Chronic ethanol increases systemic TLR3 agonist-induced neuroinflammation and neurodegeneration

Journal of Neuroinflammation

Volumn 9, Issue 1, 2012, Pages

  Qin, Liya ^a   Crews, Fulton T ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Alcohol; NADPH oxidase; Neurodegeneration; Oxidative stress; Toll like receptor 3

Indexed keywords

ALCOHOL; CASPASE 3; CELL MARKER; CYTOKINE; HIGH MOBILITY GROUP B1 PROTEIN; HYDROETHIDINE; INTERLEUKIN 1BETA; INTERLEUKIN 6; MINOCYCLINE; MONOCYTE CHEMOTACTIC PROTEIN 1; NALTREXONE; POLYINOSINIC POLYCYTIDYLIC ACID; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; TOLL LIKE RECEPTOR 3; TUMOR NECROSIS FACTOR; AUTACOID; BIOLOGICAL MARKER; TLR3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; CELL STRUCTURE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; HISTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MALE; MICROGLIA; MOUSE; NERVE DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED DISORDER; DEGENERATIVE DISEASE; DRUG ADMINISTRATION; DRUG EFFECT; DRUG POTENTIATION; INFLAMMATION; METABOLISM; PATHOLOGY; PHYSIOLOGY; UPREGULATION;

ANIMALS; BIOLOGICAL MARKERS; DRUG ADMINISTRATION SCHEDULE; DRUG SYNERGISM; ETHANOL; INFLAMMATION; INFLAMMATION MEDIATORS; MALE; MICE; MICE, INBRED C57BL; NEURODEGENERATIVE DISEASES; POLY I-C; TOLL-LIKE RECEPTOR 3; UP-REGULATION;

EID: 84862255818     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-9-130     Document Type: Article

References (63)

1. Qin L, Wu X, Block ML, Liu Y, Breese GR, Hong JS, Knapp DJ, Crews FT: Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 2007, 55:453-462
2. Liu Y, Qin L, Wilson B, Wu X, Qian L, Granholm AC, Crews FT, Hong JS: Endotoxin induces a delayed loss of TH-IR neurons in substantia nigra and motor behavioral deficits. Neurotoxicology 2008, 29:864-870
3. Crews FT, Zou J, Qin L: Induction of innate immune genes in brain create the neurobiology of addiction. Brain Behav Immun 2011, Suppl 1:S4-S12
4. Jiang W, Sun R, Wei H, Tian Z: Toll-like receptor 3 ligand attenuates LPSinduced liver injury by down-regulation of toll-like receptor 4 expression on macrophages. Proc Natl Acad Sci USA 2005, 102:17077-17082
5. Finch CE, Morgan TE: Systemic inflammation, infection, ApoE alleles, and Alzheimer disease: a position paper. Curr Alzheimer Res 2007, 4:185-189
6. Block ML, Zecca L, Hong JS: Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci 2007, 8:57-69
7. Doyle SE, O'Connell R, Vaidya SA, Chow EK, Yee K, Cheng G: Toll-like receptor 3 mediates a more potent antiviral response than Toll-like receptor 4. J Immunol 2003, 170:3565-3571
8. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA: Recognition of doublestranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 2001, 413:732-738
9. Olson JK, Miller SD: Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J Immunol 2004, 173:3916-3924
10. Re F, Strominger JL: IL-10 released by concomitant TLR2 stimulation blocks the induction of a subset of Th1 cytokines that are specifically induced by TLR4 or TLR3 in human dendritic cells. J Immunol 2004, 173:7548-7555
11. Sivori S, Falco M, Della Chiesa M, Carlomagno S, Vitale M, Moretta L, Moretta A: CpG and double-stranded RNA trigger human NK cells by Toll-like receptors: induction of cytokine release and cytotoxicity against tumors and dendritic cells. Proc Natl Acad Sci U S A 2004, 101:10116-10121
12. Scumpia PO, Kelly KM, Reeves WH, Stevens BR: Double-stranded RNA signals antiviral and inflammatory programs and dysfunctional glutamate transport in TLR3-expressing astrocytes. Glia 2005, 52:153-162
13. Chen CJ, Chen JH, Chen SY, Liao SL, Raung SL: Upregulation of RANTES gene expression in neuroglia by Japanese encephalitis virus infection. J Virol 2004, 78:12107-12119
14. Kielian T: Microglia and chemokines in infectious diseases of the nervous system: views and reviews. Front Biosci 2004, 9:732-750
15. Guha-Thakurta N, Majde JA: Early induction of proinflammatory cytokine and type I interferon mRNAs following Newcastle disease virus, poly [rI: rC], or low-dose LPS challenge of the mouse. J Interferon Cytokine Res 1997, 17:197-204
16. Schulz O, Diebold SS, Chen M, Naslund TI, Nolte MA, Alexopoulou L, Azuma YT, Flavell RA, Liljestrom P, Reis e Sousa C: Toll-like receptor 3 promotes cross-priming to virus-infected cells. Nature 2005, 433:887-892
17. Park C, Lee S, Cho IH, Lee HK, Kim D, Choi SY, Oh SB, Park K, Kim JS, Lee SJ: TLR3-mediated signal induces proinflammatory cytokine and chemokine gene expression in astrocytes: differential signaling mechanisms of TLR3-induced IP-10 and IL-8 gene expression. Glia 2006, 53:248-256
18. Carty M, Bowie AG: Evaluating the role of Toll-like receptors in diseases of the central nervous system. Biochem Pharmacol 2011, 81:825-837
19. Bsibsi M, Ravid R, Gveric D, van Noort JM: Broad expression of Toll-like receptors in the human central nervous system. J Neuropathol Exp Neurol 2002, 61:1013-1021
20. Crews FT, Nixon K: Mechanisms of neurodegeneration and regeneration in alcoholism. Alcohol Alcohol 2009, 44:115-127
21. Harper C: The neuropathology of alcohol-related brain damage. Alcohol Alcohol 2009, 44:136-140
22. Yanai H, Ban T, Wang Z, Choi MK, Kawamura T, Negishi H, Nakasato M, Lu Y, Hangai S, Koshiba R, Savitsky D, Ronfani L, Akira S, Bianchi ME, Honda K, Tamura T, Kodama T, Taniguchi T: HMGB proteins function as universal sentinels for nucleic-acid-mediated innate immune responses. Nature 2009, 462:99-103
23. Carpentier PA, Begolka WS, Olson JK, Elhofy A, Karpus WJ, Miller SD: Differential activation of astrocytes by innate and adaptive immune stimuli. Glia 2005, 49:360-374
24. Nelson S, Kolls JK: Alcohol, host defence and society. Nat Rev Immunol 2002, 2:205-209
25. He J, Crews FT: Increased MCP-1 and microglia in various regions of the human alcoholic brain. Exp Neurol 2008, 210:349-358
26. Qin L, Crews FT: NADPH oxidase and reactive oxygen species contribute to alcohol-induced microglial activation and neurodegeneration. J Neuroinflammation 2012, 9:5
27. Qin L, He J, Hanes RN, Pluzarev O, Hong JS, Crews FT: Increased systemic and brain cytokine production and neuroinflammation by endotoxin following ethanol treatment. J Neuroinflammation 2008, 5:10
28. Pruett SB, Fan R, Zheng Q: Acute ethanol administration profoundly alters poly I:C-induced cytokine expression in mice by a mechanism that is not dependent on corticosterone. Life Sci 2003, 72:1825-1839
29. Mandrekar P, Catalano D, Szabo G: Inhibition of lipopolysaccharidemediated NFkappaB activation by ethanol in human monocytes. Int Immunol 1999, 11:1781-1790
30. 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, 30:8285-8295
31. Qin L, Liu Y, Wang T, Wei SJ, Block ML, Wilson B, Liu B, Hong JS: NADPH oxidase mediates lipopolysaccharide-induced neurotoxicity and proinflammatory gene expression in activated microglia. J Biol Chem 2004, 279:1415-1421
32. Bindokas VP, Jordan J, Lee CC, Miller RJ: Superoxide production in rat hippocampal neurons: selective imaging with hydroethidine. J Neurosci 1996, 16:1324-1336
33. Wu DC, Teismann P, Tieu K, Vila M, Jackson-Lewis V, Ischiropoulos H, Przedborski S: NADPH oxidase mediates oxidative stress in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson's disease. Proc Natl Acad Sci USA 2003, 100:6145-6150
34. Crews FT, Nixon K, Wilkie ME: Exercise reverses ethanol inhibition of neural stem cell proliferation. Alcohol 2004, 33:63-71
35. McClain JA, Morris SA, Deeny MA, Marshall SA, Hayes DM, Kiser ZM, Nixon K: Adolescent binge alcohol exposure induces long-lasting partial activation of microglia. Brain Behav Immun 2011, Suppl 1:S120-S128
36. Chen WJ, Parnell SE, West JR: Neonatal alcohol and nicotine exposure limits brain growth and depletes cerebellar Purkinje cells. Alcohol 1998, 15:33-41
37. Gundersen HJ, Bendtsen TF, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sorensen FB, Vesterby A, West MJ: Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 1988, 96:379-394
38. West MJ, Gundersen HJ: Unbiased stereological estimation of the number of neurons in the human hippocampus. J Comp Neurol 1990, 296:1-22
39. Gu L, Okada Y, Clinton SK, Gerard C, Sukhova GK, Libby P, Rollins BJ: Absence of monocyte chemoattractant protein-1 reduces atherosclerosis in low density lipoprotein receptor-deficient mice. Mol Cell 1998, 2:275-281
40. Glass CK, Saijo K, Winner B, Marchetto MC, Gage FH: Mechanisms underlying inflammation in neurodegeneration. Cell 2010, 140:918-934
41. Tang SC, Arumugam TV, Xu X, Cheng A, Mughal MR, Jo DG, Lathia JD, Siler DA, Chigurupati S, Ouyang X, Magnus T, Camandola S, Mattson MP: Pivotal role for neuronal Toll-like receptors in ischemic brain injury and functional deficits. Proc Natl Acad Sci USA 2007, 104:13798-13803
42. Garg AD, Nowis D, Golab J, Vandenabeele P, Krysko DV, Agostinis P: Immunogenic cell death, DAMPs and anticancer therapeutics: an emerging amalgamation. Biochim Biophys Acta 2010, 1805:53-71
43. Plane JM, Shen Y, Pleasure DE, Deng W: Prospects for minocycline neuroprotection. Arch Neurol 2010, 67:1442-1448
44. Hutchinson MR, Shavit Y, Grace PM, Rice KC, Maier SF, Watkins LR: Exploring the neuroimmunopharmacology of opioids: an integrative review of mechanisms of central immune signaling and their implications for opioid analgesia. Pharmacol Rev 2011, 63:772-810
45. Hutchinson MR, Zhang Y, Brown K, Coats BD, Shridhar M, Sholar PW, Patel SJ, Crysdale NY, Harrison JA, Maier SF, Rice KC, Watkins LR: Nonstereoselective reversal of neuropathic pain by naloxone and naltrexone: involvement of toll-like receptor 4 (TLR4). Eur J Neurosci 2008, 28:20-29
46. Dejager L, Libert C: Tumor necrosis factor alpha mediates the lethal hepatotoxic effects of poly(I:C) in D-galactosamine-sensitized mice. Cytokine 2008, 42:55-61
47. Sims GP, Rowe DC, Rietdijk ST, Herbst R, Coyle AJ: HMGB1 and RAGE in inflammation and cancer. Annu Rev Immunol 2010, 28:367-388
48. Huang W, Tang Y, Li L: HMGB1, a potent proinflammatory cytokine in sepsis. Cytokine 2010, 51:119-126
49. Banks WA, Erickson MA: The blood-brain barrier and immune function and dysfunction. Neurobiol Dis 2010, 37:26-32
50. Zou J, Crews F: Induction of innate immune gene expression cascades in brain slice cultures by ethanol: key role of NF-kappaB and proinflammatory cytokines. Alcohol Clin Exp Res 2010, 34:777-789
51. Nguyen MD, Julien JP, Rivest S: Innate immunity: the missing link in neuroprotection and neurodegeneration? Nat Rev Neurosci 2002, 3:216-227
52. Maroso M, Balosso S, Ravizza T, Liu J, Aronica E, Iyer AM, Rossetti C, Molteni M, Casalgrandi M, Manfredi AA, Bianchi ME, Vezzani A: Toll-like receptor 4 and high-mobility group box-1 are involved in ictogenesis and can be targeted to reduce seizures. Nat Med 2010, 16:413-419
53. Zou J, Crews F: CREB and NF-kappaB transcription factors regulate sensitivity to excitotoxic and oxidative stress induced neuronal cell death. Cell Mol Neurobiol 2006, 26:385-405
54. 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, 175:6893-6899
55. Fernandez-Lizarbe S, Pascual M, Guerri C: Critical role of TLR4 response in the activation of microglia induced by ethanol. J Immunol 2009, 183:4733-4744
56. 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, 31:1574-1582
57. Blednov YA, Benavidez JM, Geil C, Perra S, Morikawa H, Harris RA: Activation of inflammatory signaling by lipopolysaccharide produces a prolonged increase of voluntary alcohol intake in mice. Brain Behav Immun 2011, Suppl 1:S92-S105
58. Blednov YA, Ponomarev I, Geil C, Bergeson S, Koob GF, Harris RA: Neuroimmune regulation of alcohol consumption: behavioral validation of genes obtained from genomic studies. Addict Biol 2012, 1:108-120
59. 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, Suppl 1:S155-S164
60. Liu J, Yang AR, Kelly T, Puche A, Esoga C, June HL Jr, Elnabawi A, Merchenthaler I, Sieghart W, Sr June HL, Aurelian L: Binge alcohol drinking is associated with GABAA alpha2-regulated Toll-like receptor 4 (TLR4) expression in the central amygdala. Proc Natl Acad Sci U SA 2011, 108:4465-4470
61. Wang Q, Zhou H, Gao H, Chen SH, Chu CH, Wilson B, Hong JS: Naloxone inhibits immune cell function by suppressing superoxide production through a direct interaction with gp91phox subunit of NADPH oxidase. J Neuroinflammation 2012, 9:32
62. Garbutt JC: Efficacy and tolerability of naltrexone in the management of alcohol dependence. Curr Pharm Des 2010, 16:2091-2097
63. Agrawal RG, Hewetson A, George CM, Syapin PJ, Bergeson SE: Minocycline reduces ethanol drinking. Brain Behav Immun 2011, Suppl 1:S165-S169