Neuropharmacological effects of honey in lipopolysaccharide-induced neuroinflammation, cognitive impairment, anxiety and motor impairment

References

• Stephenson J, Nutma E, van der Valk P, Amor S. Inflammation in CNS neurodegenerative diseases. Immunology. 2018;154(2):204–19.
   PubMed Web of Science ®Google Scholar
• Bassani TB, Vital MA, Rauh LK. Neuroinflammation in the pathophysiology of Parkinson’s disease and therapeutic evidence of anti-inflammatory drugs. Arq Neuropsiquiatr. 2015;73(7):616–23.
   PubMed Web of Science ®Google Scholar
• Clayton KA, Van Enoo AA, Ikezu T. Alzheimer’s disease: the role of microglia in brain homeostasis and proteopathy. Front Neurosci. 2017;11:680. doi:10.3389/fnins.2017.00680.
   PubMed Web of Science ®Google Scholar
• Li T, Zhang S. Microgliosis in the injured brain: infiltrating cells and reactive microglia both play a role. Neuroscientist. 2016;22(2):165–70.
   PubMed Web of Science ®Google Scholar
• Brown GC. The endotoxin hypothesis of neurodegeneration. J Neuroinflammation. 2019;16(1):180. doi:10.1186/s12974-019-1564-7.
   PubMed Web of Science ®Google Scholar
• Eduviere AT, Umukoro S, Adeoluwa OA, Omogbiya IA, Aluko OM. Possible mechanisms involved in attenuation of lipopolysaccharide-induced memory deficits by methyl jasmonate in mice. Neurochem Res. 2016;41(12):3239–49.
   PubMed Web of Science ®Google Scholar
• Emokpae O, Ben-Azu B, Ajayi AM, Umukoro S. d-Ribose-l-cysteine attenuates lipopolysaccharide-induced memory deficits through inhibition of oxidative stress, release of proinflammatory cytokines, and nuclear factor-kappa B expression in mice. Naunyn-Schmiedeberg’s Arch Pharmacol. 2020: May;393(5):909–925. doi:10.1007/s00210-019-01805-0. Epub 2020 Jan 7. PMID: 31907583.
   Google Scholar
• Zakaria R, Wan Yaacob WMH, Othman Z, Long I, Ahmad AH, Al-Rahbi B. Lipopolysaccharide-induced memory impairment in rats: a model of Alzheimer’s disease. Physiol Res. 2017;Sep 22;66(4):553–565. doi:10.33549/physiolres.933480. Epub 2017 Apr 12. PMID: 28406691.
   Google Scholar
• Ajmone-Cat MA, Bernardo A, Greco A, Minghetti L. Non-steroidal anti-inflammatory drugs and brain inflammation: effects on microglial functions. Pharmaceuticals. 2010;3(6):1949–65.
   Google Scholar
• El-Seedi HR, Khalifa SA, Abd El-Wahed A, Gao R, Guo Z, Tahir HE, et al. Honeybee products: an updated review of neurological actions. Trends Food Sci Technol. 2020;101:17–27.
   Web of Science ®Google Scholar
• Perrone MG, Centonze A, Miciaccia M, Ferorelli S, Scilimati A. Cyclooxygenase inhibition safety and efficacy in inflammation-based psychiatric disorders. Molecules. 2020;25(22):5388.
   PubMed Web of Science ®Google Scholar
• Tauber JP, Collins WR, Schwarz RS, Chen Y, Grubbs K, Huang Q, et al. Natural product medicines for honey bees: perspective and protocols. Insects. 2019;10(10):356.
   PubMed Web of Science ®Google Scholar
• Wieczorek J, Pietrzak M, Pomianowski J, Wieczorek Z. Honey as a source of bioactive compounds. Pol J Nat Sci. 2014;29:275–85.
   Google Scholar
• Escuredo O, Míguez M, Fernández-González M, Carmen Seijo M. Nutritional value and antioxidant activity of honeys produced in a European atlantic area. Food Chem. 2013;138(2-3):851–6. doi:10.1016/j.foodchem.2012.11.015.
   PubMed Web of Science ®Google Scholar
• Lachman J, Orsák M, Hejtmánková A, Kovářová E. Evaluation of antioxidant activity and total phenolics of selected Czech honeys, LWT. Food Sci Technol. 2010;43(1):52–8. doi:10.1016/j.lwt.2009.06.008. ISSN 0023-6438, https://www.sciencedirect.com/science/article/pii/S0023643809001820.
   Web of Science ®Google Scholar
• Wilczyńska A. Phenolic content and antioxidant activity of different types of Polish honey – a short report. Pol J Food Nutr Sci. 2010;60:309–13.
   Google Scholar
• Alvarez-Suarez JM, Tulipani S, Romandini S, Bertoli E, Battino M. Contribution of honey in nutrition and human health: a review. Mediterr J Nutr Metab. 2010;3:15–23.
   Google Scholar
• Othman Z, Zakaria R, Hussain N, Hazlina N, Shafin N, Hassan A, et al. Potential role of honey in learning and memory. Med Sci. 2015;3:3–15. doi:10.3390/medsci3020003.
   Google Scholar
• Alnaqdy A, Al-Jabri A, Al Mahrooqi Z, Nzeako B, Nsanze H. Inhibition effect of honey on the adherence of Salmonella to intestinal epithelial cells in vitro. Int J Food Microbiol. 2005;103:347–51.
   PubMed Web of Science ®Google Scholar
• Bansal V, Medhi B, Pandhi P. Honey – a remedy rediscovered and its therapeutic utility. Kathmandu Univ Med J. 2005;3:305–9.
   PubMedGoogle Scholar
• Al-Waili NS, Haq A. Effect of honey on antibody production against thymus-dependent and thymus-independent antigens in primary and secondary immune responses. J Med Food. 2004;7:491–4.
   PubMed Web of Science ®Google Scholar
• Yaghoobi N, Al-Waili N, Ghayour-Mobarhan M, Parizadeh SMR, Abasalti Z, Yaghoobi Z, et al. Natural honey and cardiovascular risk factors; effects on blood glucose, cholesterol, triacylglycerole, CRP and body weight compared with sucrose. Sci World J. 2008;8:463–9.
   Web of Science ®Google Scholar
• Khalil MI, Sulaiman SA. The potential role of honey and its polyphenols in preventing heart diseases: a review. Afr J Tradit Complement Altern Med. 2010;7:315–21.
   PubMed Web of Science ®Google Scholar
• Najafi M, Shaseb E, Ghaffary S, Fakhrju A, Eteraf-Oskouei T. Effects of chronic oral administration of natural honey on ischemia/reperfusion-induced arrhythmias in isolated rat heart. Iran J Basic Med Sci. 2011;14:75–81.
   Web of Science ®Google Scholar
• Beretta G, Granata P, Ferrero M, Orioli M, Maffei Facino R. Standardization of antioxidant properties of honey by a combination of spectrophotometric/fluorimetric assays and chemometrics. Anal Chim Acta. 2005;533:185–91.
   Web of Science ®Google Scholar
• Blasa M, Candiracci M, Accorsi A, Piacentini MP, Piatti E. Honey flavonoids as protection agents against oxidative damage to human red blood cells. Food Chem. 2007;104:1635–40.
   Web of Science ®Google Scholar
• Al-Waili NS, Boni NS. Natural honey lowers plasma prostaglandin concentrations in normal individuals. J Med Food. 2003;6:129–33.
   PubMedGoogle Scholar
• Markelov VV, Trushin MV. Bee venom therapy and low dose naltrexone for treatment of multiple sclerosis. Nepal J Neurosci. 2006;3:71–7.
   Google Scholar
• Bilsel Y, Bugra D, Yamaner S, Bulut T, Cevikbas U, Turkoglu U. Could honey have a place in colitis therapy? Effects of honey, prednisolone and disulfiram on inflammation, nitric oxide, and free radical formation. Dig Surg. 2002;19:306–12.
   PubMed Web of Science ®Google Scholar
• Oyefuga O, Ajani E, Salau B, Adebawo OO. Honey consumption and its anti-ageing potency in white Wister albino rats. Schol J Biol Sci. 2012;2:117–22.
   Google Scholar
• Álvarez R, Araya H, Navarro-Lisboa R, Lopez de Dicastillo C. Evaluation of polyphenols and antioxidant capacity of fruits and vegetables using a modified enzymatic extraction method. Food Technol Biotechnol. 2016;54(4). doi:10.17113/ftb.54.04.16.4497.
   PubMedGoogle Scholar
• Woong L, Lee Y, Yuk D, Choi D-Y, Ban S, Oh K, Hong J. Neuro-inflammation induced by lipopolysaccharide causes cognitive impairment through enhancement of β-amyloid generation. J Neuroinflammat. 2008;5(37). doi:10.1186/1742-2094-5-37.
   Google Scholar
• Tyagi E, Agrawal R, Nath C, Shukla R. Influence of LPS-induced neuroinflammation on acetylcholinesterase activity in rat brain. J Neuroimmunol. 2008;205:51–6. doi:10.1016/j.jneuroim.2008.08.015.
   PubMed Web of Science ®Google Scholar
• Lueptow L. Novel object recognition test for the investigation of learning and memory in mice. J Visual Exp. 2017; doi:10.3791/55718.
   PubMedGoogle Scholar
• Walf A, Frye C. The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Protoc. 2007;2:322–8. doi:10.1038/nprot.2007.44.
   PubMed Web of Science ®Google Scholar
• Onasanwo A, Chatterjee M, Palit G. Antidepressant and anxiolytic potentials of dichloromethane fraction from hedranthera barteri. Afr J Biomed Res. 2010;13(1):75–81.
   Google Scholar
• Seibenhener M, Wooten M. Use of the open field maze to measure locomotor and anxiety-like behavior in mice. J Visual Exp. 2015. doi:10.3791/52434.
   PubMedGoogle Scholar
• Garcia YJ, Rodríguez-Malaver AJ, Peñaloza N. Lipid peroxidation measurement by thiobarbituric acid assay in rat cerebellar slices. J Neurosci Methods. 2005;144(1):127–35. doi:10.1016/j.jneumeth.2004.10.018.
   PubMed Web of Science ®Google Scholar
• Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR. Analysis of nitrate, nitrite, and [15N] nitrate in biological fluids. Anal Biochem. 1982;126:131–8.
   PubMed Web of Science ®Google Scholar
• Beutler E, Duron O, Kelly BM. Improved method for the determination of blood glutathione. J Lab Clin Med. 1963;61:882–8.
   PubMed Web of Science ®Google Scholar
• Ellman GL, Courtney KD, Andres V Jr., Featherstone RM. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol. 1961;7(2):88–95.
   PubMed Web of Science ®Google Scholar
• Deak T, Bellamy C, D’Agostino L. Exposure to forced swim stress does not alter central production of IL-1. Brain Res. 2003;972:53–63. doi:10.1016/S0006-8993(03)02485-5.
   PubMed Web of Science ®Google Scholar
• Hart MN. Neuroinflammation: mechanisms and management. J Neuropathol Exp Neurol. 2003;62(4):427.
   Google Scholar
• Frühauf PK, Ineu RP, Tomazi L, Duarte T, Mello CF, Rubin MA. Spermine reverses lipopolysaccharide-induced memory deficit in mice. J Neuroinflammat. 2015;12:3. doi:10.1186/s12974-014-0220-5.
   PubMed Web of Science ®Google Scholar
• Franklin AE, Engeland CG, Kavaliers M, Ossenkopp KP. Lipopolysaccharide-induced hypoactivity and behavioral tolerance development are modulated by the light-dark cycle in male and female rats. Psychopharmacology. 2003;170(4):399–408. doi:10.1007/s00213-003-1554-3.
   PubMed Web of Science ®Google Scholar
• Sulakhiya K, Keshavlal GP, Bezbaruah BB, Dwivedi S, Gurjar SS, Munde N, et al. Lipopolysaccharide induced anxiety- and depressive-like behaviour in mice are prevented by chronic pre-treatment of esculetin. Neurosci Lett. 2016;611:106–11. doi:10.1016/j.neulet.2015.11.031.
   PubMed Web of Science ®Google Scholar
• Shytle RD, Mori T, Townsend K, Vendrame M, Sun N, Zeng J, et al. Cholinergic modulation of microglial activation by α7 nicotinic receptors. J Neurochem. 2004;89(2):337–43. doi:10.1046/j.1471-4159.2004.02347.x.
   PubMed Web of Science ®Google Scholar
• Shin LM, Liberzon I. The neurocircuitry of fear, stress and anxiety disorders. Neuropsychopharmacology. 2010;35(1):169–91. doi:10.1038/npp.2009.83.
   PubMed Web of Science ®Google Scholar
• Pennartz CMA, Ito R, Verschure PFMJ, Battaglia FP, Robbins TW. The hippocampal–striatal axis in learning, prediction and goal-directed behavior. Trends Neurosci. 2011;34(10):548–59. doi:10.1016/j.tins.2011.08.001.
   PubMed Web of Science ®Google Scholar
• Noh H, Jeon J, Seo H. Systemic injection of LPS induces region-specific neuroinflammation and mitochondrial dysfunction in normal mouse brain. Neurochem int. 2014;69:35–40. doi:10.1016/j.neuint.2014.02.008.
   Google Scholar
• Zhao X, Cao F, Liu Q, Li X, Xu G, Liu G, Ma J. Behavioral, inflammatory and neurochemical disturbances in LPS and UCMS-induced mouse models of depression. Behav Brain Res. 2017;0. doi:10.1016/j.bbr.2017.05.064.
   Google Scholar