Korean Journal of Veterinary Research (대한수의학회지)

The Korean Society of Veterinary Science (대한수의학회)
권호 표지
DOI QR코드

DOI QR Code

Alleviation of γ-enolase decrease by the chlorogenic acid administration in the stroke animal model

뇌졸중에서 클로로겐산 투여에 의한 γ-enolase 감소 완화 효과

  • Ju-Bin Kang (Department of Veterinary Anatomy and Histology, College of Veterinary Medicine, Gyeongsang National University) ;
  • Murad Ali Shah (Department of Veterinary Anatomy and Histology, College of Veterinary Medicine, Gyeongsang National University) ;
  • Min-Seo Ko (Department of Veterinary Anatomy and Histology, College of Veterinary Medicine, Gyeongsang National University) ;
  • Phil-Ok Koh (Department of Veterinary Anatomy and Histology, College of Veterinary Medicine, Gyeongsang National University)
  • 강주빈 (경상국립대학교 수의과대학 수의해부조직학교실) ;
  • ;
  • 고민서 (경상국립대학교 수의과대학 수의해부조직학교실) ;
  • 고필옥 (경상국립대학교 수의과대학 수의해부조직학교실)
  • Received : 2023.02.21
  • Accepted : 2023.03.22
  • Published : 2023.03.31
Download PDF
⟨ Previous Next ⟩

Abstract

Stroke is a major cause of death and long-term disability. Chlorogenic acid is a phenolic compound with a potent neuroprotective effect. γ-enolase is a phosphopyruvate hydratase found in mature neurons and plays an important role in neuronal survival. This study investigated whether chlorogenic acid regulates the expression of γ-enolase during cerebral ischemia. Middle cerebral artery occlusion (MCAO) was performed to induce cerebral ischemia. Adult male rats were used and chlorogenic acid (30 mg/kg) or phosphate buffered saline (PBS) was injected intraperitoneally 2 hours after MCAO surgery. Cerebral cortical tissues were collected 24 hours after MCAO surgery. Our proteomic approach identified the reduction of γ-enolase caused by MCAO damage and the mitigation of this reduction by chlorogenic acid treatment. Results of reverse transcription-polymerase chain reaction and Western blot analyses showed a decrease in γ-enolase expression in the PBS-treated MCAO group. However, chlorogenic acid treatment attenuated this decrease. Results of immunofluorescence staining showed the change of γ-enolase by chlorogenic acid treatment. These results demonstrated that chlorogenic acid regulates the γ-enolase expression during MCAO-induced ischemia. Therefore, we suggest that chlorogenic acid mediates the neuroprotective function by regulating the γ-enolase expression in cerebral ischemia and may be used as a therapeutic agent for brain diseases including stroke.

Keywords

Acknowledgement

This research was supported by the National Research Foundation of Korea (NRF) Grant funded by the Korea government (MEST) (NRF-2021R1F1A105878711).

References

  1. Ingall T. Stroke: incidence, mortality, morbidity and risk. J Insur Med 2004;36:143-152. 
  2. Grysiewicz RA, Thomas K, Pandey DK. Epidemiology of ischemic and hemorrhagic stroke: incidence, prevalence, mortality, and risk factors. Neurol Clin 2008;26:871-895.  https://doi.org/10.1016/j.ncl.2008.07.003
  3. Khoshnam SE, Winlow W, Farzaneh M, Farbood Y, Moghaddam HF. Pathogenic mechanisms following ischemic stroke. Neurol Sci 2017;38:1167-1186.  https://doi.org/10.1007/s10072-017-2938-1
  4. Tuo QZ, Zhang ST, Lei P. Mechanisms of neuronal cell death in ischemic stroke and their therapeutic implications. Med Res Rev 2022;42:259-305.  https://doi.org/10.1002/med.21817
  5. Wu LJ, Wu G, Akhavan Sharif MR, Baker A, Jia Y, Fahey FH, Luo HR, Feener EP, Clapham DE. The voltage-gated proton channel Hv1 enhances brain damage from ischemic stroke. Nat Neurosci 2012;15:565-573.  https://doi.org/10.1038/nn.3059
  6. Yang Q, Huang Q, Hu Z, Tang X. Potential neuroprotective treatment of stroke: targeting excitotoxicity, oxidative stress, and inflammation. Front Neurosci 2019;13:1036. 
  7. Rashidi R, Rezaee R, Shakeri A, Hayes AW, Karimi G. A review of the protective effects of chlorogenic acid against different chemicals. J Food Biochem 2022;46:e14254. 
  8. Miao M, Xiang L. Pharmacological action and potential targets of chlorogenic acid. Adv Pharmacol 2020;87:71-88.  https://doi.org/10.1016/bs.apha.2019.12.002
  9. Park CM, Yoon HS. Chlorogenic acid as a positive regulator in LPS-PG-induced inflammation via TLR4/MyD88-mediated NF-κB and PI3K/MAPK signaling cascades in human gingival fibroblasts. Mediators Inflamm 2022;2022:2127642. 
  10. Shi M, Sun F, Wang Y, Kang J, Zhang S, Li H. CGA restrains the apoptosis of Aβ25-35-induced hippocampal neurons. Int J Neurosci 2020;130:700-707.  https://doi.org/10.1080/00207454.2019.1702547
  11. Singh SS, Rai SN, Birla H, Zahra W, Rathore AS, Dilnashin H, Singh R, Singh SP. Neuroprotective effect of chlorogenic acid on mitochondrial dysfunction-mediated apoptotic death of DA neurons in a Parkinsonian mouse model. Oxid Med Cell Longev 2020;2020:6571484. 
  12. Zheng Y, Li L, Chen B, Fang Y, Lin W, Zhang T, Feng X, Tao X, Wu Y, Fu X, Lin Z. Chlorogenic acid exerts neuroprotective effect against hypoxia-ischemia brain injury in neonatal rats by activating Sirt1 to regulate the Nrf2-NF-κB signaling pathway. Cell Commun Signal 2022;20:84. 
  13. Shah MA, Kang JB, Park DJ, Kim MO, Koh PO. Chlorogenic acid alleviates neurobehavioral disorders and brain damage in focal ischemia animal models. Neurosci Lett 2021;760:136085. 
  14. Schmechel DE, Brightman MW, Marangos PJ. Neurons switch from non-neuronal enolase to neuron-specific enolase during differentiation. Brain Res 1980;190:195-214.  https://doi.org/10.1016/0006-8993(80)91169-5
  15. Rider CC, Taylor CB. Enolase isoenzymes in rat tissues: electrophoretic, chromatographic, immunological and kinetic properties. Biochim Biophys Acta 1974;365:285-300.  https://doi.org/10.1016/0005-2795(74)90273-6
  16. Lamande N, Mazo AM, Lucas M, Montarras D, Pinset C, Gros F, Legault-Demare L, Lazar M. Murine muscle-specific enolase: cDNA cloning, sequence, and developmental expression. Proc Natl Acad Sci U S A 1989;86:4445-4449.  https://doi.org/10.1073/pnas.86.12.4445
  17. Schmechel D, Marangos PJ, Zis AP, Brightman M, Goodwin FK. Brain endolases as specific markers of neuronal and glial cells. Science 1978;199:313-315.  https://doi.org/10.1126/science.339349
  18. Hattori T, Ohsawa K, Mizuno Y, Kato K, Kohsaka S. Synthetic peptide corresponding to 30 amino acids of the C-terminal of neuron-specific enolase promotes survival of neocortical neurons in culture. Biochem Biophys Res Commun 1994;202:25-30.  https://doi.org/10.1006/bbrc.1994.1888
  19. Hattori T, Takei N, Mizuno Y, Kato K, Kohsaka S. Neurotrophic and neuroprotective effects of neuron-specific enolase on cultured neurons from embryonic rat brain. Neurosci Res 1995;21:191-198.  https://doi.org/10.1016/0168-0102(94)00849-B
  20. Hafner A, Obermajer N, Kos J. γ-Enolase C-terminal peptide promotes cell survival and neurite outgrowth by activation of the PI3K/Akt and MAPK/ERK signalling pathways. Biochem J 2012;443:439-450.  https://doi.org/10.1042/BJ20111351
  21. Haque A, Polcyn R, Matzelle D, Banik NL. New insights into the role of neuron-specific enolase in neuro-inflammation, neurodegeneration, and neuroprotection. Brain Sci 2018;8:33. 
  22. Anand N, Stead LG. Neuron-specific enolase as a marker for acute ischemic stroke: a systematic review. Cerebrovasc Dis 2005;20:213-219.  https://doi.org/10.1159/000087701
  23. Lee K, Lee JS, Jang HJ, Kim SM, Chang MS, Park SH, Kim KS, Bae J, Park JW, Lee B, Choi HY, Jeong CH, Bu Y. Chlorogenic acid ameliorates brain damage and edema by inhibiting matrix metalloproteinase-2 and 9 in a rat model of focal cerebral ischemia. Eur J Pharmacol 2012;689:89-95.  https://doi.org/10.1016/j.ejphar.2012.05.028
  24. Shamsaei N, Erfani S, Fereidoni M, Shahbazi A. Neuroprotective effects of exercise on brain edema and neurological movement disorders following the cerebral ischemia and reperfusion in rats. Basic Clin Neurosci 2017;8:77-84.  https://doi.org/10.15412/J.BCN.03080110
  25. Li X, Blizzard KK, Zeng Z, DeVries AC, Hurn PD, McCullough LD. Chronic behavioral testing after focal ischemia in the mouse: functional recovery and the effects of gender. Exp Neurol 2004;187:94-104.  https://doi.org/10.1016/j.expneurol.2004.01.004
  26. Chen SD, Yang DI, Lin TK, Shaw FZ, Liou CW, Chuang YC. Roles of oxidative stress, apoptosis, PGC-1α and mitochondrial biogenesis in cerebral ischemia. Int J Mol Sci 2011;12:7199-7215.  https://doi.org/10.3390/ijms12107199
  27. Halliwell B. Oxidative stress and neurodegeneration: where are we now? J Neurochem 2006;97:1634-1658.  https://doi.org/10.1111/j.1471-4159.2006.03907.x
  28. Shah MA, Kang JB, Park DJ, Kim MO, Koh PO. Chlorogenic acid alleviates cerebral ischemia-induced neuroinflammation via attenuating nuclear factor kappa B activation. Neurosci Lett 2022;773:136495. 
  29. Cronberg T, Rundgren M, Westhall E, Englund E, Siemund R, Rosen I, Widner H, Friberg H. Neuron-specific enolase correlates with other prognostic markers after cardiac arrest. Neurology 2011;77:623-630.  https://doi.org/10.1212/WNL.0b013e31822a276d
  30. Takei N, Kondo J, Nagaike K, Ohsawa K, Kato K, Kohsaka S. Neuronal survival factor from bovine brain is identical to neuron-specific enolase. J Neurochem 1991;57:1178-1184.  https://doi.org/10.1111/j.1471-4159.1991.tb08277.x
  31. Sung JH, Kim MO, Koh PO. Proteomic identification of proteins differentially expressed by nicotinamide in focal cerebral ischemic injury. Neuroscience 2011;174:171-177.  https://doi.org/10.1016/j.neuroscience.2010.11.021
  32. Gim SA, Koh PO. Ferulic acid prevents the injury-induced decrease of γ-enolase expression in brain tissue and HT22 cells. Lab Anim Res 2014;30:8-13.  https://doi.org/10.5625/lar.2014.30.1.8
  33. Shah MA, Kang JB, Kim MO, Koh PO. Chlorogenic acid alleviates the reduction of Akt and Bad phosphorylation and of phospho-Bad and 14-3-3 binding in an animal model of stroke. J Vet Sci 2022;23:e84. 
  34. Watanabe T, Arai Y, Mitsui Y, Kusaura T, Okawa W, Kajihara Y, Saito I. The blood pressure-lowering effect and safety of chlorogenic acid from green coffee bean extract in essential hypertension. Clin Exp Hypertens 2006;28:439-449.  https://doi.org/10.1080/10641960600798655
  35. Tajik N, Tajik M, Mack I, Enck P. The potential effects of chlorogenic acid, the main phenolic components in coffee, on health: a comprehensive review of the literature. Eur J Nutr 2017;56:2215-2244. https://doi.org/10.1007/s00394-017-1379-1