Receptors, ion channels, and signaling mechanisms underlying Microglial dynamics

Journal of Biological Chemistry

Volumn 290, Issue 20, 2015, Pages 12443-12450

  Madry, Christian ^a   Attwell, David ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN;

BRAIN DAMAGE; BRAIN DEVELOPMENT; BRAIN INJURY; BRAIN PARENCHYMA; INNATE IMMUNES; NEURONAL ACTIVITIES; SIGNALING MECHANISMS; SIGNALING PATHWAYS;

NEURONS;

ADENOSINE; ADENOSINE DIPHOSPHATE; ADENOSINE RECEPTOR; ADENOSINE TRIPHOSPHATE; FRACTALKINE; ION CHANNEL; NITRIC OXIDE; PURINERGIC P2X RECEPTOR; PURINERGIC P2Y RECEPTOR; RECEPTOR; URIDINE TRIPHOSPHATE; CELL SURFACE RECEPTOR;

ASTROCYTE; BRAIN; BRAIN DAMAGE; CELL COMMUNICATION; CELL MOTILITY; CHEMOTAXIS; DYNAMICS; MICROGLIA; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; APOPTOSIS; BRAIN INJURY; CELL MOTION; HUMAN; IMMUNOLOGY; NERVE CELL; PATHOLOGY; PHAGOCYTOSIS; SYNAPSE;

ANIMALS; APOPTOSIS; ASTROCYTES; BRAIN INJURIES; CELL COMMUNICATION; CELL MOVEMENT; HUMANS; ION CHANNELS; MICROGLIA; NEURONS; PHAGOCYTOSIS; RECEPTORS, CELL SURFACE; SYNAPSES;

EID: 84929378470     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.R115.637157     Document Type: Review

References (75)

1. Lawson, L. J., Perry, V. H., Dri, P., and Gordon, S. (1990) Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 39, 151-170
2. 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., and Merad, M. (2010) Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330, 841-845
3. Prinz, M., and Priller, J. (2014) Microglia and brain macrophages in the molecular age: from origin to neuropsychiatric disease. Nat. Rev. Neurosci. 15, 300-312
4. Davalos, D., Grutzendler, J., Yang, G., Kim, J. V., Zuo, Y., Jung, S., Littman, D. R., Dustin, M. L., and Gan, W.-B. (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat. Neurosci. 8, 752-758
5. Nimmerjahn, A. (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308, 1314-1318
6. Koizumi, S., Shigemoto-Mogami, Y., Nasu-Tada, K., Shinozaki, Y., Ohsawa, K., Tsuda, M., Joshi, B. V., Jacobson, K. A., Kohsaka, S., and Inoue, K. (2007) UDP acting at P2Y6 receptors is a mediator of microglial phagocytosis. Nature 446, 1091-1095
7. Tremblay, M.-È., Lowery, R. L., and Majewska, A. K. (2010) Microglial interactions with synapses are modulated by visual experience. PLoS Biol. 8, e1000527
8. Wake, H., Moorhouse, A. J., Jinno, S., Kohsaka, S., and 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
9. Li, Y., Du, X.-F., Liu, C.-S., Wen, Z.-L., and Du, J.-L. (2012) Reciprocal regulation between resting microglial dynamics and neuronal activity in vivo. Dev. Cell 23, 1189-1202
10. Pascual, O., Ben Achour, S., Rostaing, P., Triller, A., and Bessis, A. (2012) Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission. Proc. Natl. Acad. Sci. U.S.A. 109, E197-E205
11. 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., and Stevens, B. (2012) Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74, 691-705
12. Hoshiko, M., Arnoux, I., Avignone, E., Yamamoto, N., and Audinat, E. (2012) Deficiency of the microglial receptor CX3CR1 impairs postnatal functional development of thalamocortical synapses in the barrel cortex. J. Neurosci. 32, 15106-15111
13. Paolicelli, R. C., Bolasco, G., Pagani, F., Maggi, L., Scianni, M., Panzanelli, P., Giustetto, M., Ferreira, T. A., Guiducci, E., Dumas, L., Ragozzino, D., and Gross, C. T. (2011) Synaptic pruning by microglia is necessary for normal brain development. Science 333, 1456-1458
14. Marín-Teva, J. L., Dusart, I., Colin, C., Gervais, A., van Rooijen, N., and Mallat, M. (2004) Microglia promote the death of developing Purkinje cells. Neuron 41, 535-547
15. Sierra, A., Encinas, J. M., Deudero, J. J. P., Chancey, J. H., Enikolopov, G., Overstreet-Wadiche, L. S., Tsirka, S. E., and Maletic-Savatic, M. (2010) Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 7, 483-495
16. Hellwig, S., Heinrich, A., and Biber, K. (2013) The brain's best friend: microglial neurotoxicity revisited. Front. Cell. Neurosci. 7, 71
17. Lambrechts, A., Van Troys, M., and Ampe, C. (2004) The actin cytoskeleton in normal and pathological cell motility. Int. J. Biochem. Cell Biol. 36, 1890-1909
18. Capani, F., Ellisman, M. H., and Martone, M. E. (2001) Filamentous actin is concentrated in specific subpopulations of neuronal and glial structures in rat central nervous system. Brain Res. 923, 1-11
19. Hines, D. J., Hines, R. M., Mulligan, S. J., and Macvicar, B. A. (2009) Microglia processes block the spread of damage in the brain and require functional chloride channels. Glia 57, 1610-1618
20. Murali, A., and Rajalingam, K. (2014) Small Rho GTPases in the control of cell shape and mobility. Cell. Mol. Life Sci. 71, 1703-1721
21. Kurpius, D., Nolley, E. P., and Dailey, M. E. (2007) Purines induce directed migration and rapid homing of microglia to injured pyramidal neurons in developing hippocampus. Glia 55, 873-884
22. Honda, S., Sasaki, Y., Ohsawa, K., Imai, Y., Nakamura, Y., Inoue, K., and Kohsaka, S. (2001) Extracellular ATP or ADP induce chemotaxis of cultured microglia through Gi/o-coupled P2Y receptors. J. Neurosci. 21, 1975-1982
23. Wu, L. J., Vadakkan, K. I., and Zhuo, M. (2007) ATP-induced chemotaxis of microglial processes requires P2Y receptor-activated initiation of outward potassium currents. Glia 55, 810-821
24. Dibaj, P., Nadrigny, F., Steffens, H., Scheller, A., Hirrlinger, J., Schomburg, E. D., Neusch, C., and Kirchhoff, F. (2010) NO mediates microglial response to acute spinal cord injury under ATP control in vivo. Glia 58, 1133-1144
25. Davalos, D., Ryu, J. K., Merlini, M., Baeten, K. M., Le Moan, N., Petersen, M. A., Deerinck, T. J., Smirnoff, D. S., Bedard, C., Hakozaki, H., Gonias Murray, S., Ling, J. B., Lassmann, H., Degen, J. L., Ellisman, M. H., and Akassoglou, K. (2012) Fibrinogen-induced perivascular microglial clustering is required for the development of axonal damage in neuroinflammation. Nat. Commun. 3, 1227
26. Cross, A. K., and Woodroofe, M. N. (1999) Chemokines induce migration and changes in actin polymerization in adult rat brain microglia and a human fetal microglial cell line in vitro. J. Neurosci. Res. 55, 17-23
27. Forstreuter, F., Lucius, R., and Mentlein, R. (2002) Vascular endothelial growth factor induces chemotaxis and proliferation of microglial cells. J. Neuroimmunol. 132, 93-98
28. Nolte, C., Möller, T., Walter, T., and Kettenmann, H. (1996) Complement 5a controls motility of murine microglial cells in vitro via activation of an inhibitory G-protein and the rearrangement of the actin cytoskeleton. Neuroscience 73, 1091-1107
29. Orr, A. G., Orr, A. L., Li, X.-J., Gross, R. E., and Traynelis, S. F. (2009) AdenosineA2A receptor mediates microglial process retraction. Nat. Neurosci. 12, 872-878
30. Ohsawa, K., Irino, Y., Nakamura, Y., Akazawa, C., Inoue, K., and Kohsaka, S. (2007) Involvement of P2X4 and P2Y12 receptors in ATP-induced microglial chemotaxis. Glia 55, 604-616
31. Arnoux, I., Hoshiko, M., Mandavy, L., Avignone, E., Yamamoto, N., and Audinat, E. (2013) Adaptive phenotype of microglial cells during the normal postnatal development of the somatosensory "Barrel" cortex. Glia 61, 1582-1594
32. Avignone, E., Ulmann, L., Levavasseur, F., Rassendren, F., and Audinat, E. (2008) Status epilepticus induces a particular microglial activation state characterized by enhanced purinergic signaling. J. Neurosci. 28, 9133-9144
33. Boucsein, C., Zacharias, R., Färber, K., Pavlovic, S., Hanisch, U.-K., and Kettenmann, H. (2003) Purinergic receptors on microglial cells: functional expression in acute brain slices and modulation of microglial activation in vitro. Eur. J. Neurosci. 17, 2267-2276
34. Haynes, S. E., Hollopeter, G., Yang, G., Kurpius, D., Dailey, M. E., Gan, W.-B., and Julius, D. (2006) The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nat. Neurosci. 9, 1512-1519
35. Ulmann, L., Levavasseur, F., Avignone, E., Peyroutou, R., Hirbec, H., Audinat, E., and Rassendren, F. (2013) Involvement of P2X4 receptors in hippocampal microglial activation after status epilepticus. Glia 61, 1306-1319
36. Zhang, Y., Chen, K., Sloan, S. A., Bennett, M. L., Scholze, A. R., O'Keeffe, S., Phatnani, H. P., Guarnieri, P., Caneda, C., Ruderisch, N., Deng, S., Liddelow, S. A., Zhang, C., Daneman, R., Maniatis, T., Barres, B. A., and Wu, J. Q. (2014) An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J. Neurosci. 34, 11929-11947
37. Dissing-Olesen, L., LeDue, J. M., Rungta, R. L., Hefendehl, J. K., Choi, H. B., and MacVicar, B. A. (2014) Activation of neuronal NMDA receptors triggers transient ATP-mediated microglial process outgrowth. J. Neurosci. 34, 10511-10527
38. Irino, Y., Nakamura, Y., Inoue, K., Kohsaka, S., and Ohsawa, K. (2008) Akt activation is involved in P2Y12 receptor-mediated chemotaxis of microglia. J. Neurosci. Res. 86, 1511-1519
39. McIlvain, H. B., Ma, L., Ludwig, B., Manners, M. T., Martone, R. L., Dunlop, J., Kaftan, E. J., Kennedy, J. D., and Whiteside, G. T. (2010) Purinergic receptor-mediated morphological changes in microglia are transient and independent from inflammatory cytokine release. Eur. J. Pharmacol. 643, 202-210
40. Ohsawa, K., Irino, Y., Sanagi, T., Nakamura, Y., Suzuki, E., Inoue, K., and Kohsaka, S. (2010) P2Y12 receptor-mediated integrin-β1 activation regulates microglial process extension induced by ATP. Glia 58, 790-801
41. Hynes, R. O. (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-687
42. Kölsch, V., Charest, P. G., and Firtel, R. A. (2008) The regulation of cell motility and chemotaxis by phospholipid signaling. J. Cell Sci. 121, 551-559
43. Färber, K., Markworth, S., Pannasch, U., Nolte, C., Prinz, V., Kronenberg, G., Gertz, K., Endres, M., Bechmann, I., Enjyoji, K., Robson, S. C., and Kettenmann, H. (2008) The ectonucleotidase cd39/ ENTPDase1 modulates purinergic-mediated microglial migration. Glia 56, 331-341
44. Ohsawa, K., Sanagi, T., Nakamura, Y., Suzuki, E., Inoue, K., and Kohsaka, S. (2012) Adenosine A3 receptor is involved in ADP-induced microglial process extension and migration. J. Neurochem. 121, 217-227
45. Gyoneva, S., Davalos, D., Biswas, D., Swanger, S. A., Garnier-Amblard, E., Loth, F., Akassoglou, K., and Traynelis, S. F. (2014) Systemic inflammation regulates microglial responses to tissue damage in vivo. Glia 62, 1345-1360
46. Dahl, G., Qiu, F., and Wang, J. (2013) The bizarre pharmacology of the ATP release channel pannexin1. Neuropharmacology 75, 583-593
47. Mitchell, C. H., Carré, D. A., McGlinn, A. M., Stone, R. A., and Civan, M. M. (1998) A release mechanism for stored ATP in ocular ciliary epithelial cells. Proc. Natl. Acad. Sci. U.S.A. 95, 7174-7178
48. Lee, J. E., Liang, K. J., Fariss, R. N., and Wong, W. T. (2008) Ex vivo dynamic imaging of retinal microglia using time-lapse confocal microscopy. Invest. Ophthalmol. Vis. Sci. 49, 4169-4176
49. Damani, M. R., Zhao, L., Fontainhas, A. M., Amaral, J., Fariss, R. N., and Wong, W. T. (2011) Age-related alterations in the dynamic behavior of microglia: Age-related changes in microglial behavior. Aging Cell 10, 263-276
50. Fontainhas, A. M., Wang, M., Liang, K. J., Chen, S., Mettu, P., Damani, M., Fariss, R. N., Li, W., and Wong, W. T. (2011) Microglial morphology and dynamic behavior is regulated by ionotropic glutamatergic and GABAergic neurotransmission. PLoS One 6, e15973
51. Braun, N., Sévigny, J., Robson, S. C., Enjyoji, K., Guckelberger, O., Hammer, K., Di Virgilio, F., and Zimmermann, H. (2000) Assignment of ectonucleoside triphosphate diphosphohydrolase-1/cd39 expression to microglia and vasculature of the brain. Eur. J. Neurosci. 12, 4357-4366
52. Hamilton, N. B., and Attwell, D. (2010) Do astrocytes really exocytose neurotransmitters? Nat. Rev. Neurosci. 11, 227-238
53. Anderson, C. M., Bergher, J. P., and Swanson, R. A. (2004) ATP-induced ATP release from astrocytes. J. Neurochem. 88, 246-256
54. Cotrina, M. L., Lin, J. H.-C., López-García, J. C., Naus, C. C. G., and Nedergaard, M. (2000) ATP-mediated glia signaling. J. Neurosci. 20, 2835-2844
55. Schipke, C. G., Boucsein, C., Ohlemeyer, C., Kirchhoff, F., and Kettenmann, H. (2002) Astrocyte Ca2+ waves trigger responses in microglial cells in brain slices. FASEB J. 16, 255-267
56. Coco, S. (2002) Storage and release of ATP from astrocytes in culture. J. Biol. Chem. 278, 1354-1362
57. Stout, C. E., Costantin, J. L., Naus, C. C. G., and Charles, A. C. (2002) Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J. Biol. Chem. 277, 10482-10488
58. Gyoneva, S., and Traynelis, S. F. (2013) Norepinephrine modulates the motility of resting and activated microglia via different adrenergic receptors. J. Biol. Chem. 288, 15291-15302
59. Wu, L.-J., and Zhuo, M. (2008) Resting microglial motility is independent of synaptic plasticity in mammalian brain. J. Neurophysiol. 99, 2026-2032
60. De Simoni, A., Allen, N. J., and Attwell, D. (2008) Charge compensation for NADPH oxidase activity in microglia in rat brain slices does not involve a proton current. Eur. J. Neurosci. 28, 1146-1156
61. Noda, M., Nakanishi, H., and Akaike, N. (1999) Glutamate release from microglia via glutamate transporter is enhanced by amyloid-β peptide. Neuroscience 92, 1465-1474
62. Noda, M., Nakanishi, H., Nabekura, J., and Akaike, N. (2000) AMPAkainate subtypes of glutamate receptor in rat cerebral microglia. J. Neurosci. 20, 251-258
63. Pankratov, Y., Lalo, U., Verkhratsky, A., and North, R. A. (2006) Vesicular release of ATP at central synapses. Pflugers Arch. 452, 589-597
64. Zujovic, V., Benavides, J., Vigé, X., Carter, C., and Taupin, V. (2000) Fractalkine modulates TNF-α secretion and neurotoxicity induced by microglial activation. Glia 29, 305-315
65. 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., and Ransohoff, R. M. (2006) Control of microglial neurotoxicity by the fractalkine receptor. Nat. Neurosci. 9, 917-924
66. Lauro, C., Di Angelantonio, S., Cipriani, R., Sobrero, F., Antonilli, L., Brusadin, V., Ragozzino, D., and Limatola, C. (2008) Activity of adenosine receptors type 1 is required for CX3CL1-mediated neuroprotection and neuromodulation in hippocampal neurons. J. Immunol. 180, 7590-7596
67. Zujovic, V., Schussler, N., Jourdain, D., Duverger, D., and Taupin, V. (2001) in vivo neutralization of endogenous brain fractalkine increases hippocampal TNF α and 8-isoprostane production induced by intracerebroventricular injection of LPS. J. Neuroimmunol. 115, 135-143
68. Bachstetter, A. D., Morganti, J. M., Jernberg, J., Schlunk, A., Mitchell, S. H., Brewster, K. W., Hudson, C. E., Cole, M. J., Harrison, J. K., Bickford, P. C., and Gemma, C. (2011) Fractalkine and CX3CR1 regulate hippocampal neurogenesis in adult and aged rats. Neurobiol. Aging. 32, 2030-2044
69. Rogers, J. T., Morganti, J. M., Bachstetter, A. D., Hudson, C. E., Peters, M. M., Grimmig, B. A., Weeber, E. J., Bickford, P. C., and Gemma, C. (2011) CX3CR1 deficiency leads to impairment of hippocampal cognitive function and synaptic plasticity. J. Neurosci. 31, 16241-16250
70. Zhan, Y., Paolicelli, R. C., Sforazzini, F., Weinhard, L., Bolasco, G., Pagani, F., Vyssotski, A. L., Bifone, A., Gozzi, A., Ragozzino, D., and Gross, C. T. (2014) Deficient neuron-microglia signaling results in impaired functional brain connectivity and social behavior. Nat. Neurosci. 17, 400-406
71. Liang, K. J., Lee, J. E., Wang, Y. D., Ma, W., Fontainhas, A. M., Fariss, R. N., and Wong, W. T. (2009) Regulation of dynamic behavior of retinal microglia by CX3CR1 signaling. Invest. Ophthalmol. Vis. Sci. 50, 4444-4451
72. Dunwiddie, T. V., Diao, L., and Proctor, W. R. (1997) Adenine nucleotides undergo rapid, quantitative conversion to adenosine in the extracellular space in rat hippocampus. J. Neurosci. 17, 7673-7682
73. Isfort, K., Ebert, F., Bornhorst, J., Sargin, S., Kardakaris, R., Pasparakis, M., Bähler, M., Schwerdtle, T., Schwab, A., and Hanley, P. J. (2011) Real-time imaging reveals that P2Y2 and P2Y12 receptor agonists are not chemoattractants and macrophage chemotaxis to complement C5a is phosphatidylinositol 3-kinase (PI3K)- and p38 mitogen-activated protein kinase (MAPK)-independent. J. Biol. Chem. 286, 44776-44787
74. Corriden, R., and Insel, P. A. (2010) Basal release of ATP: an autocrineparacrine mechanism for cell regulation. Sci. STKE. 3, re1, 10.1126/scisignal.3104re1
75. Eyo, U. B., Peng, J., Swiatkowski, P., Mukherjee, A., Bispo, A., and Wu, L.-J. (2014) Neuronal hyperactivity recruits microglial processes via neuronal NMDA receptors and microglial P2Y12 receptors after status epilepticus. J. Neurosci. 34, 10528-10540