytokines and growth factors [24].
n2:mentions: n3:21264954

Subject Item: _:vb23859424
rdf:type: n2:Context
rdf:value: As a signal transducer, STAT3 is a central node for numerous oncogenic signaling pathways involving cytokines and growth factors [>>24<<]. STAT3 is also an important transcription regulator, defining a transcriptional program at multiple levels that facilitate tumor cell proliferation, survival, invasion, cancer-promoting inflammation, and suppression of antitumor immune
n2:mentions: n3:19851315

Subject Item: _:vb23859425
rdf:type: n2:Context
rdf:value: also an important transcription regulator, defining a transcriptional program at multiple levels that facilitate tumor cell proliferation, survival, invasion, cancer-promoting inflammation, and suppression of antitumor immune responses [>>24<<].
n2:mentions: n3:19851315

Subject Item: _:vb23859426
rdf:type: n2:Context
rdf:value: For example, transforming growth factor-beta 1 (TGF-β1), an immunosuppressive cytokine that is expressed by glioma cells, is also produced by GAMs [>>25<<]. This process may be in part mediated by release of macrophage inhibitory cytokine-1 (MIC-1) by glioma stem cells [20].
n2:mentions: n3:8177493

Subject Item: _:vb23859427
rdf:type: n2:Context
rdf:value: This process may be in part mediated by release of macrophage inhibitory cytokine-1 (MIC-1) by glioma stem cells [>>20<<].
n2:mentions: n3:20667896

Subject Item: _:vb23859428
rdf:type: n4:Section
dc:title: chemoattraction
n4:contains: _:vb23859429 _:vb23859430 _:vb23859431 _:vb23859436 _:vb23859437 _:vb23859432 _:vb23859433 _:vb23859434 _:vb23859435

Subject Item: _:vb23859429
rdf:type: n2:Context
rdf:value: (collectively referred to as GAMs here) compose approximately 30% of tumor inflammatory cells and are actively recruited by gliomas through secretion of a variety of factors including chemokines, cytokines, and matrix proteins [>>9<<–13]. Among chemokine pathways involved in TAM chemoattraction, CCL2 (monocyte chemotactic protein-1 (MCP-1)) was among the first identified in gliomas [14].
n2:mentions: n3:22294205 n3:20184883 n3:21894147 n3:19424580 n3:10232541

Subject Item: _:vb23859430
rdf:type: n2:Context
rdf:value: Among chemokine pathways involved in TAM chemoattraction, CCL2 (monocyte chemotactic protein-1 (MCP-1)) was among the first identified in gliomas [>>14<<]. Although CCL2 expression can be induced by a variety of stimuli and cytokines, mechanisms responsible for its baseline expression by gliomas are being studied. Adenosine-5′-triphosphate (ATP), for example, was shown to stimulate the
n2:mentions: n3:7517920

Subject Item: _:vb23859431
rdf:type: n2:Context
rdf:value: A direct correlation between the percentage of GAMs and MCP-3 expression levels has also been demonstrated in human gliomas, suggesting MCP-3 to also participate in microglia/macrophages chemoattraction [>>12<<].
n2:mentions: n3:19424580

Subject Item: _:vb23859432
rdf:type: n2:Context
rdf:value: Stromal-derived (SDF-1) factor-1 is another chemokine that has been shown to promote microglia/macrophage trafficking in gliomas [>>17<<]. Trying to recapitulate neuropathological features of human high-grade glioma, Wang et al. established a new murine brain tumor model, ALTS1C1, which expresses high levels of SDF-1.
n2:mentions: n3:20179352

Subject Item: _:vb23859433
rdf:type: n2:Context
rdf:value: in the SDF-knockdown tumor was higher in nonhypoxic than in hypoxic regions, suggesting that SDF-1 production by tumor cells might be crucial for the accumulation of microglia/macrophages into areas of hypoxia and tumor invasiveness [>>13<<].
n2:mentions: n3:21894147

Subject Item: _:vb23859434
rdf:type: n2:Context
rdf:value: Synergistically, microglia stimulate glioma cell invasion through epidermal growth factor receptor (EGFR) activation [>>10<<]. Further, in response to glioma cells, microglia express tumor necrosis factor receptor of mouse embryo (TROY) that drives microglia migration towards glioma cells [18]. Also, the chemokine CX3CL1 expressed in glioblastoma cells promotes
n2:mentions: n3:22294205

Subject Item: _:vb23859435
rdf:type: n2:Context
rdf:value: expressed in glioblastoma cells promotes recruitment of human microglia/macrophages through its receptor CX3CR1 and enhances the expression of matrix metalloproteases 2, 9, and 14 in these cells, possibly promoting tumor invasion [>>11<<].
n2:mentions: n3:20184883

Subject Item: _:vb23859436
rdf:type: n2:Context
rdf:value: The former promote microglia migration through chemokines CCL5, vascular endothelial growth factor (VEGF) and neurotensin (NTS) release [>>19<<], while conditioned medium from the latter was shown to induce the migration of human monocytes [20].
n2:mentions: n3:21056915

Subject Item: _:vb23859437
rdf:type: n2:Context
rdf:value: The former promote microglia migration through chemokines CCL5, vascular endothelial growth factor (VEGF) and neurotensin (NTS) release [19], while conditioned medium from the latter was shown to induce the migration of human monocytes [>>20<<].
n2:mentions: n3:20667896

Subject Item: _:vb23859438
rdf:type: n4:Section
dc:title: promotion of tumor growth and invasion
n4:contains: _:vb23859448 _:vb23859449 _:vb23859444 _:vb23859445 _:vb23859446 _:vb23859447 _:vb23859440 _:vb23859441 _:vb23859442 _:vb23859443 _:vb23859439

Subject Item: _:vb23859439
rdf:type: n2:Context
rdf:value: Interestingly, primary microglia cells cocultured with glioma cells drastically increased the secretion of TGF-β1 [>>26<<]. More recently, another research group confirmed that the TGF-β1 released by microglia/macrophages enhances the invasive capacity of the CD133+ glioma cells (glioma stem-like cells) more than the CD133− committed cells, and that this
n2:mentions: n3:17684491

Subject Item: _:vb23859440
rdf:type: n2:Context
rdf:value: This occurs through the increase of MMP-2 expression and activity and the decrease of the tissue inhibitor of metalloprotease-2 (TIMP-2) in microglia-treated cells [>>28<<]. Markovic and colleagues have elegantly shown that membrane type I metalloprotease (MT1-MMP) is upregulated in GAMs and that the tumor itself induces the expression and activity of MT1-MMP [29]. This microglial metalloprotease in turn
n2:mentions: n3:19770485

Subject Item: _:vb23859441
rdf:type: n2:Context
rdf:value: Markovic and colleagues have elegantly shown that membrane type I metalloprotease (MT1-MMP) is upregulated in GAMs and that the tumor itself induces the expression and activity of MT1-MMP [>>29<<]. This microglial metalloprotease in turn seems to activate MMP-2 in gliomas, leading to even higher tumor invasiveness [29]. GAMs also express CX3CR1 and, in response to CX3CL1, increase their adhesion, migration, and expression of
n2:mentions: n3:19617536

Subject Item: _:vb23859442
rdf:type: n2:Context
rdf:value: This microglial metalloprotease in turn seems to activate MMP-2 in gliomas, leading to even higher tumor invasiveness [>>29<<]. GAMs also express CX3CR1 and, in response to CX3CL1, increase their adhesion, migration, and expression of MMP-2, -9, and -14 [11].
n2:mentions: n3:19617536

Subject Item: _:vb23859443
rdf:type: n2:Context
rdf:value: GAMs also express CX3CR1 and, in response to CX3CL1, increase their adhesion, migration, and expression of MMP-2, -9, and -14 [>>11<<].
n2:mentions: n3:20184883

Subject Item: _:vb23859444
rdf:type: n2:Context
rdf:value: Overexpression of CCL2 in the U87 glioma cell line was recently shown to enhance its invasiveness in a three-dimensional collagen matrix when these cells were cocultured with microglia (which express the CCL2 receptor CCR2) [>>30<<]. Furthermore, levels of IL-6 were increased in the coculture medium, and the expression of IL-6 in situ corresponded to the microglia/macrophages. Also, incubation of the glioma cells with recombinant IL-6 significantly increased their
n2:mentions: n3:22159219

Subject Item: _:vb23859445
rdf:type: n2:Context
rdf:value: These findings suggest that gliomas exploit microglia/macrophages through a CCL2/CCR2/IL-6 loop to increase their invasion and migration [>>30<<]. Intense angiogenesis is another hallmark of malignant gliomas whereby these tumors obtain essential nutrients and oxygen [31]. Loss of Flt-1, a VEGF receptor, signaling in microglia/macrophages leads to a decrease in tumor growth and
n2:mentions: n3:22159219

Subject Item: _:vb23859446
rdf:type: n2:Context
rdf:value: Intense angiogenesis is another hallmark of malignant gliomas whereby these tumors obtain essential nutrients and oxygen [>>31<<]. Loss of Flt-1, a VEGF receptor, signaling in microglia/macrophages leads to a decrease in tumor growth and vessel density, confirming an active role of microglia/macrophages in glioma angiogenesis [32].
n2:mentions: n3:17643088

Subject Item: _:vb23859447
rdf:type: n2:Context
rdf:value: Loss of Flt-1, a VEGF receptor, signaling in microglia/macrophages leads to a decrease in tumor growth and vessel density, confirming an active role of microglia/macrophages in glioma angiogenesis [>>32<<].
n2:mentions: n3:18794121

Subject Item: _:vb23859448
rdf:type: n2:Context
rdf:value: Moreover, this proliferative effect was specific to brain macrophages, since conditioned medium from peritoneal macrophages was unable to induce glioma cells growth [>>33<<]. As previously discussed, glioma and microglia interactions mediated through EGF and CSF-1 can also increase tumor invasion [10].
n2:mentions: n3:22062133

Subject Item: _:vb23859449
rdf:type: n2:Context
rdf:value: As previously discussed, glioma and microglia interactions mediated through EGF and CSF-1 can also increase tumor invasion [>>10<<].
n2:mentions: n3:22294205

Subject Item: _:vb23859450
rdf:type: n4:Section
dc:title: promising new therapies
n4:contains: _:vb23859452 _:vb23859453 _:vb23859454 _:vb23859455 _:vb23859451 _:vb23859468 _:vb23859469 _:vb23859470 _:vb23859464 _:vb23859465 _:vb23859466 _:vb23859467 _:vb23859460 _:vb23859461 _:vb23859462 _:vb23859463 _:vb23859456 _:vb23859457 _:vb23859458 _:vb23859459

Subject Item: _:vb23859451
rdf:type: n2:Context
rdf:value: Our group showed that conditioned medium from glioma cells increased STAT3 activity in microglia cells, resulting in overexpression of IL-6 and IL-10 and downregulation of IL-1β [>>34<<]. When STAT3 was inhibited in vitro by a pharmacological agent or small interfering RNA (siRNA), the expression profile of these cytokines was reversed. Moreover, silencing of STAT3 in a murine glioma model resulted in
n2:mentions: n3:19306372

Subject Item: _:vb23859452
rdf:type: n2:Context
rdf:value: Moreover, silencing of STAT3 in a murine glioma model resulted in microglia/macrophages activation and tumor growth inhibition [>>34<<]. Likewise, corosolic and oleanolic acids have been shown to suppress STAT3 in macrophages [35, 36]. These compounds also inhibited the expression of CD163, a marker of the M2 phenotype and the secretion of IL-10 in human macrophages,
n2:mentions: n3:19306372

Subject Item: _:vb23859453
rdf:type: n2:Context
rdf:value: Likewise, corosolic and oleanolic acids have been shown to suppress STAT3 in macrophages [>>35<<, 36]. These compounds also inhibited the expression of CD163, a marker of the M2 phenotype and the secretion of IL-10 in human macrophages, suggesting that they could potentially be used to suppress the M2 polarization of
n2:mentions: n3:21073634

Subject Item: _:vb23859454
rdf:type: n2:Context
rdf:value: Likewise, corosolic and oleanolic acids have been shown to suppress STAT3 in macrophages [35, >>36<<]. These compounds also inhibited the expression of CD163, a marker of the M2 phenotype and the secretion of IL-10 in human macrophages, suggesting that they could potentially be used to suppress the M2 polarization of
n2:mentions: n3:21922144

Subject Item: _:vb23859455
rdf:type: n2:Context
rdf:value: compounds also inhibited the expression of CD163, a marker of the M2 phenotype and the secretion of IL-10 in human macrophages, suggesting that they could potentially be used to suppress the M2 polarization of microglia/macrophages [>>35<<, 36].
n2:mentions: n3:21073634

Subject Item: _:vb23859456
rdf:type: n2:Context
rdf:value: compounds also inhibited the expression of CD163, a marker of the M2 phenotype and the secretion of IL-10 in human macrophages, suggesting that they could potentially be used to suppress the M2 polarization of microglia/macrophages [35, >>36<<].
n2:mentions: n3:21922144

Subject Item: _:vb23859457
rdf:type: n2:Context
rdf:value: Systemic administration of neutralizing antibody against CCL2 significantly inhibits the infiltration of microglia/macrophages in mice bearing gliomas [>>37<<]. Furthermore, the combination of anti-CCL2 therapy with chemotherapy (temozolomide) significantly prolonged the survival of mice, suggesting a possible new therapeutic approach [37]. Furthermore, antiphosphatidylserine antibody combined
n2:mentions: n3:21116835

Subject Item: _:vb23859458
rdf:type: n2:Context
rdf:value: Furthermore, the combination of anti-CCL2 therapy with chemotherapy (temozolomide) significantly prolonged the survival of mice, suggesting a possible new therapeutic approach [>>37<<]. Furthermore, antiphosphatidylserine antibody combined with irradiation was also investigated in a rat model of glioblastoma. Antiphosphatidylserine binds to tumor vascular cells exposing phosphatidylserine in response to irradiation and
n2:mentions: n3:21116835

Subject Item: _:vb23859459
rdf:type: n2:Context
rdf:value: This resulted in the death of tumor cells through starvation and significantly increased the median survival time of tumor-bearing animals [>>38<<].
n2:mentions: n3:19887482

Subject Item: _:vb23859460
rdf:type: n2:Context
rdf:value: Carbon nanotubes (CNTs) and cyclodextrin-based polymer are semiselectively taken up by GAMs with no toxicity [>>39<<, 40]. These nanoparticles can be used to enhance the uptake of CpG oligonucleotides, an agonist of toll-like receptor 9 (TLR-9), by glioma-associated inflammatory cells. This strategy was used to overcome the local tumor immunosuppression
n2:mentions: n3:19836468

Subject Item: _:vb23859461
rdf:type: n2:Context
rdf:value: Carbon nanotubes (CNTs) and cyclodextrin-based polymer are semiselectively taken up by GAMs with no toxicity [39, >>40<<]. These nanoparticles can be used to enhance the uptake of CpG oligonucleotides, an agonist of toll-like receptor 9 (TLR-9), by glioma-associated inflammatory cells. This strategy was used to overcome the local tumor immunosuppression and
n2:mentions: n3:19181390

Subject Item: _:vb23859462
rdf:type: n2:Context
rdf:value: This strategy was used to overcome the local tumor immunosuppression and eradicated gliomas in mice models [>>41<<].
n2:mentions: n3:21088258

Subject Item: _:vb23859463
rdf:type: n2:Context
rdf:value: Microglia/macrophages may also function as delivery vehicle into brain tumors [>>43<<]. Baek and colleagues reported using murine macrophages as carriers of nanoshells (NS) into gliomas for photothermal ablation.
n2:mentions: n3:21387452

Subject Item: _:vb23859464
rdf:type: n2:Context
rdf:value: NS composition efficiently converts absorbed near-infrared light (NIR) into heat and exposure of glioma spheroids infiltrated with NS-loaded macrophages to NIR laser resulted in complete tumor growth inhibition [>>44<<].
n2:mentions: n3:21221712

Subject Item: _:vb23859465
rdf:type: n2:Context
rdf:value: Besides, the inhibition of p38 MAPK was also shown to reduce the secretion of pro-inflammatory cytokines from microglia and tumor cells, resulting in a decrease of glioma migration [>>46<<]. Moreover, systemic administration of cyclosporine A (CsA) was shown to decrease glioma growth and angiogenesis by inhibiting microglia/macrophages infiltration by inducing cell death and blocking the expression and activity of important
n2:mentions: n3:22528800

Subject Item: _:vb23859466
rdf:type: n2:Context
rdf:value: (PPF), an atypical methylxanthine and glial modulating agent with anti-inflammatory actions, was also shown to be effective in reducing glioma growth by targeting microglia and possibly decreasing their expression of MMP-9 [>>48<<].
n2:mentions: n3:22086978

Subject Item: _:vb23859467
rdf:type: n2:Context
rdf:value: Other immunotherapy approaches that target GAMs include stimulation of microglia by IL-12 to increase their phagocytic activity and TNF-related apoptosis inducing ligand (TRAIL) release [>>49<<]. Also, stimulation of human GAMs by the TLR3 agonist poly(I:C) results in tumor cell death and inhibition of tumor cell growth and invasion [50].
n2:mentions: n3:21399879

Subject Item: _:vb23859468
rdf:type: n2:Context
rdf:value: Also, stimulation of human GAMs by the TLR3 agonist poly(I:C) results in tumor cell death and inhibition of tumor cell growth and invasion [>>50<<]. Finally, because microglia/macrophages express folate receptor β (FRβ), a recombinant immunotoxin to FRβ has been used to deplete GAMs in order to decrease tumor growth [51].
n2:mentions: n3:22015597

Subject Item: _:vb23859469
rdf:type: n2:Context
rdf:value: Finally, because microglia/macrophages express folate receptor β (FRβ), a recombinant immunotoxin to FRβ has been used to deplete GAMs in order to decrease tumor growth [>>51<<].
n2:mentions: n3:19238383

Subject Item: _:vb23859470
rdf:type: n2:Context
rdf:value: Interestingly, depletion of microglia cells abolished the effect of the α5β1 inhibitor on glioma invasion, suggesting that the α5β1 integrin promotes tumor development through interactions with microglia [>>52<<].
n2:mentions: n3:18804537

Subject Item: _:vb527785884
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