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n2:pmcid: PMC0
bibo:doi: 10.1371%2Fjournal.pone.0094281
n9:contains: _:vb30259828 _:vb30259819 _:vb30259805 _:vb30259780

Subject Item: _:vb30259780
rdf:type: n9:Section
dc:title: introduction
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Subject Item: _:vb30259781
rdf:type: n2:Context
rdf:value: Despite multimodal therapy including maximal surgical resection, radiation, and temozolomide (TMZ), the median overall survival is less than 15 months [>>1<<]. Moreover, these therapies are non-specific and are ultimately limited by toxicity to normal tissues [2]. In contrast, immunotherapy promises an exquisitely precise approach, and substantial evidence suggests that T cells can eradicate
n2:mentions: n3:15758009

Subject Item: _:vb30259782
rdf:type: n2:Context
rdf:value: Moreover, these therapies are non-specific and are ultimately limited by toxicity to normal tissues [>>2<<]. In contrast, immunotherapy promises an exquisitely precise approach, and substantial evidence suggests that T cells can eradicate large, well-established tumors in mice and humans [3]–[7].
n2:mentions: n3:2178330

Subject Item: _:vb30259783
rdf:type: n2:Context
rdf:value: In contrast, immunotherapy promises an exquisitely precise approach, and substantial evidence suggests that T cells can eradicate large, well-established tumors in mice and humans [>>3<<]–[7].
n2:mentions: n3:19451549

Subject Item: _:vb30259784
rdf:type: n2:Context
rdf:value: In contrast, immunotherapy promises an exquisitely precise approach, and substantial evidence suggests that T cells can eradicate large, well-established tumors in mice and humans [3]–[>>7<<].
n2:mentions: n3:22160384

Subject Item: _:vb30259785
rdf:type: n2:Context
rdf:value: cells regardless of major histocompatibility complex (MHC) presentation of target antigen or MHC downregulation in tumors, factors which allow tumor-escape from treatment with ex vivo expanded tumor-infiltrating lymphocytes (TILs) [>>8<<] and T-cell receptor (TCR) gene therapy [9], [10].
n2:mentions: n3:12973027

Subject Item: _:vb30259786
rdf:type: n2:Context
rdf:value: complex (MHC) presentation of target antigen or MHC downregulation in tumors, factors which allow tumor-escape from treatment with ex vivo expanded tumor-infiltrating lymphocytes (TILs) [8] and T-cell receptor (TCR) gene therapy [>>9<<], [10]. Clinical trials utilizing CARs in other tumor systems including renal cell carcinoma [11], indolent B-cell and mantle cell lymphoma [12], neuroblastoma [13], acute lymphoblastic leukemia [14], and chronic lymphoid leukemia [15]
n2:mentions: n3:16977338

Subject Item: _:vb30259787
rdf:type: n2:Context
rdf:value: complex (MHC) presentation of target antigen or MHC downregulation in tumors, factors which allow tumor-escape from treatment with ex vivo expanded tumor-infiltrating lymphocytes (TILs) [8] and T-cell receptor (TCR) gene therapy [9], [>>10<<]. Clinical trials utilizing CARs in other tumor systems including renal cell carcinoma [11], indolent B-cell and mantle cell lymphoma [12], neuroblastoma [13], acute lymphoblastic leukemia [14], and chronic lymphoid leukemia [15] have
n2:mentions: n3:23890063

Subject Item: _:vb30259788
rdf:type: n2:Context
rdf:value: Clinical trials utilizing CARs in other tumor systems including renal cell carcinoma [>>11<<], indolent B-cell and mantle cell lymphoma [12], neuroblastoma [13], acute lymphoblastic leukemia [14], and chronic lymphoid leukemia [15] have verified their remarkable potential.
n2:mentions: n3:16648493

Subject Item: _:vb30259789
rdf:type: n2:Context
rdf:value: Clinical trials utilizing CARs in other tumor systems including renal cell carcinoma [11], indolent B-cell and mantle cell lymphoma [>>12<<], neuroblastoma [13], acute lymphoblastic leukemia [14], and chronic lymphoid leukemia [15] have verified their remarkable potential.
n2:mentions: n3:22308288

Subject Item: _:vb30259790
rdf:type: n2:Context
rdf:value: Clinical trials utilizing CARs in other tumor systems including renal cell carcinoma [11], indolent B-cell and mantle cell lymphoma [12], neuroblastoma [>>13<<], acute lymphoblastic leukemia [14], and chronic lymphoid leukemia [15] have verified their remarkable potential.
n2:mentions: n3:18978797

Subject Item: _:vb30259791
rdf:type: n2:Context
rdf:value: Clinical trials utilizing CARs in other tumor systems including renal cell carcinoma [11], indolent B-cell and mantle cell lymphoma [12], neuroblastoma [13], acute lymphoblastic leukemia [14], and chronic lymphoid leukemia [>>15<<] have verified their remarkable potential.
n2:mentions: n3:21830940

Subject Item: _:vb30259792
rdf:type: n2:Context
rdf:value: However, severe adverse events, including patient deaths, have occurred from administration of CAR T cells when directed against tumor antigens simultaneously expressed on normal tissues [>>16<<], [17].
n2:mentions: n3:20357779

Subject Item: _:vb30259793
rdf:type: n2:Context
rdf:value: However, severe adverse events, including patient deaths, have occurred from administration of CAR T cells when directed against tumor antigens simultaneously expressed on normal tissues [16], [>>17<<].
n2:mentions: n3:20179677

Subject Item: _:vb30259794
rdf:type: n2:Context
rdf:value: variant of the epidermal growth factor receptor, EGFRvIII, is a type III in-frame deletion mutant of the wild-type receptor that is exclusively expressed on the cell surface of GBMs and other neoplasms but is absent on normal tissues [>>18<<]–[20]. Unlike previous CARs, an EGFRvIII-specific construct carries the potential to eliminate tumor cells without damaging normal tissue due to the tumor specificity of its target antigen.
n2:mentions: n3:7606735

Subject Item: _:vb30259795
rdf:type: n2:Context
rdf:value: of the epidermal growth factor receptor, EGFRvIII, is a type III in-frame deletion mutant of the wild-type receptor that is exclusively expressed on the cell surface of GBMs and other neoplasms but is absent on normal tissues [18]–[>>20<<]. Unlike previous CARs, an EGFRvIII-specific construct carries the potential to eliminate tumor cells without damaging normal tissue due to the tumor specificity of its target antigen.
n2:mentions: n3:1557402

Subject Item: _:vb30259796
rdf:type: n2:Context
rdf:value: This dogma has since been challenged, as T cells are now known to infiltrate CNS parenchyma in the context of neuropathology and neuroinflammation where the blood brain barrier (BBB) is known to be disrupted [>>21<<], [22]. GBM in particular has been implicated in BBB dysfunction through its modulation of the local brain microenvironment, owing in part to both the inevitable disruption of natural brain architecture by bulky tumor masses and their
n2:mentions: n3:16550326

Subject Item: _:vb30259797
rdf:type: n2:Context
rdf:value: This dogma has since been challenged, as T cells are now known to infiltrate CNS parenchyma in the context of neuropathology and neuroinflammation where the blood brain barrier (BBB) is known to be disrupted [21], [>>22<<]. GBM in particular has been implicated in BBB dysfunction through its modulation of the local brain microenvironment, owing in part to both the inevitable disruption of natural brain architecture by bulky tumor masses and their inherent
n2:mentions: n3:19664708

Subject Item: _:vb30259798
rdf:type: n2:Context
rdf:value: owing in part to both the inevitable disruption of natural brain architecture by bulky tumor masses and their inherent pathologic characteristics that increase the permeability of microvessels, thereby compromising BBB integrity [>>23<<]. While it is reasonable to suspect that T cells and chemotherapeutic agents may gain entry to tumor cores through these regions of increased permeability, the long-term therapeutic benefits of this rationale have been marred by the fact
n2:mentions: n3:12070669

Subject Item: _:vb30259799
rdf:type: n2:Context
rdf:value: have been marred by the fact that GBM is predisposed to the development of highly invasive neoplastic peninsulas that are removed from main tumor masses, residing within normal brain areas that are protected by regions of intact BBB [>>24<<]–[26]. This may explain the failure of therapeutic regimens that depend on BBB permeability for targeted treatment delivery, where main tumor cores are discriminately subjected to therapy while invasive tumor cells are able to evade
n2:mentions: n3:22339070

Subject Item: _:vb30259800
rdf:type: n2:Context
rdf:value: been marred by the fact that GBM is predisposed to the development of highly invasive neoplastic peninsulas that are removed from main tumor masses, residing within normal brain areas that are protected by regions of intact BBB [24]–[>>26<<]. This may explain the failure of therapeutic regimens that depend on BBB permeability for targeted treatment delivery, where main tumor cores are discriminately subjected to therapy while invasive tumor cells are able to evade clinical
n2:mentions: n3:8832660

Subject Item: _:vb30259801
rdf:type: n2:Context
rdf:value: that depend on BBB permeability for targeted treatment delivery, where main tumor cores are discriminately subjected to therapy while invasive tumor cells are able to evade clinical intervention and tumor recurrence becomes inevitable [>>27<<].
n2:mentions: n3:23014761

Subject Item: _:vb30259802
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rdf:value: Human tumor xenografts are often criticized due to their production of large, well-circumscribed, non-invasive intracranial masses (e.g. U87MG [>>29<<]–[31]), characteristics that impede their use as an adequate platform for evaluating novel therapies against GBM.
n2:mentions: n3:19585223

Subject Item: _:vb30259803
rdf:type: n2:Context
rdf:value: Human tumor xenografts are often criticized due to their production of large, well-circumscribed, non-invasive intracranial masses (e.g. U87MG [29]–[>>31<<]), characteristics that impede their use as an adequate platform for evaluating novel therapies against GBM.
n2:mentions: n3:17874037

Subject Item: _:vb30259804
rdf:type: n2:Context
rdf:value: D-270 MG is a tumor line derived directly from a patient’s primary GBM by direct orthotopic transplant and is known to naturally express EGFRvIII [>>32<<]. In order to monitor the in vivo efficacy of EGFRvIII+ CAR T cells against D-270 MG intracranial xenografts, we produced a cell line that co-expresses firefly luciferase (FLuc) and GFP, D-270MGFLuc/GFP, which retains the pathological
n2:mentions: n3:2253244

Subject Item: _:vb30259805
rdf:type: n9:Section
dc:title: materials and methods
n9:contains: _:vb30259806 _:vb30259807 _:vb30259808 _:vb30259809 _:vb30259810 _:vb30259811 _:vb30259812 _:vb30259813 _:vb30259814 _:vb30259815 _:vb30259816 _:vb30259817 _:vb30259818

Subject Item: _:vb30259806
rdf:type: n2:Context
rdf:value: We utilized the previously described human glioma cell line, U87MG [>>29<<]–[31], which does not express EGFRvIII, and subline U87MG.ΔEGFR [33], [34], which was stably transfected to express EGFRvIII.
n2:mentions: n3:19585223

Subject Item: _:vb30259807
rdf:type: n2:Context
rdf:value: We utilized the previously described human glioma cell line, U87MG [29]–[>>31<<], which does not express EGFRvIII, and subline U87MG.ΔEGFR [33], [34], which was stably transfected to express EGFRvIII.
n2:mentions: n3:17874037

Subject Item: _:vb30259808
rdf:type: n2:Context
rdf:value: We utilized the previously described human glioma cell line, U87MG [29]–[31], which does not express EGFRvIII, and subline U87MG.ΔEGFR [>>33<<], [34], which was stably transfected to express EGFRvIII.
n2:mentions: n3:8052651

Subject Item: _:vb30259809
rdf:type: n2:Context
rdf:value: ΔEGFR [33], [>>34<<], which was stably transfected to express EGFRvIII.
n2:mentions: n3:12067969

Subject Item: _:vb30259810
rdf:type: n2:Context
rdf:value: We also utilized the D-270 MG cell line, which was propagated directly as a xenograft from a primary human GBM harvested from a patient and has previously been shown to naturally express EGFRvIII [>>20<<], [32]. Briefly, mechanically minced tumor tissue was enzymatically dissociated into single cells using the Papain Dissociation System. After wash, tissue was homogenized and passed through a 75 μm cell strainer, re-suspended with freezing
n2:mentions: n3:1557402

Subject Item: _:vb30259811
rdf:type: n2:Context
rdf:value: We also utilized the D-270 MG cell line, which was propagated directly as a xenograft from a primary human GBM harvested from a patient and has previously been shown to naturally express EGFRvIII [20], [>>32<<]. Briefly, mechanically minced tumor tissue was enzymatically dissociated into single cells using the Papain Dissociation System. After wash, tissue was homogenized and passed through a 75 μm cell strainer, re-suspended with freezing
n2:mentions: n3:2253244

Subject Item: _:vb30259812
rdf:type: n2:Context
rdf:value: The EGFRvIII+ CAR and extGLuc retroviral vectors were utilized to generate EGFRvIII+ CAR T cells and exGluc+ EGFRvIII+ CAR T cells. The transduction procedures have previously been described [>>36<<], [45], [46].
n2:mentions: n3:19219023

Subject Item: _:vb30259813
rdf:type: n2:Context
rdf:value: The EGFRvIII+ CAR and extGLuc retroviral vectors were utilized to generate EGFRvIII+ CAR T cells and exGluc+ EGFRvIII+ CAR T cells. The transduction procedures have previously been described [36], [>>45<<], [46]. Briefly, peripheral blood mononuclear cells (PBMCs) from healthy donors and GBM patients (post-resection, prior to treatment) were thawed and cultured in AIM-V medium supplemented with 5% human AB serum, plus antibiotics, 300 IU/mL
n2:mentions: n3:15871677

Subject Item: _:vb30259814
rdf:type: n2:Context
rdf:value: The EGFRvIII+ CAR and extGLuc retroviral vectors were utilized to generate EGFRvIII+ CAR T cells and exGluc+ EGFRvIII+ CAR T cells. The transduction procedures have previously been described [36], [45], [>>46<<]. Briefly, peripheral blood mononuclear cells (PBMCs) from healthy donors and GBM patients (post-resection, prior to treatment) were thawed and cultured in AIM-V medium supplemented with 5% human AB serum, plus antibiotics, 300 IU/mL IL-2,
n2:mentions: n3:12960359

Subject Item: _:vb30259815
rdf:type: n2:Context
rdf:value: Transduced PBLs (or untransduced control PBLs from same donor) were expanded in vitro using rapid expansion protocol (REP) [>>47<<]. Briefly, T cells were cultured in complete AIM-V medium plus 10% human AB serum, 300 IU/mL IL-2, and 50 ng/mL OKT-3 in the presence of 100x excess 5000 rads irradiated allogeneic PBMC feeder cells, and allowed to expand 10–14 days.
n2:mentions: n3:1691237

Subject Item: _:vb30259816
rdf:type: n2:Context
rdf:value: Briefly, lentiviral vectors were generated by transient transfection of HEK 293T cells with a four-plasmid system [>>48<<]. Six hours post-transfection, plates were washed twice with phosphate-buffered saline (PBS) and 20 mL fresh medium was added. The supernatant was collected 30–48 hours post-transfection and cell debris was removed by centrifugation at
n2:mentions: n3:18496571

Subject Item: _:vb30259817
rdf:type: n2:Context
rdf:value: EGFRvIII expression levels by D-270MGFLuc/GFP and U87MG.ΔEGFR tumor cells were measured by qRT PCR as previously described [>>49<<].
n2:mentions: n3:18223223

Subject Item: _:vb30259818
rdf:type: n2:Context
rdf:value: Tumor growth was analyzed every three to five days for 26 days by BLI as previously described [>>51<<] until the study was terminated.
n2:mentions: n3:16462491

Subject Item: _:vb30259819
rdf:type: n9:Section
dc:title: results
n9:contains: _:vb30259820 _:vb30259821 _:vb30259822 _:vb30259823 _:vb30259824 _:vb30259825 _:vb30259826 _:vb30259827

Subject Item: _:vb30259820
rdf:type: n2:Context
rdf:value: EGFRvIII+ CAR T cells against invasive intracerebral GBM tumors, we utilized the D-270MGFLuc/GFP xenograft, which was isolated directly from a patient’s primary GBM tumor and has been previously validated to naturally express EGFRvIII [>>20<<], [32]. We first sought to histologically evaluate and compare the characteristic growth patterns of D-270MGFLuc/GFP tumor with U87MG.
n2:mentions: n3:1557402

Subject Item: _:vb30259821
rdf:type: n2:Context
rdf:value: CAR T cells against invasive intracerebral GBM tumors, we utilized the D-270MGFLuc/GFP xenograft, which was isolated directly from a patient’s primary GBM tumor and has been previously validated to naturally express EGFRvIII [20], [>>32<<]. We first sought to histologically evaluate and compare the characteristic growth patterns of D-270MGFLuc/GFP tumor with U87MG.
n2:mentions: n3:2253244

Subject Item: _:vb30259822
rdf:type: n2:Context
rdf:value: ΔEGFR, a xenograft derived from a previously described human glioma cell subline [>>33<<], [34] that is among the most frequently used models in preclinical studies of GBM.
n2:mentions: n3:8052651

Subject Item: _:vb30259823
rdf:type: n2:Context
rdf:value: ΔEGFR, a xenograft derived from a previously described human glioma cell subline [33], [>>34<<] that is among the most frequently used models in preclinical studies of GBM.
n2:mentions: n3:12067969

Subject Item: _:vb30259824
rdf:type: n2:Context
rdf:value: transduced them with a previously-described retrovirus encoding a third-generation EGFRvIII+ CAR containing the humanized 139 anti-human EGFRvIII single-chain variable fragment in tandem with the hCD28-41BB-CD3æ chain signaling domain [>>35<<]. Following transduction, we determined surface expression by flow cytometry, and T cells were found to efficiently express the EGFRvIII+ CAR construct on their cell surface ( Fig.
n2:mentions: n3:22780919

Subject Item: _:vb30259825
rdf:type: n2:Context
rdf:value: rarely metastasize outside of the brain, instead shedding neoplastic cells that migrate away from main tumor cores and develop into highly invasive peninsulas residing within the normal brain, hiding within regions of intact BBB [>>24<<]–[26]. Although T cells are able to access bulky GBM lesions through dysfunction of the local BBB, it is unknown if they can effectively migrate into the invading tumor deposits that may reside behind an intact BBB.
n2:mentions: n3:22339070

Subject Item: _:vb30259826
rdf:type: n2:Context
rdf:value: rarely metastasize outside of the brain, instead shedding neoplastic cells that migrate away from main tumor cores and develop into highly invasive peninsulas residing within the normal brain, hiding within regions of intact BBB [24]–[>>26<<]. Although T cells are able to access bulky GBM lesions through dysfunction of the local BBB, it is unknown if they can effectively migrate into the invading tumor deposits that may reside behind an intact BBB.
n2:mentions: n3:8832660

Subject Item: _:vb30259827
rdf:type: n2:Context
rdf:value: this, human donor PBLs were transduced with the external Gaussian luciferase (extGLuc) retrovirus or underwent a dual transduction with both the extGLuc and EGFRvIII+ CAR retroviruses for use in bioluminescence imaging (BLI) analysis [>>36<<]. Following transduction, T cells were cultured in vitro prior to systemic infusion into NSG mice bearing established orthotopic D-270MGFLuc/GFP tumors.
n2:mentions: n3:19219023

Subject Item: _:vb30259828
rdf:type: n9:Section
dc:title: discussion
n9:contains: _:vb30259829 _:vb30259830 _:vb30259831 _:vb30259836 _:vb30259837 _:vb30259838 _:vb30259839 _:vb30259832 _:vb30259833 _:vb30259834 _:vb30259835 _:vb30259840

Subject Item: _:vb30259829
rdf:type: n2:Context
rdf:value: The therapeutic benefits of CAR-based adoptive cell therapy have been widely demonstrated in patients suffering with cancer [>>7<<], [13]–[15]. Since its introduction, CAR design has evolved significantly to mediate a potent and robust T-cell immune response when directed against tumors in the periphery [6], [37].
n2:mentions: n3:22160384

Subject Item: _:vb30259830
rdf:type: n2:Context
rdf:value: The therapeutic benefits of CAR-based adoptive cell therapy have been widely demonstrated in patients suffering with cancer [7], [>>13<<]–[15]. Since its introduction, CAR design has evolved significantly to mediate a potent and robust T-cell immune response when directed against tumors in the periphery [6], [37].
n2:mentions: n3:18978797

Subject Item: _:vb30259831
rdf:type: n2:Context
rdf:value: The therapeutic benefits of CAR-based adoptive cell therapy have been widely demonstrated in patients suffering with cancer [7], [13]–[>>15<<]. Since its introduction, CAR design has evolved significantly to mediate a potent and robust T-cell immune response when directed against tumors in the periphery [6], [37].
n2:mentions: n3:21830940

Subject Item: _:vb30259832
rdf:type: n2:Context
rdf:value: Since its introduction, CAR design has evolved significantly to mediate a potent and robust T-cell immune response when directed against tumors in the periphery [>>6<<], [37]. Importantly, we demonstrate here that similar immune responses can be achieved against established tumors in the immunologically privileged brain, even when directed against highly invasive cancers that are considered prone to
n2:mentions: n3:21808266

Subject Item: _:vb30259833
rdf:type: n2:Context
rdf:value: Since its introduction, CAR design has evolved significantly to mediate a potent and robust T-cell immune response when directed against tumors in the periphery [6], [>>37<<]. Importantly, we demonstrate here that similar immune responses can be achieved against established tumors in the immunologically privileged brain, even when directed against highly invasive cancers that are considered prone to immune
n2:mentions: n3:23550147

Subject Item: _:vb30259834
rdf:type: n2:Context
rdf:value: However, we chose the assay conditions described here since incubation times>18 h decrease cell viability, and 18 h incubations have yielded consistent results to date [>>38<<].
n2:mentions: n3:24054399

Subject Item: _:vb30259835
rdf:type: n2:Context
rdf:value: T-cell migration across endothelium requires molecular cues provided by chemokine-chemokine receptor interaction and engagement of adhesion molecules, which are thought to be independent of TCR engagement [>>39<<], [40]. The cross-reactivity of murine adhesion molecules and chemokines with human T cells and their chemokine receptors is known to be limited [41], and although this could have negatively impacted T-cell localization, we instead
n2:mentions: n3:22926201

Subject Item: _:vb30259836
rdf:type: n2:Context
rdf:value: T-cell migration across endothelium requires molecular cues provided by chemokine-chemokine receptor interaction and engagement of adhesion molecules, which are thought to be independent of TCR engagement [39], [>>40<<]. The cross-reactivity of murine adhesion molecules and chemokines with human T cells and their chemokine receptors is known to be limited [41], and although this could have negatively impacted T-cell localization, we instead observed a
n2:mentions: n3:19836265

Subject Item: _:vb30259837
rdf:type: n2:Context
rdf:value: The cross-reactivity of murine adhesion molecules and chemokines with human T cells and their chemokine receptors is known to be limited [>>41<<], and although this could have negatively impacted T-cell localization, we instead observed a substantial influx of T cells into the invasive tumor.
n2:mentions: n3:14978070

Subject Item: _:vb30259838
rdf:type: n2:Context
rdf:value: This explanation would be consistent with two recent clinical studies where recurrence in patients treated with CARs [>>42<<] or a vaccine targeting a single antigen [43] was characterized by outgrowth of antigen-loss variants.
n2:mentions: n3:23527958

Subject Item: _:vb30259839
rdf:type: n2:Context
rdf:value: This explanation would be consistent with two recent clinical studies where recurrence in patients treated with CARs [42] or a vaccine targeting a single antigen [>>43<<] was characterized by outgrowth of antigen-loss variants.
n2:mentions: n3:20921459

Subject Item: _:vb30259840
rdf:type: n2:Context
rdf:value: may include determining factors involved in eliciting broader endogenous immune responses through mechanisms such as epitope spreading, which has emerged as a critical factor during clinical trials of immunotherapy for melanoma [>>44<<].
n2:mentions: n3:12631598

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