PD-L1 expression and prognostic impact in glioblastoma

Edjah K. Nduom, Departments of Neurosurgery, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (E.K.N., J.W., N.K.Y., N.H., L.-Y.K., K.G., X.L., A.B.H.); Department of Biostatistics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (S.Z.); Center for RNA Interference and Non-Coding RNAs, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.I.); Flow Cytometry and Cell Imaging Core Facility, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (J.K.B.); Neuropathology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.N.F.); Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.A.C.); Neuro-Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.A.C.); Melanoma Medical Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.C., K.R.); Lion Biotechnologies, Woodland Hills, California (J.Q.C., L.R.); Dept. of Immunology, H. Lee Moffitt Cancer Center, Tampa, Florida (J.Q.C., L.R.).
Jun Wei, Departments of Neurosurgery, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (E.K.N., J.W., N.K.Y., N.H., L.-Y.K., K.G., X.L., A.B.H.); Department of Biostatistics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (S.Z.); Center for RNA Interference and Non-Coding RNAs, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.I.); Flow Cytometry and Cell Imaging Core Facility, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (J.K.B.); Neuropathology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.N.F.); Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.A.C.); Neuro-Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.A.C.); Melanoma Medical Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.C., K.R.); Lion Biotechnologies, Woodland Hills, California (J.Q.C., L.R.); Dept. of Immunology, H. Lee Moffitt Cancer Center, Tampa, Florida (J.Q.C., L.R.).
Nasser K. Yaghi, Departments of Neurosurgery, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (E.K.N., J.W., N.K.Y., N.H., L.-Y.K., K.G., X.L., A.B.H.); Department of Biostatistics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (S.Z.); Center for RNA Interference and Non-Coding RNAs, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.I.); Flow Cytometry and Cell Imaging Core Facility, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (J.K.B.); Neuropathology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.N.F.); Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.A.C.); Neuro-Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.A.C.); Melanoma Medical Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.C., K.R.); Lion Biotechnologies, Woodland Hills, California (J.Q.C., L.R.); Dept. of Immunology, H. Lee Moffitt Cancer Center, Tampa, Florida (J.Q.C., L.R.).
Neal Huang, Departments of Neurosurgery, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (E.K.N., J.W., N.K.Y., N.H., L.-Y.K., K.G., X.L., A.B.H.); Department of Biostatistics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (S.Z.); Center for RNA Interference and Non-Coding RNAs, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.I.); Flow Cytometry and Cell Imaging Core Facility, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (J.K.B.); Neuropathology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.N.F.); Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.A.C.); Neuro-Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.A.C.); Melanoma Medical Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.C., K.R.); Lion Biotechnologies, Woodland Hills, California (J.Q.C., L.R.); Dept. of Immunology, H. Lee Moffitt Cancer Center, Tampa, Florida (J.Q.C., L.R.).
Ling-Yuan Kong, Departments of Neurosurgery, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (E.K.N., J.W., N.K.Y., N.H., L.-Y.K., K.G., X.L., A.B.H.); Department of Biostatistics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (S.Z.); Center for RNA Interference and Non-Coding RNAs, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.I.); Flow Cytometry and Cell Imaging Core Facility, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (J.K.B.); Neuropathology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.N.F.); Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.A.C.); Neuro-Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.A.C.); Melanoma Medical Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.C., K.R.); Lion Biotechnologies, Woodland Hills, California (J.Q.C., L.R.); Dept. of Immunology, H. Lee Moffitt Cancer Center, Tampa, Florida (J.Q.C., L.R.).
Konrad Gabrusiewicz, Departments of Neurosurgery, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (E.K.N., J.W., N.K.Y., N.H., L.-Y.K., K.G., X.L., A.B.H.); Department of Biostatistics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (S.Z.); Center for RNA Interference and Non-Coding RNAs, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.I.); Flow Cytometry and Cell Imaging Core Facility, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (J.K.B.); Neuropathology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.N.F.); Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.A.C.); Neuro-Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.A.C.); Melanoma Medical Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.C., K.R.); Lion Biotechnologies, Woodland Hills, California (J.Q.C., L.R.); Dept. of Immunology, H. Lee Moffitt Cancer Center, Tampa, Florida (J.Q.C., L.R.).
Xiaoyang Ling, Departments of Neurosurgery, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (E.K.N., J.W., N.K.Y., N.H., L.-Y.K., K.G., X.L., A.B.H.); Department of Biostatistics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (S.Z.); Center for RNA Interference and Non-Coding RNAs, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.I.); Flow Cytometry and Cell Imaging Core Facility, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (J.K.B.); Neuropathology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.N.F.); Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.A.C.); Neuro-Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.A.C.); Melanoma Medical Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.C., K.R.); Lion Biotechnologies, Woodland Hills, California (J.Q.C., L.R.); Dept. of Immunology, H. Lee Moffitt Cancer Center, Tampa, Florida (J.Q.C., L.R.).
Shouhao Zhou, Departments of Neurosurgery, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (E.K.N., J.W., N.K.Y., N.H., L.-Y.K., K.G., X.L., A.B.H.); Department of Biostatistics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (S.Z.); Center for RNA Interference and Non-Coding RNAs, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.I.); Flow Cytometry and Cell Imaging Core Facility, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (J.K.B.); Neuropathology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.N.F.); Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.A.C.); Neuro-Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.A.C.); Melanoma Medical Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.C., K.R.); Lion Biotechnologies, Woodland Hills, California (J.Q.C., L.R.); Dept. of Immunology, H. Lee Moffitt Cancer Center, Tampa, Florida (J.Q.C., L.R.).
Cristina Ivan, Departments of Neurosurgery, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (E.K.N., J.W., N.K.Y., N.H., L.-Y.K., K.G., X.L., A.B.H.); Department of Biostatistics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (S.Z.); Center for RNA Interference and Non-Coding RNAs, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.I.); Flow Cytometry and Cell Imaging Core Facility, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (J.K.B.); Neuropathology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.N.F.); Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.A.C.); Neuro-Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.A.C.); Melanoma Medical Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.C., K.R.); Lion Biotechnologies, Woodland Hills, California (J.Q.C., L.R.); Dept. of Immunology, H. Lee Moffitt Cancer Center, Tampa, Florida (J.Q.C., L.R.).
Jie Qing Chen, Departments of Neurosurgery, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (E.K.N., J.W., N.K.Y., N.H., L.-Y.K., K.G., X.L., A.B.H.); Department of Biostatistics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (S.Z.); Center for RNA Interference and Non-Coding RNAs, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.I.); Flow Cytometry and Cell Imaging Core Facility, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (J.K.B.); Neuropathology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.N.F.); Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.A.C.); Neuro-Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.A.C.); Melanoma Medical Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.C., K.R.); Lion Biotechnologies, Woodland Hills, California (J.Q.C., L.R.); Dept. of Immunology, H. Lee Moffitt Cancer Center, Tampa, Florida (J.Q.C., L.R.).
Jared K. Burks, Departments of Neurosurgery, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (E.K.N., J.W., N.K.Y., N.H., L.-Y.K., K.G., X.L., A.B.H.); Department of Biostatistics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (S.Z.); Center for RNA Interference and Non-Coding RNAs, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.I.); Flow Cytometry and Cell Imaging Core Facility, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (J.K.B.); Neuropathology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.N.F.); Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.A.C.); Neuro-Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.A.C.); Melanoma Medical Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.C., K.R.); Lion Biotechnologies, Woodland Hills, California (J.Q.C., L.R.); Dept. of Immunology, H. Lee Moffitt Cancer Center, Tampa, Florida (J.Q.C., L.R.).
Greg N. Fuller, Departments of Neurosurgery, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (E.K.N., J.W., N.K.Y., N.H., L.-Y.K., K.G., X.L., A.B.H.); Department of Biostatistics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (S.Z.); Center for RNA Interference and Non-Coding RNAs, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.I.); Flow Cytometry and Cell Imaging Core Facility, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (J.K.B.); Neuropathology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.N.F.); Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.A.C.); Neuro-Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.A.C.); Melanoma Medical Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.C., K.R.); Lion Biotechnologies, Woodland Hills, California (J.Q.C., L.R.); Dept. of Immunology, H. Lee Moffitt Cancer Center, Tampa, Florida (J.Q.C., L.R.).
George A. Calin, Departments of Neurosurgery, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (E.K.N., J.W., N.K.Y., N.H., L.-Y.K., K.G., X.L., A.B.H.); Department of Biostatistics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (S.Z.); Center for RNA Interference and Non-Coding RNAs, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.I.); Flow Cytometry and Cell Imaging Core Facility, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (J.K.B.); Neuropathology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.N.F.); Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.A.C.); Neuro-Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.A.C.); Melanoma Medical Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.C., K.R.); Lion Biotechnologies, Woodland Hills, California (J.Q.C., L.R.); Dept. of Immunology, H. Lee Moffitt Cancer Center, Tampa, Florida (J.Q.C., L.R.).
Charles A. Conrad, Departments of Neurosurgery, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (E.K.N., J.W., N.K.Y., N.H., L.-Y.K., K.G., X.L., A.B.H.); Department of Biostatistics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (S.Z.); Center for RNA Interference and Non-Coding RNAs, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.I.); Flow Cytometry and Cell Imaging Core Facility, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (J.K.B.); Neuropathology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.N.F.); Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.A.C.); Neuro-Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.A.C.); Melanoma Medical Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.C., K.R.); Lion Biotechnologies, Woodland Hills, California (J.Q.C., L.R.); Dept. of Immunology, H. Lee Moffitt Cancer Center, Tampa, Florida (J.Q.C., L.R.).
Caitlin Creasy, Departments of Neurosurgery, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (E.K.N., J.W., N.K.Y., N.H., L.-Y.K., K.G., X.L., A.B.H.); Department of Biostatistics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (S.Z.); Center for RNA Interference and Non-Coding RNAs, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.I.); Flow Cytometry and Cell Imaging Core Facility, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (J.K.B.); Neuropathology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.N.F.); Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.A.C.); Neuro-Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.A.C.); Melanoma Medical Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.C., K.R.); Lion Biotechnologies, Woodland Hills, California (J.Q.C., L.R.); Dept. of Immunology, H. Lee Moffitt Cancer Center, Tampa, Florida (J.Q.C., L.R.).
Krit Ritthipichai, Departments of Neurosurgery, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (E.K.N., J.W., N.K.Y., N.H., L.-Y.K., K.G., X.L., A.B.H.); Department of Biostatistics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (S.Z.); Center for RNA Interference and Non-Coding RNAs, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.I.); Flow Cytometry and Cell Imaging Core Facility, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (J.K.B.); Neuropathology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.N.F.); Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.A.C.); Neuro-Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.A.C.); Melanoma Medical Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.C., K.R.); Lion Biotechnologies, Woodland Hills, California (J.Q.C., L.R.); Dept. of Immunology, H. Lee Moffitt Cancer Center, Tampa, Florida (J.Q.C., L.R.).
Laszlo Radvanyi, Departments of Neurosurgery, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (E.K.N., J.W., N.K.Y., N.H., L.-Y.K., K.G., X.L., A.B.H.); Department of Biostatistics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (S.Z.); Center for RNA Interference and Non-Coding RNAs, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.I.); Flow Cytometry and Cell Imaging Core Facility, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (J.K.B.); Neuropathology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.N.F.); Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.A.C.); Neuro-Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.A.C.); Melanoma Medical Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.C., K.R.); Lion Biotechnologies, Woodland Hills, California (J.Q.C., L.R.); Dept. of Immunology, H. Lee Moffitt Cancer Center, Tampa, Florida (J.Q.C., L.R.).
Amy B. Heimberger, Departments of Neurosurgery, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (E.K.N., J.W., N.K.Y., N.H., L.-Y.K., K.G., X.L., A.B.H.); Department of Biostatistics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (S.Z.); Center for RNA Interference and Non-Coding RNAs, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.I.); Flow Cytometry and Cell Imaging Core Facility, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (J.K.B.); Neuropathology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.N.F.); Department of Experimental Therapeutics, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (G.A.C.); Neuro-Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.A.C.); Melanoma Medical Oncology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas (C.C., K.R.); Lion Biotechnologies, Woodland Hills, California (J.Q.C., L.R.); Dept. of Immunology, H. Lee Moffitt Cancer Center, Tampa, Florida (J.Q.C., L.R.).

Document Type

Article

Abstract

BACKGROUND: Therapeutic targeting of the immune checkpoints cytotoxic T-lymphocyte-associated molecule-4 (CTLA-4) and PD-1/PD-L1 has demonstrated tumor regression in clinical trials, and phase 2 trials are ongoing in glioblastoma (GBM). Previous reports have suggested that responses are more frequent in patients with tumors that express PD-L1; however, this has been disputed. At issue is the validation of PD-L1 biomarker assays and prognostic impact. METHODS: Using immunohistochemical analysis, we measured the incidence of PD-L1 expression in 94 patients with GBM. We categorized our results according to the total number of PD-L1-expressing cells within the GBMs and then validated this finding in ex vivo GBM flow cytometry with further analysis of the T cell populations. We then evaluated the association between PD-L1 expression and median survival time using the protein expression datasets and mRNA from The Cancer Genome Atlas. RESULTS: The median percentage of PD-L1-expressing cells in GBM by cell surface staining is 2.77% (range: 0%-86.6%; n = 92), which is similar to the percentage found by ex vivo flow cytometry. The majority of GBM patients (61%) had tumors with at least 1% or more PD-L1-positive cells, and 38% had at least 5% or greater PD-L1 expression. PD-L1 is commonly expressed on the GBM-infiltrating T cells. Expression of both PD-L1 and PD-1 are negative prognosticators for GBM outcome. CONCLUSIONS: The incidence of PD-L1 expression in GBM patients is frequent but is confined to a minority subpopulation, similar to other malignancies that have been profiled for PD-L1 expression. Higher expression of PD-L1 is correlated with worse outcome.

Medical Subject Headings

Adult; Aged; Animals; B7-H1 Antigen (genetics, metabolism); Biomarkers, Tumor (genetics, metabolism); Brain Neoplasms (genetics, metabolism, pathology); Cell Line, Tumor; Cell Proliferation; Female; Flow Cytometry; Follow-Up Studies; Gene Expression Regulation, Neoplastic; Glioblastoma (genetics, metabolism, pathology); Humans; Immunoenzyme Techniques; Male; Mice; Middle Aged; Neoplasm Staging; Prognosis; RNA, Messenger (genetics); Survival Rate; T-Lymphocytes (metabolism)

Publication Date

2-1-2016

Publication Title

Neuro-oncology

E-ISSN

1523-5866

Volume

18

Issue

2

First Page

195

Last Page

205

PubMed ID

26323609

Digital Object Identifier (DOI)

10.1093/neuonc/nov172

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