Skip to main content
SpringerLink
Log in

Effects of Gallic Acid on Memory Deficits and Electrophysiological Impairments Induced by Cerebral Ischemia/Reperfusion in Rats Following Exposure to Ambient Dust Storm

  • Original Paper
  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

We aimed to investigate the probable protective effects of gallic acid (GA) on cognitive deficits, hippocampal long term potentiation (LTP) impairments, and molecular changes induced by cerebral ischemia/reperfusion (I/R) in rats following exposure to ambient dust storm. After pretreatment with GA (100 mg/kg), or vehicle (Veh) (normal saline, 2 ml/kg) for ten days, and 60 minutes’ exposure to dust storm including PM (PM, 2000–8000 g/m3) every day, 4-vessel occlusion (4VO) type of I/R was induced. Three days after I/R induction, we evaluated behavioral, electrophysiological, histopathological, molecular and brain tissue inflammatory cytokine changes. Our findings indicated that pretreatment with GA significantly reduced cognitive impairments caused by I/R (P < 0.05) and hippocampal LTP impairments caused by I/R after PM exposure (P < 0.001). Additionally, after exposure to PM, I/R significantly elevated the tumor necrosis factor α content (P < 0.01) and miR-124 level (P < 0.001) while pre-treatment with GA reduced the level of miR-124 (P < 0.001). Histopathological results also revealed that I/R and PM caused cell death in the hippocampus CA1 area (P < 0.001) and that GA decreased the rate of cell death (P < 0.001). Our findings show that GA can prevent brain inflammation, and thus cognitive and LTP deficits caused by I/R, PM exposure, or both.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Kurosaki Y, Mikami M (2003) Recent frequent dust events and their relation to surface wind in East Asia. Geophys Res Lett. https://doi.org/10.1029/2003GL017261

    Article  Google Scholar 

  2. Wang X, Bi X, Sheng G, Fu J (2006) Chemical composition and sources of PM10 and PM2. 5 aerosols in Guangzhou, China. Environ Monit Assess 119(1–3):425–439

    Article  CAS  PubMed  Google Scholar 

  3. Anuforom AC (2007) Spatial distribution and temporal variability of Harmattan dust haze in sub-sahel West Africa. Atmos Environ 41(39):9079–9090

    Article  CAS  Google Scholar 

  4. Kellogg CA, Griffin DW, Garrison VH, Peak KK, Royall N, Smith RR et al (2004) Characterization of aerosolized bacteria and fungi from desert dust events in Mali, West Africa. Aerobiologia 20(2):99–110

    Article  Google Scholar 

  5. Astort F, Sittner M, Ferraro SA, Orona NS, Maglione GA, De la Hoz A et al (2014) Pulmonary inflammation and cell death in mice after acute exposure to air particulate matter from an industrial region of Buenos Aires. Arch Environ Contam Toxicol 67(1):87–96

    CAS  PubMed  Google Scholar 

  6. Davel AP, Lemos M, Pastro LM, Pedro SC, de André PA, Hebeda C et al (2012) Endothelial dysfunction in the pulmonary artery induced by concentrated fine particulate matter exposure is associated with local but not systemic inflammation. Toxicology 295(1–3):39–46

    Article  CAS  PubMed  Google Scholar 

  7. Cui Y, Sun Q, Liu Z (2016) Ambient particulate matter exposure and cardiovascular diseases: a focus on progenitor and stem cells. J Cell Mol Med 20(5):782–793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Weinmayr G, Hennig F, Fuks K, Nonnemacher M, Jakobs H, Möhlenkamp S et al (2015) Long-term exposure to fine particulate matter and incidence of type 2 diabetes mellitus in a cohort study: effects of total and traffic-specific air pollution. Environ Health 14(1):1–8

    Article  CAS  Google Scholar 

  9. Jahangiri HM, Sarkaki A, Farbood Y, Dianat M, Goudarzi G (2020) 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(5):5281–5292

    Article  Google Scholar 

  10. Xu X, Ha SU, Basnet R (2016) A review of epidemiological research on adverse neurological effects of exposure to ambient air pollution. Front public health 4:157

    Article  PubMed  PubMed Central  Google Scholar 

  11. Schmid O, Möller W, Semmler-Behnke M, Ferron A, Karg G, Lipka E (2009) Dosimetry and toxicology of inhaled ultrafine particles. Biomarkers 14(sup1):67–73

    Article  CAS  PubMed  Google Scholar 

  12. Furuyama A, Kanno S, Kobayashi T, Hirano S (2009) Extrapulmonary translocation of intratracheally instilled fine and ultrafine particles via direct and alveolar macrophage-associated routes. Arch Toxicol 83(5):429–437

    Article  CAS  PubMed  Google Scholar 

  13. Oberdörster G, Sharp Z, Atudorei V, Elder A, Gelein R, Kreyling W et al (2004) Translocation of inhaled ultrafine particles to the brain. Inhalation Toxicol 16(6–7):437–445

    Article  Google Scholar 

  14. Wilker EH, Preis SR, Beiser AS, Wolf PA, Au R, Kloog I et al (2015) Long-term exposure to fine particulate matter, residential proximity to major roads and measures of brain structure. Stroke 46(5):1161–1166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Apte JS, Marshall JD, Cohen AJ, Brauer M (2015) Addressing global mortality from ambient PM2. 5. Environ Sci Technol 49(13):8057–8066

    Article  CAS  PubMed  Google Scholar 

  16. Dai J, Sun C, Yao Z, Chen W, Yu L, Long M (2016) Exposure to concentrated ambient fine particulate matter disrupts vascular endothelial cell barrier function via the IL-6/HIF‐1α signaling pathway. FEBS open bio 6(7):720–728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Hajipour S, Farbood Y, Gharib-Naseri MK, Goudarzi G, Rashno M, Maleki H et al (2020) Exposure to ambient dusty particulate matter impairs spatial memory and hippocampal LTP by increasing brain inflammation and oxidative stress in rats. Life Sci 242:117210

    Article  CAS  PubMed  Google Scholar 

  18. Brook RD, Rajagopalan S (2010) Particulate matter air pollution and atherosclerosis. Curr Atheroscler Rep 12(5):291–300

    Article  CAS  PubMed  Google Scholar 

  19. Bhouri W, Boubaker J, Skandrani I, Ghedira K, Ghedira LC (2012) Investigation of the apoptotic way induced by digallic acid in human lymphoblastoid TK6 cells. Cancer Cell Int 12(1):1–8

    Article  Google Scholar 

  20. Bastianetto S, Yao ZX, Papadopoulos V, Quirion R (2006) Neuroprotective effects of green and black teas and their catechin gallate esters against β-amyloid‐induced toxicity. Eur J Neurosci 23(1):55–64

    Article  PubMed  Google Scholar 

  21. Sarkaki A, Farbood Y, Mansouri SMT, Badavi M, Khorsandi L, Dehcheshmeh MG et al (2019) Chrysin prevents cognitive and hippocampal long-term potentiation deficits and inflammation in rat with cerebral hypoperfusion and reperfusion injury. Life Sci 226:202–209

    Article  CAS  PubMed  Google Scholar 

  22. Pulsinelli WA, Brierley JB (1979) A new model of bilateral hemispheric ischemia in the unanesthetized rat. Stroke 10(3):267–272

    Article  CAS  PubMed  Google Scholar 

  23. 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(36):8422–8431

    Article  CAS  Google Scholar 

  24. Morris R (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11(1):47–60

    Article  CAS  PubMed  Google Scholar 

  25. 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

    Article  CAS  PubMed  Google Scholar 

  26. Musah S, DeJarnett N, Hoyle GW (2012) Tumor necrosis factor-α mediates interactions between macrophages and epithelial cells underlying proinflammatory gene expression induced by particulate matter. Toxicology 299(2–3):125–132

    Article  CAS  PubMed  Google Scholar 

  27. Mard SA, Akbari G, Dianat M, Mansouri E (2019) The effect of zinc sulfate on miR-122, miR-34a, Atioxidants, biochemical and histopathological parameters following hepatic ischemia/reperfusion injury in rats. Biol Trace Elem Res 188(2):434–440

    Article  CAS  PubMed  Google Scholar 

  28. Khoshnam SE, Sarkaki A, Khorsandi L, Winlow W, Badavi M, Moghaddam HF et al (2017) Vanillic acid attenuates effects of transient bilateral common carotid occlusion and reperfusion in rats. Biomed Pharmacother 96:667–674

    Article  CAS  PubMed  Google Scholar 

  29. Fang C, Li Q, Min G, Liu M, Cui J, Sun J et al (2017) MicroRNA-181c ameliorates cognitive impairment induced by chronic cerebral hypoperfusion in rats. Mol Neurobiol 54(10):8370–8385

    Article  CAS  PubMed  Google Scholar 

  30. Xue R, Wu G, Wei X, Lv J, Fu R, Lei X et al (2016) Tea polyphenols may attenuate the neurocognitive impairment caused by global cerebral ischemia/reperfusion injury via anti-apoptosis. Nutr Neurosci 19(2):63–69

    Article  CAS  PubMed  Google Scholar 

  31. Ten VS, Wu EX, Tang H, Bradley-Moore M, Fedarau MV, Ratner VI et al (2004) Late measures of brain injury after neonatal hypoxia–ischemia in mice. Stroke 35(9):2183–2188

    Article  PubMed  Google Scholar 

  32. Farbood Y, Sarkaki A, Hashemi S, Mansouri MT, Dianat M (2013) The effects of gallic acid on pain and memory following transient global ischemia/reperfusion in Wistar rats. Avicenna J Phytomed 3(4):329

    PubMed  PubMed Central  Google Scholar 

  33. Cechetti F, Pagnussat AS, Worm PV, Elsner VR, Ben J, da Costa MS et al (2012) Chronic brain hypoperfusion causes early glial activation and neuronal death, and subsequent long-term memory impairment. Brain Res Bull 87(1):109–116

    Article  CAS  PubMed  Google Scholar 

  34. Ailshire JA, Crimmins EM (2014) Fine particulate matter air pollution and cognitive function among older US adults. Am J Epidemiol 180(4):359–366

    Article  PubMed  PubMed Central  Google Scholar 

  35. Morgan JA, Singhal G, Corrigan F, Jaehne EJ, Jawahar MC, Baune BT (2018) TNF signalling via the TNF receptors mediates the effects of exercise on cognition-like behaviours. Behav Brain Res 353:74–82

    Article  CAS  PubMed  Google Scholar 

  36. Taylor DL, Jones F, Kubota ESCS, Pocock JM (2005) Stimulation of microglial metabotropic glutamate receptor mGlu2 triggers tumor necrosis factor α-induced neurotoxicity in concert with microglial-derived Fas ligand. J Neurosci 25(11):2952–2964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Khoshnam SE, Sarkaki A, Rashno M, Farbood Y (2018) Memory deficits and hippocampal inflammation in cerebral hypoperfusion and reperfusion in male rats: neuroprotective role of vanillic acid. Life Sci 211:126–132

    Article  CAS  PubMed  Google Scholar 

  38. Sabat R, Grütz G, Warszawska K, Kirsch S, Witte E, Wolk K et al (2010) Biology of interleukin-10. Cytokine Growth Factor Rev 21(5):331–344

    Article  CAS  PubMed  Google Scholar 

  39. Spera PA, Ellison JA, Feuerstein GZ, Barone FC (1998) IL-10 reduces rat brain injury following focal stroke. Neurosci Lett 251(3):189–192

    Article  CAS  PubMed  Google Scholar 

  40. Wang X, Zhang X, Ren X-P, Chen J, Liu H, Yang J et al (2010) MicroRNA-494 targeting both proapoptotic and antiapoptotic proteins protects against ischemia/reperfusion-induced cardiac injury. Circulation 122(13):1308–1318

    Article  PubMed  PubMed Central  Google Scholar 

  41. Peng B, Guo Q-l, He Z-j, Ye Z, Yuan Y-j, Wang N et al (2012) Remote ischemic postconditioning protects the brain from global cerebral ischemia/reperfusion injury by up-regulating endothelial nitric oxide synthase through the PI3K/Akt pathway. Brain Res 1445:92–102

    Article  CAS  PubMed  Google Scholar 

  42. Ma Q, Zhao H, Tao Z, Wang R, Liu P, Han Z et al (2016) MicroRNA-181c exacerbates brain injury in acute ischemic stroke. Aging and disease 7(6):705

    Article  PubMed  PubMed Central  Google Scholar 

  43. Miao W, Yan Y, Bao T-h, Jia W-j, Yang F, Wang Y et al (2020) Ischemic postconditioning exerts neuroprotective effect through negatively regulating PI3K/Akt2 signaling pathway by microRNA-124. Biomed Pharmacother 126:109786

    Article  CAS  PubMed  Google Scholar 

  44. He X, Zheng Y, Liu S, Shi S, Liu Y, He Y et al (2018) MiR-146a protects small intestine against ischemia/reperfusion injury by down‐regulating TLR4/TRAF6/NF‐κB pathway. J Cell Physiol 233(3):2476–2488

    Article  CAS  PubMed  Google Scholar 

  45. Nguyen LS, Fregeac J, Bole-Feysot C, Cagnard N, Iyer A, Anink J et al (2018) Role of miR-146a in neural stem cell differentiation and neural lineage determination: relevance for neurodevelopmental disorders. Mol autism 9(1):1–12

    Article  Google Scholar 

  46. Qu X, Wang N, Cheng W, Xue Y, Chen W, Qi M (2019) MicroRNA–146a protects against intracerebral hemorrhage by inhibiting inflammation and oxidative stress. Exp Ther Med 18(5):3920–3928

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are grateful to Dr. Mohammad Rashno for his contribution and scientific support.

Funding

This article was extracted from Kowsar Bavarsad’s post-Doc thesis (PD-APRC-9701). Research reported in this publication was supported by the Elite Researchers Grant Committee under award number [Grant No. 971250] from the National Institute for Medical Research Development (NIMAD), Tehran, Iran. This work was carried out in the Persian Gulf Physiology Research Center and was partially funded by Research Affaires Deputy of Ahvaz Jundishapur University of Medical Sciences.

Author information

Authors and Affiliations

  1. Department of Physiology, Faculty of Medicine, Persian Gulf Physiology Research Center, Medical Basic Sciences Research Institute, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran

    Kowsar Bavarsad, Yaghoob Farbood, Seyed Ali Mard, Seyed Esmaeil Khoshnam, Mahin Dianat & Hamzeh Mirshekari Jahangiri

  2. National Institute for Medical Research Development “NIMAD”, Tehran, Iran

    Kowsar Bavarsad, Yaghoob Farbood, Seyed Ali Mard, Seyed Esmaeil Khoshnam, Mahin Dianat, Hamzeh Mirshekari Jahangiri, Laya Sadat Khorsandi, Gholamreza Goudarzi & Alireza Sarkaki

  3. Department of Physiology, School of Medicine, Iran University of Medical Sciences, Tehran, Iran

    Hamzeh Mirshekari Jahangiri

  4. Department of Anatomical Sciences, Cellular & Molecular Research Center, Medical Basic Sciences Institute, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran

    Laya Sadat Khorsandi

  5. Department of Environmental Health Engineering, Environmental Technology Research Center, Jundishapur University of Medical Science, Ahvaz, Iran

    Gholamreza Goudarzi

  6. Medicinal Plants Research Center, Persian Gulf Physiology Research Center, Medical Basic Sciences Research Institute, Department of Physiology, Faculty of Medicine, Ahvaz Jundishapur University of Medica Sciences, Ahvaz, Iran

    Alireza Sarkaki

Authors
  1. Kowsar Bavarsad
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yaghoob Farbood
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Seyed Ali Mard
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Seyed Esmaeil Khoshnam
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mahin Dianat
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hamzeh Mirshekari Jahangiri
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Laya Sadat Khorsandi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Gholamreza Goudarzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Alireza Sarkaki
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

KB: Conceptualization, Methodology, Formal analysis, Investigation, Resources, Writing—Original Draft, Writing—Review & Editing, Visualization. YF: Conceptualization, Methodology, Visualization. SEK: Conceptualization, Methodology, Visualization. SAM: Methodology, Formal analysis, Investigation, Writing—Review & Editing, Visualization. MD: Conceptualization, Investigation, Resources, Visualization. HMJ: Conceptualization, Methodology, Formal analysis, Investigation. LSK: Methodology, Formal analysis, Investigation, Resources. GG: Methodology, Formal analysis, Investigation, Visualization. AS: Conceptualization, Methodology, Formal analysis, Investigation, Resources, Writing—Review & Editing, Visualization, Supervision, Project administration.

Corresponding author

Correspondence to Alireza Sarkaki.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bavarsad, K., Farbood, Y., Mard, S.A. et al. Effects of Gallic Acid on Memory Deficits and Electrophysiological Impairments Induced by Cerebral Ischemia/Reperfusion in Rats Following Exposure to Ambient Dust Storm. Neurochem Res 48, 2911–2923 (2023). https://doi.org/10.1007/s11064-023-03953-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-023-03953-5

Keywords

Search

Navigation