An updated assessment of microglia depletion: Current concepts and future directions

Molecular Brain

Volumn 10, Issue 1, 2017, Pages

  Han, Jinming ^a   Harris, Robert A ^a   Zhang, Xing Mei ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Depletion; Microglia; Neuroinflammation

Indexed keywords

CD11B ANTIGEN; CD45 ANTIGEN; CLODRONIC ACID; GW 2580; MAC 1 SAPORIN; PEXIDARTINIB; PLX 5622; SAPORIN; UNCLASSIFIED DRUG;

BONE MARROW CELL; CELL DIFFERENTIATION; CELL POPULATION; CELL PROLIFERATION; DEPLETION; DRUG ACTIVITY; GENETIC MANIPULATION; HEMATOPOIETIC STEM CELL; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; MACROPHAGE; MICROGLIA; MICROGLIA DEPLETION; MONOCYTE; NERVE CELL PLASTICITY; NEUROPROTECTION; NON YOLK SAC; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; YOLK SAC; ANIMAL; CYTOLOGY; GENETIC PROCEDURES; METABOLISM;

ANIMALS; GENETIC TECHNIQUES; HUMANS; MICROGLIA; MYELOID CELLS; YOLK SAC;

EID: 85020893861     PISSN: None     EISSN: 17566606     Source Type: Journal    
DOI: 10.1186/s13041-017-0307-x     Document Type: Review

References (86)

1. Sierra A, de Castro F, Del Rio-Hortega J, Rafael Iglesias-Rozas J, Garrosa M, Kettenmann H. The »Big-Bang» for modern glial biology: translation and comments on Pio del Rio-Hortega 1919 series of papers on microglia. Glia. 2016;64:1801-40.
2. Wolf SA, Boddeke HW, Kettenmann H. Microglia in physiology and disease. Annu Rev Physiol. 2016
3. Masuda T, Prinz M. Microglia: a unique versatile cell in the central nervous system. ACS Chem Neurosci. 2016;7:428-34.
4. Benarroch EE. Microglia: Multiple roles in surveillance, circuit shaping, and response to injury. Neurology. 2013;81:1079-88.
5. Grubman A, Kanninen KM, Malm T. Multitasking Microglia and Alzheimer's disease: diversity, tools and therapeutic targets. J Mol Neurosci. 2016;60:390-404.
6. Du L, Zhang Y, Chen Y, Zhu J, Yang Y, Zhang HL. Role of microglia in neurological disorders and their potentials as a therapeutic target. Mol Neurobiol. 2016
7. Guruswamy R, El Ali A. Complex roles of microglial cells in ischemic stroke pathobiology: new insights and future directions. Int J Mol Sci. 2017:18.
8. Eyo UB, Murugan M, Wu LJ. Microglia-neuron communication in epilepsy. Glia. 2017;65:5-18.
9. Hambardzumyan D, Gutmann DH, Kettenmann H. The role of microglia and macrophages in glioma maintenance and progression. Nat Neurosci. 2016;19:20-7.
10. Rodriguez MJ, Mahy N. Neuron-microglia interactions in motor neuron degeneration. The inflammatory hypothesis in amyotrophic lateral sclerosis revisited. Curr Med Chem. 2016;23:4753-72.
11. Le W, Wu J, Tang Y. Protective microglia and their regulation in Parkinson's disease. Front Mol Neurosci. 2016;9:89.
12. Zhao H, Alam A, Chen Q, AE M, Pal A, Eguchi S, et al. The role of microglia in the pathobiology of neuropathic pain development: what do we know? Br J Anaesth. 2017;118:504-16.
13. Peng J, Gu N, Zhou L, BE U, Murugan M, Gan WB, et al. Microglia and monocytes synergistically promote the transition from acute to chronic pain after nerve injury. Nat Commun. 2016;7:12029.
14. Michell-Robinson MA, Touil H, Healy LM, Owen DR, Durafourt BA, Bar-Or A, et al. Roles of microglia in brain development, tissue maintenance and repair. Brain. 2015;138:1138-1159.
15. Mosser CA, Baptista S, Arnoux I, Audinat E. Microglia in CNS development: shaping the brain for the future. Progress in neurobiology. 2017
16. Jin X, Yamashita T. Microglia in central nervous system repair after injury. J Biochem. 2016;159:491-6.
17. Colonna M, Butovsky O. Microglia function in the central nervous system during health and neurodegeneration. Annu Rev Immunol. 2017
18. Thompson KK, Tsirka SE. The diverse roles of microglia in the neurodegenerative aspects of Central Nervous System (CNS) autoimmunity. Int J Mol Sci. 2017;18
19. Shemer A, Erny D, Jung S, Prinz M. Microglia plasticity during health and disease: an immunological perspective. Trends Immunol. 2015;36:614-24.
20. Schafer DP, Stevens B. Microglia function in central nervous system development and plasticity. Cold Spring Harb Perspect Biol. 2015;7:a020545.
21. Bilimoria PM, Stevens B. Microglia function during brain development: new insights from animal models. Brain Res. 2015;1617:7-17.
22. Reemst K, Noctor SC, Lucassen PJ, Hol EM. The inedispensable roles of microglia and astrocytes during brain development. Front Hum Neurosci. 2016;10:566.
23. Hong S, Dissing-Olesen L, Stevens B. New insights on the role of microglia in synaptic pruning in health and disease. Curr Opin Neurobiol. 2016;36:128-34.
24. Frost JL, Schafer DP. Microglia: architects of the developing nervous system. Trends Cell Biol. 2016;26:587-97.
25. Kettenmann H, Kirchhoff F, Verkhratsky A. Microglia: new roles for the synaptic stripper. Neuron. 2013;77:10-8.
26. Tang Y, Le W. Differential roles of M1 and M2 microglia in neurodegenerative diseases. Mol Neurobiol. 2016;53:1181-94.
27. Fan X, Zhang H, Cheng Y, Jiang X, Zhu J, Jin T. Double roles of macrophages in human neuroimmune diseases and their animal models. Mediat Inflamm. 2016;2016:8489251.
28. Bogie JF, Stinissen P, Hendriks JJ. Macrophage subsets and microglia in multiple sclerosis. Acta Neuropathol. 2014;128:191-213.
29. Cartier N, Lewis CA, Zhang R, Rossi FM. The role of microglia in human disease: therapeutic tool or target? Acta Neuropathol. 2014;128:363-80.
30. Biber K, Moller T, Boddeke E, Prinz M. Central nervous system myeloid cells as drug targets: current status and translational challenges. Nat Rev Drug Discov. 2016;15:110-24.
31. Zhang XM, Lund H, Mia S, Parsa R, Harris RA. Adoptive transfer of cytokine-induced immunomodulatory adult microglia attenuates experimental autoimmune encephalomyelitis in DBA/1 mice. Glia. 2014;62:804-17.
32. Mia S, Warnecke A, Zhang XM, Malmstrom V, Harris RA. An optimized protocol for human M2 macrophages using M-CSF and IL-4/IL-10/TGF-beta yields a dominant immunosuppressive phenotype. Scand J Immunol. 2014;79:305-14.
33. Ginhoux F, Prinz M. Origin of microglia: current concepts and past controversies. Cold Spring Harb Perspect Biol. 2015;7:a020537.
34. Mildner A, Schmidt H, Nitsche M, Merkler D, Hanisch UK, Mack M, et al. Microglia in the adult brain arise from Ly-6ChiCCR2+ monocytes only under defined host conditions. Nat Neurosci. 2007;10:1544-53.
35. Sheng J, Ruedl C, Karjalainen K. Most tissue-resident macrophages except microglia are derived from fetal hematopoietic stem cells. Immunity. 2015;43:382-93.
36. Crotti A, Ransohoff RM. Microglial physiology and pathophysiology: insights from genome-wide transcriptional profiling. Immunity. 2016;44:505-15.
37. Ginhoux F, Greter M, Leboeuf M, Nandi S, See P, Gokhan S, et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science. 2010;330:841-5.
38. Tay TL, Hagemeyer N, Prinz M. The force awakens: insights into the origin and formation of microglia. Curr Opin Neurobiol. 2016;39:30-7.
39. Prinz M, Priller J. Microglia and brain macrophages in the molecular age: from origin to neuropsychiatric disease. Nat Rev Neurosci. 2014;15:300-12.
40. Prinz M, Erny D, Hagemeyer N. Ontogeny and homeostasis of CNS myeloid cells. Nat Immunol. 2017;18:385-92.
41. Askew K, Gomez-Nicola D. A story of birth and death: Insights into the formation and dynamics of the microglial population. Brain Behav Immun. 2017
42. Gomez Perdiguero E, Klapproth K, Schulz C, Busch K, Azzoni E, Crozet L, et al. Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature. 2015;518:547-51.
43. Derecki NC, Katzmarski N, Kipnis J, Meyer-Luehmann M. Microglia as a critical player in both developmental and late-life CNS pathologies. Acta Neuropathol. 2014;128:333-45.
44. De I, Nikodemova M, Steffen MD, Sokn E, Maklakova VI, Watters JJ, et al. CSF1 overexpression has pleiotropic effects on microglia in vivo. Glia. 2014;62:1955-67.
45. Butovsky O, Jedrychowski MP, Moore CS, Cialic R, Lanser AJ, Gabriely G, et al. Identification of a unique TGF-beta-dependent molecular and functional signature in microglia. Nat Neurosci. 2014;17:131-43.
46. Muffat J, Li Y, Yuan B, Mitalipova M, Omer A, Corcoran S, et al. Efficient derivation of microglia-like cells from human pluripotent stem cells. Nat Med. 2016;22:1358-67.
47. Hammond TR, Stevens B. Increasing the neurological-disease toolbox using iPSC-derived microglia. Nat Med. 2016;22:1206-7.
48. Xu J, Zhu L, He S, Wu Y, Jin W, Yu T, et al. Temporal-spatial resolution fate mapping reveals distinct origins for embryonic and adult microglia in zebrafish. Dev Cell. 2015;34:632-41.
49. Askew K, Li K, Olmos-Alonso A, Garcia-Moreno F, Liang Y, Richardson P, et al. Coupled proliferation and apoptosis maintain the rapid turnover of microglia in the adult brain. Cell Rep. 2017;18:391-405.
50. Hughes EG, Bergles DE. Hidden progenitors replace microglia in the adult brain. Neuron. 2014;82:253-5.
51. Elmore MR, Najafi AR, Koike MA, Dagher NN, Spangenberg EE, Rice RA, et al. Colony-stimulating factor 1 receptor signaling is necessary for microglia viability, unmasking a microglia progenitor cell in the adult brain. Neuron. 2014;82:380-97.
52. Bennett ML, Bennett FC, Liddelow SA, Ajami B, Zamanian JL, Fernhoff NB, et al. New tools for studying microglia in the mouse and human CNS. Proc Natl Acad Sci U S A. 2016;113:E1738-46.
53. Wohleb ES, Delpech JC. Dynamic cross-talk between microglia and peripheral monocytes underlies stress-induced neuroinflammation and behavioral consequences. Prog Neuro-Psychopharmacol Biol Psychiatry. 2016
54. Sousa C, Biber K, Michelucci A. Cellular and molecular characterization of microglia: a unique immune cell population. Front Immunol. 2017;8:198.
55. Glass R, Synowitz M. CNS macrophages and peripheral myeloid cells in brain tumours. Acta Neuropathol. 2014;128:347-62.
56. Waisman A, Ginhoux F, Greter M, Bruttger J. Homeostasis of microglia in the adult brain: review of novel microglia depletion systems. Trends Immunol. 2015;36:625-36.
57. Buttgereit A, Lelios I, Yu X, Vrohlings M, Krakoski NR, Gautier EL, et al. Sall1 is a transcriptional regulator defining microglia identity and function. Nat Immunol. 2016;17:1397-406.
58. Satoh J, Kino Y, Asahina N, Takitani M, Miyoshi J, Ishida T, et al. TMEM119 marks a subset of microglia in the human brain. Neuropathology. 2016;36:39-49.
59. Mills CD, Harris RA, Ley K. Macrophage polarization: decisions that affect health. Journal of clinical & cellular immunology. 2015;6
60. Harris RA. Spatial, temporal, and functional aspects of macrophages during »The Good, the Bad, and the Ugly» phases of inflammation. Front Immunol. 2014;5:612.
61. Parisi C, Napoli G, Pelegrin P, Volonte C. M1 and M2 functional imprinting of primary microglia: role of P2X7 activation and miR-125b. Mediat Inflamm. 2016;2016:2989548.
62. Pelegrin P, Surprenant A. Dynamics of macrophage polarization reveal new mechanism to inhibit IL-1beta release through pyrophosphates. EMBO J. 2009;28:2114-27.
63. Elmore MR, Lee RJ, West BL, Green KN. Characterizing newly repopulated microglia in the adult mouse: impacts on animal behavior, cell morphology, and neuroinflammation. PLoS One. 2015;10:e0122912.
64. Rice RA, Pham J, Lee RJ, Najafi AR, West BL, Green KN. Microglial repopulation resolves inflammation and promotes brain recovery after injury. Glia. 2017
65. Spangenberg EE, Lee RJ, Najafi AR, Rice RA, Elmore MR, Blurton-Jones M, et al. Eliminating microglia in Alzheimer's mice prevents neuronal loss without modulating amyloid-beta pathology. Brain J Neurol. 2016;139:1265-81.
66. Li M, Li Z, Ren H, Jin WN, Wood K, Liu Q, et al. Colony stimulating factor 1 receptor inhibition eliminates microglia and attenuates brain injury after intracerebral hemorrhage. J Cereb Blood Flow Metab. 2016
67. Szalay G, Martinecz B, Lenart N, Kornyei Z, Orsolits B, Judak L, et al. Microglia protect against brain injury and their selective elimination dysregulates neuronal network activity after stroke. Nat Commun. 2016;7:11499.
68. Yao Y, Echeverry S, Shi XQ, Yang M, Yang QZ, Wang GY, et al. Dynamics of spinal microglia repopulation following an acute depletion. Sci Rep. 2016;6:22839.
69. Jin WN, Shi SX, Li Z, Li M, Wood K, Gonzales RJ, et al. Depletion of microglia exacerbates postischemic inflammation and brain injury. J Cereb Blood Flow Metab. 2017:271678X17694185.
70. Acharya MM, Green KN, Allen BD, Najafi AR, Syage A, Minasyan H, et al. Elimination of microglia improves cognitive function following cranial irradiation. Sci Rep. 2016;6:31545.
71. Chalmers SA, Wen J, Shum J, Doerner J, Herlitz L, Putterman C. CSF-1R inhibition attenuates renal and neuropsychiatric disease in murine lupus. Clin Immunol. 2016
72. Jakel S, Dimou L. Glial cells and their function in the adult brain: a journey through the history of their ablation. Front Cell Neurosci. 2017;11:24.
73. Crespo O, Kang SC, Daneman R, Lindstrom TM, Ho PP, Sobel RA, et al. Tyrosine kinase inhibitors ameliorate autoimmune encephalomyelitis in a mouse model of multiple sclerosis. J Clin Immunol. 2011;31:1010-20.
74. Eyo UB, Wu LJ. Bidirectional microglia-neuron communication in the healthy brain. Neural Plast. 2013;2013:456857.
75. Torres L, Danver J, Ji K, Miyauchi JT, Chen D, Anderson ME, et al. Dynamic microglial modulation of spatial learning and social behavior. Brain Behav Immun. 2016;55:6-16.
76. Nelson LH, Lenz KM. Microglia depletion in early life programs persistent changes in social, mood-related, and locomotor behavior in male and female rats. Behav Brain Res. 2017;316:279-93.
77. VanRyzin JW, Yu SJ, Perez-Pouchoulen M, McCarthy MM. Temporary depletion of microglia during the early postnatal period induces lasting sex-dependent and sex-independent effects on behavior in rats. eNeuro. 2016;3
78. Gowing G, Vallieres L, Julien JP. Mouse model for ablation of proliferating microglia in acute CNS injuries. Glia. 2006;53:331-7.
79. Varvel NH, Grathwohl SA, Baumann F, Liebig C, Bosch A, Brawek B, et al. Microglial repopulation model reveals a robust homeostatic process for replacing CNS myeloid cells. Proc Natl Acad Sci U S A. 2012;109:18150-5.
80. Bennett RE, Brody DL. Acute reduction of microglia does not alter axonal injury in a mouse model of repetitive concussive traumatic brain injury. J Neurotrauma. 2014;31:1647-63.
81. Heppner FL, Greter M, Marino D, Falsig J, Raivich G, Hovelmeyer N, et al. Experimental autoimmune encephalomyelitis repressed by microglial paralysis. Nat Med. 2005;11:146-52.
82. Gowing G, Philips T, Van Wijmeersch B, Audet JN, Dewil M, Van Den Bosch L, et al. Ablation of proliferating microglia does not affect motor neuron degeneration in amyotrophic lateral sclerosis caused by mutant superoxide dismutase. J Neurosci. 2008;28:10234-44.
83. Wieghofer P, Knobeloch KP, Prinz M. Genetic targeting of microglia. Glia. 2015;63:1-22.
84. Parkhurst CN, Yang G, Ninan I, Savas JN, Yates JR 3rd, Lafaille JJ, et al. Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell. 2013;155:1596-609.
85. Bruttger J, Karram K, Wortge S, Regen T, Marini F, Hoppmann N, et al. Genetic cell ablation reveals clusters of local self-renewing microglia in the mammalian central nervous system. Immunity. 2015;43:92-106.
86. Wieghofer P, Prinz M. Genetic manipulation of microglia during brain development and disease. Biochim Biophys Acta. 1862;2016:299-309.