SpringerLink
Log in

Extract from Terminalia chebula Seeds Protect Against Experimental Ischemic Neuronal Damage Via Maintaining SODs and BDNF Levels

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

Abstract

The fruit of Terminalia chebula Retz has been used as a traditional medicine in Asia and contains tannic acid, chebulagic acid, chebulinic acid and corilagin. Extract from T. chebula seeds (TCE) has various biological functions. We observed the neuroprotective effects of TCE against ischemic damage in the hippocampal C1 region (CA1) of the gerbil that had received oral administrations of TCE (100 mg/kg) once a day for 7 days before the induction of transient cerebral ischemia. In the TCE-treated ischemia group, neuronal neuclei (a marker for neurons)-positive neurons were distinctively abundant (62% of the sham group) in the CA1 4 days after ischemia-reperfusion (I-R) compared to those (12.2% of the sham group) in the vehicle-treated ischemia group. Four days after I-R TCE treatment markedly decreased the activation of astrocytes and microglia in the ischemic CA1 compared with the vehicle-treated ischemia group. In addition, immunoreactivities of Cu, Zn-superoxide dismutase (SOD1), Mn-superoxide dismutase (SOD2) and brain-derived neurotrophic factor (BDNF) in the CA1 of the TCE-treated ischemia group were much higher than those in the vehicle-ischemia group 4 days after I-R. Protein levels of SOD1, SOD2 and BDNF in the TCE-treated ischemia group were also much higher than those in the vehicle-ischemia group 4 days after I-R. These results indicate that the repeated supplement of TCE protected neurons from ischemic damage induced by transient cerebral ischemia by maintaining SODs and BDNF levels as well as decreasing glial activation.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (France)

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  1. Kirino T (1994) Cerebral ischemia and neuronal death. No To Hattatsu 26:130–135

    PubMed  CAS  Google Scholar 

  2. Lee CH, Yoo KY, Choi JH et al (2011) Cyclin D1 immunoreactivity changes in CA1 pyramidal neurons and dentate granule cells in the gerbil hippocampus after transient forebrain ischemia. Neurol Res 33:93–100

    Article  PubMed  Google Scholar 

  3. Chan PH (2001) Reactive oxygen radicals in signaling and damage in the ischemic brain. J Cereb Blood Flow Metab 21:2–14

    Article  PubMed  CAS  Google Scholar 

  4. Hwang IK, Eum WS, Yoo KY et al (2005) Copper chaperone for Cu, Zn-SOD supplement potentiates the Cu, Zn-SOD function of neuroprotective effects against ischemic neuronal damage in the gerbil hippocampus. Free Radic Biol Med 39:392–402

    Article  PubMed  CAS  Google Scholar 

  5. Beal MF (1999) Mitochondria, NO and neurodegeneration. Biochem Soc Symp 66:43–54

    PubMed  CAS  Google Scholar 

  6. Yoo KY, Li H, Hwang IK et al (2010) Zizyphus attenuates ischemic damage in the gerbil hippocampus via its antioxidant effect. J Med Food 13:557–563

    Article  PubMed  CAS  Google Scholar 

  7. Aldarmaa J, Liu Z, Long J, Mo X, Ma J, Liu J (2010) Anti-convulsant effect and mechanism of Astragalus mongholicus extract in vitro and in vivo: protection against oxidative damage and mitochondrial dysfunction. Neurochem Res 35:33–41

    Article  PubMed  CAS  Google Scholar 

  8. de Oliveria DM, Barreto G, De Andrade DV et al (2009) Cytoprotective effect of Valeriana officinalis extract on an in vitro experimental model of Parkinson disease. Neurochem Res 34:215–220

    Article  PubMed  Google Scholar 

  9. Rajasankar S, Manivasagam T, Surendran S (2009) Ashwagandha leaf extract: a potential agent in treating oxidative damage and physiological abnormalities seen in a mouse model of Parkinson’s disease. Neurosci Lett 454:11–15

    Article  PubMed  CAS  Google Scholar 

  10. Luo Y (2001) Ginkgo biloba neuroprotection: therapeutic implications in Alzheimer’s disease. J Alzheimers Dis 3:401–407

    PubMed  CAS  Google Scholar 

  11. Perry LM, Metzger J (1980) Medicinal plants of East and Southeast Asia: attributed properties and uses. MIT Press, Cambridge, pp 80–81

    Google Scholar 

  12. Gali HU, Perchellet EM, Klish DS, Johnson JM, Perchellet JP (1992) Hydrolyzable tannins: potent inhibitors of hydroperoxide production and tumor promotion in mouse skin treated with 12-O-tetradecanoylphorbol-13-acetate in vivo. Int J Cancer 51:425–432

    Article  PubMed  CAS  Google Scholar 

  13. Kuo ML, Lee KC, Lin JK (1992) Genotoxicities of nitropyrenes and their modulation by apigenin, tannic acid, ellagic acid and indole-3-carbinol in the Salmonella and CHO systems. Mutat Res 270:87–95

    Article  PubMed  CAS  Google Scholar 

  14. Sah NK, Kumar S, Subramanian M, Devasagayam TP (1995) Variation in the modulation of superoxide-induced single-strand breaks in plasmid pBR322 DNA by biological antioxidants. Biochem Mol Biol Int 35:291–296

    PubMed  CAS  Google Scholar 

  15. Reddy DB, Reddanna P (2009) Chebulagic acid (CA) attenuates LPS-induced inflammation by suppressing NF-kappaB and MAPK activation in RAW 264.7 macrophages. Biochem Biophys Res Commun 381:112–117

    Article  PubMed  CAS  Google Scholar 

  16. Reddy DB, Reddy TC, Jyotsna G et al (2009) Chebulagic acid, a COX-LOX dual inhibitor isolated from the fruits of Terminalia chebula Retz., induces apoptosis in COLO-205 cell line. J Ethnopharmacol 124:506–512

    Article  PubMed  CAS  Google Scholar 

  17. Silva O, Ferreira E, Vaz Pato M, Caniça M, Gomes ET (2002) In vitro anti-Neisseria gonorrhoeae activity of Terminalia macroptera leaves. FEMS Microbiol Lett 211:203–206

    Article  PubMed  CAS  Google Scholar 

  18. Saleem A, Husheem M, Härkönen P, Pihlaja K (2002) Inhibition of cancer cell growth by crude extract and the phenolics of Terminalia chebula retz. fruit. J Ethnopharmacol 81:327–336

    Article  PubMed  CAS  Google Scholar 

  19. Kinoshita S, Inoue Y, Nakama S, Ichiba T, Aniya Y (2007) Antioxidant and hepatoprotective actions of medicinal herb, Terminalia catappa L. from Okinawa Island and its tannin corilagin. Phytomedicine 14:755–762

    Article  PubMed  CAS  Google Scholar 

  20. Cheng JT, Lin TC, Hsu FL (1995) Antihypertensive effect of corilagin in the rat. Can J Physiol Pharmacol 73:1425–1429

    Article  PubMed  CAS  Google Scholar 

  21. Duan W, Yu Y, Zhang L (2005) Antiatherogenic effects of phyllanthus emblica associated with corilagin and its analogue. Yakugaku Zasshi 125:587–591

    Article  PubMed  CAS  Google Scholar 

  22. Zhao L, Zhang SL, Tao JY et al (2008) Preliminary exploration on anti-inflammatory mechanism of Corilagin (beta-1-O-galloyl-3, 6-(R)-hexahydroxydiphenoyl-d-glucose) in vitro. Int Immunopharmacol 8:1059–1064

    Article  PubMed  CAS  Google Scholar 

  23. Manyam BV (1999) Dementia in ayurveda. J Altern Complement Med 5:81–88

    Article  PubMed  CAS  Google Scholar 

  24. Misra R (1998) Modern drug development from traditional medicinal plants using radioligand receptor-binding assays. Med Res Rev 18:383–402

    Article  PubMed  CAS  Google Scholar 

  25. Mahesh R, Bhuvana S, Begum VM (2009) Effect of Terminalia chebula aqueous extract on oxidative stress and antioxidant status in the liver and kidney of young and aged rats. Cell Biochem Funct 27:358–363

    Article  PubMed  CAS  Google Scholar 

  26. Suchalatha S, Devi CS (2005) Protective effect of Terminalia chebula against lysosomal enzyme alterations in isoproterenol-induced cardiac damage in rats. Exp Clin Cardiol 10:91–95

    PubMed  Google Scholar 

  27. Lee CH, Yoo KY, Choi JH et al (2010) Melatonin’s protective action against ischemic neuronal damage is associated with up-regulation of the MT2 melatonin receptor. J Neurosci Res 88:2630–2640

    Article  PubMed  CAS  Google Scholar 

  28. Nazam Ansari M, Bhandari U, Islam F, Tripathi CD (2008) Evaluation of antioxidant and neuroprotective effect of ethanolic extract of Embelia ribes Burm in focal cerebral ischemia/reperfusion-induced oxidative stress in rats. Fundam Clin Pharmacol 22:305–314

    Article  PubMed  CAS  Google Scholar 

  29. Ahn HC, Yoo KY, Hwang IK et al (2009) Ischemia-related changes in naive and mutant forms of ubiquitin and neuroprotective effects of ubiquitin in the hippocampus following experimental transient ischemic damage. Exp Neurol 220:120–132

    Article  PubMed  CAS  Google Scholar 

  30. Kirino T (1982) Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res 239:57–69

    Article  PubMed  CAS  Google Scholar 

  31. Dong Y, Benveniste EN (2001) Immune function of astrocytes. Glia 36:180–190

    Article  PubMed  CAS  Google Scholar 

  32. Hwang IK, Yoo KY, Kim DW et al (2006) Ionized calcium-binding adapter molecule 1 immunoreactive cells change in the gerbil hippocampal CA1 region after ischemia/reperfusion. Neurochem Res 31:957–965

    Article  PubMed  CAS  Google Scholar 

  33. Rogers J, Strohmeyer R, Kovelowski CJ, Li R (2002) Microglia and inflammatory mechanisms in the clearance of amyloid beta peptide. Glia 40:260–269

    Article  PubMed  Google Scholar 

  34. Naik GH, Priyadarsini KI, Naik DB, Gangabhagirathi R, Mohan H (2004) Studies on the aqueous extract of Terminalia chebula as a potent antioxidant and a probable radioprotector. Phytomedicine 11:530–538

    Article  PubMed  CAS  Google Scholar 

  35. Cheng HY, Lin TC, Yu KH, Yang CM, Lin CC (2003) Antioxidant and free radical scavenging activities of Terminalia chebula. Biol Pharm Bull 26:1331–1335

    Article  PubMed  CAS  Google Scholar 

  36. Fujimura M, Morita-Fujimura Y, Kawase M et al (1999) Manganese superoxide dismutase mediates the early release of mitochondrial cytochrome C and subsequent DNA fragmentation after permanent focal cerebral ischemia in mice. J Neurosci 19:3414–3422

    PubMed  CAS  Google Scholar 

  37. Greenlund LJ, Deckwerth TL, Johnson EM Jr (1995) Superoxide dismutase delays neuronal apoptosis: a role for reactive oxygen species in programmed neuronal death. Neuron 14:303–315

    Article  PubMed  CAS  Google Scholar 

  38. Sugawara T, Noshita N, Lewen A et al (2002) Overexpression of copper/zinc superoxide dismutase in transgenic rats protects vulnerable neurons against ischemic damage by blocking the mitochondrial pathway of caspase activation. J Neurosci 22:209–217

    PubMed  CAS  Google Scholar 

  39. Ferrer I, Ballabriga J, Marti E, Perez E, Alberch J, Arenas E (1998) BDNF up-regulates TrkB protein and prevents the death of CA1 neurons following transient forebrain ischemia. Brain Pathol 8:253–261

    Article  PubMed  CAS  Google Scholar 

  40. Larsson E, Nanobashvili A, Kokaia Z, Lindvall O (1999) Evidence for neuroprotective effects of endogenous brain-derived neurotrophic factor after global forebrain ischemia in rats. J Cereb Blood Flow Metab 19:1220–1228

    Article  PubMed  CAS  Google Scholar 

  41. Shirakura M, Inoue M, Fujikawa S et al (2004) Postischemic administration of Sendai virus vector carrying neurotrophic factor genes prevents delayed neuronal death in gerbils. Gene Ther 11:784–790

    Article  PubMed  CAS  Google Scholar 

  42. Cheng B, Mattson MP (1994) NT-3 and BDNF protect CNS neurons against metabolic/excitotoxic insults. Brain Res 640:56–67

    Article  PubMed  CAS  Google Scholar 

  43. Gardiner J, Barton D, Overall R, Marc J (2009) Neurotrophic support and oxidative stress: converging effects in the normal and diseased nervous system. Neuroscientist 15:47–61

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Mr. Sung Auk Lee for his technical help in this study. This research was supported by a grant (2010K000823) from Brain Research Center of the 21st Century Frontier Research Program funded by the Ministry of Education, Science and Technology, the Republic of Korea, and by the Regional Core Research Program funded by the Korea Ministry of Education, Science and Technology (Medical & Bio-material Research Center).

Author information

Authors and Affiliations

  1. Department of Neurobiology, School of Medicine, Kangwon National University, Chuncheon, 200-701, South Korea

    Joon Ha Park & Moo-Ho Won

  2. C&J Biotech Co. Ltd., Bio21 Center Moonsan, **ju, 660-844, Republic of Korea

    Han Seung Joo

  3. Department of Oral Anatomy, College of Dentistry, Gangneung-Wonju National University, Gangneung, 210-702, South Korea

    Ki-Yeon Yoo

  4. Department of Physiology, College of Medicine, Hallym University, Chuncheon, 200-702, South Korea

    Bich Na Shin & In Hye Kim

  5. Laboratory of Veterinary Pharmacology, College of Veterinary Medicine, Seoul National University, Seoul, 151-742, South Korea

    Choong Hyun Lee

  6. Department of Anatomy, College of Veterinary Medicine, Kangwon National University, Chuncheon, 200-701, South Korea

    Jung Hoon Choi

  7. Lee Gil Ya Cancer and Diabetes Institute, Department of Anatomy and Cell Biology, Gachon University of Medicine and Science, Incheon, 406-840, South Korea

    Kyunghee Byun & Bonghee Lee

  8. Department of Food Science and Nutrition, Hallym University, Chuncheon, 200-702, South Korea

    Soon Sung Lim

  9. Bioherb Research Institute, Kangwon National University, Chuncheon, 200-701, South Korea

    Myong Jo kim

Authors
  1. Joon Ha Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Han Seung Joo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ki-Yeon Yoo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bich Na Shin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. In Hye Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Choong Hyun Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jung Hoon Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kyunghee Byun
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Bonghee Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Soon Sung Lim
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Myong Jo kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Moo-Ho Won
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Ki-Yeon Yoo or Moo-Ho Won.

Additional information

Joon Ha Park and Han Seung Joo contributed equally to this article.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Park, J.H., Joo, H.S., Yoo, KY. et al. Extract from Terminalia chebula Seeds Protect Against Experimental Ischemic Neuronal Damage Via Maintaining SODs and BDNF Levels. Neurochem Res 36, 2043–2050 (2011). https://doi.org/10.1007/s11064-011-0528-9

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-011-0528-9

Keywords

Search

Navigation