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Anthocyanins control neuroinflammation and consequent memory dysfunction in mice exposed to lipopolysaccharide

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Abstract

Peripheral inflammatory stimuli may activate a brain neuroinflammatory processes with consequences in brain function. The present study investigated if anthocyanins (ANT) consumption was able to prevent the memory loss, the neuronal damage, and the neuroinflammatory processes triggered by the intraperitoneal lipopolysaccharide (LPS) administration. C57BL6 male mice were treated with ANT (30–100 mg/kg by gavage). With a single dose or during 10 days, before be challenged with LPS (250 μg/kg intraperitoneally single administration), a classical inductor of inflammation. The data obtained showed that ANT was able to confer protection against the memory impairment after 10 days of ANT treatment (100 mg/kg). This phytonutrient also prevented the hypothermia episode induced by LPS. Moreover, ANT prevented the increase in protein carbonyl, NOx, and MDA levels in the hippocampus and cerebral cortex (4 and 24 h) in animal challenged with LPS. ANT showed a protective effect on the increase in the pro-inflammatory cytokines content, especially Interleukin (IL)-1β, tumoral necrosis factor-α and on the reduction of IL-10 induced by LPS. ANT 100 mg/kg prevented the infiltration of peripheral immune cells in the hippocampus at 24 h post-LPS administration. In parallel, LPS increased the activity of myeloperoxidase in cortex and hippocampus, and ANT prevented this effect, also reducing microglia (Iba-1) and astrocyte (GFAP) immunoreactivity. Thus, our data support that ANT are a promising therapeutic component against brain disorders associated with process of neuroinflammation.

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References

  1. Hoogland IC, Houbolt C, van Westerloo DJ, van Gool WA, van de Beek D (2015) Systemic inflammation and microglial activation: systematic review of animal experiments. J Neuroinflammation 12:114. doi:10.1186/s12974-015-0332-6

    Article  PubMed  PubMed Central  Google Scholar 

  2. Agostinho P, Cunha RA, Oliveira C (2010) Neuroinflammation, oxidative stress and the pathogenesis of Alzheimer’s disease. Curr Pharm Des 16(25):2766–2778

    Article  CAS  PubMed  Google Scholar 

  3. Dantzer R, O’Connor JC, Freund GG, Johnson RW, Kelley KW (2008) From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 9(1):46–56. doi:10.1038/nrn2297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Guerreiro RJ, Santana I, Bras JM, Santiago B, Paiva A, Oliveira C (2007) Peripheral inflammatory cytokines as biomarkers in Alzheimer’s disease and mild cognitive impairment. Neurodegener Dis 4(6):406–412. doi:10.1159/000107700

    Article  CAS  PubMed  Google Scholar 

  5. Jacewicz M, Czapski GA, Katkowska I, Strosznajder RP (2009) Systemic administration of lipopolysaccharide impairs glutathione redox state and object recognition in male mice. The effect of PARP-1 inhibitor. Folia Neuropathol 47(4):321–328

    CAS  PubMed  Google Scholar 

  6. Noble F, Rubira E, Boulanouar M, Palmier B, Plotkine M, Warnet JM, Marchand-Leroux C, Massicot F (2007) Acute systemic inflammation induces central mitochondrial damage and mnesic deficit in adult Swiss mice. Neurosci Lett 424(2):106–110. doi:10.1016/j.neulet.2007.07.005

    Article  CAS  PubMed  Google Scholar 

  7. Kielian T (2006) Toll-like receptors in central nervous system glial inflammation and homeostasis. J Neurosci Res 83(5):711–730. doi:10.1002/jnr.20767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Rivest S (2003) Molecular insights on the cerebral innate immune system. Brain Behav Immun 17(1):13–19

    Article  CAS  PubMed  Google Scholar 

  9. Henry CJ, Huang Y, Wynne A, Hanke M, Himler J, Bailey MT, Sheridan JF, Godbout JP (2008) Minocycline attenuates lipopolysaccharide (LPS)-induced neuroinflammation, sickness behavior, and anhedonia. J Neuroinflammation 5:15. doi:10.1186/1742-2094-5-15

    Article  PubMed  PubMed Central  Google Scholar 

  10. Abraham J, Johnson RW (2009) Central inhibition of interleukin-1beta ameliorates sickness behavior in aged mice. Brain Behav Immun 23(3):396–401. doi:10.1016/j.bbi.2008.12.008

    Article  CAS  PubMed  Google Scholar 

  11. Francois A, Terro F, Quellard N, Fernandez B, Chassaing D, Janet T, Rioux Bilan A, Paccalin M et al (2014) Impairment of autophagy in the central nervous system during lipopolysaccharide-induced inflammatory stress in mice. Mol Brain 7:56. doi:10.1186/s13041-014-0056-z

    Article  PubMed  PubMed Central  Google Scholar 

  12. Carvalho FB, Gutierres JM, Bohnert C, Zago AM, Abdalla FH, Vieira JM, Palma HE, Oliveira SM et al (2015) Anthocyanins suppress the secretion of proinflammatory mediators and oxidative stress, and restore ion pump activities in demyelination. J Nutr Biochem 26(4):378–390. doi:10.1016/j.jnutbio.2014.11.006

    Article  CAS  PubMed  Google Scholar 

  13. Gutierres JM, Carvalho FB, Schetinger MR, Agostinho P, Marisco PC, Vieira JM, Rosa MM, Bohnert C et al (2014) Neuroprotective effect of anthocyanins on acetylcholinesterase activity and attenuation of scopolamine-induced amnesia in rats. Int J Dev Neurosci 33:88–97. doi:10.1016/j.ijdevneu.2013.12.006

    Article  CAS  PubMed  Google Scholar 

  14. Gutierres JM, Carvalho FB, Schetinger MR, Marisco P, Agostinho P, Rodrigues M, Rubin MA, Schmatz R et al (2014) Anthocyanins restore behavioral and biochemical changes caused by streptozotocin-induced sporadic dementia of Alzheimer’s type. Life Sci 96(1–2):7–17. doi:10.1016/j.lfs.2013.11.014

    Article  CAS  PubMed  Google Scholar 

  15. Gutierres JM, Carvalho FB, Schetinger MR, Rodrigues MV, Schmatz R, Pimentel VC, Vieira JM, Rosa MM et al (2012) Protective effects of anthocyanins on the ectonucleotidase activity in the impairment of memory induced by scopolamine in adult rats. Life Sci 91(23–24):1221–1228. doi:10.1016/j.lfs.2012.09.013

    Article  CAS  PubMed  Google Scholar 

  16. Lee SG, Kim B, Yang Y, Pham TX, Park YK, Manatou J, Koo SI, Chun OK et al (2014) Berry anthocyanins suppress the expression and secretion of proinflammatory mediators in macrophages by inhibiting nuclear translocation of NF-kappaB independent of NRF2-mediated mechanism. J Nutr Biochem 25(4):404–411. doi:10.1016/j.jnutbio.2013.12.001

    Article  CAS  PubMed  Google Scholar 

  17. McGhie TK, Walton MC (2007) The bioavailability and absorption of anthocyanins: towards a better understanding. Mol Nutr Food Res 51(6):702–713. doi:10.1002/mnfr.200700092

    Article  CAS  PubMed  Google Scholar 

  18. Miyazawa T, Nakagawa K, Kudo M, Muraishi K, Someya K (1999) Direct intestinal absorption of red fruit anthocyanins, cyanidin-3-glucoside and cyanidin-3,5-diglucoside, into rats and humans. J Agric Food Chem 47(3):1083–1091

    Article  CAS  PubMed  Google Scholar 

  19. Morazzoni P, Livio S, Scilingo A, Malandrino S (1991) Vaccinium myrtillus anthocyanosides pharmacokinetics in rats. Arzneimittelforschung 41(2):128–131

    CAS  PubMed  Google Scholar 

  20. Sparkman NL, Martin LA, Calvert WS, Boehm GW (2005) Effects of intraperitoneal lipopolysaccharide on Morris maze performance in year-old and 2-month-old female C57BL/6J mice. Behav Brain Res 159(1):145–151. doi:10.1016/j.bbr.2004.10.011

    Article  CAS  PubMed  Google Scholar 

  21. Sparkman NL, Kohman RA, Scott VJ, Boehm GW (2005) Bacterial endotoxin-induced behavioral alterations in two variations of the Morris water maze. Physiol Behav 86(1–2):244–251. doi:10.1016/j.physbeh.2005.07.016

    Article  CAS  PubMed  Google Scholar 

  22. Sparkman NL, Kohman RA, Garcia AK, Boehm GW (2005) Peripheral lipopolysaccharide administration impairs two-way active avoidance conditioning in C57BL/6J mice. Physiol Behav 85(3):278–288. doi:10.1016/j.physbeh.2005.04.015

    Article  CAS  PubMed  Google Scholar 

  23. Kranjac D, Koster KM, Kahn MS, Eimerbrink MJ, Womble BM, Cooper BG, Chumley MJ, Boehm GW (2013) Peripheral administration of D-cycloserine rescues memory consolidation following bacterial endotoxin exposure. Behav Brain Res 243:38–43. doi:10.1016/j.bbr.2012.12.053

    Article  CAS  PubMed  Google Scholar 

  24. Marisco PC, Carvalho FB, Rosa MM, Girardi BA, Gutierres JM, Jaques JA, Salla AP, Pimentel VC et al (2013) Piracetam prevents scopolamine-induced memory impairment and decrease of NTPDase, 5′-nucleotidase and adenosine deaminase activities. Neurochem Res 38(8):1704–1714. doi:10.1007/s11064-013-1072-6

    Article  CAS  PubMed  Google Scholar 

  25. Carvalho FB, Boligon AA, Athayde ML, Rubin MA, Ferreira J, Trevisan G (2016) Inhibitory effect of Scutia buxifolia extracts, fractions, and ursolic acid on Na(+), K(+)-ATPase activity in vitro in membranes purified from rat hearts. J Ethnopharmacol 179:45–54. doi:10.1016/j.jep.2015.12.035

    Article  CAS  PubMed  Google Scholar 

  26. Fiske CH, Subbarow Y (1927) The nature of the “inorganic phosphate” in voluntary muscle. Science 65(1686):401–403. doi:10.1126/science.65.1686.401

    Article  CAS  PubMed  Google Scholar 

  27. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95(2):351–358

    Article  CAS  PubMed  Google Scholar 

  28. Rossato JI, Zeni G, Mello CF, Rubin MA, Rocha JB (2002) Ebselen blocks the quinolinic acid-induced production of thiobarbituric acid reactive species but does not prevent the behavioral alterations produced by intra-striatal quinolinic acid administration in the rat. Neurosci Lett 318(3):137–140

    Article  CAS  PubMed  Google Scholar 

  29. Jaques JA, Doleski PH, Castilhos LG, da Rosa MM, Souza Vdo C, Carvalho FB, Marisco P, Thorstenberg ML et al (2013) Free and nanoencapsulated curcumin prevents cigarette smoke-induced cognitive impairment and redox imbalance. Neurobiol Learn Mem 100:98–107. doi:10.1016/j.nlm.2012.12.007

    Article  CAS  PubMed  Google Scholar 

  30. Miranda KM, Espey MG, Wink DA (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5(1):62–71. doi:10.1006/niox.2000.0319

    Article  CAS  PubMed  Google Scholar 

  31. Yan LJ, Traber MG, Packer L (1995) Spectrophotometric method for determination of carbonyls in oxidatively modified apolipoprotein B of human low-density lipoproteins. Anal Biochem 228(2):349–351. doi:10.1006/abio.1995.1362

    Article  CAS  PubMed  Google Scholar 

  32. Schneider Oliveira M, Flavia Furian A, Freire Royes LF, Rechia Fighera M, de Carvalho Myskiw J, Gindri Fiorenza N, Mello CF (2004) Ascorbate modulates pentylenetetrazol-induced convulsions biphasically. Neuroscience 128(4):721–728. doi:10.1016/j.neuroscience.2004.07.012

    Article  CAS  PubMed  Google Scholar 

  33. Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, Ahn BW, Shaltiel S et al (1990) Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186:464–478

    Article  CAS  PubMed  Google Scholar 

  34. Lloret S, Moreno JJ (1995) Effects of an anti-inflammatory peptide (antiflammin 2) on cell influx, eicosanoid biosynthesis and oedema formation by arachidonic acid and tetradecanoyl phorbol dermal application. Biochem Pharmacol 50(3):347–353

    Article  CAS  PubMed  Google Scholar 

  35. Silva MA, Trevisan G, Klafke JZ, Rossato MF, Walker CI, Oliveira SM, Silva CR, Boligon AA et al (2013) Antinociceptive and anti-inflammatory effects of Aloe saponaria Haw on thermal injury in rats. J Ethnopharmacol 146(1):393–401. doi:10.1016/j.jep.2012.12.055

    Article  CAS  PubMed  Google Scholar 

  36. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  37. Canas PM, Porciuncula LO, Cunha GM, Silva CG, Machado NJ, Oliveira JM, Oliveira CR, Cunha RA (2009) Adenosine A2A receptor blockade prevents synaptotoxicity and memory dysfunction caused by beta-amyloid peptides via p38 mitogen-activated protein kinase pathway. J Neurosci 29(47):14741–14751. doi:10.1523/JNEUROSCI.3728-09.2009

    Article  CAS  PubMed  Google Scholar 

  38. Duarte JM, Carvalho RA, Cunha RA, Gruetter R (2009) Caffeine consumption attenuates neurochemical modifications in the hippocampus of streptozotocin-induced diabetic rats. J Neurochem 111(2):368–379. doi:10.1111/j.1471-4159.2009.06349.x

    Article  CAS  PubMed  Google Scholar 

  39. Carmo MR, Simoes AP, Fonteles AA, Souza CM, Cunha RA, Andrade GM (2014) ATP P2Y1 receptors control cognitive deficits and neurotoxicity but not glial modifications induced by brain ischemia in mice. Eur J Neurosci 39(4):614–622. doi:10.1111/ejn.12435

    Article  PubMed  Google Scholar 

  40. Cunningham C (2013) Microglia and neurodegeneration: the role of systemic inflammation. Glia 61(1):71–90. doi:10.1002/glia.22350

    Article  PubMed  Google Scholar 

  41. Andres-Lacueva C, Shukitt-Hale B, Galli RL, Jauregui O, Lamuela-Raventos RM, Joseph JA (2005) Anthocyanins in aged blueberry-fed rats are found centrally and may enhance memory. Nutr Neurosci 8(2):111–120. doi:10.1080/10284150500078117

    Article  CAS  PubMed  Google Scholar 

  42. Faria A, Meireles M, Fernandes I, Santos-Buelga C, Gonzalez-Manzano S, Duenas M, de Freitas V, Mateus N et al (2014) Flavonoid metabolites transport across a human BBB model. Food Chem 149:190–196. doi:10.1016/j.foodchem.2013.10.095

    Article  CAS  PubMed  Google Scholar 

  43. Youdim KA, Dobbie MS, Kuhnle G, Proteggente AR, Abbott NJ, Rice-Evans C (2003) Interaction between flavonoids and the blood–brain barrier: in vitro studies. J Neurochem 85(1):180–192

    Article  CAS  PubMed  Google Scholar 

  44. Talavera S, Felgines C, Texier O, Besson C, Gil-Izquierdo A, Lamaison JL, Remesy C (2005) Anthocyanin metabolism in rats and their distribution to digestive area, kidney, and brain. J Agric Food Chem 53(10):3902–3908. doi:10.1021/jf050145v

    Article  CAS  PubMed  Google Scholar 

  45. Jeong JW, Lee WS, Shin SC, Kim GY, Choi BT, Choi YH (2013) Anthocyanins downregulate lipopolysaccharide-induced inflammatory responses in BV2 microglial cells by suppressing the NF-kappaB and Akt/MAPKs signaling pathways. Int J Mol Sci 14(1):1502–1515. doi:10.3390/ijms14011502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Thummayot S, Tocharus C, Pinkaew D, Viwatpinyo K, Sringarm K, Tocharus J (2014) Neuroprotective effect of purple rice extract and its constituent against amyloid beta-induced neuronal cell death in SK-N-SH cells. Neurotoxicology 45:149–158. doi:10.1016/j.neuro.2014.10.010

    Article  CAS  PubMed  Google Scholar 

  47. Qin L, Wu X, Block ML, Liu Y, Breese GR, Hong JS, Knapp DJ, Crews FT (2007) Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 55(5):453–462. doi:10.1002/glia.20467

    Article  PubMed  PubMed Central  Google Scholar 

  48. Rebola N, Simoes AP, Canas PM, Tome AR, Andrade GM, Barry CE, Agostinho PM, Lynch MA et al (2011) Adenosine A2A receptors control neuroinflammation and consequent hippocampal neuronal dysfunction. J Neurochem 117(1):100–111. doi:10.1111/j.1471-4159.2011.07178.x

    Article  CAS  PubMed  Google Scholar 

  49. Canas PM, Duarte JM, Rodrigues RJ, Kofalvi A, Cunha RA (2009) Modification upon aging of the density of presynaptic modulation systems in the hippocampus. Neurobiol Aging 30(11):1877–1884. doi:10.1016/j.neurobiolaging.2008.01.003

    Article  CAS  PubMed  Google Scholar 

  50. Glushchenko TS, Izvarina NL (1997) Na+, K(+)-ATPase activity in neurons and glial cells of the olfactory cortex of the rat brain during the development of long-term potentiation. Neurosci Behav Physiol 27(1):49–52

    Article  CAS  PubMed  Google Scholar 

  51. Scuri R, Lombardo P, Cataldo E, Ristori C, Brunelli M (2007) Inhibition of Na+/K+ ATPase potentiates synaptic transmission in tactile sensory neurons of the leech. Eur J Neurosci 25(1):159–167. doi:10.1111/j.1460-9568.2006.05257.x

    Article  PubMed  Google Scholar 

  52. Brunelli M, Garcia-Gil M, Mozzachiodi R, Scuri R, Zaccardi ML (1997) Neurobiological principles of learning and memory. Arch Ital Biol 135(1):15–36

    CAS  PubMed  Google Scholar 

  53. Wyse AT, Bavaresco CS, Reis EA, Zugno AI, Tagliari B, Calcagnotto T, Netto CA (2004) Training in inhibitory avoidance causes a reduction of Na+, K + −ATPase activity in rat hippocampus. Physiol Behav 80(4):475–479

    Article  CAS  PubMed  Google Scholar 

  54. Li S, Stys PK (2001) Na(+)-K(+)-ATPase inhibition and depolarization induce glutamate release via reverse Na(+)-dependent transport in spinal cord white matter. Neuroscience 107(4):675–683

    Article  CAS  PubMed  Google Scholar 

  55. Matos M, Augusto E, Agostinho P, Cunha RA, Chen JF (2013) Antagonistic interaction between adenosine A2A receptors and Na+/K + −ATPase-alpha2 controlling glutamate uptake in astrocytes. J Neurosci 33(47):18492–18502. doi:10.1523/JNEUROSCI.1828-13.2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Lees GJ, Lehmann A, Sandberg M, Hamberger A (1990) The neurotoxicity of ouabain, a sodium-potassium ATPase inhibitor, in the rat hippocampus. Neurosci Lett 120(2):159–162

    Article  CAS  PubMed  Google Scholar 

  57. dos Reis EA, de Oliveira LS, Lamers ML, Netto CA, Wyse AT (2002) Arginine administration inhibits hippocampal Na(+), K(+)-ATPase activity and impairs retention of an inhibitory avoidance task in rats. Brain Res 951(2):151–157

    Article  PubMed  Google Scholar 

  58. Lingrel JB, Williams MT, Vorhees CV, Moseley AE (2007) Na, K-ATPase and the role of alpha isoforms in behavior. J Bioenerg Biomembr 39(5–6):385–389. doi:10.1007/s10863-007-9107-9

    Article  CAS  PubMed  Google Scholar 

  59. Moseley AE, Williams MT, Schaefer TL, Bohanan CS, Neumann JC, Behbehani MM, Vorhees CV, Lingrel JB (2007) Deficiency in Na, K-ATPase alpha isoform genes alters spatial learning, motor activity, and anxiety in mice. J Neurosci 27(3):616–626. doi:10.1523/JNEUROSCI.4464-06.2007

    Article  CAS  PubMed  Google Scholar 

  60. Semmler A, Frisch C, Debeir T, Ramanathan M, Okulla T, Klockgether T, Heneka MT (2007) Long-term cognitive impairment, neuronal loss and reduced cortical cholinergic innervation after recovery from sepsis in a rodent model. Exp Neurol 204(2):733–740. doi:10.1016/j.expneurol.2007.01.003

    Article  PubMed  Google Scholar 

  61. Cao A, Ramos Martinez JI, Barcia R (2004) Implication of PKA and PKC in the activation of the haemocytes of Mytilus galloprovincialis Lmk by LPS and IL-2. Mol Immunol 41(1):45–52. doi:10.1016/j.molimm.2004.02.002

    Article  CAS  PubMed  Google Scholar 

  62. Suh HW, Choi SS, Lee JK, Lee HK, Han EJ, Lee J (2004) Regulation of c-fos and c-jun gene expression by lipopolysaccharide and cytokines in primary cultured astrocytes: effect of PKA and PKC pathways. Arch Pharm Res 27(4):396–401

    Article  CAS  PubMed  Google Scholar 

  63. Carvalho FB, Mello CF, Marisco PC, Tonello R, Girardi BA, Ferreira J, Oliveira MS, Rubin MA (2012) Spermidine decreases Na(+), K(+)-ATPase activity through NMDA receptor and protein kinase G activation in the hippocampus of rats. Eur J Pharmacol 684(1–3):79–86. doi:10.1016/j.ejphar.2012.03.046

    Article  CAS  PubMed  Google Scholar 

  64. Vida C, Gonzalez EM, Fuente MD (2014) Increase of oxidation and inflammation in nervous and immune systems with aging and anxiety. Curr Pharm Des

  65. Sutherland GT, Chami B, Youssef P, Witting PK (2013) Oxidative stress in Alzheimer’s disease: Primary villain or physiological by-product? Redox Rep Commun Free Radic Res 18(4):134–141. doi:10.1179/1351000213Y.0000000052

    Article  CAS  Google Scholar 

  66. Sultana R, Perluigi M, Allan Butterfield D (2013) Lipid peroxidation triggers neurodegeneration: a redox proteomics view into the Alzheimer disease brain. Free Radic Biol Med 62:157–169. doi:10.1016/j.freeradbiomed.2012.09.027

    Article  CAS  PubMed  Google Scholar 

  67. Vasconcelos AR, Kinoshita PF, Yshii LM, Marques Orellana AM, Bohmer AE, de Sa Lima L, Alves R, Andreotti DZ et al (2015) Effects of intermittent fasting on age-related changes on Na, K-ATPase activity and oxidative status induced by lipopolysaccharide in rat hippocampus. Neurobiol Aging 36(5):1914–1923. doi:10.1016/j.neurobiolaging.2015.02.020

    Article  CAS  PubMed  Google Scholar 

  68. Swarnkar S, Tyagi E, Agrawal R, Singh MP, Nath C (2009) A comparative study on oxidative stress induced by LPS and rotenone in homogenates of rat brain regions. Environ Toxicol Pharmacol 27(2):219–224. doi:10.1016/j.etap.2008.10.003

    Article  CAS  PubMed  Google Scholar 

  69. Abdel-Salam OM, Youness ER, Mohammed NA, Morsy SM, Omara EA, Sleem AA (2014) Citric acid effects on brain and liver oxidative stress in lipopolysaccharide-treated mice. J Med Food 17(5):588–598. doi:10.1089/jmf.2013.0065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Barrientos RM, Frank MG, Hein AM, Higgins EA, Watkins LR, Rudy JW, Maier SF (2009) Time course of hippocampal IL-1 beta and memory consolidation impairments in aging rats following peripheral infection. Brain Behav Immun 23(1):46–54. doi:10.1016/j.bbi.2008.07.002

    Article  CAS  PubMed  Google Scholar 

  71. Barrientos RM, Hein AM, Frank MG, Watkins LR, Maier SF (2012) Intracisternal interleukin-1 receptor antagonist prevents postoperative cognitive decline and neuroinflammatory response in aged rats. J Neurosci 32(42):14641–14648. doi:10.1523/JNEUROSCI.2173-12.2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Barrientos RM, Higgins EA, Biedenkapp JC, Sprunger DB, Wright-Hardesty KJ, Watkins LR, Rudy JW, Maier SF (2006) Peripheral infection and aging interact to impair hippocampal memory consolidation. Neurobiol Aging 27(5):723–732. doi:10.1016/j.neurobiolaging.2005.03.010

    Article  PubMed  Google Scholar 

  73. Barrientos RM, Higgins EA, Sprunger DB, Watkins LR, Rudy JW, Maier SF (2002) Memory for context is impaired by a post context exposure injection of interleukin-1 beta into dorsal hippocampus. Behav Brain Res 134(1–2):291–298

    Article  CAS  PubMed  Google Scholar 

  74. Machado I, Gonzalez PV, Vilcaes A, Carniglia L, Schioth HB, Lasaga M, Scimonelli TN (2015) Interleukin-1beta-induced memory reconsolidation impairment is mediated by a reduction in glutamate release and zif268 expression and alpha-melanocyte-stimulating hormone prevented these effects. Brain Behav Immun 46:137–146. doi:10.1016/j.bbi.2015.01.012

    Article  CAS  PubMed  Google Scholar 

  75. Hou DX, Yanagita T, Uto T, Masuzaki S, Fujii M (2005) Anthocyanidins inhibit cyclooxygenase-2 expression in LPS-evoked macrophages: structure-activity relationship and molecular mechanisms involved. Biochem Pharmacol 70(3):417–425. doi:10.1016/j.bcp.2005.05.003

    Article  CAS  PubMed  Google Scholar 

  76. Jeong HK, Jou I, Joe EH (2010) Systemic LPS administration induces brain inflammation but not dopaminergic neuronal death in the substantia nigra. Exp Mol Med 42(12):823–832. doi:10.3858/emm.2010.42.12.085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Hayashi Y, Yoshida M, Yamato M, Ide T, Wu Z, Ochi-Shindou M, Kanki T, Kang D et al (2008) Reverse of age-dependent memory impairment and mitochondrial DNA damage in microglia by an overexpression of human mitochondrial transcription factor a in mice. J Neurosci 28(34):8624–8634. doi:10.1523/JNEUROSCI.1957-08.2008

    Article  CAS  PubMed  Google Scholar 

  78. Nakanishi H, Hayashi Y, Wu Z (2011) The role of microglial mtDNA damage in age-dependent prolonged LPS-induced sickness behavior. Neuron Glia Biol 7(1):17–23. doi:10.1017/S1740925X1100010X

    Article  PubMed  Google Scholar 

  79. Michels M, Vieira AS, Vuolo F, Zapelini HG, Mendonca B, Mina F, Dominguini D, Steckert A et al (2015) The role of microglia activation in the development of sepsis-induced long-term cognitive impairment. Brain Behav Immun 43:54–59. doi:10.1016/j.bbi.2014.07.002

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This study was supported by the Christian Hansen LTDA and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq/n°115566/2013-9).

Author information

Authors and Affiliations

  1. Programa de Pós-Graduação em Ciências Biológicas: Bioquímica Toxicológica, Departamento de Bioquímica e Biologia Molecular, Centro de Ciências Naturais e Exatas, Universidade Federal de Santa Maria, Santa Maria, RS, 97105-900, Brazil

    Fabiano B. Carvalho, Jessié M. Gutierres, Adriana M. Zago, Juliano Vieira, José L. Cechella, Cristina Wayne Nogueira, Sara M. Oliveira, Roselia M. Spanevello & Cinthia M. Andrade

  2. Programa de Pós-Graduação em Medicina Veterinária, Departamento de Pequenos Animais, Centro de Ciências Rurais, Universidade Federal de Santa Maria, Santa Maria, RS, 97105-900, Brazil

    Andressa Bueno & Cinthia M. Andrade

  3. CNC-Center for Neuroscience and Cell Biology, University of Coimbra, Coimbra, Portugal FMUC-Faculty of Medicine, University of Coimbra, Coimbra, 3004-517, Portugal

    Paula Agostinho

  4. Programa de Pós-Graduação em Farmacologia, Centro de Ciências da Saúde, Universidade Federal de Santa Maria, Santa Maria, RS, 97105-900, Brazil

    Pâmela Frühauf & Thiago Duarte

  5. Programa de Pós-Graduação em Biotecnologia, Unidade de Biotecnologia, Centro de Desenvolvimento Tecnológico, Universidade Federal de Pelotas, Campus Universitário, Capão do Leão, Pelotas, RS, 96010-900, Brazil

    Caroline Rizzi & Odir A. Dellagostin

  6. Programa de Pós-Graduação em Bioquímica e Bioprospecção, Centro de Ciências Químicas, Farmacêuticas e de Alimentos, Universidade Federal de Pelotas, Campus Universitário, Capão do Leão, Pelotas, RS, 96010-900, Brazil

    Roselia M. Spanevello

  7. Departamento de Ciências da Saúde, Universidade Luterana do Brasil, Santa Maria, RS, 97020 001, Brazil

    Marta M. F. Duarte

Authors
  1. Fabiano B. Carvalho
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  2. Jessié M. Gutierres
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  3. Andressa Bueno
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  4. Paula Agostinho
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  5. Adriana M. Zago
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  6. Juliano Vieira
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  7. Pâmela Frühauf
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  8. José L. Cechella
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  9. Cristina Wayne Nogueira
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  10. Sara M. Oliveira
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  11. Caroline Rizzi
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  12. Roselia M. Spanevello
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  13. Marta M. F. Duarte
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  14. Thiago Duarte
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  15. Odir A. Dellagostin
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  16. Cinthia M. Andrade
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Corresponding authors

Correspondence to Fabiano B. Carvalho or Cinthia M. Andrade.

Ethics declarations

All procedures were carried out according to the NIH Guide for the Care and Use of Laboratory Animals and the Brazilian Society for Neuroscience and Behavior (SBNeC) recommendations for animal care. This work was approved by the ethical committee of the Federal University of Santa Maria (protocol number 23081.005466/2011-13).

Conflicts of Interest Statement

The authors declare that they have no conflicts of interest.

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Carvalho, F.B., Gutierres, J.M., Bueno, A. et al. Anthocyanins control neuroinflammation and consequent memory dysfunction in mice exposed to lipopolysaccharide. Mol Neurobiol 54, 3350–3367 (2017). https://doi.org/10.1007/s12035-016-9900-8

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  • DOI: https://doi.org/10.1007/s12035-016-9900-8

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