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Evidence-Based Complementary and Alternative Medicine
Volume 2015, Article ID 254303, 13 pages
http://dx.doi.org/10.1155/2015/254303
Research Article

A Special Extract of Bacopa monnieri (CDRI-08) Restores Learning and Memory by Upregulating Expression of the NMDA Receptor Subunit GluN2B in the Brain of Scopolamine-Induced Amnesic Mice

1Biochemistry and Molecular Biology Laboratory, Brain Research Centre, Department of Zoology, Banaras Hindu University, Varanasi, Uttar Pradesh 221 005, India
2Lumen Research Foundation, Ashok Nagar, Chennai 600083, India

Received 5 October 2014; Revised 7 February 2015; Accepted 16 February 2015

Academic Editor: Karl Wah-Keung Tsim

Copyright © 2015 Rakesh Rai et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. S. Gazzaniga, R. B. Ivry, and G. R. Mangun, Cognitive Neuroscience: The Biology of the Mind, Norton, 2009.
  2. K. L. Lerner and B. W. Lerner, Gale Encyclopedia of Science, Gale, 2004.
  3. D. W. Goodwin, J. B. Crane, and S. B. Guze, “Alcoholic ‘blackouts’: a review and clinical study of 100 alcoholics,” The American Journal of Psychiatry, vol. 126, no. 2, pp. 191–198, 1969. View at Publisher · View at Google Scholar · View at Scopus
  4. G. Köhr, “NMDA receptor function: subunit composition versus spatial distribution,” Cell and Tissue Research, vol. 326, no. 2, pp. 439–446, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. J. Z. Tsien, P. T. Huerta, and S. Tonegawa, “The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory,” Cell, vol. 87, no. 7, pp. 1327–1338, 1996. View at Publisher · View at Google Scholar · View at Scopus
  6. P. R. Zoladz, C. R. Park, J. D. Halonen et al., “Differential expression of molecular markers of synaptic plasticity in the hippocampus, prefrontal cortex, and amygdala in response to spatial learning, predator exposure, and stress-induced amnesia,” Hippocampus, vol. 22, no. 3, pp. 577–589, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. S. Cull-Candy, S. Brickley, and M. Farrant, “NMDA receptor subunits: diversity, development and disease,” Current Opinion in Neurobiology, vol. 11, no. 3, pp. 327–335, 2001. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Gielen, B. S. Retchless, L. Mony, J. W. Johnson, and P. Paoletti, “Mechanism of differential control of NMDA receptor activity by NR2 subunits,” Nature, vol. 459, no. 7247, pp. 703–707, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. D. J. A. Wyllie, M. R. Livesey, and G. E. Hardingham, “Influence of GluN2 subunit identity on NMDA receptor function,” Neuropharmacology, vol. 74, pp. 4–17, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. X.-H. Zhang, S.-S. Liu, F. Yi, M. Zhuo, and B.-M. Li, “Delay-dependent impairment of spatial working memory with inhibition of NR2B-containing NMDA receptors in hippocampal CA1 region of rats,” Molecular Brain, vol. 6, no. 1, article 13, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. W. Ling, L. Chang, Y. Song et al., “Immunolocalization of NR1, NR2A, and PSD-95 in rat hippocampal subregions during postnatal development,” Acta Histochemica, vol. 114, no. 3, pp. 285–295, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. F. J. Sepulveda, F. J. Bustos, E. Inostroza et al., “Differential roles of NMDA receptor subtypes NR2A and NR2B in dendritic branch development and requirement of RasGRF1,” Journal of Neurophysiology, vol. 103, no. 4, pp. 1758–1770, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. A. C. Gambrill and A. Barria, “NMDA receptor subunit composition controls synaptogenesis and synapse stabilization,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 14, pp. 5855–5860, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. Y. S. Jo and J. S. Choi, “Memory retrieval in response to partial cues requires NMDA receptor-dependent neurotransmission in the medial prefrontal cortex,” Neurobiology of Learning and Memory, vol. 109, pp. 20–26, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. M. M. Y. Fan, H. B. Fernandes, L. Y. J. Zhang, M. R. Hayden, and L. A. Raymond, “Altered NMDA receptor trafficking in a yeast artificial chromosome transgenic mouse model of Huntington's disease,” Journal of Neuroscience, vol. 27, no. 14, pp. 3768–3779, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. X.-L. Huo, J.-J. Min, C.-Y. Pan et al., “Efficacy of lovastatin on learning and memory deficits caused by chronic intermittent hypoxia-hypercapnia: through regulation of NR2B-containing NMDA receptor-ERK pathway,” PLoS ONE, vol. 9, no. 4, Article ID e94278, 2014. View at Publisher · View at Google Scholar · View at Scopus
  17. V. Bagetta, V. Ghiglieri, C. Sgobio, P. Calabresi, and B. Picconi, “Synaptic dysfunction in Parkinson's disease,” Biochemical Society Transactions, vol. 38, no. 2, pp. 493–497, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. B. Picconi, G. Piccoli, and P. Calabresi, “Synaptic dysfunction in Parkinson's disease,” in Synaptic Plasticity, pp. 553–572, Springer, New York, NY, USA, 2012. View at Google Scholar
  19. C. Brazell, G. C. Preston, C. Ward, C. R. Lines, and M. Traub, “The scopolamine model of dementia: chronic transdermal administration,” Journal of Psychopharmacology, vol. 3, no. 2, pp. 76–82, 1989. View at Publisher · View at Google Scholar · View at Scopus
  20. U. Ebert and W. Kirch, “Scopolamine model of dementia: electroencephalogram findings and cognitive performance,” European Journal of Clinical Investigation, vol. 28, no. 11, pp. 944–949, 1998. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Aguiar and T. Borowski, “Neuropharmacological review of the nootropic herb Bacopa monnieri,” Rejuvenation Research, vol. 16, no. 4, pp. 313–326, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. G. K. Shinomol, Muralidhara, and M. M. S. Bharath, “Exploring the role of ‘Brahmi’ (Bocopa monnieri and Centella asiatica) in brain function and therapy,” Recent Patents on Endocrine, Metabolic and Immune Drug Discovery, vol. 5, no. 1, pp. 33–49, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Deepak and A. Amit, “The need for establishing identities of ‘bacoside A and B’, the putative major bioactive saponins of Indian medicinal plant Bacopa monnieri,” Phytomedicine, vol. 11, no. 2-3, pp. 264–268, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. C. Sivaramakrishna, C. V. Rao, G. Trimurtulu, M. Vanisree, and G. V. Subbaraju, “Triterpenoid glycosides from Bacopa monnieri,” Phytochemistry, vol. 66, no. 23, pp. 2719–2728, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. P. B. S. Murthy, V. R. Raju, T. Ramakrisana et al., “Estimation of twelve bacopa saponins in Bacopa monnieri extracts and formulations by high-performance liquid chromatography,” Chemical and Pharmaceutical Bulletin, vol. 54, no. 6, pp. 907–911, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. A. Jyoti, P. Sethi, and D. Sharma, “Bacopa monniera prevents from aluminium neurotoxicity in the cerebral cortex of rat brain,” Journal of Ethnopharmacology, vol. 111, no. 1, pp. 56–62, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. G. K. Shinomol, R. B. Mythri, and M. M. Srinivas Bharath, “Bacopa monnieri extract offsets rotenone-induced cytotoxicity in dopaminergic cells and oxidative impairments in mice brain,” Cellular and Molecular Neurobiology, vol. 32, no. 3, pp. 455–465, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. X. T. Le, H. T. N. Pham, P. T. Do et al., “Bacopa monnieri ameliorates memory deficits in olfactory bulbectomized mice: possible involvement of glutamatergic and cholinergic systems,” Neurochemical Research, vol. 38, no. 10, pp. 2201–2215, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. M. K. Saraf, S. Prabhakar, K. L. Khanduja, and A. Anand, “Bacopa monniera attenuates scopolamine-induced impairment of spatial memory in mice,” Evidence-Based Complementary and Alternative Medicine, vol. 2011, Article ID 236186, 10 pages, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. X. Liu, R. Yue, J. Zhang, L. Shan, R. Wang, and W. Zhang, “Neuroprotective effects of bacopaside i in ischemic brain injury,” Restorative Neurology and Neuroscience, vol. 31, no. 2, pp. 109–123, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. M. P. Pase, J. Kean, J. Sarris, C. Neale, A. B. Scholey, and C. Stough, “The cognitive-enhancing effects of bacopa monnieri: a systematic review of randomized, controlled human clinical trials,” Journal of Alternative and Complementary Medicine, vol. 18, no. 7, pp. 647–652, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. T. Peth-Nui, J. Wattanathorn, S. Muchimapura et al., “Effects of 12-week Bacopa monnieri consumption on attention, cognitive processing, working memory, and functions of both cholinergic and monoaminergic systems in healthy elderly volunteers,” Evidence-Based Complementary and Alternative Medicine, vol. 2012, Article ID 606424, 10 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  33. M. K. Saraf, A. Anand, and S. Prabhakar, “Scopolamine induced amnesia is reversed by Bacopa monniera through participation of kinase-CREB pathway,” Neurochemical Research, vol. 35, no. 2, pp. 279–287, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. S. K. Falsafi, A. Deli, H. Höger, A. Pollak, and G. Lubec, “Scopolamine administration modulates muscarinic, nicotinic and nmda receptor systems,” PLoS ONE, vol. 7, no. 2, Article ID e32082, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. O. Buresova and J. Bures, “Role of olfactory cues in the radial maze performance of rats,” Behavioural Brain Research, vol. 3, no. 3, pp. 405–409, 1981. View at Publisher · View at Google Scholar · View at Scopus
  36. S. J. Y. Mizumori, V. Channon, M. R. Rosenzweig, and E. L. Bennett, “Short- and long-term components of working memory in the rat,” Behavioral Neuroscience, vol. 101, no. 6, pp. 782–789, 1987. View at Publisher · View at Google Scholar · View at Scopus
  37. D. S. Olton, “The radial arm maze as a tool in behavioral pharmacology,” Physiology and Behavior, vol. 40, no. 6, pp. 793–797, 1987. View at Publisher · View at Google Scholar · View at Scopus
  38. B. N. Srikumar, K. Ramkumar, T. R. Raju, and B. S. Shankaranarayana Rao, “Assay of acetylcholinesterase activity in the brain,” Brain and Behavior, pp. 142–144, 2004. View at Google Scholar
  39. G. L. Ellman, K. D. Courtney, V. Andres Jr., and R. M. Featherstone, “A new and rapid colorimetric determination of acetylcholinesterase activity,” Biochemical Pharmacology, vol. 7, no. 2, pp. 88–95, 1961. View at Publisher · View at Google Scholar · View at Scopus
  40. M. M. Bradford, “A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding,” Analytical Biochemistry, vol. 72, no. 1-2, pp. 248–254, 1976. View at Publisher · View at Google Scholar · View at Scopus
  41. K. Singh, P. Gaur, and S. Prasad, “Fragile x mental retardation (Fmr-1) gene expression is down regulated in brain of mice during aging,” Molecular Biology Reports, vol. 34, no. 3, pp. 173–181, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. T. L. Wallace and D. Bertrand, “Importance of the nicotinic acetylcholine receptor system in the prefrontal cortex,” Biochemical Pharmacology, vol. 85, no. 12, pp. 1713–1720, 2013. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Vamvakidès, “Selective M1 muscarinic agonists: failure of therapeutic strategy against Alzheimer's disease or inappropriate tactics?” Annales Pharmaceutiques Francaises, vol. 61, no. 3, pp. 207–210, 2003. View at Google Scholar · View at Scopus
  44. V. V. Giridharan, R. A. Thandavarayan, S. Sato, K. M. Ko, and T. Konishi, “Prevention of scopolamine-induced memory deficits by schisandrin B, an antioxidant lignan from Schisandra chinensis in mice,” Free Radical Research, vol. 45, no. 8, pp. 950–958, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. M. R. Picciotto, M. J. Higley, and Y. S. Mineur, “Acetylcholine as a neuromodulator: cholinergic signaling shapes nervous system function and behavior,” Neuron, vol. 76, no. 1, pp. 116–129, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. X. Zhou, X. L. Qi, K. Douglas et al., “Cholinergic modulation of working memory activity in primate prefrontal cortex,” Journal of Neurophysiology, vol. 106, no. 5, pp. 2180–2188, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. P. E. Gold, “Acetylcholine modulation of neural systems involved in learning and memory,” Neurobiology of Learning and Memory, vol. 80, no. 3, pp. 194–210, 2003. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Easton, V. Douchamps, M. Eacott, and C. Lever, “A specific role for septohippocampal acetylcholine in memory?” Neuropsychologia, vol. 50, no. 13, pp. 3156–3168, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. J. L. Muir, “Acetylcholine, aging, and Alzheimer's disease,” Pharmacology Biochemistry and Behavior, vol. 56, no. 4, pp. 687–696, 1997. View at Publisher · View at Google Scholar · View at Scopus
  50. N. Ogawa, “Central acetylcholinergic systems in the normal aged and in the patient with Alzheimer-type dementia (ATD),” Rinsho Shinkeigaku, vol. 29, no. 12, pp. 1529–1531, 1989. View at Google Scholar
  51. G. Pepeu and M. G. Giovannini, “Changes in acetylcholine extracellular levels during cognitive processes,” Learning & Memory, vol. 11, no. 1, pp. 21–27, 2004. View at Publisher · View at Google Scholar · View at Scopus
  52. A. Kar, S. Panda, and S. Bharti, “Relative efficacy of three medicinal plant extracts in the alteration of thyroid hormone concentrations in male mice,” Journal of Ethnopharmacology, vol. 81, no. 2, pp. 281–285, 2002. View at Publisher · View at Google Scholar · View at Scopus
  53. X. Wang, L. P. Wang, H. Tang et al., “Acetyl-l-carnitine rescues scopolamine-induced memory deficits by restoring insulin-like growth factor II via decreasing p53 oxidation,” Neuropharmacology, vol. 76, pp. 80–87, 2014. View at Publisher · View at Google Scholar · View at Scopus
  54. M. Jahanshahi, E. G. Nickmahzar, and F. Babakordi, “The effect of Ginkgo biloba extract on scopolamine-induced apoptosis in the hippocampus of rats,” Anatomical Science International, vol. 88, no. 4, pp. 217–222, 2013. View at Publisher · View at Google Scholar · View at Scopus
  55. F. Plattner, A. Hernández, T. M. Kistler et al., “Memory enhancement by targeting Cdk5 regulation of NR2B,” Neuron, vol. 81, no. 5, pp. 1070–1083, 2014. View at Publisher · View at Google Scholar
  56. B. L. Brim, R. Haskell, R. Awedikian et al., “Memory in aged mice is rescued by enhanced expression of the GluN2B subunit of the NMDA receptor,” Behavioural Brain Research, vol. 238, no. 1, pp. 211–226, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. M. C. Kuehl-Kovarik, K. R. Magnusson, L. S. Premkumar, and K. M. Partin, “Electrophysiological analysis of NMDA receptor subunit changes in the aging mouse cortex,” Mechanisms of Ageing and Development, vol. 115, no. 1-2, pp. 39–59, 2000. View at Publisher · View at Google Scholar · View at Scopus
  58. A. Krishnakumar, T. R. Anju, P. M. Abraham, and C. S. Paulose, “Alteration in 5-HT2C, NMDA receptor and IP3 in cerebral cortex of epileptic rats: restorative role of Bacopa monnieri,” Neurochemical Research, vol. 40, no. 1, pp. 216–225, 2015. View at Publisher · View at Google Scholar
  59. P. Piyabhan, T. Wetchateng, and S. Sirseeratawong, “Cognitive enhancement effects of Bacopa monnieri(Brahmi) on novel object recognition and NMDA receptor immunodensity in the prefrontal cortex and hippocampus of sub-chronic phencyclidine rat model of schizophrenia,” Journal of the Medical Association of Thailand, vol. 96, no. 2, pp. 231–238, 2013. View at Google Scholar · View at Scopus
  60. J. Mathew, S. Balakrishnan, S. Antony, P. Abraham, and C. S. Paulose, “Decreased GABA receptor in the cerebral cortex of epileptic rats: effect of Bacopa monnieri and Bacoside-A,” Journal of Biomedical Science, vol. 19, article 25, 2012. View at Publisher · View at Google Scholar · View at Scopus
  61. S. P. Pandey, R. Rai, P. Gaur, and S. Prasad, “Development- and age-related alterations in the expression of AMPA receptor subunit GluR2 and its trafficking proteins in the hippocampus of male mouse brain,” Biogerontology, 2015. View at Publisher · View at Google Scholar