Yokukansan, a traditional Japanese herbal medicine, promotes neurite outgrowth in PC12 cells through the activation of extracellular signal regulated kinase 1/2 and phosphatidylinositol 3-kinase/Akt

Journal of Traditional Medicines

Volumn 30, Issue 3, 2013, Pages 102-113

  Kubota, Kaori ^a   Sano, Kentaro ^a   Shiraishi, Akiko ^a   Beppu, Natsuko ^a   Nogami, A ^a   Uchida, Naoki ^b   Takasaki, Kotaro ^a   Katsurabayashi, Shutaro ^a   Mishima, Kenichi ^a   Nishimura, Ryoji ^b   Fujiwara, Michihiro ^a   Iwasaki, Katsunori ^a  

^a FUKUOKA UNIVERSITY   (Japan)

^b FUKUOKA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Alzheimer's disease; neurite outgrowth; neurotrophic factors; PC12 cells; Yokukansan

Indexed keywords

EID: 85016146978     PISSN: 18801447     EISSN: 18813747     Source Type: Journal    
DOI: 10.11339/jtm.30.102     Document Type: Article

References (53)

1. McAllister, AK.: Neurotrophins and neuronal differentiation in the central nervous system. Cell. Mol. Life Sci., 58, 1054-1060, 2001.
2. Lu, B. and Figurov, A.: Role of neurotrophins in synapse development and plasticity. Rev. Neurosci, 8, 1-12, 1997.
3. McAllister, AK., Katz, LC., and Lo, DC.:Neurotrophins and synaptic plasticity. Annu. Rev. Neurosci, 22, 295-318, 1999.
4. Thoenen, H.: Neurotrophins and activity-dependent plasticity. Prog. Brain Res, 128, 183-191, 2000.
5. Poo, MM.: Neurotrophins as synaptic modulators. Nat. Rev. Neurosci, 2, 24-32, 2001.
6. Dawbarn, D., Allen, SJ.: Neurotrophins and neurodegeneration. Neuropathol. Appl. Neurobiol, 29, 211-230, 2003.
7. Sofroniew, MV., Howe, CL., Mobley, WC.: Nerve growth factor signaling, neuroprotection, and neural repair. Annu Rev Neurosci, 24, 1217-1281, 2001.
8. Price, RD., Milne, SA., Sharkey, J., Matsuoka, N.: Advances in small molecules promoting neurotrophic function. Pharmacol. Ther., 115, 292-306, 2007.
9. Greene, LA. and Tischler, AS.: Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci. USA, 73, 2424-2428, 1976.
10. Boulton, TG., Nye, SH., Robbins, DJ., Ip, NY., Radziejewska, E., Morgenbesser, SD., DePinho, RA., Panayotatos, N., Cobb, MH., Yancopoulos, GD.: ERKs: a family of protein-serine/threonine kinases that are activated and tyrosine phosphorylated in response to insulin and NGF. Cell., 65(4), 663-675, 1991.
11. Marshall, CJ.: Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell., 80(2), 179-185, 1995.
12. Vaudry, D., Stork, PJ., Lazarovici, P., Eiden, LE.: Signaling pathways for PC12 cell differentiation: making the right connections. Science, 296, 1648-1649, 2002.
13. Mazzucchelli, C., Brambilla, R.: Ras-related and MAPK signalling in neuronal plasticity and memory formation. Cell Mol Life Sci., 57(4), 604-611, 2000.
14. Madziar, B., Lopez-Coviella, I., Zemelko, V., Berse, B.: Regulation of cholinergic gene expression by nerve growth factor depends on the phosphatidylinositol-3'-kinase pathway. J Neurochem., 92(4), 767-779, 2005.
15. Castell, X., Cheviron, N., Barnier, JV., Diebler, MF.: Exploring the regulation of the expression of ChAT and VAChT genes in NG108-15 cells: implication of PKA and PI3K signaling pathways. Neurochem Res., 28(3-4), 557-564, 2003.
16. Madziar, B., Shah, S., Brock, M., Burke, R., Lopez-Coviella, I., Nickel, AC., Cakal, EB., Blusztajn, JK., Berse, B.: Nerve growth factor regulates the expression of the cholinergic locus and the high-affinity choline transporter via the Akt/PKB signaling pathway. J Neurochem., 107(5), 1284-1293, 2008.
17. Iwasaki, K., Satoh-Nakagawa, T., Maruyama, M., Monma, Y., Nemoto, M., Tomita, N., Tanji, H., Fujiwara, H., Seki, T., Fujii, M., Arai, H., Sasaki, H.: A randomized, observer-blind, controlled trial of the traditional Chinese medicine Yi-Gan San for improvement of behavioral and psychological symptoms and activities of daily living in dementia patients. The Journal of Clinical Psychiatry, 66, 248-252, 2005.
18. Iwasaki, K., Maruyama, M., Tomita, N., Furukawa, K., Nemoto, M., Fujiwara, H., Seki, T., Fujii, M., Kodama, M., Arai, H.: Effects of the traditional Chinese herbal medicine Yi-Gan San for cholinesterase inhibitor-resistant visual hallucinations and neuropsychiatric symptoms in patients with dementia with Lewy bodies. The Journal of Clinical Psychiatry, 66, 1612-1613, 2005.
19. Mizukami, K., Asada, T., Kinoshita, T., Tanaka, K., Sonohara, K., Nakai, R., Yamaguchi, K., Hanyu, H., Kanaya, K., Takao, T., Okada, M., Kudo, S., Kotoku, H., Iwakiri, M., Kurita, H., Miyamura, T., Kawasaki, Y., Omori, K., Shiozaki, K., Odawara, T., Suzuki, T., Yamada, S., Nakamura, Y., Toba, K.: A randomized cross-over study of a traditional Japanese medicine (kampo), yokukansan, in the treatment of the behavioural and psychological symptoms of dementia. Int J Neuropsychopharmacol, 12, 191-199, 2009.
20. Uchida, N., Egashira, N., Iwasaki, K., Ishibashi, A., Tashiro, R., Nogami, A., Manome, N., Abe, M., Takasaki, K., Mishima, K., Takata, J., Oishi, R., Nishimura, R., Fujiwara, M.: Yokukansan inhibits social isolation-induced aggression and methamphetamine-induced hyperlocomotion in rodents. Biol Pharm Bull, 32, 372-375, 2009.
21. Nogami, A., Sakata, Y., Uchida, N., Yamaguchi, K., Kawasaki, C., Shindo, T., Kubota, K., Katsurabayashi, S., Takasaki, K., Mishima, K., Nishimura, R., Fujiwara, M., Iwasaki, K.: Effects of yokukansan on anxiety-like behavior in a rat model of cerebrovascular dementia. J Nat Med, 65, 275-281, 2011.
22. Egashira, N., Nogami, A., Iwasaki, K., Ishibashi, A., Uchida, N., Takasaki, K., Mishima, K., Nishimura, R., Oishi, R., Fujiwara, M.: Yokukansan Enhances Pentobarbital-Induced Sleep in Socially Isolated Mice: Possible Involvement of GABA(A) - Benzodiazepine Receptor Complex. J Pharmacol Sci., 116, 316-320, 2011.
23. Uchida, N., Takasaki, K., Sakata, Y., Nogami, A., Oishi, H., Watanabe, T., Shindo, T., Egashira, N., Kubota, K., Katsurabayashi, S., Mishima, K., Fujiwara, M., Nishimura, R., Iwasaki, K.: Cholinergic Involvement and Synaptic Dynamin 1 Expression in Yokukansan-mediated Improvement of Spatial Memory in a Rat Model of Early Alzheimer's Disease. Phytother Res. 2012 Aug 11. doi: 10.1002/ptr. 4818, 2012.
24. Kawakami, Z., Kanno, H., Ikarashi, Y., Kase, Y.: Yokukansan, a kampo medicine, protects against glutamate cytotoxicity due to oxidative stress in PC12 cells. J Ethnopharmacol, 134, 74-81, 2011.
25. Hiratsuka, T., Matsuzaki, S., Miyata, S., Kinoshita, M., Kakehi, K., Nishida, S., Katayama, T., Tohyama, M.: Yokukansan inhibits neuronal death during ER stress by regulating the unfolded protein response. PLoS One, 5, e13280, 2010.
26. Huang, EJ., Reichardt, LF.: Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem., 72, 609-642, 2003.
27. Tateno, M., Ukai, W., Ono, T., Saito, S., Hashimoto, E., Saito, T.: Neuroprotective effects of Yi-Gan San against beta amyloid-induced cytotoxicity on rat cortical neurons. Prog Neuropsychopharmacol Biol Psychiatry., 32(7), 1704-1707, 2008.
28. Higuchi, M., Onishi, K., Masuyama, N., Gotoh, Y.: The phosphatidylinositol-3 kinase (PI3K)-Akt pathway suppresses neurite branch formation in NGF-treated PC12 cells. Genes Cells, 8, 657-669, 2003.
29. Mesulam, MM., Geula, C.: Nucleus basalis (Ch4) and cortical cholinergic innervation in the human brain: observations based on the distribution of acetylcholinesterase and choline acetyltransferase. J Comp Neurol, 275, 216-240, 1988.
30. Kesner, RP.: Reevaluation of the contribution of the basal forebrain cholinergic system to memory. Neurobiol Aging, 9, 609-616, 1988.
31. Bartus, RT.: On neurodegenerative diseases, models, and treatment strategies: lessons learned and lessons forgotten a generation following the cholinergic hypothesis. Exp Neurol, 163, 495-529, 2000.
32. Perry, EK., Tomlinson, BE., Blessed, G., Bergmann, K., Gibson, PH., Perry, RH.: Correlation of cholinergic abnormalities with senile plaques and mental test scores in senile dementia. Br Med J, 2, 1457-1459, 1978.
33. Calissano, P., Matrone, C., Amadoro, G.: Nerve growth factor as a paradigm of neurotrophins related to Alzheimer's disease. Dev Neurobiol, 70, 372-383, 2010.
34. Williams, LR., Varon, S., Peterson, GM., Wictorin, K., Fischer, W., Bjorklund, A., Gage, FH.: Continuous infusion of nerve growth factor prevents basal forebrain neuronal death after fimbria fornix transaction. Proc Natl Acad Sci. USA, 83, 9231-9235, 1986.
35. Fischer, W., Wictorin, K., Björklund, A., Williams, LR., Varon, S., Gage, FH.: Amelioration of cholinergic neuron atrophy and spatial memory impairment in aged rats by nerve growth factor. Nature, 329, 65-68, 1987.
36. Nibuya, M., Morinobu, S., Duman, RS.: Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J Neurosci., 15, 7539-7547, 1995.
37. Nibuya, M., Nestler, EJ., Duman, RS.: Chronic antidepressant administration increases the expression of cAMP response element binding protein (CREB) in rat hippocampus. J Neurosci., 16, 2365-2372, 1996.
38. Vaidya, VA., Marek, GJ., Aghajanian, GK., Duman, RS.: 5-HT2A receptor-mediated regulation of brain-derived neurotrophic factor mRNA in the hippocampus and the neocortex. J Neurosci. 17, 2785-2795, 1997.
39. Meller, R., Babity, JM., Grahame-Smith, DG.: 5-HT2A receptor activation leads to increased BDNF mRNA expression in C6 glioma cells. Neuromolecular Med., 1, 197-205, 2002.
40. Trajkovska, V., Santini, MA., Marcussen, AB., Thomsen, MS., Hansen, HH., Mikkelsen, JD., Arneberg, L., Kokaia, M., Knudsen, GM., Aznar, S.: BDNF downregulates 5-HT(2A) receptor protein levels in hippocampal cultures. Neurochem Int., 55, 697-702, 2009.
41. Martinowich, K., Lu, B.: Interaction between BDNF and serotonin: role in mood disorders. Neuropsychopharmacology., 33(1), 73-83, 2008.
42. Egashira, N., Iwasaki, K., Ishibashi, A., Hayakawa, K., Okuno, R., Abe, M., Uchida, N., Mishima, K., Takasaki, K., Nishimura, R., Oishi, R., Fujiwara, M.: Repeated administration of Yokukansan inhibits DOI-induced head-twitch response and decreases expression of 5-hydroxytryptamine (5-HT) 2A receptors in the prefrontal cortex. Prog Neuropsychopharmacol Biol Psychiatry., 32(6), 1516-1520, 2008.
43. Ip, NY., Stitt, TN., Tapley, P., Klein, R., Glass, DJ., Fandl, J., Greene, LA., Barbacid, M., Yancopoulos, GD.: Similarities and differences in the way neurotrophins interact with the Trk receptors in neuronal and nonneuronal cells. Neuron., 10(2), 137-149, 1993.
44. Iwasaki, Y., Ishikawa, M., Okada, N., Koizumi, S.: Induction of a distinct morphology and signal transduction in TrkB/PC12 cells by nerve growth factor and brain-derived neurotrophic factor. J Neurochem., 68(3), 927-934, 1997.
45. Sofroniew, MV., Howe, CL., Mobley, WC.: Nerve growth factor signaling, neuroprotection, and neural repair. Annu Rev Neurosci, 24, 1217-1281, 2001.
46. Imamura, S., Tabuchi, M., Kushida, H., Nishi, A., Kanno, H., Yamaguchi, T., Sekiguchi, K., Ikarashi, Y., Kase, Y.: The blood-brain barrier permeability of geissoschizine methyl ether in Uncaria hook, a galenical constituent of the traditional Japanese medicine yokukansan. Cell Mol Neurobiol., 31, 787-793, 2011.
47. Tabuchi, M., Imamura, S., Kawakami, Z., Ikarashi, Y., Kase, Y.: The blood-brain barrier permeability of 18β-glycyrrhetinic acid, a major metabolite of glycyrrhizin in glycyrrhiza root, a constituent of the traditional Japanese medicine yokukansan. Cell Mol Neurobiol., 32, 1139-1146, 2012.
48. Obara, Y., Aoki, T., Kusano, M., Ohizumi, Y.: β-eudesmol induces neurite outgrowth in rat pheochromocytoma cells accompanied by an activation of mitogen-activated protein kinase. J Pharmacol Exp Ther, 301, 803-811, 2002.
49. Sagara, Y., Vanhnasy, J., Maher, P.: Induction of PC12 cell differentiation by flavonoids is dependent upon extracellular signal-regulated kinase activation. J Neurochem, 90, 1144-1155, 2004.
50. Nagase, H., Yamakuni, T., Matsuzaki, K., Maruyama, Y., Kasahara, J., Hinohara, Y., Kondo, S., Mimaki, Y., Sashida, Y., Tank, AW., Fukunaga, K., Ohizumi, Y.: Mechanism of neurotrophic action of nobiletin in PC12D cells. Biochemistry, 44, 13683-13691, 2005.
51. Hwang, SL., Yen, GC.: Effect of hesperetin against oxidative stress via ER- and TrkA-mediated actions in PC12 cells. J Agric Food Chem., 59, 5779-5785, 2011.
52. Liao, KK., Wu, MJ., Chen, PY., Huang, SW., Chiu, SJ., Ho, CT., Yen, JH.: Curcuminoids promote neurite outgrowth in PC12 cells through MAPK/ERK- and PKC-dependent pathways. J Agric Food Chem. 60, 433-443, 2012.
53. El Omri, A., Han, J., Kawada, K., Ben Abdrabbah, M., Isoda, H.: Luteolin enhances cholinergic activities in PC12 cells through ERK1/2 and PI3K/Akt pathways. Brain Res., 1437, 16-25, 2012.