Increasing glioma-associated monocytes leads to increased intratumoral and systemic myeloid-derived suppressor cells in a murine model

Neuro-Oncology

Volumn 17, Issue 7, 2015, Pages 978-991

  Chae, Michael ^a   Peterson, Timothy E ^a   Balgeman, Alexis ^a   Chen, Selby ^a   Zhang, Lei ^a   Renner, Danielle N ^b   Johnson, Aaron J ^b   Parney, Ian F ^a  

^a Department of Neurological Surgery ^*  (United States)

^b MAYO GRADUATE SCHOOL   (United States)

Author keywords

GL261; Glioma; immunosuppression; myeloid derived suppressor cell; tumor associated macrophage.

Indexed keywords

CD11B ANTIGEN; GREEN FLUORESCENT PROTEIN; LUCIFERASE; OVALBUMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; BONE MARROW CELL; CANCER GROWTH; CANCER SURVIVAL; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; GLIOBLASTOMA; IMMUNE DEFICIENCY; IMMUNE RESPONSE; IN VIVO STUDY; MOUSE; MURINE MODEL; MYELOID DERIVED SUPPRESSOR CELL; NONHUMAN; SPLEEN CELL; SUPPRESSOR CELL; TUMOR ASSOCIATED LEUKOCYTE; TUMOR ASSOCIATED MONOCYTE; ANIMAL; BRAIN TUMOR; C57BL MOUSE; DISEASE MODEL; GLIOMA; IMMUNOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SPLEEN; TUMOR CELL LINE;

ANIMALS; BONE MARROW CELLS; BRAIN NEOPLASMS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; GLIOMA; MICE; MICE, INBRED C57BL; MYELOID CELLS; SPLEEN;

EID: 84936797498     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/nou343     Document Type: Article

References (36)

1. Stupp R, Mason WP, van den Bent MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352(10):987-996.
2. 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. 2005;11(15):5515-5525.
3. Sampson JH, Heimberger AB, Archer GE, et al. Immunologic escape after prolonged progression-free survival with epidermal growth factor receptor variant III peptide vaccination in patients with newly diagnosed glioblastoma. J Clin Oncol. 2010;28(31): 4722-4729.
4. Parney IF, Farr-Jones MA, Chang LJ, et al. Human glioma immunobiology in vitro: Implications for immunogene therapy. Neurosurgery. 2000;46(5):1169-1177; discussion 1177-1178.
5. Parsa AT, Waldron JS, Panner A, et al. Loss of tumor suppressor PTEN function increases B7-H1 expression and immunoresistance in glioma. Nat Med. 2007;13(1):84-88.
6. Parney IF, Waldron JS, Parsa AT. Flow cytometry and in vitro analysis of human glioma-associated macrophages. Laboratory investigation. J Neurosurg. 2009;110(3):572-582.
7. Watters JJ, Schartner JM, Badie B. Microglia function in brain tumors. J Neurosci Res. 2005;81(3):447-455.
8. Rodrigues JC, Gonzalez GC, Zhang L, et al. Normal human monocytes exposed to glioma cells acquire myeloid-derived suppressor cell-like properties. Neuro Oncol. 2010;12(4): 351-365.
9. Gustafson MP, Lin Y, New KC, et al. Systemic immune suppression in glioblastoma: The interplay between CD14+HLA-DRlo/neg monocytes, tumor factors, and dexamethasone. Neuro Oncol. 2010;12(7):631-644.
10. Dix AR, Brooks WH, Roszman TL, et al. Immune defects observed in patients with primary malignant brain tumors. J Neuroimmunol. 1999;100(1-2):216-232.
11. 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. 2006;66(6):3294-3302.
12. Parney IF. Basic concepts in glioma immunology. Adv Exp Med Biol. 2012;746:42-52.
13. 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. 2006;66(2):1123-1131.
14. 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. 2005;174(4):1841-1850.
15. Bell MP, Renner DN, Johnson AJ, et al. A CD8 T-cell epitope variant enhances immune targeting to a recombinant picornavirus vaccine antigen. Viral Immunol. 2014;27(7):361-366.
16. Hao C, Parney IF, Roa WH, et al. Cytokine and cytokine receptor mRNA expression in human glioblastomas: Evidence of Th1, Th2 and Th3 cytokine dysregulation. Acta Neuropathol. 2002;103(2): 171-178.
17. Prins RM, Odesa SK, Liau LM. Immunotherapeutic targeting of shared melanoma-associated antigens in a murine glioma model. Cancer Res. 2003;63(23):8487-8491.
18. Umemura N, Saio M, Suwa T, et al. Tumor-infiltrating myeloidderived suppressor cells are pleiotropic-inflamed monocytes/macrophages that bear M1-and M2-type characteristics. J Leukocyte Biol. 2008;83(5):1136-1144.
19. Zhu X, Fujita M, Snyder LA, et al. Systemic delivery of neutralizing antibody targeting CCL2 for glioma therapy. J Neurooncol. 2011; 104(1):83-92.
20. Youn JI, Kumar V, Collazo M, et al. Epigenetic silencing of retinoblastoma gene regulates pathologic differentiation of myeloid cells in cancer. Nat Immunol. 2013;14(3):211-220.
21. Bloch O, Crane CA, Kaur R, et al. Gliomas promote immunosuppression through induction of B7-H1 expression in tumor-associated macrophages. Clin Cancer Res. 2013;19(12): 3165-3175.
22. Parsa AT, Chakrabarti I, Hurley PT, et al. Limitations of the C6/Wistar rat intracerebral glioma model: Implications for evaluating immunotherapy. Neurosurgery. 2000;47(4):993-999; discussion 999-1000.
23. Sarkaria JN, Carlson BL, Schroeder MA, et al. Use of an orthotopic xenograft model for assessing the effect of epidermal growth factor receptor amplification on glioblastoma radiation response. Clin Cancer Res. 2006;12(7 Pt 1):2264-2271.
24. Kelly JJ, Stechishin O, Chojnacki A, et al. Proliferation of human glioblastoma stem cells occurs independently of exogenous mitogens. Stem Cells. 2009;27(8):1722-1733.
25. Fujita M, Zhu X, Ueda R, et al. Effective immunotherapy against murine gliomas using type 1 polarizing dendritic cells-significant roles of CXCL10. Cancer Res. 2009;69(4):1587-1595.
26. Kuwashima N, Nishimura F, Eguchi J, et al. Delivery of dendritic cells engineered to secrete IFN-alpha into central nervous system tumors enhances the efficacy of peripheral tumor cell vaccines: Dependence on apoptotic pathways. J Immunol. 2005; 175(4):2730-2740.
27. Olin MR, Andersen BM, Zellmer DM, et al. Superior efficacy of tumor cell vaccines grown in physiologic oxygen. Clin Cancer Res. 2010; 16(19):4800-4808.
28. Fujita M, Kohanbash G, Fellows-Mayle W, et al. COX-2 blockade suppresses gliomagenesis by inhibiting myeloid-derived suppressor cells. Cancer Res. 2011;71(7):2664-2674.
29. Humphries W, Wei J, Sampson JH, et al. The role of tregs in glioma-mediated immunosuppression: Potential target for intervention. Neurosurg Clin North Am. 2010;21(1):125-137.
30. Savage PA, Malchow S, Leventhal DS. Basic principles of tumor-associated regulatory T cell biology. Trends Immunol. 2013;34(1):33-40.
31. Wainwright DA, Sengupta S, Han Y, et al. Thymus-derived rather than tumor-induced regulatory T cells predominate in brain tumors. Neuro Oncol. 2011;13(12):1308-1323.
32. Whiteside TL, Schuler P, Schilling B. Induced and natural regulatory T cells in human cancer. Expert Opin Biol Ther. 2012; 12(10):1383-1397.
33. Fricke I, Mirza N, Dupont J, et al. Vascular endothelial growth factor-trap overcomes defects in dendritic cell differentiation but does not improve antigen-specific immune responses. Clin Cancer Res. 2007;13(16):4840-4848.
34. Cantini G, Pisati F, Mastropietro A, et al. A critical role for regulatory T cells in driving cytokine profiles of Th17 cells and their modulation of glioma microenvironment. Cancer Immunol Immunother. 2011;60(12):1739-1750.
35. Maes W, Rosas GG, Verbinnen B, et al. DC vaccination with anti-CD25 treatment leads to long-term immunity against experimental glioma. Neuro Oncol. 2009;11(5):529-542.
36. Montero AJ, Diaz-Montero CM, Kyriakopoulos CE, et al. Myeloid-derived suppressor cells in cancer patients: A clinical perspective. J Immunother. 2012;35(2):107-115.