Myristicae Semen Extract Protects Excitotoxicity in Cultured Neuronal Cells

  • Kim, Ji-Ye (College of Veterinary Medicine & Research Institute of Veterinary Medicine, Chungbuk Natl. Univ.) ;
  • Ban, Ju-Yeon (College of Veterinary Medicine & Research Institute of Veterinary Medicine, Chungbuk Natl. Univ.) ;
  • Bang, Kyong-Hwan (National Institute of Crop Sci., RDA) ;
  • Seong, Nak-Sul (National Institute of Crop Sci., RDA) ;
  • Song, Kyung-Sik (College of Agriculture & Life-Sci., Kyungpook Natl. Univ.) ;
  • Bae, Ki-Whan (College of Pharmacy, Chungnam Natl. Univ.) ;
  • Seong, Yeon-Hee (College of Veterinary Medicine & Research Institute of Veterinary Medicine, Chungbuk Natl. Univ.)
  • Published : 2004.11.01

Abstract

Myristica fragrans seed from Myristica fragrans Houtt (Myristicaceae) has various pharmacological activities peripherally and centrally. The present study aims to investigate the effect of the methanol extract of Myristica fragrans seed (MF) on kainic acid (KA)-induced neurotoxicity in primary cultured rat cerebellar granule neuron. MF, over a concentration range of 0.05 to $5\;{\mu}g/ml$ inhibited KA $(500\;{\mu}M)-induced$ neuronal cell death, which was measured by trypan blue exclusion test and 3-[4,5-dimethylthiazol-2-yl]-2,5-diphenyl-tetrazolium bromide (MTT) assay. MF $(0.5\;{mu}g/ml)$ inhibited glutamate release into medium induced by KA $(500\;{\mu}M)$, which was measured by HPLC. Pretreatment of MF $(0.5\;{mu}g/ml)$ inhibited KA $(500\;{\mu}M)-induced$ elevation of cytosolic calcium concentration $([Ca^{2+}]_c)$, which was measured by a fluorescent dye, Fura 2-AM, and generation of reactive oxygen species (ROS). These results suggest that MF prevents KA-induced neuronal cell damage in vitro.

Keywords

References

  1. Arias C, Montiel T, Rapia R (1990) Transmitter release in hippocampal slices from rats with limbic seizures produced by systemic administration of kainic acid. Neurochem. Res. 15:641-646 https://doi.org/10.1007/BF00973756
  2. Baltrons MA, Saadoun S, Agullo L, Garcia A (1997) Regulation by calcium of the nitric oxide/cyclic GMP system in cerebellar granule cells and astroglia in culture. J. Neurosci. Res. 49:333-341 https://doi.org/10.1002/(SICI)1097-4547(19970801)49:3<333::AID-JNR8>3.0.CO;2-D
  3. Bardoul M, Drian MJ, Knig N (1998) Modulation of intracellular calcium in early neural cells by non-NMDA ionotropec glutamate receptors. Perspect. Dev. Neurobiol. 5:353-371
  4. Ben-Ali Y (1985) Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy, Neuroscience 14:375-403 https://doi.org/10.1016/0306-4522(85)90299-4
  5. Berridge MV, Tan AS (1993) Characterization of the cellular reduction of 3-(4,5-dimethylthiazol-2,5-diphenyltetrazolium bromide (MTT): subcellular localization, substrate dependence, and involvement of mitochondrial electron transport in MTT reduction. Arch. Biochem. Biophys. 303:474-482 https://doi.org/10.1006/abbi.1993.1311
  6. Blanchard BJ, Konopka G, Russel M, Ingram VM (1997) Mechanism and prevention of neurotoxicity caused by $\beta-amyloid peptides: relation to Alzheimer's disease. Brain Res. 776:40-50 https://doi.org/10.1016/S0006-8993(97)01003-2
  7. Bondy SC, Lee DK (1993) Oxidative stress induced by glutamate receptor agonists. Brain Res. 610:229-233 https://doi.org/10.1016/0006-8993(93)91405-H
  8. Brenner N, Frank OS, Knight E (1993) Chronic nutmeg psychosis.J. R. Soc. Med. 86:179-180
  9. Brorson JR, Manzolillo PA, Miller RJ (1994) $Ca^{2+} entry via AMPAlKA receptor and excitotoxicity in cultured cerebellar Purkinje cells.J. Neurosci. 14:187-197
  10. Carroll FY, Cheung NS, Beart PM (1998) Investigations of nonNMDA receptor-induced toxicity in serum-free antioxidantrich primary cultures of murine cerebellar granule cells. Neurochem. Int. 33:23-28 https://doi.org/10.1016/S0197-0186(05)80004-X
  11. Choi DW (1985) Glutamate neurotoxicity in cortical cell culture is calcium dependent. Neurosci. Letts. 58:293-297 https://doi.org/10.1016/0304-3940(85)90069-2
  12. Choi DW (1988) Glutamate neurotoxicity and disease of nervous system. Neuron 1:623-634 https://doi.org/10.1016/0896-6273(88)90162-6
  13. Choi DW (1992) Excitotoxic cell death. J. Neurobiol. 23:12611276 https://doi.org/10.1002/neu.480230915
  14. Coyle JT, Puttfarcken P (1993) Oxidative stress, glutamate and neurodegenerative disorders. Science 262:689-694 https://doi.org/10.1126/science.7901908
  15. Duffy S, MacViar BA (1996) In vitro ischemia promotes calcium influx and intracellular calcium release in hippocampal astrocytes. J. Neurosci. 16:71-81
  16. Dugan LL, Sensi SL, Canzoniero LM, Handran SD, Rothman SM, Lin TS, Goldberg MP, Choi DW (1995) Mithchondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl D-aspartate. J. Neurosci. 15:6377-6388 https://doi.org/10.1523/JNEUROSCI.15-10-06377.1995
  17. Dutrait N, Culcasi M, Cazevieille C, Pietri S, Tordo P, Bonne C, Muller A (1995) Calcium-dependent free radical generation in cultured retinal neurons injured by kainate. Neurosci. Lett. 198:13-16 https://doi.org/10.1016/0304-3940(95)11948-V
  18. Dykens JA (1994) Isolated cerebral and cerebellar mitochondria produce free radicals when exposed to elevated $Ca^{2+} and $Na^+: implications for neurodegeneration. J. Neurochem. 63:584-591 https://doi.org/10.1046/j.1471-4159.1994.63020584.x
  19. Ellison DW, Beal MF, Martin JB (1987) Amino acid neurotransmitters in postmortem human brain analyzed by high performance liquid chromatography with electrochemical detection. J. Neurosci. 19:305-315
  20. Evans WC (1996) Treese and Evans'Pharmcognosy. 14th ed. Singapore: Harcourt Brace & Co. Asia, p. 273-275
  21. Giusti P, Franceschini D, Petrone D, Manev H, Floreani M (1996) In vitro and in vivo protection against kainate-induced excitotoxicity by melatonin. J. Pineal Res. 20:226-231 https://doi.org/10.1111/j.1600-079X.1996.tb00263.x
  22. Gunasekar PG, Sun PW, Kanthasamy AG, Borowitz JL, Isom GE (1996) Cyanide-induced neurotoxicity involves nitric oxide and reactive oxygen species generation after N-Methyl-Daspartate receptor activation. J. Pharmacol. Exp. Ther. 277:150-155
  23. Hellier JL, Patrylo PR, Buckmaster PS, Dudek FE (1998) Recurrent spontaneous motor seizures after repeated lowdose systemic treatment with kainate: assessment of a rat model of temporal lobe epilepsy. Epilepsy Res. 31:73-84 https://doi.org/10.1016/S0920-1211(98)00017-5
  24. Huang KC (1999) The Pharmacology of Chinese herbs. CRC press LLC, Florida, USA. p. 243
  25. Jensen JB, Schousboe A, Pickering DS (1998) AMPA receptor mediated excitotoxicity in neocortical neurons is developmentally regulated and dependent upon receptor desensitization. Neurochem. Int. 32:505-513 https://doi.org/10.1016/S0197-0186(97)00130-7
  26. Koh SB, Ban JY, Lee BY, Seong YH (2003) Protective effects of fangchinoline and tetrandrine on hydrogen peroxide-induced oxidative neuronal cell damage in cultured rat cerebellar granule cells. Planta Medica 69:506-512 https://doi.org/10.1055/s-2003-40647
  27. Larm JA, Beart PM, Cheung NS (1997) Neurotoxin domoic acid produces cytotoxicity via kainate- and AMPA-sensitive receptors in cultured cortical neurons. Neurochem. Int. 31:677-682 https://doi.org/10.1016/S0197-0186(97)00030-2
  28. Larm JA, Cheung NS, Beart PM (1996) (S)-5-fluorowillardiinmediated neurotoxicity in cultured murine cortical neurons occurs via AMPA and kainate receptors. Eur. J. Pharm. 314:249-254 https://doi.org/10.1016/S0014-2999(96)00633-4
  29. Lesort M, Esclaire F, Yardin C, Hugon J (1997) NMDA induces apoptosis and necrosis in neuronal cultures. Increased APP immunoreactivity is linked to apoptotic cells. Neurosci. Letts. 221 :213-216 https://doi.org/10.1016/S0304-3940(96)13310-3
  30. Liang LP, Patel M (2004) Mitochondrial oxidative stress and increased seizure susceptibility in $SOd^{2-}/^+ mice. Free Radic. Biol. Med. 36:542-554 https://doi.org/10.1016/j.freeradbiomed.2003.11.029
  31. Mei JM, Chi WM, Trump BF, Eccles CU (1996) Involvement of nitric oxide in the deregulation of cytosolic calcium in cerebellar neurons during combined glucose-oxygen deprivation. Mol. Chern. Neuropathol. 27:155-166 https://doi.org/10.1007/BF02815091
  32. Merck Index (1989) 11th Edition; 999-1000
  33. Milatovic D, Gupta RC, Dettbam WD (2002) Involvement of nitric oxide in kainic acid-induced excitotoxicity in rat brain. Brain Res. 957:330-337 https://doi.org/10.1016/S0006-8993(02)03669-7
  34. Nadkami KM (1976) Indian Materia Medica vol. 1. Popular Prakashan. Bombay p. 830-834
  35. Nicholls DG, Budd SL (2000) Mitochondria and neuronal survival. physiol. Rev. 80:315-360 https://doi.org/10.1152/physrev.2000.80.1.315
  36. Pereira CF, Oliveira CR (2000) Oxidative glutamate toxicity involves mitochondrial dysfunction and perturbation of intracellular $Ca^{2+} homeostasis. Neurosci. Res. 37:227-236 https://doi.org/10.1016/S0168-0102(00)00124-3
  37. Ram A, Lauria P, Gupta R, Sharma VN (1996) Hypolipidaemic effect of Myristica fragrans fruit extract in rabbits. J. Ethnopharmacol. 55:49-53 https://doi.org/10.1016/S0378-8741(96)01473-0
  38. Regan RF, Choi DW (1991) Glutamate neurotoxicity in spinal cord cell culture. Neuroscience 43:585-591 https://doi.org/10.1016/0306-4522(91)90317-H
  39. Rothman SM, Olney JW (1986) Glutamate and the phathophysiology of hypoxic-ischemic brain damage. Ann. Neurol. 19:105-111 https://doi.org/10.1002/ana.410190202
  40. Sierra-Paredes G, GaIn-Valiente J, Vazquez-Illanes MD, AguilarVeiga E, Sierra-Marcuo G (2000) Effect of ionotropic glutamate receptors antagonists on the modifications in extracellular glutamate and aspartate levels during picrotoxin seizures: a microdialysis study in freely moving rats. Neurochem. Int. 37:377-386 https://doi.org/10.1016/S0197-0186(00)00038-3
  41. Simonian NA, Getz RL, Leveque JC, Konrake C, Coyle]T (1996) Kainic acid induces apoptosis in neurons. Neurosci. 75:1047-1055 https://doi.org/10.1016/0306-4522(96)00326-0
  42. Sonavane GS, Sarveiya VP, Kasture VS, Kasture SB (2002) Anxiogenic activity of Myristica fragrans seeds. Pharmacol. Biochem. Behav. 71:247-252
  43. Sperk G (1994) Kainic acid seizures in the rat. Prog. Neurobiol 42:1-32 https://doi.org/10.1016/0301-0082(94)90019-1
  44. Tecoma ES, Monyer H, Goldberg MP, Choi DW (1989) Traumatic neuronal injury in vitro is attenuated by NMDA antagonists. Neuron 2:1541-1545 https://doi.org/10.1016/0896-6273(89)90042-1
  45. Van Gils C, Cox PA (1994) Ethnobotany of nutmeg in the spice islands. J. Ethnopharmacol. 42:117-124 https://doi.org/10.1016/0378-8741(94)90105-8
  46. Van Vliet BJ, Sebben M, Dumuis A, Gabrion J, Bockaert J, Pin JP (1989) Endogenous amino acid release from cultured cerebellar neuronal cells: Effect of tetanus toxin on glutamate release. J. Neurochem. 52:1229-1230 https://doi.org/10.1111/j.1471-4159.1989.tb01870.x
  47. Weiss JH, Hartley DM, Koh J, Choi DW (1990) The calcium channel blocker nifedipine attenuates slow excitatory amino acid neurotoxicity. Science 247:1474-1477 https://doi.org/10.1126/science.2157282
  48. Weiss JH, Sensi SL (2000) $Ca^{2+}-Zn^{2+} permeable AMPA or kainite receptors: possible key factors in selective neurodegeneration, Trends Neurosci. 23:365-371 https://doi.org/10.1016/S0166-2236(00)01610-6
  49. Whit RJ, Reynolds IJ (1996) Mitochondrial depolarization in glutamate-stimulated neurons: an early signal specific to excitotoxic exposure. J. Neurosci. 16:5688-5697