Microglial calcium signaling in the adult, aged and diseased brain

Cell Calcium

Volumn 53, Issue 3, 2013, Pages 159-169

  Brawek, Bianca ^a   Garaschuk, Olga ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Calcium imaging; CNS; Microglia; Two photon microscopy

Indexed keywords

CALCIUM ION;

ADULT; AGED; BRAIN DISEASE; BRAIN INJURY; BRAIN TISSUE; CALCIUM SIGNALING; CONCENTRATION RESPONSE; DEGENERATIVE DISEASE; ENCEPHALITIS; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; MICROGLIA; MONOCYTE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; REVIEW;

AGING; ANIMALS; BRAIN; CALCIUM; CALCIUM SIGNALING; HUMANS; MICROGLIA;

EID: 84875272285     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2012.12.003     Document Type: Review

References (106)

1. Ginhoux F., Greter M., Leboeuf M., et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 2010, 330:841-845.
2. Block M.L., Zecca L., Hong J.S. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nature Reviews Neuroscience 2007, 8:57-69.
3. Nimmerjahn A., Kirchhoff F., Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005, 308:1314-1318.
4. Davalos D., Grutzendler J., Yang G., et al. ATP mediates rapid microglial response to local brain injury in vivo. Nature Neuroscience 2005, 8:752-758.
5. Hanisch U.K., Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nature Neuroscience 2007, 10:1387-1394.
6. Biber K., Neumann H., Inoue K., Boddeke H.W. Neuronal 'On' and 'Off' signals control microglia. Trends in Neurosciences 2007, 30:596-602.
7. Lucin K.M., Wyss-Coray T. Immune activation in brain aging and neurodegeneration: too much or too little?. Neuron 2009, 64:110-122.
8. 2+ mobilization and functional responses in microglia: effects of low levels of ATP. Journal of Neuroscience Research 2005, 81:349-356.
9. 12 receptor regulates microglial activation by extracellular nucleotides. Nature Neuroscience 2006, 9:1512-1519.
10. Kim J.V., Dustin M.L. Innate response to focal necrotic injury inside the blood-brain barrier. Journal of Immunology 2006, 177:5269-5277.
11. Dibaj P., Nadrigny F., Steffens H., et al. NO mediates microglial response to acute spinal cord injury under ATP control in vivo. Glia 2010, 58:1133-1144.
12. Kettenmann H., Hanisch U.K., Noda M., Verkhratsky A. Physiology of microglia. Physiological Reviews 2011, 91:461-553.
13. Ransohoff R.M., Perry V.H. Microglial physiology: unique stimuli, specialized responses. Annual Review of Immunology 2009, 27:119-145.
14. Glass C.K., Saijo K., Winner B., Marchetto M.C., Gage F.H. Mechanisms underlying inflammation in neurodegeneration. Cell 2010, 140:918-934.
15. Kreutzberg G.W. Microglia: a sensor for pathological events in the CNS. Trends in Neurosciences 1996, 19:312-318.
16. Neumann H., Kotter M.R., Franklin R.J. Debris clearance by microglia: an essential link between degeneration and regeneration. Brain 2009, 132:288-295.
17. Perry V.H., Cunningham C., Holmes C. Systemic infections and inflammation affect chronic neurodegeneration. Nature Reviews Immunology 2007, 7:161-167.
18. Sierra A., Encinas J.M., Deudero J.J., et al. Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 2010, 7:483-495.
19. 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. Journal of Neuroscience 2009, 29:3974-3980.
20. Tremblay M.E., Lowery R.L., Majewska A.K. Microglial interactions with synapses are modulated by visual experience. PLoS Biology 2010, 8:e1000527.
21. Purves D., Lichtman J.W. Elimination of synapses in the developing nervous system. Science 1980, 210:153-157.
22. Paolicelli R.C., Bolasco G., Pagani F., et al. Synaptic pruning by microglia is necessary for normal brain development. Science 2011, 333:1456-1458.
23. Schafer D.P., Lehrman E.K., Kautzman A.G., et al. Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 2012, 74:691-705.
24. Rakic P. Young neurons for old brains?. Nature Neuroscience 1998, 1:645-647.
25. Alvarez-Buylla A., Garcia-Verdugo J.M. Neurogenesis in adult subventricular zone. Journal of Neuroscience 2002, 22:629-634.
26. Ma D.K., Kim W.R., Ming G.L., Song H. Activity-dependent extrinsic regulation of adult olfactory bulb and hippocampal neurogenesis. Annals of the New York Academy of Sciences 2009, 1170:664-673.
27. Lazarini F., Gabellec M.M., Torquet N., Lledo P.M. Early activation of microglia triggers long-lasting impairment of adult neurogenesis in the olfactory bulb. Journal of Neuroscience 2012, 32:3652-3664.
28. Sierra A., Gottfried-Blackmore A.C., McEwen B.S., Bulloch K. Microglia derived from aging mice exhibit an altered inflammatory profile. Glia 2007, 55:412-424.
29. Miller K.R., Streit W.J. The effects of aging, injury and disease on microglial function: a case for cellular senescence. Neuron Glia Biology 2007, 3:245-253.
30. von Bernhardi R., Tichauer J.E., Eugenin J. Aging-dependent changes of microglial cells and their relevance for neurodegenerative disorders. Journal of Neurochemistry 2010, 112:1099-1114.
31. Itagaki S., McGeer P.L., Akiyama H., Zhu S., Selkoe D. Relationship of microglia and astrocytes to amyloid deposits of Alzheimer disease. Journal of Neuroimmunology 1989, 24:173-182.
32. Meyer-Luehmann M., Spires-Jones T.L., Prada C., et al. Rapid appearance and local toxicity of amyloid-beta plaques in a mouse model of Alzheimer's disease. Nature 2008, 451:720-724.
33. Bolmont T., Haiss F., Eicke D., et al. Dynamics of the microglial/amyloid interaction indicate a role in plaque maintenance. Journal of Neuroscience 2008, 28:4283-4292.
34. Koenigsknecht-Talboo J., Meyer-Luehmann M., Parsadanian M., et al. Rapid microglial response around amyloid pathology after systemic anti-Abeta antibody administration in PDAPP mice. Journal of Neuroscience 2008, 28:14156-14164.
35. Fuhrmann M., Bittner T., Jung C.K., et al. Microglial Cx3cr1 knockout prevents neuron loss in a mouse model of Alzheimer's disease. Nature Neuroscience 2010, 13:411-413.
36. Masuda T., Croom D., Hida H., Kirov S.A. Capillary blood flow around microglial somata determines dynamics of microglial processes in ischemic conditions. Glia 2011, 59:1744-1753.
37. Cardona A.E., Pioro E.P., Sasse M.E., et al. Control of microglial neurotoxicity by the fractalkine receptor. Nature Neuroscience 2006, 9:917-924.
38. Möller T. Calcium signaling in microglial cells. Glia 2002, 40:184-194.
39. Pocock J.M., Kettenmann H. Neurotransmitter receptors on microglia. Trends in Neurosciences 2007, 30:527-535.
40. Färber K., Kettenmann H. Functional role of calcium signals for microglial function. Glia 2006, 54:656-665.
41. Inoue K. Microglial activation by purines and pyrimidines. Glia 2002, 40:156-163.
42. 2+ sensor. Cell Calcium 2011, 49:365-375.
43. Eichhoff G., Brawek B., Garaschuk O. Microglial calcium signal acts as a rapid sensor of single neuron damage in vivo. Biochimica et Biophysica Acta 2011, 1813:1014-1024.
44. Stosiek C., Garaschuk O., Holthoff K., Konnerth A. In vivo two-photon calcium imaging of neuronal networks. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:7319-7324.
45. O. Garaschuk, Imaging microcircuit function in healthy and diseased brain, Experimental Neurology, , in press. doi:10.1016/j.expneurol.2012.02.009.
46. Saijo K., Glass C.K. Microglial cell origin and phenotypes in health and disease. Nature Reviews Immunology 2011, 11:775-787.
47. Schwendele B., Brawek B., Hermes M., Garaschuk O. High resolution in vivo imaging of microglia using a versatile non genetically-encoded marker. European Journal of Immunology 2012, 42:2193-2196.
48. Verderio C., Matteoli M. ATP mediates calcium signaling between astrocytes and microglial cells: modulation by IFN-gamma. Journal of Immunology 2001, 166:6383-6391.
49. Hegg C.C., Hu S., Peterson P.K., Thayer S.A. Beta-chemokines and human immunodeficiency virus type-1 proteins evoke intracellular calcium increases in human microglia. Neuroscience 2000, 98:191-199.
50. Möller T., Kann O., Verkhratsky A., Kettenmann H. Activation of mouse microglial cells affects P2 receptor signaling. Brain Research 2000, 853:49-59.
51. + conductance in cultured microglial cells from mouse brain. Journal of Neuroscience 1993, 13:4403-4411.
52. 2+-dependent plasminogen release from cultured microglia. British Journal of Pharmacology 1998, 123:1304-1310.
53. 6 receptors is a mediator of microglial phagocytosis. Nature 2007, 446:1091-1095.
54. 7 receptor attenuates lipopolysaccharide-mediated microglial activation and neuronal damage in inflamed brain. Journal of Neuroscience 2007, 27:4957-4968.
55. Whittemore E.R., Korotzer A.R., Etebari A., Cotman C.W. Carbachol increases intracellular free calcium in cultured rat microglia. Brain Research 1993, 621:59-64.
56. Biber K., Laurie D.J., Berthele A., et al. Expression and signaling of group I metabotropic glutamate receptors in astrocytes and microglia. Journal of Neurochemistry 1999, 72:1671-1680.
57. Noda M., Nakanishi H., Nabekura J., Akaike N. AMPA-kainate subtypes of glutamate receptor in rat cerebral microglia. Journal of Neuroscience 2000, 20:251-258.
58. Hagino Y., Kariura Y., Manago Y., et al. Heterogeneity and potentiation of AMPA type of glutamate receptors in rat cultured microglia. Glia 2004, 47:68-77.
59. Gu Q. Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience 2002, 111:815-835.
60. 2+ in cultured human microglia. Neuroscience Letters 1998, 255:33-36.
61. Suzuki T., Hide I.A., Matsubara, et al. Microglial alpha7 nicotinic acetylcholine receptors drive a phospholipase C/IP3 pathway and modulate the cell activation toward a neuroprotective role. Journal of Neuroscience Research 2006, 83:1461-1470.
62. Shen J.X., Yakel J.L. Nicotinic acetylcholine receptor-mediated calcium signaling in the nervous system. Acta Pharmacologica Sinica 2009, 30:673-680.
63. 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.
64. i transients and changes the organization of actin in microglia. Glia 1994, 11:336-344.
65. Mantyh P.W. Neurobiology of substance P and the NK1 receptor. Journal of Clinical Psychiatry 2002, 63(Suppl. 11):6-10.
66. Lazarczyk M., Matyja E., Lipkowski A. Substance P and its receptors - a potential target for novel medicines in malignant brain tumour therapies (mini-review). Folia Neuropathologica 2007, 45:99-107.
67. Rasley A., Bost K.L., Olson J.K., Miller S.D., Marriott I. Expression of functional NK-1 receptors in murine microglia. Glia 2002, 37:258-267.
68. Lai J.P., Zhan G.X., Campbell D.E., Douglas S.D., Ho W.Z. Detection of substance P and its receptor in human fetal microglia. Neuroscience 2000, 101:1137-1144.
69. Moller T., Kann O., Prinz M., Kirchhoff F., Verkhratsky A., Kettenmann H. Endothelin-induced calcium signaling in cultured mouse microglial cells is mediated through ETB receptors. Neuroreport 1997, 8:2127-2131.
70. Harrison J.K., Jiang Y., Chen S., et al. Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:10896-10901.
71. Re D.B., Przedborski S. Fractalkine: moving from chemotaxis to neuroprotection. Nature Neuroscience 2006, 9:859-861.
72. 3CR-1-expressing microglia. Journal of Immunology 1999, 163:1628-1635.
73. 3CR1-mediated activation of the mitogen-activated protein kinase cascade. Journal of Biological Chemistry 2001, 276:31831-31838.
74. Franke H., Krugel U., Illes P. P2 receptors and neuronal injury. Pflugers Archiv 2006, 452:622-644.
75. Nolte C., Moller T., Walter T., Kettenmann H. 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 1996, 73:1091-1107.
76. i signaling in mouse microglia. Journal of Neuroscience 1997, 17:615-624.
77. Noda M., Kariura Y., Amano T., et al. Expression and function of bradykinin receptors in microglia. Life Sciences 2003, 72:1573-1581.
78. 2+ exchanger. Journal of Neuroscience 2007, 27:13065-13073.
79. 2+ signaling in human microglia. Brain Research 1999, 842:159-165.
80. Sattayaprasert P., Choi H.B., Chongthammakun S., McLarnon J.G. Platelet-activating factor enhancement of calcium influx and interleukin-6 expression, but not production, in human microglia. Journal of Neuroinflammation 2005, 2:11.
81. Moller T., Hanisch U.K., Ransom B.R. Thrombin-induced activation of cultured rodent microglia\. Journal of Neurochemistry 2000, 75:1539-1547.
82. Caggiano A.O., Kraig R.P. Prostaglandin E receptor subtypes in cultured rat microglia and their role in reducing lipopolysaccharide-induced interleukin-1beta production. Journal of Neurochemistry 1999, 72:565-575.
83. Ciesielski-Treska J., Ulrich G., Taupenot L., et al. Chromogranin A induces a neurotoxic phenotype in brain microglial cells. Journal of Biological Chemistry 1998, 273:14339-14346.
84. Taupenot L., Ciesielski-Treska J., Ulrich G., Chasserot-Golaz S., Aunis D., Bader M.F. Chromogranin A triggers a phenotypic transformation and the generation of nitric oxide in brain microglial cells. Neuroscience 1996, 72:377-389.
85. Cui Y.H., Le Y., Gong W., et al. Bacterial lipopolysaccharide selectively up-regulates the function of the chemotactic peptide receptor formyl peptide receptor 2 in murine microglial cells. Journal of Immunology 2002, 168:434-442.
86. Tiffany H.L., Lavigne M.C., Cui Y.H., et al. Amyloid-beta induces chemotaxis and oxidant stress by acting at formylpeptide receptor 2, a G protein-coupled receptor expressed in phagocytes and brain. Journal of Biological Chemistry 2001, 276:23645-23652.
87. Moller T., Contos J.J., Musante D.B., Chun J., Ransom B.R. Expression and function of lysophosphatidic acid receptors in cultured rodent microglial cells. Journal of Biological Chemistry 2001, 276:25946-25952.
88. Albright A.V., Shieh J.T., Itoh T., et al. Microglia express CCR5, CXCR4, and CCR3, but of these, CCR5 is the principal coreceptor for human immunodeficiency virus type 1 dementia isolates. Journal of Virology 1999, 73:205-213.
89. Boddeke E.W., Meigel I., Frentzel S., et al. Cultured rat microglia express functional beta-chemokine receptors. Journal of Neuroimmunology 1999, 98:176-184.
90. 2+ responses in human microglia. Neuroscience Letters 2000, 281:83-86.
91. Franciosi S., Choi H.B., Kim S.U., McLarnon J.G. Interferon-gamma acutely induces calcium influx in human microglia. Journal of Neuroscience Research 2002, 69:607-613.
92. + currents in human microglia. Neuroscience 2001, 104:1175-1184.
93. Hoffmann A., Kann O., Ohlemeyer C., Hanisch U.K., Kettenmann H. Elevation of basal intracellular calcium as a central element in the activation of brain macrophages (microglia): suppression of receptor-evoked calcium signaling and control of release function. Journal of Neuroscience 2003, 23:4410-4419.
94. 2+ concentration in cultured rat microglia. European Journal of Pharmacology 1995, 288:125-130.
95. McLarnon J.G., Choi H.B., Lue L.F., Walker D.G., Kim S.U. Perturbations in calcium-mediated signal transduction in microglia from Alzheimer's disease patients. Journal of Neuroscience Research 2005, 81:426-435.
96. 7 receptor in Alzheimer disease and amyloid-beta peptide-treated microglia and in peptide-injected rat hippocampus. Journal of Neuropathology and Experimental Neurology 2006, 65:1090-1097.
97. Eichler F.S., Ren J.Q., Cossoy M., et al. Is microglial apoptosis an early pathogenic change in cerebral X-linked adrenoleukodystrophy?. Annals of Neurology 2008, 63:729-742.
98. Derecki N.C., Cronk J.C., Lu Z., et al. Wild-type microglia arrest pathology in a mouse model of Rett syndrome. Nature 2012, 484:105-109.
99. Streit W.J., Xue Q.S. Life and death of microglia. Journal of Neuroimmune Pharmacology 2009, 4:371-379.
100. Beers D.R., Henkel J.S., Xiao Q., et al. Wild-type microglia extend survival in PU.1 knockout mice with familial amyotrophic lateral sclerosis. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:16021-16026.
101. Boillee S., Yamanaka K., Lobsiger C.S., et al. Onset and progression in inherited ALS determined by motor neurons and microglia. Science 2006, 312:1389-1392.
102. Varvel N.H., Grathwohl S.A., Baumann F., et al. Microglial repopulation model reveals a robust homeostatic process for replacing CNS myeloid cells. Proceedings of the National Academy of Sciences of the United States of America 2012, 109:18150-18155.
103. Ferrari D., Villalba M., Chiozzi P., Falzoni S., Ricciardi-Castagnoli P., Di Virgilio F. Mouse microglial cells express a plasma membrane pore gated by extracellular ATP. Journal of Immunology 1996, 156:1531-1539.
104. 2+ entry in mouse microglial cells. Neuroscience 1998, 86:925-935.
105. Hide I., Tanaka M., Inoue A., et al. Extracellular ATP triggers tumor necrosis factor-alpha release from rat microglia. Journal of Neurochemistry 2000, 75:965-972.
106. 2+ influx in human microglia. Cell Calcium 2000, 27:205-212.