Table of Contents Author Guidelines Submit a Manuscript
Journal of Immunology Research
Volume 2017 (2017), Article ID 5150678, 12 pages
https://doi.org/10.1155/2017/5150678
Review Article

The Role of Microglia and Macrophages in CNS Homeostasis, Autoimmunity, and Cancer

1Department of Neurosurgery, University of Alabama at Birmingham, Birmingham, AL 35233, USA
2Department of Microbiology, University of Alabama at Birmingham, Birmingham, AL 35233, USA
3Department of Cell Biology, Tianjin Medical University, Tianjin 300070, China

Correspondence should be addressed to Jianmei W. Leavenworth; ude.cmbau@htrownevaelj

Received 29 July 2017; Revised 20 October 2017; Accepted 27 November 2017; Published 19 December 2017

Academic Editor: Hao Liu

Copyright © 2017 Jie Yin et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. P. B. Medawar, “Immunity to homologous grafted skin; the fate of skin homografts transplanted to the brain, to subcutaneous tissue, and to the anterior chamber of the eye,” British Journal of Experimental Pathology, vol. 29, pp. 58–69, 1948. View at Google Scholar
  2. V. H. Perry and J. Teeling, “Microglia and macrophages of the central nervous system: the contribution of microglia priming and systemic inflammation to chronic neurodegeneration,” Seminars in Immunopathology, vol. 35, no. 5, pp. 601–612, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. D. Davalos, J. Grutzendler, G. Yang et al., “ATP mediates rapid microglial response to local brain injury in vivo,” Nature Neuroscience, vol. 8, no. 6, pp. 752–758, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Nimmerjahn, F. Kirchhoff, and F. Helmchen, “Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo,” Science, vol. 308, no. 5726, pp. 1314–1318, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. S. Gordon and P. R. Taylor, “Monocyte and macrophage heterogeneity,” Nature Reviews Immunology, vol. 5, no. 12, pp. 953–964, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. S. R. Krutzik, B. Tan, H. Li et al., “TLR activation triggers the rapid differentiation of monocytes into macrophages and dendritic cells,” Nature Medicine, vol. 11, no. 6, pp. 653–660, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. P. J. Murray and T. A. Wynn, “Obstacles and opportunities for understanding macrophage polarization,” Journal of Leukocyte Biology, vol. 89, no. 4, pp. 557–563, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. C. Varol, A. Mildner, and S. Jung, “Macrophages: development and tissue specialization,” Annual Review of Immunology, vol. 33, no. 1, pp. 643–675, 2015. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Mildner, S. Yona, and S. Jung, “Chapter three - a close encounter of the third kind: monocyte-derived cells,” Advances in Immunology, vol. 120, pp. 69–103, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. F. Ginhoux, M. Greter, M. Leboeuf et al., “Fate mapping analysis reveals that adult microglia derive from primitive macrophages,” Science, vol. 330, no. 6005, pp. 841–845, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. C. Schulz, E. G. Perdiguero, L. Chorro et al., “A lineage of myeloid cells independent of Myb and hematopoietic stem cells,” Science, vol. 336, no. 6077, pp. 86–90, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. J. K. Hefendehl, J. J. Neher, R. B. Sühs, S. Kohsaka, A. Skodras, and M. Jucker, “Homeostatic and injury-induced microglia behavior in the aging brain,” Aging Cell, vol. 13, no. 1, pp. 60–69, 2014. View at Publisher · View at Google Scholar · View at Scopus
  13. W. T. Wong, “Microglial aging in the healthy CNS: phenotypes, drivers, and rejuvenation,” Frontiers in Cellular Neuroscience, vol. 7, p. 22, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Prinz, D. Erny, and N. Hagemeyer, “Ontogeny and homeostasis of CNS myeloid cells,” Nature Immunology, vol. 18, no. 4, pp. 385–392, 2017. View at Publisher · View at Google Scholar
  15. M. Prinz, J. Priller, S. S. Sisodia, and R. M. Ransohoff, “Heterogeneity of CNS myeloid cells and their roles in neurodegeneration,” Nature Neuroscience, vol. 14, no. 10, pp. 1227–1235, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. O. Butovsky, M. P. Jedrychowski, C. S. Moore et al., “Identification of a unique TGF-β–dependent molecular and functional signature in microglia,” Nature Neuroscience, vol. 17, no. 1, pp. 131–143, 2014. View at Publisher · View at Google Scholar · View at Scopus
  17. K. Kierdorf, D. Erny, T. Goldmann et al., “Microglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways,” Nature Neuroscience, vol. 16, no. 3, pp. 273–280, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. C. Verney, A. Monier, C. Fallet-Bianco, and P. Gressens, “Early microglial colonization of the human forebrain and possible involvement in periventricular white-matter injury of preterm infants,” Journal of Anatomy, vol. 217, no. 4, pp. 436–448, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. T. Goldmann, P. Wieghofer, M. J. C. Jordão et al., “Origin, fate and dynamics of macrophages at central nervous system interfaces,” Nature Immunology, vol. 17, no. 7, pp. 797–805, 2016. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Prinz and J. Priller, “The role of peripheral immune cells in the CNS in steady state and disease,” Nature Neuroscience, vol. 20, no. 2, pp. 136–144, 2017. View at Publisher · View at Google Scholar
  21. D. Nayak, T. L. Roth, and D. B. McGavern, “Microglia development and function,” Annual Review of Immunology, vol. 32, no. 1, pp. 367–402, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. X. M. Dai, G. R. Ryan, A. J. Hapel et al., “Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects,” Blood, vol. 99, no. 1, pp. 111–120, 2002. View at Publisher · View at Google Scholar · View at Scopus
  23. Y. Wang, K. J. Szretter, W. Vermi et al., “IL-34 is a tissue-restricted ligand of CSF1R required for the development of Langerhans cells and microglia,” Nature Immunology, vol. 13, no. 8, pp. 753–760, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Wirenfeldt, L. Dissing-Olesen, A. Anne Babcock et al., “Population control of resident and immigrant microglia by mitosis and apoptosis,” The American Journal of Pathology, vol. 171, no. 2, pp. 617–631, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. L. M. Stuart and R. A. B. Ezekowitz, “Phagocytosis: elegant complexity,” Immunity, vol. 22, no. 5, pp. 539–550, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Mukhopadhyay, Y. Chen, M. Sankala et al., “MARCO, an innate activation marker of macrophages, is a class A scavenger receptor for Neisseria meningitidis,” European Journal of Immunology, vol. 36, no. 4, pp. 940–949, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. M. A. Michell-Robinson, H. Touil, L. M. Healy et al., “Roles of microglia in brain development, tissue maintenance and repair,” Brain, vol. 138, no. 5, pp. 1138–1159, 2015. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Ueno, Y. Fujita, T. Tanaka et al., “Layer V cortical neurons require microglial support for survival during postnatal development,” Nature Neuroscience, vol. 16, no. 5, pp. 543–551, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. J. Hsieh, J. B. Aimone, B. K. Kaspar, T. Kuwabara, K. Nakashima, and F. H. Gage, “IGF-I instructs multipotent adult neural progenitor cells to become oligodendrocytes,” The Journal of Cell Biology, vol. 164, no. 1, pp. 111–122, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. J. K. Ness and T. L. Wood, “Insulin-like growth factor I, but not neurotrophin-3, sustains Akt activation and provides long-term protection of immature oligodendrocytes from glutamate-mediated apoptosis,” Molecular and Cellular Neurosciences, vol. 20, no. 3, pp. 476–488, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. T. Trang, S. Beggs, and M. W. Salter, “Brain-derived neurotrophic factor from microglia: a molecular substrate for neuropathic pain,” Neuron Glia Biology, vol. 7, no. 01, pp. 99–108, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. R. M. Ransohoff and A. E. Cardona, “The myeloid cells of the central nervous system parenchyma,” Nature, vol. 468, no. 7321, pp. 253–262, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. J. M. Frade and Y. A. Barde, “Microglia-derived nerve growth factor causes cell death in the developing retina,” Neuron, vol. 20, no. 1, pp. 35–41, 1998. View at Publisher · View at Google Scholar · View at Scopus
  34. J. L. Marı́n-Teva, I. Dusart, C. Colin, A. Gervais, N. van Rooijen, and M. Mallat, “Microglia promote the death of developing Purkinje cells,” Neuron, vol. 41, no. 4, pp. 535–547, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. Y. Wu, L. Dissing-Olesen, B. A. MacVicar, and B. Stevens, “Microglia: dynamic mediators of synapse development and plasticity,” Trends in Immunology, vol. 36, no. 10, pp. 605–613, 2015. View at Publisher · View at Google Scholar · View at Scopus
  36. R. C. Paolicelli, G. Bolasco, F. Pagani et al., “Synaptic pruning by microglia is necessary for normal brain development,” Science, vol. 333, no. 6048, pp. 1456–1458, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. A. R. Bialas and B. Stevens, “TGF-β signaling regulates neuronal C1q expression and developmental synaptic refinement,” Nature Neuroscience, vol. 16, no. 12, pp. 1773–1782, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. A. Roumier, C. Béchade, J. C. Poncer et al., “Impaired synaptic function in the microglial KARAP/DAP12-deficient mouse,” The Journal of Neuroscience, vol. 24, no. 50, pp. 11421–11428, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. C. N. Parkhurst, G. Yang, I. Ninan et al., “Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor,” Cell, vol. 155, no. 7, pp. 1596–1609, 2013. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Lee, “Neurotransmitters and microglial-mediated neuroinflammation,” Current Protein & Peptide Science, vol. 14, no. 1, pp. 21–32, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Pannell, F. Szulzewsky, V. Matyash, S. A. Wolf, and H. Kettenmann, “The subpopulation of microglia sensitive to neurotransmitters/neurohormones is modulated by stimulation with LPS, interferon-γ, and IL-4,” Glia, vol. 62, no. 5, pp. 667–679, 2014. View at Publisher · View at Google Scholar · View at Scopus
  42. J. F. J. Bogie, P. Stinissen, and J. J. A. Hendriks, “Macrophage subsets and microglia in multiple sclerosis,” Acta Neuropathologica, vol. 128, no. 2, pp. 191–213, 2014. View at Publisher · View at Google Scholar · View at Scopus
  43. M. Colonna and O. Butovsky, “Microglia function in the central nervous system during health and neurodegeneration,” Annual Review of Immunology, vol. 35, no. 1, pp. 441–468, 2017. View at Publisher · View at Google Scholar
  44. R. Glass and M. Synowitz, “CNS macrophages and peripheral myeloid cells in brain tumours,” Acta Neuropathologica, vol. 128, no. 3, pp. 347–362, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. C. C. Bailey, L. B. DeVaux, and M. Farzan, “The triggering receptor expressed on myeloid cells 2 binds apolipoprotein E,” The Journal of Biological Chemistry, vol. 290, no. 43, pp. 26033–26042, 2015. View at Publisher · View at Google Scholar · View at Scopus
  46. J. L. Cannons, S. G. Tangye, and P. L. Schwartzberg, “SLAM family receptors and SAP adaptors in immunity,” Annual Review of Immunology, vol. 29, no. 1, pp. 665–705, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. F. O. Martinez and S. Gordon, “The M1 and M2 paradigm of macrophage activation: time for reassessment,” F1000prime reports, vol. 6, p. 13, 2014. View at Publisher · View at Google Scholar · View at Scopus
  48. P. J. Murray, “Macrophage polarization,” Annual Review of Physiology, vol. 79, no. 1, pp. 541–566, 2017. View at Publisher · View at Google Scholar
  49. P. Italiani and D. Boraschi, “From monocytes to M1/M2 macrophages: phenotypical vs. functional differentiation,” Frontiers in Immunology, vol. 5, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. F. Pickford, J. Marcus, L. M. Camargo et al., “Progranulin is a chemoattractant for microglia and stimulates their endocytic activity,” The American Journal of Pathology, vol. 178, no. 1, pp. 284–295, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. H. S. Suh, Y. Lo, N. Choi, S. Letendre, and S. C. Lee, “Evidence of the innate antiviral and neuroprotective properties of progranulin,” PLoS One, vol. 9, no. 5, article e98184, 2014. View at Publisher · View at Google Scholar · View at Scopus
  52. H. Keren-Shaul, A. Spinrad, A. Weiner et al., “A unique microglia type associated with restricting development of Alzheimer’s disease,” Cell, vol. 169, no. 7, pp. 1276–1290.e17, 2017. View at Publisher · View at Google Scholar
  53. S. Krasemann, C. Madore, R. Cialic et al., “The TREM2-APOE pathway drives the transcriptional phenotype of dysfunctional microglia in neurodegenerative diseases,” Immunity, vol. 47, no. 3, pp. 566–581.e9, 2017. View at Publisher · View at Google Scholar
  54. S. M. Brendecke and M. Prinz, “Do not judge a cell by its cover—diversity of CNS resident, adjoining and infiltrating myeloid cells in inflammation,” Seminars in Immunopathology, vol. 37, no. 6, pp. 591–605, 2015. View at Publisher · View at Google Scholar · View at Scopus
  55. W. Hickey and H. Kimura, “Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in vivo,” Science, vol. 239, no. 4837, pp. 290–292, 1988. View at Publisher · View at Google Scholar
  56. G. Kunis, K. Baruch, O. Miller, and M. Schwartz, “Immunization with a myelin-derived antigen activates the brain’s choroid plexus for recruitment of immunoregulatory cells to the CNS and attenuates disease progression in a mouse model of ALS,” The Journal of Neuroscience, vol. 35, no. 16, pp. 6381–6393, 2015. View at Publisher · View at Google Scholar · View at Scopus
  57. S. J. Galli, N. Borregaard, and T. A. Wynn, “Phenotypic and functional plasticity of cells of innate immunity: macrophages, mast cells and neutrophils,” Nature Immunology, vol. 12, no. 11, pp. 1035–1044, 2011. View at Publisher · View at Google Scholar · View at Scopus
  58. T. Kawai and S. Akira, “Toll-like receptors and their crosstalk with other innate receptors in infection and immunity,” Immunity, vol. 34, no. 5, pp. 637–650, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. V. E. Miron, A. Boyd, J. W. Zhao et al., “M2 microglia and macrophages drive oligodendrocyte differentiation during CNS remyelination,” Nature Neuroscience, vol. 16, no. 9, pp. 1211–1218, 2013. View at Publisher · View at Google Scholar · View at Scopus
  60. X. Hu, R. K. Leak, Y. Shi et al., “Microglial and macrophage polarization—new prospects for brain repair,” Nature Reviews Neurology, vol. 11, no. 1, pp. 56–64, 2015. View at Publisher · View at Google Scholar · View at Scopus
  61. N. C. Derecki, A. N. Cardani, C. H. Yang et al., “Regulation of learning and memory by meningeal immunity: a key role for IL-4,” The Journal of Experimental Medicine, vol. 207, no. 5, pp. 1067–1080, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. A. J. Filiano, S. P. Gadani, and J. Kipnis, “Interactions of innate and adaptive immunity in brain development and function,” Brain Research, vol. 1617, pp. 18–27, 2015. View at Publisher · View at Google Scholar · View at Scopus
  63. D. M. Mosser and J. P. Edwards, “Exploring the full spectrum of macrophage activation,” Nature Reviews Immunology, vol. 8, no. 12, pp. 958–969, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. T. Krausgruber, K. Blazek, T. Smallie et al., “IRF5 promotes inflammatory macrophage polarization and TH1-TH17 responses,” Nature Immunology, vol. 12, no. 3, pp. 231–238, 2011. View at Publisher · View at Google Scholar · View at Scopus
  65. A. Nardin and J. P. Abastado, “Macrophages and cancer,” Frontiers in Bioscience, vol. 13, pp. 3494–3505, 2008. View at Publisher · View at Google Scholar · View at Scopus
  66. A. M. Smith, F. Z. Rahman, B. H. Hayee et al., “Disordered macrophage cytokine secretion underlies impaired acute inflammation and bacterial clearance in Crohn’s disease,” The Journal of Experimental Medicine, vol. 206, no. 9, pp. 1883–1897, 2009. View at Publisher · View at Google Scholar · View at Scopus
  67. M. S. Wilson, S. K. Madala, T. R. Ramalingam et al., “Bleomycin and IL-1β–mediated pulmonary fibrosis is IL-17A dependent,” The Journal of Experimental Medicine, vol. 207, no. 3, pp. 535–552, 2010. View at Publisher · View at Google Scholar · View at Scopus
  68. K. J. Woollard and F. Geissmann, “Monocytes in atherosclerosis: subsets and functions,” Nature Reviews Cardiology, vol. 7, no. 2, pp. 77–86, 2010. View at Publisher · View at Google Scholar · View at Scopus
  69. A. London, E. Itskovich, I. Benhar et al., “Neuroprotection and progenitor cell renewal in the injured adult murine retina requires healing monocyte-derived macrophages,” The Journal of Experimental Medicine, vol. 208, no. 1, pp. 23–39, 2011. View at Publisher · View at Google Scholar · View at Scopus
  70. U. Hadis, B. Wahl, O. Schulz et al., “Intestinal tolerance requires gut homing and expansion of FoxP3+ regulatory T cells in the lamina propria,” Immunity, vol. 34, no. 2, pp. 237–246, 2011. View at Publisher · View at Google Scholar · View at Scopus
  71. R. M. Anthony, J. F. Urban, F. Alem et al., “Memory TH2 cells induce alternatively activated macrophages to mediate protection against nematode parasites,” Nature Medicine, vol. 12, no. 8, pp. 955–960, 2006. View at Publisher · View at Google Scholar · View at Scopus
  72. R. M. Maizels, E. J. Pearce, D. Artis, M. Yazdanbakhsh, and T. A. Wynn, “Regulation of pathogenesis and immunity in helminth infections,” The Journal of Experimental Medicine, vol. 206, no. 10, pp. 2059–2066, 2009. View at Publisher · View at Google Scholar · View at Scopus
  73. T. Wynn and L. Barron, “Macrophages: master regulators of inflammation and fibrosis,” Seminars in Liver Disease, vol. 30, no. 03, pp. 245–257, 2010. View at Publisher · View at Google Scholar · View at Scopus
  74. S. K. Biswas and A. Mantovani, “Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm,” Nature Immunology, vol. 11, no. 10, pp. 889–896, 2010. View at Publisher · View at Google Scholar · View at Scopus
  75. G. Casella, L. Garzetti, A. T. Gatta et al., “IL4 induces IL6-producing M2 macrophages associated to inhibition of neuroinflammation in vitro and in vivo,” Journal of Neuroinflammation, vol. 13, no. 1, p. 139, 2016. View at Publisher · View at Google Scholar · View at Scopus
  76. H. Yong, G. Chartier, and J. Quandt, “Modulating inflammation and neuroprotection in multiple sclerosis,” Journal of Neuroscience Research, pp. 1–24, 2017. View at Publisher · View at Google Scholar
  77. C. S. Constantinescu, N. Farooqi, K. O'Brien, and B. Gran, “Experimental autoimmune encephalomyelitis (EAE) as a model for multiple sclerosis (MS),” British Journal of Pharmacology, vol. 164, no. 4, pp. 1079–1106, 2011. View at Publisher · View at Google Scholar · View at Scopus
  78. M. K. Mishra and V. W. Yong, “Myeloid cells — targets of medication in multiple sclerosis,” Nature Reviews Neurology, vol. 12, no. 9, pp. 539–551, 2016. View at Publisher · View at Google Scholar · View at Scopus
  79. F. Ebner, C. Brandt, P. Thiele et al., “Microglial activation milieu controls regulatory T cell responses,” The Journal of Immunology, vol. 191, no. 11, pp. 5594–5602, 2013. View at Publisher · View at Google Scholar · View at Scopus
  80. B. Ajami, J. L. Bennett, C. Krieger, K. M. McNagny, and F. M. V. Rossi, “Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool,” Nature Neuroscience, vol. 14, no. 9, pp. 1142–1149, 2011. View at Publisher · View at Google Scholar · View at Scopus
  81. D. Hambardzumyan, D. H. Gutmann, and H. Kettenmann, “The role of microglia and macrophages in glioma maintenance and progression,” Nature Neuroscience, vol. 19, no. 1, pp. 20–27, 2016. View at Publisher · View at Google Scholar · View at Scopus
  82. Y. Komohara, K. Ohnishi, J. Kuratsu, and M. Takeya, “Possible involvement of the M2 anti-inflammatory macrophage phenotype in growth of human gliomas,” The Journal of Pathology, vol. 216, no. 1, pp. 15–24, 2008. View at Publisher · View at Google Scholar · View at Scopus
  83. I. G. Dorward, J. Luo, A. Perry et al., “Postoperative imaging surveillance in pediatric pilocytic astrocytomas,” Journal of Neurosurgery: Pediatrics, vol. 6, no. 4, pp. 346–352, 2010. View at Publisher · View at Google Scholar · View at Scopus
  84. G. W. Simmons, W. W. Pong, R. J. Emnett et al., “Neurofibromatosis-1 heterozygosity increases microglia in a spatially and temporally restricted pattern relevant to mouse optic glioma formation and growth,” Journal of Neuropathology & Experimental Neurology, vol. 70, no. 1, pp. 51–62, 2011. View at Publisher · View at Google Scholar · View at Scopus
  85. D. H. Gutmann, M. D. McLellan, I. Hussain et al., “Somatic neurofibromatosis type 1 (NF1) inactivation characterizes NF1-associated pilocytic astrocytoma,” Genome Research, vol. 23, no. 3, pp. 431–439, 2013. View at Publisher · View at Google Scholar · View at Scopus
  86. F. Szulzewsky, A. Pelz, X. Feng et al., “Glioma-associated microglia/macrophages display an expression profile different from M1 and M2 polarization and highly express Gpnmb and Spp1,” PLoS One, vol. 10, no. 2, article e0116644, 2015. View at Publisher · View at Google Scholar · View at Scopus
  87. J. Wei, K. Gabrusiewicz, and A. Heimberger, “The controversial role of microglia in malignant gliomas,” Clinical and Developmental Immunology, vol. 2013, Article ID 285246, 12 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  88. H. Zhai, F. L. Heppner, and S. E. Tsirka, “Microglia/macrophages promote glioma progression,” Glia, vol. 59, no. 3, pp. 472–485, 2011. View at Publisher · View at Google Scholar · View at Scopus
  89. I. Bettinger, S. Thanos, and W. Paulus, “Microglia promote glioma migration,” Acta Neuropathologica, vol. 103, no. 4, pp. 351–355, 2002. View at Publisher · View at Google Scholar · View at Scopus
  90. H. Galarneau, J. Villeneuve, G. Gowing, J. P. Julien, and L. Vallieres, “Increased glioma growth in mice depleted of macrophages,” Cancer Research, vol. 67, no. 18, pp. 8874–8881, 2007. View at Publisher · View at Google Scholar · View at Scopus
  91. A. C. Carvalho da Fonseca, H. Wang, H. Fan et al., “Increased expression of stress inducible protein 1 in glioma-associated microglia/macrophages,” Journal of Neuroimmunology, vol. 274, no. 1-2, pp. 71–77, 2014. View at Publisher · View at Google Scholar · View at Scopus
  92. S. J. Coniglio, E. Eugenin, K. Dobrenis et al., “Microglial stimulation of glioblastoma invasion involves epidermal growth factor receptor (EGFR) and colony stimulating factor 1 receptor (CSF-1R) signaling,” Molecular Medicine, vol. 18, pp. 519–527, 2012. View at Publisher · View at Google Scholar
  93. A. Wesolowska, A. Kwiatkowska, L. Slomnicki et al., “Microglia-derived TGF-β as an important regulator of glioblastoma invasion—an inhibition of TGF-β-dependent effects by shRNA against human TGF-β type II receptor,” Oncogene, vol. 27, no. 7, pp. 918–930, 2008. View at Publisher · View at Google Scholar · View at Scopus
  94. W. Wick, M. Platten, and M. Weller, “Glioma cell invasion: regulation of metalloproteinase activity by TGF-β,” Journal of Neuro-Oncology, vol. 53, no. 2, pp. 177–185, 2001. View at Publisher · View at Google Scholar · View at Scopus
  95. X. Chen, L. Zhang, I. Y. Zhang et al., “RAGE expression in tumor-associated macrophages promotes angiogenesis in glioma,” Cancer Research, vol. 74, no. 24, pp. 7285–7297, 2014. View at Publisher · View at Google Scholar · View at Scopus
  96. S. M. Pyonteck, L. Akkari, A. J. Schuhmacher et al., “CSF-1R inhibition alters macrophage polarization and blocks glioma progression,” Nature Medicine, vol. 19, no. 10, pp. 1264–1272, 2013. View at Publisher · View at Google Scholar · View at Scopus
  97. J. Zhang, S. Sarkar, R. Cua, Y. Zhou, W. Hader, and V. W. Yong, “A dialog between glioma and microglia that promotes tumor invasiveness through the CCL2/CCR2/interleukin-6 axis,” Carcinogenesis, vol. 33, no. 2, pp. 312–319, 2012. View at Publisher · View at Google Scholar · View at Scopus
  98. N. Saederup, A. E. Cardona, K. Croft et al., “Selective chemokine receptor usage by central nervous system myeloid cells in CCR2-red fluorescent protein knock-in mice,” PLoS One, vol. 5, no. 10, article e13693, 2010. View at Publisher · View at Google Scholar · View at Scopus
  99. F. Hu, O. D. a Dzaye, A. Hahn et al., “Glioma-derived versican promotes tumor expansion via glioma-associated microglial/macrophages toll-like receptor 2 signaling,” Neuro-Oncology, vol. 17, no. 2, pp. 200–210, 2015. View at Publisher · View at Google Scholar · View at Scopus
  100. J. Yin, J. M. Markert, and J. W. Leavenworth, “Modulation of the intratumoral immune landscape by oncolytic herpes simplex virus virotherapy,” Frontiers in Oncology, vol. 7, 2017. View at Publisher · View at Google Scholar
  101. S. Bao, Q. Wu, R. E. McLendon et al., “Glioma stem cells promote radioresistance by preferential activation of the DNA damage response,” Nature, vol. 444, no. 7120, pp. 756–760, 2006. View at Publisher · View at Google Scholar · View at Scopus
  102. L. Yi, H. Xiao, M. Xu et al., “Glioma-initiating cells: a predominant role in microglia/macrophages tropism to glioma,” Journal of Neuroimmunology, vol. 232, no. 1-2, pp. 75–82, 2011. View at Publisher · View at Google Scholar · View at Scopus
  103. W. Zhou, S. Q. Ke, Z. Huang et al., “Periostin secreted by glioblastoma stem cells recruits M2 tumour-associated macrophages and promotes malignant growth,” Nature Cell Biology, vol. 17, no. 2, pp. 170–182, 2015. View at Publisher · View at Google Scholar · View at Scopus
  104. X. Ye, S. Xu, Y. Xin et al., “Tumor-associated microglia/macrophages enhance the invasion of glioma stem-like cells via TGF-β1 signaling pathway,” The Journal of Immunology, vol. 189, no. 1, pp. 444–453, 2012. View at Publisher · View at Google Scholar · View at Scopus
  105. S. Sarkar, A. Döring, F. J. Zemp et al., “Therapeutic activation of macrophages and microglia to suppress brain tumor-initiating cells,” Nature Neuroscience, vol. 17, no. 1, pp. 46–55, 2014. View at Publisher · View at Google Scholar · View at Scopus
  106. A. Wu, J. Wei, L. Y. Kong et al., “Glioma cancer stem cells induce immunosuppressive macrophages/microglia,” Neuro-Oncology, vol. 12, no. 11, pp. 1113–1125, 2010. View at Publisher · View at Google Scholar · View at Scopus
  107. L. M. Metz, D. K. B. Li, A. L. Traboulsee et al., “Trial of minocycline in a clinically isolated syndrome of multiple sclerosis,” The New England Journal of Medicine, vol. 376, no. 22, pp. 2122–2133, 2017. View at Publisher · View at Google Scholar
  108. M. G. Morvan and L. L. Lanier, “NK cells and cancer: you can teach innate cells new tricks,” Nature Reviews Cancer, vol. 16, no. 1, pp. 7–19, 2016. View at Publisher · View at Google Scholar · View at Scopus
  109. T. Michel, F. Hentges, and J. Zimmer, “Consequences of the crosstalk between monocytes/macrophages and natural killer cells,” Frontiers in Immunology, vol. 3, p. 403, 2013. View at Publisher · View at Google Scholar · View at Scopus
  110. E. Raz, “Organ-specific regulation of innate immunity,” Nature Immunology, vol. 8, no. 1, pp. 3-4, 2007. View at Publisher · View at Google Scholar · View at Scopus
  111. S. Nedvetzki, S. Sowinski, R. A. Eagle et al., “Reciprocal regulation of human natural killer cells and macrophages associated with distinct immune synapses,” Blood, vol. 109, no. 9, pp. 3776–3785, 2007. View at Publisher · View at Google Scholar · View at Scopus
  112. A. Lunemann, J. D. Lunemann, S. Roberts et al., “Human NK cells kill resting but not activated microglia via NKG2D- and NKp46-mediated recognition,” The Journal of Immunology, vol. 181, no. 9, pp. 6170–6177, 2008. View at Publisher · View at Google Scholar
  113. Z. Zhou, C. Zhang, J. Zhang, and Z. Tian, “Macrophages help NK cells to attack tumor cells by stimulatory NKG2D ligand but protect themselves from NK killing by inhibitory ligand Qa-1,” PLoS One, vol. 7, no. 5, article e36928, 2012. View at Publisher · View at Google Scholar · View at Scopus
  114. J. W. Leavenworth, C. Schellack, H. J. Kim, L. Lu, P. Spee, and H. Cantor, “Analysis of the cellular mechanism underlying inhibition of EAE after treatment with anti-NKG2A F(ab)2,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 6, pp. 2562–2567, 2010. View at Publisher · View at Google Scholar · View at Scopus
  115. J. W. Leavenworth, X. Wang, C. S. Wenander, P. Spee, and H. Cantor, “Mobilization of natural killer cells inhibits development of collagen-induced arthritis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 35, pp. 14584–14589, 2011. View at Publisher · View at Google Scholar · View at Scopus