Impairment of in vivo calcium signaling in amyloid plaque-associated microglia

Acta Neuropathologica

Volumn 127, Issue 4, 2014, Pages 495-505

  Brawek, Bianca ^a   Schwendele, Bernd ^a   Riester, Karin ^a   Kohsaka, Shinichi ^b   Lerdkrai, Chommanad ^a   Liang, Yajie ^a   Garaschuk, Olga ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

Author keywords

Alzheimer's disease; Inflammation; Intracellular calcium signaling

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMYLOID; CALCIUM ION; CD11B ANTIGEN; CD68 ANTIGEN;

AMYLOID PLAQUE; AMYLOID PLAQUE ASSOCIATED MICROGLIA; ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM CURRENT; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL SHAPE; CELL STRUCTURE; CONTROLLED STUDY; HYPERTROPHY; IN VIVO STUDY; MICROGLIA; NONHUMAN; PRIORITY JOURNAL;

AGE FACTORS; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CALCIUM; CALCIUM SIGNALING; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; FEMALE; GENE EXPRESSION REGULATION; HUMANS; INDOLES; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEUROGLIA; PLAQUE, AMYLOID; PRESENILIN-1; SODIUM CHANNEL BLOCKERS;

EID: 84896545589     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-013-1242-2     Document Type: Article

References (53)

1. Akiyama H, McGeer PL (1990) Brain microglia constitutively express beta-2 integrins. J Neuroimmunol 30(1):81-93 (Pubitemid 20324759)
2. Allan SM, Rothwell NJ (2001) Cytokines and acute neurodegeneration. Nat Rev Neurosci 2(10):734-744 (Pubitemid 33674819)
3. Biber K, Neumann H, Inoue K, Boddeke HW (2007) Neuronal 'On' and 'Off' signals control microglia. Trends Neurosci 30(11):596-602 (Pubitemid 350051426)
4. Bornemann KD, Wiederhold KH, Pauli C et al (2001) Abeta-induced inflammatory processes in microglia cells of APP23 transgenic mice. Am J Pathol 158(1):63-73 (Pubitemid 32096472)
5. Burnstock G (2008) Purinergic signalling and disorders of the central nervous system. Nat Rev Drug Discov 7(7):575-590
6. Busche MA, Eichhoff G, Adelsberger H et al (2008) Clusters of hyperactive neurons near amyloid plaques in a mouse model of Alzheimer's disease. Science 321(5896):1686-1689
7. Cunningham C (2013) Microglia and neurodegeneration: the role of systemic inflammation. Glia 61(1):71-90
8. Davalos D, Grutzendler J, Yang G et al (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8(6):752-758 (Pubitemid 43085841)
9. Del Rio-Hortega P (1932) Microglia. In: Penfield W (ed) Cytology and cellular pathology of the nervous system. Hoeber, New York, pp 482-534
10. Eichhoff G, Brawek B, Garaschuk O (2011) Microglial calcium signal acts as a rapid sensor of single neuron damage in vivo. Biochim Biophys Acta Mol Cell Res 1813:1014-1024
11. Eichhoff G, Busche MA, Garaschuk O (2008) In vivo calcium imaging of the aging and diseased brain. Eur J Nucl Med Mol Imaging 35(Suppl 1):S99-S106
12. Eikelenboom P, Bate C, Van Gool WA et al (2002) Neuroinflammation in Alzheimer's disease and prion disease. Glia 40(2):232-239 (Pubitemid 35337380)
13. Eikelenboom P, van Exel E, Hoozemans JJ et al (2010) Neuroinflammation: an early event in both the history and pathogenesis of Alzheimer's disease. Neurodegenerative Dis 7(1-3):38-41
14. Färber K, Kettenmann H (2005) Physiology of microglial cells. Brain Res Brain Res Rev 48(2):133-143 (Pubitemid 40585744)
15. Färber K, Kettenmann H (2006) Functional role of calcium signals for microglial function. Glia 54(7):656-665 (Pubitemid 44629629)
16. Felderhoff-Mueser U, Schmidt OI, Oberholzer A, Buhrer C, Stahel PF (2005) IL-18: a key player in neuroinflammation and neurodegeneration? Trends Neurosci 28(9):487-493 (Pubitemid 41187798)
17. Garaschuk O (2013) Imaging microcircuit function in healthy and diseased brain. Exp Neurol 242:41-49
18. Garaschuk O, Milos RI, Konnerth A (2006) Targeted bulk-loading of fluorescent indicators for two-photon brain imaging in vivo. Nat Protoc 1(1):380-386
19. Glass CK, Saijo K, Winner B, Marchetto MC, Gage FH (2010) Mechanisms underlying inflammation in neurodegeneration. Cell 140(6):918-934
20. Guerreiro R, Wojtas A, Bras J et al (2012) TREM2 variants in Alzheimer's disease. N Engl J Med 368(2):117-127
21. Hanisch UK, Kettenmann H (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10(11):1387-1394
22. Heneka MT, Kummer MP, Stutz A et al (2013) NLRP3 is activated in Alzheimer's disease and contributes to pathology in APP/PS1 mice. Nature 493(7434):674-678
23. Hermes M, Eichhoff G, Garaschuk O (2010) Intracellular calcium signalling in Alzheimer's disease. J Cell Mol Med 14(1-2):30-41
24. Hide I, Tanaka M, Inoue A et al (2000) Extracellular ATP triggers tumor necrosis factor-alpha release from rat microglia. J Neurochem 75(3):965-972 (Pubitemid 30660484)
25. Hirasawa T, Ohsawa K, Imai Y et al (2005) Visualization of microglia in living tissues using Iba1-EGFP transgenic mice. J Neurosci Res 81(3):357-362 (Pubitemid 41359290)
26. Hirase H, Qian L, Bartho P, Buzsaki G (2004) Calcium dynamics of cortical astrocytic networks in vivo. PLoS Biol 2(4):E96
27. Hoffmann A, Kann O, Ohlemeyer C, Hanisch UK, Kettenmann H (2003) 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. J Neurosci 23(11):4410-4419 (Pubitemid 36706171)
28. 2+ channels mediates TNF-alpha release from microglial cells under chronic purinergic stimulation. Biochim Biophys Acta 1833(12):2573-2585
29. Jana M, Palencia CA, Pahan K (2008) Fibrillar amyloid-beta peptides activate microglia via TLR2: implications for Alzheimer's disease. J Immunol 181(10):7254-7262
30. Jonsson T, Stefansson H, Steinberg S et al (2013) Variant of TREM2 associated with the risk of Alzheimer's disease. N Engl J Med 368(2):107-116
31. Jung S, Aliberti J, Graemmel P et al (2000) Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol 20(11):4106-4114 (Pubitemid 30314508)
32. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A (2011) Physiology of microglia. Physiol Rev 91(2):461-553
33. Koffie RM, Meyer-Luehmann M, Hashimoto T et al (2009) Oligomeric amyloid beta associates with postsynaptic densities and correlates with excitatory synapse loss near senile plaques. Proc Natl Acad Sci USA 106(10):4012-4017
34. 6 receptors is a mediator of microglial phagocytosis. Nature 446(7139):1091-1095
35. Krabbe G, Halle A, Matyash V et al (2013) Functional impairment of microglia coincides with Beta-amyloid deposition in mice with Alzheimer-like pathology. PLoS ONE 8(4):e60921
36. Kuchibhotla KV, Goldman ST, Lattarulo CR et al (2008) Abeta plaques lead to aberrant regulation of calcium homeostasis in vivo resulting in structural and functional disruption of neuronal networks. Neuron 59(2):214-225 (Pubitemid 352033686)
37. Kuchibhotla KV, Lattarulo CR, Hyman BT, Bacskai BJ (2009) Synchronous hyperactivity and intercellular calcium waves in astrocytes in Alzheimer mice. Science 323(5918):1211-1215
38. 2+ and cAMP. Nature 492(7427):123-127
39. McGeer PL, McGeer EG (2013) The amyloid cascade-inflammatory hypothesis of Alzheimer disease: implications for therapy. Acta Neuropathol 126:479-497
40. Murakami T, Ockinger J, Yu J et al (2012) Critical role for calcium mobilization in activation of the NLRP3 inflammasome. Proc Natl Acad Sci U S A 109(28):11282-11287
41. Prokop S, Miller KR, Heppner FL (2013) Microglia actions in Alzheimer's disease. Acta Neuropathol 126(4):461-477
42. Radde R, Bolmont T, Kaeser SA et al (2006) Abeta42-driven cerebral amyloidosis in transgenic mice reveals early and robust pathology. EMBO Rep 7(9):940-946 (Pubitemid 44523975)
43. Ralevic V, Burnstock G (1998) Receptors for purines and pyrimidines. Pharmacol Rev 50(3):413-492 (Pubitemid 28477681)
44. Ransohoff RM, Perry VH (2009) Microglial physiology: unique stimuli, specialized responses. Annu Rev Immunol 27:119-145
45. Rodgers KM, Hutchinson MR, Northcutt A et al (2009) The cortical innate immune response increases local neuronal excitability leading to seizures. Brain 132(Pt 9):2478-2486
46. Schwendele B, Brawek B, Hermes M, Garaschuk O (2012) High resolution in vivo imaging of microglia using a versatile non genetically-encoded marker. Eur J Immunol 42(8):2193-2196
47. 2+-ATPase of sarcoplasmic reticulum. J Biol Chem 264(30):17816-17823
48. Spires TL, Meyer-Luehmann M, Stern EA et al (2005) Dendritic spine abnormalities in amyloid precursor protein transgenic mice demonstrated by gene transfer and intravital multiphoton microscopy. J Neurosci 25(31):7278-7287 (Pubitemid 41113944)
49. Stosiek C, Garaschuk O, Holthoff K, Konnerth A (2003) In vivo two-photon calcium imaging of neuronal networks. Proc Natl Acad Sci U S A 100(12):7319-7324 (Pubitemid 36706436)
50. 2+ signaling evoked by sensory stimulation in vivo. Nat Neurosci 9(6):816-823
51. 3CR1 on microglia of aged mice after lipopolysaccharide challenge. Brain Behav Immun 24(7):1190-1201
52. Wyss-Coray T, Rogers J (2012) Inflammation in Alzheimer disease-a brief review of the basic science and clinical literature. Cold Spring Harbor Perspect Med 2(1):a006346
53. Zhang B, Gaiteri C, Bodea LG et al (2013) Integrated systems approach identifies genetic nodes and networks in late-onset Alzheimer's disease. Cell 153(3):707-720