Monocyte-derived cells of the brain and malignant gliomas: The double face of janus

World Neurosurgery

Volumn 82, Issue 6, 2014, Pages 1171-1186

  Kushchayev, Sergiy V ^a   Kushchayeva, Yevgeniya S ^a,b   Wiener, Philip C ^a   Scheck, Adrienne C ^a   Badie, Behnam ^c   Preul, Mark C ^a  

^a ST JOSEPH'S HOSPITAL AND MEDICAL CENTER   (United States)

^b WASHINGTON HOSPITAL CENTER   (United States)

^c CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

Dendritic cells; Glioblastoma; Macrophages; Microglia; Monocytes

Indexed keywords

ANGIOPOIETIN RECEPTOR;

BIOSYNTHESIS; BONE MARROW CELL; BRAIN; BRAIN TUMOR; CYTOLOGY; DENDRITIC CELL; GLIOMA; HUMAN; INFLAMMATION; MACROPHAGE; MICROGLIA; MONOCYTE; PATHOLOGY;

BRAIN; BRAIN NEOPLASMS; DENDRITIC CELLS; GLIOMA; HUMANS; INFLAMMATION; MACROPHAGES; MICROGLIA; MONOCYTES; MYELOID CELLS; RECEPTOR, TIE-2;

EID: 84917677630     PISSN: 18788750     EISSN: 18788769     Source Type: Journal    
DOI: 10.1016/j.wneu.2012.11.059     Document Type: Review

References (160)

1. Insights of the decade, breakthrough of the year 2010. Available at: http://www.sciencemag.org/site/special/insights 2010 2011. Accessed January 12, 2012
2. M.G. Abdelwahab, S.V. Kushchayev, N.L. Martirosyan, T. Sankar, A.C. Scheck, L.L. Eggink, J.K. Hoober, and M.C. Preul Administration of a synthetic peptide mimetic of macrophage activating factor improves response to radiotherapy in a murine glioma model J Neurosurg 111 2009 420
3. O. Aichel Chapter XIII. Uber Zellverschmelzung mit qualitative abnormer chromosomenverteilung W. Roux, Vorträge und Aufsätze über Entvickelungsmechanik Der Organismen 1911 Wilhelm Engelmann Leipzig, Germany
4. B. Ajami, J.L. Bennett, C. Krieger, W. Tetzlaff, and F.M. Rossi Local self-renewal can sustain CNS microglia maintenance and function throughout adult life Nat Neurosci 10 2007 1538 1543
5. E. Albesiano, J.E. Han, and M. Lim Mechanisms of local immunoresistance in glioma Neurosurg Clin N Am 21 2010 17 29
6. E. Allard, C. Passirani, E. Garcion, P. Pigeon, A. Vessieres, G. Jaouen, and J.P. Benoit Lipid nanocapsules loaded with an organometallic tamoxifen derivative as a novel drug-carrier system for experimental malignant gliomas J Control Release 130 2008 146 153
7. B. Almand, J.I. Clark, E. Nikitina, J. van Beynen, N.R. English, S.C. Knight, D.P. Carbone, and D.I. Gabrilovich Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer J Immunol 166 2001 678 689
8. C. Auffray, D. Fogg, M. Garfa, G. Elain, O. Join-Lambert, S. Kayal, S. Sarnacki, A. Cumano, G. Lauvau, and F. Geissmann Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior Science 317 2007 666 670
9. C.M. az-Montero, M.L. Salem, M.I. Nishimura, E. Garrett-Mayer, D.J. Cole, and A.J. Montero Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin-cyclophosphamide chemotherapy Cancer Immunol Immunother 58 2009 49 59
10. B. Badie, and J.M. Schartner Flow cytometric characterization of tumor-associated macrophages in experimental gliomas Neurosurgery 46 2000 957 961
11. S.K. Baek, A.R. Makkouk, T. Krasieva, C.H. Sun, S.J. Madsen, and H. Hirschberg Photothermal treatment of glioma; an in vitro study of macrophage-mediated delivery of gold nanoshells J Neurooncol 104 2011 439 448
12. B. Barleon, S. Sozzani, D. Zhou, H.A. Weich, A. Mantovani, and D. Marme Migration of human monocytes in response to vascular endothelial growth factor (VEGF) is mediated via the VEGF receptor flt-1 Blood 87 1996 3336 3343
13. M.D. Bell, R. Lopez-Gonzalez, L. Lawson, D. Hughes, I. Fraser, S. Gordon, and V.H. Perry Upregulation of the macrophage scavenger receptor in response to different forms of injury in the CNS Neurocytol 23 1994 605 613
14. L. Bingle, N.J. Brown, and C.E. Lewis The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies J Pathol 196 2002 254 265
15. S.K. Biswas, and A. Mantovani Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm Nat Immunol 11 2010 889 896
16. H. Brem, and J. Folkman Analysis of experimental antiangiogenic therapy J Pediatr Surg 28 1993 445 450
17. K. Bulloch, M.M. Miller, J. Gal-Toth, T.A. Milner, A. Gottfried-Blackmore, E.M. Waters, U.W. Kaunzner, K. Liu, R. Lindquist, M.C. Nussenzweig, R.M. Steinman, and B.S. McEwen CD11c/EYFP transgene illuminates a discrete network of dendritic cells within the embryonic, neonatal, adult, and injured mouse brain J Comp Neurol 508 2008 687 710
18. O. Butovsky, S. Bukshpan, G. Kunis, S. Jung, and M. Schwartz Microglia can be induced by IFNgamma or IL-4 to express neural or dendritic-like markers Mol Cell Neurosci 35 2007 490 500
19. N. Butowski Immunostimulants for malignant gliomas Neurosurg Clin N Am 21 2010 53 65
20. M.J. Carson, J.C. Thrash, and B. Walter The cellular response in neuroinflammation: the role of leukocytes, microglia and astrocytes in neuronal death and survival Clin Neurosci Res 6 2006 237 245
21. A.K. Chakraborty, S.J. de Freitas, E.M. Espreafico, and J.M. Pawelek Human monocyte x mouse melanoma fusion hybrids express human gene Gene 275 2001 103 106
22. W.Y. Chan, S. Kohsaka, and P. Rezaie The origin and cell lineage of microglia: new concepts Brain Res Rev 53 2007 344 354
23. S.B. Coffelt, A.O. Tal, A. Scholz, P.M. De, S. Patel, C. Urbich, S.K. Biswas, C. Murdoch, K.H. Plate, Y. Reiss, and C.E. Lewis Angiopoietin-2 regulates gene expression in TIE2-expressing monocytes and augments their inherent proangiogenic functions Cancer Res 70 2010 5270 5280
24. C.A. Crane, S.J. Han, J.J. Barry, B.J. Ahn, L.L. Lanier, and A.T. Parsa TGF-beta downregulates the activating receptor NKG2D on NK cells and CD8 T cells in glioma patients Neuro Oncol 12 2010 7 13
25. P.M. D'Agostino, A. Gottfried-Blackmore, N. Anandasabapathy, and K. Bulloch Brain dendritic cells: biology and pathology Acta Neuropathol 124 2012 599 614
26. N. Davoust, C. Vuaillat, G. Androdias, and S. Nataf From bone marrow to microglia: barriers and avenues Trends Immunol 29 2008 227 234
27. N. Davoust, C. Vuaillat, G. Cavillon, C. Domenget, E. Hatterer, A. Bernard, C. Dumontel, P. Jurdic, C. Malcus, C. Confavreux, M.F. Belin, and S. Nataf Bone marrow CD34/B220 progenitors target the inflamed brain and display in vitro differentiation potential toward microglia FASEB J 20 2006 2081 2092
28. M. De Palma, M.A. Venneri, R. Galli, S.L. Sergi, L.S. Politi, M. Sampaolesi, and L. Naldini Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors Cancer Cell 8 2005 211 226
29. M.P. Del Rio-Hortega Microglia W. Penfield, Cytology and Cellular Pathology of the Nervous System 1932 Paul B. Hoeber New York 481 534
30. J. Diao, J. Zhao, E. Winter, and M.S. Cattral Recruitment and differentiation of conventional dendritic cell precursors in tumors J Immunol 184 2010 1261 1267
31. S.P. Dineen, K.D. Lynn, S.E. Holloway, A.F. Miller, J.P. Sullivan, D.S. Shames, A.W. Beck, C.C. Barnett, J.B. Fleming, and R.A. Brekken Vascular endothelial growth factor receptor 2 mediates macrophage infiltration into orthotopic pancreatic tumors in mice Cancer Res 68 2008 4340 4346
32. L. Dolcetti, E. Peranzoni, S. Ugel, I. Marigo, G.A. Fernandez, C. Mesa, M. Geilich, G. Winkels, E. Traggiai, A. Casati, F. Grassi, and V. Bronte Hierarchy of immunosuppressive strength among myeloidderived suppressor cell subsets is determined by GM-CSF Eur J Immunol 40 2010 22 35
33. H. Dong, S.E. Strome, D.R. Salomao, H. Tamura, F. Hirano, D.B. Flies, P.C. Roche, J. Lu, G. Zhu, K. Tamada, V.A. Lennon, E. Celis, and L. Chen Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion Nat Med 8 2002 793 800
34. T.G. Douglass, L. Driggers, J.G. Zhang, N. Hoa, C. Delgado, C.C. Williams, Q. Dan, R. Sanchez, E.W. Jeffes, H.T. Wepsic, M.P. Myers, K. Koths, and M.R. Jadus Macrophage colony stimulating factor: not just for macrophages anymore! A gateway into complex biologies Int Immunopharmacol 8 2008 1354 1376
35. D. Duelli, and Y. Lazebnik Cell fusion: a hidden enemy? Cancer Cell 3 2003 445 448
36. C. Eder Ion channels in monocytes and microglia/ brain macrophages: promising therapeutic targets for neurological diseases J Neuroimmunol 224 2010 51 55
37. L. Eggink, and J.K. Hoober A biologically active peptide mimetic of Nacetylgalactosamine/galactose BMC Res Notes 2 2009 23
38. O. Fainaru, N. Almog, C.W. Yung, K. Nakai, M. Montoya-Zavala, A. Abdollahi, R. D'Amato, and D.E. Ingber Tumor growth and angiogenesis are dependent on the presence of immature dendritic cells FASEB J 24 2010 1411 1418
39. P.B. Fernandez, F.C. Lucibello, U.M. Gehling, K. Lindemann, N. Weidner, M.L. Zuzarte, J. Adamkiewicz, H.P. Elsasser, R. Muller, and K. Havemann Endothelial-like cells derived from human CD14 positive monocytes Differentiation 65 2000 287 300
40. C. Fischer, B. Jonckx, M. Mazzone, S. Zacchigna, S. Loges, L. Pattarini, E. Chorianopoulos, L. Liesenborghs, M. Koch, M.M. De, M. Autiero, S. Wyns, S. Plaisance, L. Moons, R.N. van, M. Giacca, J.M. Stassen, M. Dewerchin, D. Collen, and P. Carmeliet Anti-PlGF inhibits growth of VEGF(R)-inhibitorresistant tumors without affecting healthy vessels Cell 131 2007 463 475
41. H.G. Fischer, and G. Reichmann Brain dendritic cells and macrophages/microglia in central nervous system inflammation J Immunol 166 2001 2717 2726
42. A.L. Ford, A.L. Goodsall, W.F. Hickey, and J.D. Sedgwick Normal adult ramified microglia separated from other central nervous system macrophages by flow cytometric sorting. Phenotypic differences defined and direct ex vivo antigen presentation to myelin basic protein-reactive CD4 T cells compared J Immunol 154 1995 4309 4321
43. I. Fricke, and D.I. Gabrilovich Dendritic cells and tumor microenvironment: a dangerous liaison Immunol Invest 35 2006 459 483
44. N. Fujiwara, and K. Kobayashi Macrophages in inflammation Curr Drug Targets Inflamm Allergy 4 2005 281 286
45. D.I. Gabrilovich The mechanisms and functional significance of tumour-induced dendritic-cell defects Nat Rev Immunol 4 2004 941 952
46. D.I. Gabrilovich Myeloid-derived suppressor cells as regulators of the immune system Nat Rev Immunol 9 2009 162 174
47. D.I. Gabrilovich Vascular endothelial growth factor inhibits the development of dendritic cells and dramatically affects the differentation of multiple hematopoietic lineages Blood 92 1998 4150 4166
48. F. Geissmann, S. Jung, and D.R. Littman Blood monocytes consist of two principal subsets with distinct migratory properties Immunity 19 2003 71 82
49. F. Geissmann, M.G. Manz, S. Jung, M.H. Sieweke, M. Merad, and K. Ley Development of monocytes, macrophages, and dendritic cells Science 327 2010 656 661
50. C. Goetz, and M. Gromeier Preparing an oncolytic poliovirus recombinant for clinical application against glioblastomamultiforme Cytokine Growth Factor Rev 21 2010 197 203
51. M.E. Gonzalez-Mejia, and A.I. Doseff Regulation of monocytes and macrophages cell fate Front Biosci 14 2009 2413 2431
52. R. Govinden, and K.D. Bhoola Genealogy, expression, and cellular function of transforming growth factor-beta Pharmacol Ther 98 2003 257 265
53. M.B. Graeber, B.W. Scheithauer, and G.W. Kreutzberg Microglia in brain tumors Glia 40 2002 252 259
54. D.T. Graves, Y.L. Jiang, M.J. Williamson, and A.J. Valente Identification of monocyte chemotactic activity produced by malignant cells Science 245 1989 1490 1493
55. G.J. Guillemin, and B.J. Brew Microglia, macrophages, perivascular macrophages, and pericytes: a review of function and identification J Leukoc Biol 75 2004 388 397
56. M.P. Gustafson, Y. Lin, K.C. New, P.A. Bulur, B.P. O'Neill, D.A. Gastineau, and A.B. Dietz Systemic immune suppression in glioblastoma: the interplay between CD14HLA-DRlo/neg monocytes, tumor factors, and dexamethasone Neuro Oncol 12 2010 644
57. C. Hao, I.F. Parney, W.H. Roa, J. Turner, K.C. Petruk, and D.A. Ramsay Cytokine and cytokine receptor mRNA expression in human glioblastomas: evidence of Th1, Th2 and Th3 cytokine dysregulation Acta Neuropathol 103 2002 171 178
58. G.J. Harry, and A.D. Kraft Neuroinflammation and microglia: considerations and approaches for neurotoxicity assessment Expert Opin Drug Metab Toxicol 4 2008 1265 1277
59. J. Held-Feindt, K. Hattermann, S.S. Muerkoster, H. Wedderkopp, F. Knerlich-Lukoschus, H. Ungefroren, H.M. Mehdorn, and R. Mentlein CX3CR1 promotes recruitment of human glioma-infiltrating microglia/macrophages (GIMs) Exp Cell Res 316 2010 1553 1566
60. D.L. Herber, W. Cao, Y. Nefedova, S.V. Novitskiy, S. Nagaraj, V.A. Tyurin, A. Corzo, H.I. Cho, E. Celis, B. Lennox, S.C. Knight, T. Padhya, T.V. McCaffrey, J.C. McCaffrey, S. Antonia, M. Fishman, R.L. Ferris, V.E. Kagan, and D.I. Gabrilovich Lipid accumulation and dendritic cell dysfunction in cancer Nat Med 16 2010 880 886
61. U. Herrlinger, C.M. Kramm, K.M. Johnston, D.N. Louis, D. Finkelstein, G. Reznikoff, G. Dranoff, X.O. Breakefield, and J.S. Yu Vaccination for experimental gliomas using GM-CSF-transduced glioma cells Cancer Gene Ther 4 1997 345 352
62. S. Hiratsuka, O. Minowa, J. Kuno, T. Noda, and M. Shibuya Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angiogenesis in mice Proc Natl Acad Sci U S A 95 1998 9349 9354
63. S. Hiratsuka, A. Watanabe, H. Aburatani, and Y. Maru Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis Nat Cell Biol 8 2006 1369 1375
64. M. Hishii, T. Nitta, H. Ishida, M. Ebato, A. Kurosu, H. Yagita, K. Sato, and K. Okumura Human glioma-derived interleukin-10 inhibits antitumor immune responses in vitro Neurosurgery 37 1995 1160 1166
65. D.B. Hoelzinger, T. Demuth, and M.E. Berens Autocrine factors that sustain glioma invasion and paracrine biology in the brain microenvironment J Natl Cancer Inst 99 2007 1583 1593
66. S.F. Hussain, L.Y. Kong, J. Jordan, C. Conrad, T. Madden, I. Fokt, W. Priebe, and A.B. Heimberger A novel small molecule inhibitor of signal transducers and activators of transcription 3 reverses immune tolerance in malignant glioma patients Cancer Res 67 2007 9630 9636
67. L.C. Huysentruyt, and M.S. McGrath The role of macrophages in the development and progression of AIDS-related non-Hodgkin lymphoma J Leukoc Biol 87 2010 627 632
68. T. Ichimura, P.A. Fraser, and H.F. Cserr Distribution of extracellular tracers in perivascular spaces of the rat brain Brain Res 545 1991 103 113
69. C. Jackson, J. Ruzevick, J. Phallen, Z. Belcaid, and M. Lim Challenges in immunotherapy presented by the glioblastoma multiforme microenvironment Clin Dev Immunol 732413 2011 2011
70. W. Jia, C. Jackson-Cook, and M.R. Graf Tumor-infiltrating, myeloid-derived suppressor cells inhibit T cell activity by nitric oxide production in an intracranial rat glioma vaccination model J Neuroimmunol 223 2010 20 30.
71. J. Karman, C. Ling, M. Sandor, and Z. Fabry Initiation of immune responses in brain is promoted by local dendritic cells J Immunol 173 2004 2353 2361
72. G. Kaur, S.J. Han, I. Yang, and C. Crane Microglia and central nervous system immunity Neurosurg Clin N Am 21 2010 43 51
73. W. Kim, and L.M. Liau Dendritic cell vaccines for brain tumors Neurosurg Clin N Am 21 2010 139 157
74. W.K. Kim, X. Alvarez, J. Fisher, B. Bronfin, S. Westmoreland, J. McLaurin, and K. Williams CD163 identifies perivascular macrophages in normal and viral encephalitic brains and potential precursors to perivascular macrophages in blood Am J Pathol 168 2006 822 834
75. M. Kioi, H. Vogel, G. Schultz, R.M. Hoffman, G.R. Harsh, and J.M. Brown Inhibition of vasculogenesis, but not angiogenesis, prevents the recurrence of glioblastoma after irradiation in mice J Clin Invest 120 2010 694 705
76. H. Knowles, R. Leek, and A.L. Harris Macrophage infiltration and angiogenesis in human malignancy Novartis Found Symp 256 2004 189 200
77. J.S. Ko, A.H. Zea, B.I. Rini, J.L. Ireland, P. Elson, P. Cohen, A. Golshayan, P.A. Rayman, L. Wood, J. Garcia, R. Dreicer, R. Bukowski, and J.H. Finke Sunitinib mediates reversal of myeloid-derived suppressor cell accumulation in renal cell carcinoma patients Clin Cancer Res 15 2009 2148 2157
78. Y. Komohara, K. Ohnishi, J. Kuratsu, and M. Takeya Possible involvement of the M2 anti-inflammatory macrophage phenotype in growth of human gliomas J Pathol 216 2008 15 24
79. A.M. Kostianovsky, L.M. Maier, R.C. Anderson, J.N. Bruce, and D.E. Anderson Astrocytic regulation of human monocytic/microglial activation J Immunol 181 2008 5425 5432
80. S.V. Kushchayev, T. Sankar, L.L. Eggink, Y.S. Kushchayeva, P.C. Wiener, J.K. Hoober, J. Eschbacher, R. Lui, F.D. Shi, M.G. Abdelwahab, A.C. Scheck, and M.C. Preul Monocyte galactose/ N-acetylgalactosamine-specific C-type lectin receptor stimulant immunotherapy of an experimental glioma. Part II: combination with external radiation improves survival Cancer Manage Res 4 2012 325 334
81. S.V. Kushchayev, T. Sankar, L.L. Eggink, Y.S. Kushchayeva, P.C. Wiener, J.K. Hoober, J. Eschbacher, R. Lui, F.D. Shi, M.G. Abdelwahab, A.C. Scheck, and M.C. Preul Monocyte galactose/N-acetylgalactosamine-specific C-type lectin receptor stimulant immunotherapy of an experimental glioma. Part I: stimulatory effects on blood monocytes and monocyte-derived cells of the brain Cancer Manage Res 4 2012 309 323
82. M. Kuwana, Y. Okazaki, H. Kodama, T. Satoh, Y. Kawakami, and Y. Ikeda Endothelial differentiation potential of human monocyte-derived multipotential cells Stem Cells 24 2006 2733 2743
83. S.S. Lakka, C.S. Gondi, N. Yanamandra, W.C. Olivero, D.H. Dinh, M. Gujrati, and J.S. Rao Inhibition of cathepsin B and MMP-9 gene expression in glioblastoma cell line via RNA interference reduces tumor cell invasion, tumor growth and angiogenesis Oncogene 23 2004 4681 4689
84. C.C. Lee, K.J. Liu, and T.S. Huang Tumor-associated macrophage: its role in tumor angiogenesis J Cancer Mol 2 2006 135 140
85. J.J. Letterio, and A.B. Roberts Regulation of immune responses by TGF-beta Annu Rev Immunol 16 1998 137 161
86. C.E. Lewis, M. De Palma, and L. Naldini Tie2-expressing monocytes and tumor angiogenesis: regulation by hypoxia and angiopoietin-2 Cancer Res 67 2007 8429 8432
87. E.A. Ling, C. Kaur, and J. Lu Origin, nature, and some functional considerations of intraventricular macrophages, with special reference to the epiplexus cells Microsc Res Tech 41 1998 43 56
88. A. Mantovani, A. Sica, S. Sozzani, P. Allavena, A. Vecchi, and M. Locati The chemokine system in diverse forms of macrophage activation and polarization Trends Immunol 25 2004 677 686
89. A. Mantovani, S. Sozzani, M. Locati, P. Allavena, and A. Sica Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes Trends Immunol 23 2002 549 555
90. D.S. Markovic, K. Vinnakota, S. Chirasani, M. Synowitz, H. Raguet, K. Stock, M. Sliwa, S. Lehmann, R. Kalin, N. van Rooijen, K. Holmbeck, F.L. Heppner, J. Kiwit, V. Matyash, S. Lehnardt, B. Kaminska, R. Glass, and H. Kettenmann Gliomas induce and exploit microglial MT1-MMP expression for tumor expansion Proc Natl Acad Sci U S A 106 2009 12530 12535
91. F.O. Martinez, L. Helming, and S. Gordon Alternative activation of macrophages: an immunologic functional perspective Annu Rev Immunol 27 2009 451 483
92. P.G. McMenamin, R.J. Wealthall, M. Deverall, S.J. Cooper, and B. Griffin Macrophages and dendritic cells in the rat meninges and choroid plexus: three-dimensional localisation by environmental scanning electron microscopy and confocal microscopy Cell Tissue Res 313 2003 259 269
93. M. Menges, S. Rossner, C. Voigtlander, H. Schindler, N.A. Kukutsch, C. Bogdan, K. Erb, G. Schuler, and M.B. Lutz Repetitive injections of dendritic cells matured with tumor necrosis factor alpha induce antigen-specific protection of mice from autoimmunity J Exp Med 195 2002 15 21
94. K. Movahedi, M. Guilliams, J. Van den Bossche, R. Van den Bergh, C. Gysemans, A. Beschin, P. De Baetselier, and J.A. Van Ginderachter Identification of discrete tumor-induced myeloidderived suppressor cell subpopulations with distinct T cell-suppressive activity Blood 111 2008 4233 4244
95. P. Msaouel, A. Dispenzieri, and E. Galanis Clinical testing of engineered oncolytic measles virus strains in the treatment of cancer: an overview Curr Opin Mol Ther 11 2009 43 53
96. D.H. Munn, M.D. Sharma, J.R. Lee, K.G. Jhaver, T.S. Johnson, D.B. Keskin, B. Marshall, P. Chandler, S.J. Antonia, R. Burgess, C.L. Slingluff Jr., and A.L. Mellor Potential regulatory function of human dendritic cells expressing indoleamine 2,3-dioxygenase Science 297 2002 1867 1870
97. C. Murdoch, A. Giannoudis, and C.E. Lewis Mechanisms regulating the recruitment of macrophages into hypoxic areas of tumors and other ischemic tissues Blood 104 2004 2224 2234
98. C. Murdoch, M. Muthana, S.B. Coffelt, and C.E. Lewis The role of myeloid cells in the promotion of tumour angiogenesis Nat Rev Cancer 8 2008 618 631
99. C. Murdoch, S. Tazzyman, S. Webster, and C.E. Lewis Expression of Tie-2 by human monocytes and their responses to angiopoietin-2 J Immunol 178 2007 7405 7411
100. S. Nagaraj, and D.I. Gabrilovich Myeloid-derived suppressor cells in human cancer Cancer J 16 2010 348 353
101. S. Nagaraj, A.G. Schrum, H.I. Cho, E. Celis, and D.I. Gabrilovich Mechanism of T cell tolerance induced by myeloid-derived suppressor cells J Immunol 184 2010 3106 3116
102. S. Nataf, N. Strazielle, E. Hatterer, G. Mouchiroud, M.F. Belin, and J.F. Ghersi-Egea Rat choroid plexuses contain myeloid progenitors capable of differentiation toward macrophage or dendritic cell phenotypes Glia 54 2006 160 171
103. A. Natsume, S. Kinjo, K. Yuki, T. Kato, M. Ohno, K. Motomura, K. Iwami, and T. Wakabayashi Gliomainitiating cells and molecular pathology: implications for therapy Brain Tumor Pathol 28 2011 1 12
104. A. Nimmerjahn, F. Kirchhoff, and F. Helmchen Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo Science 308 2005 1314 1318
105. G.M. O'Keefe, V.T. Nguyen, and E.N. Benveniste Class II transactivator and class II MHC gene expression in microglia: modulation by the cytokines TGFbeta, IL-4, IL-13 and IL-10 Eur J Immunol 29 1999 1275 1285
106. A.T. Ogden, D. Horgan, A. Waziri, D. Anderson, J. Louca, G.M. McKhann, M.B. Sisti, A.T. Parsa, and J.N. Bruce Defective receptor expression and dendritic cell differentiation of monocytes in glioblastomas Neurosurgery 59 2006 902 909
107. M. Okada, M. Saio, Y. Kito, N. Ohe, H. Yano, S. Yoshimura, T. Iwama, and T. Takami Tumor-associated macrophage/microglia infiltration in human gliomas is correlated with MCP-3, but not MCP-1 Int J Oncol 34 2009 1621 1627
108. I.F. Parney, J.S. Waldron, and A.T. Parsa Flow cytometry and in vitro analysis of human glioma-associated macrophages. Laboratory investigation J Neurosurg 110 2009 572 582
109. M. Pashenkov, N. Teleshova, and H. Link Inflammation in the central nervous system: the role for dendritic cells Brain Pathol 13 2003 23 33
110. J.M. Pawelek, and A.K. Chakraborty Fusion of tumour cells with bone marrow-derived cells: a unifying explanation for metastasis Nat Rev Cancer 8 2008 377 386
111. J.M. Pawelek, and A.K. Chakraborty The cancer cell - leukocyte fusion theory of metastasis Adv Cancer Res 101 2008 397 444
112. S. Pellegatta, L. Cuppini, and G. Finocchiaro Brain cancer immunoediting: novel examples provided by immunotherapy of malignant gliomas Expert Rev Anticancer Ther 11 2011 1759 1774
113. W. Penfield Microglia and the process of phagocytosis in gliomas Am J Pathol 1 1925 77 97
114. E.D. Ponomarev, L.P. Shriver, K. Maresz, and B.N. Dittel Microglial cell activation and proliferation precedes the onset of CNS autoimmunity J Neurosci Res 81 2005 374 389
115. M.C. Preul, Z. Caramanos, J.G. Villemure, G. Shenouda, R. LeBlanc, A. Langleben, and D.L. Arnold Using proton magnetic resonance spectroscopic imaging to predict in vivo the response of recurrent malignant gliomas to tamoxifen chemotherapy Neurosurgery 46 2000 306 318
116. R. Rahman, S. Smith, C. Rahman, and R. Grundy Antiangiogenic therapy and mechanisms of tumor resistance in malignant glioma J Oncol 2010 251231
117. G.J. Randolph, C. Jakubzick, and C. Qu Antigen presentation by monocytes and monocyte-derived cells Curr Opin Immunol 20 2008 52 60
118. R.M. Ransohoff, and V.H. Perry Microglial physiology: unique stimuli, specialized responses Annu Rev Immunol 27 2009 119 145
119. J.S. Rao Molecular mechanisms of glioma invasiveness: the role of proteases Nat Rev Cancer 3 2003 489 501
120. B. Raychaudhuri, P. Rayman, J. Ireland, J. Ko, B. Rini, E.C. Borden, J. Garcia, M.A. Vogelbaum, and J. Finke Myeloid-derived suppressor cell accumulation and function in patients with newly diagnosed glioblastoma Neuro Oncol 13 2011 591 599
121. P. Rezaie, and D. Male Colonisation of the developing human brain and spinal cord by microglia: a review Microsc Res Tech 45 1999 359 382
122. R.B. Rock, G. Gekker, S. Hu, W.S. Sheng, M. Cheeran, J.R. Lokensgard, and P.K. Peterson Role of microglia in central nervous system infections Clin Microbiol Rev 17 2004 942 964
123. J.C. Rodrigues, G.C. Gonzalez, L. Zhang, G. Ibrahim, J.J. Kelly, M.P. Gustafson, Y. Lin, A.B. Dietz, P.A. Forsyth, V.W. Yong, and I.F. Parney Normal human monocytes exposed to glioma cells acquire myeloid-derived suppressor cell-like properties Neuro Oncol 12 2010 351 365
124. P.C. Rodriguez, D.G. Quiceno, J. Zabaleta, B. Ortiz, A.H. Zea, M.B. Piazuelo, A. Delgado, P. Correa, J. Brayer, E.M. Sotomayor, S. Antonia, J.B. Ochoa, and A.C. Ochoa 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 2004 5839 5849
125. A. Roy, Y.K. Fung, X. Liu, and K. Pahan Up-regulation of microglial CD11b expression by nitric oxide J Biol Chem 281 2006 14971 14980
126. T. Sankar, Z. Caramanos, R. Assina, J.G. Villemure, R. LeBlanc, A. Langleben, D.L. Arnold, and M.C. Preul Prospective serial proton MR spectroscopic assessment of response to tamoxifen for recurrent malignant glioma J Neurooncol 90 2008 63 76
127. L. Santambrogio, S.L. Belyanskaya, F.R. Fischer, B. Cipriani, C.F. Brosnan, P. Ricciardi-Castagnoli, L.J. Stern, J.L. Strominger, and R. Riese Developmental plasticity of CNS microglia Proc Natl Acad Sci U S A 98 2001 6295 6300
128. J.M. Schartner, A.R. Hagar, H.M. Van, L. Zhang, N. Nadkarni, and B. Badie Impaired capacity for upregulation of MHC class II in tumor-associated microglia Glia 51 2005 279 285
129. H.J. Scherer Structural development in gliomas Am J Cancer 34 1938 333 351
130. M.C. Schmid, and J.A. Varner Myeloid cells in the tumor microenvironment: modulation of tumor angiogenesis and tumor inflammation J Oncol 2010 2010 201026
131. C. Scotton, D. Milliken, J. Wilson, S. Raju, and F. Balkwill Analysis of CC chemokine and chemokine receptor expression in solid ovarian tumours Br J Cancer 85 2001 891 897
132. F. Shojaei, X. Wu, A.K. Malik, C. Zhong, M.E. Baldwin, S. Schanz, G. Fuh, H.P. Gerber, and N. Ferrara Tumor refractoriness to anti-VEGF treatment is mediated by CD11bGr1 myeloid cells Nat Biotechnol 25 2007 911 920
133. K. Shortman, and Y.J. Liu Mouse and human dendritic cell subtypes Nat Rev Immunol 2 2002 151 161
134. M. Sliwa, D. Markovic, K. Gabrusiewicz, M. Synowitz, R. Glass, M. Zawadzka, A. Wesolowska, H. Kettenmann, and B. Kaminska The invasion promoting effect of microglia on glioblastoma cells is inhibited by cyclosporin A Brain 130 2007 476 489
135. C. Soulas, R.E. Donahue, C.E. Dunbar, D.A. Persons, X. Alvarez, and K.C. Williams Genetically modified CD34 hematopoietic stem cells contribute to turnover of brain perivascular macrophages in long-term repopulated primates Am J Pathol 174 2009 1808 1817
136. M.L. Squadrito, and M. De Palma Macrophage regulation of tumor angiogenesis: implications for cancer therapy Mol Aspects Med 32 2011 123 145
137. N. Strazielle, and J.F. Ghersi-Egea Choroid plexus in the central nervous system: biology and physiopathology J Neuropathol Exp Neurol 59 2000 561 574
138. W.J. Streit Microglial senescence: does the brain's immune system have an expiration date? Trends Neurosci 29 2006 506 510
139. W.J. Streit, N.W. Sammons, A.J. Kuhns, and D.L. Sparks Dystrophic microglia in the aging human brain Glia 45 2004 208 212
140. W.J. Streit, and Q.S. Xue Life and death of microglia J Neuroimmune Pharmacol 4 2009 371 379
141. R. Tang, F. Beuvon, M. Ojeda, V. Mosseri, P. Pouillart, and S. Scholl M-CSF (monocyte colony stimulating factor) and M-CSF receptor expression by breast tumour cells: M-CSF mediated recruitment of tumour infiltrating monocytes? J Cell Biochem 50 1992 350 356
142. S.G. Temel, and Z. Kahveci Cyclooxygenase-2 expression in astrocytes and microglia in human oligodendroglioma and astrocytoma J Mol Histol 40 2009 369 377
143. N. Umemura, M. Saio, T. Suwa, Y. Kitoh, J. Bai, K. Nonaka, G.F. Ouyang, M. Okada, M. Balazs, R. Adany, T. Shibata, and T. Takami Tumor-infiltrating myeloid-derived suppressor cells are pleiotropic-inflamed monocytes/macrophages that bear M1- and M2-type characteristics J Leukoc Biol 83 2008 1136 1144
144. M.A. Venneri, P.M. De, M. Ponzoni, F. Pucci, C. Scielzo, E. Zonari, R. Mazzieri, C. Doglioni, and L. Naldini Identification of proangiogenic TIE2- expressing monocytes (TEMs) in human peripheral blood and cancer Blood 109 2007 5276 5285
145. J. Villeneuve, P. Tremblay, and L. Vallieres Tumor necrosis factor reduces brain tumor growth by enhancing macrophage recruitment and microcyst formation Cancer Res 65 2005 3928 3936
146. R.I. von Hanwehr, F.M. Hofman, C.R. Taylor, and M.L. Apuzzo Mononuclear lymphoid populations infiltrating the microenvironment of primary CNS tumors. Characterization of cell subsets with monoclonal antibodies J Neurosurg 60 1984 1138 1147
147. S. Vuk-Pavlovic, P.A. Bulur, Y. Lin, R. Qin, C.L. Szumlanski, X. Zhao, and A.B. Dietz Immunosuppressive CD14HLA-DRlow/- monocytes in prostate cancer Prostate 70 2010 443 455
148. J.J. Watters, J.M. Schartner, and B. Badie Microglia function in brain tumors J Neurosci Res 81 2005 447 455
149. J. Wei, A. Wu, L.Y. Kong, Y. Wang, G. Fuller, I. Fokt, G. Melillo, W. Priebe, and A.B. Heimberger Hypoxia potentiates glioma-mediated immunosuppression PLoS One 6 2011 e16195
150. A. Wesolowska, A. Kwiatkowska, L. Slomnicki, M. Dembinski, A. Master, M. Sliwa, K. Franciszkiewicz, S. Chouaib, and B. Kaminska Microglia-derived TGF-beta as an important regulator of glioblastoma invasion - an inhibition of TGF-beta-dependent effects by shRNA against human TGF-beta type II receptor Oncogene 27 2008 918 930
151. C.J. Wheeler Dendritic cell vaccines to combat glioblastoma Expert Rev Neurother 10 2010 483 486
152. T. Wierzba-Bobrowicz, I. Kuchna, and E. Matyja Reaction of microglial cells in human astrocytomas (preliminary report) Folia Neuropathol 32 1994 251 252
153. A. Wu, J. Wei, L.Y. Kong, Y. Wang, W. Priebe, W. Qiao, R. Sawaya, and A.B. Heimberger Glioma cancer stem cells induce immunosuppressive macrophages/microglia Neuro Oncol 12 2010 1113 1125
154. A. Yokoyama, L. Yang, S. Itoh, K. Mori, and J. Tanaka Microglia, a potential source of neurons, astrocytes, and oligodendrocytes Glia 45 2004 96 104
155. J.I. Youn, and D.I. Gabrilovich The biology of myeloidderived suppressor cells: the blessing and the curse of morphological and functional heterogeneity Eur J Immunol 40 2010 2969 2975
156. J.I. Youn, S. Nagaraj, M. Collazo, and D.I. Gabrilovich Subsets of myeloid-derived suppressor cells in tumor-bearing mice J Immunol 181 2008 5791 5802
157. D. Zagzag, Y. Lukyanov, L. Lan, M.A. Ali, M. Esencay, O. Mendez, H. Yee, E.B. Voura, and E.W. Newcomb Hypoxia-inducible factor 1 and VEGF upregulate CXCR4 in glioblastoma: implications for angiogenesis and glioma cell invasion Lab Invest 86 2006 1221 1232
158. A. Zampetaki, S.A. Mitsialis, J. Pfeilschifter, and S. Kourembanas Hypoxia induces macrophage inflammatory protein-2 (MIP-2) gene expression in murine macrophages via NF-kappaB: the prominent role of p42/ p44 and PI3 kinase pathways FASEB J 18 2004 1090 1092
159. L. Zhang, D. Alizadeh, M. Van Handel, M. Kortylewski, H. Yu, and B. Badie Stat3 inhibition activates tumor macrophages and abrogates glioma growth in mice Glia 57 2009 1458 1467
160. D. Zhao, D. Alizadeh, L. Zhang, W. Liu, O. Farrukh, E. Manuel, D.J. Diamond, and B. Badie Carbon nanotubes enhance CpG uptake and potentiate antiglioma immunity Clin Cancer Res 17 2011 771 782