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n3:pmcid: PMC0
bibo:doi: 10.1038%2Fmt.2013.185
n5:contains: _:vb24402551 _:vb24402532 _:vb24402542 _:vb24402521

Subject Item: _:vb24402521
rdf:type: n5:Section
dc:title: introduction
n5:contains: _:vb24402522 _:vb24402523 _:vb24402524 _:vb24402525 _:vb24402526 _:vb24402527 _:vb24402528 _:vb24402529 _:vb24402530 _:vb24402531

Subject Item: _:vb24402522
rdf:type: n3:Context
rdf:value: all primary brain tumors in adults and is virtually incurable. With the combination of radical surgery, radiotherapy, and adjuvant temozolomide, the 5-year overall survival rate is <5% and treatment-related complications are debilitating.>>1<<,2 Immunotherapy is emerging as an alternative approach that could potentially overcome these limitations of the current standard therapy.
n3:mentions: n2:15758009

Subject Item: _:vb24402523
rdf:type: n3:Context
rdf:value: primary brain tumors in adults and is virtually incurable. With the combination of radical surgery, radiotherapy, and adjuvant temozolomide, the 5-year overall survival rate is <5% and treatment-related complications are debilitating.1,>>2<< Immunotherapy is emerging as an alternative approach that could potentially overcome these limitations of the current standard therapy.
n3:mentions: n2:19269895

Subject Item: _:vb24402524
rdf:type: n3:Context
rdf:value: therapies with chimeric antigen receptor (CAR) expressing T cells have recently had substantial successes in the treatment of chronic lymphocytic leukemia, acute lymphoblastic leukemia, and neuroblastoma in first-in-man clinical trials.>>3<<,4,5,6 In preclinical models of GBM, CAR T cells have shown robust antitumor activity and are currently being investigated in phase I/II studies that target the glioma-restricted antigens IL-13Rα2, HER2, and EGFR.
n3:mentions: n2:21830940

Subject Item: _:vb24402525
rdf:type: n3:Context
rdf:value: therapies with chimeric antigen receptor (CAR) expressing T cells have recently had substantial successes in the treatment of chronic lymphocytic leukemia, acute lymphoblastic leukemia, and neuroblastoma in first-in-man clinical trials.3,>>4<<,5,6 In preclinical models of GBM, CAR T cells have shown robust antitumor activity and are currently being investigated in phase I/II studies that target the glioma-restricted antigens IL-13Rα2, HER2, and EGFR.
n3:mentions: n2:18978797

Subject Item: _:vb24402526
rdf:type: n3:Context
rdf:value: with chimeric antigen receptor (CAR) expressing T cells have recently had substantial successes in the treatment of chronic lymphocytic leukemia, acute lymphoblastic leukemia, and neuroblastoma in first-in-man clinical trials.3,4,>>5<<,6 In preclinical models of GBM, CAR T cells have shown robust antitumor activity and are currently being investigated in phase I/II studies that target the glioma-restricted antigens IL-13Rα2, HER2, and EGFR.
n3:mentions: n2:23527958

Subject Item: _:vb24402527
rdf:type: n3:Context
rdf:value: by employing a number of antigen-evasion strategies including antigen mutation, downregulation/deletion of target antigens, and selective survival of antigen-negative tumor subpopulations that could well be selected by therapy.>>10<<,11,12 These concerns are particularly relevant to GBM, which is known to be heterogeneous with varying antigen expression profile within single tumors and between patients.
n3:mentions: n2:15032581

Subject Item: _:vb24402528
rdf:type: n3:Context
rdf:value: by employing a number of antigen-evasion strategies including antigen mutation, downregulation/deletion of target antigens, and selective survival of antigen-negative tumor subpopulations that could well be selected by therapy.10,>>11<<,12 These concerns are particularly relevant to GBM, which is known to be heterogeneous with varying antigen expression profile within single tumors and between patients.
n3:mentions: n2:17603493

Subject Item: _:vb24402529
rdf:type: n3:Context
rdf:value: by employing a number of antigen-evasion strategies including antigen mutation, downregulation/deletion of target antigens, and selective survival of antigen-negative tumor subpopulations that could well be selected by therapy.10,11,>>12<< These concerns are particularly relevant to GBM, which is known to be heterogeneous with varying antigen expression profile within single tumors and between patients.
n3:mentions: n2:17129181

Subject Item: _:vb24402530
rdf:type: n3:Context
rdf:value: tumor subpopulations that could well be selected by therapy.10,11,12 These concerns are particularly relevant to GBM, which is known to be heterogeneous with varying antigen expression profile within single tumors and between patients.>>13<<,14 Targeting multiple tumor-restricted antigens could therefore offset these potential escape mechanisms.
n3:mentions: n2:17255279

Subject Item: _:vb24402531
rdf:type: n3:Context
rdf:value: subpopulations that could well be selected by therapy.10,11,12 These concerns are particularly relevant to GBM, which is known to be heterogeneous with varying antigen expression profile within single tumors and between patients.13,>>14<< Targeting multiple tumor-restricted antigens could therefore offset these potential escape mechanisms.
n3:mentions: n2:15827123

Subject Item: _:vb24402532
rdf:type: n5:Section
dc:title: materials and methods
n5:contains: _:vb24402533 _:vb24402534 _:vb24402535 _:vb24402540 _:vb24402541 _:vb24402536 _:vb24402537 _:vb24402538 _:vb24402539

Subject Item: _:vb24402533
rdf:type: n3:Context
rdf:value: Generation of retroviral constructs. The construction of the HER2-specific CAR (pSFG.FRP5.CD28.ζ) has been previously described.>>26<<,27,28 The construction of the IL-13Rα2-specific CAR is described in detail elsewhere (Krebs et al. submitted for publication).
n3:mentions: n2:20068073

Subject Item: _:vb24402534
rdf:type: n3:Context
rdf:value: Generation of retroviral constructs. The construction of the HER2-specific CAR (pSFG.FRP5.CD28.ζ) has been previously described.26,>>27<<,28 The construction of the IL-13Rα2-specific CAR is described in detail elsewhere (Krebs et al. submitted for publication).
n3:mentions: n2:17575166

Subject Item: _:vb24402535
rdf:type: n3:Context
rdf:value: Generation of retroviral constructs. The construction of the HER2-specific CAR (pSFG.FRP5.CD28.ζ) has been previously described.26,27,>>28<< The construction of the IL-13Rα2-specific CAR is described in detail elsewhere (Krebs et al. submitted for publication).
n3:mentions: n2:19532139

Subject Item: _:vb24402536
rdf:type: n3:Context
rdf:value: publication). Briefly, an IL-13 mutein with enhanced affinity to IL-13Rα2 was subcloned into a SFG retroviral vector containing an expression cassette encoding a CH2CH3 domain, a CD28 transmembrane domain, and a CD28.ζ signaling domain.>>45<<,46 For in vivo studies, a retroviral vector encoding the fusion protein eGFP-Firefly Luciferase (eGFP.
n3:mentions: n2:15068667

Subject Item: _:vb24402537
rdf:type: n3:Context
rdf:value: Briefly, an IL-13 mutein with enhanced affinity to IL-13Rα2 was subcloned into a SFG retroviral vector containing an expression cassette encoding a CH2CH3 domain, a CD28 transmembrane domain, and a CD28.ζ signaling domain.45,>>46<< For in vivo studies, a retroviral vector encoding the fusion protein eGFP-Firefly Luciferase (eGFP.
n3:mentions: n2:22966020

Subject Item: _:vb24402538
rdf:type: n3:Context
rdf:value: 45,46 For in vivo studies, a retroviral vector encoding the fusion protein eGFP-Firefly Luciferase (eGFP.FFLuc) was used to generate firefly luciferase expressing GBM cells.>>26<<
n3:mentions: n2:20068073

Subject Item: _:vb24402539
rdf:type: n3:Context
rdf:value: 45,46 For in vivo studies, a retroviral vector encoding the fusion protein eGFP-Firefly Luciferase (eGFP.FFLuc) was used to generate firefly luciferase expressing GBM cells.26,>>28<<
n3:mentions: n2:19532139

Subject Item: _:vb24402540
rdf:type: n3:Context
rdf:value: OKT3/CD28-activated T cells were transduced with retroviral vectors as described previously.>>27<< Peripheral blood mononuclear cells were isolated by Lymphoprep (Greiner Bio-One, NC) gradient centrifugation.
n3:mentions: n2:17575166

Subject Item: _:vb24402541
rdf:type: n3:Context
rdf:value: The generation of the U373 cell lines expressing an enhanced GFP firefly luciferase fusion protein (U373.eGFP.FFluc) has been previously described.>>26<< Firefly-luciferase expression was confirmed in vitro prior to usage in a luminometer.
n3:mentions: n2:20068073

Subject Item: _:vb24402542
rdf:type: n5:Section
dc:title: results
n5:contains: _:vb24402548 _:vb24402549 _:vb24402550 _:vb24402544 _:vb24402545 _:vb24402546 _:vb24402547 _:vb24402543

Subject Item: _:vb24402543
rdf:type: n3:Context
rdf:value: While GBMs are known to be heterogeneous tumors with substantial histopathological and interpatient variability,>>15<< single-cell antigen coexpression within individual tumors has not been well characterized.
n3:mentions: n2:18324354

Subject Item: _:vb24402544
rdf:type: n3:Context
rdf:value: We therefore studied the simultaneous expression pattern of three established glioma-restricted antigens (HER2, IL-13Rα2, and EphA2) in primary GBM samples.>>16<<
n3:mentions: n2:15256472

Subject Item: _:vb24402545
rdf:type: n3:Context
rdf:value: We therefore studied the simultaneous expression pattern of three established glioma-restricted antigens (HER2, IL-13Rα2, and EphA2) in primary GBM samples.16,>>17<<
n3:mentions: n2:17804706

Subject Item: _:vb24402546
rdf:type: n3:Context
rdf:value: We therefore studied the simultaneous expression pattern of three established glioma-restricted antigens (HER2, IL-13Rα2, and EphA2) in primary GBM samples.16,17,>>18<<
n3:mentions: n2:16254188

Subject Item: _:vb24402547
rdf:type: n3:Context
rdf:value: We therefore studied the simultaneous expression pattern of three established glioma-restricted antigens (HER2, IL-13Rα2, and EphA2) in primary GBM samples.16,17,18,>>19<<
n3:mentions: n2:18172271

Subject Item: _:vb24402548
rdf:type: n3:Context
rdf:value: We therefore studied the simultaneous expression pattern of three established glioma-restricted antigens (HER2, IL-13Rα2, and EphA2) in primary GBM samples.16,17,18,19,>>20<<
n3:mentions: n2:15604287

Subject Item: _:vb24402549
rdf:type: n3:Context
rdf:value: We reasoned that the enhanced in vitro activity of biCAR T cells could result from increased ζ-chain signaling by virtue of simultaneous engagement of HER2 and IL-13Rα2 and examined the intracellular expression of>>21<< pZAP-70 in T cells upon antigen encounter.
n3:mentions: n2:1423621

Subject Item: _:vb24402550
rdf:type: n3:Context
rdf:value: enhanced in vitro activity of biCAR T cells could result from increased ζ-chain signaling by virtue of simultaneous engagement of HER2 and IL-13Rα2 and examined the intracellular expression of21 pZAP-70 in T cells upon antigen encounter.>>22<<
n3:mentions: n2:7528772

Subject Item: _:vb24402551
rdf:type: n5:Section
dc:title: discussion
n5:contains: _:vb24402552 _:vb24402553 _:vb24402554 _:vb24402555 _:vb24402556 _:vb24402557 _:vb24402558 _:vb24402559 _:vb24402576 _:vb24402577 _:vb24402578 _:vb24402579 _:vb24402580 _:vb24402581 _:vb24402568 _:vb24402569 _:vb24402570 _:vb24402571 _:vb24402572 _:vb24402573 _:vb24402574 _:vb24402575 _:vb24402560 _:vb24402561 _:vb24402562 _:vb24402563 _:vb24402564 _:vb24402565 _:vb24402566 _:vb24402567

Subject Item: _:vb24402552
rdf:type: n3:Context
rdf:value: On exploring the antigen expression landscape in primary GBM, we encountered substantial heterogeneity between patients as observed by others.>>13<<,14 This makes the selection of any single antigen incapable of capturing most patients as candidates for targeted therapies.
n3:mentions: n2:17255279

Subject Item: _:vb24402553
rdf:type: n3:Context
rdf:value: On exploring the antigen expression landscape in primary GBM, we encountered substantial heterogeneity between patients as observed by others.13,>>14<< This makes the selection of any single antigen incapable of capturing most patients as candidates for targeted therapies.
n3:mentions: n2:15827123

Subject Item: _:vb24402554
rdf:type: n3:Context
rdf:value: This, in addition to the limited T cell persistence in vivo,>>23<<,24,25 could explain why targeting a single antigen using CAR T cells allows an initial robust antitumor response that is followed by relapse26,27,28,29 due to outgrowth of antigen null tumor cells.
n3:mentions: n2:20304086

Subject Item: _:vb24402555
rdf:type: n3:Context
rdf:value: This, in addition to the limited T cell persistence in vivo,23,>>24<<,25 could explain why targeting a single antigen using CAR T cells allows an initial robust antitumor response that is followed by relapse26,27,28,29 due to outgrowth of antigen null tumor cells.
n3:mentions: n2:17299405

Subject Item: _:vb24402556
rdf:type: n3:Context
rdf:value: This, in addition to the limited T cell persistence in vivo,23,24,>>25<< could explain why targeting a single antigen using CAR T cells allows an initial robust antitumor response that is followed by relapse26,27,28,29 due to outgrowth of antigen null tumor cells.
n3:mentions: n2:21849486

Subject Item: _:vb24402557
rdf:type: n3:Context
rdf:value: This, in addition to the limited T cell persistence in vivo,23,24,25 could explain why targeting a single antigen using CAR T cells allows an initial robust antitumor response that is followed by relapse>>26<<,27,28,29 due to outgrowth of antigen null tumor cells.
n3:mentions: n2:20068073

Subject Item: _:vb24402558
rdf:type: n3:Context
rdf:value: This, in addition to the limited T cell persistence in vivo,23,24,25 could explain why targeting a single antigen using CAR T cells allows an initial robust antitumor response that is followed by relapse26,>>27<<,28,29 due to outgrowth of antigen null tumor cells.
n3:mentions: n2:17575166

Subject Item: _:vb24402559
rdf:type: n3:Context
rdf:value: This, in addition to the limited T cell persistence in vivo,23,24,25 could explain why targeting a single antigen using CAR T cells allows an initial robust antitumor response that is followed by relapse26,27,>>28<<,29 due to outgrowth of antigen null tumor cells.
n3:mentions: n2:19532139

Subject Item: _:vb24402560
rdf:type: n3:Context
rdf:value: This, in addition to the limited T cell persistence in vivo,23,24,25 could explain why targeting a single antigen using CAR T cells allows an initial robust antitumor response that is followed by relapse26,27,28,>>29<< due to outgrowth of antigen null tumor cells.
n3:mentions: n2:22173710

Subject Item: _:vb24402561
rdf:type: n3:Context
rdf:value: We constructed a binominal mathematical model, comparing the odds of targeting two versus three tumor antigens to define how broad of an approach is necessary to achieve near-complete (>95%) tumor cell capture>>30<< and found that while dual targeting was clearly superior to single targeting, targeting of three antigens (or more) did not predict a significantly superior advantage in the patient cohort we studied.
n3:mentions: n2:2081244

Subject Item: _:vb24402562
rdf:type: n3:Context
rdf:value: EphA2, as recently demonstrated by our group, could well be very valid in the context of targeting multiple antigens, and paired with either HER2 or IL-13Rα2 or both, could represent a more valid option in particular patient's scenarios.>>31<< Our results indicate that bispecific T cell products, probably by virtue of being able to recognize both target antigens, efficiently offset antigen escape variants and induced uniform depletion of tumor cell populations expressing HER2
n3:mentions: n2:23070117

Subject Item: _:vb24402563
rdf:type: n3:Context
rdf:value: It has been shown that the magnitude of T cell response is influenced by the balance between the density of target antigens expressed on the tumor and the density of CAR molecules expressed on T cells.>>32<< Accordingly, biCAR T cells would have functional advantage by virtue of their ability to “see” a more antigen dense tumor cell and their collective expression of a higher density of CARs on the cell surface.
n3:mentions: n2:10680014

Subject Item: _:vb24402564
rdf:type: n3:Context
rdf:value: to “see” a more antigen dense tumor cell and their collective expression of a higher density of CARs on the cell surface. Such an advantage would be particularly favorable where the expression of individual tumor antigens is modest.>>28<< This was demonstrated by the ability of biCAR T cells to maintain their cytolytic activity even at relatively low T cell to tumor cell ratios.
n3:mentions: n2:19532139

Subject Item: _:vb24402565
rdf:type: n3:Context
rdf:value: for testing in vivo efficacy, xenogeneic models have been particularly useful in the context of preclinical testing of human T cell products developed for cancer and have served as a justification for most early-phase clinical trials.>>4<<,5,6 In addition, the ability to amplify the antitumor response in situ could compensate for small cell doses, therefore avoiding the potential for adverse reactions such as the cytokine storms associated with very high T cell doses.
n3:mentions: n2:18978797

Subject Item: _:vb24402566
rdf:type: n3:Context
rdf:value: for testing in vivo efficacy, xenogeneic models have been particularly useful in the context of preclinical testing of human T cell products developed for cancer and have served as a justification for most early-phase clinical trials.4,>>5<<,6 In addition, the ability to amplify the antitumor response in situ could compensate for small cell doses, therefore avoiding the potential for adverse reactions such as the cytokine storms associated with very high T cell doses.
n3:mentions: n2:23527958

Subject Item: _:vb24402567
rdf:type: n3:Context
rdf:value: In addition, the ability to amplify the antitumor response in situ could compensate for small cell doses, therefore avoiding the potential for adverse reactions such as the cytokine storms associated with very high T cell doses.>>33<<,34,35 Collectively, we observed multiple indicators of functional superiority of biCAR T cells to a bispecific pooled product.
n3:mentions: n2:20179677

Subject Item: _:vb24402568
rdf:type: n3:Context
rdf:value: In addition, the ability to amplify the antitumor response in situ could compensate for small cell doses, therefore avoiding the potential for adverse reactions such as the cytokine storms associated with very high T cell doses.33,>>34<<,35 Collectively, we observed multiple indicators of functional superiority of biCAR T cells to a bispecific pooled product.
n3:mentions: n2:12242449

Subject Item: _:vb24402569
rdf:type: n3:Context
rdf:value: In addition, the ability to amplify the antitumor response in situ could compensate for small cell doses, therefore avoiding the potential for adverse reactions such as the cytokine storms associated with very high T cell doses.33,34,>>35<< Collectively, we observed multiple indicators of functional superiority of biCAR T cells to a bispecific pooled product.
n3:mentions: n2:9255632

Subject Item: _:vb24402570
rdf:type: n3:Context
rdf:value: could be explained by the enhanced downstream signaling from ζ-chains upon encountering both target antigens simultaneously, as evidenced by a significantly higher degree of ZAP-70 phosphorylation upon simultaneous antigen encounter.>>21<<,22 Also, particularly important is that activation of biCAR T cells was comparable with unispecific T cells on exposure to single target antigen but was maximal only when both targets were encountered simultaneously.
n3:mentions: n2:1423621

Subject Item: _:vb24402571
rdf:type: n3:Context
rdf:value: could be explained by the enhanced downstream signaling from ζ-chains upon encountering both target antigens simultaneously, as evidenced by a significantly higher degree of ZAP-70 phosphorylation upon simultaneous antigen encounter.21,>>22<< Also, particularly important is that activation of biCAR T cells was comparable with unispecific T cells on exposure to single target antigen but was maximal only when both targets were encountered simultaneously.
n3:mentions: n2:7528772

Subject Item: _:vb24402572
rdf:type: n3:Context
rdf:value: regulatory hurdles. To overcome this, one strategy is to use internal ribosomal entry site or 2A-containing retroviral bicistronic vectors, allowing for simultaneous expression of two (or more) CAR molecules from the same RNA transcript.>>36<<,37 Alternatively, nonviral carriers such as sleeping beauty or PiggyBac transposon systems can be used to genetically modify T cells to coexpress multiple CARs with distinct specificities; we have optimized the latter system for scale up.
n3:mentions: n2:22929977

Subject Item: _:vb24402573
rdf:type: n3:Context
rdf:value: hurdles. To overcome this, one strategy is to use internal ribosomal entry site or 2A-containing retroviral bicistronic vectors, allowing for simultaneous expression of two (or more) CAR molecules from the same RNA transcript.36,>>37<< Alternatively, nonviral carriers such as sleeping beauty or PiggyBac transposon systems can be used to genetically modify T cells to coexpress multiple CARs with distinct specificities; we have optimized the latter system for scale up.
n3:mentions: n2:21772253

Subject Item: _:vb24402574
rdf:type: n3:Context
rdf:value: Alternatively, nonviral carriers such as sleeping beauty or PiggyBac transposon systems can be used to genetically modify T cells to coexpress multiple CARs with distinct specificities; we have optimized the latter system for scale up.>>37<<
n3:mentions: n2:21772253

Subject Item: _:vb24402575
rdf:type: n3:Context
rdf:value: nonviral carriers such as sleeping beauty or PiggyBac transposon systems can be used to genetically modify T cells to coexpress multiple CARs with distinct specificities; we have optimized the latter system for scale up.37,>>38<<
n3:mentions: n2:19905893

Subject Item: _:vb24402576
rdf:type: n3:Context
rdf:value: events related to lower specificity and off-target effects. Suicide genes that allow for conditional elimination of transgene expressing T cells enabling quick elimination of adoptively transferred T cells in case of adverse events.>>39<<,40,41 Our group recently showed the remarkable efficacy of such an approach using a small molecule-dimerizable iCasp9 cell-suicide system.
n3:mentions: n2:17638856

Subject Item: _:vb24402577
rdf:type: n3:Context
rdf:value: events related to lower specificity and off-target effects. Suicide genes that allow for conditional elimination of transgene expressing T cells enabling quick elimination of adoptively transferred T cells in case of adverse events.39,>>40<<,41 Our group recently showed the remarkable efficacy of such an approach using a small molecule-dimerizable iCasp9 cell-suicide system.
n3:mentions: n2:22047558

Subject Item: _:vb24402578
rdf:type: n3:Context
rdf:value: related to lower specificity and off-target effects. Suicide genes that allow for conditional elimination of transgene expressing T cells enabling quick elimination of adoptively transferred T cells in case of adverse events.39,40,>>41<< Our group recently showed the remarkable efficacy of such an approach using a small molecule-dimerizable iCasp9 cell-suicide system.
n3:mentions: n2:12850790

Subject Item: _:vb24402579
rdf:type: n3:Context
rdf:value: T cells enabling quick elimination of adoptively transferred T cells in case of adverse events.39,40,41 Our group recently showed the remarkable efficacy of such an approach using a small molecule-dimerizable iCasp9 cell-suicide system.>>42<< Alternatively, others have used a functionally bipartite CAR molecule that conditionally triggers downstream signaling only on simultaneous engagement of two distinct tumor-restricted antigens.
n3:mentions: n2:15728125

Subject Item: _:vb24402580
rdf:type: n3:Context
rdf:value: 42 Alternatively, others have used a functionally bipartite CAR molecule that conditionally triggers downstream signaling only on simultaneous engagement of two distinct tumor-restricted antigens.>>43<<
n3:mentions: n2:22526592

Subject Item: _:vb24402581
rdf:type: n3:Context
rdf:value: 42 Alternatively, others have used a functionally bipartite CAR molecule that conditionally triggers downstream signaling only on simultaneous engagement of two distinct tumor-restricted antigens.43,>>44<<
n3:mentions: n2:23242161

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