Microglia in CNS development: Shaping the brain for the future

Progress in Neurobiology

Volumn 149-150, Issue , 2017, Pages 1-20

  Mosser, Coralie Anne ^a,b   Baptista, Sofia ^a,b   Arnoux, Isabelle ^c   Audinat, Etienne ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Inflammation; Macrophage; Neurodevelopmental disorder; Neuron; Pre and postnatal development; Synapse

Indexed keywords

APOPTOSIS; CELL DEATH; CELL MATURATION; CELL MIGRATION; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; DEVELOPMENTAL DISORDER; HUMAN; MICROGLIA; NERVE CELL GROWTH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; REVIEW; SYNAPSE; ANIMAL; GROWTH, DEVELOPMENT AND AGING; NEURODEVELOPMENTAL DISORDERS; PHYSIOLOGY;

ANIMALS; CENTRAL NERVOUS SYSTEM; HUMANS; MICROGLIA; NEURODEVELOPMENTAL DISORDERS;

EID: 85011841883     PISSN: 03010082     EISSN: 18735118     Source Type: Journal    
DOI: 10.1016/j.pneurobio.2017.01.002     Document Type: Review

References (244)

1. Šišková, Z., Tremblay, M.-È., Microglia and synapse: interactions in health and neurodegeneration. Neural Plast., 2013, 2013, 425845, 10.1155/2013/425845.
2. Allendoerfer, K.L., Shatz, C.J., The subplate, a transient neocortical structure: its role in the development of connections between thalamus and cortex. Annu. Rev. Neurosci. 17 (1994), 185–218, 10.1146/annurev.ne.17.030194.001153.
3. Alliot, F., Lecain, E., Grima, B., Pessac, B., Microglial progenitors with a high proliferative potential in the embryonic and adult mouse brain. Proc. Natl. Acad. Sci. U. S. A. 88 (1991), 1541–1545.
4. Amateau, S.K., McCarthy, M.M., Induction of PGE2 by estradiol mediates developmental masculinization of sex behavior. Nat. Neurosci. 7 (2004), 643–650, 10.1038/nn1254.
5. Antony, J.M., Paquin, A., Nutt, S.L., Kaplan, D.R., Miller, F.D., Endogenous microglia regulate development of embryonic cortical precursor cells. J. Neurosci. Res. 89 (2011), 286–298, 10.1002/jnr.22533.
6. Araque, A., Carmignoto, G., Haydon, P.G., Oliet, S.H., Robitaille, R., Volterra, A., Gliotransmitters travel in time and space. Neuron 81 (2014), 728–739, 10.1016/j.neuron.2014.02.007.
7. Arno, B., Grassivaro, F., Rossi, C., Bergamaschi, A., Castiglioni, V., Furlan, R., Greter, M., Favaro, R., Comi, G., Becher, B., Martino, G., Muzio, L., Neural progenitor cells orchestrate microglia migration and positioning into the developing cortex. Nat. Commun., 5, 2014, 5611.
8. Arnoux, I., Audinat, E., Fractalkine signaling and microglia functions in the developing brain. Neural Plast. 80 (2015), 43–56, 10.1155/2015/689404.
9. Arnoux, I., Hoshiko, M., Mandavy, L., Avignone, E., Yamamoto, N., Audinat, E., Adaptive phenotype of microglial cells during the normal postnatal development of the somatosensory Barrel cortex. Glia 61 (2013), 1582–1594.
10. Arnoux, I., Hoshiko, M., Sanz, D.A., Audinat, E., Paradoxical effects of minocycline in the developing mouse somatosensory cortex. Glia 62 (2014), 399–410.
11. Ashwell, K., Development of microglia in the albino rabbit retina. J. Comp. Neurol. 287 (1989), 286–301.
12. Ashwell, K., Microglia and cell death in the developing mouse cerebellum. Brain Res. Dev. Brain Res. 55 (1990), 219–230.
13. Askew, K., Li, K., Olmos-Alonso, A., Garcia-Moreno, F., Liang, Y., Richardson, P., Tipton, T., Chapman, M.A., Riecken, K., Beccari, S., Sierra, A., Molnár, Z., Cragg, M.S., Garaschuk, O., Perry, V.H., Gomez-Nicola, D., Coupled proliferation and apoptosis maintain the rapid turnover of microglia in the adult brain. Cell Rep. 18 (2017), 391–405, 10.1016/j.celrep.2016.12.041.
14. Avignone, E., Ulmann, L., Levavasseur, F., Rassendren, F., Audinat, E., Status epilepticus induces a particular microglial activation state characterized by enhanced purinergic signaling. J. Neurosci. 28 (2008), 9133–9144.
15. Beattie, E.C., Stellwagen, D., Morishita, W., Bresnahan, J.C., Ha, B.K., Von Zastrow, M., Beattie, M.S., Malenka, R.C., Control of synaptic strength by glial TNFalpha. Science (80-.) 295 (2002), 2282–2285, 10.1126/science.1067859.
16. Bechade, C., Cantaut-Belarif, Y., Bessis, A., Microglial control of neuronal activity. Front. Cell. Neurosci., 7, 2013, 32.
17. Bergon, A., Belzeaux, R., Comte, M., Pelletier, F., Hervé, M., Gardiner, E.J., Beveridge, N.J., Liu, B., Carr, V., Scott, R.J., Kelly, B., Cairns, M.J., Kumarasinghe, N., Schall, U., Blin, O., Boucraut, J., Tooney, P.A., Fakra, E., Ibrahim, E.C., CX3CR1 is dysregulated in blood and brain from schizophrenia patients. Schizophr. Res. 168 (2015), 434–443, 10.1016/j.schres.2015.08.010.
18. Bertrand, J.Y., Jalil, A., Klaine, M., Jung, S., Cumano, A., Godin, I., Three pathways to mature macrophages in the early mouse yolk sac. Blood 106 (2005), 3004–3011.
19. Bezzi, P., Domercq, M., Brambilla, L., Galli, R., Schols, D., De Clercq, E., Vescovi, A., Bagetta, G., Kollias, G., Meldolesi, J., Volterra, A., CXCR4-activated astrocyte glutamate release via TNFalpha: amplification by microglia triggers neurotoxicity. Nat. Neurosci. 4 (2001), 702–710.
20. Bialas, A.R., Stevens, B., Supplemental_TGF-β signaling regulates neuronal C1q expression and developmental synaptic refinement. Nat. Neurosci. 16 (2013), 1773–1782, 10.1038/nn.3560.
21. Biber, K., Neumann, H., Inoue, K., Boddeke, H.W., Neuronal on and off signals control microglia. Trends Neurosci. 30 (2007), 596–602.
22. Blinzinger, K., Kreutzberg, G., Displacement of synaptic terminals from regenerating motoneurons by microglial cells. Z. Zellforsch. Mikrosk. Anat. 85 (1968), 145–157.
23. Boche, D., Perry, V.H., Nicoll, J.A., Review: activation patterns of microglia and their identification in the human brain. Neuropathol. Appl. Neurobiol. 39 (2013), 3–18.
24. Boksa, P., Effects of prenatal infection on brain development and behavior: a review of findings from animal models. Brain Behav. Immun., 2010, 10.1016/j.bbi.2010.03.005.
25. Boucsein, C., Kettenmann, H., Nolte, C., Electrophysiological properties of microglial cells in normal and pathologic rat brain slices. Eur. J. Neurosci. 12 (2000), 2049–2058 (ejn100 [pii]).
26. Brawek, B., Garaschuk, O., Microglial calcium signaling in the adult, aged and diseased brain. Cell Calcium, 2013, 10.1016/j.ceca.2012.12.003.
27. Brockhaus, J., Ilschner, S., Banati, R.B., Kettenmann, H., Membrane properties of ameboid microglial cells in the corpus callosum slice from early postnatal mice. J. Neurosci. 13 (1993), 4412–4421.
28. Brown, G.C., Neher, J.J., Microglial phagocytosis of live neurons. Nat. Rev. Neurosci. 15 (2014), 209–216, 10.1038/nrn3710.
29. Butovsky, O., Jedrychowski, M.P., Moore, C.S., Cialic, R., Lanser, A.J., Gabriely, G., Koeglsperger, T., Dake, B., Wu, P.M., Doykan, C.E., Fanek, Z., Liu, L., Chen, Z., Rothstein, J.D., Ransohoff, R.M., Gygi, S.P., Antel, J.P., Weiner, H.L., Identification of a unique TGF-β-dependent molecular and functional signature in microglia. Nat. Neurosci. 17 (2014), 131–143, 10.1038/nn.3599.
30. Caetano, L., Pinheiro, H., Patrício, P., Mateus-Pinheiro, A., Alves, N.D., Coimbra, B., Baptista, F.I., Henriques, S.N., Cunha, C., Santos, A.R., Ferreira, S.G., Sardinha, V.M., Oliveira, J.F., Ambrósio, A.F., Sousa, N., Cunha, R.A., Rodrigues, A.J., Pinto, L., Gomes, C.A., Adenosine A2A receptor regulation of microglia morphological remodeling-gender bias in physiology and in a model of chronic anxiety. Mol. Psychiatry, 2016, 10.1038/mp.2016.173.
31. Cai, Z., Pan, Z.L., Pang, Y., Evans, O.B., Rhodes, P.G., Cytokine induction in fetal rat brains and brain injury in neonatal rats after maternal lipopolysaccharide administration. Pediatr. Res. 47 (2000), 64–72, 10.1203/00006450-200001000-00013.
32. Caldero, J., Brunet, N., Ciutat, D., Hereu, M., Esquerda, J.E., Development of microglia in the chick embryo spinal cord: implications in the regulation of motoneuronal survival and death. J. Neurosci. Res. 87 (2009), 2447–2466.
33. Cao, M., Cortes, M., Moore, C.S., Leong, S.Y., Durosier, L.D., Burns, P., Fecteau, G., Desrochers, A., Auer, R.N., Barreiro, L.B., Antel, J.P., Frasch, M.G., Fetal microglial phenotype in vitro carries memory of prior in vivo exposure to inflammation. Front Cell Neurosci., 9, 2015, 294, 10.3389/fncel.2015.00294.
34. Cardona, A.E., Pioro, E.P., Sasse, M.E., Kostenko, V., Cardona, S.M., Dijkstra, I.M., Huang, D., Kidd, G., Dombrowski, S., Dutta, R., Lee, J.C., Cook, D.N., Jung, S., Lira, S.A., Littman, D.R., Ransohoff, R.M., Control of microglial neurotoxicity by the fractalkine receptor. Nat. Neurosci. 9 (2006), 917–924.
35. Cardona, A.E., Li, M., Liu, L., Savarin, C., Ransohoff, R.M., Chemokines in and out of the central nervous system: much more than chemotaxis and inflammation. J. Leukoc. Biol. 84 (2008), 587–594.
36. Chamak, B., Morandi, V., Mallat, M., Brain macrophages stimulate neurite growth and regeneration by secreting thrombospondin. J. Neurosci. Res. 38 (1994), 221–233.
37. Chamak, B., Dobbertin, A., Mallat, M., Immunohistochemical detection of thrombospondin in microglia in the developing rat brain. Neuroscience 69 (1995), 177–187.
38. Chen, S.-H., Oyarzabal, E.A., Hong, J.-S., Critical role of the Mac1/NOX2 pathway in mediating reactive microgliosis-generated chronic neuroinflammation and progressive neurodegeneration. Curr. Opin. Pharmacol. 26 (2016), 54–60, 10.1016/j.coph.2015.10.001.
39. Cho, S.H., Sun, B., Zhou, Y., Kauppinen, T.M., Halabisky, B., Wes, P., Ransohoff, R.M., Gan, L., CX3CR1 protein signaling modulates microglial activation and protects against plaque-independent cognitive deficits in a mouse model of Alzheimer disease. J. Biol. Chem. 286 (2011), 32713–32722.
40. Choi, G.B., Yim, Y.S., Wong, H., Kim, S., Kim, H., Kim, S.V., Hoeffer, C.A., Littman, D.R., Huh, J.R., The maternal interleukin-17a pathway in mice promotes autism-like phenotypes in offspring. Science (80-). 351 (2016), 933–939.
41. Christopherson, K.S., Ullian, E.M., Stokes, C.C.A., Mullowney, C.E., Hell, J.W., Agah, A., Lawler, J., Mosher, D.F., Bornstein, P., Barres, B.A., Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 120 (2005), 421–433, 10.1016/j.cell.2004.12.020.
42. Chung, W.-S., Clarke, L.E., Wang, G.X., Stafford, B.K., Sher, A., Chakraborty, C., Joung, J., Foo, L.C., Thompson, A., Chen, C., Smith, S.J., Barres, B.A., Astrocytes mediate synapse elimination through MEGF10 and MERTK pathways. Nature 504 (2013), 394–400, 10.1038/nature12776.
43. Chung, W.-S., Welsh, C.A., Barres, B.A., Stevens, B., Do glia drive synaptic and cognitive impairment in disease?. Nat. Neurosci. 18 (2015), 1539–1545, 10.1038/nn.4142.
44. Clark, A.K., Gruber-Schoffnegger, D., Drdla-Schutting, R., Gerhold, K.J., Malcangio, M., Sandkühler, J., Selective activation of microglia facilitates synaptic strength. J. Neurosci. 35 (2015), 4552–4570, 10.1523/JNEUROSCI.2061-14.2015.
45. Clarke, L.E., Barres, B.A., Emerging roles of astrocytes in neural circuit development. Nat. Rev. Neurosci. 14 (2013), 311–321, 10.1038/nrn3484.
46. Cronk, J.C., Derecki, N.C., Ji, E., Xu, Y., Lampano, A.E., Smirnov, I., Baker, W., Norris, G.T., Marin, I., Coddington, N., Wolf, Y., Turner, S.D., Aderem, A., Klibanov, A.L., Harris, T.H., Jung, S., Litvak, V., Kipnis, J., Methyl-CpG binding protein 2 regulates microglia and macrophage gene expression in response to inflammatory stimuli. Immunity 42 (2015), 679–691, 10.1016/j.immuni.2015.03.013.
47. Cuadros, M.A., Navascues, J., Early origin and colonization of the developing central nervous system by microglial precursors. Prog. Brain Res. 132 (2001), 51–59.
48. Cuadros, M.A., Rodriguez-Ruiz, J., Calvente, R., Almendros, A., Marin-Teva, J.L., Navascues, J., Microglia development in the quail cerebellum. J. Comp. Neurol. 389 (1997), 390–401.
49. Cunningham, C.L., Martinez-Cerdeno, V., Noctor, S.C., Microglia regulate the number of neural precursor cells in the developing cerebral cortex. J. Neurosci. 33 (2013), 4216–4233.
50. Dalmau, I., Finsen, B., Zimmer, J., Gonzalez, B., Castellano, B., Development of microglia in the postnatal rat hippocampus. Hippocampus 8 (1998), 458–474.
51. Dalmau, I., Vela, J.M., Gonzalez, B., Finsen, B., Castellano, B., Dynamics of microglia in the developing rat brain. J. Comp. Neurol. 458 (2003), 144–157.
52. Davalos, D., Grutzendler, J., Yang, G., Kim, J.V., Zuo, Y., Jung, S., Littman, D.R., Dustin, M.L., Gan, W.B., ATP mediates rapid microglial response to local brain injury in vivo. Nat. Neurosci. 8 (2005), 752–758.
53. De Groot, C.J., Huppes, W., Sminia, T., Kraal, G., Dijkstra, C.D., Determination of the origin and nature of brain macrophages and microglial cells in mouse central nervous system, using non-radioactive in situ hybridization and immunoperoxidase techniques. Glia 6 (1992), 301–309.
54. Degos, V., Favrais, G., Kaindl, A.M., Peineau, S., Guerrot, A.M., Verney, C., Gressens, P., Inflammation processes in perinatal brain damage. J. Neural. Transm. 117 (2010), 1009–1017.
55. Derecki, N.C., Cronk, J.C., Lu, Z., Xu, E., Abbott, S.B.G., Guyenet, P.G., Kipnis, J., Wild-type microglia arrest pathology in a mouse model of Rett syndrome. Nature 484 (2012), 105–109, 10.1038/nature10907.
56. Dinan, T.G., Cryan, J.F., Gut Instincts: microbiota as a key regulator of brain development, ageing and neurodegeneration. J. Physiol., 2016, 10.1113/jp273106.
57. Earle, K.L., Mitrofanis, J., Development of glia and blood vessels in the internal capsule of rats. J. Neurocytol. 27 (1998), 127–139.
58. Ekdahl, C.T., Microglial activation — tuning and pruning adult neurogenesis. Front. Pharmacol., 3, 2012, 41.
59. Elliott, M.R., Chekeni, F.B., Trampont, P.C., Lazarowski, E.R., Kadl, A., Walk, S.F., Park, D., Woodson, R.I., Ostankovich, M., Sharma, P., Lysiak, J.J., Harden, T.K., Leitinger, N., Ravichandran, K.S., Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 461 (2009), 282–286, 10.1038/nature08296.
60. Ellman, L.M., Deicken, R.F., Vinogradov, S., Kremen, W.S., Poole, J.H., Kern, D.M., Tsai, W.Y., Schaefer, C.A., Brown, A.S., Structural brain alterations in schizophrenia following fetal exposure to the inflammatory cytokine interleukin-8. Schizophr. Res. 121 (2010), 46–54, 10.1016/j.schres.2010.05.014.
61. Elmore, M.R., Najafi, A.R., Koike, M.A., Dagher, N.N., Spangenberg, E.E., Rice, R.A., Kitazawa, M., Matusow, B., Nguyen, H., West, B.L., Green, K.N., Colony-stimulating factor 1 receptor signaling is necessary for microglia viability, unmasking a microglia progenitor cell in the adult brain. Neuron 82 (2014), 380–397.
62. Erblich, B., Zhu, L., Etgen, A.M., Dobrenis, K., Pollard, J.W., Absence of colony stimulation factor-1 receptor results in loss of microglia, disrupted brain development and olfactory deficits. PLoS One, 6, 2011, e26317.
63. Erny, D., Hrabe de Angelis, A.L., Jaitin, D., Wieghofer, P., Staszewski, O., David, E., Keren-Shaul, H., Mahlakoiv, T., Jakobshagen, K., Buch, T., Schwierzeck, V., Utermohlen, O., Chun, E., Garrett, W.S., McCoy, K.D., Diefenbach, A., Staeheli, P., Stecher, B., Amit, I., Prinz, M., Host microbiota constantly control maturation and function of microglia in the CNS. Nat. Neurosci. 18 (2015), 965–977.
64. Erny, D., Hrabe de Angelis, A.L., Prinz, M., Communicating systems in the body: how microbiota and microglia cooperate. Immunology 150 (2017), 7–15.
65. Eyo, U.B., Wu, L.J., Bidirectional microglia-neuron communication in the healthy brain. Neural Plast., 2013, 2013, 456857.
66. Eyo, U.B., Miner, S.A., Weiner, J.A., Dailey, M.E., Developmental changes in microglial mobilization are independent of apoptosis in the neonatal mouse hippocampus. Brain Behav. Immun. 55 (2015), 49–59.
67. Fagiolini, M., Leblanc, J.J., Autism: a critical period disorder?. Neural Plast., 2011, 10.1155/2011/921680.
68. Fedoroff, S., Zhai, R., Novak, J.P., Microglia and astroglia have a common progenitor cell. J. Neurosci. Res. 50 (1997), 477–486.
69. Frade, J.M., Barde, Y.A., Microglia-derived nerve growth factor causes cell death in the developing retina. Neuron 20 (1998), 35–41.
70. Frick, L.R., Williams, K., Pittenger, C., Microglial dysregulation in psychiatric disease. Clin. Dev. Immunol., 2013, 10.1155/2013/608654.
71. Frost, J.L., Schafer, D.P., Microglia: architects of the developing nervous system. Trends Cell Biol., 2016, 10.1016/j.tcb.2016.02.006.
72. Fujita, S., Tsuchihashi, Y., Kitamura, T., Origin, morphology and function of the microglia. Prog. Clin. Biol. Res. 59A (1981), 141–169.
73. Garden, G.A., Epigenetics and the modulation of neuroinflammation. Neurotherapeutics, 2013, 10.1007/s13311-013-0207-4.
74. Ginhoux, F., Greter, M., Leboeuf, M., Nandi, S., See, P., Gokhan, S., Mehler, M.F., Conway, S.J., Ng, L.G., Stanley, E.R., Samokhvalov, I.M., Merad, M., Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science (80-.) 330 (2010), 841–845.
75. Ginhoux, F., Lim, S., Hoeffel, G., Low, D., Huber, T., Origin and differentiation of microglia. Front. Cell Neurosci., 7, 2013, 45.
76. Ginhoux, F., Schultze, J.L., Murray, P.J., Ochando, J., Biswas, S.K., New insights into the multidimensional concept of macrophage ontogeny, activation and function. Nat. Immunol. 17 (2015), 34–40, 10.1038/ni.3324.
77. Giovanoli, S., Engler, H., Engler, A., Richetto, J., Voget, M., Willi, R., Winter, C., Riva, M.A., Mortensen, P.B., Feldon, J., Schedlowski, M., Meyer, U., Brown, A.S., Pedersen, C.B., Mortensen, P.B., Herbert, M.R., Tsuchiya, K.J., Byrne, M., Mortensen, P.B., Green, J.G., Holmes, W.C., Slap, G.B., Brown, A.S., Patterson, P.H., Varese, F., Selten, J.P., Frissen, A., Lensvelt-Mulders, G., Morgan, V.A., Mednick, S.A., Machon, R.A., Huttunen, M.O., Bonett, D., Clarke, M.C., Tanskanen, A., Huttunen, M., Whittaker, J.C., Cannon, M., Bayer, T.A., Falkai, P., Maier, W., Maynard, T.M., Sikich, L., Lieberman, J.A., LaMantia, A.S., Meyer, U., Feldon, J., Fatemi, S.H., Spear, L.P., Fisher, H.L., Paus, T., Keshavan, M., Giedd, J.N., Hsiao, E.Y., McBride, S.W., Chow, J., Mazmanian, S.K., Patterson, P.H., Meyer, U., Feldon, J., Dammann, O., Frank, M.G., Baratta, M.V., Sprunger, D.B., Watkins, L.R., Maier, S.F., Franklin, T.B., Saab, B.J., Mansuy, I.M., Ransohoff, R.M., Perry, V.H., Ransohoff, R.M., Cardona, A.E., Bolton, J.L., Meyer, U., Feldon, J., Schedlowski, M., Yee, B.K., Brown, A.S., Atladóttir, H.O., Spear, L.P., Pruessner, M., Iyer, S.N., Faridi, K., Joober, R., Malla, A.K., Meyer, U., Feldon, J., Meyer, U., Patterson, P.H., Watanabe, Y., Someya, T., Nawa, H., Müller, N., Schwarz, M.J., Livak, K.J., Schmittgen, T.D., Winter, C., Vuillermot, S., Gundersen, H.J., et al. Stress in puberty unmasks latent neuropathological consequences of prenatal immune activation in mice. Science 339 (2013), 1095–1099, 10.1126/science.1228261.
78. Giovanoli, S., Weber-Stadlbauer, U., Schedlowski, M., Meyer, U., Engler, H., Prenatal immune activation causes hippocampal synaptic deficits in the absence of overt microglia anomalies. Brain Behav. Immun. 55 (2016), 25–38, 10.1016/j.bbi.2015.09.015.
79. Goldmann, T., Wieghofer, P., Jordão, M.J.C., Prutek, F., Hagemeyer, N., Frenzel, K., Amann, L., Staszewski, O., Kierdorf, K., Krueger, M., Locatelli, G., Hochgerner, H., Zeiser, R., Epelman, S., Geissmann, F., Priller, J., Rossi, F.M.V., Bechmann, I., Kerschensteiner, M., Linnarsson, S., Jung, S., Prinz, M., Origin, fate and dynamics of macrophages at central nervous system interfaces. Nat. Immunol. 17 (2016), 797–805, 10.1038/ni.3423.
80. Grabert, K., Michoel, T., Karavolos, M.H., Clohisey, S., Baillie, J.K., Stevens, M.P., Freeman, T.C., Summers, K.M., McColl, B.W., Microglial brain region-dependent diversity and selective regional sensitivities to aging. Nat. Neurosci. 19 (2016), 504–516, 10.1038/nn.4222.
81. Greter, M., Lelios, I., Pelczar, P., Hoeffel, G., Price, J., Leboeuf, M., Kundig, T.M., Frei, K., Ginhoux, F., Merad, M., Becher, B., Stroma-derived interleukin-34 controls the development and maintenance of langerhans cells and the maintenance of microglia. Immunity 37 (2012), 1050–1060.
82. Gude, D.R., Alvarez, S.E., Paugh, S.W., Mitra, P., Yu, J., Griffiths, R., Barbour, S.E., Milstien, S., Spiegel, S., Apoptosis induces expression of sphingosine kinase 1 to release sphingosine-1-phosphate as a come-and-get-me signal. FASEB J. 22 (2008), 2629–2638, 10.1096/fj.08-107169.
83. Hanamsagar, R., Bilbo, S.D., Sex differences in neurodevelopmental and neurodegenerative disorders: focus on microglial function and neuroinflammation during development. J. Steroid Biochem. Mol. Biol., 2016, 10.1016/j.jsbmb.2015.09.039.
84. Hanisch, U.K., Kettenmann, H., Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat. Neurosci. 10 (2007), 1387–1394.
85. Hao, C., Richardson, A., Fedoroff, S., Macrophage-like cells originate from neuroepithelium in culture: characterization and properties of the macrophage-like cells. Int. J. Dev. Neurosci. 9 (1991), 1–14.
86. Hart, A.D., Wyttenbach, A., Hugh Perry, V., Teeling, J.L., Age related changes in microglial phenotype vary between CNS regions: grey versus white matter differences. Brain Behav. Immun. 26 (2012), 754–765, 10.1016/j.bbi.2011.11.006.
87. Haynes, S.E., Hollopeter, G., Yang, G., Kurpius, D., Dailey, M.E., Gan, W.B., Julius, D., The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nat. Neurosci. 9 (2006), 1512–1519.
88. Heppner, F.L., Ransohoff, R.M., Becher, B., Immune attack: the role of inflammation in Alzheimer disease. Nat. Rev. Neurosci. 16 (2015), 358–372.
89. Herbomel, P., Thisse, B., Thisse, C., Zebrafish early macrophages colonize cephalic mesenchyme and developing brain retina, and epidermis through a M-CSF receptor-dependent invasive process. Dev. Biol. 238 (2001), 274–288.
90. Hirsch, E., Irikura, V.M., Paul, S.M., Hirsh, D., Functions of interleukin 1 receptor antagonist in gene knockout and overproducing mice. Proc. Natl. Acad. Sci. U. S. A. 93 (1996), 11008–11013.
91. Hoeffel, G., Ginhoux, F., Ontogeny of tissue-resident macrophages. Front. Immunol, 6, 2015, 486, 10.3389/fimmu.2015.00486.
92. Hoeppner, D.J., Hengartner, M.O., Schnabel, R., Engulfment genes cooperate with ced-3 to promote cell death in Caenorhabditis elegans. Nature 412 (2001), 202–206, 10.1038/35084103.
93. Horiuchi, M., Smith, L., Maezawa, I., Jin, L.-W., CX3CR1 ablation ameliorates motor and respiratory dysfunctions and improves survival of a Rett syndrome mouse model. Brain. Behav. Immun. 60 (2016), 106–116 Available at: http://linkinghub.elsevier.com/retrieve/pii/S0889159116300356.
94. Hoshiko, M., Arnoux, I., Avignone, E., Yamamoto, N., Audinat, E., Deficiency of the microglial receptor CX3CR1 impairs postnatal functional development of thalamocortical synapses in the barrel cortex. J. Neurosci. 32 (2012), 15106–15111, 10.1523/JNEUROSCI.1167-12.2012.
95. Hua, J.Y., Smith, S.J., Neural activity and the dynamics of central nervous system development. Nat. Neurosci. 7 (2004), 327–332.
96. Hume, D.A., Perry, V.H., Gordon, S., Immunohistochemical localization of a macrophage-specific antigen in developing mouse retina: phagocytosis of dying neurons and differentiation of microglial cells to form a regular array in the plexiform layers. J. Cell Biol. 97 (1983), 253–257.
97. Imamoto, K., Leblond, C.P., Radioautographic investigation of gliogenesis in the corpus callosum of young rats. II. Origin of microglial cells. J. Comp. Neurol. 180 (1978), 139–163, 10.1002/cne.901800109.
98. Juckel, G., Manitz, M.P., Brüne, M., Friebe, A., Heneka, M.T., Wolf, R.J., Microglial activation in a neuroinflammational animal model of schizophrenia — a pilot study. Schizophr. Res. 131 (2011), 96–100, 10.1016/j.schres.2011.06.018.
99. Kaur, C., Ling, E.A., Wong, W.C., Origin and fate of neural macrophages in a stab wound of the brain of the young rat. J. Anat. 154 (1987), 215–227.
100. Kawasaki, Y., Zhang, L., Cheng, J.-K., Ji, R.-R., Cytokine mechanisms of central sensitization: distinct and overlapping role of interleukin-1beta, interleukin-6, and tumor necrosis factor-alpha in regulating synaptic and neuronal activity in the superficial spinal cord. J. Neurosci. 28 (2008), 5189–5194, 10.1523/JNEUROSCI.3338-07.2008.
101. Kettenmann, H., Hanisch, U.K., Noda, M., Verkhratsky, A., Physiology of microglia. Physiol. Rev. 91 (2011), 461–553.
102. Kettenmann, H., Kirchhoff, F., Verkhratsky, A., Microglia: new roles for the synaptic stripper. Neuron 77 (2013), 10–18.
103. Kierdorf, K., Prinz, M., Factors regulating microglia activation. Front. Cell Neurosci., 7, 2013, 44.
104. Kierdorf, K., Erny, D., Goldmann, T., Sander, V., Schulz, C., Perdiguero, E.G., Wieghofer, P., Heinrich, A., Riemke, P., Holscher, C., Muller, D.N., Luckow, B., Brocker, T., Debowski, K., Fritz, G., Opdenakker, G., Diefenbach, A., Biber, K., Heikenwalder, M., Geissmann, F., Rosenbauer, F., Prinz, M., Microglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways. Nat. Neurosci. 16 (2013), 273–280.
105. Knuesel, I., Chicha, L., Britschgi, M., Schobel, S.A., Bodmer, M., Hellings, J.A., Toovey, S., Prinssen, E.P., Maternal immune activation and abnormal brain development across CNS disorders. Nat. Rev. Neurol. 10 (2014), 643–660, 10.1038/nrneurol.2014.187.
106. Koizumi, S., Shigemoto-Mogami, Y., Nasu-Tada, K., Shinozaki, Y., Ohsawa, K., Tsuda, M., Joshi, B.V., Jacobson, K.A., Kohsaka, S., Inoue, K., UDP acting at P2Y6 receptors is a mediator of microglial phagocytosis. Nature 446 (2007), 1091–1095, 10.1038/nature05704.
107. Kolodziejczak, M., Béchade, C., Gervasi, N., Irinopoulou, T., Banas, S.M., Cordier, C., Rebsam, A., Roumier, A., Maroteaux, L., Serotonin modulates developmental microglia via 5-HT2B receptors: potential implication during synaptic refinement of retinogeniculate projections. ACS Chem. Neurosci. 6 (2015), 1219–1230, 10.1021/cn5003489.
108. Krstic, D., Madhusudan, A., Doehner, J., Vogel, P., Notter, T., Imhof, C., Manalastas, A., Hilfiker, M., Pfister, S., Schwerdel, C., Riether, C., Meyer, U., Knuesel, I., Systemic immune challenges trigger and drive Alzheimer-like neuropathology in mice. J. Neuroinflamm., 9, 2012, 151, 10.1186/1742-2094-9-151.
109. Lai, A.Y., Todd, K.G., Microglia in cerebral ischemia: molecular actions and interactions. Can. J. Physiol. Pharmacol. 84 (2006), 49–59, 10.1139/Y05-143.
110. Lauber, K., Bohn, E., Kr??ber, S.M., Xiao, Y.J., Blumenthal, S.G., Lindemann, R.K., Marini, P., Wiedig, C., Zobywalski, A., Baksh, S., Xu, Y., Autenrieth, I.B., Schulze-Osthoff, K., Belka, C., Stuhler, G., Wesselborg, S., Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell 113 (2003), 717–730, 10.1016/S0092-8674(03)00422-7.
111. Lee, H., Brott, B.K., Kirkby, L.A., Adelson, J.D., Cheng, S., Feller, M.B., Datwani, A., Shatz, C.J., Synapse elimination and learning rules co-regulated by MHC class I H2-Db. Nature 509 (2014), 195–200, 10.1038/nature13154.
112. Lelli, A., Gervais, A., Colin, C., Cheret, C., Ruiz de, A.C., Carmeliet, P., Krause, K.H., Boillee, S., Mallat, M., Chéret, C., de Almodovar, C.R., Carmeliet, P., Krause, K.H., Boillée, S., Mallat, M., The NADPH oxidase Nox2 regulates VEGFR1/CSF-1R-mediated microglial chemotaxis and promotes early postnatal infiltration of phagocytes in the subventricular zone of the mouse cerebral cortex. Glia 61 (2013), 1542–1555, 10.1002/glia.22540.
113. 2 regulates AMPA receptor phosphorylation and promotes membrane insertion in preoptic area neurons and glia during sexual differentiation. PLoS One, 6, 2011, e18500, 10.1371/journal.pone.0018500.
114. Lenz, K.M., Nugent, B.M., Haliyur, R., McCarthy, M.M., Microglia are essential to masculinization of brain and behavior. J. Neurosci. 33 (2013), 2761–2772.
115. Lewitus, G.M., Konefal, S.C., Greenhalgh, A.D., Pribiag, H., Augereau, K., Stellwagen, D., Microglial TNF-a suppresses cocaine-Induced plasticity and behavioral sensitization. Neuron 90 (2016), 483–491, 10.1016/j.neuron.2016.03.030.
116. Li, Y., Du, X.F., Liu, C.S., Wen, Z.L., Du, J.L., Reciprocal regulation between resting microglial dynamics and neuronal activity in vivo. Dev. Cell 23 (2012), 1189–1202.
117. Liang, K.J., Lee, J.E., Wang, Y.D., Ma, W., Fontainhas, A.M., Fariss, R.N., Wong, W.T., Regulation of dynamic behavior of retinal microglia by CX3CR1 signaling. Invest Ophthalmol. Vis. Sci. 50 (2009), 4444–4451.
118. Lim, S.H., Park, E., You, B., Jung, Y., Park, A.R., Park, S.G., Lee, J.R., Neuronal synapse formation induced by microglia and interleukin 10. PLoS One, 8, 2013, 10.1371/journal.pone.0081218.
119. Ling, E.A., Monocytic origin of ramified microglia in the corpus callosum in postnatal rat. Neuropathol. Appl. Neurobiol. 20 (1994), 182–183.
120. Maggi, L., Scianni, M., Branchi, I., D'Andrea, I., Lauro, C., Limatola, C., CX(3)CR1 deficiency alters hippocampal-dependent plasticity phenomena blunting the effects of enriched environment. Front. Cell Neurosci., 5, 2011, 22, 10.3389/fncel.2011.00022.
121. Marin-Teva, J.L., Almendros, A., Calvente, R., Cuadros, M.A., Navascues, J., Tangential migration of ameboid microglia in the developing quail retina: mechanism of migration and migratory behavior. Glia 22 (1998), 31–52.
122. Marin-Teva, J.L., Almendros, A., Calvente, R., Cuadros, M.A., Navascues, J., Proliferation of actively migrating ameboid microglia in the developing quail retina. Anat. Embryol. (Berl.) 200 (1999), 289–300.
123. Marin-Teva, J.L., Cuadros, M.A., Calvente, R., Almendros, A., Navascues, J., Naturally occurring cell death and migration of microglial precursors in the quail retina during normal development. J. Comp. Neurol. 412 (1999), 255–275.
124. Marin-Teva, J.L., Dusart, I., Colin, C., Gervais, A., van, R.N., Mallat, M., Microglia promote the death of developing Purkinje cells. Neuron 41 (2004), 535–547.
125. Martinez, F.O., Gordon, S., The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime. Rep., 6, 2014, 13.
126. Matcovitch-Natan, O., Winter, D.R., Giladi, A., Vargas Aguilar, S., Spinrad, A., Sarrazin, S., Ben-Yehuda, H., David, E., Zelada Gonzalez, F., Perrin, P., Keren-Shaul, H., Gury, M., Lara-Astaiso, D., Thaiss, C.A., Cohen, M., Bahar Halpern, K., Baruch, K., Deczkowska, A., Lorenzo-Vivas, E., Itzkovitz, S., Elinav, E., Sieweke, M.H., Schwartz, M., Amit, I., Microglia development follows a stepwise program to regulate brain homeostasis. Science (80-.), 353, 2016, aad8670, 10.1126/science.aad8670.
127. McCarthy, M.M., Pickett, L.A., VanRyzin, J.W., Kight, K.E., Surprising origins of sex differences in the brain. Horm. Behav. 76 (2015), 3–10, 10.1016/j.yhbeh.2015.04.013.
128. McCullough, L.D., Mirza, M.A., Xu, Y., Bentivegna, K., Steffens, E.B., Ritzel, R., Liu, F., Stroke sensitivity in the aged: sex chromosome complement vs. gonadal hormones. Aging (Albany, NY) 8 (2016), 1432–1441, 10.18632/aging.100997.
129. Menteyne, A., Levavasseur, F., Audinat, E., Avignone, E., Predominant functional expression of Kv1.3 by activated microglia of the hippocampus after status epilepticus. PLoS One, 4, 2009.
130. Meyer, U., Murray, P.J., Urwyler, a, Yee, B.K., Schedlowski, M., Feldon, J., Adult behavioral and pharmacological dysfunctions following disruption of the fetal brain balance between pro-inflammatory and IL-10-mediated anti-inflammatory signaling. Mol. Psychiatry 13 (2008), 208–221, 10.1038/sj.mp.4002042.
131. Meyer, U., Feldon, J., Fatemi, S.H., In-vivo rodent models for the experimental investigation of prenatal immune activation effects in neurodevelopmental brain disorders. Neurosci. Biobehav. Rev., 2009, 10.1016/j.neubiorev.2009.05.001.
132. Meyer, U., Feldon, J., Yee, B.K., A review of the fetal brain cytokine imbalance hypothesis of schizophrenia. Schizophr. Bull., 2009, 10.1093/schbul/sbn022.
133. Meyer, U., Prenatal Poly(I:C) exposure and other developmental immune activation models in rodent systems. Biol. Psychiatry, 2014, 10.1016/j.biopsych.2013.07.011.
134. Minten, C., Terry, R., Deffrasnes, C., King, N.J.C., Campbell, I.L., IFN regulatory factor 8 is a key constitutive determinant of the morphological and molecular properties of microglia in the CNS. PLoS One, 7, 2012, e49851, 10.1371/journal.pone.0049851.
135. Miyamoto, A., Wake, H., Ishikawa, A.W., Eto, K., Shibata, K., Murakoshi, H., Koizumi, S., Moorhouse, A.J., Yoshimura, Y., Nabekura, J., Microglia contact induces synapse formation in developing somatosensory cortex. Nat. Commun., 7, 2016, 12540, 10.1038/ncomms12540.
136. Monier, A., Evrard, P., Gressens, P., Verney, C., Distribution and differentiation of microglia in the human encephalon during the first two trimesters of gestation. J. Comp. Neurol. 499 (2006), 565–582.
137. Monier, A., dle-Biassette, H., Delezoide, A.L., Evrard, P., Gressens, P., Verney, C., Entry and distribution of microglial cells in human embryonic and fetal cerebral cortex. J. Neuropathol. Exp. Neurol. 66 (2007), 372–382.
138. Morgan, S.C., Taylor, D.L., Pocock, J.M., Microglia release activators of neuronal proliferation mediated by activation of mitogen-activated protein kinase, phosphatidylinositol-3-kinase/Akt and delta-Notch signalling cascades. J. Neurochem. 90 (2004), 89–101, 10.1111/j.1471-4159.2004.02461.x.
139. Morganti, J.M., Nash, K.R., Grimmig, B.A., Ranjit, S., Small, B., Bickford, P.C., Gemma, C., The soluble isoform of CX3CL1 is necessary for neuroprotection in a mouse model of Parkinson's disease. J. Neurosci. 32 (2012), 14592–14601.
140. Moujahid, A., Navascués, J., Marín-Teva, J.L., Cuadros, M.A., Macrophages during avian optic nerve development: relationship to cell death and differentiation into microglia. Anat. Embryol. (Berl). 193 (1996), 131–144.
141. Murray, P.J., Allen, J.E., Biswas, S.K., Fisher, E.A., Gilroy, D.W., Goerdt, S., Gordon, S., Hamilton, J.A., Ivashkiv, L.B., Lawrence, T., Locati, M., Mantovani, A., Martinez, F.O., Mege, J.L., Mosser, D.M., Natoli, G., Saeij, J.P., Schultze, J.L., Shirey, K.A., Sica, A., Suttles, J., Udalova, I., van Ginderachter, J.A., Vogel, S.N., Wynn, T.A., Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 41 (2014), 14–20.
142. Nagata, K., Nakajima, K., Kohsaka, S., Plasminogen promotes the development of rat mesencephalic dopaminergic neurons in vitro. Brain Res. Dev. Brain Res. 75 (1993), 31–37.
143. Nagata, K., Takei, N., Nakajima, K., Saito, H., Kohsaka, S., Microglial conditioned medium promotes survival and development of cultured mesencephalic neurons from embryonic rat brain. J. Neurosci. Res. 34 (1993), 357–363, 10.1002/jnr.490340313.
144. Navascues, J., Calvente, R., Marin-Teva, J.L., Cuadros, M.A., Entry, dispersion and differentiation of microglia in the developing central nervous system. An. Acad. Bras. Cienc. 72 (2000), 91–102.
145. Nayak, D., Roth, T.L., McGavern, D.B., Microglia development and function. Annu. Rev. Immunol. 32 (2014), 367–402.
146. Nikodemova, M., Kimyon, R.S., De, I., Small, A.L., Collier, L.S., Watters, J.J., Microglial numbers attain adult levels after undergoing a rapid decrease in cell number in the third postnatal week. J. Neuroimmunol. 278 (2015), 280–288.
147. Nimmerjahn, A., Kirchhoff, F., Helmchen, F., Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science (80-.) 308 (2005), 1314–1318.
148. Ohsawa, K., Irino, Y., Nakamura, Y., Akazawa, C., Inoue, K., Kohsaka, S., Involvement of P2 × 4 and P2Y12 receptors in ATP-induced microglial chemotaxis. Glia 55 (2007), 604–616.
149. Oppenheim, R.W., Cell death during development of the nervous system. Annu. Rev. Neurosci. 14 (1991), 453–501.
150. Orr, A.G., Orr, A.L., Li, X.J., Gross, R.E., Traynelis, S.F., Adenosine A(2A) receptor mediates microglial process retraction. Nat. Neurosci. 12 (2009), 872–878.
151. Pagani, F., Paolicelli, R.C., Murana, E., Cortese, B., Di Angelantonio, S., Zurolo, E., Guiducci, E., Ferreira, T.A., Garofalo, S., Catalano, M., D'Alessandro, G., Porzia, A., Peruzzi, G., Mainiero, F., Limatola, C., Gross, C.T., Ragozzino, D., Defective microglial development in the hippocampus of Cx3cr1 deficient mice. Front. Cell Neurosci., 9, 2015, 111, 10.3389/fncel.2015.00111.
152. Palis, J., Robertson, S., Kennedy, M., Wall, C., Keller, G., Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse. Development 126 (1999), 5073–5084.
153. Paloneva, J., Kestilä, M., Wu, J., Salminen, A., Böhling, T., Ruotsalainen, V., Hakola, P., Bakker, A.B., Phillips, J.H., Pekkarinen, P., Lanier, L.L., Timonen, T., Peltonen, L., Loss-of-function mutations in TYROBP (DAP12) result in a presenile dementia with bone cysts. Nat. Genet. 25 (2000), 357–361, 10.1038/77153.
154. Paolicelli, R.C., Bolasco, G., Pagani, F., Maggi, L., Scianni, M., Panzanelli, P., Giustetto, M., Ferreira, T.A., Guiducci, E., Dumas, L., Ragozzino, D., Gross, C.T., Synaptic pruning by microglia is necessary for normal brain development. Science (80-.) 333 (2011), 1456–1458.
155. Paolicelli, R.C., Bisht, K., Tremblay, M.E., Fractalkine regulation of microglial physiology and consequences on the brain and behavior. Front. Cell Neurosci., 8, 2014, 129.
156. Parkhurst, C.N., Yang, G., Ninan, I., Savas, J.N., Yates, J.R. III, Lafaille, J.J., Hempstead, B.L., Littman, D.R., Gan, W.B., Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell 155 (2013), 1596–1609.
157. Pascual, O., Ben Achour, S., Rostaing, P., Triller, A., Bessis, A., Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission. Proc. Natl. Acad. Sci. 109 (2012), E197–E205, 10.1073/pnas.1111098109.
158. Perry, V.H., Hume, D.A., Gordon, S., Immunohistochemical localization of macrophages and microglia in the adult and developing mouse brain. Neuroscience 15 (1985), 313–326.
159. Pfeiffer, T., Avignone, E., Nägerl, U.V., Induction of hippocampal long-term potentiation increases the morphological dynamics of microglial processes and prolongs their contacts with dendritic spines. Sci. Rep., 6, 2016, 32422, 10.1038/srep32422.
160. Pollard, J.W., Trophic macrophages in development and disease. Nat. Rev. Immunol. 9 (2009), 259–270.
161. Pont-Lezica, L., Bechade, C., Belarif-Cantaut, Y., Pascual, O., Bessis, A., Physiological roles of microglia during development. J. Neurochem. 119 (2011), 901–908.
162. Pont-Lezica, L., Beumer, W., Colasse, S., Drexhage, H., Versnel, M., Bessis, A., Microglia shape corpus callosum axon tract fasciculation: functional impact of prenatal inflammation. Eur. J. Neurosci. 39 (2014), 1551–1557, 10.1111/ejn.12508.
163. Poon, V.Y., Choi, S., Park, M., Growth factors in synaptic function. Front. Synaptic Neurosci., 2013, 10.3389/fnsyn.2013.00006.
164. Pozner, A., Xu, B., Palumbos, S., Gee, J.M., Tvrdik, P., Capecchi, M.R., Intracellular calcium dynamics in cortical microglia responding to focal laser injury in the PC:G5-tdT reporter mouse. Front. Mol. Neurosci. 8 (2015), 1–10, 10.3389/fnmol.2015.00012.
165. Prinz, M., Priller, J., Microglia and brain macrophages in the molecular age: from origin to neuropsychiatric disease. Nat. Rev. Neurosci. 15 (2014), 300–312.
166. Rachal Pugh, C., Fleshner, M., Watkins, L.R., Maier, S.F., Rudy, J.W., The immune system and memory consolidation: a role for the cytokine IL-1beta. Neurosci. Biobehav. Rev. 25 (2001), 29–41.
167. Rakic, S., Zecevic, N., Programmed cell death in the developing human telencephalon. Eur. J. Neurosci. 12 (2000), 2721–2734.
168. Ransohoff, R.M., Perry, V.H., Microglial physiology: unique stimuli, specialized responses. Annu. Rev. Immunol. 27 (2009), 119–145, 10.1146/annurev.immunol.021908.132528.
169. Ransohoff, R.M., A polarizing question: do M1 and M2 microglia exist?. Nat. Neurosci. 19 (2016), 987–991, 10.1038/nn.4338.
170. Reddien, P.W., Cameron, S., Horvitz, H.R., Phagocytosis promotes programmed cell death in C. elegans. Nature 412 (2001), 198–202, 10.1038/35084096.
171. Rezaie, P., Trillo-Pazos, G., Greenwood, J., Everall, I.P., Male, D.K., Motility and ramification of human fetal microglia in culture: an investigation using time-lapse video microscopy and image analysis. Exp. Cell Res. 274 (2002), 68–82.
172. Ribeiro Xavier, A.L., Kress, B.T., Goldman, S.A., Lacerda de Menezes, J.R., Nedergaard, M., A distinct population of microglia supports adult neurogenesis in the subventricular zone. J. Neurosci. 35 (2015), 11848–11861, 10.1523/JNEUROSCI.1217-15.2015.
173. Rigato, C., Buckinx, R., Le-Corronc, H., Rigo, J.M., Legendre, P., Pattern of invasion of the embryonic mouse spinal cord by microglial cells at the time of the onset of functional neuronal networks. Glia 59 (2011), 675–695.
174. Rigato, C., Swinnen, N., Buckinx, R., Couillin, I., Mangin, J.M., Rigo, J.M., Legendre, P., Le, C.H., Microglia proliferation is controlled by P2 × 7 receptors in a pannexin-1-Independent manner during early embryonic spinal cord invasion. J. Neurosci. 32 (2012), 11559–11573.
175. Rodrigues, R.J., Tome, A.R., Cunha, R.A., ATP as a multi-target danger signal in the brain. Front. Neurosci., 9, 2015, 148.
176. Rogers, J.T., Morganti, J.M., Bachstetter, A.D., Hudson, C.E., Peters, M.M., Grimmig, B.A., Weeber, E.J., Bickford, P.C., Gemma, C., CX3CR1 deficiency leads to impairment of hippocampal cognitive function and synaptic plasticity. J. Neurosci. 31 (2011), 16241–16250.
177. Roumier, A., Bechade, C., Poncer, J.C., Smalla, K.H., Tomasello, E., Vivier, E., Gundelfinger, E.D., Triller, A., Bessis, A., Impaired synaptic function in the microglial KARAP/DAP12-deficient mouse. J. Neurosci. 24 (2004), 11421–11428.
178. Roumier, A., Pascual, O., Béchade, C., Wakselman, S., Poncer, J.C., Réal, E., Triller, A., Bessis, A., Bechade, C., Wakselman, S., Poncer, J.C., Real, E., Triller, A., Bessis, A., Prenatal activation of microglia induces delayed impairment of glutamatergic synaptic function. PLoS One, 3, 2008, e2595, 10.1371/journal.pone.0002595.
179. Rousset, C.I., Chalon, S., Cantagrel, S., Bodard, S., Andres, C., Gressens, P., Saliba, E., Maternal exposure to LPS induces hypomyelination in the internal capsule and programmed cell death in the deep gray matter in newborn rats. Pediatr. Res. 59 (2006), 428–433, 10.1203/01.pdr.0000199905.08848.55.
180. Rymo, S.F., Gerhardt, H., Wolfhagen, S.F., Lang, R., Uv, A., Betsholtz, C., A two-way communication between microglial cells and angiogenic sprouts regulates angiogenesis in aortic ring cultures. PLoS One, 6, 2011, e15846.
181. Salter, M.W., Beggs, S., Sublime microglia: expanding roles for the guardians of the CNS. Cell 158 (2014), 15–24.
182. Samokhvalov, I.M., Samokhvalova, N.I., Nishikawa, S., Cell tracing shows the contribution of the yolk sac to adult haematopoiesis. Nature 446 (2007), 1056–1061.
183. Schafer, D.P., Lehrman, E.K., Kautzman, A.G., Koyama, R., Mardinly, A.R., Yamasaki, R., Ransohoff, R.M., Greenberg, M.E., Barres, B.A., Stevens, B., Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74 (2012), 691–705.
184. Schafer, D.P., Lehrman, E.K., Stevens, B., The quad-partite synapse: microglia-synapse interactions in the developing and mature CNS. Glia 61 (2013), 24–36.
185. Schafer, D.P., Heller, C.T., Gunner, G., Heller, M., Gordon, C., Hammond, T., Wolf, Y., Jung, S., Stevens, B., Microglia contribute to circuit defects in Mecp2 null mice independent of microglia-specific loss of Mecp2 expression. Elife, 5, 2016, 10.7554/elife.15224.
186. Schilling, T., Nitsch, R., Heinemann, U., Haas, D., Eder, C., Astrocyte-released cytokines induce ramification and outward K+ channel expression in microglia via distinct signalling pathways. Eur. J. Neurosci. 14 (2001), 463–473.
187. Schlegelmilch, T., Henke, K., Peri, F., Microglia in the developing brain: from immunity to behaviour. Curr. Opin. Neurobiol. 21 (2011), 5–10.
188. Schmidtmayer, J., Jacobsen, C., Miksch, G., Sievers, J., Blood monocytes and spleen macrophages differentiate into microglia-like cells on monolayers of astrocytes: membrane currents. Glia 12 (1994), 259–267, 10.1002/glia.440120403.
189. Schnell, L., Fearn, S., Klassen, H., Schwab, M.E., Perry, V.H., Acute inflammatory responses to mechanical lesions in the CNS: differences between brain and spinal cord. Eur. J. Neurosci. 11 (1999), 3648–3658, 10.1046/j.1460-9568.1999.00792.x.
190. Schulz, C., Gomez, P.E., Chorro, L., Szabo-Rogers, H., Cagnard, N., Kierdorf, K., Prinz, M., Wu, B., Jacobsen, S.E., Pollard, J.W., Frampton, J., Liu, K.J., Geissmann, F., A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science (80-.) 336 (2012), 86–90.
191. Schwarz, J.M., Bilbo, S.D., Sex, glia, and development: interactions in health and disease. Horm. Behav. 62 (2012), 243–253, 10.1016/j.yhbeh.2012.02.018.
192. Scianni, M., Antonilli, L., Chece, G., Cristalli, G., Di Castro, M.A., Limatola, C., Maggi, L., Fractalkine (CX3CL1) enhances hippocampal N-methyl-D-aspartate receptor (NMDAR) function via D-serine and adenosine receptor type A2 (A2AR) activity. J. Neuroinflammation., 10, 2013, 108.
193. Sedel, F., Bechade, C., Vyas, S., Triller, A., Macrophage-derived tumor necrosis factor alpha, an early developmental signal for motoneuron death. J. Neurosci. 24 (2004), 2236–2246.
194. Shatz, C.J., Competitive interactions between retinal ganglion cells during prenatal development. J. Neurobiol. 21 (1990), 197–211, 10.1002/neu.480210113.
195. Shatz, C.J., MHC class I: an unexpected role in neuronal plasticity. Neuron 64 (2009), 40–45, 10.1016/j.neuron.2009.09.044.
196. Shemer, A., Erny, D., Jung, S., Prinz, M., Microglia plasticity during health and disease: an immunological perspective. Trends Immunol. 36 (2015), 614–624.
197. Sheridan, G.K., Murphy, K.J., Neuron-glia crosstalk in health and disease: fractalkine and CX3CR1 take centre stage. Open Biol., 3, 2013, 130181.
198. Shigemoto-Mogami, Y., Hoshikawa, K., Goldman, J.E., Sekino, Y., Sato, K., Microglia enhance neurogenesis and oligodendrogenesis in the early postnatal subventricular zone. J. Neurosci. 34 (2014), 2231–2243.
199. Shklover, J., Levy-Adam, F., Kurant, E., Apoptotic cell clearance in development. Current Topics in Developmental Biology, 2015, 10.1016/bs.ctdb.2015.07.024 pp. 297–334.
200. Shklyar, B., Sellman, Y., Shklover, J., Mishnaevski, K., Levy-Adam, F., Kurant, E., Developmental regulation of glial cell phagocytic function during Drosophila embryogenesis. Dev. Biol. 393 (2014), 255–269, 10.1016/j.ydbio.2014.07.005.
201. Sierra, A., Encinas, J.M., Deudero, J.J., Chancey, J.H., Enikolopov, G., Overstreet-Wadiche, L.S., Tsirka, S.E., Maletic-Savatic, M., Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 7 (2010), 483–495.
202. Sierra, A., Abiega, O., Shahraz, A., Neumann, H., Janus-faced microglia: beneficial and detrimental consequences of microglial phagocytosis. Front. Cell Neurosci., 7, 2013, 6, 10.3389/fncel.2013.00006.
203. Sierra, A., Beccari, S., Diaz-Aparicio, I., Encinas, J.M., Comeau, S., Tremblay, M. Ève, Surveillance, phagocytosis, and inflammation: how never-resting microglia influence adult hippocampal neurogenesis. Neural Plast., 2014, 610343, 10.1155/2014/610343.
204. Sierra, A., de Castro, F., del R??o-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 64 (2016), 1801–1840, 10.1002/glia.23046.
205. Sievers, J., Parwaresch, R., Wottge, H.U., Blood monocytes and spleen macrophages differentiate into microglia-like cells on monolayers of astrocytes: morphology. Glia 12 (1994), 245–258.
206. Sipe, G.O., Lowery, R.L., Tremblay, M.E., Kelly, E.A., Lamantia, C.E., Majewska, A.K., Microglial P2Y12 is necessary for synaptic plasticity in mouse visual cortex. Nat. Commun., 7, 2016, 10905.
207. Smith, S.E.P., Li, J., Garbett, K., Mirnics, K., Patterson, P.H., Maternal immune activation alters fetal brain development through interleukin-6. J. Neurosci. 27 (2007), 10695–11702, 10.1523/JNEUROSCI.2178-07.2007.
208. Smolders, S., Smolders, S.M.T., Swinnen, N., Gärtner, A., Rigo, J.-M., Legendre, P., Brône, B., Maternal immune activation evoked by polyinosinic:polycytidylic acid does not evoke microglial cell activation in the embryo. Front. Cell Neurosci., 9, 2015, 301, 10.3389/fncel.2015.00301.
209. Sorge, R.E., Mapplebeck, J.C.S., Rosen, S., Beggs, S., Taves, S., Alexander, J.K., Martin, L.J., Austin, J.-S., Sotocinal, S.G., Chen, D., Yang, M., Shi, X.Q., Huang, H., Pillon, N.J., Bilan, P.J., Tu, Y., Klip, A., Ji, R.-R., Zhang, J., Salter, M.W., Mogil, J.S., Different immune cells mediate mechanical pain hypersensitivity in male and female mice. Nat. Neurosci. 18 (2015), 1–5, 10.1038/nn.4053.
210. Spassky, N., de, C.F., Le, B.B., Heydon, K., Queraud-LeSaux, F., Bloch-Gallego, E., Chedotal, A., Zalc, B., Thomas, J.L., Directional guidance of oligodendroglial migration by class 3 semaphorins and netrin-1. J. Neurosci. 22 (2002), 5992–6004.
211. Squarzoni, P., Oller, G., Hoeffel, G., Pont-Lezica, L., Rostaing, P., Low, D., Bessis, A., Ginhoux, F., Garel, S., Microglia modulate wiring of the embryonic forebrain. Cell Rep. 8 (2014), 1271–1279, 10.1016/j.celrep.2014.07.042.
212. Stellwagen, D., Beattie, E.C., Seo, J.Y., Malenka, R.C., Differential regulation of AMPA receptor and GABA receptor trafficking by tumor necrosis factor-alpha. J. Neurosci. 25 (2005), 3219–3228.
213. Stephan, A.H., Barres, B.A., Stevens, B., The complement system: an unexpected role in synaptic pruning during development and disease. Annu. Rev. Neurosci. 35 (2012), 369–389, 10.1146/annurev-neuro-061010-113810.
214. Stevens, B., Allen, N.J., Vazquez, L.E., Howell, G.R., Christopherson, K.S., Nouri, N., Micheva, K.D., Mehalow, A.K., Huberman, A.D., Stafford, B., Sher, A., Litke, A.M., Lambris, J.D., Smith, S.J., John, S.W., Barres, B.A., The classical complement cascade mediates CNS synapse elimination. Cell 131 (2007), 1164–1178.
215. Swinnen, N., Smolders, S., Avila, A., Notelaers, K., Paesen, R., Ameloot, M., Brone, B., Legendre, P., Rigo, J.M., Complex invasion pattern of the cerebral cortex bymicroglial cells during development of the mouse embryo. Glia 61 (2013), 150–163.
216. Takahashi, K., Naito, M., Takeya, M., Development and heterogeneity of macrophages and their related cells through their differentiation pathways. Pathol. Int. 46 (1996), 473–485.
217. Tan, H., Cao, J., Zhang, J., Zuo, Z., Critical role of inflammatory cytokines in impairing biochemical processes for learning and memory after surgery in rats. J. Neuroinflamm., 11, 2014, 93, 10.1186/1742-2094-11-93.
218. Tremblay, M.E., Lowery, R.L., Majewska, A.K., Microglial interactions with synapses are modulated by visual experience. PLoS Biol., 8, 2010, e1000527.
219. Tremblay, M.E., Stevens, B., Sierra, A., Wake, H., Bessis, A., Nimmerjahn, A., The role of microglia in the healthy brain. J. Neurosci. 31 (2011), 16064–16069.
220. Truman, L.A., Ford, C.A., Pasikowska, M., Pound, J.D., Wilkinson, S.J., Dumitriu, I.E., Melville, L., Melrose, L.A., Ogden, C.A., Nibbs, R., Graham, G., Combadiere, C., Gregory, C.D., CX3CL1/fractalkine is released from apoptotic lymphocytes to stimulate macrophage chemotaxis. Blood 112 (2008), 5026–5036, 10.1182/blood-2008-06-162404.
221. Ueno, M., Fujita, Y., Tanaka, T., Nakamura, Y., Kikuta, J., Ishii, M., Yamashita, T., Layer V cortical neurons require microglial support for survival during postnatal development. Nat. Neurosci. 16 (2013), 543–551, 10.1038/nn.3358.
222. Ullian, E.M., Christopherson, K.S., Barres, B.A., Role for glia in synaptogenesis. Glia 47 (2004), 209–216.
223. Upender, M.B., Naegele, J.R., Activation of microglia during developmentally regulated cell death in the cerebral cortex. Dev. Neurosci. 21 (1999), 491–505.
224. Upton, A.L., Salichon, N., Lebrand, C., Ravary, A., Blakely, R., Seif, I., Gaspar, P., Excess of serotonin (5-HT) alters the segregation of ispilateral and contralateral retinal projections in monoamine oxidase A knock-out mice: possible role of 5-HT uptake in retinal ganglion cells during development. J. Neurosci. 19 (1999), 7007–7024.
225. Verkhratsky, A., Steardo, L., Parpura, V., Montana, V., Translational potential of astrocytes in brain disorders. Prog. Neurobiol., 2015, 10.1016/j.pneurobio.2015.09.003.
226. Verney, C., Monier, A., Fallet-Bianco, C., Gressens, P., Early microglial colonization of the human forebrain and possible involvement in periventricular white-matter injury of preterm infants. J. Anat. 217 (2010), 436–448, 10.1111/j.1469-7580.2010.01245.x.
227. Vilhardt, F., Haslund-Vinding, J., Jaquet, V., Mcbean, G., Microglia antioxidant systems and redox signalling. Br. J. Pharmacol, 2016, 10.1111/bph.13426.
228. Voineagu, I., Wang, X., Johnston, P., Lowe, J.K., Tian, Y., Horvath, S., Mill, J., Cantor, R.M., Blencowe, B.J., Geschwind, D.H., Transcriptomic analysis of autistic brain reveals convergent molecular pathology. Nature 474 (2011), 380–384, 10.1038/nature10110.
229. Wake, H., Moorhouse, A.J., Jinno, S., Kohsaka, S., Nabekura, J., Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J. Neurosci. 29 (2009), 3974–3980.
230. Wakselman, S., Bechade, C., Roumier, A., Bernard, D., Triller, A., Bessis, A., Developmental neuronal death in hippocampus requires the microglial CD11b integrin and DAP12 immunoreceptor. J. Neurosci. 28 (2008), 8138–8143.
231. Wang, Y., Szretter, K.J., Vermi, W., Gilfillan, S., Rossini, C., Cella, M., Barrow, A.D., Diamond, M.S., Colonna, M., IL-34 is a tissue-restricted ligand of CSF1R required for the development of Langerhans cells and microglia. Nat. Immunol. 13 (2012), 753–760.
232. Wang, J., Wegener, J.E., Huang, T., Sripathy, S., De Jesus-Cortex, H., Xu, P., Tran, S., Al, E., Wild-type microglia do not reverse pathology in mouse models of Rett syndrome. Nature 521 (2015), E1–E4, 10.1038/nature10907.
233. Wollmer, M.A., Lucius, R., Wilms, H., Held-Feindt, J., Sievers, J., Mentlein, R., ATP and adenosine induce ramification of microglia in vitro. J. Neuroimmunol. 115 (2001), 19–27.
234. Wright, C.L., McCarthy, M.M., Prostaglandin E2-induced masculinization of brain and behavior requires protein kinase A AMPA/kainate, and metabotropic glutamate receptor signaling. J. Neurosci. 29 (2009), 13274–13282, 10.1523/JNEUROSCI.3603-09.2009.
235. Wright, C.L., Burks, S.R., McCarthy, M.M., Identification of prostaglandin E2 receptors mediating perinatal masculinization of adult sex behavior and neuroanatomical correlates. Dev. Neurobiol. 68 (2008), 1406–1419, 10.1002/dneu.20665.
236. Wu, L.J., Stevens, B., Duan, S., MacVicar, B.A., Microglia in neuronal circuits. Neural Plast., 2013, 2013, 586426.
237. Xu, D.-X., Chen, Y.-H., Wang, H., Zhao, L., Wang, J.-P., Wei, W., Tumor necrosis factor alpha partially contributes to lipopolysaccharide-induced intra-uterine fetal growth restriction and skeletal development retardation in mice. Toxicol. Lett. 163 (2006), 20–29, 10.1016/j.toxlet.2005.09.009.
238. Xu, J., Wang, T., Wu, Y., Jin, W., Wen, Z., Microglia colonization of developing zebrafish midbrain is promoted by apoptotic neuron and lysophosphatidylcholine. Dev. Cell 38 (2016), 214–222, 10.1016/j.devcel.2016.06.018.
239. Yamada, J., Hayashi, Y., Jinno, S., Wu, Z., Inoue, K., Kohsaka, S., Nakanishi, H., Reduced synaptic activity precedes synaptic stripping in vagal motoneurons after axotomy. Glia 56 (2008), 1448–1462.
240. Yeo, W., Gautier, J., Early neural cell death: dying to become neurons. Dev. Biol. 274 (2004), 233–244.
241. Zhan, Y., Paolicelli, R.C., Sforazzini, F., Weinhard, L., Bolasco, G., Pagani, F., Vyssotski, A.L., Bifone, A., Gozzi, A., Ragozzino, D., Gross, C.T., Deficient neuron-microglia signaling results in impaired functional brain connectivity and social behavior. Nat. Neurosci. 17 (2014), 400–406.
242. van Berckel, B.N., Bossong, M.G., Boellaard, R., Kloet, R., Schuitemaker, A., Caspers, E., Luurtsema, G., Windhorst, A.D., Cahn, W., Lammertsma, A.A., Kahn, R.S., Microglia activation in recent-Onset schizophrenia: a quantitative (R)-[11C]PK11195 positron emission tomography study. Biol. Psychiatry 64 (2008), 820–822, 10.1016/j.biopsych.2008.04.025.
243. van Kleef, E.S., Gaspar, P., Bonnin, A., Insights into the complex influence of 5-HT signaling on thalamocortical axonal system development. Eur. J. Neurosci. 35 (2012), 1563–1572.
244. van Tilborg, E., Heijnen, C.J., Benders, M.J., van Bel, F., Fleiss, B., Gressens, P., Nijboer, C.H., Impaired oligodendrocyte maturation in preterm infants: potential therapeutic targets. Prog. Neurobiol. 136 (2016), 28–49, 10.1016/j.pneurobio.2015.11.002.