Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
Journal of Neuroinflammation
Published in: Journal of Neuroinflammation 1/2018

Open Access 01-12-2018 | Research

Transcriptome analysis of alcohol-treated microglia reveals downregulation of beta amyloid phagocytosis

Authors: Sergey Kalinin, Marta González-Prieto, Hannah Scheiblich, Lucia Lisi, Handojo Kusumo, Michael T. Heneka, Jose L. M. Madrigal, Subhash C. Pandey, Douglas L. Feinstein

Published in: Journal of Neuroinflammation | Issue 1/2018

Login to get access

Abstract

Background

Microglial activation contributes to the neuropathology associated with chronic alcohol exposure and withdrawal, including the expression of inflammatory and anti-inflammatory genes. In the current study, we examined the transcriptome of primary rat microglial cells following incubation with alcohol alone, or alcohol together with a robust inflammatory stimulus.

Methods

Primary microglia were prepared from mixed rat glial cultures. Cells were incubated with 75 mM ethanol alone or with proinflammatory cytokines (“TII”: IL1β, IFNγ, and TNFα). Isolated mRNA was used for RNAseq analysis and qPCR. Effects of alcohol on phagocytosis were determined by uptake of oligomeric amyloid beta.

Results

Alcohol induced nitrite production in control cells and increased nitrite production in cells co-treated with TII. RNAseq analysis of microglia exposed for 24 h to alcohol identified 312 differentially expressed mRNAs (“Alc-DEs”), with changes confirmed by qPCR analysis. Gene ontology analysis identified phagosome as one of the highest-ranking KEGG pathways including transcripts regulating phagocytosis. Alcohol also increased several complement-related mRNAs that have roles in phagocytosis, including C1qa, b, and c; C3; and C3aR1. RNAseq analysis identified over 3000 differentially expressed mRNAs in microglia following overnight incubation with TII; and comparison to the group of Alc-DEs revealed 87 mRNAs modulated by alcohol but not by TII, including C1qa, b, and c. Consistent with observed changes in phagocytosis-related mRNAs, the uptake of amyloid beta1–42, by primary microglia, was reduced by alcohol.

Conclusions

Our results define alterations that occur to microglial gene expression following alcohol exposure and suggest that alcohol effects on phagocytosis could contribute to the development of Alzheimer’s disease.
Appendix
Available only for authorised users
Literature
1.
Robinson G, Most D, Ferguson LB, Mayfield J, Harris RA, Blednov YA. Neuroimmune pathways in alcohol consumption: evidence from behavioral and genetic studies in rodents and humans. Int Rev Neurobiol. 2014;118:13–39.CrossRefPubMedPubMedCentral
2.
Warden A, Erickson E, Robinson G, Harris RA, Mayfield RD. The neuroimmune transcriptome and alcohol dependence: potential for targeted therapies. Pharmacogenomics. 2016;17:2081–96.CrossRefPubMedPubMedCentral
3.
4.
5.
Wu Y, Lousberg EL, Moldenhauer LM, Hayball JD, Robertson SA, Coller JK, Watkins LR, Somogyi AA, Hutchinson MR. Attenuation of microglial and IL-1 signaling protects mice from acute alcohol-induced sedation and/or motor impairment. Brain Behav Immun. 2011;25(Suppl 1):S155–64.CrossRefPubMed
6.
Martinez JM, Groot JA, Curtis DC, Allison CL, Marquardt PC, Holmes AN, Edwards DS, Trotter DR, Syapin PJ, Finn DA, Bergeson SE. Effective reduction of acute ethanol withdrawal by the tetracycline derivative, tigecycline, in female and male DBA/2J mice. Alcohol Clin Exp Res. 2016;40:2499–505.CrossRefPubMedPubMedCentral
7.
Blanco AM, Pascual M, Valles SL, Guerri C. Ethanol-induced iNOS and COX-2 expression in cultured astrocytes via NF-kappa B. Neuroreport. 2004;15:681–5.CrossRefPubMed
8.
Alfonso-Loeches S, Urena-Peralta J, Morillo-Bargues MJ, Gomez-Pinedo U, Guerri C. Ethanol-induced TLR4/NLRP3 neuroinflammatory response in microglial cells promotes leukocyte infiltration across the BBB. Neurochem Res. 2016;41:193–209.CrossRefPubMed
9.
Alfonso-Loeches S, Pascual-Lucas M, Blanco AM, Sanchez-Vera I, Guerri C. Pivotal role of TLR4 receptors in alcohol-induced neuroinflammation and brain damage. J Neurosci. 2010;30:8285–95.CrossRefPubMedPubMedCentral
10.
Fernandez-Lizarbe S, Pascual M, Guerri C. Critical role of TLR4 response in the activation of microglia induced by ethanol. J Immunol. 2009;183:4733–44.CrossRefPubMed
11.
Fernandez-Lizarbe S, Pascual M, Gascon MS, Blanco A, Guerri C. Lipid rafts regulate ethanol-induced activation of TLR4 signaling in murine macrophages. Mol Immunol. 2008;45:2007–16.CrossRefPubMed
12.
Blanco AM, Guerri C. Ethanol intake enhances inflammatory mediators in brain: role of glial cells and TLR4/IL-1RI receptors. Front Biosci. 2007;12:2616–30.CrossRefPubMed
13.
Valles SL, Blanco AM, Pascual M, Guerri C. Chronic ethanol treatment enhances inflammatory mediators and cell death in the brain and in astrocytes. Brain Pathol. 2004;14:365–71.CrossRefPubMed
14.
Fernandez-Lizarbe S, Montesinos J, Guerri C. Ethanol induces TLR4/TLR2 association, triggering an inflammatory response in microglial cells. J Neurochem. 2013;126:261–73.CrossRefPubMed
15.
16.
Blanco AM, Valles SL, Pascual M, Guerri C. Involvement of TLR4/type I IL-1 receptor signaling in the induction of inflammatory mediators and cell death induced by ethanol in cultured astrocytes. J Immunol. 2005;175:6893–9.CrossRefPubMed
17.
Montesinos J, Alfonso-Loeches S, Guerri C. Impact of the innate immune response in the actions of ethanol on the central nervous system. Alcohol Clin Exp Res. 2016;40:2260–70.CrossRefPubMed
18.
Gustot T, Lemmers A, Moreno C, Nagy N, Quertinmont E, Nicaise C, Franchimont D, Louis H, Deviere J, Le Moine O. Differential liver sensitization to toll-like receptor pathways in mice with alcoholic fatty liver. Hepatology. 2006;43:989–1000.CrossRefPubMed
19.
Lippai D, Bala S, Petrasek J, Csak T, Levin I, Kurt-Jones EA, Szabo G. Alcohol-induced IL-1beta in the brain is mediated by NLRP3/ASC inflammasome activation that amplifies neuroinflammation. J Leukoc Biol. 2013;94:171–82.CrossRefPubMedPubMedCentral
20.
Crews FT, Qin L, Sheedy D, Vetreno RP, Zou J. High mobility group box 1/toll-like receptor danger signaling increases brain neuroimmune activation in alcohol dependence. Biol Psychiatry. 2013;73:602–12.CrossRefPubMed
21.
Most D, Leiter C, Blednov YA, Harris RA, Mayfield RD. Synaptic microRNAs coordinately regulate synaptic mRNAs: perturbation by chronic alcohol consumption. Neuropsychopharmacology. 2016;41:538–48.CrossRefPubMed
22.
Osterndorff-Kahanek E, Ponomarev I, Blednov YA, Harris RA. Gene expression in brain and liver produced by three different regimens of alcohol consumption in mice: comparison with immune activation. PLoS One. 2013;8:e59870.CrossRefPubMedPubMedCentral
23.
Osterndorff-Kahanek EA, Tiwari GR, Lopez MF, Becker HC, Harris RA, Mayfield RD. Long-term ethanol exposure: temporal pattern of microRNA expression and associated mRNA gene networks in mouse brain. PLoS One. 2018;13:e0190841.CrossRefPubMedPubMedCentral
24.
McCarthy GM, Farris SP, Blednov YA, Harris RA, Mayfield RD. Microglial-specific transcriptome changes following chronic alcohol consumption. Neuropharmacology. 2018;128:416–24.
25.
Venegas C, Kumar S, Franklin BS, Dierkes T, Brinkschulte R, Tejera D, Vieira-Saecker A, Schwartz S, Santarelli F, Kummer MP, et al. Microglia-derived ASC specks cross-seed amyloid-beta in Alzheimer's disease. Nature. 2017;552:355–61.CrossRefPubMed
26.
27.
Zuroff L, Daley D, Black KL, Koronyo-Hamaoui M. Clearance of cerebral Abeta in Alzheimer’s disease: reassessing the role of microglia and monocytes. Cell Mol Life Sci. 2017;74:2167–201.CrossRefPubMedPubMedCentral
28.
Hersi M, Irvine B, Gupta P, Gomes J, Birkett N, Krewski D. Risk factors associated with the onset and progression of Alzheimer’s disease: a systematic review of the evidence. Neurotoxicology. 2017;61:143–87.CrossRefPubMed
29.
Heymann D, Stern Y, Cosentino S, Tatarina-Nulman O, Dorrejo JN, Gu Y. The association between alcohol use and the progression of Alzheimer’s disease. Curr Alzheimer Res. 2016;13:1356–62.CrossRefPubMedPubMedCentral
30.
31.
Luchsinger JA, Tang MX, Siddiqui M, Shea S, Mayeux R. Alcohol intake and risk of dementia. J Am Geriatr Soc. 2004;52:540–6.CrossRefPubMed
32.
Gabr AA, Lee HJ, Onphachanh X, Jung YH, Kim JS, Chae CW, Han HJ. Ethanol-induced PGE2 up-regulates Abeta production through PKA/CREB signaling pathway. Biochim Biophys Acta. 1863;2017:2942–53.
33.
34.
Kim SR, Jeong HY, Yang S, Choi SP, Seo MY, Yun YK, Choi Y, Baik SH, Park JS, Gwon AR, et al. Effects of chronic alcohol consumption on expression levels of APP and Abeta-producing enzymes. BMB Rep. 2011;44:135–9.CrossRefPubMed
35.
Karavitis J, Kovacs EJ. Macrophage phagocytosis: effects of environmental pollutants, alcohol, cigarette smoke, and other external factors. J Leukoc Biol. 2011;90:1065–78.CrossRefPubMedPubMedCentral
36.
Karavitis J, Murdoch EL, Deburghgraeve C, Ramirez L, Kovacs EJ. Ethanol suppresses phagosomal adhesion maturation, Rac activation, and subsequent actin polymerization during FcgammaR-mediated phagocytosis. Cell Immunol. 2012;274:61–71.CrossRefPubMedPubMedCentral
37.
Madrigal JL, Feinstein DL, Dello Russo C. Norepinephrine protects cortical neurons against microglial-induced cell death. J Neurosci Res. 2005;81:390–6.CrossRefPubMed
38.
Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29:15–21.CrossRefPubMed
39.
40.
Chen Z, Liu J, Ng HK, Nadarajah S, Kaufman HL, Yang JY, Deng Y. Statistical methods on detecting differentially expressed genes for RNA-seq data. BMC Syst Biol. 2011;5(Suppl 3):S1.CrossRefPubMedPubMedCentral
41.
Huang DW, Sherman BT, Tan Q, Collins JR, Alvord WG, Roayaei J, Stephens R, Baseler MW, Lane HC, Lempicki RA. The DAVID Gene Functional Classification Tool: a novel biological module-centric algorithm to functionally analyze large gene lists. Genome Biol. 2007;8:R183.CrossRefPubMedPubMedCentral
42.
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000;25:25–9.CrossRefPubMedPubMedCentral
43.
The Gene Ontology Consortium. Expansion of the Gene Ontology knowledgebase and resources. Nucleic Acids Res. 2017;45:D331–d338.CrossRef
44.
Lovinger DM, Crabbe JC. Laboratory models of alcoholism: treatment target identification and insight into mechanisms. Nat Neurosci. 2005;8:1471–80.CrossRefPubMed
45.
Kimpel MW, Strother WN, McClintick JN, Carr LG, Liang T, Edenberg HJ, McBride WJ. Functional gene expression differences between inbred alcohol-preferring and -non-preferring rats in five brain regions. Alcohol. 2007;41:95–132.CrossRefPubMedPubMedCentral
46.
Tabakoff B, Saba L, Kechris K, Hu W, Bhave SV, Finn DA, Grahame NJ, Hoffman PL. The genomic determinants of alcohol preference in mice. Mamm Genome. 2008;19:352–65.CrossRefPubMedPubMedCentral
47.
Saba LM, Flink SC, Vanderlinden LA, Israel Y, Tampier L, Colombo G, Kiianmaa K, Bell RL, Printz MP, Flodman P, et al. The sequenced rat brain transcriptome—its use in identifying networks predisposing alcohol consumption. FEBS J. 2015;282:3556–78.CrossRefPubMedPubMedCentral
48.
Carr LG, Kimpel MW, Liang T, McClintick JN, McCall K, Morse M, Edenberg HJ. Identification of candidate genes for alcohol preference by expression profiling of congenic rat strains. Alcohol Clin Exp Res. 2007;31:1089–98.CrossRefPubMedPubMedCentral
49.
Liu J, Lewohl JM, Harris RA, Iyer VR, Dodd PR, Randall PK, Mayfield RD. Patterns of gene expression in the frontal cortex discriminate alcoholic from nonalcoholic individuals. Neuropsychopharmacology. 2006;31:1574–82.CrossRefPubMed
50.
Mayfield RD, Lewohl JM, Dodd PR, Herlihy A, Liu J, Harris RA. Patterns of gene expression are altered in the frontal and motor cortices of human alcoholics. J Neurochem. 2002;81:802–13.CrossRefPubMed
51.
Lewohl JM, Wang L, Miles MF, Zhang L, Dodd PR, Harris RA. Gene expression in human alcoholism: microarray analysis of frontal cortex. Alcohol Clin Exp Res. 2000;24:1873–82.CrossRefPubMed
52.
Mamdani M, Williamson V, McMichael GO, Blevins T, Aliev F, Adkins A, Hack L, Bigdeli T, van der Vaart AD, Web BT, et al. Integrating mRNA and miRNA weighted gene co-expression networks with eQTLs in the nucleus accumbens of subjects with alcohol dependence. PLoS One. 2015;10:e0137671.CrossRefPubMedPubMedCentral
53.
Chan KT, Roadcap DW, Holoweckyj N, Bear JE. Coronin 1C harbours a second actin-binding site that confers co-operative binding to F-actin. Biochem J. 2012;444:89–96.CrossRefPubMed
54.
Jansen EJ, Martens GJ. Novel insights into V-ATPase functioning: distinct roles for its accessory subunits ATP6AP1/Ac45 and ATP6AP2/(pro) renin receptor. Curr Protein Pept Sci. 2012;13:124–33.CrossRefPubMed
55.
Serezani CH, Aronoff DM, Sitrin RG, Peters-Golden M. FcgammaRI ligation leads to a complex with BLT1 in lipid rafts that enhances rat lung macrophage antimicrobial functions. Blood. 2009;114:3316–24.CrossRefPubMedPubMedCentral
56.
57.
Montalbetti N, Simonin A, Kovacs G, Hediger MA. Mammalian iron transporters: families SLC11 and SLC40. Mol Asp Med. 2013;34:270–87.CrossRef
58.
Mao Y, Finnemann SC. Essential diurnal Rac1 activation during retinal phagocytosis requires alphavbeta5 integrin but not tyrosine kinases focal adhesion kinase or Mer tyrosine kinase. Mol Biol Cell. 2012;23:1104–14.CrossRefPubMedPubMedCentral
59.
60.
Alvey C, Discher DE. Engineering macrophages to eat cancer: from “marker of self” CD47 and phagocytosis to differentiation. J Leukoc Biol. 2017;102:31–40.CrossRefPubMedPubMedCentral
61.
62.
Daitoku S, Takenaka K, Yamauchi T, Yurino A, Jinnouchi F, Nunomura T, Eto T, Kamimura T, Higuchi M, Harada N, et al. Calreticulin mutation does not contribute to disease progression in essential thrombocythemia by inhibiting phagocytosis. Exp Hematol. 2016;44:817–825.e813.CrossRefPubMed
63.
Voss OH, Tian L, Murakami Y, Coligan JE, Krzewski K. Emerging role of CD300 receptors in regulating myeloid cell efferocytosis. Mol Cell Oncol. 2015;2:e964625.CrossRefPubMedPubMedCentral
64.
Couturier J, Stancu IC, Schakman O, Pierrot N, Huaux F, Kienlen-Campard P, Dewachter I, Octave JN. Activation of phagocytic activity in astrocytes by reduced expression of the inflammasome component ASC and its implication in a mouse model of Alzheimer disease. J Neuroinflammation. 2016;13:20.CrossRefPubMedPubMedCentral
65.
Smathers RL, Chiang DJ, McMullen MR, Feldstein AE, Roychowdhury S, Nagy LE. Soluble IgM links apoptosis to complement activation in early alcoholic liver disease in mice. Mol Immunol. 2016;72:9–18.CrossRefPubMedPubMedCentral
66.
Cohen JI, Roychowdhury S, McMullen MR, Stavitsky AB, Nagy LE. Complement and alcoholic liver disease: role of C1q in the pathogenesis of ethanol-induced liver injury in mice. Gastroenterology. 2010;139:664–74. 674.e661CrossRefPubMed
67.
Sebastian BM, Roychowdhury S, Tang H, Hillian AD, Feldstein AE, Stahl GL, Takahashi K, Nagy LE. Identification of a cytochrome P4502E1/Bid/C1q-dependent axis mediating inflammation in adipose tissue after chronic ethanol feeding to mice. J Biol Chem. 2011;286:35989–97.CrossRefPubMedPubMedCentral
68.
Bodea LG, Wang Y, Linnartz-Gerlach B, Kopatz J, Sinkkonen L, Musgrove R, Kaoma T, Muller A, Vallar L, Di Monte DA, et al. Neurodegeneration by activation of the microglial complement-phagosome pathway. J Neurosci. 2014;34:8546–56.CrossRefPubMedPubMedCentral
69.
Conway Morris A, Kefala K, Wilkinson TS, Dhaliwal K, Farrell L, Walsh T, Mackenzie SJ, Reid H, Davidson DJ, Haslett C, et al. C5a mediates peripheral blood neutrophil dysfunction in critically ill patients. Am J Respir Crit Care Med. 2009;180:19–28.CrossRefPubMed
70.
Morris MR, Doull IJ, Dewitt S, Hallett MB. Reduced iC3b-mediated phagocytotic capacity of pulmonary neutrophils in cystic fibrosis. Clin Exp Immunol. 2005;142:68–75.CrossRefPubMedPubMedCentral
71.
Czirr E, Castello NA, Mosher KI, Castellano JM, Hinkson IV, Lucin KM, Baeza-Raja B, Ryu JK, Li L, Farina SN, et al. Microglial complement receptor 3 regulates brain Abeta levels through secreted proteolytic activity. J Exp Med. 2017;214:1081–92.CrossRefPubMedPubMedCentral
72.
Fu H, Liu B, Frost JL, Hong S, Jin M, Ostaszewski B, Shankar GM, Costantino IM, Carroll MC, Mayadas TN, Lemere CA. Complement component C3 and complement receptor type 3 contribute to the phagocytosis and clearance of fibrillar Abeta by microglia. Glia. 2012;60:993–1003.CrossRefPubMedPubMedCentral
73.
Hong S, Beja-Glasser VF, Nfonoyim BM, Frouin A, Li S, Ramakrishnan S, Merry KM, Shi Q, Rosenthal A, Barres BA, et al. Complement and microglia mediate early synapse loss in Alzheimer mouse models. Science. 2016;352:712–6.CrossRefPubMedPubMedCentral
74.
Choucair-Jaafar N, Laporte V, Levy R, Poindron P, Lombard Y, Gies JP. Complement receptor 3 (CD11b/CD18) is implicated in the elimination of beta-amyloid peptides. Fundam Clin Pharmacol. 2011;25:115–22.CrossRefPubMed
75.
Morland B, Morland J. Reduced Fc-receptor function in human monocytes exposed to ethanol in vitro. Alcohol Alcohol. 1984;19:211–7.PubMed
76.
Zuiable A, Wiener E, Wickramasinghe SN. In vitro effects of ethanol on the phagocytic and microbial killing activities of normal human monocytes and monocyte-derived macrophages. Clin Lab Haematol. 1992;14:137–47.CrossRefPubMed
77.
Saito M, Chakraborty G, Hui M, Masiello K, Saito M. Ethanol-induced neurodegeneration and glial activation in the developing brain. Brain Sci. 2016;6:31.
78.
Ahlers KE, Karacay B, Fuller L, Bonthius DJ, Dailey ME. Transient activation of microglia following acute alcohol exposure in developing mouse neocortex is primarily driven by BAX-dependent neurodegeneration. Glia. 2015;63:1694–713.CrossRefPubMedPubMedCentral
79.
80.
Gaikwad S, Larionov S, Wang Y, Dannenberg H, Matozaki T, Monsonego A, Thal DR, Neumann H. Signal regulatory protein-beta1: a microglial modulator of phagocytosis in Alzheimer's disease. Am J Pathol. 2009;175:2528–39.CrossRefPubMedPubMedCentral
81.
Paradisi S, Matteucci A, Fabrizi C, Denti MA, Abeti R, Breit SN, Malchiodi-Albedi F, Mazzanti M. Blockade of chloride intracellular ion channel 1 stimulates Abeta phagocytosis. J Neurosci Res. 2008;86:2488–98.CrossRefPubMed
82.
Kok EH, Karppinen TT, Luoto T, Alafuzoff I, Karhunen PJ. Beer drinking associates with lower burden of amyloid beta aggregation in the brain: Helsinki sudden death series. Alcohol Clin Exp Res. 2016;40:1473–8.CrossRefPubMed
83.
Weyerer S, Schaufele M, Wiese B, Maier W, Tebarth F, van den Bussche H, Pentzek M, Bickel H, Luppa M, Riedel-Heller SG. Current alcohol consumption and its relationship to incident dementia: results from a 3-year follow-up study among primary care attenders aged 75 years and older. Age Ageing. 2011;40:456–63.CrossRefPubMed
84.
Venkataraman A, Kalk N, Sewell G, Ritchie CW, Lingford-Hughes A. Alcohol and Alzheimer’s disease-does alcohol dependence contribute to beta-amyloid deposition, neuroinflammation and neurodegeneration in Alzheimer’s disease? Alcohol Alcohol. 2017;52:151–8.PubMed
85.
Piazza-Gardner AK, Gaffud TJ, Barry AE. The impact of alcohol on Alzheimer’s disease: a systematic review. Aging Ment Health. 2013;17:133–46.CrossRefPubMed
86.
Munoz G, Urrutia JC, Burgos CF, Silva V, Aguilar F, Sama M, Yeh HH, Opazo C, Aguayo LG. Low concentrations of ethanol protect against synaptotoxicity induced by Abeta in hippocampal neurons. Neurobiol Aging. 2015;36:845–56.CrossRefPubMed
87.
Ehrlich D, Pirchl M, Humpel C. Effects of long-term moderate ethanol and cholesterol on cognition, cholinergic neurons, inflammation, and vascular impairment in rats. Neuroscience. 2012;205:154–66.CrossRefPubMed
Metadata
Title
Transcriptome analysis of alcohol-treated microglia reveals downregulation of beta amyloid phagocytosis
Authors
Sergey Kalinin
Marta González-Prieto
Hannah Scheiblich
Lucia Lisi
Handojo Kusumo
Michael T. Heneka
Jose L. M. Madrigal
Subhash C. Pandey
Douglas L. Feinstein
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Journal of Neuroinflammation / Issue 1/2018
Electronic ISSN: 1742-2094
DOI
https://doi.org/10.1186/s12974-018-1184-7

Other articles of this Issue 1/2018

Journal of Neuroinflammation 1/2018 Go to the issue

Research

MicroRNA-124 regulates the expression of MEKK3 in the inflammatory pathogenesis of Parkinson’s disease

Research

Unveiling anti-oxidative and anti-inflammatory effects of docosahexaenoic acid and its lipid peroxidation product on lipopolysaccharide-stimulated BV-2 microglial cells

Research

Counteracting neuroinflammation in experimental Parkinson’s disease favors recovery of function: effects of Er-NPCs administration

Research

α1-antitrypsin mitigates NLRP3-inflammasome activation in amyloid β1–42-stimulated murine astrocytes

Research

Monocyte infiltration rather than microglia proliferation dominates the early immune response to rapid photoreceptor degeneration

Research

Neuroinflammation is increased in the parietal cortex of atypical Alzheimer’s disease