The dietary excitotoxins β-N-methylamino-L-alanine and β-N- oxalylamino-L-alanine induce necrotic- and apoptotic-like death of rat cerebellar granule cells

Journal of Neurochemistry

Volumn 69, Issue 4, 1997, Pages 1508-1518

  Staton, Penelope C ^a   Bristow, David R ^a,b  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b G38 Stopford Building   (United Kingdom)

Author keywords

Apoptosis; Cerebellar granule cells; Glutamate; Necrosis; N Methylamino L alanine; N Oxalylamino L alanine

Indexed keywords

2 AMINO 3 METHYLAMINOPROPIONIC ACID; 2 AMINO 5 PHOSPHONOVALERIC ACID; BETA (N OXYLAMINO)ALANINE; GLUTAMIC ACID; KYNURENIC ACID; NEUROTOXIN; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CEREBELLUM; CONTROLLED STUDY; DIETARY INTAKE; GRANULE CELL; NERVE CELL NECROSIS; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALIA;

EID: 0030984173     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1997.69041508.x     Document Type: Article

References (56)

1. Ankarcrona M., Dypbukt J. M., Bonfoco E., Zhivotovsky B., Orrenius S., Lipton S. A., and Nicotera P. (1995) Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15, 961-973.
2. Armstrong R. C., Aja T. J., Hoang K. D., Gaur S., Bai X., Alnemri E. S., Litwack G., Karanewsky D. S., Fritz L. C., and Tomaselli K. J. (1997) Activation of the CED3/ICE-related protease CPP32 in cerebellar granule neurons undergoing apoptosis but not necrosis. J. Neurosci. 17, 553-562.
3. Aronica E., Nicoletti F., Condorelli D. F., and Balazs R. (1993) Pharmacological characterization of metabotropic glutamate receptors in cultured cerebellar granule cells. Neurochem. Res. 18, 605-612.
4. Batistatou A. and Greene L. A. (1991) Aurintricarboxylic acid rescues PC12 cells and sympathetic neurons from cell death caused by nerve growth factor deprivation: correlation with suppression of endonuclease activity. J. Cell Biol. 115, 461-471.
5. Bonfoco E., Krainc D., Ankarcrona M., Nicotera P., and Lipton S. A. (1995) Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartale or nitric oxide/superoxide in cortical cell cultures. Proc. Nail. Acad. Sci. USA 92, 7162-7166.
6. Bortner C. D., Oldenburg N. B. E., and Cidlowski J. A. (1995) The role of DNA fragmentation in apoptosis. Trends Cell Biol. 5, 21-26.
7. A receptor α1 subunit protein in rat cerebellar granule cells. Br. J. Pharmacol. 118, 1103-1110.
8. Burgoyne R. D. and Cambray-Deakin M. A. (1988) The cellular neurobiology of neuronal development: the cerebellar granule cell. Brain Res. Rev. 13, 77-101.
9. Choi D.W. (1996) Ischemia-induced neuronal apoptosis. Curr. Opin. Neurobiol. 6, 667-672.
10. Choi D. W., Maulucci-Gedde M., and Kriegstein A. R. (1987) Glutamate neurotoxicity in cortical cell culture. J. Neurosci. 7, 357-368.
11. Chuang D.M., Gao X. M., and Paul S. M. (1992) N-Methyl-D-aspartate exposure blocks glutamate toxicity in cultured cerebellar granule cells. Mol. Pharmacol. 42, 210-216.
12. Clarke P. G. (1990) Developmental cell death: morphological diversity and multiple mechanisms. Anat. Embryol. (Berl.) 181, 195-213.
13. Cohen G. M., Sun X.-M., Snowden R. T., Dinsdale D., and Skilleter D. N. (1992) Key morphological features of apoptosis may occur in the absence of internucleosomal DNA fragmentation. Biochem. J. 286, 331-334.
14. Cohen J. J. (1991) Programmed cell death in the immune system. Adv. Immunol. 50, 55-85.
15. Copani A., Canonico P. L., Catania M. V., Aronica E., Bruno V., Ratti E., van Amsterdam F. T. M., Gaviragha G., and Nicoletti F. (1991) Interaction between β-methylamino-L-alanine (BMAA) and excitatory amino acid receptors in brain slice and neuronal cultures. Brain Res. 558, 79-86.
16. Copani A., Bruno V., Battaglia G., Leanza G., Pellitteri R., Russo A., Stanzani S., and Nicoletti F. (1995) Activation of metabotropic glutamate receptors protects cultured neurons against apoptosis induced by beta-amyloid peptide. Mol. Pharmacol. 47, 890-897.
17. Dessi F., Charriaut-Marlangue C., Khrestchatisky M., and Ben-Ari Y. (1993) Glutamate-induced neuronal death is not a programmed cell death in cerebellar culture. J. Neurochem. 60, 1953-1955.
18. D'Mello S. R., Galli C., Ciotti T., and Calissano P. (1993) Induction of apoptosis in cerebellar granule neurons by low potassium-inhibition of death by insulin-like growth factor-I and cAMP. Proc. Natl. Acad. Sci. USA 90, 10989-10993.
19. Duke R. C. and Cohen J. J. (1986) IL-2 addiction: withdrawal of growth factor activates a suicide program in dependent T cells. Cytokine Res. 5, 289-299.
20. Duncan M. V., Marini A. M., Watters R., Kopin I. I., and Markey S. P. (1992) Zinc, a neurotoxin to cultured neurons, contaminates cycad flour prepared by traditional Guamian methods. J. Neurosci. 12, 1523-1537.
21. Escargueil-BIanc I., Salvayre R., and Negre-Salvayre A. (1994) Necrosis and apoptosis induced by oxidized low density lipoproteins occur through two calcium-dependent pathways in lymphoblastoid cells. FASEB J. 8, 1075-1080.
22. Finiels F., Robert J.-J., Samolyk M.-L., Privat A., Mallet J., and Revah F. (1995) Induction of neuronal apoptosis by excitotoxins associated with long-lasting increase of 12-O-tetradeca-noylphorbol 13-acetate-responsive element-binding activity. J. Neurochem. 65, 1027-1034.
23. Gerschenson L. E. and Rotello R. J. (1992) Apoptosis: a different type of cell death. FASEB J. 6, 2450-2555.
24. Herón A., Pollard H., Dessi F., Moreau J., Lasbennes F., Ben-Ari Y., and Charriaut-Marlangue C. (1993) Regional variability in DNA fragmentation after global ischemia evidenced by combined histological and gel electrophoresis observations in rat brain. J. Neurochem. 61, 1973-1975.
25. Johnston G. A. R. (1973) Convulsions induced in 10-day-old rats by intraperitoneal injection of monosodium glutamate and related excitant amino acids. Biochem. Pharmacol. 22, 137-140.
26. Jones K. H. and Senft J. A. (1985) An improved method to determine cell viability by simultaneous staining with fluorescein diacetate-propidium iodide. J. Histochem. Cytochem. 33, 77-79.
27. Kure S., Tominaga T., Yoshimoto T., Tada K., and Narisawa K. (1991) Glutamate triggers internucleosomal DNA cleavage in neuronal cells. Biochem. Biophys. Res. Commun. 179, 39-45.
28. La Bella V., Alexianu M. E., Colom L. V., Ionescu A., Mohamed A. H., and Appel S. H. (1996) Apoptosis induced by β-N-oxalylamino-L-alanine on a motoneuron hybrid cell line. Neuroscience 70, 1039-1052.
29. Linnik M. D. (1995) Programmed cell death in cerebral ischaemia: therapeutic implications. CNS Drugs 3, 239-244.
30. Linnik M. D., Zobrist R. H., and Hatfield M. D. (1993) Evidence supporting a role for programmed cell death in focal cerebral ischemia in rats. Stroke 24, 2002-2009.
31. MacManus J. P., Buchan A. M., Hill I. E., and Preston E. (1993) Global ischemia can cause fragmentation indicative of apoptosis in rat brain. Neurosci. Lett. 164, 89-92.
32. MacManus J. P., Hill I. E., Huang Z. G., Rasquinha I., Xue D., and Buchan A. M. (1994) DNA damage consistent with apoptosis in transient focal ischemia in neocortex. Neuroreport 5, 493-496.
33. Miller T. M. and Johnson E. M. Jr. (1996) Metabolic and genetic analyses of apoptosis in potassium/serum-deprived rat cerebellar granule cells. J. Neurosci. 16, 7487-7495.
34. Montpied P., Weller M., and Paul S. M. ( 1993) N-Methyl-D-aspartate receptor agonists decrease protooncogene BCL-2 mRNA expression in cultured rat cerebellar granule neurons. Biochem. Biophys. Res. Commun. 195, 623-629.
35. Nunn P. B., Seelig M., Zagoren J. C., and Spencer P. S. (1987) Stereospecific acute neuronotoxicity of uncommon plant amino acids linked to human motor system diseases. Brain Res. 410, 375-379.
36. Olney J. W., Misra C. H., and Rhee V. (1976) Brain and retinal damage from the lathyrus excitotoxin, β-N-oxalyl-L-α,β-diaminopropionic acid (ODAP). Nature 264, 659-661.
37. Portera-Cailliau C., Hedreen J. C., Price D. L., and Koliatsos V. E. (1995) Evidence for apoptotic cell death in Huntington disease and excitotoxic animal models. J. Neurosci. 15, 3775-3787.
38. Ross S. M., Seelig M., and Spencer P. S. (1987) Specific antagonism of excitotoxic action of "uncommon" amino acids assayed in organotypic mouse cortical cultures. Brain Res. 425, 120-127.
39. Ross S. M., Roy D. N., and Spencer P. S. (1989) β-N-Oxalylamino-L-alanine action on glutamate receptors. J. Neurochem. 53, 710-715.
40. Samples S. D. and Dubinsky J. M. (1993) Aurintricarboxylic acid protects hippocampal neurons from glutamate excitotoxicity in vitro. J. Neurochem. 61, 382-385.
41. Schramm M., Eimerl S., and Costa E. (1990) Serum and depolarizing agents cause acute neurotoxicity in cultured cerebellar granule cells: role of the glutamate receptor responsive to N-methyl-D-aspartate. Proc. Natl. Acad. Sci. USA 87, 1193-1197.
42. Schwartzman R. A. and Cidlowski J. A. (1993) Apoptosis-the biochemistry and molecular biology of programmed cell death. Endocr. Rev. 14, 133-151.
43. Searle J., Kerr J. F. R., and Bishop C. J. (1982) Necrosis and apoptosis: distinct modes of cell death with fundamentally different significance. Pathol. Annu. 17, 229-259.
44. Seawright A. D., Brown A. D., Nolan C. C., and Kavanagh J. B. (1990) Selective degeneration of cerebellar cortical neurons caused by cycad neurotoxin β-methylaminoalanine (L-BMAA) in rats. Neuropathol. Appl. Neurobiol. 16, 153-169.
45. Siman R. and Card J. P. (1988) Excitatory amino acid neurotoxicity in hippocampal slice preparation. Neuroscience 26, 433-447.
46. Spencer P. S., Ludolph A. C., Dwivedi M. P., Roy D. N., Hugon J., and Schambure H. H. (1986) Lathyrism: evidence for a role of the neuroexcitatory amino acid BOAA. Lancet 2, 1066-1067.
47. Spencer P. S., Nunn P. B., Hugon J., Ludolph A. C., Ross S. M., Roy D. N., and Robertson R. C. (1987) Guam amyotrophic lateral sclerosis-parkinsonism-dementia linked to a plant excitant neurotoxin. Science 237, 517-522.
48. Staton P. C. and Bristow D. R. (1996) Mechanisms of β-methylamino-L-alanine (BMAA)- and β-oxalylamino-L-alanine (BOAA)-induced death in rat cerebellar granule cells. (Abstr.) Br. J. Pharmacol. 117, 189P.
49. van Lookeren Campagne M., Lucassen P. J., Vermeulen J. P., and Balazs R. (1995) NMDA and kainate induce internucleosomal DNA cleavage associated with both apoptotic and necrotic cell death in the neonatal rat brain. Eur. J. Neurosci. 7, 1627-1640.
50. Weiss J. H. and Choi D. W. (1988) Beta-N-methylamino-L-alanine neurotoxicity: requirement for bicarbonate as a cofactor. Science 241, 973-975.
51. Weiss J. H., Koh J.-Y., and Choi D. W. (1989) Neurotoxicity of β-N-methylamino-L-alanine (BMAA) and β-N-oxalylamino-L-alanine (BOAA) on cultured cortical neurons. Brain Res. 497, 64-71.
52. Willis C. L., Meldrum B. S., Nunn P. B., Anderton B. H., and Leigh P. N. (1993) Neuronal damage induced by beta-N-oxalylamino-L-alanine, in the rat hippocampus, can be prevented by a non-NMDA antagonist, 2,3-dihydroxy-6-nitro-7-sulfamoylbenzo(F)quinoxaline. Brain Res. 627, 55-62.
53. Willis C. L., Meldrum B. S., Nunn P. B., Anderton B. H., and Leigh P. N. (1994) Neuroprotective effect of free radical scavengers on beta-N-oxalylamino-L-alanine (BOAA)-induced neuronal damage in rat hippocampus. Neurosci. Lett. 182, 159-162.
54. Wyllie A. H. (1980) Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284, 555-556.
55. Yan B.-M., Ni B., Weller M., Wood K. A., and Paul S. M. (1994) Depolarisation of glutamate receptor activation blocks apoptotic cell death of cultured cerebellar granule neurons. Brain Res. 656, 43-51.
56. Zeevalk G. D., Schoepp D., and Nicklas W. J. (1995) Excitotoxicity at both NMDA and non-NMDA glutamate receptors is antagonized by aurintricarboxylic acid: evidence for differing mechanisms of action. J. Neurochem. 64, 1749-1758.