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Current Molecular Pharmacology

Editor-in-Chief

ISSN (Print): 1874-4672
ISSN (Online): 1874-4702

Research Article

Neuroprotective Effects of Shogaol in Metals (Al, As and Pb) and High-fat diet-induced Neuroinflammation and Behavior in Mice

Author(s): Sara Ishaq, Sohana Siyar, Rabia Basri, Amna Liaqat, Armeen Hameed and Touqeer Ahmed*

Volume 16, Issue 7, 2023

Published on: 21 November, 2022

Article ID: e280922209229 Pages: 26

DOI: 10.2174/1874467215666220928110557

Price: $65

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Abstract

Background: Increased exposure of humans to toxic metals and high-fat diet (HFD) consumption severely damages brain health. Natural plant extracts have shown huge potential to treat multiple human diseases.

Objective: The present study was designed to evaluate the protective effects of Shogaol (an active component of ginger) in neuroinflammation and behavioral paradigms in mice treated with metals and HFD.

Methods: 8-11 weeks old male mice model was developed by giving a combination of metals, i.e., Arsenic (As), Lead (Pb) and Aluminum (Al), 25mg/kg each mixed in drinking water with laboratory prepared HFD (40% fat) for a total duration of 72 days. Shogaol treated groups received two doses (2mg/kg & 12mg/kg) of Shogaol along with metals and HFD. The biochemical parameters, including body weights, blood glucose, and kidney and liver functions, were assessed along with the integrity of the blood-brain barrier (BBB). The expression analysis of neuroinflammatory genes (TNF-α, IL-1β & GFAP) was performed using q-PCR in the hippocampus and cortex. The exploratory and anxiety-like behavior was assessed using an open field test, and depressive behavior was assessed through the forced swim test, while learning and memory were assessed using the Morris water maze test and y-maze test.

Results: Shogaol (2mg/kg & 12mg/kg) treatment improved metabolic profile and reduced expression of neuroinflammatory genes in the cortex and the hippocampus. Shogaol treatment improved BBB integrity. Results of the behavioral analysis showed that Shogaol treatment (2mg/kg & 12mg/kg) rescued behavioral impairment and improved anxiety and depression.

Conclusion: Shogaol treatment showed strong therapeutic potential in metals & HFD induced neuroinflammation and improved cognitive functions; thus, can be considered a potential drug candidate in the future.

Keywords: Anxiety, neuroinflammation, blood brain barrier, heavy metals, shogaol, metabolic profile.

Graphical Abstract
[1]
Scott, A.J. Industrialization and urbanization: A geographical agenda. Ann. Assoc. Am. Geogr., 1986, 76(1), 25-37.
[http://dx.doi.org/10.1111/j.1467-8306.1986.tb00101.x]
[2]
Karri, V.; Schuhmacher, M.; Kumar, V. Heavy metals (Pb, Cd, As and MeHg) as risk factors for cognitive dysfunction: A general review of metal mixture mechanism in brain. Environ. Toxicol. Pharmacol., 2016, 48, 203-213.
[http://dx.doi.org/10.1016/j.etap.2016.09.016] [PMID: 27816841]
[3]
Kinuthia, G.K.; Ngure, V.; Beti, D.; Lugalia, R.; Wangila, A.; Kamau, L. Levels of heavy metals in wastewater and soil samples from open drainage channels in Nairobi, Kenya: Community health implication. Sci. Rep., 2020, 10(1), 8434.
[http://dx.doi.org/10.1038/s41598-020-65359-5] [PMID: 32439896]
[4]
Garbarino, J.R.; Hayes, H.C.; Roth, D.A.; Antweiler, R.C.; Brinton, T.I.; Taylor, H.E. Heavy metals in the Mississippi River. US Geological Survey Circular Usgs. Circulation, 1996, 53-72.
[5]
Gardener, H.; Bowen, J.; Callan, S.P. Lead and cadmium contamination in a large sample of United States infant formulas and baby foods. Sci. Total Environ., 2019, 651(Pt 1), 822-827.
[http://dx.doi.org/10.1016/j.scitotenv.2018.09.026] [PMID: 30253364]
[6]
Balistrieri, L.S.; Seal, R.R.; Piatak, N.M.; Paul, B. Assessing the concentration, speciation, and toxicity of dissolved metals during mixing of acid-mine drainage and ambient river water downstream of the Elizabeth Copper Mine, Vermont, USA. Appl. Geochem., 2007, 22(5), 930-952.
[http://dx.doi.org/10.1016/j.apgeochem.2007.02.005]
[7]
Vane, C.H.; Kim, A.W.; Moss-Hayes, V.; Turner, G.; Mills, K.; Chenery, S.R.; Barlow, T.S.; Kemp, A.C.; Engelhart, S.E.; Hill, T.D.; Horton, B.P.; Brain, M. Organic pollutants, heavy metals and toxicity in oil spill impacted salt marsh sediment cores, Staten Island, New York City, USA. Mar. Pollut. Bull., 2020, 151, 110721.
[http://dx.doi.org/10.1016/j.marpolbul.2019.110721] [PMID: 32056581]
[8]
Mo, L.; Zhou, Y.; Gopalakrishnana, G.; Li, X. Spatial distribution and risk assessment of toxic metals in agricultural soils from endemic nasopharyngeal carcinoma region in South China. Open Geosci., 2020, 12(1), 568-579.
[http://dx.doi.org/10.1515/geo-2020-0110]
[9]
Fu, J.; Hu, X.; Tao, X.; Yu, H.; Zhang, X. Risk and toxicity assessments of heavy metals in sediments and fishes from the Yangtze River and Taihu Lake, China. Chemosphere, 2013, 93(9), 1887-1895.
[http://dx.doi.org/10.1016/j.chemosphere.2013.06.061] [PMID: 23856465]
[10]
Yin, H.; Deng, J.; Shao, S.; Gao, F.; Gao, J.; Fan, C. Distribution characteristics and toxicity assessment of heavy metals in the sediments of Lake Chaohu, China. Environ. Monit. Assess., 2011, 179(1-4), 431-442.
[http://dx.doi.org/10.1007/s10661-010-1746-3] [PMID: 20976547]
[11]
Ding, Y. Heavy metal pollution and transboundary issues in ASEAN countries. Water Policy, 2019, 21(5), 1096-1106.
[http://dx.doi.org/10.2166/wp.2019.003]
[12]
Islam, M.S.; Proshad, R.; Ahmed, S. Ecological risk of heavy metals in sediment of an urban river in Bangladesh. Hum. Ecol. Risk Assess., 2018, 24(3), 699-720.
[http://dx.doi.org/10.1080/10807039.2017.1397499]
[13]
Rahman, M.M.; Chowdhury, U.K.; Mukherjee, S.C.; Mondal, B.K.; Paul, K.; Lodh, D.; Biswas, B.K.; Chanda, C.R.; Basu, G.K.; Saha, K.C.; Roy, S.; Das, R.; Palit, S.K.; Quamruzzaman, Q.; Chakraborti, D. Chronic arsenic toxicity in Bangladesh and West Bengal, India--a review and commentary. J. Toxicol. Clin. Toxicol., 2001, 39(7), 683-700.
[http://dx.doi.org/10.1081/CLT-100108509] [PMID: 11778666]
[14]
Kumar, A.; Ramanathan, A.; Prasad, M.B.K.; Datta, D.; Kumar, M.; Sappal, S.M. Distribution, enrichment, and potential toxicity of trace metals in the surface sediments of sundarban mangrove ecosystem, Bangladesh: A baseline study before sundarban oil spill of December, 2014. Environ. Sci. Pollut. Res. Int., 2016, 23(9), 8985-8999.
[http://dx.doi.org/10.1007/s11356-016-6086-6] [PMID: 26822216]
[15]
Brahman, K.D.; Kazi, T.G.; Afridi, H.I.; Naseem, S.; Arain, S.S.; Ullah, N. Evaluation of high levels of fluoride, arsenic species and other physicochemical parameters in underground water of two sub districts of Tharparkar, Pakistan: A multivariate study. Water Res., 2013, 47(3), 1005-1020.
[http://dx.doi.org/10.1016/j.watres.2012.10.042] [PMID: 23260172]
[16]
Rehman, W.; Zeb, A.; Noor, N.; Nawaz, M. Heavy metal pollution assessment in various industries of Pakistan. Environ. Geol., 2008, 55(2), 353-358.
[http://dx.doi.org/10.1007/s00254-007-0980-7]
[17]
Nawab, J.; Farooqi, S.; Xiaoping, W.; Khan, S.; Khan, A. Levels, dietary intake, and health risk of potentially toxic metals in vegetables, fruits, and cereal crops in Pakistan. Environ. Sci. Pollut. Res. Int., 2018, 25(6), 5558-5571.
[http://dx.doi.org/10.1007/s11356-017-0764-x] [PMID: 29222655]
[18]
Khan, M.N.; Wasim, A.A.; Sarwar, A.; Rasheed, M.F. Assessment of heavy metal toxicants in the roadside soil along the N-5, National Highway, Pakistan. Environ. Monit. Assess., 2011, 182(1-4), 587-595.
[http://dx.doi.org/10.1007/s10661-011-1899-8] [PMID: 21336485]
[19]
Bibi, M.; Hashmi, M.Z.; Malik, R.N. The level and distribution of heavy metals and changes in oxidative stress indices in humans from Lahore district, Pakistan. Hum. Exp. Toxicol., 2016, 35(1), 78-90.
[http://dx.doi.org/10.1177/0960327115578063] [PMID: 25791319]
[20]
Iqbal, G.; Zada, W.; Mannan, A.; Ahmed, T. Elevated heavy metals levels in cognitively impaired patients from Pakistan. Environ. Toxicol. Pharmacol., 2018, 60, 100-109.
[http://dx.doi.org/10.1016/j.etap.2018.04.011] [PMID: 29684799]
[21]
Shakir, S.K.; Azizullah, A.; Waheed, M.; Farhat, N.; Shafiq, R. Toxic Metal Pollution in Pakistan and Its Possible Risks to Public Health; de Voogt Ed,;.Reviews of Environmental Contamination and Toxicology. Springer, Cham. Vol. 242. 2016.
[22]
Farhat, S.M.; Ali, M. Concentration of aluminum in drinking water of pakistan and its implications on human health. Life Sci., 2020, 1(2), 5.
[http://dx.doi.org/10.37185/LnS.1.1.52]
[23]
Chandravanshi, L.P.; Yadav, R.S.; Shukla, R.K.; Singh, A.; Sultana, S.; Pant, A.B.; Parmar, D.; Khanna, V.K. Reversibility of changes in brain cholinergic receptors and acetylcholinesterase activity in rats following early life arsenic exposure. Int. J. Dev. Neurosci., 2014, 34(1), 60-75.
[http://dx.doi.org/10.1016/j.ijdevneu.2014.01.007] [PMID: 24517892]
[24]
Chandravanshi, L.P.; Gupta, R.; Shukla, R.K. Arsenic-induced neurotoxicity by dysfunctioning cholinergic and dopaminergic system in brain of developing rats. Biol. Trace Elem. Res., 2019, 189(1), 118-133.
[http://dx.doi.org/10.1007/s12011-018-1452-5] [PMID: 30051311]
[25]
Sun, X.; He, Y.; Guo, Y.; Li, S.; Zhao, H.; Wang, Y.; Zhang, J.; Xing, M. Arsenic affects inflammatory cytokine expression in Gallus gallus brain tissues. BMC Vet. Res., 2017, 13(1), 157.
[http://dx.doi.org/10.1186/s12917-017-1066-8] [PMID: 28583123]
[26]
Basha, D.C.; Rani, M.U.; Devi, C.B.; Kumar, M.R.; Reddy, G.R. Perinatal lead exposure alters postnatal cholinergic and aminergic system in rat brain: Reversal effect of calcium co-administration. Int. J. Dev. Neurosci., 2012, 30(4), 343-350.
[http://dx.doi.org/10.1016/j.ijdevneu.2012.01.004] [PMID: 22326442]
[27]
Tang, M.; Luo, L.; Zhu, D.; Wang, M.; Luo, Y.; Wang, H.; Ruan, D.Y. Muscarinic cholinergic modulation of synaptic transmission and plasticity in rat hippocampus following chronic lead exposure. Naunyn Schmiedebergs Arch. Pharmacol., 2009, 379(1), 37-45.
[http://dx.doi.org/10.1007/s00210-008-0344-1] [PMID: 18716758]
[28]
Wu, Z.; Du, Y.; Xue, H.; Wu, Y.; Zhou, B. Aluminum induces neurodegeneration and its toxicity arises from increased iron accumulation and Reactive Oxygen Species (ROS) production. Neurobiol. Aging, 2012, 33(1), 199.
[29]
Roskams, A.J.; Connor, J.R. Aluminum access to the brain: A role for transferrin and its receptor. Proc. Natl. Acad. Sci., 1990, 87(22), 9024-9027.
[http://dx.doi.org/10.1073/pnas.87.22.9024] [PMID: 2247478]
[30]
Kawahara, M.; Muramoto, K.; Kobayashi, K.; Mori, H.; Kuroda, Y. Aluminum promotes the aggregation of Alzheimer’s amyloid β-protein in vitro. Biochem. Biophys. Res. Commun., 1994, 198(2), 531-535.
[http://dx.doi.org/10.1006/bbrc.1994.1078] [PMID: 7507666]
[31]
Campbell, A.; Kumar, A.; La Rosa, F.G.; Prasad, K.N.; Bondy, S.C. Aluminum increases levels of β-amyloid and ubiquitin in neuroblastoma but not in glioma cells. Proc. Soc. Exp. Biol. Med., 2000, 223(4), 397-402.
[http://dx.doi.org/10.1046/j.1525-1373.2000.22356.x] [PMID: 10721010]
[32]
Kawahara, M.; Kato, M.; Kuroda, Y. Effects of aluminum on the neurotoxicity of primary cultured neurons and on the aggregation of β-amyloid protein. Brain Res. Bull., 2001, 55(2), 211-217.
[http://dx.doi.org/10.1016/S0361-9230(01)00475-0] [PMID: 11470317]
[33]
Gulya, K.; Rakonczay, Z.; Kása, P. Cholinotoxic effects of aluminum in rat brain. J. Neurochem., 1990, 54(3), 1020-1026.
[http://dx.doi.org/10.1111/j.1471-4159.1990.tb02352.x] [PMID: 2303807]
[34]
Ghribi, O.; Herman, M.M.; Forbes, M.S.; DeWitt, D.A.; Savory, J. GDNF protects against aluminum-induced apoptosis in rabbits by upregulating Bcl-2 and Bcl-XL and inhibiting mitochondrial Bax translocation. Neurobiol. Dis., 2001, 8(5), 764-773.
[http://dx.doi.org/10.1006/nbdi.2001.0429] [PMID: 11592846]
[35]
Kawahara, M.; Kato-Negishi, M.; Hosoda, R.; Imamura, L.; Tsuda, M.; Kuroda, Y. Brain-derived neurotrophic factor protects cultured rat hippocampal neurons from aluminum maltolate neurotoxicity. J. Inorg. Biochem., 2003, 97(1), 124-131.
[http://dx.doi.org/10.1016/S0162-0134(03)00255-1] [PMID: 14507468]
[36]
Boucher, D.S.; Platts, W. In prospecting for native metals in lunar polar craters. In 7th Symposium on Space Resource Utilization, 13-17 Jan, 2014, National Harbor, Maryland, 2014.
[http://dx.doi.org/10.2514/6.2014-0338]
[37]
He, J.; Chen, J.P. A comprehensive review on biosorption of heavy metals by algal biomass: Materials, performances, chemistry, and modeling simulation tools. Bioresour. Technol., 2014, 160, 67-78.
[http://dx.doi.org/10.1016/j.biortech.2014.01.068] [PMID: 24630371]
[38]
Cobbina, S.J.; Chen, Y.; Zhou, Z.; Wu, X.; Feng, W.; Wang, W.; Mao, G.; Xu, H.; Zhang, Z.; Wu, X.; Yang, L. Low concentration toxic metal mixture interactions: Effects on essential and non-essential metals in brain, liver, and kidneys of mice on sub-chronic exposure. Chemosphere, 2015, 132, 79-86.
[http://dx.doi.org/10.1016/j.chemosphere.2015.03.013] [PMID: 25828250]
[39]
Huang, M.Y.; Duan, R.Y.; Ji, X. The influence of long-term cadmium exposure on phonotaxis in male Pelophylax nigromaculata. Chemosphere, 2015, 119, 763-768.
[http://dx.doi.org/10.1016/j.chemosphere.2014.08.014] [PMID: 25192651]
[40]
Andrade, V.; Mateus, M.L.; Batoréu, M.C.; Aschner, M.; dos Santos, A.P.M. Urinary delta-ALA: A potential biomarker of exposure and neurotoxic effect in rats co-treated with a mixture of lead, arsenic and manganese. Neurotoxicology, 2013, 38, 33-41.
[http://dx.doi.org/10.1016/j.neuro.2013.06.003] [PMID: 23764341]
[41]
Rai, A.; Maurya, S.K.; Khare, P.; Srivastava, A.; Bandyopadhyay, S. Characterization of developmental neurotoxicity of As, Cd, and Pb mixture: Synergistic action of metal mixture in glial and neuronal functions. Toxicol. Sci., 2010, 118(2), 586-601.
[http://dx.doi.org/10.1093/toxsci/kfq266] [PMID: 20829427]
[42]
Micha, R.; Khatibzadeh, S.; Shi, P.; Fahimi, S.; Lim, S.; Andrews, K.G.; Engell, R.E.; Powles, J.; Ezzati, M.; Mozaffarian, D. Global, regional, and national consumption levels of dietary fats and oils in 1990 and 2010: A systematic analysis including 266 country-specific nutrition surveys. BMJ, 2014, 348, g2272.
[http://dx.doi.org/10.1136/bmj.g2272] [PMID: 24736206]
[43]
Haider, A.; Zaidi, M. Food consumption patterns and nutrition disparity in Pakistan., 2017. Available from: https://mpra.ub.uni-muenchen.de/83522/1/MPRA_paper_83522.pdf
[44]
Freeman, L.R.; Haley-Zitlin, V.; Rosenberger, D.S.; Granholm, A.C. Damaging effects of a high-fat diet to the brain and cognition: A review of proposed mechanisms. Nutr. Neurosci., 2014, 17(6), 241-251.
[http://dx.doi.org/10.1179/1476830513Y.0000000092] [PMID: 24192577]
[45]
Molteni, R.; Barnard, R.J.; Ying, Z.; Roberts, C.K.; Gómez-Pinilla, F. A high-fat, refined sugar diet reduces hippocampal brain-derived neurotrophic factor, neuronal plasticity, and learning. Neuroscience, 2002, 112(4), 803-814.
[http://dx.doi.org/10.1016/S0306-4522(02)00123-9] [PMID: 12088740]
[46]
Molteni, R.; Wu, A.; Vaynman, S.; Ying, Z.; Barnard, R.J.; Gómez-Pinilla, F. Exercise reverses the harmful effects of consumption of a high-fat diet on synaptic and behavioral plasticity associated to the action of brain-derived neurotrophic factor. Neuroscience, 2004, 123(2), 429-440.
[http://dx.doi.org/10.1016/j.neuroscience.2003.09.020] [PMID: 14698750]
[47]
Cavaliere, G.; Trinchese, G.; Penna, E.; Cimmino, F.; Pirozzi, C.; Lama, A.; Annunziata, C.; Catapano, A.; Mattace Raso, G.; Meli, R.; Monda, M.; Messina, G.; Zammit, C.; Crispino, M.; Mollica, M.P. High-fat diet induces neuroinflammation and mitochondrial impairment in mice cerebral cortex and synaptic fraction. Front. Cell. Neurosci., 2019, 13, 509.
[http://dx.doi.org/10.3389/fncel.2019.00509] [PMID: 31798417]
[48]
White, C.L.; Pistell, P.J.; Purpera, M.N.; Gupta, S.; Fernandez-Kim, S.O.; Hise, T.L.; Keller, J.N.; Ingram, D.K.; Morrison, C.D.; Bruce-Keller, A.J. Effects of high fat diet on Morris maze performance, oxidative stress, and inflammation in rats: Contributions of maternal diet. Neurobiol. Dis., 2009, 35(1), 3-13.
[http://dx.doi.org/10.1016/j.nbd.2009.04.002] [PMID: 19374947]
[49]
Park, H.R.; Park, M.; Choi, J.; Park, K.Y.; Chung, H.Y.; Lee, J. A high-fat diet impairs neurogenesis: Involvement of lipid peroxidation and brain-derived neurotrophic factor. Neurosci. Lett., 2010, 482(3), 235-239.
[http://dx.doi.org/10.1016/j.neulet.2010.07.046] [PMID: 20670674]
[50]
Li, W.; Prakash, R.; Chawla, D.; Du, W.; Didion, S.P.; Filosa, J.A.; Zhang, Q.; Brann, D.W.; Lima, V.V.; Tostes, R.C.; Ergul, A. Early effects of high-fat diet on neurovascular function and focal ischemic brain injury. Am. J. Physiol. Regul. Integr. Comp. Physiol., 2013, 304(11), R1001-R1008.
[http://dx.doi.org/10.1152/ajpregu.00523.2012] [PMID: 23576615]
[51]
Han, Q.; Yuan, Q.; Xie, G.; Huo, J.; Bao, Y.; Xie, G. 6-Shogaol attenuates LPS-induced inflammation in BV2 microglia cells by activating PPAR-γ. Oncotarget, 2017, 8(26), 42001-42006.
[http://dx.doi.org/10.18632/oncotarget.16719] [PMID: 28410218]
[52]
Ray, A.; Vasudevan, S.; Sengupta, S. 6-Shogaol inhibits breast cancer cells and stem cell-like spheroids by modulation of notch signaling pathway and induction of autophagic cell death. PLoS One, 2015, 10(9), e0137614.
[http://dx.doi.org/10.1371/journal.pone.0137614] [PMID: 26355461]
[53]
Na, J.Y.; Song, K.; Lee, J.W.; Kim, S.; Kwon, J. Pretreatment of 6-Shogaol attenuates oxidative stress and inflammation in middle cerebral artery occlusion-induced mice. Eur. J. Pharmacol., 2016, 788, 241-247.
[http://dx.doi.org/10.1016/j.ejphar.2016.06.044] [PMID: 27346834]
[54]
Na, J.Y.; Song, K.; Lee, J.W.; Kim, S.; Kwon, J. 6-Shogaol has anti-amyloidogenic activity and ameliorates Alzheimer’s disease via CysLT1R-mediated inhibition of cathepsin B. Biochem. Biophys. Res. Commun., 2016, 477(1), 96-102.
[http://dx.doi.org/10.1016/j.bbrc.2016.06.026] [PMID: 27286707]
[55]
Na, J.Y.; Song, K.; Lee, J.W.; Kim, S.; Kwon, J. Sortilin-related receptor 1 interacts with amyloid precursor protein and is activated by 6-Shogaol, leading to inhibition of the amyloidogenic pathway. Biochem. Biophys. Res. Commun., 2017, 484(4), 890-895.
[http://dx.doi.org/10.1016/j.bbrc.2017.02.029] [PMID: 28188785]
[56]
Moon, M.; Kim, H.G.; Choi, J.G.; Oh, H.; Lee, P.K.J.; Ha, S.K.; Kim, S.Y.; Park, Y.; Huh, Y.; Oh, M.S. 6-Shogaol, an active constituent of ginger, attenuates neuroinflammation and cognitive deficits in animal models of dementia. Biochem. Biophys. Res. Commun., 2014, 449(1), 8-13.
[http://dx.doi.org/10.1016/j.bbrc.2014.04.121] [PMID: 24796668]
[57]
Lu, J.; Zheng, Y.; Wu, D.; Sun, D.; Shan, Q.; Fan, S. Trace amounts of copper induce neurotoxicity in the cholesterol-fed mice through apoptosis. FEBS Lett., 2006, 580(28-29), 6730-6740.
[http://dx.doi.org/10.1016/j.febslet.2006.10.072] [PMID: 17134702]
[58]
National Research Council. Guide for the Care and Use of Laboratory Animals; 8th edi; National Academies Press: Washington, D.C., 2010.
[59]
Patlolla, A.; Tchounwou, P. Serum acetyl cholinesterase as a biomarker of arsenic induced neurotoxicity in sprague-dawley rats. Int. J. Environ. Res. Public Health, 2005, 2(1), 80-83.
[http://dx.doi.org/10.3390/ijerph2005010080] [PMID: 16705804]
[60]
Yadav, R.S.; Chandravanshi, L.P.; Shukla, R.K.; Sankhwar, M.L.; Ansari, R.W.; Shukla, P.K.; Pant, A.B.; Khanna, V.K. Neuroprotective efficacy of curcumin in arsenic induced cholinergic dysfunctions in rats. Neurotoxicology, 2011, 32(6), 760-768.
[http://dx.doi.org/10.1016/j.neuro.2011.07.004] [PMID: 21839772]
[61]
Sethi, P.; Jyoti, A.; Hussain, E.; Sharma, D. Curcumin attenuates aluminium-induced functional neurotoxicity in rats. Pharmacol. Biochem. Behav., 2009, 93(1), 31-39.
[http://dx.doi.org/10.1016/j.pbb.2009.04.005] [PMID: 19376155]
[62]
Shi-lei, S.; Guang-yu, M.A.; Bachelor, L.I.H.; Bachelor, Z.; Hong-mei, D.; Xiao-hu, X.U. Effect of naloxone on aluminum-induced learning and memory impairment in rats. Neurol. India, 2005, 53(1), 79-82.
[http://dx.doi.org/10.4103/0028-3886.15066] [PMID: 15805661]
[63]
Gu, H.; Robison, G.; Hong, L.; Barrea, R.; Wei, X.; Farlow, M.R.; Pushkar, Y.N.; Du, Y.; Zheng, W. Increased β-amyloid deposition in Tg-SWDI transgenic mouse brain following in vivo lead exposure. Toxicol. Lett., 2012, 213(2), 211-219.
[http://dx.doi.org/10.1016/j.toxlet.2012.07.002] [PMID: 22796588]
[64]
Basha, M.R.; Wei, W.; Bakheet, S.A.; Benitez, N.; Siddiqi, H.K.; Ge, Y.W.; Lahiri, D.K.; Zawia, N.H. The fetal basis of amyloidogenesis: Exposure to lead and latent overexpression of amyloid precursor protein and β-amyloid in the aging brain. J. Neurosci., 2005, 25(4), 823-829.
[http://dx.doi.org/10.1523/JNEUROSCI.4335-04.2005] [PMID: 15673661]
[65]
Gu, C.; Chen, S.; Xu, X.; Zheng, L.; Li, Y.; Wu, K.; Liu, J.; Qi, Z.; Han, D.; Chen, G.; Huo, X. Lead and cadmium synergistically enhance the expression of divalent metal transporter 1 protein in central nervous system of developing rats. Neurochem. Res., 2009, 34(6), 1150-1156.
[http://dx.doi.org/10.1007/s11064-008-9891-6] [PMID: 19083094]
[66]
Pratha, A.A.; Prabakar, J. Comparing the effect of carbonated and energy drinks on salivary pH- in vivo randomized controlled trial. Res. J. Pharm. Technol., 2019, 12(10), 4699-4702.
[http://dx.doi.org/10.5958/0974-360X.2019.00809.6]
[67]
Islam, R.; Faysal, S.M.; Amin, R.; Juliana, F.M.; Islam, M.J.; Alam, M.J.; Hossain, M.N.; Asaduzzaman, M. Assessment of pH and Total Dissolved Substances (TDS) in the commercially available bottled drinking water. IORS J. Nurs. Health Sci. Ver., 2017, 6(5), 35-40.
[68]
Satarug, S. Dietary cadmium intake and its effects on kidneys. Toxics, 2018, 6(1), 15.
[http://dx.doi.org/10.3390/toxics6010015] [PMID: 29534455]
[69]
Mahurpawar, M. Effects of heavy metals on human health. Int. J. Res. Granthaalayah, 2015, 3(9), 2394-3629.
[70]
Park, H.Y.; Choi, J.W.; Park, Y.; Oh, M.S.; Ha, S.K. Fermentation enhances the neuroprotective effect of Shogaol-enriched ginger extract via an increase in 6-paradol content. J. Funct. Foods, 2016, 21, 147-152.
[http://dx.doi.org/10.1016/j.jff.2015.11.045]
[71]
Waggas, A.M. Neuroprotective evaluation of extract of ginger (Zingiber officinale) root in monosodium glutamate-induced toxicity in different brain areas male albino rats. Pak. J. Biol. Sci., 2009, 12(3), 201-212.
[http://dx.doi.org/10.3923/pjbs.2009.201.212] [PMID: 19579948]
[72]
Ohnishi, M.; Ohshita, M.; Tamaki, H.; Marutani, Y.; Nakayama, Y.; Akagi, M.; Miyata, M.; Maehara, S.; Hata, T.; Inoue, A. Shogaol but not gingerol has a neuroprotective effect on hemorrhagic brain injury: Contribution of the αβ-unsaturated carbonyl to heme oxygenase-1 expression. Eur. J. Pharmacol., 2019, 842, 33-39.
[http://dx.doi.org/10.1016/j.ejphar.2018.10.029] [PMID: 30365933]
[73]
Gaire, B.P.; Kwon, O.W.; Park, S.H.; Chun, K.H.; Kim, S.Y.; Shin, D.Y.; Choi, J.W. Neuroprotective effect of 6-paradol in focal cerebral ischemia involves the attenuation of neuroinflammatory responses in activated microglia. PLoS One, 2015, 10(3), e0120203.
[http://dx.doi.org/10.1371/journal.pone.0120203] [PMID: 25789481]
[74]
Kyung, K.S.; Gon, J.H.; Geun, K.Y.; Sup, J.J.; Suk, W.J.; Ho, K.J. 6-Shogaol, a natural product, reduces cell death and restores motor function in rat spinal cord injury. Eur. J. Neurosci., 2006, 24(4), 1042-1052.
[http://dx.doi.org/10.1111/j.1460-9568.2006.04908.x] [PMID: 16930431]
[75]
Seow, S.L.S.; Hong, S.L.; Lee, G.S.; Malek, S.N.A.; Sabaratnam, V. 6-Shogaol, a neuroactive compound of ginger (Jahe gajah) induced neuritogenic activity via NGF responsive pathways in PC-12 cells. BMC Complement. Altern. Med., 2017, 17(1), 334.
[http://dx.doi.org/10.1186/s12906-017-1837-6] [PMID: 28646880]
[76]
Sapkota, A.; Park, S.J.; Choi, J.W. Neuroprotective effects of 6-Shogaol and its metabolite, 6-paradol, in a mouse model of multiple sclerosis. Biomol. Ther., 2019, 27(2), 152-159.
[http://dx.doi.org/10.4062/biomolther.2018.089] [PMID: 30001610]
[77]
Hussein, U.; Hassan, N.; Elhalwagy, M.; Zaki, A.; Abubakr, H.; Nagulapalli Venkata, K.; Jang, K.; Bishayee, A. Ginger and propolis exert neuroprotective effects against monosodium glutamate-induced neurotoxicity in rats. Molecules, 2017, 22(11), 1928.
[http://dx.doi.org/10.3390/molecules22111928] [PMID: 29117134]
[78]
Iqbal, G.; Iqbal, A.; Mahboob, A.; Farhat, S.M.; Ahmed, T. Memory enhancing effect of black pepper in the AlCl3 induced neurotoxicity mouse model is mediated through its active component chavicine. Curr. Pharm. Biotechnol., 2016, 17(11), 962-973.
[http://dx.doi.org/10.2174/1389201017666160709202124] [PMID: 27396401]
[79]
Mahboob, A.; Farhat, S.M.; Iqbal, G.; Babar, M.M.; Zaidi, N.S.S.; Nabavi, S.M.; Ahmed, T. Alpha-lipoic acid-mediated activation of muscarinic receptors improves hippocampus- and amygdala-dependent memory. Brain Res. Bull., 2016, 122, 19-28.
[http://dx.doi.org/10.1016/j.brainresbull.2016.02.014] [PMID: 26912408]
[80]
Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-∆ ∆ C(T)). Method. Methods, 2001, 25(4), 402-408.
[http://dx.doi.org/10.1006/meth.2001.1262] [PMID: 11846609]
[81]
Manaenko, A.; Chen, H.; Kammer, J.; Zhang, J.H.; Tang, J. Comparison evans blue injection routes: Intravenous versus intraperitoneal, for measurement of blood–brain barrier in a mice hemorrhage model. J. Neurosci. Methods, 2011, 195(2), 206-210.
[http://dx.doi.org/10.1016/j.jneumeth.2010.12.013] [PMID: 21168441]
[82]
Eltokhi, A.; Kurpiers, B.; Pitzer, C. Behavioral tests assessing neuropsychiatric phenotypes in adolescent mice reveal strain- and sex-specific effects. Sci. Rep., 2020, 10(1), 11263.
[http://dx.doi.org/10.1038/s41598-020-67758-0] [PMID: 32647155]
[83]
Hånell, A.; Marklund, N. Structured evaluation of rodent behavioral tests used in drug discovery research. Front. Behav. Neurosci., 2014, 8, 252-252.
[PMID: 25100962]
[84]
McIlwain, K.L.; Merriweather, M.Y.; Yuva-Paylor, L.A.; Paylor, R. The use of behavioral test batteries: Effects of training history. Physiol. Behav., 2001, 73(5), 705-717.
[http://dx.doi.org/10.1016/S0031-9384(01)00528-5] [PMID: 11566205]
[85]
Wolf, A.; Bauer, B.; Abner, E.L.; Ashkenazy-Frolinger, T.; Hartz, A.M.S. A comprehensive behavioral test battery to assess learning and memory in 129S6/Tg2576 mice. PLoS One, 2016, 11(1), e0147733.
[http://dx.doi.org/10.1371/journal.pone.0147733] [PMID: 26808326]
[86]
Farhat, S.M.; Mahboob, A.; Ahmed, T. Cortex-and amygdala-dependent learning and nicotinic acetylcholine receptor gene expression is severely impaired in mice orally treated with AlCl3. Biol. Trace Elem. Res., 2017, 179(1), 91-101.
[http://dx.doi.org/10.1007/s12011-017-0942-1] [PMID: 28101715]
[87]
Dellu, F.; Mayo, W.; Cherkaoui, J.; Le Moal, M.; Simon, H. A two-trial memory task with automated recording: Study in young and aged rats. Brain Res., 1992, 588(1), 132-139.
[http://dx.doi.org/10.1016/0006-8993(92)91352-F] [PMID: 1393562]
[88]
Abel, E.L.; Bilitzke, P.J. A possible alarm substance in the forced swimming test. Physiol. Behav., 1990, 48(2), 233-239.
[http://dx.doi.org/10.1016/0031-9384(90)90306-O] [PMID: 2255725]
[89]
Morris, R. Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods, 1984, 11(1), 47-60.
[http://dx.doi.org/10.1016/0165-0270(84)90007-4] [PMID: 6471907]
[90]
Bromley-Brits, K.; Deng, Y.; Song, W. Morris water maze test for learning and memory deficits in Alzheimer’s disease model mice. J. Vis. Exp., 2011, 20(53), e2920.
[http://dx.doi.org/10.3791/2920] [PMID: 21808223]
[91]
Pistell, P.J.; Morrison, C.D.; Gupta, S.; Knight, A.G.; Keller, J.N.; Ingram, D.K.; Bruce-Keller, A.J. Cognitive impairment following high fat diet consumption is associated with brain inflammation. J. Neuroimmunol., 2010, 219(1-2), 25-32.
[http://dx.doi.org/10.1016/j.jneuroim.2009.11.010] [PMID: 20004026]
[92]
Francis, H.; Stevenson, R. The longer-term impacts of western diet on human cognition and the brain. Appetite, 2013, 63, 119-128.
[http://dx.doi.org/10.1016/j.appet.2012.12.018] [PMID: 23291218]
[93]
Uranga, R.M.; Bruce-Keller, A.J.; Morrison, C.D.; Fernandez-Kim, S.O.; Ebenezer, P.J.; Zhang, L.; Dasuri, K.; Keller, J.N. Intersection between metabolic dysfunction, high fat diet consumption, and brain aging. J. Neurochem., 2010, 114(2), 344-361.
[http://dx.doi.org/10.1111/j.1471-4159.2010.06803.x] [PMID: 20477933]
[94]
Kosari, S.; Badoer, E.; Nguyen, J.C.D.; Killcross, A.S.; Jenkins, T.A. Effect of western and high fat diets on memory and cholinergic measures in the rat. Behav. Brain Res., 2012, 235(1), 98-103.
[http://dx.doi.org/10.1016/j.bbr.2012.07.017] [PMID: 22820146]
[95]
Al-Attar, A.M. Antioxidant effect of vitamin E treatment on some heavy metals-induced renal and testicular injuries in male mice. Saudi J. Biol. Sci., 2011, 18(1), 63-72.
[http://dx.doi.org/10.1016/j.sjbs.2010.10.004] [PMID: 23961105]
[96]
Carpenter, D.O. Effects of metals on the nervous system of humans and animals. Int. J. Occup. Med. Environ. Health, 2001, 14(3), 209-218.
[PMID: 11764847]
[97]
Nuran Ercal, B.S.P.; Hande Gurer-Orhan, B.S.P.; Nukhet Aykin-Burns, B.S.P. Toxic metals and oxidative stress part I: Mechanisms involved in metal-induced oxidative damage. Curr. Top. Med. Chem., 2001, 1(6), 529-539.
[http://dx.doi.org/10.2174/1568026013394831] [PMID: 11895129]
[98]
Solomons, N.W.; Gross, R. Urban nutrition in developing countries. Nutr. Rev., 1995, 53(4 Pt 1), 90-95.
[PMID: 7624063]
[99]
Bryzgalova, G.; Lundholm, L.; Portwood, N.; Gustafsson, J.Å.; Khan, A.; Efendic, S.; Dahlman-Wright, K. Mechanisms of antidiabetogenic and body weight-lowering effects of estrogen in high-fat diet-fed mice. Am. J. Physiol. Endocrinol. Metab., 2008, 295(4), E904-E912.
[http://dx.doi.org/10.1152/ajpendo.90248.2008] [PMID: 18697913]
[100]
Adam, C.L.; Gratz, S.W.; Peinado, D.I.; Thomson, L.M.; Garden, K.E.; Williams, P.A.; Richardson, A.J.; Ross, A.W. Effects of dietary fibre (pectin) and/or increased protein (casein or pea) on satiety, body weight, adiposity and caecal fermentation in high fat diet-induced obese rats. PLoS One, 2016, 11(5), e0155871.
[http://dx.doi.org/10.1371/journal.pone.0155871] [PMID: 27224646]
[101]
Choi, B.K.; Park, S.B.; Lee, D.R.; Lee, H.J.; Jin, Y.Y.; Yang, S.H.; Suh, J.W. Green coffee bean extract improves obesity by decreasing body fat in high-fat diet-induced obese mice. Asian Pac. J. Trop. Med., 2016, 9(7), 635-643.
[http://dx.doi.org/10.1016/j.apjtm.2016.05.017] [PMID: 27393090]
[102]
Wang, X.; Mukherjee, B.; Park, S.K. Associations of cumulative exposure to heavy metal mixtures with obesity and its comorbidities among U.S. adults in NHANES 2003–2014. Environ. Int., 2018, 121(Pt 1), 683-694.
[http://dx.doi.org/10.1016/j.envint.2018.09.035] [PMID: 30316184]
[103]
Duc, H. N.; Oh, H.; Kim, M. S. The effect of mixture of heavy metals on obesity in individuals ≥ 50 years of age. 2022, 200(8), 3554-3571.
[104]
Nammi, S.; Sreemantula, S.; Roufogalis, B.D. Protective effects of ethanolic extract of Zingiber officinale rhizome on the development of metabolic syndrome in high-fat diet-fed rats. Basic Clin. Pharmacol. Toxicol., 2009, 104(5), 366-373.
[http://dx.doi.org/10.1111/j.1742-7843.2008.00362.x] [PMID: 19413656]
[105]
Wang, J.; Ke, W.; Bao, R.; Hu, X.; Chen, F. Beneficial effects of ginger Zingiber officinale Roscoe on obesity and metabolic syndrome: A review. Ann. N. Y. Acad. Sci., 2017, 1398(1), 83-98.
[http://dx.doi.org/10.1111/nyas.13375] [PMID: 28505392]
[106]
Rajasekaran, S.; Sivagnanam, K.; Subramanian, S. Antioxidant effect of Aloe vera gel extract in streptozotocin-induced diabetes in rats. Pharmacol. Rep., 2005, 57(1), 90-96.
[PMID: 15849382]
[107]
Feng, W.; Cui, X.; Liu, B.; Liu, C.; Xiao, Y.; Lu, W.; Guo, H.; He, M.; Zhang, X.; Yuan, J.; Chen, W.; Wu, T. Association of urinary metal profiles with altered glucose levels and diabetes risk: A population-based study in China. PLoS One, 2015, 10(4), e0123742.
[http://dx.doi.org/10.1371/journal.pone.0123742] [PMID: 25874871]
[108]
Zang, Y.; Zhang, L.; Igarashi, K.; Yu, C. The anti-obesity and anti-diabetic effects of kaempferol glycosides from unripe soybean leaves in high-fat-diet mice. Food Funct., 2015, 6(3), 834-841.
[http://dx.doi.org/10.1039/C4FO00844H] [PMID: 25599885]
[109]
Roopchand, D.E.; Carmody, R.N.; Kuhn, P.; Moskal, K.; Rojas-Silva, P.; Turnbaugh, P.J.; Raskin, I. Dietary polyphenols promote growth of the gut bacterium Akkermansia muciniphila and attenuate high-fat diet–induced metabolic syndrome. Diabetes, 2015, 64(8), 2847-2858.
[http://dx.doi.org/10.2337/db14-1916] [PMID: 25845659]
[110]
Jiang, H.; Xie, Z.; Koo, H.J.; McLaughlin, S.P.; Timmermann, B.N.; Gang, D.R. Metabolic profiling and phylogenetic analysis of medicinal Zingiber species: Tools for authentication of ginger (Zingiber officinale Rosc.). Phytochemistry, 2006, 67(15), 1673-1685.
[http://dx.doi.org/10.1016/j.phytochem.2005.08.001] [PMID: 16169024]
[111]
Wei, C.K.; Tsai, Y.H.; Korinek, M.; Hung, P.H.; El-Shazly, M.; Cheng, Y.B.; Wu, Y.C.; Hsieh, T.J.; Chang, F.R. 6-Paradol and 6-Shogaol, the pungent compounds of ginger, promote glucose utilization in adipocytes and myotubes, and 6-paradol reduces blood glucose in high-fat diet-fed mice. Int. J. Mol. Sci., 2017, 18(1), 168.
[http://dx.doi.org/10.3390/ijms18010168] [PMID: 28106738]
[112]
Walker, H.K.; Hall, W.D.; Hurst, J.W. Clinical methods: The history, physical, and laboratory examinations. 3rd edi; , 1990.
[113]
Nolan, C.V.; Shaikh, Z.A. Lead nephrotoxicity and associated disorders: Biochemical mechanisms. Toxicology, 1992, 73(2), 127-146.
[http://dx.doi.org/10.1016/0300-483X(92)90097-X] [PMID: 1319092]
[114]
He, L.; Poblenz, A.T.; Medrano, C.J.; Fox, D.A. Lead and calcium produce rod photoreceptor cell apoptosis by opening the mitochondrial permeability transition pore. J. Biol. Chem., 2000, 275(16), 12175-12184.
[http://dx.doi.org/10.1074/jbc.275.16.12175] [PMID: 10766853]
[115]
Oberbach, A.; Jehmlich, N.; Schlichting, N.; Heinrich, M.; Lehmann, S.; Wirth, H.; Till, H.; Stolzenburg, J.U.; Völker, U.; Adams, V.; Neuhaus, J. Molecular fingerprint of high fat diet induced urinary bladder metabolic dysfunction in a rat model. PLoS One, 2013, 8(6), e66636-e66636.
[http://dx.doi.org/10.1371/journal.pone.0066636] [PMID: 23826106]
[116]
Kalhan, S.C. Protein metabolism in pregnancy. In: Principles of Perinatal—Neonatal Metabolism; Springer: Cham, 1998; pp. 207-220.
[http://dx.doi.org/10.1007/978-1-4612-1642-1_11]
[117]
Liu, T.; Liang, X.; Lei, C.; Huang, Q.; Song, W.; Fang, R.; Li, C.; Li, X.; Mo, H.; Sun, N.; Lv, H.; Liu, Z. High-fat diet affects heavy metal accumulation and toxicity to mice liver and kidney probably via gut microbiota. Front. Microbiol., 2020, 11, 1604.
[http://dx.doi.org/10.3389/fmicb.2020.01604] [PMID: 32849333]
[118]
Rao, M.; Acharya, Y.; Naik, J.; Fatteh, S.; Fateh, A.; Pawar, A.; Jayalakshmi, G.; Sandhya, B.; Arja, S.B. Effect of heavy metals on the activity levels of hepatic enzymes in the maternal and embryonic tissue of viviparous scorpion (H. Fulvipes). Int. J. Life Sci. Sci. Res., 2017, 3, 1-186.
[119]
Limdi, J.K.; Hyde, G.M. Evaluation of abnormal liver function tests. Postgrad. Med. J., 2003, 79(932), 307-312.
[http://dx.doi.org/10.1136/pmj.79.932.307] [PMID: 12840117]
[120]
Song, L. Chapter one - Calcium and bone metabolism indices. In: Advances in Clinical Chemistry; Makowski, G.S., Ed.; Elsevier: Amsterefam, 2017; Vol. 82, pp. 1-46.
[121]
Glerup, H.; Mikkelsen, K.; Poulsen, L.; Hass, E.; Overbeck, S.; Andersen, H.; Charles, P.; Eriksen, E.F.; Hypovitaminosis, D. Hypovitaminosis D myopathy without biochemical signs of osteomalacic bone involvement. Calcif. Tissue Int., 2000, 66(6), 419-424.
[http://dx.doi.org/10.1007/s002230010085] [PMID: 10821877]
[122]
Ross, P.D.; Kress, B.C.; Parson, R.E.; Wasnich, R.D.; Armour, K.A.; Mizrahi, I.A. Serum bone alkaline phosphatase and calcaneus bone density predict fractures: A prospective study. Osteoporos. Int., 2000, 11(1), 76-82.
[http://dx.doi.org/10.1007/s001980050009] [PMID: 10663362]
[123]
Niu, J.; Liberda, E.N.; Qu, S.; Guo, X.; Li, X.; Zhang, J.; Meng, J.; Yan, B.; Li, N.; Zhong, M.; Ito, K.; Wildman, R.; Liu, H.; Chen, L.C.; Qu, Q. The role of metal components in the cardiovascular effects of PM2.5. PLoS One, 2013, 8(12), e83782.
[http://dx.doi.org/10.1371/journal.pone.0083782] [PMID: 24386277]
[124]
Kawakami, T.; Hanao, N.; Nishiyama, K.; Kadota, Y.; Inoue, M.; Sato, M.; Suzuki, S. Differential effects of cobalt and mercury on lipid metabolism in the white adipose tissue of high-fat diet-induced obesity mice. Toxicol. Appl. Pharmacol., 2012, 258(1), 32-42.
[http://dx.doi.org/10.1016/j.taap.2011.10.004] [PMID: 22019852]
[125]
Kojima, M.; Nemoto, K.; Murai, U.; Yoshimura, N.; Ayabe, Y.; Degawa, M. Altered gene expression of hepatic lanosterol 14α-demethylase (CYP51) in lead nitrate-treated rats. Arch. Toxicol., 2002, 76(7), 398-403.
[http://dx.doi.org/10.1007/s00204-002-0365-3] [PMID: 12111004]
[126]
Giri, B.; Dey, S. Is it possible to avert arsenic effects on cells and tissues bypassing its toxicity and suppressive consequences of energy production? A hypothesis. BLDE Uni. J. Health Sci., 2017, 2(2), 91.
[http://dx.doi.org/10.4103/bjhs.bjhs_28_17]
[127]
Huang, B.W.; Chiang, M.T.; Yao, H.T.; Chiang, W. The effect of high-fat and high-fructose diets on glucose tolerance and plasma lipid and leptin levels in rats. Diabetes Obes. Metab., 2004, 6(2), 120-126.
[http://dx.doi.org/10.1111/j.1462-8902.2004.00323.x] [PMID: 14746577]
[128]
Buettner, R.; Parhofer, K.G.; Woenckhaus, M.; Wrede, C.E.; Kunz-Schughart, L.A.; Schölmerich, J.; Bollheimer, L.C. Defining high-fat-diet rat models: Metabolic and molecular effects of different fat types. J. Mol. Endocrinol., 2006, 36(3), 485-501.
[http://dx.doi.org/10.1677/jme.1.01909] [PMID: 16720718]
[129]
Sánchez-Sarasúa, S.; Moustafa, S.; García-Avilés, Á.; López-Climent, M.F.; Gómez-Cadenas, A.; Olucha-Bordonau, F.E.; Sánchez-Pérez, A.M. The effect of abscisic acid chronic treatment on neuroinflammatory markers and memory in a rat model of high-fat diet induced neuroinflammation. Nutr. Metab., 2016, 13(1), 73.
[http://dx.doi.org/10.1186/s12986-016-0137-3] [PMID: 27795733]
[130]
Calderón-Garcidueñas, L.; Serrano-Sierra, A.; Torres-Jardón, R.; Zhu, H.; Yuan, Y.; Smith, D.; Delgado-Chávez, R.; Cross, J.V.; Medina-Cortina, H.; Kavanaugh, M.; Guilarte, T.R. The impact of environmental metals in young urbanites’ brains. Exp. Toxicol. Pathol., 2013, 65(5), 503-511.
[http://dx.doi.org/10.1016/j.etp.2012.02.006] [PMID: 22436577]
[131]
Hussien, H.M.; Abd-Elmegied, A.; Ghareeb, D.A.; Hafez, H.S.; Ahmed, H.E.A.; El-moneam, N.A. Neuroprotective effect of berberine against environmental heavy metals-induced neurotoxicity and Alzheimer’s-like disease in rats. Food Chem. Toxicol., 2018, 111, 432-444.
[http://dx.doi.org/10.1016/j.fct.2017.11.025] [PMID: 29170048]
[132]
Jolad, S.D.; Lantz, R.C.; Solyom, A.M.; Chen, G.J.; Bates, R.B.; Timmermann, B.N. Fresh organically grown ginger (Zingiber officinale): Composition and effects on LPS-induced PGE2 production. Phytochemistry, 2004, 65(13), 1937-1954.
[http://dx.doi.org/10.1016/j.phytochem.2004.06.008] [PMID: 15280001]
[133]
Bischoff-Kont, I.; Fürst, R. Benefits of ginger and its constituent 6-Shogaol in inhibiting inflammatory processes. Pharmaceuticals, 2021, 14(6), 571.
[http://dx.doi.org/10.3390/ph14060571] [PMID: 34203813]
[134]
Zhang, L.; Zhao, W.; Li, B.; Alkon, D.L.; Barker, J.L.; Chang, Y.H.; Wu, M.; Rubinow, D.R. TNF-α induced over-expression of GFAP is associated with MAPKs. Neuroreport, 2000, 11(2), 409-412.
[http://dx.doi.org/10.1097/00001756-200002070-00037] [PMID: 10674496]
[135]
Ye, L.; Huang, Y.; Zhao, L.; Li, Y.; Sun, L.; Zhou, Y.; Qian, G.; Zheng, J.C. IL-1β and TNF-α induce neurotoxicity through glutamate production: A potential role for neuronal glutaminase. J. Neurochem., 2013, 125(6), 897-908.
[http://dx.doi.org/10.1111/jnc.12263] [PMID: 23578284]
[136]
Abd-El-Basset, E.M.; Rao, M.S.; Alshawaf, S.M.; Ashkanani, H.K.; Kabli, A.H. Tumor Necrosis Factor (TNF) induces astrogliosis, microgliosis and promotes survival of cortical neurons. AIMS Neurosci., 2021, 8(4), 558-584.
[http://dx.doi.org/10.3934/Neuroscience.2021031] [PMID: 34877406]
[137]
Clausen, B.H.; Wirenfeldt, M.; Høgedal, S.S.; Frich, L.H.; Nielsen, H.H.; Schrøder, H.D.; Østergaard, K.; Finsen, B.; Kristensen, B.W.; Lambertsen, K.L. Characterization of the TNF and IL-1 systems in human brain and blood after ischemic stroke. Acta Neuropathol. Commun., 2020, 8(1), 81.
[http://dx.doi.org/10.1186/s40478-020-00957-y] [PMID: 32503645]
[138]
Hyvärinen, T.; Hagman, S.; Ristola, M.; Sukki, L.; Veijula, K.; Kreutzer, J.; Kallio, P.; Narkilahti, S. Co-stimulation with IL-1β and TNF-α induces an inflammatory reactive astrocyte phenotype with neurosupportive characteristics in a human pluripotent stem cell model system. Sci. Rep., 2019, 9(1), 16944.
[http://dx.doi.org/10.1038/s41598-019-53414-9] [PMID: 31729450]
[139]
Greenbaum, D.; Colangelo, C.; Williams, K.; Gerstein, M. Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biol., 2003, 4(9), 117.
[http://dx.doi.org/10.1186/gb-2003-4-9-117] [PMID: 12952525]
[140]
Koussounadis, A.; Langdon, S.P.; Um, I.H.; Harrison, D.J.; Smith, V.A. Relationship between differentially expressed mRNA and mRNA-protein correlations in a xenograft model system. Sci. Rep., 2015, 5(1), 10775.
[http://dx.doi.org/10.1038/srep10775] [PMID: 26053859]
[141]
Morrey, J.D.; Olsen, A.L.; Siddharthan, V.; Motter, N.E.; Wang, H.; Taro, B.S.; Chen, D.; Ruffner, D.; Hall, J.O. Increased blood–brain barrier permeability is not a primary determinant for lethality of West Nile virus infection in rodents. J. Gen. Virol., 2008, 89(2), 467-473.
[http://dx.doi.org/10.1099/vir.0.83345-0] [PMID: 18198377]
[142]
Belayev, L.; Saul, I.; Busto, R.; Danielyan, K.; Vigdorchik, A.; Khoutorova, L.; Ginsberg, M.D. Albumin treatment reduces neurological deficit and protects blood-brain barrier integrity after acute intracortical hematoma in the rat. Stroke, 2005, 36(2), 326-331.
[http://dx.doi.org/10.1161/01.STR.0000152949.31366.3d] [PMID: 15637329]
[143]
Mychaskiw, G., II; Badr, A.E.; Tibbs, R.; Clower, B.R.; Zhang, J.H. Optison (FS069) disrupts the blood-brain barrier in rats. Anesth. Analg., 2000, 91(4), 798-803.
[http://dx.doi.org/10.1097/00000539-200010000-00007] [PMID: 11004029]
[144]
Hellal, F.; Bonnefont-Rousselot, D.; Croci, N.; Palmier, B.; Plotkine, M.; Marchand-Verrecchia, C. Pattern of cerebral edema and hemorrhage in a mice model of diffuse brain injury. Neurosci. Lett., 2004, 357(1), 21-24.
[http://dx.doi.org/10.1016/j.neulet.2003.12.036] [PMID: 15036604]
[145]
Kim, D.W.; Im, S.H.; Kim, J.Y.; Kim, D.E.; Oh, G.T.; Jeong, S.W. Decreased brain edema after collagenase-induced intracerebral hemorrhage in mice lacking the inducible nitric oxide synthase gene. J. Neurosurg., 2009, 111(5), 995-1000.
[http://dx.doi.org/10.3171/2009.3.JNS081285] [PMID: 19374494]
[146]
Zheng, W.; Aschner, M.; Ghersi-Egea, J.F. Brain barrier systems: A new frontier in metal neurotoxicological research. Toxicol. Appl. Pharmacol., 2003, 192(1), 1-11.
[http://dx.doi.org/10.1016/S0041-008X(03)00251-5] [PMID: 14554098]
[147]
Kim, J.H.; Byun, H.M.; Chung, E.C.; Chung, H.Y.; Bae, O.N. Loss of integrity: Impairment of the blood-brain barrier in heavy metal-associated ischemic stroke. Toxicol. Res., 2013, 29(3), 157-164.
[http://dx.doi.org/10.5487/TR.2013.29.3.157] [PMID: 24386515]
[148]
Elhaik Goldman, S.; Goez, D.; Last, D.; Naor, S.; Liraz Zaltsman, S.; Sharvit-Ginon, I.; Atrakchi-Baranes, D.; Shemesh, C.; Twitto-Greenberg, R.; Tsach, S.; Lotan, R.; Leikin-Frenkel, A.; Shish, A.; Mardor, Y.; Schnaider Beeri, M.; Cooper, I. High-fat diet protects the blood-brain barrier in an Alzheimer’s disease mouse model. Aging Cell, 2018, 17(5), e12818-e12818.
[http://dx.doi.org/10.1111/acel.12818] [PMID: 30079520]
[149]
Li, C.; Shi, L.; Wang, Y.; Peng, C.; Wu, L.; Zhang, Y.; Du, Z. Highfat diet exacerbates lead-induced blood-brain barrier disruption by disrupting tight junction integrity. 2021, 36(7), 1412-1421.
[http://dx.doi.org/10.1002/tox.23137]
[150]
de Paula, G.C.; Brunetta, H.S.; Engel, D.F.; Gaspar, J.M.; Velloso, L.A.; Engblom, D.; de Oliveira, J.; de Bem, A.F. Hippocampal function is impaired by a short-term high-fat diet in mice: Increased blood–brain barrier permeability and neuroinflammation as triggering events. Front. Neurosci., 2021, 15, 734158.
[http://dx.doi.org/10.3389/fnins.2021.734158] [PMID: 34803583]
[151]
Hom, J.; Reitan, R.M. Effect of lateralized cerebral damage upon contralateral and ipsilateral sensorimotor performances. J. Clin. Neuropsychol., 1982, 4(3), 249-268.
[http://dx.doi.org/10.1080/01688638208401133] [PMID: 7142422]
[152]
Foerch, C.; Misselwitz, B.; Sitzer, M.; Berger, K.; Steinmetz, H.; Neumann-Haefelin, T. Difference in recognition of right and left hemispheric stroke. Lancet, 2005, 366(9483), 392-393.
[http://dx.doi.org/10.1016/S0140-6736(05)67024-9] [PMID: 16054939]
[153]
Hedna, V.S.; Bodhit, A.N.; Ansari, S.; Falchook, A.D.; Stead, L.; Heilman, K.M.; Waters, M.F. Hemispheric differences in ischemic stroke: Is left-hemisphere stroke more common? J. Clin. Neurol., 2013, 9(2), 97-102.
[http://dx.doi.org/10.3988/jcn.2013.9.2.97] [PMID: 23626647]
[154]
Goldstein, G.; Shelly, C. Does the right hemisphere age more rapidly than the left? J. Clin. Neuropsychol., 1981, 3(1), 65-78.
[http://dx.doi.org/10.1080/01688638108403114] [PMID: 7276197]
[155]
Simon, A.; Darcsi, A.; Kéry, Á.; Riethmüller, E. Blood-brain barrier permeability study of ginger constituents. J. Pharm. Biomed. Anal., 2020, 177, 112820.
[http://dx.doi.org/10.1016/j.jpba.2019.112820] [PMID: 31476432]
[156]
Bassett, D.S.; Gazzaniga, M.S. Understanding complexity in the human brain. Trends Cogn. Sci., 2011, 15(5), 200-209.
[http://dx.doi.org/10.1016/j.tics.2011.03.006] [PMID: 21497128]
[157]
Abdel-Aziz, H.; Windeck, T.; Ploch, M.; Verspohl, E.J. Mode of action of gingerols and Shogaols on 5-HT3 receptors: Binding studies, cation uptake by the receptor channel and contraction of isolated guinea-pig ileum. Eur. J. Pharmacol., 2006, 530(1-2), 136-143.
[http://dx.doi.org/10.1016/j.ejphar.2005.10.049] [PMID: 16364290]
[158]
Jin, Z.; Lee, G.; Kim, S.; Park, C.S.; Park, Y.S.; Jin, Y.H. Ginger and its pungent constituents non-competitively inhibit serotonin currents on visceral afferent neurons. Korean J. Physiol. Pharmacol., 2014, 18(2), 149-153.
[http://dx.doi.org/10.4196/kjpp.2014.18.2.149] [PMID: 24757377]
[159]
Park, G.; Kim, H.G.; Ju, M.S.; Ha, S.K.; Park, Y.; Kim, S.Y.; Oh, M.S. 6-Shogaol, an active compound of ginger, protects dopaminergic neurons in Parkinson’s disease models via anti-neuroinflammation. Acta Pharmacol. Sin., 2013, 34(9), 1131-1139.
[http://dx.doi.org/10.1038/aps.2013.57] [PMID: 23811724]
[160]
Negishi, T.; Kawasaki, K.; Sekiguchi, S.; Ishii, Y.; Kyuwa, S.; Kuroda, Y.; Yoshikawa, Y. Attention-deficit and hyperactive neurobehavioural characteristics induced by perinatal hypothyroidism in rats. Behav. Brain Res., 2005, 159(2), 323-331.
[http://dx.doi.org/10.1016/j.bbr.2004.11.012] [PMID: 15817195]
[161]
Harsha, S.; Anilakumar, K. Anxiolytic effects of the extracts of Zingiber officinale in mice. J. Pharm. Res., 2012, 5(1), 219-13.
[162]
Yadav, N.; Gaidhani, S. Anxiolytic activity of 6-Shogaol in experimental models of anxiety in mice. Adv. Pharmacol. Toxicol., 2015, 16(2), 11.
[163]
Takeda, H.; Tsuji, M.; Inazu, M.; Egashira, T.; Matsumiya, T. Rosmarinic acid and caffeic acid produce antidepressive-like effect in the forced swimming test in mice. Eur. J. Pharmacol., 2002, 449(3), 261-267.
[http://dx.doi.org/10.1016/S0014-2999(02)02037-X] [PMID: 12167468]
[164]
Orisakwe, O. The role of lead and cadmium in psychiatry. N. Am. J. Med. Sci., 2014, 6(8), 370-376.
[http://dx.doi.org/10.4103/1947-2714.139283] [PMID: 25210669]
[165]
Vagena, E.; Ryu, J.K.; Baeza-Raja, B.; Walsh, N.M.; Syme, C.; Day, J.P.; Houslay, M.D.; Baillie, G.S. A high-fat diet promotes depression-like behavior in mice by suppressing hypothalamic PKA signaling. Transl. Psychiatry, 2019, 9(1), 141.
[http://dx.doi.org/10.1038/s41398-019-0470-1] [PMID: 31076569]
[166]
Sibi, P.I.; Meera, P. In silico docking analysis of constituents of Zingiber officinale as antidepressant. J. Pharmacogn. Phytother., 2013, 5(6), 101-105.
[http://dx.doi.org/10.5897/JPP2013.0280]
[167]
Wietrzych, M.; Meziane, H.; Sutter, A.; Ghyselinck, N.; Chapman, P.F.; Chambon, P.; Krȩżel, W. Working memory deficits in retinoid X receptor γ;-deficient mice. Learn. Mem., 2005, 12(3), 318-326.
[http://dx.doi.org/10.1101/lm.89805] [PMID: 15897255]
[168]
Houpert, P.; Frelon, S.; Lestaevel, P.; Bussy, C.; Gourmelon, P.; Paquet, F. Parental exposure to enriched uranium induced delayed hyperactivity in rat offspring. Neurotoxicology, 2007, 28(1), 108-113.
[http://dx.doi.org/10.1016/j.neuro.2006.08.003] [PMID: 16965816]
[169]
Vorhees, C.V.; Williams, M.T. Morris water maze: Procedures for assessing spatial and related forms of learning and memory. Nat. Protoc., 2006, 1(2), 848-858.
[http://dx.doi.org/10.1038/nprot.2006.116] [PMID: 17406317]
[170]
Chen, P.; Miah, M.R.; Aschner, M. Metals and neurodegeneration. F1000 Res., 2016, 5, 366.
[http://dx.doi.org/10.12688/f1000research.7431.1] [PMID: 27006759]
[171]
Gabriel, M.O.; Nikou, M.; Akinola, O.B.; Pollak, D.D.; Sideromenos, S. Western diet-induced fear memory impairment is attenuated by 6-Shogaol in C57BL/6N mice. Behav. Brain Res., 2020, 380, 112419.
[http://dx.doi.org/10.1016/j.bbr.2019.112419] [PMID: 31816337]
[172]
Kazi, T.G.; Afridi, H.I.; Kazi, N.; Jamali, M.K.; Arain, M.B.; Sarfraz, R.A.; Jalbani, N.; Ansari, R.; Shah, A.Q.; Memon, A.R.; Khandhro, G.A. Distribution of zinc, copper and iron in biological samples of Pakistani myocardial infarction (1st, 2nd and 3rd heart attack) patients and controls. Clin. Chim. Acta, 2008, 389(1-2), 114-119.
[http://dx.doi.org/10.1016/j.cca.2007.12.004] [PMID: 18158921]
[173]
Le Bars, D.; Gozariu, M.; Cadden, S.W. Animal models of nociception. Pharmacol. Rev., 2001, 53(4), 597-652.
[PMID: 11734620]
[174]
Tyebji, S.; Seizova, S.; Garnham, A.L.; Hannan, A.J.; Tonkin, C.J. Impaired social behaviour and molecular mediators of associated neural circuits during chronic toxoplasma gondii infection in female mice. Brain Behav. Immun., 2019, 80, 88-108.
[http://dx.doi.org/10.1016/j.bbi.2019.02.028] [PMID: 30807837]
[175]
Stasko, M.R.; Costa, A.C.S. Experimental parameters affecting the Morris water maze performance of a mouse model of Down syndrome. Behav. Brain Res., 2004, 154(1), 1-17.
[http://dx.doi.org/10.1016/j.bbr.2004.01.012] [PMID: 15302106]
[176]
Young, M.E.; Clark, M.H.; Goffus, A.; Hoane, M.R. Mixed effects modeling of Morris water maze data: Advantages and cautionary notes. Learn. Motiv., 2009, 40(2), 160-177.
[http://dx.doi.org/10.1016/j.lmot.2008.10.004]
[177]
Fu, Y.; Chen, Y.; Li, L.; Wang, Y.; Kong, X.; Wang, J. Food restriction affects Y-maze spatial recognition memory in developing mice. Int. J. Dev. Neurosci., 2017, 60(1), 8-15.
[http://dx.doi.org/10.1016/j.ijdevneu.2017.03.010] [PMID: 28377130]
[178]
Marashi, V.; Barnekow, A.; Ossendorf, E.; Sachser, N. Effects of different forms of environmental enrichment on behavioral, endocrinological, and immunological parameters in male mice. Horm. Behav., 2003, 43(2), 281-292.
[http://dx.doi.org/10.1016/S0018-506X(03)00002-3] [PMID: 12694638]

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