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Metabolic Brain Disease

, Volume 34, Issue 1, pp 245–255 | Cite as

Berberine ameliorates lipopolysaccharide-induced learning and memory deficit in the rat: insights into underlying molecular mechanisms

  • Sepideh Sadraie
  • Zahra Kiasalari
  • Mohadeseh Razavian
  • Shekoofe Azimi
  • Ladan Sedighnejad
  • Siamak Afshin-Majd
  • Tourandokht Baluchnejadmojarad
  • Mehrdad RoghaniEmail author
Original Article
  • 79 Downloads

Abstract

Systemic lipopolysaccharide (LPS) triggers neuroinflammation with consequent development of behavioral and cognitive deficits. Neuroinflammation plays a crucial role in the pathogenesis of neurodegenerative disorders including Alzheimer’s disease (AD). Berberine is an isoquinoline alkaloid in Berberis genus with antioxidant and anti-inflammatory property and protective effects in neurodegenerative disorders. In this research, beneficial effect of this alkaloid against LPS-induced cognitive decline was assessed in the adult male rats. LPS was intraperitoneally administered at a dose of 1 mg/kg to induce neuroinflammation and berberine was given via gavage at doses of 10 or 50 mg/kg, one h after LPS, for 7 days. Treatment of LPS group with berberine at a dose of 50 mg/kg (but not at a dose of 10 mg/kg) improved spatial recognition memory in Y maze, performance in novel object recognition task (NORT), and prevented learning and memory dysfunction in passive avoidance tasks. Furthermore, berberine lowered hippocampal activity of acetylcholinesterase (AChE), malondialdehyde (MDA), protein carbonyl, activity of caspase 3, and DNA fragmentation and improved antioxidant capacity through enhancing glutathione peroxidase (GPx), superoxide dismutase (SOD), catalase, and glutathione (GSH). Besides, berberine attenuated inflammation-related indices, as was evident by lower levels of nuclear factor-kappa B (NF-κB), toll-like receptor 4 (TLR4), tumor necrosis factor α (TNFα), and interleukin 6 (IL-6). Berberine also appropriately restored hippocampal 3-nitrotyrosine (3-NT), cyclooxygenase 2 (Cox 2), glial fibrillary acidic protein (GFAP), sirtuin 1, and mitogen-activated protein kinase (p38 MAPK) with no significant alteration of brain-derived neurotrophic factor (BDNF). In summary, berberine could partially ameliorate LPS-induced cognitive deficits via partial suppression of apoptotic cascade, neuroinflammation, oxido-nitrosative stress, AChE, MAPK, and restoration of sirtuin 1.

Keywords

Berberine Lipopolysaccharide Learning and memory Apoptosis Oxidative stress Neuroinflammation 

Abbreviations

3-NT

3-nitrotyrosine

AChE

acetylcholinesterase

AD

Alzheimer’s disease

BDNF

brain-derived neurotrophic factor

Cox 2

cyclooxygenase 2

GFAP

glial fibrillary acidic protein

GSH

glutathione

GPx

glutathione peroxidase

IL-6

interleukin 6

LPS

lipopolysaccharide

MDA

malondialdehyde

MAPK

mitogen-activated protein kinase

NF-κB

nuclear factor-kappa B

NORT

novel object recognition task

RNS

reactive nitrogen species

ROS

reactive oxygen species

Sirt 1

sirtuin 1

SOD

superoxide dismutase

TLR4

toll-like receptor 4

TNFα

tumor necrosis factor α

Notes

Acknowledgements

This research project was the result of MD thesis project (Sepideh Sadraie), approved and financially supported in part by Shahed University in 2016.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

References

  1. Abdel Moneim AE (2015) The neuroprotective effect of berberine in mercury-induced neurotoxicity in rats. Metab Brain Dis 30:935–942.  https://doi.org/10.1007/s11011-015-9652-6 CrossRefPubMedGoogle Scholar
  2. Abdel-Salam OM, Omara EA, Mohammed NA, Youness ER, Khadrawy YA, Sleem AA (2013) Cerebrolysin attenuates cerebral and hepatic injury due to lipopolysaccharide in rats. Drug Discov Ther 7:261–271CrossRefGoogle Scholar
  3. Ahshin-Majd S, Zamani S, Kiamari T, Kiasalari Z, Baluchnejadmojarad T, Roghani M (2016) Carnosine ameliorates cognitive deficits in streptozotocin-induced diabetic rats: possible involved mechanisms. Peptides 86:102–111.  https://doi.org/10.1016/j.peptides.2016.10.008 CrossRefPubMedGoogle Scholar
  4. Al-Amin MM, Choudhury MFR, Chowdhury AS, Chowdhury TR, Jain P, Kazi M, Alkholief M, Alshehri SM, Reza HM (2018) Pretreatment with risperidone ameliorates systemic LPS-induced oxidative stress in the cortex and Hippocampus. Front Neurosci 12:384.  https://doi.org/10.3389/fnins.2018.00384 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Ali MR, Abo-Youssef AM, Messiha BA, Khattab MM (2016) Tempol and perindopril protect against lipopolysaccharide-induced cognition impairment and amyloidogenesis by modulating brain-derived neurotropic factor, neuroinflammation and oxido-nitrosative stress. Naunyn Schmiedeberg's Arch Pharmacol 389:637–656.  https://doi.org/10.1007/s00210-016-1234-6 CrossRefGoogle Scholar
  6. Andrade VS, Rojas DB, de Andrade RB, Kim TDH, Vizuete AF, Zanatta A, Wajner M, Goncalves CS, Wannmacher CMD (2017) A possible anti-inflammatory effect of proline in the brain cortex and cerebellum of rats. Mol Neurobiol.  https://doi.org/10.1007/s12035-017-0626-z
  7. Antunes M, Biala G (2012) The novel object recognition memory: neurobiology, test procedure, and its modifications. Cogn Process 13:93–110.  https://doi.org/10.1007/s10339-011-0430-z CrossRefPubMedGoogle Scholar
  8. Aski ML, Rezvani ME, Khaksari M, Hafizi Z, Pirmoradi Z, Niknazar S, Mehrjerdi FZ (2018) Neuroprotective effect of berberine chloride on cognitive impairment and hippocampal damage in experimental model of vascular dementia. Iran J Basic Med Sci 21:53–58.  https://doi.org/10.22038/ijbms.2017.23195.5865 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Baluchnejadmojarad T, Kiasalari Z, Afshin-Majd S, Ghasemi Z, Roghani M (2017) S-allyl cysteine ameliorates cognitive deficits in streptozotocin-diabetic rats via suppression of oxidative stress, inflammation, and acetylcholinesterase. Eur J Pharmacol 794:69–76.  https://doi.org/10.1016/j.ejphar.2016.11.033 CrossRefPubMedGoogle Scholar
  10. 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 72:248–254CrossRefGoogle Scholar
  11. Carvalho FB, Gutierres JM, Bueno A, Agostinho P, Zago AM, Vieira J, Fruhauf P, Cechella JL, Nogueira CW, Oliveira SM, Rizzi C, Spanevello RM, Duarte MM, Duarte T, Dellagostin OA, Andrade CM (2016) Anthocyanins control neuroinflammation and consequent memory dysfunction in mice exposed to lipopolysaccharide. Mol Neurobiol.  https://doi.org/10.1007/s12035-016-9900-8
  12. Cayero-Otero MD, Espinosa-Oliva AM, Herrera AJ, Garcia-Dominguez I, Fernandez-Arevalo M, Martin-Banderas L, de Pablos RM (2018) Potential use of nanomedicine for the anti-inflammatory treatment of neurodegenerative diseases. Curr Pharm Des.  https://doi.org/10.2174/1381612824666180403113015
  13. Chowdhury AA, Gawali NB, Munshi R, Juvekar AR (2017) Trigonelline insulates against oxidative stress, proinflammatory cytokines and restores BDNF levels in lipopolysaccharide induced cognitive impairment in adult mice. Metab Brain Dis.  https://doi.org/10.1007/s11011-017-0147-5
  14. Claiborne A (1985) Catalase activity. In: CRC Handbook of Methods for Oxygen Radical Research, edited by Greenwald RA. Boca Raton, FL: CRC.: 283–284Google Scholar
  15. Czerniawski J, Miyashita T, Lewandowski G, Guzowski JF (2015) Systemic lipopolysaccharide administration impairs retrieval of context-object discrimination, but not spatial, memory: evidence for selective disruption of specific hippocampus-dependent memory functions during acute neuroinflammation. Brain Behav Immun 44:159–166.  https://doi.org/10.1016/j.bbi.2014.09.014 CrossRefPubMedGoogle Scholar
  16. Domitrovic R, Cvijanovic O, Pernjak-Pugel E, Skoda M, Mikelic L, Crncevic-Orlic Z (2013) Berberine exerts nephroprotective effect against cisplatin-induced kidney damage through inhibition of oxidative/nitrosative stress, inflammation, autophagy and apoptosis. Food Chem Toxicol 62:397–406.  https://doi.org/10.1016/j.fct.2013.09.003 CrossRefPubMedGoogle Scholar
  17. Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77CrossRefGoogle Scholar
  18. Ellman GL, Courtney KD, Andres V Jr, Feather-Stone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95CrossRefGoogle Scholar
  19. Fan LW, Kaizaki A, Tien LT, Pang Y, Tanaka S, Numazawa S, Bhatt AJ, Cai Z (2013) Celecoxib attenuates systemic lipopolysaccharide-induced brain inflammation and white matter injury in the neonatal rats. Neuroscience 240:27–38.  https://doi.org/10.1016/j.neuroscience.2013.02.041 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Fischer R, Maier O (2015) Interrelation of oxidative stress and inflammation in neurodegenerative disease: role of TNF. Oxidative Med Cell Longev 2015:610813–610818.  https://doi.org/10.1155/2015/610813 CrossRefGoogle Scholar
  21. Fruhauf PK, Ineu RP, Tomazi L, Duarte T, Mello CF, Rubin MA (2015) Spermine reverses lipopolysaccharide-induced memory deficit in mice. J Neuroinflammation 12:3.  https://doi.org/10.1186/s12974-014-0220-5 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Gotz T, Gunther A, Witte OW, Brunkhorst FM, Seidel G, Hamzei F (2014) Long-term sequelae of severe sepsis: cognitive impairment and structural brain alterations - an MRI study (LossCog MRI). BMC Neurol 14:145.  https://doi.org/10.1186/1471-2377-14-145 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Gu SM, Park MH, Hwang CJ, Song HS, Lee US, Han SB, Oh KW, Ham YW, Song MJ, Son DJ, Hong JT (2015) Bee venom ameliorates lipopolysaccharide-induced memory loss by preventing NF-kappaB pathway. J Neuroinflammation 12:124.  https://doi.org/10.1186/s12974-015-0344-2 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Haba R, Shintani N, Onaka Y, Wang H, Takenaga R, Hayata A, Baba A, Hashimoto H (2012) Lipopolysaccharide affects exploratory behaviors toward novel objects by impairing cognition and/or motivation in mice: possible role of activation of the central amygdala. Behav Brain Res 228:423–431.  https://doi.org/10.1016/j.bbr.2011.12.027 CrossRefPubMedGoogle Scholar
  25. 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.  https://doi.org/10.1186/1742-2094-5-15 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Huang SX, Qiu G, Cheng FR, Pei Z, Yang Z, Deng XH, Zhu JH, Chen L, Chen CC, Lin WF, Liu Y, Liu Z, Zhu FQ (2018) Berberine protects secondary injury in mice with traumatic brain injury through anti-oxidative and anti-inflammatory modulation. Neurochem Res 43:1814–1825.  https://doi.org/10.1007/s11064-018-2597-5 CrossRefPubMedGoogle Scholar
  27. Hussien HM, Abd-Elmegied A, Ghareeb DA, Hafez HS, Ahmed HEA, El-Moneam NA (2018) Neuroprotective effect of berberine against environmental heavy metals-induced neurotoxicity and Alzheimer's-like disease in rats. Food Chem Toxicol 111:432–444.  https://doi.org/10.1016/j.fct.2017.11.025 CrossRefPubMedGoogle Scholar
  28. Islam MT (2017) Oxidative stress and mitochondrial dysfunction-linked neurodegenerative disorders. Neurol Res 39:73–82.  https://doi.org/10.1080/01616412.2016.1251711 CrossRefPubMedGoogle Scholar
  29. Jangra A, Sriram CS, Lahkar M (2016) Lipopolysaccharide-induced behavioral alterations are alleviated by sodium Phenylbutyrate via attenuation of oxidative stress and Neuroinflammatory Cascade. Inflammation 39:1441–1452.  https://doi.org/10.1007/s10753-016-0376-5 CrossRefPubMedGoogle Scholar
  30. Jiang W, Li S, Li X (2015) Therapeutic potential of berberine against neurodegenerative diseases. Sci China Life Sci 58:564–569.  https://doi.org/10.1007/s11427-015-4829-0 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Khajevand-Khazaei MR, Ziaee P, Motevalizadeh SA, Rohani M, Afshin-Majd S, Baluchnejadmojarad T, Roghani M (2018) Naringenin ameliorates learning and memory impairment following systemic lipopolysaccharide challenge in the rat. Eur J Pharmacol 826:114–122.  https://doi.org/10.1016/j.ejphar.2018.03.001 CrossRefPubMedGoogle Scholar
  32. Kim M, Cho KH, Shin MS, Lee JM, Cho HS, Kim CJ, Shin DH, Yang HJ (2014) Berberine prevents nigrostriatal dopaminergic neuronal loss and suppresses hippocampal apoptosis in mice with Parkinson's disease. Int J Mol Med 33:870–878.  https://doi.org/10.3892/ijmm.2014.1656 CrossRefPubMedGoogle Scholar
  33. Leal G, Bramham CR, Duarte CB (2017) BDNF and hippocampal synaptic plasticity. Vitam Horm 104:153–195.  https://doi.org/10.1016/bs.vh.2016.10.004 CrossRefPubMedGoogle Scholar
  34. Lee YY, Park JS, Jung JS, Kim DH, Kim HS (2013) Anti-inflammatory effect of ginsenoside Rg5 in lipopolysaccharide-stimulated BV2 microglial cells. Int J Mol Sci 14:9820–9833.  https://doi.org/10.3390/ijms14059820 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, Ahn BW, Shaltiel S, Stadtman ER (1990) Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186:464–478CrossRefGoogle Scholar
  36. Li M, Li C, Yu H, Cai X, Shen X, Sun X, Wang J, Zhang Y, Wang C (2017) Lentivirus-mediated interleukin-1beta (IL-1beta) knock-down in the hippocampus alleviates lipopolysaccharide (LPS)-induced memory deficits and anxiety- and depression-like behaviors in mice. J Neuroinflammation 14:190.  https://doi.org/10.1186/s12974-017-0964-9 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Lin Y, Sheng M, Weng Y, Xu R, Lu N, Du H, Yu W (2017) Berberine protects against ischemia/reperfusion injury after orthotopic liver transplantation via activating Sirt1/FoxO3alpha induced autophagy. Biochem Biophys Res Commun 483:885–891.  https://doi.org/10.1016/j.bbrc.2017.01.028 CrossRefPubMedGoogle Scholar
  38. Liu L, Zhang Q, Cai Y, Sun D, He X, Wang L, Yu D, Li X, Xiong X, Xu H, Yang Q, Fan X (2016) Resveratrol counteracts lipopolysaccharide-induced depressive-like behaviors via enhanced hippocampal neurogenesis. Oncotarget 7:56045–56059.  https://doi.org/10.18632/oncotarget.11178 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Lykhmus O, Mishra N, Koval L, Kalashnyk O, Gergalova G, Uspenska K, Komisarenko S, Soreq H, Skok M (2016) Molecular mechanisms regulating LPS-induced inflammation in the brain. Front Mol Neurosci 9:19.  https://doi.org/10.3389/fnmol.2016.00019 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Lykhmus O, Uspenska K, Koval L, Lytovchenko D, Voytenko L, Horid'ko T, Kosiakova H, Gula N, Komisarenko S, Skok M (2017) N-Stearoylethanolamine protects the brain and improves memory of mice treated with lipopolysaccharide or immunized with the extracellular domain of alpha7 nicotinic acetylcholine receptor. Int Immunopharmacol 52:290–296.  https://doi.org/10.1016/j.intimp.2017.09.023 CrossRefPubMedGoogle Scholar
  41. Maleki SN, Aboutaleb N, Souri F (2018) Berberine confers neuroprotection in coping with focal cerebral ischemia by targeting inflammatory cytokines. J Chem Neuroanat 87:54–59.  https://doi.org/10.1016/j.jchemneu.2017.04.008 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Mayer AM (1998) Therapeutic implications of microglia activation by lipopolysaccharide and reactive oxygen species generation in septic shock and central nervous system pathologies: a review. Medicina (Buenos Aires) 58:377–385Google Scholar
  43. Mirahmadi SM, Shahmohammadi A, Rousta AM, Azadi MR, Fahanik-Babaei J, Baluchnejadmojarad T, Roghani M (2018) Soy isoflavone genistein attenuates lipopolysaccharide-induced cognitive impairments in the rat via exerting anti-oxidative and anti-inflammatory effects. Cytokine 104:151–159.  https://doi.org/10.1016/j.cyto.2017.10.008 CrossRefPubMedGoogle Scholar
  44. Moghaddam HK, Baluchnejadmojarad T, Roghani M, Khaksari M, Norouzi P, Ahooie M, Mahboobi F (2014) Berberine ameliorate oxidative stress and astrogliosis in the hippocampus of STZ-induced diabetic rats. Mol Neurobiol 49:820–826.  https://doi.org/10.1007/s12035-013-8559-7 CrossRefPubMedGoogle Scholar
  45. Moraes CA, Santos G, de Sampaio e Spohr TC, D′Avila JC, Lima FR, Benjamim CF, Bozza FA, Gomes FC (2015) Activated Microglia-Induced Deficits in Excitatory Synapses Through IL-1beta: Implications for Cognitive Impairment in Sepsis. Mol Neurobiol 52:653–663.  https://doi.org/10.1007/s12035-014-8868-5 CrossRefPubMedGoogle Scholar
  46. Morris G, Reiche EMV, Murru A, Carvalho AF, Maes M, Berk M, Puri BK (2018) Multiple immune-inflammatory and oxidative and Nitrosative stress pathways explain the frequent presence of depression in multiple sclerosis. Mol Neurobiol 55:6282–6306.  https://doi.org/10.1007/s12035-017-0843-5 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Movsesyan VAYA, Dabaghyan EA, Stoica BA, Faden AI (2002) Ceramide induces neuronal apoptosis through the caspase-9/caspase-3 pathway. Biochem Biophys Res Commun 299:201–207CrossRefGoogle Scholar
  48. Nitta A, Murai R, Suzuki N, Ito H, Nomoto H, Katoh G, Furukawa Y, Furukawa S (2002) Diabetic neuropathies in brain are induced by deficiency of BDNF. Neurotoxicol Teratol 24:695–701CrossRefGoogle Scholar
  49. Nolan Y, Vereker E, Lynch AM, Lynch MA (2003) Evidence that lipopolysaccharide-induced cell death is mediated by accumulation of reactive oxygen species and activation of p38 in rat cortex and hippocampus. Exp Neurol 184:794–804.  https://doi.org/10.1016/s0014-4886(03)00301-7 CrossRefPubMedGoogle Scholar
  50. Notter T, Coughlin JM, Gschwind T, Weber-Stadlbauer U, Wang Y, Kassiou M, Vernon AC, Benke D, Pomper MG, Sawa A, Meyer U (2018) Translational evaluation of translocator protein as a marker of neuroinflammation in schizophrenia. Mol Psychiatry 23:323–334.  https://doi.org/10.1038/mp.2016.248 CrossRefPubMedGoogle Scholar
  51. Ownby RL (2010) Neuroinflammation and cognitive aging. Curr Psychiatry Rep 12:39–45.  https://doi.org/10.1007/s11920-009-0082-1 CrossRefPubMedGoogle Scholar
  52. Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–169PubMedGoogle Scholar
  53. Pardon MC (2015) Lipopolysaccharide hyporesponsiveness: protective or damaging response to the brain? Romanian J Morphol Embryol 56:903–913Google Scholar
  54. Patil S, Tawari S, Mundhada D, Nadeem S (2015) Protective effect of berberine, an isoquinoline alkaloid ameliorates ethanol-induced oxidative stress and memory dysfunction in rats. Pharmacol Biochem Behav 136:13–20.  https://doi.org/10.1016/j.pbb.2015.07.001 CrossRefPubMedGoogle Scholar
  55. Patrignani C, Lafont DT, Muzio V, Gréco B, Hooft van Huijsduijnen R, Zaratin PF (2010) Characterization of protein tyrosine phosphatase H1 knockout mice in animal models of local and systemic inflammation. J Inflamm (Lond) 7:16.  https://doi.org/10.1186/1476-9255-7-16
  56. Qiao Y, Bai XF, Du YG (2011) Chitosan oligosaccharides protect mice from LPS challenge by attenuation of inflammation and oxidative stress. Int Immunopharmacol 11:121–127.  https://doi.org/10.1016/j.intimp.2010.10.016 CrossRefPubMedGoogle Scholar
  57. Raoufi S, Baluchnejadmojarad T, Roghani M, Ghazanfari T, Khojasteh F, Mansouri M (2015) Antidiabetic potential of salvianolic acid B in multiple low-dose streptozotocin-induced diabetes. Pharm Biol 53:1803–1809.  https://doi.org/10.3109/13880209.2015.1008148 CrossRefPubMedGoogle Scholar
  58. Roghani M, Joghataie MT, Jalali MR, Baluchnejadmojarad T (2006) Time course of changes in passive avoidance and Y-maze performance in male diabetic rats. Iran Biomed J 10:99–104Google Scholar
  59. Sedaghat R, Taab Y, Kiasalari Z, Afshin-Majd S, Baluchnejadmojarad T, Roghani M (2017) Berberine ameliorates intrahippocampal kainate-induced status epilepticus and consequent epileptogenic process in the rat: underlying mechanisms. Biomed Pharmacother 87:200–208.  https://doi.org/10.1016/j.biopha.2016.12.109 CrossRefPubMedGoogle Scholar
  60. Sedlak J, Lindsay RH (1968) Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman's reagent. Anal Biochem 25:192–205CrossRefGoogle Scholar
  61. Shagirtha K, Pari L (2011) Hesperetin, a citrus flavonone, protects potentially cadmium induced oxidative testicular dysfunction in rats. Ecotoxicol Environ Saf 74:2105–2111.  https://doi.org/10.1016/j.ecoenv.2011.06.002 CrossRefPubMedGoogle Scholar
  62. Shah SA, Khan M, Jo MH, Jo MG, Amin FU, Kim MO (2017) Melatonin stimulates the SIRT1/Nrf2 signaling pathway counteracting lipopolysaccharide (LPS)-induced oxidative stress to rescue postnatal rat brain. CNS Neurosci Ther 23:33–44.  https://doi.org/10.1111/cns.12588 CrossRefPubMedGoogle Scholar
  63. Shen JD, Ma LG, Hu CY, Pei YY, Jin SL, Fang XY, Li YC (2016) Berberine up-regulates the BDNF expression in hippocampus and attenuates corticosterone-induced depressive-like behavior in mice. Neurosci Lett 614:77–82.  https://doi.org/10.1016/j.neulet.2016.01.002 CrossRefPubMedGoogle Scholar
  64. Silverman HA, Dancho M, Regnier-Golanov A, Nasim M, Ochani M, Olofsson PS, Ahmed M, Miller EJ, Chavan SS, Golanov E, Metz CN, Tracey KJ, Pavlov VA (2014) Brain region-specific alterations in the gene expression of cytokines, immune cell markers and cholinergic system components during peripheral endotoxin-induced inflammation. Mol Med 20:601–611.  https://doi.org/10.2119/molmed.2014.00147 CrossRefGoogle Scholar
  65. Sohanaki H, Baluchnejadmojarad T, Nikbakht F, Roghani M (2016) Pelargonidin improves passive avoidance task performance in a rat amyloid Beta25-35 model of Alzheimer’s disease via estrogen receptor independent pathways. Acta Medica Iranica:245–250Google Scholar
  66. Stuart SA, Robertson JD, Marrion NV, Robinson ES (2013) Chronic pravastatin but not atorvastatin treatment impairs cognitive function in two rodent models of learning and memory. PLoS One 8:e75467.  https://doi.org/10.1371/journal.pone.0075467 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Tan XS, Ma JY, Feng R, Ma C, Chen WJ, Sun YP, Fu J, Huang M, He CY, Shou JW, He WY, Wang Y, Jiang JD (2013) Tissue distribution of berberine and its metabolites after oral administration in rats. PLoS One 8:e77969.  https://doi.org/10.1371/journal.pone.0077969
  68. Tanila H (2017) The role of BDNF in Alzheimer's disease. Neurobiol Dis 97:114–118.  https://doi.org/10.1016/j.nbd.2016.05.008 CrossRefPubMedGoogle Scholar
  69. Tyagi E, Agrawal R, Nath C, Shukla R (2010) Effect of melatonin on neuroinflammation and acetylcholinesterase activity induced by LPS in rat brain. Eur J Pharmacol 640:206–210.  https://doi.org/10.1016/j.ejphar.2010.04.041 CrossRefPubMedGoogle Scholar
  70. Vasconcelos AR, Yshii LM, Viel TA, Buck HS, Mattson MP, Scavone C, Kawamoto EM (2014) Intermittent fasting attenuates lipopolysaccharide-induced neuroinflammation and memory impairment. J Neuroinflammation 11:85.  https://doi.org/10.1186/1742-2094-11-85 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Wang Y (2013) Attenuation of berberine on lipopolysaccharide-induced inflammatory and apoptosis responses in beta-cells via TLR4-independent JNK/NF-kappaB pathway. Pharm Biol.  https://doi.org/10.3109/13880209.2013.840851
  72. Wang J, Zhang Y (2018) Neuroprotective effect of berberine agonist against impairment of learning and memory skills in severe traumatic brain injury via Sirt1/p38 MAPK expression. Mol Med Rep 17:6881–6886.  https://doi.org/10.3892/mmr.2018.8674 CrossRefPubMedGoogle Scholar
  73. Wang SX, Xiong XM, Song T, Liu LY (2005) Protective effects of cariporide on endothelial dysfunction induced by high glucose. Acta Pharmacol Sin 26:329–333.  https://doi.org/10.1111/j.1745-7254.2005.00042.x CrossRefPubMedGoogle Scholar
  74. Wang HC, Wang BD, Chen MS, Chen H, Sun CF, Shen G, Zhang JM (2018a) Neuroprotective effect of berberine against learning and memory deficits in diffuse axonal injury. Exp Ther Med 15:1129–1135.  https://doi.org/10.3892/etm.2017.5496 CrossRefPubMedGoogle Scholar
  75. Wang J, Li L, Wang Z, Cui Y, Tan X, Yuan T, Liu Q, Liu Z, Liu X (2018b) Supplementation of lycopene attenuates lipopolysaccharide-induced amyloidogenesis and cognitive impairments via mediating neuroinflammation and oxidative stress. J Nutr Biochem 56:16–25.  https://doi.org/10.1016/j.jnutbio.2018.01.009 CrossRefPubMedGoogle Scholar
  76. Wang Y, Wang M, Fan K, Li T, Yan T, Wu B, Bi K, Jia Y (2018c) Protective effects of Alpinae Oxyphyllae Fructus extracts on lipopolysaccharide-induced animal model of Alzheimer's disease. J Ethnopharmacol 217:98–106.  https://doi.org/10.1016/j.jep.2018.02.015 CrossRefPubMedGoogle Scholar
  77. Widmann CN, Heneka MT (2014) Long-term cerebral consequences of sepsis. Lancet Neurol 13:630–636.  https://doi.org/10.1016/s1474-4422(14)70017-1 CrossRefPubMedGoogle Scholar
  78. Yu L, Li Q, Yu B, Yang Y, Jin Z, Duan W, Zhao G, Zhai M, Liu L, Yi D, Chen M, Yu S (2016) Berberine attenuates myocardial ischemia/reperfusion injury by reducing oxidative stress and inflammation response: role of silent information regulator 1. Oxidative Med Cell Longev 2016:1689602.  https://doi.org/10.1155/2016/1689602 CrossRefGoogle Scholar
  79. Zakaria R, Wan Yaacob WM, Othman Z, Long I, Ahmad AH, Al-Rahbi B (2017) Lipopolysaccharide-induced memory impairment in rats: a model of Alzheimer's disease. Physiol Res 66:553–565PubMedGoogle Scholar
  80. Zarezadeh M, Baluchnejadmojarad T, Kiasalari Z, Afshin-Majd S, Roghani M (2017) Garlic active constituent s-allyl cysteine protects against lipopolysaccharide-induced cognitive deficits in the rat: possible involved mechanisms. Eur J Pharmacol 795:13–21.  https://doi.org/10.1016/j.ejphar.2016.11.051 CrossRefPubMedGoogle Scholar
  81. Zhang J, Yu C, Zhang X, Chen H, Dong J, Lu W, Song Z, Zhou W (2018) Porphyromonas gingivalis lipopolysaccharide induces cognitive dysfunction, mediated by neuronal inflammation via activation of the TLR4 signaling pathway in C57BL/6 mice. J Neuroinflammation 15:37.  https://doi.org/10.1186/s12974-017-1052-x CrossRefPubMedPubMedCentralGoogle Scholar
  82. Zhu B, Wang ZG, Ding J, Liu N, Wang DM, Ding LC, Yang C (2014) Chronic lipopolysaccharide exposure induces cognitive dysfunction without affecting BDNF expression in the rat hippocampus. Exp Ther Med 7:750–754.  https://doi.org/10.3892/etm.2014.1479 CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Sepideh Sadraie
    • 1
  • Zahra Kiasalari
    • 2
  • Mohadeseh Razavian
    • 1
  • Shekoofe Azimi
    • 3
  • Ladan Sedighnejad
    • 3
  • Siamak Afshin-Majd
    • 2
    • 4
  • Tourandokht Baluchnejadmojarad
    • 5
  • Mehrdad Roghani
    • 2
    Email author
  1. 1.School of MedicineShahed UniversityTehranIran
  2. 2.Neurophysiology Research CenterShahed UniversityTehranIran
  3. 3.Department of Physiology, School of MedicineShahed UniversityTehranIran
  4. 4.Department of Neurology, School of MedicineShahed UniversityTehranIran
  5. 5.Department of Physiology, School of MedicineIran University of Medical SciencesTehranIran

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