Resveratrol mitigates lipopolysaccharide- and Aβ-mediated microglial inflammation by inhibiting the TLR4/NF-κB/STAT signaling cascade

Journal of Neurochemistry

Volumn 120, Issue 3, 2012, Pages 461-472

  Capiralla, Hemachander ^a   Vingtdeux, Valérie ^a   Zhao, Haitian ^a   Sankowski, Roman ^a   Al Abed, Yousef ^a   Davies, Peter ^a,b   Marambaud, Philippe ^a  

^a FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

A ; Alzheimer's disease; microglia; NF B; resveratrol; TLR4

Indexed keywords

AMYLOID BETA PROTEIN; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; I KAPPA B; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; RESVERATROL; STAT1 PROTEIN; STAT3 PROTEIN; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

AMYLOID PLAQUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG EFFICACY; DRUG POTENCY; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MACROPHAGE ACTIVATION; MALE; MICROGLIA; MOUSE; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CELL LINE, TRANSFORMED; CYTOKINES; DISEASE MODELS, ANIMAL; DRUG INTERACTIONS; HUMANS; I-KAPPA B PROTEINS; INFLAMMATION MEDIATORS; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, TRANSGENIC; MICROGLIA; PRESENILIN-1; SIGNAL TRANSDUCTION; STATISTICS, NONPARAMETRIC; STILBENES; TIME FACTORS; TOLL-LIKE RECEPTORS; TUMOR NECROSIS FACTOR-ALPHA;

MURINAE; MUS;

EID: 84855686976     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07594.x     Document Type: Article

References (79)

1. Akiyama H., Barger S., Barnum S., et al. (2000) Inflammation and Alzheimer's disease. Neurobiol. Aging 21, 383-421. (Pubitemid 30349107)
2. Bolmont T., Haiss F., Eicke D., Radde R., Mathis C. A., Klunk W. E., Kohsaka S., Jucker M., and, Calhoun M. E., (2008) Dynamics of the microglial/amyloid interaction indicate a role in plaque maintenance. J. Neurosci. 28, 4283-4292.
3. Bornemann K. D., Wiederhold K. H., Pauli C., Ermini F., Stalder M., Schnell L., Sommer B., Jucker M., and, Staufenbiel M., (2001) Abeta-induced inflammatory processes in microglia cells of APP23 transgenic mice. Am. J. Pathol. 158, 63-73. (Pubitemid 32096472)
4. Borra M. T., Smith B. C., and, Denu J. M., (2005) Mechanism of human SIRT1 activation by resveratrol. J. Biol. Chem. 280, 17187-17195. (Pubitemid 41389185)
5. Buee L., Bussiere T., Buee-Scherrer V., Delacourte A., and, Hof P. R., (2000) Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res. Brain Res. Rev. 33, 95-130.
6. Chen J., Zhou Y., Mueller-Steiner S., Chen L. F., Kwon H., Yi S., Mucke L., and, Gan L., (2005) SIRT1 protects against microglia-dependent amyloid-beta toxicity through inhibiting NF-kappaB signaling. J. Biol. Chem. 280, 40364-40374. (Pubitemid 41779174)
7. Chen K., Iribarren P., Hu J., Chen J., Gong W., Cho E. H., Lockett S., Dunlop N. M., and, Wang J. M., (2006) Activation of Toll-like receptor 2 on microglia promotes cell uptake of Alzheimer disease-associated amyloid beta peptide. J. Biol. Chem. 281, 3651-3659. (Pubitemid 43845983)
8. Chen C. Y., Peng W. H., Tsai K. D., and, Hsu S. L., (2007) Luteolin suppresses inflammation-associated gene expression by blocking NF-kappaB and AP-1 activation pathway in mouse alveolar macrophages. Life Sci. 81, 1602-1614.
9. Dasgupta B., and, Milbrandt J., (2007) Resveratrol stimulates AMP kinase activity in neurons. Proc. Natl. Acad. Sci. USA 104, 7217-7222. (Pubitemid 47186035)
10. Duyckaerts C., Delatour B., and, Potier M. C., (2009) Classification and basic pathology of Alzheimer disease. Acta Neuropathol. 118, 5-36.
11. Fassbender K., Walter S., Kuhl S., et al. (2004) The LPS receptor (CD14) links innate immunity with Alzheimer's disease. FASEB J. 18, 203-205.
12. Fitzgerald K. A., McWhirter S. M., Faia K. L., Rowe D. C., Latz E., Golenbock D. T., Coyle A. J., Liao S. M., and, Maniatis T., (2003) IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4, 491-496. (Pubitemid 36592443)
13. Fremont L., (2000) Biological effects of resveratrol. Life Sci. 66, 663-673.
14. Fuhrmann M., Bittner T., Jung C. K., Burgold S., Page R. M., Mitteregger G., Haass C., LaFerla F. M., Kretzschmar H., and, Herms J., (2010) Microglial Cx3cr1 knockout prevents neuron loss in a mouse model of Alzheimer's disease. Nat. Neurosci. 13, 411-413.
15. Galimberti D., and, Scarpini E., (2011) Inflammation and oxidative damage in Alzheimer's disease: friend or foe? Front. Biosci. (Schol Ed) 3, 252-266.
16. Giulian D., Haverkamp L. J., Yu J. H., Karshin W., Tom D., Li J., Kirkpatrick J., Kuo L. M., and, Roher A. E., (1996) Specific domains of beta-amyloid from Alzheimer plaque elicit neuron killing in human microglia. J. Neurosci. 16, 6021-6037. (Pubitemid 26313978)
17. Gonzalez R., Ballester I., Lopez-Posadas R., Suarez M. D., Zarzuelo A., Martinez-Augustin O., and, Sanchez de Medina F., (2011) Effects of flavonoids and other polyphenols on inflammation. Crit. Rev. Food Sci. Nutr. 51, 331-362.
18. Han Y. S., Zheng W. H., Bastianetto S., Chabot J. G., and, Quirion R., (2004) Neuroprotective effects of resveratrol against beta-amyloid-induced neurotoxicity in rat hippocampal neurons: involvement of protein kinase C. Br. J. Pharmacol. 141, 997-1005. (Pubitemid 38510083)
19. Hanisch U. K., and, Kettenmann H., (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat. Neurosci. 10, 1387-1394. (Pubitemid 350014685)
20. Harold D., Abraham R., Hollingworth P., et al. (2009) Genome-wide association study identifies variants at CLU and PICALM associated with Alzheimer's disease. Nat. Genet. 41, 1088-1093.
21. Ho L., Chen L. H., Wang J., et al. (2009) Heterogeneity in red wine polyphenolic contents differentially influences Alzheimer's disease-type neuropathology and cognitive deterioration. J. Alzheimer's Dis. 16, 59-72.
22. Hou X., Xu S., Maitland-Toolan K., et al. (2008) SIRT1 regulates hepatocyte lipid metabolism through activating AMP-activated protein kinase. J. Biol. Chem. 283, 20015-20026.
23. Howitz K. T., Bitterman K. J., Cohen H. Y., et al. (2003) Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 425, 191-196. (Pubitemid 37150899)
24. Imai Y., and, Kohsaka S., (2002) Intracellular signaling in M-CSF-induced microglia activation: role of Iba1. Glia 40, 164-174. (Pubitemid 35337374)
25. Iribarren P., Chen K., Hu J., Gong W., Cho E. H., Lockett S., Uranchimeg B., and, Wang J. M., (2005) CpG-containing oligodeoxynucleotide promotes microglial cell uptake of amyloid beta 1-42 peptide by up-regulating the expression of the G-protein- coupled receptor mFPR2. FASEB J. 19, 2032-2034. (Pubitemid 41759755)
26. Jang J. H., and, Surh Y. J., (2003) Protective effect of resveratrol on beta-amyloid-induced oxidative PC12 cell death. Free Radic. Biol. Med. 34, 1100-1110.
27. Jankowsky J. L., Fadale D. J., Anderson J., et al. (2004) Mutant presenilins specifically elevate the levels of the 42 residue beta-amyloid peptide in vivo: evidence for augmentation of a 42-specific gamma secretase. Hum. Mol. Genet. 13, 159-170. (Pubitemid 38111354)
28. Kaeberlein M., McDonagh T., Heltweg B., et al. (2005) Substrate-specific activation of sirtuins by resveratrol. J. Biol. Chem. 280, 17038-17045. (Pubitemid 41389166)
29. Karuppagounder S. S., Pinto J. T., Xu H., Chen H. L., Beal M. F., and, Gibson G. E., (2009) Dietary supplementation with resveratrol reduces plaque pathology in a transgenic model of Alzheimer's disease. Neurochem. Int. 54, 111-118.
30. Kawai T., and, Akira S., (2007) Signaling to NF-kappaB by Toll-like receptors. Trends Mol. Med. 13, 460-469.
31. Kunnumakkara A. B., Nair A. S., Ahn K. S., Pandey M. K., Yi Z., Liu M., and, Aggarwal B. B., (2007) Gossypin, a pentahydroxy glucosyl flavone, inhibits the transforming growth factor beta-activated kinase-1-mediated NF-kappaB activation pathway, leading to potentiation of apoptosis, suppression of invasion, and abrogation of osteoclastogenesis. Blood 109, 5112-5121. (Pubitemid 46890525)
32. Lagouge M., Argmann C., Gerhart-Hines Z., et al. (2006) Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 127, 1109-1122. (Pubitemid 44894520)
33. Lambert J. C., Heath S., Even G., et al. (2009) Genome-wide association study identifies variants at CLU and CR1 associated with Alzheimer's disease. Nat. Genet. 41, 1094-1099.
34. Lan F., Cacicedo J. M., Ruderman N., and, Ido Y., (2008) SIRT1 modulation of the acetylation status, cytosolic localization, and activity of LKB1. Possible role in AMP-activated protein kinase activation. J. Biol. Chem. 283, 27628-27635.
35. Landreth G. E., and, Reed-Geaghan E. G., (2009) Toll-like receptors in Alzheimer's disease. Curr. Top. Microbiol. Immunol. 336, 137-153.
36. Lee J. H., Jung H. S., Giang P. M., Jin X., Lee S., Son P. T., Lee D., Hong Y. S., Lee K., and, Lee J. J., (2006) Blockade of nuclear factor-kappaB signaling pathway and anti-inflammatory activity of cardamomin, a chalcone analog from Alpinia conchigera. J. Pharmacol. Exp. Ther. 316, 271-278. (Pubitemid 41832606)
37. Lindsay J., Laurin D., Verreault R., Hebert R., Helliwell B., Hill G. B., and, McDowell I., (2002) Risk factors for Alzheimer's disease: a prospective analysis from the Canadian Study of Health and Aging. Am. J. Epidemiol. 156, 445-453. (Pubitemid 34976983)
38. Liu Y., Walter S., Stagi M., Cherny D., Letiembre M., Schulz-Schaeffer W., Heine H., Penke B., Neumann H., and, Fassbender K., (2005) LPS receptor (CD14): a receptor for phagocytosis of Alzheimer's amyloid peptide. Brain 128, 1778-1789. (Pubitemid 41373649)
39. London J. A., Biegel D., and, Pachter J. S., (1996) Neurocytopathic effects of beta-amyloid-stimulated monocytes: a potential mechanism for central nervous system damage in Alzheimer disease. Proc. Natl. Acad. Sci. U S A 93, 4147-4152. (Pubitemid 26144255)
40. Luchsinger J. A., Tang M. X., Siddiqui M., Shea S., and, Mayeux R., (2004) Alcohol intake and risk of dementia. J. Am. Geriatr. Soc. 52, 540-546. (Pubitemid 38480630)
41. Manna S. K., Aggarwal R. S., Sethi G., Aggarwal B. B., and, Ramesh G. T., (2007) Morin (3,5,7,2′,4′-Pentahydroxyflavone) abolishes nuclear factor-kappaB activation induced by various carcinogens and inflammatory stimuli, leading to suppression of nuclear factor-kappaB-regulated gene expression and up-regulation of apoptosis. Clin. Cancer Res. 13, 2290-2297. (Pubitemid 46649899)
42. Marambaud P., and, Robakis N. K., (2005) Genetic and molecular aspects of Alzheimer's disease shed light on new mechanisms of transcriptional regulation. Genes Brain Behav. 4, 134-146. (Pubitemid 40559140)
43. Marambaud P., Zhao H., and, Davies P., (2005) Resveratrol promotes clearance of Alzheimer's disease amyloid-beta peptides. J. Biol. Chem. 280, 37377-37382. (Pubitemid 41642343)
44. Medzhitov R., Preston-Hurlburt P., and, Janeway C. A., Jr, (1997) A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388, 394-397. (Pubitemid 27334820)
45. Monick M. M., Carter A. B., Robeff P. K., Flaherty D. M., Peterson M. W., and, Hunninghake G. W., (2001) Lipopolysaccharide activates Akt in human alveolar macrophages resulting in nuclear accumulation and transcriptional activity of beta-catenin. J. Immunol. 166, 4713-4720. (Pubitemid 32233759)
46. Naj A. C., Jun G., Beecham G. W., et al. (2011) Common variants at MS4A4/MS4A6E, CD2AP, CD33 and EPHA1 are associated with late-onset Alzheimer's disease. Nat. Genet. 43, 436-441.
47. Ono K., Yoshiike Y., Takashima A., Hasegawa K., Naiki H., and, Yamada M., (2003) Potent anti-amyloidogenic and fibril-destabilizing effects of polyphenols in vitro: implications for the prevention and therapeutics of Alzheimer's disease. J. Neurochem. 87, 172-181. (Pubitemid 37210651)
48. Orgogozo J. M., Dartigues J. F., Lafont S., Letenneur L., Commenges D., Salamon R., Renaud S., and, Breteler M. B., (1997) Wine consumption and dementia in the elderly: a prospective community study in the Bordeaux area. Rev. Neurol. 153, 185-192. (Pubitemid 27262834)
49. Pacholec M., Bleasdale J. E., Chrunyk B., et al. (2010) SRT1720, SRT2183, SRT1460, and resveratrol are not direct activators of SIRT1. J. Biol. Chem. 285, 8340-8351.
50. Pandey M. K., Sandur S. K., Sung B., Sethi G., Kunnumakkara A. B., and, Aggarwal B. B., (2007) Butein, a tetrahydroxychalcone, inhibits nuclear factor (NF)-kappaB and NF-kappaB-regulated gene expression through direct inhibition of IkappaBalpha kinase beta on cysteine 179 residue. J. Biol. Chem. 282, 17340-17350. (Pubitemid 47100316)
51. Patel N. S., Paris D., Mathura V., Quadros A. N., Crawford F. C., and, Mullan M. J., (2005) Inflammatory cytokine levels correlate with amyloid load in transgenic mouse models of Alzheimer's disease. J. Neuroinflammation 2, 9.
52. Ramassamy C., (2006) Emerging role of polyphenolic compounds in the treatment of neurodegenerative diseases: a review of their intracellular targets. Eur. J. Pharmacol. 545, 51-64.
53. Ransohoff R. M., and, Cardona A. E., (2010) The myeloid cells of the central nervous system parenchyma. Nature 468, 253-262.
54. Rhee S. H., and, Hwang D., (2000) Murine TOLL-like receptor 4 confers lipopolysaccharide responsiveness as determined by activation of NF kappa B and expression of the inducible cyclooxygenase. J. Biol. Chem. 275, 34035-34040.
55. Riviere C., Richard T., Quentin L., Krisa S., Merillon J. M., and, Monti J. P., (2007) Inhibitory activity of stilbenes on Alzheimer's beta-amyloid fibrils in vitro. Bioorg. Med. Chem. 15, 1160-1167. (Pubitemid 44880692)
56. Saitoh S., Akashi S., Yamada T., et al. (2004) Lipid A antagonist, lipid IVa, is distinct from lipid A in interaction with Toll-like receptor 4 (TLR4)-MD-2 and ligand-induced TLR4 oligomerization. Int. Immunol. 16, 961-969. (Pubitemid 38960874)
57. Salh B., Wagey R., Marotta A., Tao J. S., and, Pelech S., (1998) Activation of phosphatidylinositol 3-kinase, protein kinase B, and p70 S6 kinases in lipopolysaccharide-stimulated Raw 264.7 cells: differential effects of rapamycin, Ly294002, and wortmannin on nitric oxide production. J. Immunol. 161, 6947-6954. (Pubitemid 28562242)
58. Sanjo H., Takeda K., Tsujimura T., Ninomiya-Tsuji J., Matsumoto K., and, Akira S., (2003) TAB2 is essential for prevention of apoptosis in fetal liver but not for interleukin-1 signaling. Mol. Cell. Biol. 23, 1231-1238. (Pubitemid 36177033)
59. Savaskan E., Olivieri G., Meier F., Seifritz E., Wirz-Justice A., and, Muller-Spahn F., (2003) Red wine ingredient resveratrol protects from beta-amyloid neurotoxicity. Gerontology 49, 380-383. (Pubitemid 37465118)
60. Selkoe D. J., (2001) Alzheimer's disease: genes, proteins, and therapy. Physiol. Rev. 81, 741-766. (Pubitemid 32267077)
61. Sharma S., tenOever B. R., Grandvaux N., Zhou G. P., Lin R., and, Hiscott J., (2003) Triggering the interferon antiviral response through an IKK-related pathway. Science 300, 1148-1151. (Pubitemid 36583100)
62. Shim J. H., Xiao C., Paschal A. E., et al. (2005) TAK1, but not TAB1 or TAB2, plays an essential role in multiple signaling pathways in vivo. Genes Dev. 19, 2668-2681. (Pubitemid 41627934)
63. Sugama S., Takenouchi T., Cho B. P., Joh T. H., Hashimoto M., and, Kitani H., (2009) Possible roles of microglial cells for neurotoxicity in clinical neurodegenerative diseases and experimental animal models. Inflamm. Allergy Drug Targets 8, 277-284.
64. Sung B., Pandey M. K., and, Aggarwal B. B., (2007) Fisetin, an inhibitor of cyclin-dependent kinase 6, down-regulates nuclear factor-kappaB-regulated cell proliferation, antiapoptotic and metastatic gene products through the suppression of TAK-1 and receptor-interacting protein-regulated IkappaBalpha kinase activation. Mol. Pharmacol. 71, 1703-1714. (Pubitemid 47010923)
65. Truelsen T., Thudium D., and, Gronbaek M., (2002) Amount and type of alcohol and risk of dementia: the Copenhagen City Heart Study. Neurology 59, 1313-1319. (Pubitemid 35285979)
66. Udan M. L., Ajit D., Crouse N. R., and, Nichols M. R., (2008) Toll-like receptors 2 and 4 mediate Abeta(1-42) activation of the innate immune response in a human monocytic cell line. J. Neurochem. 104, 524-533. (Pubitemid 350293880)
67. Um J. H., Park S. J., Kang H., Yang S., Foretz M., McBurney M. W., Kim M. K., Viollet B., and, Chung J. H., (2010) AMPK-deficient mice are resistant to the metabolic effects of resveratrol. Diabetes 59, 554-563.
68. Vingtdeux V., Dreses-Werringloer U., Zhao H., Davies P., and, Marambaud P., (2008) Therapeutic potential of resveratrol in Alzheimer's disease. BMC Neurosci. 9 (Suppl. 2), S6.
69. Vingtdeux V., Giliberto L., Zhao H., et al. (2010) AMP-activated protein kinase signaling activation by resveratrol modulates amyloid-beta peptide metabolism. J. Biol. Chem. 285, 9100-9113.
70. Vingtdeux V., Chandakkar P., Zhao H., d'Abramo C., Davies P., and, Marambaud P., (2011) Novel synthetic small-molecule activators of AMPK as enhancers of autophagy and amyloid-beta peptide degradation. FASEB J. 25, 219-231.
71. Walter S., Letiembre M., Liu Y., et al. (2007) Role of the toll-like receptor 4 in neuroinflammation in Alzheimer's disease. Cell. Physiol. Biochem. 20, 947-956. (Pubitemid 350059737)
72. Wang C., Deng L., Hong M., Akkaraju G. R., Inoue J., and, Chen Z. J., (2001) TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 412, 346-351. (Pubitemid 32694385)
73. Wang J., Ho L., Zhao Z., Seror I., Humala N., Dickstein D. L., Thiyagarajan M., Percival S. S., Talcott S. T., and, Pasinetti G. M., (2006) Moderate consumption of Cabernet Sauvignon attenuates Abeta neuropathology in a mouse model of Alzheimer's disease. FASEB J. 20, 2313-2320. (Pubitemid 44953861)
74. Wyss-Coray T., and, Mucke L., (2002) Inflammation in neurodegenerative disease - a double-edged sword. Neuron 35, 419-432. (Pubitemid 34879943)
75. Youn H. S., Lee J. Y., Fitzgerald K. A., Young H. A., Akira S., and, Hwang D. H., (2005) Specific inhibition of MyD88-independent signaling pathways of TLR3 and TLR4 by resveratrol: molecular targets are TBK1 and RIP1 in TRIF complex. J. Immunol. 175, 3339-3346. (Pubitemid 41170555)
76. Youn H. S., Lee J. Y., Saitoh S. I., Miyake K., Kang K. W., Choi Y. J., and, Hwang D. H., (2006) Suppression of MyD88- and TRIF-dependent signaling pathways of Toll-like receptor by (-)-epigallocatechin-3-gallate, a polyphenol component of green tea. Biochem. Pharmacol. 72, 850-859. (Pubitemid 44313886)
77. Zhang H., Tay P. N., Cao W., Li W., and, Lu J., (2002) Integrin-nucleated Toll-like receptor (TLR) dimerization reveals subcellular targeting of TLRs and distinct mechanisms of TLR4 activation and signaling. FEBS Lett. 532, 171-176. (Pubitemid 35375884)
78. Zhang F., Liu J., and, Shi J. S., (2010) Anti-inflammatory activities of resveratrol in the brain: role of resveratrol in microglial activation. Eur. J. Pharmacol. 636, 1-7.
79. Zhao H., Dreses-Werringloer U., Davies P., and, Marambaud P., (2008) Amyloid-beta peptide degradation in cell cultures by mycoplasma contaminants. BMC Res. Notes 1, 38.