The "quad-partite" synapse: Microglia-synapse interactions in the developing and mature CNS

GLIA

Volumn 61, Issue 1, 2013, Pages 24-36

  Schafer, Dorothy P ^a   Lehrman, Emily K ^a   Stevens, Beth ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Cortex; Glia; Hippocampus; Neurotransmission; Plasticity; Pruning; Retinogeniculate

Indexed keywords

ARTICLE; CENTRAL NERVOUS SYSTEM DISEASE; MICROGLIA; NERVE CELL; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEUROTRANSMITTER RELEASE; PRIORITY JOURNAL; SYNAPSE;

ANIMALS; CENTRAL NERVOUS SYSTEM; HUMANS; MICROGLIA; NEURONAL PLASTICITY; SYNAPSES;

EID: 84869157553     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22389     Document Type: Article

References (144)

1. Alexander JJ, Anderson AJ, Barnum SR, Stevens B, Tenner AJ. 2008. The complement cascade: Yin-Yang in neuroinflammation-neuro-protection and -degeneration. J Neurochem 107: 1169-1187.
2. Awasaki T, Tatsumi R, Takahashi K, Arai K, Nakanishi Y, Ueda R, Ito K. 2006. Essential role of the apoptotic cell engulfment genes draper and ced-6 in programmed axon pruning during Drosophila metamorphosis. Neuron 50: 855-867.
3. Awasaki T, Ito, K. 2004. Engulfing action of glial cells is required for programmed axon pruning during Drosophila metamorphosis. Curr Biol 14: 668-677.
4. Belmonte MK, Allen G, Beckel-Mitchener A, Boulanger LM, Carper RA, Webb SJ. 2004. Autism and abnormal development of brain connectivity. J Neurosci 24: 9228-9231.
5. Ben Achour S, Pascual O. 2010. Glia: The many ways to modulate synaptic plasticity. Neurochem Int 57: 440-445.
6. Bence M, Levelt CN. 2005. Structural plasticity in the developing visual system. Prog Brain Res 147: 125-139.
7. Berbel P, Innocenti GM. 1988. The development of the corpus callosum in cats: A light- and electron-microscopic study. J Comp Neurol 276: 132-156.
8. Bessis A, Bechade C, Bernard D, Roumier A. 2007. Microglial control of neuronal death and synaptic properties. Glia 55: 233-238.
9. Biber K, Neumann H, Inoue K, Boddeke HW. 2007. Neuronal 'On' and 'Off' signals control microglia. Trends Neurosci 30: 596-602.
10. Bilbo SD. 2010. Early-life infection is a vulnerability factor for aging-related glial alterations and cognitive decline. Neurobiol Learn Mem 94: 57-64.
11. Bilbo SD, Rudy JW, Watkins LR, Maier SF. 2006. A behavioural characterization of neonatal infection-facilitated memory impairment in adult rats. Behav Brain Res 169: 39-47.
12. Bishop DL, Misgeld T, Walsh MK, Gan WB, Lichtman JW. 2004. Axon branch removal at developing synapses by axosome shedding. Neuron 44: 651-661.
13. Bitanihirwe BK, Peleg-Raibstein D, Mouttet F, Feldon J, Meyer U. 2010. Late prenatal immune activation in mice leads to behavioral and neurochemical abnormalities relevant to the negative symptoms of schizophrenia. Neuropsychopharmacology 35: 2462-2478.
14. Bjartmar L, Huberman AD, Ullian EM, Renteria RC, Liu X, Xu W, Prezioso J, Susman MW, Stellwagen D, Stokes CC, Cho R, Worley P, Malenka RC, Ball S, Peachey NS, Copenhagen D, Chapman B, Nakamoto M, Barres BA, Perin MS. et al. 2006. Neuronal pentraxins mediate synaptic refinement in the developing visual system. J Neurosci 26: 6269-6281.
15. Blinzinger K, Kreutzberg GW. 1968. Displacement of synaptic terminals from regenerating motoneurons by microglial cells. Z Zellforsch Mikrosk Anat 85: 145-157.
16. Boulanger LM. 2009. Immune proteins in brain development and synaptic plasticity. Neuron 64: 93-109.
17. Cardona AE, Pioro EP, Sasse ME, Kostenko V, Cardona SM, Dijkstra IM, Huang D, Kidd G, Dombrowski S, Dutta R, Lee JC, Cook DN, Jung S, Lira SA, Littman DR, Ransohoff RM. et al. 2006. Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci 9: 917-924.
18. Chen C, Regehr WG. 2000. Developmental remodeling of the retinogeniculate synapse. Neuron 28: 955-966.
19. Chen RZ, Akbarian S, Tudor M, Jaenish R. 2001. Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat Genet 27: 327-331.
20. Chen SK, Tvrdik P, Peden E, Cho S, Wu S, Spangrude G, Capecchi MR. 2010. Hematopoietic origin of pathological grooming in Hoxb8 mutant mice. Cell 141: 775-785.
21. Coleman P, Federoff H, Kurlan R. 2004. A focus on the synapse for neuroprotection in Alzheimer disease and other dementias. Neurology 63: 1155-1162.
22. Cook PM, Prusky G, Ramoa AS. 1999. The role of spontaneous retinal activity before eye opening in the maturation of form and function in the retinogeniculate pathway of the ferret. Visual Neurosci 16: 491-501.
23. Corriveau RA, Huh GS, Shatz CJ. 1998. Regulation of class I MHC gene expression in the developing and mature CNS by neural activity. Neuron 21: 505-520.
24. Coull JA, Beggs S, Boudreau D, Boivin D, Tsuda M, Inoue K, Gravel C, Salter MW, De Koninck Y. 2005. BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 438: 1017-1021.
25. Cullheim S, Thams S. 2007. The microglial networks of the brain and their role in neuronal network plasticity after lesion. Brain Res Rev 55: 89-96.
26. Datwani A, McConnell MJ, Kanold PO, Micheva KD, Busse B, Shamloo M, Smith SJ, Shatz CJ. 2009. Classical MHCI molecules regulate retinogeniculate refinement and limit ocular dominance plasticity. Neuron 64: 463-470.
27. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, Littman DR, Dustin ML, Gan WB. 2005. ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8: 752-758.
28. del Rio-Hortega P. 1932. Microglia. In: Penfield W, editor. Cytology and cellular pathology of the nervous system. New York: Hoeber.
29. Del Rio T, Feller MB. 2006. Early retinal activity and visual circuit development. Neuron 52: 221-222.
30. Derecki NC, Cronk JC, Lu Z, Xu E, Abbott SB, Guyenet PG, Kipnis J. 2012. Wild-type microglia arrest pathology in a mouse model of Rett syndrome. Nature 484: 105-109.
31. Dunn TA, Wang CT, Colicos MA, Zaccolo M, DiPilato LM, Zhang J, Tsien RY, Feller MB. 2006. Imaging of cAMP levels and protein kinase A activity reveals that retinal waves drive oscillations in second-messenger cascades. J Neurosci 26: 12807-12815.
32. Elward K, Gasque P. 2003. "Eat me" and "don't eat me" signals govern the innate immune response and tissue repair in the CNS: Emphasis on the critical role of the complement system. Mol Immunol 40: 85-94.
33. Farber K, Kettenmann H. 2006. Purinergic signaling and microglia. Pflugers Arch 452: 615-621.
34. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, Lichtman JW, Sanes JR. 2000. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28: 41-51.
35. Fontainhas AM, Wang M, Liang KJ, Chen S, Mettu P, Damani M, Fariss RN, Li W, Wong WT. 2011. Microglial morphology and dynamic behavior is regulated by ionotropic glutamatergic and GABAergic neurotransmission. PLoS One 6: e15973.
36. Freeman MR. 2006. Sculpting the nervous system: glial control of neuronal development. Curr Opin Neurobiol 16: 119-125.
37. Fuentes-Medel Y, Logan MA, Ashley J, Ataman B, Budnik V, Freeman MR. 2009. Glia and muscle sculpt neuromuscular arbors by engulfing destabilized synaptic boutons and shed presynaptic debris. PLoS Biol 7: e1000184.
38. Gasque P. 2004. Complement: A unique innate immune sensor for danger signals. Mol Immunol 41: 1089-1098.
39. Goddard CA, Butts DA, Shatz CJ. 2007. Regulation of CNS synapses by neuronal MHC class I. Proc Natl Acad Sci U S A 104: 6828-6833.
40. Godement P, Salaun J, Imbert M. 1984. Prenatal and postnatal development of retinogeniculate and retinocollicular projections in the mouse. J Comp Neurol 230: 552-575.
41. Gordon JA, Stryker MP. 1996. Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse. J Neurosci 16: 3274-3286.
42. Griffiths MR, Gasque P, Neal JW. 2009. The multiple roles of the innate immune system in the regulation of apoptosis and inflammation in the brain. J Neuropathol Exp Neurol 68: 217-226.
43. Grimsley C, Ravichandran KS. 2003. Cues for apoptotic cell engulfment: eat-me, don't eat-me and come-get-me signals. Trends Cell Biol 13: 648-656.
44. Grinberg YY, Milton JG, Kraig RP. 2011. Spreading depression sends microglia on Levy flights. PLoS One 6: e19294.
45. Guido W. 2008. Refinement of the retinogeniculate pathway. J Physiol 586: 4357-4362.
46. Guy J, Hendrich B, Holmes M, Martin JE, Bird A. 2001. A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat Genet 27: 322-326.
47. Hamerman JA, Tchao NK, Lowell CA, Lanier LL. 2005. Enhanced toll-like receptor responses in the absence of signaling adaptor DAP12. Nat Immunol 6: 579-586.
48. Hanisch UK, Kettenmann H. 2007. Microglia: Active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10: 1387-1394.
49. Harrison JK, Jiang Y, Chen S, Xia Y, Maciejewski D, Mcnamara RK, Streiti WJ, Salafranca MN, Adhikari S, Thompson DA, Botti P, Bacon KB, Feng L. et al. 1998. Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc Natl Acad Sci U S A 95: 10896-10901.
50. Hashimoto K. 2008. Microglial activation in schizophrenia and minocycline treatment. Prog Neuropsychopharmacol Biol Psychiatry 32: 1758-1759; author reply 1760.
51. Håvik B, Le Hellard S, Rietschel M, Lybæk H, Djurovic S, Mattheisen M, Mühleisen TW, Degenhardt F, Priebe L, Maier W, Breuer R, Schulze TG, Agartz I, Melle I, Hansen T, Bramham CR, Nöthen MM, Stevens B, Werge T, Andreassen OA, Cichon S, Steen VM. 2011. The complement control-related genes CSMD1 and CSMD2 associate to Schizophrenia. Biol Psychiatry 70: 35-42.
52. Hayashi Y, Ishibashi H, Hashimoto K, Nakanishi H. 2006. Potentiation of the NMDA receptor-mediated responses through the activation of the glycine site by microglia secreting soluble factors. Glia 53: 660-668.
53. Haynes SE, Hollopeter G, Yang G, Kurpius D, Dailey ME, Gan WB, Julius D. 2006. The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nat Neurosci 9: 1512-1519.
54. Hirasawa T, Ohsawa K, Imai Y, Ondo Y, Akazawa C, Uchino S, Kohsaka S. 2005. Visualization of microglia in living tissues using Iba1-EGFP transgenic mice. J Neurosci Res 81: 357-362.
55. Hong YK, Chen C. 2011. Wiring and rewiring of the retinogeniculate synapse. Curr Opin Neurobiol 21: 228-237.
56. Hooks BM, Chen C. 2006. Distinct roles for spontaneous and visual activity in remodeling of the retinogeniculate synapse. Neuron 52: 281-291.
57. Hooks BM, Chen C. 2007. Critical periods in the visual system: Changing views for a model of experience-dependent plasticity. Neuron 56: 312-326.
58. Hua JY, Smith SJ. 2004. Neural activity and the dynamics of central nervous system development. Nat Neurosci 7: 327-332.
59. Huberman AD. 2007. Mechanisms of eye-specific visual circuit development. Curr Opin Neurobiol 17: 73-80.
60. Huberman AD, Feller MB, Chapman B. 2008. Mechanisms underlying development of visual maps and receptive fields. Annu Rev Neurosci 31: 479-509.
61. Huh GS, Boulanger LM, Du H, Riquelme PA, Brotz TM, Shatz CJ. 2000. Functional requirement for class I MHC in CNS development and plasticity. Science 290: 2155-2159.
62. Inoue K, Koizumi S, Tsuda M. 2007. The role of nucleotides in the neuron-Glia communication responsible for the brain functions. J Neurochem 102: 1447-1458.
63. Ito HT, Smith SE, Hsiao E, Patterson PH. 2010. Maternal immune activation alters nonspatial information processing in the hippocampus of the adult offspring. Brain Behav Immun 24: 930-941.
64. Jaubert-Miazza L, Green E, Lo FS, Bui K, Mills J, Guido W. 2005. Structural and functional composition of the developing retinogeniculate pathway in the mouse. Vis Neurosci 22: 661-676.
65. Jung S, Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW, Sher A, Littman DR. 2000. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol 20: 4106-4114.
66. Katz LC, Shatz CJ. 1996. Synaptic activity and the construction of cortical circuits. Science 274: 1133-1138.
67. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A. 2011. Physiology of microglia. Physiol Rev 91: 461-553.
68. Kreutzberg GW. 1993. Dynamic changes in motoneurons during regeneration. Restor Neurol Neurosci 5: 59-60.
69. Kreutzberg GW. 1996. Microglia: A sensor for pathological events in the CNS. Trends Neurosci 19: 312-318.
70. Lambris JD, Tsokos GC. 1986. The biology and pathophysiology of complement receptors. Anticancer Res 6: 515-523.
71. LeBlanc JJ, Fagiolini M. 2011. Autism: A "critical period" disorder? Neural Plast 2011: 921680.
72. Linnartz B, Kopatz J, Tenner AJ, Neumann H. 2012. Sialic acid on the neuronal glycocalyx prevents complement c1 binding and complement receptor-3-mediated removal by microglia. J Neurosci 32: 946-952.
73. Logan MA, Hackett R, Doherty J, Sheehan A, Speese SD, Freeman MR. 2012. Negative regulation of glial engulfment activity by Draper terminates glial responses to axon injury. Nat Neurosci 15: 722-730.
74. MacDonald JM, Beach MG, Porpiglia E, Sheehan AE, Watts RJ, Freeman MR. 2006. The Drosophila cell corpse engulfment receptor Draper mediates glial clearance of severed axons. Neuron 50: 869-881.
75. Maezawa I, Jin LW. 2010. Rett syndrome microglia damage dendrites and synapses by the elevated release of glutamate. J Neurosci 30: 5346-5356.
76. Majewska A, Sur M. 2003. Motility of dendritic spines in visual cortex in vivo: Changes during the critical period and effects of visual deprivation. Proc Natl Acad Sci U S A 100: 16024-16029.
77. Mallat M, Marin-Teva JL, Cheret C. 2005. Phagocytosis in the developing CNS: More than clearing the corpses. Curr Opin Neurobiol 15: 101-107.
78. Mandolesi G, Grasselli G, Musumeci G, Centonze D. 2010. Cognitive deficits in experimental autoimmune encephalomyelitis: neuroinflammation and synaptic degeneration. Neurol Sci 31: S255-S259.
79. McKercher SR, Torbett BE, Anderson KL, Henkel GW, Vestal DJ, Baribault H, Klemsz M, Feeney AJ, Wu GE, Paige CJ, Maki RA. etal. 1996. Targeted disruption of the PU. 1 gene results in multiple hematopoietic abnormalities. EMBO J 15: 5647-5658.
80. Melom JE, Littleton JT. 2011. Synapse development in health and disease. Curr Opin Genet Dev 21: 256-261.
81. Milnerwood AJ, Raymond LA. 2010. Early synaptic pathophysiology in neurodegeneration: Insights from Huntington's disease. Trends Neurosci 33: 513-523.
82. Monji A, Kato T, Kanba S. 2009a. Cytokines and schizophrenia: Microglia hypothesis of schizophrenia. Psychiatry Clin Neurosci 63: 257-265.
83. Monji A, Kato T, Kanba S. 2009b. Cytokines and schizophrenia: Microglia hypothesis of schizophrenia. Psychiatry Clin Neurosci 63: 257-265.
84. Morgan JT, Chana G, Pardo CA, Achim C, Semendeferi K, Buckwalter J, Courchesne E, Everall IP. 2010. Microglial activation and increased microglial density observed in the dorsolateral prefrontal cortex in autism. Biol Psychiatry 68: 368-376.
85. Moriguchi S, Mizoguchi Y, Tomimatsua Y, Hayashia Y, Kadowaki T, Kagamiishi Y, Katsube N, Yamamoto K, Inoue K, Watanabe S, Nabekura J, Nakanishi H. et al. 2003. Potentiation of NMDA receptor-mediated synaptic responses by microglia. Mol Brain Res 119: 160-169.
86. Mower GD, Christen WG, Caplan CJ. 1983. Very brief visual experience eliminates plasticity in the cat visual cortex. Science 221: 178-180.
87. Nagata S, Hanayama R, Kawane K. 2010. Autoimmunity and the clearance of dead cells. Cell 140: 619-630.
88. Nimmerjahn A, Kirchhoff F, Helmchen F. 2005. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308: 1314-1318.
89. O'Leary DD, McLaughlin T. 2005. Mechanisms of retinotopic map development: Ephs, ephrins, and spontaneous correlated retinal activity. 147: 43-65.
90. Orr AG, Orr AL, Li XJ, Gross RE, Traynelis SF. 2009. Adenosine A(2A) receptor mediates microglial process retraction. Nat Neurosci 12: 872-878.
91. Paolicelli RC, Bolasco G, Pagani F, Maggi L, Scianni M, Panzanelli P, Giustetto M, Ferreira TA, Guiducci E, Dumas L, Ragozzino D, Gross CT. et al. 2011. Synaptic pruning by microglia is necessary for normal brain development. Science 333: 1456-1458.
92. Pardo CA, Vargas DL, Zimmerman AW. 2005. Immunity, neuroglia and neuroinflammation in autism. Int Rev Psychiatry 17: 485-495.
93. Parkhurst CN, Littman DN, Gan W. 2011. Generation of characterization of a CX3CR1-CreER for the study of microglia function in the CNS. Soc Neurosci 2011 Abstract 664.16/I10.
94. Pascual O, Ben Achour S, Rostaing P, Triller A, Bessis A. 2011. Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission. Proc Natl Acad Sci U S A 109: E197-E205.
95. Penn A, Riquelme P, Feller MB, Shatz C. 1998. Competition in retinogeniculate patterning driven by spontaneous activity. Science 279: 2108-2112.
96. Perry VH, O'Connor V. 2010. The role of microglia in synaptic stripping and synaptic degeneration: a revised perspective. ASN Neuro 2: e00047.
97. Philpot BD, Sekhar AK, Shouval HZ, Bear MF. 2001. Visual experience and deprivation bidirectionally modify the composition and function of NMDA receptors in visual cortex. Neuron 29: 157-169.
98. Pocock JM, Kettenmann H. 2007. Neurotransmitter receptors on microglia. Trends Neurosci 30: 527-535.
99. Prinz M, Priller J, Sisodia SS, Ransohoff RM. 2011. Heterogeneity of CNS myeloid cells and their roles in neurodegeneration. Nat Neurosci 14: 1227-1235.
100. Ransohoff RM, Perry VH. 2009. Microglial physiology: Unique stimuli, specialized responses. Annu Rev Immunol 27: 119-145.
101. Ravichandran KS. 2011. Beginnings of a good apoptotic meal: The find-me and eat-me signaling pathways. Immunity 35: 445-455.
102. Rogers JT, Morganti JM, Bachstetter AD, Hudson CE, Peters MM, Grimmig BA, Weeber EJ, Bickford PC, Gemma C. 2011. CX3CR1 deficiency leads to impairment of hippocampal cognitive function and synaptic plasticity. J Neurosci 31: 16241-16250.
103. Rosen AM, Stevens B. 2010. The role of the classical complement cascade in synapse loss during development and glaucoma. Adv Exp Med Biol 703: 75-93.
104. Roumier A, Bechade C, Poncer JC, Smalla KH, Tomasello E, Vivier E, Gundelfinger ED, Triller A, Bessis A. 2004. Impaired synaptic function in the microglial KARAP/DAP12-deficient mouse. J Neurosci 24: 11421-11428.
105. Roumier A, Pascual O, Bechade C, Wakselman S, Poncer JC, Real E, Triller A, Bessis A. 2008. Prenatal activation of microglia induces delayed impairment of glutamatergic synaptic function. PLoS One 3: e2595.
106. Rubenstein JL, Merzenich MM. 2003. Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav 2: 255-267.
107. Sanes JR, Lichtman JW. 1999. Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 22: 389-442.
108. Schafer DP, Lehrman EK, Kautzman AG, Koyama R, Mardinly AR, Yamasaki R, Ransohoff RM, Greenberg ME, Barres BA, Stevens B. 2012. Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74: 691-705.
109. Schafer DP, Stevens B. 2010. Synapse elimination during development and disease: immune molecules take centre stage. Biochem Soc Trans 38: 476-481.
110. Scott EW, Simon MC, Anastasi J, Singh H. 1994. Requirement of transcription factor PU.1 in the development of multiple hematopoietic lineages. Science 265: 1573-1577.
111. Shatz CJ. 1990. Competitive interactions between retinal ganglion cells during prenatal development. J Neurobiol 21: 197-211.
112. Shatz CJ, Stryker MP. 1988. Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents. Science 242: 87-89.
113. Shi L, Fatemi SH, Sidwell RW, Patterson PH. 2003. Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. J Neurosci 23: 297-302.
114. Siskova Z, Page A, O'Connor V, Perry VH. 2009. Degenerating synaptic boutons in prion disease: microglia activation without synaptic stripping. Am J Pathol 175: 1610-1621.
115. Sretavan DW, Shatz CJ. 1986. Prenatal development of retinal ganglion cell axons: Segregation into eye-specific layers within the cat's lateral geniculate nucleus. J Neurosci 6: 234-251.
116. Steiner J, Bielau H, Brisch R, Danos P, Ullrich O, Mawrin C, Bernstein HG, Bogerts B. 2008. Immunological aspects in the neurobiology of suicide: Elevated microglial density in schizophrenia and depression is associated with suicide. J Psychiatr Res 42: 151-157.
117. Stellwagen D, Malenka RC. 2006. Synaptic scaling mediated by glial TNF-alpha. Nature 440: 1054-1059.
118. Stellwagen D, Shatz CJ. 2002. An instructive role for retinal waves in the development of retinogeniculate connectivity. Neuron 33: 357-367.
119. Stellwagen D, Shatz CJ, Feller MB. 1999. Dynamics of retinal waves are controlled by cyclic AMP. Neuron 24: 673-685.
120. Stephan AH, Barres BA, Stevens B. 2012. The complement system: an unexpected role in synaptic pruning during development and disease. Annu Rev Neurosci 35: 369-389.
121. Stevens B, Allen NJ, Vazquez LE, Howell GR, Christopherson KS, Nouri N, Micheva KD, Mehalow AK, Huberman AD, Stafford B, Sher A, Litke AM, Lambris JD, Smith SJ, John SW, Barres BA. etal. 2007. The classical complement cascade mediates CNS synapse elimination. Cell 131: 1164-1178.
122. Syken J, Grandpre T, Kanold PO, Shatz CJ. 2006. PirB restricts ocular-dominance plasticity in visual cortex. Science 313: 1795-1800.
123. Tomasello E, Desmoulins PO, Chemin K, Guia S, Cremer H, Ortaldo J, Love P, Kaiserlian D, Vivier E. 2000. Combined natural killer cell and dendritic cell functional deficiency in KARAP/DAP12 loss-of-function mutant mice. Immunity 13: 355-364.
124. Tomasello E, Olcese L, Vely F, Geourgeon C, Blery M, Moqrich A, Gautheret D, Djabali M, Matteii M, Vivier E. 1998. Gene structure, expression pattern, and biological activity of mouse killer cell activating receptor-associated protein (KARAP)/DAP-12. J Biol Chem 273: 34115-34119.
125. Torborg CL, Feller MB. 2005. Spontaneous patterned retinal activity and the refinement of retinal projections. Prog Neurobiol 76: 213-235.
126. Trapp BD, Wujek JR, Criste GA, Jalabi W, Yin X, Kidd GJ, Stohlman S, Ransohoff R. 2007. Evidence for synaptic stripping by cortical microglia. Glia 55: 360-368.
127. Tremblay MÈ. 2012. The role of microglia at synapses in the healthy CNS: Novel insights from recent imaging studies. Neuron Glia Biol 15: 1-10.
128. Tremblay ME, Lowery RL, Majewska AK. 2010. Microglial interactions with synapses are modulated by visual experience. PLoS Biol 8: e1000527.
129. Tremblay ME, Zettel ML, Ison JR, Allen PD, Majewska AK. 2012. Effects of aging and sensory loss on glial cells in mouse visual and auditory cortices. Glia 60: 541-558.
130. Tropea D, Majewska AK, Garcia R, Sur M. 2010. Structural dynamics of synapses in vivo correlate with functional changes during experience-dependent plasticity in visual cortex. J Neurosci 30: 11086-11095.
131. Tsuda M, Shigemoto-Mogami Y, Koizumi S, Mizokoshi A, Kohsaka S, Salter MW, Inoue K. 2003. P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 424: 778-783.
132. Turnbull IR, McDunn JE, Takai T, Townsend RR, Cobb JP, Colonna M. 2005. DAP12 (KARAP) amplifies inflammation and increases mortality from endotoxemia and septic peritonitis. J Exp Med 202: 363-369.
133. Turrigiano GG. 2008. The self-tuning neuron: Synaptic scaling of excitatory synapses. Cell 135: 422-435.
134. Turrigiano GG, Nelson SB. 2004. Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5: 97-107.
135. van Lookeren Campagne M, Wiesmann C, Brown EJ. 2007. Macrophage complement receptors and pathogen clearance. Cell Microbiol 9: 2095-2102.
136. Vargas DL, Nascimbene C, Krishnan C, Zimmerman AW, Pardo CA. 2005. Neuroglial activation and neuroinflammation in the brain of patients with autism. Ann Neurol 57: 67-81.
137. Viegi A, Cotrufo T, Berardi N, Mascia L, Maffei L. 2002. Effects of dark rearing on phosphorylation of neurotrophin Trk receptors. Eur J Neurosci 16: 1925-1930.
138. Waites CL, Garner CC. 2011. Presynaptic function in health and disease. Trends Neurosci 34: 326-337.
139. Wake H, Moorhouse AJ, Jinno S, Kohsaka S, Nabekura J. 2009. Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J Neurosci 29: 3974-3980.
140. Yang XW, Lu XH. 2011. Molecular and cellular basis of obsessive-compulsive disorder-like behaviors: Emerging view from mouse models. Curr Opin Neurol 24: 114-118.
141. Watts RJ, Schuldiner O, Perrino J, Larsen C, Luo L. 2004. Glia engulf degenerating axons during developmental axon pruning. Curr Biol 14:678-684.
142. Yoshiyama Y, Higuchi M, Zhang B, Huang SM, Iwata N, Saido TC, Maeda J, Suhara T, Trojanowski JQ, Lee VM. 2007. Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model. Neuron 53: 337-351.
143. Ziburkus J, Guido W. 2006. Loss of binocular responses and reduced retinal convergence during the period of retinogeniculate axon segregation. J Neurophysiol 96: 2775-2784.
144. Ziegenfuss JS, Biswas R, Avery MA, Hong K, Sheehan AE, Yeung YG, Stanley ER, Freeman MR. 2008. Draper-dependent glial phagocytic activity is mediated by Src and Syk family kinase signalling. Nature 453: 935-939.