Myeloid-derived suppressor cells in glioma

References

• Holland EC. Progenitor cells and glioma formation. Curr. Opin. Neurol. 14(6), 683–688 (2001).
   PubMed Web of Science ®Google Scholar
• Surawicz TS, Davis F, Freels S, Laws ER Jr, Menck HR. Brain tumor survival: results from the National Cancer Data Base. J. Neurooncol. 40(2), 151–160 (1998).
   PubMed Web of Science ®Google Scholar
• Ohgaki H, Kleihues P. Epidemiology and etiology of gliomas. Acta Neuropathol. 109(1), 93–108 (2005).
   PubMed Web of Science ®Google Scholar
• Stupp R, Hegi ME, Mason WP et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 10(5), 459–466 (2009).
   PubMed Web of Science ®Google Scholar
• Lefranc F, Sadeghi N, Camby I, Metens T, Dewitte O, Kiss R. Present and potential future issues in glioblastoma treatment. Expert Rev. Anticancer Ther. 6(5), 719–732 (2006).
   PubMed Web of Science ®Google Scholar
• Batich K, Choi B, Mitchell D. Immunotherapy of high-grade gliomas: preclinical in vivo experiments in animal models. In: Animal Models of Brain Tumors. Martínez Murillo R, Martínez A ( Eds). Humana Press, New York, NY, USA, 245–273 (2013).
   Google Scholar
• Liau LM, Black KL, Prins RM et al. Treatment of intracranial gliomas with bone marrow-derived dendritic cells pulsed with tumor antigens. J. Neurosurg. 90(6), 1115–1124 (1999).
   PubMed Web of Science ®Google Scholar
• Parney IF, Petruk KC, Zhang C, Farr-Jones M, Sykes DB, Chang LJ. Granulocyte-macrophage colony-stimulating factor and B7-2 combination immunogene therapy in an allogeneic Hu-PBL-SCID/beige mouse-human glioblastoma multiforme model. Hum. Gene Ther. 8(9), 1073–1085 (1997).
   PubMed Web of Science ®Google Scholar
• Sampson JH, Archer GE, Ashley DM et al. Subcutaneous vaccination with irradiated, cytokine-producing tumor cells stimulates CD8+ cell-mediated immunity against tumors located in the “immunologically privileged” central nervous system. Proc. Natl Acad. Sci. USA 93(19), 10399–10404 (1996).
   PubMed Web of Science ®Google Scholar
• Liau LM, Prins RM, Kiertscher SM et al. Dendritic cell vaccination in glioblastoma patients induces systemic and intracranial T-cell responses modulated by the local central nervous system tumor microenvironment. Clin. Cancer Res. 11(15), 5515–5525 (2005).
   PubMed Web of Science ®Google Scholar
• Parney IF, Chang LJ, Farr-Jones MA, Hao C, Smylie M, Petruk KC. Technical hurdles in a pilot clinical trial of combined B7-2 and GM-CSF immunogene therapy for glioblastomas and melanomas. J. Neurooncol. 78(1), 71–80 (2006).
   PubMed Web of Science ®Google Scholar
• Yu JS, Liu G, Ying H, Yong WH, Black KL, Wheeler CJ. Vaccination with tumor lysate-pulsed dendritic cells elicits antigen-specific, cytotoxic T-cells in patients with malignant glioma. Cancer Res. 64(14), 4973–4979 (2004).
   PubMed Web of Science ®Google Scholar
• Ardon H, Van Gool SW, Verschuere T et al. Integration of autologous dendritic cell-based immunotherapy in the standard of care treatment for patients with newly diagnosed glioblastoma: results of the HGG-2006 phase I/II trial. Cancer Immunol. Immunother. 61(11), 2033–2044 (2012).
   PubMed Web of Science ®Google Scholar
• De Vleeschouwer S, Ardon H, Van Calenbergh F et al. Stratification according to HGG-IMMUNO RPA model predicts outcome in a large group of patients with relapsed malignant glioma treated by adjuvant postoperative dendritic cell vaccination. Cancer Immunol. Immunother. 61(11), 2105–2112 (2012).
   PubMed Web of Science ®Google Scholar
• Rodrigues JC, Gonzalez GC, Zhang L et al. Normal human monocytes exposed to glioma cells acquire myeloid-derived suppressor cell-like properties. Neuro Oncol. 12(4), 351–365 (2010).
   PubMed Web of Science ®Google Scholar
• Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 144(5), 646–674 (2011).
   PubMed Web of Science ®Google Scholar
• Gomez GG, Kruse CA. Mechanisms of malignant glioma immune resistance and sources of immunosuppression. Gene Ther. Mol. Biol. 10(A), 133–146 (2006).
   PubMed Web of Science ®Google Scholar
• Parney IF, Farr-Jones MA, Chang LJ, Petruk KC. Human glioma immunobiology in vitro: implications for immunogene therapy. Neurosurgery 46(5), 1169–1177, discussion 1177–1178 (2000).
   PubMed Web of Science ®Google Scholar
• Vandenberk L, Van Gool SW. Treg infiltration in glioma: a hurdle for antiglioma immunotherapy. Immunotherapy 4(7), 675–678 (2012).
   PubMed Web of Science ®Google Scholar
• Sonabend AM, Rolle CE, Lesniak MS. The role of regulatory T cells in malignant glioma. Anticancer Res. 28(2B), 1143–1150 (2008).
   PubMed Web of Science ®Google Scholar
• Hao C, Parney IF, Roa WH, Turner J, Petruk KC, Ramsay DA. Cytokine and cytokine receptor mRNA expression in human glioblastomas: evidence of Th1, Th2 and Th3 cytokine dysregulation. Acta Neuropathol. 103(2), 171–178 (2002).
   PubMed Web of Science ®Google Scholar
• Morimura T, Neuchrist C, Kitz K et al. Monocyte subpopulations in human gliomas: expression of Fc and complement receptors and correlation with tumor proliferation. Acta Neuropathol. 80(3), 287–294 (1990).
   PubMed Web of Science ®Google Scholar
• Parney IF, Waldron JS, Parsa AT. Flow cytometry and in vitro analysis of human glioma-associated macrophages. Laboratory investigation. J. Neurosurg. 110(3), 572–582 (2009).
   PubMed Web of Science ®Google Scholar
• Hussain SF, Yang D, Suki D, Aldape K, Grimm E, Heimberger AB. The role of human glioma-infiltrating microglia/macrophages in mediating antitumor immune responses. Neuro Oncol. 8(3), 261–279 (2006).
   PubMed Web of Science ®Google Scholar
• Flugel A, Labeur MS, Grasbon-Frodl EM, Kreutzberg GW, Graeber MB. Microglia only weakly present glioma antigen to cytotoxic T cells. Int. J. Dev. Neurosci. 17(5–6), 547–556 (1999).
   PubMed Web of Science ®Google Scholar
• Taniguchi Y, Ono K, Yoshida S, Tanaka R. Antigen-presenting capability of glial cells under glioma-harboring conditions and the effect of glioma-derived factors on antigen presentation. J. Neuroimmunol. 111(1–2), 177–185 (2000).
   PubMed Web of Science ®Google Scholar
• Wagner S, Czub S, Greif M et al. Microglial/macrophage expression of interleukin 10 in human glioblastomas. Int. J. Cancer 82(1), 12–16 (1999).
   PubMed Web of Science ®Google Scholar
• Badie B, Schartner J, Prabakaran S, Paul J, Vorpahl J. Expression of Fas ligand by microglia: possible role in glioma immune evasion. J. Neuroimmunol. 120(1–2), 19–24 (2001).
   PubMed Web of Science ®Google Scholar
• Prins RM, Scott GP, Merchant RE, Graf MR. Irradiated tumor cell vaccine for treatment of an established glioma. II. Expansion of myeloid suppressor cells that promote tumor progression. Cancer Immunol. Immunother. 51(4), 190–199 (2002).
   PubMed Web of Science ®Google Scholar
• Jia W, Jackson-Cook C, Graf MR. Tumor-infiltrating, myeloid-derived suppressor cells inhibit T cell activity by nitric oxide production in an intracranial rat glioma + vaccination model. J. Neuroimmunol. 223(1–2), 20–30 (2010).
   PubMed Web of Science ®Google Scholar
• Almand B, Clark JI, Nikitina E et al. Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer. J. Neuroimmunol. 166(1), 678–689 (2001).
   Google Scholar
• Mirza N, Fishman M, Fricke I et al. All-trans-retinoic acid improves differentiation of myeloid cells and immune response in cancer patients. Cancer Res. 66(18), 9299–9307 (2006).
   PubMed Web of Science ®Google Scholar
• Cohen PA, Ko JS, Storkus WJ et al. Myeloid-derived suppressor cells adhere to physiologic STAT3- vs STAT5-dependent hematopoietic programming, establishing diverse tumor-mediated mechanisms of immunologic escape. Immunol. Invest. 41(6–7), 680–710 (2012).
   PubMed Web of Science ®Google Scholar
• Zhu B, Bando Y, Xiao S et al. CD11b+Ly-6C(hi) suppressive monocytes in experimental autoimmune encephalomyelitis. J. Immunol. 179(8), 5228–5237 (2007).
   PubMed Web of Science ®Google Scholar
• Makarenkova VP, Bansal V, Matta BM, Perez LA, Ochoa JB. CD11b+/Gr-1+ myeloid suppressor cells cause T cell dysfunction after traumatic stress. J. Immunol. 176(4), 2085–2094 (2006).
   PubMed Web of Science ®Google Scholar
• Serafini P, Borrello I, Bronte V. Myeloid suppressor cells in cancer: recruitment, phenotype, properties, and mechanisms of immune suppression. Semin. Cancer Biol. 16(1), 53–65 (2006).
   PubMed Web of Science ®Google Scholar
• Meyer C, Sevko A, Ramacher M et al. Chronic inflammation promotes myeloid-derived suppressor cell activation blocking antitumor immunity in transgenic mouse melanoma model. Proc. Natl Acad. Sci. USA 108(41), 17111–17116 (2011).
   PubMed Web of Science ®Google Scholar
• Dolcetti L, Peranzoni E, Ugel S et al. Hierarchy of immunosuppressive strength among myeloid-derived suppressor cell subsets is determined by GM-CSF. Eur. J. Immunol. 40(1), 22–35 (2010).
   PubMed Web of Science ®Google Scholar
• Fujita M, Kohanbash G, Fellows-Mayle W et al. COX-2 blockade suppresses gliomagenesis by inhibiting myeloid-derived suppressor cells. Cancer Res. 71(7), 2664–2674 (2011).
   PubMed Web of Science ®Google Scholar
• Fujita M, Scheurer ME, Decker SA et al. Role of type 1 IFNs in antiglioma immunosurveillance--using mouse studies to guide examination of novel prognostic markers in humans. Clin. Cancer Res. 16(13), 3409–3419 (2010).
   PubMed Web of Science ®Google Scholar
• Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 9(3), 162–174 (2009).
   PubMed Web of Science ®Google Scholar
• Youn JI, Nagaraj S, Collazo M, Gabrilovich DI. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J. Immunol. 181(8), 5791–5802 (2008).
   PubMed Web of Science ®Google Scholar
• Mandruzzato S, Solito S, Falisi E et al. IL4Ralpha+ myeloid-derived suppressor cell expansion in cancer patients. J. Immunol. 182(10), 6562–6568 (2009).
   PubMed Web of Science ®Google Scholar
• Filipazzi P, Valenti R, Huber V et al. Identification of a new subset of myeloid suppressor cells in peripheral blood of melanoma patients with modulation by a granulocyte-macrophage colony-stimulation factor-based antitumor vaccine. J. Clin. Oncol. 25(18), 2546–2553 (2007).
   PubMed Web of Science ®Google Scholar
• Schmielau J, Finn OJ. Activated granulocytes and granulocyte-derived hydrogen peroxide are the underlying mechanism of suppression of t-cell function in advanced cancer patients. Cancer Res. 61(12), 4756–4760 (2001).
   PubMed Web of Science ®Google Scholar
• Zea AH, Rodriguez PC, Atkins MB et al. Arginase-producing myeloid suppressor cells in renal cell carcinoma patients: a mechanism of tumor evasion. Cancer Res. 65(8), 3044–3048 (2005).
   PubMed Web of Science ®Google Scholar
• Poschke I, Mougiakakos D, Hansson J, Masucci GV, Kiessling R. Immature immunosuppressive CD14+HLA-DR-/low cells in melanoma patients are Stat3hi and overexpress CD80, CD83, and DC-sign. Cancer Res. 70(11), 4335–4345 (2010).
   PubMed Web of Science ®Google Scholar
• Gowda M, Godder K, Kmieciak M et al. Distinct signatures of the immune responses in low risk versus high risk neuroblastoma. J. Transl. Med. 9, 170 (2011).
   PubMed Web of Science ®Google Scholar
• Biswas SK, Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat. Immunol. 11(10), 889–896 (2010).
   PubMed Web of Science ®Google Scholar
• Fridlender ZG, Sun J, Kim S et al. Polarization of tumor-associated neutrophil phenotype by TGF-beta: “N1” versus “N2” TAN. Cancer Cell 16(3), 183–194 (2009).
   PubMed Web of Science ®Google Scholar
• Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. Coordinated regulation of myeloid cells by tumours. Nat. Rev. Immunol. 12(4), 253–268 (2012).
   PubMed Web of Science ®Google Scholar
• Corzo CA, Condamine T, Lu L et al. HIF-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J. Exp. Med. 207(11), 2439–2453 (2010).
   PubMed Web of Science ®Google Scholar
• Fridlender ZG, Sun J, Mishalian I et al. Transcriptomic analysis comparing tumor-associated neutrophils with granulocytic myeloid-derived suppressor cells and normal neutrophils. PLoS ONE 7(2), e31524 (2012).
   Web of Science ®Google Scholar
• Umemura N, Saio M, Suwa T et al. Tumor-infiltrating myeloid-derived suppressor cells are pleiotropic-inflamed monocytes/macrophages that bear M1- and M2-type characteristics. J. Leukoc. Biol. 83(5), 1136–1144 (2008).
   PubMed Web of Science ®Google Scholar
• Movahedi K, Guilliams M, Van Den Bossche J et al. Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood 111(8), 4233–4244 (2008).
   PubMed Web of Science ®Google Scholar
• Maes W, Verschuere T, Van Hoylandt A, Boon L, Van Gool S. Depletion of regulatory T cells in a mouse experimental glioma model through anti-CD25 treatment results in the infiltration of non-immunosuppressive myeloid cells in the brain. Clin. Dev. Immunol. 2013, 952469 (2013).
   PubMedGoogle Scholar
• Zhu X, Fujita M, Snyder LA, Okada H. Systemic delivery of neutralizing antibody targeting CCL2 for glioma therapy. J. Neurooncol. 104(1), 83–92 (2011).
   PubMed Web of Science ®Google Scholar
• Raychaudhuri B, Rayman P, Ireland J et al. Myeloid-derived suppressor cell accumulation and function in patients with newly diagnosed glioblastoma. Neuro Oncol. 13(6), 591–599 (2011).
   PubMed Web of Science ®Google Scholar
• Sippel TR, White J, Nag K et al. Neutrophil degranulation and immunosuppression in patients with GBM: restoration of cellular immune function by targeting arginase I. Clin. Cancer Res. 17(22), 6992–7002 (2011).
   PubMed Web of Science ®Google Scholar
• Rotondo R, Barisione G, Mastracci L et al. IL-8 induces exocytosis of arginase 1 by neutrophil polymorphonuclears in nonsmall cell lung cancer. Int. J. Cancer 125(4), 887–893 (2009).
   PubMed Web of Science ®Google Scholar
• Liu CY, Wang YM, Wang CL et al. Population alterations of L-arginase- and inducible nitric oxide synthase-expressed CD11b+/CD14(−)/CD15+/CD33+ myeloid-derived suppressor cells and CD8+ T lymphocytes in patients with advanced-stage non-small cell lung cancer. J. Cancer Res. Clin. Oncol. 136(1), 35–45 (2010).
   PubMed Web of Science ®Google Scholar
• Rong Y, Durden DL, Van Meir EG, Brat DJ. ‘Pseudopalisading’ necrosis in glioblastoma: a familiar morphologic feature that links vascular pathology, hypoxia, and angiogenesis. J. Neuropathol. Exp. Neurol. 65(6), 529–539 (2006).
   PubMed Web of Science ®Google Scholar
• Waugh DJ, Wilson C. The interleukin-8 pathway in cancer. Clin. Cancer Res. 14(21), 6735–6741 (2008).
   PubMed Web of Science ®Google Scholar
• Kusmartsev S, Nefedova Y, Yoder D, Gabrilovich DI. Antigen-specific inhibition of CD8+ T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species. J. Immunol. 172(2), 989–999 (2004).
   PubMed Web of Science ®Google Scholar
• Rodriguez PC, Ernstoff MS, Hernandez C et al. Arginase I-producing myeloid-derived suppressor cells in renal cell carcinoma are a subpopulation of activated granulocytes. Cancer Res. 69(4), 1553–1560 (2009).
   PubMed Web of Science ®Google Scholar
• Lindau D, Gielen P, Kroesen M, Wesseling P, Adema GJ. The immunosuppressive tumour network: myeloid-derived suppressor cells, regulatory T cells and natural killer T cells. Immunology 138(2), 105–115 (2013).
   PubMed Web of Science ®Google Scholar
• Kotsakis A, Harasymczuk M, Schilling B, Georgoulias V, Argiris A, Whiteside TL. Myeloid-derived suppressor cell measurements in fresh and cryopreserved blood samples. J. Immunol. Methods 381(1–2), 14–22 (2012).
   PubMed Web of Science ®Google Scholar
• Rodriguez PC, Zea AH, Culotta KS, Zabaleta J, Ochoa JB, Ochoa AC. Regulation of T cell receptor CD3zeta chain expression by L-arginine. J. Biol. Chem. 277(24), 21123–21129 (2002).
   PubMed Web of Science ®Google Scholar
• Corzo CA, Cotter MJ, Cheng P et al. Mechanism regulating reactive oxygen species in tumor-induced myeloid-derived suppressor cells. J. Immunol. 182(9), 5693–5701 (2009).
   PubMed Web of Science ®Google Scholar
• Bronte V, Serafini P, Mazzoni A, Segal DM, Zanovello P. L-arginine metabolism in myeloid cells controls T-lymphocyte functions. Trends Immunol. 24(6), 302–306 (2003).
   PubMed Web of Science ®Google Scholar
• Xia Y, Roman LJ, Masters BS, Zweier JL. Inducible nitric-oxide synthase generates superoxide from the reductase domain. J. Biol. Chem. 273(35), 22635–22639 (1998).
   PubMed Web of Science ®Google Scholar
• Hildeman DA, Mitchell T, Aronow B, Wojciechowski S, Kappler J, Marrack P. Control of Bcl-2 expression by reactive oxygen species. Proc. Natl Acad. Sci. USA 100(25), 15035–15040 (2003).
   PubMed Web of Science ®Google Scholar
• Srivastava MK, Sinha P, Clements VK, Rodriguez P, Ostrand-Rosenberg S. Myeloid-derived suppressor cells inhibit T-cell activation by depleting cystine and cysteine. Cancer Res. 70(1), 68–77 (2010).
   PubMed Web of Science ®Google Scholar
• Ishii I, Akahoshi N, Yu XN et al. Murine cystathionine gamma-lyase: complete cDNA and genomic sequences, promoter activity, tissue distribution and developmental expression. Biochem. J. 381(Pt. 1), 113–123 (2004).
   PubMedGoogle Scholar
• Arner ES, Holmgren A. Physiological functions of thioredoxin and thioredoxin reductase. Eur. J. Biochem. 267(20), 6102–6109 (2000).
   PubMedGoogle Scholar
• Angelini G, Gardella S, Ardy M et al. Antigen-presenting dendritic cells provide the reducing extracellular microenvironment required for T lymphocyte activation. Proc. Natl Acad. Sci. USA 99(3), 1491–1496 (2002).
   PubMed Web of Science ®Google Scholar
• Bingisser RM, Tilbrook PA, Holt PG, Kees UR. Macrophage-derived nitric oxide regulates T cell activation via reversible disruption of the Jak3/STAT5 signaling pathway. J. Immunol. 160(12), 5729–5734 (1998).
   PubMed Web of Science ®Google Scholar
• Mazzoni A, Bronte V, Visintin A et al. Myeloid suppressor lines inhibit T cell responses by an NO-dependent mechanism. J. Immunol. 168(2), 689–695 (2002).
   PubMed Web of Science ®Google Scholar
• Harari O, Liao JK. Inhibition of MHC II gene transcription by nitric oxide and antioxidants. Curr. Pharm. Des. 10(8), 893–898 (2004).
   PubMed Web of Science ®Google Scholar
• Rivoltini L, Carrabba M, Huber V et al. Immunity to cancer: attack and escape in T lymphocyte-tumor cell interaction. Immunol. Rev. 188, 97–113 (2002).
   PubMed Web of Science ®Google Scholar
• Molon B, Ugel S, Del Pozzo F et al. Chemokine nitration prevents intratumoral infiltration of antigen-specific T cells. J. Exp. Med. 208(10), 1949–1962 (2011).
   PubMed Web of Science ®Google Scholar
• Nagaraj S, Youn JI, Gabrilovich DI. Reciprocal Relationship between Myeloid-Derived Suppressor Cells and T Cells. J. Immunol. 191(1), 17–23 (2013).
   PubMed Web of Science ®Google Scholar
• Gabrilovich DI, Velders MP, Sotomayor EM, Kast WM. Mechanism of immune dysfunction in cancer mediated by immature Gr-1+ myeloid cells. J. Immunol. 166(9), 5398–5406 (2001).
   PubMed Web of Science ®Google Scholar
• Sinha P, Clements VK, Ostrand-Rosenberg S. Interleukin-13-regulated M2 macrophages in combination with myeloid suppressor cells block immune surveillance against metastasis. Cancer Res. 65(24), 11743–11751 (2005).
   PubMed Web of Science ®Google Scholar
• Huang B, Pan PY, Li Q et al. Gr-1+CD115+ immature myeloid suppressor cells mediate the development of tumor-induced T regulatory cells and T-cell anergy in tumor-bearing host. Cancer Res. 66(2), 1123–1131 (2006).
   PubMed Web of Science ®Google Scholar
• Nagaraj S, Gabrilovich DI. Tumor escape mechanism governed by myeloid-derived suppressor cells. Cancer Res. 68(8), 2561–2563 (2008).
   PubMed Web of Science ®Google Scholar
• Nagaraj S, Gupta K, Pisarev V et al. Altered recognition of antigen is a mechanism of CD8+ T cell tolerance in cancer. Nat. Med. 13(7), 828–835 (2007).
   PubMed Web of Science ®Google Scholar
• Lu T, Ramakrishnan R, Altiok S et al. Tumor-infiltrating myeloid cells induce tumor cell resistance to cytotoxic T cells in mice. J. Clin. Invest. 121(10), 4015–4029 (2011).
   PubMed Web of Science ®Google Scholar
• Morford LA, Elliott LH, Carlson SL, Brooks WH, Roszman TL. T cell receptor-mediated signaling is defective in T cells obtained from patients with primary intracranial tumors. J. Immunol. 159(9), 4415–4425 (1997).
   PubMed Web of Science ®Google Scholar
• Dix AR, Brooks WH, Roszman TL, Morford LA. Immune defects observed in patients with primary malignant brain tumors. J. Neuroimmunol. 100(1–2), 216–232 (1999).
   PubMed Web of Science ®Google Scholar
• Fecci PE, Mitchell DA, Whitesides JF et al. Increased regulatory T-cell fraction amidst a diminished CD4 compartment explains cellular immune defects in patients with malignant glioma. Cancer Res. 66(6), 3294–3302 (2006).
   PubMed Web of Science ®Google Scholar
• Macdonald KP, Rowe V, Clouston AD et al. Cytokine expanded myeloid precursors function as regulatory antigen-presenting cells and promote tolerance through IL-10-producing regulatory T cells. J. Immunol. 174(4), 1841–1850 (2005).
   PubMed Web of Science ®Google Scholar
• Jacobs JF, Nierkens S, Figdor CG, De Vries IJ, Adema GJ. Regulatory T cells in melanoma: the final hurdle towards effective immunotherapy? Lancet Oncol. 13(1), e32–42 (2012).
   PubMed Web of Science ®Google Scholar
• Chen W, Jin W, Hardegen N et al. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J. Exp. Med. 198(12), 1875–1886 (2003).
   PubMed Web of Science ®Google Scholar
• Yu P, Lee Y, Liu W et al. Intratumor depletion of CD4+ cells unmasks tumor immunogenicity leading to the rejection of late-stage tumors. J. Exp. Med. 201(5), 779–791 (2005).
   PubMed Web of Science ®Google Scholar
• Ghiringhelli F, Puig PE, Roux S et al. Tumor cells convert immature myeloid dendritic cells into TGF-beta-secreting cells inducing CD4+CD25+ regulatory T cell proliferation. J. Exp. Med. 202(7), 919–929 (2005).
   PubMed Web of Science ®Google Scholar
• Kim YC, Bhairavabhotla R, Yoon J et al. Oligodeoxynucleotides stabilize Helios-expressing Foxp3+ human T regulatory cells during in vitro expansion. Blood 119(12), 2810–2818 (2012).
   PubMed Web of Science ®Google Scholar
• Thornton AM, Korty PE, Tran DQ et al. Expression of Helios, an Ikaros transcription factor family member, differentiates thymic-derived from peripherally induced Foxp3+ T regulatory cells. J. Immunol. 184(7), 3433–3441 (2010).
   PubMed Web of Science ®Google Scholar
• Yadav M, Louvet C, Davini D et al. Neuropilin-1 distinguishes natural and inducible regulatory T cells among regulatory T cell subsets in vivo. J. Exp. Med. 209(10), 1713–1722, S1711–1719 (2012).
   PubMed Web of Science ®Google Scholar
• Weiss JM, Bilate AM, Gobert M et al. Neuropilin 1 is expressed on thymus-derived natural regulatory T cells, but not mucosa-generated induced Foxp3+ T reg cells. J. Exp. Med. 209(10), 1723–1742, S1721 (2012).
   PubMed Web of Science ®Google Scholar
• Yang R, Cai Z, Zhang Y, Yutzy WHT, Roby KF, Roden RB. CD80 in immune suppression by mouse ovarian carcinoma-associated Gr-1+CD11b+ myeloid cells. Cancer Res. 66(13), 6807–6815 (2006).
   PubMed Web of Science ®Google Scholar
• Serafini P, Mgebroff S, Noonan K, Borrello I. Myeloid-derived suppressor cells promote cross-tolerance in B-cell lymphoma by expanding regulatory T cells. Cancer Res. 68(13), 5439–5449 (2008).
   PubMed Web of Science ®Google Scholar
• Li H, Han Y, Guo Q, Zhang M, Cao X. Cancer-expanded myeloid-derived suppressor cells induce anergy of NK cells through membrane-bound TGF-beta 1. J. Immunol. 182(1), 240–249 (2009).
   PubMed Web of Science ®Google Scholar
• Liu C, Yu S, Kappes J et al. Expansion of spleen myeloid suppressor cells represses NK cell cytotoxicity in tumor-bearing host. Blood 109(10), 4336–4342 (2007).
   PubMed Web of Science ®Google Scholar
• Hoechst B, Voigtlaender T, Ormandy L et al. Myeloid derived suppressor cells inhibit natural killer cells in patients with hepatocellular carcinoma via the NKp30 receptor. Hepatology 50(3), 799–807 (2009).
   PubMed Web of Science ®Google Scholar
• Oberlies J, Watzl C, Giese T et al. Regulation of NK cell function by human granulocyte arginase. J. Immunol. 182(9), 5259–5267 (2009).
   PubMed Web of Science ®Google Scholar
• Alizadeh D, Zhang L, Brown CE, Farrukh O, Jensen MC, Badie B. Induction of anti-glioma natural killer cell response following multiple low-dose intracerebral CpG therapy. Clin. Cancer Res. 16(13), 3399–3408 (2010).
   PubMed Web of Science ®Google Scholar
• Hix LM, Shi YH, Brutkiewicz RR, Stein PL, Wang CR, Zhang M. CD1d-expressing breast cancer cells modulate NKT cell-mediated antitumor immunity in a murine model of breast cancer metastasis. PLoS ONE 6(6), e20702 (2011).
   PubMed Web of Science ®Google Scholar
• Vivier E, Ugolini S, Blaise D, Chabannon C, Brossay L. Targeting natural killer cells and natural killer T cells in cancer. Nat. Rev. Immunol. 12(4), 239–252 (2012).
   PubMed Web of Science ®Google Scholar
• Ambrosino E, Terabe M, Halder RC et al. Cross-regulation between type I and type II NKT cells in regulating tumor immunity: a new immunoregulatory axis. J. Immunol. 179(8), 5126–5136 (2007).
   PubMed Web of Science ®Google Scholar
• Fujii S, Shimizu K, Smith C, Bonifaz L, Steinman RM. Activation of natural killer T cells by alpha-galactosylceramide rapidly induces the full maturation of dendritic cells in vivo and thereby acts as an adjuvant for combined CD4 and CD8 T cell immunity to a coadministered protein. J. Exp. Med. 198(2), 267–279 (2003).
   PubMed Web of Science ®Google Scholar
• Crane CA, Han SJ, Barry JJ, Ahn BJ, Lanier LL, Parsa AT. TGF-beta downregulates the activating receptor NKG2D on NK cells and CD8+ T cells in glioma patients. Neuro Oncol. 12(1), 7–13 (2010).
   PubMed Web of Science ®Google Scholar
• Ko HJ, Lee JM, Kim YJ, Kim YS, Lee KA, Kang CY. Immunosuppressive myeloid-derived suppressor cells can be converted into immunogenic APCs with the help of activated NKT cells: an alternative cell-based antitumor vaccine. J. Immunol. 182(4), 1818–1828 (2009).
   PubMed Web of Science ®Google Scholar
• Kohanbash G, Okada H. Myeloid-derived suppressor cells (MDSCs) in gliomas and glioma-development. Immunol. Invest. 41(6–7), 658–679 (2012).
   PubMed Web of Science ®Google Scholar
• Ko JS, Zea AH, Rini BI et al. Sunitinib mediates reversal of myeloid-derived suppressor cell accumulation in renal cell carcinoma patients. Clin. Cancer Res. 15(6), 2148–2157 (2009).
   PubMed Web of Science ®Google Scholar
• Cao M, Xu Y, Youn JI et al. Kinase inhibitor Sorafenib modulates immunosuppressive cell populations in a murine liver cancer model. Lab. Invest. 91(4), 598–608 (2011).
   PubMed Web of Science ®Google Scholar
• Wu L, Du H, Li Y, Qu P, Yan C. Signal transducer and activator of transcription 3 (Stat3C) promotes myeloid-derived suppressor cell expansion and immune suppression during lung tumorigenesis. Am. J. Pathol. 179(4), 2131–2141 (2011).
   PubMed Web of Science ®Google Scholar
• Roth F, De La Fuente AC, Vella JL, Zoso A, Inverardi L, Serafini P. Aptamer-mediated blockade of IL4Ralpha triggers apoptosis of MDSCs and limits tumor progression. Cancer Res. 72(6), 1373–1383 (2012).
   PubMed Web of Science ®Google Scholar
• Pak AS, Ip G, Wright MA, Young MR. Treating tumor-bearing mice with low-dose gamma-interferon plus tumor necrosis factor alpha to diminish immune suppressive granulocyte-macrophage progenitor cells increases responsiveness to interleukin 2 immunotherapy. Cancer Res. 55(4), 885–890 (1995).
   PubMed Web of Science ®Google Scholar
• Zoglmeier C, Bauer H, Norenberg D et al. CpG blocks immunosuppression by myeloid-derived suppressor cells in tumor-bearing mice. Clin. Cancer Res. 17(7), 1765–1775 (2011).
   PubMed Web of Science ®Google Scholar
• Okada H, Kalinski P, Ueda R et al. Induction of CD8+ T-cell responses against novel glioma-associated antigen peptides and clinical activity by vaccinations with {alpha}-type 1 polarized dendritic cells and polyinosinic-polycytidylic acid stabilized by lysine and carboxymethylcellulose in patients with recurrent malignant glioma. J. Clin. Oncol. 29(3), 330–336 (2011).
   PubMed Web of Science ®Google Scholar
• Zhu X, Nishimura F, Sasaki K et al. Toll like receptor-3 ligand poly-ICLC promotes the efficacy of peripheral vaccinations with tumor antigen-derived peptide epitopes in murine CNS tumor models. J. Transl. Med. 5, 10 (2007).
   PubMed Web of Science ®Google Scholar
• Tu SP, Jin H, Shi JD et al. Curcumin induces the differentiation of myeloid-derived suppressor cells and inhibits their interaction with cancer cells and related tumor growth. Cancer Prev. Res. 5(2), 205–215 (2012).
   PubMed Web of Science ®Google Scholar
• Yoshimura T, Robinson EA, Tanaka S, Appella E, Kuratsu J, Leonard EJ. Purification and amino acid analysis of two human glioma-derived monocyte chemoattractants. J. Exp. Med. 169(4), 1449–1459 (1989).
   PubMed Web of Science ®Google Scholar
• Gebhardt C, Nemeth J, Angel P, Hess J. S100A8 and S100A9 in inflammation and cancer. Biochem. Pharmacol. 72(11), 1622–1631 (2006).
   PubMed Web of Science ®Google Scholar
• Murat A, Migliavacca E, Hussain SF et al. Modulation of angiogenic and inflammatory response in glioblastoma by hypoxia. PLoS ONE 4(6), e5947 (2009).
   PubMed Web of Science ®Google Scholar
• Baggio R, Emig FA, Christianson DW, Ash DE, Chakder S, Rattan S. Biochemical and functional profile of a newly developed potent and isozyme-selective arginase inhibitor. J. Pharmacol. Exp. Ther. 290(3), 1409–1416 (1999).
   PubMed Web of Science ®Google Scholar
• Berkowitz DE, White R, Li D et al. Arginase reciprocally regulates nitric oxide synthase activity and contributes to endothelial dysfunction in aging blood vessels. Circulation 108(16), 2000–2006 (2003).
   PubMed Web of Science ®Google Scholar
• Santhanam L, Christianson DW, Nyhan D, Berkowitz DE. Arginase and vascular aging. J. Appl. Physiol. 105(5), 1632–1642 (2008).
   PubMed Web of Science ®Google Scholar
• Yang XD, Ma JY, Barger MW, Ma JK. Transport and utilization of arginine and arginine-containing peptides by rat alveolar macrophages. Pharm. Res. 19(6), 825–831 (2002).
   PubMed Web of Science ®Google Scholar
• Scheurer ME, El-Zein R, Thompson PA et al. Long-term anti-inflammatory and antihistamine medication use and adult glioma risk. Cancer Epidemiol. Biomarkers Prev. 17(5), 1277–1281 (2008).
   PubMed Web of Science ®Google Scholar
• Sinha P, Clements VK, Fulton AM, Ostrand-Rosenberg S. Prostaglandin E2 promotes tumor progression by inducing myeloid-derived suppressor cells. Cancer Res. 67(9), 4507–4513 (2007).
   PubMed Web of Science ®Google Scholar
• Rodriguez PC, Quiceno DG, Ochoa AC. L-arginine availability regulates T-lymphocyte cell-cycle progression. Blood 109(4), 1568–1573 (2007).
   PubMed Web of Science ®Google Scholar
• Bierie B, Moses HL. Transforming growth factor beta (TGF-beta) and inflammation in cancer. Cytokine Growth Factor Rev. 21(1), 49–59 (2010).
   PubMed Web of Science ®Google Scholar
• Laterra JJ, Grossman SA, Carson KA et al. Suramin and radiotherapy in newly diagnosed glioblastoma: phase 2 NABTT CNS Consortium study. Neuro Oncol. 6(1), 15–20 (2004).
   PubMed Web of Science ®Google Scholar
• Grossman SA, Phuphanich S, Lesser G et al. Toxicity, efficacy, and pharmacology of suramin in adults with recurrent high-grade gliomas. J. Clin. Oncol. 19(13), 3260–3266 (2001).
   PubMed Web of Science ®Google Scholar
• Hjelmeland MD, Hjelmeland AB, Sathornsumetee S et al. SB-431542, a small molecule transforming growth factor-beta-receptor antagonist, inhibits human glioma cell line proliferation and motility. Mol. Cancer Ther. 3(6), 737–745 (2004).
   PubMed Web of Science ®Google Scholar
• Uhl M, Aulwurm S, Wischhusen J et al. SD-208, a novel transforming growth factor beta receptor I kinase inhibitor, inhibits growth and invasiveness and enhances immunogenicity of murine and human glioma cells in vitro and in vivo. Cancer Res. 64(21), 7954–7961 (2004).
   PubMed Web of Science ®Google Scholar
• Yang XD, Ai W, Asfaha S et al. Histamine deficiency promotes inflammation-associated carcinogenesis through reduced myeloid maturation and accumulation of CD11b+Ly6G+ immature myeloid cells. Nat. Med. 17(1), 87–95 (2011).
   PubMed Web of Science ®Google Scholar
• Scheurer ME, Amirian ES, Davlin SL, Rice T, Wrensch M, Bondy ML. Effects of antihistamine and anti-inflammatory medication use on risk of specific glioma histologies. Int. J. Cancer 129(9), 2290–2296 (2011).
   PubMed Web of Science ®Google Scholar
• Prosniak M, Harshyne LA, Andrews DW et al. Glioma grade is associated with the accumulation and activity of cells bearing M2 monocyte markers. Clin. Cancer Res. 19(14), 3776–3786 (2013).
   PubMed Web of Science ®Google Scholar
• Kjellman C, Olofsson SP, Hansson O et al. Expression of TGF-beta isoforms, TGF-beta receptors, and SMAD molecules at different stages of human glioma. Int. J. Cancer 89(3), 251–258 (2000).
   PubMed Web of Science ®Google Scholar
• Nitta T, Hishii M, Sato K, Okumura K. Selective expression of interleukin-10 gene within glioblastoma multiforme. Brain Res. 649(1–2), 122–128 (1994).
   PubMed Web of Science ®Google Scholar
• Wei J, Barr J, Kong LY et al. Glioma-associated cancer-initiating cells induce immunosuppression. Clin. Cancer Res. 16(2), 461–473 (2010).
   PubMed Web of Science ®Google Scholar
• Heimberger AB, Abou-Ghazal M, Reina-Ortiz C et al. Incidence and prognostic impact of FoxP3+ regulatory T cells in human gliomas. Clin. Cancer Res. 14(16), 5166–5172 (2008).
   PubMed Web of Science ®Google Scholar
• Komohara Y, Ohnishi K, Kuratsu J, Takeya M. Possible involvement of the M2 anti-inflammatory macrophage phenotype in growth of human gliomas. J. Pathol. 216(1), 15–24 (2008).
   PubMed Web of Science ®Google Scholar