Excitotoxic death of a subset of embryonic rat motor neurons in vitro

Journal of Neurochemistry

Volumn 72, Issue 2, 1999, Pages 500-513

  Fryer, Hugh J L ^a   Knox, Ronald J ^a   Strittmatter, Stephen M ^a   Kalb, Robert G ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Ca2+ imaging; Ca2+ dependent cell death; Cell culture; Excitotoxicity; Ionotropic glutamate receptors; L type Ca2+ channels; Motor neurons

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; CALCIUM CHANNEL; CALCIUM ION; DIZOCILPINE; EXCITOTOXIN; GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR AGONIST; GLUTAMATE RECEPTOR ANTAGONIST; GLUTAMIC ACID; GLUTAMINE; GLYCINE; KAINIC ACID; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR STIMULATING AGENT; NIFEDIPINE; POTASSIUM ION;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; IN VITRO STUDY; NERVE CELL CULTURE; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD MOTONEURON;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; CALCIUM; CALCIUM CHANNELS; CALCIUM CHANNELS, L-TYPE; CELL CULTURE TECHNIQUES; CELL DEATH; CELLS, CULTURED; DIZOCILPINE MALEATE; DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; GLUTAMIC ACID; GLUTAMINE; GLYCINE; KAINIC ACID; MEMBRANE POTENTIALS; MOTOR NEURONS; N-METHYLASPARTATE; NERVE TISSUE PROTEINS; NEUROTOXINS; POTASSIUM; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; RECEPTORS, KAINIC ACID; RECEPTORS, N-METHYL-D-ASPARTATE; SPINAL CORD;

EID: 0032924609     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1999.0720500.x     Document Type: Article

References (75)

1. Abele A. E., Scholz K. P., Scholz W. K., and Miller R. J. (1990) Excitotoxicity induced by enhanced excitatory neurotransmission in cultured hippocampal pyramidal neurons. Neuron 2, 413-419.
2. Bading H., Ginty D. D., and Greenberg M. E. (1993) Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways. Science 260, 181-186.
3. Blahos J. and Wenthold R. J. (1996) Relationship between N-methyl-D-aspartate receptor NR1 splice variants and NR2 subunits. J. Biol. Chem. 271, 15669-15674.
4. 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-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc. Natl. Acad. Sci. USA 92, 7162-7166.
5. 2+ entry via AMPA/kainate receptors and excitotoxicity in cultured cerebellar Purkinje cells. J. Neurosci. 14, 187-197.
6. Brorson J. R., Manzolillo P. A., Gibbons S. J., and Miller R. J. (1995) AMPA receptor desensitization predicts the selective vulnerability of cerebellar Purkinje cells to excitotoxicity. J. Neurosci. 15, 4515-4524.
7. Bruning G. and Mayer B. (1996) Prenatal development of nitric oxide synthase in the mouse spinal cord. Neurosci. Lett. 202, 189-192.
8. Calderó J., Ciutat D., Lladó J., Castán E., Oppenheim R. W. and Esquerda J. E. (1997) Effects of excitatory amino acids on neuromuscular development in the chick embryo. J. Comp. Neurol. 387, 73-95.
9. Camu W. and Henderson C. E. (1992) Purification of embryonic rat motoneurons by panning on a monoclonal antibody to the low-affinity NGF receptor. J. Neurosci. Methods 44, 59-70.
10. Camu W. and Henderson C. E. (1994) Rapid purification of embryonic rat motoneurons: an in vitro model for studying MND/ALS pathologies. J. Neurol Sci. 124, 73-74.
11. 2+ dependent. Neuroreport 6, 945-948.
12. Carriedo S. G., Yin H. Z., and Weiss J. H. (1996) Motor neurons are selectively vulnerable to AMPA/kainate receptor-mediated injury in vitro. J. Neurosci. 16, 4069-4079.
13. Choi D. W. (1987) Ionic dependence of glutamate neurotoxicity. J. Neurosci. 7, 369-379.
14. Choi D. W. (1988) Glutamate neurotoxicity and diseases of the nervous system. Neuron I, 623-634.
15. Choi D. W. (1990) The role of glutamate neurotoxicity in hypoxicischemic neuronal death. Annu. Rev. Neurosci. 13, 171-182.
16. Choi D. W. (1995) Calcium: still center-stage in hypoxic-ischemic neuronal death. Trends Neurosci. 18, 58-60.
17. Choi D. W., Maulucci-Gedde M. A., and Kriegstein A. R. (1987) Glutamate neurotoxicity in cortical cell cultures. J. Neurosci. 7, 357-368.
18. Ciutat D., Esquerda J. E., and Calderó J. (1995) Evidence for calcium regulation of spinal cord motoneuron death in the chick embryo in vivo. Dev. Brain Res. 86, 167-179.
19. Curthoys N. P. and Watford M. (1993) Regulation of glutaminase activity and glutamine metabolism. Annu. Rev. Nutr. 15, 133-159.
20. Dawson V. L. and Dawson T. M. (1996) Nitric oxide neurotoxicity. J. Chem. Neuroanat. 10, 179-190.
21. Dawson V. L., Dawson T. M., London E. D., Bredt D. S., and Snyder S. H. (1991) Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc. Natl. Acad. Sci. USA 88, 6368-6371.
22. Dawson V. L., Dawson T. M., Bartley D. A., Uhl G. R., and Snyder S. H. (1993) Mechanisms of nitric oxide-mediated neurotoxicity in primary brain cell cultures. J. Neurosci. 13, 2651-2661.
23. Ericson J., Thor S., Edlund T., Jessell T. M., and Yamada T. (1992) Early stages of motor neuron differentiation revealed by expression of homeobox gene Islet-1. Science 256, 1555-1560.
24. Estevez A. G., Stutzmann J.-M., and Barbeito L. (1995) Protective effect of riluzole on excitatory amino acid-mediated neurotoxicity in motoneuron-enriched cultures. Eur. J. Pharmacol. 280, 47-53.
25. Flanagan A. E. H. (1974) Differentiation and degeneration in the motor horn of the fetal mouse. J. Morphol. 129, 281-306.
26. Ghosh A., Carnahan J., and Greenberg M. E. (1994) Requirement for BDNF in activity-dependent survival of cortical neurons. Science 263, 1618-1623.
27. Grynkiewicz G., Poenie M., and Tsien R. Y. (1985) A new generation of calcium indicators with greatly improved fluorescent properties. J. Biol. Chem. 260, 3440-3448.
28. 2+ accumulation in cortical cell culture correlates with subsequent neuronal degeneration. J. Neurosci. 13, 1993-2000.
29. Henderson C. E., Camu W., Mettling C., Gouin A., Poulsen K., Karihaloo M., Rullamas J., Evans T., McMahan S. B., Armanini M. P., Berkemeier L., Philips H. S., and Rosenthal A. (1993) Neurotrophins promote motor neuron survival and are present in embryonic limb bud. Nature 363, 266-270.
30. Hivert B., Bouhanna S., Diochot S., Camu W., Dayanithi G., Henderson C. E., and Valmier J. (1995) Embryonic rat motoneurons express a functional P-type voltage-dependent calcium channel. Int. J. Dev. Neurosci. 13, 429-436.
31. Hory-Lee F. and Frank E. (1995) The nicotinic blocking agents d-tubocurare and α-bungarotoxin save motoneurons from naturally occurring death in the absence of neuromuscular blockade. J. Neurosci. 15, 6453-6460.
32. Hugon J., Vallat J. M., Spencer P. S., Leboutet M. J., and Barthe D. (1989) Kainic acid induces early and delayed degenerative neuronal changes in at spinal cord. Neurosci. Lett. 104, 258-262.
33. Jakowec M. W., Fox A. J., Martin L. J., and Kalb R. G. (1995) Quantitative and qualitative changes in AMPA receptor expression during spinal cord development. Neuroscience 67, 893-907.
34. Johnson J. W. and Ascher P. (1987) Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325, 529-531.
35. Kalb R. G. and Agostini J. (1993) Molecular evidence for nitric oxide-mediated motor neuron development. Neuroscience 57, 1-8.
36. Kato K., Puttfarcken P. S., Lyons W. E., and Coyle J. T. (1991) Developmental time course and ionic dependence of kainate-mediated toxicity in rat cerebellar granule cell cultures. J. Pharmacol. Exp. Ther. 256, 402-411.
37. 2+ release in peptidergic neurons of Aplysia californica. J. Physiol. (Lond.) 494, 627-639.
38. Koh J.-Y., Goldberg M. P., Hartley D. M., and Choi D. W. (1990) Non-NMDA receptor-mediated neurotoxicity in cortical cultures. J. Neurosci. 10, 693-705.
39. Kwak S. and Nakamura R. (1995) Acute and late neurotoxicity in the rat spinal cord in vivo induced by glutamate receptor agonists J. Neurol. Sci. 129, 99-103.
40. Lees G. J. (1993) Contributory mechanisms in the causation of neurodegenerative disorders. Neuroscience 54, 287-322.
41. LeRay C. F., Prevette D., Oppenheim R. W., and Fontaine-Perus J. (1993) Interactions between spinal cord stimulation and activity blockade in the regulation of synaptogenesis and motoneuron survival in the chick embryo. J. Neurobiol. 24, 1142-1156.
42. Lipton S. A. and Rosenberg P. A. (1994) Excitatory amino acids as a final common pathway for neurologic disorders. N. Engl. J. Med. 330, 613-622.
43. Metzger F., Weise S., and Sendtner M. (1998) Effect of glutamate on dendritic growth in embryonic rat motoneurons. J. Neurosci. 18, 1735-1742.
44. Murphy T. H. and Baraban J. M. (1990) Glutamate toxicity in immature cortical neurons precedes development of glutamate receptor currents. Dev. Brain Res. 57, 146-150.
45. Nag S. and Riopelle R. J. (1990) Spinal neuronal pathology associated with continuous intrathecal infusion of N-methyl-D-aspartate in the rat. Acta Neuropathol. 81, 7-13.
46. Neve R. L., Howe J. R., Hong S., and Kalb R. G. (1997) Introduction of the glutamate receptor subunit 1 into motor neurons in vitro and in vivo using a recombinant Herpes simplex virus. Neuroscience 79, 435-447.
47. Oppenheim R. W. (1986) The absence of significant postnatal motoneuron death in the brachial and lumbar spinal cord of the rat. J. Comp. Neurol. 246, 281-286.
48. Oppenheim R. W., Houenou L., Pincon-Raymond M., Powell J. A., Rieger F., and Standish L. J. (1986) The development of motoneurons in the embryonic spinal cord of the mouse mutant, muscular dysgenesis (mdg/mdg): survival, morphology, and biochemical differentiation. Dev. Biol. 114, 426-436.
49. Peterson C., Neal J. H., and Cotman C. W. (1989) Development of N-methyl-D-aspartate excitotoxicity in cultured hippocampal neurons. Dev. Brain Res. 48, 187-195.
50. Petralia R. S. and Wenthold R. J. (1992) Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J. Comp. Neurol. 318, 329-354.
51. Petralia R. S., Wang Y. X., and Wenthold R. J. (1994a) Histological and ultrastructural localization of the kainate receptor subunits. KA2 and GluR6/7, in the rat nervous system using selective antipeptide antibodies. J. Comp. Neurol. 349, 85-110.
52. Petralia R. S., Yokotani N., and Wenthold R. J. (1994b) Light and electron microscope distribution of the NMDA receptor subunit NMDAR1 in the rat nervous system using a selective anti-peptide antibody. J. Neurosci. 14, 667-696.
53. Regan R. F. (1996) The vulnerability of spinal cord neurons to excitotoxic injury: comparison with cortical neurons. Neurosci. Lett. 213, 9-12.
54. Regan R. F. and Choi D. W. (1991) Glutamate neurotoxicity in spinal cord cell culture. Neuroscience 43, 585-591.
55. Roberg B., Torgner I. A., and Kvamme E. (1995) The orientation of phosphate activated glutaminase in the inner mitochondrial membrane of synaptic and non-synaptic rat brain mitochondria. Neurochem. Int. 27, 367-376.
56. Rosenberg P. A. (1991) Accumulation of extracellular glutamate and neuronal death in astrocyte-poor cortical cultures exposed to glutamine. Glia 4, 91-100.
57. Samdani A. F., Newcamp C., Resink A., Facchinetti F., Hoffman B. E., Dawson V. L., and Dawson T. M. (1997) Differential susceptibility to neurotoxicity mediated by neurotrophins and neuronal nitric oxide synthase. J. Neurosci. 17, 4633-4641.
58. Shaw P. J. (1994) Excitotoxicity and motor neuron disease: a review of the evidence. J. Neurol. Sci. 124 (Suppl.), 6-13.
59. Solum D., Hughes D., Major M. S., and Parks T. M. (1997) Prevention of normally occurring and deafferentation-induced neuronal death in chick brainstem auditory neurons by periodic blockade of AMPA/kainate receptors. J. Neurosci. 17, 4744-4751.
60. Stewart G. R., Olney J. W., Pathikonda M., and Snider W. D. (1991) Excitotoxicity in the embryonic chick spinal cord. Ann. Neurol. 30, 758-766.
61. + channels, glutamate release, and NMDA receptors mediates delayed neurodegeneration through nitric oxide formation. J. Neurosci. 16, 5004-5013.
62. Tsuji K., Nakamura Y., Ogata T., Mitani A., Kataoka K., Shibata T., Ishida M., and Shinozaki H. (1995) Neurotoxicity of acromelic acid in cultured neurons from rat spinal cord. Neuroscience 68, 585-591.
63. Tymianski M. and Tator C. H. (1996) Normal and abnormal calcium homeostasis in neurons: a basis for the pathophysiology of traumatic and ischemic central nervous system injury. Neurosurgery 38, 1176-1195.
64. Tymianski M., Charlton M. P., Carlen P. L., and Tator C. H. (1993) Source specificity of early calcium neurotoxicity in cultured embryonic spinal neurons. J. Neurosci. 13, 2085-2104.
65. Urca G. and Urea R. (1990) Neurotoxic effects of excitatory amino acids in the mouse spinal cord: quisqualate and kainate but not N-methyl-D-aspartate induce permanent neural damage. Brain Res. 529, 7-15.
66. Vorndran C., Minta A., and Poenie M. (1995) New fluorescent calcium indicators designed for cytosolic retention or measuring calcium near membranes. Biophys. J. 69, 2112-2124.
67. A receptors, and glutamate receptors develop sequentially on embryonic rat spinal cord cells. J. Neurosci. 13, 2068-2084.
68. Watanabe M., Mishina M., and Inoue Y. (1994) Distinct spatiotemporal distribution of the N-methyl-D-aspartate receptor channel subunit mRNAs in the mouse cervical cord. J. Comp. Neurol. 345, 314-319.
69. Watkins J. C., Krogsgaard-Larsen P., and Honoré T. (1990) Structure-activity relationships in the development of excitatory amino acid receptor agonists and competitive antagonists. Trends Pharmacol. Sci. 11, 25-33.
70. Wells K., Anderson D. K., Farooqui A. A., and Horrocks L. A. (1994) Excitotoxicity of glutamate and four analogs in primary spinal cord cell cultures. Neurochem. Int. 25, 377-384.
71. Wetts R., Phelps P. E., and Vaughn J. E. (1995) Transient and continuous expression of NADPH diaphorase in different neuronal populations of developing rat spinal cord. Dev. Dyn. 202, 215-228.
72. Wu W., Liuzzi F. J., Depto A. S., Li Y., Mong J. A., Dawson T. M., and Synder S. H. (1994) Neuronal nitric oxide synthase is induced in spinal neurons by traumatic injury. Neuroscience 61, 719-726.
73. Yan Q. and Johnson E. M. (1988) An immunohistochemical study of the nerve growth factor receptor in developing rats. J. Neurosci. 8, 3481-3498.
74. Yin H. Z., Park D. D., Lindsay A. D., and Weiss J. H. (1995) Spinal cord neurons are vulnerable to rapidly triggered kainate neurotoxicity in vitro. Brain Res. 689, 265-270.
75. Ziskind-Conhaim L. (1990) NMDA receptors mediate poly- and monosynaptic potentials in motoneurons of rat embryos. J. Neurosci. 10, 125-135.