Critical role of TLR4 response in the activation of microglia induced by ethanol

Journal of Immunology

Volumn 183, Issue 7, 2009, Pages 4733-4744

  Fernandez Lizarbe, Sara ^a   Pascual, Maria ^a   Guerri, Consuelo ^a  

^a CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; BETA INTERFERON; CD11B ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; MITOGEN ACTIVATED PROTEIN KINASE; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 4; AUTACOID; TLR4 PROTEIN, MOUSE; TLR4 PROTEIN, RAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL ACTIVATION; CYTOKINE PRODUCTION; ENCEPHALITIS; FEMALE; IN VITRO STUDY; INFLAMMATION; MICROGLIA; MOUSE; NERVE CELL NECROSIS; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL DEATH; DRUG EFFECT; GENETICS; IMMUNOLOGY; INTRAPERITONEAL DRUG ADMINISTRATION; METABOLISM; MOUSE MUTANT; NERVE CELL; PHYSIOLOGY; WISTAR RAT;

ANIMALS; ANIMALS, NEWBORN; CELL DEATH; CELLS, CULTURED; ETHANOL; FEMALE; INFLAMMATION MEDIATORS; INJECTIONS, INTRAPERITONEAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROGLIA; NEURONS; RATS; RATS, WISTAR; TOLL-LIKE RECEPTOR 4;

EID: 70449732755     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0803590     Document Type: Article

References (69)

1. Streit, W. J., R. E. Mrak, and W. S. Griffin. 2004. Microglia and neuroinflammation: a pathological perspective. J. Neuroinflammation. 1: 14.
2. Kreutzberg, G. W. 1996. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 19: 312-318.
3. Nakajima, K., and S. Kohsaka. 2001. Microglia: activation and their significance in the central nervous system. J. Biochem. 130: 169-175.
4. Bjorkqvist, M., E. J. Wild, J. Thiele, A. Silvestroni, R. Andre, N. Lahiri, E. Raibon, R. V. Lee, C. L. Benn, D. Soulet, et al. 2008. A novel pathogenic pathway of immune activation detectable before clinical onset in Huntington's disease. J. Exp. Med. 205: 1869-1877.
5. Lopes, K. O., D. L. Sparks, and W. J. Streit. 2008. Microglial dystrophy in the aged and Alzheimer's disease brain is associated with ferritin immunoreactivity. Glia 56: 1048-1060.
6. Aravalli, R. N., P. K. Peterson, and J. R. Lokensgard. 2007. Toll-like receptors in defense and damage of the central nervous system. J. Neuroimmune Pharmacol. 2: 297-312.
7. Block, M. L., L. Zecca, and J. S. Hong. 2007. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat. Rev. Neurosci. 8: 57-69.
8. Garantziotis, S., J. W. Hollingsworth, A. K. Zaas, and D. A. Schwartz. 2008. The effect of Toll-like receptors and Toll-like receptor genetics in human disease. Annu. Rev. Med. 59: 343-359. (Pubitemid 351287942)
9. Carpentier, P. A., D. S. Duncan, and S. D. Miller. 2008. Glial Toll-like receptor signaling in central nervous system infection and autoimmunity. Brain Behav. Immun. 22: 140-147.
10. Lehnardt, S., C. Lachance, S. Patrizi, S. Lefebvre, P. L. Follett, F. E. Jensen, P. A. Rosenberg, J. J. Volpe, and T. Vartanian. 2002. The Toll-like receptor TLR4 is necessary for lipopolysaccharide-induced oligodendrocyte injury in the CNS. J. Neurosci. 22: 2478-2486.
11. Lehnardt, S., L. Massillon, P. Follett, F. E. Jensen, R. Ratan, P. A. Rosenberg, J. J. Volpe, and T. Vartanian. 2003. Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway. Proc. Natl. Acad. Sci. USA 100: 8514-8519.
12. Liu, B., K. Wang, H. M. Gao, B. Mandavilli, J. Y. Wang, and J. S. Hong. 2001. Molecular consequences of activated microglia in the brain: overactivation induces apoptosis. J. Neurochem. 77: 182-189. (Pubitemid 32245092)
13. Jung, D. Y., H. Lee, B. Y. Jung, J. Ock, M. S. Lee, W. H. Lee, and K. Suk. 2005. TLR4, but not TLR2, signals autoregulatory apoptosis of cultured microglia: a critical role of IFN-β as a decision maker. J. Immunol. 174: 6467-6476.
14. Takeda, K., T. Kaisho, and S. Akira. 2003. Toll-like receptors. Annu. Rev. Immunol. 21: 335-376.
15. O'Neill, L. A. 2003. The role of MyD88-like adapters in Toll-like receptor signal transduction. Biochem. Soc. Trans. 31: 643-647.
16. Toshchakov, V., B. W. Jones, P. Y. Perera, K. Thomas, M. J. Cody, S. Zhang, B. R. Williams, J. Major, T. A. Hamilton, M. J. Fenton, and S. N. Vogel. 2002. TLR4, but not TLR2, mediates IFN-β-induced STAT1α/β- dependent gene expression in macrophages. Nat. Immunol. 3: 392-398.
17. Campbell, A. 2004. Inflammation, neurodegenerative diseases, and environmental exposures. Ann. NY Acad. Sci. 1035: 117-132. (Pubitemid 40362330)
18. de la Monte, S. M. 1988. Disproportionate atrophy of cerebral white matter in chronic alcoholics. Arch. Neurol. 45: 990-992.
19. Harper, C., and I. Matsumoto. 2005. Ethanol and brain damage. Curr. Opin. Pharmacol. 5: 73-78.
20. Pfefferbaum, A. 2004. Alcoholism damages the brain, but does moderate alcohol use? Lancet Neurol. 3: 143-144. (Pubitemid 38229946)
21. Valles, S. L., A. M. Blanco, M. Pascual, and C. Guerri. 2004. Chronic ethanol treatment enhances inflammatory mediators and cell death in the brain and in astrocytes. Brain Pathol. 14: 365-371.
22. Blanco, A. M., and C. Guerri. 2007. Ethanol intake enhances inflammatory mediators in brain: role of glial cells and TLR4/IL-1RI receptors. Front. Biosci. 12: 2616-2630.
23. Blanco, A. M., S. L. Valles, M. Pascual, and C. Guerri. 2005. 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. 175: 6893-6899.
24. Fernandez-Lizarbe, S., M. Pascual, M. S. Gascon, A. Blanco, and C. Guerri. 2008. Lipid rafts regulate ethanol-induced activation of TLR4 signaling in murine macrophages. Mol. Immunol. 45: 2007-2016. (Pubitemid 351226271)
25. Giulian, D., and T. J. Baker. 1986. Characterization of ameboid microglia isolated from developing mammalian brain. J. Neurosci. 6: 2163-2178. (Pubitemid 16043659)
26. Saura, J., J. M. Tusell, and J. Serratosa. 2003. High-yield isolation of murine microglia by mild trypsinization. Glia 44: 183-189. (Pubitemid 37484470)
27. Jones, A. W., and B. Sternebring. 1992. Kinetics of ethanol and methanol in alcoholics during detoxification. Alcohol Alcohol. 27: 641-647.
28. Adachi, J., Y. Mizoi, T. Fukunaga, Y. Ogawa, Y. Ueno, and H. Imamichi. 1991. Degrees of alcohol intoxication in 117 hospitalized cases. J. Stud. Alcohol. 52: 448-453.
29. Weinstein, J. R., S. Swarts, C. Bishop, U. K. Hanisch, and T. Moller. 2008. Lipopolysaccharide is a frequent and significant contaminant in microglia-activating factors. Glia 56: 16-26.
30. Lin, C. H., I. H. Kuan, C. H. Wang, H. M. Lee, W. S. Lee, J. R. Sheu, G. Hsiao, C. H. Wu, and H. P. Kuo. 2002. Lipoteichoic acid-induced cyclooxygenase-2 expression requires activations of p44/42 and p38 mitogen-activated protein kinase signal pathways. Eur. J. Pharmacol. 450: 1-9.
31. Pascual, M., and C. Guerri. 2007. The peptide NAP promotes neuronal growth and differentiation through extracellular signal-regulated protein kinase and Akt pathways, and protects neurons co-cultured with astrocytes damaged by ethanol. J. Neurochem. 103: 557-568.
32. Ishida, N., T. Hara, T. Kamura, M. Yoshida, K. Nakayama, and K. I. Nakayama. 2002. Phosphorylation of p27Kip1 on serine 10 is required for its binding to CRM1 and nuclear export. J. Biol. Chem. 277: 14355-14358.
33. Pan, X. D., X. C. Chen, Y. G. Zhu, J. Zhang, T. W. Huang, L. M. Chen, Q. Y. Ye, and H. P. Huang. 2008. Neuroprotective role of tripchlorolide on inflammatory neurotoxicity induced by lipopolysaccharide-activated microglia. Biochem. Pharmacol. 76: 362-372.
34. Meng, X. L., J. Y. Yang, G. L. Chen, L. J. Zhang, L. H. Wang, J. Li, J. M. Wang, and C. F. Wu. 2008. RV09, a novel resveratrol analogue, inhibits NO and TNF-α production by LPS-activated microglia. Int. Immunopharmacol. 8: 1074-1082.
35. Akira, S., and S. Sato. 2003. Toll-like receptors and their signaling mechanisms. Scand. J. Infect. Dis. 35: 555-562.
36. Grunblatt, E., S. Mandel, and M. B. Youdim. 2000. Neuroprotective strategies in Parkinson's disease using the models of 6-hydroxydopamine and MPTP. Ann. NY Acad. Sci. 899: 262-273. (Pubitemid 30352792)
37. Park, K. W., H. G. Lee, B. K. Jin, and Y. B. Lee. 2007. Interleukin-10 endogenously expressed in microglia prevents lipopolysaccharide-induced neurodegeneration in the rat cerebral cortex in vivo. Exp. Mol. Med. 39: 812-819.
38. Takeda, K., and S. Akira. 2005. Toll-like receptors in innate immunity. Int. Immunol. 17: 1-14.
39. Barnes, B., B. Lubyova, and P. M. Pitha. 2002. On the role of IRF in host defense. J. Interferon Cytokine Res. 22: 59-71.
40. O'Neill, L. A., and A. G. Bowie. 2007. The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat. Rev. Immunol. 7: 353-364.
41. Servant, M. J., B. ten Oever, C. LePage, L. Conti, S. Gessani, I. Julkunen, R. Lin, and J. Hiscott. 2001. Identification of distinct signaling pathways leading to the phosphorylation of interferon regulatory factor 3. J. Biol. Chem. 276: 355-363.
42. Blanco, A. M., A. Perez-Arago, S. Fernandez-Lizarbe, and C. Guerri. 2008. Ethanol mimics ligand-mediated activation and endocytosis of IL-1RI/TLR4 receptors via lipid rafts caveolae in astroglial cells. J. Neurochem. 106: 625-639.
43. Pais, T. F., C. Figueiredo, R. Peixoto, M. H. Braz, and S. Chatterjee. 2008. Necrotic neurons enhance microglial neurotoxicity through induction of glutaminase by a MyD88-dependent pathway. J. Neuroinflammation 5: 43.
44. Gurley, C., J. Nichols, S. Liu, N. K. Phulwani, N. Esen, and T. Kielian. 2008. Microglia and astrocyte activation by Toll-like receptor ligands: modulation by PPAR-γ agonists. PPAR Res. 2008: 453120.
45. Jin, J. J., H. D. Kim, J. A. Maxwell, L. Li, and K. Fukuchi. 2008. Toll-like receptor 4-dependent upregulation of cytokines in a transgenic mouse model of Alzheimer's disease. J. Neuroinflammation 5: 23.
46. Liu, B., and J. S. Hong. 2003. Role of microglia in inflammation-mediated neurodegenerative diseases: mechanisms and strategies for therapeutic intervention. J. Pharmacol. Exp. Ther. 304: 1-7.
47. Dheen, S. T., C. Kaur, and E. A. Ling. 2007. Microglial activation and its implications in the brain diseases. Curr. Med. Chem. 14: 1189-1197.
48. Kloss, C. U., M. Bohatschek, G. W. Kreutzberg, and G. Raivich. 2001. Effect of lipopolysaccharide on the morphology and integrin immunoreactivity of ramified microglia in the mouse brain and in cell culture. Exp. Neurol. 168: 32-46.
49. Probert, L., and K. Akassoglou. 2001. Glial expression of tumor necrosis factor in transgenic animals: how do these models reflect the "normal situation"? Glia 36: 212-219.
50. Sriram, K., J. M. Matheson, S. A. Benkovic, D. B. Miller, M. I. Luster, and J. P. O'Callaghan. 2006. Deficiency of TNF receptors suppresses microglial activation and alters the susceptibility of brain regions to MPTP-induced neurotoxicity: role of TNF-α. FASEB J. 20: 670-682.
51. Boje, K. M., and P. K. Arora. 1992. Microglial-produced nitric oxide and reactive nitrogen oxides mediate neuronal cell death. Brain Res. 587: 250-256.
52. Chao, C. C., S. Hu, T. W. Molitor, E. G. Shaskan, and P. K. Peterson. 1992. Activated microglia mediate neuronal cell injury via a nitric oxide mechanism. J. Immunol. 149: 2736-2741.
53. Qin, L., J. He, R. N. Hanes, O. Pluzarev, J. S. Hong, and F. T. Crews. 2008. Increased systemic and brain cytokine production and neuroinflammation by endotoxin following ethanol treatment. J. Neuroinflammation 5: 10.
54. He, J., and F. T. Crews. 2008. Increased MCP-1 and microglia in various regions of the human alcoholic brain. Exp. Neurol. 210: 349-358.
55. Kawai, T., O. Takeuchi, T. Fujita, J. Inoue, P. F. Muhlradt, S. Sato, K. Hoshino, and S. Akira. 2001. Lipopolysaccharide stimulates the MyD88-independent pathway and results in activation of IFN-regulatory factor 3 and the expression of a subset of lipopolysaccharide-inducible genes. J. Immunol. 167: 5887-5894.
56. Takeda, K., and S. Akira. 2004. TLR signaling pathways. Semin. Immunol. 16: 3-9.
57. Qin, H., C. A. Wilson, S. J. Lee, X. Zhao, and E. N. Benveniste. 2005. LPS induces CD40 gene expression through the activation of NF-κB and STAT-1α in macrophages and microglia. Blood 106: 3114-3122. (Pubitemid 41565908)
58. Lee, J., J. Hur, P. Lee, J. Y. Kim, N. Cho, S. Y. Kim, H. Kim, M. S. Lee, and K. Suk. 2001. Dual role of inflammatory stimuli in activation-induced cell death of mouse microglial cells: initiation of two separate apoptotic pathways via induction of interferon regulatory factor-1 and caspase-11. J. Biol. Chem. 276: 32956-32965.
59. Hritz, I., P. Mandrekar, A. Velayudham, D. Catalano, A. Dolganiuc, K. Kodys, E. Kurt-Jones, and G. Szabo. 2008. The critical role of Toll-like receptor (TLR) 4 in alcoholic liver disease is independent of the common TLR adapter MyD88. Hepatology 48: 1224-1231.
60. Uesugi, T., M. Froh, G. E. Arteel, B. U. Bradford, and R. G. Thurman. 2001. Toll-like receptor 4 is involved in the mechanism of early alcohol-induced liver injury in mice. Hepatology 34: 101-108. (Pubitemid 32591488)
61. Szabo, G., and P. Mandrekar. 2002. Ethanol-mediated regulation of transcription factors in immunocompetent cells. Front. Biosci. 7: a80-89.
62. Goral, J., and E. J. Kovacs. 2005. In vivo ethanol exposure down-regulates TLR2-, TLR4-, and TLR9-mediated macrophage inflammatory response by limiting p38 and ERK1/2 activation. J. Immunol. 174: 456-463. (Pubitemid 40007435)
63. Szabo, G. 1999. Consequences of alcohol consumption on host defence. Alcohol Alcohol. 34: 830-841. (Pubitemid 30042527)
64. Karavitis, J., E. L. Murdoch, C. R. Gomez, L. Ramirez, and E. J. Kovacs. 2008. Acute ethanol exposure attenuates pattern recognition receptor activated macrophage functions. J. Interferon Cytokine Res. 28: 413-422. (Pubitemid 351986399)
65. Zhang, Z., G. J. Bagby, D. Stoltz, P. Oliver, P. O. Schwarzenberger, and J. K. Kolls. 2001. Prolonged ethanol treatment enhances lipopolysaccharide/ phorbol myristate acetate-induced tumor necrosis factor-α production in human monocytic cells. Alcohol. Clin. Exp. Res. 25: 444-449.
66. Shi, L., R. Kishore, M. R. McMullen, and L. E. Nagy. 2002. Chronic ethanol increases lipopolysaccharide-stimulated Egr-1 expression in RAW 264.7 macrophages: contribution to enhanced tumor necrosis factor production. J. Biol. Chem. 277: 14777-14785. (Pubitemid 34952550)
67. Norkina, O., A. Dolganiuc, D. Catalano, K. Kodys, P. Mandrekar, A. Syed, M. Efros, and G. Szabo. 2008. Acute alcohol intake induces SOCS1 and SOCS3 and inhibits cytokine-induced STAT1 and STAT3 signaling in human monocytes. Alcohol. Clin. Exp. Res. 32: 1565-1573.
68. Kagan, J. C., T. Su, T. Horng, A. Chow, S. Akira, and R. Medzhitov. 2008. TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-β. Nat. Immunol. 9: 361-368.
69. Kagan, J. C., and R. Medzhitov. 2006. Phosphoinositide-mediated adaptor recruitment controls Toll-like receptor signaling. Cell 125: 943-955. (Pubitemid 43795199)