The interplay between metabolic remodeling and immune regulation in glioblastoma

1891, II. Contribution to the knowledge of sarcoma, Ann Surg, 14, 199

2006, The toxins of William B. Coley and the treatment of bone and soft-tissue sarcomas, Iowa Orthop J, 26, 154

1924, Uber den Stoffwechsel der Carcinomzelle, Biochem Zeitschr, 152, 309

1927, The metabolism of tumors in the body, J Gen Physiol, 8, 519, 10.1085/jgp.8.6.519

2012, The blockade of immune checkpoints in cancer immunotherapy, Nat Rev Cancer, 12, 252, 10.1038/nrc3239

2009, Understanding the Warburg effect: the metabolic requirements of cell proliferation, Science, 324, 1029, 10.1126/science.1160809

2012, Metabolic reprogramming: a cancer hallmark even warburg did not anticipate, Cancer Cell, 21, 297, 10.1016/j.ccr.2012.02.014

2012, The metabolomic signature of malignant glioma reflects accelerated anabolic metabolism, Cancer Res, 72, 5878, 10.1158/0008-5472.CAN-12-1572-T

2013, Metabolic pathways in immune cell activation and quiescence, Immunity, 38, 633, 10.1016/j.immuni.2013.04.005

2012, Commitment to glycolysis sustains survival of NO-producing inflammatory dendritic cells, Blood, 120, 1422, 10.1182/blood-2012-03-419747

2010, Toll-like receptor-induced changes in glycolytic metabolism regulate dendritic cell activation, Blood, 115, 4742, 10.1182/blood-2009-10-249540

2015, Metabolic reprogramming of immune cells in cancer progression, Immunity, 43, 435, 10.1016/j.immuni.2015.09.001

2014, Metabolism of stromal and immune cells in health and disease, Nature, 511, 167, 10.1038/nature13312

2013, Cutting edge: hypoxia-induced Nanog favors the intratumoral infiltration of regulatory T cells and macrophages via direct regulation of TGF-β1, J Immunol, 191, 5802, 10.4049/jimmunol.1302140

2013, Immune-suppressive properties of the tumor microenvironment, Cancer Immunol Immunother, 62, 1137, 10.1007/s00262-013-1434-6

2011, Suppression of T-cell responses by tumor metabolites, Cancer Immunol Immunother, 60, 425, 10.1007/s00262-010-0967-1

1998, Prevention of allogeneic fetal rejection by tryptophan catabolism, Science, 281, 1191, 10.1126/science.281.5380.1191

2013, Indoleamine 2,3 dioxygenase and metabolic control of immune responses, Trends Immunol, 34, 137, 10.1016/j.it.2012.10.001

2012, Tryptophan catabolism in cancer: beyond IDO and tryptophan depletion, Cancer Res, 72, 5435, 10.1158/0008-5472.CAN-12-0569

2015, Tryptophan-degrading enzymes in tumoral immune resistance, Front Immunol, 6, 34

2004, Expression of indoleamine 2,3-dioxygenase by plasmacytoid dendritic cells in tumor-draining lymph nodes, J Clin Invest, 114, 280, 10.1172/JCI21583

2011, An endogenous tumour-promoting ligand of the human aryl hydrocarbon receptor, Nature, 478, 197, 10.1038/nature10491

2010, An interaction between kynurenine and the aryl hydrocarbon receptor can generate regulatory T cells, J Immunol, 185, 3190, 10.4049/jimmunol.0903670

2010, Aryl hydrocarbon receptor negatively regulates dendritic cell immunogenicity via a kynurenine-dependent mechanism, Proc Natl Acad Sci U S A, 107, 19961, 10.1073/pnas.1014465107

2008, Control of T(reg) and T(H)17 cell differentiation by the aryl hydrocarbon receptor, Nature, 453, 65, 10.1038/nature06880

2015, Tumor-expressed IDO recruits and activates MDSCs in a treg-dependent manner, Cell Rep, 13, 412, 10.1016/j.celrep.2015.08.077

2010, Kynurenic acid is a potent endogenous aryl hydrocarbon receptor ligand that synergistically induces interleukin-6 in the presence of inflammatory signaling, Toxicol Sci, 115, 89, 10.1093/toxsci/kfq024

2008, Inflammatory signaling and aryl hydrocarbon receptor mediate synergistic induction of interleukin 6 in MCF-7 cells, Cancer Res, 68, 3609, 10.1158/0008-5472.CAN-07-6168

2007, Reduced inflammation in the tumor microenvironment delays the accumulation of myeloid-derived suppressor cells and limits tumor progression, Cancer Res, 67, 10019, 10.1158/0008-5472.CAN-07-2354

1956, The metabolism of tryptophan. 2. The metabolism of tryptophan in patients suffering from cancer of the bladder, Biochem J, 64, 578, 10.1042/bj0640578

2015, The role of IDO in brain tumor immunotherapy, J Neurooncol, 123, 395, 10.1007/s11060-014-1687-8

2002, Indoleamine 2,3-dioxygenase contributes to tumor cell evasion of T cell-mediated rejection, Int J Cancer, 101, 151, 10.1002/ijc.10645

2012, IDO expression in brain tumors increases the recruitment of regulatory T cells and negatively impacts survival, Clin Cancer Res, 18, 6110, 10.1158/1078-0432.CCR-12-2130

2014, Durable therapeutic efficacy utilizing combinatorial blockade against IDO, CTLA-4, and PD-L1 in mice with brain tumors, Clin Cancer Res, 20, 5290, 10.1158/1078-0432.CCR-14-0514

2014, The indoleamine 2,3-dioxygenase pathway controls complement-dependent enhancement of chemo-radiation therapy against murine glioblastoma, J Immunother Cancer, 2, 21, 10.1186/2051-1426-2-21

2013, The endogenous tryptophan metabolite and NAD+ precursor quinolinic acid confers resistance of gliomas to oxidative stress, Cancer Res, 73, 3225, 10.1158/0008-5472.CAN-12-3831

2009, Arginase: an emerging key player in the mammalian immune system, Br J Pharmacol, 158, 638, 10.1111/j.1476-5381.2009.00291.x

2014, Metabolism via arginase or nitric oxide synthase: two competing arginine pathways in macrophages, Front Immunol, 5, 532

2013, M2 microglia and macrophages drive oligodendrocyte differentiation during CNS remyelination, Nat Neurosci, 16, 1211, 10.1038/nn.3469

2016, Differential roles of M1 and M2 microglia in neurodegenerative diseases, Mol Neurobiol, 53, 1181, 10.1007/s12035-014-9070-5

2016, A polarizing question: do M1 and M2 microglia exist?, Nat Neurosci, 19, 987, 10.1038/nn.4338

2017, A relay pathway between arginine and tryptophan metabolism confers immunosuppressive properties on dendritic cells, Immunity, 46, 233, 10.1016/j.immuni.2017.01.005

1973, Favorable remission induction rate with twice weekly doses of L-asparaginase, Cancer Res, 33, 1

2013, Targeting arginine-dependent cancers with arginine-degrading enzymes: opportunities and challenges, Cancer Res Treat, 45, 251, 10.4143/crt.2013.45.4.251

2015, Diversion of aspartate in ASS1-deficient tumours fosters de novo pyrimidine synthesis, Nature, 527, 379, 10.1038/nature15529

2003, L-arginine consumption by macrophages modulates the expression of CD3 zeta chain in T lymphocytes, J Immunol, 171, 1232, 10.4049/jimmunol.171.3.1232

2004, Arginase I production in the tumor microenvironment by mature myeloid cells inhibits T-cell receptor expression and antigen-specific T-cell responses, Cancer Res, 64, 5839, 10.1158/0008-5472.CAN-04-0465

2015, Human recombinant arginase I (Co)-PEG5000 [HuArgI (Co)-PEG5000]-induced arginine depletion is selectively cytotoxic to human glioblastoma cells, J Neurooncol, 122, 75, 10.1007/s11060-014-1698-5

2015, Arginine deprivation affects glioblastoma cell adhesion, invasiveness and actin cytoskeleton organization by impairment of β-actin arginylation, Amino Acids, 47, 199, 10.1007/s00726-014-1857-1

2008, Enhanced tumor growth elicited by L-type amino acid transporter 1 in human malignant glioma cells, Neurosurgery, 62, 493, 10.1227/01.neu.0000316018.51292.19

2015, l-Arginine depletion blunts antitumor T-cell responses by inducing myeloid-derived suppressor cells, Cancer Res, 75, 275, 10.1158/0008-5472.CAN-14-1491

2001, Role of G-protein-coupled adenosine receptors in downregulation of inflammation and protection from tissue damage, Nature, 414, 916, 10.1038/414916a

2003, The critical role of adenosine A2A receptors in downregulation of inflammation and immunity in the pathogenesis of infectious diseases, Microbes Infect, 5, 515, 10.1016/S1286-4579(03)00068-6

2007, Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression, J Exp Med, 204, 1257, 10.1084/jem.20062512

2010, Generation and accumulation of immunosuppressive adenosine by human CD4+CD25highFOXP3+ regulatory T cells, J Biol Chem, 285, 7176, 10.1074/jbc.M109.047423

2011, Adenosine receptors and cancer, Biochim Biophys Acta, 1808, 1400, 10.1016/j.bbamem.2010.09.020

2015, A2aR antagonists: next generation checkpoint blockade for cancer immunotherapy, Comput Struct Biotechnol J, 13, 265, 10.1016/j.csbj.2015.03.008

2015, A non-canonical adenosinergic pathway led by CD38 in human melanoma cells induces suppression of T cell proliferation, Oncotarget, 6, 25602, 10.18632/oncotarget.4693

2016, Mesenchymal stromal cells derived from cervical cancer produce high amounts of adenosine to suppress cytotoxic T lymphocyte functions, J Transl Med, 14, 302, 10.1186/s12967-016-1057-8

2011, Mesenchymal stromal cells up-regulate CD39 and increase adenosine production to suppress activated T-lymphocytes, Stem Cell Res, 7, 66, 10.1016/j.scr.2011.04.001

2016, Adenosine-generating ovarian cancer cells attract myeloid cells which differentiate into adenosine-generating tumor associated macrophages—a self-amplifying, CD39- and CD73-dependent mechanism for tumor immune escape, J Immunother Cancer, 4, 49, 10.1186/s40425-016-0154-9

2016, Adenosine A3 receptor elicits chemoresistance mediated by multiple resistance-associated protein-1 in human glioblastoma stem-like cells, Oncotarget, 7, 67373, 10.18632/oncotarget.12033

2012, Regulation of immune responses by prostaglandin E2, J Immunol, 188, 21, 10.4049/jimmunol.1101029

2016, The role of prostaglandin E(2) in tumor-associated immunosuppression, Trends Mol Med, 22, 1, 10.1016/j.molmed.2015.11.003

2011, Positive feedback between PGE2 and COX2 redirects the differentiation of human dendritic cells toward stable myeloid-derived suppressor cells, Blood, 118, 5498, 10.1182/blood-2011-07-365825

2015, Cyclooxygenase-dependent tumor growth through evasion of immunity, Cell, 162, 1257, 10.1016/j.cell.2015.08.015

2010, Adenosine and prostaglandin E2 cooperate in the suppression of immune responses mediated by adaptive regulatory T cells, J Biol Chem, 285, 27571, 10.1074/jbc.M110.127100

2015, Tryptophan-2,3-dioxygenase is regulated by prostaglandin E2 in malignant glioma via a positive signaling loop involving prostaglandin E receptor-4, J Neurochem

2000, Expression of cyclooxygenase 2 (COX-2) in human glioma and in vitro inhibition by a specific COX-2 inhibitor, NS-398, Cancer Res, 60, 4926

2001, Cyclooxygenase-2 expression in human gliomas: prognostic significance and molecular correlations, Cancer Res, 61, 4375

2008, Induction of prostaglandin E2 synthesis and microsomal prostaglandin E synthase-1 expression in murine microglia by glioma-derived soluble factors. Laboratory investigation, J Neurosurg, 108, 311, 10.3171/JNS/2008/108/2/0311

2015, Enhanced immunosuppression by therapy-exposed glioblastoma multiforme tumor cells, Int J Cancer, 136, 2566, 10.1002/ijc.29309

1996, Glucose catabolism in cancer cells: amplification of the gene encoding type II hexokinase, Cancer Res, 56, 2468

2016, Targeting hexokinase 2 enhances response to radio-chemotherapy in glioblastoma, Oncotarget, 7, 69518, 10.18632/oncotarget.11680

2015, Ras-mediated modulation of pyruvate dehydrogenase activity regulates mitochondrial reserve capacity and contributes to glioblastoma tumorigenesis, Neuro Oncol, 17, 1220, 10.1093/neuonc/nou369

2010, Metabolic modulation of glioblastoma with dichloroacetate, Sci Transl Med, 2, 31ra34

2015, Metabolic competition in the tumor microenvironment is a driver of cancer progression, Cell, 162, 1229, 10.1016/j.cell.2015.08.016

2014, Trial watch: IDO inhibitors in cancer therapy, Oncoimmunology, 3, e957994, 10.4161/21624011.2014.957994

2015, The kynurenine to tryptophan ratio as a prognostic tool for glioblastoma patients enrolling in immunotherapy, J Clin Neurosci, 22, 1964, 10.1016/j.jocn.2015.06.018

2014, Increased tryptophan uptake on PET has strong independent prognostic value in patients with a previously treated high-grade glioma, Neuro Oncol, 16, 1373, 10.1093/neuonc/nou042

2013, CD73 promotes anthracycline resistance and poor prognosis in triple negative breast cancer, Proc Natl Acad Sci U S A, 110, 11091, 10.1073/pnas.1222251110

PRECISION Trial Investigators, 2016, Cardiovascular safety of celecoxib, naproxen, or ibuprofen for arthritis, N Engl J Med, 375, 2519, 10.1056/NEJMoa1611593

2013, COX-2 in cancer: Gordian knot or Achilles heel?, Front Pharmacol, 4, 34

2009, Cancer-associated IDH1 mutations produce 2-hydroxyglutarate, Nature, 462, 739, 10.1038/nature08617

2012, IDH mutation impairs histone demethylation and results in a block to cell differentiation, Nature, 483, 474, 10.1038/nature10860

2012, Metabolism of [U-13 C]glucose in human brain tumors in vivo, NMR Biomed, 25, 1234, 10.1002/nbm.2794

2012, Analysis of tumor metabolism reveals mitochondrial glucose oxidation in genetically diverse human glioblastomas in the mouse brain in vivo, Cell Metab, 15, 827, 10.1016/j.cmet.2012.05.001

2015, Bevacizumab treatment induces metabolic adaptation toward anaerobic metabolism in glioblastomas, Acta Neuropathol, 129, 115, 10.1007/s00401-014-1352-5