Browse > Article
http://dx.doi.org/10.4062/biomolther.2014.019

Neuroprotective Effect of Steamed and Fermented Codonopsis lanceolata  

Weon, Jin Bae (Department of Medical Biomaterials Engineering, College of Biomedical Science)
Yun, Bo-Ra (Department of Medical Biomaterials Engineering, College of Biomedical Science)
Lee, Jiwoo (Department of Medical Biomaterials Engineering, College of Biomedical Science)
Eom, Min Rye (Department of Medical Biomaterials Engineering, College of Biomedical Science)
Ko, Hyun-Jeong (Laboratory of Microbiology and Immunology, College of Pharmacy, Kangwon National University)
Lee, Hyeon Yong (Department of Teaics, Seowon University)
Park, Dong-Sik (Department of Agrofood Resources, Functional food & Nutrition Division)
Chung, Hee-Chul (Newtree CO., LTD.)
Chung, Jae Youn (Newtree CO., LTD.)
Ma, Choong Je (Department of Medical Biomaterials Engineering, College of Biomedical Science)
Publication Information
Biomolecules & Therapeutics / v.22, no.3, 2014 , pp. 246-253 More about this Journal
Abstract
Codonopsis lanceolata has been used as an herbal medicine for several lung inflammatory diseases, such as asthma, tonsillitis, and pharyngitis. Previously, we showed the neuroprotective effect of steamed and fermented C. lanceolata (SFC) in vitro and in vivo. In the current study, the treatment of HT22 cells with SFC decreased glutamate-induced cell death, suggesting that SFC protected HT22 cells from glutamate-induced cytotoxicity. Based on these, we sought to elucidate the mechanisms of the neuroprotective effect of SFC by measuring the oxidative stress parameters and the expression of Bax and caspase-3 in HT22 cells. SFC reduced contents of ROS, $Ca^{2+}$ and NO. Moreover, SFC restored contents of glutathione and glutathione reductase as well as inhibited Bax and caspase-3 activity in HT22 cells. These results indicate that steamed and fermented C. lanceolata (SFC) extract protected HT22 cells by anti-oxidative effect and inhibition of the expression of Bax and caspase-3.
Keywords
Codonopsis lanceolata; Steam and fermentation; Neuroprotective activity; Antioxidative activity; Bax; Caspase-3;
Citations & Related Records
Times Cited By KSCI : 4  (Citation Analysis)
연도 인용수 순위
1 Weon, J. B., Kim, C. Y., Yang, H. J. and Ma, C. J. (2012) Neuroprotective compounds isolated from Cynanchum paniculatum. Arch. Pharm. Res. 35, 617-621.   DOI   ScienceOn
2 Weon, J. B., Yun, B.- R., Lee, J., Eom, M. R., Kim, J. S., Lee, H. Y., Park, D. S., Chung, H. C., Chung, J. Y. and Ma, C. J. (2013) Effect of Codonopsis lanceolata with steamed and fermented process on scopolamine-Induced memory impairment in mice. Biomol. Ther. 21, 405-410.   DOI
3 Xiang, J., Chao, D. T. and Korsmeyer, S. J. (1996) Bax-induced cell death may not require interleukin 1 beta-converting enzyme-like proteases. Proc. Natl. Acad. Sci. U.S.A. 93, 14559-14563.   DOI   ScienceOn
4 Xu, J., Xilouri, M., Bruban, J., Shioi, J., Shao, Z., Papazoglou, I., Vekrellis, K. and Robakis, N. K. (2011) Extracellular progranulin protects cortical neurons from toxic insults by activating survival signaling. Neurobiol. Aging 32, 2326.e5-2326.e16
5 Yang, H. J., Weon, J. B., Lee, B. and Ma, C. J. (2011) The alteration of components in the fermented Hwangryunhaedok-tang and its neuroprotective activity. Pharmacogn. Mag. 7, 207-212.   DOI   ScienceOn
6 Yongxu, S. and Jicheng, L. (2008) Structural characterization of a water- soluble polysaccharide from the roots of Codonopsis pilosula and its immunity activity. Int. J. Biol. Macromol. 43, 279-282.   DOI   ScienceOn
7 Zhang, Y. M. and Bhavnani, B. R. (2005) Glutamate-induced apoptosis in primary cortical neurons is inhibited by equine estrogens via down-regulation of caspase-3 and prevention of mitochondrial cytochrome c release. BMC Neurosci. 6, 13.   DOI
8 Nutt, L. K., Pataer, A., Pahler, J., Fang, B., Roth, J., McConkey, D. J. and Swisher, S. G. (2002) Bax and Bak promote apoptosis by modulating endoplasmic reticular and mitochondrial $Ca^{2+}$ stores. J. Biol. Chem. 277, 9219-9225.   DOI   ScienceOn
9 Ola, M. S., Nawaz, M. and Ahsan, H. (2011) Role of Bcl-2 family proteins and caspases in the regulation of apoptosis. Mol. Cell. Biochem. 351, 41-58.   DOI
10 Reynolds, I. J. and Hastings, T. G. (1995) Glutamate induces the production of reactive oxygen species in cultured forebrain neurons following NMDA receptor activation. J. Neurosci. 15, 3318-3327.
11 Ryu, H. S. (2009) Effect of Codonopsis lanceolatae Extracts on mouse IL-2, IFN-, IL-10 cytokine production by peritoneal macrophage and the ratio of IFN-, IL-10 cytokine. Kor. J. Food Nutr. 22, 69-74.   과학기술학회마을
12 Satoh, T., Enokido, Y., Kubo, T., Yamada, M. and Hatanaka, H. (1998) Oxygen toxicity induces apoptosis in neuronal cells. Cell. Mol. Neurobiol. 18, 649-666.   DOI   ScienceOn
13 Suzuki, Y. S., Forman, H. J., Sevanian, A. (1997) Oxidants as stimulators of signal transduction. Free Radic. Biol. Med. 22, 269-285.   DOI   ScienceOn
14 Ushijima, M., Komoto, N., Sugizono, Y., Mizuno, I., Sumihiro, M., Ichikawa, M., Hayama, M., Kawahara, N., Nakane, T., Shirota, O., Sekita, S. and Kuroyanagi, M. (2008) Triterpene glycosides from the roots of Codonopsis lanceolata. Chem. Pharm. Bull. 56, 308-314.   DOI   ScienceOn
15 Tan, S., Sagara, Y., Liu, Y., Maher, P. and Schubert, D. (1998a) The regulation of reactive oxygen species production during programmed cell death. J. Cell. Biol. 141, 1423-1432.   DOI   ScienceOn
16 Tan, S., Wood, M. and Maher, P. (1998b) Oxidative stress induces a form of programmed cell death with characteristics of both apoptosis and necrosis in neuronal cells. J. Neurochem. 71, 95-105.
17 Tanovic, A. and Alfaro, V. (2006) Glutamate-related excitotoxicity neuroprotection with memantine, an uncompetitive antagonist of NMDA-glutamate receptor, in Alzheimer's disease and vascular dementia. Rev. Neurol. 42, 607-616.
18 Wang, G. J., Randall, R. D. and Thayer, S. A. (1994) Glutamate-induced intracellular acidification of cultured hippocampal neurons demonstrates altered energy metabolism resulting from $Ca^{2+}$ loads. J. Neurophysiol. 72, 2563-2569.
19 Kane, D. J., Sarafian, T. A., Anton, R., Hahn, H., Gralla, E. B., Valentine, J. S., Ord, T. and Bredesen, D. E. (1993) Bcl-2 inhibition of neuronal death: decreased generation of reactive oxygen species. Science 262, 1274-1277.   DOI
20 Knowles, R. G., Palacios, M., Palmer, R. M. J. and Moncada, S. (1989) Formation of nitric oxide from L-arginnie in central nervous system: a transduction mechanism for stimulation of the soluble guanylate cyclase. Proc. Natl. Acad. Sci. U.S.A. 86, 5159-5162.   DOI   ScienceOn
21 Ly, J. D., Grubb, D. R. and Lawen, A. (2003) The mitochondrial membrane potential ($\Psi$) in apoptosis; an update. Apoptosis 8, 115-128.   DOI   ScienceOn
22 Lafon-Cazal, M., Culcasi, M., Gaven, F., Pietri, S. and Bockaert, J. (1993) Nitric oxide, superoxide and peroxynitrite: putative mediators of NMDA-induced cell death in cerebellar granule cells. Neuro pharmacology 32, 1259-1266.
23 Lewerenz, J., Klein, M. and Methner, A. (2006) Cooperative action of glutamate transporters and cystine/glutamate antiporter system X-c(-) protects from oxidative glutamate toxicity. J. Neurochem. 98, 916-925.   DOI
24 Li, J. P., Liang, Z. M. and Yuan, Z. (2007) Triterpenoid saponins and anti-inflammatory activity of Codonopsis lanceolata. Pharmazie. 62, 463-466.
25 Moncada, S. and Erusalimsky, J. D. (2002) Does nitric oxide modulate mitochondrial energy generation and apoptosis? Nat. Rev. Mol. Cell Biol. 3, 214-220.   DOI   ScienceOn
26 Murphy, T. H., Miyamoto, M., Sastre, A., Schnaar, R. L. and Coyle, J. T. (1989) Glutamate toxicity in neuronal cell line involves inhibition of cystine transport leading to oxidative stress. Neuron 2, 1547-1558.   DOI   ScienceOn
27 Gross, A., McDonnell, J. M. and Korsmeyer, J. S. (1999) BCL-2 family members and the mitochondria in apoptosis. Genes Dev. 13, 1899-1911.   DOI   ScienceOn
28 He, X., Zou, Y., Yoon, W. B., Park, S. J., Park, D. S. and Ahn, J. (2011) Effects of probiotic fermentation on the enhancement of biological and pharmacological activities of Codonopsis lanceolata extracted by high pressure treatment. J. Biosci. Bioeng. 112, 188-193.   DOI   ScienceOn
29 Choi, D. W. (1985) Glutamate neurotoxicity in cortical cell cultures is calcium dependent. Neurosci. Lett. 58, 293-297.   DOI   ScienceOn
30 Cho, J. Y., Kim, H. S., Kim, D. H., Yan, J. J., Suh, H. W. and Song, D. K. (2005) Inhibitory effects of long-term administration of ferulic acid on astrocyte activation induced by intracerebroventricular injection of beta-amyloid peptide (1-42) in mice. Prog. Neuropsychopharmacol. Biol. Psychiatry 29, 901-907.   DOI
31 Choi, D. W. (1988) Glutamate neurotoxicity and diseases of the nervous system. Neuron 1, 623-634.   DOI   ScienceOn
32 Conrad, M. and Sato, H. (2012) The oxidative stress-inducible cystine/ glutamate antiporter, system x(c)(-): cystine supplier and beyond. Amino Acids 42, 231-246.   DOI
33 Coyle, J. T. and Puttfarcken, P. (1993) Oxidative stress, glutamate, and neurodegenerative disorders. Science 262, 689-695.   DOI   ScienceOn
34 Crapper, D. R. and DeBoni, U. (1978) Brain aging and Alzheimer's disease. Can. Psychiatr. Assoc. j. 23, 229-233.
35 Deckwerth, T. L., Elliot, J. L., Knudson, C. M., Johnson, Jr. E. M., Snider, W. D. and Korsmeyer, S. J. (1996) Bax is required for neuronal death after trophic factor deprivation and during development. Neuron 17, 401-411.   DOI
36 Duchen, M. (2000) Mitochondria and calcium: from cell signaling to cell death. J. Physiol. 529, 57-68.   DOI   ScienceOn
37 Epand, R. F., Martinou, J. C., Montessuit, S., Epand, R. M. and Yip, C.M. (2002) Direct evidence for membrane pore formation by the apoptotic protein Bax. Biochem. Biophys. Res. Commun. 298, 744-749.   DOI   ScienceOn
38 Garthwaite, J. (1991) Glutamate, nitric oxide and cell-cell signalling in the nervous system. Trends Neurosci. 14, 60-67.   DOI   ScienceOn
39 Fukui, M., Song, J. H., Choi, J., Choi, H. J. and Zhu, B. T. (2009) Mechanism of glutamate-induced neurotoxicity in HT22 mouse hippocampal cells. Eur. J. Pharmacol. 617, 1-11.   DOI   ScienceOn
40 Gan, M., Lin, S., Zhang, Y., Zi, J., Song, W., Hu, J., Chen, N., Wang, L., Wang, X. and Shi, J. (2011) Liposoluble constituents from Iodes cirrhosa and their neuroprotective and potassium channel-blocking activity. Zhongguo Zhong Yao Za Zhi 36, 1183-1189.
41 Albrecht, P., Lewerenz, J., Dittmer, S., Noack, R., Maher, P. and Methner, A. (2010) Mechanisms of oxidative glutamate toxicity: the glutamate/cystine antiporter system xc- as a neuroprotective drug target. CNS Neurol. Disord. Drug Targets 9, 373-382.   DOI
42 Antonsson, B. (2004) Mitochondria and the Bcl-2 family proteins in apoptosis signaling pathways. Mol. Cell. Biochem. 256, 141-155.   DOI
43 Ban, J. Y., Nguyen, H. T., Lee, H. J., Cho, S. O., Ju, H. S., Kim, J. Y., Bae, K., Song, K. S. and Seong, Y. H. (2008) Neuroprotective properties of gallic acid from Sanguisorbae radix on amyloid beta protein (25--35)-induced toxicity in cultured rat cortical neurons. Biol. Pharm. Bull. 31, 149-153.   DOI   ScienceOn
44 Butterfield, D. A. and Pocernich, C. B. (2003) The glutamatergic system and Alzheimer's disease: therapeutic implications. CNS Drugs 17, 641-652.   DOI
45 Byeon, S. E., Choi, W. S., Hong, E. K., Lee, J., Rhee, M. H., Park, H. J. and Cho, J. Y. (2009) Inhibitory effect of saponin fraction from Codonopsis lanceolata on immune cell-mediated inflammatory responses. Arch. Pharm. Res. 32, 813-822.   DOI
46 Ghayur, M. N., Kazim, S. F., Rasheed, H., Khalid, A., Jumani, M. I., Choudhary, M. I. and Gilani, A. H. (2011) Identification of antiplatelet and acetylcholinesterase inhibitory constituents in betel nut. Zhong Xi Yi Jie He Xue Bao 9, 619-625.   DOI
47 Liu, J. Li, L. Suo, W. Z. (2009) HT22 hippocampal neuronal cell line possesses functional cholinergic properties. Life Sci. 84, 267-271.   DOI   ScienceOn
48 Wyllie, A. H., Kerr, J. F. and Currie, A. R. (1980) Cell death: the significance of apoptosis. Int. Rev. Cytol. 68, 251-306.   DOI
49 Randall, R. D. and Thayer, S. A. (1992) Glutamate-induced calcium transient triggers delayed calcium overload and neurotoxicity in rat hippocampal neurons. J. Neurosci. 12, 1882-1895.
50 Jung, I. H., Jang, S. E., Joh, E. H., Chung, J., Han, M. J. and Kim, D. H. (2012) Lancemaside A isolated from Codonopsis lanceolata and its metabolite echinocystic acid ameliorate scopolamine-induced memory and learning deficits in mice. Phytomedicine 20, 84-88.   DOI   ScienceOn