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Effect of Beta-Asarone on Impairment of Spatial Working Memory and Apoptosis in the Hippocampus of Rats Exposed to Chronic Corticosterone Administration

  • Lee, Bombi (Acupuncture and Meridian Science Research Center, College of Korean Medicine, Kyung Hee University) ;
  • Sur, Bongjun (Acupuncture and Meridian Science Research Center, College of Korean Medicine, Kyung Hee University) ;
  • Cho, Seong-Guk (The Graduate School of Basic Science of Korean Medicine, College of Korean Medicine, Kyung Hee University) ;
  • Yeom, Mijung (Acupuncture and Meridian Science Research Center, College of Korean Medicine, Kyung Hee University) ;
  • Shim, Insop (Acupuncture and Meridian Science Research Center, College of Korean Medicine, Kyung Hee University) ;
  • Lee, Hyejung (Acupuncture and Meridian Science Research Center, College of Korean Medicine, Kyung Hee University) ;
  • Hahm, Dae-Hyun (Acupuncture and Meridian Science Research Center, College of Korean Medicine, Kyung Hee University)
  • Received : 2015.03.09
  • Accepted : 2015.08.12
  • Published : 2015.11.01

Abstract

${\beta}$-asarone (BAS) is an active component of Acori graminei rhizoma, a traditional medicine used clinically in treating dementia and chronic stress in Korea. However, the cognitive effects of BAS and its mechanism of action have remained elusive. The purpose of this study was to examine whether BAS improved spatial cognitive impairment induced in rats following chronic corticosterone (CORT) administration. CORT administration (40 mg/kg, i.p., 21 days) resulted in cognitive impairment in the avoidance conditioning test (AAT) and the Morris water maze (MWM) test that was reversed by BAS (200 mg/kg, i.p). Additionally, as assessed by immunohistochemistry and RT-PCR analysis, the administration of BAS significantly alleviated memory-associated decreases in the expression levels of brain-derived neurotrophic factor (BDNF) and cAMP-response element-binding protein (CREB) proteins and mRNAs in the hippocampus. Also, BAS administration significantly restored the expression of Bax and Bcl-2 mRNAs in the hippocampus. Thus, BAS may be an effective therapeutic for learning and memory disturbances, and its neuroprotective effect was mediated, in part, by normalizing the CORT response, resulting in regulation of BDNF and CREB functions and anti-apoptosis in rats.

Keywords

References

  1. Aisen, P. S., Davis, K. L., Berg, J. D., Schafer, K., Campbell, K., Thomas, R. G., Weiner, M. F., Farlow, M. R., Sano, M., Grundman, M. and Thal, L. J. (2000) A randomized controlled trial of prednisone in Alzheimer's disease. Alzheimer's Disease Cooperative Study. Neurology 54, 588-593. https://doi.org/10.1212/WNL.54.3.588
  2. Alkadhi, K. A., Srivareerat, M. and Tran, T. T. (2010) Intensification of long-term memory deficit by chronic stress and prevention by nicotine in a rat model of Alzheimer's disease. Mol. Cell. Neurosci. 45, 289-296. https://doi.org/10.1016/j.mcn.2010.06.018
  3. Bekinschtein, P., Cammarota, M., Katche, C., Slipczuk, L., Rossato, J. I., Goldin, A., Izquierdo, I. and Medina, J. H. (2008) BDNF is essential to promote persistence of long-term memory storage. Proc. Natl. Acad Sci. U.S.A. 105, 2711-2716. https://doi.org/10.1073/pnas.0711863105
  4. Browne, K. D., Iwata, A., Putt, M. E. and Smith, D. H. (2006) Chronic ibuprofen administration worsens cognitive outcome following trau matic brain injury in rats. Exp. Neurol. 201, 301-307. https://doi.org/10.1016/j.expneurol.2006.04.008
  5. Chen, Y., Wei, G., Nie, H., Lin, Y., Tian, H., Liu, Y., Yu, X., Cheng, S., Yan, R., Wang, Q., Liu, D. H., Deng, W., Lai, Y., Zhou, J. H., Zhang, S.X., Lin, W. W. and Chen, D. F. (2014) ${\beta}$-Asarone prevents autophagy and synaptic loss by reducing ROCK expression in asenescence-accelerated prone 8 mice. Brain Res. 1552, 41-54. https://doi.org/10.1016/j.brainres.2014.01.005
  6. Cho, J., Kim, Y. H., Kong, J. Y., Yang, C. H. and Park, C. G. (2002) Protection of cultured rat cortical neurons from excitotoxicity by asarone, a major essential oil component in the rhizomes of Acorus gramineus. Life Sci. 71, 591-599. https://doi.org/10.1016/S0024-3205(02)01729-0
  7. Cory, S and Adams, J. M. (2002) The Bcl2 family: regulators of the cellular life-or-death switch. Nat. Rev. Cancer 2, 647-656. https://doi.org/10.1038/nrc883
  8. Csernansky, J. G., Dong, H., Fagan, A. M., Wang, L., Xiong, C., Holtzman, D. M. and Morris, J. C. (2006) Plasma cortisol and progression of dementia in subjects with Alzheimer-type dementia. Am. J. Psychiatry 163, 2164-2169. https://doi.org/10.1176/ajp.2006.163.12.2164
  9. Dobarro, M., Orejana, L., Aguirre, N. and Ramirez, M. J. (2013) Propranolol reduces cognitive deficits, amyloid ${\beta}$ levels, tau phosphorylation and insulin resistance in response to chronic corticosterone administration. Int. J. Neuropsychopharmacol. 16, 1351-1360. https://doi.org/10.1017/S1461145712001393
  10. Efimova, O. I., Ierusalimskii, V. N., Anokhin, K. V. and Balaban, P. M. (2007) Immunohistochemical detection of the activation of CREB and c-Fos transcription factors in the nervous system of the terrestrial snail induced by pentylenetetrazole. Neurosci. Behav. Physiol. 37, 853-856. https://doi.org/10.1007/s11055-007-0092-6
  11. Endo, Y., Nishimura, J. I., Kobayashi, S. and Kimura, F. (1999) Chronic stress exposure influences local cerebral blood flow in the rat hippocampus. Neuroscience 93, 551-555. https://doi.org/10.1016/S0306-4522(99)00176-1
  12. Geng, Y., Li, C., Liu, J., Xing, G., Zhou, L., Dong, M., Li, X. and Niu, Y. (2010) Beta-asarone improves cognitive function by suppressing neuronal apoptosis in the beta-amyloid hippocampus injection rats. Biol. Pharm. Bull. 33, 836-843. https://doi.org/10.1248/bpb.33.836
  13. Grauer, S. M., Pulito, V. L., Navarra, R. L., Kelly, M. P., Kelley, C., Graf, R., Langen, B., Logue, S., Brennan, J., Jiang, L., Charych, E., Egerland, U., Liu, F., Marquis, K. L., Malamas, M., Hage, T., Comery, T. A. and Brandon, N. J. (2009) Phosphodiesterase 10A inhibitor activity in preclinical models of the positive, cognitive, and negative symptoms of schizophrenia. J. Pharmacol. Exp. Ther. 331, 574-590. https://doi.org/10.1124/jpet.109.155994
  14. Janak, P. H., Manly, J. J. and Martinez, J. L. Jr. (1994) [Leu] enkephalin enhances active avoidance conditioning in rats and mice. Neuropsychopharmacology 10, 53-60. https://doi.org/10.1038/npp.1994.7
  15. Janasson, Z. (2005) Meta-analysis of sex differences in rodent models of learning and memory: a review of behavioral and biological data. Neurosci. Biobehav. Rev. 28, 811-825. https://doi.org/10.1016/j.neubiorev.2004.10.006
  16. Kim, B. K., Ko, I. G., Kim, S. E., Kim, C. J., Yoon, J. S., Baik, H. H., Jin, B. K., Lee, C. Y., Baek, S. B. and Shin, M. S. (2013) Impact of several types of stresses on short-term memory and apoptosis in the hippocampus of rats. Int. Neuroural. J. 17, 114-120. https://doi.org/10.5213/inj.2013.17.3.114
  17. Kim, S. E., Ko, I. G., Kim, B. K., Shin, M. S., Cho, S. and Kim, C. J. (2010) Treadmill exercise prevents aging-induced failure of memory through an increase in neurogenesis and suppression of apoptosis in rat hippocampus. Exp. Gerontol. 45, 357-365. https://doi.org/10.1016/j.exger.2010.02.005
  18. Kim, H., Yi, J. H., Choi, K., Hong, S., Shin, K. S. and Kang, S. J. (2014) Regional differences in acute corticosterone-induced dendritic remodeling in the rat brain and their behavioral consequences. BMC Neurosci. 22, 65-60.
  19. Kudryashov, I. E., Yakovlev, A. A., Kudryashova, I. and Gulyaeva, N. V. (2002) Foot-shock stress alters early postnatal development of electrophysiological responses and caspase-3 activity in rat hippocampus. Neurosci Lett. 332, 95-98. https://doi.org/10.1016/S0304-3940(02)00937-0
  20. Kuhn, H. G., Biebl, M., Wilhelm, D., Li, M., Friendlander, R. M., Winkler, J. (2005) Increased generation of granule cells in adult Bcl-2-overexporessing mice: a role for cell death during continued hippocampal neurogenesis. Eur. J. Neurosci. 22, 1907-1915. https://doi.org/10.1111/j.1460-9568.2005.04377.x
  21. Lee, J. Y., Lee, J. Y., Yun, B. S. and Hwang, B. K. (2004) Antifungal activity of beta-asarone from rhizomes of Acorus gramineus. J. Agric. Food Chem. 52, 776-780. https://doi.org/10.1021/jf035204o
  22. Lee, B., Sur, B. J., Kwon, S., Jung, E., Shim, I., Lee, H. and Hahm, D. H. (2012) Acupuncture stimulation alleviates corticosteroneinduced impairments of spatial memory and cholinergic neurons in rats. Evid. Based Complement. Alternat. Med. 2012, 670536.
  23. Lee, B., Sur, B., Shim, I., Lee, H. and Hahm, D. H. (2014) Baicalin improves chronic corticosterone-induced learning and memory deficits via the enhancement of impaired hippocampal brain-derived neurotrophic factor and cAMP response element-binding protein expression in the rat. J. Nat. Med. 68, 132-143. https://doi.org/10.1007/s11418-013-0782-z
  24. Lee, M. R., Yun, B. S., Park, S. Y., Ly, S. Y., Kim, S. N., Han, B. H. and Sung, C. K. (2010) Anti-amnesic effect of Chong-Myung-Tang on scopolamine-induced memory impairments in mice. J. Ethnopharmacol. 132, 70-74. https://doi.org/10.1016/j.jep.2010.07.041
  25. Li, C., Xing, G., Dong, M., Zhou, L., Li, J., Wang, G., Zou, D., Wang, R., Liu, J. and Niu, Y. (2010) Beta-asarone protection against betaamyloid-induced neurotoxicity in PC12 cells via JNK signaling and modulation of Bcl-2 family proteins. Eur. J. Pharmacol. 635, 96-102. https://doi.org/10.1016/j.ejphar.2010.03.013
  26. Li, Z., Zhao, G., Qian, S., Yang, Z., Chen, X., Chen, J., Cai, C., Liang, X. and Guo, J. (2012) Cerebrovascular protection of ${\beta}$-asarone in Alzheimer's disease rats: a behavioral, cerebral blood flow, biochemical and genic study. J. Ethnopharmacol. 144, 305-312. https://doi.org/10.1016/j.jep.2012.09.013
  27. Limon, I.D., Mendieta, L., Diaz, A., Chamorro, G., Espinosa, B., Zenteno, E. and Guevara, J. (2009) Neuroprotective effect of alpha-asarone on spatial memory and nitric oxide levels in rats injected with amyloid-beta (25-35). Neurosci. Lett. 453, 98-103. https://doi.org/10.1016/j.neulet.2009.02.011
  28. Liu, J., Li, C., Xing, G., Zhou, L., Dong, M., Geng, Y., Li, X., Li, J., Wang, G., Zou, D. and Niu, Y. (2010) Beta-asarone attenuates neuronal apoptosis induced by Beta amyloid in rat hippocampus. Yakugaku Zasshi. 130, 737-746. https://doi.org/10.1248/yakushi.130.737
  29. Lucassen, P. J., Vollmann-Honsdorf, G. K., Gleisberg, M., Czeh, B., De Kloet, E. R. and Fuchs, E. (2001) Chronic psychosocial stress differentially affects apoptosis in hippocampal subregions and cortex of the adult tree shrew. Eur. J. Neurosci. 14, 161-166. https://doi.org/10.1046/j.0953-816x.2001.01629.x
  30. Morris, K. A. and Gold, P. E. (2012) Age-related impairments in memory and in CREB and pCREB expression in hippocampus and amygdala following inhibitory avoidance training. Mech. Ageing Dev. 133, 291-299. https://doi.org/10.1016/j.mad.2012.03.004
  31. Nacher, J., Pham, K., Gil-Fernandez, V. and McEwen, B. S. (2004) Chronic restraint stress and chronic corticosterone treatment modulate differentially the expression of molecules related to structural plasticity in the adult rat piriform cortex. Neuroscience 126, 503-509. https://doi.org/10.1016/j.neuroscience.2004.03.038
  32. Paxinos, G. and Watson, C. (1986) The rat brain in stereotaxic coordinates. 3, 54-85. Academic Press. New York, USA.
  33. Plaschke, K., Feindt, J., Djuric, Z., Heiland, S., Autschbach, F., Lewicka, S., Martin, E., Bardenheuer, H. J., Nawroth, P. P. and Bierhaus, A. (2006) Chronic corticosterone-induced deterioration in rat behaviour is not paralleled by changes in hippocampal NF-kappaB-activation. Stress 9, 97-106. https://doi.org/10.1080/10253890600691551
  34. Rashidy-Pour, A., Vafaei, A. A., Taherian, A. A., Miladi-Gorji, H., Sadeghi, H., Fathollahi, Y. and Bandegi, A. R. (2009) Verapamil enhances acute stress or glucocorticoid-induced deficits in retrieval of long-term memory in rats. Behav. Brain Res. 203, 76-80. https://doi.org/10.1016/j.bbr.2009.04.018
  35. Reagan, L. P. and McEwen, B. S. (1997) Controversies surrounding glucocorticoid-mediated cell death in the hippocampus. J. Chem. Neuroanat. 13, 149-167. https://doi.org/10.1016/S0891-0618(97)00031-8
  36. Roozendaal, B., Hahn, E. L., Nathan, S. V., de Quervain, D. J. and McGaugh, J. L. (2004) Glucocorticoid effects on memory retrieval require concurrent noradrenergic activity in the hippocampus and basolateral amygdala. J. Neurosci. 24, 8161-8169. https://doi.org/10.1523/JNEUROSCI.2574-04.2004
  37. Roozendaal, B., Okuda, S., de Quervain, D. J. and McGaugh, J. L. (2006) Glucocorticoids interact with emotion-induced noradrenergic activation in influencing different memory functions. Neuroscience 138, 901-910. https://doi.org/10.1016/j.neuroscience.2005.07.049
  38. Sajadi, A. A., Samaei, S. A. and Rashidy-Pour, A (2007) Blocking effects of intra-hippocampal naltrexone microinjections on glucocorticoid-induced impairment of spatial memory retrieval in rats. Neuropharmacology 52, 347-354. https://doi.org/10.1016/j.neuropharm.2006.08.021
  39. Sapolsky, R. M. (1996) Stress, glucocorticoids, and damage to the nervous system: the current state of confusion. Stress 1, 1-19. https://doi.org/10.3109/10253899609001092
  40. Saura, C. A. (2012) CREB-regulated transcription coactivator 1-dependent transcription in Alzheimer's disease mice. Neurodegener Dis. 10, 250-252. https://doi.org/10.1159/000333341
  41. Saura, C. A. and Valero, J. (2011) The role of CREB signaling in Alzheimer's disease and other cognitive disorders. Rev. Neurosci. 22, 153-169.
  42. Sun, X. Q., Xu, Z. P., Zhang, S., Cao, X. S. and Liu, T. S. (2009) Simulated weightlessness aggravates hypergravity-induced impairment of learning and memory and neuronal apoptosis in rats. Behav Brain Res. 199, 197-202. https://doi.org/10.1016/j.bbr.2008.11.035
  43. Vaynman, S., Ying, Z. and Gomez-Pinilla, F. (2008) Interplay between brain-derived neurotrophic factor and signal transduction modulators in the regulation of the effects of exercise on synaptic-plasticity. Neuroscience, 122, 647-657.
  44. Walesiuk, A. and Braszko, J. J. (2010) Gingkoselect alleviates chronic corticosterone-induced spatial memory deficits in rats. Fitoterapia. 81, 25-29. https://doi.org/10.1016/j.fitote.2009.06.020
  45. Walesiuk, A., Trofimiuk, E. and Braszko, J. J. (2006) Ginkgo biloba normalizes stress- and corticosterone-induced impairment of recall in rats. Pharmacol. Res. 53, 123-128. https://doi.org/10.1016/j.phrs.2005.09.007
  46. Wang, W., Liao, Q. P., Quan, L. H., Liu, C. Y., Chang, Q., Liu, X. M. and Liao, Y. H. (2010) The effect of Acorus gramineus on the bioavailabilities and brain concentrations of ginsenosides Rg1, Re and Rb1 after oral administration of Kai-Xin-San preparations in rats. J. Ethnopharmacol. 131, 313-320. https://doi.org/10.1016/j.jep.2010.06.034
  47. Willians, C. M., El Mohsen, M. A., Vauzour, D., Rendeiro, C., Butler, L. T., Ellis, J. A., Whiteman, M. and Spencer, J. P. (2008) Blueberryinduced changes in spatial working memory correlate with changes in hippocampal CREB phosphorylation and brain-derived neurotrophic factor (BDNF) levels. Free Radic Biol Med. 45, 295-305. https://doi.org/10.1016/j.freeradbiomed.2008.04.008
  48. Wuppen, K., Oesterle, D., Lewicka, S., Kopitz, J. and Plaschke, K. (2010) A subchronic application period of glucocorticoids leads to rat cognitive dysfunction whereas physostigmine induces a mild neuroprotection. J. Neural. Transm. 117, 1055-1065. https://doi.org/10.1007/s00702-010-0441-4
  49. Xu, Y., Lin, D., Li, S., Li, G., Shyamala, S. G., Barish, P. A., Vernon, M. M., Pan, J. and Ogle, W. O. (2009) Curcumin reverses impaired cognition and neuronal plasticity induced by chronic stress. Neuropharmacology 57, 463-471. https://doi.org/10.1016/j.neuropharm.2009.06.010
  50. Zou, D. J., Wang, G., Liu, J. C., Dong, M. X., Li, X. M., Zhang, C., Zhou, L., Wang, R., Niu, Y. C. (2011) Beta-asarone attenuates beta-amyloid-induced apoptosis through the inhibition of the activation of apoptosis signal-regulating kinase 1 in SH-SY5Y cells. Pharmazie. 66, 44-51.

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