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Rehmannia glutinosa Ameliorates Scopolamine-Induced Learning and Memory Impairment in Rats

  • Lee, Bom-Bi (Acupuncture and Meridian Science Research Center, College of Oriental Medicine, Kyung Hee University) ;
  • Shim, In-Sop (Acupuncture and Meridian Science Research Center, College of Oriental Medicine, Kyung Hee University) ;
  • Lee, Hye-Jung (Acupuncture and Meridian Science Research Center, College of Oriental Medicine, Kyung Hee University) ;
  • Hahm, Dae-Hyun (Acupuncture and Meridian Science Research Center, College of Oriental Medicine, Kyung Hee University)
  • Received : 2011.04.11
  • Accepted : 2011.05.10
  • Published : 2011.08.28

Abstract

Many studies have shown that the steamed root of Rehmannia glutinosa (SRG), which is widely used in the treatment of various neurodegenerative diseases in the context of Korean traditional medicine, is effective for improving cognitive and memory impairments. The purpose of this study was to examine whether SRG extracts improved memory defects caused by administering scopolamine (SCO) into the brains of rats. The effects of SRG on the acetylcholinergic system and proinflammatory cytokines in the hippocampus were also investigated. Male rats were administered daily doses of SRG (50, 100, and 200 mg/kg, i.p.) for 14 days, 1 h before scopolamine injection (2 mg/kg, i.p.). After inducing cognitive impairment via scopolamine administration, we conducted a passive avoidance test (PAT) and the Morris water maze (MWM) test as behavioral assessments. Changes in cholinergic system reactivity were also examined by measuring the immunoreactive neurons of choline acetyltransferase (ChAT) and the reactivity of acetylcholinesterase (AchE) in the hippocampus. Daily administration of SRG improved memory impairment according to the PAT, and reduced the escape latency for finding the platform in the MWM. The administration of SRG consistently significantly alleviated memory-associated decreases in cholinergic immunoreactivity and decreased interleukin-$1{\beta}$ (IL-$1{\beta}$) and tumor necrosis factor-${\alpha}$ (TNF-${\alpha}$) mRNA expression in the hippocampus. The results demonstrated that SRG had a significant neuroprotective effect against the neuronal impairment and memory dysfunction caused by scopolamine in rats. These results suggest that SRG may be useful for improving cognitive functioning by stimulating cholinergic enzyme activities and alleviating inflammatory responses.

Keywords

References

  1. Blennow, K., D. M. J. Leon, and H. Zetterberg. 2006. Alzheimer's disease [Review]. Lancet 368: 387-403. https://doi.org/10.1016/S0140-6736(06)69113-7
  2. Blokand, A., E. Geraerts, and A. Been. 2004. A detailed analysis of rat's spatial memory in a probe trial of a Morris task. Behav. Brain Res. 154: 71-75. https://doi.org/10.1016/j.bbr.2004.01.022
  3. Counts, S. E., B. He, S. Che, S. D. Ginsberg, and E. J. Mufson. 2008. Galanin hyperimmervation upregulates choline acetyltransferase expression in cholinergic basal forebrain neurons in Alzheimer's disease. Neurodegener. Dis. 5: 228-231. https://doi.org/10.1159/000113710
  4. Dashniani, M. G., G. V. Beseliia, G. A. Maglakelidze, M. A. Burdzhanadze, and N. T. Chkhikwishvili. 2009. Effects of the selective lesions of cholinergic septohippocampal neurons on different forms of memory and learning process. Georgian Med. News 166: 81-85.
  5. Drever, B. D., W. G. Anderson, H. Johnson, M. O'Callaghan, S. Seo, D. Y. Choi, G. Riedel, and B. Platt. 2007. Memantine acts as a cholinergic stimulant in the mouse hippocampus. J. Alzheimers Dis. 12: 319-333. https://doi.org/10.3233/JAD-2007-12405
  6. Dickson, D. W., S. C. Lee, L. A. Mattiace, S. H. Yen, and C. Brosnan. 1993. Microglia and cytokines in neurological disease, with special reference to AIDS and Alzheimer's disease. Glia 7: 75-83. https://doi.org/10.1002/glia.440070113
  7. Ebert, U. and W. Kirch. 1998. Scopolamine model of dementia: Electroencephalogram findings and cognitive performance. Eur. J. Clin. Invest. 28: 944-949. https://doi.org/10.1046/j.1365-2362.1998.00393.x
  8. Eikelenboom, P., S. S. Zhan, W. A. van Gool, and D. Allsop. 1994. Inflammatory mechanisms in Alzheimer's disease. Trends Pharmacol. Sci. 15: 447-450. https://doi.org/10.1016/0165-6147(94)90057-4
  9. Elvander, E., P. A. Schött, J. Sandin, B. Bjelke, J. Kehr, T. Yoshitake, and S. O. Ogren. 2004. Intraseptal muscarinic ligands and galanin: Influence on hippocampal acetylcholine and cognition. Neuroscience 126: 541-557. https://doi.org/10.1016/j.neuroscience.2004.03.058
  10. Giacobini, E. 2002. Long term stabilizing effect of cholinesterase inhibitors in the therapy of Alzheimer's disease. J. Neural Transm. Suppl. 62: 181-187.
  11. Griffin, W. S., J. G. Sheng, G. W. Roberts, and R. E. Mrak. 1995. Interleukin-1 expression in different plaque types in Alzheimer's disease: Significance in plaque evolution. J. Neuropathol. Exp. Neurol. 54: 276-281. https://doi.org/10.1097/00005072-199503000-00014
  12. Hasselmo, M. E. 2006. The role of acetylcholine in learning and memory. Curr. Opin. Neurobiol. 16: 710-715. https://doi.org/10.1016/j.conb.2006.09.002
  13. Heinrich, M. and H. I. Teoh. 2004. Galanthamine from snowdropthe development of a modern drug against Alzheimer's disease from local Caucasian knowledge. J. Ethnopharmacol. 92: 147-162. https://doi.org/10.1016/j.jep.2004.02.012
  14. Jackson, J. J. and M. R. Soliman. 1996. Effects of tacrine (THA) on spatial reference memory and cholinergic enzymes in specific rat brain regions. Life Sci. 58: 47-54.
  15. Jonasson, Z. 2005. Meta-analysis of sex differences in rodent models of learning and memory: A review of behavioral and biological data [Review]. Neurosci. Biobehav Rev. 28: 811-825. https://doi.org/10.1016/j.neubiorev.2004.10.006
  16. Kang, D. G., E. J. Sohn, M. K. Moon, Y. M. Lee, and H. S. Lee. 2005. Rehmannia glutinosa ameliorates renal function in the ischemia/reperfusion-induced acute renal failure rats. Biol. Pharm. Bull. 28: 1662-1667. https://doi.org/10.1248/bpb.28.1662
  17. Kim, H. M., C. S. An, K. Y. Jung, Y. K. Choo, J. K. Park, and S. Y. Nam. 1999. Rehmannia glutinosa inhibits tumor necrosis factor-alpha and interleukin-1 secretion from mouse astrocyte. Pharmacol. Res. 40: 171-176. https://doi.org/10.1006/phrs.1999.0504
  18. Lee, B., J. Park, S. Kwon, M. W. Park, S. M. Oh, M. J. Yeom, I. Shim, H. J. Lee, and D. H. Hahm. 2010. Effect of wild ginseng on scopolamine-induced acetylcholine depletion in the rat hippocampus. J. Pharm. Pharmacol. 62: 263-271. https://doi.org/10.1211/jpp.62.02.0015
  19. Ling, F. A., D. Z. Hui, and S. M. Ji. 2007. Protective effect of recombinant human somatotropin on amyloid beta-peptide induced learning and memory deficits in mice. Growth Horm. IGF Res. 17: 336-341.
  20. Liu, Y., F. Liu, Y. Zhao, W. H. Wu, and X. S. Wen. 2007. Compounds from Rehmannia glutinosa and their changes during the postharvest processing. World Phytomed. 22: 102- 108.
  21. Lorenzini, C. A., E. Baldi, C. Bucherelli, B. Sacchett, and G. Tassoni. 1996. Role of dorsal hippocampus in acquisition, consolidation and retrieval of rat's passive avoidance response: A tetrodotoxin functional inactivation study. Brain Res. 730: 32-39. https://doi.org/10.1016/0006-8993(96)00427-1
  22. Mingaud, F., L. C. Moine, N. Etchamendy, C. Mormede, R. Jaffard, and A. Marighetto. 2007. The hippocampus plays a critical role at encoding discontiguous events for subsequent declarative memory expression in mice. Hippocampus 17: 264- 270. https://doi.org/10.1002/hipo.20262
  23. Mohamed, A. F., K. Matsumoto, K. Tabata, H. Takayama, M. Kitajima, and H. Watanabe. 2000. Effects of Uncaria tomentosa total alkaloid and its components on experimental amnesia in mice: Elucidation using the passive avoidance test. J. Pharm. Pharmacol. 52: 1553-1561. https://doi.org/10.1211/0022357001777612
  24. Mohapel, P., G. Leanza, M. Kokaia, and O. Linvall. 2005. Forebrain acetylcholine regulates adult hippocampal neurogenesis and learning. Neurobiol. Aging 36: 939-946.
  25. Paxinos, G. and C. Watson. 1986. The Rat Brain in Stereotaxic Coordinates. New York, Academic Press.
  26. Rothwell, N., S. Allan, and S. Toulmond. 1997. The role of interleukin 1 in acute neurodegeneration and stroke: Pathophysiological and therapeutic implications. J. Clin. Invest. 100: 2648-2652. https://doi.org/10.1172/JCI119808
  27. Shahidi, S., A. Komaki, M. Mahmoodi, N. Atrvash, and M. Ghodrati. 2008. Ascorbic acid supplementation could affect passive avoidance learning and memory in rat. Brain Res. Bull. 76: 109-113. https://doi.org/10.1016/j.brainresbull.2008.01.003
  28. Sharma, D., M. Puri, A. K. Tiwary, N. Singh, and A. S. Jaggi. 2010. Antiamnesic effect of stevioside in scopolamine-treated rats. Indian J. Pharmacol. 42: 164-167. https://doi.org/10.4103/0253-7613.66840
  29. Sharma, D., M. Puri, A. K. Tiwary, N. Singh, and A. S. Jaggi. 2010. Antiamnesic effect of stevioside in scopolamine-treated rats. Indian J. Pharmacol. 42: 164-167. https://doi.org/10.4103/0253-7613.66840
  30. Shors, T. J., T. B. Seib, S. Levine, and R. F. Thompson. 1989. Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. Science 244: 224-226. https://doi.org/10.1126/science.2704997
  31. Tian, Y. Y., L. J. An, L. Jiang, Y. L. Duan, J. Chen, and B. Jiang. 2006. Catalpol protects dopaminergic neurons from LPSinduced neurotoxicity in mesencephalic neuron-glia cultures. Life Sci. 80: 193-199. https://doi.org/10.1016/j.lfs.2006.09.010
  32. Wang, Z., Q. Liu, R. Zhang, S. Liu, Z. Xia, and Y. Hu. 2009. Catalpol ameliorates beta amyloid-induced degeneration of cholinergic neurons by elevating brain-derived neurotrophic factors. Neuroscience 163: 1363-1372. https://doi.org/10.1016/j.neuroscience.2009.07.041
  33. Wei, J., D. X. Lu, R. B. Qi, H. D. Wang, and X. H. Jiang. 2010. Effect of Kangshiai Yizhi Formula I on learning and memory dysfunction induced by scopolamine in mice. Chin. J. Integr. Med. 16: 252-257. https://doi.org/10.1007/s11655-010-0252-3
  34. Yamada, M., T. Chiba, J. Sasabe, K. Terashita, S. Aiso, and M. Matsuoka. 2008. Nasal colivelin treatment ameliorates memory impairment related to Alzheimer's disease. Neuropsychopharmacology 33: 2020-2032. https://doi.org/10.1038/sj.npp.1301591
  35. Zhang, X. L., B. Jiang, Z. B. Li, S. Hao, and L. J. An. 2007. Catalpol ameliorates cognition deficits and attenuates oxidative damage in the brain of senescent mice induced by D-galactose. Pharmacol. Biochem. Behav. 88: 64-72. https://doi.org/10.1016/j.pbb.2007.07.004
  36. Zhang, Z. J. 2004. Therapeutic effects of herbal extracts and constituents in animal model of psychiatric disorders. Life Sci. 75: 1659-1699. https://doi.org/10.1016/j.lfs.2004.04.014

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