Neuroprotective effect of forsythiaside against transient cerebral global ischemia in gerbil

European Journal of Pharmacology

Volumn 660, Issue 2-3, 2011, Pages 326-333

  Kim, Jong Min ^a   Kim, Sunho ^a,f   Kim, Dong Hyun ^a   Lee, Choong Ho ^b   Park, Se Jin ^a   Jung, Ji Wook ^c   Ko, Kwang Ho ^d   Cheong, Jae Hoon ^e   Lee, Seung Ho ^b   Ryu, Jong Hoon ^a  

^a Kyung Hee University   (South Korea)

^b Yeungnam University   (South Korea)

^c Daegu Haany University   (South Korea)

^d Seoul National University   (South Korea)

^e Sahmyook University   (South Korea)

^f National Institute of Food and Drug Safety Evaluation   (South Korea)

Author keywords

Astrocyte; Forsythiaside; Global ischemia; Microglia; Y maze task

Indexed keywords

CALCIUM BINDING PROTEIN; DIZOCILPINE; FORSYTHIASIDE; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 1BETA; IONIZED CALCIUM BINDING ADAPTOR MOLECULE 1; PLANT GLYCOSIDE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CAROTID ARTERY OBSTRUCTION; COGNITIVE DEFECT; CONTROLLED STUDY; DRUG EFFECT; GERBIL; HIPPOCAMPAL CA1 REGION; MAZE TEST; MICROGLIA; NERVE CELL DEGENERATION; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSIENT ISCHEMIC ATTACK;

ANIMALS; ASTROCYTES; CAROTID STENOSIS; CELL DEATH; GENE EXPRESSION REGULATION; GERBILLINAE; GLYCOSIDES; HIPPOCAMPUS; INTERLEUKIN-1BETA; ISCHEMIC ATTACK, TRANSIENT; MAZE LEARNING; MEMORY DISORDERS; MICROGLIA; NEURONS; NEUROPROTECTIVE AGENTS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 79956069931     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2011.03.051     Document Type: Article

References (68)

1. Antonawich, F.J., Fiore, S.M., Welicky, L.M., 2004. Regulation of ischemic cell death by the lipoic acid-palladium complex, Poly MVA, in gerbils. Exp. Neurol. 189, 10-15.
2. Benquet, P., Gee, C.E., Gerber, U., 2008. Transient brain ischemia: NMDA receptor modulation and delayed neuronal death. Med. Sci. Paris 24, 185-190.
3. Boje, K.M., Arora, P.K., 1992. Microglial-produced nitric oxide and reactive nitrogen oxides mediate neuronal cell death. Brain Res. 587, 250-256.
4. Boutin, H., LeFeuvre, R.A., Horai, R., Asano, M., Iwakura, Y., Rothwell, N.J., 2001. Role of IL-1α and IL-1β in ischemic brain damage. J. Neurosci. 21, 5528-5534. (Pubitemid 32692151)
5. Candelario-Jalil, E., Alvarez, D., Merino, N., Leon, O.S., 2003. Delayed treatment with nimesulide reduces measures of oxidative stress following global ischemic brain injury in gerbils. Neurosci. Res. 47, 245-253.
6. Castillo, J., Davalos, A., Noya, M., 1997. Progression of ischaemic stroke and excitotoxic aminoacids. Lancet 349, 79-83. (Pubitemid 27023423)
7. Cheng, L.F., Chu, Y., Hu, C.X., Guo, J.H., Wan, M.X., Zhou, S.P., Guo, Z.X., Yan, X.J., 2010. Investigation of pharmacokinetics and plasma protein binding of forsythiaside A in rats. Chin. J. New Drugs 19, 2138-2141.
8. Choi, D.W., Rothman, S.M., 1990. The role of glutamate neurotoxicity in hypoxic-ischemic neuronal death. Annu. Rev. Neurosci. 13, 171-182.
9. Davalos, A., Castillo, J., Serena, J., Noya, M., 1997. Duration of glutamate release after acute ischemic stroke. Stroke 28, 708-710. (Pubitemid 27161450)
10. Denes, A., Vidyasagar, R., Feng, J., Narvainen, J., McColl, B.W., Kauppinen, R.A., Allan, S.M., 2007. Proliferating resident microglia after focal cerebral ischaemia in mice. J. Cereb. Blood Flow Metab. 27, 1941-1953.
11. Di Virgilio, F., 2004.Newpathways for reactive oxygen species generation in inflammation and potential novel pharmacological targets. Curr. Pharm. Des. 10, 1647-1652.
12. Douhou, A., Debeir, T., Michel, P.P., Stankovski, L., Oueghlani-Bouslama, L., Verney, C., Raisman-Vozari, R., 2003. Differential activation of astrocytes and microglia during post-natal development of dopaminergic neuronal death in the weaver mouse. Dev. Brain Res. 145, 9-17.
13. Eng, L.F., Ghirnikar, R.S., Lee, Y.L., 2000. Glial fibrillary acidic protein: GFAP-thirty-one years (1969-2000). Neurochem. Res. 25, 1439-1451.
14. Faust, K., Gehrke, S., Yang, Y., Yang, L., Beal, M.F., Lu, B., 2009. Neuroprotective effects of compounds with antioxidant and anti-inflammatory properties in a Drosophila model of Parkinson's disease. BMC Neurosci. 10, 109.
15. Frantseva, M.V., Carlen, P.L., Perez Velazquez, J.L., 2001. Dynamics of intracellular calcium and free radical production during ischemia in pyramidal neurons. Free Radic. Biol. Med. 31, 1216-1227.
16. Gehrmann, J., Bonnekoh, P., Miyazawa, T., Oschlies, U., Dux, E., Hossmann, K.A., Kreutzberg, G.W., 1992. The microglial reaction in the rat hippocampus following global ischemia: immuno-electron microscopy. Acta Neuropathol. 84, 588-595.
17. Green, E.J., Pazos, A.J., Dietrich, W.D., McCabe, P.M., Schneiderman, N., Lin, B., Busto, R., Globus, M.Y., Ginsberg, M.D., 1995. Combined postischemic hypothermia and delayed MK-801 treatment attenuates neurobehavioral deficits associated with transient global ischemia in rats. Brain Res. 702, 145-152.
18. Guo, H., Liu, A.H., Li, L., Guo, D.A., 2007. Simultaneous determination of 12 major constituents in Forsythia suspensa by high performance liquid chromatography - DAD method. J. Pharm. Biomed. Anal. 43, 1000-1006.
19. Hagan, J.J., Beaughard, M., 1990. The effects of forebrain ischaemia on spatial learning. Behav. Brain Res. 41, 151-160.
20. Hallenbeck, J.M., 2002. The many faces of tumor necrosis factor in stroke. Nat. Med. 8, 1363-1368.
21. Institoris, A., Farkas, E., Berczi, S., Sule, Z., Bari, F., 2007. Effects of cyclooxygenase (COX) inhibition on memory impairment and hippocampal damage in the early period of cerebral hypoperfusion in rats. Eur. J. Pharmacol. 574, 29-38.
22. Ito, D., Tanaka, K., Suzuki, S., Dembo, T., Fukuuchi, Y., 2001. Enhanced expression of Iba1, ionized calcium-binding adapter molecule 1, after transient focal cerebral ischemia in rat brain. Stroke 32, 1208-1215. (Pubitemid 32825812)
23. Kato, H., Kogure, K., Araki, T., Itoyama, Y., 1994. Astroglial and microglial reactions in the gerbil hippocampus with induced ischemic tolerance. Brain Res. 664, 69-76. (Pubitemid 24347597)
24. Kato, H., Takahashi, A., Itoyama, Y., 2003. Cell cycle protein expression in proliferating microglia and astrocytes following transient global cerebral ischemia in the rat. Brain Res. Bull. 60, 215-221.
25. Kim, J.B., Yu, Y.M., Kim, S.W., Lee, J.K., 2005. Anti-inflammatory mechanism is involved in ethyl pyruvate-mediated efficacious neuroprotection in the postischemic brain. Brain Res. 1060, 188-192.
26. Kim, D.H., Jeon, S.J., Son, K.H., Jung, J.W., Lee, S., Yoon, B.H., Choi, J.W., Cheong, J.H., Ko, K.H., Ryu, J.H., 2006. Effect of the flavonoid, oroxylin A, on transient cerebral hypoperfusion-induced memory impairment in mice. Pharmacol. Biochem. Behav. 85, 658-668.
27. Kim, S.H., Kim, D.H., Choi, J.J., Lee, J.G., Lee, C.H., Park, S.J., Jung, W.Y., Park, D.H., Ko, K.H., Lee, S.H., Ryu, J.H., 2009. Forsythiaside, a constituent of the fruits of Forsythia suspensa, ameliorates scopolamine-induced memory impairment in mice. Biomol. Ther. 17, 249-255.
28. Kimura, Y., Okuda, H., Nishibe, S., Arichi, S., 1987. Effects of caffeoylglycosides on arachidonate metabolism in leukocytes. Planta Med. 53, 148-153. (Pubitemid 17057064)
29. Kirino, T., 2000. Delayed neuronal death. Neuropathology 20 (Suppl), S95-S97.
30. Lavine, S.D., Hofman, F.M., Zlokovic, B.V., 1998. Circulating antibody against tumor necrosis factor-α protects rat brain from reperfusion injury. J. Cereb. Blood Flow Metab. 18, 52-58.
31. Ling, E.A., Ng, Y.K., Wu, C.H., Kaur, C., 2001. Microglia: its development and role as a neuropathology sensor. Prog. Brain Res. 132, 61-79.
32. Mal, H., Dehoux, M., Sleiman, C., Boczkowski, J., Leseche, G., Pariente, R., Fournier, M., 1998. Early release of proinflammatory cytokines after lung transplantation. Chest 113, 645-651. (Pubitemid 28130936)
33. Murakami, Y., Zhao, Q., Harada, K., Tohda, M., Watanabe, H., Matsumoto, K., 2005. Choto-san, a Kampo formula, improves chronic cerebral hypoperfusion-induced spatial learning deficit via stimulation of muscarinic M1 receptor. Pharmacol. Biochem. Behav. 81, 616-625.
34. Nakamura, T., Minamisawa, H., Katayama, Y., Ueda, M., Terashi, A., Nakamura, K., Kudo, Y., 1999. Increased intracellular Ca2+ concentration in the hippocampal CA1 area during global ischemia and reperfusion in the rat: a possible cause of delayed neuronal death. Neuroscience 88, 57-67. (Pubitemid 28440391)
35. Nedergaard, M., 1988. Mechanisms of brain damage in focal cerebral ischemia. Acta Neurol. Scand. 77, 81-101.
36. Neigh, G.N., Glasper, E.R., Kofler, J., Traystman, R.J., Mervis, R.F., Bachstetter, A., DeVries, A.C., 2004. Cardiac arrest with cardiopulmonary resuscitation reduces dendritic spine density in CA1 pyramidal cells and selectively alters acquisition of spatial memory. Eur. J. Neurosci. 20, 1865-1872.
37. Nitatori, T., Sato, N., Waguri, S., Karasawa, Y., Araki, H., Shibanai, K., Kominami, E., Uchiyama, Y., 1995. Delayed neuronal death in the CA1 pyramidal cell layer of the gerbil hippocampus following transient ischemia is apoptosis. J. Neurosci. 15, 1001-1011.
38. Ouyang, Y.B., Voloboueva, L.A., Xu, L.J., Giffard, R.G., 2007. Selective dysfunction of hippocampal CA1 astrocytes contributes to delayed neuronal damage after transient forebrain ischemia. J. Neurosci. 27, 4253-4260. (Pubitemid 46640722)
39. Park, C.K., Nehls, D.G., Graham, D.I., Teasdale, G.M., McCulloch, J., 1988. The glutamate antagonist MK-801 reduces focal ischemic brain damage in the rat. Ann. Neurol. 24, 543-551.
40. Petito, C.K., Halaby, I.A., 1993. Relationship between ischemia and ischemic neuronal necrosis to astrocyte expressionof glial fibrillary acidic protein. Int. J.Dev.Neurosci. 11, 239-247.
41. Petito, C.K., Morgello, S., Felix, J.C., Lesser, M.L., 1990. The two patterns of reactive astrocytosis in postischemic rat brain. J. Cereb. Blood Flow Metab. 10, 850-859.
42. Qu, H., Zhang, Y., Wang, Y., Li, B., Sun, W., 2008. Antioxidant and antibacterial activity of two compounds (forsythiaside and forsythin) isolated from Forsythia suspensa. J. Pharm. Pharmacol. 60, 261-266.
43. Ransohoff, R.M., Perry, V.H., 2009. Microglial physiology: unique stimuli, specialized responses. Annu. Rev. Immunol. 27, 119-145.
44. Reuter, S., Gupta, S.C., Chaturvedi, M.M., Aggarwal, B.B., 2010. Oxidative stress, inflammation, and cancer: how are they linked? Free Radic. Biol. Med. 49, 1603-1616.
45. Sarter, M., Bodewitz, G., Stephens, D.N., 1988. Attenuation of scopolamine-induced impairment of spontaneous alteration behaviour by antagonist but not inverse agonist and agonist β-carbolines. Psychopharmacol. Berl. 94, 491-495.
46. Sawada, M., Suzumura, A., Marunouchi, T., 1992. TNF α induces IL-6 production by astrocytes but not by microglia. Brain Res. 583, 296-299.
47. Schielke, G.P., Yang, G.Y., Shivers, B.D., Betz, A.L., 1998. Reduced ischemic brain injury in interleukin-1β converting enzyme-deficient mice. J. Cereb. Blood Flow Metab. 18, 180-185.
48. Schinella, G.R., Tournier, H.A., Prieto, J.M., Mordujovich de Buschiazzo, P., Rios, J.L., 2002. Antioxidant activity of anti-inflammatory plant extracts. Life Sci. 70, 1023-1033. (Pubitemid 34085094)
49. Seabrook, T.J., Jiang, L., Maier, M., Lemere, C.A., 2006. Minocycline affects microglia activation, Abeta deposition, and behavior in APP-tg mice. Glia 53, 776-782.
50. Sheng, H., Laskowitz, D.T., Mackensen, G.B., Kudo, M., Pearlstein, R.D., Warner, D.S., 1999. Apolipoprotein E deficiency worsens outcome from global cerebral ischemia in the mouse. Stroke 30, 1118-1124. (Pubitemid 29211636)
51. Shin, B.Y., Kim, D.H., Hyun, S.K., Jung, H.A., Kim, J.M., Park, S.J., Kim, S.Y., Cheong, J.H., Choi, J.S., Ryu, J.H., 2010. Alaternin attenuates delayed neuronal cell death induced by transient cerebral hypoperfusion in mice. Food Chem. Toxicol. 48, 1528-1536.
52. Shuaib, A., Mahmood, R.H., Wishart, T., Kanthan, R., Murabit, M.A., Ijaz, S., Miyashita, H., Howlett, W., 1995. Neuroprotective effects of lamotrigine in global ischemia in gerbils. A histological, in vivo microdialysis and behavioral study. Brain Res. 702, 199-206.
53. Sims, N.R., Anderson, M.F., 2002. Mitochondrial contributions to tissue damage in stroke. Neurochem. Int. 40, 511-526.
54. Sironi, L., Mitro, N., Cimino, M., Gelosa, P., Guerrini, U., Tremoli, E., Saez, E., 2008. Treatment with LXR agonists after focal cerebral ischemia prevents brain damage. FEBS Lett. 582, 3396-3400.
55. Streit, W.J., Graeber, M.B., Kreutzberg, G.W., 1988. Functional plasticity of microglia: a review. Glia 1, 301-307.
56. Sugawara, T., Lewen, A., Noshita, N., Gasche, Y., Chan, P.H., 2002. Effects of global ischemia duration on neuronal, astroglial, oligodendroglial, and microglial reactions in the vulnerable hippocampal CA1 subregion in rats. J. Neurotrauma 19, 85-98. (Pubitemid 34126348)
57. Tang, X.N., Wang, Q., Koike, M.A., Cheng, D., Goris, M.L., Blankenberg, F.G., Yenari, M.A., 2007. Monitoring the protective effects of minocycline treatment with radiolabeled annexin V in an experimental model of focal cerebral ischemia. J. Nucl. Med. 48, 1822-1828.
58. Tichauer, J., Saud, K., von Bernhardi, R., 2007. Modulation by astrocytes of microglial cell-mediated neuroinflammation: effect on the activation of microglial signaling pathways. Neuroimmunomodulation 14, 168-174. (Pubitemid 350249113)
59. Tikka, T., Fiebich, B.L., Goldsteins, G., Keinanen, R., Koistinaho, J., 2001. Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J. Neurosci. 21, 2580-2588. (Pubitemid 32298200)
60. Wang, C.X., Shuaib, A., 2002. Involvement of inflammatory cytokines in central nervous system injury. Prog. Neurobiol. 67, 161-172.
61. Wang, Q., Tang, X.N., Yenari, M.A., 2007. The inflammatory response in stroke. J. Neuroimmunol. 184, 53-68. (Pubitemid 46365991)
62. White, B.C., Daya, A., DeGracia, D.J., O'Neil, B.J., Skjaerlund, J.M., Trumble, S., Krause, G.S., Rafols, J.A., 1993. Fluorescent histochemical localization of lipid peroxidation during brain reperfusion following cardiac arrest. Acta Neuropathol. 86, 1-9. (Pubitemid 23249066)
63. Won, M.H., Kang, T., Park, S., Jeon, G., Kim, Y., Seo, J.H., Choi, E., Chung, M., Cho, S.S., 2001. The alterations of N-Methyl-D-aspartate receptor expressions and oxidative DNA damage in the CA1 area at the early time after ischemia-reperfusion insult. Neurosci. Lett. 301, 139-142.
64. Wu, Y.P., Ling, E.A., 1998. Induction of microglial and astrocytic response in the adult rat lumbar spinal cord following middle cerebral artery occlusion. Exp. Brain Res. 118, 235-242.
65. Yamanaka, H., Hagiwara, K., Kirisawa, R., Iwai, H., 2003. Transient detection of proinflammatory cytokines in sera of colostrum-fed newborn calves. J. Vet. Med. Sci. 65, 813-816.
66. Yang, G.Y., Zhao, Y.J., Davidson, B.L., Betz, A.L., 1997. Overexpression of interleukin-1 receptor antagonist in themouse brain reduces ischemic brain injury. Brain Res. 751, 181-188. (Pubitemid 27132547)
67. Yrjanheikki, J., Keinanen, R., Pellikka, M., Hokfelt, T., Koistinaho, J., 1998. Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc. Natl. Acad. Sci. U S A 95, 15769-15774.
68. Zielasek, J., Hartung, H.P., 1996. Molecular mechanisms of microglial activation. Adv. Neuroimmunol. 6 191-122.