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Evidence-Based Complementary and Alternative Medicine
Volume 2013 (2013), Article ID 514908, 18 pages
http://dx.doi.org/10.1155/2013/514908
Research Article

NBM-T-L-BMX-OS01, Semisynthesized from Osthole, Is a Novel Inhibitor of Histone Deacetylase and Enhances Learning and Memory in Rats

1Department of Biotechnology and Animal Science, College of Bioresources, National Ilan University, Ilan 260, Taiwan
2New Drug Research & Development Center, NatureWise Biotech & Medicals Corporation, Taipei 112, Taiwan
3Graduate Institute of Pharmacognosy, Taipei Medical University, Taipei 110, Taiwan
4Institute of Traditional Medicine, School of Medicine, National Yang-Ming University, Taipei 112, Taiwan
5Graduate Institute of Acupuncture Science, China Medical University, Taichung 404, Taiwan
6Department of Education and Research, Taipei City Hospital, Taipei 103, Taiwan

Received 10 December 2012; Revised 19 February 2013; Accepted 25 February 2013

Academic Editor: Alfredo Vannacci

Copyright © 2013 Ying-Chen Yang 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. Bhasin, E. L. Reinherz, and P. A. Reche, “Recognition and classification of histones using support vector machine,” Journal of Computational Biology, vol. 13, no. 1, pp. 102–112, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. A. Mai, S. Massa, D. Rotili et al., “Histone deacetylation in epigenetics: an attractive target for anticancer therapy,” Medicinal Research Reviews, vol. 25, no. 3, pp. 261–309, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. D. C. Drummond, C. O. Noble, D. B. Kirpotin, Z. Guo, G. K. Scott, and C. C. Benz, “Clinical development of histone deacetylase inhibitors as anticancer agents,” Annual Review of Pharmacology and Toxicology, vol. 45, pp. 495–528, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. X. J. Yang and E. Seto, “HATs and HDACs: from structure, function and regulation to novel strategies for therapy and prevention,” Oncogene, vol. 26, no. 37, pp. 5310–5318, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Fischer, F. Sananbenesi, X. Wang, M. Dobbin, and L. H. Tsai, “Recovery of learning and memory is associated with chromatin remodelling,” Nature, vol. 447, no. 7141, pp. 178–182, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. D. Kim, C. L. Frank, M. M. Dobbin et al., “Deregulation of HDAC1 by p25/Cdk5 in neurotoxicity,” Neuron, vol. 60, no. 5, pp. 803–817, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. J. S. Guan, S. J. Haggarty, E. Giacometti et al., “HDAC2 negatively regulates memory formation and synaptic plasticity,” Nature, vol. 459, no. 7243, pp. 55–60, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. S. C. McQuown and M. A. Wood, “HDAC3 and the molecular brake pad hypothesis,” Neurobiology of Learning and Memory, vol. 96, no. 1, pp. 27–34, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. N. Federman, M. S. Fustiñana, and A. Romano, “Histone acetylation is recruited in consolidation as a molecular feature of stronger memories,” Learning & Memory, vol. 16, no. 10, pp. 600–606, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. C. G. Vecsey, J. D. Hawk, K. M. Lattal et al., “Histone deacetylase inhibitors enhance memory and synaptic plasticity via CREB: CBP-dependent transcriptional activation,” Journal of Neuroscience, vol. 27, no. 23, pp. 6128–6140, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. C. Sgobio, V. Ghiglieri, C. Costa et al., “Hippocampal synaptic plasticity, memory, and epilepsy: effects of long-term valproic acid treatment,” Biological Psychiatry, vol. 67, no. 6, pp. 567–574, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. J. M. Alarcón, G. Malleret, K. Touzani et al., “Chromatin acetylation, memory, and LTP are impaired in CBP+/- mice: a model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration,” Neuron, vol. 42, no. 6, pp. 947–959, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Peleg, F. Sananbenesi, A. Zovoilis et al., “Altered histone acetylation is associated with age-dependent memory impairment in mice,” Science, vol. 328, no. 5979, pp. 753–756, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. E. Hockly, V. M. Richon, B. Woodman et al., “Suberoylanilide hydroxamic acid, a histone deacetylase inhibitor, ameliorates motor deficits in a mouse model of Huntington's disease,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 4, pp. 2041–2046, 2003. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Kilgore, C. A. Miller, D. M. Fass et al., “Inhibitors of class 1 histone deacetylases reverse contextual memory deficits in a mouse model of alzheimer's disease,” Neuropsychopharmacology, vol. 35, no. 4, pp. 870–880, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. D. M. Fass, S. A. Reis, B. Ghosh et al., “Crebinostat: a novel cognitive enhancer that inhibits histone deacetylase activity and modulates chromatin-mediated neuroplasticity,” Neuropharmacology, vol. 64, no. 1, pp. 81–96, 2013. View at Google Scholar
  17. I. Oehme, H. E. Deubzer, D. Wegener et al., “Histone deacetylase 8 in neuroblastoma tumorigenesis,” Clinical Cancer Research, vol. 15, no. 1, pp. 91–99, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. J. Y. Kim, S. Shen, K. Dietz et al., “HDAC1 nuclear export induced by pathological conditions is essential for the onset of axonal damage,” Nature Neuroscience, vol. 13, no. 2, pp. 180–189, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. K. M. Miller, J. V. Tjeertes, J. Coates et al., “Human HDAC1 and HDAC2 function in the DNA-damage response to promote DNA nonhomologous end-joining,” Nature Structural & Molecular Biology, vol. 17, no. 9, pp. 1144–1151, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Jawerka, D. Colak, L. Dimou et al., “The specific role of histone deacetylase 2 in adult neurogenesis,” Neuron Glia Biology, vol. 6, no. 2, pp. 93–107, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Mishra, J. Huang, Y. Y. Lee et al., “Gastrodia elata modulates amyloid precursor protein cleavage and cognitive functions in mice,” BioScience Trends, vol. 5, no. 3, pp. 129–138, 2011. View at Google Scholar
  22. Z. Lin, J. Gu, J. Xiu, T. Mi, J. Dong, and J. K. Tiwari, “Traditional chinese medicine for senile dementia,” Evidence-Based Complementary and Alternative Medicine, vol. 2012, Article ID 692621, 13 pages, 2012. View at Publisher · View at Google Scholar
  23. B. Lee, I. Shim, H. Lee, and D. H. Hahm, “Rehmannia glutinosa ameliorates scopolamine-induced learning and memory impairment in rats,” Journal of Microbiology and Biotechnology, vol. 21, no. 8, pp. 874–883, 2011. View at Google Scholar
  24. J. X. Liu, W. P. Zhang, and Q. S. Lian, “Phytoestrogen-like effect of Cnidium monnieri (L) cuss,” Chinese Journal of Clinical Rehabilitation, vol. 9, no. 23, pp. 186–189, 2005. View at Google Scholar · View at Scopus
  25. C. M. Zhang, X. Feng, and Y. Zhong, “The advancement in the chemical and pharmacological study of Cnidium monnieri (l.) cusson,” Practical Pharmacy and Clinical Remedies, vol. 9, pp. 55–57, 2006. View at Google Scholar
  26. J. Allard and F. Giuliano, “Central nervous system agents in the treatment of erectile dysfunction: how do they work?” Current Urology Reports, vol. 2, no. 6, pp. 488–494, 2001. View at Google Scholar · View at Scopus
  27. P. L. Kuo, Y. L. Hsu, C. H. Chang, and J. K. Chang, “Osthole-mediated cell differentiation through bone morphogenetic protein-2/p38 and extracellular signal-regulated kinase 1/2 pathway in human osteoblast cells,” Journal of Pharmacology and Experimental Therapeutics, vol. 314, no. 3, pp. 1290–1299, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. J. H. Guh, S. M. Yu, F. N. Ko, T. S. Wu, and C. M. Teng, “Antiproliferative effect in rat vascular smooth muscle cells by osthole, isolated from Angelica pubescens,” European Journal of Pharmacology, vol. 298, no. 2, pp. 191–197, 1996. View at Publisher · View at Google Scholar · View at Scopus
  29. J. J. Luszczki, M. Andres-Mach, W. Cisowski, I. Mazol, K. Glowniak, and S. J. Czuczwar, “Osthole suppresses seizures in the mouse maximal electroshock seizure model,” European Journal of Pharmacology, vol. 607, no. 1–3, pp. 107–109, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. Z. Qi, J. Xue, Y. Zhang, H. Wang, and M. Xie, “Osthole ameliorates insulin resistance by increment of adiponectin release in high-fat and high-sucrose-induced fatty liver rats,” Planta Medica, vol. 77, no. 3, pp. 231–235, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. W. B. Liu, J. Zhou, Y. Qu et al., “Neuroprotective effect of osthole on MPP+-induced cytotoxicity in PC12 cells via inhibition of mitochondrial dysfunction and ROS production,” Neurochemistry International, vol. 57, no. 3, pp. 206–215, 2010. View at Publisher · View at Google Scholar · View at Scopus
  32. M. T. Hsieh, C. L. Hsieh, W. H. Wang, C. S. Chen, C. J. Lin, and C. R. Wu, “Osthole improves aspects of spatial performance in ovariectomized rats,” American Journal of Chinese Medicine, vol. 32, no. 1, pp. 11–20, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. C. R. Wu, L. W. Lin, C. L. Hsieh, W. H. Wang, Y. T. Lin, and M. T. Hsieh, “Petroleum ether extract of Cnidium monnieri ameliorated scopolamine-induced amnesia through adrenal gland-mediated mechanism in male rats,” Journal of Ethnopharmacology, vol. 117, no. 3, pp. 403–407, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. W. J. Huang, C. C. Chen, S. W. Chao et al., “Synthesis of n-hydroxycinnamides capped with a naturally occurring moiety as inhibitors of histone deacetylase,” ChemMedChem, vol. 5, no. 4, pp. 598–607, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. J. Shi, Y. Wang, and G. Luo, “Ligustrazine phosphate ethosomes for treatment of alzheimer's disease, in vitro and in animal model studies,” AAPS PharmSciTech, vol. 13, no. 2, pp. 485–492, 2012. View at Google Scholar
  36. X. Wang, Z. H. Wang, Y. Y. Wu et al., “Melatonin attenuates scopolamine-induced memory/synaptic disorder by rescuing epacs/mir-124/egr1 pathway,” Molecular Neurobiology, vol. 47, no. 1, pp. 373–381, 2013. View at Google Scholar
  37. C. C. Liang, C. Y. Hong, C. F. Chen, and T. H. Tsai, “Measurement and pharmacokinetic study of tetramethylpyrazine in rat blood and its regional brain tissue by high-performance liquid chromatography,” Journal of Chromatography B, vol. 724, no. 2, pp. 303–309, 1999. View at Publisher · View at Google Scholar · View at Scopus
  38. Y. M. Tsai, C. F. Chien, L. C. Lin, and T. H. Tsai, “Curcumin and its nano-formulation: the kinetics of tissue distribution and blood-brain barrier penetration,” International Journal of Pharmaceutics, vol. 416, no. 1, pp. 331–338, 2011. View at Google Scholar
  39. Y. C. Yang, C. H. Lin, and E. H. Y. Lee, “Serum- and glucocorticoid-inducible kinase 1 (SGK1) increases neurite formation through microtubule depolymerization by SGK1 and by SGK1 phosphorylation of tau,” Molecular and Cellular Biology, vol. 26, no. 22, pp. 8357–8370, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. T. Y. Kuo, C. L. Huang, J. M. Yang et al., “The role of ribosylated-bsa in regulating pc12 cell viability,” Cell Biology and Toxicology, vol. 28, no. 4, pp. 255–267, 2012. View at Google Scholar
  41. Y. C. Yang, Y. L. Ma, W. T. Liu, and E. H. Lee, “Laminin-beta1 impairs spatial learning through inhibition of erk/mapk and sgk1 signaling,” Neuropsychopharmacology, vol. 36, no. 12, pp. 2571–2586, 2011. View at Google Scholar
  42. W. Classen and C. Mondadori, “Facilitation or inhibition of memory by morphine: a question of experimental parameters,” Experientia, vol. 40, no. 5, pp. 506–509, 1984. View at Google Scholar · View at Scopus
  43. H. G. Van Oyen, N. E. Van De Poll, and J. P. C. De Bruin, “Sex, age and shock-intensity as factors in passive avoidance,” Physiology and Behavior, vol. 23, no. 5, pp. 915–918, 1979. View at Publisher · View at Google Scholar · View at Scopus
  44. K. Tóth, K. László, E. Lukács, and L. Lénárd, “Intraamygdaloid microinjection of acylated-ghrelin influences passive avoidance learning,” Behavioural Brain Research, vol. 202, no. 2, pp. 308–311, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. A. M. Huang, H. L. Wang, Y. P. Tang, and E. H. Y. Lee, “Expression of integrin-associated protein gene associated with memory formation in rats,” Journal of Neuroscience, vol. 18, no. 11, pp. 4305–4313, 1998. View at Google Scholar · View at Scopus
  46. G. Arqué, V. Fotaki, D. Fernández, M. M. de Lagrán, M. L. Arbonés, and M. Dierssen, “Impaired spatial learning strategies and novel object recognition in mice haploinsufficient for the dual specificity tyrosine-regulated kinase-1A (Dyrk1A),” PLoS ONE, vol. 3, no. 7, Article ID e2575, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. J. B. Lee, J. Wei, W. Liu, J. Cheng, J. Feng, and Z. Yan, “Histone deacetylase 6 gates the synaptic action of acute stress in prefrontal cortex,” Journal of Physiology, vol. 590, part 7, pp. 1535–1546, 2012. View at Google Scholar
  48. S. J. Park, D. H. Kim, J. M. Jung et al., “The ameliorating effects of stigmasterol on scopolamine-induced memory impairments in mice,” European Journal of Pharmacology, vol. 676, no. 1–3, pp. 64–70, 2012. View at Google Scholar
  49. J. Chen, Y. Long, M. Han, T. Wang, Q. Chen, and R. Wang, “Water-soluble derivative of propolis mitigates scopolamine-induced learning and memory impairment in mice,” Pharmacology Biochemistry and Behavior, vol. 90, no. 3, pp. 441–446, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. D. H. Kim, S. J. Park, J. M. Kim et al., “Cognitive dysfunctions induced by a cholinergic blockade and abeta 25-35 peptide are attenuated by salvianolic acid b,” Neuropharmacology, vol. 61, no. 8, pp. 1432–1440, 2011. View at Google Scholar
  51. M. Haberland, M. H. Mokalled, R. L. Montgomery, and E. N. Olson, “Epigenetic control of skull morphogenesis by histone deacetylase 8,” Genes & Development, vol. 23, no. 14, pp. 1625–1630, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. I. Oehme, H. E. Deubzer, M. Lodrini, T. Milde, and O. Witt, “Targeting of HDAC8 and investigational inhibitors in neuroblastoma,” Expert Opinion on Investigational Drugs, vol. 18, no. 11, pp. 1605–1617, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. D. A. Frank and M. E. Greenberg, “CREB: a mediator of long-term memory from mollusks to mammals,” Cell, vol. 79, no. 1, pp. 5–8, 1994. View at Publisher · View at Google Scholar · View at Scopus
  54. S. B. McHugh, T. G. Campbell, A. M. Taylor, J. N. P. Rawlins, and D. M. Bannerman, “A role for dorsal and ventral hippocampus in inter-temporal choice cost-benefit decision making,” Behavioral Neuroscience, vol. 122, no. 1, pp. 1–8, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. N. J. Broadbent, L. R. Squire, and R. E. Clark, “Spatial memory, recognition memory, and the hippocampus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 40, pp. 14515–14520, 2004. View at Publisher · View at Google Scholar · View at Scopus
  56. A. Ennaceur and J. Delacour, “A new one-trial test for neurobiological studies of memory in rats. 1: behavioral data,” Behavioural Brain Research, vol. 31, no. 1, pp. 47–59, 1988. View at Google Scholar · View at Scopus
  57. N. Plath, O. Ohana, B. Dammermann et al., “Arc/arg3. 1 is essential for the consolidation of synaptic plasticity and memories,” Neuron, vol. 52, no. 3, pp. 437–444, 2006. View at Google Scholar
  58. V. Ramírez-Amaya, A. Vazdarjanova, D. Mikhael, S. Rosi, P. F. Worley, and C. A. Barnes, “Spatial exploration-induced Arc mRNA and protein expression: evidence for selective, network-specific reactivation,” Journal of Neuroscience, vol. 25, no. 7, pp. 1761–1768, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. D. P. Stefanko, R. M. Barrett, A. R. Ly, G. K. Reolon, and M. A. Wood, “Modulation of long-term memory for object recognition via HDAC inhibition,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 23, pp. 9447–9452, 2009. View at Publisher · View at Google Scholar · View at Scopus
  60. D. Y. Choi, Y. J. Lee, S. Y. Lee et al., “Attenuation of scopolamine-induced cognitive dysfunction by obovatol,” Archives of Pharmacal Research, vol. 35, no. 7, pp. 1279–1286, 2012. View at Google Scholar
  61. R. D'Hooge and P. P. De Deyn, “Applications of the Morris water maze in the study of learning and memory,” Brain Research Reviews, vol. 36, no. 1, pp. 60–90, 2001. View at Publisher · View at Google Scholar · View at Scopus
  62. W. Liskowsky and R. Schliebs, “Muscarinic acetylcholine receptor inhibition in transgenic Alzheimer-like Tg2576 mice by scopolamine favours the amyloidogenic route of processing of amyloid precursor protein,” International Journal of Developmental Neuroscience, vol. 24, no. 2-3, pp. 149–156, 2006. View at Publisher · View at Google Scholar · View at Scopus
  63. Y. Fan, J. Hu, J. Li et al., “Effect of acidic oligosaccharide sugar chain on scopolamine-induced memory impairment in rats and its related mechanisms,” Neuroscience Letters, vol. 374, no. 3, pp. 222–226, 2005. View at Publisher · View at Google Scholar · View at Scopus
  64. S. H. Kwon, H. K. Lee, J. A. Kim et al., “Neuroprotective effects of chlorogenic acid on scopolamine-induced amnesia via anti-acetylcholinesterase and anti-oxidative activities in mice,” European Journal of Pharmacology, vol. 649, no. 1–3, pp. 210–217, 2010. View at Publisher · View at Google Scholar · View at Scopus
  65. A. Salminen, T. Tapiola, P. Korhonen, and T. Suuronen, “Neuronal apoptosis induced by histone deacetylase inhibitors,” Molecular Brain Research, vol. 61, no. 1-2, pp. 203–206, 1998. View at Publisher · View at Google Scholar · View at Scopus
  66. J. R. Davie, “Inhibition of histone deacetylase activity by butyrate,” Journal of Nutrition, vol. 133, no. 7, supplement, pp. 2485S–2493S, 2003. View at Google Scholar
  67. Ø. Bruserud, C. Stapnes, E. Ersvær, B. T. Gjertsen, and A. Ryningen, “Histone deacetylase inhibitors in cancer treatment: a review of the clinical toxicity and the modulation of gene expression in cancer cells,” Current Pharmaceutical Biotechnology, vol. 8, no. 6, pp. 388–400, 2007. View at Publisher · View at Google Scholar · View at Scopus
  68. S. Balasubramanian, J. Ramos, W. Luo, M. Sirisawad, E. Verner, and J. J. Buggy, “A novel histone deacetylase 8 (HDAC8)-specific inhibitor PCI-34051 induces apoptosis in T-cell lymphomas,” Leukemia, vol. 22, no. 5, pp. 1026–1034, 2008. View at Publisher · View at Google Scholar · View at Scopus
  69. L. P. Sun, A. L. Chen, H. C. Hung et al., “Chrysin: a histone deacetylase 8 inhibitor with anticancer activity and a suitable candidate for standardization of chinese propolis,” Journal of Agricultural and Food Chemistry, vol. 60, no. 47, pp. 11748–11758, 2012. View at Google Scholar
  70. J. Gao, B. Siddoway, Q. Huang, and H. Xia, “Inactivation of CREB mediated gene transcription by HDAC8 bound protein phosphatase,” Biochemical and Biophysical Research Communications, vol. 379, no. 1, pp. 1–5, 2009. View at Publisher · View at Google Scholar · View at Scopus