Glioblastoma-infiltrated innate immune cells resemble M0 macrophage phenotype

JCI Insight

Volumn 1, Issue 2, 2016, Pages

  Gabrusiewicz, Konrad ^a   Rodriguez, Benjamin ^b   Wei, Jun ^a   Hashimoto, Yuuri ^a   Healy, Luke M ^c   Maiti, Sourindra N ^a   Thomas, Ginu ^a   Zhou, Shouhao ^a   Wang, Qianghu ^a   Elakkad, Ahmed ^a   Liebelt, Brandon D ^a   Yaghi, Nasser K ^a   Ezhilarasan, Ravesanker ^a   Huang, Neal ^a   Weinberg, Jeffrey S ^a   Prabhu, Sujit S ^a   Rao, Ganesh ^a   Sawaya, Raymond ^a   Langford, Lauren A ^a   Bruner, Janet M ^a   Fuller, Gregory N ^a   Bar Or, Amit ^c   Li, Wei ^b   Colen, Rivka R ^a   Curran, Michael A ^a   Bhat, Krishna P ^a   Antel, Jack P ^c   Cooper, Laurence J ^a   Sulman, Erik P ^a   Heimberger, Amy B ^a   more..

^a UNIVERSITY OF TEXAS   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84975276172     PISSN: None     EISSN: 23793708     Source Type: Journal    
DOI: 10.1172/jci.insight.85841     Document Type: Article

References (73)

1. Badie B, Schartner JM. Flow cytometric characterization of tumor-associated macrophages in experimental gliomas. Neurosurgery. 2000; 46(4):957-961.
2. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A. Physiology of microglia. Physiol Rev. 2011; 91(2):461-553.
3. Roggendorf W, Strupp S, Paulus W. Distribution and characterization of microglia/macrophages in human brain tumors. Acta Neuropathol (Berl). 1996; 92(3):288-293.
4. Morimura T, et al. Monocyte subpopulations in human gliomas: expression of Fc and complement receptors and correlation with tumor proliferation. Acta Neuropathol (Berl). 1990; 80(3):287-294.
5. Wierzba-Bobrowicz T, Kuchna I, Matyja E. Reaction of microglial cells in human astrocytomas (preliminary report). Folia Neuropathol. 1994; 32(4):251-252.
6. Graeber MB, Scheithauer BW, Kreutzberg GW. Microglia in brain tumors. Glia. 2002; 40(2):252-259.
7. Sica A, et al. Macrophage polarization in tumour progression. Semin Cancer Biol. 2008; 18(5):349-355.
8. Wu A, et al. Glioma cancer stem cells induce immunosuppressive macrophages/microglia. Neuro Oncol. 2010; 12(11):1113-1125.
9. Kong LY, et al. Intratumoral mediated immunosuppression is prognostic in genetically engineered murine models of glioma and correlates to immunotherapeutic responses. Clin Cancer Res. 2010; 16(23):5722-5733.
10. 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. 2006; 8(3):261-279.
11. Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol. 2012; 12(4):253-268.
12. Umemura N, et al. Tumor-infiltrating myeloid-derived suppressor cells are pleiotropic-inflamed monocytes/macrophages that bear M1- and M2-type characteristics. J Leukoc Biol. 2008; 83(5):1136-1144.
13. 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. 2010; 223(1-2):20-30.
14. Martinez FO, Sica A, Mantovani A, Locati M. Macrophage activation and polarization. Front Biosci. 2008; 13:453-461.
15. Pollard JW. Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer. 2004; 4(1):71-78.
16. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 2004; 25(12):677-686.
17. Komohara Y, Ohnishi K, Kuratsu J, Takeya M. Possible involvement of the M2 anti-inflammatory macrophage phenotype in growth of human gliomas. J Pathol. 2008; 216(1):15-24.
18. Prosniak M, et al. Glioma grade is associated with the accumulation and activity of cells bearing M2 monocyte markers. Clin Cancer Res. 2013; 19(14):3776-3786.
19. Gabrusiewicz K, et al. Macrophage ablation reduces M2-like populations and jeopardizes tumor growth in a MAFIA-based glioma model. Neoplasia. 2015; 17(4):374-384.
20. Gielen PR, et al. Increase in both CD14-positive and CD15-positive myeloid-derived suppressor cell subpopulations in the blood of patients with glioma but predominance of CD15-positive myeloid-derived suppressor cells in glioma tissue. J Neuropathol Exp Neurol. 2015; 74(5):390-400.
21. Raychaudhuri B, et al. Myeloid-derived suppressor cell accumulation and function in patients with newly diagnosed glioblastoma. Neuro Oncol. 2011; 13(6):591-599.
22. Wang J, et al. The clinical significance of tumor-infiltrating neutrophils and neutrophil-to-CD8+ lymphocyte ratio in patients with resectable esophageal squamous cell carcinoma. J Transl Med. 2014; 12:7.
23. Hao S, Andersen M, Yu H. Detection of immune suppressive neutrophils in peripheral blood samples of cancer patients. Am J Blood Res. 2013; 3(3):239-245.
24. Ellert-Miklaszewska A, Dabrowski M, Lipko M, Sliwa M, Maleszewska M, Kaminska B. Molecular definition of the pro-tumorigenic phenotype of glioma-activated microglia. Glia. 2013; 61(7):1178-1190.
25. Zhang H, Qian PY, Ravasi T. Selective phosphorylation during early macrophage differentiation. Proteomics. 2015; 15(21):3731-3743.
26. Gabrusiewicz K, Ellert-Miklaszewska A, Lipko M, Sielska M, Frankowska M, Kaminska B. Characteristics of the alternative phenotype of microglia/macrophages and its modulation in experimental gliomas. PLoS One. 2011; 6(8):e23902.
27. 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.
28. Sedgwick JD, Schwender S, Imrich H, Dorries R, Butcher GW, ter Meulen V. Isolation and direct characterization of resident microglial cells from the normal and inflamed central nervous system. Proc Natl Acad Sci U S A. 1991; 88(16):7438-7442.
29. Szulzewsky F, et al. Glioma-associated microglia/macrophages display an expression profile different from m1 and m2 polarization and highly express gpnmb and spp1. PLoS One. 2015; 10(2):e0116644.
30. Pinton L, et al. Activated T cells sustain myeloid-derived suppressor cell-mediated immune suppression [published online ahead of print December 18, 2015]. Oncotarget. doi:10.18632/oncotarget.6662.
31. Yu J, et al. Myeloid-derived suppressor cells suppress antitumor immune responses through IDO expression and correlate with lymph node metastasis in patients with breast cancer. J Immunol. 2013; 190(7):3783-3797.
32. Lechner MG, et al. Functional characterization of human Cd33+ and Cd11b+ myeloid-derived suppressor cell subsets induced from peripheral blood mononuclear cells co-cultured with a diverse set of human tumor cell lines. J Transl Med. 2011; 9:90.
33. Doucette TA, et al. Immune heterogeneity of glioblastoma subtypes: extrapolation from the cancer genome atlas. Cancer Immunol Res. 2013; 1(2):112-122.
34. Verhaak RG, et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell. 2010; 17(1):98-110.
35. Radhakrishnan A, et al. A pathway map of prolactin signaling. J Cell Commun Signal. 2012; 6(3):169-173.
36. Martinez FO, Gordon S, Locati M, Mantovani A. Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J Immunol. 2006; 177(10):7303-7311.
37. Derlindati E, et al. Transcriptomic analysis of human polarized macrophages: more than one role of alternative activation?. PLoS One. 2015; 10(3):e0119751.
38. Squadrito ML, Etzrodt M, De Palma M, Pittet MJ. MicroRNA-mediated control of macrophages and its implications for cancer. Trends Immunol. 2013; 34(7):350-359.
39. Hsieh CS, Heimberger AB, Gold JS, O'Garra A, Murphy KM. Differential regulation of T helper phenotype development by interleukins 4 and 10 in an alpha beta T-cell-receptor transgenic system. Proc Natl Acad Sci U S A. 1992; 89(13):6065-6069.
40. Hattermann K, et al. Chemokine expression profile of freshly isolated human glioblastoma-associated macrophages/microglia. Oncol Rep. 2014; 32(1):270-276.
41. Mieczkowski J, et al. Down-regulation of IKKbeta expression in glioma-infiltrating microglia/macrophages is associated with defective inflammatory/immune gene responses in glioblastoma. Oncotarget. 2015; 6(32):33077-33090.
42. Tran CT, et al. Differential expression of MHC class II molecules by microglia and neoplastic astroglia: relevance for the escape of astrocytoma cells from immune surveillance. Neuropathol Appl Neurobiol. 1998; 24(4):293-301.
43. Dubinski D, et al. CD4+ T effector memory cell dysfunction is associated with the accumulation of granulocytic myeloid-derived suppressor cells in glioblastoma patients [published online ahead of print November 17, 2015]. Neuro Oncol.doi:10.1093/ neuonc/nov280.
44. Fu C, et al. Identification of a novel membrane protein, HP59, with therapeutic potential as a target of tumor angiogenesis. Clin Cancer Res. 2001; 7(12):4182-4194.
45. Fujita M, et al. COX-2 blockade suppresses gliomagenesis by inhibiting myeloid-derived suppressor cells. Cancer Res. 2011; 71(7):2664-2674.
46. Kohanbash G, et al. GM-CSF promotes the immunosuppressive activity of glioma-infiltrating myeloid cells through interleukin-4 receptor-alpha. Cancer Res. 2013; 73(21):6413-6423.
47. Verschuere T, et al. Glioma-derived galectin-1 regulates innate and adaptive antitumor immunity. Int J Cancer. 2014; 134(4):873-884.
48. Pello OM, et al. Role of c-MYC in alternative activation of human macrophages and tumor-associated macrophage biology. Blood. 2012; 119(2):411-421.
49. Beyer M, et al. High-resolution transcriptome of human macrophages. PLoS One. 2012; 7(9):e45466.
50. O'Neill LA, Hardie DG. Metabolism of inflammation limited by AMPK and pseudo-starvation. Nature. 2013; 493(7432):346-355.
51. Kramer PA, Ravi S, Chacko B, Johnson MS, Darley-Usmar VM. A review of the mitochondrial and glycolytic metabolism in human platelets and leukocytes: implications for their use as bioenergetic biomarkers. Redox biology. 2014; 2:206-210.
52. Yan J, et al. FGL2 as a multimodality regulator of tumor-mediated immune suppression and therapeutic target in gliomas. J Natl Cancer Inst. 2015; 107(8):djv137.
53. Bhat KP, et al. Mesenchymal differentiation mediated by NF-kappaB promotes radiation resistance in glioblastoma. Cancer Cell. 2013; 24(3):331-346.
54. Jan HJ, et al. Osteopontin regulates human glioma cell invasiveness and tumor growth in mice. Neuro Oncol. 2010; 12(1):58-70.
55. Engler JR, et al. Increased microglia/macrophage gene expression in a subset of adult and pediatric astrocytomas. PLoS One. 2012; 7(8):e43339.
56. Lu DY, Yeh WL, Huang SM, Tang CH, Lin HY, Chou SJ. Osteopontin increases heme oxygenase-1 expression and subsequently induces cell migration and invasion in glioma cells. Neuro Oncol. 2012; 14(11):1367-1378.
57. Sreekanthreddy P, et al. Identification of potential serum biomarkers of glioblastoma: serum osteopontin levels correlate with poor prognosis. Cancer Epidemiol Biomarkers Prev. 2010; 19(6):1409-1422.
58. Bergenfelz C, Janols H, Wullt M, Jirstrom K, Bredberg A, Leandersson K. Wnt5a inhibits human monocyte-derived myeloid dendritic cell generation. Scand J Immunol. 2013; 78(2):194-204.
59. Pukrop T, et al. Wnt 5a signaling is critical for macrophage-induced invasion of breast cancer cell lines. Proc Natl Acad Sci U S A. 2006; 103(14):5454-5459.
60. van Bruggen N, et al. VEGF antagonism reduces edema formation and tissue damage after ischemia/reperfusion injury in the mouse brain. J Clin Invest. 1999; 104(11):1613-1620.
61. Schmidt H, et al. Elevated neutrophil and monocyte counts in peripheral blood are associated with poor survival in patients with metastatic melanoma: a prognostic model. Br J Cancer. 2005; 93(3):273-278.
62. Fossati G, Ricevuti G, Edwards SW, Walker C, Dalton A, Rossi ML. Neutrophil infiltration into human gliomas. Acta Neuropathol. 1999; 98(4):349-354.
63. McNamara MG, et al. Factors impacting survival following second surgery in patients with glioblastoma in the temozolomide treatment era, incorporating neutrophil/lymphocyte ratio and time to first progression. J Neurooncol. 2014; 117(1):147-152.
64. Fallah P, et al. miR-146a and miR-150 promote the differentiation of CD133+ cells into T-lymphoid lineage. Mol Biol Rep. 2013; 40(8):4713-4719.
65. Xiao WZ, Lu AQ, Liu XW, Li Z, Zi Y, Wang ZW. Role of miRNA-146 in proliferation and differentiation of mouse neural stem cells. Biosci Rep. 2015; 35(5):e00245.
66. Xu S, et al. Effect of miR-142-3p on the M2 macrophage and therapeutic efficacy against murine glioblastoma. J Natl Cancer Inst. 2014; 106(8):dju162.
67. Wei J, et al. miR-124 Inhibits STAT3 signaling to enhance T cell-mediated immune clearance of glioma. Cancer Res. 2013; 73(13):3913-3926.
68. Ziegler-Heitbrock HW, Ulevitch RJ. CD14: cell surface receptor and differentiation marker. Immunol Today. 1993; 14(3):121-125.
69. Dolmans MM, et al. Evaluation of Liberase, a purified enzyme blend, for the isolation of human primordial and primary ovarian follicles. Hum Reprod. 2006; 21(2):413-420.
70. Hussain SF, Yang D, Suki D, Grimm E, Heimberger AB. Innate immune functions of microglia isolated from human glioma patients. J Transl Med. 2006; 4(1): PMC1501057.
71. Nikodemova M, Watters JJ. Efficient isolation of live microglia with preserved phenotypes from adult mouse brain. J Neuroinflammation. 2012; 9:147.
72. Durafourt BA, et al. Comparison of polarization properties of human adult microglia and blood-derived macrophages. Glia. 2012; 60(5):717-727.
73. Melief J, et al. Phenotyping primary human microglia: tight regulation of LPS responsiveness. Glia. 2012; 60(10):1506-1517.