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Journal of Neuroinflammation
Published in: Journal of Neuroinflammation 1/2016

Open Access 01-12-2016 | Research

Electroconvulsive shock attenuated microgliosis and astrogliosis in the hippocampus and ameliorated schizophrenia-like behavior of Gunn rat

Authors: Erlyn Limoa, Sadayuki Hashioka, Tsuyoshi Miyaoka, Keiko Tsuchie, Ryosuke Arauchi, Ilhamuddin A. Azis, Rei Wake, Maiko Hayashida, Tomoko Araki, Motohide Furuya, Kristian Liaury, Andi J. Tanra, Jun Horiguchi

Published in: Journal of Neuroinflammation | Issue 1/2016

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Abstract

Background

Although electroconvulsive therapy (ECT) is regarded as one of the efficient treatments for intractable psychiatric disorders, the mechanism of therapeutic action remains unclear. Recently, many studies indicate that ECT affects the immune-related cells, such as microglia, astrocytes, and lymphocytes. Moreover, microglial activation and astrocytic activation have been implicated in the postmortem brains of schizophrenia patients. We previously demonstrated that Gunn rats showed schizophrenia-like behavior and microglial activation in their brains. The present study examined the effects of electroconvulsive shock (ECS), an animal counterpart of ECT, on schizophrenia-like behavior, microgliosis, and astrogliosis in the brain of Gunn rats.

Methods

The rats were divided into four groups, i.e., Wistar sham, Wistar ECS, Gunn sham, and Gunn ECS. ECS groups received ECS once daily for six consecutive days. Subsequently, prepulse inhibition (PPI) test was performed, and immunohistochemistry analysis was carried out to determine the activation degree of microglia and astrocytes in the hippocampus by using anti-CD11b and anti-glial fibrillary acidic protein (GFAP) antibody, respectively.

Results

We found PPI deficit in Gunn rats compared to Wistar rats, and it was significantly improved by ECS. Immunohistochemistry analysis revealed that immunoreactivity of CD11b and GFAP was significantly increased in Gunn rats compared to Wistar rats. ECS significantly attenuated the immunoreactivity of both CD11b and GFAP in Gunn rats.

Conclusions

ECS ameliorated schizophrenia-like behavior of Gunn rats and attenuated microgliosis and astrogliosis in the hippocampus of Gunn rats. Accordingly, therapeutic effects of ECT may be exerted, at least in part, by inhibition of glial activation. These results may provide crucial information to elucidate the role of activated glia in the pathogenesis of schizophrenia and to determine whether future therapeutic interventions should attempt to up-regulate or down-regulate glial functions.
Literature
1.
Group TUER. Efficacy and safety of electroconvulsive therapy in depressive disorders: a systematic review and meta-analysis. Lancet. 2003;361:799–808.CrossRef
2.
Guloksuz S, Arts B, Walter S, Drukker M, Rodriguez L, Myint AM, Schwarz MJ, Ponds R, van Os J, Kenis G, Rutten BP. The impact of electroconvulsive therapy on the tryptophan-kynurenine metabolic pathway. Brain Behav Immun. 2015;48:48–52.CrossRefPubMed
3.
Pompili M, Lester D, Dominici G, Longo L, Marconi G, Forte A, Serafini G, Amore M, Girardi P. Indications for electroconvulsive treatment in schizophrenia: a systematic review. Schizophr Res. 2013;146:1–9.CrossRefPubMed
4.
Abrams R. Electroconvulsive therapy, 4th ed. New York: Oxford University Press; 2002.
5.
Anderson IM, Fergusson GM. Mechanism of action of ECT. 2013. p. 1–7.
6.
Scott AIF. Mode of action of electroconvulsive therapy: an update. Adv Psychiatr Treat. 2011;17:15–22.CrossRef
7.
Fluitman SB, Heijnen CJ, Denys DA, Nolen WA, Balk FJ, Westenberg HG. Electroconvulsive therapy has acute immunological and neuroendocrine effects in patients with major depressive disorder. J Affect Disord. 2011;131:388–92.CrossRefPubMed
8.
Hestad KA, Tonseth S, Stoen CD, Ueland T, Aukrust P. Raised plasma levels of tumor necrosis factor alpha in patients with depression: normalization during electroconvulsive therapy. J ECT. 2003;19:183–8.CrossRefPubMed
9.
Hashioka S, Han YH, Fujii S, Kato T, Monji A, Utsumi H, Sawada M, Nakanishi H, Kanba S. Phosphatidylserine and phosphatidylcholine-containing liposomes inhibit amyloid beta and interferon-gamma-induced microglial activation. Free Radic Biol Med. 2007;42:945–54.CrossRefPubMed
10.
Hashioka S, McLarnon JG, Ryu JK, Youssef AM, Abd-El-Aziz AS, Neeland EG, Klegeris A. Pyrazole compound 2-MBAPA as a novel inhibitor of microglial activation and neurotoxicity in vitro and in vivo. J Alzheimers Dis. 2011;27:531–41.PubMed
11.
Hashioka S, McGeer PL, Miyaoka T, Wake R, Horiguchi J. Can inhibition of microglial activation cure schizophrenia? Schizophr Res. 2015;168(1-2):583–4.CrossRefPubMed
12.
Smith RS, Maes M. The macrophage-T-lymphocyte theory of schizophrenia: additional evidence. Med Hypotheses. 1995;45:135–41.CrossRefPubMed
13.
Bayer TA, Buslei R, Havas L, Falkai P. Evidence for activation of microglia in patients with psychiatric illnesses. Neurosci Lett. 1999;271:126–8.CrossRefPubMed
14.
Busse S, Busse M, Schiltz K, Bielau H, Gos T, Brisch R, Mawrin C, Schmitt A, Jordan W, Muller UJ, et al. Different distribution patterns of lymphocytes and microglia in the hippocampus of patients with residual versus paranoid schizophrenia: further evidence for disease course-related immune alterations? Brain Behav Immun. 2012;26:1273–9.CrossRefPubMed
15.
Doorduin J, de Vries EF, Willemsen AT, de Groot JC, Dierckx RA, Klein HC. Neuroinflammation in schizophrenia-related psychosis: a PET study. J Nucl Med. 2009;50:1801–7.CrossRefPubMed
16.
Fillman SG, Cloonan N, Catts VS, Miller LC, Wong J, McCrossin T, Cairns M, Weickert CS. Increased inflammatory markers identified in the dorsolateral prefrontal cortex of individuals with schizophrenia. Mol Psychiatry. 2013;18:206–14.CrossRefPubMed
17.
Radewicz K, Garey LJ, Gentleman SM, Reynolds R. Increase in HLA-DR immunoreactive microglia in frontal and temporal cortex of chronic schizophrenics. J Neuropathol Exp Neurol. 2000;59:137–50.CrossRefPubMed
18.
Wierzba-Bobrowicz T, Lewandowska E, Lechowicz W, Stepien T, Pasennik E. Quantitative analysis of activated microglia, ramified and damage of processes in the frontal and temporal lobes of chronic schizophrenics. Folia Neuropathol. 2005;43:81–9.PubMed
19.
Rothermundt M, Ahn JN, Jorgens S. S100B in schizophrenia: an update. Gen Physiol Biophys. 2009; 28 Spec No Focus:F76-81.
20.
Steiner J, Bernstein HG, Bielau H, Farkas N, Winter J, Dobrowolny H, Brisch R, Gos T, Mawrin C, Myint AM, Bogerts B. S100B-immunopositive glia is elevated in paranoid as compared to residual schizophrenia: a morphometric study. J Psychiatr Res. 2008;42:868–76.CrossRefPubMed
21.
Miyaoka T, Seno H, Itoga M, Iijima M, Inagaki T, Horiguchi J. Schizophrenia-associated idiopathic unconjugated hyperbilirubinemia (Gilbert’s syndrome). J Clin Psychiatry. 2000;61:868–71.CrossRefPubMed
22.
Radhakrishnan R, Kanigere M, Menon J, Calvin S, Janish A, Srinivasan K. Association between unconjugated bilirubin and schizophrenia. Psychiatry Res. 2011;189:480–2.CrossRefPubMed
23.
24.
Izquierdo I, Zand R. Behavioural observations in Gunn rats. Psychopharmacology (Berl). 1978;57:155–61.CrossRef
25.
Hayashida M, Miyaoka T, Tsuchie K, Yasuda H, Wake R, Nishida A, Inagaki T, Toga T, Nagami H, Oda T, Horiguchi J. Hyperbilirubinemia-related behavioral and neuropathological changes in rats: a possible schizophrenia animal model. Prog Neuropsychopharmacol Biol Psychiatry. 2009;33:581–8.CrossRefPubMed
26.
Tsuchie K, Miyaoka T, Furuya M, Liaury K, Ieda M, Wake R, Horiguchi J, Takechi M. The effects of antipsychotics on behavioral abnormalities of the Gunn rat (unconjugated hyperbilirubinemia rat), a rat model of schizophrenia. Asian J Psychiatr. 2013;6:119–23.CrossRefPubMed
27.
Liaury K, Miyaoka T, Tsumori T, Furuya M, Wake R, Ieda M, Tsuchie K, Taki M, Ishihara K, Tanra AJ, Horiguchi J. Morphological features of microglial cells in the hippocampal dentate gyrus of Gunn rat: a possible schizophrenia animal model. J Neuroinflammation. 2012;9:56.CrossRefPubMedCentral
28.
Liaury K, Miyaoka T, Tsumori T, Furuya M, Hashioka S, Wake R, Tsuchie K, Fukushima M, Limoa E, Tanra AJ, Horiguchi J. Minocycline improves recognition memory and attenuates microglial activation in Gunn rat: a possible hyperbilirubinemia-induced animal model of schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry. 2014;50:184–90.CrossRefPubMed
29.
Lamont SR, Paulls A, Stewart CA. Repeated electroconvulsive stimulation, but not antidepressant drugs, induces mossy fibre sprouting in the rat hippocampus. Brain Res. 2001;893:53–8.CrossRefPubMed
30.
Shapiro SM, Hecox KE. Development of brainstem auditory evoked potentials in heterozygous and homozygous jaundiced Gunn rats. Brain Res. 1988;469:147–57.CrossRefPubMed
31.
Shapiro SM, Hecox KE. Brain stem auditory evoked potentials in jaundiced Gunn rats. Ann Otol Rhinol Laryngol. 1989;98:308–17.CrossRefPubMed
32.
Levi G, Sohmer H, Kapitulnik J. Auditory nerve and brain stem responses in homozygous jaundiced Gunn rats. Arch Otorhinolaryngol. 1981;232:139–43.CrossRefPubMed
33.
Cereser KM, Frey BN, Bernardes FB, Costa SC, Andreazza AC, Feier G, Souza D, Tramontina F, Goncalves CA, Kapczinski F, Quevedo J. Glial fibrillary acidic protein expression after electroconvulsive shocks in rat brain. Prog Neuropsychopharmacol Biol Psychiatry. 2006;30:663–7.CrossRefPubMed
34.
Chrzaszcz M, Venkatesan C, Dragisic T, Watterson DM, Wainwright MS. Minozac treatment prevents increased seizure susceptibility in a mouse “two-hit” model of closed skull traumatic brain injury and electroconvulsive shock-induced seizures. J Neurotrauma. 2010;27:1283–95.CrossRefPubMedPubMedCentral
35.
Dwork AJ, Christensen JR, Larsen KB, Scalia J, Underwood MD, Arango V, Pakkenberg B, Lisanby SH. Unaltered neuronal and glial counts in animal models of magnetic seizure therapy and electroconvulsive therapy. Neuroscience. 2009;164:1557–64.CrossRefPubMedPubMedCentral
36.
Jansson L, Wennstrom M, Johanson A, Tingstrom A. Glial cell activation in response to electroconvulsive seizures. Prog Neuropsychopharmacol Biol Psychiatry. 2009;33:1119–28.CrossRefPubMed
37.
Jinno S, Kosaka T. Reduction of Iba1-expressing microglial process density in the hippocampus following electroconvulsive shock. Exp Neurol. 2008;212:440–7.CrossRefPubMed
38.
Kragh J, Bolwig TG, Woldbye DP, Jorgensen OS. Electroconvulsive shock and lidocaine-induced seizures in the rat activate astrocytes as measured by glial fibrillary acidic protein. Biol Psychiatry. 1993;33:794–800.CrossRefPubMed
39.
Okada-Tsuchioka M, Segawa M, Kajitani N, Hisaoka-Nakashima K, Shibasaki C, Morinobu S, Takebayashi M. Electroconvulsive seizure induces thrombospondin-1 in the adult rat hippocampus. Prog Neuropsychopharmacol Biol Psychiatry. 2014;48:236–44.CrossRefPubMed
40.
Wennström M, Hellsten J, Ekdahl CT, Tingström A. Electroconvulsive seizures induce proliferation of NG2-expressing glial cells in adult rat hippocampus. Biol Psychiatry. 2003;54:1015–24.CrossRefPubMed
41.
Kaae SS, Chen F, Wegener G, Madsen TM, Nyengaard JR. Quantitative hippocampal structural changes following electroconvulsive seizure treatment in a rat model of depression. Synapse. 2012;66:667–76.CrossRefPubMed
42.
Wennstrom M, Hellsten J, Ekstrand J, Lindgren H, Tingstrom A. Corticosterone-induced inhibition of gliogenesis in rat hippocampus is counteracted by electroconvulsive seizures. Biol Psychiatry. 2006;59:178–86.CrossRefPubMed
43.
Braff D, Stone C, Callaway E, Geyer M, Glick I, Bali L. Prestimulus effects on human startle reflex in normals and schizophrenics. Psychophysiology. 1978;15:339–43.CrossRef
44.
Braff DL, Grillon C, Geyer MA. Gating and habituation of the startle reflex in schizophrenic patients. Arch Gen Psychiatry. 1992;49:206–15.CrossRefPubMed
45.
Braff DL, Swerdlow NR, Geyer MA. Symptom correlates of prepulse inhibition deficits in male schizophrenic patients. Am J Psychiatry. 1999;156:596–602.PubMed
46.
Dawson ME, Schell AM, Hazlett EA, Nuechterlein KH, Filion DL. On the clinical and cognitive meaning of impaired sensorimotor gating in schizophrenia. Psychiatry Res. 2000;96:187–97.CrossRefPubMed
47.
Parwani A, Duncan EJ, Bartlett E, Madonick SH, Efferen TR, Rajan R, Sanfilipo M, Chappell PB, Chakravorty S, Gonzenbach S, et al. Impaired prepulse inhibition of acoustic startle in schizophrenia. Biol Psychiatry. 2000;47:662–9.CrossRefPubMed
48.
Swerdlow NR, Light GA, Cadenhead KS, Sprock J, Hsieh MH, Braff DL. Startle gating deficits in a large cohort of patients with schizophrenia: relationship to medications, symptoms, neurocognition, and level of function. Arch Gen Psychiatry. 2006;63:1325–35.CrossRefPubMed
49.
Kumari V, Soni W, Mathew VM, Sharma T. Prepulse inhibition of the startle response in men with schizophrenia: effects of age of onset of illness, symptoms, and medication. Arch Gen Psychiatry. 2000;57:609–14.CrossRefPubMed
50.
Kumari V, Soni W, Sharma T. Normalization of information processing deficits in schizophrenia with clozapine. Am J Psychiatry. 1999;156:1046–51.PubMed
51.
Sadock B, Sadock V, Ruiz P. Kaplan and Sadock’s synopsis of psychiatry: behavioral sciences/clinical psychiatry. 2014.
52.
Kristensen D, Bauer J, Hageman I, Jorgensen MB. Electroconvulsive therapy for treating schizophrenia: a chart review of patients from two catchment areas. Eur Arch Psychiatry Clin Neurosci. 2011;261:425–32.CrossRefPubMed
53.
Iancu I, Pick N, Seener-Lorsh O, Dannon P. Patients with schizophrenia or schizoaffective disorder who receive multiple electroconvulsive therapy sessions: characteristics, indications, and results. Neuropsychiatr Dis Treat. 2015;11:853–62.PubMedCentral
54.
Chao YL, Chen HH, Chen CH. Effects of repeated electroconvulsive shock on methamphetamine-induced behavioral abnormalities in mice. Brain Stimul. 2012;5:393–401.CrossRef
55.
Hazlett EA, Romero MJ, Haznedar MM, New AS, Goldstein KE, Newmark RE, Siever LJ, Buchsbaum MS. Deficient attentional modulation of startle eyeblink is associated with symptom severity in the schizophrenia spectrum. Schizophr Res. 2007;93:288–95.CrossRefPubMed
56.
Schulz-Juergensen S, Thiemann A, Gebhardt J, Baumgarten-Walczak A, Eggert P. Prepulse inhibition of acoustic startle and the influence of methylphenidate in children with ADHD. J Atten Disord. 2014;18:117–22.CrossRefPubMed
57.
Egeland J. Differentiating attention deficit in adult ADHD and schizophrenia. Arch Clin Neuropsychol. 2007;22:763–71.CrossRefPubMed
58.
Darbra S, Modol L, Pallares M. Allopregnanolone infused into the dorsal (CA1) hippocampus increases prepulse inhibition of startle response in Wistar rats. Psychoneuroendocrinology. 2012;37:581–5.CrossRefPubMed
59.
Ma J, Leung LS. Schizophrenia-like behavioral changes after partial hippocampal kindling. Brain Res. 2004;997:111–8.CrossRefPubMed
60.
Swerdlow NR, Hanlon FM, Henning L, Kim YK, Gaudet I, Halim ND. Regulation of sensorimotor gating in rats by hippocampal NMDA: anatomical localization. Brain Res. 2001;898:195–203.CrossRefPubMed
61.
Harrison PJ. The hippocampus in schizophrenia: a review of the neuropathological evidence and its pathophysiological implications. Psychopharmacology (Berl). 2004;174:151–62.CrossRef
62.
Tamminga CA, Stan AD, Wagner AD. The hippocampal formation in schizophrenia. Am J Psychiatry. 2010;167:1178–93.CrossRefPubMed
63.
Tamminga CA, Thomas BP, Chin R, Mihalakos P, Youens K, Wagner AD, Preston AR. Hippocampal novelty activations in schizophrenia: disease and medication effects. Schizophr Res. 2012;138:157–63.CrossRefPubMed
64.
Green HF, Nolan YM. Inflammation and the developing brain: consequences for hippocampal neurogenesis and behavior. Neurosci Biobehav Rev. 2014;40:20–34.CrossRefPubMed
65.
66.
Furuya M, Miyaoka T, Tsumori T, Liaury K, Hashioka S, Wake R, Tsuchie K, Fukushima M, Ezoe S, Horiguchi J. Yokukansan promotes hippocampal neurogenesis associated with the suppression of activated microglia in Gunn rat. J Neuroinflammation. 2013;10:145.CrossRefPubMedPubMedCentral
67.
Cardoso FL, Brites D, Brito MA. Looking at the blood-brain barrier: molecular anatomy and possible investigation approaches. Brain Res Rev. 2010;64:328–63.CrossRefPubMed
68.
Gazzin S, Berengeno AL, Strazielle N, Fazzari F, Raseni A, Ostrow JD, Wennberg R, Ghersi-Egea JF, Tiribelli C. Modulation of Mrp1 (ABCc1) and Pgp (ABCb1) by bilirubin at the blood-CSF and blood-brain barriers in the Gunn rat. PLoS One. 2011;6:e16165.CrossRefPubMedPubMedCentral
69.
Ostrow JD, Pascolo L, Shapiro SM, Tiribelli C. New concepts in bilirubin encephalopathy. Eur J Clin Invest. 2003;33:988–97.CrossRefPubMed
70.
Gordo AC, Falcao AS, Fernandes A, Brito MA, Silva RF, Brites D. Unconjugated bilirubin activates and damages microglia. J Neurosci Res. 2006;84:194–201.CrossRefPubMed
71.
Silva SL, Vaz AR, Barateiro A, Falcao AS, Fernandes A, Brito MA, Silva RF, Brites D. Features of bilirubin-induced reactive microglia: from phagocytosis to inflammation. Neurobiol Dis. 2010;40:663–75.CrossRefPubMed
72.
Fernandes A, Barateiro A, Falcao AS, Silva SL, Vaz AR, Brito MA, Silva RF, Brites D. Astrocyte reactivity to unconjugated bilirubin requires TNF-alpha and IL-1beta receptor signaling pathways. Glia. 2011;59:14–25.CrossRefPubMed
73.
74.
Pekny M, Pekna M. Astrocyte reactivity and reactive astrogliosis: costs and benefits. Physiol Rev. 2014;94:1077–98.CrossRefPubMed
75.
Zarubenko II, Yakovlev AA, Stepanichev MY, Gulyaeva NV. Electroconvulsive shock induces neuron death in the mouse hippocampus: correlation of neurodegeneration with convulsive activity. Neurosci Behav Physiol. 2005;35:715–21.CrossRefPubMed
76.
Madsen TM, Treschow A, Bengzon J, Bolwig TG, Lindvall O, Tingstrom A. Increased neurogenesis in a model of electroconvulsive therapy. Biol Psychiatry. 2000;47:1043–9.CrossRefPubMed
77.
Ito M, Seki T, Liu J, Nakamura K, Namba T, Matsubara Y, Suzuki T, Arai H. Effects of repeated electroconvulsive seizure on cell proliferation in the rat hippocampus. Synapse. 2010;64:814–21.CrossRefPubMed
78.
Nakamura K, Ito M, Liu Y, Seki T, Suzuki T, Arai H. Effects of single and repeated electroconvulsive stimulation on hippocampal cell proliferation and spontaneous behaviors in the rat. Brain Res. 2013;1491:88–97.CrossRefPubMed
79.
Conti G, Gale K, Kondratyev A. Immunohistochemical evaluation of the protein expression of nerve growth factor and its TrkA receptor in rat limbic regions following electroshock seizures. Neurosci Res. 2009;65:201–9.CrossRefPubMedPubMedCentral
80.
Girgenti MJ, Collier E, Sathyanesan M, Su XW, Newton SS. Characterization of electroconvulsive seizure-induced TIMP-1 and MMP-9 in hippocampal vasculature. Int J Neuropsychopharmacol. 2011;14:535–44.CrossRefPubMed
81.
Newton SS, Girgenti MJ, Collier EF, Duman RS. Electroconvulsive seizure increases adult hippocampal angiogenesis in rats. Eur J Neurosci. 2006;24:819–28.CrossRefPubMed
82.
Ploski JE, Newton SS, Duman RS. Electroconvulsive seizure-induced gene expression profile of the hippocampus dentate gyrus granule cell layer. J Neurochem. 2006;99:1122–32.CrossRefPubMed
83.
Stewart CA, Davies SN. Repeated electroconvulsive stimulation impairs synaptic plasticity in the dentate gyrus in vivo but has no effect in CA1 in vitro. Neurosci Lett. 1996;213:177–80.CrossRefPubMed
84.
Rothermundt M, Arolt V, Weitzsch C, Eckhoff D, Kirchner H. Immunological dysfunction in schizophrenia: a systematic approach. Neuropsychobiology. 1998;37:186–93.CrossRefPubMed
85.
Drexhage RC, Hoogenboezem TA, Cohen D, Versnel MA, Nolen WA, van Beveren NJ, Drexhage HA. An activated set point of T-cell and monocyte inflammatory networks in recent-onset schizophrenia patients involves both pro- and anti-inflammatory forces. Int J Neuropsychopharmacol. 2011;14:746–55.CrossRefPubMed
86.
Zorrilla EP, Cannon TD, Gur RE, Kessler J. Leukocytes and organ-nonspecific autoantibodies in schizophrenics and their siblings: markers of vulnerability or disease? Biol Psychiatry. 1996;40:825–33.CrossRefPubMed
87.
Nikkila HV, Muller K, Ahokas A, Miettinen K, Rimon R, Andersson LC. Accumulation of macrophages in the CSF of schizophrenic patients during acute psychotic episodes. Am J Psychiatry. 1999;156:1725–9.PubMed
Metadata
Title
Electroconvulsive shock attenuated microgliosis and astrogliosis in the hippocampus and ameliorated schizophrenia-like behavior of Gunn rat
Authors
Erlyn Limoa
Sadayuki Hashioka
Tsuyoshi Miyaoka
Keiko Tsuchie
Ryosuke Arauchi
Ilhamuddin A. Azis
Rei Wake
Maiko Hayashida
Tomoko Araki
Motohide Furuya
Kristian Liaury
Andi J. Tanra
Jun Horiguchi
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Journal of Neuroinflammation / Issue 1/2016
Electronic ISSN: 1742-2094
DOI
https://doi.org/10.1186/s12974-016-0688-2

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