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n4:pmcid: PMC0
bibo:doi: 10.1084%2Fjem.20130678
n5:contains: _:vb26774790 _:vb26774784

Subject Item: _:vb26774784
rdf:type: n5:Section
dc:title: materials and methods
n5:contains: _:vb26774788 _:vb26774789 _:vb26774785 _:vb26774786 _:vb26774787

Subject Item: _:vb26774785
rdf:type: n4:Context
rdf:value: Subsequently, cells were transfected with pCEP4-mIgG3, pCEP4-mIl-12mIgG3, or pCEP4-mIl-23mIgG3, and cytokine production was detected by ELISA and RT-PCR, as previously described (Eisenring et al., >>2010<<). SMA-560 spontaneous murine astrocytoma cells were characterized previously (Uhl et al., 2004). B16-F10 C57BL/6 murine melanoma cells were purchased from American Type Culture Collection.
n4:mentions: n2:20935648

Subject Item: _:vb26774786
rdf:type: n4:Context
rdf:value: SMA-560 spontaneous murine astrocytoma cells were characterized previously (Uhl et al., >>2004<<). B16-F10 C57BL/6 murine melanoma cells were purchased from American Type Culture Collection.
n4:mentions: n2:15520202

Subject Item: _:vb26774787
rdf:type: n4:Context
rdf:value: Implantation of osmotic minipumps has been described previously (vom Berg et al., >>2012<<). The previous burr hole of the glioma injection was located, the bone wax and periosteal bone was removed, and the infusion cannula was lowered through the burr hole 3 mm into the putative center of the tumor. Pumps were explanted at day
n4:mentions: n2:23178247

Subject Item: _:vb26774788
rdf:type: n4:Context
rdf:value: The frontal part of the tumor-bearing cerebral hemisphere was harvested, and cells were prepared for flow cytometry as described previously (vom Berg et al., >>2012<<). Cells were restimulated for 3 h at 37°C and 5% CO2 in RPMI 1640 medium. RPMI 1640 was supplemented with 10% FCS and phorbol 12-myristate 13-acetate (50 ng/ml), ionomycin (500 ng/µl), and brefeldin A (1 µl/ml medium; GolgiPlug; BD). For
n4:mentions: n2:23178247

Subject Item: _:vb26774789
rdf:type: n4:Context
rdf:value: Immunostaining of cryosections was performed as described previously (Eisenring et al., >>2010<<). Alternatively, sections were stained with hematoxylin and eosin. Brains were also fixed in 4% formalin, embedded in paraffin and 2–3 µm sections were processed. Pictures were generated using an Olympus BX41 light microscope equipped
n4:mentions: n2:20935648

Subject Item: _:vb26774790
rdf:type: n5:Section
dc:title: results and discussion
n5:contains: _:vb26774820 _:vb26774821 _:vb26774822 _:vb26774816 _:vb26774817 _:vb26774818 _:vb26774819 _:vb26774812 _:vb26774813 _:vb26774814 _:vb26774815 _:vb26774808 _:vb26774809 _:vb26774810 _:vb26774811 _:vb26774804 _:vb26774805 _:vb26774806 _:vb26774807 _:vb26774800 _:vb26774801 _:vb26774802 _:vb26774803 _:vb26774796 _:vb26774797 _:vb26774798 _:vb26774799 _:vb26774792 _:vb26774793 _:vb26774794 _:vb26774795 _:vb26774791

Subject Item: _:vb26774791
rdf:type: n4:Context
rdf:value: IL-12 and IL-23 are suitable candidates to overcome the local immunosuppressive environment in GB and to trigger rejection, we expressed either of these two cytokines in C57BL/6 syngeneic GL-261 mouse glioma cells (Szatmári et al., >>2006<<). First, we generated a GL-261 line that constitutively expressed Photinus pyralis luciferase (hereafter, termed GL-261luc) for bioluminescence imaging (BLI).
n4:mentions: n2:16734735

Subject Item: _:vb26774792
rdf:type: n4:Context
rdf:value: This contrasts studies on IL-23–induced glioma rejection using neural stemlike cell– or DC-based approaches that showed potent antiglioma activity (Hu et al., >>2006<<; Yuan et al., 2006).
n4:mentions: n2:16951206

Subject Item: _:vb26774793
rdf:type: n4:Context
rdf:value: This contrasts studies on IL-23–induced glioma rejection using neural stemlike cell– or DC-based approaches that showed potent antiglioma activity (Hu et al., 2006; Yuan et al., >>2006<<). However, in various other models of solid tumors, it is also becoming increasingly apparent that IL-23 has primarily protumorigenic effects (Ngiow et al., 2013). Therefore, for the remainder of this study, we focused on the effector
n4:mentions: n2:16510582

Subject Item: _:vb26774794
rdf:type: n4:Context
rdf:value: However, in various other models of solid tumors, it is also becoming increasingly apparent that IL-23 has primarily protumorigenic effects (Ngiow et al., >>2013<<). Therefore, for the remainder of this study, we focused on the effector mechanisms of IL-12–mediated glioma rejection.
n4:mentions: n2:23954142

Subject Item: _:vb26774795
rdf:type: n4:Context
rdf:value: Although there is precedence for a role of NKT cells in IL-12–mediated tumor rejection (Cui et al., >>1997<<), the effective IL-12–mediated tumor rejection in Il15ra−/− mice further dismisses a critical role of NK and NKT cells because both populations depend on IL-15R signaling (Gordy et al., 2011).
n4:mentions: n2:9374462

Subject Item: _:vb26774796
rdf:type: n4:Context
rdf:value: IL-12–mediated tumor rejection (Cui et al., 1997), the effective IL-12–mediated tumor rejection in Il15ra−/− mice further dismisses a critical role of NK and NKT cells because both populations depend on IL-15R signaling (Gordy et al., >>2011<<).
n4:mentions: n2:22084435

Subject Item: _:vb26774797
rdf:type: n4:Context
rdf:value: In agreement with earlier studies (Daga et al., >>2007<<; Liu et al., 2002), we observed a rapid rejection of the newly implanted tumors within days in rechallenged survivors.
n4:mentions: n2:17582604

Subject Item: _:vb26774798
rdf:type: n4:Context
rdf:value: In agreement with earlier studies (Daga et al., 2007; Liu et al., >>2002<<), we observed a rapid rejection of the newly implanted tumors within days in rechallenged survivors.
n4:mentions: n2:11916248

Subject Item: _:vb26774799
rdf:type: n4:Context
rdf:value: Previous studies investigated the mechanisms of IL-12 in glioma rejection, many of these in a DC vaccination setting (Joki et al., >>1999<<; Yamanaka et al., 2002, 2003). A crucial involvement of NK cells and T cells (CD4+ and/or CD8+) in the IL-12–mediated rejection of experimental gliomas was described (Joki et al., 1999; Yamanaka et al., 2002, 2003).
n4:mentions: n2:10417770

Subject Item: _:vb26774800
rdf:type: n4:Context
rdf:value: Previous studies investigated the mechanisms of IL-12 in glioma rejection, many of these in a DC vaccination setting (Joki et al., 1999; Yamanaka et al., >>2002<<, 2003). A crucial involvement of NK cells and T cells (CD4+ and/or CD8+) in the IL-12–mediated rejection of experimental gliomas was described (Joki et al., 1999; Yamanaka et al., 2002, 2003).
n4:mentions: n2:12296646

Subject Item: _:vb26774801
rdf:type: n4:Context
rdf:value: Previous studies investigated the mechanisms of IL-12 in glioma rejection, many of these in a DC vaccination setting (Joki et al., 1999; Yamanaka et al., 2002, >>2003<<). A crucial involvement of NK cells and T cells (CD4+ and/or CD8+) in the IL-12–mediated rejection of experimental gliomas was described (Joki et al., 1999; Yamanaka et al., 2002, 2003).
n4:mentions: n2:14567611

Subject Item: _:vb26774802
rdf:type: n4:Context
rdf:value: A crucial involvement of NK cells and T cells (CD4+ and/or CD8+) in the IL-12–mediated rejection of experimental gliomas was described (Joki et al., >>1999<<; Yamanaka et al., 2002, 2003).
n4:mentions: n2:10417770

Subject Item: _:vb26774803
rdf:type: n4:Context
rdf:value: A crucial involvement of NK cells and T cells (CD4+ and/or CD8+) in the IL-12–mediated rejection of experimental gliomas was described (Joki et al., 1999; Yamanaka et al., >>2002<<, 2003). These reports present contradictory findings regarding the contribution of NK cells and the TH1 hallmark cytokine IFN-γ compared with a study where IL-12 was produced in situ and mouse mutants were used (Vetter et al., 2009). Some
n4:mentions: n2:12296646

Subject Item: _:vb26774804
rdf:type: n4:Context
rdf:value: A crucial involvement of NK cells and T cells (CD4+ and/or CD8+) in the IL-12–mediated rejection of experimental gliomas was described (Joki et al., 1999; Yamanaka et al., 2002, >>2003<<). These reports present contradictory findings regarding the contribution of NK cells and the TH1 hallmark cytokine IFN-γ compared with a study where IL-12 was produced in situ and mouse mutants were used (Vetter et al., 2009). Some of
n4:mentions: n2:14567611

Subject Item: _:vb26774805
rdf:type: n4:Context
rdf:value: These reports present contradictory findings regarding the contribution of NK cells and the TH1 hallmark cytokine IFN-γ compared with a study where IL-12 was produced in situ and mouse mutants were used (Vetter et al., >>2009<<). Some of these studies have investigated tumors derived from s.c. injection of glioma cell lines (Joki et al., 1999). However, in s.c. tumors, a subpopulation of ILCs seems to be crucial for IL-12–mediated tumor control, regardless of
n4:mentions: n2:19525900

Subject Item: _:vb26774806
rdf:type: n4:Context
rdf:value: Some of these studies have investigated tumors derived from s.c. injection of glioma cell lines (Joki et al., >>1999<<). However, in s.c.
n4:mentions: n2:10417770

Subject Item: _:vb26774807
rdf:type: n4:Context
rdf:value: tumors, a subpopulation of ILCs seems to be crucial for IL-12–mediated tumor control, regardless of the tissue origin of the tumor cells used (Eisenring et al., >>2010<<). Using an IL-12–expressing syngeneic glioma cell line and various genetic mutants, we established T cells as the crucial effector cell type of IL-12–mediated glioma rejection. Further characterization of the tumor-infiltrating T cells
n4:mentions: n2:20935648

Subject Item: _:vb26774808
rdf:type: n4:Context
rdf:value: CTLA-4 is the prototypic co-inhibitory receptor limiting T cell responses and its blockade has been shown to boost antitumor activity in metastatic melanoma in patients (Hodi et al., >>2010<<; Walker and Sansom, 2011). We observed a slight increase in the numbers of CTLA-4–positive CD4+FoxP3− T cells in GL-261luc:
n4:mentions: n2:20525992

Subject Item: _:vb26774809
rdf:type: n4:Context
rdf:value: CTLA-4 is the prototypic co-inhibitory receptor limiting T cell responses and its blockade has been shown to boost antitumor activity in metastatic melanoma in patients (Hodi et al., 2010; Walker and Sansom, >>2011<<). We observed a slight increase in the numbers of CTLA-4–positive CD4+FoxP3− T cells in GL-261luc:
n4:mentions: n2:22116087

Subject Item: _:vb26774810
rdf:type: n4:Context
rdf:value: 3 A; Eisenring et al., >>2010<<). Switching to a therapeutic setting, we challenged mice with GL-261luc:
n4:mentions: n2:20935648

Subject Item: _:vb26774811
rdf:type: n4:Context
rdf:value: The fact that accumulation of T reg cells is a key feature of human GB and correlates with outcome (Jacobs et al., >>2010<<) underlines the clinical significance of the treatment approach used here.
n4:mentions: n2:20537408

Subject Item: _:vb26774812
rdf:type: n4:Context
rdf:value: The mechanism by which CTLA-4 blockade inhibits T reg cell function remains a subject of intense debate (Walker and Sansom, >>2011<<). Recent studies demonstrate that selective opsonization of T reg cells with CTLA-4 antibodies can elicit potent antibody-dependent cell-mediated cytotoxicity (ADCC) within the tumor site (Selby et al., 2013; Simpson et al., 2013). In
n4:mentions: n2:22116087

Subject Item: _:vb26774813
rdf:type: n4:Context
rdf:value: Recent studies demonstrate that selective opsonization of T reg cells with CTLA-4 antibodies can elicit potent antibody-dependent cell-mediated cytotoxicity (ADCC) within the tumor site (Selby et al., 2013; Simpson et al., >>2013<<). In regard to the tumor-suppressing effector cells, IL-12 increased the expression of perforin-1 in CD8 T cells and NK cells, but not in CD4 cells (Fig. 4 E), indicating that CTLs are ultimately responsible for tumor control.
n4:mentions: n2:23897981

Subject Item: _:vb26774814
rdf:type: n4:Context
rdf:value: SMA-560 is derived from a spontaneous murine astrocytoma (Uhl et al., >>2004<<). Here, we initiated treatment on day 7 after tumor cell implantation.
n4:mentions: n2:15520202

Subject Item: _:vb26774815
rdf:type: n4:Context
rdf:value: The poor activity of CTLA-4 monotherapy observed in our study contrasts with previous studies using similar models (Fecci et al., >>2007<<; Grauer et al., 2007; Agarwalla et al., 2012). In those studies CTLA-4 blockade was initiated at much earlier time points after seeding, the disease course progressed at a slower pace, and/or a different mAb was used in treatments.
n4:mentions: n2:17404100

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rdf:value: The poor activity of CTLA-4 monotherapy observed in our study contrasts with previous studies using similar models (Fecci et al., 2007; Grauer et al., >>2007<<; Agarwalla et al., 2012). In those studies CTLA-4 blockade was initiated at much earlier time points after seeding, the disease course progressed at a slower pace, and/or a different mAb was used in treatments.
n4:mentions: n2:17315190

Subject Item: _:vb26774817
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rdf:value: The poor activity of CTLA-4 monotherapy observed in our study contrasts with previous studies using similar models (Fecci et al., 2007; Grauer et al., 2007; Agarwalla et al., >>2012<<). In those studies CTLA-4 blockade was initiated at much earlier time points after seeding, the disease course progressed at a slower pace, and/or a different mAb was used in treatments.
n4:mentions: n2:22576343

Subject Item: _:vb26774818
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rdf:value: We used a different anti–CTLA-4 mAb (9D9, IgG2b), which has been reported to confer weaker ADCC of T reg cells than the 9H10 hamster mAb used by Fecci et al. (>>2007<<; Selby et al., 2013; Simpson et al., 2013).
n4:mentions: n2:17404100

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rdf:value: We used a different anti–CTLA-4 mAb (9D9, IgG2b), which has been reported to confer weaker ADCC of T reg cells than the 9H10 hamster mAb used by Fecci et al. (2007; Selby et al., 2013; Simpson et al., >>2013<<). It is therefore tempting to speculate that the combination of i.t. IL-12Fc in combination with systemic CTLA-4 blockade through a strong ADCC-inducing mAb may yield even better synergy. To expand our treatment strategy toward other
n4:mentions: n2:23897981

Subject Item: _:vb26774820
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rdf:value: B16 is an extremely aggressive melanoma cell line and poorly immunogenic (Becker et al., >>2010<<). In this rapidly progressing model of intracranial melanoma, only combination therapy led to a significant, albeit very modest survival advantage when compared with vehicle controls (Fig. 4 G).
n4:mentions: n2:19849715

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rdf:value: Systemic anti–CTLA-4 treatment is FDA-approved for metastatic melanoma based on clinical trials demonstrating clinical benefit (Hodi et al., >>2010<<) and has been further tested for various other solid cancers (Grosso and Jure-Kunkel, 2013).
n4:mentions: n2:20525992

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rdf:value: Systemic anti–CTLA-4 treatment is FDA-approved for metastatic melanoma based on clinical trials demonstrating clinical benefit (Hodi et al., 2010) and has been further tested for various other solid cancers (Grosso and Jure-Kunkel, >>2013<<). In light of the data presented here, a combination therapy consisting of systemic checkpoint blockade and local administration of IL-12 is a highly promising candidate for swift clinical translation in GB.
n4:mentions: n2:23390376

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