Abstract
Dust storms are environmental natural events that transport high concentrations of particulate matter (PM) in living spaces. Recent epidemiological studies have shown that air pollution is associated with stroke. In the present study we aimed to investigate the probable protective effects of gallic acid (GA) on blood-brain barrier (BBB) disruption, brain oxidative stress, anxiety, depression, locomotion behaviors, and changes of hippocampal local electroencephalogram (local EEG) power induced by 4-vessel transient occlusion (4VO I/R) following exposure to dusty PM in rats. Male Wistar rats were divided randomly into eight groups: (1) vehicle+Sham (Veh + Sh), (2) vehicle+4VO I/R (Veh + I/R), (3) gallic acid+sham (GA + Sh), (4) gallic acid+4VO I/R (GA + I/R), (5) vehicle+PM (Veh + PM), (6) PM + 4VO I/R (PM + I/R), (7) gallic acid+PM + Sham (GA + PM + Sh), and (8) gallic acid+PM + 4Vo I/R (GA + PM + I/R). 4VO type of I/R was induced after 10 days of pretreatment by GA 100 mg/kg/2 ml/ip, or 2 ml/kg/ip, normal saline as vehicle (Veh) and exposure to dust storm composed of dusty PM (DPM, 2000–8000 μg/m3), 60 min daily for consecutive 10 days) simultaneously. Seventy-two hours after I/R induction, all behavioral tests and BBB permeability evaluation were done. Hippocampus local EEG was recorded just before and 72 h after I/R induction, and finally brain tissue oxidative stress was assayed. Data showed that 4VO I/R following exposure to DPM increased BBB permeability (p < 0.001), brain oxidative stress (p < 0.001), induced anxiety (p < 0.001), depression (p < 0.01), locomotion impairment (p < 0.001), superoxide dismutase (SOD) activity, and local EEG power also were decreased in PM + Sh (p < 0.001). Pretreatment with GA reversed BBB permeability and MDA. Our findings suggest that GA is a probable protective agent against adverse effects of both I/R and exposure to DPM and also in I/R subjects exposed to DPM. The beneficial effects of GA may induce by its antioxidative and anti-inflammatory properties.
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Babadjouni RM, Hodis DM, Radwanski R, Durazo R, Patel A, Liu Q, Mack WJ (2017) Clinical effects of air pollution on the central nervous system; a review. J Clin Neurosci 43:16–24
Can OD, Turan N, Demir Ozkay U, Ozturk Y (2017) Antidepressant-like effect of gallic acid in mice: Dual involvement of serotonergic and catecholaminergic systems. Life Sci 190:110–117
Chen T, Dai S-H, Li X, Luo P, Zhu J, Wang Y-H, Fei Z, Jiang X-F (2018) Sirt1-Sirt3 axis regulates human blood-brain barrier permeability in response to ischemia. Redox Biol 14:229–236
Chhillar R, Dhingra D (2013) Antidepressant-like activity of gallic acid in mice subjected to unpredictable chronic mild stress. Fundam Clin Pharmacol 27:409–418
Dhingra D, Chhillar R, Gupta A (2012) Antianxiety-like activity of gallic acid in unstressed and stressed mice: possible involvement of nitriergic system. Neurochem Res 37:487–494
Draxler RR (2011): Hysplit (hybrid single-particle lagrangian integrated trajectory) model access via NOAA ARL ready website. http://ready. arl. noaa. gov/HYSPLIT. php
Fang C, Li Q, Min G, Liu M, Cui J, Sun J, Li L (2017) Microrna-181c ameliorates cognitive impairment induced by chronic cerebral hypoperfusion in rats. Mol Neurobiol 54:8370–8385
Farbood Y, Sarkaki A, Dianat M, Khodadadi A, Haddad MK, Mashhadizadeh S (2015) Ellagic acid prevents cognitive and hippocampal long-term potentiation deficits and brain inflammation in rat with traumatic brain injury. Life Sci 124:120–127
Hoffmann C, Funk R, Sommer M, Li Y (2008) Temporal variations in PM10 and particle size distribution during Asian dust storms in Inner Mongolia. Atmos Environ 42:8422–8431
Jia Z, Wei Y, Li X, Yang L, Liu H, Guo C, Zhang L, Li N, Guo S, Qian Y (2018) Exposure to ambient air particles increases the risk of mental disorder: Findings from a natural experiment in Beijing. Int J Environ Res Public Health 15:160
Kannan MM, Quine SD (2011) Ellagic acid ameliorates isoproterenol induced oxidative stress: Evidence from electrocardiological, biochemical and histological study. Eur J Pharmacol 659:45–52
Korani MS, Farbood Y, Sarkaki A, Moghaddam HF, Mansouri MT (2014) Protective effects of gallic acid against chronic cerebral hypoperfusion-induced cognitive deficit and brain oxidative damage in rats. Eur J Pharmacol 733:62–67
Li Z, Wang Y, Xie Y, Yang Z, Zhang T (2011) Protective effects of exogenous hydrogen sulfide on neurons of hippocampus in a rat model of brain ischemia. Neurochem Res 36:1840–1849
Naimabadi A, Ghadiri A, Idani E, Babaei AA, Alavi N, Shirmardi M, Khodadadi A, Marzouni MB, Ankali KA, Rouhizadeh A (2016) Chemical composition of PM10 and its in vitro toxicological impacts on lung cells during the Middle Eastern Dust (MED) storms in Ahvaz, Iran. Environ Pollut 211:316–324
Nejad KH, Sarkaki A, Dianat M, Farbood Y, Badavi M, Gharib-Naseri MK (2017) Preventive effects of ellagic acid on nucleus tractus solitarius electrical activity and oxidative stress altered by cerebral global ischemia/reperfusion in rat. Braz Arch Biol Technol:60
Organization WH (2014): http://www. who. int/mediacentre/factsheets/fs340/en. url > http://www. who. int/mediacentre/factsheets/fs241/en/</url
Pietrelli A, Lopez-Costa J, Goni R, Brusco A, Basso N (2012) Aerobic exercise prevents age-dependent cognitive decline and reduces anxiety-related behaviors in middle-aged and old rats. Neuroscience 202:252–266
Pulsinelli WA, Brierley JB (1979) A new model of bilateral hemispheric ischemia in the unanesthetized rat. Stroke 10:267–272
Qi D-S, J-h T, Zhang L-Q, Li M, Wang M, Qu R, Zhang S-C, Liu P, Liu F, Miu J-C (2016) Neuroprotection of cilostazol against ischemia/reperfusion-induced cognitive deficits through inhibiting JNK3/caspase-3 by enhancing Akt1. Brain Res 1653:67–74
Rosenberg GA (2012) Neurological diseases in relation to the blood–brain barrier. J Cereb Blood Flow Metab 32:1139–1151
Salehi A, Rabiei Z, Setorki M (2018) Effect of gallic acid on chronic restraint stress-induced anxiety and memory loss in male BALB/c mice. Iran j basic med sci 21:1232–1237
Sarkaki A, Farbood Y, Dolatshahi M, Mansouri SMT, Khodadadi A (2016) Neuroprotective effects of ellagic acid in a rat model of Parkinson's disease. Acta Medica Iranica 54:494–502
Schweizer S, Meisel A, Märschenz S (2013) Epigenetic mechanisms in cerebral ischemia. J Cereb Blood Flow Metab 33:1335–1346
Shih C-H, Chen J-K, Kuo L-W, Cho K-H, Hsiao T-C, Lin Z-W, Lin Y-S, Kang J-H, Lo Y-C, Chuang K-J (2018) Chronic pulmonary exposure to traffic-related fine particulate matter causes brain impairment in adult rats. Part fibre toxicol 15:44
Szekeres T, Fritzer-Szekeres M, Saiko P, Jäger W (2010) Resveratrol and resveratrol analogues—structure—activity relationship. Pharm Res 27:1042–1048
Takata F, Dohgu S, Matsumoto J, Machida T, Kaneshima S, Matsuo M, Sakaguchi S, Takeshige Y, Yamauchi A, Kataoka Y (2013) Metformin induces up-regulation of blood–brain barrier functions by activating AMP-activated protein kinase in rat brain microvascular endothelial cells. Biochem Biophys Res Commun 433:586–590
van Putten MJ, Hofmeijer J (2016) EEG monitoring in cerebral ischemia: basic concepts and clinical applications. J Clin Neurophysiol 33:203–210
Wright JC, Ding Y (2016) Pathophysiological effects of particulate matter air pollution on the central nervous system. Environ Disease 1:85
Xue R, Wu G, Wei X, Lv J, Fu R, Lei X, Zhang Z, Li W, He J, Zhao H (2016) Tea polyphenols may attenuate the neurocognitive impairment caused by global cerebral ischemia/reperfusion injury via anti-apoptosis. Nutr Neurosci 19:63–69
Zare N, Khalifeh S, Khodagholi F, Shahamati SZ, Motamedi F, Maghsoudi N (2015) Geldanamycin reduces Aβ-associated anxiety and depression, concurrent with autophagy provocation. J Mol Neurosci 57:317–324
Zhang X, Zhao L, Tong DQ, Wu G, Dan M, Teng B (2016) A systematic review of global desert dust and associated human health effects. Atmosphere 7:158
Zhu JX, Shan JL, Hu WQ, Zeng JX, Shu JC (2019) Gallic acid activates hippocampal BDNF-Akt-mTOR signaling in chronic mild stress. Metab Brain Dis 34:93–101
Acknowledgments
This article extracted as a part of Mr. Hamzeh Mirshekari Jahangiri’s M.Sc. thesis. This work was supported by Persian Gulf Physiology Research Center (grant no. APRC-9708), funded by the Vice Chancellor of Research, Ahvaz Jundishapur University of Medical Sciences (Iran) and also as a part of a research project (grant no. 971250) supported by National Institute for Medical Research Development (NIMAD). We are also grateful to Dr. Seyed Esmaeil Khoshnam and Dr. Mohammad Rashno for their contribution and scientific supports.
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Mirshekari Jahangiri, H., Sarkaki, A., Farbood, Y. et al. Gallic acid affects blood-brain barrier permeability, behaviors, hippocampus local EEG, and brain oxidative stress in ischemic rats exposed to dusty particulate matter. Environ Sci Pollut Res 27, 5281–5292 (2020). https://doi.org/10.1007/s11356-019-07076-9
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DOI: https://doi.org/10.1007/s11356-019-07076-9