Activation of serotonin receptors promotes microglial injury-induced motility but attenuates phagocytic activity

Brain, Behavior, and Immunity

Volumn 26, Issue 3, 2012, Pages 419-428

  Krabbe, Grietje ^a   Matyash, Vitali ^a   Pannasch, Ulrike ^b   Mamer, Lauren ^a   Boddeke, Hendrikus W G M ^c   Kettenmann, Helmut ^a  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Focal lesion; Microglia; Phagocytosis; Receptor; Serotonin

Indexed keywords

CALCIUM; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; NITRIC OXIDE; RNA; SEROTONIN RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; BRAIN CORTEX; BRAIN ELECTROPHYSIOLOGY; BRAIN INJURY; CALCIUM CELL LEVEL; CELL CULTURE; CELL MOTILITY; CHEMOTAXIS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOKINE RELEASE; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MICROGLIA; MOUSE; NEUROMODULATION; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA ISOLATION; SEROTONIN RELEASE;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANIMALS, NEWBORN; BRAIN; CELL MOVEMENT; CELLS, CULTURED; CHEMOTAXIS; MICE; MICROGLIA; PHAGOCYTOSIS; RECEPTORS, SEROTONIN; RNA, MESSENGER; SEROTONIN;

EID: 84857194922     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2011.12.002     Document Type: Article

References (52)

1. Agnati L.F., Guidolin D., Guescini M., Genedani S., Fuxe K. Understanding wiring and volume transmission. Brain Res. Rev. 2010, 64:137-159.
2. Bessis A., Bechade C., Bernard D., Roumier A. Microglial control of neuronal death and synaptic properties. Glia 2007, 55:233-238.
3. Biber K., Neumann H., Inoue K., Boddeke H.W. Neuronal 'On' and 'Off' signals control microglia. Trends Neurosci. 2007, 30:596-602.
4. Boucsein C., Kettenmann H., Nolte C. Electrophysiological properties of microglial cells in normal and pathologic rat brain slices. Eur. J. Neurosci. 2000, 12:2049-2058.
5. Boucsein C., Zacharias R., Farber K., Pavlovic S., Hanisch U.K., Kettenmann H. Purinergic receptors on microglial cells: functional expression in acute brain slices and modulation of microglial activation in vitro. Eur. J. Neurosci. 2003, 17:2267-2276.
6. 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. 1993, 13:4412-4421.
7. Bunin M.A., Prioleau C., Mailman R.B., Wightman R.M. Release and uptake rates of 5-hydroxytryptamine in the dorsal raphe and substantia nigra reticulata of the rat brain. J. Neurochem. 1998, 70:1077-1087.
8. Burnstock G. Purinergic cotransmission. F1000 Biol. Rep. 2009, 1:46.
9. Butt A.M. ATP: a ubiquitous gliotransmitter integrating neuron-glial networks. Semin Cell Dev. Biol. 2011, 22:205-213.
10. 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. 2005, 8:752-758.
11. De-Miguel F.F., Trueta C. Synaptic and extrasynaptic secretion of serotonin. Cell Mol. Neurobiol. 2005, 25:297-312.
12. de Haas A.H., Boddeke H.W., Brouwer N., Biber K. Optimized isolation enables ex vivo analysis of microglia from various central nervous system regions. Glia 2007, 55:1374-1384.
13. Depboylu C., Schafer M.K., Arias-Carrion O., Oertel W.H., Weihe E., Hoglinger G.U. Possible involvement of complement factor C1q in the clearance of extracellular neuromelanin from the substantia nigra in Parkinson disease. J. Neuropathol. Exp. Neurol. 2011, 70:125-132.
14. Descarries L., Mechawar N. Ultrastructural evidence for diffuse transmission by monoamine and acetylcholine neurons of the central nervous system. Prog. Brain Res. 2000, 125:27-47.
15. Doggrell S.A. Further analysis of the inhibitory effects of dihydroergotamine, cyproheptadine and ketanserin on the responses of the rat aorta to 5-hydroxytryptamine. J. Auton. Pharmacol. 1992, 12:223-236.
16. Filip M., Bader M. Overview on 5-HT receptors and their role in physiology and pathology of the central nervous system. Pharmacol. Rep. 2009, 61:761-777.
17. Green A.R. Neuropharmacology of 5-hydroxytryptamine. Br. J. Pharmacol. 2006, 147(Suppl 1):S145-S152.
18. Gunther S., Maroteaux L., Schwarzacher S.W. Endogenous 5-HT2B receptor activation regulates neonatal respiratory activity in vitro. J. Neurobiol. 2006, 66:949-961.
19. Haas S., Brockhaus J., Verkhratsky A., Kettenmann H. ATP-induced membrane currents in ameboid microglia acutely isolated from mouse brain slices. Neuroscience 1996, 75:257-261.
20. Hamill O.P., Marty A., Neher E., Sakmann B., Sigworth F.J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981, 391:85-100.
21. Hayashi-Takagi A., Barker P.B., Sawa A. Readdressing synaptic pruning theory for schizophrenia: combination of brain imaging and cell biology. Commun. Integr. Biol. 2011, 4:211-212.
22. Hensler J.G. Serotonergic modulation of the limbic system. Neurosci. Biobehav. Rev. 2006, 30:203-214.
23. Hines D.J., Hines R.M., Mulligan S.J., Macvicar B.A. Microglia processes block the spread of damage in the brain and require functional chloride channels. Glia 2009, 57:1610-1618.
24. Honda S., Sasaki Y., Ohsawa K., Imai Y., Nakamura Y., Inoue K., Kohsaka S. Extracellular ATP or ADP induce chemotaxis of cultured microglia through Gi/o-coupled P2Y receptors. J. Neurosci. 2001, 21:1975-1982.
25. Inoue K. Purinergic systems in microglia. Cell Mol. Life Sci. 2008, 65:3074-3080.
26. Jung S., Aliberti J., Graemmel P., Sunshine M.J., Kreutzberg G.W., Sher A., Littman D.R. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol. Cell Biol. 2000, 20:4106-4114.
27. Katoh N., Soga F., Nara T., Tamagawa-Mineoka R., Nin M., Kotani H., Masuda K., Kishimoto S. Effect of serotonin on the differentiation of human monocytes into dendritic cells. Clin. Exp. Immunol. 2006, 146:354-361.
28. Kaur C., Dheen S.T., Ling E.A. From blood to brain: amoeboid microglial cell, a nascent macrophage and its functions in developing brain. Acta Pharmacol. Sin. 2007, 28:1087-1096.
29. Kershman J. Genesis of microglia in the human brain. Arch. Neurol. Psychiatry 1939, 41:24-50.
30. Kettenmann H., Hanisch U.K., Noda M., Verkhratsky A. Physiology of microglia. Physiol. Rev. 2011, 91:461-553.
31. Kettenmann H., Hoppe D., Gottmann K., Banati R., Kreutzberg G. Cultured microglial cells have a distinct pattern of membrane channels different from peritoneal macrophages. J. Neurosci. Res. 1990, 26:278-287.
32. 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 2007, 446:1091-1095.
33. Mahe C., Loetscher E., Dev K.K., Bobirnac I., Otten U., Schoeffter P. Serotonin 5-HT7 receptors coupled to induction of interleukin-6 in human microglial MC-3 cells. Neuropharmacology 2005, 49:40-47.
34. Muller T., Durk T., Blumenthal B., Grimm M., Cicko S., Panther E., Sorichter S., Herouy Y., Di Virgilio F., Ferrari D., Norgauer J., Idzko M. 5-hydroxytryptamine modulates migration, cytokine and chemokine release and T-cell priming capacity of dendritic cells in vitro and in vivo. PLoS One 2009, 4:e6453.
35. Napoli I., Neumann H. Microglial clearance function in health and disease. Neuroscience 2009, 158:1030-1038.
36. Nimmerjahn A., Kirchhoff F., Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005, 308:1314-1318.
37. O'Connell P.J., Wang X., Leon-Ponte M., Griffiths C., Pingle S.C., Ahern G.P. A novel form of immune signaling revealed by transmission of the inflammatory mediator serotonin between dendritic cells and T cells. Blood 2006, 107:1010-1017.
38. 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 2011, 333:1456-1458.
39. Pocock J.M., Kettenmann H. Neurotransmitter receptors on microglia. Trends Neurosci. 2007, 30:527-535.
40. Radja F., Laporte A.M., Daval G., Verge D., Gozlan H., Hamon M. Autoradiography of serotonin receptor subtypes in the central nervous system. Neurochem. Int. 1991, 18:1-15.
41. Rappert A., Bechmann I., Pivneva T., Mahlo J., Biber K., Nolte C., Kovac A.D., Gerard C., Boddeke H.W., Nitsch R., Kettenmann H. CXCR3-dependent microglial recruitment is essential for dendrite loss after brain lesion. J. Neurosci. 2004, 24:8500-8509.
42. Rezaie P., Male D. Mesoglia & microglia-a historical review of the concept of mononuclear phagocytes within the central nervous system. J. Hist. Neurosci. 2002, 11:325-374.
43. Risch S.C., Nemeroff C.B. Neurochemical alterations of serotonergic neuronal systems in depression. J Clin Psychiatry 1992, (Suppl, 3-7):53.
44. Seifert S., Pannell M., Uckert W., Farber K., Kettenmann H. Transmitter- and hormone-activated Ca(2+) responses in adult microglia/brain macrophages in situ recorded after viral transduction of a recombinant Ca(2+) sensor. Cell Calcium 2011, 49:365-375.
45. Sharma H.S., Patnaik R., Patnaik S., Mohanty S., Sharma A., Vannemreddy P. Antibodies to serotonin attenuate closed head injury induced blood brain barrier disruption and brain pathology. Ann. N Y Acad. Sci. 2007, 1122:295-312.
46. 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 2007, 131:1164-1178.
47. Stiefel M.F., Marmarou A. Cation dysfunction associated with cerebral ischemia followed by reperfusion: a comparison of microdialysis and ion-selective electrode methods. J. Neurosurg. 2002, 97:97-103.
48. Temel Y., Boothman L.J., Blokland A., Magill P.J., Steinbusch H.W., Visser-Vandewalle V., Sharp T. Inhibition of 5-HT neuron activity and induction of depressive-like behavior by high-frequency stimulation of the subthalamic nucleus. Proc. Natl. Acad. Sci. USA 2007, 104:17087-17092.
49. Tremblay M.E., Lowery R.L., Majewska A.K. Microglial interactions with synapses are modulated by visual experience. PLoS Biol 2010, 8:e1000527.
50. Vazquez-Borsetti P., Cortes R., Artigas F. Pyramidal neurons in rat prefrontal cortex projecting to ventral tegmental area and dorsal raphe nucleus express 5-HT2A receptors. Cereb. Cortex 2009, 19:1678-1686.
51. 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. 2009, 29:3974-3980.
52. Walther D.J., Peter J.U., Bashammakh S., Hortnagl H., Voits M., Fink H., Bader M. Synthesis of serotonin by a second tryptophan hydroxylase isoform. Science 2003, 299:76.