Regulation of glutamate level in rat brain through activation of glutamate dehydrogenase by Corydalis ternata

Lee, Kwan-Ho;Huh, Jae-Wan;Choi, Myung-Min;Yoon, Seung-Yong;Yang, Seung-Ju;Hong, Hea-Nam;Cho, Sung-Woo

  • Published : 2005.08.31

Abstract

When treated with protopine and alkalized extracts of the tuber of Corydalis ternata for one year, significant decrease in glutamate level and increase in glutamate dehydrogenase (GDH) activity was observed in rat brains. The expression of GDH between the two groups remained unchanged as determined by Western and Northern blot analysis, suggesting a post-translational regulation of GDH activity in alkalized extracts treated rat brains. The stimulatory effects of alkalized extracts and pro - topine on the GDH activity was further examined in vitro with two types of human GDH isozymes, hGDH1 (house-keeping GDH) and hGDH2 (nerve-specific GDH). Alkalized extracts and protopine activated the human GDH isozymes up to 4.8-fold. hGDH2 (nervespecific GDH) was more sensitively affected by 1 mM ADP than hGDH1 (house-keeping GDH) on the activation by alkalized extracts. Studies with cassette mutagenesis at ADP-binding site showed that hGDH2 was more sensitively regulated by ADP than hGDH1 on the activation by Corydalis ternata. Our results suggest that prolonged exposure to Corydalis ternata may be one of the ways to regulate glutamate concentration in brain through the activation of GDH.

Keywords

References

  1. Aoki C, Milner TA, Sheu K-FR, Blass JP, Pickel VM. Regional distribution of astrocytes with intense immunoreactivity for glutamate dehydrogenase in rat brain: implications for neuron-glia interactions in glutamate transmission. J Neurosci 1987; 7:2214-31
  2. Bailey J, Bell ET, Bell JE. Regulation of bovine glutamate dehydrogenase. J Biol Chem 1982;257:5579-83
  3. Burki F, Kaessmann H. Birth and adaptive evolution of a hominoid gene that supports high neurotransmitter flux. Nature Genet 2004;36:1061-3 https://doi.org/10.1038/ng1431
  4. Chang C-K, Chueh FY, Hsieh MT, Lin MT. The neuroprotective effect of DL-tetrahydropalmatine in rat heatstroke. Neurosci Lett 1999;267:109-12 https://doi.org/10.1016/S0304-3940(99)00322-5
  5. Chang C-K, Lin M-T. DL-Tetrahydropalmatine may act through inhibition of amygdaloid release of dopamine to inhibit an epileptic attack in rats. Neurosci Lett 2001;307: 163-6 https://doi.org/10.1016/S0304-3940(01)01962-0
  6. Cho S-W, Yoon H-Y, Ahn J-Y, Lee E-Y, Lee J. Cassette mutagenesis of lysine 130 of human glutamate dehydrogenase: An essential residue in catalysis. Eur J Biochem 2001;268: 3205-13 https://doi.org/10.1046/j.1432-1327.2001.02209.x
  7. Choi SY, Hong JW, Song M-S, Jeon SG, Bahn JH, Lee BY, Ahn J-Y, Cho S-W. Different antigenic reactivities of bovine brain glutamate dehydrogenase isoproteins. J Neurochem 1999;72: 2162-9 https://doi.org/10.1046/j.1471-4159.1999.0722162.x
  8. Heinrikson RL, Meredith SC. Amino acid analysis by reverse- phase high-performance liquid chromatography: precolumn derivatization with phenylisothiocyanate. Anal Biochem 1984; 136:65-74 https://doi.org/10.1016/0003-2697(84)90307-5
  9. Hussain MH, Zannis VI, Plaitakis A. Characterization of glutamate dehydrogenase isoproteins purified from the cerebellum of normal subjects and patients with degenerative neurological disorders and from human neoplastic cell lines. J Biol Chem 1989;264:20730-5
  10. Ito C, Itoigawa M, Tokuda H, Kuchide M, Nishino H, Furukawa H. Chemopreventive activity of isoquinoline alkaloids from Corydalis plants. Planta Med 2001;67;473-5 https://doi.org/10.1055/s-2001-15815
  11. Janbaz KH, Saeed SA, Gilani AH. An assessment of the potential of protopine to inhibit microsomal drug metabolising enzymes and prevent chemical-induced hepatotoxicity in rodents. Pharmacol Res 1998;38:215-9 https://doi.org/10.1006/phrs.1998.0353
  12. Jang SH, Kim AY, Bahn JH, Eum WS, Kim DW, Park J, Lee KS, Kang T-C, Won MH, Kang JH, Kwon O-S, Yoon H-Y, Lee E-Y, Cho S-W, Choi SY. Human glutamate dehydrogenase is immunologically distinct from other mammalian orthologues. Exp Mol Med 2003;35:249-56
  13. Kardos J, Blasko G, Simonyi M. Enhancement of gammaaminobutyric acid receptor binding by protopine-type alkaloids. Arzneimittelforschung Drug Res 1986;36:939-40
  14. Kim S, Hwang S, Jang Y, Park M, Markelonis G, Oh T, Kim YC. Protopine from Corydalis ternata has anticholinesterase and antiamnesic activities. Plant Med 1999;65:218-21 https://doi.org/10.1055/s-1999-13983
  15. Kim Y-S, Jhon D-Y, Lee K-Y. Involvement of ROS and JNK1 in selenite-induced apoptosis in Chang liver cells. Exp Mol Med 2004;36:157-164
  16. Ko FN, Wu TS, Lu ST, Wu YC, Huang TF, Teng CM. $Ca^{2+-}$channel blockade in rat thoracic aorta by protopine isolated from Corydalis tubers. Jpn J Pharmacol 1992;58:1-9 https://doi.org/10.1254/jjp.58.1
  17. Kubo M, Matsuda H, Tokuoka K, Ma S, Shiomoto H. Antiinflammatory activities of methanolic extract and alkyalodal components from Corydalis tuber. Biol Oharma Bull 1994; 17:262-5
  18. Lee E-Y, Yoon HY, Ahn J-Y, Choi SY, Cho S-W. Identification of GTP binding site of human glutamate dehydrogenase using cassette mutagenesis and photoaffinity labeling. J Biol Chem 2001;276:47930-6
  19. Liu GG, Algeris A, Garattini S. DL-Tetrahydropalmatine as a monoamine depletor. Arch Int Pharmacodyn Ther 1982;258: 39-50
  20. Mathern GW, Mendoza D, Lozada A, Pretorius JK, Dehnes Y, Danbolt NC, Nelson, JP, Leite L. Hippocampal GABA and glutamate transporter immunoreactivity in patients with temporal lobe epilepsy. Neurology 1999;52:453–72
  21. Matsuda H, Shiomoto H, Namba K, Kubo M. Effects of protopine on blood platelet aggregation; 1. Plant Med 1988;54:498-501 https://doi.org/10.1055/s-2006-962528
  22. Matthews CC, Zielke HR, Wollack JB, Fishman PS. Enzymatic degradation protects neurons from glutamate excitotoxicity. J Neurochem 2000;75:1045-52 https://doi.org/10.1046/j.1471-4159.2000.0751045.x
  23. Mavrothalassitis G, Tzimagiorgis G, Mitsialis A, Zannis VI, Plaitakis A, Papamatheakis J, Moschonas NK. Isolation and characterization of cDNA clones encoding human liver glutamate dehydrogenase : evidence for a small gene family. Proc Natl Acad Sci USA 1988;85:3494-8 https://doi.org/10.1073/pnas.85.10.3494
  24. Plaitakis A, Berl S, Yahr MD. Abnormal glutamate metabolism in an adult-onset degenerative neurological disorder. Science 1982;216:193-6 https://doi.org/10.1126/science.6121377
  25. Plaitakis A, Shashidharan P. Glutamate transport and metabolism in dopaminergic neurons of substantia nigra: implications for the pathogenesis of Parkinson's disease. J Neurol 2000;247(suppl):II25-35
  26. Shashidharan P, Michaelidis TM, Robakis NK, Kresovali A, Papamatheakis J, Pliatakis A. Novel human glutamate dehydrogenase expressed in neural and testicular tissues and encoded by an X-linked intronless gene. J Biol Chem 1994;269:16971-6
  27. Song LS, Ren GJ, Chen ZL, Chen ZH, Zhou ZN, Cheng H. Electrophysiological effects of protopine in cardiac myocytes: inhibition of multiple cation channel currents. Br J Pharmacol 2000;129:893-900 https://doi.org/10.1038/sj.bjp.0703132
  28. Tanaka T, Metori K, Mineo S, Hirotani M, Furuga T, Kobayashi S. Inhibitory effects of berberine-type alkaloids on elastase. Plant Med 1993;59:200-2 https://doi.org/10.1055/s-2006-959651
  29. Ustunes L, Laekeman GM, Gozler B, Vlietinck AJ, Ozer A, Herman AG. In vitro study of the anticholinergic and antihistaminic activities of protopine and some derivatives. J Nat Prod 1988;51:1021-2 https://doi.org/10.1021/np50059a043
  30. Yang S-J, Huh J-W, Hong H-N, Kim TU, Cho S-W. Important role of Ser443 in different thermal stability of human glutamate dehydrogenase isozymes. FEBS Lett 2004;562: 59-64 https://doi.org/10.1016/S0014-5793(04)00183-8
  31. Yoon H-Y, Cho EH, Kwon HY, Choi SY, Cho, S-W. Importance of Glutamate-279 for the Coenzyme Binding of Human Glutamate Dehydrogenase. J Biol Chem 2002a; 277:41448-54 https://doi.org/10.1074/jbc.M208208200
  32. Yoon H-Y, Lee E-Y, Cho S-W. Cassette mutagenesis and photoaffinity labeling of adenine binding domain of ADP regulatory site within human glutamate dehydrogenase. Biochemistry 2002b;41:6817-23 https://doi.org/10.1021/bi0121757