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Neuroprotective Effect of Visnagin on Kainic Acid-induced Neuronal Cell Death in the Mice Hippocampus

  • Kwon, Min-Soo (Department of Aerospace Medical Research, Aerospace Medical Center, ROKAF (Republic of Korea Air Force)) ;
  • Lee, Jin-Koo (Department of Pharmacology, Institute of Natural Medicine, College of Medicine, Hallym University) ;
  • Park, Soo-Hyun (Department of Pharmacology, Institute of Natural Medicine, College of Medicine, Hallym University) ;
  • Sim, Yun-Beom (Department of Pharmacology, Institute of Natural Medicine, College of Medicine, Hallym University) ;
  • Jung, Jun-Sub (Department of Pharmacology, Institute of Natural Medicine, College of Medicine, Hallym University) ;
  • Won, Moo-Ho (Department of Anatomy and Neurobiology, and Institute of Neurodegeneration and Neuroregeneration, College of Medicine, Hallym University) ;
  • Kim, Seon-Mi (Department of Pharmacology, Institute of Natural Medicine, College of Medicine, Hallym University) ;
  • Suh, Hong-Won (Department of Pharmacology, Institute of Natural Medicine, College of Medicine, Hallym University)
  • Received : 2010.05.11
  • Accepted : 2010.09.10
  • Published : 2010.10.31

Abstract

Visnagin (4-methoxy-7-methyl-5H-furo[3,2-g][1]-benzopyran-5-one), which is an active principle extracted from the fruits of Ammi visnaga, has been used as a treatment for low blood-pressure and blocked blood vessel contraction by inhibition of calcium influx into blood cells. However, the neuroprotective effect of visnagin was not clearly known until now. Thus, we investigated whether visnagin has a neuroprotective effect against kainic acid (KA)-induced neuronal cell death. In the cresyl violet staining, pre-treatment or post-treatment visnagin (100 mg/kg, p.o. or i.p.) showed a neuroprotective effect on KA ($0.1{\mu}g$) toxicity. KA-induced gliosis and proinflammatory marker (IL-$1{\beta}$, TNF-${\alpha}$, IL-6, and COX-2) inductions were also suppressed by visnagin administration. These results suggest that visnagin has a neuroprotective effect in terms of suppressing KA-induced pathogenesis in the brain, and that these neuroprotective effects are associated with its anti-inflammatory effects.

Keywords

References

  1. Sperk G. Kainic acid seizures in the rat. Prog Neurobiol. 1994;42:1-32. https://doi.org/10.1016/0301-0082(94)90019-1
  2. Beal MF. Mechanisms of excitotoxicity in neurologic diseases. Faseb J. 1992;6:3338-3344. https://doi.org/10.1096/fasebj.6.15.1464368
  3. Rothman SM, Olney JW. Glutamate and the pathophysiology of hypoxic--ischemic brain damage. Ann Neurol. 1986;19:105-111. https://doi.org/10.1002/ana.410190202
  4. Jin Y, Lim CM, Kim SW, Park JY, Seo JS, Han PL, Yoon SH, Lee JK. Fluoxetine attenuates kainic acid-induced neuronal cell death in the mouse hippocampus. Brain Research. 2009;1281:108-116. https://doi.org/10.1016/j.brainres.2009.04.053
  5. Penkowa M, Florit S, Giralt M, Quintana A, Molinero A, Carrasco J, Hidalgo J. Metallothionein reduces central nervous system inflammation, neurodegeneration, and cell death following kainic acid-induced epileptic seizures. J Neurosci Res. 2005;79:522-534. https://doi.org/10.1002/jnr.20387
  6. Kreutzberg GW. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 1996;19:312-318. https://doi.org/10.1016/0166-2236(96)10049-7
  7. Ridet JL, Malhotra SK, Privat A, Gage FH. Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci. 1997;20:570-577. https://doi.org/10.1016/S0166-2236(97)01139-9
  8. Kim JB, Yu YM, Kim SW, Lee JK. Anti-inflammatory mechanism is involved in ethyl pyruvate-mediated efficacious neuroprotection in the postischemic brain. Brain Research. 2005;1060:188-192. https://doi.org/10.1016/j.brainres.2005.08.029
  9. Smith E, Pucci LA, Bywater WG. Crystalline Visnagan. Science. 1952;115:520-521. https://doi.org/10.1126/science.115.2993.520
  10. Anrep GV, Barsoum GS, Kenawy MR, Misrahy G. Ammi Visnaga in the treatment of the anginal syndrome. Br Heart J. 1946;8:171-177. https://doi.org/10.1136/hrt.8.4.171
  11. Anrep GV, Barsoum GS, Kenawy MR. The pharmacological actions of the crystalline principles of Ammi Visnaga Linn. J Pharm Pharmacol. 1949;1:164-176. https://doi.org/10.1111/j.2042-7158.1949.tb12395.x
  12. Duarte J, Perez-Vizcaino F, Torres AI, Zarzuelo A, Jimenez J, Tamargo J. Vasodilator effects of visnagin in isolated rat vascular smooth muscle. Eur J Pharmacol. 1995;286:115-122. https://doi.org/10.1016/0014-2999(95)00418-K
  13. Rauwald HW, Brehm O, Odenthal KP. The involvement of a $Ca^{2+}$ channel blocking mode of action in the pharmacology of Ammi visnaga fruits. Planta Medica. 1994;60:101-105. https://doi.org/10.1055/s-2006-959426
  14. Ubeda A, Tejerina T, Tamargo J, Villar A. Effects of khellin on contractile responses and $45Ca^{2+}$ movements in rat isolated aorta. J Pharm Pharmacol. 1991;43:46-48. https://doi.org/10.1111/j.2042-7158.1991.tb05447.x
  15. Duarte J, Torres AI, Zarzuelo A. Cardiovascular effects of visnagin on rats. Planta Medica. 2000;66:35-39. https://doi.org/10.1055/s-2000-11108
  16. Laursen SE, Belknap JK. Intracerebroventricular injections in mice. Some methodological refinements. J Pharmacol Methods. 1986;16:355-357. https://doi.org/10.1016/0160-5402(86)90038-0
  17. Sapolsky RM, Krey LC, McEwen BS. Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging. J Neurosci. 1985;5:1222-1227. https://doi.org/10.1523/JNEUROSCI.05-05-01222.1985
  18. Franklin KBJ, Paxinos G. The mouse brain in stereotaxic coordinates. 3rd ed. San Diego: Academic Press; 1997.
  19. Kwon MS, Seo YJ, Choi SM, Choi HW, Jung JS, Park SH, Suh HW. The differential effects of single or repeated restraint stress on kainic acid-induced neuronal death in the hippocampal CA3 region: the role of glucocorticoid and various signal molecules. J Neurochem. 2007;103:1530-1541. https://doi.org/10.1111/j.1471-4159.2007.04865.x
  20. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987;162:156-159.
  21. Kim SW, Yu YM, Piao CS, Kim JB, Lee JK. Inhibition of delayed induction of p38 mitogen-activated protein kinase attenuates kainic acid-induced neuronal loss in the hippocampus. Brain Research. 2004;1007:188-191. https://doi.org/10.1016/j.brainres.2004.02.009
  22. Weiss JH, Sensi SL, Koh JY. Zn($^{2+}$): a novel ionic mediator of neural injury in brain disease. Trends Pharmacol Sci. 2000;21:395-401. https://doi.org/10.1016/S0165-6147(00)01541-8
  23. McEwen BS. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev. 2007;87:873-904. https://doi.org/10.1152/physrev.00041.2006
  24. White BC, Sullivan JM, DeGracia DJ, O'Neil BJ, Neumar RW, Grossman LI, Rafols JA, Krause GS. Brain ischemia and reperfusion: molecular mechanisms of neuronal injury. J Neurol Sci. 2000;179:1-33. https://doi.org/10.1016/S0022-510X(00)00386-5
  25. Hudson J, Towers GHN. Phytomedicines as antivirals. Drugs Future. 1999;24:295-300. https://doi.org/10.1358/dof.1999.024.03.858620
  26. Cho IH, Kim SW, Kim JB, Kim TK, Lee KW, Han PL, Lee JK. Ethyl pyruvate attenuates kainic acid-induced neuronal cell death in the mouse hippocampus. J Neurosci Res. 2006;84:1505-1511. https://doi.org/10.1002/jnr.21052
  27. Yoo KY, Hwang IK, Kim JD, Kang IJ, Park J, Yi JS, Kim JK, Bae YS, Won MH. Antiinflammatory effect of the ethanol extract of Berberis koreana in a gerbil model of cerebral ischemia/reperfusion. Phytother Res. 2008;22:1527-1532. https://doi.org/10.1002/ptr.2527
  28. Beattie EC, Stellwagen D, Morishita W, Bresnahan JC, Ha BK, Von Zastrow M, Beattie MS, Malenka RC. Control of synaptic strength by glial TNFalpha. Science. 2002;295:2282-2285. https://doi.org/10.1126/science.1067859
  29. Stellwagen D, Beattie EC, Seo JY, Malenka RC. Differential regulation of AMPA receptor and GABA receptor trafficking by tumor necrosis factor-alpha. J Neurosci. 2005;25:3219-3228. https://doi.org/10.1523/JNEUROSCI.4486-04.2005
  30. Viviani B, Bartesaghi S, Gardoni F, Vezzani A, Behrens MM, Bartfai T, Binaglia M, Corsini E, Di Luca M, Galli CL, Marinovich M. Interleukin-1beta enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases. J Neurosci. 2003;23:8692-8700. https://doi.org/10.1523/JNEUROSCI.23-25-08692.2003
  31. Wang S, Cheng Q, Malik S, Yang J. Interleukin-1beta inhibits gamma-aminobutyric acid type A (GABA(A)) receptor current in cultured hippocampal neurons. J Pharmacol Exp Ther. 2000;292:497-504.
  32. McGeer PL, Schulzer M, McGeer EG. Arthritis and antiinflammatory agents as possible protective factors for Alzheimer's disease: a review of 17 epidemiologic studies. Neurology. 1996;47:425-432. https://doi.org/10.1212/WNL.47.2.425
  33. Nogawa S, Zhang F, Ross ME, Iadecola C. Cyclo-oxygenase-2 gene expression in neurons contributes to ischemic brain damage. J Neurosci. 1997;17:2746-2755. https://doi.org/10.1523/JNEUROSCI.17-08-02746.1997
  34. Nakayama M, Uchimura K, Zhu RL, Nagayama T, Rose ME, Stetler RA, Isakson PC, Chen J, Graham SH. Cyclooxygenase-2 inhibition prevents delayed death of CA1 hippocampal neurons following global ischemia. Proc Natl Acad Sci U S A. 1998;95:10954-10959. https://doi.org/10.1073/pnas.95.18.10954
  35. Coyle JT, Puttfarcken P. Oxidative stress, glutamate, and neurodegenerative disorders. Science. 1993;262:689-695. https://doi.org/10.1126/science.7901908
  36. Funk CD. Prostaglandins and leukotrienes: advances in eicosanoid biology. Science. 2001;294:1871-1875. https://doi.org/10.1126/science.294.5548.1871
  37. Aboul-Enein HY, Kladna A, Kruk I, Lichszteld K, Michalska T. Effect of psoralens on Fenton-like reaction generating reactive oxygen species. Biopolymers. 2003;72:59-68. https://doi.org/10.1002/bip.10285
  38. Buttini M, Appel K, Sauter A, Gebicke-Haerter PJ, Boddeke HW. Expression of tumor necrosis factor alpha after focal cerebral ischaemia in the rat. Neuroscience. 1996;71:1-16. https://doi.org/10.1016/0306-4522(95)00414-9
  39. Chao CC, Hu S, Molitor TW, Shaskan EG, Peterson PK. Activated microglia mediate neuronal cell injury via a nitric oxide mechanism. J Immunol. 1992;149:2736-2741.
  40. Barger SW, Basile AS. Activation of microglia by secreted amyloid precursor protein evokes release of glutamate by cystine exchange and attenuates synaptic function. J Neurochem. 2001;76:846-854.
  41. Piani D, Spranger M, Frei K, Schaffner A, Fontana A. Macrophage-induced cytotoxicity of N-methyl-D-aspartate receptor positive neurons involves excitatory amino acids rather than reactive oxygen intermediates and cytokines. Eur J Immunol. 1992;22:2429-2436. https://doi.org/10.1002/eji.1830220936
  42. Liang J, Takeuchi H, Doi Y, Kawanokuchi J, Sonobe Y, Jin S, Yawata I, Li H, Yasuoka S, Mizuno T, Suzumura A. Excitatory amino acid transporter expression by astrocytes is neuroprotective against microglial excitotoxicity. Brain Research. 2008;1210:11-19. https://doi.org/10.1016/j.brainres.2008.03.012

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