Resveratrol Protects Hippocampal Astrocytes Against LPS-Induced Neurotoxicity Through HO-1, p38 and ERK Pathways

Neurochemical Research

Volumn 40, Issue 8, 2015, Pages 1600-1608

  Bellaver, Bruna ^a   Souza, Débora Guerini ^a   Bobermin, Larissa Daniele ^a   Souza, Diogo Onofre ^a   Gonçalves, Carlos Alberto ^a   Quincozes Santos, André ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

Astrocytes; Cytokines; HO 1; LPS; NF B; Resveratrol

Indexed keywords

GLUTATHIONE; HEME OXYGENASE 1; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE; RESVERATROL; SYNAPTOPHYSIN; TUMOR NECROSIS FACTOR ALPHA; HEME OXYGENASE; HMOX1 PROTEIN, RAT; NEUROPROTECTIVE AGENT; STILBENE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; ASTROCYTE; CELL PROTECTION; CONTROLLED STUDY; HIPPOCAMPUS; INFLAMMATION; MALE; NEUROTOXICITY; NEWBORN; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; WISTAR RAT;

VITACEAE;

ANIMALS; ASTROCYTES; CELLS, CULTURED; HEME OXYGENASE (DECYCLIZING); HIPPOCAMPUS; LIPOPOLYSACCHARIDES; MALE; MAP KINASE SIGNALING SYSTEM; NEUROPROTECTIVE AGENTS; RATS; RATS, WISTAR; STILBENES;

EID: 84939255795     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-015-1636-8     Document Type: Article

References (67)

1. Belanger M, Allaman I, Magistretti PJ (2011) Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab 14(6):724–738. doi:10.1016/j.cmet.2011.08.016
2. Maragakis NJ, Rothstein JD (2006) Mechanisms of disease: astrocytes in neurodegenerative disease. Nat Clin Pract Neurol 2(12):679–689. doi:10.1038/ncpneuro0355
3. He F, Sun YE (2007) Glial cells more than support cells? Int J Biochem Cell Biol 39(4):661–665. doi:10.1016/j.biocel.2006.10.022
4. Ransom BR, Ransom CB (2012) Astrocytes: multitalented stars of the central nervous system. Methods Mol Biol 814:3–7. doi:10.1007/978-1-61779-452-0_1
5. Parpura V, Heneka MT, Montana V, Oliet SH, Schousboe A, Haydon PG, Stout RF Jr, Spray DC, Reichenbach A, Pannicke T, Pekny M, Pekna M, Zorec R, Verkhratsky A (2012) Glial cells in (patho)physiology. J Neurochem 121(1):4–27. doi:10.1111/j.1471-4159.2012.07664.x
6. Hertz L, Zielke HR (2004) Astrocytic control of glutamatergic activity: astrocytes as stars of the show. Trends Neurosci 27(12):735–743. doi:10.1016/j.tins.2004.10.008
7. Allaman I, Belanger M, Magistretti PJ (2011) Astrocyte-neuron metabolic relationships: for better and for worse. Trends Neurosci 34(2):76–87. doi:10.1016/j.tins.2010.12.001
8. Farina C, Aloisi F, Meinl E (2007) Astrocytes are active players in cerebral innate immunity. Trends Immunol 28(3):138–145. doi:10.1016/j.it.2007.01.005
9. Gorina R, Font-Nieves M, Marquez-Kisinousky L, Santalucia T, Planas AM (2011) Astrocyte TLR4 activation induces a proinflammatory environment through the interplay between MyD88-dependent NFkappaB signaling, MAPK, and Jak1/Stat1 pathways. Glia 59(2):242–255. doi:10.1002/glia.21094
10. Rivest S (2009) Regulation of innate immune responses in the brain. Nat Rev Immunol 9(6):429–439. doi:10.1038/nri2565
11. Zong Y, Sun L, Liu B, Deng YS, Zhan D, Chen YL, He Y, Liu J, Zhang ZJ, Sun J, Lu D (2012) Resveratrol inhibits LPS-induced MAPKs activation via activation of the phosphatidylinositol 3-kinase pathway in murine RAW 264.7 macrophage cells. PLoS One 7(8):e44107. doi:10.1371/journal.pone.0044107
12. Guerra MC, Tortorelli LS, Galland F, Da Re C, Negri E, Engelke DS, Rodrigues L, Leite MC, Goncalves CA (2011) Lipopolysaccharide modulates astrocytic S100B secretion: a study in cerebrospinal fluid and astrocyte cultures from rats. J Neuroinflammation 8:128. doi:10.1186/1742-2094-8-128
13. Carpentier PA, Duncan DS, Miller SD (2008) Glial toll-like receptor signaling in central nervous system infection and autoimmunity. Brain Behav Immun 22(2):140–147. doi:10.1016/j.bbi.2007.08.011
14. Zhong LM, Zong Y, Sun L, Guo JZ, Zhang W, He Y, Song R, Wang WM, Xiao CJ, Lu D (2012) Resveratrol inhibits inflammatory responses via the mammalian target of rapamycin signaling pathway in cultured LPS-stimulated microglial cells. PLoS One 7(2):e32195. doi:10.1371/journal.pone.0032195
15. Lee M, Cho T, Jantaratnotai N, Wang YT, McGeer E, McGeer PL (2010) Depletion of GSH in glial cells induces neurotoxicity: relevance to aging and degenerative neurological diseases. FASEB J 24(7):2533–2545. doi:10.1096/fj.09-149997
16. Chang L, Karin M (2001) Mammalian MAP kinase signalling cascades. Nature 410(6824):37–40. doi:10.1038/35065000
17. Rigon AP, Cordova FM, Oliveira CS, Posser T, Costa AP, Silva IG, Santos DA, Rossi FM, Rocha JB, Leal RB (2008) Neurotoxicity of cadmium on immature hippocampus and a neuroprotective role for p38 MAPK. Neurotoxicology 29(4):727–734. doi:10.1016/j.neuro.2008.04.017
18. Bramanti V, Tomassoni D, Bronzi D, Grasso S, Curro M, Avitabile M, Li Volsi G, Renis M, Ientile R, Amenta F, Avola R (2010) Alpha-lipoic acid modulates GFAP, vimentin, nestin, cyclin D1 and MAP-kinase expression in astroglial cell cultures. Neurochem Res 35(12):2070–2077. doi:10.1007/s11064-010-0256-6
19. Baur JA, Sinclair DA (2006) Therapeutic potential of resveratrol: the in vivo evidence. Nat Rev Drug Discov 5(6):493–506. doi:10.1038/nrd2060
20. Fremont L (2000) Biological effects of resveratrol. Life Sci 66(8):663–673. doi:10.1016/S0024-3205(99)00410-5
21. Bastianetto S, Menard C, Quirion R (2014) Neuroprotective action of resveratrol. Biochim Biophys Acta. doi:10.1016/j.bbadis.2014.09.011
22. Quincozes-Santos A, Bobermin LD, Latini A, Wajner M, Souza DO, Goncalves CA, Gottfried C (2013) Resveratrol protects C6 astrocyte cell line against hydrogen peroxide-induced oxidative stress through heme oxygenase 1. PLoS One 8(5):e64372. doi:10.1371/journal.pone.0064372
23. Quincozes-Santos A, Gottfried C (2011) Resveratrol modulates astroglial functions: neuroprotective hypothesis. Ann N Y Acad Sci 1215:72–78. doi:10.1111/j.1749-6632.2010.05857.x
24. Bobermin LD, Quincozes-Santos A, Guerra MC, Leite MC, Souza DO, Goncalves CA, Gottfried C (2012) Resveratrol prevents ammonia toxicity in astroglial cells. PLoS One 7(12):e52164. doi:10.1371/journal.pone.0052164
25. Pervaiz S (2003) Resveratrol: from grapevines to mammalian biology. FASEB J 17(14):1975–1985. doi:10.1096/fj.03-0168rev
26. Delmas D, Jannin B, Latruffe N (2005) Resveratrol: preventing properties against vascular alterations and ageing. Mol Nutr Food Res 49(5):377–395. doi:10.1002/mnfr.200400098
27. Jang M, Cai L, Udeani GO, Slowing KV, Thomas CF, Beecher CW, Fong HH, Farnsworth NR, Kinghorn AD, Mehta RG, Moon RC, Pezzuto JM (1997) Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 275(5297):218–220. doi:10.1126/science.275.5297.218
28. Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, Kalra A, Prabhu VV, Allard JS, Lopez-Lluch G, Lewis K, Pistell PJ, Poosala S, Becker KG, Boss O, Gwinn D, Wang M, Ramaswamy S, Fishbein KW, Spencer RG, Lakatta EG, Le Couteur D, Shaw RJ, Navas P, Puigserver P, Ingram DK, de Cabo R, Sinclair DA (2006) Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444(7117):337–342. doi:10.1038/nature05354
29. Bellaver B, de Souza DG, Souza DO, Quincozes-Santos A (2013) Resveratrol increases antioxidant defenses and decreases proinflammatory cytokines in hippocampal astrocyte cultures from newborn, adult and aged Wistar rats. Toxicol In Vitro 28(4):479–484. doi:10.1016/j.tiv.2014.01.006
30. Tiwari V, Chopra K (2011) Resveratrol prevents alcohol-induced cognitive deficits and brain damage by blocking inflammatory signaling and cell death cascade in neonatal rat brain. J Neurochem 117(4):678–690. doi:10.1111/j.1471-4159.2011.07236.x
31. Khan MM, Ahmad A, Ishrat T, Khan MB, Hoda MN, Khuwaja G, Raza SS, Khan A, Javed H, Vaibhav K, Islam F (2010) Resveratrol attenuates 6-hydroxydopamine-induced oxidative damage and dopamine depletion in rat model of Parkinson’s disease. Brain Res 1328:139–151. doi:10.1016/j.brainres.2010.02.031
32. Huang TC, Lu KT, Wo YY, Wu YJ, Yang YL (2011) Resveratrol protects rats from Abeta-induced neurotoxicity by the reduction of iNOS expression and lipid peroxidation. PLoS One 6(12):e29102. doi:10.1371/journal.pone.0029102
33. Wu Z, Xu Q, Zhang L, Kong D, Ma R, Wang L (2009) Protective effect of resveratrol against kainate-induced temporal lobe epilepsy in rats. Neurochem Res 34(8):1393–1400. doi:10.1007/s11064-009-9920-0
34. Sakata Y, Zhuang H, Kwansa H, Koehler RC, Dore S (2010) Resveratrol protects against experimental stroke: putative neuroprotective role of heme oxygenase 1. Exp Neurol 224(1):325–329. doi:10.1016/j.expneurol.2010.03.032
35. Frozza RL, Bernardi A, Hoppe JB, Meneghetti AB, Battastini AM, Pohlmann AR, Guterres SS, Salbego C (2013) Lipid-core nanocapsules improve the effects of resveratrol against Abeta-induced neuroinflammation. J Biomed Nanotechnol 9(12):2086–2104. doi:10.1166/jbn.2013.1709
36. Frozza RL, Bernardi A, Hoppe JB, Meneghetti AB, Matte A, Battastini AM, Pohlmann AR, Guterres SS, Salbego C (2013) Neuroprotective effects of resveratrol against Abeta administration in rats are improved by lipid-core nanocapsules. Mol Neurobiol 47(3):1066–1080. doi:10.1007/s12035-013-8401-2
37. Quincozes-Santos A, Nardin P, de Souza DF, Gelain DP, Moreira JC, Latini A, Goncalves CA, Gottfried C (2009) The janus face of resveratrol in astroglial cells. Neurotox Res 16(1):30–41. doi:10.1007/s12640-009-9042-0
38. dos Santos AQ, Nardin P, Funchal C, de Almeida LM, Jacques-Silva MC, Wofchuk ST, Goncalves CA, Gottfried C (2006) Resveratrol increases glutamate uptake and glutamine synthetase activity in C6 glioma cells. Arch Biochem Biophys 453(2):161–167. doi:10.1016/j.abb.2006.06.025
39. de Almeida LM, Pineiro CC, Leite MC, Brolese G, Tramontina F, Feoli AM, Gottfried C, Goncalves CA (2007) Resveratrol increases glutamate uptake, glutathione content, and S100B secretion in cortical astrocyte cultures. Cell Mol Neurobiol 27(5):661–668. doi:10.1007/s10571-007-9152-2
40. Vieira de Almeida LM, Pineiro CC, Leite MC, Brolese G, Leal RB, Gottfried C, Goncalves CA (2008) Protective effects of resveratrol on hydrogen peroxide induced toxicity in primary cortical astrocyte cultures. Neurochem Res 33(1):8–15. doi:10.1007/s11064-007-9399-5
41. Bramanti V, Tomassoni D, Grasso S, Bronzi D, Napoli M, Campisi A, Li Volti G, Ientile R, Amenta F, Avola R (2012) Cholinergic precursors modulate the expression of heme oxigenase-1, p21 during astroglial cell proliferation and differentiation in culture. Neurochem Res 37(12):2795–2804. doi:10.1007/s11064-012-0873-3
42. Dore S (2005) Unique properties of polyphenol stilbenes in the brain: more than direct antioxidant actions; gene/protein regulatory activity. Neurosignals 14(1–2):61–70. doi:10.1159/000085386
43. Calabrese V, Cornelius C, Mancuso C, Pennisi G, Calafato S, Bellia F, Bates TE, Giuffrida Stella AM, Schapira T, Dinkova Kostova AT, Rizzarelli E (2008) Cellular stress response: a novel target for chemoprevention and nutritional neuroprotection in aging, neurodegenerative disorders and longevity. Neurochem Res 33(12):2444–2471. doi:10.1007/s11064-008-9775-9
44. Wakabayashi N, Slocum SL, Skoko JJ, Shin S, Kensler TW (2010) When NRF2 talks, who’s listening? Antioxid Redox Signal 13(11):1649–1663. doi:10.1089/ars.2010.3216
45. Bellaver B, Souza DG, Souza DO, Quincozes-Santos A (2014) Resveratrol increases antioxidant defenses and decreases proinflammatory cytokines in hippocampal astrocyte cultures from newborn, adult and aged Wistar rats. Toxicol In Vitro 28(4):479–484. doi:10.1016/j.tiv.2014.01.006
46. Quincozes-Santos A, Bobermin LD, Souza DG, Bellaver B, Goncalves CA, Souza DO (2014) Guanosine protects C6 astroglial cells against azide-induced oxidative damage: a putative role of heme oxygenase 1. J Neurochem 130(1):61–74. doi:10.1111/jnc.12694
47. Quincozes-Santos A, Bobermin LD, de Souza DG, Bellaver B, Goncalves CA, Souza DO (2013) Gliopreventive effects of guanosine against glucose deprivation in vitro. Purinergic Signal. doi:10.1007/s11302-013-9377-0
48. Browne RW, Armstrong D (1998) Reduced glutathione and glutathione disulfide. Methods Mol Biol 108:347–352. doi:10.1385/0-89603-472-0:347
49. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265–275
50. Gloire G, Legrand-Poels S, Piette J (2006) NF-kappaB activation by reactive oxygen species: fifteen years later. Biochem Pharmacol 72(11):1493–1505. doi:10.1016/j.bcp.2006.04.011
51. Bi XL, Yang JY, Dong YX, Wang JM, Cui YH, Ikeshima T, Zhao YQ, Wu CF (2005) Resveratrol inhibits nitric oxide and TNF-alpha production by lipopolysaccharide-activated microglia. Int Immunopharmacol 5(1):185–193. doi:10.1016/j.intimp.2004.08.008
52. Tanabe K, Matsushima-Nishiwaki R, Yamaguchi S, Iida H, Dohi S, Kozawa O (2010) Mechanisms of tumor necrosis factor-alpha-induced interleukin-6 synthesis in glioma cells. J Neuroinflammation 7:16. doi:10.1186/1742-2094-7-16
53. de Rivero Vaccari JP, Dietrich WD, Keane RW (2014) Activation and regulation of cellular inflammasomes: gaps in our knowledge for central nervous system injury. J Cereb Blood Flow Metab 34(3):369–375. doi:10.1038/jcbfm.2013.227
54. Bossu P, Ciaramella A, Salani F, Vanni D, Palladino I, Caltagirone C, Scapigliati G (2010) Interleukin-18, from neuroinflammation to Alzheimer’s disease. Curr Pharm Des 16(38):4213–4224. doi:10.2174/138161210794519147
55. Tukhovskaya EA, Turovsky EA, Turovskaya MV, Levin SG, Murashev AN, Zinchenko VP, Godukhin OV (2014) Anti-inflammatory cytokine interleukin-10 increases resistance to brain ischemia through modulation of ischemia-induced intracellular Ca(2)(+) response. Neurosci Lett 571:55–60. doi:10.1016/j.neulet.2014.04.046
56. Green HF, Nolan YM (2012) GSK-3 mediates the release of IL-1beta, TNF-alpha and IL-10 from cortical glia. Neurochem Int 61(5):666–671. doi:10.1016/j.neuint.2012.07.003
57. Hu D, Wan L, Chen M, Caudle Y, LeSage G, Li Q, Yin D (2014) Essential role of IL-10/STAT3 in chronic stress-induced immune suppression. Brain Behav Immun 36:118–127. doi:10.1016/j.bbi.2013.10.016
58. Zhang F, Shi JS, Zhou H, Wilson B, Hong JS, Gao HM (2010) Resveratrol protects dopamine neurons against lipopolysaccharide-induced neurotoxicity through its anti-inflammatory actions. Mol Pharmacol 78(3):466–477. doi:10.1124/mol.110.064535
59. Collino M, Aragno M, Mastrocola R, Benetti E, Gallicchio M, Dianzani C, Danni O, Thiemermann C, Fantozzi R (2006) Oxidative stress and inflammatory response evoked by transient cerebral ischemia/reperfusion: effects of the PPAR-alpha agonist WY14643. Free Radic Biol Med 41(4):579–589. doi:10.1016/j.freeradbiomed.2006.04.030
60. Lee EO, Park HJ, Kang JL, Kim HS, Chong YH (2010) Resveratrol reduces glutamate-mediated monocyte chemotactic protein-1 expression via inhibition of extracellular signal-regulated kinase 1/2 pathway in rat hippocampal slice cultures. J Neurochem 112(6):1477–1487. doi:10.1111/j.1471-4159.2009.06564.x
61. Lu X, Ma L, Ruan L, Kong Y, Mou H, Zhang Z, Wang Z, Wang JM, Le Y (2010) Resveratrol differentially modulates inflammatory responses of microglia and astrocytes. J Neuroinflammation 7:46. doi:10.1186/1742-2094-7-46
62. Kakita H, Aoyama M, Hussein MH, Kato S, Suzuki S, Ito T, Togari H, Asai K (2009) Diclofenac enhances proinflammatory cytokine-induced nitric oxide production through NF-kappaB signaling in cultured astrocytes. Toxicol Appl Pharmacol 238(1):56–63. doi:10.1016/j.taap.2009.04.014
63. Okun E, Griffioen KJ, Mattson MP (2011) Toll-like receptor signaling in neural plasticity and disease. Trends Neurosci 34(5):269–281. doi:10.1016/j.tins.2011.02.005
64. Shen HM, Pervaiz S (2006) TNF receptor superfamily-induced cell death: redox-dependent execution. FASEB J 20(10):1589–1598. doi:10.1111/j.1471-4159.2009.06564.x
65. Hamby ME, Gragnolati AR, Hewett SJ, Hewett JA (2008) TGF beta 1 and TNF alpha potentiate nitric oxide production in astrocyte cultures by recruiting distinct subpopulations of cells to express NOS-2. Neurochem Int 52(6):962–971. doi:10.1016/j.neuint.2007.10.010
66. Arredondo F, Echeverry C, Abin-Carriquiry JA, Blasina F, Antunez K, Jones DP, Go YM, Liang YL, Dajas F (2010) After cellular internalization, quercetin causes Nrf2 nuclear translocation, increases glutathione levels, and prevents neuronal death against an oxidative insult. Free Radic Biol Med 49(5):738–747. doi:10.1016/j.freeradbiomed.2010.05.020
67. Calkins MJ, Johnson DA, Townsend JA, Vargas MR, Dowell JA, Williamson TP, Kraft AD, Lee JM, Li J, Johnson JA (2009) The Nrf2/ARE pathway as a potential therapeutic target in neurodegenerative disease. Antioxid Redox Signal 11(3):497–508. doi:10.1089/ARS.2008.2242